A mesenchymal-like ZEB1+ niche harbors dorsal radial glial fibrillary acidic protein-positive stem cells in the spinal cord

Stem Cells

Volumn 27, Issue 11, 2009, Pages 2722-2733

  Sabourin, Jean Charles ^a   Ackema, Karin B ^b   Ohayon, David ^a   Guichet, Pierre Olivier ^a   Perrin, Florence E ^a   Garces, Alain ^a   Ripoll, Chantal ^a   Charité, Jeroen ^c   Simonneau, Lionel ^d   Kettenmann, H ^e   Zine, Azel ^a   Privat, Alain ^a   Valmier, Jean ^a   Pattyn, Alexandre ^a   Hugnot, Jean Philippe ^a  

^a HÔPITAL SAINT ELOI   (France)

^b UNIVERSITY OF BASEL   (Switzerland)

^c ERASMUS MEDICAL CENTER   (Netherlands)

^d UNIV MONTPELLIER   (France)

^e MAX DELBRÜCK CENTER FOR MOLECULAR MEDICINE   (Germany)

Author keywords

Neural stem cells; Niche; Spinal cord; ZEB1

Indexed keywords

CD15 ANTIGEN; DOUBLECORTIN; GLIAL FIBRILLARY ACIDIC PROTEIN; GREEN FLUORESCENT PROTEIN; JAGGED1; SMOOTH MUSCLE ACTIN; TRANSCRIPTION FACTOR HES 1; UNCLASSIFIED DRUG; ZINC FINGER E BOX BINDING PROTEIN 1; ZINC FINGER PROTEIN;

ADULT; ANIMAL EXPERIMENT; ARTICLE; CELL PROLIFERATION; CELL SURVIVAL; CENTRAL NERVOUS SYSTEM; CERVICAL SPINAL CORD; DEGENERATIVE DISEASE; ECOLOGICAL NICHE; EPENDYMA CELL; HIPPOCAMPUS; HOX GENE; HUMAN; IN VITRO STUDY; LUMBAR SPINAL CORD; MESENCHYMAL STEM CELL; MICRODISSECTION; MOUSE; NERVE CELL; NEURAL STEM CELL; NEUROBLASTOMA; NONHUMAN; PIA MATER; POSTNATAL DEVELOPMENT; SCREENING; SIGNAL TRANSDUCTION; SPINAL CORD; SPINAL CORD INJURY; STEM CELL; SUBVENTRICULAR ZONE; SURFACE PROPERTY; TRANSGENIC MOUSE;

ACTINS; ANIMALS; CELL PROLIFERATION; GENE EXPRESSION REGULATION, DEVELOPMENTAL; GLIAL FIBRILLARY ACIDIC PROTEIN; GREEN FLUORESCENT PROTEINS; HOMEODOMAIN PROTEINS; KRUPPEL-LIKE TRANSCRIPTION FACTORS; MICE; MICE, TRANSGENIC; NEURONS; SPINAL CORD; STEM CELL NICHE; STEM CELLS;

MUS MUSCULUS; RODENTIA;

EID: 73049111612     PISSN: 10665099     EISSN: None     Source Type: Journal    
DOI: 10.1002/stem.226     Document Type: Article

References (51)

