Sequence of oligodendrocyte development in the human fetal telencephalon

GLIA

Volumn 49, Issue 4, 2005, Pages 480-491

  Jakovcevski, Igor ^a   Zecevic, Nada ^a  

^a UNIVERSITY OF CONNECTICUT HEALTH CENTER   (United States)

Author keywords

Midgestation; Myelination; Organotypic slice culture

Indexed keywords

ANTIBODY; MESSENGER RNA;

ARTICLE; BRAIN CORTEX; CELL DENSITY; CELL MIGRATION; CELL POLARITY; CENTRAL NERVOUS SYSTEM; DIENCEPHALON; FETUS; FOREBRAIN; GESTATIONAL AGE; HUMAN; HUMAN CELL; HUMAN TISSUE; MYELINATION; NERVE CELL DIFFERENTIATION; NERVE FIBER; NEURAL STEM CELL; OLIGODENDROCYTE PROGENITOR CELL; OLIGODENDROGLIA; PRIORITY JOURNAL; TELENCEPHALON; WHITE MATTER;

ANTIGENS; BIOLOGICAL MARKERS; CELL COMMUNICATION; CELL DIFFERENTIATION; CELL LINEAGE; CELL MOVEMENT; CELL SHAPE; FETAL DEVELOPMENT; FLUORESCENT ANTIBODY TECHNIQUE; HUMANS; MEMBRANE PROTEINS; MYELIN PROTEOLIPID PROTEIN; MYELIN SHEATH; NERVE FIBERS, MYELINATED; NERVE TISSUE PROTEINS; OLIGODENDROGLIA; ORGAN CULTURE TECHNIQUES; PHENOTYPE; PROTEOGLYCANS; RECEPTOR, PLATELET-DERIVED GROWTH FACTOR BETA; RNA, MESSENGER; SIGNAL TRANSDUCTION; STEM CELLS; TELENCEPHALON; THALAMUS;

EID: 14844366333     PISSN: 08941491     EISSN: None     Source Type: Journal    
DOI: 10.1002/glia.20134     Document Type: Article

References (75)

