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The Journal of=20 Neuroscience, November 15, 2006, 26(46):12089-12099;=20 doi:10.1523/JNEUROSCI.3047-06.2006

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Development/Plasticity/Repair
Leukemia Inhibitory Factor Promotes Neural Stem Cell = Self-Renewal in the=20 Adult Brain

Sylvian Bauer and Paul = H.=20 Patterson

Biology Division, California Institute of Technology, Pasadena, = California=20 91125=20


3D"   =20 Abstract
Top
3D"Abstract
3D"Introduction
3D"Materials and Methods
3D"Results
3D"Discussion
3D"References
 
A= lthough=20 neural stem cells (NSCs) persist in various areas of the = adult brain,=20 their contribution to brain repair after injury is very = limited.=20 Treatment with exogenous growth factors can mitigate this = limitation,=20 suggesting that the brain environment is normally deficient = in=20 permissive cues and that it may be possible to stimulate the = latent=20 regenerative potential of endogenous progenitors with = appropriate=20 signals. We analyzed the effects of overexpressing the = cytokine=20 leukemia inhibitory factor (LIF) on adult neurogenesis in the = normal=20 brain. We found that LIF reduces neurogenesis in the = olfactory bulb=20 and subventricular zone by acting directly on NSCs. LIF = appears to=20 promote NSC self-renewal, preventing the emergence of more=20 differentiated cell types. This ultimately leads to an = expansion of=20 the NSC pool. Our results have implications for the = development of=20 therapeutic strategies for brain repair and suggest that LIF = may be=20 useful, in combination with other factors, in promoting=20 regeneration in the adult brain.

Key words: IL-6; CNTF; adult neurogenesis; stem cell = niche;=20 brain repair; IdU; CldU


3D"   =20 Introduction
Top
Abstract
3D"Introduction
3D"Materials and Methods
3D"Results
3D"Discussion
3D"References
 
T= he adult=20 brain contains multipotent neural stem cells (NSCs) and = committed=20 progenitors that participate in brain repair, albeit to a = very=20 limited extent (Magavi et al., 20003DGo;=20 Arvidsson et al., 20023DGo;=20 Nakatomi et al., 20023DGo).=20 It may be possible to stimulate brain repair from endogenous=20 precursors in the injured brain by finding conditions that = will=20 unleash and channel this dormant potential.

Many types of injuries to the nervous system are accompanied = by a=20 rapid and transient increased expression of leukemia inhibitory=20 factor (LIF) (Banner and Patterson, 19943DGo;=20 Banner et al., 19973DGo; Jankowsky and Patterson, 19993DGo;=20 Suzuki et al., 20003DGo;=20 Minami et al., 20023DGo;=20 Bauer et al., 20033DGo;=20 Sriram et al., 20043DGo).=20 In this context, LIF is known to regulate neuronal phenotype = (Rao=20 et al., 19933DGo;=20 Corness et al., 19963DGo;=20 Sun and Zigmond, 19963DGo;=20 Holmberg and Patterson, 20063DGo)=20 and coordinate the astrocyte, oligodendrocyte, microglia, and = inflammatory cell responses (Sugiura et al., 20003DGo;=20 Kerr and Patterson, 20043DGo,=20 2005; Holmberg and Patterson, 20063DGo).=20 Importantly, LIF is required for the lesion-induced proliferation = of=20 neuronal progenitors in the regenerating adult olfactory = epithelium=20 (Bauer et al., 20033DGo),=20 suggesting that LIF may promote neurogenesis after other = types of=20 injury.

LIF is a member of the cytokine family that signals through = the=20 heterodimeric glycoprotein 130 (gp130)/LIF receptor (LIFR) = complex,=20 which also includes ciliary neurotrophic factor (CNTF), = interleukin=20 (IL)-6, IL-11, OSM (oncostatin M), CT-1 (cardiotrophin-1), = and=20 CLC/NNT-1 (cardiotrophin-like cytokine/novel neurotrophin-1)=20 (Heinrich et al., 20033DGo).=20 LIF signaling activates the Jak (Janus kinase)/STAT (signal=20 transducer and activator of transcription) and MAP = (mitogen-activated=20 protein) kinase pathways, which promote astrogliogenesis = in=20 vitro (Bonni et al., 19973DGo;=20 Molne et al., 20003DGo;=20 Viti et al., 20033DGo;=20 Chang et al., 20043DGo;=20 Barnabe-Heider et al., 20053DGo;=20 He et al., 20053DGo).=20 In addition, LIF is well known for promoting mouse embryonic = stem=20 (ES) cell self-renewal (Williams et al., 19883DGo)=20 and the long-term growth of embryonic human NSCs in culture = (Wright=20 et al., 20033DGo).=20 Other reports indicate that LIF signaling supports the=20 maintenance/self-renewal of cultured mouse embryonic NSCs = (Shimazaki=20 et al., 20013DGo;=20 Pitman et al., 20043DGo;=20 Bonaguidi et al., 20053DGo;=20 Gregg and Weiss, 20053DGo),=20 possibly by activating Notch signaling (Chojnacki et al., = 20033DGo).=20 However, little is known about the influence of LIF signaling = on=20 NSCs and neurogenesis in vivo: gp130 regulates = cell-cycle=20 reentry of embryonic cortical progenitors (Hatta et al., = 20023DGo),=20 and exogenous CNTF enhances neurogenesis in the adult brain=20 (Emsley and Hagg, 20033DGo;=20 Kokoeva et al., 20053DGo).

To clarify the effects of LIF on NSCs and neurogenesis in = vivo,=20 we overexpressed LIF in the uninjured, adult mouse forebrain. = In contrast to CNTF (Emsley and Hagg, 20033DGo;=20 Kokoeva et al., 20053DGo),=20 we find that exogenous LIF reduces neurogenesis in the = subventricular=20 zone (SVZ)/olfactory bulb (OB) system. This is attributable, = in part,=20 to a direct effect of LIF on adult NSCs: LIF maintains them = in a loop=20 of symmetric/self-renewing divisions in vivo, which = prevents=20 the emergence of more differentiated progeny. LIF ultimately=20 increases the pool of NSCs, which could be exploited to = accelerate=20 the regeneration of the SVZ. Our data suggest that LIF may be = useful=20 for cell replacement in situ.


3D"   =20 Materials and Methods
Top
Abstract
3D"Introduction
3D"Materials and Methods
3D"Results
3D"Discussion
3D"References
 
<= FONT=20 size=3D-1>Animals. We used adult male C57BL/6J mice of = various=20 ages. In the first experiment, 16-month-old animals were = obtained=20 from the National Institute on Aging and our own breeding = colonies=20 and were injected with recombinant adenoviruses (see below). = All=20 other experiments were performed on 2- to 6-month-old animals = obtained from The Jackson Laboratory (Bar Harbor, ME). All=20 experiments were approved by the California Institute of = Technology=20 Institutional Animal Care and Use Committee.

Bromodeoxyuridine. Bromodeoxyuridine = (BrdU;=20 Sigma, St. Louis, MO) was dissolved in 0.9% NaCl, sterile = filtered,=20 and injected intraperitoneally (100 mg/kg) according to the = protocols=20 indicated below.

Adenovirus injection. Recombinant = adenoviruses=20 (3D{approx}2.7 x 106 pfu in 3 =B5l of = sterile=20 PBS) encoding LacZ (Ad:LacZ) or LIF (Ad:LIF) (Zhu et al., 20013DGo) were injected into the right lateral = ventricle (=960.1=20 mm anteroposterior relative to bregma, 0.9 mm lateral from = the=20 midline, and 2.5 mm below the dura) using a 5 =B5l Hamilton=20 syringe attached to a 28-gauge needle. Injections were = performed=20 over 3=965 min, and the needle was left in place for another = 6=9610=20 min before withdrawal.

In the first experiment, mice were injected with Ad:LIF or = Ad:LacZ=20 (n =3D 5 per group) and received single BrdU injections for = 7=20 d, starting 2 weeks after adenovirus injection. These mice = were=20 killed 2 weeks after the first BrdU injection (1 week after = the=20 last BrdU injection and 4 weeks after adenovirus injection).

Other mice were killed 3 weeks after adenovirus injection and = were=20 used to obtain SVZ-derived neurospheres or to assess long-term,=20 label-retaining cells in the SVZ (see below).

Retrovirus production and injections. = A=20 replication-incompetent green fluorescent protein (GFP) retrovirus, = pseudotyped with vesicular stomatitis virus glycoprotein G = (VSV-G),=20 was produced according to published methods. Human embryonic=20 kidney 293 (HEK293) cells were transiently transfected with=20 plasmids containing gag-pol and vsv-g under the = control of=20 the cytomegalovirus (CMV) promoter, and the virus plasmid = (pNIT)=20 containing long terminal repeat-driven GFP (a gift from F. H. = Gage, The Salk Institute, San Diego, CA), using Polyfect = (Qiagen,=20 Valencia, CA). Medium containing viral particles was = collected=20 40 and 64 h after transfection and centrifuged each day at = 50,000=20 x g for 2 h at 4=B0C = (Beckman=20 centrifuge model L8-M, rotor SW-28; Beckman Coulter, = Fullerton, CA).=20 Pellets obtained after each centrifugation were resuspended = in=20 sterile PBS, mixed together, and centrifuged again. The final = pellet=20 was resuspended in 200 =B5l of sterile PBS (concentrated by a = factor of=20 1800), aliquoted, and stored at =9680=B0C. Titer was = determined=20 to be >1 x 107 = cfu=20 (colony-forming units)/ml using HEK293 cells.