1. Weiss S, Dunne C, Hewson J et al. Multipotent CNS stem cells are present in the adult mammalian spinal cord and ventricular neuroaxis. J Neurosci 1996;16:7599-7609. (Pubitemid 26389699)
2. Kehl LJ, Fairbanks CA, Laughlin TM et al. Neurogenesis in postnatal rat spinal cord: a study in primary culture. Science 1997;276:586-589.
3. Shihabuddin LS, Ray J, Gage FH. FGF-2 is sufficient to isolate progenitors found in the adult mammalian spinal cord. Exp Neurol 1997;148:577-586. (Pubitemid 28068850)
4. Martens DJ, Seaberg RM, Van der Kooy D. In vivo infusions of exogenous growth factors into the fourth ventricle of the adult mouse brain increase the proliferation of neural progenitors around the fourth ventricle and the central canal of the spinal cord. Eur J Neurosci 2002;16:1045-1057.
5. Barnabé-Heider F, Frisen J. Stem cells for spinal cord repair. Cell Stem Cell 2008;3:16-24.
6. Danilov AI, Covacu R, Moe MC et al. Neurogenesis in the adult spinal cord in an experimental model of multiple sclerosis. Eur J Neurosci 2006;23:394-400.
7. Shechter R, Ziv Y, Schwartz M. New GABAergic interneurons supported by myelin-specific T cells are formed in intact adult spinal cord. Stem Cells 2007;25:2277-2282. (Pubitemid 47480486)
8. Ke Y, Chi L, Xu R et al. Early response of endogenous adult neural progenitor cells to acute spinal cord injury in mice. Stem Cells 2006;24:1011-1019. (Pubitemid 44464734)
9. Chi L, Ke Y, Luo C et al. Motor neuron degeneration promotes neural progenitor cell proliferation, migration, and neurogenesis in the spinal cords of amyotrophic lateral sclerosis mice. Stem Cells 2006;24:34-43.
10. Moreno-Manzano V, Rodriguez-Jimenez FJ, Garcia-Rosello M et al. Activated spinal cord ependymal stem cells rescue neurological function. Stem Cells 2009;27:733-743.
11. Meletis K, Barnabe-Heider F, Carlen M et al. Spinal cord injury reveals multilineage differentiation of ependymal cells. Plos Biol 2008;6:e182.
12. Johansson CB, Momma S, Clarke DL et al. Identification of a neural stem cell in the adult mammalian central nervous system. Cell 1999;96:25-34. (Pubitemid 29044150)
13. Corti S, Locatelli F, Papadimitriou D et al. Transplanted ALDHhiS-SClo neural stem cells generate motor neurons and delay disease progression of nmd mice, an animal model of SMARD1. Hum Mol Genet 2006;15:167-187. (Pubitemid 43125973)
14. Dromard C, Guillon H, Rigau V et al. Adult human spinal cord harbors neural precursor cells that generate neurons and glial cells in vitro. J Neurosci Res 2008;86:1916-1926.
15. Nolte C, Matyash M, Pivneva T et al. GFAP promoter-controlled EGFP-expressing transgenic mice: a tool to visualize astrocytes and astrogliosis in living brain tissue. Glia 2001;33:72-86. (Pubitemid 32102818)
16. Deleyrolle L, Marchal-Victorion S, Dromard C et al. Exogenous and fibroblast growth factor 2/epidermal growth factor-regulated endogenous cytokines regulate neural precursor cell growth and differentiation. Stem Cells 2006;24:748-762. (Pubitemid 44464780)
17. Dromard C, Bartolami S, Deleyrolle L et al. NG2 and Olig2 expression provides evidence for phenotypic deregulation of cultured central nervous system and peripheral nervous system neural precursor cells. Stem Cells 2007;25:340-353. (Pubitemid 46232788)
18. Louis SA, Rietze RL, Deleyrolle L et al. Enumeration of neural stem and progenitor cells in the neural colony-forming cell assay. Stem Cells 2008;26:988-996.
19. Gurok U, Steinhoff C, Lipkowitz B et al. Gene expression changes in the course of neural progenitor cell differentiation. J Neurosci 2004;24:5982-6002. (Pubitemid 38859395)
20. Capela A, Temple S. LeX is expressed by principle progenitor cells in the embryonic nervous system, is secreted into their environment and binds Wnt-1. Dev Biol 2006;291:300-313.
21. Fu H, Qi Y, Tan M et al. Molecular mapping of the origin of postnatal spinal cord ependymal cells: evidence that adult ependymal cells are derived from Nkx6.1+ ventral neural progenitor cells. J Comp Neurol 2003;456:237-244. (Pubitemid 36110246)
22. Peinado H, Olmeda D, Cano A. Snail, Zeb and Bhlh factors in tumour progression: an alliance against the epithelial phenotype? Nat Rev Cancer 2007;7:415-428.
23. Chojnacki AK, Mak GK, Weiss S. Identity crisis for adult periventricular neural stem cells: subventricular zone astrocytes, ependymal cells or both? Nat Rev Neurosci 2009;10:153-163.
24. Postigo AA, Dean DC. ZEB, a vertebrate homolog of Drosophila Zfh-1, is a negative regulator of muscle differentiation. EMBO J 1997;16:3935-3943.