1. Back SA, Luo NL, Borenstein NS, Levine JM, Volpe JJ, Kinney HC. 2001. Late oligodendrocyte progenitors coincide with the developmental widow of vulnerability for human perinatal white matter injury. J Neurosci 21:1302-1312.
2. Back SA, Han BH, Luo NL, Chricton CA, Xanthaudakis S, Tam J, Arvin KL, Holtzman DM. 2002. Selective vulnerability of late oligodendrocyte progenitors to hypoxia-ischemia. J Neurosci 22:455-463.
3. Bansal R, Warrington AE, Gard AL, Ranscht B, Pfeiffer SE. 1989. Multiple and novel specificities of monoclonal antibodies O1, O4 and R-mAb used in the analysis of oligodendrocyte development. J Neurosci Res 24:548-557.
4. Bansal R, Lakhina V, Remedios R, Tole S. 2003. Expression of FGF receptors 1, 2, 3 in the embryonic and postnatal mouse brain compared with Pdgfralpha, Olig2 and Plp/dm20: implications for oligodendrocyte development. Dev Neurosci 25:83-95.
5. Barres BA, Raff MC. 1993. Proliferation of oligodendrocyte precursor cells depends on electrical activity in axons. Nature 361:258-260.
6. Boulder Committee. 1970. Embryonic vertebrate central nervous system: revised terminology. Anat Rec 166:257-261.
7. Butt AM, Duncan A, Hornby MF, Kirvell SL, Hunter A, Levine JM, Berry M. 1999. Cells expressing the NG2 antigen contact nodes of Ranvier in adult CNS white matter. Glia 26:84-91.
8. Butt AM, Kiff J, Hubbard P, Berry M. 2002. Synantocytes: new functions for novel NG2 expressing glia. J Neurocytol 31:551-565.
9. Chang A, Nishiyama A, Peterson J, Prineas J, Trapp BD. 2000. NG2-positive oligodendrocyte progenitor cells in adult human brain and multiple sclerosis lesions. J Neurosci 20:6404-6412.
10. Colello RJ, Devey LR, Imperato E, Pott U. 1995. The chronology of oligodendrocyte differentiation in the rat optic nerve: evidence for a signaling step initiating myelination in the CNS. J Neurosci 15: 7665-7672.
11. Curtis R, Cohen J, Fok-Seang J, Hanley MR, Gregson NA, Reynolds R, Wilkin GP. 1988. Development of macroglial cells in rat cerebellum. I. Use of antibodies to follow early in vivo development and migration of oligodendrocytes. J Neurocytol 17:43-54.
12. Dahl D, Rueger DC, Bignami A, Weber K, Osborn M. 1981. Vimentin, the 57,000 molecular weight protein of fibroblast filaments, is the major cytoskeleton component in immature glia. Eur J Cell Biol 24:191-196.
13. Dou CL, Levine JM. 1994. Inhibition of neurite growth by the NG2 chondroitin sulfate proteoglycan. J Neurosci 14:7616-7628.
14. Filipovic R, Rakic S, Zecevic N. 2002. Expression of Golli proteins in adult human brain and multiple sclerosis lesions. J Neuroimmunology 127:1-12.
15. Filipovic R, Jakovcevski I, Zecevic N. 2003. GRO-alpha and CXCR2 in the human fetal brain and multiple sclerosis lesions. Dev Neurosci 25:279-290.
16. 2 may influence oligodendrocyte development in the human fetal brain. Soc. Neurosci. Abstract. 141.6.
17. Franklin RJ. 2002. Why does remyelination fail in multiple sclerosis? Nat Rev Neurosci 3:705-714.
18. Gogate N, Verma L, Zhou JM, Milward E, Rusten R, O'Connor M, Kufta C, Kim J, Hudson L, Dubois-Dalcq M. 1994. Plasticity in the adult human oligodendrocyte lineage. J Neurosci 14:4571-4587.
19. Greenwood K, Butt AM. 2003. Evidence that perinatal and adult NG2-glia are not conventional oligodendrocyte progenitors and do not depend on axons for their survival. Mol Cell Neurosci 23:544-558.
20. Hajihosseini M, Tham TN, Dubois-Dalcq M. 1996. Origin of oligodendrocytes within the human spinal cord. J Neurosci 16:7981-7994.
21. Hardy R, Reynolds R. 1991. Proliferation and differentiation potential of rat forebrain oligodendroglial progenitors both in vitro and in vivo. Development 111:1061-1080.
22. Hubener M, Gotz M, Klostermann S, Bolz J. 1995. Guidance of thalamocortical axons by growth-promoting molecules in developing rat cerebral cortex. Eur J Neurosci 7:1963-1972.
23. Hunter DD, Llinas R, Ard M, Merlie JP, Sanes JR. 1992. Expression of s-laminin and laminin in the developing rat central nervous system. J Comp Neurol 323:238-251.
24. Kakita A, Goldman JE. 1999. Patterns and dynamics of SVZ cell migration in the postnatal forebrain: monitoring living progenitors in slice preparations. Neuron 23:461-472.
25. Kinney HC, Back SA. 1998. Human oligodendroglial development: relationship to periventricular leukomalacia. Semin Pediatr Neurol 5:180-189.
