The Cerebrospinal Fluid Provides a Proliferative Niche for Neural Progenitor Cells

Neuron

Volumn 69, Issue 5, 2011, Pages 893-905

  Lehtinen, Maria K ^a,b   Zappaterra, Mauro W ^a,b,c   Chen, Xi ^a,b,d   Yang, Yawei J ^a,b,c,d   Hill, Anthony D ^a,b   Lun, Melody ^a,b,f   Maynard, Thomas ^e   Gonzalez, Dilenny ^a,b   Kim, Seonhee ^h   Ye, Ping ^g   D'Ercole, A Joseph ^g   Wong, Eric T ^f   LaMantia, Anthony S ^e   Walsh, Christopher A ^a,b,c  

^a BOSTON CHILDREN S HOSPITAL   (United States)

^b BROAD INSTITUTE OF MIT AND HARVARD   (United States)

^c HARVARD MEDICAL SCHOOL   (United States)

^d HARVARD MIT DIVISION OF HEALTH SCIENCES AND TECHNOLOGY   (United States)

^e GEORGE WASHINGTON UNIVERSITY SCHOOL OF MEDICINE AND HEALTH SCIENCES   (United States)

^f BETH ISRAEL DEACONESS MEDICAL CENTER   (United States)

^g UNIVERSITY OF NORTH CAROLINA SCHOOL OF MEDICINE   (United States)

^h UNIVERSITY OF TEXAS MEDICAL SCHOOL   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

MEMBRANE PROTEIN; PHOSPHATIDYLINOSITOL 3,4,5 TRISPHOSPHATE 3 PHOSPHATASE; PROTEIN ASSOCIATED WITH LIN 7; SOMATOMEDIN B; UNCLASSIFIED DRUG;

ANIMAL CELL; ANIMAL TISSUE; ARTICLE; BINDING SITE; BRAIN CORTEX; CELL CYCLE; CELL CYCLE REGULATION; CELL DEATH; CELL PROLIFERATION; CELL STRUCTURE; CELL SURVIVAL; CELL VIABILITY; CEREBROSPINAL FLUID; CHOROID PLEXUS; CONTROLLED STUDY; GENE DISRUPTION; GENE FREQUENCY; GENE MUTATION; HETEROZYGOSITY; IMMUNOREACTIVITY; MOUSE; NERVOUS SYSTEM DEVELOPMENT; NONHUMAN; PRIORITY JOURNAL; PROMOTER REGION; PROTEIN BINDING; PROTEIN DOMAIN; PROTEIN FUNCTION; PROTEIN LOCALIZATION; PROTEIN PHOSPHORYLATION; PROTEIN PROTEIN INTERACTION; RAT; SIGNAL TRANSDUCTION; STEM CELL; UPREGULATION;

ANALYSIS OF VARIANCE; ANIMALS; BRAIN NEOPLASMS; CELL PROLIFERATION; CEREBRAL CORTEX; CEREBROSPINAL FLUID; GLIOBLASTOMA; HUMANS; INSULIN-LIKE GROWTH FACTOR II; MEMBRANE PROTEINS; MICE; NEURAL STEM CELLS; NEURONS; NUCLEOSIDE-PHOSPHATE KINASE; PTEN PHOSPHOHYDROLASE; RECEPTOR, IGF TYPE 1; STATISTICS, NONPARAMETRIC;

EID: 79952215175     PISSN: 08966273     EISSN: 10974199     Source Type: Journal    
DOI: 10.1016/j.neuron.2011.01.023     Document Type: Article

References (70)