The GFP retrovirus was injected bilaterally into the SVZ of=20 2-month-old mice. Three injections of 400 nl each were = performed=20 per SVZ using a 1 =B5l Hamilton syringe attached to a beveled = glass micropipette (3D{approx}=2014 =B5m inner = diameter) at the=20 following coordinates [anterior relative to bregma, lateral, = depth=20 below the dura (in mm)]: 0, 2, 2; 0.5, 1.2, 2.2; and 1,1, 2.=20 Immediately after the injection of the GFP retrovirus, = animals=20 received an injection of Ad:LIF or Ad:LacZ (n =3D 2 in = each=20 group) into the right lateral ventricle.

SVZ regeneration. Cytosine-3Dbeta=20-D-arabinofuranoside (AraC; 2%; Sigma) in saline = was=20 infused for 6 d into the lateral ventricle (same coordinates = as=20 for adenovirus injection) using osmotic mini-pumps (model = 1007D,=20 Alzet; Durect<= /A>,=20 Cupertino, CA) implanted subcutaneously on the back of the = animals=20 and connected to a brain infusion kit 2 or 3 cannula = (Alzet).=20

Recombinant mouse LIF protein (Millipore, Billerica, MA), human=20 epidermal growth factor (EGF; Invitrogen, Carlsbad, CA), or = PBS=20 [with or without bovine serum albumin (BSA)] were infused = before or=20 after AraC using mini-pump model 1003D (for 1 and 3 d; 1 = =B5l/h) or=20 1007D (for 7 d; 0.5 =B5l/h; Alzet). Mini-pumps were filled = with LIF=20 protein diluted in PBS (5 =B5g/ml), resulting in the delivery = of 60 or=20 120 ng of LIF per day (for pump models 1007D and 1003D,=20 respectively). EGF (16.67 =B5g/ml) was dissolved in PBS = containing 0.1%=20 BSA and infused at 400 ng/d, similar to other studies = (Shimazaki et=20 al., 20013DGo;=20 Doetsch et al., 20023DGo).

Mice (n =3D 3 per group and per experiment) were killed at = 1,=20 3, or 7 d after AraC removal, 1=962 h after a single BrdU=20 injection.

Double nucleoside administration. = Mice (2=20 months of age) were given iododeoxyuridine (IdU) or=20 chlorodeoxyuridine (CldU) (both from Sigma) in their drinking = water (1 mg/ml), supplemented with 2.5% sucrose. The solution = was made fresh and changed daily.

IdU was administered first for 2 weeks, followed by 1 week with=20 regular water containing no marker. Animals were then = injected=20 with Ad:LIF or Ad:LacZ in the lateral ventricle (n =3D 3 = per=20 group) and treated on the following day with CldU for another = 2=20 weeks. Animals were perfused after 1 more week with regular = water=20 containing no marker (i.e., a total of 4 weeks after the end = of IdU=20 treatment). All animals drank similar amounts of water = throughout the=20 treatment period (an average of 5.5 ml/d).

Tissue processing and histology. = Animals were=20 perfused transcardially with 0.1 M phosphate = buffer=20 (PB), pH 7.5, followed by fresh, cold 4% paraformaldehyde in=20 PB. Brains were dissected and fixed another 3=965 h at 4=B0C, = washed overnight in PB at 4=B0C, and immersed overnight at = 4=B0C in=20 PB containing 20% sucrose. Brains were then embedded in = freezing=20 media (optimum cutting temperature), frozen in chilled = isopentane=20 (=9625=B0C), and stored at =9680=B0C until sectioning. =

Coronal brain sections (14 =B5m) were collected on Superfrost = Plus=20 slides (Fisher Scientific, Pittsburgh, PA) using a cryostat = (model=20 CM3050; Leica Microsystems, Bannockburn, IL) and dried = overnight at=20 room temperature before being stored at =9620=B0C.

Immunohistochemical staining was performed according to standard = procedures. Staining for BrdU and double staining for IdU and = CldU were as described previously (Bauer and Patterson, 20053DGo). The primary antibodies used were mouse = anti-NeuN=20 (Millipore), mouse anti-Ki67 and anti-mammalian achaete-scute = homolog=20 1 (Mash1) (both from BD Biosciences PharMingen, San Jose, = CA),=20 rabbit anti-LIFR and goat anti-doublecortin (Dcx) (both from=20 Santa Cruz Biotechnology, Santa Cruz, CA), sheep anti-EGF=20 receptor (EGFR; Millipore), rabbit anti-GFP (Invitrogen), = rabbit=20 anti-S100 (Dako, Carpinteria, CA), rabbit anti-phosphorylated = Stat3=20 (Y705; Cell Signaling Technology, Beverly, MA), goat = anti-Olig2=20 (R & D Systems, Minneapolis, MN), and rat or mouse = anti-BrdU=20 (Oxford Biotechnology, Oxfordshire, UK and BD Biosciences = PharMingen,=20 respectively). Species-specific secondary antibodies = conjugated=20 to Alexa 488, 568, or 633 were from Invitrogen.

Quantification and image analysis. = Staining was=20 analyzed with a Nikon (Tokyo, Japan) microscope (model = Diaphot 300)=20 and an LSM510 confocal microscope (Zeiss, Thornwood, NY) = equipped=20 with an argon/krypton laser (488 nm), two helium/neon lasers = (543 and=20 633 nm), and a Coherent (Santa Clara, CA) Chameleon = two-photon laser=20 [used at 725 nm to image DAPI (4',6'-diamidino-2-phenylindole = dihydrochloride) staining]. Pictures were obtained with a = Spot RT=20 Slider camera and associated software (version 3.4; = Diagnostic=20 Instruments, Sterling Heights, MI) or with the LSM software = (Zeiss).=20 Colocalizations were investigated by performing = z-stack=20 acquisitions and three-dimensional reconstructions. Adobe = Photoshop=20 version 7.0.1 (Adobe Systems, San Jose, CA) was used to = adjust=20 contrast and brightness.

Sections sampled at similar anatomical levels of the OB or the = SVZ=20 (between +0.3 and +0.7 mm anterior relative to bregma) were = processed=20 at the same time for each type of staining. Quantification = was=20 performed at the confocal microscope or with the Nikon microscope=20 using a 40x or an = oil-immersion 63x objective. Single and = double-labeled=20 cells were hand scored in various structures of interest by = an=20 observer blind to the treatment of the animals. Cells were = quantified=20 on two to six equally spaced (42 =B5m) sections per animal. = Cell=20 numbers are expressed as mean =B1 SEM per section for each = structure=20 (no difference in the size of the OB or SVZ was observed = between=20 animals from different experimental groups).

For image analysis of the Dcx and GFP staining, black-and-white=20 pictures of three to four equally spaced (42 =B5m) sections = per=20 animal were taken with the Nikon microscope using constant = settings=20 across various animals from the same experiment. Image = analysis was=20 performed using the NIH ImageJ software (version 1.34s) by=20 quantifying the staining area after adjusting the threshold = manually.=20 Results are expressed as mean =B1 SEM pixel2 per=20 section.

Neurosphere cultures and = quantification.=20 Neurospheres were obtained from micro-dissected adult mouse = SVZ=20 (Doetsch et al., 1999a3DGo).=20 SVZ fragments were digested in papain (Sigma) and trypsin=20 (Invitrogen) solution for 20 min at 37=B0C and mechanically = dissociated=20 by passing through a 26-gauge needle (Charrier et al., 20063DGo).=20 Single cells were seeded at 10 cells per microliter in = 24-well plates=20 (500 microliters per well) in serum-free media consisting of = DMEM=20 supplemented with B27, penicillin/streptomycin, 20 ng/ml EGF = with or=20 without 10 ng/ml basic fibroblast growth factor (FGF) (all = from=20 Invitrogen), and sodium pyruvate (Sigma).

After 6=969 d in cultures, spheres were collected, incubated = in=20 TripLE Express (Invitrogen) for 30=9660 min at 37=B0C, = mechanically=20 dissociated, and reseeded as single cells as described above. = Experiments involving single cells or neurospheres exposed to = LIF (20=20 ng/ml) were performed after four or more passages.

In each experiment, neurospheres were quantified in three to = six=20 wells and further classified according to their size (3D≥100 = =B5m diameter).=20 Results are presented as mean =B1 SEM neurospheres per well = (i.e., per=20 5000 cells). Each experiment was repeated at least three = times.=20

Statistics. Statistics were performed = using the=20 unpaired Student's t test. Results are considered = significant=20 when the p value is <0.05.

