Oligodendrocyte and astrocyte development in rodents: An in situ and immunohistological analysis during embryonic development

GLIA

Volumn 40, Issue 1, 2002, Pages 25-43

  Liu, Ying ^a,b   Wu, Yuanyuan ^b   Lee, Jeffrey C ^a,b   Xue, Haipeng ^a   Pevny, Larysa H ^c   Kaprielian, Zaven ^d   Rao, Mahendra S ^a  

^a NATIONAL INSTITUTE ON AGING   (United States)

^b UNIVERSITY OF UTAH SCHOOL OF MEDICINE   (United States)

^c UNIVERSITY OF NORTH CAROLINA SCHOOL OF MEDICINE   (United States)

^d ALBERT EINSTEIN COLLEGE OF MEDICINE   (United States)

Author keywords

Astrocyte; Development; E NCAM; Glioblast; NEP; Neuroblast; Oligodendrocyte; Self renewal

Indexed keywords

BASIC HELIX LOOP HELIX TRANSCRIPTION FACTOR; DNA BINDING PROTEIN; GLIAL FIBRILLARY ACIDIC PROTEIN; HERMES ANTIGEN; HIGH MOBILITY GROUP PROTEIN; HOMEODOMAIN PROTEIN; MESSENGER RNA; NERVE PROTEIN; NEUROG3 PROTEIN, RAT; NKX 2.2 HOMEDOMAIN PROTEIN; NKX-2.2 HOMEDOMAIN PROTEIN; PLATELET DERIVED GROWTH FACTOR ALPHA RECEPTOR; SOX-10 TRANSCRIPTION FACTOR; TRANSCRIPTION FACTOR; TRANSCRIPTION FACTOR SOX10;

ANIMAL; ARTICLE; ASTROCYTE; CELL CULTURE; CELL DIFFERENTIATION; CELL DIVISION; CENTRAL NERVOUS SYSTEM; CYTOLOGY; FETUS; GENE EXPRESSION REGULATION; GENETICS; GROWTH, DEVELOPMENT AND AGING; IMMUNOHISTOCHEMISTRY; IN SITU HYBRIDIZATION; METABOLISM; NEWBORN; OLIGODENDROGLIA; PHYSIOLOGY; PRENATAL DEVELOPMENT; RAT; SPRAGUE DAWLEY RAT; STEM CELL;

ANIMALS; ANIMALS, NEWBORN; ANTIGENS, CD44; ASTROCYTES; BASIC HELIX-LOOP-HELIX TRANSCRIPTION FACTORS; CELL DIFFERENTIATION; CELL DIVISION; CELLS, CULTURED; CENTRAL NERVOUS SYSTEM; DNA-BINDING PROTEINS; FETUS; GENE EXPRESSION REGULATION, DEVELOPMENTAL; GLIAL FIBRILLARY ACIDIC PROTEIN; HIGH MOBILITY GROUP PROTEINS; HOMEODOMAIN PROTEINS; IMMUNOHISTOCHEMISTRY; IN SITU HYBRIDIZATION; NERVE TISSUE PROTEINS; OLIGODENDROGLIA; RATS; RATS, SPRAGUE-DAWLEY; RECEPTOR, PLATELET-DERIVED GROWTH FACTOR ALPHA; RNA, MESSENGER; STEM CELLS; TRANSCRIPTION FACTORS;

EID: 0036794961     PISSN: 08941491     EISSN: None     Source Type: Journal    
DOI: 10.1002/glia.10111     Document Type: Article

References (73)

