From: Subject: Distinct Populations of Forebrain Neural Stem and Progenitor Cells Can Be Isolated Using Side-Population Analysis -- Kim and Morshead 23 (33): 10703 -- Journal of Neuroscience Date: Sun, 8 Nov 2009 10:32:12 +0100 MIME-Version: 1.0 Content-Type: multipart/related; type="text/html"; boundary="----=_NextPart_000_008E_01CA605E.BBAC6430" X-MimeOLE: Produced By Microsoft MimeOLE V6.00.2900.5579 This is a multi-part message in MIME format. ------=_NextPart_000_008E_01CA605E.BBAC6430 Content-Type: text/html; charset="Windows-1252" Content-Transfer-Encoding: quoted-printable Content-Location: http://www.jneurosci.org/cgi/content/full/23/33/10703 Distinct Populations of Forebrain Neural Stem and = Progenitor Cells Can Be Isolated Using Side-Population Analysis -- Kim = and Morshead 23 (33): 10703 -- Journal of Neuroscience
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The Journal of = Neuroscience, November 19,=20 2003, 23(33):10703-10709

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Cellular/Molecular
Distinct Populations of Forebrain Neural Stem and = Progenitor=20 Cells Can Be Isolated Using Side-Population Analysis =

Mina Kim and Cindi M.=20 Morshead

Department of Surgery, University of Toronto, Toronto, = Ontario,=20 Canada M5S 1A8=20


   Abstract =
Top
3D"Abstract
3D"Introduction
3D"Materials and Methods
3D"Results
3D"Discussion
3D"References
 
T= he=20 absence of stem cell-specific markers has posed challenges = to=20 the identification and isolation of stem cells. We report = the=20 isolation of a discrete and highly enriched population of=20 neural stem cells from clonally derived colonies of neural = stem cell and progenitor cells (neurospheres) after = exposure=20 to the fluorescent DNA binding dye Hoeschst 33342 and = subsequent analysis via dual wavelength flow = cytometry. The=20 low fluorescent side population comprised only 3.6% = of all=20 live cells sorted yet contained >99% of all the = neural=20 stem cells as assayed by the formation of = neurospheres in=20 culture. Most neurosphere-derived cells are = progenitor cells,=20 and these are found within the higher fluorescence = (non-side=20 population) fraction. The isolation of a highly = enriched=20 population of self-renewing, multipotential neural = stem cells=20 was seen from both adult- and embryonic-derived = neurospheres;=20 however, the relative percentage of cells comprising = the=20 side-population and the mechanism of dye efflux varied = between=20 adult and embryonic donor tissue. Combining the=20 side-population analysis with markers recently shown = to=20 enrich for neural stem cells afforded no further = enrichment=20 in the case of peanut agglutinin expression and size=20 criteria; however, when the side-population analysis = was=20 combined with Lewis X (LeX) expression, a slight = enrichment=20 was seen over side-population analysis alone.

Key words: neural stem cells; FACS=20 analysis; neurospheres; side-population;=20 Hoechst; enrichment


   Introduction =
Top
Abstract
3D"Introduction
3D"Materials and Methods
3D"Results
3D"Discussion
3D"References
 
S= tem=20 cell biology in general suffers from the lack of a specific = marker that unambiguously labels all stem cells and only = stem=20 cells, enabling their prospective identification. Neural = stem=20 cells are no exception. The difficulty in isolating a pure = population of neural stem cells seriously limits the = study of=20 neural stem behavior and factors that regulate them. = Two=20 recent studies have described the use of antibody = staining to=20 characterize neural stem cells from the adult mouse=20 forebrain. One study used cell size combined with a = number of=20 negative selection criteria to isolate neural stem = cells=20 (Rietze et al., 2001), and more recently = expression of LeX,=20 a carbohydrate moiety (the trisaccharide=20 3-Fucosyl-N-acetyllactosamine or CD15, leukocyte=20 cluster of differentiation 15) (Gooi et al., 19813DGo), was found to be enriched = in stem cell=20 populations (Capela and Temple, 20023DGo). Here, we have taken advantage of the = "side-population" analysis described originally to = isolate a=20 highly enriched population of hematopoietic stem = cells from=20 adult bone marrow (Goodell et al., 19963DGo) and have shown that it is a simple = and=20 effective means by which to isolate embryonic and = adult=20 neural stem cells.

Bone marrow cells exposed to a fluorescent DNA binding = dye,=20 Hoeschst 33342, and observed using fluorescent-activated = cell=20 sorting (FACS) at two emission wavelengths (red and blue)=20 simultaneously resulted in a distinct staining = profile. Two=20 populations of cells were observed: (1) a = side-population=20 (SP; low fluorescence) and (2) a non-side-population = (non-SP;=20 higher fluorescence). The bone marrow-derived SP = fraction=20 comprised 3D~=201% of all of = the=20 total bone marrow and accounted for virtually all of the=20 hematopietic stem cell activity using an in = vivo bone=20 marrow repopulation assay (Goodell et al., 19963DGo). This distinct SP region was = shown to=20 be the result of differential efflux of the Hoechst dye = because=20 incubating bone marrow cells in the presence of verapamil = (an=20 inhibitor of ATP binding cassette (ABC)-transporter = protein=20 activity) resulted in the complete loss of the SP fraction = (Goodell et al., 19963DGo; 19973DGo; Storms et al., 2000).

We hypothesized that stem cells in general have an = enhanced=20 ability to pump out toxins relative to more differentiated = progeny and tested this hypothesis using neural = tissue. We=20 performed an SP analysis on a mixed population of = neural stem=20 and progenitor cells derived from adult and embryonic = mouse=20 neurospheres [clonally derived colonies of cells with = each=20 single neurosphere composed of neural stem cells, = progenitor=20 cells, and no differentiated neurons and glia = (Tropepe et=20 al., 1999)] that provided a pre-enriched = starting=20 population. FACS analysis revealed two distinct populations = from both embryonic and adult neurospheres: (1) SP cells = that=20 are highly enriched for neural stem cells and (2) non-SP=20 cells that account for the vast majority of sorted = cells and=20 consist of neural progenitor cells. These findings = suggest=20 that an enhanced ability to pump out toxins is common = among=20 stem cells regardless of the tissue of origin; = however, our=20 findings suggest that different members of the ABC = protein=20 family mediate the dye efflux in a tissue-dependent = manner.=20 In addition, we compared the enrichment profile using = the SP=20 analysis with marker expression profiles described = recently=20 by other groups (Rietze et al., 2001; Capela and Temple, 20023DGo) for stem cell isolation. We = observed a=20 slightly augmented enrichment within the SP profile using = LeX=20 expression that was dependent on the age of the starting=20 population of neural stem cells (adult- or = embryonic-derived=20 neurosphere cells).