1. Ayer-le Lievre C., Ståhlbom P.A., Sara V.R. Expression of IGF-I and -II mRNA in the brain and craniofacial region of the rat fetus. Development 1991, 111:105-115.
2. Baker J., Liu J.P., Robertson E.J., Efstratiadis A. Role of insulin-like growth factors in embryonic and postnatal growth. Cell 1993, 75:73-82.
3. Bendall S.C., Stewart M.H., Menendez P., George D., Vijayaragavan K., Werbowetski-Ogilvie T., Ramos-Mejia V., Rouleau A., Yang J., Bossé M., et al. IGF and FGF cooperatively establish the regulatory stem cell niche of pluripotent human cells in vitro. Nature 2007, 448:1015-1021.
4. Binoux M., Lassarre C., Gourmelen M. Specific assay for insulin-like growth factor (IGF) II using the IGF binding proteins extracted from human cerebrospinal fluid. J. Clin. Endocrinol. Metab. 1986, 63:1151-1155.
5. Bondy C., Werner H., Roberts C.T., LeRoith D. Cellular pattern of type-I insulin-like growth factor receptor gene expression during maturation of the rat brain: Comparison with insulin-like growth factors I and II. Neuroscience 1992, 46:909-923.
6. Bultje R.S., Castaneda-Castellanos D.R., Jan L.Y., Jan Y.N., Kriegstein A.R., Shi S.H. Mammalian Par3 regulates progenitor cell asymmetric division via notch signaling in the developing neocortex. Neuron 2009, 63:189-202.
7. Cappello S., Attardo A., Wu X., Iwasato T., Itohara S., Wilsch-Bräuninger M., Eilken H.M., Rieger M.A., Schroeder T.T., Huttner W.B., et al. The Rho-GTPase cdc42 regulates neural progenitor fate at the apical surface. Nat. Neurosci. 2006, 9:1099-1107.
8. Chalhoub N., Zhu G., Zhu X., Baker S.J. Cell type specificity of PI3K signaling in Pdk1- and Pten-deficient brains. Genes Dev. 2009, 23:1619-1624.
9. Clemmons D.R. Insulin-like growth factor binding proteins and their role in controlling IGF actions. Cytokine Growth Factor Rev. 1997, 8:45-62.
10. Cohen E., Binet S., Meininger V. Ciliogenesis and centriole formation in the mouse embryonic nervous system. An ultrastructural analysis. Biol. Cell 1988, 62:165-169.
11. DeChiara T.M., Robertson E.J., Efstratiadis A. Parental imprinting of the mouse insulin-like growth factor II gene. Cell 1991, 64:849-859.
12. De Meyer G., Shapiro F., Vanderstichele H., Vanmechelen E., Engelborghs S., De Deyn P.P., Coart E., Hansson O., Minthon L., Zetterberg H., et al. Diagnosis-independent Alzheimer disease biomarker signature in cognitively normal elderly people. Arch. Neurol. 2010, 67:949-956. Alzheimer's Disease Neuroimaging Initiative.
13. Doetsch F., Caillé I., Lim D.A., García-Verdugo J.M., Alvarez-Buylla A. Subventricular zone astrocytes are neural stem cells in the adult mammalian brain. Cell 1999, 97:703-716.
14. Dugas J.C., Mandemakers W., Rogers M., Ibrahim A., Daneman R., Barres B.A. A novel purification method for CNS projection neurons leads to the identification of brain vascular cells as a source of trophic support for corticospinal motor neurons. J. Neurosci. 2008, 28:8294-8305.
15. Dziegielewska K.M., Evans C.A., Lai P.C., Lorscheider F.L., Malinowska D.H., Møllgård K., Saunders N.R. Proteins in cerebrospinal fluid and plasma of fetal rats during development. Dev. Biol. 1981, 83:193-200.
16. Feng W., Wu H., Chan L.N., Zhang M. Par-3-mediated junctional localization of the lipid phosphatase PTEN is required for cell polarity establishment. J. Biol. Chem. 2008, 283:23440-23449.