1. Alfei L, Aita M, Caronti B, De Vita R, Margotta V, Medolago Albani L, Valente AM. 1999. Hyaluronate receptor CD44 is expressed by astrocytes in the adult chicken and in astrocyte cell precursors in early development of the chick spinal cord. Eur J Histochem 43:29-38.
2. Aloisi F, Giampaolo A, Russo G, Peschle C, Levi G. 1992. Developmental appearance, antigenic profile, and proliferation of glial cells of the human embryonic spinal cord: an immunocytochemical study using dissociated cultured cells. Glia 5:171-181.
3. Blakemore WF, Keirstead HS. 1999. The origin of remyelinating cells in the central nervous system. J Neuroimmunol 98:69-76.
4. Bogler O, Furnari FB, Kindler-Roehrborn A, Sykes VW, Yung R, Huang HJ, Cavenee WK. 2000. SETA: a novel SH3 domain-containing adapter molecule associated with malignancy in astrocytes. Neuro-Oncology 2:6-15.
5. Cai J, Rao M. 2002. Neural stem cell and aging: Stem cells, a cellular fountain of youth. New York: Elsevier (in press).
6. Cameron RS, Rakic P. 1991. Glial cell lineage in the cerebral cortex: a review and synthesis. Glia 4:124-137.
7. Collignon J, Sockanathan S, Hacker A, Cohen-Tannoudji M, Norris D, Rastan S, Stevanovic M, Goodfellow PN, Lovell-Badge R. 1996. A comparison of the properties of Sox-3 with Sry and two related genes, Sox-1 and Sox-2. Development 122:509-520.
8. Compston A, Zajicek J, Sussman J, Webb A, Hall G, Muir D, Shaw C, Wood A, Scolding N. 1997. Glial lineages and myelination in the central nervous system. J Anat 190(Pt 2):161-200.
9. Dahl D, Rueger DC, Bignami A, Weber K, Osborn M. 1981. Vimentin, the 57 000 molecular weight protein of fibroblast filaments, is the major cytoskeletal component in immature glia. Eur J Cell Biol 24:191-196.
10. Dawson MR, Levine JM, Reynolds R. 2000. NG2-expressing cells in the central nervous system: are they oligodendroglial progenitors? J Neurosci Res 61:471-479.
11. Diers-Fenger M, Kirchhoff F, Kettenmann H, Levine JM, 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.
12. 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.
13. Dupouey P, Benjelloun S, Gomes D. 1985. Immunohistochemical demonstration of an organized cytoarchitecture of the radial glia in the CNS of the embryonic mouse. Dev Neurosci 7:81-93.
14. Fu H, Qi Y, Tan M, Cai J, Takebayashi H, Nakafuku M, Richardson W, Qiu M. 2002. Dual origin of spinal oligodendrocyte progenitors and evidence for the cooperative role of Olig2 and Nkx2.2 in the control of oligodendrocyte differentiation. Development 129:681-693.
15. -) under different mitogenic control. Neuron 5:615-625.
16. Gensert JM, Goldman JE. 2001. Heterogeneity of cycling glial progenitors in the adult mammalian cortex and white matter. J Neurobiol 48:75-86.
17. Gregori N, Proschel C, Noble M, Mayer-Proschel M. 2002. The tripotential glial-restricted precursor (GRP) cell and glial development in the spinal cord: generation of bipotential oligodendrocyte-type-2 astrocyte progenitor cells and dorsal-ventral differences in GRP cell function. J Neurosci 22:248-256.
18. Gudino-Cabrera G, Nieto-Sampedro M. 1999. Estrogen receptor immunoreactivity in Schwann-like brain macroglia. J Neurobiol 40: 458-470.
19. Hall A, Giese NA, Richardson WD. 1996. Spinal cord oligodendrocytes develop from ventrally derived progenitor cells that express PDGF alpha-receptors. Development 122:4085-4094.
20. Hartfuss E, Galli R, Heins N, Gotz M. 2001. Characterization of CNS precursor subtypes and radial glia. Dev Biol 229:15-30.
21. Herrera J, Yang H, Zhang SC, Proschel C, Tresco P, Duncan ID, Luskin M, Mayer-Proschel M. 2001. Embryonic-derived glial-restricted precursor cells (GRP cells) can differentiate into astrocytes and oligodendrocytes in vivo. Exp Neurol 171:11-21.
22. Hirano M, Goldman JE. 1988. Gliogenesis in rat spinal cord: evidence for origin of astrocytes and oligodendrocytes from radial precursors. J Neurosci Res 21:155-167.
23. Jacobson M. 1991. Developmental neurobiology. New York: Plenum Press.
24. 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.