   Materials and Methods=20
Top
Abstract
3D"Introduction
3D"Materials and = Methods
3D"Results
3D"Discussion
3D"References
 
<= I>Isolation=20 and culturing of neural stem cells. Neural stem cells=20 were isolated from embryonic day 14 forebrain germinal = zones=20 and from dissections of the adult forebrain subependyma = from=20 CD1 (Charles River) or C57BL/6 (Jackson Laboratories) mice = as=20 described previously (Tropepe et al., 1999). Bulk cultures were = established (20 cells per=20 microliter), and the medium included epidermal growth = factor=20 (EGF, 20 ng/ml) (Upstate Biotechnology, Lake Placid, = NY),=20 basic fibroblast growth factor (FGF, 10 ng/ml) = (Upstate=20 Biotechnology), and 1% penicillin/streptomycin (Tropepe = et=20 al., 1999). The cultures were passaged every 5-7 = d as=20 described (Tropepe et al., 1999). For single sphere passaging, each = sphere=20 was collected in a 200 =B5l pipette tip, transferred = to a=20 500 =B5l Eppendorf tube containing 100 =B5l of medium, = triturated=20 40-50 times, and then transferred to a 24-well plate = in a=20 final volume of 500 =B5l of medium.

SP cell analysis and flow cytometry. Neurospheres were = collected, centrifuged at 1500 rpm for 5 min at room=20 temperature, triturated, and resuspended in the = described=20 media (in the absence of EGF and FGF) in a = single-cell=20 suspension of 1 x = 106=20 cells/ml. Hoechst (Sigma, St. Louis, MO) was added at = a final=20 concentration of 5 =B5g/ml (embryonic cells) or 2.5 = =B5g/ml=20 (adult cells). The procedure was followed as = described=20 previously (Goodell et al., 19963DGo, 19973DGo). For blocking experiments, verapamil = was=20 added at 50 =B5M final = concentration (Sigma).=20 For immunostaining, the suspension was incubated for = 20 min=20 at 4=B0C with FITC-conjugated PNA (1:200; Vecta) = (Rietze et=20 al., 2001) or FITC-conjugated CD15 = antibody=20 (1:200; Becton-Dickinson) and then rinsed twice with=20 serum-free media (SFM) by centrifugation at 4=B0C.

Flow cytometric sorting was conducted as described = (Goodell=20 et al., 19963DGo, 19973DGo) using a FACStar Plus (Becton = Dickinson)=20 or FACSDiva. The gating on forward and side scatter was = not=20 stringent. A live gate was defined on the flow cytometer=20 using Hoechst red and blue axes to exclude dead cells = and=20 debris. Cell viability ranged from 40 to 70% during = the=20 sorting procedure. Sorting of antibody-labeled cells = used=20 FACS gates set with unlabeled cells. SP and non-SP = cells were=20 collected separately in plating medium.

SP versus non-SP cell culture. Sorted cells were = plated in=20 the presence of EGF and FGF (Tropepe et al., 1999). SP and non-SP cells were = plated at=20 equivalent densities (ranging from 1 to 10 cells per=20 microliter depending on the numbers of cells isolated). = The=20 numbers of neurospheres were counted after 10-14 d in = vitro.=20

Immunohistochemistry on neurospheres. Single- and=20 double-label immunocytochemistry were performed as = described=20 previously (Tropepe et al., 1999). Briefly, single spheres were plated = onto=20 glass coverslips coated with MATRI-GEL (Becton = Dickinson) in=20 SFM containing 10% fetal bovine serum. Five to 7 d = later the=20 cells were fixed with 4% paraformaldehyde and stained = with=20 antibodies to MAP2 (mouse monoclonal IgG; Boehringer=20 Mannheim, Mannheim, Germany), glial fibrillary acidic = protein=20 antisera (rabbit polyclonal; Chemicon), and 04 (mouse = monoclonal, IgM; Boehringer Mannheim). Appropriate = secondary=20 antibodies (FITC goat anti-rabbit, TRITC goat = anti-mouse,=20 dichlorotriazinyl-aminofluorescein goat anti-mouse; = all from=20 Jackson ImmunoResearch) were used.

Reverse transcription-PCR. Total RNA was isolated from = equal numbers of SP and non-SP cells (4000-30,000,=20 respectively) immediately after FACS-sort using = RNeasy Mini=20 Kit (Qiagen), precipitated in ethanol, and treated = with DNase=20 I (Inv= itrogen)=20 before resuspension in 12 =B5l of RNase-free water. = Reverse=20 transcription (RT) and PCR were performed = sequentially in the=20 same tube on equal amounts of isolated RNA (1-2 =B5g = per=20 sample) using the OneStep RT-PCR kit (Qiagen). The = primers=20 used for PCR amplification were as follows: ABCG2 5' = end=20 primer 5'-GTC AGC TGT GGA GCT GTT CGT AG, and ABCG2 = 3' end=20 primer 5'-CAC AAG TGC TGT TGT CCG TTA CA; GFAP 5' end = primer=20 5'-GTT GTG AAG GTC TAT TCC TGG C, and GFAP 3' end = primer=20 5'-TCC CTT AGC TTG GAG AGC AA. After 40 cycles of=20 amplification, 7 =B5l of the reaction mix was = electrophoresed=20 on 2% agarose gels and stained with ethidium = bromide.=20


   Results =
Top
Abstract
3D"Introduction
3D"Materials and Methods
3D"Results
3D"Discussion
3D"References
 
N= eural=20 stem cell cultures were established from the forebrain=20 germinal zones of embryonic and adult mice. The = dissociated=20 germinal zone cells were cultured in the presence of EGF = and=20 FGF2 to produce neurospheres, clonally derived colonies of = cells each originating from a single neural stem = cell.=20 Typically, each neurosphere contains 15,000-20,000 = cells, of=20 which most are progenitor cells that have limited=20 self-renewal capacity and more restricted lineage = potential=20 (Tropepe et al., 2000). Approximately 0.2-0.8% of = neurosphere=20 cells are neural stem cells with the ability to self = renew=20 (form new spheres after dissociation) and are = multipotential=20 (can generate neurons and glia). This range is based = on the=20 frequency of observing newly generated neurospheres = after the=20 plating of single cells from a dissociated = neurosphere=20 (range, 50-130 new spheres from a 15,000-20,000 cell = sphere)=20 (Morshead et al., 2002). Neural stem cells = represent 0.2-0.4%=20 of the cells found within the adult forebrain = subependyma=20 (Morshead et al., 1998) and hence significantly = less in a=20 dissection of the whole adult forebrain. Virtually = all of the=20 cells within a neurosphere express nestin, a marker = of=20 undifferentiated cells (Lendahl et al., 19903DGo); therefore, the use of=20 neurosphere-derived cells as a starting population = afforded=20 us an enriched population of neural stem and progenitor = cells=20 in the absence of differentiated cell types. Neurospheres=20 were collected from bulk cultures that could be maintained = by=20 passaging in the presence of EGF and FGF2.

