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doi:10.1016/j.neuron.2006.06.012   &n= bsp;3D"How  =20

Article

PDGFR=CE=B1-Positive B Cells Are Neural Stem Cells in the Adult SVZ = that Form=20 Glioma-like Growths in Response to Increased PDGF Signaling =

Erica L. Jackson1,=20 Jose Manuel Garcia-Verdugo3,=20 Sara Gil-Perotin3,=20 Monica Roy1,=20 Alfredo Quinones-Hinojosa1,=20 4,=20 Scott VandenBerg2=20 and Arturo Alvarez-Buylla1,=20 ,
1Department of=20 Neurological Surgery and Program in Developmental and Stem Cell Biology, = University of California, San Francisco, San Francisco, California = 94143
2Departments of Neurological Surgery and = Pathology,=20 University of California, San Francisco, San Francisco, California = 94143
3University of Valencia, Burjasot-4610 = Valencia, Spain=20
Received 4 January 2006;  revised 19 April 2006;  accepted = 9 June=20 2006.  Published: July 19, 2006.  Available online 19 July = 2006.=20

Referred to by: The Bad Seed: PDGF Receptors Link Adult Neural=20 Progenitors to Glioma Stem = Cells
Neuron, Volume=20 51, Issue 2, 20 July 2006, Pages = 151-153
Santosh=20 Kesari and Charles D. Stiles
SummaryPlus=20 | Full=20 Text + Links | PDF (78 K)

Summary

Neurons and oligodendrocytes are produced in the adult brain = subventricular=20 zone (SVZ) from neural stem cells (B cells), which express GFAP and have = morphological properties of astrocytes. We report here on the = identification B=20 cells expressing the PDGFR=CE=B1 in the adult SVZ. Specifically labeled = PDGFR=CE=B1=20 expressing B cells in vivo generate neurons and oligodendrocytes. = Conditional=20 ablation of PDGFR=CE=B1 in a subpopulation of postnatal stem cells = showed that this=20 receptor is required for oligodendrogenesis, but not neurogenesis. = Infusion of=20 PDGF alone was sufficient to arrest neuroblast production and induce SVZ = B cell=20 proliferation contributing to the generation of large hyperplasias with = some=20 features of gliomas. The work demonstrates that PDGFR=CE=B1 signaling = occurs early in=20 the adult stem cell lineage and may help regulate the balance between=20 oligodendrocyte and neuron production. Excessive PDGF activation in the = SVZ in=20 stem cells is sufficient to induce hallmarks associated with early = stages of=20 tumor formation.


Author Keywords:STEMCELL; DEVBIO; MOLNEURO =


Article Outline

Introduction
Results
PDGFR=CE=B1=20 Is Expressed by a Subpopulation of SVZ B Cells
SVZ=20 B Cells Activate the PDGFR=CE=B1 in Response to Exogenous = PDGF-AA
PDGF=20 Works in Conjunction with FGF to Stimulate Neurosphere Formation In=20 Vitro
PDGFR=CE=B1+=20 B Cells in the Adult SVZ Give Rise to Neurons and = Oligodendrocytes
Infusion=20 of PDGF-A into the Lateral Ventricle Blocks Neuroblast = Differentiation and=20 Induces the Growth of Atypical Hyperplasias in the SVZ
Removal=20 of PDGF-AA Results in Regression of Hyperplasias and Increased=20 Oligodendrocyte Production
PDGFR=CE=B1=20 Signaling Is Required for SVZ Oligodendrogenesis but Not for=20 Neurogenesis
Discussion
Identification=20 of PDGFR=CE=B1+ SVZ Type B Cells in the Adult Brain
PDGF=20 Blocks the Differentiation of SVZ Stem Cell Progeny and Induces the=20 Formation of Tumor-like Growths
Experimental=20 Procedures
Animals=20 Used
Human=20 Postmortem Specimens
Immunohistochemistry
PDGF=20 Administration
Ara-C=20 Infusion
Neurosphere=20 Experiments
AAV5-GFP=20 Infection
RCAS=20 Infection with PDGF Infusion and Analysis
Coinfection=20 with AAV5-GFP and RCAS-AP
P0=20 Infection of PDGFR=CE=B1Fl/Fl; Z/EG Mice with AdCre
Western=20 Blots
Acknowledgements
Supplemental=20 Data
References

Introduction

The subventricular zone (SVZ) in the walls of the lateral ventricles = is the=20 largest germinal center and source of stem cells in the adult brain. The = stem=20 cells in the SVZ of the adult rodent brain continue to generate neurons = destined=20 for the olfactory bulb (reviewed in Lim=20 and Alvarez-Buylla [2001]). A population of GFAP-expressing cells in = the SVZ=20 (B cells) are the primary precursor cells. They first produce a=20 transit-amplifying cell population (C cells) that then give rise to the=20 neuroblasts (A cells) that migrate to the olfactory bulb where they = mature into=20 neurons (Doetsch=20 et al., 1999a, Garcia=20 et al., 2004 and Parras=20 et al., 2004). Although the SVZ stem cells have characteristics of=20 astrocytes and express GFAP, additional markers that enable further=20 characterization of the stem cells are lacking. New oligodendrocytes are = also=20 generated in the SVZ of adult mice (Nait-Oumesmar=20 et al., 1999), and B cells located in this region also serve as = their=20 primary progenitors (Menn=20 et al., 2006). Again, additional markers and factors regulating SVZ=20 oligodendrogenesis have not been well characterized.

During mouse development, the platelet-derived growth factor = receptor-=CE=B1=20 (PDGFR=CE=B1) is expressed by neuroepithelial cells as early as E8.5 (Andrae=20 et al., 2001). However, the role of PDGF in neuroepithelial stem = cells is=20 not understood. Instead, PDGF is considered to function later in = development as=20 a potent mitogen of oligodendrocyte precursor cells (OPCs). OPCs were = first=20 identified and characterized in cultures from rat perinatal optic nerve = (Raff=20 et al., 1983), where they give rise to either oligodendrocytes or = type-2=20 astrocytes. In the rat optic nerve and spinal cord, OPCs express = PDGFR=CE=B1 (Hall=20 et al., 1996), and PDGF is important for regulating OPC number and=20 oligodendrocyte production in vivo (Calver=20 et al., 1998 and Fruttiger=20 et al., 1999). While most OPCs differentiate into mature = oligodendrocytes=20 early in postnatal life, it is believed that a slowly dividing = population of=20 OPCs remains widely distributed within the adult brain (Ffrench-Constant=20 et al., 1986 and Wolswijk=20 and Noble, 1989). The adult CNS retains the capacity to generate new = oligodendrocytes (McCarthy=20 and Leblond, 1988), and here PDGF is also thought to regulate OPC = number (Woodruff=20 et al., 2004).

In addition to these developmental roles, PDGF signaling has been = widely=20 implicated in the formation of brain tumors. Activation of the pathway = has been=20 observed in >80% of oligodendrogliomas and in 50%=E2=80=93100% of = astrocytomas and=20 astrocytoma cell lines (Guha=20 et al., 1995 and Varela=20 et al., 2004) occurring mainly through overexpression of the ligand = and=20 cognate receptor. Overexpression of PDGF/PDGFR occurs with equal = frequency in=20 low- and high-grade tumors, suggesting that activation of the pathway = may be=20 important for tumor initiation. Thus, understanding which cells in the = adult=20 brain normally respond to PDGF may provide insights into the glioma cell = of=20 origin and events regulating brain tumor initiation.

Some tumors in the adult human brain have anatomical connections with = the=20 ventricular wall (Globus=20 and Kuhlenbeck, 1944), and it has been suggested that brain tumors = may arise=20 from neural stem or progenitor cells (Dai=20 et al., 2001 and Recht=20 et al., 2003). Support for this hypothesis comes from oncogenic=20 transformation of progenitor cells (Holland=20 et al., 1998) and from a murine astrocytoma model in which tumors = appear to=20 initiate in the SVZ (Zhu=20 et al., 2005). Further support comes from work demonstrating the = presence of=20 neural stem-like cells within brain tumors (Ignatova=20 et al., 2002, Hemmati=20 et al., 2003, Galli=20 et al., 2004 and Singh=20 et al., 2004). However, it has not been shown in vivo that tumor = stem cells=20 are derived from normal stem cells or that a specific population of = cells with=20 demonstrated stem cell properties is capable of initiating tumor = formation.