Online supple= mental=20 material. Supplemental Figure S1 illustrates the = bioactivity of=20 virally overexpressed LIF, assessed by phosphorylated Stat3=20 (pStat3) staining. Supplemental Figure S2 shows expression of = LIFR=20 on various SVZ cell types. Supplemental Figure S3 offers a=20 comparison between the in vitro and in vivo = effects of=20 LIF. The supple= mental=20 material is available at http://www.jneurosci.org/. =


3D"   =20 Results
Top
Abstract
3D"Introduction
3D"Materials and Methods
3D"Results
3D"Discussion
3D"References
 
<= STRONG>LIF=20 reduces neurogenesis in the OB
We focused our study on the = SVZ, a=20 well described system that generates neurons in the OB (for = review,=20 see Doetsch, 20033DGo). The SVZ contains NSCs, the type B cells = that express=20 the astrocyte marker glial fibrillary acidic protein (GFAP) = (Doetsch=20 et al., 1999a3DGo;=20 Garcia et al., 20043DGo),=20 the immediate progeny of which are the transit-amplifying, = type C=20 cells. Type C cells divide rapidly and generate neuroblasts, = the type=20 A cells, which migrate toward the OB (Doetsch et al., 19973DGo).

To investigate the effects of overexpressing LIF on adult NSCs = and=20 neurogenesis, adult mice were injected in the lateral ventricle = with=20 an adenovirus encoding a secreted form of LIF (Ad:LIF) or = -galactosidase=20 (Ad:LacZ) as a control (Zhu et al., 20013DGo). Two weeks after virus inoculation, mice = received=20 daily intraperitoneal injections of BrdU for 7 d and were = killed 1=20 week later (2 weeks after the first BrdU injection). =

Adenoviruses efficiently infect ependymal cells when injected = into=20 the lateral ventricle (Doetsch et al., 1999a3DGo).=20 Accordingly, we found that LIF or X-Gal=20 (5-bromo-4-chloro-3-indolyl-3Dbeta=20-D-galactopyranoside) staining is confined to = ependymal=20 cells (data not shown). To confirm LIF activity in = vivo, we=20 performed pStat3 staining. Staining is abundant and localized = to cell=20 nuclei in Ad:LIF-treated animals, but not in Ad:LacZ-injected = controls (supplemental Fig. S1, available at http://www.jneurosci.org/ as supple= mental=20 material). pStat3 staining intensity appears stronger in = areas=20 immediately adjacent to the ventricle, whereas it decreases = farther=20 away from the ventricle in a gradient-like pattern, = suggesting=20 maximal LIF activity in and around the SVZ.

In the OB, BrdU+ cells, either single labeled or colabeled with=20 the mature neuronal marker NeuN, are mostly found in the = subependymal=20 and granule cell layers (Fig. = 1),=20 where newborn neurons are expected 1=962 weeks after being = generated.=20 Overexpression of LIF significantly reduces the number of = both=20 classes of cells in these anatomical layers, without = affecting the=20 percentage of newly generated neurons (Fig. = 1).=20 This suggests that LIF does not alter early neuronal = differentiation=20 or radial migration in the OB proper, but rather reduces the = number=20 of newly generated cells coming from the SVZ that reach the = OB. Thus,=20 LIF may act "upstream" of the OB by altering SVZ cell = fate.=20



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  		Figure 1. LIF = reduces=20 neurogenesis in the OB. A, Double staining for = BrdU=20 and the mature neuronal marker NeuN indicates that most = BrdU+ cells=20 are found in the two deepest anatomical layers of the OB: = the=20 subependymal layer (SEL) and the granule cell layer (GCL).=20 B, An example of colocalization between BrdU = and NeuN.=20 C, The number of BrdU+ cells, as well as the = number of=20 newly generated neurons (BrdU+/NeuN+), is reduced by = 41=9651% in=20 animals overexpressing LIF (Ad:LIF) compared with controls=20 (Ad:LacZ), whereas the percentage of newly generated neurons = is=20 unchanged (6.3 =B1 0.8 vs 7.2 =B1 0.9% and 25.0 =B1 1.4 vs = 23.5 =B1 1.4% in=20 Ad:LacZ- vs Ad:LIF-treated animals in the SEL and GCL, = respectively;=20 p =3D 0.2). Data are mean =B1 SEM of n =3D 5 = animals per=20 group (2=963 sections analyzed per animal). **p < = 0.01 and=20 ***p < 0.001 compared with Ad:LacZ-treated = controls=20 (Student's t test). Scale bars: A, 300 = =B5m;=20 B, 10 =B5m. RMS, Rostral migratory stream; = Gran, granule=20 cell layer. =

 = ;
LIF=20 impairs neuroblast formation in the SVZ
We first checked = whether=20 cell proliferation in the SVZ is altered by LIF = overexpression. In=20 Ad:LIF-treated mice, the number of cells labeled with BrdU or = with=20 the endogenous cell-cycle marker Ki67 is only one-half of = that in=20 controls (Fig. = 2),=20 indicating that exogenous LIF strongly reduces SVZ cell=20 proliferation. In contrast to the SVZ, other areas analyzed = at the=20 same anatomical level [i.e., the corpus callosum, striatum, = and=20 septum (hereafter referred to as periventricular areas)], as = well as=20 the cortex, all contain more Ki67+ or BrdU+ cells after LIF=20 overexpression (Fig.=20 2).



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  		Figure 2. LIF = reduces=20 cell proliferation in the SVZ. A, Double = staining for=20 BrdU and the endogenous cell-cycle marker Ki67 is shown on=20 representative sections from a control animal (Ad:LacZ) and = an=20 animal overexpressing LIF (Ad:LIF). CC, Corpus callosum; St, = striatum; LV, lateral ventricle. Note the highly organized = aspect of=20 the SVZ in the control animal compared with treatment with = Ad:LIF,=20 in which fewer labeled cells are seen in the SVZ, but more = in=20 periventricular areas. B, Higher magnification = of SVZ=20 cells double stained with BrdU and Ki67. C,=20 D, Quantification of BrdU+ (C) = and Ki67+=20 (D) cells is shown for various brain regions = at the=20 anatomical level analyzed (between +0.3 and +0.7 mm anterior = to=20 bregma). There is a 53=9655% reduction in both classes of = labeled=20 cells in the SVZ of Ad:LIF-treated animals. In contrast, LIF = overexpression triggers an increase in BrdU+ as well as = Ki67+ cells=20 in periventricular areas [CC, St, and septum (Sept)] and the = cortex=20 (Cx). Data are mean =B1 SEM of n =3D 5 animals per = group (2=963=20 sections analyzed per animal). *p < 0.05 and = ***p=20 < 0.001 compared with Ad:LacZ-treated controls (Student's = t test). Sept SVZ, The ependyma lining the septal = side of the=20 lateral ventricle. Scale bars: A, 150 =B5m;=20 B, 15 =B5m. =

 = ;
In=20 the SVZ, most of the proliferating cells correspond to neuroblasts=20 (type A) and transit-amplifying cells (type C) (Doetsch et = al.,=20 19973DGo).=20 In Ad:LIF-treated animals, Dcx-expressing neuroblasts (Brown = et al.,=20 2003) are virtually absent (Fig. = 3)=20 (image analysis of Dcx staining in the SVZ: 6334.80 =B1 = 309.89 vs=20 935.73 =B1 90.65 pixel2 in Ad:LacZ- vs = Ad:LIF-treated=20 animals; p < 0.001), and Mash1-expressing type C = cells (Fig. = 3)=20 (Parras et al., 20043DGo)=20 are greatly reduced (down 3D~70%; 57.80 =B1 4.39 vs 16.80 =B1 1.61 Mash1+ cells = in Ad:LacZ-=20 vs Ad:LIF-treated animals; p < 0.001), indicating = that LIF=20 overexpression depletes the SVZ of cells in the neuronal=20 lineage.



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  		Figure 3. LIF = reduces=20 neuronal differentiation in the SVZ, and LIFR is expressed = by some=20 SVZ astrocytes. A, Dcx-expressing neuroblasts = (type A=20 cells) are greatly reduced in the SVZ of animals treated = with Ad:LIF=20 (see Results for image analysis data). B, High = magnification of SVZ cells stained with Mash1, a marker of=20 transit-amplifying, type C cells. Note the mitosis (arrows = and=20 insets). C, LIFR immunoreactivity is detected = on some=20 GFAP-expressing astrocytes in the SVZ. Scale bars: = A,=20 200 =B5m; B, 30 =B5m (insets, 15 =B5m); = C, 15=20 =B5m. =

 = ;
To=20 better understand how LIF may be acting in the SVZ, we stained=20 sections from naive animals with LIFR antibodies. = Immunoreactivity=20 is detected in all SVZ cell types (supplemental Fig. S2, = available=20 at http://www.jneurosci.org/ as supple= mental=20 material), including some GFAP+ astrocytes (type B cells) = (Fig. = 3).=20 Thus, the previous data could be explained by several = different=20 mechanisms: LIF could directly (1) reduce the proliferation = or (2)=20 alter the fate of type A and C cells. It is also possible = that the=20 depletion of neuronal cells in the SVZ could be the = consequence of=20 (3) a direct effect of LIF on NSCs (type B), which would = prevent=20 the normal generation of NSC progeny, the type C and type A=20 cells.