Neural stem cells sort to the = SP
Embryonic=20 neurosphere-derived cells were collected from cultures=20 passaged <10x = (<P10) and=20 sorted on the basis of Hoechst fluorescence. Because=20 continual passaging (>10x) leads=20 to cellular transformations in the cultures (Morshead = et al.,=20 2002), we kept the number of = passages low=20 enough to avoid transformations yet still be able to = harvest=20 vast numbers of cells. The analysis revealed SP and = non-SP=20 components similar to those seen with bone marrow = cells (Fig. = 1a,b). Samples of the SP and non-SP cells = were=20 collected separately and plated in the presence of = EGF and=20 FGF2 at equal densities (1-10 cells per microliter). = The SP=20 comprised 3.6 =B1 1.2% (Fig. = 1d) of the live cells sorted [dead cells = were=20 excluded on the basis of propidium iodide (PI) = uptake] but=20 contained 98.7 =B1 21.7% of all of the = neurosphere-forming=20 cells. Thus, the frequency of isolating a stem cell = is 1 in=20 12 SP cells and 1 in 3333 non-SP cells (Table= =20 1). This represents a 278-fold enrichment = comparing the=20 SP and non-SP cells. Considering the frequency of = stem cells=20 within a neurosphere, the SP fraction represents a = 10- to=20 40-fold increase over baseline conditions. = Importantly, the=20 SP versus non-SP fractions contain distinct = populations of=20 stem versus progenitor cells, respectively. =


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  = 		Figure = 1.=20 Neurosphere-derived cells reveal an SP that is = highly=20 enriched for neural stem cell activity. a, = Primary=20 mouse bone marrow cells exposed to Hoechst dye and=20 subsequently sorted on the basis of dual wavelength = flow=20 cytometry reveal a low fluorescing SP (outlined) = that=20 comprised 1% of all of the live cells sorted. b, = c,=20 Neurospheres derived from embryonic (b) and = adult=20 (c) forebrain germinal zones were passaged=20 (<10x) before = sorting.=20 After exposure to Hoechst dye, SPs were observed = that=20 comprised small percentages (means =B1 SEM) of all = of the live=20 cells sorted (d, white bars) yet contained = the vast=20 majority of neural stem cells (d, black bars; = mean=20 percentage =B1 SD of all neurospheres formed from SP = and=20 non-SP cultures combined). e, Embryonic = neurosphere=20 cells were exposed to Hoechst dye and verapamil = before the=20 SP analysis. In the presence of verapamil, the SP = population=20 was completely lost (compare with b). =

 = ;


View=20 this table:
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  = 		Table = 1. Summary chart of enrichment = profile for=20 neural stem cells after an SP analysis =

 
The=20 adult neurosphere sorting profile revealed a smaller = enrichment=20 (7.5-fold) (1 of 46 SP cells and 1 of 345 non-SP cells = formed=20 neurospheres) (Fig. = 1c,d) (Table= =20 1). This may be attributable to increased death = of adult=20 stem cells after exposure to Hoechst. This hypothesis = is=20 supported by the fact that a lower Hoechst = concentration (2.5=20 vs 5.0 =B5g/ml) during sorting resulted in a = significant=20 increase in cell viability when adult-derived = neurospheres=20 were analyzed. This increased cell viability was not = seen=20 with embryonic cells. Alternatively, adult neural stem = cells=20 may represent a less homogenous population of cells = relative=20 to embryonic cells.

To rule out the possibility that the neural stem cell = enrichment=20 that we observed between the SP and non-SP fractions was = an=20 artifact of the toxicity of the Hoechst dye selectively=20 killing the potentially neurosphere-forming cells in = the=20 non-SP (i.e., cells with greater levels of Hoechst = dye), we=20 performed a number of controls. The control groups = consisted=20 of (1) Hoechst only (Hoechst stained but not exposed = to the=20 FACS machine), (2) FACS machine (Hoechst stained, run = through=20 the FACS machine but not sorted into SP and non-SP), = and (3)=20 untreated (no exposure to Hoechst or FACS machine). = Cells=20 from each group were cultured at 2 cells per = microliter. The=20 number of neurospheres was counted and compared = between each=20 control group. There was a fivefold decrease in the = average=20 number of neurospheres formed after exposure to = Hoechst=20 (Hoechst only and FACS machine groups) when compared = with the=20 average number of neurospheres formed in the absence = of=20 Hoechst (untreated). There was no significant difference,=20 however, in the average number of spheres between the=20 Hoechst-only group and the FACS machine group (4.8 vs = 4.3=20 neurospheres per 1000 cells plated, respectively), = suggesting=20 that although Hoechst does exert toxic effects on = cells=20 during staining, exposure to the FACS machine has no = effect=20 on the viability of these cells. More importantly, = the=20 absolute numbers of neurospheres that formed after = the=20 plating of equal numbers of sorted cells (SP plus = non-SP) was=20 virtually identical to the total numbers of = neurospheres=20 formed from Hoechst-treated cells (Hoechst only and = FACS=20 machine groups) (51.3 vs 56.8 cells formed neurospheres = per=20 10,000 cells plated, respectively). Because the non-SP = fraction=20 contained <0.09% of the total numbers of neurospheres = that=20 formed, virtually all of the neurosphere-forming cells are = within the SP fraction. These data confirm that the = SP=20 fraction represents a true enrichment of neural stem=20 cells.

Exposing the Hoechst-labeled neurosphere cells to = verapamil,=20 an inhibitor of the ABC transporter protein, resulted in a = block of the formation of the SP fraction (Fig. = 1e). This suggests that the distinct = staining=20 pattern observed by the neurosphere cells may be = caused by a=20 high level of dye efflux activity mediated by members = of the=20 ABC transporter protein family. One candidate member = is=20 Bcrp1/ABCG2, which is observed in hematopoietic stem = cells=20 (Zhou et al., 2001). To test this hypothesis, RT-PCR = for=20 Bcrp1/ABCG2 was conducted on equal amounts of RNA isolated = from SP and non-SP fractions from adult- and=20 embryonic-derived neurosphere cells (Fig. = 2). The non-SP fractions (progenitor cells) from = both=20 adult and embryonic neurospheres expressed Bcrp1/ABCG2 = as=20 well as SP cells from embryonic neurospheres. = Interestingly,=20 there was absolutely no expression from adult SP cells.=20 Notably, although the SP fraction is enriched in = neural stem=20 cells, it also contains progenitor cells. The = inability to=20 detect Bcrp1/ABCG2 in the adult SP fraction suggests = that all=20 progenitor cells within a neurosphere are not = identical and=20 those that sort to the SP fraction are differentially = expressing Bcrp1/ABCG2 compared with those that sort = to the=20 non-SP. We cannot formally rule out the possibility = that=20 Bcrp1/ABCG2 is expressed at such low levels that it = is=20 undetectable using RT-PCR; however, this seems = unlikely=20 because increasing the number of cycles of amplification = did=20 not result in Bcrp1/ABCG2 detection (data not shown). = Hence,=20 Bcrp1/ABCG2 is expressed in progenitor cells at both ages = but=20 is not expressed in neural stem cells derived from the = adult.=20


