NG2+ glial cells: A novel glial cell population in the adult brain

Journal of Neuropathology and Experimental Neurology

Volumn 58, Issue 11, 1999, Pages 1113-1124

  Nishiyama, Akiko ^a,b   Chang, Ansi ^a   Trapp, Bruce D ^a  

^a LERNER RESEARCH INSTITUTE   (United States)

^b UNIVERSITY OF CONNECTICUT   (United States)

Author keywords

Demyelination; EAE; Glioma; NG2; Oligodendrocyte; PDGF receptor; Progenitor

Indexed keywords

ANTIGEN; GALACTOSYLCERAMIDE; GANGLIOSIDE; GLIAL FIBRILLARY ACIDIC PROTEIN; MYELIN PROTEIN; PLATELET DERIVED GROWTH FACTOR RECEPTOR; PROTEOCHONDROITIN SULFATE; PROTEOGLYCAN; SULFATIDE; TYROSINE KINASE RECEPTOR;

ALLERGIC ENCEPHALOMYELITIS; BRAIN; CELL DIFFERENTIATION; CELL PROLIFERATION; DEMYELINATION; GLIA CELL; GLIOMA; IMMUNOHISTOCHEMISTRY; NERVOUS SYSTEM DEVELOPMENT; NONHUMAN; OLIGODENDROGLIA; PRIORITY JOURNAL; REVIEW; STEM CELL;

EID: 0032758116     PISSN: 00223069     EISSN: None     Source Type: Journal    
DOI: 10.1097/00005072-199911000-00001     Document Type: Review

References (106)

