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doi:10.1016/j.neuron.2006.06.016 &n= bsp; 3D"How

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Minireview

Drosophila Neuroblast Asymmetric Cell Division: Recent = Advances and=20 Implications for Stem Cell Biology

Fengwei Yu¹^,=20²,=20 Chay T. Kuo¹=20 and Yuh Nung Jan¹^,=20^,
¹Howard = Hughes=20 Medical Institute and Departments of Physiology, Biochemistry, and = Biophysics,=20 University of California, Rock Hall, 1550 Fourth Street, San Francisco,=20 California 94143
²Temasek Life Sciences = Laboratory and Department of Biological Sciences, National University of = Singapore, 1 Research Link, 117604, Singapore

Available online 5 = July=20 2006.

Asymmetric cell division is an evolutionarily conserved mechanism = widely used=20 to generate cellular diversity during development. Drosophila = neuroblasts=20 have been a useful model system for studying the molecular mechanisms of = asymmetric cell division. In this minireview, we focus on recent = progress in=20 understanding the role of heterotrimeric G proteins and their regulators = in=20 asymmetric spindle geometry, as well as the role of an = Inscuteable-independent=20 microtubule pathway in asymmetric localization of proteins in = neuroblasts. We=20 also discuss issues of progenitor proliferation and differentiation = associated=20 with asymmetric cell division and their broader implications for stem = cell=20 biology.

Article Outline

Main=20 Text Receptor-Independent=20 Activation of Heterotrimeric G Proteins in Drosophila NBs Heterotrimeric=20 G Proteins and Asymmetric Spindle Geometry Asymmetric=20 Protein Localization and Mitotic Spindle Orientation Asymmetric=20 Cell Division Coordinates Proliferation and Differentiation Implications=20 for Mammalian Stem Cell Biology
References

Main Text

Asymmetric cell division is one of the primary mechanisms used by = progenitor=20 cells to generate neuronal diversity in Drosophila central and = peripheral=20 nervous systems (CNS and PNS, respectively). The study of its underlying = mechanisms started about 12 years ago with the discovery that Numb = functions as=20 an intrinsic cell-fate determinant that is segregated into only one of = the two=20 daughter cells during neural precursor division (Rhyu=20 et al., 1994). Since then, largely through the efforts of a handful = of labs,=20 considerable insights into the inner workings of this fundamental = pathway have=20 been gained. In this minireview, we will discuss recent progress in this = field.=20 Before doing so, we will first start with a brief overview of the = =E2=80=9Cstate of the=20 field=E2=80=9D until just a couple of years ago.

In the Drosophila embryonic CNS, each abdominal segment of the = ventral=20 nerve cord (VNC) consists of approximately 700 neurons and 60 glial = cells that=20 have distinct fates and morphologies. These neurons and glia are = together=20 derived from roughly 60 progenitor cells called neuroblasts (NBs). To = generate=20 the diversity of cell fates from a single precursor cell, NBs undergo = programmed=20 asymmetric cell division. During Drosophila embryogenesis, NBs = are=20 specified from a monolayer of epithelial cells called the neuroectoderm = through=20 a process of lateral inhibition. Once specified, NBs delaminate from the = epithelium layer and enter mitosis. During prophase of the cell cycle, = two=20 centrosomes migrate laterally to opposite sites of the NB with parallel=20 alignment to the epithelium layer. At metaphase, the mitotic spindle = rotates by=20 90=C2=B0 to be oriented along the apical-basal axis. Upon cytokinesis, = each NB gives=20 rise to two daughter cells with distinct size and fate. The larger = apical=20 daughter cell maintains a NB identity and continues to divide in a=20 stem-cell-like fashion, whereas the smaller basal daughter cell becomes = a=20 ganglion mother cell (GMC) which undergoes terminal division to generate = two=20 postmitotic neurons or glia (Figure=20 1; also reviewed by Betschinger=20 and Knoblich, 2004, Chia=20 and Yang, 2002 and Jan=20 and Jan, 2001).=20

Display=20 Full Size version of this image = (38K)

Figure 1. Asymmetric Cell Division of Drosophila NB
A schematic representation of NB delaminating from epithelium. As = the NB is=20 delaminating from the epithelium, it forms an apical stalk, which is = in=20 contact with the surrounding epithelial cells. During prophase,=20 Par/Insc/Pins/G=CE=B1i proteins (red crescent) are asymmetrically = localized at the=20 apical cortex, whereas Numb/Pon/Pros/Mira (yellow crescent) proteins = are=20 localized at the basal cortex. The two centrosomes and the mitotic = spindle=20 (green) are aligned parallel to the surface of epithelium. During = metaphase,=20 the mitotic spindle rotates 90=C2=B0 to become aligned perpendicular = to the=20 epithelial layer. During anaphase/telophase, asymmetric spindle = geometry is=20 generated, which divides the neuroblast into two daughter cells of = distinct=20 fate and size: a large apical NB and a smaller basal GMC. The basal = daughter=20 GMC preferentially inherits cell-fate determinants Numb and Pros.=20

The apical-basal polarity of an epithelial cell is established = through an=20 evolutionarily conserved protein complex consisting of Bazooka (Baz, the = fly=20 homolog of C. elegans Par-3), Par-6, and atypical PKC (aPKC), = also known=20 as the Par complex. This protein complex is maintained in the specified = NB and=20 utilized by the NB to preserve its cellular polarity. When a NB = delaminates from=20 the epithelium, it forms a cellular structure called the =E2=80=9Capical = stalk,=E2=80=9D which=20 is in contact with the surrounding epithelial cells (Figure=20 1). The Par complex in the apical stalk colocalizes with the = NB-specific=20 protein Inscuteable (Insc), establishing an apical-basal polarity in the = delaminating NB. During mitosis, the Insc/Par complex localizes to the = apical=20 cortex as a crescent and recruits another evolutionarily conserved = protein=20 complex, comprised of Partner of Inscuteable (Pins) and the = heterotrimeric G=20 protein subunit G=CE=B1i, that maintains apical-basal polarity. This = sequential=20 recruitment model explains how apical-basal polarity of a NB is first=20 established and subsequently maintained during the first round of = asymmetric=20 cell division (Parmentier=20 et al., 2000, Schaefer=20 et al., 2000 and Yu=20 et al., 2000).

The primary roles of the two protein complexes are distinct: the = Pins/G=CE=B1i=20 complex is mainly involved in spindle orientation (metaphase NBs align = their=20 spindles perpendicular to the epithelium layer), whereas the Par complex = appears=20 to play a primary role in the basal localization of cell-fate = determinants (Wodarz=20 et al., 1999, Schober=20 et al., 1999 and Izumi=20 et al., 2004). The apical Par complex directs the basal localization = and=20 segregation of cell-fate determinants, such as Prospero (Pros) and Numb = and=20 their adaptor proteins, Miranda (Mira) and Partner of Numb (Pon) through = two=20 cortically localized tumor suppressors, Discs large (Dlg) and Lethal (2) = giant=20 larvae (Lgl) (Ohshiro=20 et al., 2000, Peng=20 et al., 2000 and Betschinger=20 et al., 2003). Dlg and Lgl are primarily involved in localizing = basal=20 proteins and have only a mild effect on the crescent formation of the = apical=20 proteins (Ohshiro=20 et al., 2000, Peng=20 et al., 2000 and Siegrist=20 and Doe, 2005), although Dlg can also interact with apical protein = Pins (Bellaiche,=20 et al., 2001). Phosphorylation of Lgl by apically localized aPKC = leads to=20 Lgl inactivation and prevents its association with the apical cortex, = while=20 nonphosphorylated Lgl at the basal cortex is in an active state and = recruits=20 cell-fate determinants (Betschinger=20 et al., 2003). The phosphorylation state of Lgl also restricts = myosin II=20 activity to the apical cortex, which results in the = =E2=80=9Cpush=E2=80=9D of cell-fate=20 determinants to the basal cortex (Barros=20 et al., 2003). In contrast to the function of Myosin II in excluding = cell-fate determinants from the apical cortex, Myosin VI (also termed = Jaguar)=20 positively regulates basal localization and segregation of Mira/Pros via = vesicle=20 transport machinery (Petritsch=20 et al., 2003).

