From: Subject: Epidermal and Fibroblast Growth Factors Behave as Mitogenic Regulators for a Single Multipotent Stem Cell-Like Population from the Subventricular Region of the Adult Mouse Forebrain -- Gritti et al. 19 (9): 3287 -- Journal of Neuroscience Date: Sun, 20 Jan 2008 14:53:14 +0100 MIME-Version: 1.0 Content-Type: multipart/related; type="text/html"; boundary="----=_NextPart_000_0083_01C85B74.2F4823D0" X-MimeOLE: Produced By Microsoft MimeOLE V6.00.2900.3198 This is a multi-part message in MIME format. ------=_NextPart_000_0083_01C85B74.2F4823D0 Content-Type: text/html; charset="Windows-1252" Content-Transfer-Encoding: quoted-printable Content-Location: http://www.jneurosci.org/cgi/content/full/19/9/3287?ijkey=65195e9c4c00ad1edd5c602c6fc7154180505e82 Epidermal and Fibroblast Growth Factors Behave as = Mitogenic Regulators for a Single Multipotent Stem Cell-Like Population = from the Subventricular Region of the Adult Mouse Forebrain -- Gritti et = al. 19 (9): 3287 -- Journal of Neuroscience
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The Journal of Neuroscience, May 1, 1999,=20 19(9):3287-3297

Epidermal and Fibroblast Growth Factors Behave as Mitogenic = Regulators for a=20 Single Multipotent Stem Cell-Like Population from the Subventricular = Region of=20 the Adult Mouse Forebrain

Angela = Gritti1,=20 Paola Fr=F6lichsthal-Schoeller1, Rossella = Galli1,=20 Eugenio A. Parati1, Lidia Cova1, Stefano = F.=20 Pagano1, Christopher R. Bjornson2, and = Angelo L.=20 Vescovi1

1 Laboratory of Neuropharmacology, National = Neurological=20 Institute C. Besta, Milan, Italy I-20133, and = 2 Department=20 of Biochemistry, University of Washington, Seattle, Washington = 98195-7350=20


    ABSTRACT
TOP
ABSTRACT
INTRODUCTION
MATERIALS AND METHODS
RESULTS
DISCUSSION
REFERENCES =

The subventricular zone (SVZ) of the adult mammalian forebrain = contains=20 kinetically distinct precursor populations that contribute = new=20 neurons to the olfactory bulb. Because among forebrain precursors=20 there are stem-like cells that can be cultured in the = presence=20 of mitogens such as epidermal growth factor (EGF) and = fibroblast=20 growth factor 2 (FGF2), we asked whether distinct subsets of=20 stem-like cells coexist within the SVZ or whether the = proliferation=20 of a single type of SVZ stem-like cell is controlled by = several=20 GFs. We show that the latter is the case. Thus cells isolated = from the SVZ coexpress the EGF and FGF receptors; by = quantitative=20 analysis, the number of stem-like cells isolated from the SVZ = by=20 either FGF2 or EGF is the same, whereas no additive effect = occurs=20 when these factors are used together. Furthermore, short-term = administration of high-dose [3H]thymidine in = vivo=20 depletes both the EGF- and FGF2-responsive stem-like cell = populations=20 equally, showing they possess closely similar proliferation = kinetics=20 and likely belong to the constitutively proliferating SVZ=20 compartment. By subcloning and population analysis, we = demonstrate=20 that responsiveness to more than one GF endows SVZ cells with = an=20 essential stem cell feature, the ability to vary = self-renewal, that=20 was until now undocumented in CNS stem-like cells. The = multipotent=20 stem cell-like population that expands slowly in the presence = of FGF2=20 in culture switches to a faster growth mode when exposed to = EGF alone=20 and expands even faster when exposed to both GFs together. = Analogous=20 responses are observed when the GFs are used in the reverse = order,=20 and furthermore, these growth rate modifications are = fully=20 reversible.

Key words: EGF; FGF; stem cells; adult brain; neurogenesis; neural = progenitors

    INTRODUCTION
TOP
ABSTRACT
INTRODUCTION
MATERIALS AND METHODS
RESULTS
DISCUSSION
REFERENCES =

The principal source of mature neural cells is the embryonic = periventricular=20 neuroepithelium (His, 1889), = whose=20 undifferentiated precursor cells give rise to neurons and = glia during=20 development (for review, see McKay, 1997). = Because the=20 germinal epithelium atrophies soon after birth and there was = no=20 evidence of postnatal neuronal generation, the idea that = neurogenesis=20 is completed early in postnatal life was widely accepted = until the=20 early 1960s (for review, see Altman and Bayer, 1993). = This changed=20 after the observation that new neurons could form postnatally = in=20 mouse cerebellar cortex (Sidman and Miale, 1959; = Uzman, 1960; = Miale and=20 Sidman, 1961). =

It is now clear that specific regions of primary embryonic germinal=20 epithelium give rise to secondary and tertiary germinal = matrices=20 (Altman, 1982; = Altman and=20 Bayer, 1990a,b; = Bayer and=20 Altman, 1991) = within which=20 neurogenesis continues after birth. De novo = neurogenesis has=20 been reported in the subgranular region of the dentate gyrus, = the=20 olfactory bulb (Altman, 1962, = 1969; = Kaplan=20 and Hinds, 1977; = Gueneau et=20 al., 1982; = Altman and=20 Bayer, 1990a,b;=20 Corotto et al., 1993; = Lois and=20 Alvarez-Buylla, 1994), = and the=20 cortex (Kaplan, 1981; = Huang and Lim,=20 1990) of = various=20 adult rodent and higher mammalian species (Altman, 1966a; = Das and=20 Altman, 1971;=20 Kaplan and Hinds, 1977; = Kaplan, 1982; = Rakic and=20 Kormack, 1993). =

The periventricular region and particularly the component underlying = the=20 ependymal layer of the lateral ventricles [subventricular = zone (SVZ)]=20 persist in neonate (Luskin, 1993) = and adult=20 mammals as a mitotically active layer (Allen, 1912; = Kershnam,=20 1938; = Smart,=20 1961) = long thought=20 to give rise to glia in the postnatal brain (Smart, 1961; = Smart and=20 Leblond, 1961; = Altman,=20 1966b; = Lewis, 1968;=20 Patterson et al., 1973; = Levison and=20 Goldman, 1993). = It is=20 now emerging that the adult SVZ is a late germinal matrix = whose=20 molecular and cellular microenvironment is able to sustain=20 neurogenesis via the proliferation of undifferentiated = multipotent=20 neural progenitors. In fact, the adult SVZ contains multiple=20 precursor cell types (Doetsch et al., 1997) = and at least=20 two cell populations, as distinguished by their differing = kinetic=20 profiles [relatively quiescent and constitutively = proliferating=20 (Morshead and van der Kooy, 1994)].=20 In vivo, their progeny can undergo cell death (Morshead and = van der Kooy, 1992) or = give rise=20 to neuronal progenitors that migrate to the olfactory bulb = (Wichterle=20 et al., 1997) to = replace=20 granule cells and periglomerular neurons (Lois and = Alvarez-Buylla,=20 1994). =

The proliferation requirements and lineage relationships of the = various cell=20 types in the SVZ of the adult mammalian forebrain remain=20 undetermined. Previous studies showed that cells from SVZ = explants=20 proliferate and generate neurons and glia (Lois and Alvarez-Buylla, = 1993), = whereas=20 stem-like cells have been isolated from the striatum of adult = rodents=20 by culturing in the presence of epidermal growth factor (EGF) = (Reynolds and Weiss, 1992) or = fibroblast=20 growth factor 2 (FGF2) (Richards et al., 1992; = Gritti et al.,=20 1996; = Johe et=20 al., 1996). = Hence, the=20 question arises: is more than one stem-like cell type present = in the=20 adult SVZ or is there a single precursor type that responds = to both=20 EGF and FGF2, displaying stem-like features (Stemple and = Mahanthappa,=20 1997)? =

We found previously that EGF-responsive stem-like cells generate = progeny that=20 proliferates and gives rise to neurons and glia when exposed = to FGF2=20 in vitro (Gritti et al., 1995),=20 suggesting that FGF2-responsive cells could be the progeny of = EGF-generated precursors. Here, we sought to determine the = lineage=20 relationships between EGF- and FGF2-responsive SVZ stem-like = cells=20 and to elucidate the roles of these GFs in regulating the = activity of=20 these multipotent cells of the adult mammalian = forebrain.=20


