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Article

Subventricular Zone Astrocytes Are Neural Stem Cells in the Adult = Mammalian=20 Brain

Fiona Doetsch¹,=20 Isabelle Caill=C3=A9¹,=20 Daniel A. Lim¹,=20 Jose Manuel Garc=C3=ADa-Verdugo²=20 and Arturo Alvarez-Buylla^,^,¹^,=20^=E2=80=A1=20
¹ The Rockefeller University, = New York,=20 New York 10021, USA
² University of = Valencia,=20 Burjassot-46100, Valencia, Spain
Received 15 December 1998; = Revised 10=20 May 1999. Available online 28 June 2004.

Abstract

Neural stem cells reside in the subventricular zone (SVZ) of the = adult=20 mammalian brain. This germinal region, which continually generates new = neurons=20 destined for the olfactory bulb, is composed of four cell types: = migrating=20 neuroblasts, immature precursors, astrocytes, and ependymal cells. Here = we show=20 that SVZ astrocytes, and not ependymal cells, remain labeled with = proliferation=20 markers after long survivals in adult mice. After elimination of = immature=20 precursors and neuroblasts by an antimitotic treatment, SVZ astrocytes = divide to=20 generate immature precursors and neuroblasts. Furthermore, in untreated = mice,=20 SVZ astrocytes specifically infected with a retrovirus give rise to new = neurons=20 in the olfactory bulb. Finally, we show that SVZ astrocytes give rise to = cells=20 that grow into multipotent neurospheres in vitro. We conclude that SVZ=20 astrocytes act as neural stem cells in both the normal and regenerating = brain.=20

Article Outline

=E2=80=A2=20 Introduction
=E2=80=A2=20 Results =E2=80=A2=20 Type B Cells Divide Early during Regeneration of the SVZ =E2=80=A2=20 Dividing Type B Cells Give Rise to Type C Cells and Neuroblasts =E2=80=A2=20 Type B Cells Are the Only Label-Retaining Cells in the Adult SVZ =E2=80=A2=20 GFAP-Positive Cells in Untreated Mice Give Rise to New Neurons in = the=20 Olfactory Bulb =E2=80=A2=20 Neurospheres Are Derived from SVZ Cells =E2=80=A2=20 Neurospheres Are Derived from Type B Cells
=E2=80=A2=20 Discussion
=E2=80=A2=20 Experimental Procedures =E2=80=A2=20 Ara-C Infusions =E2=80=A2=20 Immunohistochemistry =E2=80=A2=20 BrdU Administration and Detection =E2=80=A2=20 [³H]Thymidine Autoradiography and EM Analysis =E2=80=A2=20 Retroviral Injections for In Vivo Studies =E2=80=A2=20 Whole-Mount Cultures =E2=80=A2=20 Neurosphere Preparation and Differentiation =E2=80=A2=20 Adenoviral Vectors =E2=80=A2=20 Production of pAd5-GFAPp-GFP Adenoviral Vector =E2=80=A2=20 Adenoviral Injections into the SVZ =E2=80=A2=20 Labeling of the Ependymal Layer with Vital Dyes =E2=80=A2=20 Fluorescent Tracers =E2=80=A2=20 Adenoviral Tracers =E2=80=A2=20 Scoring of Vitally Labeled Cells and Neurospheres
=E2=80=A2=20 Acknowledgements
=E2=80=A2=20 References

Introduction

Neurons and macroglia (astrocytes and oligodendrocytes) arise from = precursors=20 in the germinal layers of the developing brain, the ventricular and=20 subventricular zones (VZ and SVZ, respectively). Multipotential neural = stem=20 cells are present in these regions during development ([62,=20 65,=20 13,=20 31,=20 67=20 and 52]).=20 However, separate precursors for glial cells and neurons have also been=20 described ( [53,=20 38,=20 50,=20 39,=20 54=20 and 58]).=20 It has long been thought that lineages for neurons and macroglia become=20 progressively segregated during development ( [29]),=20 suggesting that multipotential stem cells are only present early on = during brain=20 histogenesis. Neurogenesis and gliogenesis, however, continue throughout = life,=20 and multipotent stem cells can be isolated from the adult brain = (reviewed in [21,=20 67,=20 40=20 and 63]).=20 In nonneural epithelia and the hematopoietic system, the continued = production of=20 new cells throughout adulthood has permitted experimental manipulations = that led=20 to the identification of stem cells in several tissues ( [49,=20 61=20 and 12]).

The generation of large numbers of new neurons destined for the = olfactory=20 bulb throughout adult life ([1,=20 35=20 and 15])=20 provides an experimental opportunity for the identification of their in = vivo=20 primary precursors. These new neurons are born in the SVZ, a thin layer = of=20 dividing cells that persists along the lateral wall of the lateral = ventricles. A=20 layer of epithelial cells known as ependymal cells separates the SVZ = from the=20 lateral ventricles. SVZ neuroblasts migrate as a network of tangentially = oriented chains ( [15=20 and 36])=20 that converge on the rostral migratory stream (RMS) to reach the = olfactory bulb,=20 where they differentiate into local interneurons ( [37,=20 35=20 and 15]).=20 Within the SVZ, the migrating neuroblasts (type A cells) advance as = chains=20 through tubes defined by the processes of slowly proliferating SVZ = astrocytes=20 (type B cells). Clusters of rapidly dividing immature precursors (type C = cells)=20 are scattered along the network of migrating chains ( [16]).=20 The identification of the in vivo stem cells will allow elucidation of = the=20 molecular mechanisms for their proliferation and differentiation. = Furthermore,=20 the targeted manipulation of these cells in vivo and the isolation of = specific=20 pools of adult-derived precursors may be of use for brain repair.

Neural stem cells that have the capacity to self-renew and = differentiate into=20 neurons and glia can be cultured from the adult SVZ ([42=20 and 26]).=20 These cells grow as spherical floating clusters (neurospheres) in the = presence=20 of epidermal growth factor (EGF) or basic fibroblast growth factor = (bFGF) ( [55=20 and 25]).=20 Previous work has suggested that SVZ neural stem cells correspond to a = rare=20 population of relatively quiescent cells ( [42]).=20 More recently, it has been suggested that ciliated ependymal cells = correspond to=20 the neural stem cells ( [30]).

We show here that SVZ astrocytes (type B cells) are the in vivo = precursors of=20 new neurons. SVZ astrocytes divide to regenerate the SVZ network of = migrating=20 neuroblasts after elimination of all migrating neuroblasts and type C = cells. In=20 untreated mice, only SVZ astrocytes, and not ependymal cells, remain = labeled in=20 the SVZ following long survivals after administration of proliferation = markers.=20 Furthermore, following the targeted introduction of a retrovirus into = glial=20 fibrillary acidic protein (GFAP)-positive cells of untreated mice, = retrovirally=20 labeled migrating neuroblasts and fully differentiated neurons were = observed in=20 the olfactory bulb. Finally, we show that SVZ astrocytes give rise to = cells that=20 grow into multipotent neurospheres in vitro. These findings identify SVZ = astrocytes, or a subpopulation of these cells, as the in vivo precursors = of=20 newly generated neurons in the adult mammalian brain and suggest that = they act=20 as stem cells in this region.

Results

In work to be presented elsewhere, we show that the SVZ of the adult = mouse=20 brain completely regenerates after elimination of migrating neuroblasts = (type A=20 cells) and precursor cells (type C cells) with the antimitotic drug=20 cytosine-=CE=B2-D-arabinofuranoside (Ara-C) (F. D. et al., unpublished = data).=20 Immediately after Ara-C treatment, SVZ astrocytes (type B cells) and = ependymal=20 cells remain; 2 and 4 days later, type C and A cells appear = consecutively. These=20 findings suggest that either SVZ astrocytes or ependymal cells divide to = regenerate the SVZ.