For the remainder of this minireview, we will focus on four aspects = of NB=20 asymmetric cell division that have been highlighted by recent studies. = We will=20 first discuss how heterotrimeric G proteins are activated in a=20 receptor-independent manner. Next, we will explore how asymmetric = spindle=20 geometry is generated during anaphase/telophase and what factors orient = mitotic=20 spindle along the apical-basal axis. And finally, we return to a = fundamental=20 question of how proliferation and differentiation are coordinated during = asymmetric cell division and the implications of these studies for = mammalian=20 stem cell biology. A review of another area of considerable recent = progress,=20 namely, the role of endocytic pathway in asymmetric cell division of=20 Drosophila sensory organ precursors (SOPs) can be found elsewhere = (Somers=20 and Chia, 2005).

Receptor-Independent Activation of Heterotrimeric G = Proteins in=20 Drosophila NBs

In the canonical model of heterotrimeric G protein signaling, = extracellular=20 signals can be transduced to targets within the cell through a = seven-pass=20 transmembrane receptor called G protein coupled receptor (GPCR). In the = inactive=20 state, the GDP-G=CE=B1G=CE=B2=CE=B3 heterotrimer associates with GPCR. = Upon ligand binding,=20 GPCR acts as a guanine nucleotide exchange factor (GEF) to stimulate = release of=20 GDP from the G=CE=B1 subunit, which in turn is converted to the GTP = bound form.=20 GTP-G=CE=B1 dissociates from the G=CE=B2=CE=B3 complex and each = activates its downstream=20 effectors. G protein signaling is attenuated through the hydrolysis of = GTP to=20 GDP by the intrinsic GTPase activity of G=CE=B1. The hydrolysis rate is = accelerated=20 by GTPase-activating proteins (GAPs), which typically contain regulator = of G=20 protein signaling (RGS) domain(s) (Figure=20 2A).=20

Display=20 Full Size version of this image = (33K)

Figure 2. Canonical and Noncanonical Models of Heterotrimeric = G=20 Protein Signaling
(A) In the canonical model, upon ligand binding, a seven-pass = transmembrane=20 protein, GPCR, can act as a GEF to activate heterotrimeric G proteins. = In the=20 Drosophila NBs, heterotrimeric G proteins can also be activated = in a=20 receptor-independent manner.
(B) In a possible noncanonical cycle, two GDIs, Pins, Loco, and a = putative=20 cytosolic GEF, Ric-8, may act synergistically to activate = heterotrimeric G=20 proteins. The attenuation of G proteins may be mediated by Loco acting = as a=20 GAP.=20

Heterotrimeric G proteins can also be activated through a=20 receptor-independent mechanism by cytosolic proteins containing = GoLoco/GPR=20 domains, a mechanism employed in Drosophila NB asymmetric cell = division.=20 GoLoco/GPR domain proteins can interact with GDP-G=CE=B1 and compete = with G=CE=B2=CE=B3 for=20 GDP-G=CE=B1 binding. In this capacity, GoLoco/GPR domain proteins act as = guanine=20 nucleotide dissociation inhibitors (GDIs) to dissociate GDP-G=CE=B1 from = G=CE=B2=CE=B3 dimer.=20 In the absence of ligand binding to GPCR, this mechanism may initiate = the=20 noncanonical heterotrimeric G protein signaling pathway. In = Drosophila,=20 the GoLoco/GPR domain-containing proteins Pins and Loco act as GDIs for = G=CE=B1i (Schaefer=20 et al., 2001 and Yu=20 et al., 2005). pins, loco, or G=CE=B1i = single mutants=20 display similar phenotypes in spindle geometry and daughter cell size=20 difference. Simultaneous inactivation of Pins and Loco results in a much = more=20 severe disruption of spindle geometry and daughter cell size difference, = similar=20 to G=CE=B2 13F or G=CE=B31 mutants which = remove =CE=B2 and =CE=B3=20 subunits of heterotrimeric G proteins respectively, suggesting that Pins = and=20 Loco may act redundantly to dissociate the inactive heterotrimer in=20 Drosophila NBs (Yu=20 et al., 2005; Figure=20 2B). Loco also contains the RGS domain that shows GAP activity for = G=CE=B1i,=20 indicating that Loco may act as a GAP to hydrolyze GTP-G=CE=B1i to = GDP-G=CE=B1i (Yu=20 et al., 2005; Figure=20 2B).

A question remains as to how GDP-G=CE=B1i is converted to = GTP-G=CE=B1i in the absence=20 of GPCRs acting as receptor GEFs. One candidate molecule that performs = this=20 function could be the evolutionally conserved Ric-8. Mammalian Ric-8A = can act as=20 a cytosolic GEF for GoLoco bound myristoylated G=CE=B1i (Tall=20 and Gilman, 2005). In nematodes, Ric-8 exhibits GEF activity for = only one of=20 two redundant G=CE=B1 proteins implicated in the asymmetric cell = division of one-cell=20 zygotes (Afshar=20 et al., 2004 and Afshar=20 et al., 2005). In Drosophila, Ric-8 is required for the=20 membrane-targeting of heterotrimeric G proteins (David=20 et al., 2005, Hampoelz=20 et al., 2005 and Wang=20 et al., 2005). However, it remains to be determined whether=20 Drosophila Ric-8 possesses a GEF activity for G=CE=B1i. One = plausible model=20 for receptor-independent cycling of heterotrimeric G proteins is = illustrated in=20 Figure=20 2B.

In the canonical mode, GTP-G=CE=B1i is generally considered the = active protein=20 that activates various downstream effectors. It remains to be determined = whether=20 the GDP bound or GTP bound G=CE=B1i is active in the = receptor-independent model. In=20 Drosophila, embryos overexpressing GTP-G=CE=B1i exhibit mild = defects, whereas=20 overexpression of GDP-G=CE=B1i produces much stronger defects (Schaefer=20 et al., 2001 and Yu=20 et al., 2005), suggesting that GDP-G=CE=B1i, together with Pins and = Loco, might=20 play important roles in Drosophila NBs. Furthermore, it would be=20 important to identify the downstream effectors of activated G=CE=B1i and = G=CE=B2=CE=B3 during=20 NB asymmetric cell divisions.

Heterotrimeric G Proteins and Asymmetric Spindle = Geometry

One important aspect of NB asymmetric cell divisions is the = correlation=20 between asymmetric spindle geometry and daughter cell size. The mitotic = NB forms=20 an apically-biased spindle during anaphase/telophase with the following=20 characteristics (Figure=20 1): first, the apical centrosome is larger in size than the basal = one;=20 second, astral microtubules emanating from the apical centrosome grow = more=20 robustly; third, the apical centrosome is located far from the proximal = cortex=20 whereas the basal centrosome is almost attached to the basal cortex (so = called=20 =E2=80=9Cbasal displacement of mitotic spindle=E2=80=9D); fourth, the = apical half of spindle=20 that extends from the apical centrosome to the cleavage plane is longer = than the=20 basal one (Bonaccorsi=20 et al., 2000, Kaltschmidt=20 et al., 2000 and Fuse=20 et al., 2003). Asymmetric spindle geometry, in general, correlates = well with=20 daughter cell size differences during NB asymmetric cell divisions (Cai=20 et al., 2003, Fuse=20 et al., 2003, Izumi=20 et al., 2004 and Yu=20 et al., 2003). It results in dramatic size disparity between the NB = daughter=20 and GMC daughter: the diameter of a NB is three times larger than that = of a GMC=20 (Cai=20 et al., 2003, Fuse=20 et al., 2003 and Izumi=20 et al., 2004). One exception to this correlation, however, is the=20 asterless (asl) mutant, whose NBs divide asymmetrically in = the=20 absence of centrosomes and astral microtubules (Bonaccorsi=20 et al., 2000). It remains possible that asl mutant NBs retain = a=20 residual amount of functional astral microtubules and centrosomes.

