Adult ependymal cells are postmitotic and are derived from radial glial cells during embryogenesis

Journal of Neuroscience

Volumn 25, Issue 1, 2005, Pages 10-18

  Spassky, Nathalie ^a,b   Merkle, Florian T ^a   Flames, Nuria ^c   Tramontin, Anthony D ^a   García Verdugo, José Manuel ^c   Alvarez Buylla, Arturo ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b PITIÉ SALPÊTRIÈRE HOSPITAL   (France)

^c UNIVERSITY OF VALENCIA   (Spain)

Author keywords

Cilia; Deuterosomes; Ependyma; Lateral ventricle; Proliferation; Radial glia; Ventricular zone

Indexed keywords

BROXURIDINE; THYMIDINE DERIVATIVE; THYMIDINE H 3; UNCLASSIFIED DRUG;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CELL DIFFERENTIATION; CELL DIVISION; CELL LABELING; CELL MATURATION; CELL PROLIFERATION; CELL TRANSFORMATION; CONFOCAL MICROSCOPY; CONTROLLED STUDY; ELECTRON MICROSCOPY; EMBRYO; EMBRYO DEVELOPMENT; EPENDYMA CELL; GLIA CELL; MALE; MITOSIS; MOUSE; NEWBORN; NONHUMAN; PRIORITY JOURNAL;

AGE FACTORS; AMINO ACID TRANSPORT SYSTEM X-AG; ANIMALS; BROMODEOXYURIDINE; CELL DIFFERENTIATION; CELL LINEAGE; CELL NUCLEUS; CILIA; EPENDYMA; GLUTAMATE PLASMA MEMBRANE TRANSPORT PROTEINS; IMMUNOHISTOCHEMISTRY; MALE; MICE; MITOSIS; NEUROGLIA; ORGANELLES; S100 PROTEINS; STEM CELLS; SYMPORTERS; THYMIDINE; TIME FACTORS; TRITIUM;

EID: 12144262775     PISSN: 02706474     EISSN: None     Source Type: Journal    
DOI: 10.1523/JNEUROSCI.1108-04.2005     Document Type: Article

References (56)