We report here the identification of PDGFR=CE=B1-expressing = astrocytes (B cells)=20 in the adult SVZ that are neural stem cells. We show that PDGF = stimulates growth=20 and self-renewal of SVZ stem cells in neurosphere cultures in vitro and = that=20 PDGFR=CE=B1+ B cells generate new neurons and = oligodendrocytes in vivo. In=20 addition, we find that these cells are sensitive to alterations in the = PDGF=20 pathway and form atypical hyperplasias in vivo in response to excess = PDGF=20 signaling.

Results

PDGFR=CE=B1 Is Expressed by a Subpopulation of SVZ B = Cells

The expression of PDGFR=CE=B1 was analyzed by immunostaining in the = adult mouse=20 SVZ using a rabbit polyclonal and a mouse monoclonal antibody, which = showed very=20 similar staining patterns. Large numbers of PDGFR=CE=B1-expressing cells = were=20 observed in the dorsal region of the SVZ (Figure=20 1A), with scattered PDGFR=CE=B1-positive cells present in the = central and ventral=20 portions (Figure=20 1B). PDGFR=CE=B1-expressing cells were also observed in the medial = wall of the=20 lateral ventricle. PDGFR=CE=B2 was detected in cortical neurons (Smits=20 et al., 1991), but not in the SVZ.=20

Display=20 Full Size version of this image = (191K)

Figure 1. PDGFR=CE=B1 Expression in the Adult SVZ

Confocal optical sections of coronal sections of the mouse SVZ=20 coimmunostained for: (A) PDGFR=CE=B1 (red) and GFAP (green). Numerous = cells express=20 both PDGFR=CE=B1 and GFAP in the dorsal wedge region of the SVZ (top = panels). The=20 bottom panels show double-positive cells located more ventrally, about = midway=20 between the dorsal and ventral SVZ. Note that the staining is mainly = localized=20 in the processes and that many of the PDGFR=CE=B1+ cells = have a short=20 radial process.

(B) Nestin (red) and PDGFR=CE=B1 (green). Some = PDGFR=CE=B1-expressing cells also=20 express Nestin (arrows).

(C) Confocal optical sections of adult human SVZ coimmunostained = for PDGFR=CE=B1=20 (red) and GFAP (green). Note that a subpopulation of the B cells = express the=20 PDGFR=CE=B1 (arrows).

(D) Confocal optical section of mouse SVZ showing costaining for = PDGFR=CE=B1=20 (red, arrow) and EGFR (green). Note the absence of double-positive = cells.

Scale bars =3D 20 =CE=BCm.=20

We analyzed sections coimmunostained for the PDGFR=CE=B1 and SVZ cell = type-specific markers at the confocal microscope to identify which cells = in the=20 adult mouse SVZ expressed the PDGFR=CE=B1. A subset of GFAP+ = SVZ=20 astrocytes (B cells) expressed the PDGFR=CE=B1. The PDGFR=CE=B1 signal = was highest in the=20 astrocytic processes, with only a subset of cells exhibiting = immunostaining in=20 the cell body (Figure=20 1A). To determine what proportion of SVZ B cells express the = PDGFR=CE=B1, we=20 analyzed only those cells for which we could detect GFAP immunostaining = in the=20 cell body encompassing the nucleus. Using the mouse anti-PDGFR=CE=B1 = 82.5% =C2=B1 4.9%=20 (mean =C2=B1 SEM, n =3D 3 mice) of SVZ B cells were = PDGFR=CE=B1+. This was very=20 similar to results obtained using rabbit anti-PDGFR=CE=B1 in which case = 78.1% =C2=B1 0.95%=20 (n =3D 3) of the B cells were PDGFR=CE=B1+.

In the SVZ, PDGFR=CE=B1 was not detected on the Dlx2+ C = cells, nor did=20 the staining colocalize with that of PSA-NCAM or doublecortin, which = mark A=20 cells (Bonfanti=20 and Theodosis, 1994 and Doetsch=20 et al., 1999a; see Figures=20 S1C and S1D in the Supplemental=20 Data available with this article online). Intriguingly, many of the=20 PDGFR=CE=B1+ cells also expressed Nestin (Figure=20 1B), a marker of neural stem and progenitor cells (Lendahl=20 et al., 1990). Furthermore, the PDGFR=CE=B1 was not expressed by = EGFR+=20 cells in the SVZ (Figure=20 1D), most of which are transit-amplifying C cells (Doetsch=20 et al., 2002). To further verify the identity of the = PDGFR=CE=B1+=20 cells in the murine SVZ, we performed pre-embedding immunostaining in=20 conjunction with electron microscopy (EM). Analysis of semithin sections = revealed that SVZ B cells with various morphologies expressed the = PDGFR=CE=B1 (Figure=20 S1A). Under the electron microscope, cells expressing the = PDGFR=CE=B1 had=20 ultrastructural characteristics of astrocytes including a light = cytoplasm and=20 thick bundles of intermediate filaments (Figure=20 S1B).

We next determined whether PDGF-expressing cells existed in the adult = human=20 SVZ, where a subpopulation of astrocytes can function as stem cells in = vitro (Sanai=20 et al., 2004). Costaining for PDGFR=CE=B1 and GFAP was performed on = sections of=20 postmortem adult human brain. Interestingly, a subset of the = GFAP+=20 SVZ astrocytes expressed the PDGFR=CE=B1 (Figure=20 1C).

SVZ B Cells Activate the PDGFR=CE=B1 in Response to = Exogenous=20 PDGF-AA

We next investigated whether PDGF signaling occurs in adult SVZ B = cells. The=20 presence of the activated receptor was examined by staining with = antibodies=20 specific to the phosphorylated PDGFR=CE=B1 (phospho-Tyr720). This = analysis revealed a=20 small subpopulation of SVZ B cells in which the PDGFR=CE=B1 was = activated (Figure=20 2A). Interestingly, Western blots of SVZ lysates revealed abundant = levels of=20 PDGF-A ligand relative to levels in the cortex (Figure=20 2B, left). The converse was true of the PDGF-B ligand (Figure=20 2B, right), and PDGF-C ligand was not detected in Western blots.=20

Display=20 Full Size version of this image = (129K)

Figure 2. PDGFR=CE=B1 Signaling in Astrocytes of the Adult SVZ

(A) Confocal optical sections showing costaining for GFAP (red) and = PDGFR=CE=B1-phosphoTyr720 (green) on coronal sections of brain from = untreated mice.=20 Note the presence of GFAP+/phospho-PDGFR=CE=B1+ = astrotcytes=20 in the untreated brain ([A], inset).

(B) Western blots of lysates from SVZ and cortex probed for PDGF-A = ligand=20 (left) or PDGF-B ligand (right). Note the abundant expression of = PDGF-A (30 kDa=20 band) in the SVZ as compared to the cortex, while the opposite is true = for=20 PDGF-B.

(C) Levels of PDGFR=CE=B1 (left) or phospho-PDGFR=CE=B1-Tyr720 = (right) in lysates=20 from cortex, SVZ, and SVZ after injection of PDGF-A ligand into the = lateral=20 ventricle. A single band of 3D"not,170=20 kDa is observed.

(D) Confocal optical sections showing costaining for GFAP (red) and = phospho-PDGFR=CE=B1 (green) on coronal sections of brain from mice = given two=20 injections of PDGF-A ligand into the lateral ventricle separated by 20 = min.=20 Many more phospho-PDGFR=CE=B1+ B cells are present after = injection of=20 ligand. Scale bar =3D 50 =CE=BCm. Inset scale bar =3D 20 =CE=BCm.