Both the spindle geometry and daughter cell size difference are = controlled by=20 two redundant pathways mediated by the Insc/Baz/Par-6/aPKC proteins and = the=20 Pins/G=CE=B1i/Loco proteins (Cai=20 et al., 2003, Yu=20 et al., 2003 and Yu=20 et al., 2005). The majority of mutant NBs that lose a single = component of=20 either complex still divide asymmetrically to produce daughter cells of = unequal=20 size. However, the spindle asymmetry and daughter cell size difference = are=20 entirely disrupted when an additional component of the = Insc/Baz/Par-6/aPKC=20 complex is removed in pins, loco, or G=CE=B1i = mutants. In=20 G=CE=B213F or G=CE=B31 mutant, the majority = of NBs exhibit=20 symmetric spindle structure and divide into two equally sized daughter = cells (Fuse=20 et al., 2003 and Izumi=20 et al., 2004), suggesting that cortically localized G=CE=B2=CE=B3 = proteins play a more=20 prominent role than other apical proteins in this process.

There are currently several models for how cortically localized = G=CE=B213F can=20 affects daughter cell size asymmetry. The first model proposes that = active G=CE=B213F=20 functions to suppress the length of basal spindle arm while its activity = at the=20 apical side is antagonized by G=CE=B1i, resulting in the formation of an = asymmetric=20 spindle (Fuse=20 et al., 2003). This is supported by the fact that = G=CE=B213F mutant=20 NBs form a large symmetric spindle whereas the elevated activity of=20 G=CE=B213F results in a small symmetric spindle. The = second model uses=20 the data that Insc/aPKC and Pins/G=CE=B1i are delocalized in = G=CE=B213F=20 mutant NBs, which suggests that G=CE=B213F may control = both the=20 Insc/Par and Pins/G=CE=B1i pathways to regulate spindle geometry (Yu=20 et al., 2003). The third model suggests that = G=CE=B213F regulates=20 spindle geometry by restricting G=CE=B1i localization to the apical side = (Wang=20 et al., 2005), which are supported by the following: first, in=20 G=CE=B213F mutant embryos, G=CE=B1i is localized uniformly = around the NB=20 cortex, raising a possibility that cortically localized G=CE=B1i may be = active to=20 regulate spindle geometry from both apical and basal sides; second, a=20 G=CE=B213F ric-8 double mutant, in which G=CE=B1i and Pins = are cytosolic,=20 resembles a ric-8 or G=CE=B1i single mutant but not = G=CE=B213F mutant in terms of daughter cell size = differences.

Thus, G=CE=B1i may be a key regulator in controlling spindle geometry = and daughter=20 cell size difference, such that the high frequency of symmetric division = in=20 G=CE=B213F or G=CE=B31 mutants is the = indirect consequence of=20 the cortical localization of G=CE=B1i/Pins, which may override polarity = cues from Par=20 proteins (Wang=20 et al., 2005). It was also reported that a different ric-8 = mutant=20 allele exhibits equal size division in the majority of NBs, similar to = that seen=20 in G=CE=B213F mutants. This evidence supports the view = that=20 Ric-8-mediated G=CE=B213F localization to the cortex may be a key = pathway in=20 controlling spindle geometry and daughter cell size difference (Hampoelz=20 et al., 2005). In the future, the roles of G=CE=B1i and G=CE=B213F = in spindle geometry=20 and daughter cell size difference could be further assessed if double = germline=20 clone mutants of G=CE=B213F G=CE=B1i can be = generated and compared to=20 either G=CE=B213F or G=CE=B1i single = mutants.

In mammalian cells, the G=CE=B1 subunit can bind microtubules (Willard=20 et al., 2004). However, it is not known whether heterotrimeric G = proteins=20 can directly regulate spindle geometry by binding microtubules in=20 Drosophila. Evidence from the ric-8 mutant, in which = cytosolic G=CE=B1i=20 fails to associate with the mitotic spindle, suggests at least that = GDP-G=CE=B1i (and=20 Pins) are unlikely to possess an affinity for microtubules in = Drosophila.=20 Thus, one important remaining question is what mechanisms control the=20 reorganization of microtubules that coordinates the formation of the = cleavage=20 furrow to generate daughter cell size differences during NB asymmetric = cell=20 division.

Asymmetric Protein Localization and Mitotic Spindle=20 Orientation

The sequential recruitment model described earlier in this minireview = explains how apical-basal polarity is initially established and = subsequently=20 maintained in order for NBs to orient their mitotic spindle along the=20 apical-basal axis during the first round of asymmetric cell division. = However,=20 it is not clear how the NB can =E2=80=9Cmemorize=E2=80=9D this = apical-basal polarity to always=20 divide perpendicular to the epithelial surface. During in vitro culture=20 conditions, NBs maintain an intrinsic polarity and divide into two = unequal-sized=20 daughter cells in the absence of neighboring cell contacts (Siegrist=20 and Doe, 2006). However, in these isolated NB cultures, NBs = randomize the=20 spindle axis orientation over a series of divisions, leading to the = generation=20 of daughter GMCs from random cortical positions. In contrast, in a = culture of=20 clustered cells, NBs that retain contact with epithelial cells orient = their=20 mitotic spindle perpendicular to the epithelial surface and consequently = bud off=20 GMC daughters at the same site away from epithelial cells. This suggests = that=20 cortical polarity and/or spindle orientation in NBs is regulated by = either=20 extrinsic signals emanating from epithelial cells or by cell-cell = contact=20 between the NB and neighboring epithelial cells (Figure=20 1; Siegrist=20 and Doe, 2006).

Support for this idea comes from the Drosophila sensory organ=20 precursors (SOPs), located in the developing PNS. SOPs divide = asymmetrically=20 along the anterior-posterior axis within the plane of the epithelium, = and the=20 orientation of their division depends on receptors such as Frizzled and = Flamingo=20 (Gho=20 and Schweisguth, 1998 and Lu=20 et al., 1999). Although NBs divide under the epithelium plane unlike = SOPs,=20 it is still possible that some unidentified receptor(s) could be = clustered at=20 the site of contact between NBs and epithelial cells and thereby = recruits the=20 apical complex. Interestingly, the intercellular region of Echinoid, a=20 transmembrane cell adhesion molecule, interacts with the PDZ domains of = Baz to=20 regulate cell adhesion in the wing disc epithelial cells (Wei=20 et al., 2005), raising the possibility that this or some other = similar=20 interactions may be responsible for providing polarity cues to NBs.

One hallmark of asymmetric cell division in Drosophila is the = coupling=20 of asymmetrically localized proteins to each centrosome, leading to = mitotic=20 spindle alignment and subsequent asymmetric protein segregation. Given = that=20 apically localized proteins are required to orient the mitotic spindle = during=20 mitosis, one may expect that adaptor proteins that can interact = simultaneously=20 with apical cortical proteins, and microtubules could serve to align the = spindle=20 along the apical-basal axis. In C. elegans, Lin-5, a=20 microtubule-associated protein, can interact with GPR-1/2, the nematode=20 counterpart of Drosophila Pins, to displace the mitotic spindle = toward=20 the posterior cortex in the one-cell zygote (Srinivasan=20 et al., 2003). In mammals, the microtubule binding protein, NuMA can = interact with LGN, the mammalian homolog of Drosophila Pins, to = control=20 spindle dynamics (Du=20 and Macara, 2004). The fly homolog of Lin-5/NuMA is Mushroom body = defect=20 (Mud), a large coiled-coil domain protein, which can interact with the=20 N-terminal region of Pins containing seven TPR repeats, and is localized = to both=20 the apical cortex and centrosomes during mitosis. Loss of mud = function=20 leads to uncoupling of mitotic spindle with apical crescent in some = mitotic NBs=20 (Bowman=20 et al., 2006, Izumi=20 et al., 2006 and Siller=20 et al., 2006). Thus, it appears that Pins can align the mitotic = spindle=20 along the apical-basal axis through direct interactions with the=20 microtubule-associated adaptor protein Mud (Bowman=20 et al., 2006, Izumi=20 et al., 2006 and Siller=20 et al., 2006).