1. Altman J (1963) Autoradiographic investigation of cell proliferation in the brains of rats and cats. Anat Rec 145:573-591.
2. Alvarez-Buylla A, Garcia-Verdugo JM, Mateo AS, Merchant-Larios H (1998) Primary neural precursors and intermitotic nuclear migration in the ventricular zone of adult canaries. J Neurosci 18:1020-1037.
3. Alvarez-Buylla A, Garcia-Verdugo JM, Tramontin AD (2001) A unified hypothesis on the lineage of neural stem cells. Nat Rev Neurosci 2:287-293.
4. Alvarez-Buylla A, Seri B, Doetsch F (2002) Identification of neural stem cells in the adult vertebrate brain. Brain Res Bull 57:751-758.
5. Bleier R (1971) The relations of ependyma to neurons and capillaries in the hypothalamus: a Golgi-Cox study. J Comp Neurol 142:439-463.
6. Brody SL, Yan XH, Wuerffel MK, Song SK, Shapiro SD (2000) Ciliogenesis and left-right axis defects in forkhead factor HFH-4-null mice. Am J Respir Cell Mol Biol 23:45-51.
7. Bruni JE (1998) Ependymal development, proliferation, and functions: a review. Microsc Res Tech 41:2-13.
8. Capela A, Temple S (2002) LeX/ssea-1 is expressed by adult mouse CNS stem cells, identifying them as nonependymal. Neuron 35:865-875.
9. Cathcart III RS, Worthington Jr WC (1964) Ciliary movement in the rat cerebral ventricles: clearing action and directions of currents. J Neuropathol Exp Neurol 23:609-618.
10. Chauhan AN, Lewis PD (1979) A quantitative study of cell proliferation in ependyma and choroid plexus in the postnatal rat brain. Neuropathol Appl Neurobiol 5:303-309.
11. Chiasson BJ, Tropepe V, Morshead CM, van der Kooy D (1999) Adult mammalian forebrain ependymal and subependymal cells demonstrate proliferative potential, but only subependymal cells have neural stem cell characteristics. J Neurosci 19:4462-4471.
12. Del Bigio MR (1995) The ependyma: a protective barrier between brain and cerebrospinal fluid. Glia 14:1-13.
13. de Vitry F, Picart R, Jacque C, Tixier-Vidal A (1981) Glial fibrillary acidic protein. A cellular marker of tanycytes in the mouse hypothalamus. Dev Neurosci 4:457-460.
14. Didier M, Harandi M, Aguera M, Bancel B, Tardy M, Fages C, Calas A, Stagaard M, Mollgard K, Belin MF (1986) Differential immunocytochemical staining for glial fibrillary acidic (GFA) protein, S-100 protein and glutamine synthetase in the rat subcommissural organ, nonspecialized ventricular ependyma and adjacent neuropil. Cell Tissue Res 245:343-351.
15. Dirksen ER (1971) Centriole morphogenesis in developing ciliated epithelium of the mouse oviduct. J Cell Biol 51:286-302.
16. Doetsch F, Alvarez-Buylla A (1996) Network of tangential pathways for neuronal migration in adult mammalian brain. Proc Natl Acad Sci USA 93:14895-14900.
17. Doetsch F, Garcia-Verdugo JM, Alvarez-Buylla A (1997) Cellular composition and three-dimensional organization of the subventricular germinal zone in the adult mammalian brain. J Neurosci 17:5046-5061.
18. Doetsch F, Caille I, Lim DA, Garcia-Verdugo JM, Alvarez-Buylla A (1999) Subventricular zone astrocytes are neural stem cells in the adult mammalian brain. Cell 97:703-716.
19. Doetsch F, Petreanu L, Caille I, Garcia-Verdugo JM, Alvarez-Buylla A (2002) EGF converts transit-amplifying neurogenic precursors in the adult brain into multipotent stem cells. Neuron 36:1021-1034.
20. Garcia-Verdugo JM, Perron S, Flames N, Collado L, Desfilis E, Font E (2002) The proliferative ventricular zone in adult vertebrates: a comparative study using reptiles, birds, and mammals. Brain Res Bull 57:765-775.
21. Gregg C, Weiss S (2003) Generation of functional radial glial cells by embryonic and adult forebrain neural stem cells. J Neurosci 23:11587-11601.
22. Hagiwara H, Shibasaki S, Ohwada N (1992) Ciliogenesis in the human oviduct epithelium during the normal menstrual cycle. J Electron Microsc (Tokyo) 41:321-329.
23. Hagiwara H, Ohwada N, Aoki T, Takata K (2000) Ciliogenesis and ciliary abnormalities. Med Electron Microsc 33:109-114.
24. Herrera DG, Garcia-Verdugo JM, Alvarez-Buylla A (1999) Adult-derived neural precursors transplanted into multiple regions in the adult brain. Ann Neurol 46:867-877.
25. Hinds JW, Ruffett TL (1971) Cell proliferation in the neural tube: an electron microscopic and Golgi analysis in the mouse cerebral vesicle. Z Zellforsch Mikrosk Anat 115:226-264.
26. Imamoto K, Paterson JA, Leblond CP (1978) Radioautographic investigation of gliogenesis in the corpus callosum of young rats. I. Sequential changes in oligodendrocytes. J Comp Neurol 180:115-128, 132-137.
27. Johansson CB, Momma S, Clarke DL, Risling M, Lendahl U, Frisen J (1999) Identification of a neural stem cell in the adult mammalian central nervous system. Cell 96:25-34.