    MATERIALS AND = METHODS
TOP
ABSTRACT
INTRODUCTION
MATERIALS AND METHODS
RESULTS
DISCUSSION
REFERENCES =

Primary cultures. Four- to eight-month-old CD-1 albino mice = were=20 anesthetized by intraperitoneal injection of pentobarbital=20 (120 mg/kg) and killed by cervical dislocation. The brains = were=20 removed and placed in artificial CSF (aCSF) (124 mM NaCl, 5 mM = KCl,=20 1.3 mM MgCl2, 0.1 mM CaCl2, 26 mM=20 NaHCO3, and 10 mM D-glucose, pH 7.3) aerated with 95% = O2/5%=20 CO2 at room temperature. Striatal tissue, = excluding=20 subependyma, or subependyma alone was isolated after coronal=20 sectioning and cut into 1 mm3 pieces. Pieces were = transferred=20 into 30 ml of aCSF containing 1.3 mg/ml trypsin = (Type XII,=20 9000 BASF units/mg; Sigma, St. Louis, MO), = 0.67 mg/ml=20 hyaluronidase (2000 units/mg; Sigma), and 0.2 mg/ml = kynurenic acid (Sigma) and incubated, under continuous oxygenation=20 and stirring, for 90 min at 32-34=B0C. Tissue sections were = then=20 rinsed in aCSF for 10 min, transferred to DMEM/F12 (1:1 v/v;=20 Life Technologies, Gaithersburg, MD) medium containing = 0.7 mg/ml=20 ovomucoid (Sigma), and carefully triturated with a = fire-polished=20 Pasteur pipette. The cells were collected by centrifugation = and=20 resuspended in GF-free, chemically defined DMEM/F12 medium = containing=20 2 mM L-glutamine, 0.6%=20 glucose, 9.6 gm/ml putrescine, 6.3 ng/ml progesterone,=20 5.2 ng/ml sodium selenite, 0.025 mg/ml insulin, = 0.1 mg/ml=20 transferrin, and 2 =B5g/ml heparin (sodium salt, grade = II; Sigma)=20 (control medium).

For RNA extraction and molecular analysis of GF receptors, = subependymal=20 tissue was immediately frozen in liquid nitrogen and = processed as=20 described below.

Cell culturing, propagation, cloning, and population analysis. = Cells=20 prepared as described above were plated into 35 mm Petri = dishes=20 (Corning, Corning, NY) containing control medium with either = FGF2=20 (human recombinant, 20 ng/ml; Peprotech, Rocky Hill, NJ, = or=20 Upstate Biotechnology, Lake Placid, NY), EGF (human recombinant,=20 20 ng/ml; Peprotech), or both. Medium was changed every = 3-4=20 d.

For population analyses, primary cells were plated at=20 3500 cells/cm2, and the spheres formed after 8-10 d were = harvested, collected by centrifugation (10 min at=20 800 =D7 g), mechanically dissociated to a = single-cell=20 suspension, and replated in medium containing the appropriate = GF(s).=20 This procedure was repeated every 8-10 d in vitro = (DIV) for up=20 to 6 months. The total number of viable cells was = assessed at=20 each passage by trypan blue exclusion and confirmed by the=20 calcein/propidium iodide technique.

To assess stem-like cell number in primary cultures, we established = culture=20 conditions that allowed quantitative determination of the = number of=20 stem-like cells (plated on a dish) that were responsive to = EGF, FGF2,=20 or both. The methodology was developed from our work on=20 FGF2-responsive adult neural stem cells (Gritti et al., = 1996), = itself=20 borrowed from the classical assay for assessing the type and = number=20 of clonogenic cells isolated from various hemopoietic tissues = (Bodine=20 et al., 1991, = 1992). = Striata=20 were dissected into parenchymal tissue that excluded the=20 subventricular region and subventricular tissue. The tissues = were=20 dissociated to a suspension of single cells that were = embedded in a=20 methylcellulose gel matrix (1.5% final concentration; Dow = Methocell=20 A4 M, premium grade) to prevent aggregation, plated at a = final=20 density of <10 viable cells/cm2, as described=20 previously (Gritti et al., 1996), = and=20 cultured in the presence of the appropriate GF until = spherical clones=20 were formed (8-10 DIV). Counting the number of spheres formed = in=20 the presence of FGF2, EGF, or both yielded the number of stem = cells plated, which could proliferate under the conditions = tested.=20 To assess the number of single cells, doublets, and triplets = in=20 these cultures, we seeded samples onto glass coverslips and=20 counted the cell nuclei, counterstained with=20 4',6-diamidino2-phenylindole dihydrochloride (DAPI; = 1 mg/ml in=20 methanol; 15 min at 37=B0C).

For the tritiated thymidine ([3H]Thy) cytotoxicity = experiments,=20 4- to 8-month-old CD-1 mice received three intraperitoneal=20 injections, one every 4 hr, of 0.9 ml of saline = containing=20 1 mCi/ml [3H]Thy (64 Ci/mmol; ICN = Biochemicals,=20 Costa Mesa, CA). The animals were killed 12 hr after the = last=20 injection. Control animals received saline only. The animals = were=20 coded, and the number of stem-like cells isolated from SVZ = explants=20 devoid of striatal parenchyma was determined blind, as = described in=20 the previous paragraph and in the Results.

At every other subculturing step and after a growth factor switch, an = aliquot=20 of the cells was withdrawn from culture, and clonal spheres = were=20 generated by embedding dissociated single cells in = methylcellulose=20 and plating at a clonal density (<1 cell/cm2) in the = presence of=20 the appropriate GF. Clonal spheres were used to assay for=20 self-renewal capacity and multipotentiality, in serial = subcloning=20 experiments. For self-renewal, individual spheres were = collected by=20 micromanipulation, dissociated to a single-cell suspension, = embedded=20 in methylcellulose, and replated as described above for = primary=20 cultures in medium containing the appropriate GF(s). The = number of=20 spheres generated under the various conditions was assessed = after=20 8-10 d and normalized by the total number of cells plated = into each=20 well, as determined by direct observation 30 min after = plating.=20

Retention of multipotentiality by stem cells after GF switches was = assessed=20 as described by Gritti et al. (1996). = Briefly,=20 a single-cell suspension was prepared, and individual cells = were=20 selected under high-power magnification, transferred into a = single=20 well by micromanipulation, and grown in isolation = (1 cell/well).=20 A mark was notched on the well to facilitate identification = of=20 the field, and microphotographs were taken at the appropriate = intervals. After a clonal sphere was formed, it was further=20 subcultured and expanded, and the progeny generated was = plated onto=20 multiple glass coverslips, differentiated, and processed for = multiple=20 immunocytochemistry, as described in the next = section.=20

Immunocytochemistry assays. Multiple immunofluorescence assays = were=20 performed as described previously (Gritti et al., 1996).=20 Briefly, freshly dissociated cells from subependymal tissue=20 (1000 cells/cm2) and serially passaged clonal = spheres=20 were plated onto polyornithine-coated glass coverslips. For=20 differentiation experiments, cells were plated in GF-free = culture=20 medium for 5 d, followed by the addition of fetal bovine = serum=20 for a further 2-5 DIV. Primary or differentiated cultures = were fixed=20 (20 min) with 4% paraformaldehyde in PBS, pH = 7.4, and=20 rinsed three times with PBS. The coverslips were then = incubated for=20 90 min at 37=B0C in PBS containing 10% normal goat serum = (NGS),=20 0.3% Triton X-100, and the appropriate primary antibodies or=20 antisera. After thorough washing with PBS and 10% NGS, cells = were=20 reacted for 45 min (room temperature) with secondary = fluorescein=20 isothiocyanate- or rhodamine isothiocyanate-conjugated goat=20 anti-mouse or anti-rabbit IgG antibodies (1:100; Boehringer = Mannheim,=20 Indianapolis, IN) or with donkey anti-mouse IgM antibodies = coupled to=20 7-amino-4-methylcoumarin-3-acetic acid (1:100; Jackson=20 ImmunoResearch, West Grove, PA). The coverslips were rinsed = three=20 times in PBS and once in distilled water and mounted on glass = slides=20 with Fluorsave (Calbiochem, La Jolla, CA).