LIF stimulates the proliferation of parenchymal glial = progenitors in=20 periventricular areas
LIF may promote glial cell fate at the = expense=20 of the neuronal lineage in vivo, as it does in = vitro=20 (Bonni et al., 19973DGo;=20 Chang et al., 20043DGo;=20 Barnabe-Heider et al., 20053DGo;=20 He et al., 20053DGo), which could explain the depletion of = neuronal cells=20 in the SVZ. Consistent with this hypothesis, phenotypic = analysis in=20 periventricular areas and the cortex of Ad:LIF-treated = animals=20 reveals a threefold to fivefold increase in BrdU+ cells = expressing=20 Olig2 or S100, two glial cell markers (Fig. = 4). No=20 newly generated Dcx+ neurons are found, indicating that LIF = does not=20 stimulate neurogenesis in these areas (data not shown). =



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  		Figure 4. LIF = promotes=20 the proliferation or formation of glial progenitors in=20 periventricular areas and in the SVZ. A,=20 B, Quantification of cells coexpressing BrdU = and S100=20 (A) or BrdU and Olig2 (B) = indicates that=20 LIF overexpression induces a threefold to fivefold increase = in the=20 number of these newly generated glial cells in all brain = regions=20 examined, including the SVZ. C, = D, A=20 GFP-replication-incompetent retrovirus was injected into the = SVZ=20 before treatment with Ad:LacZ (control) or Ad:LIF, and = brains were=20 examined 3 weeks after injection. C, A GFP+ = neuron in=20 the OB displays dendritic spines but lacks expression of the = immature neuron marker Dcx. D, Representative = OB=20 sections show that GFP+ cells are concentrated in the center = of the=20 OB and are reduced in animals treated with Ad:LIF (see = Results for=20 image analysis data). E, In the SVZ of = Ad:LIF-treated=20 animals, many cells that are double stained with BrdU and = S100 also=20 express GFAP, a marker of NSCs. Data are mean =B1 SEM of = n =3D 5=20 animals per group (2=963 sections analyzed per animal). = ***p=20 < 0.001 compared with Ad:LacZ-treated controls (Student's = t test). Sept SVZ, Ependyma lining the septal side of = the=20 lateral ventricle; Cx, cortex; CC, corpus callosum; LV, = lateral=20 ventricle; St, striatum; Sept, septum. Scale bars: = C,=20 50 =B5m; D, 300 =B5m; E, 10 = =B5m. =

 = ;
Interestingly,=20 BrdU+ cells appear to be distributed in a gradient-like = pattern=20 similar to the pStat3 staining, suggesting that LIF could = induce SVZ=20 cells to migrate out of the SVZ and invade periventricular = areas,=20 where they would adopt a glial phenotype. To check whether = BrdU+=20 cells are derived from the SVZ or from local, parenchymal=20 progenitors, we labeled SVZ cells and their progeny by = injecting a=20 GFP-replication-incompetent retrovirus in the SVZ before = treatment=20 with Ad:LIF or Ad:LacZ. Three weeks after virus injections, = GFP+=20 cells with the morphology and phenotype of immature neurons = were seen=20 in the OB of all animals (Fig.=20 4). However, no GFP+ cells were found in the striatum or=20 septum of either group of mice (data not shown), suggesting = that=20 cells derived from the SVZ do not migrate normally in these=20 areas and that LIF does not promote such ectopic migration. = The=20 corpus callosum in both Ad:LIF and Ad:LacZ mice contains some = GFP+ cells, likely because of the lesion induced at the time = of=20 virus injections. These results indicate that LIF-induced=20 proliferation in periventricular areas, mostly glial in = nature,=20 originates from parenchymal, "activated" glial progenitors = and not=20 from SVZ-derived cells, which suggests a reactive gliosis = that=20 could be attributable to the proinflammatory effects of LIF=20 (Sugiura et al., 20003DGo;=20 Kerr and Patterson, 20043DGo).=20 Thus, the reduction in SVZ progenitors and OB neurogenesis = cannot be=20 explained by an emigration or a change in cell fate of cells = from the=20 SVZ.

We also found that the number of GFP+ cells is reduced by 3D~=2060% = in the OB of=20 Ad:LIF-treated animals (Fig. = 4)=20 (image analysis of GFP staining in the OB: 1703.75 =B1 127.76 = vs=20 576.60 =B1 45.18 pixel2 in Ad:LacZ- vs = Ad:LIF-treated=20 animals; p < 0.001), consistent with and confirming = our=20 previous observations with BrdU and NeuN. Given that the GFP=20 retrovirus is likely infecting a majority of type C and A = cells when=20 injected into the SVZ, this result suggests that LIF is = acting=20 directly on these types of progenitors.

LIF impairs the amplification of type C cells and stimulates = the=20 formation of SVZ astrocytes
The above data indicate that the = depletion of neuronal cells observed in the SVZ after LIF=20 overexpression results from a deregulation of cell lineage=20 homeostasis that is spatially restricted to the SVZ. It is = possible=20 that LIF impairs the amplification of type C cells and the = transition=20 to type A cells. We studied self-renewal/cell cycle kinetics = in the=20 SVZ by analyzing Ki67/BrdU double staining using animals that = were=20 killed 1 week after the last BrdU injection. This 1 week = survival=20 allows most migrating BrdU+ neuroblasts to be cleared from = the SVZ=20 and reach the OB. Hence, BrdU+ cells that are left in the SVZ = and=20 that coexpress Ki67 correspond to self-renewing cells or to = cells=20 with a long cell cycle (>1 week; i.e., type C or type B = cells).=20 Given that the NSC fraction (B cells) is estimated to = represent=20 only 0.2=960.4% of the SVZ, and that C cells reside for 3D~=202 weeks = in the=20 SVZ (Morshead et al., 19983DGo),=20 the majority of the Ki67+/BrdU+ cells in our experiment = likely=20 correspond to self-renewing type C cells. LIF reduces the = number of=20 Ki67+/BrdU+ cells by 3D~50% (33.3 =B1 2.0 vs 17.5 =B1 2.2 Ki67+/BrdU+ = cells in=20 Ad:LacZ- vs Ad:LIF-treated animals; p < 0.001), = consistent=20 with the reduction of C cells observed with Mash1. Because = LIF=20 also reduces proliferation, an index of self-renewal was = calculated=20 by dividing the number of self-renewing cells (BrdU+/Ki67+) = by=20 the total number of BrdU+ cells. This ratio is significantly=20 decreased in the dorsolateral corner of the SVZ (14.6 =B1 = 2.1 vs=20 8.9 =B1 1.7% in Ad:LacZ- vs Ad:LIF-treated animals; p = =3D 0.02),=20 suggesting that LIF overexpression reduces type C cell=20 self-renewal.

It is also possible that LIF could act directly on NSCs, as=20 suggested by the localization of LIFR on SVZ GFAP+ cells (Fig.=20 3), and impair type C cell production. Interestingly, we = found=20 that the SVZ of Ad:LIF-treated animals contains fivefold more = Olig2+ or S100+ cells colabeled with BrdU compared with = controls (Fig.=20 4), indicating that the depletion of neuronal cells is=20 counterbalanced by an increased formation of glial cells.=20 Interestingly, Olig2 expression has recently been identified = in a=20 subset of type B cells and colocalizes with S100 in some SVZ = cells=20 (Menn et al., 20063DGo).=20 Most noteworthy, many S100+/BrdU+ cells in the SVZ of = Ad:LIF-treated=20 animals also express GFAP (Fig. = 4), a=20 marker of neural stem type B cells (Doetsch et al., 1999a3DGo;=20 Garcia et al., 20043DGo).=20 Thus, LIF appears to promote the proliferation or formation = of SVZ=20 astrocytes, at the expense of other SVZ cell types. These SVZ = astrocytes may correspond to differentiated astrocytes that = lose=20 their stem cell potential, which would be consistent with the = well=20 known astrocyte-promoting effect of LIF in vitro, or = to=20 putative NSCs. Either effect would decrease the formation of = type C=20 and type A cells and reduce subsequent OB neurogenesis. =

Infusion of LIF after AraC impairs SVZ regeneration in=20 vivo
To address the possibility that LIF directly = affects NSCs=20 in vivo, we examined how the SVZ regenerates in the = presence=20 of LIF, after infusion of the antimitotic drug AraC (Doetsch = et=20 al., 1999b3DGo).=20 AraC kills actively proliferating SVZ cells, type A and C = cells, but=20 spares type B cells (NSCs), which proliferate after AraC = removal and=20 sequentially regenerate type C and type A cells (Doetsch et = al.,=20 1999b). AraC was infused in the lateral ventricle = for 6 d and=20 was followed by infusion of recombinant LIF protein or PBS as = a=20 control. Mice were killed 1=962 h after a single BrdU = injection 1, 3,=20 or 7 d after AraC removal/LIF infusion, when type B, type C, = and type=20 A cells reappear and massively proliferate, respectively = (Doetsch et=20 al., 1999b3DGo).

