Defective oligodendrocyte development and severe hypomyelination in PDGF-A knockout mice

Development

Volumn 126, Issue 3, 1999, Pages 457-467

  Fruttiger, Marcus ^a   Karlsson, Linda ^b   Hall, Anita C ^a,d   Abramsson, Alexandra ^b   Calver, Andrew R ^a   Boström, Hans ^b   Willetts, Karen ^c   Bertold, Claes Henric ^b   Heath, John K ^c   Betsholtz, Christer ^b   Richardson, William D ^a  

^a UNIVERSITY COLLEGE LONDON   (United Kingdom)

^b UNIVERSITY OF GOTHENBURG   (Sweden)

^c UNIVERSITY OF BIRMINGHAM   (United Kingdom)

^d KING'S COLLEGE LONDON   (United Kingdom)

Author keywords

Central nervous system; Knockout mouse; MBP; Myelin; Oligodendrocyte; PDGF; PDGF receptor; PLP DM 20; Progenitor cell

Indexed keywords

PLATELET DERIVED GROWTH FACTOR A; PLATELET DERIVED GROWTH FACTOR B; PLATELET DERIVED GROWTH FACTOR RECEPTOR; PROTEOLIPID PROTEIN;

ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CEREBELLUM; CONTROLLED STUDY; EMBRYO; KNOCKOUT MOUSE; MEDULLA OBLONGATA; MOUSE; MYELINATION; NERVE CELL DIFFERENTIATION; NERVOUS SYSTEM DEVELOPMENT; NONHUMAN; OLIGODENDROGLIA; PRIORITY JOURNAL; SPINAL CORD; STEM CELL; TREMOR;

ANIMALS; BRAIN; CELL DIFFERENTIATION; CELL DIVISION; CENTRAL NERVOUS SYSTEM; MICE; MICE, KNOCKOUT; MYELIN PROTEOLIPID PROTEIN; MYELIN SHEATH; OLIGODENDROGLIA; PLATELET-DERIVED GROWTH FACTOR; PROTO-ONCOGENE PROTEINS; PROTO-ONCOGENE PROTEINS C-SIS; RECEPTOR, PLATELET-DERIVED GROWTH FACTOR ALPHA; RECEPTORS, PLATELET-DERIVED GROWTH FACTOR;

ANIMALIA;

EID: 0033031266     PISSN: 09501991     EISSN: None     Source Type: Journal    
DOI: None     Document Type: Article

References (60)

