Defining the NG2-expressing cell of the adult CNS

Journal of Neurocytology

Volumn 31, Issue 6-7, 2002, Pages 469-480

  Borner, Philip J ^a   Thallmair, Michaela ^b   Gage, Fred H ^b  

^a UNIVERSITY OF WASHINGTON SCHOOL OF MEDICINE   (United States)

^b SALK INSTITUTE FOR BIOLOGICAL STUDIES   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BROXURIDINE; GREEN FLUORESCENT PROTEIN; NG2 PROTEOGLYCAN; PLATELET DERIVED GROWTH FACTOR ALPHA RECEPTOR; PROTEOCHONDROITIN SULFATE; UNCLASSIFIED DRUG;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; BRAIN DEVELOPMENT; CELL MIGRATION; CELL PROLIFERATION; CENTRAL NERVOUS SYSTEM; CONTROLLED STUDY; GENE EXPRESSION; IN SITU HYBRIDIZATION; KNOCKOUT MOUSE; MOUSE; MYELINATION; NERVE CELL PLASTICITY; NONHUMAN; OLIGODENDROGLIA; PRIORITY JOURNAL; REVIEW; SPINAL CORD; STEM CELL; TRANSGENIC MOUSE;

ANIMALS; ANTIGENS; CELL DIFFERENTIATION; CELL LINEAGE; CENTRAL NERVOUS SYSTEM; HUMANS; NERVE REGENERATION; NEUROGLIA; NEURONAL PLASTICITY; PROTEOGLYCANS; STEM CELLS;

ANIMALIA; MUS MUSCULUS;

EID: 0242347594     PISSN: 03004864     EISSN: None     Source Type: Journal    
DOI: 10.1023/A:1025739630398     Document Type: Review

References (73)

