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Subject: Chemical genetics reveals a complex functional ground state of neural stem cells: Nature Chemical Biology
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<H1 class=3Dpage-header>Letter</H1>
<HR>

<P id=3Dcite><SPAN class=3Djournalname>Nature Chemical Biology</SPAN> =
<SPAN=20
class=3Db>3</SPAN>, 268-273 (2007) <BR><ABBR=20
title=3D"Digital Object Identifier">doi</ABBR>:10.1038/nchembio873</P>
<H2 id=3Datl>Chemical genetics reveals a complex functional ground state =
of neural=20
stem cells</H2>
<P id=3Daug>Phedias Diamandis<SUP><A title=3D"affiliated with "=20
href=3D"http://www.nature.com/nchembio/journal/v3/n5/full/nchembio873.htm=
l#a1">1</A>,</SUP><SUP><A=20
title=3D"affiliated with "=20
href=3D"http://www.nature.com/nchembio/journal/v3/n5/full/nchembio873.htm=
l#a2">2</A>,</SUP><SUP><A=20
title=3D"affiliated with "=20
href=3D"http://www.nature.com/nchembio/journal/v3/n5/full/nchembio873.htm=
l#a3">3</A>,</SUP><SUP><A=20
title=3D"affiliated with "=20
href=3D"http://www.nature.com/nchembio/journal/v3/n5/full/nchembio873.htm=
l#a4">4</A></SUP>,=20
Jan Wildenhain<SUP><A title=3D"affiliated with "=20
href=3D"http://www.nature.com/nchembio/journal/v3/n5/full/nchembio873.htm=
l#a4">4</A></SUP>,=20
Ian D Clarke<SUP><A title=3D"affiliated with "=20
href=3D"http://www.nature.com/nchembio/journal/v3/n5/full/nchembio873.htm=
l#a1">1</A>,</SUP><SUP><A=20
title=3D"affiliated with "=20
href=3D"http://www.nature.com/nchembio/journal/v3/n5/full/nchembio873.htm=
l#a2">2</A></SUP>,=20
Adrian G Sacher<SUP><A title=3D"affiliated with "=20
href=3D"http://www.nature.com/nchembio/journal/v3/n5/full/nchembio873.htm=
l#a1">1</A>,</SUP><SUP><A=20
title=3D"affiliated with "=20
href=3D"http://www.nature.com/nchembio/journal/v3/n5/full/nchembio873.htm=
l#a2">2</A></SUP>,=20
Jeremy Graham<SUP><A title=3D"affiliated with "=20
href=3D"http://www.nature.com/nchembio/journal/v3/n5/full/nchembio873.htm=
l#a1">1</A>,</SUP><SUP><A=20
title=3D"affiliated with "=20
href=3D"http://www.nature.com/nchembio/journal/v3/n5/full/nchembio873.htm=
l#a2">2</A></SUP>,=20
David S Bellows<SUP><A title=3D"affiliated with "=20
href=3D"http://www.nature.com/nchembio/journal/v3/n5/full/nchembio873.htm=
l#a3">3</A></SUP>,=20
Erick K M Ling<SUP><A title=3D"affiliated with "=20
href=3D"http://www.nature.com/nchembio/journal/v3/n5/full/nchembio873.htm=
l#a1">1</A>,</SUP><SUP><A=20
title=3D"affiliated with "=20
href=3D"http://www.nature.com/nchembio/journal/v3/n5/full/nchembio873.htm=
l#a2">2</A>,</SUP><SUP><A=20
title=3D"affiliated with "=20
href=3D"http://www.nature.com/nchembio/journal/v3/n5/full/nchembio873.htm=
l#a5">5</A></SUP>,=20
Ryan J Ward<SUP><A title=3D"affiliated with "=20
href=3D"http://www.nature.com/nchembio/journal/v3/n5/full/nchembio873.htm=
l#a1">1</A>,</SUP><SUP><A=20
title=3D"affiliated with "=20
href=3D"http://www.nature.com/nchembio/journal/v3/n5/full/nchembio873.htm=
l#a2">2</A>,</SUP><SUP><A=20
title=3D"affiliated with "=20
href=3D"http://www.nature.com/nchembio/journal/v3/n5/full/nchembio873.htm=
l#a5">5</A></SUP>,=20
Leanne G Jamieson<SUP><A title=3D"affiliated with "=20
href=3D"http://www.nature.com/nchembio/journal/v3/n5/full/nchembio873.htm=
l#a1">1</A>,</SUP><SUP><A=20
title=3D"affiliated with "=20
href=3D"http://www.nature.com/nchembio/journal/v3/n5/full/nchembio873.htm=
l#a2">2</A>,</SUP><SUP><A=20
title=3D"affiliated with "=20
href=3D"http://www.nature.com/nchembio/journal/v3/n5/full/nchembio873.htm=
l#a5">5</A></SUP>,=20
Mike Tyers<SUP><A title=3D"affiliated with "=20
href=3D"http://www.nature.com/nchembio/journal/v3/n5/full/nchembio873.htm=
l#a3">3</A>,</SUP><SUP><A=20
title=3D"affiliated with "=20
href=3D"http://www.nature.com/nchembio/journal/v3/n5/full/nchembio873.htm=
l#a4">4</A></SUP>=20
and Peter B Dirks<SUP><A title=3D"affiliated with "=20
href=3D"http://www.nature.com/nchembio/journal/v3/n5/full/nchembio873.htm=
l#a1">1</A>,</SUP><SUP><A=20
title=3D"affiliated with "=20
href=3D"http://www.nature.com/nchembio/journal/v3/n5/full/nchembio873.htm=
l#a2">2</A>,</SUP><SUP><A=20
title=3D"affiliated with "=20
href=3D"http://www.nature.com/nchembio/journal/v3/n5/full/nchembio873.htm=
l#a5">5</A>,</SUP><SUP><A=20
title=3D"affiliated with "=20
href=3D"http://www.nature.com/nchembio/journal/v3/n5/full/nchembio873.htm=
l#a6">6</A></SUP></P>
<DIV id=3Darticlebody>
<HR class=3Dseparator>

<DIV id=3Dabs>
<P class=3Dlead>The identification of self-renewing and multipotent =
neural stem=20
cells (NSCs) in the mammalian brain holds promise for the treatment of=20
neurological diseases and has yielded new insight into brain =
cancer<SUP><A=20
href=3D"http://www.nature.com/nchembio/journal/v3/n5/full/nchembio873.htm=
l#B1">1,</A></SUP><SUP><A=20
href=3D"http://www.nature.com/nchembio/journal/v3/n5/full/nchembio873.htm=
l#B2">2,</A></SUP><SUP><A=20
href=3D"http://www.nature.com/nchembio/journal/v3/n5/full/nchembio873.htm=
l#B3">3</A></SUP>.=20
However, the complete repertoire of signaling pathways that governs the=20
proliferation and self-renewal of NSCs, which we refer to as the 'ground =
state',=20
remains largely uncharacterized. Although the candidate gene approach =
has=20
uncovered vital pathways in NSC biology<SUP><A=20
href=3D"http://www.nature.com/nchembio/journal/v3/n5/full/nchembio873.htm=
l#B4">4,</A></SUP><SUP><A=20
href=3D"http://www.nature.com/nchembio/journal/v3/n5/full/nchembio873.htm=
l#B5">5,</A></SUP><SUP><A=20
href=3D"http://www.nature.com/nchembio/journal/v3/n5/full/nchembio873.htm=
l#B6">6,</A></SUP><SUP><A=20
href=3D"http://www.nature.com/nchembio/journal/v3/n5/full/nchembio873.htm=
l#B7">7,</A></SUP><SUP><A=20
href=3D"http://www.nature.com/nchembio/journal/v3/n5/full/nchembio873.htm=
l#B8">8</A></SUP>,=20
so far only a few highly studied pathways have been investigated. Based =
on the=20
intimate relationship between NSC self-renewal and neurosphere=20
proliferation<SUP><A=20
href=3D"http://www.nature.com/nchembio/journal/v3/n5/full/nchembio873.htm=
l#B8">8</A></SUP>,=20
we undertook a chemical genetic screen for inhibitors of neurosphere=20
proliferation in order to probe the operational circuitry of the NSC. =
The screen=20
recovered small molecules known to affect neurotransmission pathways =
previously=20
thought to operate primarily in the mature central nervous system; these =

compounds also had potent inhibitory effects on cultures enriched for =
brain=20
cancer stem cells. These results suggest that clinically approved=20
neuromodulators may remodel the mature central nervous system and find=20
application in the treatment of brain cancer.</P></DIV>
<HR class=3Dseparator>

<P class=3Dnorm>To profile the signaling network of primary cultures of =
neural=20
precursor cells (NPCs), we screened 1,267 compounds in the library of=20
pharmacologically active compounds (LOPAC) for inhibitors of neurosphere =

proliferation, as measured by incorporation of the vital dye thiazolyl =
blue=20
tetrazolium bromide (MTT) (<A=20
href=3D"http://www.nature.com/nchembio/journal/v3/n5/full/nchembio873.htm=
l#f1">Fig.=20
1a,b</A> and <A=20
href=3D"http://www.nature.com/nchembio/journal/v3/n5/suppinfo/nchembio873=
_S1.html">Supplementary=20
Table 1</A> online). A Z' factor<SUP><A=20
href=3D"http://www.nature.com/nchembio/journal/v3/n5/full/nchembio873.htm=
l#B9">9</A></SUP>=20
of 0.78 and a Pearson correlation coefficient of 0.981 for replicate =
screens=20
indicated that the assay was reliable (<A=20
href=3D"http://www.nature.com/nchembio/journal/v3/n5/suppinfo/nchembio873=
_S1.html">Supplementary=20
Methods</A> online). 160 compounds that significantly inhibited =
neurosphere=20
proliferation (<I>P</I> &lt; 0.01) were clustered into groups of known=20
pharmacologic action (<A=20
href=3D"http://www.nature.com/nchembio/journal/v3/n5/full/nchembio873.htm=
l#t1">Table=20
1</A> and <A=20
href=3D"http://www.nature.com/nchembio/journal/v3/n5/suppinfo/nchembio873=
_S1.html">Supplementary=20
Table 2</A> online). Known cytotoxic compounds that target essential =
cellular=20
processes predictably scored as hits in the screen. Unexpectedly, =
however, many=20
agents that modulate neurotransmission in the dopamine, serotonin, =
opioid,=20
glutamate, vanilloid and other pathways potently inhibited growth of =
NPCs. Many=20
of these agents are used in the clinical treatment of neurological =
disorders and=20
are traditionally thought to act on mature central nervous system (CNS) =
cell=20
populations. These compounds induced a variety of neurosphere =
phenotypes,=20
including changes in sphere number, sphere size, and cell-cell or =
cell-surface=20
adhesion properties, which suggests that an elaborate balance of these =
signaling=20
pathways dictates NPC fate (<A=20
href=3D"http://www.nature.com/nchembio/journal/v3/n5/full/nchembio873.htm=
l#f1">Fig.=20
1c</A>).</P>
<DIV class=3Dfigure-table id=3Df1>
<H5 class=3Dnorm><A=20
href=3D"http://www.nature.com/nchembio/journal/v3/n5/fig_tab/nchembio873_=
F1.html">Figure=20
1:&nbsp;HTS of NPCs.</A></H5><A=20
href=3D"http://www.nature.com/nchembio/journal/v3/n5/fig_tab/nchembio873_=
F1.html"><IMG=20
class=3Dthumb=20
alt=3D"Figure 1 : HTS of NPCs. Unfortunately we are unable to provide =
accessible alternative text for this. If you require assistance to =
access this image, or to obtain a text description, please contact =
npg@nature.com"=20
src=3D"http://www.nature.com/nchembio/journal/v3/n5/thumbs/nchembio873-F1=
.jpg"></A>
<P class=3D"">(<B>a</B>) Neurospheres are derived from self-renewing =
multipotent=20
NSCs and contain a heterogeneous mixture of stem cells, progenitor =
cells, and a=20
very small number of differentiated cells. (<B>b</B>) Scatter plot of =
all 1,267=20
compounds of the LOPAC library screened against NPCs. 160 compounds =
(<IMG=20
style=3D"BORDER-TOP-WIDTH: 0px; BORDER-LEFT-WIDTH: 0px; =
BORDER-BOTTOM-WIDTH: 0px; VERTICAL-ALIGN: bottom; BORDER-RIGHT-WIDTH: =
0px"=20
alt=3Dcircle =
src=3D"http://www.nature.com/__chars/circle/black/med/base/glyph.gif">)=20
were identified as inhibitors of neurosphere proliferation (<I>P</I> =
&lt; 0.01),=20
19 compounds (<IMG=20
style=3D"BORDER-TOP-WIDTH: 0px; BORDER-LEFT-WIDTH: 0px; =
BORDER-BOTTOM-WIDTH: 0px; VERTICAL-ALIGN: middle; BORDER-RIGHT-WIDTH: =
0px"=20
alt=3Dsquare =
src=3D"http://www.nature.com/__chars/square/black/med/base/glyph.gif">)=20
were identified as activators (<I>P</I> &lt; 0.01) and the remaining =
agents=20
(<IMG=20
style=3D"BORDER-TOP-WIDTH: 0px; BORDER-LEFT-WIDTH: 0px; =
BORDER-BOTTOM-WIDTH: 0px; VERTICAL-ALIGN: bottom; BORDER-RIGHT-WIDTH: =
0px"=20
alt=3D"filled triangle"=20
src=3D"http://www.nature.com/__chars/triangle/special/filled/black/med/ba=
se/glyph.gif">)=20
screened did not have any significant effects on proliferation (<I>P</I> =
&gt;=20
0.01). (<B>c</B>) Examples of phenotypic variation observed in response =
to=20
particular agents. Scale bars, 250 <IMG=20
style=3D"BORDER-TOP-WIDTH: 0px; BORDER-LEFT-WIDTH: 0px; =
BORDER-BOTTOM-WIDTH: 0px; VERTICAL-ALIGN: middle; BORDER-RIGHT-WIDTH: =
0px"=20
alt=3Dmu =
src=3D"http://www.nature.com/__chars/mu/black/med/base/glyph.gif">m. =
HTS,=20
high-throughput screen.</P>
<P class=3Dbuttons><A class=3Dfull=20
href=3D"http://www.nature.com/nchembio/journal/v3/n5/fig_tab/nchembio873_=
F1.html">Full=20
figure and legend (80K)</A><A class=3Dfull=20
href=3D"http://www.nature.com/nchembio/journal/v3/n5/fig_tab/nchembio873_=
ft.html">Figures,=20
schemes &amp; tables index</A></P><SPAN class=3Dcleardiv><!-- =
--></SPAN></DIV><BR=20
class=3Dclear>
<DIV class=3D"figure-table clearfix" id=3Dt1>
<H5 class=3Dnorm><A=20
href=3D"http://www.nature.com/nchembio/journal/v3/n5/fig_tab/nchembio873_=
T1.html">Table=20
1: HTS bioactive pharmacological classes</A></H5><A=20
href=3D"http://www.nature.com/nchembio/journal/v3/n5/fig_tab/nchembio873_=
T1.html"><IMG=20
class=3Dthumb alt=3D"Table 1 - HTS bioactive pharmacological classes"=20
src=3D"http://www.nature.com/common/images/table_thumb.gif"></A>
<P class=3Dbuttons><BR><A class=3Dfull=20
href=3D"http://www.nature.com/nchembio/journal/v3/n5/fig_tab/nchembio873_=
T1.html">Full=20
table</A><A class=3Dfull=20
href=3D"http://www.nature.com/nchembio/journal/v3/n5/fig_tab/nchembio873_=
ft.html">Figures,=20
schemes &amp; tables index</A></P><SPAN class=3Dcleardiv><!-- =
--></SPAN></DIV><BR=20
class=3Dclear>
<P class=3Dnorm>To verify hits from the primary screen, 43 =
representative=20
candidates were retested at the original screen concentration of 3 <IMG=20
style=3D"BORDER-TOP-WIDTH: 0px; BORDER-LEFT-WIDTH: 0px; =
BORDER-BOTTOM-WIDTH: 0px; VERTICAL-ALIGN: middle; BORDER-RIGHT-WIDTH: =
0px"=20
alt=3Dmu =
src=3D"http://www.nature.com/__chars/mu/black/med/base/glyph.gif">M; of=20
these, 40 (93%) showed significant activity (<I>P</I>&lt;0.05) (<A=20
href=3D"http://www.nature.com/nchembio/journal/v3/n5/suppinfo/nchembio873=
_S1.html">Supplementary=20
Table 3</A> online). Because other neural cell types express and signal =
through=20
a number of neurotransmitter receptors<SUP><A=20
href=3D"http://www.nature.com/nchembio/journal/v3/n5/full/nchembio873.htm=
l#B10">10</A></SUP>,=20
we assessed the selectivity and potency of each agent for a normal mouse =