Type B Cells Divide Early during Regeneration of the = SVZ

In order to confirm the identification of type B cells in the SVZ = immediately=20 after Ara-C treatment, we performed immunostaining for GFAP, a marker of = SVZ=20 astrocytes. At the light microscope (Figure=20 1A), all cells appeared GFAP positive. However, since GFAP-negative = cells=20 may appear labeled if surrounded by GFAP-positive processes, we used=20 postembedding immunogold staining for GFAP to identify labeled cells at = the=20 electron microscope (EM). This analysis confirmed that after Ara-C = treatment,=20 remaining cells in the SVZ were labeled by GFAP antibodies. GFAP = immunostaining=20 was localized to the bundles of intermediate filaments that characterize = type B=20 cells ( Figure=20 1B and Figure=20 1C). Type B cells after Ara-C treatment were also lightly stained = for S100=CE=B2=20 and vimentin (not shown).=20

Display=20 Full Size version of this image = (3K)

Figure 1. Cells Remaining in the SVZ after Ara-C Treatment Are GFAP = PositiveGFAP-postembedding immunostaining of the SVZ in 1.5 =CE=BCm = semithin (A)=20 and 70 nm=20 ultrathin sections (B and C).(A) SVZ cells immediately after Ara-C are = GFAP=20 positive. Asterisks show cell bodies of labeled cells.(B) = Silver-enhanced=20 immunogold labeling for GFAP immediately after Ara-C treatment. At the = EM,=20 these cells are characterized by dense bundles of intermediate = filaments that=20 are immunostained by GFAP antibodies.(C) Detail of immunostained = intermediate=20 filaments shown in (B) (rectangle). Scale bars: (A), 20 =CE=BCm; (B), = 1 =CE=BCm; (C),=20 0.25 =CE=BCm.Dividing cells reappear scattered throughout the SVZ 0.5 = days after=20 termination of Ara-C treatment (F. D. et al., unpublished data). To = identify=20 which cells divided after Ara-C treatment, mice were injected = systemically=20 with [³H]thymidine, a marker of DNA synthesis, 0.5 days = after Ara-C=20 treatment and killed 1 hr later. [³H]thymidine-labeled = cells in=20 both the injected and contralateral hemispheres were identified at the = EM (Figure=20 2A and Table=20 1). Of 154 cells studied, 152 corresponded to type B cells and 2 = to=20 microglia. None corresponded to ependymal cells. Some=20 [³H]thymidine-labeled cells were very close to the = ependymal layer=20 but were always separated from the ventricle by the cytoplasm of an = ependymal=20 cell.=20

Display=20 Full Size version of this image = (3K)

Figure 2. Proliferating Type B Cells Give Rise to Type C Cells and=20 NeuroblastsTime lines illustrate the duration of Ara-C treatment and = time of=20 pulse labeling (double arrow) with [³H]thymidine (top = panels) or=20 retrovirus (bottom panels). Thin arrows indicate the time points at = which the=20 SVZ was analyzed with respect to the end of Ara-C treatment.(A) In=20 [³H]thymidine-injected mice killed 1 hr after pulse = labeling, type=20 B cells (b) were observed with the EM; upper inset shows the same cell = with=20 silver grains overlying its nucleus in a semithin section (see Table=20 1). Lower right inset shows a bundle of intermediate filaments,=20 characteristic of type B cells, in the = [³H]thymidine-labeled=20 cell.(B) Two days after pulse labeling proliferating astrocytes, type = C cells=20 (c) were observed in addition to type B cells. Inset shows silver = grains=20 overlying the nuclei of the two cells identified at the EM as type C = cells.(C)=20 Alkaline phosphatase=E2=80=93positive cells with a stellate morphology = were observed 1=20 day after infection with DAP retrovirus.(D) At 4 days, small clusters = of=20 tightly associated cells are present.(E) At 6 days, many cells with = the=20 morphology of migrating neuroblasts (type A cells) were observed.(F) = Semithin=20 section of =CE=B2-galactosidase retrovirally labeled cell (blue = precipitate) 1.5=20 days after Ara-C.(G) This same cell analyzed at the EM corresponds to = a type B=20 cell. Scale bars: (A) and (B), upper inset, 10 =CE=BCm; = photomicrograph, 2.5 =CE=BCm;=20 lower inset, 0.5 =CE=BCm; (C), 30 =CE=BCm; (D), 40 =CE=BCm; (E), 20 = =CE=BCm; (F), 10 =CE=BCm; (G), 2=20 =CE=BCm.=20

Table 2. Characterization of Cellular Composition of Retrovirally = Infected=20 Clusters after Ara-C Treatment

Table 1. Cell Types Labeled with [³H]thymidine after = Pulse=20 Labeling at 12 Hr after Ara-C Treatment

[³H]thymidine-labeled cell types at different survivals = following=20 pulse labeling at 12 hr after Ara-C treatment. [³H]thymidine = was=20 injected at 0.5 days after Ara-C treatment and mice killed 1 hr or 1.5 = or 5.5=20 days later. Percentage of each cell type labeled with = [³H]thymidine=20 of total labeled cells analyzed at the EM (absolute numbers of cells in=20 brackets).

Dividing Type B Cells Give Rise to Type C Cells and=20 Neuroblasts

To test whether type B cells divide to give rise to other cell types, = we=20 injected [³H]thymidine systemically 0.5 days after Ara-C = treatment to=20 label proliferating type B cells. Mice were then killed 1.5 or 5.5 days = after=20 [³H]thymidine injection. After processing for = autoradiography,=20 [³H]thymidine-labeled cells were identified at the EM. One = and a half=20 days after [³H]thymidine injection, more than one-third of = the=20 labeled cells corresponded to type C cells (Figure=20 2B and Table=20 1). These results indicate that proliferating type B cells divided = to give=20 rise to type C cells. In mice pulse labeled at 12 hr and killed 5.5 days = later,=20 labeled type A cells were identified, indicating that they too are = derived from=20 type B cells ( Table=20 1). Labeled type A cells, however, had only a few grains overlying = their=20 nuclei, suggesting multiple divisions of their progenitors.

To confirm that type A cells were derived from proliferating type B = cells,=20 three different replication-incompetent retroviruses, which are stably = inherited=20 by the progeny of dividing cells without dilution upon division, were = used to=20 infect proliferating type B cells 0.5 days after Ara-C treatment. A = retrovirus=20 encoding human placental alkaline phosphatase (DAP) ([19])=20 was used to analyze the morphology of retrovirally labeled cells. Since = the DAP=20 precipitate could not be localized at the EM, we used a retrovirus = encoding=20 =CE=B2-galactosidase (=CE=B2-gal) ( [51])=20 to characterize labeled cells at the EM. Finally, a retrovirus encoding = green=20 fluorescent protein (GFP) (LZRS-CA-gapEGFP; [44])=20 was used to follow live cells in culture (see below).

At different survivals after retroviral infection with DAP following = Ara-C=20 treatment, whole mounts were dissected and processed for alkaline = phosphatase=20 (AP) histochemistry, and the morphology of AP-positive cells was = analyzed. One=20 day after infection with the DAP retrovirus, AP-positive stellate cells = with=20 multiple processes were observed (Figure=20 2C). This branched morphology suggested that these cells correspond = to type=20 B cells ( [16]).=20 In order to confirm the identity of retrovirally labeled cells, 11 cells = that=20 were infected with a =CE=B2-gal-encoding retrovirus were studied at the = EM 1 day=20 after infection. All 11 corresponded to type B cells (e.g. Figure=20 2F and Figure=20 2G). By 4 days after infection with the DAP retrovirus, tight = clusters of=20 AP-positive cells were observed ( Figure=20 2D). These clusters contained globular and branched cells. Five and = a half=20 days after infection, many smaller AP-positive cells with the morphology = of=20 migrating neuroblasts (type A cells) ( [32];=20 [68])=20 were present. Their cell bodies were round or elongated, with a thin = leading=20 process tipped by a growth cone and occasionally with a trailing process = ( Figure=20 2E). Some type A cells were dispersed, suggesting that they had = already=20 migrated tangentially.

We analyzed the composition of retrovirally infected clusters in = whole-mount=20 preparations at different survivals after Ara-C treatment (Table=20 2). AP-positive cells within each cluster were classed as branched,=20 globular, or migratory based on their morphology ( Table=20 2). Initially, all of the clusters comprised only one or two cells, = and all=20 contained branched cells. Over time, more mixed clusters with both = branched and=20 globular morphologies were observed, and then clusters containing = branched,=20 globular, and migratory morphologies appeared. Six days after = termination of=20 Ara-C treatment, most of the clusters contained the three cell = morphologies,=20 indicating that many of the single infected cells we observed at one and = a half=20 days eventually formed part of neurogenic clusters.