(E) Costaining for GFAP (red) and phospho-PDGFR=CE=B1 (green) on = sections of=20 adult human SVZ demonstrating the occurrence of endogenous PDGF = signaling.=20 Scale bar =3D 20 =CE=BCm.=20

To explore whether SVZ cells respond to increased levels of PDGF = ligand, we=20 injected PDGF-AA, which binds specifically to the PDGFR=CE=B1, or = vehicle into the=20 lateral ventricle. The number of phospho-PDGFR=CE=B1+ B cells = was=20 dramatically increased in the PDGF-injected mice (Figure=20 2D) as compared to vehicle infused or untreated brain (Figure=20 2A). Together, these data indicate that PDGF signaling occurs in the = normal=20 SVZ as a result of endogenous signals and that signaling through this = pathway=20 can be stimulated by the administration of exogenous PDGF-AA.

We also examined the human SVZ for the presence of astrocytes in = which the=20 PDGFR=CE=B1 was actively signaling. Again, costaining for = phospho-PDGFR=CE=B1 revealed the=20 presence of a subset of GFAP+ astrocytes in which the = PDGFR=CE=B1 was=20 phosphorylated (Figure=20 2E), suggesting that endogenous signaling also occurs in adult human = SVZ=20 astrocytes.

PDGF Works in Conjunction with FGF to Stimulate = Neurosphere=20 Formation In Vitro

Based on our findings that some B cells expressed the PDGFR=CE=B1, we = hypothesized=20 that PDGF signaling regulates stem cell properties such as survival,=20 proliferation, or self-renewal. Cells from the SVZ grown in vitro in the = presence of EGF, bFGF, or both, form neurospheres (NS), which contain=20 multipotent neural stem cells (Morshead=20 et al., 2003). We studied the effects of PDGF on SVZ stem cells in = NS=20 assays. Equal numbers of cells dissociated from the SVZ of adult mice = were=20 divided into culture media containing PDGF-AA, bFGF, or bFGF and = PDGF-AA.=20 Although PDGF-AA alone did not support NS growth, there was a = significant=20 increase (45% =C2=B1 9%, p < 0.001) in the number of primary NS = generated in media=20 containing bFGF and PDGF-AA as compared to bFGF alone (Figure=20 3A), suggesting that PDGF promotes the survival and/or proliferation = of SVZ=20 stem cells. In addition, there was a 76% increase (p =3D 0.001) in the = number of=20 secondary NS generated from a single primary NS in the presence of bFGF = and=20 PDGF-AA compared to bFGF alone (Figure=20 3B), indicating that PDGF-AA also stimulates self-renewal. Upon=20 differentiation, NS derived in bFGF and PDGF-AA were capable of = generating=20 neurons, oligodendrocytes, and astrocytes, showing that NS derived in = the=20 presence of PDGF-AA retained their multipotency (Figure=20 3D). The cooperative effects of PDGF-AA and bFGF observed in vitro = prompted=20 us to compare the expression patterns of the FGFR and PDGFR in the SVZ. = Many of=20 the PDGFR=CE=B1-expressing cells were also FGFR+ (Figure=20 3E, arrows). In contrast to the cooperative effects of bFGF and = PDGF-AA,=20 there was no difference in the number of NS derived from cells cultured = in EGF=20 alone versus EGF and PDGF (Figure=20 3C). These data, together with the nonoverlapping staining pattern = of PDGFR=CE=B1=20 and EGFR (Figure=20 1D), suggest that these two growth factors affect different subsets = of SVZ=20 cells.=20

Display=20 Full Size version of this image = (97K)

Figure 3. PDGF Cooperates with bFGF to Enhance Neurosphere = Formation=20 and Stimulate Stem Cell Self-Renewal

(A) Freshly dissociated SVZ cells were cultured under neurosphere=20 conditions in the presence of PDGF, bFGF, or bFGF + PDGF. No NS grew = in PDGF=20 alone, but the addition of PDGF to bFGF containing growth media = resulted in an=20 increase in the number of primary neuroshperes generated over bFGF = alone (data=20 from three independent experiments; mean =C2=B1 SEM).

(B) The number of secondary NS derived from the dissociation of a = single=20 primary NS increased 76% when cultured in bFGF + PDGF compared to bFGF = alone.

(C) Freshly dissociated SVZ cells were cultured under neurosphere=20 conditions in the presence of PDGF, EGF, or EGF + PDGF. PDGF did not = enhance=20 NS formation in conjunction with EGF.

(D) Triple labeling of a differentiated NS derived in bFGF + PDGF = showing=20 immunoreactivity for astrocyte (GFAP in blue), oligodendrocyte (O4 in = green),=20 and neuron-specific (Tuj1 in red) markers.

(E) Confocal optical section of a coronal section of the SVZ = showing=20 costaining for FGFR (red) and PDGFR=CE=B1 (green).=20

PDGFR=CE=B1+ B Cells in the Adult SVZ Give = Rise to Neurons=20 and Oligodendrocytes

Administration of cytosine-=CE=B2-D-arabinofuranosidase (Ara-C) kills = the rapidly=20 dividing cells, depleting the SVZ of C and A cells but sparing a = subpopulation=20 of slowly dividing B cells (Doetsch=20 et al., 1999b). Following Ara-C treatment, B cells divide to = repopulate the=20 SVZ, producing C cells which in turn generate A cells. We used this = method to=20 determine if the repopulating stem cells express the PDGFR=CE=B1. Mice = were infused=20 with Ara-C for 6 days and sacrificed 12 hr later after receiving a = single=20 injection of BrdU 1 hr prior to sacrifice. Costaining for PDGFR=CE=B1 = and GFAP=20 revealed PDGFR=CE=B1+ B cells remaining in the SVZ (Figure=20 4A), consistent with the hypothesis that they function as primary=20 progenitors not transit-amplifying precursors. We also performed = costaining for=20 PDGFR=CE=B1 and BrdU to determine whether the PDGFR=CE=B1+ = cells contribute to=20 regeneration of the SVZ. Because the PDGFR signal is localized to the = processes,=20 it was difficult to colocalize this marker with the nuclear BrdU = staining.=20 However, we could be certain that a subset of the BrdU+ B = cells were=20 also PDGFR=CE=B1+ (Figure=20 4B). This is consistent with the idea that the = PDGFR=CE=B1+ B cells=20 are induced to re-enter the cell cycle after removal of Ara-C.=20

Display=20 Full Size version of this image = (126K)

Figure 4. PDGFR=CE=B1-Expressing B Cells Have Characteristics = of Stem Cells

(A and B) PDGFR=CE=B1+ B cells remain in the SVZ after = elimination of=20 C cells and neuroblasts by Ara-C treatment, and some of these cells = divide=20 after removal of the drug.

(A) Costaining for GFAP (green) and PDGFR=CE=B1 (red) after 6 day = Ara-C=20 infusion.

(B) Costaining for BrdU (green) and PDGFR=CE=B1 (red) 12 hr after = Ara-C=20 treatment.

(C) Some label-retaining cells express the PDGFR=CE=B1. Mice = received BrdU=20 continuously in the drinking water for 1 week followed by a 3 week = survival.=20 Costaining for BrdU (green) and PDGFR=CE=B1 (red).=20

In several organs the slowly dividing, label-retaining cells (LRCs)=20 correspond to the resident stem cell population (Bickenbach,=20 1981 and Morris=20 and Potten, 1994). We examined LRCs in the SVZ to see if they were=20 PDGFR=CE=B1+. BrdU was administered in the drinking water for = one week and=20 then removed for 3 weeks, sufficient time for the rapidly dividing C and = A cells=20 that were in the SVZ at the time of BrdU administration to complete = division=20 and/or migrate to the olfactory bulb (Lois=20 and Alvarez-Buylla, 1994 and Luskin=20 and Boone, 1994). Thus, any LRCs remaining in the SVZ at this time = are good=20 candidates for stem cells that divided and remained in the germinal = zone. Again,=20 we found that a subset of the BrdU-labeled B cells were also = PDGFR=CE=B1+=20 (Figure=20 4C).

