Platelet-derived growth factor regulates oligodendrocyte progenitor numbers in adult CNS and their response following CNS demyelination

Molecular and Cellular Neuroscience

Volumn 25, Issue 2, 2004, Pages 252-262

  Woodruff, Rachel H ^a   Fruttiger, Marcus ^a,b   Richardson, William D ^a   Franklin, Robin J M ^b  

^a UNIVERSITY COLLEGE LONDON   (United Kingdom)

^b UNIVERSITY OF CAMBRIDGE   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

CUPRIZONE; GLIAL FIBRILLARY ACIDIC PROTEIN; LYSOPHOSPHATIDYLCHOLINE; PLATELET DERIVED GROWTH FACTOR A;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CELL COUNT; CONTROLLED STUDY; DEMYELINATING DISEASE; MORPHOLOGY; MOUSE; NONHUMAN; OLIGODENDROGLIA; PRIORITY JOURNAL; PROMOTER REGION; PROTEIN EXPRESSION; REGULATORY MECHANISM; REMYELINIZATION; STEM CELL; TRANSGENIC ANIMAL; WHITE MATTER; WILD TYPE;

ANIMALS; CENTRAL NERVOUS SYSTEM; CUPRIZONE; DEMYELINATING DISEASES; DISEASE MODELS, ANIMAL; GLIAL FIBRILLARY ACIDIC PROTEIN; LYSOPHOSPHATIDYLCHOLINES; MICE; MICE, TRANSGENIC; NERVE REGENERATION; OLIGODENDROGLIA; PLATELET-DERIVED GROWTH FACTOR; PROMOTER REGIONS (GENETICS); STEM CELLS; UP-REGULATION;

MUS MUSCULUS;

EID: 1542425338     PISSN: 10447431     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.mcn.2003.10.014     Document Type: Article

References (58)