At all time points examined after AraC removal, SVZ cell = proliferation=20 (BrdU staining) is reduced by 3D~=2050% in animals = infused with=20 LIF compared with controls (Fig. = 5). As=20 expected, the number of BrdU+ cells increases in controls = between 1=20 and 3 d of regeneration, reflecting the reappearance of type = C cells=20 from NSCs (Doetsch et al., 1999b3DGo).=20 However, no such increase is apparent in LIF-treated animals = (Fig. = 5),=20 suggesting that type C cells do not fully reappear. Indeed,=20 proliferating C cells, identified by coexpression of BrdU and = the=20 EGFR (Doetsch et al., 20023DGo)=20 (Fig. = 5),=20 are strongly reduced (>70%) in LIF-treated animals (71.67 = =B1=20 4.65 vs 21.33 =B1 3.52 BrdU+/EGFR+ cells in PBS-infused = controls=20 vs LIF-treated animals; p < 0.001). Furthermore,=20 BrdU+/EGFR+ cells account for only 50% of the proliferating = cells in=20 animals infused with LIF, whereas their proportion reaches = 70% in=20 controls (p =3D 0.005), as reported previously = (Doetsch et al.,=20 1999b). Thus, these results indicate a lack of or = delay in=20 the generation of type C cells from NSCs when the SVZ = regenerates in=20 the presence of LIF. Some neuroblasts do reappear 7 d after = AraC=20 removal/LIF infusion, but to a much lower extent than in = control (Fig. = 5)=20 (image analysis of Dcx staining in the SVZ: 4383.22 =B1 = 595.84 vs=20 1116.22 =B1 92.10 pixel2 in PBS vs LIF-infused = animals;=20 p < 0.001).



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  		Figure 5. = Infusion of LIF=20 after a 6 d AraC treatment impairs SVZ regeneration in = vivo=20 by acting directly on NSCs. A, Quantification = of BrdU+=20 cells in the SVZ indicates that LIF reduces the number of = BrdU+=20 cells at 1, 3, and 7 d after AraC removal. B, = High=20 magnification of SVZ cells double stained for BrdU and EGFR, = a=20 marker of transit-amplifying cells (type C). = C,=20 Representative sections stained with Dcx (a marker of = neuroblasts) 7=20 d after AraC removal/LIF infusion. LIF strongly impairs the=20 reappearance of neuroblasts (see Results for image analysis = data).=20 Data are mean =B1 SEM of n =3D 3 animals per group = (2=963 sections=20 analyzed per animal). **p < 0.01 and ***p = <=20 0.001 compared with PBS-infused controls (Student's t = test).=20 Scale bars: B, 15 =B5m (inset, 30 =B5m); = C,=20 200 =B5m. =

 = ;
Altogether,=20 our results indicate that LIF acts directly on NSCs in = vivo=20 and prevents the normal generation of NSCs progeny during the = regeneration process.

LIF promotes adult NSC self-renewal in vivo and in=20 vitro
LIF could prevent the emergence of more = differentiated=20 progeny as a result of promoting symmetric cell division and=20 self-renewal of adult NSCs in vivo. To analyze the = effects of=20 LIF on NSC self-renewal, we first used the neurosphere assay = in=20 vitro. Adult SVZ-derived neurospheres were grown in = proliferative=20 conditions for 6 d in vitro (DIV) and exposed to LIF = for the=20 last 2 DIV, which does not change the number or size of the=20 neurospheres (supplemental Fig. 3, available at http://www.jneurosci.org/ as supple= mental=20 material). Neurospheres were then dissociated, and single = cells=20 were replated in normal proliferative conditions without LIF = for=20 another 7=969 DIV to score the number of secondary = neurospheres=20 generated. The transient incubation in LIF during the last 2 = DIV=20 increases secondary sphere formation by nearly 70% (Fig. = 6).=20 These neurospheres could be passaged and were multipotent = (data not=20 shown), suggesting that LIF promotes the self-renewal of=20 sphere-forming cells with NSC characteristics in = vitro.=20



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  		Figure 6. LIF = stimulates=20 the self-renewal of sphere-forming cells in vitro, as = well as=20 the renewal of long-term, label-retaining cells in = vivo.=20 A, Schematic representation of the protocol = used in=20 vitro. Growing neurospheres were incubated with LIF (20 = ng/ml)=20 during the last 2 DIV. These neurospheres were then = dissociated to=20 assess secondary neurosphere formation. B,=20 Quantification of secondary spheres. Neurospheres pretreated = with=20 LIF during the last 2 DIV (from 6 to 8 DIV) yield 70% more = secondary=20 neurospheres compared with neurospheres that were not = exposed to=20 LIF. This increase is observed on the total population of = spheres as=20 well as on larger neurospheres (3D≥=20100 = =B5m=20 diameter). C, Pictures illustrate an example = of the=20 IdU and CldU double staining. D, LIF induces a = 30%=20 increase in the number of long-term, label-retaining cells = (IdU+),=20 as well as a twofold increase in the number of long-term,=20 label-retaining cells that reenter the cell cycle = (IdU+/CldU+). LIF=20 also increases the proportion of IdU+/CldU+ cells among the = total=20 IdU+ cells (Index; i.e., the proportion of self-renewing, = long-term,=20 label-retaining cells that reenter the cell cycle). Data are = mean =B1=20 SEM of n =3D 3 animals per group (3 sections analyzed = per=20 animal) or n =3D 3=966 wells per condition = (independent=20 experiments were performed at least 3 times and gave similar = results). **p < 0.01 and ***p < 0.001 = compared=20 with Ad:LacZ-treated control animals or spheres incubated = without=20 LIF (Student's t test). Scale bar: C, = 30 =B5m=20 (inset, 60 =B5m). =

 = ;
To=20 determine whether LIF also stimulates the self-renewal of = NSCs in=20 vivo, we made use of the fact that stem cells retain = exogenous=20 thymidine analogs after long-term survival (Morshead et al., = 19943DGo,=20 1998; Doetsch et al., 1999a3DGo).=20 We further refined this method by using a double nucleoside = labeling=20 strategy to monitor the proportion of long-term, = label-retaining=20 cells that reenter the cell cycle (Maslov et al., 20043DGo).=20 In this experiment, adult mice were given nucleoside analogs = in their=20 drinking water, starting with a 2 week treatment with IdU, = followed=20 by 1 week without label and by an Ad:LIF or Ad:LacZ = injection. Mice=20 were then given CldU for another 2 weeks, followed by 1 week=20 without label before they were killed, a total of 4 weeks = after=20 the end of IdU administration. In this experiment, the SVZ=20 should contain long-term, label-retaining cells that are = IdU+,=20 some of which become quiescent, whereas others are still=20 proliferating and likely correspond to self-renewing NSCs, = which can=20 thus be identified by the incorporation of both markers, IdU = and=20 CldU.

Ad:LIF treatment increases the number of IdU+ cells (by 3D~=2030%) = (Fig. = 6),=20 indicating that LIF promotes the retention of long-term,=20 label-retaining cells in the SVZ. Importantly, LIF also = produces=20 a twofold increase in the number of cells double labeled with = IdU and CldU and increases the proportion of self-renewing = cells=20 (IdU+/CldU+) among the total number of long-term, = label-retaining=20 cells (IdU+) (Fig. = 6).=20 These data indicate that LIF promotes the formation of = long-term,=20 label-retaining cells that reenter the cell cycle, which are=20 candidate NSCs. Although it is possible that some IdU+/CldU+ = cells=20 correspond to type C cells, their contribution in our = experiment is=20 likely minimal, because we find that LIF strongly reduces the = number=20 of C cells. Furthermore, previous studies found that the only = SVZ=20 cells labeled 1 month after nucleoside administration are the = type B=20 cells (Doetsch et al., 1999a3DGo).=20 Thus, the increase in IdU+/CldU+ cells likely reflects a = greater=20 number of NSCs that reenter the cell cycle, suggesting that = LIF=20 promotes the self-renewal of proliferating NSCs in = vivo.=20

In conclusion, our results strongly suggest that LIF expands = the=20 pool of adult NSCs by promoting their self-renewal, thereby=20 preventing the emergence of more differentiated progeny, both = in vivo and in vitro.

Infusion of LIF before AraC promotes SVZ=20 regeneration
Therapeutic strategies for brain repair include = the=20 stimulation of endogenous progenitors to promote cell = replacement.=20 Thus, it is of interest to determine whether the increased=20 number of NSCs induced by LIF treatment in vivo may be = useful=20 in regeneration of cell populations. Given the strong = correlation=20 between the effects of LIF on sphere formation in = vitro and on=20 the early phases of SVZ regeneration in vivo = (supplemental=20 Fig. 3, available at http://www.jneurosci.org/ as supple= mental=20 material), and because LIF exposure for the last 2 DIV = strongly=20 stimulates secondary sphere formation, we asked whether a = previous,=20 short-term exposure to LIF in vivo in a normal SVZ=20 environment, before infusing AraC, leads to a stimulation of = the=20 regenerative process (the equivalent of an increased = secondary sphere=20 formation).