The above results suggest that type B cells give rise to neurons via = an=20 intermediate globular cell type. In order to directly follow the = production of=20 neuroblasts from type B cells, we used a retrovirus encoding GFP = injected in=20 vivo 0.5 days after termination of Ara-C treatment. One day after = infection,=20 GFP-labeled cells with the branched morphology of type B cells were = observed in=20 whole-mount preparations of the SVZ (Figure=20 3A). These whole mounts were sectioned and double stained for GFAP. = The=20 processes of GFP-positive cells were stained for GFAP ( Figure=20 3B=E2=80=933D), confirming that they were SVZ astrocytes.=20

Display=20 Full Size version of this image = (4K)

Figure 3. GFAP-Positive Cells Give Rise to Neuroblasts In Vitro(A)=20 Whole-mount dissection of the lateral wall of the lateral ventricle 1 = day=20 after infection with a retrovirus encoding GFP. The retrovirus was = injected=20 0.5 days after the end of Ara-C treatment. Only cells with a branched=20 morphology were present at this survival. These whole mounts were = sectioned=20 transversely and stained with an anti-GFAP mAb.(B) One micrometer = confocal=20 optical slice showing the GFP-labeled cells.(C) GFAP staining of this = same=20 section.(D) GFP-positive cells are GFAP positive. The ependymal layer = in (B=E2=80=93D)=20 came off during immunocytochemical processing. Ependymal cells were = not=20 labeled by the reporter gene.(E=E2=80=93K) Direct observation of the = production of=20 neuroblasts by type B cells. Proliferating type B cells were infected = as in=20 (A). One day after infection, whole mounts were dissected, embedded in = a=20 collagen gel, and cultured to follow the fate of GFP-labeled cells = daily. (E)=20 Two GFP cells with a branched morphology after 1 day in culture. (F) = The lower=20 of the two branched cells divided and generated a tight cluster of = globular=20 cells (arrowhead). The upper cell also divided into branched (arrow) = and=20 unbranched cells. (G) By 3 days, the lower cluster began to disperse, = and some=20 cells with a leading process and a growth cone typical of type A cells = (arrow)=20 were present. By this time, the upper cell had also generated a tight = cluster=20 of globular cells (arrowhead). (H) One day later, several type A cells = were=20 present (arrows), and some had moved away from the clusters. = (I=E2=80=93K) At this=20 time, the cultures were fixed and stained for TuJ1, revealing that = some=20 GFP-positive cells (arrow) were TuJ1 positive. (E=E2=80=93H) are = photomicrographs of=20 live three-dimensional cultures. (B=E2=80=93D) and (I=E2=80=93K) are = confocal 1 =CE=BCm optical=20 sections through fixed cultures. Scale bars: (A=E2=80=93D), 10 = =CE=BCm; (E=E2=80=93K), 5 =CE=BCm.To=20 follow the fate of individual live GFP-labeled cells over time, = dividing cells=20 were infected 0.5 days after Ara-C treatment in vivo. One day after = infection,=20 fragments of the SVZ were dissected and cultured in a collagen gel. = Individual=20 GFP-positive cells were marked and photographed daily to follow their=20 progression (Figure=20 3E=E2=80=933K). Some of the branched cells divided to give rise to = tight clusters=20 of globular cells ( Figure=20 3F). The tight clusters dispersed after 4 days ( Figure=20 3G), and cells with a small round or elongated cell body and a = leading=20 process appeared ( Figure=20 3H). Some of these cells were TuJ1 positive, confirming their = neuronal=20 identity ( Figure=20 3I=E2=80=933K). These results directly show that dividing type B = cells give rise=20 to neurons after Ara-C treatment via an intermediate globular cell = type.=20

Type B Cells Are the Only Label-Retaining Cells in the = Adult=20 SVZ

Although SVZ astrocytes regenerate the network of chains of = neuroblasts after=20 Ara-C treatment, these cells may behave as neuronal precursors only = during=20 regeneration. A recent paper has suggested that under normal conditions, = ependymal cells are the in vivo precursors of new neurons ([30]).

Cells that remain labeled in germinal layers for extended periods = after=20 [³H]thymidine injection are considered candidate stem cells = ([49=20 and 12]).=20 We therefore studied which dividing cell types in the SVZ of normal = adult mice=20 remained labeled at long survivals after BrdU or = [³H]thymidine=20 treatment. Single injections of [³H]thymidine had previously = revealed=20 that migrating neuroblasts (type A cells), type C cells, and SVZ = astrocytes=20 (type B cells) are proliferating. However, more slowly proliferating = cells may=20 not be labeled with single injections. We therefore used the same = protocol as=20 [30],=20 in which BrdU was administered continuously to mice in their drinking = water for=20 2 weeks. Sections were double stained for both BrdU and mCD24 ( [9])=20 or S100=CE=B2 ( [14]),=20 both highly expressed by ependymal cells. In mice killed immediately = after=20 treatment, many BrdU-labeled cells were encountered in the SVZ, but none = corresponded to ependymal cells (not shown). In mice killed 1 week after = the end=20 of treatment, the number of BrdU-positive nuclei was greatly reduced. = Again some=20 labeled nuclei were found close to the ventricular surface, but no = labeled=20 ependymal cells were observed. Strongly labeled S100=CE=B2 (not shown) = or mCD24 ( Figure=20 4A) processes separated these nuclei from the ventricular cavity.=20

Display=20 Full Size version of this image = (5K)

Figure 4. Type B Cells in the SVZ Are Labeled at Long Survivals = after BrdU=20 Administration or [³H]Thymidine InjectionsBrdU was = administered=20 continuously in the drinking water for 2 weeks, and sections were = double=20 stained for BrdU (green) and mCD24 (red).(A) One week after treatment, = no=20 BrdU-positive mCD24 ependymal cells were observed. While BrdU-labeled = nuclei=20 were closely associated with ependymal cells, these nuclei were not = surrounded=20 by mCD24 staining. Ependymal nuclei (arrows) were surrounded on all = sides by=20 mCD24.(B) Upper inset shows silver grains overlying the nucleus = (arrow) of a=20 ³H-labeled cell in the SVZ after [³H]thymidine = was=20 infused into the lateral ventricles for 12 days. Labeled nuclei that = at the=20 light microscope appeared to be in the ependymal layer were studied at = the EM.=20 These cells did not correspond to ependymal cells but had the = ultrastructural=20 characteristics of type B cells. Thin ependymal cell processes = separate most=20 of these cells from the ventricle.(C) Upper inset shows silver grains=20 overlying the nucleus (arrow) of a ³H-labeled cell in the = SVZ 30=20 days after four [³H]thymidine injections. Ultrastructural = analysis=20 of this labeled cell (asterisk) reveals that it is a type B cell (b) = adjacent=20 to a chain of type A cells (a). Scale bars: (A), 10 =CE=BCm; = (B=E2=80=93C), inset, 10 =CE=BCm;=20 photomicrograph, 2 =CE=BCm. LV, lateral ventricle.=20

Since SVZ cells and ependymal cells are so tightly associated, = electron=20 microscopy is required to confirm the membrane boundaries of labeled = cells. We=20 infused [³H]thymidine into the lateral ventricle continuously = for 12=20 days with a mini-osmotic pump. We then analyzed = [³H]thymidine-labeled=20 cells close to the ventricle (Figure=20 4B). ³H-labeled cells were identified in 2 =CE=BCm = autoradiograms and=20 analyzed at the EM. One hundred and fifteen cells were studied, none of = which=20 corresponded to ependymal cells. In a separate experiment,=20 [³H]thymidine was injected systemically four times and mice = allowed=20 to survive 15 or 30 days. Twenty-four ³H-labeled cells were = analyzed=20 at the EM. With the exception of 1 microglial cell, the remaining 23 = cells all=20 corresponded to type B cells. Figure=20 4C shows a labeled type B cell adjacent to a chain of neuroblasts.

The above results indicate that type B cells remain labeled with=20 proliferation markers in the SVZ after long survivals under normal = conditions.=20 In contrast, we did not observe labeled ependymal cells after continuous = BrdU=20 administration for 2 weeks or after 12 days of continuous infusion of=20 [³H]thymidine into the lateral ventricle. The finding that = type B=20 cells were the only label-retaining cells in the SVZ at long survivals = suggests=20 that these cells may have divided asymmetrically and that one of the = daughter=20 cells generated progeny that had died or migrated away. Alternatively, = this=20 labeling could simply reflect endogenous glial turnover.

GFAP-Positive Cells in Untreated Mice Give Rise to New = Neurons in=20 the Olfactory Bulb

To determine whether type B cells are also neuronal precursors under = normal=20 conditions, a retrovirus encoding AP was specifically targeted into=20 GFAP-expressing cells using transgenic mice engineered to express the = receptor=20 for avian leukosis virus under the GFAP promoter (GFAP-Tva mice) ([27]).=20 Mammalian cells do not normally express the receptor for the avian = leukosis=20 virus and therefore cannot be infected by these viruses. However, when=20 replication-competent avian leukosis virus encoding alkaline phosphatase = (RCAS-AP) is injected into the brain of GFAP-Tva mice, GFAP-expressing = cells=20 undergoing division become infected ( [27])=20 and express the marker gene alkaline phosphatase. This allows the = progeny of=20 infected GFAP-expressing cells to be followed.