For quantitative analysis, after immunostaining, coverslips were=20 counterstained with DAPI. The primary antibodies or antisera = used=20 were mouse monoclonal anti-microtubule-associated protein-2 = (MAP2;=20 IgG; 1:100; Boehringer Mannheim), anti-tau-microtubule-associated=20 protein (IgG; 1:100; Boehringer Mannheim), anti-3D"beta-tubulin=20 (IgG; 1:1250; Sigma), anti-galactocerebroside (GalC; IgG; = 1:50;=20 Boehringer Mannheim), and anti-O4 (IgM; 1:200; Boehringer = Mannheim)=20 and rabbit antisera against glial fibrillary acidic protein = (GFAP;=20 ready to use; Incstar), monoclonal anti-EGF receptor (EGFR; = IgG;=20 1:100; Immunotech, Marseille, France), and polyclonal = anti-FGF=20 type-1 receptor (FGFR1; 1:800; gift from=20 D. L. T. Williams). Samples were viewed and=20 photographed with an inverted Zeiss Axiophot=20 fluorescence microscope. No labeling was ever observed in = control=20 experiments when primary antibodies or antisera were omitted = or,=20 alternatively, when normal nonimmune serum was used. = Furthermore,=20 coverslips incubated with single primary antibodies or = antisera and=20 followed by all three secondary steps only exhibited = immunoreactivity=20 with the appropriate filter. Therefore there was no evidence = of=20 cross-reactivity.

Molecular analysis. A reverse transcription (RT)-PCR assay of = mRNA was=20 used to evaluate the expression of FGFR1 and EGFR in primary = and=20 serially passaged cell cultures. Total RNA from EGF- or = FGF2-grown=20 cell lines and from subependymal tissue was extracted using = an=20 adaptation of the method of Chomczynski and Sacchi (1987).=20 This was reverse transcribed for 90 min at 42=B0C, using = 200 U=20 of Superscript RNase H reverse transcriptase (Life = Technologies)=20 in a 20 =B5l volume containing 5=D7 first strand buffer, = 0.1 M DTT, 0.5 =B5g/=B5l = oligo-dT12-18=20 (Pharmacia, Uppsala, Sweden), and 10 mM dNTPs.

For analysis of murine FGFR1, primers corresponding to nucleotides = (nt)=20 1143-1166 at the 5'-end of mRNA (5'-GGAAGAGAGACCAGCTGTGATGAC-3') = and=20 nt 1617-1640 at the 3'-end of mRNA (3'-AACGGAGAAGG = ACCTGTCGGATCT-5')=20 were designed (size of the amplified product, 500 bp). For=20 analysis of murine EGFR, nucleotide primers corresponding to = nt=20 2058-2078 at the 5'-end of mRNA (5'-GGCCTATTCATGCGAAGACG-3') = and to=20 nt 2399-2419 at the 3'-end of mRNA = (3'-CAGGAGGCGGCATACATGAG-5') were=20 designed (size of amplified product, 320 bp). Then = 2.5 =B5l=20 of each RT reaction was amplified in a final volume of = 25 =B5l=20 containing 10=D7 PCR buffer, 25 mM=20 MgCl2, 10 mM dNTPs, each primer = at=20 50 =B5M, and 5 U/=B5l Taq=20 polymerase (Appligene Oncor, Gaithersburg, MD). PCR = amplification=20 included initial denaturation at 94=B0C for 2 min, followed = by=20 cycles consisting of denaturation at 94=B0C for 1 min, = primer=20 annealing at 65=B0C for 1 min, and extension at 72=B0C = for=20 1 min. The PCR products were removed for analysis after=20 30 cycles and then separated on 1.5% agarose gels at=20 10 V/cm for 2 hr; bands were visualized with = ethidium=20 bromide.


    RESULTS
TOP
ABSTRACT
INTRODUCTION
MATERIALS AND METHODS
RESULTS
DISCUSSION
REFERENCES =

Cells from adult SVZ express both EGF and FGF=20 type-1 receptors

We investigated the expression of the FGF type-1 receptor = demonstrated=20 previously in striatal embryonic stem-like cells (Vescovi et = al.,=20 1993) = and the EGF=20 receptor in cells from adult mouse SVZ. RT-PCR on mRNA = isolated from=20 SVZ explants showed the presence of both FGFR1 and EGFR = transcripts=20 (Fig. 1A).=20 In situ immunohistochemical colocalization of GF = receptors in=20 SVZ cells is difficult, because of the scattered or fibrous=20 distribution of antigens as shown by Morshead et al. (1994). We = therefore=20 investigated the expression of FGFR1 and EGFR at the level of = individual, freshly dissociated SVZ cells using double=20 immunofluorescence. All SVZ cells displayed=20 anti-FGFR1-immunoreactivity (-IR) (Fig. 1B),=20 with a subset of these cells also labeled with anti-EGFR; = however, no=20 cells labeled with anti-EGFR antibody alone (Fig. 1C).=20 By immunohistochemistry on forebrain slices, we were able to = confirm=20 previous findings (Morshead et al., 1994) = showing that=20 the anti-EGFR-immunoreactivity is expressed in the ependymal = and/or=20 subependymal region but not in the surrounding brain = parenchyma in=20 vivo (data not shown). Thus, we conclude that virtually = all the=20 potential EGF-responsive forebrain cells that reside in the = SVZ cells=20 also express the FGFR1 receptor and, hence, may be capable of = proliferating in response to both GFs.



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  		Figure 1. =   Cells=20 from mouse SVZ express both EGF and FGF type-1 receptors. = A,=20 EGFR and FGFR1 transcripts detected in SVZ explants. Bands = of the=20 expected size are visible in the ethidium bromide-stained = gel after=20 RT-PCR on RNA extracts. L, Ladder; lane 1, = EGFR,=20 320 bp; lane 2, FGFR1, 500 bp. B, = C,=20 Cells from SVZ explants processed for double = immunofluorescence=20 labeling using antibodies against the FGFR1 (B) and = EGFR=20 (C) 1 hr after tissue dissociation. Virtually = all the=20 SVZ cells contain the FGFR1 (B), whereas only a = subset=20 displays IR to both receptors (B, C, = arrows).=20 Although cells expressing only FGFR1 were observed = (B,=20 C, arrowheads), cells displaying only EGFR = were never=20 seen. Scale bar, 20 =B5m.

FGF2- and EGF-responsive stem-like cells colocalize = within the=20 SVZ of the adult mouse forebrain

We sought to determine whether FGF2-responsive stem-like cells = isolated from=20 the adult striatum (Gritti et al., 1996) = are=20 located in the forebrain SVZ and to establish their lineage=20 relationship with their EGF-responsive counterparts that also = reside=20 there (Morshead et al., 1994). = To this end,=20 primary cells were plated under clonal conditions (see = below), and=20 the number of stem-like cells in a dish was determined,=20 retrospectively, by counting the number of spheres formed = 8-10 d=20 later in response to GFs. For this approach to be reliable, = it is=20 essential that the vast majority, if not all, of the spheres = formed=20 are derived from a single cell. To verify that this was the = case,=20 aliquots of the same cell suspensions that were plated for = cell=20 quantification were seeded onto glass coverslips, fixed soon = after=20 and up to 48 hr later, stained with DAPI, and counted. = As shown=20 in Figure 2A,=20 >99% of the cells plated after tissue dissociation were = single=20 cells. Moreover, as expected from the high cell death rate = typical of=20 this type of assay, the number of doublets and triplets = dramatically=20 declined over the first 2 DIV (Fig. 2A).=20 We also adopted measures in the assays to prevent the = formation of=20 cell doublets and triplets because of reaggregation and = clustering.=20 Because of the high rate of cell death attributable to the = low cell=20 density and lack of serum, the plating efficiency was ~0.03% = (see=20 also Reynolds and Weiss, 1992). = Thus,=20 24 hr after plating, cell density was ~10 viable=20 cells/cm23D---=20a=20 condition under which cell aggregation does not occur. Furthermore, = embedding in methylcellulose gel prevented cell flotation and = aggregation but did not hinder substrate attachment. We = conclude=20 from these investigations that virtually each sphere = generated=20 in this system was produced from a single cell. As shown = previously=20 (Reynolds and Weiss, 1992; = Gritti et al.,=20 1996), = preliminary=20 experiments confirmed that individual spheres contained cells = capable=20 of self-renewal and able to give rise to all three major = neural cell=20 lineages3D---neurons, astrocytes, and oligodendrocytes = (data not=20 shown) (see also Figs. 6,=20 7).=20 Thus, counting the number of spheres in a well provides a = reliable=20 index of the number of stem-like cells initially plated and = capable=20 of proliferating under the conditions tested.