1. ADRIAN, E. K. & WALKER, B. E. (1962) Incorporation of thymidine-H3 by cells in normal and injured mouse spinal cord. Journal of Neuropathology and Experimental Neurology 21, 597-609.
2. ALTMAN, J. & BAYER, S. A. (1990) Migration and distribution of two populations of hippocampal granule cell precursors during the prenatal and postnatal periods. journal of Comparative Neurology 301, 365-381.
3. ALTMAN, J. & DAS, G. D. (1965a) Post-natal origin of microneurones in the rat brain. Nature 207, 953-956.
4. ALTMAN, J. & DAS, G. D. (1965b) Autoradiographic and histological evidence of postnatal hippocampal neurogenesis in rats. Journal of Comparative Neurology 124, 1098-1101.
5. BAYER, S. A., YACKEL, J. W. & PURI, P. S. (1982) Neurons in the rat dentate gyrus granular layer substantially increase during juvenile and adult life. Science 216, 890-892.
6. BIEBL, M., COOPER, C. M., WINKLER, J. & KUHN, H. G. (2000) Analysis of neurogenesis and programmed cell death reveals a self-renewing capacity in the adult rat brain. Neuroscience Letters 291, 17-20.
7. BJUGN, R. (1993) The use of the optical disector to estimate the number of neurons, glial and endothelial cells in the spinal cord of the mouse - with a comparative note on the rat spinal cord. Brain Research 627, 25-33.
8. BJUGN, R. & GUNDERSEN, H. J. (1993) Estimate of the total number of neurons and glial and endothelial cells in the rat spinal cord by means of the optical disector. Journal of Comparative Neurology 328, 406-414.
9. BUTT, A. M., DUNCAN, A., HORNBY, M. F., KIRVELL, S. L., HUNTER, A., LEVINE, J. M. & BERRY, M. (1999) Cells expressing the NG2 antigen contact nodes of Ranvier in adult CNS white matter. Glia 26, 84-91.
10. CAMERON, H. A., WOOLLEY, C. S., McEWEN, B. S. & GOULD, E. (1993) Differentiation of newly born neurons and glia in the dentate gyrus of the adult rat. Neuroscience 56, 337-344.
11. CHANG, A., NISHIYAMA, A., PETERSON, J., PRINEAS, J. & TRAPP, B. D. (2000) NG2-positiveoligodendrocyte progenitor cells in adult human brain and multiple sclerosis lesions. Journal of Neuroscience 20, 6404-6412.
12. DAWSON, M. R., LEVINE, J. M. & REYNOLDS, R. (2000) NG2-expressing cells in the central nervous system: Are they oligodendroglial progenitors? Journal of Neuroscience Research 61, 471-479.
13. DIERS-FENGER, M., KIRCHHOFF, F., KETTENMANN, H., LEVINE, J. M. & TROTTER, J. (2001) AN2/NG2 protein-expressing glial progenitor cells in the murine CNS: Isolation, differentiation, and association with radial glia. Glia 34, 213-228.
14. ENGEL, U. & WOLSWIJK, G. (1996) Oligodendrocyte-type-2 astrocyte (O-2A) progenitor cells derived from adult rat spinal cord: In vitro characteristics and response to PDGF, bFGF and NT-3. Glia 16, 16-26.
15. ERLANDSSON, A., ENARSSON, M. & FORSBERG-NILSSON, K. (2001) Immature neurons from CNS stem cells proliferate in response to platelet-derived growth factor. Journal of Neuroscience 21, 3483-3491.
16. FANG, X., BURG, M. A., BARRITT, D., DAHLIN-HUPPE, K., NISHIYAMA, A. & STALLCUP, W. B. (1999) Cytoskeletal reorganization induced by engagement of the NG2 proteoglycan leads to cell spreading and migration. Molecular Biology of the Cell 10, 3373-3387.
17. FRANKLIN, R. J., GILSON, J. M. & BLAKEMORE, W. F. (1997) Local recruitment of remyelinating cells in the repair of demyelination in the central nervous system. Journal of Neuroscience Research 50, 337-344.
18. FRUTTIGER, M., KARLSSON, L., HALL, A. C., ABRAMSSON, A., CALVER, A. R., BOSTROM, H., WILLETTS, K., BERTOLD, C. H., HEATH, J. K., BETSHOLTZ, C. & RICHARDSON, W. D. (1999) Defective oligodendrocyte development and severe hypomyelination in PDGF-A knockout mice. Development 126, 457-467.
19. GAGE, F. H. (2000) Mammalian neural stem cells. Science 287, 1433-1438.
20. GAIANO, N. & FISHELL, G. (1998) Transplantation as a tool to study progenitors within the vertebrate nervous system. Journal of Neurobiology 36, 152-161.
21. GENSERT, J. M. & GOLDMAN, J. E. (1996) In vivo characterization of endogenous proliferating cells in adult rat subcortical white matter. Glia 17, 39-51.
22. GENSERT, J. M. & GOLDMAN, J. E. (1997) Endogenous progenitors remyelinate demyelinated axons in the adult CNS. Neuron 19, 197-203.
23. GENSERT, J. M. & GOLDMAN, J. E. (2001) Heterogeneity of cycling glial progenitors in the adult mammalian cortex and white matter. Journal of Neurobiology 48, 75-86.
24. GORETZKI, L., BURG, M. A., GRAKO, K. A. & STALLCUP, W. B. (1999) High-affinity binding of basic fibroblast growth factor and platelet-derived growth factor-AA to the core protein of the NG2 proteoglycan. Journal of Biological Chemistry 274, 16831-16837.
25. GRAKO, K. A., OCHIYA, T., BARRITT, D., NISHIYAMA, A. & STALLCUP, W. B. (1999) PDGF (alpha)-receptoris unresponsive to PDGF-AA in aortic smooth muscle cells from the NG2 knockout mouse. Journal of Cell Science 112, 905-915.