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  = 		Figure = 2.=20 RT-PCR on SP and non-SP fractions. Amplified = products of the=20 one-step RT-PCR conducted on RNA isolated from = FACS-sorted=20 cells. SP and non-SP fractions from embryonic- and=20 adult-derived cells reveal ABCG2 transporter = expression in=20 embryonic SP, embryonic non-SP, and adult non-SP = cells and=20 the complete absence in adult SP cells. GFAP = expression was=20 detected in both SP and non-SP fractions of = adult-derived=20 neurosphere cells. =

 = ;
SP-derived=20 neurospheres display the properties of neural stem = cells
By=20 definition, stem cells are (1) self-renewing and (2) = multipotential=20 cells. To confirm that the neurospheres that formed after=20 Hoechst exposure and sorting were derived from neural = stem=20 cells, we first tested the SP-derived neurospheres to = determine whether they were passageable (i.e., = displayed the=20 property of self-renewal). Single spheres derived = from both=20 adult and embryonic SP regions were dissociated and = plated in=20 the presence of EGF and FGF2. Each of the = neurospheres from=20 the SP region (adult or embryonic) gave rise to new = spheres=20 (131 =B1 16.5 new spheres per single dissociated = sphere).=20 Interestingly, when neurospheres derived from = embryonic=20 non-SP cells were tested (albeit few in number), 100% = of=20 non-SP-derived single spheres failed to passage (0 of = 6),=20 suggesting that they were derived from progenitor = cells=20 rather than neural stem cells (Seaberg and van der Kooy,=20 2002). Accordingly, the embryonic SP = population=20 contains 100% of all neural stem cells. When adult = non-SP=20 neurospheres were passaged, 66% (8 of 12) of = neurospheres=20 failed to passage. This suggests that the frequency = of a=20 neural stem cell among the adult non-SP cells is 1 in = 1045=20 cells, and therefore the relative enrichment in the = SP=20 fraction is 22.8x. =

Single neurospheres derived from the SP region were = examined=20 for multipotentiality. Immunocytochemistry confirmed that = all=20 of the SP-derived spheres contain neurons (MAP2+'ve or = BIII=20 tubulin+'ve) and glia (GFAP+'ve astrocytes and O4+'ve=20 oligodendrocytes) (Fig. = 3).


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  = 		Figure = 3.=20 SP-derived neurospheres are multipotential. = Photomicrographs=20 showing 3D{beta}III-tubulin=20 positive neurons (a), GFAP-positive = astrocytes=20 (b), and O4-positive oligodendrocytes = (c)=20 after 7 d exposure to differentiation conditions. = The=20 photomicrographs are representative of the=20 immunohistochemical staining observed from 100% of = the adult=20 and embryonic SP-derived neurospheres. Scale bars, = 50 =B5m. =

 = ;
It=20 has been shown recently that adult forebrain neurospheres = are=20 clonally derived from GFAP-expressing cells (Morshead et = al.,=20 2003). Neurospheres do not form after the = in=20 vivo or in vitro ablation of = GFAP-expressing=20 cells, and furthermore, RT-PCR reveals that GFAP is = expressed=20 at low levels in whole neurospheres (Morshead et al., = 2003). A prediction from these findings = is=20 that GFAP expression would be seen in the SP fraction in=20 which the neural stem cells are found. To test this=20 hypothesis we performed RT-PCR on adult SP and non-SP = fractions and observed a positive signal from both = fractions=20 (Fig. = 2). Detection of GFAP expression in the non-SP = fraction=20 suggests that (1) non-SP cells express low levels of = GFAP or=20 (2) a small subpopulation of non-SP cells express = GFAP.=20 Hence, the observation that GFAP is expressed in SP = cells is=20 consistent with reports that neural stem cells are = GFAP=20 positive; however, detection in the non-SP fraction = reveals=20 that GFAP is not a unique marker of neural stem = cells.=20

Further enrichment of neural stem = cells
Rietze et=20 al. (2001) reported the purification of neural = stem=20 cells from the primary dissociation of adult brain. Two of = the selection criteria were (1) cell size of >12 = =B5m=20 and (2) the low expression of peanut agglutinin. We = asked=20 whether using these selection criteria would enrich = further=20 the frequency of neural stem cells within the SP = region=20 isolated from neurospheres.

A twofold enrichment in neural stem cell isolation was = obtained=20 by Rietze et al. (2001) when cells were sorted on the = basis of=20 size alone (>12 =B5m); they reported that 80% of neural = stem=20 cells were in the >12 =B5m diameter population of = cells.=20 Because we observed >80% of all the neural stem cell=20 activity within the SP region, we sorted the SP on the = basis=20 of size to determine whether we could further enrich for = the=20 stem cells. A profile from a forward light scatter of=20 neurosphere-derived SP cells revealed that 41 =B1 8% = of the=20 cells were <10 =B5m in diameter (small) and 23 =B1 = 6% were=20 >12 =B5m in diameter (large) (Table= =20 2). Furthermore, 5.5% of the small diameter cells = and=20 9.7% of the large diameter cells gave rise to = spheres;=20 however, a purity check on these SP fractions (large = vs=20 small) before plating revealed a high degree of overlap=20 whereby after the re-sort only 36 =B1 16% of the = small=20 cells remained in this "small" fraction, and 19 =B1 = 9% of=20 the cells (originally founding the small fraction) were=20 subsequently found in the large fraction. There was a = similar=20 degree of overlap after a purity check of the large = cells (Table= =20 2). To test the possibility that the large cells = were in=20 fact the result of more than one event (i.e., = clumping), we=20 plated large SP cells directly from the FACS analysis = into=20 wells of a 24-well plate at a density of one event = per well.=20 The wells were examined 16 hr later to determine the=20 frequency of observing more than one cell per well. = We found=20 that 40% of the wells contained cells (38 of 96), and = of=20 these, 47% had more than one cell per well (18 of = 38),=20 suggesting that large cells were likely to be the = result of=20 more than one cell per well. Indeed, this finding = decreases=20 by 3D~50%=20 the frequency that a single "large" cell is a neural = stem=20 cell that will form a neurosphere and suggests that = the 50%=20 increase in stem cell frequency within the large cell = fraction can be accounted for entirely by clumping during=20 sorting.