While the above experiments indicate that PDGFR=CE=B1+ B = cells divide=20 and possibly function as neural stem cells in vivo, they do not directly = demonstrate that the PDGFR=CE=B1+ B cells generate neurons in = vivo. To do=20 this, we needed a method to specifically label these cells and follow = the fates=20 of their progeny. Recent work identified the PDGFR as a receptor for=20 adeno-associated virus serotype 5 (AAV5; Di=20 Pasquale et al., 2003 and Lotery=20 et al., 2003). AAV5 integrates into the host genome and is stably = inherited=20 by the daughter cells. We first verified that AAV5 infection in the SVZ = is=20 limited to PDGFR=CE=B1+ cells. Freshly isolated SVZ cells = were infected in=20 vitro with an AAV5-encoding GFP (AAV5-GFP), and coexpression of = PDGFR=CE=B1 and GFP=20 was evaluated 24 hr later by costaining. We analyzed all of the cells in = 15=20 random fields. Of 155 cells analyzed, we found 73 GFP+=20 (AAV5-infected) cells, all of which expressed the PDGFR=CE=B1 (Figure=20 5A). Furthermore, we used conditional ablation of the PDGFR=CE=B1 to = confirm that=20 it is required for AAV5 infection of SVZ cells in vivo. Adenovirus = encoding Cre=20 recombinase (AdCre, n =3D 4) or LacZ (AdLacZ, n =3D 4) as a control was = injected=20 stereotaxically in the SVZ of mice homozygous for a floxed allele of = PDGFR=CE=B1=20 (PDGFR=CE=B1Fl/Fl; Klinghoffer=20 et al., 2002). Nine days later, AAV5-GFP was injected into the SVZ.=20 PDGFR=CE=B1Fl/Fl mice that received AdCre had 5-fold fewer = GFP+=20 cells than those that received AdLacZ (p =3D 0.002; Figure=20 S3A). Of the GFP+ cells present in the four mice injected = with=20 AdCre, only seven cells also expressed Cre; all these cells still = exhibited=20 PDGFR=CE=B1 protein expression (Figure=20 S3B). Thus, AAV5-GFP virus provides a method to specifically label B = cells=20 expressing PDGFR=CE=B1.=20

Display=20 Full Size version of this image = (152K)

Figure 5. Specific Labeling of PDGFR=CE=B1-Expressing B Cells = Demonstrates=20 that These Cells Generate Neurons and Oligodendrocytes In Vivo

(A) Immunostaining of dissociated SVZ cells after 24 hr AAV5-GFP = infection=20 for PDGFR=CE=B1 (red) and GFP (green). The merged image shows that all = AAV5-infected GFP+ cells express the PDGFR=CE=B1. See Figure=20 S4 for additional controls.

(B=E2=80=93E) Mice were treated with Ara-C for 6 days to eliminate = C and A cells.=20 Twenty-four hours after Ara-C treatment, the animals were infected = with=20 AAV5-GFP in the SVZ and allowed to survive for 12 days.

(B) Section of OB immunostained for GFP showing numerous = GFP+=20 cells.

(C) Confocal optical section of the RMS coimmunostained for = doublecortin=20 (red) and GFP (green). The arrow indicates a = GFP/doublecortin+=20 migrating neuroblast.

(D=E2=80=93E) Confocal optical section of OB coimmunostained for = doublecortin (red)=20 and GFP (green). The arrow indicates a GFP/doublecortin+ = neuron in=20 (D) granule cell layer or (E) a periglomerular cell. Scale bar =3D 20 = =CE=BCm.

(F) Section of CC of a mouse 21 days after coinfection with = AAV5-GFP and=20 RCAS-AP showing immunostaining for GFP in brown and NBT/BCIP = histochemistry=20 for AP in purple. Note the presence of a = GFP+/AP+ cell=20 with characteristic oligodendrocyte morphology (arrow).=20

To confirm that PDGFR=CE=B1+ B cells are neurogenic stem = cells in vivo,=20 we used Ara-C to deplete C and A cells from the SVZ then labeled = remaining=20 PDGFR=CE=B1+ B cells by infection with AAV5-GFP. Twelve days = after=20 infection, numerous GFP+ neurons were present in the OB, = including=20 both granule and periglomerular cells, which were identified by their=20 characteristic morphology (Figure=20 5B) and by costaining for GFP and doublecortin (Figure=20 5D). GFP+/doublecortin+ neuroblasts were also = present=20 in the migratory stream between the SVZ and OB (Figure=20 5C), suggesting the continuing production of neurons by = PDGFR=CE=B1+ B=20 cells. Together, these data demonstrate that the PDGFR=CE=B1+ = B cells=20 function as precursors of new neurons. Since AAV5-GFP infection was done = after=20 elimination of transit-amplifying C cells in the SVZ, this experiment = further=20 suggests that PDGFR=CE=B1+ B cells correspond to the primary = neural=20 precursors.

We also noted the presence of GFP+ oligodendrocytes in the = CC,=20 suggesting that the PDGFR=CE=B1+ B cells in the SVZ also = generated=20 oligodendrocytes. However, we could not rule out infection of local=20 PDGFR=CE=B1+ OPCs in the CC by the AAV5-GFP because the = injection needle=20 passed through the CC. Therefore, to specifically label = PDGFR=CE=B1+ B=20 cells, we performed a coinfection in GFAP-Tva mice, which express the = receptor=20 for RCAS virus only in GFAP-expressing cells. Infection of Gtv-a mice = with an=20 RCAS virus encoding alkaline phosphatase (RCAS-AP) results in specific = infection=20 of dividing GFAP-positive cells and labeling of their progeny (Holland=20 and Varmus, 1998 and Doetsch=20 et al., 1999a). Costaining showed that expression of tvaR only = occurs in=20 GFAP-positive cells in Gtva-a mice (Figure=20 S3C). Injection of RCAS-AP virus into nontransgenic mice did not = result in=20 AP labeling. Thus, after confirming the specificity of RCAS infection, = we=20 injected a mixture RCAS-AP and AAV5-GFP into the SVZ. The mice were = sacrificed=20 21 days later, and the CC was analyzed for the presence of=20 AP/GFP-double-positive cells. Indeed, AP+/GFP+ = cells with=20 obvious oligodendrocyte morphology were present in the CC (Figure=20 5E), corresponding to the progeny of PDGFR=CE=B1+ B = cells.

These experiments indicate that PDGFR=CE=B1+ B cells in = the SVZ produce=20 both neurons and oligodendrocytes. In addition, numerous=20 GFP+/GFAP+ cells were present in the SVZ after = AAV5-GFP=20 infection (Figure=20 S4). However, we could not distinguish whether these were the = original B=20 cells that were infected by the AAV5 virus or if they were newly = generated SVZ=20 astrocytes.

Infusion of PDGF-A into the Lateral Ventricle Blocks = Neuroblast=20 Differentiation and Induces the Growth of Atypical Hyperplasias in the = SVZ

Having established that the PDGFR=CE=B1+ B cells function = as primary=20 SVZ progenitors, we examined their sensitivity to alterations in PDGF = signaling.=20 PDGF-AA ligand, which specifically binds to the PDGFR=CE=B1, was infused = into the=20 lateral ventricle for 6 days. One hundred percent of the PDGF-AA infused = mice (n=20 =3D 5) developed atypical hyperplasias in either the lateral or medial = wall of the=20 ipsilateral ventricle (Figure=20 6A). The hyperplastic nodules showed infiltrating cells invading = surrounding=20 tissues including the striatum, CC, and/or septum (Figure=20 6A), and some also grew inside the lateral ventricles. Furthermore, = they=20 contained a large proportion of proliferating cells as determined by = BrdU=20 incorporation (Figure=20 6B). Examination of hematoxylin and eosin-stained sections revealed = a=20 heterogeneous population of cells that varied in cytoarchitecture from = polygonal=20 cells with short stout processes to more fusiform cells with delicate = processes.=20 The cells within the hyperplastic nodules had a high nuclear to = cytoplasmic=20 ratio and displayed nuclear pleiomorphism and hyperchromasia.=20

Display=20 Full Size version of this image = (133K)

Figure 6. PDGF Induces the Hyperproliferation of B cells = Resulting in=20 the Formation of Tumor-like Growths

(A=E2=80=93C) Six day infusion of vehicle or PDGF-A (40 ng/day) = into the lateral=20 ventricle.