astrocyte cell line versus NPCs. Dose-response curves were generated for =
28=20
compounds in both neurosphere and astrocyte cultures and used to =
determine the=20
effective concentration needed to decrease proliferation by 50%=20
(EC<SUB>50</SUB>) (<A=20
href=3D"http://www.nature.com/nchembio/journal/v3/n5/full/nchembio873.htm=
l#f2">Fig.=20
2a=96f</A> and <A=20
href=3D"http://www.nature.com/nchembio/journal/v3/n5/suppinfo/nchembio873=
_S1.html">Supplementary=20
Table 3</A>). A neurosphere selectivity ratio, defined as=20
EC<SUB>50(astrocytes)</SUB>/EC<SUB>50(neurospheres)</SUB>, was =
determined for=20
each compound and compared with that of known nonspecific inhibitors of=20
proliferation (<A=20
href=3D"http://www.nature.com/nchembio/journal/v3/n5/full/nchembio873.htm=
l#f2">Fig.=20
2a=96c</A>). Compounds that had a neurosphere selectivity ratio greater =
than that=20
observed in these control agents (&gt;5.08) were defined as NPC-specific =
agents=20
(<A=20
href=3D"http://www.nature.com/nchembio/journal/v3/n5/full/nchembio873.htm=
l#f2">Fig.=20
2d=96f</A> and <A=20
href=3D"http://www.nature.com/nchembio/journal/v3/n5/full/nchembio873.htm=
l#t2">Table=20
2</A>); 12 of the compounds tested showed high selectivity for NPCs. =
Notably,=20
the serotonin agonist =
<I>p</I>-aminophenethyl-<I>m</I>-trifluoromethylphenyl=20
pierazine (PAPP, <A class=3Dcompound=20
href=3D"http://www.nature.com/nchembio/journal/v3/n5/compound/nchembio873=
_COMP14.html"><SPAN=20
class=3Dhidden>Compound </SPAN>14</A>) and the vanilloid receptor ligand =

dihydrocapsaicin were respectively 702- and 192-fold more selective for =
normal=20
NPCs than for astrocyte cultures.</P>
<DIV class=3Dfigure-table id=3Df2>
<H5 class=3Dnorm><A=20
href=3D"http://www.nature.com/nchembio/journal/v3/n5/fig_tab/nchembio873_=
F2.html">Figure=20
2:&nbsp;Identification of potent NPC-specific compounds.</A></H5><A=20
href=3D"http://www.nature.com/nchembio/journal/v3/n5/fig_tab/nchembio873_=
F2.html"><IMG=20
class=3Dthumb=20
alt=3D"Figure 2 : Identification of potent NPC-specific compounds. =
Unfortunately we are unable to provide accessible alternative text for =
this. If you require assistance to access this image, or to obtain a =
text description, please contact npg@nature.com"=20
src=3D"http://www.nature.com/nchembio/journal/v3/n5/thumbs/nchembio873-F2=
.jpg"></A>
<P class=3D"">(<B>a</B>=96<B>f</B>) Dose-response curves and chemical =
structures of=20
controls: cycloheximide (<B>a</B>), etoposide (<B>b</B>) and carboplatin =

(<B>c</B>), and of selected newly identified compounds: dihydrocapsaicin =

(<B>d</B>), apomorphine (<B>e</B>) and PAPP (<B>f</B>). Each plot shows =
the=20
fitted sigmoidal logistic curve to MTT proliferation assay readings of =
both=20
astrocytes (- -<IMG=20
style=3D"BORDER-TOP-WIDTH: 0px; BORDER-LEFT-WIDTH: 0px; =
BORDER-BOTTOM-WIDTH: 0px; VERTICAL-ALIGN: baseline; BORDER-RIGHT-WIDTH: =
0px"=20
alt=3D"filled circle"=20
src=3D"http://www.nature.com/__chars/circle/special/filled/black/med/base=
/glyph.gif">-=20
-) and neurosphere cultures (=96<IMG=20
style=3D"BORDER-TOP-WIDTH: 0px; BORDER-LEFT-WIDTH: 0px; =
BORDER-BOTTOM-WIDTH: 0px; VERTICAL-ALIGN: bottom; BORDER-RIGHT-WIDTH: =
0px"=20
alt=3D"filled triangle"=20
src=3D"http://www.nature.com/__chars/triangle/special/filled/black/med/ba=
se/glyph.gif">=96).=20
Values represent the mean and s.e.m. of three independent experiments.=20
(<B>g</B>) Replating colony forming efficiency of pretreated neurosphere =

cultures. Values represent the number of progeny neurospheres arising =
from 2,000=20
or 1,000 cells plated in fresh medium after a 7-d pretreatment of NPCs =
with the=20
indicated inhibitor at the estimated EC<SUB>75</SUB> value. As the=20
EC<SUB>75</SUB> of apomorphine did not allow the recovery of sufficient =
cells,=20
an EC<SUB>50</SUB> pretreatment was used for this agent. Sphere counts =
for=20
vehicle-treated cells represent the mean and s.d. of six separate =
replicates=20
conducted during two independent experiments. All other values represent =
the=20
mean of two independent experiments. Asterisks indicate a reproduced=20
statistically significant (<I>P</I> &lt; 0.05) reduction in replating =
efficiency=20
when compared to vehicle control. The larger <I>P</I> value (of the two=20
experiments) is reported. These differences (at both 2,000 and 1,000 =
cells per=20
well) were confirmed (two-tailed paired <I>t</I>-test) for cultures =
treated with=20
PAPP (<I>P</I><SUB>2,000</SUB> =3D 0.02; <I>P</I><SUB>1,000</SUB> =3D =
0.008) and=20
apomorphine (<I>P</I><SUB>2,000</SUB> =3D 0.01; <I>P</I><SUB>1,000</SUB> =
=3D 0.02)=20
in three independent trials.</P>
<P class=3Dbuttons><A class=3Dfull=20
href=3D"http://www.nature.com/nchembio/journal/v3/n5/fig_tab/nchembio873_=
F2.html">Full=20
figure and legend (95K)</A><A class=3Dfull=20
href=3D"http://www.nature.com/nchembio/journal/v3/n5/fig_tab/nchembio873_=
ft.html">Figures,=20
schemes &amp; tables index</A></P><SPAN class=3Dcleardiv><!-- =
--></SPAN></DIV><BR=20
class=3Dclear>
<DIV class=3D"figure-table clearfix" id=3Dt2>
<H5 class=3Dnorm><A=20
href=3D"http://www.nature.com/nchembio/journal/v3/n5/fig_tab/nchembio873_=
T2.html">Table=20
2: Highly potent and highly selective compounds identified by HTS of=20
neurospheres</A></H5><A=20
href=3D"http://www.nature.com/nchembio/journal/v3/n5/fig_tab/nchembio873_=
T2.html"><IMG=20
class=3Dthumb=20
alt=3D"Table 2 - Highly potent and highly selective compounds identified =
by HTS of neurospheres"=20
src=3D"http://www.nature.com/common/images/table_thumb.gif"></A>
<P class=3Dbuttons><BR><A class=3Dfull=20
href=3D"http://www.nature.com/nchembio/journal/v3/n5/fig_tab/nchembio873_=
T2.html">Full=20
table</A><A class=3Dfull=20
href=3D"http://www.nature.com/nchembio/journal/v3/n5/fig_tab/nchembio873_=
ft.html">Figures,=20
schemes &amp; tables index</A></P><SPAN class=3Dcleardiv><!-- =
--></SPAN></DIV><BR=20
class=3Dclear>
<P class=3Dnorm>Neurospheres are comprised of a heterogeneous population =
of NSCs=20
and lineage-restricted progenitor cells. To determine whether the =
inhibitors=20
affected NSC self-renewal, as opposed to proliferation of more committed =

precursor populations, we analyzed the higher order colony-forming =
efficiency of=20
treated neurosphere cultures. With the exception of dihydrocapsaicin,=20
representative compounds from the main neurotransmission classes =
significantly=20
reduced higher order neurosphere formation upon re-culture in the =
absence of=20
drug (<A=20
href=3D"http://www.nature.com/nchembio/journal/v3/n5/full/nchembio873.htm=
l#f2">Fig.=20
2g</A>). The various inhibitors therefore seem to target the neural =
precursor=20
pool that is predominantly responsible for sphere formation.</P>
<P class=3Dnorm>To further delineate the mechanism through which =
neuromodulatory=20
agents impede expansion of NPCs in culture, we performed time-course =
analyses=20
for both cell viability and apoptosis. Unlike etoposide (<A=20
href=3D"http://www.nature.com/nchembio/journal/v3/n5/full/nchembio873.htm=
l#f3">Fig.=20
3a</A>) and cycloheximide (data not shown), which have immediate effects =
on cell=20
proliferation and viability, the neurotransmission modulators PAPP and=20
ifenprodil decreased viable cell numbers only after 2 d post-treatment =
(<A=20
href=3D"http://www.nature.com/nchembio/journal/v3/n5/full/nchembio873.htm=
l#f3">Fig.=20
3a</A>). Similar delayed-onset effects were observed for butaclamol,=20
<I>p</I>-fluoro-hexahydrosila-difenidol (<I>p</I>-F-HHSiD, <A =
class=3Dcompound=20
href=3D"http://www.nature.com/nchembio/journal/v3/n5/compound/nchembio873=
_COMP8.html"><SPAN=20
class=3Dhidden>Compound </SPAN>8</A>) and carbetapentane (data not =
shown).=20
Consistently, caspase-3 and caspase-7 concentrations were unchanged =
after 12 h=20
of PAPP and ifenprodil treatment, but increased significantly=20
(<I>P</I>&lt;0.001) after 2 d of drug treatment (<A=20
href=3D"http://www.nature.com/nchembio/journal/v3/n5/full/nchembio873.htm=
l#f3">Fig.=20
3b</A>). This increase in the apoptotic response of treated cells =
occurred at=20
concentrations of drugs that did not abolish the initial proliferation =
or=20
viability of these cells (<A=20
href=3D"http://www.nature.com/nchembio/journal/v3/n5/full/nchembio873.htm=
l#f3">Fig.=20
3c</A>). Finally, expression of the immature NPC marker nestin was =
substantially=20
decreased after treatment for 2 d with ifenprodil (<A=20
href=3D"http://www.nature.com/nchembio/journal/v3/n5/full/nchembio873.htm=
l#f3">Fig.=20
3d</A>) and PAPP (data not shown). These results suggest that =
appropriate=20
neurotransmission signaling is required to maintain NSC proliferation, =
survival=20
and identity.</P>
<DIV class=3Dfigure-table id=3Df3>
<H5 class=3Dnorm><A=20
href=3D"http://www.nature.com/nchembio/journal/v3/n5/fig_tab/nchembio873_=
F3.html">Figure=20
3:&nbsp;Temporal effects of neuromodulators on NPC viability and =
apoptotic=20
response.</A></H5><A=20
href=3D"http://www.nature.com/nchembio/journal/v3/n5/fig_tab/nchembio873_=
F3.html"><IMG=20
class=3Dthumb=20
alt=3D"Figure 3 : Temporal effects of neuromodulators on NPC viability =
and apoptotic response. Unfortunately we are unable to provide =
accessible alternative text for this. If you require assistance to =
access this image, or to obtain a text description, please contact =
npg@nature.com"=20
src=3D"http://www.nature.com/nchembio/journal/v3/n5/thumbs/nchembio873-F3=
.jpg"></A>
<P class=3D"">(<B>a</B>) Proliferation dynamics of PAPP-, ifenprodil- =
and=20
etoposide-treated NPCs. (<B>b</B>) Normalized caspase-3 and caspase-7 =
activity=20
in NPCs after 12 h and 48 h of drug treatment. Asterisk indicates a =
significant=20
change (two-tailed <I>t</I>-test) from the corresponding vehicle-treated =
data=20
point. (<B>c</B>) Corresponding MTT values taken at 12 h and 2 d for the =