When RCAS-AP was injected into nontransgenic mice, no AP-positive = cells were=20 observed, confirming that RCAS-AP does not infect mammalian cells. When = DAP=20 retrovirus is injected into nontransgenic mice, AP-positive migrating = cells,=20 globular cells, and branched cells are present in the SVZ 1 day later. = In=20 contrast, 1 day after infection of GFAP-Tva mice with the RCAS-AP = retrovirus,=20 only labeled cells with branched morphologies were observed (n =3D 5, = 8=E2=80=9320 cells=20 per hemisphere) (Figure=20 5A); no AP-positive migrating cells or globular cells were observed = at this=20 short survival. Furthermore, no labeled ependymal cells were observed,=20 substantiating the above finding that ependymal cells do not divide in = vivo.=20 This confirms that the RCAS-AP virus is selectively infecting type B = cells. In=20 GFAP-Tva mice allowed to survive 3.5 days (n =3D 2) after infection, = AP-positive=20 migrating neuroblasts were encountered in the SVZ and RMS. The latter = were=20 oriented in the direction of the olfactory bulb ( Figure=20 5B). By 14 days (n =3D 5) after infection, many cells had reached = the=20 olfactory bulb and differentiated into granular and periglomerular = neurons ( Figure=20 5C and Figure 5D). Interestingly, infected cells remained labeled in = the SVZ=20 at 14 days, suggesting that stem cells had been originally infected. At = this=20 time, the SVZ contained both solitary branched cells and clusters that = contained=20 a mixture of the globular, branched, and migratory neurons ( Figure=20 5E). These results show that astrocytes in the SVZ produce new = neurons under=20 normal conditions in untreated mice.=20

Display=20 Full Size version of this image = (4K)

Figure 5. GFAP-Expressing Cells Generate Olfactory Bulb Neurons = under=20 Normal ConditionsAlkaline phosphatase=E2=80=93positive cells observed = after the=20 targeted infection of GFAP-positive cells using GFAP-Tva mice.(A) = Section=20 through an AP-positive branched cell in the SVZ 1 day after infection. = At this=20 time, no globular or migrating neuroblasts were encountered.(B) Three = and a=20 half days after infection, AP-positive migrating cells were observed = in the=20 RMS en route to the olfactory bulb (arrows).(C and D) Fourteen days = after=20 infection, many AP-labeled cells were found in the olfactory bulb. = These cells=20 had the typical morphology of granule (C) and periglomerular neurons = (D).(E)=20 In the SVZ of these mice, clusters containing branched globular and = migratory=20 cells were found. Scale bars: (A=E2=80=93E), 20 =CE=BCm.=20

Neurospheres Are Derived from SVZ Cells

The above results indicate that SVZ astrocytes are the primary = precursors for=20 new neurons in vivo. Neural stem cells, which grow in vitro as = neurospheres ([55]),=20 can be isolated from the adult SVZ ( [42]).=20 A recent study suggests that the majority of neurospheres are derived = from=20 ciliated ependymal cells ( [30]).=20 However, the long-term BrdU and [³H]thymidine administration=20 experiments described above indicate that ependymal cells do not divide = in vivo.=20 We tested whether ependymal cells lining the walls of the lateral = ventricles=20 could give rise to neurospheres. We injected DiI into the lateral = ventricle to=20 vitally label the ependymal cells (Figure=20 6A). Neurospheres were prepared from the contralateral hemisphere to = avoid=20 contamination of cells labeled along the injection track. After 10 days = in the=20 presence of EGF, 780 neurospheres grew, of which 191 contained = DiI-labeled cells=20 ( Figure=20 6B and Figure=20 6C). However, we noticed that uninternalized DiI or DiI-labeled = cellular=20 debris was present in these cultures. Since the labeling of the = neurospheres was=20 not homogeneous, it is possible that DiI may have labeled some = neurospheres=20 during or after dissociation. In addition, DiI may have been transferred = between=20 cells in vivo.=20

Display=20 Full Size version of this image = (4K)

Figure 6. Ependymal Cells Do Not Give Rise to Neurospheres(A) = Frontal=20 section showing the labeling of the ependymal layer in the = contralateral=20 hemisphere of a mouse that received an intraventricular injection of = DiI.(B=E2=80=93E)=20 Phase contrast (B and D) and epifluorescent (C and E) images of two=20 neurospheres cultured from the lateral wall of the lateral ventricle = of=20 DiI-injected mice. Both the contralateral (B and C) and the = ipsilateral=20 hemispheres (D and E) gave rise to neurospheres containing = DiI-positive cells.=20 However, we noticed that these cultures contained unincorporated DiI = (arrow)=20 and patchy DiI labeling of neurospheres.(F) Section showing the = labeling of=20 the ependymal layer in the contralateral hemisphere of a mouse that = received=20 an intraventricular injection of rhodamine beads.(G) Confocal image = showing=20 the region marked by a rectangle in (F) at higher magnification.=20 Rhodamine-positive cells are also immunopositive for mCD24 (green), = which=20 labels ependymal cells.(H=E2=80=93K) Phase contrast (H and J) and = epifluorescent (I=20 and K) images of two neurospheres cultured from the lateral wall of = the=20 lateral ventricle of rhodamine bead=E2=80=93injected mice. = Neurospheres arising from=20 the contralateral hemisphere did not show any rhodamine labeling (H = and I),=20 whereas some neurospheres from the ipsilateral hemisphere were = fluorescent (J=20 and K).(L) Section showing the labeling of the ependymal layer in the=20 contralateral hemisphere of a mouse that received an intraventricular=20 injection of an adenovirus carrying LacZ.(M and N) Nomarski images of = five DIV=20 neurospheres from the lateral wall of the lateral ventricle of = =CE=B2-gal=20 adenovirus-infected mice. Neurospheres grown from the contralateral = hemisphere=20 (M) are X-gal negative, whereas some neurospheres from the ipsilateral = hemisphere are X-gal positive (N). These small neurospheres were = allowed to=20 attach to poly-L-ornithine for 5 hr for staining. Scale bars: (A), 100 = =CE=BCm;=20 (B=E2=80=93E), 25 =CE=BCm; (F), 100 =CE=BCm; (G), 10 =CE=BCm; = (H=E2=80=93K), 50 =CE=BCm; (L), 100 =CE=BCm; (M and N),=20 25 =CE=BCm. LV, lateral ventricle; CL, contralateral; IL, ipsilateral. =

We therefore repeated this experiment using rhodamine fluorescent = beads,=20 which, unlike DiI, are internalized and not transferred between cells. = When=20 these beads were injected intraventricularly into one hemisphere, = ependymal=20 cells in the contralateral hemisphere were homogeneously labeled (Figure=20 6F). Double staining with mCD24 antibodies that strongly label the = ependymal=20 cells ( [9])=20 showed that the rhodamine bead labeling was restricted to the ependymal = layer (=20 Figure=20 6G). From the contralateral hemispheres of rhodamine = bead=E2=80=93injected mice, 936=20 neurospheres grew in EGF. None of these neurospheres were labeled with=20 fluorescent beads ( Figure=20 6H and Figure=20 6I). Brightly labeled fluorescent cells could be identified = immediately=20 after plating, but after 1 day, most of them had died and by 2 days = could not be=20 detected. It could be argued that rhodamine beads were not incorporated = into=20 stem cells or that beads were cytotoxic to the stem cells. However, from = the=20 ipsilateral side in which both SVZ cells and ependymal cells were = labeled with=20 rhodamine beads, 146 of 1022 neurospheres grown in EGF were = fluorescently=20 labeled ( Figure=20 6J and Figure=20 6K). Moreover, similar numbers of neurospheres were obtained from=20 noninjected animals, indicating that the rhodamine beads did not kill=20 neurosphere precursors.