We tested this by infusing LIF or PBS for 3 d in the lateral=20 ventricle before a 6 d AraC infusion. Animals received a = single=20 BrdU injection 1 h before they were killed, 3 d after AraC = removal.=20 Remarkably, the number of BrdU+ or Ki67+ cells is = significantly=20 increased in the SVZ of animals treated with LIF before AraC, = as is the number of proliferating EGFR+ type C cells (Table=20 1). In contrast, a 3 d infusion of EGF instead of LIF = before=20 AraC infusion has no effect on subsequent SVZ regeneration = (Table=20 1), indicating that the effects of LIF are specific. = Because=20 EGF acts primarily on type C but not type B (NSCs) cells=20 (Doetsch et al., 20023DGo),=20 this suggests that LIF-mediated acceleration of SVZ = regeneration=20 results from an effect on NSCs. Furthermore, we find that SVZ = cell=20 proliferation, although strongly decreased by a 3 d LIF = infusion,=20 quickly returns to near-control levels as soon as 1 d after = LIF=20 removal (data not shown), making it unlikely that type C = cells could=20 be protected from AraC-induced degeneration.


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  		Table = 1. Infusion=20 of LIF for 3 d before a 6 d AraC treatment promotes = subsequent SVZ=20 regeneration, whereas EGF instead of LIF has no effect =

 
Thus,=20 our data indicate that LIF infusion, before inducing SVZ=20 degeneration, accelerates the subsequent regenerative = process,=20 possibly as a result of expanding the pool of NSCs through = the=20 promotion of self-renewing divisions. This could be = attributable=20 to a direct effect of LIF on NSCs or, alternatively, could be = mediated indirectly, through cells activated by LIF outside = the=20 SVZ.


3D"   =20 Discussion
Top
Abstract
3D"Introduction
3D"Materials and Methods
3D"Results
3D"Discussion
3D"References
 
T= he adult=20 SVZ, where new OB neurons are born, contains rapidly dividing = progenitors, neuroblasts and transit-amplifying cells, the = type A and=20 type C cells, respectively. We find that exogenous LIF = strongly=20 reduces SVZ cell proliferation and subsequent neurogenesis in = the=20 adult OB. At the same time, we find that LIF promotes the=20 self-renewal of NSCs, ultimately expanding this discrete cell = population, which normally represents only 0.2=960.4% of the = SVZ cells.=20 Thus, chronic overexpression of LIF in vivo maintains = NSCs in=20 a loop of symmetric/self-renewing divisions, preventing the = emergence=20 of more differentiated progeny. A similar deregulation of the = SVZ=20 cell lineage in vivo has been described after = application of=20 exogenous EGF, which also reduces neurogenesis but does so by = acting=20 on transit-amplifying cells (Doetsch et al., 20023DGo).

Our results are consistent with and expand on recent studies=20 examining the in vitro effects of LIF on embryonic=20 neurospheres (Pitman et al., 20043DGo;=20 Bonaguidi et al., 20053DGo),=20 in which LIF promotes secondary sphere formation. Although = LIF=20 induces a marker of astrocyte differentiation (GFAP), the = morphology=20 and phenotype of these LIF-treated cells is distinct from=20 astrocytes generated in the presence of bone morphogenic = proteins=20 (BMPs), another gliogenic cytokine family (Bonaguidi et al., = 20053DGo). Major differences include = bipolar/elongated/radial=20 morphology in LIF but a stellate morphology in BMPs and = expression of=20 radial glial markers such as vimentin in LIF but not in BMPs=20 (Bonaguidi et al., 20053DGo).=20 Furthermore, proliferation continues in the presence of LIF = but is=20 strongly inhibited in BMPs, and neurospheres can be obtained = very=20 efficiently from LIF-generated astrocytes, but not from = astrocytes=20 generated in BMPs (Bonaguidi et al., 20053DGo).=20 Interestingly, the bipolar/elongated/radial morphology of=20 LIF-generated astrocytes is reminiscent of the morphology = described=20 in vivo for adult GFAP-expressing NSCs (Garcia et al., = 20043DGo)=20 and is consistent with our findings (Fig. = 4).=20 Overexpressing BMP in vivo prevents cell proliferation = and=20 neurogenesis in the adult SVZ (Lim et al., 20003DGo),=20 similar to our findings with LIF. In the hippocampus, = overexpression=20 of BMPs reduces proliferation and downregulates the = expression of=20 neural progenitor markers in GFAP+ cells (Bonaguidi et al., = 20053DGo).=20 Thus, BMPs induce differentiation of GFAP-expressing NSCs = into=20 astrocytes that lose their stem cell potential, whereas LIF = maintains=20 their stem cell characteristics. Despite our findings that = LIF acts=20 on NSCs during SVZ regeneration and that LIFR is expressed on = some=20 GFAP+ cells, we cannot exclude the possibility that LIF = promotes GFAP=20 expression in a subset of type C cells, which may = dedifferentiate and=20 acquire NSC characteristics, similar to the effects of = exogenous EGF=20 treatment (Doetsch et al., 20023DGo).=20 Indeed, EGFR signaling synergizes with LIF to induce = astrocyte=20 differentiation (Viti et al., 20033DGo),=20 and we also find colocalization of EGFR with LIFR = (supplemental Fig.=20 2, available at http://www.jneurosci.org/ as supple= mental=20 material).

In contrast to the effects of LIF described in our study, = exogenous=20 CNTF stimulates SVZ cell proliferation (Shimazaki et al., 20013DGo) and neurogenesis in the adult brain (Emsley = and Hagg,=20 2003; Kokoeva et al., 20053DGo),=20 suggesting that LIF and CNTF have different biological = effects.=20 Indeed, slightly more neurospheres were derived from the = ependyma of=20 adult mice infused with CNTF (Shimazaki et al., 20013DGo),=20 whereas we derived fewer neurospheres from mice treated with = Ad:LIF=20 (our unpublished results). Given that up to 70% of = neurospheres come=20 from type C cells (Doetsch et al., 20023DGo),=20 this suggests that CNTF may increase the number of type C = cells,=20 whereas we find that LIF decreases it. The dose of CNTF used = may also=20 be an issue. For example, a high dose of CNTF results in the=20 promotion of neurogenesis in the hypothalamus [656 ng/d = (Kokoeva et=20 al., 20053DGo)], whereas we used a much lower dose of LIF = (60=96120=20 ng/d). In another example, the dose of EGF has been reported = to=20 differentially affect type C cell phenotype (Doetsch et al., = 20023DGo).=20 Discrepancies also exist in vitro, because some = reports=20 indicate that CNTF or LIF do not affect neurosphere formation = (Shimazaki et al., 20013DGo;=20 Gregg and Weiss, 20053DGo),=20 whereas others find that they do (Pitman et al., 20043DGo;=20 present study; our unpublished results). Nevertheless, CNTF = exposure=20 for the last 4 DIV increases secondary neurosphere formation=20 (Shimazaki et al., 20013DGo),=20 similar to the effect of LIF (present study). Whether LIF and = CNTF=20 have similar effects on adult NSCs in vivo remains to = be=20 determined.

Endogenous LIFR signaling promotes the maintenance of embryonic=20 and adult NSCs in vivo and in vitro (Shimazaki et = al.,=20 2001; Pitman et al., 20043DGo),=20 and intracerebroventricular injection of anti-CNTF antibodies = decreases adult neurogenesis (Emsley and Hagg, 20033DGo).=20 We did not address the role of endogenous LIF in this study, = but LIF=20 expression is generally very low under physiological = conditions.=20 Thus, LIF knock-out mice display no difference in olfactory = precursor=20 cell proliferation unless injury is performed, at which point = LIF is=20 required for proliferation (Bauer et al., 20033DGo).=20 Interestingly, brain injuries are potent inducers of LIF = expression=20 and also increase SVZ or hippocampal cell proliferation, = suggesting=20 that LIF may be a key signaling molecule that triggers = progenitor=20 cell recruitment after injury. Endogenous LIF promotes cell=20 proliferation after spinal cord injury, which is further = potentiated=20 by exogenous LIF treatment (Kerr and Patterson, 20043DGo).=20 We demonstrate here that exogenous LIF accelerates SVZ = regeneration=20 when infused before AraC, possibly by promoting NSC = self-renewal,=20 which suggests that LIF could be used to stimulate brain = repair after=20 injury.

In this context, the effects of chronic versus acute LIF = treatment=20 are important to consider. Indeed, chronic exposure to LIF is = not physiological, because LIF expression after injury is = rapid=20 and transient. Our data emphasize that downregulation of LIF = is=20 necessary to end the stimulation of NSC self-renewal and = allow the=20 harnessing of the regenerative potential of NSCs. The = transient=20 expression of LIF observed after injury may thus trigger a = period of=20 increased NSC self-renewal, which likely constitutes the = first step=20 toward regeneration. Our data also suggest a model for the=20 development of successful therapeutic regenerative strategies = from=20 endogenous NSCs, whereby brain repair may be achieved with = critically=20 timed exposure to factors that stimulate NSC self-renewal = first,=20 followed by exposure to other factors that promote survival,=20 migration, and differentiation of NSC progeny.