28. Kerns JM, Hinsman EJ (1973) Neuroglial response to sciatic neurectomy. I. Light microscopy and autoradiography. J Comp Neurol 151:237-254.
29. Kobayashi Y, Watanabe M, Okada Y, Sawa H, Takai H, Nakanishi M, Kawase Y, Suzuki H, Nagashima K, Ikeda K, Motoyama N (2002) Hydrocephalus, situs inversus, chronic sinusitis, and male infertility in DNA polymerase lambda-deficient mice: possible implication for the pathogenesis of immotile cilia syndrome. Mol Cell Biol 22:2769-2776.
30. Korr H (1978) Combination of metallic impregnation and autoradiography of brain sections. A method for differentiation of proliferating glial cells in the brain of adult rats and mice. Histochemistry 59:111-116.
31. Korr H (1980) Proliferation of different cell types in the brain. Adv Anat Embryol Cell Biol 61:1-72.
32. 3H] thymidine in cerebrospinal tissue of young mice. J Neurol Sci 26:555-563.
33. Kuchler S, Graff MN, Gobaille S, Vincendon G, Roche AC, Delaunoy JP, Monsigny M, Zanetta JP (1994) Mannose dependent tightening of the rat ependymal cell barrier. In vivo and in vitro study using neoglycoproteins. Neurochem Int 24:43-55.
34. Lange BM, Faragher AJ, March P, Gull K (2000) Centriole duplication and maturation in animal cells. Curr Top Dev Biol 49:235-249.
35. Laywell ED, Rakic P, Kukekov VG, Holland EC, Steindler DA (2000) Identification of a multipotent astrocytic stem cell in the immature and adult mouse brain. Proc Natl Acad Sci USA 97:13883-13888.
36. Lim DA, Tramontin AD, Trevejo JM, Herrera DG, Garcia-Verdugo JM, Alvarez-Buylla A (2000) Noggin antagonizes BMP signaling to create a niche for adult neurogenesis. Neuron 28:713-726.
37. Loots GP, Nel PP (1989) Early stages of ciliogenesis in the respiratory epithelium of the nasal cavity of rabbit embryos. Cell Tissue Res 255:589-594.
38. Malatesta P, Hartfuss E, Gotz M (2000) Isolation of radial glial cells by fluorescent-activated cell sorting reveals a neuronal lineage. Development 127:5253-5263.
39. Malatesta P, Hack MA, Hartfuss E, Kettenmann H, Klinke W, Kirchhoff F, Gotz M (2003) Neuronal or glial progeny: regional differences in radial glia fate. Neuron 37:751-764.
40. Merkle FT, Tramontin AD, García-Verdugo JM, Alvarez-Buylla A (2004) Radial glia give rise to adult neural stem cells in the subventricular zone. Proc Natl Acad Sci USA, in press.
41. Millhouse OE (1971) A Golgi study of third ventricle tanycytes in the adult rodent brain. Z Zellforsch Mikrosk Anat 121:1-13.
42. Miyata T, Kawaguchi A, Okano H, Ogawa M (2001) Asymmetric inheritance of radial glial fibers by cortical neurons. Neuron 31:727-741.
43. Noctor SC, Flint AC, Weissman TA, Dammerman RS, Kriegstein AR (2001) Neurons derived from radial glial cells establish radial units in neocortex. Nature 409:714-720.
44. Novak A, Guo C, Yang W, Nagy A, Lobe CG (2000) Z/EG, a double reporter mouse line that expresses enhanced green fluorescent protein upon Cre-mediated excision. Genesis 28:147-155.
45. Rakic P, Sidman RL (1968) Subcommissural organ and adjacent ependyma: autoradiographic study of their origin in the mouse brain. Am J Anat 122:317-335.
46. Roth Y, Kimhi Y, Edery H, Aharonson E, Priel Z (1985) Ciliary motility in brain ventricular system and trachea of hamsters. Brain Res 330:291-297.
47. Sarnat HB (1992) Role of human fetal ependyma. Pediatr Neurol 8:163-178.
48. Sarnat HB (1995) Ependymal reactions to injury. A review. J Neuropathol Exp Neurol 54:1-15.
49. Smart I (1961) The subependymal layer of the mouse brain and its cell production as shown by radioautography after thymidine-H3 injection. J Comp Neurol 116:325-338.
50. Soriano P (1999) Generalized lacZ expression with the ROSA26 Cre reporter strain. Nat Genet 21:70-71.
51. Sorokin SP (1968) Centriole formation and ciliogenesis. Aspen Emphysema Conf 11:213-216.
52. Tamamaki N, Nakamura K, Okamoto K, Kaneko T (2001) Radial glia is a progenitor of neocortical neurons in the developing cerebral cortex. Neurosci Res 41:51-60.
53. Taulman PD, Haycraft CJ, Balkovetz DF, Yoder BK (2001 ) Polaris, a protein involved in left-right axis patterning, localizes to basal bodies and cilia. Mol Biol Cell 12:589-599.
54. Tramontin AD, Garcia-Verdugo JM, Lim DA, Alvarez-Buylla A (2003) Postnatal development of radial glia and the ventricular zone (VZ): a continuum of the neural stem cell compartment. Cereb Cortex 13:580-587.
55. Voigt T (1989) Development of glial cells in the cerebral wall of ferrets: direct tracing of their transformation from radial glia into astrocytes. J Comp Neurol 289:74-88.
56. Worthington Jr WC, Cathcart III RS (1963) Ependymal cilia: distribution and activity in the adult human brain. Science 139:221-222.