17. Fishell G., Kriegstein A.R. Neurons from radial glia: The consequences of asymmetric inheritance. Curr. Opin. Neurobiol. 2003, 13:34-41.
18. Fuchs J.L., Schwark H.D. Neuronal primary cilia: A review. Cell Biol. Int. 2004, 28:111-118.
19. Gorski J.A., Talley T., Qiu M., Puelles L., Rubenstein J.L., Jones K.R. Cortical excitatory neurons and glia, but not GABAergic neurons, are produced in the Emx1-expressing lineage. J. Neurosci. 2002, 22:6309-6314.
20. Groszer M., Erickson R., Scripture-Adams D.D., Lesche R., Trumpp A., Zack J.A., Kornblum H.I., Liu X., Wu H. Negative regulation of neural stem/progenitor cell proliferation by the Pten tumor suppressor gene in vivo. Science 2001, 294:2186-2189.
21. Grove E.A., Tole S., Limon J., Yip L., Ragsdale C.W. The hem of the embryonic cerebral cortex is defined by the expression of multiple Wnt genes and is compromised in Gli3-deficient mice. Development 1998, 125:2315-2325.
22. Haskell G.T., LaMantia A.S. Retinoic acid signaling identifies a distinct precursor population in the developing and adult forebrain. J. Neurosci. 2005, 25:7636-7647.
23. Hébert J.M., Mishina Y., McConnell S.K. BMP signaling is required locally to pattern the dorsal telencephalic midline. Neuron 2002, 35:1029-1041.
24. Hodge R.D., D'Ercole A.J., O'Kusky J.R. Insulin-like growth factor-I accelerates the cell cycle by decreasing G1 phase length and increases cell cycle reentry in the embryonic cerebral cortex. J. Neurosci. 2004, 24:10201-10210.
25. Huang X., Liu J., Ketova T., Fleming J.T., Grover V.K., Cooper M.K., Litingtung Y., Chiang C. Transventricular delivery of Sonic hedgehog is essential to cerebellar ventricular zone development. Proc. Natl. Acad. Sci. USA 2010, 107:8422-8427.
26. Johansson P.A., Cappello S., Gotz M. Stem cell niches during development - lessons from the cerebral cortex. Curr. Opin. Neurobiol. 2010, 20:1-8.
27. Kappeler L., De Magalhaes Filho C., Dupont J., Leneuve P., Cervera P., Périn L., Loudes C., Blaise A., Klein R., Epelbaum J., et al. Brain IGF-1 receptors control mammalian growth and lifespan through a neuroendocrine mechanism. PLoS Biol. 2008, 6:e254. 10.1371/journal.pbio.0060254.
28. Kemphues K. PARsing embryonic polarity. Cell 2000, 101:345-348.
29. Kim S., Lehtinen M.K., Sessa A., Zappaterra M.W., Cho S.H., Gonzalez D., Boggan B., Austin C.A., Wijnholds J., Gambello M.J., et al. The apical complex couples cell fate and cell survival to cerebral cortical development. Neuron 2010, 66:69-84.
30. LaMantia A.S., Colbert M.C., Linney E. Retinoic acid induction and regional differentiation prefigure olfactory pathway formation in the mammalian forebrain. Neuron 1993, 10:1035-1048.
31. Levine A.J., Brivanlou A.H. GDF3 at the crossroads of TGF-beta signaling. Cell Cycle 2006, 5:1069-1073.
32. Liu W., Ye P., O'Kusky J.R., D'Ercole A.J. Type 1 insulin-like growth factor receptor signaling is essential for the development of the hippocampal formation and dentate gyrus. J. Neurosci. Res. 2009, 87:2821-2832.
33. Llorens-Martín M., Torres-Alemán I., Trejo J.L. Exercise modulates insulin-like growth factor 1-dependent and -independent effects on adult hippocampal neurogenesis and behaviour. Mol. Cell. Neurosci. 2010, 44:109-117.
34. Louis D.N. Molecular pathology of malignant gliomas. Annu. Rev. Pathol. 2006, 1:97-117.
35. Macdonald D.R., Cascino T.L., Schold S.C., Cairncross J.G. Response criteria for phase II studies of supratentorial malignant glioma. J. Clin. Oncol. 1990, 8:1277-1280.
