Proliferation and differentiation of progenitor cells throughout the intact adult rat spinal cord

Journal of Neuroscience

Volumn 20, Issue 6, 2000, Pages 2218-2228

  Horner, Philip J ^a   Power, Ann E ^b   Kempermann, Gerd ^a,c   Kuhn, H Georg ^c   Palmer, Theo D ^a   Winkler, Jürgen ^b,c   Thal, Leon J ^b   Gage, Fred H ^a  

^a SALK INSTITUTE FOR BIOLOGICAL STUDIES   (United States)

^b UNIVERSITY OF CALIFORNIA   (United States)

^c UNIVERSITY OF REGENSBURG   (Germany)

Author keywords

Adult; Gliogenesis; Neurogenesis; Progenitor; Proliferation; Rat; Spinal cord; Stem cell

Indexed keywords

BROXURIDINE;

ADOLESCENT; ANIMAL CELL; ANIMAL TISSUE; ARTICLE; ASTROCYTE; CELL DIFFERENTIATION; CELL FATE; CELL MIGRATION; CELL PROLIFERATION; CELL STRUCTURE; GLIA CELL; MALE; NERVOUS SYSTEM DEVELOPMENT; NONHUMAN; OLIGODENDROGLIA; PLASTICITY; PRIORITY JOURNAL; RAT; SPINAL CORD; SPINAL CORD NERVE CELL; STEM CELL;

EID: 0034653399     PISSN: 02706474     EISSN: None     Source Type: Journal    
DOI: 10.1523/jneurosci.20-06-02218.2000     Document Type: Article

References (50)