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  = 		Table = 2. Sorting on basis of size within = the SP=20 fraction of embryonic-derived neurosphere cells =

 
The=20 PNA binding criteria reported by Rietze et al. (2001) involved sorting for = PNAlo=20 cells and resulted in an additional 22x enrichment in this = population.=20 Neurosphere-derived cells from SP populations were = sorted=20 further on the basis of their expression of PNA-FITC, = and the=20 sorting profile reveals a unimodal distribution of=20 SP-PNA-expressing cells from both the adult- and=20 embryonic-derived cell population. We arbitrarily = sorted the=20 SP-PNA profile into a small proportion (range 3-17%) = of=20 PNAlo-expressing cells (SP-PNAlo) (Fig. = 4a,b) and an = SP-PNAhi-expressing=20 population that comprised 36% of virtually all of the = remaining cells within the profile. When the=20 SP-PNAlo and SP-PNAhi fractions from = adult-derived=20 neurospheres were plated separately, the relative = frequency=20 of neurosphere formation did not differ between the = two=20 fractions (1% of the cells in both = SP-PNAlo and=20 SP-PNAhi fractions formed neurospheres).=20 Interestingly, when the SP cells from embryonic-derived=20 neurospheres were sorted into SP-PNAlo and = SP-PNAhi fractions, >95% of the = neurospheres=20 were found in the PNAhi-expressing population.=20 Because SP-PNAhi cells comprise the majority of = the SP=20 fraction (range, 65-97%), the observation that = >95% of the=20 stem cells are found here does not represent a true=20 enrichment. Hence, the PNA criteria do not enhance = the=20 enrichment of neural stem cells from embryonic or = adult=20 neurospheres over that obtained with the SP = analysis.=20


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  = 		Figure = 4.=20 PNA and LeX binding profiles of SP cells. a, = SP cells=20 were examined before exposure to the = PNA-FITC-conjugated=20 antibody to reveal the profile of PNA negative = cells.=20 b, SP cells were incubated with PNA-FITC = antibody and=20 then sorted on the basis of their FITC fluorescence. = The=20 profile of SP-PNA expression is unimodal and was = divided=20 into PNAlo cells (low) and = PNAhi cells=20 (high). The SP-PNA profile shown is from adult = neurosphere=20 cells and is not different from that observed with = embryonic=20 neurosphere cells. c, d, Adult SP cells were = examined=20 in the absence (c) and presence (d) of = CD15-FITC antibody and sorted on the basis of their = FITC=20 fluorescence. The LeX-positive (LeX pos) and = -negative=20 fractions were plated separately and assayed for = neurosphere=20 formation. Adult and embryonic SP-LeX-FITC had = similar=20 unimodal profiles. =

 = ;
Enrichment=20 for neural stem cells has been described recently = using=20 LeX/ssea-1 expression as a criterion for identification=20 (Capela and Temple, 20023DGo). FACS analysis of acutely = isolated=20 subventricular zone cells reveals that 4% of the cells are = LeX positive (LeX+), and this = subpopulation=20 contains the neurosphere-forming cells. Initial = examination=20 of neurosphere-derived cells revealed that = LeX+=20 cells are found within the SP and non-SP fractions of = embryonic- and adult-derived neurosphere cells (data not=20 shown); therefore, isolation of cells on the basis of LeX=20 expression alone did not enrich for neural stem = cells.=20 Accordingly, we set out to determine whether we could = further=20 enrich for neural stem cells by sorting for = LeX+=20 within the SP fraction. LeX+ cells = represented 48%=20 (range, 33-68%) (Fig. = 4d) of all of the embryonic-derived SP = cells=20 sorted and gave rise to 80% of all of the = neurospheres that=20 formed (11.6% of all cells plated in the = LeX+=20 fraction gave rise to neurospheres). This represents = a 38%=20 enrichment compared with sorting for SP alone (1 of 8.5=20 SP-LeX+ cells formed a neurosphere vs 1 in 12 = cells=20 from SP-only sorting). The adult-derived neurosphere = cells=20 revealed a profile whereby 65% (range, 56-73%) of the = SP=20 cells were LeX+, and this population gave = rise to=20 72% of the neurospheres that formed, thereby = reflecting only=20 a small 10% enrichment compared with sorting for SP = only.=20 Thus, sorting for LeX+ cells within the SP = does=20 enrich for neural stem cells from embryonic neurosphere=20 cells.


   Discussion =
Top
Abstract
3D"Introduction
3D"Materials and Methods
3D"Results
3D"Discussion
3D"References
 
U= nderstanding=20 of the basic biology and therapeutic potential of = neural stem=20 cells has been hindered by the inability to prospectively=20 identify neural stem cells and enrich for them. To = overcome=20 this barrier we have used a strategy developed for the=20 isolation of hematopoietic stem cells that involves = FACS=20 analysis on the basis of the enhanced ability of stem = cells=20 to efflux Hoechst dye (Goodell et al., 19963DGo). This dye exclusion paradigm = revealed=20 that neural stem and progenitor cells derived from=20 neurospheres exhibit a sorting profile containing a = low=20 fluorescing SP that is highly enriched for neural = stem cells.=20 Sorting of embryonic-derived neurosphere cells = results in an=20 SP region that comprises only 3.6% of all the live = cells yet=20 contains 99% of all the neurospheres, representing a = 278-fold=20 enrichment of neural stem cells. Importantly, the SP = cells=20 give rise to neurospheres that are self renewing and=20 multipotent. None of the non-SP-derived neurospheres = elicited=20 the cardinal stem cell property of self-renewal (Potten = and=20 Loeffler, 1990), and therefore non-SP neurospheres = (1% of=20 all the neurospheres that formed) were derived from=20 progenitor cells and not neural stem cells (Seaberg = and van=20 der Kooy, 2002). Accordingly, 100% of the = neural stem=20 cells derived from embryonic neurospheres are found = within=20 the SP fraction; the non-SP fraction is entirely = progenitor=20 cells, and the 278-fold enrichment is a minimum=20 estimate.

FACS using monoclonal antibodies to cell surface markers = also=20 has been reported to enrich for neural stem cells. P75=20 receptor immunoreactivity prospectively identified = putative=20 neural stem cells from the peripheral nervous system=20 (Morrison et al., 19993DGo), and CD133 = immunoreactivity allowed=20 isolation of neural stem cells from human fetal brain = (Uchida=20 et al., 2000). Rietze et al. (2001) used an immuno-FACS strategy to = isolate adult=20 neural stem cells from primary adult forebrain = tissue. The=20 selection criteria were cell diameter >12 =B5m, = low peanut=20 agglutinin expression, and low heat-stable antigen=20 expression. These criteria resulted in neurosphere = formation=20 from 1 to 1.3 of the cells isolated (Rietze et al., = 2001). Using the size criteria in an = attempt=20 to further enrich for neural stem cells within the SP=20 fraction, we found that sorting on the basis of size = criteria=20 is not reliable because the purity of the population is = poor,=20 with up to 20% of the fractions overlapping after = reanalysis=20 of sorted populations (compared with >98% purity of the = SP=20 fraction). The unreliable nature of forward scatter = sorting=20 to separate cells on the basis of cell diameter also may=20 explain the discrepancy between Rietze et al. (2001) and the recent findings of = Murayama et=20 al. (2002), which reported that SP cells = were=20 present only in the small cell fraction isolated from the=20 adult subventricular zone. The size criterion is = compromised=20 further by clumping of cells (i.e., more than one cell per = event). Sorting for clumps of cells artificially = increases=20 the frequency of isolating neural stem cells. Hence, = the=20 inability to reliably separate cells on the basis of = cell=20 diameter, in combination with the fact that single = events are=20 actually representative of more than one cell, makes = cell=20 size a weak criterion on which to base sorting=20 procedures.