(A) Hematoxylin and eosin-stained sections of vehicle-infused (left = panel)=20 or PDGF-infused brains (two right panels).

(B) BrdU immunostaining of vehicle (left panel) or PDGF-infused = brain=20 (right panel). Mice received a single injection of BrdU 1 hr prior to=20 sacrifice.

(C) Photomicrograph of SVZ of mice infected with RCAS-GFP virus at = the time=20 of initiation of PDGF infusion showing that a subpopulation of the = cells in=20 the tumor-like growths are derived from SVZ B cells.

(D) Section of hyperplasia coimmunostained for Olig2 (green) and = nestin=20 (red). The right panel shows the merge of the green and red panels = showing=20 that most, but not all, cells are double labeled.=20

To ascertain whether the atypical hyperplasias were derived from B = cells or=20 their immediate progeny, we labeled a subset of SVZ B cells by infection = with=20 RCAS-GFP virus in GFAP-Tva mice, immediately prior to the onset of = PDGF-AA=20 infusion. Many cells in the hyperplasias were GFP labeled, indicating = that they=20 were derived from SVZ B cells (Figure=20 6C). Since all the mice studied (n =3D 6) had hyperplasias that = included both=20 positive and negative cells, we conclude that these growths have a = polyclonal=20 origin, and it is possible that other PDGFRa+ cells = contribute to=20 their growth.

Immunohistochemistry was performed for a variety of cell = type-specific=20 markers to further characterize the cells comprising the atypical = hyperplasias.=20 As expected, the cells showed robust expression of the PDGFR=CE=B1 (Figure=20 S5A). Interestingly, the majority of cells within the hyperplastic = nodule=20 did not express the normal markers of cells in the SVZ lineage, such as = Dlx2,=20 PSA-NCAM, or doublecortin, suggesting that the cells were no longer = undergoing=20 their normal differentiation program. Only a few cells expressed the B = cell=20 marker GFAP, but based on morphology they appeared to be a subpopulation = of the=20 hyperproliferating cells rather than reactive astrocytes (Figure=20 S5B). Cells in the hyperplastic nodule did express Nestin, and the = majority=20 of cells stained positively for Olig2 (Figure=20 6D), which is expressed by OPCs and is also a marker of human = gliomas of all=20 subtypes (Lu=20 et al., 2001).

While examining marker expression in the hyperplasias, we noted a = striking=20 absence of A cells close to the nodule. This suggested that activation = of the=20 PDGF pathway interferes with the ability of B cells to generate neurons. = To=20 address this, we infused PDGF-AA into the lateral ventricle for 6 days = at a=20 higher concentration and faster flow rate (10 ng/=CE=BCl; 1 =CE=BCl/hr) = to provide enough=20 PDGF-AA to stimulate a larger population of B cells in the SVZ and not = just=20 adjacent to the infusion cannula. Mice were given a single injection of = BrdU 1=20 hr prior to sacrifice. Costaining for BrdU and doublecortin revealed a = 7.7-fold=20 reduction in the number of proliferating neuroblasts in the SVZ of = PDGF-infused=20 mice compared to vehicle-infused controls (Figure=20 7). Thus, PDGF infusion inhibited neuroblast production and resulted = in the=20 formation of large atypical hyperplasias.=20

Display=20 Full Size version of this image = (98K)

Figure 7. PDGF Arrests Neuroblast Formation

(A and B) Coronal sections of SVZ from animals labeled with = RCAS-GFP before=20 6 day infusion with (A) PDGF-A or (B) vehicle showing immunostaining = for GFP=20 (green) and doublecortin (red). Note the increased number of = GFP+=20 cells and absence of doublecortin+ cells in the SVZ of = PDGF-infused=20 mice.

(C) Histogram showing a 7.7-fold decrease in the number (mean = =C2=B1 SEM) of=20 doublecortin+ neuroblasts in the SVZ of PDGF infused mice = (n =3D 3; p=20 < 0.001).=20

Removal of PDGF-AA Results in Regression of Hyperplasias = and=20 Increased Oligodendrocyte Production

Next, we determined whether the hyperproliferative cells continued to = require=20 exogenous PDGF-AA for their proliferation and survival. We infused = PDGF-AA into=20 the lateral ventricle for 14 days and waited 21 days before sacrificing = the=20 animals. Strikingly, the SVZ architecture of the PDGF-infused animals = looked=20 comparable to that of saline infused controls, indicating a complete = regression=20 of the nodule upon growth factor withdrawal (Figure=20 8A).=20

Display=20 Full Size version of this image = (119K)

Figure 8. PDGF Infusion Results in Increased Production of=20 Oligodendrocytes, and Decreased Production of Neurons from the SVZ and = PDGFR=CE=B1=20 Is Required for SVZ-Derived Oligodendrogenesis

(A) H&E-stained section of brain immediately after (left) and = 21 days=20 after (right) 14 day PDGF infusion. No atypical hyperplasia is = observed in the=20 SVZ 21 days after infusion.

(B=E2=80=93E) Mice were infected with RCAS-GFP virus immediately = prior to 6 day=20 infusion of high concentration PDGF followed by a 21 day recovery = period.

(B) IF for GFP (green) on the CC of vehicle-infused (left) and = PDGF-infused=20 (right) mice.

(C) Example of characteristic morphology of GFP+ cells = in the=20 CC.

(D) GFP immunostaining (green) of olfactory bulb of vehicle-infused = (left)=20 and PDGF-infused mice.

(E) Histogram showing the number (mean =C2=B1 SEM) of = GFP+ cells in=20 the CC (total cells counted) and OB (cells per section) of = vehicle-infused (n=20 =3D 4) or PDGF-infused (n =3D 4) mice. Note the decreased number of = neurons (p =3D=20 0.005) and increased number of oligodendrocytes (p =3D 0.004) in the=20 PDGF-infused mice.

(F and G) PDGFR=CE=B1 is required for oligodendrogenesis but not = neurogenesis.=20 PDGFR=CE=B1Flox/Flox; Z/EG mice and their littermates were = infected with=20 Adeno-Cre virus at P0 to delete the PDGFR=CE=B1 and GFP label a = subpopulation of=20 stem cells.

(F) Histogram showing the number (mean =C2=B1 SEM) of = GFP+ OB neurons=20 in PDGFR=CE=B1Flox/Flox (n =3D 4) and control mice (n =3D = 4).

(G) Histogram showing the number (mean =C2=B1 SEM) of = GFP+=20 oligodendrocytes in the CC of PDGFR=CE=B1Flox/Flox mice and = their=20 littermate controls. Note the reduction in the number of = GFP+=20 oligodendrocytes in the PDGFR=CE=B1Flox/Flox mice (p =3D = 0.044).=20

To follow the fate of SVZ cells after exposure to PDGF-AA, we = infected the=20 SVZ with RCAS-GFP virus immediately prior to a 6 day infusion of high=20 concentration PDGF-AA into the lateral ventricle and analyzed brains 21 = days=20 latter. GFP-positive neurons were detected in the OBs of both = saline-infused and=20 PDGF-infused mice, however the PDGF-infused mice had significantly fewer = (99.6 =C2=B1=20 13.4) OB cells than vehicle-infused mice (191.3 =C2=B1 26.5, p =3D = 0.005; Figures=20 8B and 8E). In contrast, there were significantly more GFP-positive = cells in=20 the CC of the PDGF-infused animals (178 =C2=B1 71.3) than in the vehicle = infused mice=20 (92.7 =C2=B1 38, p =3D 0.004; Figures=20 8C=E2=80=938E). These cells had the typical branched morphology of = nonmyelinating=20 and myelinating oligodendrocytes. This provides further evidence that = the=20 PDGFR=CE=B1+ B cells also generate oligodendrocytes and = suggests that PDGF=20 stimulates oligodendrocyte production by these cells.