caspase-3 and caspase-7 experiments shown in <B>b</B>. All values =
represent the=20
mean and s.d. of one representative experiment (from three independent =
trials)=20
of NPCs treated with PAPP (1 <IMG=20
style=3D"BORDER-TOP-WIDTH: 0px; BORDER-LEFT-WIDTH: 0px; =
BORDER-BOTTOM-WIDTH: 0px; VERTICAL-ALIGN: middle; BORDER-RIGHT-WIDTH: =
0px"=20
alt=3Dmu =
src=3D"http://www.nature.com/__chars/mu/black/med/base/glyph.gif">M),=20
ifenprodil (3 <IMG=20
style=3D"BORDER-TOP-WIDTH: 0px; BORDER-LEFT-WIDTH: 0px; =
BORDER-BOTTOM-WIDTH: 0px; VERTICAL-ALIGN: middle; BORDER-RIGHT-WIDTH: =
0px"=20
alt=3Dmu =
src=3D"http://www.nature.com/__chars/mu/black/med/base/glyph.gif">M),=20
etoposide (3 <IMG=20
style=3D"BORDER-TOP-WIDTH: 0px; BORDER-LEFT-WIDTH: 0px; =
BORDER-BOTTOM-WIDTH: 0px; VERTICAL-ALIGN: middle; BORDER-RIGHT-WIDTH: =
0px"=20
alt=3Dmu =
src=3D"http://www.nature.com/__chars/mu/black/med/base/glyph.gif">M) or=20
vehicle. (<B>d</B>) Flow cytometric analysis of the neural precursor =
marker=20
nestin in NPCs after 2 d of treatment with ifenprodil (5 <IMG=20
style=3D"BORDER-TOP-WIDTH: 0px; BORDER-LEFT-WIDTH: 0px; =
BORDER-BOTTOM-WIDTH: 0px; VERTICAL-ALIGN: middle; BORDER-RIGHT-WIDTH: =
0px"=20
alt=3Dmu =
src=3D"http://www.nature.com/__chars/mu/black/med/base/glyph.gif">M) or=20
vehicle. Representative histograms of vehicle-treated (20% nestin =
negative) and=20
ifenprodil-treated (63% nestin negative) cells compared with the isotype =
control=20
(100% nestin negative) are shown from two independent experiments.</P>
<P class=3Dbuttons><A class=3Dfull=20
href=3D"http://www.nature.com/nchembio/journal/v3/n5/fig_tab/nchembio873_=
F3.html">Full=20
figure and legend (73K)</A><A class=3Dfull=20
href=3D"http://www.nature.com/nchembio/journal/v3/n5/fig_tab/nchembio873_=
ft.html">Figures,=20
schemes &amp; tables index</A></P><SPAN class=3Dcleardiv><!-- =
--></SPAN></DIV><BR=20
class=3Dclear>
<P class=3Dnorm>As gene expression profiles of brain tumors resemble =
those of=20
normal and embryonic NPCs<SUP><A=20
href=3D"http://www.nature.com/nchembio/journal/v3/n5/full/nchembio873.htm=
l#B11">11,</A></SUP><SUP><A=20
href=3D"http://www.nature.com/nchembio/journal/v3/n5/full/nchembio873.htm=
l#B12">12,</A></SUP><SUP><A=20
href=3D"http://www.nature.com/nchembio/journal/v3/n5/full/nchembio873.htm=
l#B13">13,</A></SUP><SUP><A=20
href=3D"http://www.nature.com/nchembio/journal/v3/n5/full/nchembio873.htm=
l#B14">14</A></SUP>,=20
agents that inhibit normal neural precursor growth may also inhibit =
cultures of=20
brain tumors that are enriched for cancer stem cells<SUP><A=20
href=3D"http://www.nature.com/nchembio/journal/v3/n5/full/nchembio873.htm=
l#B1">1,</A></SUP><SUP><A=20
href=3D"http://www.nature.com/nchembio/journal/v3/n5/full/nchembio873.htm=
l#B2">2,</A></SUP><SUP><A=20
href=3D"http://www.nature.com/nchembio/journal/v3/n5/full/nchembio873.htm=
l#B11">11</A></SUP>.=20
We therefore assessed the activity of a subset of NPC-specific =
inhibitors=20
against low-passage (&lt;4) neurosphere cultures derived from =
spontaneously=20
formed medulloblastomas in heterozygous patched =
(<I>Ptch1<SUP>+/-</SUP></I>) and=20
<I>Ptch1<SUP>+/-</SUP></I><I>Trp53<SUP>-/-</SUP></I> mice<SUP><A=20
href=3D"http://www.nature.com/nchembio/journal/v3/n5/full/nchembio873.htm=
l#B15">15</A></SUP>.=20
Like their normal counterparts, cancerous NPCs from these tumors grow as =
spheres=20
in serum-free culture and express the neural precursor marker prominin1 =
(CD133)=20
(<A=20
href=3D"http://www.nature.com/nchembio/journal/v3/n5/full/nchembio873.htm=
l#f4">Fig.=20
4a,b</A>). The NPC-specific agents also potently suppressed the =
proliferation of=20
both <I>Ptch1<SUP>+/-</SUP></I> and=20
<I>Ptch1</I><SUP>+/-</SUP><I>Trp53<SUP>-/-</SUP></I> medulloblastoma =
precursor=20
cell populations (<A=20
href=3D"http://www.nature.com/nchembio/journal/v3/n5/full/nchembio873.htm=
l#f4">Fig.=20
4c</A> and <A=20
href=3D"http://www.nature.com/nchembio/journal/v3/n5/full/nchembio873.htm=
l#t2">Table=20
2</A>). Notably, some of these agents were an order of an magnitude more =

effective in the inhibition of tumor cell growth <I>in vitro</I> than =
the=20
hedgehog signaling inhibitor cyclopamine<SUP><A=20
href=3D"http://www.nature.com/nchembio/journal/v3/n5/full/nchembio873.htm=
l#B16">16</A></SUP>.=20
The expansion of normal human NPCs and human glioblastoma cells was also =

inhibited by neuromodulators (<A=20
href=3D"http://www.nature.com/nchembio/journal/v3/n5/suppinfo/nchembio873=
_S1.html">Supplementary=20
Table 4</A> online). For example, PAPP and ifenprodil had =
EC<SUB>50</SUB> values=20
comparable to those of commonly used nonspecific brain tumor =
chemotherapeutic=20
drugs, such as carboplatin and etoposide. Re-deployment of =
well-tolerated=20
pharmacologically active agents may thus afford a new generation of=20
chemotherapeutic agents specific for brain tumor stem cells.</P>
<DIV class=3Dfigure-table id=3Df4>
<H5 class=3Dnorm><A=20
href=3D"http://www.nature.com/nchembio/journal/v3/n5/fig_tab/nchembio873_=
F4.html">Figure=20
4:&nbsp;Neuromodulator drug sensitivity in normal and cancerous =
NPCs.</A></H5><A=20
href=3D"http://www.nature.com/nchembio/journal/v3/n5/fig_tab/nchembio873_=
F4.html"><IMG=20
class=3Dthumb=20
alt=3D"Figure 4 : Neuromodulator drug sensitivity in normal and =
cancerous NPCs. Unfortunately we are unable to provide accessible =
alternative text for this. If you require assistance to access this =
image, or to obtain a text description, please contact npg@nature.com"=20
src=3D"http://www.nature.com/nchembio/journal/v3/n5/thumbs/nchembio873-F4=
.jpg"></A>
<P class=3D"">(<B>a</B>) <I>Ptch1<SUP>+/-</SUP></I> tumors contain cells =
with=20
self-renewing neurosphere-forming potential <I>in vitro</I>. Scale bar, =
125 <IMG=20
style=3D"BORDER-TOP-WIDTH: 0px; BORDER-LEFT-WIDTH: 0px; =
BORDER-BOTTOM-WIDTH: 0px; VERTICAL-ALIGN: middle; BORDER-RIGHT-WIDTH: =
0px"=20
alt=3Dmu =
src=3D"http://www.nature.com/__chars/mu/black/med/base/glyph.gif">m.=20
(<B>b</B>) <I>Ptch1</I><SUP>+/-</SUP> tumor cells stain positive (M1) =
for the=20
early precursor marker prominin-1 (CD133 homolog) at levels comparable =
to those=20
of primary human medulloblastomas (11.6%)<SUP><A=20
href=3D"http://www.nature.com/nchembio/journal/v3/n5/full/nchembio873.htm=
l#B29">29</A></SUP>.=20
Unstained (black) and stained (red) specimens are shown. (<B>c</B>)=20
EC<SUB>50</SUB> values (mean and s.d.) for inhibition of=20
<I>Ptch1</I><SUP>+/-</SUP><I>Trp53<SUP>-/-</SUP></I> tumor sphere MTT=20
proliferation by various neuromodulators. Compound identity indicated in =
<A=20
href=3D"http://www.nature.com/nchembio/journal/v3/n5/full/nchembio873.htm=
l#t2">Table=20
2</A>. (<B>d</B>) RT-PCR gene expression profiles of a selection of=20
neurotransmitter receptors in different precursor populations. mRNA from =

serum-differentiated neurospheres and mouse erythroid leukemia (MEL) =
cells were=20
used as positive and negative controls, respectively. Vertical black =
line=20
indicates noncontiguous lanes from the same experiment. (<B>e</B>) =
Inhibition of=20
colony formation by bromocriptine in cultures with and without (<IMG=20
style=3D"BORDER-TOP-WIDTH: 0px; BORDER-LEFT-WIDTH: 0px; =
BORDER-BOTTOM-WIDTH: 0px; VERTICAL-ALIGN: baseline; BORDER-RIGHT-WIDTH: =
0px"=20
alt=3Dplusminus=20
src=3D"http://www.nature.com/__chars/plus/special/plusmn/black/med/base/g=
lyph.gif">)-sulpiride=20
supplementation. Normalized mean and s.e.m. values of three independent=20
triplicate cultures are shown. Sulpiride challenge significantly shifted =
the=20
EC<SUB>50</SUB> of bromocriptine from 1.2 <IMG=20
style=3D"BORDER-TOP-WIDTH: 0px; BORDER-LEFT-WIDTH: 0px; =
BORDER-BOTTOM-WIDTH: 0px; VERTICAL-ALIGN: middle; BORDER-RIGHT-WIDTH: =
0px"=20
alt=3Dmu =
src=3D"http://www.nature.com/__chars/mu/black/med/base/glyph.gif">M=20
(without sulpiride) to 2.5 <IMG=20
style=3D"BORDER-TOP-WIDTH: 0px; BORDER-LEFT-WIDTH: 0px; =
BORDER-BOTTOM-WIDTH: 0px; VERTICAL-ALIGN: middle; BORDER-RIGHT-WIDTH: =
0px"=20
alt=3Dmu =
src=3D"http://www.nature.com/__chars/mu/black/med/base/glyph.gif">M =
(with=20
sulpiride) (<I>P</I> &lt; 0.05), thereby indicating a rescue effect. =
(<B>f</B>)=20
Representative micrographs of the inhibitory effects of bromocriptine on =
NPC=20
expansion when challenged with a competitive antagonist. Scale bars, 500 =
<IMG=20
style=3D"BORDER-TOP-WIDTH: 0px; BORDER-LEFT-WIDTH: 0px; =
BORDER-BOTTOM-WIDTH: 0px; VERTICAL-ALIGN: middle; BORDER-RIGHT-WIDTH: =
0px"=20
alt=3Dmu =
src=3D"http://www.nature.com/__chars/mu/black/med/base/glyph.gif">m.=20
(<B>g</B>,<B>h</B>) Functional ground state of NSCs: current models of =
the NSC=20
hierarchy focus on developmental signaling pathways such as Wnt, Notch =
and Sonic=20
Hedgehog (<B>g</B>); compounds identified in the HTS approach reveal =
that the=20
NSC ground state and cell fate decision-making depend on a complex =
circuitry=20
that includes many neurotransmission signaling pathways (<B>h</B>).</P>
<P class=3Dbuttons><A class=3Dfull=20
href=3D"http://www.nature.com/nchembio/journal/v3/n5/fig_tab/nchembio873_=
F4.html">Full=20
figure and legend (97K)</A><A class=3Dfull=20
href=3D"http://www.nature.com/nchembio/journal/v3/n5/fig_tab/nchembio873_=
ft.html">Figures,=20
schemes &amp; tables index</A></P><SPAN class=3Dcleardiv><!-- =
--></SPAN></DIV><BR=20
class=3Dclear>
<P class=3Dnorm>As even well-characterized agents may exert biological =
effects=20
through off-target pathways<SUP><A=20
href=3D"http://www.nature.com/nchembio/journal/v3/n5/full/nchembio873.htm=
l#B17">17</A></SUP>,=20
we verified that a number of the known receptors for various agents are =
indeed=20
expressed in both normal and tumor NPCs. The dopamine (DRD2), =
acetylcholine=20
(M3), NMDA (NR1) and serotonin (5HT-1A) receptors were present in =
primary and=20
secondary normal mouse neurosphere cultures and =
<I>Ptch1</I><SUP>+/-</SUP> tumor=20
neurosphere cultures, as determined by RT-PCR (<A=20
href=3D"http://www.nature.com/nchembio/journal/v3/n5/full/nchembio873.htm=
l#f4">Fig.=20
4d</A>). In addition, we were able to use pharmacological inhibitors as =
a means=20
to assess whether the growth inhibition caused by the dopamine class of=20
neuromodulators depends on transmission through a known receptor.</P>
<P class=3Dnorm>In one example, (<IMG=20
style=3D"BORDER-TOP-WIDTH: 0px; BORDER-LEFT-WIDTH: 0px; =
BORDER-BOTTOM-WIDTH: 0px; VERTICAL-ALIGN: baseline; BORDER-RIGHT-WIDTH: =
0px"=20
alt=3Dplusminus=20
src=3D"http://www.nature.com/__chars/plus/special/plusmn/black/med/base/g=
lyph.gif">)-sulpride=20
(<A class=3Dcompound=20
href=3D"http://www.nature.com/nchembio/journal/v3/n5/compound/nchembio873=
_COMP17.html"><SPAN=20
class=3Dhidden>Compound </SPAN>17</A>), a D2 dopamine receptor =
antagonist, was=20
able to competitively rescue the inhibitory effects of the D2 and D3 =
dopamine=20
receptor agonist bromocriptine (<A class=3Dcompound=20
href=3D"http://www.nature.com/nchembio/journal/v3/n5/compound/nchembio873=
_COMP18.html"><SPAN=20
class=3Dhidden>Compound </SPAN>18</A>), as judged by both colony =
formation (<A=20
href=3D"http://www.nature.com/nchembio/journal/v3/n5/full/nchembio873.htm=
l#f4">Fig.=20
4e,f</A>) and MTT values (data not shown). To further assess the =
potential for=20
off-target effects of neuromodulators in other classes, we clustered the =
160=20
bioactive agents from the primary screen based on their chemical =
structures (<A=20
href=3D"http://www.nature.com/nchembio/journal/v3/n5/suppinfo/nchembio873=
_S1.html">Supplementary=20
Table 1</A>). This analysis demonstrated substantial chemical structural =

diversity within each of the different neuromodulator classes. For =
example, the=20
22 bioactive dopamine agents identified in the screen spanned 10 =
different=20
structural motif clusters; similarly, the 12 active serotonergic agents =
covered=20
10 different chemical clusters (<A=20
href=3D"http://www.nature.com/nchembio/journal/v3/n5/suppinfo/nchembio873=
_S1.html">Supplementary=20
Fig. 1</A> online). The observed sensitivity of NPCs to these =
structurally=20
diverse agents is thus likely to arise through effects on known=20
neurotransmission receptors, as opposed to some unknown coincident =
target.</P>
<P class=3Dnorm>The <I>ex vivo</I> and <I>in situ</I> manipulation of =
NSCs for=20
treating neurological disorders, including brain cancer, will require an =

understanding of the global signaling network that regulates NSC =
behavior.=20
Through a chemical genetic approach we have uncovered the existence of a =
complex=20
functional 'ground state', whereby NSC proliferation and self-renewal is =

regulated by numerous signaling pathways (<A=20
href=3D"http://www.nature.com/nchembio/journal/v3/n5/full/nchembio873.htm=
l#f4">Fig.=20
4g,h</A>). Importantly, this cohort includes many neurotransmission =
pathways=20
previously thought to function only in mature cells of the CNS. =
Therefore, we=20
infer that NSC proliferation and self-renewal requires an appropriate =
local=20
environment of neurotransmitter activities, which may be provided by a =
basal=20
level of autocrine feedback from more committed cells within the =
neurosphere or=20
even the NSC itself. Indeed, recent studies on individual pathways =
support the=20
notion that proliferation of different progenitor subpopulations <I>in =
vivo</I>=20
may respond to dopamine, serotonin, acetylcholine and glutamate<SUP><A=20
href=3D"http://www.nature.com/nchembio/journal/v3/n5/full/nchembio873.htm=
l#B18">18</A></SUP>.=20
Notably, our chemical genetic profile demonstrates the simultaneous =
operation of=20
these pathways in NPCs cultured under uniform experimental conditions. =
This=20
sensitivity of NPC cultures to a spectrum of neuroactive compounds also =
supports=20
the notion of lineage priming in the NSC compartment, similar to that =
seen in=20
hematopoietic stem cells<SUP><A=20
href=3D"http://www.nature.com/nchembio/journal/v3/n5/full/nchembio873.htm=
l#B19">19</A></SUP>.</P>
<P class=3Dnorm>Though we have yet to definitively identify the =
precursor=20
subpopulations targeted by each inhibitor identified in the screen, the =
strong=20
selectivity of many agents for NPCs and primary brain tumor cells =
suggests that=20
the affected pathways lie high in the hierarchical organization of the =
neuronal=20
lineage. Indeed, the often complete inhibition of neurosphere =
proliferation and=20
the effects on secondary replating suggest that stem cells and/or very =
early=20
progenitor components of the population are affected by these agents. =
The=20
finding that both inhibitors and activators of specific pathways inhibit =