Finally, it is interesting to note that our results are = reminiscent=20 of LIF action on mouse ES cells, suggesting a continuum from = ES=20 cells to adult NSCs. This view is supported by recent findings=20 showing that mouse ES cells plated in minimal conditions = default=20 to a neural fate and transform into LIF-dependent primordial=20 NSCs, which in turn generate FGF2-dependent definitive NSCs=20 (Smukler et al., 20063DGo).=20 In those experiments, LIF appears to maintain a population of = primordial NSCs in an undifferentiated state by preventing = additional=20 neural differentiation of the ES cells (Smukler et al., = 20063DGo).=20 LIF-dependent, primordial NSCs similar to those derived from = ES cells=20 have also been obtained from embryonic day 5.5 mouse = neuroectoderm=20 (Hitoshi et al., 20043DGo),=20 suggesting that the continuum from ES cells to NSCs described = in=20 vitro may also exist in vivo. Together with these = studies,=20 our data show that LIF exerts a similar range of actions from = ES cells to adult NSCs and suggest that common mechanisms = participate=20 in the maintenance of these various types of stem cells. =


3D"   =20 Footnotes
 
Received July = 18, 2006;=20 revised Oct. 15, 2006; accepted Oct. 17, 2006.

S. Bauer's present address:=20 Physiologie Neurov=E9g=E9tative, Unit=E9 Mixte de Recherche = 6153, Centre=20 National de la Recherche Scientifique-1147 Institut National = de la=20 Recherche Agronomique, Universit=E9 Paul = C=E9zanne-Aix-Marseille-3,=20 Avenue Escadrille Normandie-Niemen, BP 351-352, 13397 = Marseille=20 Cedex 20, France.

This work was supported by a fellowship = from The=20 John Douglas French Alzheimer's Foundation (S.B.) and by = grants from=20 the National Institute of Neurological Disorders and Stroke = and=20 the McGrath Foundation (P.H.P.). We are grateful to D. = McDowell,=20 B. Kennedy, and members of the California Institute of = Technology=20 Office of Laboratory Animal Resources for their excellent = assistance.=20 We also thank F. H. Gage (The Salk Institute, San Diego, CA)=20 for the generous gift of the retroviral plasmids and N. L. = Nadon=20 (National Institute on Aging, Bethesda, MD) for the = 16-month-old=20 C57BL/6J mice. We are grateful to C. Charrier for help with = the=20 neurosphere culture and to A. Lukaszewicz for critical reading = of=20 this manuscript.

Correspondence should be addressed to = Paul H.=20 Patterson, Biology Division, 216-76, California Institute of Technology, = 1200 E.=20 California Boulevard, Pasadena, CA 91125. Email: php{at}caltech.edu

Copyright =A9 2006 Society for Neuroscience = 0270-6474/06/2612089-11$15.00/0=20


3D"   =20 References
Top
Abstract
3D"Introduction
3D"Materials and Methods
3D"Results
3D"Discussion
3D"References
&nb= sp;