PDGFR=CE=B1 Signaling Is Required for SVZ = Oligodendrogenesis but Not for=20 Neurogenesis

To further elucidate the role of PDGFR=CE=B1 signaling in the SVZ, we = performed a=20 loss-of-function analysis using Cre-mediated gene ablation in = PDGFR=CE=B1=20 Fl/Fl mice. These mice were crossed to the Z/EG reporter = strain (Novak=20 et al., 2000) that expresses GFP upon Cre-mediated recombination to = enable=20 permanent GFP labeling of cells that lose PDGFR=CE=B1. Adeno-Cre = infection was=20 targeted to a small subpopulation of radial glia in neonatal (P0) mice = (Merkle=20 et al., 2004). These cells function as the progenitors of adult = neural stem=20 cells. PDGFR=CE=B1Flox/+; Z/EG and PDGFR=CE=B1 = +/+; Z/EG littermates=20 were infected as controls. The animals were sacrificed at 8 weeks of = age. While=20 GFP+ neurons were detected at similar numbers in the = olfactory bulbs=20 of PDGFR=CE=B1Flox/Flox (155.8 =C2=B1 34.8) and control mice = (181.4 =C2=B1 36.3; Figure=20 8F), there was a 19-fold reduction (p =3D 0.044) in the number of=20 GFP+ oligodendrocytes (Figure=20 8G) present in the CC of PDGFR=CE=B1Flox/Flox mice (n =3D = 4) compared to=20 control mice (n =3D 4).

Discussion

We have identified a subpopulation of PDGFR=CE=B1-expressing B cells = in the adult=20 murine SVZ and have demonstrated that these cells function as = progenitors of=20 neurons and oligodendrocytes in vivo. We describe the effects of PDGF=20 stimulation on neurosphere formation in vitro and show that = PDGFR=CE=B1+ B=20 cells act as primary progenitors during SVZ regeneration in vivo after=20 elimination of transit-amplifying precursors and migrating neuroblasts.=20 Furthermore, we show that increased PDGF signaling in these cells = stimulates=20 their proliferation and blocks their ability to give rise to = differentiated=20 progeny, causing them to form tumor-like growths resembling = astrocytomas.=20 Interestingly, we also found that similar PDGFR=CE=B1-expressing = astrocytes exist in=20 the adult human SVZ.

Identification of PDGFR=CE=B1+ SVZ Type B = Cells in the Adult=20 Brain

Several lines of evidence indicate that oligodendrocytes are produced = from=20 the adult SVZ. Studies of demyelinating lesions of the CC suggest that=20 progenitors in the SVZ produce oligodendrocytes after injury (Nait-Oumesmar=20 et al., 1999) and that PDGF promotes this process (Lachapelle=20 et al., 2002). We have recently determined that B cells are the = primary=20 progenitors of SVZ-derived oligodendrocytes (Menn=20 et al., 2006). PDGF has long been recognized as a mitogen for OPCs = that=20 gives rise to oligodendrocytes and type 2 astrocytes in vitro (Raff=20 et al., 1983 and Ffrench-Constant=20 et al., 1986). Although OPCs have been viewed as glial-restricted=20 progenitors, it was recently demonstrated that they can be reprogrammed = to a=20 neural stem cell-like cell (NSLC) in vitro after first being induced to = form=20 type 2 astrocytes (Kondo=20 and Raff, 2000). However, the relevance of this finding to in vivo=20 neurogenesis was not clear.

Our analysis of PDGF receptor expression in the adult SVZ revealed = for the=20 first time the presence of a PDGFR=CE=B1-expressing GFAP+ B = cell=20 population present in both the murine and human brain. Furthermore, we=20 demonstrate that these PDGFR=CE=B1+ B cells are not only = precursors of=20 oligodendrocytes, but also of neurons. Depleting SVZ C and A cells and = labeling=20 the remaining PDGFR=CE=B1+ B cells with AAV5-GFP resulted in = many labeled=20 granule and periglomerular neurons. In addition, by coinfecting the SVZ = with=20 RCAS-AP virus and AAV5-GFP, we showed that PDGFR=CE=B1+ B = cells in the SVZ=20 also generate oligodendrocytes. The PDGFR=CE=B1 is commonly used as a = marker of OPCs=20 or glial-restricted progenitors (GRPs) in the CNS (Grinspan=20 and Franceschini, 1995 and Redwine=20 et al., 1997). Our work demonstrates that these = PDGFR=CE=B1+ B cells=20 are not GRPs but instead function as the primary progenitors of both=20 oligodendrocytes and new neurons produced throughout adult life. A = common=20 progenitor population of neurons and oligodendrocytes also exists during = development. Oligodendrocytes and neurons are derived from the same = population=20 of progenitors in the ventral region of the embryonic spinal cord (Lu=20 et al., 2002, Takebayashi=20 et al., 2002 and Zhou=20 and Anderson, 2002) and in the developing cerebral cortex (He=20 et al., 2001). Furthermore, it has recently been shown that = PDGF-responsive=20 progenitors capable of generating multipotent neurospheres can be = isolated from=20 the embryonic medial ganglionic eminence (Chojnacki=20 and Weiss, 2004).

Our data suggest that PDGF signaling may be involved in the normal = regulation=20 of oligodendrogenesis and neurogenesis in the SVZ. We confirmed the = presence of=20 PDGF-A and to a lesser extent PDGF-B ligand in the SVZ by Western blot, = and=20 cells actively signaling from the PDGFR=CE=B1 were revealed by = immunostaining for=20 phospho-PDGFR=CE=B1. Analysis of PDGFR=CE=B1Fl/Fl; Z/EG = animals demonstrated=20 that the PDGFR=CE=B1 is required for SVZ-derived oligodendrogenesis, and = prelabeling=20 B cells with RCAS-GFP demonstrated that PDGF infusion increased = oligodendrocyte=20 production from the SVZ. In contrast, loss of the PDGFR=CE=B1 did not = interfere with=20 the production of neurons, and PDGF infusion blocked neuroblast = production=20 during infusion and resulted in decreased numbers of GFP+ = neurons=20 present in the OB 21 days after treatment. Together, these data are = consistent=20 with a role for PDGF signaling in balancing neuron and oligodendrocyte=20 production from PDGFR=CE=B1+ SVZ B cells. The robust = expression of the=20 bHLH transcription factor Olig2 by the cells responding to PDGF = stimulation=20 suggests a mechanism for this regulation. The Olig family of = transcription=20 factors is required for oligodendrocyte development (Lu=20 et al., 2002 and Zhou=20 and Anderson, 2002). Olig2 repressor function is sufficient to = repress=20 neuronal differentiation in the postnatal (Marshall=20 et al., 2005) and adult SVZ (Hack=20 et al., 2005). Thus, PDGF may function upstream of Olig2 in = regulating fate=20 choice in the SVZ. It will be important to determine the source of PDGF = in vivo.

In contrast to our findings, previous in vitro studies addressing the = effects=20 of PDGF stimulation on embryonic CNS stem/progenitor cells indicate that = PDGF=20 directs neuronal differentiation from these cells (Johe=20 et al., 1996 and Williams=20 et al., 1997). A similar study showed that PDGF increased = proliferation of=20 immature neurons and delayed their differentiation (Erlandsson=20 et al., 2001). This discrepancy could be explained by differences in = growth=20 factor responsiveness between embryonic and adult cells. It is also = likely that=20 cells in vivo encounter a complex network of secreted, ECM-associated, = and cell=20 surface-associated factors that in combination elicit responses = different to=20 that of any single factor in vitro. Our findings that PDGF alone does = not=20 support neurosphere growth but robustly stimulates B cell proliferation = in vivo=20 are consistent with this notion.