neurosphere proliferation (for example, dopamine receptor agonists and=20
antagonists) suggests that a complex signaling landscape dictates NSC=20
fate<SUP><A=20
href=3D"http://www.nature.com/nchembio/journal/v3/n5/full/nchembio873.htm=
l#B20">20</A></SUP>.=20
We note that the pro-proliferative culture conditions used in the =
neurosphere=20
assay may have biased the assay against identification of significant =
numbers of=20
small molecules that stimulate proliferation. A small-molecule activator =
of=20
embryonic stem cell proliferation has recently been identified<SUP><A=20
href=3D"http://www.nature.com/nchembio/journal/v3/n5/full/nchembio873.htm=
l#B21">21</A></SUP>,=20
which suggests that analogous screens may succeed in identifying =
activators of=20
NPC proliferation.</P>
<P class=3Dnorm>The unanticipated actions of well-characterized clinical =
agents on=20
NPCs may account in whole or in part for the observed clinical benefits =
of these=20
agents and/or the adverse side effects that arise after prolonged =
therapy.=20
Effective <I>in vivo</I> concentrations of the anti-Parkinsonian drug=20
apomorphine reach 6=967 <IMG=20
style=3D"BORDER-TOP-WIDTH: 0px; BORDER-LEFT-WIDTH: 0px; =
BORDER-BOTTOM-WIDTH: 0px; VERTICAL-ALIGN: middle; BORDER-RIGHT-WIDTH: =
0px"=20
alt=3Dmu =
src=3D"http://www.nature.com/__chars/mu/black/med/base/glyph.gif">M<SUP><=
A=20
href=3D"http://www.nature.com/nchembio/journal/v3/n5/full/nchembio873.htm=
l#B22">22</A></SUP>,=20
which is substantially higher than doses that affect NPCs <I>in =
vitro</I>. Thus=20
the regulation of NSC proliferation by neurotransmitters may also =
dictate how=20
the CNS is wired both during development and in the adult brain<SUP><A=20
href=3D"http://www.nature.com/nchembio/journal/v3/n5/full/nchembio873.htm=
l#B23">23</A></SUP>.=20
Recent evidence suggests that appropriate GABA stimulation of NPCs is =
required=20
for the proper integration of neurons in the adult hippocampus<SUP><A=20
href=3D"http://www.nature.com/nchembio/journal/v3/n5/full/nchembio873.htm=
l#B24">24</A></SUP>.=20
Through structure-activity analysis, we also identified specific =
chemical=20
substitutions that are important for the bioactivity of these agents in =
our=20
<I>in vitro</I> system (<A=20
href=3D"http://www.nature.com/nchembio/journal/v3/n5/suppinfo/nchembio873=
_S1.html">Supplementary=20
Figs. 2</A> and <A=20
href=3D"http://www.nature.com/nchembio/journal/v3/n5/suppinfo/nchembio873=
_S1.html">3</A>=20
online). Such modifications to the core chemical structure of many =
clinically=20
used agents may afford a way to regulate the potentially therapeutic or =
harmful=20
effects these drugs have on NPCs.</P>
<P class=3Dnorm>In light of the evidence that CNS tumors are maintained =
by cancer=20
stem cells<SUP><A=20
href=3D"http://www.nature.com/nchembio/journal/v3/n5/full/nchembio873.htm=
l#B1">1,</A></SUP><SUP><A=20
href=3D"http://www.nature.com/nchembio/journal/v3/n5/full/nchembio873.htm=
l#B3">3</A></SUP>,=20
which have similarities to normal NSCs<SUP><A=20
href=3D"http://www.nature.com/nchembio/journal/v3/n5/full/nchembio873.htm=
l#B11">11</A></SUP>,=20
the potent and selective antiproliferative agents identified in this =
study may=20
presage a new generation of therapeutic agents in brain cancer, although =
further=20
<I>in vivo</I> testing is required<SUP><A=20
href=3D"http://www.nature.com/nchembio/journal/v3/n5/full/nchembio873.htm=
l#B3">3</A></SUP>.=20
Notably, a retrospective analysis of cancer incidence in individuals =
with=20
Parkinson disease revealed a significant reduction in the incidence of =
brain=20
tumors relative to the expected incidence in the general =
population<SUP><A=20
href=3D"http://www.nature.com/nchembio/journal/v3/n5/full/nchembio873.htm=
l#B25">25</A></SUP>;=20
this correlation may derive from the effect of anti-Parkinsonian drugs =
on the=20
NPCs from which brain tumors are thought to arise. As the complex NSC =
ground=20
state we propose is likely to at least in part define the identity of =
brain=20
tumor stem cells, re-deployment of pharmacologically approved =
neuroactive agents=20
may provide an immediate and nontoxic means to treat often intractable =
CNS=20
tumors.</P>
<DIV id=3DMethods><A class=3Dbacktotop=20
href=3D"http://www.nature.com/nchembio/journal/v3/n5/full/nchembio873.htm=
l#top">Top<SPAN=20
class=3Dhidden> of page</SPAN></A>
<H3>Methods</H3>
<DIV id=3DPrimary-embryonic-mouse-NSC-isolation-and-culture.>
<H4 class=3Dnorm>Primary embryonic mouse NSC isolation and culture.</H4>
<P class=3Dfollows-h4>Isolation and culture of primary embryonic (e14.5) =
mouse=20
NSCs was performed as previously described in chemically defined NSC=20
medium<SUP><A=20
href=3D"http://www.nature.com/nchembio/journal/v3/n5/full/nchembio873.htm=
l#B26">26</A></SUP>=20
containing 20 ng ml<SUP>-1</SUP> human recombinant epidermal growth =
factor=20
(Sigma), 20 ng ml<SUP>-1</SUP> basic fibroblast growth factor (Upstate) =
and 2=20
<IMG=20
style=3D"BORDER-TOP-WIDTH: 0px; BORDER-LEFT-WIDTH: 0px; =
BORDER-BOTTOM-WIDTH: 0px; VERTICAL-ALIGN: middle; BORDER-RIGHT-WIDTH: =
0px"=20
alt=3Dmu =
src=3D"http://www.nature.com/__chars/mu/black/med/base/glyph.gif">g=20
ml<SUP>-1</SUP> heparin (Sigma). Cells were fed every 2=963 d<SUP><A=20
href=3D"http://www.nature.com/nchembio/journal/v3/n5/full/nchembio873.htm=
l#B27">27</A></SUP>.</P></DIV>
<DIV id=3DSecondary-mouse-NSC-neurosphere-culture-and-chemical-screens.>
<H4 class=3Dnorm>Secondary mouse NSC neurosphere culture and chemical=20
screens.</H4>
<P class=3Dfollows-h4>Before chemical screens and other manipulations, =
the NSC=20
fraction in culture was expanded by growing freshly dissected cells as =
primary=20
neurospheres<SUP><A=20
href=3D"http://www.nature.com/nchembio/journal/v3/n5/full/nchembio873.htm=
l#B28">28</A></SUP>=20
in bulk culture (10<SUP>6</SUP> cells ml<SUP>-1</SUP>). After 7 d, =
primary=20
neurospheres were collected and enzymatically digested for 3 min at 37 =
=B0C using=20
Accutase (Sigma), mechanically dissociated with a 1-ml pipette and =
passed=20
through a cell strainer (Falcon). Viable cells were plated at low cell =
densities=20
(20 cells <IMG=20
style=3D"BORDER-TOP-WIDTH: 0px; BORDER-LEFT-WIDTH: 0px; =
BORDER-BOTTOM-WIDTH: 0px; VERTICAL-ALIGN: middle; BORDER-RIGHT-WIDTH: =
0px"=20
alt=3Dmu=20
src=3D"http://www.nature.com/__chars/mu/black/med/base/glyph.gif">l<SUP>-=
1</SUP>)=20
in 96-well plates (Falcon) in a final volume of 100 <IMG=20
style=3D"BORDER-TOP-WIDTH: 0px; BORDER-LEFT-WIDTH: 0px; =
BORDER-BOTTOM-WIDTH: 0px; VERTICAL-ALIGN: middle; BORDER-RIGHT-WIDTH: =
0px"=20
alt=3Dmu =
src=3D"http://www.nature.com/__chars/mu/black/med/base/glyph.gif">l and=20
screened in singlets against the LOPAC library (Sigma) at a =
concentration of 3=20
<IMG=20
style=3D"BORDER-TOP-WIDTH: 0px; BORDER-LEFT-WIDTH: 0px; =
BORDER-BOTTOM-WIDTH: 0px; VERTICAL-ALIGN: middle; BORDER-RIGHT-WIDTH: =
0px"=20
alt=3Dmu =
src=3D"http://www.nature.com/__chars/mu/black/med/base/glyph.gif">M =
(0.03%=20
DMSO). On day 4, each well in the screen was supplemented with an =
additional 50=20
<IMG=20
style=3D"BORDER-TOP-WIDTH: 0px; BORDER-LEFT-WIDTH: 0px; =
BORDER-BOTTOM-WIDTH: 0px; VERTICAL-ALIGN: middle; BORDER-RIGHT-WIDTH: =
0px"=20
alt=3Dmu =
src=3D"http://www.nature.com/__chars/mu/black/med/base/glyph.gif">l of=20
fresh mouse NSC medium and another aliquot of the LOPAC library =
(maintaining the=20
final concentration of each compound at 3 <IMG=20
style=3D"BORDER-TOP-WIDTH: 0px; BORDER-LEFT-WIDTH: 0px; =
BORDER-BOTTOM-WIDTH: 0px; VERTICAL-ALIGN: middle; BORDER-RIGHT-WIDTH: =
0px"=20
alt=3Dmu =
src=3D"http://www.nature.com/__chars/mu/black/med/base/glyph.gif">M).=20
Secondary neurosphere cultures were then incubated for an additional 3 d =
(until=20
day 7), at which point the effect of each compound was assessed by =
quantifying=20
the total proliferation of each well using the incorporation of the =
vital dye=20
MTT (Sigma) as previously described<SUP><A=20
href=3D"http://www.nature.com/nchembio/journal/v3/n5/full/nchembio873.htm=
l#B29">29</A></SUP>.</P></DIV>
<DIV id=3DStatistical-analysis-for-chemical-screen.>
<H4 class=3Dnorm>Statistical analysis for chemical screen.</H4>
<P class=3Dfollows-h4>Background plate effects (<A=20
href=3D"http://www.nature.com/nchembio/journal/v3/n5/suppinfo/nchembio873=
_S1.html">Supplementary=20
Methods</A>) occurring from the evaporation of medium over the course of =
the=20
experiment were estimated by:</P>
<P class=3Dnorm></P>
<P class=3Dnorm><IMG class=3Dalign-middle=20
alt=3D"Unfortunately we are unable to provide accessible alternative =
text for this. If you require assistance to access this image, or to =
obtain a text description, please contact npg@nature.com"=20
src=3D"http://www.nature.com/nchembio/journal/v3/n5/images/nchembio873-M1=
.gif"></P>
<P class=3Dnorm></P>
<P class=3Dnorm>where <I>x'<SUB>i,j</SUB></I> is the value at well =
<I>i</I> of=20
plate <I>j</I>, <I>N<SUB>i</SUB><SUP>h</SUP></I> is the number of =
excluded hits=20
or outliers that were 2 s.d. below the mean, <I>N</I> is the total =
number of=20
plates in the screen, and <I>b</I><SUB><I>i</I></SUB> is the estimated=20
background at each well position<SUP><A=20
href=3D"http://www.nature.com/nchembio/journal/v3/n5/full/nchembio873.htm=
l#B30">30</A></SUP>.=20
The respective background was then subtracted from the raw MTT value =
measured=20
for each point (<A=20
href=3D"http://www.nature.com/nchembio/journal/v3/n5/suppinfo/nchembio873=
_S1.html">Supplementary=20
Methods</A>). To calculate significance (<I>z</I> score and <I>P</I> =
value), the=20
theoretical probability density function <I>N</I>(1.0, 0.11) was fitted =
to the=20
empirical normalized distribution obtained from the screen (<A=20
href=3D"http://www.nature.com/nchembio/journal/v3/n5/suppinfo/nchembio873=
_S1.html">Supplementary=20
Methods</A>). Compounds that caused optical density readings to =
significantly=20
deviate from this predicted underlying distribution function (<I>P</I> =
&lt;=20
0.01) were designated as bioactive<SUP><A=20
href=3D"http://www.nature.com/nchembio/journal/v3/n5/full/nchembio873.htm=
l#B31">31</A></SUP>.</P></DIV>
<DIV id=3DDose-response-curves-and-EC50-calculations.>
<H4 class=3Dnorm>Dose-response curves and EC<SUB>50</SUB> =
calculations.</H4>
<P class=3Dfollows-h4>Potency of confirmed bioactive compounds was =
quantified by=20
generating dose-response curves for mouse NSC under the same cell =
density and=20
culture conditions described for the initial screen. Starting from =
initial=20
concentrations between 300 and 30 <IMG=20
style=3D"BORDER-TOP-WIDTH: 0px; BORDER-LEFT-WIDTH: 0px; =
BORDER-BOTTOM-WIDTH: 0px; VERTICAL-ALIGN: middle; BORDER-RIGHT-WIDTH: =
0px"=20
alt=3Dmu =
src=3D"http://www.nature.com/__chars/mu/black/med/base/glyph.gif">M, =
each=20
compound was titrated across a series of ten half-log dilutions. Each =
agent was=20
tested in triplicate in at least three independent experiments. =
EC<SUB>50</SUB>=20
values for each agent were calculated by fitting the data points to the=20