1. Nishiyama A, Dahlin KJ, Prince JT, Johnstone SR, Stallcup WB. The primary structure of NG2, a novel membrane-spanning proteoglycan. J Cell Biol 1991;114:359-71. (See also J Cell Biol 1999;145:1117 for correction.)
2. Stallcup WB, Beasley L. Bipotential glial precursor cells of the optic nerve express the NG2 proteoglycan. J Neurosci 1987;7: 2737-44
3. Levine JM, Stallcup WB. Plasticity of developing cerebellar cells in vitro studied with antibodies against the NG2 antigen. J Neurosci 1987;7:2721-31
4. Nishiyama A, Dahlin KJ, Stallcup WB. The expression of NG2 proteoglycan in the developing rat limb. Development 1991;111: 933-44
5. Levine JM, Nishiyama A. The NG2 chondroitin sulfate proteoglycan: A multifunctional proteoglycan associated with immature cells. Persp Dev Neurobiol 1996;3:245-59
6. Heldin CH, Westermark B. Platelet-derived growth factor: Three isoforms and two receptor types. TIG 1989;5:108-11
7. Richardson WD, Pringle N, Mosley MJ, Westermark B, Dubois-Dalcq M. A role for platelet-derived growth factor in normal gliogenesis in the central nervous system. Cell 1988;53:309-19
8. Pringle NP, Mudhar HS, Collarini EJ, Richardson WD. 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 1992;115:535-51
9. Pringle NP, Richardson WD. A singularity of PDGF alpha-receptor expression in the dorsoventral axis of the neural tube may define the origin of the oligodendrocyte lineage. Development 1993;117:525-33
10. Nishiyama A, Lin X-H, Giese N, Heldin C-H, Stallcup WB. Colocalization of NG2 proteoglycan and PDGF alpha receptor on O2A progenitor cells in the developing rat brain. J Neurosci Res 1996;43:299-314
11. Nishiyama A, Lin X-H, Giese N, Heldin C-H, Stallcup WB. Interaction between NG2 proteoglycan and PDGF alpha receptor on O2A progenitor cells is required for optimal response to PDGF. J Neurosci Res 1996;43:315-30
12. Stallcup WB, Arner LS, Levine JM. An antiserum against the PC12 cell line defines cell surface antigens specific for neurons and Schwann cells. J Neurosci 1983;3:53-68
13. Levine JM, Stincone F, Lee YS. Development and differentiation of glial precursor cells in the rat cerebellum. Glia 1993;7: 307-21
14. Nishiyama A, Yu M, Drazba JA, Tuohy VK. Normal and reactive NG2+ glial cells are distinct from resting and activated microglia. J Neurosci Res 1997;48:299-312
15. McCarthy KD, de Vellis J. Preparation of separate astroglial and oligodendroglial cell cultures from rat cerebral tissue. J Cell Biol 1980;85:890-902
16. Raff MC, Miller RH, Noble M. A glial progenitor cell that develops in vitro into an astrocyte or an oligodendrocyte depending on culture medium. Nature 1983;303:390-96
17. Raff MC. Glial cell diversification in the rat optic nerve. Science 1989;243:1450-55
18. Richardson WD, Raff M, Noble M. The oligodendrocyte-type-2-astrocyte lineage. Semin Neurosci 1990;2:445-54
19. Eisenbarth GS, Walsh FS, Nirenberg M. Monoclonal antibody to a plasma membrane antigen of neurons. Proc Natl Acad Sci USA 1979;76:4913-17
20. Sommer I, Schachner M. Monoclonal antibodies (O1 and O4) to oligodendrocyte surfaces: An immunocytological study in the central nervous system. Dev Biol 1981;83:311-27
21. Bansal R, Warrington AE, Gard AL, Ranscht B, Pfeiffer SE. Multiple and novel specificities of monoclonal antibodies O1, O4, and R-mAb used in the analysis of oligodendrocyte development. J Neurosci Res 1989;24:548-57
22. Gard AL, Pfeiffer SE. Two proliferative stages of the oligodendrocyte lineage (A2B5+O4-and O4+GalC-) under different mitogenic control. Neuron 1990;5:615-25
23. Lillien LE, Raff MC. Analysis of the cell-cell interactions that control type-2 astrocyte development in vitro. Neuron 1990;4: 525-34
24. Grove EA, Williams BP, Li D, Hajihosseini M, Friedrich A, Price J. Multiple restricted lineages in the embryonic rat cerebral cortex. Development 1993;117:553-61
25. Espinosa de los Monteros A, Zhang MS, Gordon M, Aymie M, de Vellis J. Transplantation of cultured premyelinating oligodendrocytes into normal and myelin-deficient rat brain. Dev Neurosci 1992;14:98-104
26. Franklin RJM, Bayley SA, Milner R, ffrench-Constant C, Blakemore WF. Differentiation of the O-2A progenitor cell line CG-4 into oligodendrocytes and astrocytes following transplantation into glia-deficient areas of CNS white matter. Glia 1995;13:39-44