PDGF Blocks the Differentiation of SVZ Stem Cell Progeny = and=20 Induces the Formation of Tumor-like Growths

The =E2=80=9Cblocked differentiation=E2=80=9D model of cancer = proposes that malignant=20 transformation interferes with a cells ability to differentiate, holding = the=20 cell in a proliferative state (Buick=20 et al., 1979). Human gliomas often express the progenitor marker = Nestin (Tohyama=20 et al., 1992), supporting the notion that the tumor cells do not = fully=20 differentiate. Moreover, differentiation state is one criteria used to=20 distinguish among low-grade astrocytoma, anaplastic astrocytoma, and = GBM.=20 Previous studies also suggested that blocking the differentiation of = postnatal=20 glial progenitor cells by increased PDGF signaling contributed to the = formation=20 of oligodendrogliomas in mice (Uhrbom=20 et al., 1998 and Dai=20 et al., 2001). Our data suggest that an uncoupling of proliferation = and=20 differentiation by increased PDGF signaling may be important for glioma=20 initiation.

Activation of the PDGF pathway is a common event in gliomagenesis and = has=20 been implicated in tumor initiation, since PDGF/PDGFR overexpression = occurs with=20 equal frequency in both low- and high-grade gliomas (Varela=20 et al., 2004). Our work provides compelling evidence that activation = of the=20 PDGF pathway in adult murine SVZ stem cells (B cells) is sufficient to = induce=20 the formation of atypical hyperplasias. Importantly, we show that PDGF=20 stimulation blocks the ability of B cells to give rise to differentiated = progeny, resulting in a dramatic reduction in the number of=20 doublecortin+ neuroblasts in the SVZ. This leads to the = accumulation=20 of a large number of rapidly proliferating cells in the SVZ that invade = the=20 adjacent parenchyma. Interestingly, we found that most SVZ C and A cells = do not=20 normally express the PDGFR=CE=B1. Together these data suggest that PDGF = signaling may=20 be involved in the regulation of primary precursors, being downregulated = during=20 neuronal differentiation but maintained in the early stages = oligodendrocyte=20 formation (Hart=20 et al., 1989, Barres=20 et al., 1992 and Ellison=20 and De Vellis, 1994).

We do not propose that the PDGFR=CE=B1+ B cells undergo = neoplastic or=20 malignant transformation upon PDGF infusion. However, increasing the = levels of=20 PDGF ligand available to the B cells is sufficient to induce atypical=20 hyperplasias with a similar degree of cellular atypia and pleomorphism = as that=20 found in low- to intermediate-grade human gliomas. This suggests that = these=20 cells may be particularly susceptible to neoplastic transformation. = Activation=20 of PDGFR signaling may provide a first step in this process. There is a=20 long-held belief that cells must accumulate numerous genetic alterations = to be=20 transformed. For example, cultured human astrocytes require = overexpression of=20 hTERT, Ras, and human papillomavirus E6/E7 to form xenograft tumors (Sonoda=20 et al., 2001). However, the initial growth events that allow for the = accumulations of these mutations are poorly understood, and new evidence = suggests that physiological levels of oncogene expression may be = sufficient to=20 initiate transformation (Tuveson=20 et al., 2004). Targeting mutations to the appropriate cell of origin = may be=20 crucial for understanding requirements for transformation. This study = identifies=20 a subpopulation of cells that under epigenetic stimulation can give rise = to=20 large hyperplasias that may serve as a substrate for accumulation of=20 transforming mutations.

The robust expression of the bHLH transcription factor Olig2 by a = large=20 proportion of the cells responding to PDGF stimulation is also = intriguing. In=20 addition to its physiological roles in specifying oligodendrocyte = development,=20 overexpression of Olig2 is also a common event in gliomas of all grades = and=20 classes (Lu=20 et al., 2001 and Ligon=20 et al., 2004), and Olig2 has also been directly implicated in = tumorigenesis=20 in other tissues (Wang=20 et al., 2000 and Chatterjee=20 et al., 2002). Future studies examining if Olig2 is a critical = mediator of=20 PDGF-induced hyperproliferation may yield new insights into the putative = growth-promoting properties of this transcription factor.

We have identified a population of PDGFR=CE=B1+ B cells in = the adult=20 SVZ and shown that they give rise to both neurons and oligodendrocytes = in vivo.=20 These findings are significant due to our limited knowledge of surface = markers=20 for neural stem cells. Our data also provide evidence of a link between = these=20 PDGFR=CE=B1+ B cells and the early changes associated with = tumor=20 initiation, suggesting they may be targets of neoplastic transformation. = The=20 regression of atypical hyperplasia after PDGF removal described here = suggests=20 that inhibition of PDGF signaling could provide a useful therapy for = those=20 gliomas in which the pathway is upregulated, especially given the = recovery of=20 the normal architecture after regression of the hyperplasia.

Experimental Procedures

Animals Used

For all adult experiments, we used 2- to 4-month-old CD-1 or GFAP-Tva = mice.=20 For PDGFR loss-of-function experiments, we used P0 = PDGFR=CE=B1Flox/Flox;=20 Z/EG mice. All animal procedures were approved by the Institutional = Animal Care=20 and Use Committee.

Human Postmortem Specimens

Three brains (ages 18, 50, and 80 years) were collected at autopsy. = All=20 specimens were obtained within 12 hr of death from patients without = clinical or=20 postmortem evidence of brain pathology and processed as described in Quinones-Hinojosa=20 et al. (2006). Collection of pathology specimens was in accordance = with the=20 guidelines of the UCSF Committee on Human Research (Approval #=20 H11170-19113-03B).

Immunohistochemistry

Mice were perfused with 4% paraformaldehyde, and the brains were = postfixed=20 overnight at 4=C2=B0C. Fifty micrometer sections were cut on the = Vibratome, blocked=20 in 5% goat serum in PBS (except where noted), and incubated overnight at = 4=C2=B0C in=20 primary antibody. Polyclonal PDGFR=CE=B1 (ready-to-use no dilution; = Spring=20 Biosciences), monoclonal PDGFR=CE=B1 (required antigen retrieval by = boiling in 10 mM=20 citrate buffer for 10 min, 1:50 dilution; Spring Biosciences), = polyclonal=20 PDGFR=CE=B1-phosphoTyr720 (Blocked in 5% donkey serum, 1:50 dilution in = PBS=20 containing 1.5% donkey serum; Santa Cruz Biotechnology), monoclonal = FGF-R1 and 2=20 (1:500; Chemicon), monoclonal GFAP (1:1000; Chemicon), polyclonal GFAP = (1:500;=20 DAKO), PSA-NCAM (1:400; AbCys), Doublecortin (1:500 + 0.5% Triton-X 100; = Chemicon), Nestin (1:500 + 0.5% Triton-X 100; Chemicon), Olig2 = (1:10,000; a kind=20 gift of Charles Stiles), O4 (1:100; Chemicon), Tuj1 (1:500; Covance), = and GFP=20 (1:500; Aves Labs). Controls in which primary antibody was omitted = resulted in=20 no immunostaining. Preincubation of the rabbit polyclonal PDGFR=CE=B1 = antibody with=20 blocking peptide resulted in no immunostaining for this antibody.

PDGF Administration

For receptor activation analysis, two injections of PDGF-AA (R&D = Systems;=20 6.6 ng) in vehicle (2 =CE=BCl) or vehicle (1 mg/ml BSA/0.9% saline) = alone, separated=20 by 20 min, were administered and animals perfused immediately after the = last=20 injection. For infusions, PDGF-AA (40 ng/day for low-concentration and = 240=20 ng/day for high-concentration experiments) in vehicle or vehicle alone = was=20 infused into the lateral ventricle for 6 or 14 days with a miniosmotic = pump=20 (Alzet). At least three mice per group were infused for all = experiments.

Ara-C Infusion

Two percent Ara-C (Sigma) was infused as previously described (Doetsch=20 et al., 1999b).

Neurosphere Experiments

Neurospheres were prepared from the SVZ of adult mice (five mice per=20 experiment; Doetsch=20 et al., 1999a). Cells were plated at a density of 25 cells/=CE=BCl = in the=20 presence of bFGF (10 ng/ml), PDGF-AA (20 ng/ml), or EGF (20 ng/ml) as = indicated.=20 Primary neurospheres were counted 9 days after plating, and secondary=20 neurospheres were counted 7 days after passaging. Neurosphere = differentiation=20 was performed as described Doetsch=20 et al. (1999a).