four-parameter logistic sigmoidal dose-response curve:</P>
<P class=3Dnorm></P>
<P class=3Dnorm><IMG class=3Dalign-middle=20
alt=3D"Unfortunately we are unable to provide accessible alternative =
text for this. If you require assistance to access this image, or to =
obtain a text description, please contact npg@nature.com"=20
src=3D"http://www.nature.com/nchembio/journal/v3/n5/images/nchembio873-M2=
.gif"></P>
<P class=3Dnorm></P>
<P class=3Dnorm>where <I>X</I> is the logarithm of concentration and =
<I>Y</I> is=20
the predicted response. Curve fitting was performed with GraphPad Prism =
software=20
(GraphPad Software, Inc.).</P></DIV></DIV>
<P class=3Dnorm><I>Note: <A=20
href=3D"http://www.nature.com/nchembio/journal/v3/n5/suppinfo/nchembio873=
_S1.html">Supplementary=20
information</A> and <A=20
href=3D"http://www.nature.com/nchembio/journal/v3/n5/compound/nchembio873=
_ci.html">chemical=20
compound information</A>is available on the Nature Chemical Biology=20
website.</I></P></DIV>
<DIV id=3DAcknowledgements><A class=3Dbacktotop=20
href=3D"http://www.nature.com/nchembio/journal/v3/n5/full/nchembio873.htm=
l#top">Top<SPAN=20
class=3Dhidden> of page</SPAN></A>
<H3>Acknowledgments</H3>
<P class=3Dfollows-h5>We thank L. Lee, P. Northcode and S. Dolma for =
technical=20
expertise, G. Giaever and C. Nislow for access to cheminformatics =
software, and=20
S. Cordes for critical suggestions regarding pharmacological rescue =
experiments.=20
P.D. is supported by a Canadian Institutes of Health Research (CIHR) =
MD/PhD=20
studentship. P.B.D. is supported by grants from the National Cancer =
Institute of=20
Canada, with funds from the Canadian Cancer Society, CIHR and the Stem =
Cell=20
Network, and from donations from BrainChild and the Durigon (Jessica's=20
Footprint), Baker, Blyth and Kolic families. M.T. is supported by grants =
from=20
the CIHR and a Canada Research Chair in Bioinformatics and Functional=20
Genomics.</P></DIV>
<DIV id=3Dancillary-details><A class=3Dhidden=20
href=3D"http://www.nature.com/nchembio/journal/v3/n5/full/nchembio873.htm=
l#top">Top<SPAN=20
class=3Dhidden> of page</SPAN></A>
<H3 class=3Dhidden>Ancillary details</H3>
<DIV id=3Dcompeting-interests>
<H4 class=3Dnorm>Competing interests</H4>
<P class=3Dfollows-h4>The authors declare that they have no competing =
financial=20
interests.</P></DIV>
<P class=3Dprdates>Received 14 September 2006; Accepted 14 March 2007; =
Published=20
online 8 April 2007.</P></DIV>
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t">PubMed</A>&nbsp;|&nbsp;<A=20
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  title=3D"Article on ChemPort - GABA sets the tempo for =
activity-dependent adult neurogenesis"=20
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href=3D"http://chemport.cas.org/cgi-bin/sdcgi?APP=3Dftslink&amp;action=3D=
reflink&amp;origin=3Dnpg&amp;version=3D1.0&amp;coi=3D1:CAS:528:DC%2BD2sXh=
sFWrsA%3D%3D&amp;pissn=3D1552-4450&amp;pyear=3D2007&amp;md5=3Df4b83e46893=
9c27c12f45a7f8d10c3de">ChemPort</A>&nbsp;|
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answer from Parkinson's disease"=20
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;|&nbsp;<A=20
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for breast cancer? An answer from Parkinson's disease"=20
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md=3DRetrieve&amp;db=3DPubMed&amp;list_uids=3D14659314&amp;dopt=3DAbstrac=
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sp;<A=20
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response to EGF and FGF in the developing mouse telencephalon"=20
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in response to EGF and FGF in the developing mouse telencephalon"=20
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reflink&amp;origin=3Dnpg&amp;version=3D1.0&amp;coi=3D1:CAS:528:DyaK1MXhsl=
ejtLc%3D&amp;pissn=3D1552-4450&amp;pyear=3D2007&amp;md5=3D8f050c9814c3c30=
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<SPAN=20
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behave as mitogenic regulators for a single multipotent stem cell-like =
population from the subventricular region of the adult mouse forebrain"=20
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t">PubMed</A>&nbsp;|&nbsp;<A=20
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behave as mitogenic regulators for a single multipotent stem cell-like =
population from the subventricular region of the adult mouse forebrain"=20
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rd&amp;KeyUT=3D000079883700002&amp;DestApp=3DWOS_CPL">ISI</A>&nbsp;|&nbsp=
;<A=20
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behave as mitogenic regulators for a single multipotent stem cell-like =
population from the subventricular region of the adult mouse forebrain"=20
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reflink&amp;origin=3Dnpg&amp;version=3D1.0&amp;coi=3D1:CAS:528:DyaK1MXisl=
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33e3b3f416c721d8c">ChemPort</A>&nbsp;|
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t">PubMed</A>&nbsp;|&nbsp;<A=20
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human brain tumors"=20
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human brain tumors"=20
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reflink&amp;origin=3Dnpg&amp;version=3D1.0&amp;coi=3D1:CAS:528:DC%2BD3sXn=
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sp;<A=20
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in high-throughput screening"=20
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md=3DRetrieve&amp;db=3DPubMed&amp;list_uids=3D16103415&amp;dopt=3DAbstrac=
t">PubMed</A>&nbsp;|
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<DIV class=3Dno-header><A class=3Dbacktotop=20
href=3D"http://www.nature.com/nchembio/journal/v3/n5/full/nchembio873.htm=
l#top">Top<SPAN=20
class=3Dhidden> of page</SPAN></A></DIV>
<DIV id=3Daffiliations-notes>
<OL>
  <LI id=3Da1>The Arthur and Sonia Labatt Brain Tumor Research Centre, =
The=20
  Hospital for Sick Children and University of Toronto, 555 University =
Avenue,=20
  Toronto M5G 1X8, Canada.
  <LI id=3Da2>Program in Developmental and Stem Cell Biology, The =
Hospital for=20
  Sick Children and University of Toronto, 555 University Avenue, =
Toronto M5G=20
  1X8, Canada.
  <LI id=3Da3>Samuel Lunenfeld Research Institute, Mount Sinai Hospital, =
600=20
  University Avenue, Toronto M5G 1X5, Canada.
  <LI id=3Da4>Department of Medical Genetics and Microbiology, =
University of=20
  Toronto, 1 Kings College Circle, Toronto M5S 1A8, Canada.
  <LI id=3Da5>Department of Laboratory Medicine and Pathobiology, =
Faculty of=20
  Medicine, University of Toronto, Banting Institute, 100 College =
Street,=20
  Toronto M5G 1L5, Canada.
  <LI id=3Da6>Division of Neurosurgery, The Hospital for Sick Children =
and=20
  University of Toronto, 555 University Avenue, Toronto M5G 1X8, =
Canada.</LI></OL>
<P class=3Dcaff>Correspondence to: Mike Tyers<SUP><A title=3D"affiliated =
with "=20
href=3D"http://www.nature.com/nchembio/journal/v3/n5/full/nchembio873.htm=
l#a3">3</A>,</SUP><SUP><A=20
title=3D"affiliated with "=20
href=3D"http://www.nature.com/nchembio/journal/v3/n5/full/nchembio873.htm=
l#a4">4</A></SUP>=20
Email:&nbsp;<A =
href=3D"mailto:tyers@mshri.on.ca">tyers@mshri.on.ca</A></P>
<P class=3Dcaff>Correspondence to: Peter B Dirks<SUP><A =
title=3D"affiliated with "=20
href=3D"http://www.nature.com/nchembio/journal/v3/n5/full/nchembio873.htm=
l#a1">1</A>,</SUP><SUP><A=20
title=3D"affiliated with "=20
href=3D"http://www.nature.com/nchembio/journal/v3/n5/full/nchembio873.htm=
l#a2">2</A>,</SUP><SUP><A=20
title=3D"affiliated with "=20
href=3D"http://www.nature.com/nchembio/journal/v3/n5/full/nchembio873.htm=
l#a5">5</A>,</SUP><SUP><A=20
title=3D"affiliated with "=20
href=3D"http://www.nature.com/nchembio/journal/v3/n5/full/nchembio873.htm=
l#a6">6</A></SUP>=20
Email:&nbsp;<A=20
href=3D"mailto:peter.dirks@sickkids.ca">peter.dirks@sickkids.ca</A></P></=
DIV></DIV>
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	FONT-STYLE: italic
}
H1.page-header {
	FONT-WEIGHT: bold; FONT-SIZE: 140%; PADDING-BOTTOM: 4px; MARGIN: 15px =
0px 10px; BORDER-BOTTOM: #eaeaea 1px solid
}
SPAN.page-header-spacer {
	DISPLAY: block; FONT-WEIGHT: bold; FONT-SIZE: 140%; VISIBILITY: hidden; =
PADDING-BOTTOM: 4px; MARGIN: 15px 0px 0px
}
SPAN.booktitle {
	FONT-STYLE: italic
}
SPAN.journalname {
	FONT-STYLE: italic
}
SPAN.journalnumber {
	FONT-WEIGHT: bold
}
SPAN.tm {
	VERTICAL-ALIGN: super
}
LEGEND {
	COLOR: #000
}
* HTML #breadcrumb DIV {
	MARGIN-TOP: 0px; PADDING-LEFT: 5px; PADDING-TOP: 1px
}
#breadcrumb DIV {
	CLEAR: left; MARGIN-TOP: 0px; PADDING-LEFT: 5px; BACKGROUND: #fff; =
PADDING-BOTTOM: 10px; PADDING-TOP: 1px
}
#breadcrumb DIV A:link {
	FONT-SIZE: 70%; COLOR: #000; TEXT-DECORATION: none
}
#breadcrumb DIV A:visited {
	FONT-SIZE: 70%; COLOR: #000; TEXT-DECORATION: none
}
#breadcrumb DIV A:hover {
	COLOR: #000; TEXT-DECORATION: underline
}
#breadcrumb SPAN.divider {
	FONT-SIZE: 70%; COLOR: #000
}
#breadcrumb SPAN.thisitem {
	FONT-SIZE: 70%; COLOR: #000
}
#login-inpage {
	MARGIN: 0px; COLOR: #000; BACKGROUND-COLOR: #eaeaea
}
#login-inpage A {
	FONT-SIZE: 70%
}
#login-inpage DIV.userpassbox {
	FLOAT: left; WIDTH: 8em
}
#login-inpage .passdetails {
	CLEAR: left
}
#login-inpage INPUT.text {
	FONT-SIZE: 80%; MARGIN: 0px; WIDTH: 9em; COLOR: #000
}
#login-inpage LABEL {
	FONT-SIZE: 70%
}
#login-inpage INPUT.button {
	MARGIN-TOP: 5px
}
#login-inpage #savepass-inpage {
	MARGIN-BOTTOM: -2px
}
#login-inpage DIV.error {
	PADDING-LEFT: 20px; FONT-SIZE: 80%; BACKGROUND: =
url(/common/images/login_error.gif) no-repeat 0px 4px; MARGIN-BOTTOM: =
5px; COLOR: #c30
}
#login-inpage DIV.error SPAN {
	FONT-WEIGHT: bold
}
#head-er HR {
	DISPLAY: none
}
#head-er .header-nonad-wrapper {
	PADDING-BOTTOM: 15px; BORDER-BOTTOM: #fff 1px solid
}
#head-er .accessibility-login-wrap {
	FLOAT: left; WIDTH: 100%; BORDER-BOTTOM: #000 1px solid; =
BACKGROUND-COLOR: #eaeaea
}
#head-er .accessibility-login {
	PADDING-RIGHT: 0px; PADDING-LEFT: 0px; PADDING-BOTTOM: 5px; =
PADDING-TOP: 4px; TEXT-ALIGN: right
}
#head-er .accessibility-login A.nature-link {
	FLOAT: left; FONT: bold 160%/80% Garamond, serif; WIDTH: 4.9em; COLOR: =
#b1062e; MARGIN-RIGHT: 20px; TEXT-ALIGN: left; TEXT-DECORATION: none
}
* HTML #head-er .accessibility-login A.nature-link:hover {
	BACKGROUND: none transparent scroll repeat 0% 0%
}
#head-er .accessibility-login A.nature-link:hover {
	BACKGROUND: =
url(/common/includes/header/images/nature.com.underline.gif) no-repeat =
left bottom
}
#head-er .accessibility-login IMG.nature-logo {
	BORDER-TOP-WIDTH: 0px; BORDER-LEFT-WIDTH: 0px; FLOAT: left; =
BORDER-BOTTOM-WIDTH: 0px; MARGIN: 1px 20px 0px 0px; WIDTH: 82px! =
important; HEIGHT: 11px; BORDER-RIGHT-WIDTH: 0px
}
#head-er .accessibility-login .jumplinks {
	PADDING-RIGHT: 0px; PADDING-LEFT: 0px; FLOAT: left; PADDING-BOTTOM: =
0px; MARGIN: 0px; WIDTH: 45%; PADDING-TOP: 0px; LIST-STYLE-TYPE: none; =
TEXT-ALIGN: left
}