27. Raff MC, Abney ER, Fok-Seang J. Reconstitution of a developmental clock in vitro: A critical role for astrocytes in the timing of oligodendrocyte differentiation. Cell 1985;42:61-69
28. Temple S, Raff MC. Clonal analysis of oligodendrocyte development in culture: Evidence for a developmental clock that counts cell divisions. Cell 1986;44:773-79
29. Yeh HJ, Ruit KG, Wang YX, Parks WC, Snider WD, Deuel TF. PDGF A-chain gene is expressed by mammalian neurons during development and in maturity. Cell 1991;64:209-16
30. Sasahara M, Fries JWU, Raines EW, et al. PDGF B-chain in neurons of the central nervous system, posterior pituitary, and in a transgenic model. Cell 1991;64:217-27
31. ffrench-Constant C, Raff MC. The oligodendrocyte-type-2 astrocyte cell lineage is specialized for myelination. Nature 1986;323: 335-38
32. Wolswijk G, Noble M. Identification of an adult-specific glial progenitor cell. Development 1989;105:387-400
33. perinatal progenitor cells. J Cell Biol 1992;118:889-900
34. Chan CLH, Wigley CB, Berry M. Oligodendrocyte-type 2 astrocyte (O-2A) progenitor cells from neonatal and adult rat optic nerve differ in their responsiveness to platelet-derived growth factor. Dev Brain Res 1990;55:275-82
35. Shi J, Marinovich A, Barres BA. Purification and characterization of adult oligodendrocyte precursor cells from the rat optic nerve. J Neurosci 1998;18:4627-36
36. Armstrong R, Friedrich VL, Jr., Holmes KV, Dubois-Dalcq M. In vitro analysis of the oligodendrocyte lineage in mice during demyelination and remyelination. J Cell Biol 1990;111:1183-95
37. Engel U, Wolswijk G. 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 1996;16: 16-26
38. Warf BC, Fok-Seang J, Miller RH. Evidence for the ventral origin of oligodendrocyte precursors in the rat spinal cord. J Neurosci 1991;11:2477-88
39. Noll E, Miller RH. Oligodendrocyte precursors originate at the ventral ventricular zone dorsal to the ventral midline region in the embryonic rat spinal cord. Development 1993;118:563-73
40. Mori S, Leblond CP. Electron microscopic idenfication of three classes of oligodendrocytes and a preliminary study of their proliferative activity in the corpus callosum of young rats. J Comp Neurol 1970;139:1-30
41. LeVine SM, Goldman JE. Spatial and temporal patterns of oligodendrocyte differentiation in rat cerebrum and cerebellum. J Comp Neurol 1988;277:441-55
42. LeVine SM, Goldman JE. Embryonic divergence of oligodendrocyte and astrocyte lineages in developing rat cerebrum. J Neurosci 1988;8:3992-4006
43. Reynolds R, Wilkin GP. Development of macroglial cells in rat cerebellum. II. An in situ immunohistochemical study of oligodendroglial lineage from precursor to mature myelinating cell. Development 1988;102:409-25
44. Wolswijk G. Strongly GD3+ cells in the developing and adult rat cerebellum belong to the microglial lineage rather than to the oligodendrocyte lineage. Glia 1995;13:13-26
45. Ellison JA, de Vellis J. Amoeboid microglia expressing GD3 ganglioside are concentrated in regions of oligodendrogenesis during development of the rat corpus callosum. Glia 1995;14:123-32
46. Levison SW, Goldman JE. Both oligodendrocytes and astrocytes develop from progenitors in the subventricular zone of postnatal rat forebrain. Neuron 1993;10:201-12
47. Ellison JA, de Vellis J. Platelet-derived growth factor receptor is expressed by cells in the early oligodendrocyte lineage. J Neurosci Res 1994;37:116-28
48. Timsit S, Martinez S, Allinquant B, Peyron F, Puelles L, Zalc B. Oligodendrocytes originate in a restricted zone of the embryonic ventral neural tube defined by DM-20 mRNA expression. J Neurosci 1995;15:1012-24
49. Hardy RJ, Friedrich VL, Jr. Oligodendrocyte progenitors are generated throughout the embryonic mouse brain, but differentiate in restricted foci. Development 1996;122:2059-69
50. Trapp BD, Nishiyama A, Cheng D, Macklin WB. Differentiation and death of premyelinating oligodendrocytes in developing rodent brain. J Cell Biol 1997;137:459-68
51. Reynolds R, Hardy R. Oligodendroglial progenitors labeled with the O4 antibody persist in the adult rat cerebral cortex in vivo. J Neurosci Res 1997;47:455-70
52. Kligman D, Hilt DC. The S100 protein family. TIBS 1988;13: 437-43