We further tested whether ependymal cells could give rise to = neurospheres by=20 using a replication-defective adenovirus carrying =CE=B2-galactosidase = as a reporter=20 gene. This virus infects both dividing and nondividing cells, and when = injected=20 intraventricularly in one hemisphere, it resulted in labeling of the = ependymal=20 wall of the contralateral hemisphere (Figure=20 6L). As with the above experiments, in order to avoid contamination = of cells=20 that became labeled along the injection track, we used the contralateral = noninjected hemisphere. Seven hundred and thirty-two neurospheres grew = with EGF=20 from the contralateral hemisphere. These neurospheres were cultured for = 4 days=20 and stained with X-gal for detection of =CE=B2-gal activity. None of the = neurospheres=20 were X-gal positive ( Figure=20 6M). In control experiments, we used the ipsilateral side, where the = virus=20 infected some SVZ cells. In this latter case, 17 neurospheres out of 652 = were=20 X-gal labeled. This indicates that SVZ cells and not ependymal cells = give rise=20 to neurospheres. However, neurospheres from the contralateral side may = have=20 diluted the viral reporter gene below detection after repeated division. = To=20 follow the fate of virally labeled cells during the initial plating = procedure,=20 an adenovirus carrying GFP was used. This virus resulted in similar = ependymal=20 cell labeling as its =CE=B2-gal counterpart (not shown). After 10 days = in vitro=20 (DIV), 422 neurospheres from the contralateral hemisphere grew with EGF, = of=20 which none were GFP positive. We followed the fate of fluorescently = labeled=20 cells in culture during the initial period after plating. Soon after=20 dissociation, brightly fluorescent cells could be detected, but 1 day = later, no=20 GFP-labeled cells were present in our cultures. This suggests that = ependymal=20 cells, under these conditions, die soon after plating. Control = experiments using=20 the ipsilateral side, where the GFP adenovirus infected the SVZ, = resulted in=20 GFP-labeled cells that gave rise to neurospheres. In this latter case, = 12=20 GFP-labeled neurospheres out of 387 were observed. Taken together, the = above=20 experiments suggest that ependymal cells are not the precursors for=20 neurospheres.

We repeated the above experiments using bFGF+EGF to grow neurospheres = after=20 labeling the ependymal cells with adenovirus and fluorescent beads. We = found no=20 evidence for ependymal cells giving rise to neurospheres when grown with = bFGF+EGF (not shown).

Neurospheres Are Derived from Type B Cells

In order to vitally label type B cells in the SVZ, we constructed an=20 adenoviral vector expressing GFP under the control of the GFAP promoter = ([72,=20 73=20 and 5])=20 (GFAPp-GFP AV). When this virus was injected into the SVZ and animals = allowed to=20 survive for 48 hr, type B cells and adjacent astrocytes in the striatum = and=20 corpus callosum became selectively labeled ( Figure=20 7A=E2=80=937FFigure=20 7H, and Figure=20 7K). Double labeling for GFAP confirmed that the reporter gene was=20 specifically expressed in GFAP-containing cells ( Figure=20 7A=E2=80=937F). Using cell-specific markers, we showed that the = reporter gene was=20 not expressed in ependymal cells or in type A cells ( Figure=20 7G=E2=80=937L). Labeling of type B cells with GFP was confirmed by = preembedding=20 anti-GFP immunogold staining and EM (not shown). Ependymal cells were = not=20 labeled.=20

Display=20 Full Size version of this image = (3K)

Figure 7. GFAPp-GFP Adenovirus Selectively Labels AstrocytesAll = panels are=20 1 =CE=BCm confocal optical sections of frontal sections through the = SVZ (A=E2=80=93C and=20 G=E2=80=93L) and striatum (D=E2=80=93F) of mice infected with the = GFAPp-GFP adenovirus 48 hr=20 earlier. The rhodamine channel is shown in the left column and the = FITC=20 channel (GFP) in the middle column, and the two are merged in the = right=20 column.(A=E2=80=93F) GFP-positive cells in the SVZ (B) and striatum = (E) are GFAP=20 positive (A and D and C and F). Arrows in (A) indicate the = GFAP-negative=20 regions that correspond to chains of migrating neuroblasts in the = SVZ.(G=E2=80=93I)=20 CD24-positive cells in the ependymal wall (G) were not GFP positive (H = and I).=20 The GFP-positive cells correspond to SVZ cells.(J=E2=80=93L) = PSA-NCAM-positive cells=20 ([J], the migrating neuroblasts, type A cells) were not GFP positive = (K and=20 L). Instead, astrocytes around PSA-NCAM-positive migrating neuroblasts = were=20 positive. Scale bars: 10 =CE=BCm. LV, lateral ventricle. The schematic = at the=20 bottom shows the GFAP promoter reporter construct used for the = adenoviral=20 vector.=20

After dissociation of the walls of the ventricle in mice that were = injected=20 with the GFAP-GFP adenovirus, 0.4%=E2=80=931.2% of the total cells were = brightly=20 fluorescent. Wells containing single GFP-positive cells were marked and = these=20 fluorescent cells followed on a daily basis (Figure=20 8A=E2=80=938F). Results for four independent experiments are shown = in Figure=20 8. Of the fluorescently labeled cells scored, 9%=E2=80=9314.3% gave = rise to=20 neurospheres. Half of the neurospheres derived from GFP-expressing cells = were=20 plated for differentiation and shown to generate neurons and glia. In = addition,=20 the other half of the neurospheres differentiated into neurons and glia = after=20 forming secondary neurospheres ( Figure=20 8G). This experiment indicates that neurospheres can be derived from = GFAP-expressing cells in the SVZ.=20

Display=20 Full Size version of this image = (5K)

Figure 8. GFAP-GFP-Positive Cells Give Rise to = Neurospheres(A=E2=80=93F) SVZ cells=20 were infected in vivo with the GFAPp-GFP adenovirus; 48 hr later, = cells were=20 dissociated and cultured in multiwell plates. Epifluorescent (A, C, = and E) and=20 phase contrast (B, D, and F) images of a GFP-positive cell monitored = as it=20 generated a neurosphere. The GFP fluorescence is progressively reduced = as the=20 neurosphere grows due to dilution of the adenovirus or to promoter=20 inactivation (E). (A and B): 3DIV; (C and D): 5DIV, (E and F): = 8DIV.(G) Double=20 staining with Tuj1 (red) and GFAP (green) of a secondary neurosphere = derived=20 from the neurosphere shown in (F) differentiated into neurons and glia = upon=20 removal of growth factor and plating onto an adhesive substrate. Scale = bars:=20 (A=E2=80=93F), 25 =CE=BCm; (G), 50 =CE=BCm. The table shows the = percentage of GFP-positive cells=20 after dissociation and the proportion of these cells that gave rise to = neurospheres in four independent experiments.=20

Discussion

By taking advantage of the ability of the SVZ to regenerate following = elimination of dividing cells, we have identified SVZ astrocytes as the = primary=20 precursors for new neurons generated in the adult rodent brain. Three=20 observations identify type B cells as the primary precursors during = generation:=20 (1) with the exception of microglial cells, only type B cells = incorporated=20 [³H]thymidine shortly after Ara-C treatment; (2) pulse = labeling of=20 proliferating type B cells with [³H]thymidine or retrovirus = shortly=20 after Ara-C treatment resulted in labeled type C and A cells, = consecutively; (3)=20 we followed the generation of migrating neuroblasts from individual = retrovirally=20 GFP-labeled type B cells in vitro. Interestingly, dividing type B cells = gave=20 rise to clusters of globular cells that remain tightly associated until=20 neuroblasts appeared. Similar clusters of type C cells are present in = vivo in=20 untreated animals ([16=20 and 22]).=20 These results suggest that type B cells divide to give rise to type C = cells,=20 which in turn divide repeatedly, forming tight clusters that then = generate type=20 A cells ( Figure=20 9).=20

Display=20 Full Size version of this image = (4K)

Figure 9. Model of Neurogenesis in the SVZ of the Adult Mouse = BrainSVZ=20 astrocytes (type B cells, blue) are the primary neuronal precursors in = the=20 SVZ. These cells divide to give rise to clusters of type C cells = (green),=20 which in turn generate migrating neuroblasts (type A cells, red). = Ependymal=20 cells (gray) line the wall of the ventricles and in our experiments = did not=20 divide.=20

Our experiments using GFAP-Tva transgenic mice show that type B cells = are=20 also the primary precursors of new neurons under normal conditions. = Specific=20 infection of dividing SVZ cells expressing GFAP shows that SVZ = astrocytes give=20 rise to new granule and periglomerular neurons in the olfactory bulb. At = long=20 survivals after infection, clusters of branched and globular cells were = still=20 present in the SVZ, suggesting that cells initially infected had = undergone=20 self-renewal. These results provide direct evidence that GFAP-positive = type B=20 cells are neurogenic.