#head-er .accessibility-login .jumplinks LI {
	DISPLAY: inline; PADDING-LEFT: 15px
}
#head-er .accessibility-login .jumplinks LI.first {
	PADDING-LEFT: 0px
}
#head-er .accessibility-login .jumplinks A {
	PADDING-LEFT: 10px; BACKGROUND: =
url(/common/images/icons/b1062e/arrow_down.gif) no-repeat left center; =
COLOR: #000; TEXT-DECORATION: none
}
#head-er .accessibility-login .jumplinks A:hover {
	TEXT-DECORATION: underline
}
#head-er DIV.logon {
=09
}
#head-er .logon .onlyformacie {
	FONT-SIZE: 3px
}
#head-er .logon .onlyformacie {
	DISPLAY: none
}
#head-er .logon A.login {
	PADDING-RIGHT: 15px; PADDING-LEFT: 0px; FONT-WEIGHT: bold; BACKGROUND: =
url(/common/includes/header/images/logon.gif) no-repeat right center; =
PADDING-BOTTOM: 0px; TEXT-TRANSFORM: uppercase; COLOR: #b1062e; =
PADDING-TOP: 0px; LETTER-SPACING: -0.1em; TEXT-DECORATION: none
}
#head-er .logon A.login:hover {
	BACKGROUND: url(/common/includes/header/images/logon_over.gif) =
no-repeat right center; TEXT-DECORATION: underline
}
#head-er .logon A.login:active {
	BACKGROUND: url(/common/includes/header/images/logon.gif) no-repeat =
right center
}
#head-er .logon A.logoff {
	PADDING-RIGHT: 15px; PADDING-LEFT: 15px; FONT-WEIGHT: bold; BACKGROUND: =
url(/common/includes/header/images/logoff.gif) no-repeat right center; =
PADDING-BOTTOM: 0px; TEXT-TRANSFORM: uppercase; COLOR: #b1062e; =
PADDING-TOP: 0px; LETTER-SPACING: -0.1em; TEXT-DECORATION: none
}
#head-er .logon P {
	MARGIN: 0px
}
#head-er .logon .user {
	FONT-WEIGHT: bold
}
#head-er .logon .inst {
	FONT-WEIGHT: bold
}
#head-er .image-user-services-wrap {
	FLOAT: left; WIDTH: 100%; BACKGROUND-COLOR: #d6335c
}
#head-er .image-user-services {
	BORDER-BOTTOM: transparent 1px solid
}
* HTML #head-er .image-user-services {
	BORDER-BOTTOM-WIDTH: 0px
}
#head-er .image-user-services IMG.journal-header {
	BORDER-TOP-WIDTH: 0px; BORDER-LEFT-WIDTH: 0px; FLOAT: left; =
BORDER-BOTTOM-WIDTH: 0px; MARGIN: 0px; WIDTH: 344px; HEIGHT: 74px; =
BORDER-RIGHT-WIDTH: 0px
}
#head-er .user-services {
	FLOAT: right
}
#head-er .div1.user-services {
	WIDTH: 12.35em! important
}
#head-er .div2.user-services {
	WIDTH: 8.7em! important
}
#head-er .user-services UL {
	BORDER-RIGHT: #fff 0px solid; PADDING-RIGHT: 0px; BORDER-TOP: #fff 1px =
solid; PADDING-LEFT: 0px; PADDING-BOTTOM: 0px; MARGIN: 22px 0px 21px; =
BORDER-LEFT: #fff 1px solid; PADDING-TOP: 0px; BORDER-BOTTOM: #fff 0px =
solid; LIST-STYLE-TYPE: none; TEXT-ALIGN: right
}
#head-er .user-services UL.list1 {
	BORDER-RIGHT: #fff 1px solid
}
#head-er .user-services LI {
	BORDER-BOTTOM: #fff 1px solid
}
#head-er .user-services A {
	PADDING-RIGHT: 13px; DISPLAY: block; PADDING-LEFT: 0px; BACKGROUND: =
url(/common/images/icons/fff/arrow_s.gif) #767474 no-repeat right =
center; PADDING-BOTTOM: 1px; TEXT-TRANSFORM: uppercase; COLOR: #fff; =
PADDING-TOP: 1px; TEXT-DECORATION: none
}
#head-er .user-services A:hover {
	BACKGROUND: url(/common/images/icons/fff/arrow_s.gif) #000 no-repeat =
right center
}
#head-er .publications-search-wrap {
	BACKGROUND: #000
}
* HTML #head-er .publications-search {
	PADDING-BOTTOM: 3px; PADDING-TOP: 3px
}
#head-er .publications-search {
	PADDING-RIGHT: 0px; PADDING-LEFT: 0px; PADDING-BOTTOM: 4px; =
PADDING-TOP: 4px
}
* HTML #head-er .publications {
	MARGIN: 6px 0px 0px
}
#head-er .publications {
	PADDING-RIGHT: 0px; PADDING-LEFT: 0px; FLOAT: left; PADDING-BOTTOM: =
0px; MARGIN: 4px 0px 0px; PADDING-TOP: 0px; LIST-STYLE-TYPE: none
}
#head-er .publications LI {
	DISPLAY: inline; MARGIN-LEFT: 10px
}
#head-er .publications LI.first {
	MARGIN-LEFT: 0px
}
#head-er .publications A {
	PADDING-RIGHT: 15px; BACKGROUND: =
url(/common/images/icons/fff/arrow_s.gif) no-repeat right center; =
TEXT-TRANSFORM: uppercase; COLOR: #fff; TEXT-DECORATION: none
}
#head-er .publications A:hover {
	TEXT-DECORATION: underline
}
#head-er .search {
	TEXT-ALIGN: right
}
#head-er .search FORM {
	DISPLAY: inline; MARGIN: 0px
}
#head-er .search FORM A {
	PADDING-RIGHT: 14px; BACKGROUND: =
url(/common/images/icons/fff/arrow_s.gif) no-repeat right center; =
TEXT-TRANSFORM: uppercase; COLOR: #fff; TEXT-DECORATION: none
}
#head-er .search FORM A:hover {
	TEXT-DECORATION: underline
}
#head-er #searchtext {
	WIDTH: 10em
}
#head-er .publications-search LABEL {
	TEXT-TRANSFORM: uppercase; COLOR: #fff
}
#head-er INPUT {
	FONT-SIZE: 100%
}
#head-er SELECT {
	FONT-SIZE: 100%
}
#head-er .publications-search INPUT.button {
	PADDING-RIGHT: 3px; PADDING-LEFT: 3px; FONT-WEIGHT: bold; BACKGROUND: =
#eaeaea; PADDING-BOTTOM: 0px; COLOR: #000; PADDING-TOP: 0px
}
#head-er .accessibility-login {
	PADDING-RIGHT: 1%; PADDING-LEFT: 1%
}
#head-er .image-user-services {
	PADDING-RIGHT: 1%; PADDING-LEFT: 1%
}
#head-er .publications-search {
	PADDING-RIGHT: 1%; PADDING-LEFT: 1%
}
.header-leaderboard-wrap {
	PADDING-RIGHT: 1%; PADDING-LEFT: 1%; BACKGROUND: =
url(/common/includes/header/images/bg_leaderboard.gif) no-repeat 50% =
0px; OVERFLOW: hidden
}
.header-leaderboard {
	MAX-HEIGHT: 105px; TEXT-ALIGN: center
}
* HTML .header-leaderboard IMG {
	BORDER-BOTTOM-WIDTH: 1px
}
* HTML .header-leaderboard ilayer {
	BORDER-BOTTOM-WIDTH: 1px
}
* HTML .header-leaderboard IFRAME {
	BORDER-BOTTOM-WIDTH: 1px
}
* HTML .header-leaderboard EMBED {
	BORDER-BOTTOM-WIDTH: 1px
}
.header-leaderboard IMG {
	BORDER-TOP-WIDTH: 0px; PADDING-RIGHT: 0px; PADDING-LEFT: 0px; =
BORDER-LEFT-WIDTH: 0px; MIN-HEIGHT: 90px; MAX-WIDTH: 728px; =
PADDING-BOTTOM: 0px; PADDING-TOP: 0px; BORDER-BOTTOM: #fff 1px solid; =
HEIGHT: 90px; BORDER-RIGHT-WIDTH: 0px
}
.header-leaderboard ilayer {
	BORDER-TOP-WIDTH: 0px; PADDING-RIGHT: 0px; PADDING-LEFT: 0px; =
BORDER-LEFT-WIDTH: 0px; MIN-HEIGHT: 90px; MAX-WIDTH: 728px; =
PADDING-BOTTOM: 0px; PADDING-TOP: 0px; BORDER-BOTTOM: #fff 1px solid; =
HEIGHT: 90px; BORDER-RIGHT-WIDTH: 0px
}
.header-leaderboard IFRAME {
	BORDER-TOP-WIDTH: 0px; PADDING-RIGHT: 0px; PADDING-LEFT: 0px; =
BORDER-LEFT-WIDTH: 0px; MIN-HEIGHT: 90px; MAX-WIDTH: 728px; =
PADDING-BOTTOM: 0px; PADDING-TOP: 0px; BORDER-BOTTOM: #fff 1px solid; =
HEIGHT: 90px; BORDER-RIGHT-WIDTH: 0px
}
.header-leaderboard EMBED {
	BORDER-TOP-WIDTH: 0px; PADDING-RIGHT: 0px; PADDING-LEFT: 0px; =
BORDER-LEFT-WIDTH: 0px; MIN-HEIGHT: 90px; MAX-WIDTH: 728px; =
PADDING-BOTTOM: 0px; PADDING-TOP: 0px; BORDER-BOTTOM: #fff 1px solid; =
HEIGHT: 90px; BORDER-RIGHT-WIDTH: 0px
}
.header-leaderboard TABLE {
	BORDER-TOP-WIDTH: 0px; PADDING-RIGHT: 0px; PADDING-LEFT: 0px; =
BORDER-LEFT-WIDTH: 0px; MAX-WIDTH: 728px; PADDING-BOTTOM: 0px; =
MARGIN-LEFT: auto; WIDTH: 100%; MARGIN-RIGHT: auto; PADDING-TOP: 0px; =
BORDER-BOTTOM: #fff 1px solid; BORDER-RIGHT-WIDTH: 0px
}
* HTML .header-leaderboard TABLE IMG {
	HEIGHT: auto
}
#constrain {
	MARGIN-TOP: 14px
}
#global-subject-areas {
	BORDER-RIGHT: #ebebeb 1px solid; BORDER-TOP: #ebebeb 1px solid; =
BACKGROUND: #ebebeb; MARGIN: 0px 0px 20px; BORDER-LEFT: #ebebeb 1px =
solid; BORDER-BOTTOM: #ebebeb 1px solid
}
#global-subject-areas ABBR {
	BORDER-TOP-WIDTH: 0px; BORDER-LEFT-WIDTH: 0px; BORDER-BOTTOM-WIDTH: =
0px; BORDER-RIGHT-WIDTH: 0px; TEXT-DECORATION: none
}
#global-subject-areas A:link {
	FONT-WEIGHT: bold; COLOR: #9d0006; TEXT-DECORATION: none
}
#global-subject-areas A:visited {
	FONT-WEIGHT: bold; COLOR: #9d0006; TEXT-DECORATION: none
}
#global-subject-areas A:hover {
	TEXT-DECORATION: underline
}
#global-subject-areas H2 {
	PADDING-RIGHT: 10px; PADDING-LEFT: 10px; FONT-SIZE: 110%; BACKGROUND: =
#b1062e; PADDING-BOTTOM: 5px; MARGIN: 0px; COLOR: #fff; PADDING-TOP: =
5px; BORDER-BOTTOM: #fff 1px solid
}
#global-subject-areas H3 {
	PADDING-RIGHT: 10px; PADDING-LEFT: 10px; FONT-SIZE: 110%; BACKGROUND: =
#b1062e; PADDING-BOTTOM: 5px; MARGIN: 0px; COLOR: #fff; PADDING-TOP: =
5px; BORDER-BOTTOM: #fff 1px solid
}
#global-subject-areas H4 {
	PADDING-RIGHT: 10px; PADDING-LEFT: 10px; FONT-SIZE: 110%; BACKGROUND: =
#b1062e; PADDING-BOTTOM: 5px; MARGIN: 0px; COLOR: #fff; PADDING-TOP: =
5px; BORDER-BOTTOM: #fff 1px solid
}
#global-subject-areas H5 {
	PADDING-RIGHT: 10px; PADDING-LEFT: 10px; FONT-SIZE: 110%; BACKGROUND: =
#b1062e; PADDING-BOTTOM: 5px; MARGIN: 0px; COLOR: #fff; PADDING-TOP: =
5px; BORDER-BOTTOM: #fff 1px solid
}
#global-subject-areas H3.view {
	PADDING-RIGHT: 17px; PADDING-LEFT: 17px; FONT-SIZE: 100%; BACKGROUND: =
url(/common/images/bg.7x1.b1062e.gif) #fff repeat-y left top; =
PADDING-BOTTOM: 5px; MARGIN: 0px; COLOR: #9d0006; PADDING-TOP: 5px; =
BORDER-BOTTOM: #fff 1px solid
}
#global-subject-areas H4.view {
	PADDING-RIGHT: 17px; PADDING-LEFT: 17px; FONT-SIZE: 100%; BACKGROUND: =
url(/common/images/bg.7x1.b1062e.gif) #fff repeat-y left top; =
PADDING-BOTTOM: 5px; MARGIN: 0px; COLOR: #9d0006; PADDING-TOP: 5px; =
BORDER-BOTTOM: #fff 1px solid
}
#global-subject-areas H5.view {
	PADDING-RIGHT: 17px; PADDING-LEFT: 17px; FONT-SIZE: 100%; BACKGROUND: =
url(/common/images/bg.7x1.b1062e.gif) #fff repeat-y left top; =
PADDING-BOTTOM: 5px; MARGIN: 0px; COLOR: #9d0006; PADDING-TOP: 5px; =
BORDER-BOTTOM: #fff 1px solid
}
#global-subject-areas UL {
	PADDING-RIGHT: 0px; PADDING-LEFT: 0px; FONT-SIZE: 100%; PADDING-BOTTOM: =
0px; MARGIN: 0px; PADDING-TOP: 0px; LIST-STYLE-TYPE: none
}
#global-subject-areas UL UL {
	FONT-SIZE: 100%
}
#global-subject-areas UL LI {
	PADDING-RIGHT: 5px; PADDING-LEFT: 5px; PADDING-BOTTOM: 5px; =
LINE-HEIGHT: 150%; PADDING-TOP: 5px; BORDER-BOTTOM: #fff 1px solid
}
#global-subject-areas UL LI LI {
	PADDING-RIGHT: 0px; PADDING-LEFT: 5px; BORDER-BOTTOM-WIDTH: 0px; =
PADDING-BOTTOM: 0px; PADDING-TOP: 0px
}
#global-subject-areas UL LI H4 {
	BORDER-TOP-WIDTH: 0px; PADDING-RIGHT: 0px; PADDING-LEFT: 0px; =
FONT-WEIGHT: normal; BORDER-LEFT-WIDTH: 0px; FONT-SIZE: 100%; =
BACKGROUND: none transparent scroll repeat 0% 0%; BORDER-BOTTOM-WIDTH: =
0px; PADDING-BOTTOM: 0px; MARGIN: 0px; COLOR: #666; PADDING-TOP: 0px; =
FONT-STYLE: italic; BORDER-RIGHT-WIDTH: 0px
}
#global-subject-areas UL LI H5 {
	BORDER-TOP-WIDTH: 0px; PADDING-RIGHT: 0px; PADDING-LEFT: 0px; =
FONT-WEIGHT: normal; BORDER-LEFT-WIDTH: 0px; FONT-SIZE: 100%; =
BACKGROUND: none transparent scroll repeat 0% 0%; BORDER-BOTTOM-WIDTH: =
0px; PADDING-BOTTOM: 0px; MARGIN: 0px; COLOR: #666; PADDING-TOP: 0px; =
FONT-STYLE: italic; BORDER-RIGHT-WIDTH: 0px
}
#global-subject-areas UL LI H6 {
	BORDER-TOP-WIDTH: 0px; PADDING-RIGHT: 0px; PADDING-LEFT: 0px; =
FONT-WEIGHT: normal; BORDER-LEFT-WIDTH: 0px; FONT-SIZE: 100%; =
BACKGROUND: none transparent scroll repeat 0% 0%; BORDER-BOTTOM-WIDTH: =
0px; PADDING-BOTTOM: 0px; MARGIN: 0px; COLOR: #666; PADDING-TOP: 0px; =
FONT-STYLE: italic; BORDER-RIGHT-WIDTH: 0px
}
MAP.journal-nav {
	DISPLAY: block; MARGIN-BOTTOM: 20px
}
MAP.journal-nav UL {
	PADDING-RIGHT: 0px; PADDING-LEFT: 0px; PADDING-BOTTOM: 0px; MARGIN: =
0px; PADDING-TOP: 0px; LIST-STYLE-TYPE: none; TEXT-ALIGN: left
}
MAP.journal-nav UL LI {
	MARGIN: 0px; BORDER-BOTTOM: #fff 1px solid; BACKGROUND-COLOR: #eaeaea
}
MAP.journal-nav UL LI.grouped {
	BORDER-BOTTOM: #eaeaea 1px solid
}
* HTML MAP.journal-nav UL LI A {
	PADDING-RIGHT: 5px; PADDING-LEFT: 5px; PADDING-BOTTOM: 3px; =
PADDING-TOP: 2px
}
* HTML MAP.journal-nav UL LI A:visited {
	PADDING-RIGHT: 5px; PADDING-LEFT: 5px; PADDING-BOTTOM: 3px; =