53. Levine JM, Card JP. Light and electron microscopic localization of a cell surface antigen (NG2) in the rat cerebellum: Association with smooth protoplasmic astrocytes. J Neurosci 1987;7:2711-20
54. Reyners H, Gianfelici de Reyners E, Maisin JR. The beta astrocyte: A newly recognized radiosensitive glial cell type in the cerebral cortex. J Neurocytol 1982;11:967-83
55. Reyners H, Gianfelici de Reyners E, Regniers L, Maisin JR. A glial progenitor cell in the cerebral cortex of the adult rat. J Neurocytol 1986;15:53-61
56. Ramon-Moliner E. A study of neuroglia: The problem of transitional forms. J Comp Neurol 1958;110:157-71
57. Leong S-K, Ling E-A. Amoeboid and ramified microglia: Their interrelationship and response to brain injury. Glia 1992;6:39-47
58. Streit WJ, Kreutzberg GW. Lectin binding by resting and reactive microglia. J Neurocytol 1987;16:249-60
59. Austyn JM, Gordon S. F4/80, a monoclonal antibody directed specifically against the mouse macrophage. Eur J Immunol 1981;11: 805-15
60. McKnight AJ, Macfarlane AJ, Dri P, Turley L, Willis AC, Gordon S. Molecular cloning of F4/80, a murine macrophage-restricted cell surface glycoprotein with homology to the G-protein-linked transmembrane 7 hormone receptor family. J Biol Chem 1996;271:486-89
61. Keirstead HS, Levine JM, Blakemore WF. Response of the oligodendrocyte progenitor cell population (defined by NG2 labelling) to demyelination of the adult spinal cord. Glia 1998;22: 161-70
62. Nave KA, Lai C, Bloom FE, Milner RJ. Jimpy mutant mouse: A 74-base deletion in the mRNA for myelin proteolipid protein and evidence for a primary defect in RNA splicing. Proc Natl Acad Sci USA 1986;83:9264-68
63. Nave KA, Bloom FE, Milner RJ. A single nucleotide difference in the gene for myelin proteolipid protein defines the jimpy mutation in mouse. J Neurochem 1987;49:1873-77
64. Ikenaka K, Furuichi T, Iwasaki Y, Moriguchi A, Okano H, Mikoshiba K. Myelin proteolipid protein gene structure and its regulation of expression in normal and jimpy mutant mice. J Mol Biol 1988;199:587-96
65. Sidman RL, Dickie MM, Appel SH. Mutant mice (Quaking and Jimpy) with deficient myelination in the central nervous system. Science 1964;144:309-11
66. Skoff RP. Increased proliferation of oligodendrocytes in the hypomyelinated mouse mutant-jimpy. Brain Res 1982;248:19-31
67. Knapp PE, Skoff RP, Redsone DW. Oligodendroglial cell death in jimpy mice: An explanantion for the myelin deficit. J Neurosci 1986;6:2813-22
68. Nishiyama A, Wu Q. NG2+ glial progenitor cells in normal adult brain and in the dysmyelinating mutant Jimpy. In: Uyemura K. et al, eds. Neural development/Keio University symposia for life science and medicine. Tokyo: Springer-Verlag, 1998:339-44
69. Skoff RP, Price DL, Stocks A. Electron microscopic autoradiographic studies of gliogenesis in rat optic nerve. I. Cell proliferation. J Comp Neurol 1976;169:291-311
70. Skoff RP, Price DL, Stocks A. Electron microscopic autoradiographic studies of gliogenesis in rat optic nerve. II. Time of origin. J Comp Neurol 1976;169:313-34
71. Ludwin SK. Central nervous system demyelination and remyelination in the mouse. Lab Invest 1978;39:597-612
72. Raine CS, Scheinberg L, Waltz J. Multiple sclerosis: Oligodendrocyte survival and proliferation in an active established lesion. Lab Invest 1981;45:534-46
73. Arenella LS, Herndon RM. Mature oligodendrocytes: Division following experimental demyelination in adult animals. Arch Neurol 1984;41:1162-65
74. Wood PM, Bunge RP. The origin of remyelinating cells in the adult central nervous system: The role of the mature oligodendrocyte. Glia 1991;4:225-32
75. Ludwin SK. Remyelination in demyelinating diseases of the central nervous system. CRC Crit Rev Neurobiol 1987;3:1-28
76. Ludwin SK. An autoradiographic study of cellular proliferation in remyelination of the central nervous system. Am J Pathol 1979;95: 683-96
77. Prineas JW, Kwon EE, Goldenberg PZ, et al. Multiple sclerosis: Oligodendrocyte proliferation and differentiation in fresh lesions. Lab Invest 1989;61:489-503
78. Armstrong RC, Dorn HH, Kufta CV, Friedman E, Dubois-Dalcq M. Pre-oligodendrocytes from adult human CNS. J Neurosci 1992;12:1538-47
79. Godfraind C, Friedrich VL, Holmes KV, Dubois-Dalcq M. In vivo analysis of glial cell phenotypes during a viral demyelinating disease in mice. J Cell Biol 1989;109:2405-16