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  		Figure 2. =   EGF- and=20 FGF2-responsive CNS stem-like cells derive from the same = adult SVZ=20 precursor population that constitutively proliferates in=20 vivo. Cells dissociated from SVZ tissue and from = striatal tissue=20 (excluding the SVZ) were plated in the presence of either = EGF or=20 FGF2 at 20 ng/ml. To determine proportions of single = cells,=20 doublets, and triplets in the dissociated cells, we plated = the cells=20 onto coverslips and labeled the cells with the fluorescent=20 nuclear-staining DAPI. A, The percentages of single = cells,=20 doublets, and triplets of all cells in culture are shown, = determined=20 soon after plating and 48 hr later. These data show = that the=20 vast majority (99%) of the cells that will eventually give = rise to=20 spheres in these cultures are single cells. B, = Because the=20 vast majority of spheres are formed from single cells, we = were=20 justified in using the number of spheres per well formed = after 8-10=20 DIV as a measure of the number of stem-like cells (see also = Gritti=20 et al., 1996).=20 Spheres were generated exclusively from dissociated SVZ = explants.=20 Closely similar numbers of spheres were formed in response = to EGF=20 and FGF2. Data are the mean =B1 SE of four = independent=20 experiments in triplicate. C, Freshly dissociated SVZ = cells=20 were plated in the presence of either EGF or FGF2 at = 20 ng/ml=20 or both. The cell populations that give rise to EGF- and=20 FGF2-responsive cells are the same, because no increase in = the=20 number of clonal spheres per well was observed in the = presence of=20 both GFs compared with cultures exposed to either EGF or = FGF2. Data=20 are the mean =B1 SE of four independent = experiments in=20 triplicate. D, The number of spheres per well was = assessed in=20 SVZ cultures established from animals injected with high = doses of=20 [3H]thymidine or saline (control) over = 12 hr.=20 [3H]thymidine caused a significant and equal = decrease in=20 the numbers of spheres generated in the presence of EGF and = FGF2,=20 showing that the SVZ precursors from which these spheres = derive=20 possess closely similar proliferation kinetics in = vivo. Data=20 are the mean =B1 SE of three independent = experiments in=20 quadruplicate (p < 0.01 vs saline,=20 Student's t test).

From these assays, we were able to show that FGF2- and EGF-generated = spheres=20 formed only in cultures obtained from SVZ-containing tissue = (Fig. 2B)=20 and that the number of spheres formed in the presence of EGF = was the=20 same as the number formed in the presence of FGF2. Both EGF- = and=20 FGF2-generated primary spheres could be serially subcloned, = retaining=20 self-renewal capacity and multipotency over long-term = culturing (up=20 to 21 and 18 passages for EGF- and FGF2-responsive = cells,=20 respectively; see also below). Culturing the striatal = parenchyma=20 alone (excluding the SVZ), in either an EGF- or = FGF2-containing=20 medium, resulted in the production of few spheres that could = not be=20 subcultured. These observations identify the adult SVZ as the = site of=20 origin of equal quantities of EGF- and FGF2-responsive = stem-like=20 cells.

EGF- and FGF2-responsive stem-like cells derive from = the same=20 adult SVZ precursor population

The above findings suggest that EGF- and FGF2-responsive stem-like = cells from=20 adult SVZ may be a single stem-like cell type. We performed = two=20 further experiments to establish this hypothesis. First, if = EGF- and=20 FGF2-responsive stem-like cells are colocalized but distinct = SVZ=20 populations, we would expect at least a partial increase in = the=20 number of spheres formed in vitro when primary cells = are=20 cultured in the presence of FGF2 and EGF together compared = with the=20 numbers generated in response to only one GF. We found not = even a=20 slight increase in the number of spheres formed in the = presence of=20 both GFs (Fig. 2C).=20

Second, if EGF- and FGF2-responsive stem-like cells form a = single-cell=20 population, they should show similar in vivo proliferation=20 kinetics. We therefore compared the numbers of EGF- and=20 FGF2-responsive stem-like cells that could be cultured from = the SVZ=20 of animals treated with high doses of [3H]Thy with = the=20 numbers obtained from saline-injected mice (control). = Preliminary=20 experiments based on 5-bromo-2'-deoxyuridine incorporation = in=20 vivo confirmed that, as reported previously by Morshead et = al.=20 (1994), = administration=20 of [3H]Thy produced a significant decrease (~50%) in the = number=20 of constitutively proliferating cells within the SVZ in = vivo=20 (data not shown). As shown in Figure 2D,=20 the numbers of EGF- and FGF2-responsive stem-like cells = isolated=20 in vitro after [3H]Thy administration were both = decreased by=20 50%, showing that a significant fraction of both EGF- and=20 FGF2-responsive stem-like cells possesses closely similar=20 proliferation characteristics in vivo.

Together, these experiments show that there is a precursor cell = subtype in=20 the SVZ of the adult mouse forebrain that is able to respond = to both=20 EGF and FGF2. These EGF/FGF2-responsive cells have a cell = cycle time=20 of 12 hr or less and are the source of the EGF- and=20 FGF2-responsive stem-like cells isolated previously in = vitro=20 (Reynolds and Weiss, 1992; = Gritti et al.,=20 1996). =

EGF and FGF2 are both mitogenic regulators of the = same adult=20 SVZ stem-like cell

Stem cells must be able to self-renew, i.e., give rise to at least = one=20 daughter identical to the mother cell at each cycle (Davis = and=20 Temple, 1994; = Loeffler and=20 Potten, 1997). = Because=20 no specific markers are available to unequivocally identify = SVZ=20 stem-like cells, their self-renewal can only be assessed by=20 demonstrating the persistence of stem cell functional = features in the=20 progeny to which they give rise (Loeffler and Potten, 1997). = In the=20 present case we expect that EGF/FGF2-responsive SVZ stem-like = cells=20 grown by EGF stimulation will remain responsive to FGF2 after = long-term subculturing and vice versa.

We tested this first by showing that EGFR and FGFR1 transcripts were = present=20 (Fig. 3A)=20 in the progeny of SVZ stem-like cells subcultured for longer = than=20 2 months in the presence of either EGF or FGF2. = Furthermore,=20 cells bearing both EGFR (Fig. 3B,D)=20 and FGFR1 (Fig. 3C,E)=20 were present in the same long-term cultures, as observed in = cells=20 freshly dissociated from SVZ explants.



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  		Figure 3. =   SVZ=20 stem-like cells retain simultaneous expression of EGFR and = FGFR1=20 after long-term subculturing and expansion by means of = either EGF or=20 FGF2. SVZ stem-like cell cultures serially subcultured for = at least=20 2 months with either EGF or FGF2 contain mRNA = transcripts of=20 both EGFR and FGFR1. A, After RT-PCR on RNA extract = from SVZ=20 cultures grown in EGF, the transcripts of EGFR (lane = 1) and=20 FGFR1 (lane 2) are present. Both receptor transcripts = are=20 also present in cells cultured with FGF2 (lane 3, = EGFR;=20 lane 4, FGFR1). L, Ladder. B-E, Cells=20 coexpressing EGFR (B, D) and FGFR1 (C,=20 E) are detected by double immunofluorescence assay on = cells=20 serially subcultured in the presence of either EGF = (B,=20 C, arrows) or FGF2 (D, E,=20 arrows). As in primary SVZ cultures, cells bearing = FGFR1 but=20 not EGFR were found in EGF- (B, C, = arrowheads)=20 and FGF2-cultured SVZ cells (D, E, = arrowheads);=20 cells displaying only EGFR-IR were never detected. Scale = bar,=20 B-E, 25 =B5m.

Second, we performed serial clonal analysis and found that the = progeny of=20 stem-like cells subcultured for several months in the = presence of EGF=20 included cells that retained responsiveness to FGF2 and = preserved=20 both multipotentiality and the ability to self-renew. This = phenomenon=20 was also observed when the GFs were used in the reverse = order.=20 Individual EGF- or FGF2-generated clonal spheres (up to = passage 17;=20 referred to as primary spheres) were dissociated and replated = as=20 single cells at clonal density, one-half in the presence of = EGF and=20 one-half in the presence of FGF2. Each EGF-generated primary = sphere=20 contained several cells with the capacity to form secondary = spheres=20 not only in the presence of EGF (EGF3Dright-arrow=20EGF=20 spheres) but also in the presence of FGF2 (EGF3Dright-arrow=20FGF2 spheres), although to a significantly = lesser=20 extent (16.21 =B1 1.46 and = 11.65 =B1 0.99% of=20 the total number of cells plated for EGF3Dright-arrow=20EGF=20 and EGF3Dright-arrow=20FGF2,=20 respectively; p < 0.05, Student's t = test).=20 Similar results were obtained when FGF2-generated clonal = spheres=20 were dissociated and subcloned in the presence of EGF or = FGF2.=20 Even in this case, the number of secondary spheres formed in = the=20 presence of EGF (FGF23Dright-arrow=20EGF=20 spheres) was significantly higher than that formed in the = presence of=20 FGF2 (FGF23Dright-arrow=20FGF2=20 spheres; 10.21 =B1 0.94 and = 5.01 =B1 0.77% of=20 the total number cells plated for FGF23Dright-arrow=20EGF and=20 FGF23Dright-arrow=20FGF2, respectively;=20 p < 0.05, Student's t test; all data are = the=20 mean of three independent experiments; 7-13 individual = primary=20 spheres were used in each experiment). We also found that = secondary=20 spheres could be subcloned to produce EGF- and FGF-generated=20 tertiary spheres that, when randomly sampled and = differentiated, were=20 shown to differentiate into the three major neural cell types = (data not shown) (see also next paragraph).