A recent report suggests that ependymal cells divide and are the in = vivo=20 neural stem cells ([30]).=20 Our results do not support this conclusion. Following continuous BrdU or = [³H]thymidine treatment for 14 and 12 days, respectively, we = detected=20 no labeled ependymal cells. Some labeled cells were very closely = associated with=20 the ependymal layer. However, analysis of = [³H]thymidine-labeled cells=20 at the EM did not reveal any labeled ependymal cells. Likewise, during=20 regeneration, when many stem cells are likely recruited, we did not = detect=20 mitoses or [³H]thymidine-labeled ependymal cells. This = suggests that=20 ependymal cells do not divide under normal conditions or during = regeneration of=20 the SVZ. We cannot exclude the possibility that ependymal cells may = divide=20 extremely rarely or under certain conditions. It will be interesting to=20 determine whether the conditioned media used in the study of [30]=20 may induce ependymal cells to divide in vitro and form neurospheres. Our = intraventricular labeling experiments with fluorescent latex beads or = adenovirus=20 suggest that ependymal cells are not the precursors for the majority of=20 neurospheres. We provide direct evidence that GFAP-expressing SVZ = astrocytes=20 specifically labeled with an adenovirus carrying GFP give rise to = EGF-responsive=20 stem cells in vitro. As 48 hr is necessary for sufficient GFP to = accumulate in=20 these cells before culturing, it is possible that some of the = fluorescent cells=20 that gave rise to neurospheres had already transformed into type C = cells. Thus,=20 while our data suggest that the primary precursors of neurospheres are=20 astrocytes, we do not know which are the immediate precursors. It is = possible=20 that multiple populations of cells in the SVZ have the capacity to give = rise to=20 neurospheres.

We have observed that during regeneration and in normal mice, type B = cells=20 occasionally contact the ventricle. However, type B cells contacting the = ventricle are morphologically very different from ependymal cells. Most=20 importantly, these cells do not have multiple long cilia characteristic = of=20 ependymal cells but occasionally display a single short cilium (our = unpublished=20 observation) similar to that described in neuronal precursors in the = embryonic=20 neuroepithelium ([60])=20 and in adult birds ( [4]).=20 In order for type B cells to become neurogenic, they may need to contact = the=20 ventricle as neuroepithelial cells normally do during development.

Type B cells express glial markers and have the ultrastructural=20 characteristics of astrocytes, that is, bundles of intermediate = filaments, dense=20 bodies in the cytoplasm, gap junctions, and multiple processes ([48]).=20 Based on these characteristics, we and others ( [59];=20 [47])=20 have identified these cells as SVZ astrocytes. We do not know whether = only a=20 subpopulation of astrocyte-like cells in the SVZ has the capacity to act = as in=20 vivo neuronal precursors or whether many can but are inhibited from = following a=20 pathway toward neuronal production by local environmental signals.

Many astrocytes express EGF and bFGF receptors ([43,=20 71=20 and 23]).=20 Interestingly, using these growth factors, neural stem cells can be = isolated in=20 vitro not only from the adult SVZ ( [42])=20 but also from other brain regions ( [45=20 and 31]),=20 including the spinal cord ( [66]),=20 diencephalon ( [66]),=20 and hippocampus ( [46]).=20 Our results raise the intriguing possibility that neural stem cells that = have=20 been cultured from other brain regions may actually be derived from=20 astrocyte-like cells in vivo. Astrocytes encompass a heterogeneous = population of=20 cells ( [70])=20 that are widely distributed in the adult brain and continue to divide in = situ (=20 [41,=20 33=20 and 17]).=20 After injury, astrocytes proliferate to form glial scars ( [10=20 and 34])=20 but not neurons. It is possible that a neurogenic potential is latent in = many=20 astrocytes throughout the CNS but that inhibitory signals may suppress = these=20 cells from producing neurons. Neurogenic factors may only be present = close to=20 the brain ventricles or within the adult SVZ. Alternatively, SVZ = astrocytes that=20 act as stem cells in vitro and generate neurons in vivo may correspond = to a=20 fundamentally different cell type that resembles astrocytes and = expresses GFAP=20 and other glial markers. If this is the case, then our work suggests = that use of=20 markers such as GFAP, a hallmark of glial cells ( [6]),=20 may not be a reliable indication of fully differentiated glia. Further = work is=20 required to characterize those SVZ astrocytes that can act as primary = neuronal=20 precursors and to determine how they differ from other astrocytes within = the SVZ=20 and the rest of the brain.

During neural development, astrocytes are derived from radial glia = ([57=20 and 64]).=20 Adult cortical astrocytes assume the characteristics of radial glia upon = exposure to embryonic brain extracts ( [28]).=20 Interestingly, radial glia divide and have been hypothesized to function = as=20 neuronal precursors ( [20,=20 3=20 and 24]).=20 The identification of SVZ astrocytes as neuronal precursors in the adult = brain=20 further suggests that what has classically been considered an astrocytic = lineage, including radial glia, may in fact correspond to embryonic and = adult=20 neuroepithelial cells that retain some of the properties of neural stem = cells.

The present results demonstrate that SVZ astrocytes are the in vivo = primary=20 precursors for new neurons during regeneration and under normal = conditions.=20 Furthermore, neurospheres in vitro can be derived from SVZ astrocytes = labeled in=20 vivo, indicating that these cells can act as neural stem cells. = Exploitation of=20 the regenerative capacity and neurogenic potential of SVZ astrocytes may = have=20 powerful implications for brain repair.

Experimental Procedures

Ara-C Infusions

All animal care was in accordance with institutional guidelines.=20 Cytosine-=CE=B2-D-arabinofuranoside (2%; Ara-C, Sigma) in 0.9% saline or = vehicle=20 alone was infused onto the surface of the brain of adult CD-1 male mice = (2=E2=80=933=20 months) with a mini-osmotic pump (Alzet Model 1007D flow rate 0.5 = =CE=BCl/hr, 7=20 days). Cannulas were implanted stereotaxically onto the surface of the = brain at=20 the following coordinates: anterior (A), 0; lateral (L), 1.1; depth (D), = 0.1=20 (relative to Bregma and the surface of the brain). After 6 days of = infusion, the=20 pump was removed and mice were killed at the indicated survivals.

Immunohistochemistry

For preembedding immunostaining for EM, brains were perfused with 3%=20 paraformaldehyde and 0.5% glutaraldehyde, postfixed overnight, and = immunostained=20 for GFAP (1:500 DAKO), vimentin (1:1 40E-C [[2]])=20 as described before ( [16])=20 or GFP (1:500 Clontech) as described ( [8]).=20 For postembedding immunostaining, brains were perfused with 3% = paraformaldehyde=20 and 1% glutaraldehyde, embedded in araldite (Durcupan), and = immunostained for=20 GFAP (1:300 Dako [polyclonal] or 1:200 [monoclonal, Boehringer = Mannheim]) and=20 S100=CE=B2 (Dako 1:200) in 1.5 =CE=BCm semithin or 50 nm ultrathin = sections ( [7]).=20 Frontal sections containing the entire dorsoventral lateral wall of the = lateral=20 ventricle were analyzed for GFAP immunoreactivity.

For light microscopy, brains were fixed by perfusion with 3%=20 paraformaldehyde, postfixed overnight, and 50 =CE=BCm thick sections cut = with a=20 vibratome. Differentiated neurospheres were fixed by immersion in 3%=20 paraformaldehyde for 15 min at room temperature. After three rinses in=20 phosphate-buffered saline (PBS; pH 7.4), neurospheres or sections were = incubated=20 for 1 hr in PBS containing 10% normal goat serum and 0.1% Triton X-100. = The=20 following primary antibodies were used: anti-Tuj1, mouse monoclonal IgG, = dilution 1:1000 (Babco); anti-PSA-NCAM, mouse monoclonal IgM ([56]),=20 dilution 1:1000; anti-CD24, rat IgG, dilution 1:1000 (both gifts from = Dr. G.=20 Rougon, Universit=C3=A9 de Marseilles); and anti-GFAP, rabbit polyclonal = IgG (DAKO),=20 dilution 1:1000. Incubations in primary antibodies were carried out at = 4=C2=B0C=20 overnight for neurospheres or for 48 hr for sections. Neurospheres or = sections=20 were washed in PBS three times and incubated with fluorescent secondary=20 antibodies. For detection of Tuj1, Cy3-conjugated anti-mouse IgG (Sigma) = diluted=20 1:1000 was used. For the detection of PSA-N-CAM, TRITC-conjugated = anti-mouse IgM=20 (Jackson Laboratories) diluted 1:200 was used. A biotinylated anti-rat = IgG=20 diluted 1:200 (Vector Laboratories) followed by Cy2 streptavidin diluted = 1:1000=20 (Jackson Laboratories) was used for detection of CD24. A = fluorescein-conjugated=20 anti-rabbit IgG diluted 1:200 (Vector Laboratories) was used to detect = GFAP. All=20 secondary antibodies were incubated for 1 hr at room temperature. = Sections or=20 neurospheres were rinsed three times in PBS and coverslipped. = Double-labeled=20 sections were observed with a Zeiss LSM510 confocal microscope.