1. Armstrong, R., Harvath, L. and Dubois-Dalcq, M. (1991). Astrocytes and O-2A progenitors migrate toward distinct molecules in a microchemotaxis chamber. Ann. NY Acad. Sci. 633, 520-522.
2. Barres, B. A., Hart, I. K., Coles, H. S. R., Burne, J. F., Voyvodic, J. T., Richardson, W. D. and Raff, M. C. (1992). Cell death and control of cell survival in the oligodendrocyte lineage. Cell 70, 31-46.
3. Barres, B. A., Raff, M. C., Gaese, F., Bartke, I., Dechant, G. and Barde, Y. A. (1994). A crucial role for neurotrophin-3 in oligodendrocyte development. Nature 367, 371-375.
4. Belichenko, P. V. and Celio, M. R. (1997). Relationships between oligodendrocytes and axons. Neuroreport 8, 3965-3967.
5. Boström, H., Willetts, K., Pekny, M., Leveén, P., Lindahl, P., Hedstrand, H., Pekna, M., Hellström, M., Gebre-Medhin, S., Schalling, M., Nilsson, M., Kurland, S., Törnell, J., Heath, J. K. and Betsholtz, C. (1996). PDGF-A signaling is a critical event in lung alveolar myofibroblast development and alveogenesis. Cell 85, 863-873.
6. Bögler, O., Wren, D., Barnett, S. C., Land, H. and Noble, M. (1990) Cooperation between two growth factors promotes extended self-renewal and inhibits differentiation of O-2A progenitor cells. Proc. Natl. Acad. Sci. USA 87, 6368-6372.
7. Butt, A. M., Colquhoun, K., Tutton, M. and Berry, M. (1994) Three-dimensional morphology of astrocytes and oligodendrocytes in the intact mouse optic nerve. J. Neurocytol. 23, 469-485.
8. Butt, A. M., Ibrahim, M., Ruge, F. M. and Berry, M. (1995). Biochemical subtypes of oligodendrocyte in the anterior medullary velum of the rat as revealed by the monoclonal antibody Rip. Glia 14, 185-197.
9. Butt, A. M., Ibrahim, M. and Berry, M. (1997). The relationship between developing oligodendrocyte units and maturing axons during myelinogenesis in the anterior medullary velum of neonatal rats. J. Neurocytol. 27, 327-338.
10. Calver, A. R., Hall, A. C., Yu, W.-P., Walsh, F. S., Heath, J. K., Betsholtz, C. and Richardson, W. D. (1998). Oligodendrocyte population dynamics and the role of PDGF in vivo. Neuron 20, 869-882.
11. Canoll, P. D., Musacchio, M. A., Hardy, R., Reynolds, R., Marchionni, M. A. and Salzer, J. L. (1996). GGF/neuregulin is a neuronal signal that promotes the proliferation and survival and inhibits differentiation of oligodendrocyte progenitors. Neuron 17, 229-243.
12. del Rio Hortega, P. (1942). La neuroglia normal. Conceptos de neuroglioma y angioglioma. Arch. de Histol. Norm. y Patol. 1, 5-71.
13. Ellison, J. A., Scully, S. A. and de Vellis, J. (1996). Evidence for neuronal regulation of oligodendrocyte development: cellular localization of platelet-derived growth factor alpha-receptor and A-chain mRNA during cerebral cortex development in the rat. J. Neurosci. Res. 45, 28-39.
14. Fanarraga, M. L. and Milward, E. A. (1997). Characterization of a putative novel type of oligodendrocyte in cultures from rat spinal cord. Eur J. Neurosci. 9, 2213-2217.
15. Fanarraga, M. L., Griffiths, I. R., Zhao, M. and Duncan, I. D. (1998). Oligodendrocytes are not inherently programmed to myeltnate a specific size of axon. J. Comp. Neurol. 399, 94-100.
16. Hall, A., Giese, N. A. and Richardson, W. D. (1996). Spinal cord oligodendrocytes develop from ventrally-derived progenitor cells that express PDGF alpha-receptors. Development 122, 4085-4094.
17. Hardy, R. J. (1997). Dorsoventral patterning and oligodendroglial specification in the developing central nervous system. J. Neurosci. Res. 50, 139-145.
18. Hardy, R. J. and Friedrich, V., Jr. (1996). Oligodendrocyte progenitors are generated throughout the embryonic mouse brain, but differentiate in restricted foci. Development 122, 2059-2069.
19. Heldin, C.-H. and Westermark, B. (1989). Platelet-derived growth factor: three isoforms and two receptor types. Trends Genet. 5, 108-111.
20. Hildebrand, C., Remahl, S., Persson, H. and Bjartmar, C. (1993). Myelinated nerve fibres in the CNS. Prog Neurobiol. 40, 319-384.