36. Margolis B., Borg J.P. Apicobasal polarity complexes. J. Cell Sci. 2005, 118:5157-5159.
37. Martín C., Bueno D., Alonso M.I., Moro J.A., Callejo S., Parada C., Martín P., Carnicero E., Gato A. FGF2 plays a key role in embryonic cerebrospinal fluid trophic properties over chick embryo neuroepithelial stem cells. Dev. Biol. 2006, 297:402-416.
38. Mirzadeh Z., Han Y.-G., Soriano-Navarro M., García-Verdugo J.M., Alvarez-Buylla A. Cilia organize ependymal planar polarity. J. Neurosci. 2010, 30:2600-2610.
39. Noctor S.C., Flint A.C., Weissman T.A., Wong W.S., Clinton B.K., Kriegstein A.R. Dividing precursor cells of the embryonic cortical ventricular zone have morphological and molecular characteristics of radial glia. J. Neurosci. 2002, 22:3161-3173.
40. Orkin S.H., Zon L.I. Hematopoiesis: An evolving paradigm for stem cell biology. Cell 2008, 132:631-644.
41. Palmer T.D., Willhoite A.R., Gage F.H. Vascular niche for adult hippocampal neurogenesis. J. Comp. Neurol. 2000, 425:479-494.
42. Parada C., Gato A., Bueno D. Mammalian embryonic cerebrospinal fluid proteome has greater apolipoprotein and enzyme pattern complexity than the avian proteome. J. Proteome Res. 2005, 4:2420-2428.
43. Pinal N., Goberdhan D.C., Collinson L., Fujita Y., Cox I.M., Wilson C., Pichaud F. Regulated and polarized PtdIns(3,4,5)P3 accumulation is essential for apical membrane morphogenesis in photoreceptor epithelial cells. Curr. Biol. 2006, 16:140-149.
44. Popken G.J., Hodge R.D., Ye P., Zhang J., Ng W., O'Kusky J.R., D'Ercole A.J. In vivo effects of insulin-like growth factor-I (IGF-I) on prenatal and early postnatal development of the central nervous system. Eur. J. Neurosci. 2004, 19:2056-2068.
45. Purves D. Body and Brain. A Trophic Theory of Neural Connections 1988, Harvard University Press, Cambridge, MA.
46. Randhawa R., Cohen P. The role of the insulin-like growth factor system in prenatal growth. Mol. Genet. Metab. 2005, 86:84-90.
47. Reynolds B.A., Weiss S. Clonal and population analyses demonstrate that an EGF-responsive mammalian embryonic CNS precursor is a stem cell. Dev. Biol. 1996, 175:1-13.
48. Sawamoto K., Wichterle H., Gonzalez-Perez O., Cholfin J.A., Yamada M., Spassky N., Murcia N.S., Garcia-Verdugo J.M., Marin O., Rubenstein J.L., et al. New neurons follow the flow of cerebrospinal fluid in the adult brain. Science 2006, 311:629-632.
49. Scadden D.T. The stem-cell niche as an entity of action. Nature 2006, 441:1075-1079.
50. Schubert M., Brazil D.P., Burks D.J., Kushner J.A., Ye J., Flint C.L., Farhang-Fallah J., Dikkes P., Warot X.M., Rio C., et al. Insulin receptor substrate-2 deficiency impairs brain growth and promotes tau phosphorylation. J. Neurosci. 2003, 23:7084-7092.
51. Shen Q., Goderie S.K., Jin L., Karanth N., Sun Y., Abramova N., Vincent P., Pumiglia K., Temple S. Endothelial cells stimulate self-renewal and expand neurogenesis of neural stem cells. Science 2004, 304:1338-1340.
52. Shen Q., Wang Y., Kokovay E., Lin G., Chuang S.M., Goderie S.K., Roysam B., Temple S. Adult SVZ stem cells lie in a vascular niche: A quantitative analysis of niche cell-cell interactions. Cell Stem Cell 2008, 3:289-300.
53. Shimogori T., Banuchi V., Ng H.Y., Strauss J.B., Grove E.A. Embryonic signaling centers expressing BMP, WNT and FGF proteins interact to pattern the cerebral cortex. Development 2004, 131:5639-5647.