26. HART, I. K., RICHARDSON, W. D., HELDIN, C. H., WESTERMARK, B. & RAFF, M. C. (1989) PDGF receptors on cells of the oligodendrocyte-type-2 astrocyte (O-2A) cell lineage. Development 105, 595-603.
27. HARTMANN, U. & MAURER, P. (2001) Proteoglycans in the nervous system - the quest for functional roles in vivo. Matrix Biology 20, 23-35.
28. HINKS, G. L. & FRANKLIN, R. J. (1999) Distinctive patterns of PDGF-A, FGF-2, IGF-I, and TGF-beta1 gene expression during remyelination of experimentally-induced spinal cord demyelination. Molecular and Cellular Neuroscience 14, 153-168.
29. HORNER, P. J., POWER, A. E., KEMPERMANN, G., KUHN, H. G., PALMER, T. D., WINKLER, J., THAL, L. J. & GAGE, F. H. (2000) Proliferation and differentiation of progenitor cells throughout the intact adult rat spinal cord. Journal of Neuroscience 20, 2218-2228.
30. IJICHI, A., NOEL, F., SAKUMA, S., WEIL, M. M. & TOFILON, P. J. (1996) Ex vivo gene delivery of platelet-derived growth factor increases 0-2A progenitors in adult rat spinal cord. Gene Therapy 3, 389-395.
31. JONES, L. L., YAMAGUCHI, Y., STALLCUP, W. B. & TUSZYNSKI, M. H. (2002) NG2 is a major chondroitin sulfate proteoglycan produced after spinal cord injury and is expressed by macrophages and oligodendrocyte progenitors. Journal of Neuroscience 22, 2792-2803.
32. KAKITA, A. & GOLDMAN, J. E. (1999) Patterns and dynamics of SVZ cell migration in the postnatal forebrain: Monitoring living progenitors in slice preparations. Neuron 23, 461-472.
33. KEIRSTEAD, H. S., LEVINE, J. M. & BLAKEMORE, W. F. (1998) Response of the oligodendrocyte progenitor cell population (defined by NG2 labelling) to demyelination of the adult spinal cord. Glia 22, 161-170.
34. KUHN, H. G., DICKINSON-ANSON, H. & GAGE, F. H. (1996) Neurogenesis in the dentate gyrus of the adult rat: Age-related decrease of neural progenitor populations. Journal of Neuroscience 16, 2027-2033.
35. LEVINE, J. M. (1994) Increased expression of the NG2 chondroitin-sulfate proteoglycan after brain injury. Journal of Neuroscience 14, 4716-4730.
36. LEVINE, J. M., BEASLEY, L. & STALLCUP, W. B. (1986) Localization of a neurectoderm-associated cell surface antigen in the developing and adult rat. Brain Research 392, 211-222.
37. LEVINE, J. M. & CARD, J. P. (1987) Light and electron microscopic localization of a cell surface antigen (NG2) in the rat cerebellum: Association with smooth protoplasmic astrocytes. Journal of Neuroscience 7, 2711-2720.
38. LEVINE, J. M. & NISHIYAMA, A. (1996) The NG2 chondroitin sulfate proteoglycan: A multifunctional proteoglycan associated with immature cells. Perspectives on Developmental Neurobiology 3, 245-259.
39. LEVINE, J. M. & STALLCUP, W. B. (1987) Plasticity of developing cerebellar cells in vitro studied with antibodies against the NG2 antigen. Journal of Neuroscience 7, 2721-2731.
40. LEVINE, J. M., STINCONE, F. &LEE, Y. S. (1993) Development and differentiation of glial precursor cells in the rat cerebellum. Glia 7, 307-321.
41. LEWIS, P. D. (1968) The fate of the subependymal cell in the adult rat, with a note on the origin of microglia. Brain 91, 721-736.
42. MALLON, B. S., SHICK, H. E., KIDD, G. J. & MACKLIN, W. B. (2002) Proteolipid promoter activity distinguishes two populations of NG2-positive cells throughout neonatal cortical development. Journal of Neuroscience 22, 876-885.
43. McKINNON, R. D., MATSUI, T., DUBOIS-DALCQ, M. & AARONSON, S. A. (1990) FGF modulates the PDGF-driven pathway of oligodendrocy te development. Neuron 5, 603-614.
44. McTIGUE, D. M., WEI, P. & STOKES, B. T. (2001) Proliferation of NG2-positive cells and altered oligodendrocyte numbers in the contused rat spinal cord. Journal of Neuroscience 21, 3392-3400.
45. MORSHEAD, C. M., CRAIG, C. G. & VAN DER KOOY, D. (1998) In vivo clonal analyses reveal the properties of endogenous neural stem cell proliferation in the adult mammalian forebrain. Development 125, 2251-2261.
46. MORSHEAD, C. M., REYNOLDS, B. A., CRAIG, C. G., MCBURNEY, M. W., STAINES, W. A., 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.
47. NISHIYAMA, A., CHANG, A. & TRAPP, B. D. (1999) NG2+ glial cells: A novel glial cell population in the adult brain. Journal of Neuropathology and Experimental Neurology 58, 1113-1124.
48. NISHIYAMA, A., LIN, X. H., GIESE, N., HELDIN, C. H. & STALLCUP, W. B. (1996a) Interaction between NG2 proteoglycan and PDGF alpha-receptor on O2A progenitor cells is required for optimal response to PDGF. Journal of Neuroscience Research 43, 315-330.
49. NISHIYAMA, A., LIN, X. H., GIESE, N., HELDIN, C. H. & STALLCUP, W. B. (1996b) Co-localization of NG2 proteoglycan and PDGF alpha-receptor on O2A progenitor cells in the developing rat brain. Journal of Neuroscience Research 43, 299-314.