21. Ikenaka, K., Kagawa, T. and Mikoshiba, K. (1993). Selective expression of DM-20, an alternatively spliced rnyelin proteolipid protein gene product, in developing nervous system and in nonglial cells. J. Neurochem. 58, 2248-2253.
22. Leber, S. M. and Sanes, J. R. (1995). Migratory paths of neurons and glia in the embryonic chick spinal cord. J. Neurosci. 15, 1236-1248.
23. Leveén, P., Pekny, M., Gebre-Medhin, S., Swolin, B., Larsson, E. and Betsholtz, C. (1994). Mice deficient for PDCF B show renal, cardiovascular and hematological abnormalities. Genes Dev. 8, 1875-1887.
24. Levison, S. W., Chuang, C., Abramson, B. J. and Coldman, J. E. (1993). The migrational patterns and developmental fates of glial precursors in the rat subventricular zone are temporally regulated. Development 119, 611-622.
25. Levison, S. W. and Goldman, J. E. (1993). Both oligodendrocytes and astrocytes develop from progenitors in the subventricular zone of postnatal rat forebrain. Neuron 10, 201-212.
26. Lindahl, P., Johansson, B., Levéen, P. and Betsholtz, C. (1997a). Pericyte loss and microaneurysm formation in platelet-derived growth factor B-chain-deficient mice. Science 277, 242-245.
27. Lindahl, P., Karlsson, L., Hellström, M., Gebre-Medhin, S., Willetts, K., Heath, J. K. and Betsholtz, C. (1997b). Alveogenesis failure in PDGF-A-deficient mice is coupled to lack of distal spreading of alveolar smooth muscle cell progenitors during lung development. Development 124, 3943-3953.
28. Lindahl, P. and Betsholtz, C. (1998). Not all myofibroblasts are alike: revisiting the role of PDGF-A and PDGF-B using PDGF-targeted mice. Curt: Opin. Nephrol. Hypertens. 7, 21-26.
29. Lindahl, P., Hellström, M., Kalén, M., Karlsson, L., Pekny, M., Pekna, M., Soriano, P. and Betsholtz, C. (1998). Paracrine PDGF B/PDGFRβ signaling controls mesangial cell development in kidney glomeruli. Development 125, 3313-3322.
30. Luna, L. G. (1968). Manual of Histological Staining Methods of the Armed Forces Institute of Pathology. 203 pp. McGraw Publishing Co., New York.
31. Magaud, J. P., Sargent, I., Clarke, P. J., Ffrench, M., Rimokh, R. and Mason, D. Y. (1989). Double immunocytochemistry labelling of cell and tissue samples with monoclonal anti-bromodeoxyuridine. J. Histochem. Cytochem. 37, 1517-1527.
32. McKinnon, R. D., Matsui, T., Dubois-Dalcq, M. and Aaronson, S. A. (1990). FGF modulates the PDGF-driven pathway of oligodendrocyte development. Neuron 5, 603-614.
33. McMorris, F. A. and Dubois-Dalcq, M. (1998). Insulin-like growth factor I promotes cell proliferation and oligodendroglial commitment in rat glial progenitor cells developing in vitro. J. Neurosci. Res. 21, 199-209.
34. Mudhar, H. S., Pollock, R. A., Wang, C., Stiles, C. D. and Richardson, W. D. (1993). PDGF and its receptors in the developing rodent retina and optic nerve. Development 118, 539-552.
35. Nait-Oumesmar, B., Vignais, L. and Baron-Van Evercooren, A. (1997). Developmental expression of platelet-derived growth factor alpha-receptor in neurons and glial cells of the mouse CNS. J. Neurosci. 17, 125-139.
36. Nishiyama, A., Lin, X.-H., Giese, N. Heldin, C.-H. and Stallcup, W. B. (1996). Co-localization of NG2 proteoglycan and PDGF -receptor on O2A progenitor cells in the developing rat brain. J. Neurosci. Res. 43, 299-314.
37. Noble, M., Murray, K., Stroobant, P., Waterfield, M. D. and Riddle, P. (1988). Platelet-derived growth factor promotes division and motilily and inhibits premature differentiation of the oligodendrocyte/type-2 astrocyte progenitor cell. Nature 333, 560-562.
38. Noll, E. and Miller, R. H. (1993). Oligodendrocyte precursors originate at the ventral ventricular zone dorsal to the ventral midline region in the embryonic rat spinal cord. Development 118, 563-573.
39. Ono, K., Bansal, R., Payne, J., Rutishauser, U. and Miller, R. H. (1995). Early development and dispersal of oligodendrocyte precursors in the embryonic chick spinal cord. Development 121, 1743-1754.
40. Ono, K., Yasui, Y., Rutishauser, U. and Miller, R. H. (1997). Focal ventricular origin and migration of oligodendrocyte precursors into the chick optic nerve. Neuron 19, 283-292.