These results indicate that EGF and FGF2 are able to substitute for = each=20 other in maintaining and expanding the SVZ stem-like cell = population,=20 although EGF seems to be more effective.

To provide further evidence of this, we extended our investigation by = studying the renewal and expansion characteristics of = multipotent SVZ=20 stem-like cells in response to EGF and FGF2 at the cell = population=20 level (Loeffler and Potten, 1997).=20 Stem-like cell cultures were established from SVZ using = either EGF or=20 FGF2 as the mitogen. After at least three passages, cultures = were=20 rinsed with control medium and dissociated, with one-half of = the=20 suspension of individual cells replated in the presence of = EGF and=20 one-half replated in the presence of FGF2 for further = subculturing.=20 This "GF switch" paradigm was sequentially repeated at least=20 twice for both EGF- and FGF2-generated stem-like cell = cultures.=20 The number of viable cells was assessed at each subculturing=20 step to produce cell growth curves for each switching=20 regimen.

We found from these experiments that stem-like cells established from = adult=20 SVZ had extended self-renewal capacity; not only did they=20 proliferate, but they consistently expanded in number when = grown in=20 FGF2-containing medium for up to 5 months (Fig. 4A).=20 Removal of GF promptly stopped proliferation and triggered=20 differentiation, as shown previously (Gritti et al., 1996). = However,=20 if after removal of FGF2 cells were exposed to EGF (Fig. 4A,=20 arrow), they retained their self-renewal properties = and,=20 additionally, grew at a rate similar to that of SVZ stem-like = cells=20 always grown in only EGF (compare Fig. 4A,B).=20 Importantly, when after a few passages in EGF these cultures = were=20 switched back to medium containing FGF2 (the GF used for = initial=20 isolation; Fig. 4A,=20 arrowhead), they resumed their original, slower = expansion=20 profile (Fig. 4A;=20 see doubling rates in the inset). Similarly, stem-like = cells=20 initially isolated by EGF continued to proliferate and, when = plated=20 in medium containing FGF2 (Fig. 4B,=20 arrow), displayed the slower expansion rate typical of = cells=20 isolated by FGF2. Behavior typical of EGF-responsive = stem-like cells=20 was restored when these cells were switched back to the = original=20 medium containing EGF (Fig. 4B,=20 arrowhead; see also inset). The peculiar = behavior of=20 both EGF- and FGF2-isolated cells after the GF switch could = be=20 reproduced consistently at any point over serial subculturing = (data=20 not shown).



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  		Figure 4. =   EGF and=20 FGF2 are interchangeable mitogenic regulators for the same = SVZ=20 stem-like cell population in culture. Cell growth curves = were=20 obtained by assessing the total cell number after each = subculturing=20 step, under the various growth conditions analyzed. The rate = of=20 doubling (reciprocal of the doubling time; see=20 insets) =B1 SE for the growth curves was = calculated=20 after cell growth had stabilized under the new conditions = (in=20 bold in the insets) after each GF switch. The = data=20 best fitted the equation: y =3D a=20 =B7 2sx, where y is the total = number of=20 cells, x is the time (DIV), s is the rate of = doubling,=20 and a is a constant. A, After serial = subculturing in=20 the continuous presence of FGF2, stem-like cells were = dissociated,=20 with one-half replated (arrow) in the presence of EGF = (FGF23Dright-arrow=20EGF; open circles) and = one-half=20 replated in the presence of FGF2 (FGF2; = open=20 squares) for further serial subculturing. = FGF2-responsive=20 stem-like cells continued to proliferate and expand in = number in the=20 presence of EGF, faster than they did in response to FGF2 = (see=20 inset). After serial subculturing in EGF, stem-like = cells=20 were replated in FGF2 medium (arrowhead), in which = they=20 resumed their slow growth mode (see inset; = FGF2EGF3Dright-arrow=20FGF2; filled squares). = B,=20 Stem-like cells serially subcultured in the presence of EGF = (open=20 circles) continued to grow and expand when exposed to = FGF2=20 (arrow; EGF3Dright-arrow=20FGF2; open squares). = The cells=20 proliferated at a slower rate in FGF2 than in EGF. However, = the=20 faster growth mode was restored when the cells were returned = to EGF=20 medium (arrowhead; EGF3Dright-arrow=20FGF23Dright-arrow=20EGF; filled circles; = see=20 inset). At various times, cells underwent clonal = analysis to=20 confirm the retention of multipotentiality (A, = B,=20 asterisks; examples shown in Figs. 6,=20 7).=20 The data are from one of three representative experiments = yielding=20 closely similar results.

Finally, we investigated the combined effect of EGF and FGF2 on the = growth=20 and/or expansion characteristics of SVZ stem-like cells. = After=20 isolation, SVZ cells were serially passaged in the presence = of either=20 EGF (Fig. 5A)=20 or FGF2 (Fig. 5B)=20 alone. Each culture was then dissociated and replated, = one-half in=20 medium containing the initial GF and one-half in the presence = of=20 both GFs (Fig. 5A,B,=20 arrows). Irrespective of the GF used for their initial = isolation, switching to medium containing both EGF and FGF2=20 determined a very fast expansion of the cell population, not = observed=20 previously (see also Fig. 5,=20 insets). Once again, this phenomenon occurred = irrespective of=20 the number of previous passages in the presence of the = original GF.=20 Furthermore, the original growth characteristics were = restored when=20 the cells were switched back to medium containing the = original GF=20 (Fig. 5A,B,=20 arrowhead; insets).



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  		Figure 5. =   The=20 expansion rate of the stem-like cell population is faster in = the=20 presence of EGF and FGF2 together than in the presence of = either GF=20 alone. Cell growth curves were obtained by assessing the = total cell=20 number after each subculturing step, under the various = growth=20 conditions. The rate of doubling (reciprocal of the doubling = time;=20 see insets) =B1 SE for the growth curves = was=20 calculated after cell growth had stabilized under the new = conditions=20 (in bold in the insets) after each GF switch. = The data=20 were best fitted to the following equation:=20 y =3D a = =B7 2sx, where=20 y is the total number of cells, x is the time = (DIV),=20 s is the rate of doubling, and a is a = constant.=20 A, B, Cells isolated and serially passaged in = the=20 presence of EGF (A, open circles) or FGF2 = (B,=20 open squares) were dissociated and replated either in = the=20 presence of the initial GF or with both EGF and FGF2 = (A,=20 B, arrows). The expansion rate is much higher = in the=20 presence of both GFs, regardless of whether the cultures = were=20 established by EGF or FGF2 (EGF or FGF2EGF+FGF2; filled = triangles). The=20 original expansion rate was resumed when the cultures were = replated=20 in medium containing the original GF (A, = arrowhead;=20 EGF3Dright-arrow=20EGF+FGF23Dright-arrow=20EGF; filled circles; = B,=20 arrowhead; FGF23Dright-arrow=20FGF2+EGF3Dright-arrow=20FGF2; filled squares; = see=20 insets for rates of doubling). At various times cells = underwent clonal analysis to confirm retention of = multipotentiality=20 (A, B, asterisks; examples shown in = Figs. 6,=20 7).=20 The data are from one of three experiments yielding closely = similar=20 results.

Over the course of these switching experiments, clonal analysis was = routinely=20 performed to show that SVZ stem-like cells retained their=20 multipotentiality under all the conditions tested. Regardless = of the=20 number and the nature of the manipulations to which they were = subjected, stem-like cells originally established either by = EGF or by=20 FGF2 always retained their ability to give rise to neurons,=20 astrocytes, and oligodendrocytes (Figs. 6,=20 7).=20 Note also that the capacity of both EGF- and FGF2-generated = stem-like=20 cells to give rise to the three neural lineages (after GF = removal)=20 was preserved after all the growth factor switches. We=20 determined this by assessing the number of MAP2-, GFAP-, and = GalC-IR=20 cells as proportions of the total number of cells established = in=20 the presence of FGF2, switched to EGF-containing medium,=20 switched back to FGF2, and differentiated (see also Figs. 6,=20 7).=20 We found that 13.28 =B1 0.91% neurons,=20 74.50 =B1 1.24% astrocytes, and = 3.69 =B1 0.45%=20 oligodendrocytes were generated. This compares with=20 12.07 =B1 0.84% neurons, 77.88 =B1 1.23% = astrocytes,=20 and 4.34 =B1 0.41% oligodendrocytes generated when = cells=20 established in EGF were switched to FGF2, switched back to = EGF, and=20 differentiated (mean =B1 SE; n =3D 6).