PADDING-TOP: 2px
}
MAP.journal-nav UL LI A {
	PADDING-RIGHT: 5px; DISPLAY: block; PADDING-LEFT: 5px; FONT-WEIGHT: =
bold; FONT-SIZE: 80%; PADDING-BOTTOM: 4px; MARGIN: 0px; COLOR: #000; =
PADDING-TOP: 4px; TEXT-DECORATION: none
}
MAP.journal-nav UL LI A:visited {
	PADDING-RIGHT: 5px; DISPLAY: block; PADDING-LEFT: 5px; FONT-WEIGHT: =
bold; FONT-SIZE: 80%; PADDING-BOTTOM: 4px; MARGIN: 0px; COLOR: #000; =
PADDING-TOP: 4px; TEXT-DECORATION: none
}
MAP.journal-nav UL LI A:hover {
	COLOR: #fff; BACKGROUND-COLOR: #c00; TEXT-DECORATION: none
}
MAP.journal-nav UL LI A.on {
	COLOR: #fff; BACKGROUND-COLOR: #c00
}
MAP.journal-nav UL LI A.on:visited {
	COLOR: #fff; BACKGROUND-COLOR: #c00
}
MAP.journal-nav UL LI A.submission {
	PADDING-LEFT: 20px! important; BACKGROUND: =
url(/common/images/online_submissions.gif) no-repeat left center
}
MAP.journal-nav UL LI UL.subnav {
	BORDER-TOP-WIDTH: 0px; PADDING-RIGHT: 0px; PADDING-LEFT: 0px; =
PADDING-BOTTOM: 0px; MARGIN: 0px; PADDING-TOP: 0px; LIST-STYLE-TYPE: =
none; TEXT-ALIGN: left
}
MAP.journal-nav UL LI UL.subnav LI {
	BACKGROUND: url(/common/images/nav_dots2.gif) #fafafa no-repeat 11px =
5px; BORDER-BOTTOM-WIDTH: 0px; MARGIN: 0px
}
MAP.journal-nav UL LI UL.subnav LI.on {
	BACKGROUND: url(/common/images/nav_dots1.gif) #c00 no-repeat 11px 5px; =
BORDER-BOTTOM: #fafafa 1px solid
}
* HTML MAP.journal-nav UL LI UL.subnav A {
	PADDING-RIGHT: 10px! important; PADDING-LEFT: 20px! important; =
PADDING-BOTTOM: 2px! important; PADDING-TOP: 2px! important
}
MAP.journal-nav UL LI UL.subnav A:link {
	PADDING-RIGHT: 10px; DISPLAY: block; PADDING-LEFT: 20px; FONT-WEIGHT: =
normal; FONT-SIZE: 70%; PADDING-BOTTOM: 2px; MARGIN: 0px; COLOR: #000; =
PADDING-TOP: 2px; TEXT-DECORATION: none
}
MAP.journal-nav UL LI UL.subnav A:visited {
	PADDING-RIGHT: 10px; DISPLAY: block; PADDING-LEFT: 20px; FONT-WEIGHT: =
normal; FONT-SIZE: 70%; PADDING-BOTTOM: 2px; MARGIN: 0px; COLOR: #000; =
PADDING-TOP: 2px; TEXT-DECORATION: none
}
MAP.journal-nav UL LI UL.subnav A:hover {
	BACKGROUND: url(/common/images/nav_dots1.gif) #fab934 no-repeat 11px =
5px; COLOR: #fff; TEXT-DECORATION: none
}
MAP.journal-nav UL LI UL.subnav A.on {
	COLOR: #fff
}
MAP.journal-nav UL LI UL.subnav A.on:visited {
	COLOR: #fff
}
#journalnav MAP.supplementary UL A {
	FONT-WEIGHT: normal; FONT-SIZE: 70%
}
#journalnav MAP.supplementary UL A:visited {
	FONT-WEIGHT: normal; FONT-SIZE: 70%
}
H2.society-resources {
	PADDING-RIGHT: 5px; PADDING-LEFT: 5px; FONT-WEIGHT: bold; FONT-SIZE: =
80%; PADDING-BOTTOM: 2px; MARGIN: 0px; COLOR: #fff; PADDING-TOP: 2px; =
BACKGROUND-COLOR: #fab934
}
UL.society-resources {
	PADDING-RIGHT: 0px; PADDING-LEFT: 0px; PADDING-BOTTOM: 0px; MARGIN: 0px =
0px 20px; PADDING-TOP: 0px; LIST-STYLE-TYPE: none; TEXT-ALIGN: left
}
UL.society-resources LI {
	MARGIN: 0px; BACKGROUND-COLOR: #eaeaea
}
UL.society-resources A {
	PADDING-RIGHT: 5px! important; DISPLAY: block; PADDING-LEFT: 5px! =
important; FONT-SIZE: 70%; PADDING-BOTTOM: 3px! important; MARGIN: 0px; =
COLOR: #000; PADDING-TOP: 3px! important; TEXT-DECORATION: none
}
UL.society-resources A:visited {
	PADDING-RIGHT: 5px! important; DISPLAY: block; PADDING-LEFT: 5px! =
important; FONT-SIZE: 70%; PADDING-BOTTOM: 3px! important; MARGIN: 0px; =
COLOR: #000; PADDING-TOP: 3px! important; TEXT-DECORATION: none
}
UL.society-resources A:hover {
	COLOR: #fff; BACKGROUND-COLOR: #fab934; TEXT-DECORATION: none
}
DIV.society-logo {
	MARGIN-BOTTOM: 20px; TEXT-ALIGN: center
}
DIV.society-logo IMG {
	WIDTH: 100%
}
H2.npg-resources {
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Content-Type: text/css;
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url(/common/images/arrow_blue.gif) no-repeat 0px 0.5em
}
#article-related #browser-plugins LI A:visited {
	PADDING-LEFT: 10px; FONT-SIZE: 70%; BACKGROUND: =
url(/common/images/arrow_blue.gif) no-repeat 0px 0.5em
}
#article-related #browser-plugins LI A:hover {
	BACKGROUND: url(/common/images/arrow_red.gif) no-repeat 0px 0.5em
}
#article-related #content DIV.container-image-text H4 {
	FONT-SIZE: 90%; MARGIN-BOTTOM: 0px; PADDING-BOTTOM: 0px
}
#article-related #content DIV.container-image-text P.norm {
	PADDING-RIGHT: 0px; PADDING-LEFT: 0px; FONT-SIZE: 90%; PADDING-BOTTOM: =
0px; MARGIN: 0px; PADDING-TOP: 0px
}
.icon {
	PADDING-RIGHT: 0px; BACKGROUND-POSITION: left center; DISPLAY: block; =
PADDING-LEFT: 20px; PADDING-BOTTOM: 2px; PADDING-TOP: 2px; =
BACKGROUND-REPEAT: no-repeat
}
.i-audio {
	BACKGROUND-IMAGE: url(/common/images/icons/fafafa/audio.gif)
}
.i-audio-grey {
	BACKGROUND-IMAGE: url(/common/images/icons/fafafa/audio_grey.gif)
}
.i-bitmap {
	BACKGROUND-IMAGE: url(/common/images/icons/fafafa/bitmap.gif)
}
.i-bitmap-grey {
	BACKGROUND-IMAGE: url(/common/images/icons/fafafa/bitmap_grey.gif)
}
.i-compressed {
	BACKGROUND-IMAGE: url(/common/images/icons/fafafa/compressed.gif)
}
.i-compressed-grey {
	BACKGROUND-IMAGE: url(/common/images/icons/fafafa/compressed_grey.gif)
}
.i-markup {
	BACKGROUND-IMAGE: url(/common/images/icons/fafafa/markup.gif)
}
.i-markup-grey {
	BACKGROUND-IMAGE: url(/common/images/icons/fafafa/markup_grey.gif)
}
.i-movie {
	BACKGROUND-IMAGE: url(/common/images/icons/fafafa/movie.gif)
}
.i-movie-grey {
	BACKGROUND-IMAGE: url(/common/images/icons/fafafa/movie_grey.gif)
}
.i-pdf {
	BACKGROUND-IMAGE: url(/common/images/icons/fafafa/pdf.gif)
}
.i-pdf-grey {
	BACKGROUND-IMAGE: url(/common/images/icons/fafafa/pdf_grey.gif)
}
.i-postscript {
	BACKGROUND-IMAGE: url(/common/images/icons/fafafa/postscript.gif)
}
.i-postscript-grey {
	BACKGROUND-IMAGE: url(/common/images/icons/fafafa/postscript_grey.gif)
}
.i-powerpoint {
	BACKGROUND-IMAGE: url(/common/images/icons/fafafa/powerpoint.gif)
}
.i-powerpoint-grey {
	BACKGROUND-IMAGE: url(/common/images/icons/fafafa/powerpoint_grey.gif)
}
.i-svg {
	BACKGROUND-IMAGE: url(/common/images/icons/fafafa/svg.gif)
}
.i-svg-grey {
	BACKGROUND-IMAGE: url(/common/images/icons/fafafa/svg_grey.gif)
}
.i-word {
	BACKGROUND-IMAGE: url(/common/images/icons/fafafa/word.gif)
}
.i-word-grey {
	BACKGROUND-IMAGE: url(/common/images/icons/fafafa/word_grey.gif)
}
.i-xls {
	BACKGROUND-IMAGE: url(/common/images/icons/fafafa/xls.gif)
}
.i-xls-grey {
	BACKGROUND-IMAGE: url(/common/images/icons/fafafa/xls_grey.gif)
}
.plugin-audio {
	BACKGROUND-IMAGE: url(/common/images/icons/eaeaea/audio.gif)
}
.plugin-audio-grey {
	BACKGROUND-IMAGE: url(/common/images/icons/eaeaea/audio_grey.gif)
}
.plugin-bitmap {
	BACKGROUND-IMAGE: url(/common/images/icons/eaeaea/bitmap.gif)
}
.plugin-bitmap-grey {
	BACKGROUND-IMAGE: url(/common/images/icons/eaeaea/bitmap_grey.gif)
}
.plugin-compressed {
	BACKGROUND-IMAGE: url(/common/images/icons/eaeaea/compressed.gif)
}
.plugin-compressed-grey {
	BACKGROUND-IMAGE: url(/common/images/icons/eaeaea/compressed_grey.gif)
}
.plugin-markup {
	BACKGROUND-IMAGE: url(/common/images/icons/eaeaea/markup.gif)
}
.plugin-markup-grey {
	BACKGROUND-IMAGE: url(/common/images/icons/eaeaea/markup_grey.gif)
}
.plugin-movie {
	BACKGROUND-IMAGE: url(/common/images/icons/eaeaea/movie.gif)
}
.plugin-movie-grey {
	BACKGROUND-IMAGE: url(/common/images/icons/eaeaea/movie_grey.gif)
}
.plugin-pdf {
	BACKGROUND-IMAGE: url(/common/images/icons/eaeaea/pdf.gif)
}
.plugin-pdf-grey {
	BACKGROUND-IMAGE: url(/common/images/icons/eaeaea/pdf_grey.gif)
}
.plugin-postscript {
	BACKGROUND-IMAGE: url(/common/images/icons/eaeaea/postscript.gif)
}
.plugin-postscript-grey {
	BACKGROUND-IMAGE: url(/common/images/icons/eaeaea/postscript_grey.gif)
}
.plugin-powerpoint {
	BACKGROUND-IMAGE: url(/common/images/icons/eaeaea/powerpoint.gif)
}
.plugin-powerpoint-grey {
	BACKGROUND-IMAGE: url(/common/images/icons/eaeaea/powerpoint_grey.gif)
}
.plugin-svg {
	BACKGROUND-IMAGE: url(/common/images/icons/eaeaea/svg.gif)
}
.plugin-svg-grey {
	BACKGROUND-IMAGE: url(/common/images/icons/eaeaea/svg_grey.gif)
}
.plugin-word {
	BACKGROUND-IMAGE: url(/common/images/icons/eaeaea/word.gif)
}
.plugin-word-grey {
	BACKGROUND-IMAGE: url(/common/images/icons/eaeaea/word_grey.gif)
}
.plugin-xls {
	BACKGROUND-IMAGE: url(/common/images/icons/eaeaea/xls.gif)
}
.plugin-xls-grey {
	BACKGROUND-IMAGE: url(/common/images/icons/eaeaea/xls_grey.gif)
}
.plugin-microarray {
	BACKGROUND-IMAGE: url(/common/images/icons/eaeaea/microarray.gif)
}
.plugin-chemical-structures {
	BACKGROUND-IMAGE: =
url(/common/images/icons/eaeaea/chemical_structures.gif)
}
.plugin-text {
	BACKGROUND-IMAGE: url(/common/images/icons/eaeaea/text.gif)
}
#extranav .sponsor {
	PADDING-RIGHT: 15px; PADDING-LEFT: 15px; MARGIN-BOTTOM: 1.5em; =
PADDING-BOTTOM: 15px; PADDING-TOP: 15px; TEXT-ALIGN: center
}
#extranav .sponsor H1 {
	MARGIN-TOP: 0px; FONT-WEIGHT: normal; FONT-SIZE: 80%; TEXT-TRANSFORM: =
uppercase; PADDING-TOP: 0px
}
#extranav .sponsor IMG {
	BORDER-TOP-WIDTH: 0px; BORDER-LEFT-WIDTH: 0px; BORDER-BOTTOM-WIDTH: =
0px; MARGIN-BOTTOM: 5px; MAX-WIDTH: 105px; WIDTH: 100%; HEIGHT: 48px; =
BORDER-RIGHT-WIDTH: 0px
}
#extranav DIV.home-page-links LI {
	BACKGROUND-COLOR: #cce8f0
}
DIV.reg-rec UL {
	BORDER-RIGHT: #008cb4 1px solid; PADDING-RIGHT: 6px; BORDER-TOP: =
#008cb4 1px solid; PADDING-LEFT: 6px; PADDING-BOTTOM: 6px; MARGIN: 0px; =
BORDER-LEFT: #008cb4 1px solid; PADDING-TOP: 6px; BORDER-BOTTOM: #008cb4 =
1px solid; LIST-STYLE-TYPE: none; BACKGROUND-COLOR: #cce8f0
}
#extranav DIV.reg-rec UL LI {
	BACKGROUND-COLOR: #cce8f0
}
#extranav DIV.reg-rec UL.toc {
	BACKGROUND: #fafafa
}
#extranav DIV.reg-rec UL.toc LI {
	BACKGROUND: #fafafa
}
#extranav DIV.reg-rec A SPAN.rest {
	COLOR: #000
}
DIV.reg-rec UL LI {
	MARGIN: 0.5em 0px
}
DIV.reg-rec UL LI.first {
	MARGIN-TOP: 0.1em
}
DIV.reg-rec UL LI.last {
	MARGIN-BOTTOM: 0px
}
DIV.reg-rec UL A:link {
	PADDING-RIGHT: 0px; DISPLAY: block; PADDING-LEFT: 22px; FONT-SIZE: 70%; =
PADDING-BOTTOM: 0px; MARGIN: 0px; COLOR: #000; PADDING-TOP: 0px; =
TEXT-DECORATION: none
}
DIV.reg-rec UL A:visited {
	PADDING-RIGHT: 0px; DISPLAY: block; PADDING-LEFT: 22px; FONT-SIZE: 70%; =
PADDING-BOTTOM: 0px; MARGIN: 0px; COLOR: #000; PADDING-TOP: 0px; =
TEXT-DECORATION: none
}
DIV.reg-rec UL LI SPAN.link {
	PADDING-RIGHT: 0px; PADDING-LEFT: 0px; PADDING-BOTTOM: 0px; MARGIN: =
0px; PADDING-TOP: 0px
}
DIV.reg-rec UL A:hover {
	TEXT-DECORATION: underline
}
DIV.reg-rec UL A.e-alerts {
	BACKGROUND: url(/common/images/icons/cce8f0/envelope.gif) no-repeat 0px =
0.3em
}
* HTML DIV.reg-rec UL A.e-alerts {
	BACKGROUND: url(/common/images/icons/cce8f0/envelope.gif) no-repeat 0px =
0.7em
}
DIV.reg-rec UL A.recommend {
	BACKGROUND: url(/common/images/icons/cce8f0/tick.gif) no-repeat 0px =
0.2em; PADDING-BOTTOM: 1px; PADDING-TOP: 1px
}
* HTML DIV.reg-rec UL A.recommend {
	BACKGROUND: url(/common/images/icons/cce8f0/tick.gif) no-repeat 0px =
0.5em
}
#extranav DIV.reg-rec A.newsfeed:link {
	COLOR: #666
}
#extranav DIV.reg-rec A.newsfeed:visited {
	COLOR: #666
}
#extranav DIV.home-page-links UL A.pdf:link {
	PADDING-LEFT: 22px; BACKGROUND: =
url(/common/images/icons/fafafa/pdf.gif) #fafafa no-repeat 0px 2px; =
PADDING-BOTTOM: 3px; PADDING-TOP: 2px
}
#extranav DIV.home-page-links UL A.pdf:visited {
	PADDING-LEFT: 22px; BACKGROUND: =