26. Kinney HC, Karthigasan J, Borenshteyn NI, Flax JD, Kirschner DA. 1994. Myelination in the developing human brain: biochemical correlates. Neurochem Res 19:983-996.
27. Kostovic I, Judas M. 2002. Correlation between the sequential ingrowth of afferents and transient patterns of cortical lamination in preterm infants. Anat Rec 267:1-6.
28. Kostovic I, Rakic P. 1990. Developmental history of the transient subplate zone in the visual and somatosensory cortex of the macaque monkey and human brain. J Comp Neurol 297:441-470.
29. Levine JM, Stincone F, Lee YS. 1993. Development and differentiation of glial precursor cells in the rat cerebellum. Glia 7:307-321.
30. Levine JM, Reynolds R, Fawcett JW. 2001. The oligodendrocyte precursor cell in health and disease. Trends Neurosci 24:39-47.
31. Linington C, Bradl M, Lassmann H, Brunner C, Vass K. 1988. Augmentation of demyelination in rat acute allergic encephalomyelitis by circulating mouse monoclonal antibodies directed against a myelin/oligodendrocyte glycoprotein. Am J Pathol 130:443-454.
32. 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.
33. Mallon BS, Shick HE, Kidd GJ, Macklin WB. 2002. Proteolipid promoter activity distinguishes two populations of NG2-positive cells throughout neonatal cortical development. J Neurosci 22:876-885.
34. Marshall CA, Goldman JE. 2002. Subpallial Dlx2-expressing cells give rise to astrocytes and oligodendrocytes in the cerebral cortex and white matter. J Neurosci 22:9821-9830.
35. Nakajima K, Ikenaka K, Kagawa T, Aruga J, Nakao J, Nakahira K, Shiota C, Kim SU, Mikoshiba K. 1993. Novel isoforms of mouse myelin basic protein predominantly expressed in embryonic stage. J Neurochem 60:1554-1563.
36. Nery S, Wichterle H, Fishell G. 2001. Sonic hedgehog contributes to oligodendrocyte specification in the mammalian forebrain. Development 128:527-540.
37. Nishiyama A, Lin X-H, Giese N, Heldin C-H, Stallcup WB. 1996. Co-localisation of NG2 proteoglycan and PDGF alpha receptor on O2A progenitor cells in the developing rat brain. J Neurosci Res 43:299-314.
38. + glial cells are distinct from resting and activated microglia. J Neurosci Res 48:299-312.
39. Nishiyama A, Watanabe M, Yang Z, Bu J. 2002. Identity, distribution, and development of polydendrocytes: NG2-expressing glial cells. J Neurocytol 31:437-455.
40. Ong WY, Levine JM. 1999. A light and electron microscopic study of NG2 chondroitin sulfate proteoglycan-positive oligodendrocyte precursor cells in the normal arid kainate-lesioned rat hippocampus. Neuroscience 92:83-95.
41. Pearlman AL, Sheppard AM. 1996. Extracellular matrix in early cortical development. Prog Brain Res 108:117-134.
42. Pfeiffer SE, Warrington AE, Bansal, R. 1993. The OL and its many cellular processes. Trends Cell Biol 3:191-197.
43. Pribyl TM, Campagnoni CW, Kampf K, Ellison JA, Landry CF, Kashima T, McMahon J, Campagnoni AT. 1996. Expression of the myelin basic protein gene locus in neurons and oligodendrocytes in the human fetal central nervous system. J Comp Neurol 374:342-353.
44. Pringle NP, Richardson WD. 1993. A singularity of PDGF alpha-receptor expression in the dorsoventral axis of the neural tube may define the origin of the oligodendrocyte lineage. Development 117: 525-533.
45. 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.
46. Rakic S, Zecevic N. 2003. Early oligodendrocyte progenitor cells in the human fetal telencephalon. Glia 41:117-127.
47. Rivkin MJ, Flax J, Mozell R, Osathanondh R, Volpe JJ, Villa-Komaroff L. 1995. Oligodendroglial development in human fetal cerebrum. Ann Neurol 38:92-101.
48. Sauvageot CM, Stiles CD. 2002. Molecular mechanisms controlling cortical gliogenesis. Curr Opin Neurobiol 12:244-249.
49. Scolding NJ, Frith S, Linington C, Morgan BP, Campbell AK, Compston DA. 1989. Myelin-oligodendrocyte glycoprotein (MOG) is a surface marker of oligodendrocyte maturation. J Neuroimmunol 22:169-176.
50. Scolding N, Franklin R, Stevens S, Heldin CH, Compston A, Newcombe J. 1998. Oligodendrocyte progenitors are present in the normal adult human CNS and in the lesions of multiple sclerosis. Brain 121:2221-2228.
51. Sheppard AM, Hamilton SK, Pearlman AL. 1991. Changes in the distribution of extracellular matrix components accompany early morphogenetic events of mammalian cortical development. J Neurosci 11:3928-3942.