54. Siegenthaler J.A., Ashique A.M., Zarbalis K., Patterson K.P., Hecht J.H., Kane M.A., Folias A.E., Choe Y., May S.R., Kume T., et al. Retinoic acid from the meninges regulates cortical neuron generation. Cell 2009, 139:597-609.
55. Siller K.H., Doe C.Q. Spindle orientation during asymmetric cell division. Nat. Cell Biol. 2009, 11:365-374.
56. Soroceanu L., Kharbanda S., Chen R., Soriano R.H., Aldape K., Misra A., Zha J., Forrest W.F., Nigro J.M., Modrusan Z., et al. Identification of IGF2 signaling through phosphoinositide-3-kinase regulatory subunit 3 as a growth-promoting axis in glioblastoma. Proc. Natl. Acad. Sci. USA 2007, 104:3466-3471.
57. Stylianopoulou F., Efstratiadis A., Herbert J., Pintar J. Pattern of the insulin-like growth factor II gene expression during rat embryogenesis. Development 1988, 103:497-506.
58. Sun Y., Goderie S.K., Temple S. Asymmetric distribution of EGFR receptor during mitosis generates diverse CNS progenitor cells. Neuron 2005, 45:873-886.
59. Tavazoie M., Van der Veken L., Silva-Vargas V., Louissaint M., Colonna L., Zaidi B., Garcia-Verdugo J.M., Doetsch F. A specialized vascular niche for adult neural stem cells. Cell Stem Cell 2008, 3:279-288.
60. Vasioukhin V., Bauer C., Degenstein L., Wise B., Fuchs E. Hyperproliferation and defects in epithelial polarity upon conditional ablation of alpha-catenin in skin. Cell 2001, 104:605-617.
61. Vescovi A.L., Reynolds B.A., Fraser D.D., Weiss S. bFGF regulates the proliferative fate of unipotent (neuronal) and bipotent (neuronal/astroglial) EGF-generated CNS progenitor cells. Neuron 1993, 11:951-966.
62. von Stein W., Ramrath A., Grimm A., Müller-Borg M., Wodarz A. Direct association of Bazooka/PAR-3 with the lipid phosphatase PTEN reveals a link between the PAR/aPKC complex and phosphoinositide signaling. Development 2005, 132:1675-1686.
63. Weber M.M., Melmed S., Rosenbloom J., Yamasaki H., Prager D. Rat somatotroph insulin-like growth factor-II (IGF-II) signaling: role of the IGF-I receptor. Endocrinology 1992, 131:2147-2153.
64. Wodarz A. Molecular control of cell polarity and asymmetric cell division in Drosophila neuroblasts. Curr. Opin. Cell Biol. 2005, 17:475-481.
65. Wu H., Feng W., Chen J., Chan L.N., Huang S., Zhang M. PDZ domains of Par-3 as potential phosphoinositide signaling integrators. Mol. Cell 2007, 28:886-898.
66. Ye P., Popken G.J., Kemper A., McCarthy K., Popko B., D'Ercole A.J. Astrocyte-specific overexpression of insulin-like growth factor-I promotes brain overgrowth and glial fibrillary acidic protein expression. J. Neurosci. Res. 2004, 78:472-484.
67. Ye P., Hu Q., Liu H., Yan Y., D'Ercole A.J. β-catenin mediates insulin-like growth factor-I actions to promote cyclin D1 mRNA expression, cell proliferation and survival in oligodendroglial cultures. Glia 2010, 58:1031-1041.
68. Zappaterra M.D., Lisgo S.N., Lindsay S., Gygi S.P., Walsh C.A., Ballif B.A. A comparative proteomic analysis of human and rat embryonic cerebrospinal fluid. J. Proteome Res. 2007, 6:3537-3548.
69. Zhang C.C., Lodish H.F. Insulin-like growth factor 2 expressed in a novel fetal liver cell population is a growth factor for hematopoietic stem cells. Blood 2004, 103:2513-2521.
70. Zhou C.J., Borello U., Rubenstein J.L., Pleasure S.J. Neuronal production and precursor proliferation defects in the neocortex of mice with loss of function in the canonical Wnt signaling pathway. Neuroscience 2006, 142:R1119-1131.