Not only the apical proteins are able to orient the mitotic spindle, = this=20 interaction is not a one-way street, as recent study suggests that a=20 microtubule-dependent pathway can also asymmetrically localize apical = proteins=20 such as Pins/G=CE=B1i in metaphase NBs (Siegrist=20 and Doe, 2005). How does the microtubule-dependent pathway exert its = function at the cellular cortex during metaphase? Kinesin heavy chain 73 = (Khc-73), a microtubule-based plus-end motor protein, plays an important = role,=20 as it can interact with cortical protein Dlg in vivo. Through this = interaction,=20 Khc-73 may act to change the conformation of Dlg: in the absence of = Khc-73, the=20 GK domain of Dlg can bind intramolecularly to its SH3 domain, whereas in = the=20 presence of Khc-73, the GK domain may preferentially associate with the = Khc-73=20 MAGUK binding site (MBS), freeing the SH3 domain to bind Pins in an=20 intermolecular interaction. How might Khc-73 function in vivo? One model = is as=20 follows: at metaphase, Khc-73 present at the plus end of astral = microtubules can=20 cluster Dlg to one side of the cortex. Then the Khc-73 bound Dlg = proteins expose=20 their SH3 domains and interact with Pins, thereby localizing = Pins/G=CE=B1i=20 asymmetrically.

The Dlg/Khc-73/microtubule pathway is primarily active at metaphase, = whereas=20 the Insc/Par pathway used to localize Pins/G=CE=B1i at the apical cortex = is active=20 prior to metaphase. When the Insc/Par pathway is inactivated, = Pins/G=CE=B1i are=20 uniformly localized around the cell cortex prior to metaphase. However, = the=20 Dlg/Khc-73/microtubule pathway can act independently of Insc/Par to = induce=20 Pins/G=CE=B1i crescent at metaphase. Although the Pins/G=CE=B1i crescent = is formed=20 overlying one of the centrosomes, its position along the cortex is = randomized=20 and not restricted to the normal apical side, leading to formation of a=20 misoriented spindles. When the Dlg/Khc-73/microtubule pathway is = inactivated,=20 Pins/G=CE=B1i can be recruited to the apical cortex by the Insc/Par = complex, as in=20 wild-type NBs. Yet, the apical Pins/G=CE=B1i crescent fails to overlie = one of=20 centrosomes, leading to formation of a misoriented spindle that is = uncoupled=20 from apical proteins. Only when the microtubule and the Insc/Par = pathways are=20 simultaneously activated can mitotic spindle oriented along the = apical-basal=20 axis be coupled to the asymmetric localization of proteins (Siegrist=20 and Doe, 2005; Figure=20 3).=20

Display=20 Full Size version of this image = (45K)

Figure 3. Both Insc/Par and Dlg/Khc-73 Are Required for = Pins/G=CE=B1i=20 Crescent Formation and Spindle Alignment
In the wild-type NB, Insc/Par (red crescent) and Pins/G=CE=B1i = (blue crescent)=20 are colocalized at the apical cortex during prophase/metaphase and = overlie the=20 apical centrosome. In insc mutant NBs, during prophase = Pins/G=CE=B1i (blue)=20 is localized uniformly around the cortex and becomes a randomly placed = crescent overlying one centrosome during metaphase. In dlg or=20 khc-73-RNAi mutants, the Pins/G=CE=B1i crescent forms during=20 prophase/metaphase, but the mitotic spindle becomes uncoupled during=20 metaphase. In mutant NBs lacking insc/dlg or=20 insc/khc-73, Pins/G=CE=B1i fails to form a crescent = during metaphase,=20 suggesting that Pins crescent formation and spindle alignment require = both=20 pathways. Centrosomes are represented as green dots.=20

This model of the microtubule/Khc-73/Dlg pathway helps to explain how = Pins/G=CE=B1i forms a crescent at metaphase in insc mutants. = Moreover, this=20 model may also explain how spindle rotation occurs at metaphase in the = wild-type=20 situation. When Khc-73/Dlg and Dlg/Pins complexes form at the apical = cortex,=20 Khc-73 may depolymerize astral microtubules at their plus ends to pull = one of=20 the centrosomes toward the apical side. It's a mechanism similar to=20 kinetochore-attached kinesin acting as a microtubule-destabilizing = enzyme to=20 disassemble tubulin monomers at the plus ends of kinetochore = microtubules and=20 thereby generate a pulling force leading to sister chromatid separation = at=20 anaphase (Rogers=20 et al., 2004). The potential role of Khc-73 as a microtubule = depolymerase=20 remains to be determined in Drosophila NBs.

But how is a particular centrosome chosen to migrate toward the = apical end?=20 Previous studies showed that a basally positioned interphase centrosome = can=20 cause an anticlockwise spindle rotation, whereas an apically positioned=20 interphase centrosome frequently leads to a clockwise spindle rotation = at=20 metaphase (Kaltschmidt=20 et al., 2000). The mechanisms underlying this phenomenon are = currently=20 unknown. One possibility is that the two centrosomes in a mitotic NB may = be=20 intrinsically different. For example, the mother centrosome may produce = more=20 astral microtubules than the daughter centrosome, reminiscent of budding = yeast=20 division (Wang=20 et al., 2003). At metaphase, the mother centrosome may = preferentially=20 migrate to the apical side by actively emanating its astral microtubules = to=20 capture the apical cortex. It would be of great interest to determine = whether in=20 mitotic NB such a mechanism exists and whether the apical daughter NB=20 consistently inherits the mother centrosome following each round of = asymmetric=20 cell division.

In summary, at least two mechanisms, mediated by Khc-73/Dlg and Mud, = can=20 contribute to spindle orientation during NB asymmetric cell division. In = the=20 case of khc-73/dlg or mud mutants, each exhibit low = penetrance in=20 spindle-orientation defects. It remains possible that double-stranded = RNA=20 interference of khc-73 only reduces its protein level, and = maternal=20 components of mud may compensate for its zygotic loss. It is also = possible that Dlg/Khc-73 and Mud may synergistically align mitotic = spindle, and=20 each may compensate for defects in the other.

Asymmetric Cell Division Coordinates Proliferation and=20 Differentiation

During Drosophila neurogenesis, a NB divides to produce a=20 proliferating NB (regenerative) and a GMC daughter cell that terminally=20 differentiates. This process is tightly controlled, and disrupting these = asymmetric cell divisions can lead to both uncontrolled proliferation = and=20 aberrant terminal differentiation (Figure=20 4). Several recent studies provide insights into how this process is = regulated during development and how its misregulation may contribute to = the=20 tumor formation (Betschinger=20 et al., 2006, Caussinus=20 and Gonzalez, 2005, Lee=20 et al., 2006a and Lee=20 et al., 2006b). For example, transplantation studies revealed that = mutant=20 larval brain tissue from pins, mira, numb, or = pros=20 when transplanted into wild-type adult abdomen grows to sizes more than = 100-fold=20 larger than control wild-type transplants (Caussinus=20 and Gonzalez, 2005). NBs, which are highly enriched in the = transplanted=20 mutant tissue, exhibits genomic instability and altered centrosome, = which likely=20 contribute to the observed uncontrolled proliferation. Strikingly, the=20 transplanted NBs can form malignant tumors that migrate away from the=20 implantation site to invade neighboring tissues. These studies support = the=20 notion that at least some tumors may be derived from mutant = stem/progenitor=20 cells.=20

Display=20 Full Size version of this image = (46K)

Figure 4. Asymmetrically Segregated Proteins aPKC and = Brat/Pros Can=20 Regulate Proliferation/Differentiation of Daughter Cells Following = Larval NB=20 Division
In the wild-type situation (top row), during cell division a larval = NB=20 segregates aPKC (red) to a proliferating NB daughter cell, and = Brat/Pros=20 (yellow) to a differentiating GMC daughter cell. Brat/Pros can = suppress the=20 expression of cell cycle genes and dMyc in the GMC daughter cell, = thereby=20 inducing differentiation. In the double mutants of lgl/pins or=20 overexpression of a membrane-tethered aPKC (middle row), aPKC is = segregated=20 into both daughter cells, leading to a transformation of GMC into=20 proliferating NB. In the brat or pros mutant larval NBs = (bottom=20 row), cell cycle progression and protein synthesis are not inhibited = in the=20 GMC, also leading to the transformation of GMC into proliferating NB.=20