50. NISHIYAMA, A., YU, M., DRAZBA, J. A. & TUOHY, V. K. (1997) Normal and reactive NG2+ glial cells are distinct from resting and activated microglia. Journal of Neuroscience Research 48, 299-312.
51. ONG, W. Y. & LEVINE, J. M. (1999) A light and electron microscopic study of NG2 chondroitin sulfate proteoglycan-positive oligodendrocyte precursor cells in the normal and kainate-lesioned rat hippocampus. Neuroscience 92, 83-95.
52. OUMESMAR, B. N., VIGNAIS, L. & BARON-VAN EVERCOOREN, A. (1997) Developmental expression of platelet-derived growth factor alpha-receptor in neurons and glial cells of the mouse CNS. Journal of Neuroscience 17, 125-139.
53. PALMER, T. D., MARKAKIS, E. A., WILLHOITE, A. R., SAFAR, F. & GAGE, F. H. (1999) Fibroblast growth factor-2 activates a latent neurogenic program in neural stem cells from diverse regions of the adult CNS. Journal of Neuroscience 19, 8487-8497.
54. PALMER, T. D., RAY, J. & GAGE, F. H. (1995) FGF-2-responsive neuronal progenitors reside in proliferative and quiescent regions of the adult rodent brain. Molecular and Cellular Neuroscience 6, 474-486.
55. PALMER, T. D., TAKAHASHI, J. & GAGE, F. H. (1997) The adult rat hippocampus contains primordial neural stem cells. Molecular and Cellular Neuroscience 8, 389-404.
56. PRINGLE, N. P., MUDHAR, H. S., COLLARINI, E. J. & RICHARDSON, W. D. (1992) PDGF receptors in the rat CNS: During late neurogenesis, PDGF alpha-receptor expression appears to be restricted to glial cells of the oligodendrocyte lineage. Development 115, 535-551.
57. RAFF, M. C. (1989) Glial cell diversification in the rat optic nerve. Science 243, 1450-1455.
58. RAFF, M. C., MILLER, R. H. & 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.
59. REDWINE, J. M., BLINDER, K. L. & ARMSTRONG, R. C. (1997) In situ expression of fibroblast growth factor receptors by oligodendrocyte progenitors and oligodendrocytes in adult mouse central nervous system. Journal of Neuroscience Research 50, 229-237.
60. REYNOLDS, R. & HARDY, R. (1997) Oligodendroglial progenitors labeled with the O4 antibody persist in the adult rat cerebral cortex in vivo. Journal of Neuroscience Research 47, 455-470.
61. ROGISTER, B., BEN-HUR, T. & DUBOIS-DALCQ, M. (1999) From neural stem cells to myelinating oligodendrocytes. Molecular and Cellular Neuroscience 14, 287-300.
62. SHIHABUDDIN, L. S., HORNER, P. J., RAY, J. & GAGE, F. H. (2000) Adult spinal cord stem cells generate neurons after transplantation in the adult dentate gyrus. Journal of Neuroscience 20, 8727-8735.
63. SHIHABUDDIN, L. S., RAY, J. & GAGE, F. H. (1997) FGF-2 is sufficient to isolate progenitors found in the adult mammalian spinal cord. Experimental Neurology 148, 577-586.
64. SPASSKY, N., OLIVIER, C., PEREZ-VILLEGAS, E., GOUJET-ZALC, C., MARTINEZ, S., THOMAS, J. & ZALC, B. (2000) Single or multiple oligodendroglial lineages: A controversy. Glia 29, 143-148.
65. STALLCUP, W. B. & BEASLEY, L. (1987) Bipotential glial precursor cells of the optic nerve express the NG2 proteoglycan. Journal of Neuroscience 7, 2737-2744.
66. TEMPLE, S. & RAFF, M. C. (1986) Clonal analysis of oligodendrocyte development in culture: Evidence for a developmental clock that counts cell divisions. Cell 44, 773-779.
67. VIGNAIS, L., OUMESMAR, B. N. & BARON-VAN EVERCOOREN, A. B. (1995) PDGF-alpha receptor is expressed by mature neurones of the central nervous system. Neuroreport 6, 1993-1996.
68. WARRINGTON, A. E. & PFEIFFER, S. E. (1992) Proliferation and differentiation of 04+ oligodendrocytes in postnatal rat cerebellum: Analysis in unfixed tissue slices using anti-glycolipid antibodies. Journal of Neuroscience Research 33, 338-353.
69. WEISS, S., DUNNE, C., HEWSON, J., WOHL, C., WHEATLEY, M., PETERSON, A. C. & REYNOLDS, B. A. (1996) Multipotent CNS stem cells are present in the adult mammalian spinal cord and ventricular neuroaxis. Journal of Neuroscience 16, 7599-7609.
70. WOLSWIJK, G., RIDDLE, P. N. & NOBLE, M. (1990) Co-existence of perinatal and adult forms of a glial progenitor cell during development of the rat optic nerve. Development 109, 691-698.
71. WU, Q., MILLER, R. H., RANSOHOFF, R. M., ROBINSON, S., BU, J. & NISHIYAMA, A. (2000) Elevated levels of the chemokine GRO-1 correlate with elevated oligodendrocyte progenitor proliferation in the jimpy mutant. Journal of Neuroscience 20, 2609-2617.
72. YAMAMOTO, S., YAMAMOTO, N., KITAMURA, T., NAKAMURA, K. & NAKAFUKU, M. (2001) Proliferation of parenchymal neural progenitors in response to injury in the adult rat spinal cord. Experimental Neurology 172, 115-127.
73. ZHANG, S. C., GE, B. & DUNCAN, I. D. (1999) Adult brain retains the potential to generate oligodendroglial progenitors with extensive myelination capacity. Proceeding of the National Academy of Sciences of the USA 96, 4089-4094.