41. Orr-Urtreger, A. and Lonai, P. (1992). Platelet-derived growth factor-A and its receptor are expressed in separate, but adjacent cell layers of the mouse embryo. Development 115, 1045-1058.
42. Peyron, F., Timsit, S., Thomas, J.-L., Kagawa, T., Ikenaka, K. and Zalc, B. (1997). In situ expression of PLP/DM-20, MBP and CNP during embryonic and postnatal development of the jimpy mutant and of transgenic mice overexpressing PLP. J. Neurosci. Res. 50, 190-201.
43. Pfeiffer, S. E., Warrington, A. E. and Bansal, R. (1994). The oligodendrocyte and its many cellular processes. Trends Cell Biol. 3, 191-197.
44. Pringle, N., Collarini, E. J., Mosley, M. J., Heldin, C.-H., Westermark, B. and Richardson, W. D. (1989). PDGF A chain homodimers drive proliferation of bipotential (O-2A) glial progenitor cells in the developing rat optic nerve. EMBO J. 8, 1049-1056.
45. Pringle, N. P. and Richardson, W. D. (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.
46. Pringle, N. P., Yu, W.-P., Guthrie, S., Roelink, H., Lumsden, A., Peterson, A. C. and Richardson, W. D. (1996). Determination of neuroepithelial cell fate: induction of the oligodendrocyte lineage by ventral midline cells and Sonic hedgehog. Dev. Biol. 177, 30-42.
47. Pringle, N. P., Guthrie, S., Lumsden, A. and Richardson, W. D. (1998). Dorsal spinal cord neuroepithelium generates astrocytes but not oligodendrocytes. Neuron 20, 883-893.
48. Raff, M. C., Miller, R. H. and Noble, M. (1983). A glial progenitor cell that develops in vitro into an astrocyte or an oligodendrocyte depending on the culture medium. Nature 303, 390-396.
49. Raff, M. C., Lillien, L. E., Richardson, W. D., Burne, J. F. and Noble, M. (1988). Platelet-derived growth factor from astrocytes drives the clock that times oligodendrocyte development in culture. Nature 333, 562-565.
50. Richardson, W. D., Pringle, N., Mosley, M. J., Westermark, B. and Dubois-Dalcq, M. (1988). A role for platelet-derived growth factor in normal gliogenesis in the central nervous system. Cell 53, 309-319.
51. Sasahara, M., Fries, J. W. U., Raines, E. W., Gown, A. M., Westrum, L. E., Frosch, M. P., Bonthron, D. T., Ross, R. and Collins, T. (1991). PDGF B-chain in neurons of the central nervous system, posterior pituitary and in a transgenic model. Cell 64, 217-227.
52. Sasahara, M., Sato, H., Iihara, K., Wang, J., Chue, C. H., Takayama, S., Hayase, Y. and Hazama, F. (1995). Expression of platelet-derived growth factor B-chain in the mature rat brain and pituitary gland. Brain Res. Mol. Brain Res. 32, 63-74.
53. Spassky, N., Goujet-Zalc, C., Parmantier, E., Olivier, C., Martinez, S., Ivanova, A., Ikenaka, K., Macklin, W., Cerruti, I., Zalc, B. and Thomas, J.-L. (1998). Multiple restricted origins of oligodendrocytes. J. Neurosci. 18, 8331-8343.
54. Timsit, S. G., Bally-Cuif, L., Colman, D. R. and Zalc, B. (1992). DM 20 mRNA is expressed during the embryonic development of the nervous system of the mouse. J. Neurochem. 58, 1172-1175.
55. Timsit, S., Martinez, S., Allinquant, B., Peyron, F., Puelles, L. and Zalc, B. (1995). Oligodendrocytes originate in a restricted zone of the embryonic ventral neural tube defined by DM-20 mRNA expression. J. Neurosci. 15, 1012-1024.
56. Vaughn, J. E. (1969). An electron microscope analysis of gliogenesis in rat optic nerves. Z. Zellforsch. 94, 293-324.
57. Vignais, L., Nait Oumesmar, B. and Baron-Van Evercooren, A. (1995). PDGF-α receptor is expressed by mature neurons of the central nervous system. NeuroReport 6, 1993-1996.
58. Williams, B. P., Park, J. K., Alberta, J. A., Muhlebach, S. G., Hwang, G. Y., Roberts, T. M. and Stiles, C. D. (1997). A PDGF-mediated immediate early response initiates neuronal differentiation in ventricular zone progenitor cells. Neuron 18, 553-562.
59. Yeh, H.-J., Ruit, K. G., Wang, Y. -X., Parks, W. C., Snider, W. D. and Deuel, T. F. (1991). PDGF A-chain gene is expressed by mammalian neurons during development and in maturity. Cell 64, 209-216.
60. Yu, W.-P., Collarini, E. J., Pringle, N. P. and Richardson, W. D. (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.