How are the proliferation/differentiation capacities of daughter = cells=20 coordinated following each round of asymmetric cell division? One = possibility is=20 that NBs use the asymmetric localization/segregation machinery to = distribute=20 =E2=80=9Cproliferation factors=E2=80=9D to the NB daughter and/or = =E2=80=9Cdifferentiation factors=E2=80=9D to=20 the GMC daughter during asymmetric cell division. Then what might these = factors=20 be? Recent work indicates that aPKC is sufficient to promote NB = self-renewal and=20 that the daughter cell destined to be a NB inherits aPKC and continues = to=20 proliferate, whereas the GMC daughter cell without aPKC undergoes=20 differentiation (Lee=20 et al., 2006a). As described above, aPKC preferentially = phosphorylates and=20 inactivates Lgl on one side of the cell, while nonphosphorylated Lgl at = the=20 opposite side can positively direct asymmetric localization of Mira/Pros = and=20 Pon/Numb in both NBs and SOPs (Betschinger=20 et al., 2003 and Mayer=20 et al., 2005). However, in larval NBs, Lgl appears to negatively = regulate=20 aPKC activity, which limits its self-renewal ability to the apical = daughter (NB)=20 by restricting aPKC kinase activity to the apical cortex, inherited by = the NB=20 daughter. When Lgl is absent, aPKC, although localized nonuniformly, is=20 partially delocalized to the basal cortex in some metaphase larval NBs,=20 resulting in the generation of supernumerary NBs at the expense of = neurons.=20 Uniform cortical localization of aPKC in the pins lgl double = mutant leads=20 to the generation of more self-renewing NBs. That is consistent with=20 overexpression of a membrane-tethered aPKC, which localizes uniformly = around the=20 cortex, which is sufficient to induce NB self-renewal. All of these data = point=20 to aPKC kinase activity is sufficient for promoting NB self-renewal (Figure=20 4; Lee=20 et al., 2006a).

Concurrently, inhibition of daughter cell proliferation may also be = achieved=20 by asymmetric segregation of key differentiation factors into the GMC. = One such=20 factor is the basally locaized Brain Tumor (Brat) (Betschinger=20 et al., 2006 and Lee=20 et al., 2006b). Brat was independently isolated in a genetic screen = for=20 mutations that increase the number of NBs in larval brain (Lee=20 et al., 2006b) and in a biochemical assay analyzing the basal Mira = protein=20 complex (Betschinger=20 et al., 2006). Brat is a translational repressor containing an=20 evolutionarily conserved NHL (NCL-1, HT2A, and LIN-41) domain that = recruits the=20 Pumilio-Nanos-hunchback mRNA complex through an interaction between its = NHL=20 domain and Pumilio during early embryogenesis (Sonoda=20 and Wharton, 2001). In embryonic NBs, Brat colocalizes with Mira at = the=20 basal cortex as a crescent from prometaphase to telophase. Upon = cytokinesis,=20 Brat is segregated to the basal GMC and released from the cellular = cortex. In=20 brat mutant larval brains, supernumerary NBs are produced at the = expense=20 of neurons. Like wild-type NBs, brat mutant NBs divide = asymmetrically=20 into two daughter cells of unequal size, but the GMC daughter fails to=20 terminally differentiate. Instead, the mutant =E2=80=9CGMC=E2=80=9D = continues to grow, enlarge,=20 and express NB markers such as Deadpan and Mira. Moreover, MARCM clones=20 generated from a single larval brat mutant NB form a large number = of=20 Mira, Worniu, and CycE-positive NBs, indicating that brat = functions in a=20 cell-autonomous manner (Bello=20 et al., 2006, Betschinger=20 et al., 2006 and Lee=20 et al., 2006b). Thus, these data suggest that asymmetric segregation = of Brat=20 into GMCs is intended to inhibit cellular proliferation.

So how does Brat inhibit GMC proliferation? One possibility is that = in GMCs=20 Brat acts to inhibit the translation of dMyc protein, an important = regulator of=20 cell cycle progression and cell growth. dMyc is specifically expressed = in NBs=20 but not GMCs. Although the role of dMyc in NB proliferation is not yet = clear,=20 loss of brat function elevates dMyc levels in all daughter cells, = suggesting that Brat may act as a posttranscriptional inhibitor of dMyc = in GMCs=20 (Betschinger=20 et al., 2006).

Similarly to Brat, Pros also functions as a tumor suppressor in = larval brain=20 (Bello=20 et al., 2006, Betschinger=20 et al., 2006 and Lee=20 et al., 2006b; Figure=20 4). In fact, there may be some functional relationships between Brat = and=20 Pros. Brat is required for the asymmetric localization of Pros in larval = NBs,=20 and in pros mutant clones, Brat expression is downregulated (Betschinger=20 et al., 2006 and Lee=20 et al., 2006b). Tumorigenesis phenotypes in brat and = pros=20 larva brain may thus be due to mutual dependency on the = expression/localization=20 of these two proteins (Betschinger=20 et al., 2006 and Lee=20 et al., 2006b). Ectopic expression of Pros in brat mutant = clones can=20 rescue the NB overproliferation phenotype, also suggesting that Brat may = function through Pros (Bello=20 et al., 2006). Given that mutations in lgl perturb the = asymmetric=20 segregation of Pros and Brat and can cause tumor formation in larval = brains, Lgl=20 may function at least in part by ensuring that Brat and Pros segregate=20 specifically into GMCs (Betschinger=20 et al., 2006). However, since neither the removal of aPKC nor the=20 overexpression of Lgl3A (a suppressor of aPKC-induced NB = overproliferation) in=20 brat mutants can rescue the overproliferation defect, these = results=20 suggest that aPKC may not be required for NB self-renewal in brat = mutants.

Several interesting questions are raised by these findings. For = example, what=20 are the NB-specific substrates that are phosphorylated and activated by = aPKC=20 during NB self-renewal? It is important to determine how the = aPKC-dependent and=20 Brat/Pros-dependent pathways coordinate to regulate proliferation versus = differentiation during larval NB cell division.

Implications for Mammalian Stem Cell Biology

These studies in Drosophila NB have provided some insights to = our=20 general understanding of how stem and progenitor cells divide, = proliferate, and=20 differentiate. With more mammalian homologs of fly asymmetric cell = division=20 machinery being identified, it is now clear that considerable = mechanistic=20 conservation exists across species. For example, the mammalian = G=CE=B2=CE=B3 subunit of=20 the heterotrimeric G protein complex and activator of G protein = signaling-3=20 (AGS3) have been shown to control mitotic spindle orientation and cell = fate=20 during mouse cortical neurogenesis (Sanada=20 and Tsai, 2005). Likewise, mammalian aPKC, Par-3, and LGN are = thought to be=20 involved in asymmetric division of basal epidermal progenitor cells in = the skin=20 (Lechler=20 and Fuchs, 2005). The once elusive mammalian homolog of the fly = insc=20 has also been cloned (Katoh=20 and Katoh, 2003, Lechler=20 and Fuchs, 2005 and Zigman=20 et al., 2005). Although its role in mammalian asymmetric cell = division is=20 not yet clear, it is be reasonable to suspect that mammalian insc = plays=20 similarly important roles during progenitor cell division. These results = make=20 the point that asymmetric cell division is a fundamental process that = regulates=20 stem/progenitor cell division and fate determination, and it is likely = that more=20 examples of mechanistic conservation will come out of future studies of = such=20 mammalian homologs.