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  		Figure 6. =   SVZ=20 stem-like cells retain multipotentiality after multiple = sequential=20 changes in culturing conditions: FGF23Dright-arrow=20EGF3Dright-arrow=20FGF2. After each GF switch, samples were = taken from=20 the culture (indicated by asterisks in Figs. 4,=20 5)=20 and used to establish clonal spheres. In this case, the = culture was=20 initially established with FGF2, grown for ~1 month in EGF, = then=20 returned to FGF2, and cultured for ~2 months in this GF. = Single=20 cells were transferred to single wells (1 cell/well) by = micromanipulation and followed by time-lapse = microphotography. A=20 mark was incised on the vessel to mark the field containing = the=20 cell. The progeny of a single cell was plated onto glass = coverslips=20 and allowed to differentiate for 5 DIV by removal of = growth=20 factors. The cells retained multipotentiality under all the = growth=20 conditions exemplified in Figures 4=20 and 5.=20 A, B, The single cell shown in A formed = a clone=20 by 10 DIV (B). C-E, Progeny of this cell = included=20 neuronal (MAP2-IR; C, arrow), astroglial = (GFAP-IR;=20 D, arrowhead), and oligodendroglial (O4-IR; = E)=20 type cells. Scale bars: A, B, 25 =B5m;=20 C-E, 10 =B5m.



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  		Figure 7. =   SVZ=20 stem-like cells retain multipotentiality after multiple = sequential=20 changes in culturing conditions: EGF3Dright-arrow=20FGF23Dright-arrow=20EGF. After each GF switch, samples were = taken from=20 the culture (indicated by asterisks in Figs. 4,=20 5)=20 and used to establish clonal spheres. In this case, the = culture was=20 initially established in EGF, grown in the presence of FGF2 = for=20 almost 60 d, and returned to EGF for 2 months. = Single=20 cells were transferred to single wells (1 cell/well) by = micromanipulation and followed by time-lapse = microphotography. A=20 mark was incised on the vessel to mark the field containing = the=20 cell. The progeny of a single cell was plated onto glass = coverslips=20 and allowed to differentiate for 5 DIV by removal of = growth=20 factors. The cells retained multipotentiality under all the = growth=20 conditions exemplified in Figures 4=20 and 5.=20 A, B, The single cell shown in A formed = a clone=20 by 7 DIV (B). C-E, Progeny of this cell = included=20 neuronal (MAP2-IR; C, arrows), astroglial = (GFAP-IR;=20 D, arrowhead), and oligodendroglial (O4-IR; = E)=20 type cells. Scale bars: A, B, 12 =B5m;=20 C-E, 10 =B5m.

Overall these data show that EGF and FGF2 are mitogenic effectors for = a=20 single SVZ stem-like cell population that, in turn, is able = to vary=20 reversibly its growth profile according to the GF, or GF = combination,=20 to which it is exposed.


    DISCUSSION
TOP
ABSTRACT
INTRODUCTION
MATERIALS AND METHODS
RESULTS
DISCUSSION
REFERENCES =

We investigated the lineage relationships between the multipotential = neural=20 stem-like cell populations from adult mouse SVZ that are = isolated and=20 classified by their response to different GFs. We showed that = both=20 EGF- and FGF2-responsive stem-like cells derive from a single = precursor cell type able to respond to both GFs. A major = fraction of=20 these precursors is constitutively proliferating within the = SVZ in=20 vivo. We also found that EGF and FGF2 can act = interchangeably to=20 support the self-renewal of this population and that each GF = confers=20 different growth behavior to these cells in culture. The stem = cell-like population expands faster in the presence of EGF = than in=20 the presence of FGF2 and expands even faster when exposed to = both GFs=20 together. These modifications are fully reversible. Hence, we = have=20 shown that stem-like cells from the adult mammalian CNS can = modulate=20 their self-renewal characteristics and access alternative = functional=20 states in response to changes in the extracellular=20 environment.

The same, constitutively proliferating SVZ precursor = type is=20 the source of both EGF- and FGF2-responsive multipotent stem-like cells = of the=20 adult CNS

Several lines of evidence support this conclusion. First, both EGF- = and=20 FGF2-responsive multipotent stem-like cells share a common = anatomical=20 origin, occurring exclusively in the SVZ. The very few cells = from the=20 striatal parenchyma that proliferated in response to FGF2 = (Palmer et=20 al., 1995) = did not=20 display self-renewal potential in our hands; their limited=20 proliferative capacity suggests they are a transiently = dividing=20 subset of FGF-responsive neural progenitors (Loeffler and = Potten,=20 1997) = that may be=20 generated from multipotent neural stem-like cells (Vescovi et = al.,=20 1993).=20 Alternatively, these cells may be a subset of = FGF2-only-dependent=20 forebrain precursors that may require different growth = conditions=20 to display stem cell features, as shown previously for = hippocampal=20 precursor cells (Suhonen et al., 1996). =

Second, by extending work showing the presence of both EGFR and FGFR = in the=20 SVZ (Wanaka et al., 1991; = Morshead et=20 al., 1994;=20 Gonzalez et al., 1995; = Weickert and=20 Blum, 1995), = we found=20 that the vast majority of SVZ cells bearing the EGF receptor = also=20 coexpress the FGFR1, indicating that most EGF-responsive = stem-like=20 cells can also be stimulated by FGF2.

Third, we showed that the numbers of multipotential stem-like cells = that can=20 be isolated from the SVZ by culturing with either EGF or FGF2 = are=20 experimentally identical, as expected if the two stem = cell-like=20 populations derive from the same type of precursor. More = importantly,=20 we found no increase in the number of cells isolated when the = two GFs=20 were used in combination, further indicating that the two = stem-like=20 cell populations are the same.

Finally, the SVZ contains at least two subsets of mitotically active = cells,=20 the constitutively proliferating population (with a cell = cycle of=20 12.7 hr) and the relatively quiescent population [with a = cell=20 cycle of up to 28 d (Morshead and van der Kooy, 1992;=20 Morshead et al., 1994)]. = In=20 vivo administration of high doses of [3H]Thy = for=20 12 hr is known to deplete severely the constitutively=20 proliferating population, leaving the quiescent cells = unchanged=20 (Morshead et al., 1994). = The equal=20 decreases (50%) in the numbers of stem-like cells isolated = from the=20 SVZ by either EGF or FGF2 that we observed after in = vivo=20 administration of [3H]Thy for 12 hr show that the = precursors=20 from which these stem-like cells derive display closely = similar=20 proliferation kinetics. This finding reconciles previously=20 incompatible properties of EGF-responsive stem-like cells. It = was=20 initially thought that these cells originate exclusively from = the=20 relatively quiescent population (Morshead et al., 1994), = but it was=20 suggested recently that they derive from the constitutively=20 proliferating pool (Craig et al., 1996).=20 The fact that at least one-half of the EGF-responsive elements3D---=20which we now call EGF/FGF2-responsive3D---=20have a=20 cell cycle time of 12 hr or less confirms that a = significant=20 fraction of these cells derives from the constitutively = proliferating=20 SVZ precursor population.

The SVZ stem-like cell population can vary its = self-renewal and=20 expansion properties in a reversible manner, in response to EGF or FGF2, = in=20 vitro

The existence of an SVZ precursor that proliferates and shows = stem-like cell=20 properties when exposed either to EGF or FGF2 raises = questions as to=20 the functional role of this "multiple" mitogenic=20 regulation.

A fundamental characteristic of stem cells is the ability to = self-renew. At=20 the single-cell level, this can be achieved by asymmetric = division=20 generating one stem cell and one differentiated cell or by = symmetric=20 division in which both progenies are identical to the mother = cell=20 (Loeffler and Potten, 1997). = In a given=20 population, both mechanisms may occur, along with symmetric = division=20 generating two nonstem daughter cells, and the balance = between these=20 modes determines the maintenance or expansion of the = population at=20 each generation (Loeffler and Potten, 1997). = Our=20 subcloning experiments showed that a single SVZ cell always = gave rise=20 to progeny containing more than one multipotential stem-like = cell, in=20 the presence both of EGF and of FGF2. However, a greater = percentage=20 of the progeny generated by EGF had stem-like cell = characteristics,=20 compared with those generated by FGF2. Thus, although = symmetric=20 divisions giving two stem-like cells take place in the = presence of=20 either GF, these divisions occur more frequently in the = presence of=20 EGF. Thus a substantial difference between these GFs is that = EGF=20 imposes significantly faster expansion of the SVZ stem = cell-like=20 pool than does FGF2. We cannot rule out the possibility that = EGF=20 and FGF2 may also exert differential control on cell cycle=20 length, with SVZ stem-like cells cycling slower in the = presence of=20 FGF2; studies are presently underway to clarify = this.