25. Kalyani AJ, Piper D, Mujtaba T, Lucero MT, Rao MS. 1998. Spinal cord neuronal precursors generate multiple neuronal phenotypes in culture. J Neurosci 18:7856-7868.
26. Kondo T, Raff M. 2000. Oligodendrocyte precursor cells reprogrammed to become multipotential CNS stem cells. Science 289: 1754-1757.
27. Kuhlbrodt K, Herbarth B, Sock E, Hermans-Borgmeyer I, Wegner M. 1998. Sox10, a novel transcriptional modulator in glial cells. J Neurosci 18:237-250.
28. Kukekov VG, Laywell ED, Suslov O, Davies K, Scheffler B, Thomas LB, O'Brien TF, Kusakabe M, Steindler DA. 1999. Multipotent stem/progenitor cells with similar properties arise from two neurogenic regions of adult human brain. Exp Neurol 156:333-344.
29. Laywell ED, Steindler DA. 1991. Boundaries and wounds, glia and glycoconjugates: cellular and molecular analyses of developmental partitions and adult brain lesions. Ann NY Acad Sci 633:122-141.
30. 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.
31. Lee JC, Mayer-Proschel M, Rao MS. 2000. Gliogenesis in the central nervous system. Glia 30:105-121.
32. Levitt P, Cooper ML, Rakic P. 1981. Coexistence of neuronal and glial precursor cells in the cerebral ventricular zone of the fetal monkey: an ultrastructural immunoperoxidase analysis. J Neurosci 1:27-39.
33. Lu B, Yokoyama M, Dreyfus CF, Black IB. 1991. NGF gene expression in actively growing brain glia. J Neurosci 11:318-326.
34. Lu QR, Yuk D, Alberta JA, Zhu Z, Pawlitzky I, Chan J, McMahon AP, Stiles CD, Rowitch DH. 2000. Sonic hedgehog: regulated oligodendrocyte lineage genes encoding bHLH proteins in the mammalian central nervous system. Neuron 25:317-329.
35. Lu QR, Sun T, Zhu Z, Ma N, Garcia M, Stiles CD, Rowitch DH. 2002. Common developmental requirement for olig function indicates a motor neuron/oligodendrocyte connection. Cell 109:75-86.
36. Mabie PC, Mehler MF, Kessler JA. 1999. Multiple roles of bone morphogenetic protein signaling in the regulation of cortical cell number and phenotype. J Neurosci 19:7077-7088.
37. 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.
38. Mayer-Proschel M, Kalyani AJ, Mujtaba T, Rao MS. 1997. Isolation of lineage-restricted neuronal precursors from multipotent neuroepithelial stem cells. Neuron 19:773-785.
39. Miller RH, David S, Patel R, Abney ER, Raff MC. 1985. A quantitative immunohistochemical study of macroglial cell development in the rat optic nerve: in vivo evidence for two distinct astrocyte lineages. Dev Biol 111:35-41.
40. Misson JP, Edwards MA, Yamamoto M, Caviness VS Jr. 1988. Identification of radial glial cells within the developing murine central nervous system: studies based upon a new immunohistochemical marker. Brain Res Dev Brain Res 44:95-108.
41. Moretto G, Xu RY, Kim SU. 1993. CD44 expression in human astro cytes and oligodendrocytes in culture. J Neuropathol Exp Neurol 52:419-423.
42. Nishiyama A, Lin XH, Giese N, Heldin CH, Stallcup WB. 1996a. Co-localization of NG2 proteoglycan and PDGF alpha-receptor on O2A progenitor cells in the developing rat brain. J Neurosci Res 43:299-314.
43. Nishiyama A, Lin XH, Giese N, Heldin CH, Stallcup WB. 1996b. Interaction between NG2 proteoglycan and PDGF alpha-receptor on O2A progenitor cells is required for optimal response to PDGF. J Neurosci Res 43:315-330.
44. Nishiyama A. 2001. NG2 cells in the brain: a novel glial cell population. Hum Cell 14:77-82.
45. Noble M, Fok-Seang J, Cohen J. 1984. Glia area unique substrate for the in vitro growth of central nervous system neurons. J Neurosci 4:1892-1903.
46. Noble M, Fok-Seang J, Wolswijk G, Wren D. 1990. Development and regeneration in the central nervous system. Philos Trans R Soc Lond B Biol Sci 327:127-143.
47. Noetzel MJ, Agrawal HC. 1985. Immunoblot identification of glial fibrillary acidic protein in rat sciatic nerve, brain, and spinal cord during development. Neurochem Res 10:737-753.
48. Orentas DM, Miller RH. 1996. A novel form of migration of glial precursors. Glia 16:27-39.