25. Carpenter EM. Hox genes and spinal cord development. Dev Neurosci 2002;24:24-34.
26. Mirzadeh Z, Merkle FT, Soriano-Navarro M et al. Neural stem cells confer unique pinwheel architecture to the ventricular surface in neurogenic regions of the adult brain. Cell Stem Cell 2008;3:265-278.
27. Doetsch F, Garcia-Verdugo JM, Alvarez-Buylla A. Regeneration of a germinal layer in the adult mammalian brain. Proc Natl Acad Sci U S A 1999;96:11619-11624. (Pubitemid 29487430)
28. Vigh B, Manzano e Silva MJ, Frank CL et al. The system of cerebrospinal fluid-contacting neurons: its supposed role in the nonsynaptic signal transmission of the brain. Histol Histopathol 2004;19:607-628.
29. Bruni JE. Ependymal development, proliferation, and functions: a review. Microsc Res Tech 1998;41:2-13.
30. Ramon y Cajal S. Histologie du Système Nerveux de L'hommes et des Vertébrés. Paris: Maloine, 1911.
31. Roelofs RF, Fischer DF, Houtman SH et al. Adult human subventricular, subgranular, and subpial zones contain astrocytes with a specialized intermediate filament cytoskeleton. Glia 2005;52:289-300.
32. Doetsch F, Petreanu L, Caille I et al. EGF converts transit-amplifying neurogenic precursors in the adult brain into multipotent stem cells. Neuron 2002;36:1021-1034. (Pubitemid 36044505)
33. Rafols JA, Goshgarian HG. Spinal tanycytes in the adult rat: a correlative Golgi gold-toning study. Anat Rec 1985;211:75-86. (Pubitemid 15174477)
34. Bruni JE, Reddy K. Ependyma of the central canal of the rat spinal cord: a light and transmission electron microscopic study. J Anat 1987;152:55-70. (Pubitemid 17121524)
35. Seitz R, Lohler J, Schwendemann G. Ependyma and meninges of the spinal cord of the mouse: a light-and electron-microscopic study. Cell Tissue Res 1981;220:61-72. (Pubitemid 12227278)
36. Anthony TE, Klein C, Fishell G et al. Radial glia serve as neuronal progenitors in all regions of the central nervous system. Neuron 2004;41:881-890. (Pubitemid 38429732)
37. Tavazoie M, Van der Veken L, Silva-Vargas V et al. A specialized vascular niche for adult neural stem cells. Cell Stem Cell 2008;3:279-288.
38. Shen Q, Wang Y, Kokovay E et al. Adult SVZ stem cells lie in a vascular niche: a quantitative analysis of niche cell-cell interactions. Cell Stem Cell 2008;3:289-300.
39. Marichal N, Garcia G, Radmilovich M et al. Enigmatic central canal contacting cells: immature neurons in "standby mode"? J Neurosci 2009;29:10010-10024.
40. Anthony TE, Mason HA, Gridley T et al. Brain lipid-binding protein is a direct target of Notch signaling in radial glial cells. Genes Dev 2005;19:1028-1033. (Pubitemid 40632448)
41. Carlén M, Meletis K, Goritz C et al. Forebrain ependymal cells are Notch-dependent and generate neuroblasts and astrocytes after stroke. Nat Neurosci 2009;12:259-267.
42. Ninkovic J, Gotz M. Signaling in adult neurogenesis: from stem cell niche to neuronal networks. Curr Opin Neurobiol 2007;17:338-344. (Pubitemid 46887663)
43. Balemans W, Van Hul W. Extracellular regulation of BMP signaling in vertebrates: a cocktail of modulators. Dev Biol 2002;250:231-250. (Pubitemid 35216412)
44. Alvarez-Buylla A, Lim DA. For the long run: maintaining germinal niches in the adult brain. Neuron 2004;41:683-686. (Pubitemid 38326831)
45. Morel AP, Lievre M, Thomas C et al. Generation of breast cancer stem cells through epithelial-mesenchymal transition. Plos One 2008;3:e2888.
46. Mani SA, Guo W, Liao MJ et al. The epithelial-mesenchymal transition generates cells with properties of stem cells. Cell 2008;133:704-715. (Pubitemid 351636299)
47. Nishimura G, Manabe I, Tsushima K et al. DeltaEF1 mediates TGF-beta signaling in vascular smooth muscle cell differentiation. Dev Cell 2006;11:93-104. (Pubitemid 43960803)
48. Leatherman JL, Dinardo S. Zfh-1 controls somatic stem cell self-renewal in the Drosophila testis and nonautonomously influences germline stem cell self-renewal. Cell Stem Cell 2008;3:44-54.
49. Lledo PM, Merkle FT, Alvarez-Buylla A. Origin and function of olfactory bulb interneuron diversity. Trends Neurosci 2008;31:392-400.
50. Kulbatski I, Tator CH. Region-specific differentiation potential of adult rat spinal cord neural stem/precursors and their plasticity in response to in vitro manipulation. J Histochem Cytochem 2009;57:405-423.
51. Thuret S, Moon LD, Gage FH. Therapeutic interventions after spinal cord injury. Nat Rev Neurosci 2006;7:628-643. (Pubitemid 44106745)