BrdU Administration and Detection

BrdU (1 mg/ml, Sigma) was given to mice in their drinking water for 2 = weeks.=20 Mice were killed immediately after treatment or 1 week later and their = brains=20 dehydrated and embedded in polyethylene glycol ([2]).=20 Three micron sections were cut on a rotating microtome and mounted on = silanated=20 slides (Sigma). Double staining for S100=CE=B2 and BrdU was performed by = digesting=20 with pepsin (0.25% in 0.1 N HCl) for 2 min at 37=C2=B0C followed by = blocking in 10%=20 goat serum. Sections were incubated overnight at 4=C2=B0C in a 1:1000 = dilution of=20 rabbit anti-S100=CE=B2 (Dako) and revealed with biotinylated secondaries = (1:200,=20 Vector) followed by streptavidin Cy3 (1:2000, Jackson Immuno). Sections = were=20 then processed for BrdU immunostaining by incubating 20 min at 37=C2=B0C = in 2 N HCl=20 followed by blocking in 10% horse serum. Sections were incubated = overnight in=20 1:200 mouse anti-BrdU (Dako) in blocking solution and revealed with = anti-mouse=20 Cy2 (1:500, Jackson Immuno). Thirty micrometer floating vibratome = sections were=20 stained sequentially for mCD24 (1:1000) and BrdU as for S100=CE=B2, = except that no=20 pepsin was used.

[³H]Thymidine Autoradiography and EM = Analysis

For pulse-labeling experiments, mice were injected with 50 =CE=BCl of = 6.7 Ci/mmol=20 [³H]thymidine 0.5 days after pump removal and were killed = either 1 hr=20 later or 2 or 6 days after pump removal and brains processed for = autoradiography=20 and EM analysis as previously described ([16]).=20 Briefly, cells overlaid by nine or more silver grains in three = consecutive=20 semithin sections were considered labeled. These sections were detached = from the=20 slide and reembedded in Araldite for ultrathin sectioning and analysis = of the=20 [³H]thymidine-labeled cells at the EM. For long survival = experiments,=20 mice were injected four times every 4 hr with [³H]thymidine = and then=20 allowed to survive 15 or 30 days. For continuous infusion of=20 [³H]thymidine into the lateral ventricle, mini-osmotic pumps = (Alzet=20 2002, 0.5 =CE=BCl/hr) filled with 200 =CE=BCl of = [³H]thymidine (6.7 Ci/mmol)=20 were implanted with the aid of a stereotaxic apparatus at A: 0, L: 1.1, = D: 2 mm=20 for 12 days.

Retroviral Injections for In Vivo Studies

Replication-incompetent retroviruses encoding either the marker gene = human=20 placental alkaline phosphatase (DAP) or =CE=B2-gal (BAG) were harvested = from the psi2=20 DAP cell line (ATCC 1949-CRL) or from the psi2 BAG cell line (ATCC = 9560-CRL),=20 concentrated, titered, and tested for helper virus ([11]).=20 The titer was 10⁸ colony-forming units/ml. Twelve hours after = Ara-C=20 pump removal, 2 =CE=BCl of retrovirus and 8 =CE=BCg/ml of polybrene were = injected=20 stereotaxically into each lateral ventricle (above coordinates). Control = injections of retrovirus into one lateral ventricle resulted in no = retrovirally=20 labeled cells in the contralateral SVZ. Mice were killed 1.5, 2.5, 4, or = 6 days=20 after pump removal and whole mounts of the lateral wall of the lateral = ventricle=20 dissected ([15]),=20 fixed for 3=E2=80=934 hr in 3% paraformaldehyde, and enzyme = histochemistry for alkaline=20 phosphatase performed as described ( [19]).=20 Whole mounts were analyzed for the presence and morphology of labeled = cells.=20 =CE=B2-gal-infected cells were analyzed at the EM as described ( [69]).

For production of RCAS-AP, chicken embryo fibroblasts (CEFs) were = prepared=20 from the trunk of E10 embryos. After two passages, CEFs were calcium = phosphate=20 transfected with 5 =CE=BCg of a plasmid encoding RCAS-AP. Three hours = after=20 transfection, cells were glycerol shocked for 90 s ([11]).=20 The cells were carried until the entire dish was infected, as assayed by = histochemical staining for alkaline phosphatase. RCAS-AP was harvested = and=20 concentrated as described ( [18]).=20 RCAS-AP retroviruses (0.2 =CE=BCl or 0.5 =CE=BCl) were injected into the = SVZ at three=20 coordinates (A, L, and D: 0, 1.4, 1.6; 0.5, 1.1, 1.7; 1, 1, 2.3) of = GFAP-Tva=20 mice. Whole mounts (n =3D 5 for 1 day after infection, N =3D 2 for 3.5 = days after=20 infection, and N =3D 5 for 14 days after infection) were dissected and = stained for=20 AP as described above. Fifty micrometer vibratome sections were cut = through the=20 olfactory bulb and stained for AP as above.

Pseudotyped retrovirus encoding green fluorescent protein as a marker = (LZRS-CA-gapEGFP; gift of R. Lansford and S. Fraser) was injected (0.5 = =CE=BCl into=20 the lateral ventricle). One day after infection, whole mounts were = dissected.=20 Whole mounts processed for double staining were fixed for 2 hr in 3%=20 paraformaldehyde, sectioned on a vibratome at 50 =CE=BCm, blocked in 10% = horse serum,=20 incubated with 1:200 dilution of GFAP monoclonal antibody (Boehringer = Mannheim)=20 for 24=E2=80=9348 hr, and revealed using 1:1000 Cy3-anti-mouse secondary = antibodies=20 (Jackson Immuno). Sections were analyzed with an LSM510 Zeiss confocal=20 microscope.

Whole-Mount Cultures

For whole-mount cultures, regions of the SVZ with GFP-positive cells = were=20 identified and small fragments ( 3D"not, 1 mm)=20 dissected. Thirty-five millimeter dishes (Falcon) were prepared as in = [68].=20 Whole-mount fragments were placed with the ventricular surface facing = down=20 embedded in collagen gels ( [68])=20 and covered with 1 ml of Neurobasal medium. Dishes were incubated at = 37=C2=B0C in a=20 tissue culture incubator with constant slow rocking on a Varimix mixer = that had=20 been modified to rock at 1 rpm. Cultures were photographed daily on an = inverted=20 Olympus IX70 microscope. The experiment was repeated in eight = Ara-C-treated mice=20 (one to three cultures/mouse). When GFP-positive cells with the = morphology of=20 neurons were observed, cultures were fixed for 30 min in 3% = paraformaldehyde=20 washed extensively and stained for TuJ1 (1:1000 Babco) and revealed = using 1:1000=20 Cy3 anti-mouse secondary antibody (Jackson Immuno). Six cultures = containing=20 GFP-labeled cells gave rise to neurons. Immunostained cultures were = studied with=20 an LSM510 Zeiss confocal microscope.

Neurosphere Preparation and Differentiation

Adult CD1 mice were killed by cervical dislocation (n =3D 5 per = preparation)=20 and their brains removed and placed into Pipes buffer (20 mM Pipes, 25 = mM=20 glucose, 0.12 M NaCl, 0.5 mM KCl [pH 7.4]). The lateral walls of the = lateral=20 ventricle were dissected, collected in Pipes buffer, and incubated in a = mixture=20 containing 1 ml of activated papain and 4 ml of Pipes buffer. Papain was = activated half an hour in advance by placing 3 mg of papain (Worthington = Biochemical) in 1 ml of 1.1 mM EDTA, 5.5 mM cysteine HCl. The pieces of = tissue=20 were incubated in papain solution at 37=C2=B0C on a rocking platform for = 1 hr,=20 collected by centrifugation at 200 g for 2 min, and resuspended in 1 ml = of=20 DMEM-F12 (GIBCO) containing 0.7 mg of ovomucoid inhibitor and 1 mg of = DNase. The=20 cells were dissociated using a fire-polished pasteur pipette, and cells = were=20 collected by centrifugation at 300 g for 7 min. The cellular pellets = were=20 resuspended in 1 ml of DMEM-F12 (GIBCO) supplemented with N2 (GIBCO), 2 = mM=20 glutamine, 0.6% (w/v) glucose, 0.02 mg/ml insulin, and 15 mM HEPES. The = cells=20 were counted and plated in uncoated 35 mm dishes (50,000 cells per dish) = in the=20 same medium containing 20 ng/ml of EGF. Neurospheres were passaged by = harvesting=20 them by centrifugation (200 g for 5 min) and triturating them in 100 = =CE=BCl of=20 medium with an automatic pipetter (P200 Gilson). For differentiation,=20 neurospheres that had been grown for 8 to 12 days in vitro were plated = onto=20 laminin-coated (10 =CE=BCg/ml) Lab-Tek 16-well chamber slides (Nunc) in = the medium=20 described above without EGF for 5=E2=80=938 days.