49. Owh P, da Cruz LA, Ackerley CA, Moscarello MA. 1997. Increased expression of CD44 on astrocytoma cells induced by binding myelin basic protein. Eur J Cell Biol 74:172-180.
50. Parnavelas JG, Nadarajah B. 2001. Radial glial cells: are they really glia? Neuron 31:881-884.
51. Pevny LH, Sockanathan S, Placzek M, Lovell-Badge R. 1998. A role for SOX1 in neural determination. Development 125:1967-1978.
52. Pixley SK, Kobayashi Y, de Vellis J. 1984. Monoclonal antibody to intermediate filament proteins in astrocytes. J Neurosci Res 12: 525-541.
53. Powell EM, Geller HM. 1999. Dissection of astrocyte-mediated cues in neuronal guidance and process extension. Glia 26:73-83.
54. Pringle NP, Richardson WD. 1993. A singularity of PDGF alphareceptor expression in the dorsoventral axis of the neural tube may define the origin of the oligodendrocyte lineage. Development 117: 525-533.
55. Qi Y, Cai J, Wu Y, Wu R, Lee J, Fu H, Rao M, Sussel L, Rubenstein J, Qiu M. 2001. Control of oligodendrocyte differentiation by the Nkx2.2 homeodomain transcription factor. Development 128:2723-2733.
56. Rakic P. 1991. Glial cells in development: in vivo and in vitro approaches. Ann NY Acad Sci 633:96-99.
57. Rao MS, Mayer-Proschel M. 1997. Glial-restricted precursors are derived from multipotent neuroepithelial stem cells. Dev Biol 188: 48-63.
58. Rao MS, Noble M, Mayer-Proschel M. 1998. A tripotential glial precursor cell is present in the developing spinal cord. Proc Natl Acad Sci USA 95:3996-4001.
59. Rao MS. 1999. Multipotent and restricted precursors in the central nervous system. Anat Rec 257:137-148.
60. Roessmann U, Velasco ME, Sindely SD, Gambetti P. 1980. Glial fibrillary acidic protein (GFAP) in ependymal cells during development: an immunocytochemical study. Brain Res 200:13-21.
61. Schaeren-Wiemers N, Gerfin-Moser A. 1993. A single protocol to detect transcripts of various types and expression levels in neural tissue and cultured cells: in situ hybridization using digoxigenin-labelled cRNA probes. Histochemistry 100:431-440.
62. Schmidt-Kastner R, Szymas J. 1990. Immunohistochemistry of glial fibrillary acidic protein, vimentin and S-100 protein for study of astrocytes in hippocampus of rat. J Chem Neuroanat 3:179-192.
63. Singer HS, Chiu AY, Meiri KF, Morell P, Nelson PG, Tennekoon G. 1994. Advances in understanding the development of the nervous system. Curr Opin Neurol 7:153-159.
64. Spassky N, Goujet-Zalc C, Parmantier E, Olivier C, Martinez S, Ivanova A, Ikenaka K, Macklin W, Cerruti I, Zalc B, Thomas JL. 1998. Multiple restricted origin of oligodendrocytes. J Neurosci 18:8331-8343.
65. Takebayashi H, Yoshida S, Sugimori M, Kosako H, Kominami R, Nakafuku M, Nabeshima Y. 2000. Dynamic expression of basic helix-loop-helix Olig family members: implication of Olig2 in neuron and oligodendrocyte differentiation and identification of a new member, Olig3. Mech Dev 99:143-148.
66. Van Raay TJ, Wang YK, Stark MR, Rasmussen JT, Francke U, Vetter ML, Rao MS. 2001. Frizzled 9 is expressed in neural precursor cells in the developing neural tube. Dev Genes Evol 211:453-457.
67. Vernadakis A. 1996. Glia-neuron intercommunications and synaptic plasticity. Prog Neurobiol 49:185-214.
68. Wolswijk G. 1998. Chronic stage multiple sclerosis lesions contain a relatively quiescent population of oligodendrocyte precursor cells. J Neurosci 18:601-609.
69. Wood PM, Bunge RP. 1991. The origin of remyelinating cells in the adult central nervous system: the role of the mature oligodendrocyte. Glia 4:225-232.
70. Wu YY, Mujtaba T, Han SS, Fischer I, Rao MS. 2002. Isolation of a glial-restricted tripotential cell line from embryonic spinal cord cultures. Glia 38:65-79.
71. Ylagan LR, Quinn B. 1997. CD44 expression in astrocytic tumors. Mod Pathol 10:1239-1246.
72. Zhou Q, Wang S, Anderson DJ. 2000. Identification of a novel family of oligodendrocyte lineage-specific basic helix-loop-helix transcription factors. Neuron 25:331-343.
73. Zhou Q, Anderson DJ. 2002. The bHLH transcription factors OLIG2 and OLIG1 couple neuronal and glial subtype specification. Cell 109:61-73.