Perhaps the most significant difference between the = enrichment=20 paradigms for isolating neural stem cells is the starting=20 populations of cells: neurosphere-derived cells = versus=20 primary dissociated tissue. Using neurosphere-derived = cells=20 was advantageous because we could generate millions = of cells=20 for sorting, and more importantly, neurospheres are = already=20 enriched for neural stem cells (Morshead et al., = 2002). Interestingly, Rietze et al. (2001) report that SP sorting of = primary=20 adult forebrain tissue is not a viable approach to = isolating=20 neural stem cells. In contrast, we did find that the = SP from=20 primary tissue was enriched for neural stem cells. = Indeed,=20 100% of all of the embryonic neural stem cells were = found in=20 the SP; however, only 9 of 10,000 cells plated were = neural=20 stem cells (our unpublished observations). The lower=20 frequency of neural stem cells within the SP from = forebrain=20 dissections may reflect contamination with differentiated=20 cells from the primary dissociation and highlights the=20 prepurification achieved using neurospheres as a = starting=20 population (containing only neural stem and = progenitor=20 cells).

The PNAlo criteria for isolating neural stem cells = also=20 was investigated using a starting population of = neurosphere=20 cells. Rietze et al. (2001) reported an enrichment on the basis = of=20 sorting for PNAlo-expressing cells from primary = dissections of adult tissue. We found, however, that=20 regardless of the starting population of = neurosphere-derived=20 cells (adult or embryonic), SP cells sorted on the = basis of=20 PNA expression showed no further enrichment when we = compared=20 the relative percentages of SP-PNAlo and=20 SP-PNAhi cells that formed neurospheres. Accordingly, = the subsequent PNA profile offers no advantage over = the SP=20 sort alone. The contradiction between our findings = and the=20 findings of Rietze et al. (2001) may reflect the different starting=20 populations; however, it is worth noting that if = single=20 events are sometimes the result of more than one = cell, then=20 the possibility remains that the = PNAhi-expressing=20 cells (which comprise the vast majority of cells) are = contaminating the cultures of Rietze et al. (2001) and giving rise to = neurospheres.=20

We also observed a difference between the embryonic and = adult=20 enrichment profiles when examining SP cells on the basis = of=20 LeX/ssea-1 expression. LeX+ is a carbohydrate = moiety=20 highly expressed on pluripotent stem cells (Solter = and=20 Knowles, 1978) and has recently been = shown to be=20 expressed in adult subventricular zone cells, = including stem=20 cells (Capela and Temple, 20023DGo). We observed a further = enrichment=20 among SP cells in the LeX+ fraction from = both=20 embryonic- and adult-derived neurosphere cells. The=20 enrichment was enhanced to a greater extent in the = embryonic=20 than in the adult SP-LeX+ fraction. In general, = less=20 neural stem cell enrichment was achieved from adult=20 neurosphere cells than from embryonic neurosphere = cells. One=20 possibility is that adult neural stem cells are a = less=20 homogenous population of cells relative to embryonic = cells or=20 there are age-related differences among stem cell=20 populations. Further support for age-related changes = in=20 neural stem cells comes from studies examining the = relative=20 frequencies of neurosphere-forming cells at various = ages of=20 development (ranging from embryonic day 10.5 to = adult) using=20 the parameters of cell size, granularity, nestin-enhanced=20 green fluorescent protein expression, Notch1 expression, = and=20 cell adhesion molecules such as E-NCAM (Kawaguchi et al., = 20013DGo; Cai et al., 20023DGo; Murayama et al., 2002). Similarly, these studies = concluded=20 that the characteristics of neural stem cells were = not=20 uniform and changed through development.

The substrate responsible for the efflux of Hoechst dye in=20 hematopoietic stem cells is the ABC transporter = Bcrp1/ABCG2=20 (Zhou et al., 2001). Bcrp1/ABCG2 is expressed in a wide = variety of=20 stem cells and was suggested as the molecular basis = for the=20 SP phenotype isolated from bone marrow and skeletal = muscle=20 (Zhou et al., 2001). Contrary to the results from the = hematopoietic=20 system, there is no evidence that neural stem cells = express=20 Bcrp1/ABCG2 in the adult. Indeed, the fact that = embryonic SP=20 (and not adult SP) expresses the protein further = supports the=20 hypothesis that there are age-related changes among = neural=20 stem cells. These data suggest that although = differential dye=20 efflux can be used to isolate neural stem cells, the = protein=20 involved is not Bcrp1/ABCG2.

It has been shown that GFAP-expressing cells in the adult=20 subventricular zone give rise to neurospheres in = vitro=20 (Doetsch et al., 19993DGo; Morshead et al., 2003); therefore, a strong prediction is = that=20 the SP fraction will contain GFAP-expressing cells. = Indeed,=20 we detected GFAP expression within the SP using RT-PCR.=20 Interestingly, Rietze et al. (2001) were unable to detect GFAP in their = isolated=20 neural stem cell population; however, the authors suggest=20 that their method of detection was relatively = insensitive=20 (using an adenoviral vector expressing green = fluorescent=20 protein under the control of a GFAP promoter). The=20 observation that GFAP is found within the SP fraction = is=20 consistent with the fact that neurospheres arise from = this=20 fraction; however, GFAP was also detected in the = non-SP=20 fraction (composed of progenitor cells) using RT-PCR. = Taken=20 together, these results suggest that GFAP is not a = good=20 selection marker for neural stem cells.

Overall, the Hoechst dye exclusion protocol is a quick,=20 efficient, and reliable technique to enrich for = neural stem=20 cells and, importantly, to obtain a virtually pure = population=20 of progenitor cells (the non-SP fraction). Combining = the=20 side-population analysis with markers shown recently = to=20 enrich for neural stem cells afforded no further = enrichment=20 in the case of PNA expression and size criterion = (Rietze et=20 al., 2001); however, combining the=20 side-population analysis with LeX expression resulted in = a=20 slight enrichment over side-population analysis alone. = Although=20 the dye exclusion protocol is able to enrich for stem = cells=20 from primary tissue, the number of stem cells that are=20 isolated is restrictively low; hence the use of = neurospheres=20 as a starting population is beneficial because the = neural=20 stem cells have already undergone symmetric divisions = during=20 neurosphere formation, thereby increasing their = numbers.=20 Furthermore, differential dye efflux can be used to = isolate=20 stem cells from various tissues, suggesting that the=20 conserved SP phenotype may represent a common feature = of stem=20 cells in general. Interestingly, our data suggest = that this=20 common mechanism of dye efflux is mediated by different=20 members of the ABC transport family in a tissue- and=20 age-dependent manner.