Adenoviral Vectors

Three different replication-defective adenoviruses were used: one = expressing=20 LacZ as a reporter gene (Ad5-CMV-LacZ, 1.9 =C3=97 10¹¹ = pfu/ml) ([72]),=20 one expressing GFP as a reporter gene (Ad5-CMV-GFP, 1.3 =C3=97 = 10¹² viral=20 particles/ml), and a third one that we produced in which GFP was driven = by the=20 GFAP promoter.

Production of pAd5-GFAPp-GFP Adenoviral Vector

The mouse 2.5 kb GFAP promoter region was removed from GFAP 1L/PIP200 = ([5])=20 (a kind gift of Dr. H. Baba) with a HindIII digest, filled in, and = ligated into=20 subcloning plasmid pSL at the StuI site. The GFAP promoter was then = released=20 from pSL with NotI and XbaI and ligated into adenoviral transfer plasmid = pAd5(HS)V ( [72])=20 that had been digested with NotI and XbaI to remove the CMV promoter. = The=20 humanized GFP cDNA ( [73])=20 was isolated from pGFP-neo with NotI, filled in, and ligated into a = filled-in=20 SalI site 3=E2=80=B2 of the GFAP promoter start site in the adenoviral = transfer plasmid,=20 resulting in the clone pAd5-GFAPp-GFP. The adenoviral vector was = generated by=20 cotransfection of the pAd5-GFAPp-GFP and the pJM17 adenovirus genome = plasmids=20 into 293 human embryonic kidney cells. pJM17 contains the Ad5 genome = with an=20 insertion in the E1 region that prevents viral packaging. Recombination = between=20 pJM17 with pAd5-GFAPp-GFP produces an adenoviral genome that can be = efficiently=20 packaged. 293 cells provide the E1 gene products for complementation. = The=20 adenoviral vector Ad5-GFAPp-GFP was recovered after transfection, plaque = purified twice, and verified by both PCR and restriction enzyme analysis = of=20 HIRT-extracted viral DNA. A viral stock was purified by cesium chloride = banding=20 twice. The titer was 1 =C3=97 10¹² viral particles/ml.

Adenoviral Injections into the SVZ

The GFAPp-GFP adenovirus was injected stereotaxically into the SVZ. = Two=20 hundred nanoliters of a viral suspension was injected bilaterally into = the SVZ=20 at the following coordinates A, L, D: 1, 1, 2.2; 0.5, 1.1, 1.7; 0.5, 1, = 2.1; 0,=20 1.4, 1.6; 0, 1.3, 1.8. The mice were sacrificed for neurosphere = preparation 48=20 hr after infection. The efficiency of infection was verified by = whole-mount=20 dissections of the lateral wall of the lateral ventricle ([15]).=20 Three control mice, having received GFAPp-GFP adenovirus infections, = were=20 perfused and their brains processed for immunohistochemistry as = described=20 above.

Labeling of the Ependymal Layer with Vital Dyes

Labeling of the ependymal layer was performed by intraventricular = stereotaxic=20 injections (A: =E2=88=920.5; L: 1.1; D: 2) of vital dyes. For each type = of injection,=20 two mice were perfused and their brains sectioned to assess the = specificity of=20 the ependymal labeling. The ipsilateral and contralateral hemispheres = were=20 processed independently for neurosphere preparation.

Fluorescent Tracers

For DiI labeling, mice were injected with 2 =CE=BCl of a 1% solution = of DiI=20 (1,1=E2=80=B2-dioctadecyl-3,3,3=E2=80=B2,3=E2=80=B2-tetramethylindocarboc= yanine perchlorate; Molecular=20 Probes) in 300 mM saccharose and sacrificed 4 hr after injection. For = rhodamine=20 bead labeling, mice were injected with 2 =CE=BCl of a 1:100 suspension = of rhodamine=20 beads (rhodamine-labeled latex microspheres; Lumafluor, NY) in PBS and=20 sacrificed 16 hr later. Neurospheres were prepared from these labeled = walls and=20 cells plated and scored as described below.

Adenoviral Tracers

Mice were injected with 2 =CE=BCl of an adenovirus expressing LacZ or = 10 =CE=BCl of an=20 adenovirus expressing GFP and sacrificed 48 hr after injection. In the = case of=20 the =CE=B2-gal adenovirus, neurospheres were grown for 4 days and = allowed to attach=20 onto poly-L-ornithine for 5 hr before fixing with 3% paraformaldehyde = for 10=20 min, rinsed in PBS, and incubated at 37=C2=B0C overnight in X-gal = solution (2 mM=20 MgCl₂, 4 mM potassium ferrocyanide, 4 mM potassium = ferricyanide, 1=20 mg/ml 5-bromo-4-chloro-3-indolyl =CE=B2-d-galactoside in PBS [pH = 7.3]).

Scoring of Vitally Labeled Cells and Neurospheres

After fluorescent labeling of the ependymal cells with DiI, rhodamine = beads,=20 or GFP adenovirus and of SVZ cells with GFAP-GFP adenovirus, cells were=20 dissociated, counted, and plated in clonal isolation dishes (10 cm = diameter=20 hybridoma tissue culture dishes, Marsh) at a density of 100,000 cells = per dish.=20 Fluorescent cells were then identified under an inverted Olympus IX70 = microscope=20 and their position scored with an objective marker (Nikon). The survival = and=20 growth of fluorescently labeled cells were monitored daily. =

Acknowledgements

We thank F. Nottebohm, C. Scharff, and H. Wichterle for critical = reading of=20 the manuscript and discussion; B. Haripal and A. Mateo for technical = assistance;=20 M. Blasco-Iba=C3=B1ez and M. Portoles for advice on postembedding = immunostaining; and=20 J. Hyer for advice on CEF preparation. J. Trevejo and E. Falk-Pedersen = provided=20 critical assistance for the production of the adenoviral vectors. We are = very=20 grateful to H. Baba for providing the plasmid containing the GFAP = promoter; E.=20 Holland and H. Varmus for the GFAP-Tva mice and RCAS-AP plasmid; R. = Lansford and=20 S. Fraser for the GFP retrovirus; and G. Rougon for the PSA-NCAM and = mCD-24=20 antibodies. F. D. is a Baker Fellow. I. C. was supported by a Human = Frontier=20 fellowship (LT0727/1997-B). D. A. L. was supported by NIH grant GM07739. = This=20 work was supported by NIH grants HD32116 and NS28478.

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72.=20 S.O. Yoon, C. Lois, M. Alvirez, A. Alvarez-Buylla, E. Falck-Pederson and = M.V.=20 Chao, Adenovirus-mediated gene delivery into neuronal precursors of the = adult=20 mouse brain. Proc. Natl. Acad. Sci. USA 93 = (1996), pp.=20 11974=E2=80=9311979. View Record in Scopus | Cited By in Scopus (30)

73.=20 S. Zolotukhin, M. Potter, W.W. Hauswirth, J. Guy and N. Muzyczka, A = =E2=80=9Chumanized=E2=80=9D=20 green fluorescent protein cDNA adapted for high-level expression in = mammalian=20 cells. J. Virol. 70 (1996), pp. = 4646=E2=80=934654. View Record in Scopus | Cited By in Scopus (393)

Corresponding author. Correspondence: Arturo = Alvarez-Buylla,=20 212 327 7729 (phone), 212 327 8312 (fax)

^=E2=80=A1=20 To whom correspondence should be addressed (e-mail:=20 alvarez@rockvax.rockefeller.edu).

Volume=20 97, Issue 6, 11 June 1999, Pages 703-716

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