1. 3 by cells in normal and injured mouse spinal cord. J Neuropathol Exp Neurol 21:597-609.
2. Altman J (1963) Autoradiographic investigation of cell proliferation in the brains of rats and cats. Anat Rec 145:573-591.
3. Antal M, Sholomenko GN, Moschovakis AK, Storm-Mathisen J, Heizmann CW, Hunziker W (1992) The termination pattern and postsynaptic targets of rubrospinal fibers in the rat spinal cord: a light and electron microscopic study. J Comp Neurol 325:22-37.
4. Arsenio Nunes ML, Sotelo C (1985) Development of the spinocerebellar system in the postnatal rat. J Comp Neurol 237:291-306.
5. Ashwell KW, Zhang LL (1992) Ontogeny of afferents to the fetal rat cerebellum. Acta Anat (Basel) 145:17-23.
6. Barres BA, Raff MC (1993) Proliferation of oligodendrocyte precursor cells depends on electrical activity in axons. Nature 361:258-260.
7. Barres BA, Raff MC (1994) Control of oligodendrocyte number in the developing rat optic nerve. Neuron 12:935-942.
8. Beattie MS, Bresnahan JC, Komon J, Tovar CA, Van Meter M, Anderson DK, Faden AI, Hsu CY, Noble LJ, Salzman S, Young W (1997) Endogenous repair after spinal cord contusion injuries in the rat. Exp Neurol 148:453-463.
9. Bhat RV, Axt KJ, Fosnaugh JS, Smith KJ, Johnson KA, Hill DE, Kinzler KW, Baraban JM (1996) Expression of the APC tumor suppressor protein in oligodendroglia. Glia 17:169-174.
10. Boyes BE, Kim SU, Lee V, Sung SC (1986) Immunohistochemical co-localization of S-100β and the glial fibrillary acidic protein in rat brain. Neuroscience 17:857-865.
11. Brakeman JS, Gu SH, Wang XB, Dolin G, Baraban J M (1999) Neuronal localization of the Adenomatous polyposis coli tumor suppressor protein. Neuroscience 91:661-672.
12. Bruni J E, Del Bigio MR, Clattenburg RE (1985) Ependyma: normal and pathological. A review of the literature. Brain Res 356:1-19.
13. Burne JF, Staple JK, Raff MC (1996) Glial cells are increased proportionally in transgenic optic nerves with increased numbers of axons. J Neurosci 16:2064-2073.
14. 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.
15. 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.
16. Espinosa de los Monteros A, Zhao P, Huang C, Pan T, Chang R, Nazarian R, Espejo D, de Vellis J (1997) Transplantation of CG4 oligodendrocyte progenitor cells in the myelin-deficient rat brain results in myelination of axons and enhanced oligodendroglial markers. J Neurosci Res 50:872-887.
17. Franklin RJ, Blakemore WF (1997) Transplanting oligodendrocyte progenitors into the adult CNS. J Anat 190:23-33.
18. Friedman B, Hockfield S, Black JA, Woodruff KA, Waxman SG (1989) In situ demonstration of mature oligodendrocytes and their processes: an immunocytochemical study with a new monoclonal antibody. Rip. Glia 2:380-390.
19. Frisen J, Johansson CB, Torok C, Risling M, Lendahl U (1995) Rapid, widespread, and long-lasting induction of nestin contributes to the generation of glial scar tissue after CNS injury. J Cell Biol 131:453-464.
20. Garcia-Verdugo JM, Doetsch F, Wichterle H, Lim DA, Alvarez-Buylla A (1998) Architecture and cell types of the adult subventricular zone: in search of the stem cells. J Neurobiol 36:234-248.
21. Gensert JM, Goldman JE (1996) In vivo characterization of endogenous proliferating cells in adult rat subcortical white matter. Glia 17:39-51.
22. Ghandour MS, Lahourdette G, Vincendon G, Gombos G (1981) A biochemical and immunohistological study of S100 protein in developing rat cerebellum. Dev Neurosci 4:98-109.
23. Hammang JP, Archer DR, Duncan ID (1997) Myelination following transplantation of EGF-responsive neural stem cells into a myelin-deficient environment. Exp Neurol 147:84-95.
24. Hommes OR, Leblond CP (1967) Mitotic division of neuroglia in the normal adult rat. J Comp Neurol 129:269-278.
25. Jhaveri S, Erzurumlu RS, Friedman B, Schneider GE (1992) Oligodendrocytes and myelin formation along the optic tract of the developing hamster: an immunohistochemical study using the Rip antibody. Glia 6:138-148.
26. 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.
27. Joosten EA, Gribnau AA, Dederen PJ (1987) An anterograde tracer study of the developing corticospinal tract in the rat: three components. Brain Res 433:121-130.
28. Kaplan MS, Hinds JW (1980) Gliogenesis of astrocytes and oligodendrocytes in the neocortical grey and white matter of the adult rat: electron microscopic analysis of light radioautographs. J Comp Neurol 193:711-727.
29. Keirstead HS, Levine JM, Blakemore WF (1998) Response of the oligodendrocyte progenitor cell population (defined by NG2 labeling) to demyelination of the adult spinal cord. Glia 22:161-170.
30. Korr H, Horsmann C, Schurmann M, Delaunoy JP, Labourdette G (1994) Problems encountered when immunocytochemistry is used for quantitative glial cell identification in autoradiographic studies of cell proliferation in the brain of the unlesioned adult mouse. Cell Tissue Res 278:85-95.
31. Kudo N, Furukawa F, Okado N (1993) Development of descending fibers to the rat embryonic spinal cord. Neurosci Res 16:131-141.
32. Laeng P, Molthagen M, Yu EG, Bartsch U (1996) Transplantation of oligodendrocyte progenitor cells into the rat retina: extensive myelination of retinal ganglion cell axons. Glia 18:200-210.
33. Lee MK, Tuttle JB, Rebhun LI, Cleveland DW, Frankfurter A (1990) The expression and posttranslational modification of a neuron-specific β-tubulin isotype during chick embryogenesis. Cell Motil Cytoskel 17:118-132.
34. Levine JM, Stallcup W B (1987) Plasticity of developing cerebellar cells in vitro studied with antibodies against the NG2 antigen. J Neurosci 7:2721-2731.
35. Mares V, Lodin Z, Jilek M (1975) An estimate of the number of cells arising by division in mouse cerebral hemispheres from age one to 12 months: an autoradiographic study of DNA synthesis. J Comp Neurol 161:471-482.
36. McCarthy GF, Leblond CP (1988) Radioautographic evidence for slow astrocyte turnover and modest oligodendrocyte production in the corpus callosum of adult mice infused with 3H-thymidine. J Comp Neurol 271:589-603.
37. McTigue DM, Horner PJ, Stokes BT, Gage FH (1998) Neurotrophin-3 and brain-derived neurotrophic factor induce oligodendrocyte proliferation, migration, and myelination in the contused adult rat spinal cord. J Neurosci 18:5354-5365.
38. Morshead CM, Reynolds BA, Craig CG, McBurney MW, Staines WA, Morassutti D, Weiss S, van der Kooy D (1994) Neural stem cells in the adult mammalian forebrain: a relatively quiescent subpopulation of subependymal cells. Neuron 13:1071-1082.
39. Nishiyama A, Lin XH, Giese N, Heldin CH, Stallcup W B (1996) Colocalization of NG2 proteoglycan and PDGF alpha-receptor on O2A progenitor cells in the developing rat brain. J Neurosci Res 43:299-314.
40. Prayoonwiwat N, Rodriguez M (1993) The potential for oligodendrocyte proliferation during demyelinating disease. J Neuropathol Exp Neurol 52:55-63.
41. Raff MC, Miller RH, Noble M (1983) A glial progenitor cell that develops in vitro into an astrocyte or an oligodendrocyte depending on culture medium. Nature 303:390-396.
42. Reynolds R, Hardy R (1997) Oligodendroglial progenitors labeled with the O4 antibody persist in the adult rat cerebral cortex in vivo. J Neurosci Res 47:455-470.
43. Sarnat HB, Nochlin D, Born DE (1998) Neuronal nuclear antigen (NeuN): a marker of neuronal maturation in early human fetal nervous system. Brain Dev 20:88-94.
44. Senda T, Iino S, Matsushita K, Matsumine A, Kobayashi S, Akiyama T (1998) Localization of the adenomatous polyposis coli tumour suppressor protein in the mouse central nervous system. Neuroscience 83:857-866.
45. Shihabuddin LS, Ray J, Gage FH (1997) FGF-2 is sufficient to isolate progenitors found in the adult mammalian spinal cord. Exp Neurol 148:577-586.
46. Takahashi T, Nowakowski RS, Caviness VS (1996) The leaving or Q fraction of the murinc cerebral proliferative epithelium: a general model of neocortical neuronogenesis. J Neurosci 16:6183-6196.
47. Warrington AE, Barbarese E, Pfeiffer SE (1992) Stage specific, (O4+GalC-) isolated oligodendrocyte progenitors produce MBP+ myelin in vivo. Dev Neurosci 14:93-97.
48. Weiss S, Dunne C, Hewson J, Wohl C, Wheatley M, Peterson AC, Reynolds BA (1996) Multipoint CNS stem cells are present in the adult mammalian spinal cord. J Neurosci 16:7599-7609.
49. Wolf HK, Buslei R, Schmidt-Kastner R, Schmidt-Kastner PK, Pietsch T, Wiestler OD, Bluhmke I (1996) NeuN: a useful neuronal marker for diagnostic histopathology. J Histochem Cytochem 44:1167-1171.
50. Wren D, Wolswijk G, Noble M (1992) In vitro analysis of the origin and maintenance of O-2Aadult progenitor cells. J Cell Biol 116: 167-176.