80. Wolswijk G. Chronic stage multiple sclerosis lesions contain a relatively quiescent population of oligodendrocyte precursor cells. J Neurosci 1998;18:601-9
81. Stallcup WB, Dahlin K, Healy P. Interaction of the NG2 chondroitin sulfate proteoglycan with type VI collagen. J Cell Biol 1990;111:3177-88
82. Morgan AC, Galloway DR, Reisfeld RA. Hybridoma 1981;1: 27-36
83. Bumol TF, Reisfeld RA. Unique glycoprotein-proteoglycan complex defined by monoclonal antibody on human melanoma cells. Proc Natl Acad Sci USA 1982;79:1245-49
84. Harper JR, Reisfeld RA. Cell-associated proteoglycans in human malignant melanoma. In: Wight TN, Mecham RP, eds. Biology of proteoglycans. San Diego: Academic Press, Inc., 1987:345-66
85. Pluschke G, Vanek M, Evans A, et al. Molecular cloning of a human melanoma-associated chondroitin sulfate proteoglycan. Proc Natl Acad Sci USA 1996;93:9710-15
86. Real FX, Houghton AN, Albino AP, et al. Surface antigens of melanomas and melanocytes defined by mouse monoclonal antibodies: Specificity analysis and comparison of antigen expression in cultured cells and tissues. Cancer Res 1985;45:4401-11
87. Schrappe M, Klier FG, Spiro RC, Waltz TA, Reisfeld RA, Gladson CL. Correlation of chondroitin sulfate proteoglycan expression on proliferating brain capillary endothelial cells with the malignant phenotype of astroglial cells. Cancer Res 1991;51:4986-93
88. Ono K, Yasui Y, Rutishauser U, Miller RH. Focal ventricular origin and migration of oligodendrocyte precursors into the chick optic nerve. Neuron 1997;19:283-92
89. Ueda H, Levine JM, Miller RH, and Trapp BD. Development of rat optic nerve oligodendrocytes is independent of retinal ganglion cell axons. J Cell Biol (in press)
90. Chao MV. Neurotrophin receptors: A window into neuronal differentiation. Neuron 1992;9:583-93
91. Prayoonwiwat N, Rodriguez M. The potential for oligodendrocyte proliferation during demyelinating disease. J Neuropathol Exp Neurol 1993;52:55-63
92. Reynolds R, Wilkin GP. Cellular reaction to an acute demyelinating/remyelinating lesion of the rat brain stem: Localisation of GD3 ganglioside immunoreactivity. J Neurosci Res 1993;36: 405-22
93. Gensert JM, Goldman JE. Endogenous progenitors remyelinate demyelinated axons in the adult CNS. Neuron 1997;19:197-203
94. Carroll WM, Jennings AR. In vivo CNS remyelination: HNK-1 labels newly differentiated oligodendrocytes but not precursors. J Neurocytol 1993;22:583-89
95. Carroll WM, Jennings AR, Ironside LJ. Identification of the adult resting progenitor cell by autoradiographic tracking of oligodendrocyte precursors in experimental CNS demyelination. Brain 1998;121:293-302
96. Keirstead HS, Blakemore WF. Identification of post-mitotic oligodendrocytes incapable of remyelination within the demyelinated adult spinal cord. J Neuropathol Exp Neurol 1997;56:1191-201
97. Ibarrola N, Mayer-Proschel M, Rodriguez-Pena A, Noble M. Evidence for the existence of at least two timing mechanisms that contribute to oligodendrocyte generation in vitro. Dev Biol 1996;180:1-21
98. Yu M, Nishiyama A, Trapp BD, Tuohy VK. Interferon-β inhibits progression of relapsing-remitting experimental autoimmune encephalomyelitis. J Neuroimmunol 1996;64:91-100
99. Levine JM, Enquist LW, Card JP. Reactions of oligodendrocyte precursor cells to alpha herpesvirus infection of the central nervous system. Glia 1998;23:316-28
100. Bailey P, Cushing H. A classification of the tumors of the glioma group on a histogenetic basis with a correlated study of prognosis. Philadelphia: J. B. Lippincott Company, 1926
101. Bruner JM. Neuropathology of malignant gliomas. Sem Oncol l994;21:126-38
102. Kleihues P, Soylemezoglu F, Schauble B, Scheithauer BW, Burger PC. Histopathology, classification, and grading of gliomas. Glia 1995;15:211-21
103. Sung CC, Collins R, Li J, et al. Glycolipids and myelin proteins in human oligodendrogliomas. Glycoconj J 1996;13:433-43
104. Shoshan Y, Nishiyama A, Mork S, et al. Oligodendrogliomas and pilocytic astrocytomas express phenotypic marker of oligodendrocyte progenitor cells. Proc Natl Acad Sci (in press)
105. 3H-thymidine. J Comp Neurol 1988;271:589-603
106. Weiss S, Reynolds BA, Vescovi AL, Morshead C, Craig CG, van der Kooy D. Is there a neural stem cell in the mammalian forebrain? TINS 1996;19:387-93