Beyond developmental biology, there has been considerable recent = interest in=20 stem cells and cancer. Not only is it hypothesized that oncogenic = mutations in=20 adult stem cells can give rise to cancer, but that some tumors may = actually be=20 propagated at the core by slowly dividing =E2=80=9Ctumor stem = cells=E2=80=9D (Brabletz=20 et al., 2005 and Feinberg=20 et al., 2006). Although these ideas make attractive models, there = remains=20 one universal property of stem cells, which is the ability for = self-renewal.=20 Therefore, oncogenic mutations in stem cells that limit self-renewal are = unlikely to generate cancer stem cells. Similarly, oncogenic mutations = in=20 differentiated cells which gained the ability to self renew may give = rise to=20 cancer stem cells. As we have discussed, since asymmetric cell division = governs=20 self-renewal and differentiation of stem cells, it is conceivable that = mutations=20 in part of this machinery maybe linked to tumor formation.

By showing that Brat and Prospero asymmetrically segregate during fly = neuroblast division to inhibit the self-renewal capacity of one daughter = cell=20 (Betschinger=20 et al., 2006 and Lee=20 et al., 2006b), these investigators established a mechanism of = action=20 between asymmetric cell division and cell proliferation. Betschlinger=20 et al. (2006), then went on to demonstrate Brat's inhibitory action = on dMyc=20 (the fly homolog of the mammalian oncogene MYC), thereby showing a = possible link=20 between asymmetric cell division and oncogenesis. Although these results = are=20 very exciting, the upregulation of dMyc in the absence of Brat leaves = several=20 unanswered questions. It is not clear if Brat directly inhibits=20 posttranslational inhibition of dMyc or if the observed dMyc = upregulation=20 results from other processes, such as extracellular signals, that drive = cellular=20 proliferation. The MYC transcription factor responds to many cellular = signals=20 that govern proliferation; thus, loss of Brat inhibition may represent = only part=20 of the cascade that leads to dMyc activation in Brat mutant daughter = cells.=20 Future experiments will be needed to fully elucidate this interaction.

If mutations in the asymmetric cell division pathway that = downregulate=20 proliferative capacity can indeed lead to stem cell hyperproliferation = and=20 cancer, one might expect to find genetic mutations in the mammalian = homologs of=20 Brat and Prospero in mammalian tumors. Very little is known about the = putative=20 Brat mammalian homolog Tripartite motif proteins (Trim2, 3, and 32) in = cellular=20 proliferation (van=20 Diepen et al., 2005), but the Prospero homolog Prospero-related = homeobox 1=20 (Prox1) has conserved functions in regulating retinal progenitor cell=20 proliferation (Dyer=20 et al., 2003). Prox1 expression can force retinal progenitor cells = to exit=20 the cell cycle and differentiate (Dyer=20 et al., 2003). In addition, mutations in and aberrant DNA = methylation of=20 prox1 have been observed in some liver tumors and lymphomas (Nagai=20 et al., 2003 and Schneider=20 et al., 2006). Although the number of such reported cases are few = and=20 despite the fact that Prox1 has so far not been implicated in mammalian=20 asymmetric cell division, more investigators looking in the right places = may=20 eventually shed light on the links between asymmetric cell division, = stem cell=20 proliferation, and cancer.

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Zigman=20 et al., 2005 M. Zigman, M. Cayouette, C. Charalambous, A. = Schleiffer, O.=20 Hoeller, D. Dunican, C.R. McCudden, N. Firnberg, B.A. Barres, D.P. = Siderovski=20 and J.A. Knoblich, Neuron 48 (2005), pp. = 539=E2=80=93545. SummaryPlus=20 | Full=20 Text + Links | PDF (524 K) | View Record in Scopus | Cited By in Scopus (15)

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Volume=20 51, Issue 1, 6 July 2006, Pages 13-20