AAV5-GFP Infection

0.1=CE=BCl of AAV5-GFP (1012 PFU/ml) was injected into the = SVZ of CD-1=20 mice 24 hr after Ara-C treatment at three coordinates: anterior, = lateral, depth=20 (mm) relative to bregma, the midline, and the surface of the brain, = respectively=20 (0, 1.4, 1.6; 0.5, 1.1, 1.7; and 1, 1, 2.3). (See Supplemental=20 Experimental Procedures for in vivo controls for the specificity of = AAV5-GFP=20 infection in PDGFR=CE=B1-expressing cells).

RCAS Infection with PDGF Infusion and Analysis

0.2 =CE=BCl of RCAS-GFP virus (3D"not,2 =C3=97=20 107 PFU/ml) was injected into the SVZ of GFAP-Tva mice at = three=20 coordinates: (0, 1.4, 1.6; 0.5, 1.1, 1.7; and 1, 1, 2.3). PDGF or = vehicle was=20 infused at the time of retrovirus injection, and mice were sacrificed 6 = days (n=20 =3D 3) or 27 days (n =3D 4) after infection. For quantification of = GFP+=20 cells 21 days after pump removal, 50 =CE=BCm coronal vibratome sections = from four=20 saline-infused and four PDGF-infused mice, were immunostained for GFP. = The total=20 number of green cells present in the CC was counted in three sets of six = sections spanning the SVZ from anterior to posterior. For quantification = of=20 GFP+ cells present in the olfactory bulb, all green cells = present in=20 three equivalent OB sections were counted per mouse.

Coinfection with AAV5-GFP and RCAS-AP

0.2 =CE=BCl of a 1:1 mixture of AAV5-GFP (1012 PFU/ml) and = RCAS-AP=20 virus (3D"not,107 PFU/ml) was injected into the SVZ of GFAP-Tva = mice at=20 three coordinates: (0, 1.4, 1.6; 0.5, 1.1, 1.7; and 1, 1, 2.3). Mice = were=20 sacrificed 21 days after infection. Mice were perfused with 4% = paraformaldehyde=20 and postfixed overnight. The brains were cryoprotected in 30% sucrose = then=20 frozen in OCT prior to cutting (12 =CE=BCm sections) on a cryostat. = Endogenous AP was=20 inactivated by heating at 65=C2=B0C in PBS for 30 min. The sections were = then washed=20 in AP detection buffer (100 mM Tris-HCl [pH 9.5], 100 mM NaCl, 5 mM = MgCl2) then=20 incubated in AP buffer containing NBT/BCIP (200 =CE=BCl/10ml; Roche) = overnight at=20 room temperature. The reaction was halted by washing in PBS and IHC for = GFP was=20 performed.

P0 Infection of PDGFR=CE=B1Fl/Fl; Z/EG Mice = with AdCre

P0 infections were performed as previously described (Merkle=20 et al., 2004). Brains were analyzed at 8 weeks of age. For = quantification of=20 GFP+ cells, 50 =CE=BCm coronal vibratome sections from four = control and=20 four PDGFR=CE=B1Fl/Fl mice were immunostained for GFP. The = total number of=20 green cells present in the CC was counted in six sections spanning the = SVZ from=20 anterior to posterior. For quantitation of GFP+ neurons, all = green=20 cells present in three equivalent OB sections were counted per mouse.

Western Blots

Tissues were lysed in RIPA buffer containing protease and phosphatase = inhibitors. SDS-PAGE was performed using 20 =CE=BCg total protein per = lane. Western=20 blotting was performed using the SuperSignal West Pico kit (Pierce=20 Biotechnology) as per manufacturer's instructions. The primary = antibodies used=20 were as follows: PDGF-A (1:200; Santa Cruz), PDGF-B (1:200; Santa Cruz); = rabbit=20 anti-PDGFR=CE=B1 (1:200; Spring Bioscience); phospho-PDGFR=CE=B1 (1:100; = Santa Cruz).=20


Acknowledgments

This work was supported by the Goldhirsh Foundation and NIH grant = HD-32116.=20 E.L.J. was supported by American Brain Tumor Association and American = Cancer=20 Society Fellowships. A.A.-B. holds the Heather and Melanie Muss Endowed = Chair.=20 The authors would also like to acknowledge John and Frances Bowes for = their=20 support of this research. We are grateful to C. Stiles and D. Rowitch = for=20 providing us with the Olig2 antibody and B. Davidson for providing = AAV5-GFP. The=20 PDGFR=CE=B1Fl/Fl mice were a generous gift from P. Soriano, = and GFAP-Tva=20 mice were a kind gift from E. Holland. We thank F. Merkle, N. Sanai, and = C.=20 Yaschine for editorial comments and general discussion and support of = this work.=20 We also thank three anonymous reviewers for their comments, which helped = improve=20 this study.


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Zhu=20 et al., 2005 Y. Zhu, F. Guignard, D. Zhao, L. Liu, D.K. Burns, R.P. = Mason,=20 A. Messing and L.F. Parada, Early inactivation of p53 tumor suppressor = gene=20 cooperating with NF1 loss induces malignant astrocytoma, Cancer = Cell=20 8 (2005), pp. 119=E2=80=93130. SummaryPlus=20 | Full=20 Text + Links | PDF (1719 K) | View Record in Scopus | Cited By in Scopus (33)


Supplemental Data


(891 K)
Document_S1..pdf    3D"Help
Acrobat PDF file 1.=20

Document S1. Five Figures and Supplemental Experimental = Procedures. =20



Corresponding author
4 Present address: Department of = Neurosurgery,=20 Johns Hopkins University, Baltimore, Maryland 21218.



Volume=20 51, Issue 2, 20 July 2006, Pages 187-199
 
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A:hover { TEXT-DECORATION: none } TABLE.sdMainNavCenter TD { FONT-SIZE: 1em; BORDER-LEFT: white 0.01em solid; HEIGHT: 1.82em } TABLE.sdMainNavCenter TBODY { FONT-SIZE: 1em } TD { FONT-SIZE: 1em } TR { FONT-SIZE: 1em } DIV { FONT-SIZE: 1em } TABLE.sdMainNavCenter { BORDER-RIGHT: white 0.01em solid; HEIGHT: 1.82em } TABLE.sdMainNav A { FONT-WEIGHT: normal; PADDING-BOTTOM: 0.33em; VERTICAL-ALIGN: middle; = COLOR: white; PADDING-TOP: 0.19em; HEIGHT: 1.82em; TEXT-DECORATION: none } TABLE.sdMainNav A:link { FONT-WEIGHT: normal; PADDING-BOTTOM: 0.33em; VERTICAL-ALIGN: middle; = COLOR: white; PADDING-TOP: 0.19em; HEIGHT: 1.82em; TEXT-DECORATION: none } TABLE.sdMainNav A:visited { FONT-WEIGHT: normal; PADDING-BOTTOM: 0.33em; VERTICAL-ALIGN: middle; = COLOR: white; PADDING-TOP: 0.19em; HEIGHT: 1.82em; TEXT-DECORATION: none } DIV.sdMainNavPadding { PADDING-RIGHT: 1em; PADDING-LEFT: 1em } .alphaDivider { DISPLAY: inline; WIDTH: 0px; POSITION: relative; HEIGHT: 0px } .alphaSelect { LEFT: 0px; 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; WIDTH: 415px } ------=_NextPart_000_0000_01C8586C.7651BE40 Content-Type: application/octet-stream Content-Transfer-Encoding: quoted-printable Content-Location: http://ad.doubleclick.net/adj/scidir.rbi/;dcopt=ist;abr=!webtv;categ=neuroscigen;acct=d51dc24a2b132512122a31f7d7dda950;sz=728x90;ptile=1;ord=762277? document.write('\n
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