url(/common/images/icons/fafafa/pdf.gif) #fafafa no-repeat 0px 2px; =
PADDING-BOTTOM: 3px; PADDING-TOP: 2px
}
* HTML #extranav DIV.home-page-links UL A.pdf:link {
	PADDING-LEFT: 22px; PADDING-BOTTOM: 0px; PADDING-TOP: 2px
}
* HTML #extranav DIV.home-page-links UL A.pdf:visited {
	PADDING-LEFT: 22px; PADDING-BOTTOM: 0px; PADDING-TOP: 2px
}
DIV.reg-rec UL A.newsfeeds {
	BACKGROUND: url(/common/images/icons/cce8f0/newsfeeds.gif) no-repeat =
0px 0.1em; PADDING-BOTTOM: 3px; COLOR: #000
}
* HTML DIV.reg-rec UL A.newsfeeds {
	BACKGROUND: url(/common/images/icons/cce8f0/newsfeeds.gif) no-repeat =
0px 0.2em
}
DIV.reg-rec UL.toc {
	BORDER-TOP-WIDTH: 0px; BACKGROUND-COLOR: #fafafa
}
DIV.reg-rec UL.toc A.purchase {
	BACKGROUND: url(/common/images/icons/fafafa/purchase-issue.gif) =
no-repeat 0px 0px; PADDING-BOTTOM: 4px; PADDING-TOP: 1px
}
DIV.reg-rec UL.toc A.bookmark {
	BACKGROUND: url(/common/images/icons/fafafa/bookmark.gif) no-repeat 0px =
0px; PADDING-BOTTOM: 4px; PADDING-TOP: 1px
}
DIV.reg-rec UL.toc A.pdf {
	BACKGROUND: url(/common/images/icons/fafafa/pdf.gif) no-repeat 0px 0px; =
PADDING-BOTTOM: 4px; PADDING-TOP: 1px
}
* HTML DIV.reg-rec UL.toc A.pdf {
	BACKGROUND: url(/common/images/icons/fafafa/pdf.gif) no-repeat 0px 0px; =
PADDING-BOTTOM: 0px; PADDING-TOP: 0px
}
#extranav DIV.home-page-links UL {
	BORDER-RIGHT: #008cb4 1px solid; PADDING-RIGHT: 6px; PADDING-LEFT: 6px; =
PADDING-BOTTOM: 6px; MARGIN: 0px; BORDER-LEFT: #008cb4 1px solid; =
BORDER-TOP-STYLE: none; PADDING-TOP: 6px; BORDER-BOTTOM: #008cb4 1px =
solid; LIST-STYLE-TYPE: none; BACKGROUND-COLOR: #fafafa
}
#extranav DIV.home-page-links UL LI {
	MARGIN: 0.5em 0px
}
#extranav DIV.home-page-links UL LI.first {
	MARGIN-TOP: 0.1em
}
#extranav DIV.home-page-links UL LI.last {
	MARGIN-BOTTOM: 0px
}
#extranav DIV.home-page-links UL A:link {
	PADDING-RIGHT: 0px; DISPLAY: block; PADDING-LEFT: 22px; FONT-SIZE: 70%; =
BACKGROUND: url(/common/images/arrow_black.gif) #fafafa no-repeat 0.5em =
0.5em; PADDING-BOTTOM: 0px; MARGIN: 0px; COLOR: #000; PADDING-TOP: 0px; =
TEXT-DECORATION: none
}
#extranav DIV.home-page-links UL A:visited {
	PADDING-RIGHT: 0px; DISPLAY: block; PADDING-LEFT: 22px; FONT-SIZE: 70%; =
BACKGROUND: url(/common/images/arrow_black.gif) #fafafa no-repeat 0.5em =
0.5em; PADDING-BOTTOM: 0px; MARGIN: 0px; COLOR: #000; PADDING-TOP: 0px; =
TEXT-DECORATION: none
}
* HTML #extranav DIV.home-page-links UL A:link {
	BACKGROUND: url(/common/images/arrow_black.gif) #fafafa no-repeat 0.5em =
0.8em
}
* HTML #extranav DIV.home-page-links UL A:visited {
	BACKGROUND: url(/common/images/arrow_black.gif) #fafafa no-repeat 0.5em =
0.8em
}
#extranav DIV.home-page-links UL LI SPAN.link {
	PADDING-RIGHT: 0px; PADDING-LEFT: 0px; PADDING-BOTTOM: 0px; MARGIN: =
0px; PADDING-TOP: 0px
}
#extranav DIV.home-page-links UL A:hover {
	TEXT-DECORATION: underline
}
#extranav DIV.ad-vert {
	MARGIN-TOP: 1.5em; BACKGROUND: #eaeaea
}
#extranav DIV.ad-vert P {
	PADDING-RIGHT: 0px; PADDING-LEFT: 0px; PADDING-BOTTOM: 0px; MARGIN: =
0px; PADDING-TOP: 0px
}
#extranav DIV.extra {
	BORDER-RIGHT: #000 1px solid; PADDING-RIGHT: 5px; BORDER-TOP: #000 1px =
solid; PADDING-LEFT: 5px; PADDING-BOTTOM: 5px; MARGIN: 1em 0px; =
BORDER-LEFT: #000 1px solid; PADDING-TOP: 5px; BORDER-BOTTOM: #000 1px =
solid
}
#extranav DIV.liteblue {
	BACKGROUND-COLOR: #cce8f0
}
#extranav DIV.liteblue LI {
	BORDER-BOTTOM: #cce8f0 1px solid
}
#extranav DIV.blue LI {
	BORDER-BOTTOM: #f7f9fd 1px solid; BACKGROUND-COLOR: #f7f9fd
}
#extranav DIV.extra H2 {
	FONT-SIZE: 70%; BACKGROUND: none transparent scroll repeat 0% 0%; =
MARGIN: 0px 0px 0.5em; COLOR: #c03; TEXT-ALIGN: left
}
#extranav DIV.extra UL {
	PADDING-RIGHT: 0px; PADDING-LEFT: 0px; PADDING-BOTTOM: 0px; MARGIN: =
0px; PADDING-TOP: 0px; LIST-STYLE-TYPE: none; BACKGROUND-COLOR: =
transparent
}
#extranav DIV.extra LI {
	PADDING-RIGHT: 0px; DISPLAY: block; PADDING-LEFT: 0px; PADDING-BOTTOM: =
2px; PADDING-TOP: 2px; BACKGROUND-COLOR: transparent
}
#extranav DIV.extra LI A:link {
	DISPLAY: block; PADDING-LEFT: 7px; FONT-SIZE: 70%; BACKGROUND: =
url(/common/images/arrow_blue.gif) no-repeat 0px 0.5em; COLOR: #008cb4; =
TEXT-DECORATION: underline
}
#extranav DIV.extra LI A:visited {
	DISPLAY: block; PADDING-LEFT: 7px; FONT-SIZE: 70%; BACKGROUND: =
url(/common/images/arrow_blue.gif) no-repeat 0px 0.5em; COLOR: #008cb4; =
TEXT-DECORATION: underline
}
#extranav DIV.extra LI A:hover {
	BACKGROUND: url(/common/images/arrow_red.gif) no-repeat 0px 0.5em; =
COLOR: #c03
}
#extranav DIV.extra UL LI.more A:link {
	BACKGROUND: url(/common/images/arrow_red.gif) no-repeat 0px 0.5em; =
COLOR: #c03
}
#extranav DIV.extra UL LI.more A:visited {
	BACKGROUND: url(/common/images/arrow_red.gif) no-repeat 0px 0.5em; =
COLOR: #c03
}
* HTML #extranav DIV.extra LI A:link {
	BACKGROUND: url(/common/images/arrow_blue.gif) no-repeat 0px 0.9em
}
* HTML #extranav DIV.extra LI A:visited {
	BACKGROUND: url(/common/images/arrow_blue.gif) no-repeat 0px 0.9em
}
* HTML #extranav DIV.extra LI A:hover {
	BACKGROUND: url(/common/images/arrow_blue.gif) no-repeat 0px 0.9em
}
#toc #content P.norm {
	FONT-SIZE: 90%
}
#toc #content A.arrow:link {
	PADDING-LEFT: 10px; FONT-SIZE: 70%; BACKGROUND: =
url(/common/images/arrow_blue.gif) no-repeat 0px 0.5em; MARGIN: 0px; =
COLOR: #008cb4
}
#toc #content A.arrow:visited {
	PADDING-LEFT: 10px; FONT-SIZE: 70%; BACKGROUND: =
url(/common/images/arrow_blue.gif) no-repeat 0px 0.5em; MARGIN: 0px; =
COLOR: #008cb4
}
#toc #content A.arrow:hover {
	BACKGROUND: url(/common/images/arrow_red.gif) no-repeat 0px 0.5em; =
COLOR: #c03
}
#toc #content H2 {
	PADDING-RIGHT: 0px; PADDING-LEFT: 0px; FONT-WEIGHT: bold; FONT-SIZE: =
90%; PADDING-BOTTOM: 3px; MARGIN: 1em 0px 0px; COLOR: #008cb4; =
PADDING-TOP: 3px
}
#toc #content #article {
	MARGIN: 1em 0px
}
#toc #content H3 {
	PADDING-RIGHT: 0px; PADDING-LEFT: 0px; FONT-SIZE: 90%; PADDING-BOTTOM: =
0px; MARGIN: 1em 0px 0px; PADDING-TOP: 0px
}
#toc #content P.aug {
	PADDING-RIGHT: 0px; PADDING-LEFT: 0px; PADDING-BOTTOM: 0px; MARGIN: 5px =
0px; PADDING-TOP: 0px
}
#toc #content P.errorcor {
	PADDING-RIGHT: 0px; PADDING-LEFT: 0px; PADDING-BOTTOM: 0px; MARGIN: 5px =
0px; PADDING-TOP: 0px
}
#toc #content H4.norm {
	PADDING-RIGHT: 0px; PADDING-LEFT: 0px; PADDING-BOTTOM: 0px; MARGIN: 5px =
0px; PADDING-TOP: 0px
}
#toc #content SPAN.page {
	PADDING-RIGHT: 0px; PADDING-LEFT: 0px; PADDING-BOTTOM: 0px; MARGIN: 5px =
0px; PADDING-TOP: 0px
}
#toc #content P.seealso {
	PADDING-RIGHT: 0px; PADDING-LEFT: 0px; PADDING-BOTTOM: 0px; MARGIN: 5px =
0px; PADDING-TOP: 0px
}
#toc #content P.aug {
	FONT-SIZE: 90%
}
#toc #content P.errorcor {
	FONT-SIZE: 70%
}
#toc #content DIV P.articlelinks {
	FONT-SIZE: 70%
}
#toc #content IMG.cover {
	FLOAT: left; MARGIN: 1em 10px 1em 0px
}
#toc #content UL {
	PADDING-RIGHT: 0px; PADDING-LEFT: 0px; PADDING-BOTTOM: 1px; MARGIN: 1px =
0px 0px; PADDING-TOP: 0px; LIST-STYLE-TYPE: none; TEXT-ALIGN: left
}
#toc #content UL LI {
	MARGIN: 0px
}
#toc #content UL A.arrow-down:link {
	PADDING-RIGHT: 5px; PADDING-LEFT: 14px; FONT-SIZE: 80%; BACKGROUND: =
url(/common/images/arrow_black_down.gif) no-repeat 5px 8px; =
PADDING-BOTTOM: 3px; MARGIN: 0px; COLOR: #000; PADDING-TOP: 3px; =
TEXT-DECORATION: underline
}
#toc #content UL A.arrow-down:visited {
	PADDING-RIGHT: 5px; PADDING-LEFT: 14px; FONT-SIZE: 80%; BACKGROUND: =
url(/common/images/arrow_black_down.gif) no-repeat 5px 8px; =
PADDING-BOTTOM: 3px; MARGIN: 0px; COLOR: #000; PADDING-TOP: 3px; =
TEXT-DECORATION: underline
}
#toc #content UL A.arrow-down:hover {
	BACKGROUND: url(/common/images/arrow_red_down.gif) no-repeat 5px 8px; =
COLOR: #c03; TEXT-DECORATION: underline
}
#toc #content UL LI.about-the-cover {
	MARGIN-TOP: 0.5em
}
#toc #content UL LI A.arrow:link {
	PADDING-RIGHT: 0px; PADDING-LEFT: 10px; FONT-SIZE: 70%; BACKGROUND: =
url(/common/images/arrow_blue.gif) no-repeat 0px 0.5em; PADDING-BOTTOM: =
0px; MARGIN: 3em 0px 0px 5px; PADDING-TOP: 0px
}
#toc #content UL LI A.arrow:visited {
	PADDING-RIGHT: 0px; PADDING-LEFT: 10px; FONT-SIZE: 70%; BACKGROUND: =
url(/common/images/arrow_blue.gif) no-repeat 0px 0.5em; PADDING-BOTTOM: =
0px; MARGIN: 3em 0px 0px 5px; PADDING-TOP: 0px
}
#toc #content UL LI A.arrow:hover {
	BACKGROUND: url(/common/images/arrow_red.gif) no-repeat 0px 0.5em
}
#toc #content UL A.page:link {
	BACKGROUND: url(/common/images/arrow_black_down.gif) no-repeat 4px 8px
}
#toc #content UL A.page:visited {
	BACKGROUND: url(/common/images/arrow_black_down.gif) no-repeat 4px 8px
}
#toc #content UL A.page:hover {
	COLOR: #000
}
#toc #content DIV.articlenav {
	DISPLAY: block; MARGIN-BOTTOM: 20px; WIDTH: 130px
}
#toc #content DIV.articlenav H2 {
	PADDING-RIGHT: 0px; PADDING-LEFT: 0px; FONT-WEIGHT: bold; FONT-SIZE: =
70%; PADDING-BOTTOM: 3px; MARGIN: 0px; COLOR: #fff; PADDING-TOP: 3px; =
BACKGROUND-COLOR: #008cb4; TEXT-ALIGN: center
}
#toc #content DIV.articlenav DIV.prevnext {
	PADDING-RIGHT: 0px; PADDING-LEFT: 0px; FONT-SIZE: 70%; PADDING-BOTTOM: =
3px; MARGIN: 0px; PADDING-TOP: 3px; BACKGROUND-COLOR: #cce8f0; =
TEXT-ALIGN: center
}
#toc #content DIV.articlenav DIV.prevnext A.prev {
	PADDING-LEFT: 7px; BACKGROUND: url(/common/images/arrow_black_left.gif) =
no-repeat left center
}
#toc #content DIV.articlenav DIV.prevnext A.next {
	PADDING-RIGHT: 7px; BACKGROUND: url(/common/images/arrow_black.gif) =
no-repeat right center
}
#toc #content DIV.articlenav DIV.prevnext A:link {
	COLOR: #000; TEXT-DECORATION: none
}
#toc #content DIV.articlenav DIV.prevnext A:visited {
	COLOR: #000; TEXT-DECORATION: none
}
#toc #content DIV.articlenav DIV.prevnext A:hover {
	COLOR: #000; TEXT-DECORATION: underline
}
#toc #content H2.atl {
	PADDING-RIGHT: 0px; PADDING-LEFT: 0px; FONT-WEIGHT: bold; FONT-SIZE: =
90%; BACKGROUND: url(/common/images/dots.gif) repeat-x left bottom; =
PADDING-BOTTOM: 3px; MARGIN: 1.5em 0px 0px; COLOR: #c03; PADDING-TOP: =
3px
}
#toc #content H3.atl {
	PADDING-RIGHT: 0px; PADDING-LEFT: 0px; FONT-WEIGHT: bold; FONT-SIZE: =
90%; BACKGROUND: url(/common/images/dots.gif) repeat-x left bottom; =
PADDING-BOTTOM: 3px; MARGIN: 1.5em 0px 0px; COLOR: #c03; PADDING-TOP: =
3px
}
#toc #content H4.norm {
	DISPLAY: inline; FONT-SIZE: 90%
}
#toc #content SPAN.page {
	FONT-WEIGHT: bold; FONT-SIZE: 90%; COLOR: #999999
}
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------=_NextPart_000_0000_01C8592E.A4BB86E0
Content-Type: application/octet-stream
Content-Transfer-Encoding: quoted-printable
Content-Location: http://www.nature.com/common/scripts/global.js

(function($) {=0A=
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=0A=
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visibility aat small resolutions=0A=
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		=0A=
			var dropdownAd =3D false;=0A=
		=0A=
			// for each descendant of .leaderboard that isn't a <script>, =
determine if it's taller than standard leaderboard height=0A=
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				if($(this).height() > 90) {=0A=
					dropdownAd =3D true;=0A=
				}=0A=
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}) (jQuery);
------=_NextPart_000_0000_01C8592E.A4BB86E0--