Our subcloning assays further showed that EGF-generated stem-like = cells gave=20 rise to progeny that was both stem cell-like and responsive = to FGF2;=20 the same phenomenon was observed when the GFs were used in = the=20 reverse order. This was expected because, having the capacity = to=20 self-renew, EGF- and FGF2-responsive stem-like cells must = retain=20 responsiveness to both GFs, irrespective of which was used = for the=20 original culturing.

Furthermore, these results suggest that SVZ stem cells grown in EGF=20 self-renew and expand at a lower rate when exposed to FGF2 = alone.=20 Similarly, cells isolated by FGF2 can still self-renew in EGF = but=20 adopt a higher rate of expansion. Confirmation of this came = from cell=20 population analysis. In fact, the proliferation kinetics of a = stem=20 cell compartment cannot be inferred only from the behavior of = individual cells3D---=20as in=20 clonal experiments3D---=20but requires analysis of a large pool of = cells over an=20 extended period (Loeffler and Potten, 1997). = We=20 investigated the growth and expansion characteristics of SVZ=20 stem-like cells at the population level for over = 6 months,=20 showing that SVZ stem-like cells expand in response to both = GFs and=20 that, in agreement with the subcloning data, the total cell = number=20 increased significantly faster in the presence of EGF than in = the=20 presence of FGF2. Furthermore, stem-like cells initially = isolated by=20 FGF2 continued to proliferate, retained multipotentiality, = and=20 adopted a faster, EGF-like expansion kinetic profile when = switched to=20 EGF. More importantly, this change was fully reversible and=20 independent of the time in culture. Closely similar results = were=20 obtained when the order of GF application was inverted. = Furthermore,=20 when stem-like cells cultured from either EGF or FGF2 were = exposed to=20 both GFs simultaneously, they expanded faster than in the = presence of=20 either GF alone and returned to their initial growth rate = when=20 returned to the original GF. These findings show that these = adult CNS=20 cells are endowed with an important, yet undocumented stem = cell=20 feature: the ability to vary reversibly their self-renewal=20 characteristics (Loeffler and Potten, 1997). =

Whether cells become committed to division, quiescence, or = differentiation=20 depends on a complex series of events and stimuli, involving=20 regulation by combinations of extracellular mitogenic = stimuli,=20 including, essentially, peptide growth factors (Lukas et al., = 1996). = For example,=20 multiple GFs are reported to control proliferation in the = hemopoietic=20 system in which various interleukins, as well as the kit = ligand stem=20 cell factor, are mitogenic for early stem-like precursor = cells=20 (Bodine et al., 1991, = 1992).=20 Similarly, the satellite stem cells of skeletal muscles = possess=20 receptors for, and undergo proliferation in response to, = insulin-like=20 GFs (Dodson et al., 1985; = Allen and=20 Boxhorn, 1989) = and FGF2=20 (Allen et al., 1984; = Allen and=20 Boxhorn, 1989). = To the best=20 of our knowledge, however, this is the first report = indicating that=20 flexible, multifaceted epigenetic growth control may operate = in=20 stem-like cells from the adult mammalian SVZ. This is not a=20 functional characteristic of all adult CNS stem-like cells, = however,=20 because stem-like cells from adult spinal cord are incapable = of=20 extensive proliferation in the presence of EGF or FGF alone = but=20 require simultaneous exposure to both GFs to display = self-renewal=20 (Weiss et al., 1996). =

The capacity of SVZ stem-like cells to adopt different modes of = proliferation=20 and/or expansion when presented with alternative combinations = of=20 epigenetic signals may be best understood in the light of = their stem=20 cell function. Although under normal conditions the number of = stem=20 cells is stable, this can change significantly to compensate = for=20 tissue alterations (for review, see Morrison et al., 1997), = implying that=20 stem cells may react to different extracellular cues by = varying their=20 functional state. This hypothesis is consistent with previous = findings indicating that (1) responsiveness to FGF2 and/or = EGF may be=20 a fundamental property of immortalized multipotent neural = stem-like=20 embryonic progenitors (Kitchens et al., 1994), = (2) FGF2 may=20 increase EGF responsiveness in embryonic striatal precursors=20 (Ciccolini and Svendsen, 1998), = and (3)=20 FGF2 may influence the differentiation fate of cortical stem=20 cells (Qian et al., 1997). =

Thus, the differential growth regulation exerted by EGF and FGF2 on = SVZ=20 stem-like cells could be part of a basic growth regulatory = module=20 that allows neural stem cells to participate in CNS tissue=20 homeostasis. Support for this perspective comes from the = finding=20 that a prominent function of SVZ progenitors3D---=20the=20 contribution of new neurons to the olfactory epithelium (Lois = and=20 Alvarez-Buylla, 1994)3D---=20can be=20 significantly altered by in vivo infusion of either of = these=20 GFs (Craig et al., 1996; = Kuhn et al.,=20 1997). =

We suggest, finally, that our approach of investigating the = functional=20 properties of CNS stem-like cells at the single-cell and = population=20 level may be useful for identifying and characterizing other=20 epigenetic effectors that regulate stem-like cell activity in = the=20 CNS. Such studies could provide additional means for manipulating = or=20 activating stem-like cells, with a view to their therapeutic = use in=20 neurodegenerative disorders, perhaps via previous ex vivo=20 expansion, modification, and subsequent intracerebral = transplantation=20 or via in situ manipulation.


    FOOTNOTES

Received July 22, 1998; revised Jan. 12, 1999; accepted = Feb.=20 10, 1999.

The research was supported by the Italian Association of Parkinsonian = Patients, the Spinal Cord Society of Fergus Falls, and the = Comitato=20 Telethon (Grant A.116). We are grateful to Drs.=20 R. D. McKay, S. Temple, A. Calof, and=20 C. Svendsen for critically reading a previous version of = this=20 manuscript and to D. C. Ward for help with the = English=20 version of this manuscript.=20

Correspondence should be addressed to Dr. Angelo L. Vescovi, = Laboratory=20 of Neuropharmacology, National Neurological Institute = C. Besta,=20 Via Celoria 11, Milan, Italy I-20133.


    REFERENCES
TOP
ABSTRACT
INTRODUCTION
MATERIALS AND METHODS
RESULTS
DISCUSSION
REFERENCES =

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Copyright =A9=20 1999 Society for Neuroscience=20  0270-6474/99/1993287-11$05.00/0