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POSITION: absolute; TOP: -11px; HEIGHT: 14px; = BACKGROUND-COLOR: #777777 } .libBannerText { FONT-SIZE: smaller; FONT-FAMILY: Verdana, Arial, Helvetica, sans-serif } .sci_dirBtn { BACKGROUND-COLOR: #7aa544 } .sci_dirBtnHov { COLOR: #ffffff; BACKGROUND-COLOR: #1d6b2f } .blueBtn { BACKGROUND-COLOR: #0000aa } .blueBtnHov { COLOR: #0000aa; BACKGROUND-COLOR: #bad3f3 } .greenBtn { BACKGROUND-COLOR: #007703 } .greenBtnHov { COLOR: #007703; BACKGROUND-COLOR: #c2edc0 } .greyBtn { BACKGROUND-COLOR: #7f7f7f } .greyBtnHov { COLOR: #7f7f7f; BACKGROUND-COLOR: #e6e6e6 } .redBtn { BACKGROUND-COLOR: #990000 } .redBtnHov { COLOR: #990000; BACKGROUND-COLOR: #f7cece } .orangeBtn { BACKGROUND-COLOR: #cc5200 } .orangeBtnHov { COLOR: #cc5200; BACKGROUND-COLOR: #ffdfca } INPUT.btn { BORDER-RIGHT: #666666 1px solid; PADDING-RIGHT: 1px; BORDER-TOP: = #666666 1px solid; PADDING-LEFT: 1px; FONT-WEIGHT: bold; FONT-SIZE: = 12px; PADDING-BOTTOM: 0px; MARGIN: 0px 1px 0px 0px; VERTICAL-ALIGN: = middle; OVERFLOW: visible; BORDER-LEFT: #666666 1px solid; WIDTH: auto; = CURSOR: pointer; COLOR: #ffffff; PADDING-TOP: 0px; BORDER-BOTTOM: = #666666 1px solid; TEXT-DECORATION: none } INPUT.btnhov { BORDER-RIGHT: #666666 1px solid; PADDING-RIGHT: 1px; BORDER-TOP: = #666666 1px solid; PADDING-LEFT: 1px; FONT-WEIGHT: bold; FONT-SIZE: = 12px; PADDING-BOTTOM: 0px; MARGIN: 0px 1px 0px 0px; VERTICAL-ALIGN: = middle; OVERFLOW: visible; BORDER-LEFT: #666666 1px solid; WIDTH: auto; = CURSOR: pointer; PADDING-TOP: 0px; BORDER-BOTTOM: #666666 1px solid; = TEXT-DECORATION: none } A.articleBtn { BORDER-RIGHT: medium none; PADDING-RIGHT: 20px; BORDER-TOP: medium = none; PADDING-LEFT: 20px; FONT-WEIGHT: bold; FONT-SIZE: 12px; = PADDING-BOTTOM: 1px; MARGIN: 0px; BORDER-LEFT: medium none; CURSOR: = pointer; COLOR: #ffffff; PADDING-TOP: 1px; BORDER-BOTTOM: medium none; = BACKGROUND-COLOR: #999999; TEXT-DECORATION: none } A.articleBtn:hover { BORDER-RIGHT: medium none; PADDING-RIGHT: 20px; BORDER-TOP: medium = none; PADDING-LEFT: 20px; FONT-WEIGHT: bold; FONT-SIZE: 12px; = PADDING-BOTTOM: 1px; MARGIN: 0px; BORDER-LEFT: medium none; CURSOR: = pointer; COLOR: #ffffff; PADDING-TOP: 1px; BORDER-BOTTOM: medium none; = BACKGROUND-COLOR: #999999; TEXT-DECORATION: none } A.articleBtnActive { CURSOR: default; BACKGROUND-COLOR: #7aa544; TEXT-DECORATION: none } A.articleBtnActive:hover { CURSOR: default; BACKGROUND-COLOR: #7aa544; TEXT-DECORATION: none } A.articleBtn:hover { BACKGROUND-COLOR: #7aa544 } A.btn { BORDER-RIGHT: #666666 1px solid; PADDING-RIGHT: 5px; BORDER-TOP: = #666666 1px solid; PADDING-LEFT: 5px; FONT-WEIGHT: bold; FONT-SIZE: = 12px; PADDING-BOTTOM: 1px; MARGIN: 0px 1px 0px 0px; VERTICAL-ALIGN: = middle; BORDER-LEFT: #666666 1px solid; COLOR: #ffffff; PADDING-TOP: = 1px; BORDER-BOTTOM: #666666 1px solid; FONT-FAMILY: arial, verdana, = helvetica, sans-serif; HEIGHT: 1.17em; TEXT-DECORATION: none } A.btn:hover { BORDER-RIGHT: #666666 1px solid; PADDING-RIGHT: 5px; BORDER-TOP: = #666666 1px solid; PADDING-LEFT: 5px; FONT-WEIGHT: bold; FONT-SIZE: = 12px; PADDING-BOTTOM: 1px; MARGIN: 0px 1px 0px 0px; VERTICAL-ALIGN: = middle; BORDER-LEFT: #666666 1px solid; COLOR: #ffffff; PADDING-TOP: = 1px; BORDER-BOTTOM: #666666 1px solid; FONT-FAMILY: arial, verdana, = helvetica, sans-serif; HEIGHT: 1.17em; TEXT-DECORATION: none } A.sci_dirBtn { BACKGROUND-COLOR: #7aa544 } A.sci_dirBtn:hover { COLOR: #ffffff; BACKGROUND-COLOR: #1d6b2f } A.blueBtn { BACKGROUND-COLOR: #0000aa } A.blueBtn:hover { COLOR: #0000aa; BACKGROUND-COLOR: #bad3f3 } A.greenBtn { BACKGROUND-COLOR: #007703 } A.greenBtn:hover { COLOR: #007703; BACKGROUND-COLOR: #c2edc0 } A.greyBtn { BACKGROUND-COLOR: #7f7f7f } A.greyBtn:hover { COLOR: #7f7f7f; BACKGROUND-COLOR: #e6e6e6 } A.redBtn { BACKGROUND-COLOR: #990000 } A.redBtn:hover { COLOR: #990000; BACKGROUND-COLOR: #f7cece } A.orangeBtn { BACKGROUND-COLOR: #cc5200 } A.orangeBtn:hover { COLOR: #cc5200; BACKGROUND-COLOR: #ffdfca } A.noul:hover { TEXT-DECORATION: none } .tableFmBg { PADDING-RIGHT: 0px; BORDER-TOP: #8cc919 2px solid; PADDING-LEFT: 0px; = PADDING-BOTTOM: 0px; MARGIN: 0px; PADDING-TOP: 0px; BORDER-BOTTOM: = #8cc919 2px solid; BACKGROUND-COLOR: #efefef } .sci_dirBorder { BORDER-TOP: #8cc919 2px solid; BORDER-BOTTOM: #8cc919 2px solid } .blueBorder { BORDER-TOP: #0000aa 2px solid; BORDER-BOTTOM: #0000aa 2px solid } .greenBorder { BORDER-TOP: #007703 2px solid; BORDER-BOTTOM: #007703 2px solid } .greyBorder { BORDER-TOP: #7f7f7f 2px solid; BORDER-BOTTOM: #7f7f7f 2px solid } .redBorder { BORDER-TOP: #990000 2px solid; BORDER-BOTTOM: #990000 2px solid } .orangeBorder { BORDER-TOP: #cc5200 2px solid; BORDER-BOTTOM: #cc5200 2px solid } .sci_dirBorderBtm { BORDER-BOTTOM: #8cc919 2px solid } .blueBorderBtm { BORDER-BOTTOM: #0000aa 2px solid } .greenBorderBtm { BORDER-BOTTOM: #007703 2px solid } .greyBorderBtm { BORDER-BOTTOM: #7f7f7f 2px solid } .redBorderBtm { BORDER-BOTTOM: #990000 2px solid } .orangeBorderBtm { BORDER-BOTTOM: #cc5200 2px solid } .tableFmBgGray { FONT-SIZE: 1em; FONT-FAMILY: arial, helvetica, sans-serif; = BACKGROUND-COLOR: #efefef } .tableFmBgGrayNoCell { PADDING-RIGHT: 5px; PADDING-LEFT: 5px; FONT-SIZE: 1em; PADDING-BOTTOM: = 5px; MARGIN: 5px; PADDING-TOP: 5px; FONT-FAMILY: arial, helvetica, = sans-serif; BACKGROUND-COLOR: #efefef } .tableFmBgPad { MARGIN-TOP: 5px; MARGIN-BOTTOM: 5px; PADDING-BOTTOM: 5px; PADDING-TOP: = 5px; BACKGROUND-COLOR: #efefef } .tableFmCell { PADDING-LEFT: 10px; FONT-WEIGHT: bold; PADDING-BOTTOM: 3px; = MARGIN-LEFT: 10px; VERTICAL-ALIGN: top; PADDING-TOP: 3px; TEXT-ALIGN: = right } .tableFmCellTop { FONT-WEIGHT: bold; VERTICAL-ALIGN: top; PADDING-TOP: 0px; TEXT-ALIGN: = right } .tableFmCellAbove { PADDING-RIGHT: 5px; PADDING-LEFT: 5px; FONT-WEIGHT: bold; = PADDING-BOTTOM: 5px; PADDING-TOP: 5px; TEXT-ALIGN: left } .tableFmCellL { PADDING-LEFT: 10px; FONT-WEIGHT: bold; PADDING-BOTTOM: 3px; = MARGIN-LEFT: 10px; VERTICAL-ALIGN: top; PADDING-TOP: 3px; TEXT-ALIGN: = left } .tableFmDivider { PADDING-RIGHT: 0px; PADDING-LEFT: 0px; PADDING-BOTTOM: 0px; MARGIN: = 0px; WIDTH: 100%; PADDING-TOP: 0px; HEIGHT: 2px; BACKGROUND-COLOR: = #ffffff } .redtableFmDivider { PADDING-RIGHT: 0px; PADDING-LEFT: 0px; PADDING-BOTTOM: 0px; MARGIN: = 0px; WIDTH: 100%; PADDING-TOP: 0px; HEIGHT: 2px; BACKGROUND-COLOR: = #990000 } .SDtxtLarger { FONT-WEIGHT: bold; FONT-SIZE: larger; FONT-FAMILY: arial, helvetica, = sans-serif } .SDtxtSmall { FONT-SIZE: xx-small; COLOR: #000000; FONT-FAMILY: arial, helvetica, = sans-serif } .SDtxtSmallBold { FONT-WEIGHT: bold; FONT-SIZE: 0.9em } .SDtxtNote { FONT-SIZE: 1em; COLOR: #000000; FONT-FAMILY: arial, helvetica, = sans-serif } .SDtxtNoteSmall { FONT-SIZE: 10px; COLOR: #000000; FONT-FAMILY: arial, helvetica, = sans-serif } .SDtxtPgTitleBlack { FONT-WEIGHT: bold; FONT-SIZE: 150%; COLOR: #000000; FONT-FAMILY: arial, = helvetica, sans-serif } A.errMsg { COLOR: #ff0000; TEXT-DECORATION: none } A.errMsg:hover { TEXT-DECORATION: underline } .boldText { FONT-WEIGHT: bold } .sci_dirColor { COLOR: #7aa544 } .blueColor { COLOR: #0000aa } .greenColor { COLOR: #007703 } .greyColor { COLOR: #7f7f7f } .redColor { COLOR: #990000 } .orangeColor { COLOR: #cc5200 } .tablePlainWhite { PADDING-RIGHT: 0px; PADDING-LEFT: 0px; PADDING-BOTTOM: 0px; = PADDING-TOP: 0px; BACKGROUND-COLOR: #ffffff } .inputBox { BORDER-RIGHT: #666666 1px solid; BORDER-TOP: #666666 1px solid; = FONT-SIZE: 1em; VERTICAL-ALIGN: top; BORDER-LEFT: #666666 1px solid; = BORDER-BOTTOM: #666666 1px solid; BACKGROUND-COLOR: #ffffff } A.tabActive { BORDER-RIGHT: medium none; PADDING-RIGHT: 20px; BORDER-TOP: medium = none; PADDING-LEFT: 20px; FONT-WEIGHT: bold; FONT-SIZE: 1em; = PADDING-BOTTOM: 1px; MARGIN: 0px 2px 0px 0px; BORDER-LEFT: medium none; = COLOR: #ffffff; PADDING-TOP: 1px; BORDER-BOTTOM: medium none; = TEXT-DECORATION: none } A.tabActive:hover { BORDER-RIGHT: medium none; PADDING-RIGHT: 20px; BORDER-TOP: medium = none; PADDING-LEFT: 20px; FONT-WEIGHT: bold; FONT-SIZE: 1em; = PADDING-BOTTOM: 1px; MARGIN: 0px 2px 0px 0px; BORDER-LEFT: medium none; = COLOR: #ffffff; PADDING-TOP: 1px; BORDER-BOTTOM: medium none; = TEXT-DECORATION: none } A.tab { BORDER-RIGHT: medium none; PADDING-RIGHT: 20px; BORDER-TOP: medium = none; PADDING-LEFT: 20px; FONT-WEIGHT: bold; FONT-SIZE: 1em; = PADDING-BOTTOM: 1px; MARGIN: 0px 2px 0px 0px; BORDER-LEFT: medium none; = COLOR: #ffffff; PADDING-TOP: 1px; BORDER-BOTTOM: medium none; = BACKGROUND-COLOR: #999999; TEXT-DECORATION: none } A.tab:hover { BORDER-RIGHT: medium none; PADDING-RIGHT: 20px; BORDER-TOP: medium = none; PADDING-LEFT: 20px; FONT-WEIGHT: bold; FONT-SIZE: 1em; = PADDING-BOTTOM: 1px; MARGIN: 0px 2px 0px 0px; BORDER-LEFT: medium none; = COLOR: #ffffff; PADDING-TOP: 1px; BORDER-BOTTOM: medium none; = BACKGROUND-COLOR: #999999; TEXT-DECORATION: none } A.sci_dirTabActive { CURSOR: default; BACKGROUND-COLOR: #7aa544; TEXT-DECORATION: none } A.sci_dirTabActive:hover { CURSOR: default; BACKGROUND-COLOR: #7aa544; TEXT-DECORATION: none } A.sci_dirTab:hover { BACKGROUND-COLOR: #7aa544 } A.blueTabActive { CURSOR: default; BACKGROUND-COLOR: #0000aa; TEXT-DECORATION: none } A.blueTabActive:hover { CURSOR: default; BACKGROUND-COLOR: #0000aa; TEXT-DECORATION: none } A.blueTab:hover { BACKGROUND-COLOR: #0000aa } A.greenTabActive { CURSOR: default; BACKGROUND-COLOR: #007703; TEXT-DECORATION: none } A.greenTabActive:hover { CURSOR: default; BACKGROUND-COLOR: #007703; TEXT-DECORATION: none } A.greenTab:hover { BACKGROUND-COLOR: #007703 } A.greyTabActive { CURSOR: default; BACKGROUND-COLOR: #7f7f7f; TEXT-DECORATION: none } A.greyTabActive:hover { CURSOR: default; BACKGROUND-COLOR: #7f7f7f; TEXT-DECORATION: none } A.greyTab:hover { BACKGROUND-COLOR: #7f7f7f } A.redTabActive { CURSOR: default; BACKGROUND-COLOR: #990000; TEXT-DECORATION: none } A.redTabActive:hover { CURSOR: default; BACKGROUND-COLOR: #990000; TEXT-DECORATION: none } A.redTab:hover { BACKGROUND-COLOR: #990000 } A.orangeTabActive { CURSOR: default; BACKGROUND-COLOR: #cc5200; TEXT-DECORATION: none } A.orangeTabActive:hover { CURSOR: default; BACKGROUND-COLOR: #cc5200; TEXT-DECORATION: none } A.orangeTab:hover { BACKGROUND-COLOR: #cc5200 } .textBoxMultipleRow { FONT-SIZE: 1em; FONT-FAMILY: Arial, Helvetica, sans-serif; = BACKGROUND-COLOR: #ffffff } A.nextPrev { FONT-SIZE: 1em; MARGIN: 0px 10px; WIDTH: 1%; COLOR: #ffffff; = TEXT-DECORATION: none } A.nextPrev:hover { FONT-SIZE: 1em; MARGIN: 0px 10px; WIDTH: 1%; COLOR: #ffffff; = TEXT-DECORATION: underline } INPUT.nextPrev { BORDER-RIGHT: medium none; PADDING-RIGHT: 1px; BORDER-TOP: medium none; = PADDING-LEFT: 1px; FONT-SIZE: 1em; PADDING-BOTTOM: 0px; MARGIN: 0px 5px; = VERTICAL-ALIGN: middle; OVERFLOW: visible; BORDER-LEFT: medium none; = WIDTH: auto; COLOR: #0000ee; PADDING-TOP: 0px; BORDER-BOTTOM: medium = none; BACKGROUND-COLOR: transparent; TEXT-DECORATION: none } INPUT.nextPrevHov { BORDER-RIGHT: medium none; PADDING-RIGHT: 1px; BORDER-TOP: medium none; = PADDING-LEFT: 1px; FONT-SIZE: 1em; PADDING-BOTTOM: 0px; MARGIN: 0px 5px; = VERTICAL-ALIGN: middle; OVERFLOW: visible; BORDER-LEFT: medium none; = WIDTH: auto; COLOR: #0000ee; PADDING-TOP: 0px; BORDER-BOTTOM: medium = none; BACKGROUND-COLOR: transparent; TEXT-DECORATION: underline } .smCaps { FONT-VARIANT: small-caps } .nowrap { WHITE-SPACE: nowrap } SPAN.hit { FONT-WEIGHT: bold; COLOR: #ff0000 } SPAN.bf { FONT-WEIGHT: bold } SPAN.it { FONT-STYLE: italic } SPAN.monospace { FONT-FAMILY: courier } SPAN.sans-serif { FONT-FAMILY: sans-serif } SPAN.underline { TEXT-DECORATION: underline } SPAN.pit { FONT-SIZE: 0.9em; COLOR: #737373; FONT-FAMILY: arial, verdana, = helvetica, sans-serif } .charImg { BORDER-RIGHT: medium none; BORDER-TOP: medium none; VERTICAL-ALIGN: = baseline; BORDER-LEFT: medium none; BORDER-BOTTOM: medium none } SPAN.cross-out { TEXT-DECORATION: line-through } .refersTable { FONT-SIZE: 1em; LINE-HEIGHT: 16px; FONT-FAMILY: arial, helvetica, = sans-serif; BACKGROUND-COLOR: #efefef } .refersLeftColumn { PADDING-LEFT: 5px; FONT-WEIGHT: bold; VERTICAL-ALIGN: top; WIDTH: 55px; = TEXT-ALIGN: right } .refersDivider { PADDING-RIGHT: 0px; PADDING-LEFT: 0px; PADDING-BOTTOM: 0px; MARGIN: = 0px; WIDTH: 100%; PADDING-TOP: 0px; HEIGHT: 2px; BACKGROUND-COLOR: = #ffffff } .articleTitle { FONT-WEIGHT: bold; FONT-SIZE: 18px; FONT-FAMILY: Arial, Helvetica, = sans-serif } .h1 { FONT-WEIGHT: bold; FONT-SIZE: 2em; FONT-FAMILY: = arial,verdana,helvetica,sans-serif } .h2 { FONT-WEIGHT: bold; FONT-SIZE: 1.3em; FONT-FAMILY: = arial,verdana,helvetica,sans-serif } .h3 { FONT-WEIGHT: bold; FONT-SIZE: 1.2em; FONT-FAMILY: = arial,verdana,helvetica,sans-serif } .h4 { FONT-WEIGHT: bold; FONT-SIZE: 1.1em; FONT-FAMILY: = arial,verdana,helvetica,sans-serif } .h5 { FONT-WEIGHT: bold; FONT-SIZE: 1em; FONT-FAMILY: = arial,verdana,helvetica,sans-serif } .ImageScroller { OVERFLOW: auto; WIDTH: 435px } .ImageScrollerPurchHist { OVERFLOW: auto; WIDTH: 455px } .ImageScrollerPurchCurr { OVERFLOW: auto; 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