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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_004F_01C85935.65742B70 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.appendChild(e);=0A= }=0A= else if (src.nodeType =3D=3D 3) { /* Node.TEXT_NODE */=0A= dst.appendChild(document.createTextNode(src.nodeValue));=0A= }=0A= }=0A= =0A= /* =0A= * It is unclear that this is the right thing to be calling=0A= * from copy_xml_to_html, but it appears that Safari decides=0A= * to convert & to the NCR #, and then encodes that=0A= * NCR to &%26%2338;. So, I'm going to treat the DOM Attr=0A= * value as a plain string, and run our XML string input=0A= * through the decoding routine below.=0A= */=0A= function unescape_xml_string(s) {=0A= return s.replace(/'/g, "'")=0A= .replace(/'/g, "'")=0A= .replace(/"/g, "\"")=0A= .replace(/"/g, "\"")=0A= .replace(/>/g, ">")=0A= .replace(/>/g, ">")=0A= .replace(/</g, "<")=0A= .replace(/</g, "<")=0A= .replace(/&/g, "&")=0A= .replace(/&/g, "&");=0A= }=0A= =0A= /*=0A= * Parse set of CSS rules and apply them to an element.=0A= * This is quite horrifying, but I'm unable to determine=0A= * how else to handle this with IE 6. FireFox and other=0A= * sane browsers let you simply set the style attribute=0A= * or use e.style.setProperty(rule, value, priority),=0A= * IE 6 appears to have neither of these capabilities..=0A= */=0A= function set_css_style(css, e, priority) {=0A= var rules =3D css.split(";");=0A= for (var i =3D 0; i < rules.length; i++) {=0A= var nvpair =3D rules[i].split(":");=0A= if (nvpair.length =3D=3D 2) {=0A= try {=0A= var name =3D nvpair[0]; /* style attribute */=0A= var value =3D nvpair[1]; /* attribute value */=0A= =0A= /*=0A= * For each possible style attribute, set the=0A= * appropriate style property in the element.=0A= */=0A= if (name =3D=3D "background") {=0A= e.style.background =3D value;=0A= }=0A= else if (name =3D=3D "background-attachment") {=0A= e.style.backgroundAttachment =3D value;=0A= }=0A= else if (name =3D=3D "background-color") {=0A= e.style.backgroundColor =3D value;=0A= }=0A= else if (name =3D=3D "background-image") {=0A= e.style.backgroundImage =3D value;=0A= }=0A= else if (name =3D=3D "background-position") {=0A= e.style.backgroundPosition =3D value;=0A= }=0A= else if (name =3D=3D "background-position-x") {=0A= e.style.backgroundPositionX =3D value;=0A= }=0A= else if (name =3D=3D "background-position-y") {=0A= e.style.backgroundPositionY =3D value;=0A= }=0A= else if (name =3D=3D "background-repeat") {=0A= e.style.backgroundRepeat =3D value;=0A= }=0A= else if (name =3D=3D "behavior") {=0A= e.style.behavior =3D value;=0A= }=0A= else if (name =3D=3D "border") {=0A= e.style.border =3D value;=0A= }=0A= else if (name =3D=3D "border-bottom") {=0A= e.style.borderBottom =3D value;=0A= }=0A= else if (name =3D=3D "border-bottom-color") {=0A= e.style.borderBottomColor =3D value;=0A= }=0A= else if (name =3D=3D "border-bottom-style") {=0A= e.style.borderBottomStyle =3D value;=0A= }=0A= else if (name =3D=3D "border-bottom-width") {=0A= e.style.borderBottomWidth =3D value;=0A= }=0A= else if (name =3D=3D "border-collapse") {=0A= e.style.borderCollapse =3D value;=0A= }=0A= else if (name =3D=3D "border-color") {=0A= e.style.borderColor =3D value;=0A= }=0A= else if (name =3D=3D "border-left") {=0A= e.style.borderLeft =3D value;=0A= }=0A= else if (name =3D=3D "border-left-color") {=0A= e.style.borderLeftColor =3D value;=0A= }=0A= else if (name =3D=3D "border-left-style") {=0A= e.style.borderLeftStyle =3D value;=0A= }=0A= else if (name =3D=3D "border-left-width") {=0A= e.style.borderLeftWidth =3D value;=0A= }=0A= else if (name =3D=3D "border-right") {=0A= e.style.borderRight =3D value;=0A= }=0A= else if (name =3D=3D "border-right-color") {=0A= e.style.borderRightColor =3D value;=0A= }=0A= else if (name =3D=3D "border-right-style") {=0A= e.style.borderRightStyle =3D value;=0A= }=0A= else if (name =3D=3D "border-right-width") {=0A= e.style.borderRightWidth =3D value;=0A= }=0A= else if (name =3D=3D "border-style") {=0A= e.style.borderStyle =3D value;=0A= }=0A= else if (name =3D=3D "border-top") {=0A= e.style.borderTop =3D value;=0A= }=0A= else if (name =3D=3D "border-top-color") {=0A= e.style.borderTopColor =3D value;=0A= }=0A= else if (name =3D=3D "border-top-style") {=0A= e.style.borderTopStyle =3D value;=0A= }=0A= else if (name =3D=3D "border-top-width") {=0A= e.style.borderTopWidth =3D value;=0A= }=0A= else if (name =3D=3D "border-width") {=0A= e.style.borderWidth =3D value;=0A= }=0A= else if (name =3D=3D "bottom") {=0A= e.style.bottom =3D value;=0A= }=0A= else if (name =3D=3D "clear") {=0A= e.style.clear =3D value;=0A= }=0A= else if (name =3D=3D "clip") {=0A= e.style.clip =3D value;=0A= }=0A= else if (name =3D=3D "color") {=0A= e.style.color =3D value;=0A= }=0A= else if (name =3D=3D "cssText") {=0A= e.style.Sets =3D value;=0A= }=0A= else if (name =3D=3D "cursor") {=0A= e.style.cursor =3D value;=0A= }=0A= else if (name =3D=3D "direction") {=0A= e.style.direction =3D value;=0A= }=0A= else if (name =3D=3D "display") {=0A= e.style.display =3D value;=0A= }=0A= else if (name =3D=3D "font") {=0A= e.style.font =3D value;=0A= }=0A= else if (name =3D=3D "font-family") {=0A= e.style.fontFamily =3D value;=0A= }=0A= else if (name =3D=3D "font-size") {=0A= e.style.fontSize =3D value;=0A= }=0A= else if (name =3D=3D "font-style") {=0A= e.style.fontStyle =3D value;=0A= }=0A= else if (name =3D=3D "font-variant") {=0A= e.style.fontVariant =3D value;=0A= }=0A= else if (name =3D=3D "font-weight") {=0A= e.style.fontWeight =3D value;=0A= }=0A= else if (name =3D=3D "height") {=0A= e.style.height =3D value;=0A= }=0A= else if (name =3D=3D "ime-mode") {=0A= e.style.imeMode =3D value;=0A= }=0A= else if (name =3D=3D "layout-flow") {=0A= e.style.layoutFlow =3D value;=0A= }=0A= else if (name =3D=3D "layout-grid") {=0A= e.style.layoutGrid =3D value;=0A= }=0A= else if (name =3D=3D "layout-grid-char") {=0A= e.style.layoutGridChar =3D value;=0A= }=0A= else if (name =3D=3D "layout-grid-line") {=0A= e.style.layoutGridLine =3D value;=0A= }=0A= else if (name =3D=3D "layout-grid-mode") {=0A= e.style.layoutGridMode =3D value;=0A= }=0A= else if (name =3D=3D "layout-grid-type") {=0A= e.style.layoutGridType =3D value;=0A= }=0A= else if (name =3D=3D "left") {=0A= e.style.left =3D value;=0A= }=0A= else if (name =3D=3D "letter-spacing") {=0A= e.style.letterSpacing =3D value;=0A= }=0A= else if (name =3D=3D "line-break") {=0A= e.style.lineBreak =3D value;=0A= }=0A= else if (name =3D=3D "line-height") {=0A= e.style.lineHeight =3D value;=0A= }=0A= else if (name =3D=3D "list-style") {=0A= e.style.listStyle =3D value;=0A= }=0A= else if (name =3D=3D "list-style-image") {=0A= e.style.listStyleImage =3D value;=0A= }=0A= else if (name =3D=3D "list-style-position") {=0A= e.style.listStylePosition =3D value;=0A= }=0A= else if (name =3D=3D "list-style-type") {=0A= e.style.listStyleType =3D value;=0A= }=0A= else if (name =3D=3D "margin") {=0A= e.style.margin =3D value;=0A= }=0A= else if (name =3D=3D "margin-bottom") {=0A= e.style.marginBottom =3D value;=0A= }=0A= else if (name =3D=3D "margin-left") {=0A= e.style.marginLeft =3D value;=0A= }=0A= else if (name =3D=3D "margin-right") {=0A= e.style.marginRight =3D value;=0A= }=0A= else if (name =3D=3D "margin-top") {=0A= e.style.marginTop =3D value;=0A= }=0A= else if (name =3D=3D "min-height") {=0A= e.style.minHeight =3D value;=0A= }=0A= else if (name =3D=3D "overflow") {=0A= e.style.overflow =3D value;=0A= }=0A= else if (name =3D=3D "overflow-x") {=0A= e.style.overflowX =3D value;=0A= }=0A= else if (name =3D=3D "overflow-y") {=0A= e.style.overflowY =3D value;=0A= }=0A= else if (name =3D=3D "padding") {=0A= e.style.padding =3D value;=0A= }=0A= else if (name =3D=3D "padding-bottom") {=0A= e.style.paddingBottom =3D value;=0A= }=0A= else if (name =3D=3D "padding-left") {=0A= e.style.paddingLeft =3D value;=0A= }=0A= else if (name =3D=3D "padding-right") {=0A= e.style.paddingRight =3D value;=0A= }=0A= else if (name =3D=3D "padding-top") {=0A= e.style.paddingTop =3D value;=0A= }=0A= else if (name =3D=3D "page-break-after") {=0A= e.style.pageBreakAfter =3D value;=0A= }=0A= else if (name =3D=3D "page-break-before") {=0A= e.style.pageBreakBefore =3D value;=0A= }=0A= else if (name =3D=3D "pixelBottom") {=0A= e.style.pixelBottom =3D value;=0A= }=0A= else if (name =3D=3D "pixelHeight") {=0A= e.style.pixelHeight =3D value;=0A= }=0A= else if (name =3D=3D "pixelLeft") {=0A= e.style.pixelLeft =3D value;=0A= }=0A= else if (name =3D=3D "pixelRight") {=0A= e.style.pixelRight =3D value;=0A= }=0A= else if (name =3D=3D "pixelTop") {=0A= e.style.pixelTop =3D value;=0A= }=0A= else if (name =3D=3D "pixelWidth") {=0A= e.style.pixelWidth =3D value;=0A= }=0A= else if (name =3D=3D "posBottom") {=0A= e.style.posBottom =3D value;=0A= }=0A= else if (name =3D=3D "posHeight") {=0A= e.style.posHeight =3D value;=0A= }=0A= else if (name =3D=3D "position") {=0A= e.style.position =3D value;=0A= }=0A= else if (name =3D=3D "posLeft") {=0A= e.style.posLeft =3D value;=0A= }=0A= else if (name =3D=3D "posRight") {=0A= e.style.posRight =3D value;=0A= }=0A= else if (name =3D=3D "posTop") {=0A= e.style.posTop =3D value;=0A= }=0A= else if (name =3D=3D "posWidth") {=0A= e.style.posWidth =3D value;=0A= }=0A= else if (name =3D=3D "right") {=0A= e.style.right =3D value;=0A= }=0A= else if (name =3D=3D "ruby-align") {=0A= e.style.rubyAlign =3D value;=0A= }=0A= else if (name =3D=3D "ruby-overhang") {=0A= e.style.rubyOverhang =3D value;=0A= }=0A= else if (name =3D=3D "ruby-position") {=0A= e.style.rubyPosition =3D value;=0A= }=0A= else if (name =3D=3D "scrollbar-3dlight-color") {=0A= e.style.scrollbar3dLightColor =3D value;=0A= }=0A= else if (name =3D=3D "scrollbar-arrow-color") {=0A= e.style.scrollbarArrowColor =3D value;=0A= }=0A= else if (name =3D=3D "scrollbar-base-color") {=0A= e.style.scrollbarBaseColor =3D value;=0A= }=0A= else if (name =3D=3D "scrollbar-darkshadow-color") {=0A= e.style.scrollbarDarkShadowColor =3D value;=0A= }=0A= else if (name =3D=3D "scrollbar-face-color") {=0A= e.style.scrollbarFaceColor =3D value;=0A= }=0A= else if (name =3D=3D "scrollbar-highlight-color") {=0A= e.style.scrollbarHighlightColor =3D value;=0A= }=0A= else if (name =3D=3D "scrollbar-shadow-color") {=0A= e.style.scrollbarShadowColor =3D value;=0A= }=0A= else if (name =3D=3D "scrollbar-track-color") {=0A= e.style.scrollbarTrackColor =3D value;=0A= }=0A= else if (name =3D=3D "float") {=0A= e.style.styleFloat =3D value;=0A= }=0A= else if (name =3D=3D "table-layout") {=0A= e.style.tableLayout =3D value;=0A= }=0A= else if (name =3D=3D "text-align") {=0A= e.style.textAlign =3D value;=0A= }=0A= else if (name =3D=3D "text-align-last") {=0A= e.style.textAlignLast =3D value;=0A= }=0A= else if (name =3D=3D "text-autospace") {=0A= e.style.textAutospace =3D value;=0A= }=0A= else if (name =3D=3D "text-decoration") {=0A= e.style.textDecoration =3D value;=0A= }=0A= else if (name =3D=3D "textDecorationBlink") {=0A= e.style.textDecorationBlink =3D value;=0A= }=0A= else if (name =3D=3D "textDecorationLineThrough") {=0A= e.style.textDecorationLineThrough =3D value;=0A= }=0A= else if (name =3D=3D 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quoted-printable Content-Location: http://www.jneurosci.org/javascript/entrez/callback.js /************************************************************************= *****=0A= * javascript/entrez/callback.js=0A= *=0A= * Entrez Linking callback to populate content box.=0A= *=0A= * Copyright 2006 Board of Trustees of the Leland Stanford Junior = University.=0A= = *************************************************************************= ***/=0A= =0A= /*=0A= * Execute callback to fill content box with Entrez Linking information.=0A= */=0A= function entrez_callback(pmid, callback_url) {=0A= /*=0A= * MSIE 5.5 and below have issues with the JavaScript=0A= * used for Entrez Linking. 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