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S.=20 Ferron, H. Mira, S. Franco, M. Cano-Jaimez, E. Bellmunt, C. = Ramirez, I.=20 Farinas, and M. A. Blasco
Telomere shortening and = chromosomal=20 instability abrogates proliferation of adult but not embryonic = neural stem=20 cells
Development, August 15, 2004; 131(16): = 4059 -=20 4070.
[Abst= ract]=20 [Full=20 Text] [PDF]=20
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E.=20 Garcion, A. Halilagic, A. Faissner, and C.=20 ffrench-Constant
Generation of an environmental niche = for=20 neural stem cell development by the extracellular matrix molecule = tenascin=20 C
Development, July 15, 2004; 131(14): 3423 = - 3432.=20
[Abst= ract]=20 [Full=20 Text] [PDF]=20
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B.=20 Greco, H. P. Low, E. C. Johnson, R. A. Salmonsen, J. Gallant, S. = N. Jones,=20 A. H. Ross, and L. D. Recht
Differentiation Prevents = Assessment=20 of Neural Stem Cell Pluripotency after Blastocyst=20 Injection
Stem Cells, July 1, 2004; 22(4): = 600 -=20 608.
[Abstract]=20 [Fu= ll=20 Text] [PDF]=20
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M. A.=20 Lopez-Toledano and M. L. Shelanski
Neurogenic Effect of = {beta}-Amyloid Peptide in the Development of Neural Stem=20 Cells
J. Neurosci., June 9, 2004; 24(23): = 5439 -=20 5444.
[Abstra= ct]=20 [Full=20 Text] [PDF] =
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D.=20 Derouet, F. Rousseau, F. Alfonsi, J. Froger, J. Hermann, F. = Barbier, D.=20 Perret, C. Diveu, C. Guillet, L. Preisser, et=20 al.
Neuropoietin, a new IL-6-related cytokine = signaling=20 through the ciliary neurotrophic factor receptor
PNAS, = April 6, 2004; 101(14): 4827 - 4832.
[Abstract]<= /A>=20 [Full = Text]=20 [PDF] =
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B.=20 Moreno-Lopez, C. Romero-Grimaldi, J. A. Noval, M. = Murillo-Carretero, E. R.=20 Matarredona, and C. Estrada
Nitric Oxide Is a = Physiological=20 Inhibitor of Neurogenesis in the Adult Mouse Subventricular Zone = and=20 Olfactory Bulb
J. Neurosci., = January 7, 2004; 24(1):=20 85 - 95.
[Abstract]= =20 [Full=20 Text] [PDF]=20
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J.=20 Imitola, E. Y. Snyder, and S. J. Khoury
Genetic = programs and=20 responses of neural stem/progenitor cells during demyelination: = potential=20 insights into repair mechanisms in multiple = sclerosis
Physiol=20 Genomics, August 15, 2003; 14(3): 171 - 197.
[Abstract]=20 = [Full=20 Text] [PDF]= =20
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R.=20 Galli, A. Gritti, L. Bonfanti, and A. L. Vescovi
Neural = Stem=20 Cells: An Overview
Circ. Res., = April 4, 2003; 92(6):=20 598 - 608.
[Ab= stract]=20 [Full=20 Text] [PDF]=20
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R.=20 Dono
Fibroblast growth factors as regulators of central = nervous=20 system development and function
Am J Physiol = Regulatory=20 Integrative Comp Physiol, April 1, 2003; 284(4): R867 - = R881.=20
[A= bstract]=20 [Full = Text] [PDF]=20
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M.=20 V.T. Lobo, F. J. M. Alonso, C. Redondo, M. A. Lopez-Toledano, E. = Caso, A.=20 S. Herranz, C. L. Paino, D. Reimers, and E. = Bazan
Cellular=20 Characterization of Epidermal Growth Factor-expanded Free-floating = Neurospheres
J. Histochem. Cytochem.,=20 January 1, 2003; 51(1): 89 - 103.
[Abstract] = [Full = Text] [PDF]
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F.=20 Ciccolini, T. J. Collins, J. Sudhoelter, P. Lipp, M. J. Berridge, = and M.=20 D. Bootman
Local and Global Spontaneous Calcium Events = Regulate=20 Neurite Outgrowth and Onset of GABAergic Phenotype during Neural = Precursor=20 Differentiation
J. Neurosci., = January 1, 2003;=20 23(1): 103 - 111.
[Abstract= ]=20 [Full=20 Text] [PDF] =
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L.=20 Elghazi, C. Cras-Meneur, P. Czernichow, and R. = Scharfmann
Role=20 for FGFR2IIIb-mediated signals in controlling pancreatic endocrine = progenitor cell proliferation
PNAS, = March 19, 2002;=20 99(6): 3884 - 3889.
[Abstract]=20 [Full = Text]=20 [PDF] =
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A.=20 Gritti, L. Bonfanti, F. Doetsch, I. Caille, A. Alvarez-Buylla, D. = A. Lim,=20 R. Galli, J. M. G. Verdugo, D. G. Herrera, and A. L.=20 Vescovi
Multipotent Neural Stem Cells Reside into the = Rostral=20 Extension and Olfactory Bulb of Adult Rodents
J. = Neurosci.,=20 January 15, 2002; 22(2): 437 - 445.
[Abstract= ]=20 [Full=20 Text] [PDF] =
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R.=20 Galli, R. Fiocco, L. De Filippis, L. Muzio, A. Gritti, S. = Mercurio, V.=20 Broccoli, M. Pellegrini, A. Mallamaci, and A. L. = Vescovi
Emx2=20 regulates the proliferation of stem cells of the adult mammalian = central=20 nervous system
Development, January 4, 2002; = 129(7):=20 1633 - 1644.
[Abstr= act]=20 [Full=20 Text] [PDF] =
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M.=20 Mitome, H. P. Low, A. van den Pol, J. J. Nunnari, M. K. Wolf, S.=20 Billings-Gagliardi, and W. J. Schwartz
Towards the=20 reconstruction of central nervous system white matter using neural = precursor cells
Brain, November 1, 2001; = 124(11):=20 2147 - 2161.
[Abstract]=20 [Fu= ll=20 Text] [PDF]=20
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Y.=20 Arsenijevic, S. Weiss, B. Schneider, and P.=20 Aebischer
Insulin-Like Growth Factor-I Is Necessary for = Neural=20 Stem Cell Proliferation and Demonstrates Distinct Actions of = Epidermal=20 Growth Factor and Fibroblast Growth Factor-2
J. = Neurosci.,=20 September 15, 2001; 21(18): 7194 - 7202.
[Abstra= ct]=20 [Full=20 Text] [PDF] =
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V.=20 Pencea, K. D. Bingaman, S. J. Wiegand, and M. B.=20 Luskin
Infusion of Brain-Derived Neurotrophic Factor = into the=20 Lateral Ventricle of the Adult Rat Leads to New Neurons in the = Parenchyma=20 of the Striatum, Septum, Thalamus, and Hypothalamus
J. = Neurosci., September 1, 2001; 21(17): 6706 - 6717. =
[Abstra= ct]=20 [Full=20 Text] [PDF] =
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V.=20 Calaora, B. Rogister, K. Bismuth, K. Murray, H. Brandt, P. = Leprince, M.=20 Marchionni, and M. Dubois-Dalcq
Neuregulin Signaling = Regulates=20 Neural Precursor Growth and the Generation of Oligodendrocytes In=20 Vitro
J. Neurosci., July 1, 2001; 21(13): = 4740 -=20 4751.
[Abstra= ct]=20 [Full=20 Text] [PDF] =
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C.=20 Cras-Meneur, L. Elghazi, P. Czernichow, and R.=20 Scharfmann
Epidermal Growth Factor Increases = Undifferentiated=20 Pancreatic Embryonic Cells In Vitro: A Balance Between = Proliferation and=20 Differentiation
Diabetes, July 1, 2001; = 50(7): 1571=20 - 1579.
[Abstract]=20 = [Full=20 Text] [PDF]= =20
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B.-S.=20 Li, W. Ma, L. Zhang, J. L. Barker, D. A. Stenger, and H. C.=20 Pant
Activation of Phosphatidylinositol-3 Kinase = (PI-3K) and=20 Extracellular Regulated Kinases (Erk1/2) Is Involved in Muscarinic = Receptor-Mediated DNA Synthesis in Neural Progenitor = Cells
J.=20 Neurosci., March 1, 2001; 21(5): 1569 - 1579.
[Abstrac= t]=20 [Full=20 Text] [PDF] =
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L. S.=20 Shihabuddin, P. J. Horner, J. Ray, and F. H. Gage
Adult = Spinal=20 Cord Stem Cells Generate Neurons after Transplantation in the = Adult=20 Dentate Gyrus
J. Neurosci., = December 1, 2000;=20 20(23): 8727 - 8735.
[Abstra= ct]=20 [Full=20 Text] [PDF] =
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S. F.=20 Pagano, F. Impagnatiello, M. Girelli, L. Cova, E. Grioni, M. = Onofri, M.=20 Cavallaro, S. Etteri, F. Vitello, S. Giombini, et=20 al.
Isolation and Characterization of Neural Stem = Cells=20 from the Adult Human Olfactory Bulb
Stem Cells,=20 July 1, 2000; 18(4): 295 - 300.
[Abstract]=20 [Fu= ll=20 Text]
3D""=20 = 		3D""=20
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F. H.=20 Gage
Mammalian Neural Stem Cells
Science,=20 February 25, 2000; 287(5457): 1433 - 1438.
[Ab= stract]=20 [Full=20 Text]
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D. J.=20 Martens, V. Tropepe, and D. van der Kooy
Separate = Proliferation=20 Kinetics of Fibroblast Growth Factor-Responsive and Epidermal = Growth=20 Factor-Responsive Neural Stem Cells within the Embryonic Forebrain = Germinal Zone
J. Neurosci., = February 1, 2000; 20(3):=20 1085 - 1095.
[Abstrac= t]=20 [Full=20 Text] [PDF] =
=20 		3D""=20
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T. D.=20 Palmer, E. A. Markakis, A. R. Willhoite, F. Safar, and F. H.=20 Gage
Fibroblast Growth Factor-2 Activates a Latent = Neurogenic=20 Program in Neural Stem Cells from Diverse Regions of the Adult=20 CNS
J. Neurosci., October 1, 1999; 19(19): = 8487 -=20 8497.
[Abstra= ct]=20 [Full=20 Text] [PDF] =
=20 		3D""=20

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