52. Sommer I, Schachner M. 1981. Monoclonal antibodies (O1 to O4) to oligodendrocyte cell surfaces: an immunocytological study in the central nervous system. Dev Biol 83:311-327.
53. 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.
54. Spassky N, Heydon K, Mangatal A, Jankovski A, Olivier C, Queraud-Lesaux F, Goujet-Zalc C, Thomas JL, Zalc B. 2001. Sonic hedgehog-dependent emergence of oligodendrocytes in the telencephalon: evidence for a source of oligodendrocytes in the olfactory bulb that is independent of PDGFRalpha signaling. Development 128:4993-5004.
55. Spassky N, de Castro F, Le Bras B, Heydon K, Queraud-LeSaux F, Bloch-Gallego E, Chedotal A, Zalc B, Thomas JL. 2002. Directional guidance of oligodendroglial migration by class 3 semaphorins and netrin-1. J Neurosci 22:5992-6004.
56. Stallcup WB, Beasley L. 1987. Bipotential glial precursor cells of the optic nerve express NG2 proteoglycan. J Neurosci 7:2737-2744.
57. Stallcup WB. 2002. The NG2 proteoglycan: past insights and future prospects. J Neurocytol 31:423-435.
58. Timsit SG, Bally-Cuif L, Colman DR, Zalc B. 1992. DM-20 mRNA is expressed during the embryonic development of the nervous system of the mouse. J Neurochem 58:1172-1175.
59. Timsit S, Martinez S, Allinquant B, Peyron F, Puelles L, Zalc B. 1995. Oligodendrocytes originate from restricted zone of embryonic ventral neural tube defined by DM20 mRNA. J Neurosci 15:1012-1024.
60. Tosic M, Rakic S, Matthieu JM, Zecevic N. 2002. Identification of Golli and myelin basic proteins in human brain during early development. Glia 37:219-228.
61. Trapp BD, Nishiyama A, Cheng D, Macklin W. 1997. Differentiation and death of premyelinating oligodendrocytes in developing rodent brain. J Cell Biol 137:459-468.
62. Ulfig N, Nickel J, Saretzki U. 1998. Alterations in myelin formation in fetal brains of twins. Pediatric Neurol 19:287-293.
63. Ulfig N, Neudorfer F, Bohl J. 1999. Distribution patterns of vimentin-immunoreactive structures in the human prosencephalon during the second half of gestation. J Anat 195:87-100.
64. Ulfig N, Briese M, Bohl J. 2002. Expression of oligodendrocyte-specific protein (OSP/claudin-11) in the human fetal forebrain. Neuroembryology 1:48-53.
65. Volpe JJ. 2001. Neurobiology of periventricular leukomalacia in the premature infant. Pediatr Res 50:553-562.
66. + oligodendrocytes in the postnatal rat cerebellum: analysis in unfixed tissue slices using anti-glycolipid antibodies. J Neurosci Res 33:338-353.
67. Warrington AE, Barbarese E, Pfeiffer SE. 1993. Differential myelinogenic capacity of specific developmental stages of the oligodendrocyte lineage upon transplantation into hypomyelinating hosts. J Neurosci Res 34:1-13.
68. Weidenheim KM, Kress Y, Epshteyn I, Rashbaum WK, Lyman WD. 1992. Early myelination in the human fetal lumbosacral spinal cord: characterization by light and electron microscopy. J Neuropathol Exp Neurol 51:142-149.
69. Weidenheim KM, Epshteyn I, Rashbaum WK, Lyman WD. 1993. Neuroanatomical localization of myelin basic protein in the late first and early second trimester human foetal spinal cord and brainstem. J Neurocytol 22:507-516.
70. Woodruff RH, Tekki-Kessaris N, Stiles CD, Rowitch DH, Richardson WD. 2001. Oligodendrocyte development in the spinal cord and telencephalon: common themes and new perspectives. Int J Dev Neurosci 19:379-385.
71. Yakovlev PI, Lecourse AR. 1967. The myelinogenetic cycles in regional maturation of the brain. In: Minkowsky A, editor. Regional development of the brain in early life. Oxford: Blackwell. p 3-70.
72. Yu WP, Collarini EJ, Pringle NP, Richardson WD. 1994. Embryonic expression of myelin genes: evidence for a focal source of oligodendrocyte precursors in the ventricular zone of the neural tube. Neuron 12:1353-1362.
73. Zecevic N, Andjelkovic A, Matthieu J-M, Tosic M. 1998. Myelin basic protein is expressed in the human embryonic CNS. Dev Brain Res 105:97-108.
74. Zerlin M, Levison SW, Goldman JE. 1995. Early patterns of migration, morphogenesis, and intermediate filament expression of subventricular zone cells in the postnatal rat forebrain. J Neurosci 15:7238-7249.
75. Zhang S-C, Ge B, Duncan ID. 2000. Tracing human oligodendroglial development in vitro. J Neurosci Res 59:421-429.