   Footnotes=20
 
Received Aug 13, = 2003;=20 revised September 29, 2003; accepted October 1, 2003.

This work was supported by = operating=20 grants to C.M.M. from the E. A. Baker Foundation and = the=20 Canadian Institutes of Health Research. We thank = Derek van=20 der Kooy for his support and insightful = comments.

Correspondence should be = addressed to=20 Cindi M. Morshead, 1 King's College Circle, Room = 1182,=20 Toronto, Ontario, Canada M5S 1A8. E-mail: cindi.morshead{at}utoronto.ca .

Copyright =A9 2003 Society for = Neuroscience=20 0270-6474/03/2310703-07$15.00/0


   References =
Top
Abstract
3D"Introduction
3D"Materials and Methods
3D"Results
3D"Discussion
3D"References
&nb= sp;

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L. Patrawala, T. Calhoun, = R.=20 Schneider-Broussard, J. Zhou, K. Claypool, and D. G.=20 Tang
Side Population Is Enriched in = Tumorigenic,=20 Stem-Like Cancer Cells, whereas ABCG2+ and ABCG2- Cancer = Cells Are=20 Similarly Tumorigenic
Cancer Res.,=20 July 15, 2005; 65(14): 6207 - 6219.
[Abstract]=20 [F= ull=20 Text] [PDF]=20
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M. T. Budak, O. S. = Alpdogan, M. Zhou,=20 R. M. Lavker, M.A. M. Akinci, and J. M. = Wolosin
Ocular=20 surface epithelia contain ABCG2-dependent side population = cells=20 exhibiting features associated with stem = cells
J. Cell=20 Sci., April 15, 2005; 118(8): 1715 - 1724. =
[Abstr= act]=20 [Full=20 Text] [PDF]=20
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Opera = requires=0A= the Sun Java Runtime Environment .=0A= =0A= by Andrew Gregory=0A= http://www.scss.com.au/family/andrew/webdesign/xmlhttprequest/=0A= =0A= This work is licensed under the Creative Commons Attribution License. To = view a=0A= copy of this license, visit = http://creativecommons.org/licenses/by-sa/2.5/ or=0A= send a letter to Creative Commons, 559 Nathan Abbott Way, Stanford, = California=0A= 94305, USA.=0A= =0A= Attribution: Leave my name and web address in this script intact.=0A= =0A= Not Supported in Opera=0A= ----------------------=0A= * user/password authentication=0A= * responseXML data member=0A= =0A= Not Fully Supported in Opera=0A= ----------------------------=0A= * async requests=0A= * abort()=0A= * getAllResponseHeaders(), getAllResponseHeader(header)=0A= =0A= */=0A= // IE support=0A= if (window.ActiveXObject && !window.XMLHttpRequest) {=0A= window.XMLHttpRequest =3D function() {=0A= var msxmls =3D new Array(=0A= 'Msxml2.XMLHTTP.5.0',=0A= 'Msxml2.XMLHTTP.4.0',=0A= 'Msxml2.XMLHTTP.3.0',=0A= 'Msxml2.XMLHTTP',=0A= 'Microsoft.XMLHTTP');=0A= for (var i =3D 0; i < msxmls.length; i++) {=0A= try {=0A= return new ActiveXObject(msxmls[i]);=0A= } catch (e) {=0A= }=0A= }=0A= return null;=0A= };=0A= }=0A= // Gecko support=0A= /* ;-) */=0A= // Opera support=0A= if (window.opera && !window.XMLHttpRequest) {=0A= window.XMLHttpRequest =3D function() {=0A= this.readyState =3D 0; // = 0=3Duninitialized,1=3Dloading,2=3Dloaded,3=3Dinteractive,4=3Dcomplete=0A= this.status =3D 0; // HTTP status codes=0A= this.statusText =3D '';=0A= this._headers =3D [];=0A= this._aborted =3D false;=0A= this._async =3D true;=0A= this._defaultCharset =3D 'ISO-8859-1';=0A= this._getCharset =3D function() {=0A= var charset =3D _defaultCharset;=0A= var contentType =3D = this.getResponseHeader('Content-type').toUpperCase();=0A= val =3D contentType.indexOf('CHARSET=3D');=0A= if (val !=3D -1) {=0A= charset =3D contentType.substring(val);=0A= }=0A= val =3D charset.indexOf(';');=0A= if (val !=3D -1) {=0A= charset =3D charset.substring(0, val);=0A= }=0A= val =3D charset.indexOf(',');=0A= if (val !=3D -1) {=0A= charset =3D charset.substring(0, val);=0A= }=0A= return charset;=0A= };=0A= this.abort =3D function() {=0A= this._aborted =3D true;=0A= };=0A= this.getAllResponseHeaders =3D function() {=0A= return this.getAllResponseHeader('*');=0A= };=0A= this.getAllResponseHeader =3D function(header) {=0A= var ret =3D '';=0A= for (var i =3D 0; i < this._headers.length; i++) {=0A= if (header =3D=3D '*' || this._headers[i].h =3D=3D header) {=0A= ret +=3D this._headers[i].h + ': ' + this._headers[i].v + '\n';=0A= }=0A= }=0A= return ret;=0A= };=0A= this.getResponseHeader =3D function(header) {=0A= var ret =3D getAllResponseHeader(header);=0A= var i =3D ret.indexOf('\n');=0A= if (i !=3D -1) {=0A= ret =3D ret.substring(0, i);=0A= }=0A= return ret;=0A= };=0A= this.setRequestHeader =3D function(header, value) {=0A= this._headers[this._headers.length] =3D {h:header, v:value};=0A= };=0A= this.open =3D function(method, url, async, user, password) {=0A= this.method =3D method;=0A= this.url =3D url;=0A= this._async =3D true;=0A= this._aborted =3D false;=0A= this._headers =3D [];=0A= if (arguments.length >=3D 3) {=0A= this._async =3D async;=0A= }=0A= if (arguments.length > 3) {=0A= opera.postError('XMLHttpRequest.open() - user/password not = supported');=0A= }=0A= this.readyState =3D 1;=0A= if (this.onreadystatechange) {=0A= this.onreadystatechange();=0A= }=0A= };=0A= this.send =3D function(data) {=0A= if (!navigator.javaEnabled()) {=0A= alert("XMLHttpRequest.send() - Java must be installed and = enabled.");=0A= return;=0A= }=0A= if (this._async) {=0A= setTimeout(this._sendasync, 0, this, data);=0A= // this is not really asynchronous and won't execute until the = current=0A= // execution context ends=0A= } else {=0A= this._sendsync(data);=0A= }=0A= }=0A= this._sendasync =3D function(req, data) {=0A= if (!req._aborted) {=0A= req._sendsync(data);=0A= }=0A= };=0A= this._sendsync =3D function(data) {=0A= this.readyState =3D 2;=0A= if (this.onreadystatechange) {=0A= this.onreadystatechange();=0A= }=0A= // open connection=0A= var url =3D new java.net.URL(new = java.net.URL(window.location.href), this.url);=0A= var conn =3D url.openConnection();=0A= for (var i =3D 0; i < this._headers.length; i++) {=0A= conn.setRequestProperty(this._headers[i].h, this._headers[i].v);=0A= }=0A= this._headers =3D [];=0A= if (this.method =3D=3D 'POST') {=0A= // POST data=0A= conn.setDoOutput(true);=0A= var wr =3D new = java.io.OutputStreamWriter(conn.getOutputStream(), this._getCharset());=0A= wr.write(data);=0A= wr.flush();=0A= wr.close();=0A= }=0A= // read response headers=0A= // NOTE: the getHeaderField() methods always return nulls for me :(=0A= var gotContentEncoding =3D false;=0A= var gotContentLength =3D false;=0A= var gotContentType =3D false;=0A= var gotDate =3D false;=0A= var gotExpiration =3D false;=0A= var gotLastModified =3D false;=0A= for (var i =3D 0; ; i++) {=0A= var hdrName =3D conn.getHeaderFieldKey(i);=0A= var hdrValue =3D conn.getHeaderField(i);=0A= if (hdrName =3D=3D null && hdrValue =3D=3D null) {=0A= break;=0A= }=0A= if (hdrName !=3D null) {=0A= this._headers[this._headers.length] =3D {h:hdrName, = v:hdrValue};=0A= switch (hdrName.toLowerCase()) {=0A= case 'content-encoding': gotContentEncoding =3D true; break;=0A= case 'content-length' : gotContentLength =3D true; break;=0A= case 'content-type' : gotContentType =3D true; break;=0A= case 'date' : gotDate =3D true; break;=0A= case 'expires' : gotExpiration =3D true; break;=0A= case 'last-modified' : gotLastModified =3D true; break;=0A= }=0A= }=0A= }=0A= // try to fill in any missing header information=0A= var val;=0A= val =3D conn.getContentEncoding();=0A= if (val !=3D null && !gotContentEncoding) = this._headers[this._headers.length] =3D {h:'Content-encoding', v:val};=0A= val =3D conn.getContentLength();=0A= if (val !=3D -1 && !gotContentLength) = this._headers[this._headers.length] =3D {h:'Content-length', v:val};=0A= val =3D conn.getContentType();=0A= if (val !=3D null && !gotContentType) = this._headers[this._headers.length] =3D {h:'Content-type', v:val};=0A= val =3D conn.getDate();=0A= if (val !=3D 0 && !gotDate) this._headers[this._headers.length] = =3D {h:'Date', v:(new Date(val)).toUTCString()};=0A= val =3D conn.getExpiration();=0A= if (val !=3D 0 && !gotExpiration) = this._headers[this._headers.length] =3D {h:'Expires', v:(new = Date(val)).toUTCString()};=0A= val =3D conn.getLastModified();=0A= if (val !=3D 0 && !gotLastModified) = this._headers[this._headers.length] =3D {h:'Last-modified', v:(new = Date(val)).toUTCString()};=0A= // read response data=0A= var reqdata =3D '';=0A= var stream =3D conn.getInputStream();=0A= if (stream) {=0A= var reader =3D new java.io.BufferedReader(new = java.io.InputStreamReader(stream, this._getCharset()));=0A= var line;=0A= while ((line =3D reader.readLine()) !=3D null) {=0A= if (this.readyState =3D=3D 2) {=0A= this.readyState =3D 3;=0A= if (this.onreadystatechange) {=0A= this.onreadystatechange();=0A= }=0A= }=0A= reqdata +=3D line + '\n';=0A= }=0A= reader.close();=0A= this.status =3D 200;=0A= this.statusText =3D 'OK';=0A= this.responseText =3D reqdata;=0A= this.readyState =3D 4;=0A= if (this.onreadystatechange) {=0A= this.onreadystatechange();=0A= }=0A= if (this.onload) {=0A= this.onload();=0A= }=0A= } else {=0A= // error=0A= this.status =3D 404;=0A= this.statusText =3D 'Not Found';=0A= this.responseText =3D '';=0A= this.readyState =3D 4;=0A= if (this.onreadystatechange) {=0A= this.onreadystatechange();=0A= }=0A= if (this.onerror) {=0A= this.onerror();=0A= }=0A= }=0A= };=0A= };=0A= }=0A= // ActiveXObject emulation=0A= if (!window.ActiveXObject && window.XMLHttpRequest) {=0A= window.ActiveXObject =3D function(type) {=0A= switch (type.toLowerCase()) {=0A= case 'microsoft.xmlhttp':=0A= case 'msxml2.xmlhttp':=0A= case 'msxml2.xmlhttp.3.0':=0A= case 'msxml2.xmlhttp.4.0':=0A= case 'msxml2.xmlhttp.5.0':=0A= return new XMLHttpRequest();=0A= }=0A= return null;=0A= };=0A= }=0A= ------=_NextPart_000_008E_01CA605E.BBAC6430 Content-Type: application/octet-stream Content-Transfer-Encoding: quoted-printable Content-Location: http://www.jneurosci.org/javascript/ajax/utility.js /************************************************************************= *****=0A= * javascript/ajax/utility.js=0A= *=0A= * Utility functions for working with XMLHttpRequest data.=0A= *=0A= * Copyright 2006 Board of Trustees of the Leland Stanford Junior = University.=0A= = *************************************************************************= ***/=0A= =0A= /*=0A= * Copy XML nodes into an HTMLElement. This effectively=0A= * clones XML markup which uses XHTML naming conventions=0A= * into an HTML DOM.=0A= */=0A= function copy_xml_to_html(src, dst) {=0A= if (src.nodeType =3D=3D 1) { /* Node.ELEMENT_NODE */=0A= var e =3D document.createElement(src.nodeName);=0A= for (var i =3D 0; i < src.childNodes.length; i++) {=0A= copy_xml_to_html(src.childNodes[i], e);=0A= }=0A= for (var i =3D 0; i < src.attributes.length; i++) {=0A= var n =3D src.attributes[i].name;=0A= var v =3D unescape_xml_string(src.attributes[i].value); =0A= e.setAttribute(n, v);=0A= if (n =3D=3D "class") {=0A= e.className =3D v;=0A= }=0A= else if (n =3D=3D "style") {=0A= set_css_style(v, e, "");=0A= }=0A= }=0A= dst.