1. Allamargot C., Pouplard-Barthelaix A., Fressinaud C. A single intracerebral microinjection of platelet-derived growth factor (PDGF) accelerates the rate of remyelination in vivo. Brain Res. 918:2001;28-39.
2. Alonso G. Prolonged corticosterone treatment of adult rats inhibits the proliferation of oligodendrocyte progenitors present throughout white and gray matter regions of the brain. Glia. 31:2000;219-231.
3. Armstrong R.C., Harvath L., Duboisdalcq M.E. Type-1 astrocytes and oligodendrocyte-type-2 astrocyte glial progenitors migrate toward distinct molecules. J. Neurosci. Res. 27:1990;400-407.
4. Armstrong R.C., Dorn H.H., Kufta C.V., Friedman E., Dubois-Dalcq M.E. Pre-oligodendrocytes from adult human CNS. J. Neurosci. 12:1992;1538-1547.
5. Armstrong R.C., Le T.Q., Frost E.E., Borke R.C., Vana A.C. Absence of fibroblast growth factor 2 promotes oligodendroglial repopulation of demyelinated white matter. J. Neurosci. 22:2002;8574-8585.
6. Belachew S., Chittajallu R., Aguirre A.A., Yuan X., Kirby M., Anderson S., Gallo V. Postnatal NG2 proteoglycan-expressing progenitor cells are intrinsically multipotent and generate functional neurons. J. Cell Biol. 161:2003;169-186.
7. Bieber A.J., Warrington A., Asakura K., Ciric B., Kaveri S.V., Pease L.R., Rodriguez M. Human antibodies accelerate the rate of remyelination following lysolecithin-induced demyelination in mice. Glia. 37:2002;241-249.
8. Blakemore W.F. Remyelination of the superior cerebellar peduncle in the mouse following demyelination induced by feeding cuprizone. J. Neurol. Sci. 20:1973;73-83.
9. Blakemore W.F., Chari D.M., Gilson J.M., Crang A.J. Modelling large areas of demyelination in the rat reveals the potential and possible limitations of transplanted glial cells for remyelination in the CNS. Glia. 38:2002;155-168.
10. Calver A.R., Hall A.C., Yu W.P., Walsh F.S., Heath J.K., Betsholtz C., Richardson W.D. Oligodendrocyte population dynamics and the role of PDGF in vivo. Neuron. 20:1998;869-882.
11. Cannella B., Hoban C.J., Gao Y.L., Garcia-Arenas R., Lawson D., Marchionni M., Gwynne D., Raine C.S. The neuregulin, glial growth factor 2, diminishes autoimmune demyelination and enhances remyelination in a chronic relapsing model for multiple sclerosis. Proc. Natl. Acad. Sci. U. S. A. 95:1998;10100-10105.
12. Carroll W.M., Jennings A.R. Early recruitment of oligodendrocyte precursors in CNS remyelination. Brain. 117:1994;563-578.
13. Carroll W.M., Jennings A.R., Ironside L.J. Identification of the adult resting progenitor cell by autoradiographic tracking of oligodendrocyte precursors in experimental CNS demyelination. Brain. 121:1998;293-302.
14. Cenci di Bello I., Dawson M.R.L., Levine J.M., Reynolds R. Generation of oligodendroglial progenitors in acute inflammatory demyelinating lesions of the rat brain stem is stimulated by demyelination rather than inflammation. J. Neurocytol. 28:1999;365-381.
15. Chang A., Nishiyama A., Peterson J., Prineas J., Trapp B.D. NG2-positive oligodendrocyte progenitor cells in adult human brain and multiple sclerosis lesions. J. Neurosci. 20:2000;6404-6412.
16. Chang A., Tourtellotte W.W., Rudick R., Trapp B.D. Premyelinating oligodendrocytes in chronic lesions of multiple sclerosis. N. Engl. J. Med. 346:2002;165-173.
17. Charles P., Reynolds R., Seilhean D., Rougon G., Aigrot M.S., Niezgoda A., Zalc B., Lubetzki C. Re-expression of PSA-NCAM by demyelinated axons: an inhibitor or remyelination in multiple sclerosis? Brain. 25:2002;72-79.
18. 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. 16:1996;16-26.
19. Franklin R.J.M. Why does remyelination fail in multiple sclerosis? Nat. Rev., Neurosci. 3:2002;705-714.
20. Fruttiger M., Karlsson L., Hall A.C., Abramsson A., Calver A.R., Boström H., Willetts K., Bertold C.H., Heath J.K., Betsholtz C., Richardson W.D. Defective oligodendrocyte development and severe hypomyelination in PDGF-A knockout mice. Development. 126:1999;457-467.
21. Fruttiger M., Calver A.R., Richardson W.D. Platelet-derived growth factor is constitutively secreted from neuronal cell bodies but not from axons. Curr. Biol. 10:2000;1283-1286.
22. Gensert J.M., Goldman J.E. Endogenous progenitors remyelinate demyelinated axons in the adult CNS. Neuron. 19:1997;197-203.
23. Hall S.M. The effect of injections of lysophosphatidyl choline into white matter of the adult mouse spinal cord. J. Cell Sci. 10:1972;535-546.
24. Hinks G.L., Franklin R.J.M. Distinctive patterns of PDGF-A, FGF-2, IGF-I and TGF-beta1 gene expression during remyelination of experimentally-induced spinal cord demyelination. Mol. Cell. Neurosci. 14:1999;153-168.
25. Hinks G.L., Franklin R.J.M. Delayed changes in growth factor gene expression during slow remyelination in the CNS of aged rats. Mol. Cell. Neurosci. 16:2000;542-556.
26. Horner P.J., Power A.E., Kempermann G., Kuhn H.G., Palmer T.D., Winkler J., Thal L.J., Gage F.H. Proliferation and differentiation of progenitor cells throughout the intact adult rat spinal cord. J. Neurosci. 20:2000;2218-2228.
27. John G.R., Shankar S.L., Shafit-Zagardo B., Massimi A., Lee S.C., Raine C.S., Brosnan C.F. Multiple sclerosis: re-expression of a developmental pathway that restricts oligodendrocyte maturation. Nat. Med. 8:2002;1115-1121.
28. Keirstead H.S., Levine J.M., Blakemore W.F. Response of oligodendocyte progenitor cell population (defined by NG2 labelling) to demyelination of the adult spinal cord. Glia. 22:1998;161-170.
29. Kondo T., Raff M. Oligodendrocyte precursor cells reprogrammed to become multipotential CNS stem cells. Science. 289:2000;1754-1757.
30. Levine J.M., Reynolds R. Activation and proliferation of endogenous oligodendrocyte precursor cells during ethidium bromide-induced demyelination. Exp. Neurol. 160:1999;333-347.
31. Levine J.M., Reynolds R., Fawcett J.W. The oligodendrocyte precursor cell in health and disease. Trends Neurosci. 24:2001;39-47.
32. Lovas G., Szilagyi N., Majtenyi K., Palkovits M., Komoly S. Axonal changes in chronic demyelinated cervical spinal cord plaques. Brain. 123:2000;308-317.
33. Ludwin S.K. Remyelination in demyelinating diseases of the central nervous system. CRC Crit. Rev. Neurobiol. 3:1987;1-28.
34. Magaud J.P., Sargent I., Clarke P.J., ffrench M., Rimokh R., Mason D.Y. Double immunocytochemical labeling of cell and tissue samples with monoclonal anti-bromodeoxyuridine. J. Histochem. Cytochem. 37:1989;1517-1527.
35. Messersmith D.J., Murtie J.C., Le T.Q., Frost E.E., Armstrong R.C. Fibroblast growth factor 2 (FGF2) and FGF receptor expression in an experimental demyelinating disease with extensive remyelination. J. Neurosci. Res. 62:2000;241-256.
36. Milner R., Anderson H.J., Rippon R.F., McKay J.S., Franklin R.J.M., Marchionni M.A., Reynolds R., ffrench-Constant C. Contrasting effects of mitogenic growth factors on oligodendrocyte precursor cell migration. Glia. 19:1997;85-90.
37. Morell P., Barrett C.V., Mason J.L., Toews A.D., Hostettler J.D., Knapp G.W., Matsushima G.K. Gene expression in brain during cuprizone-induced demyelination and remyelination. Mol. Cell. Neurosci. 12:2000;220-227.
38. Noble M., Murray K., Stroobant P., Waterfield M.D., Riddle P. Platelet-derived growth factor promotes division and motility and inhibits permature differentiation of the oligodendrocyte/type-2 astrocyte progenitor cell. Nature. 333:1988;560-565.
39. O'Leary M.T., Hinks G.L., Charlton H.M., Franklin R.J.M. Increasing local levels of IGF-I mRNA expression using adenoviral vectors does not alter oligodendrocyte remyelination in the CNS of aged rats. Mol. Cell. Neurosci. 19:2002;32-42.
40. Pavelko K.D., Van Engelen B.G.M., Rodriguez M. Acceleration in the rate of CNS remyelination in lysolecithin-induced demyelination. J. Neurosci. 18:1998;2498-2505.
41. Prineas J.W., Connell F. Remyelination in multiple sclerosis. Ann. Neurol. 5:1979;22-31.
42. Prineas J.W., Barnard R.O., Revesz T., Kwon E.E., Sharer L., Cho E.-S. Multiple sclerosis: pathology of recurrent lesions. Brain. 116:1993;681-693.
43. Raine C.S., Wu E. Multiple sclerosis: remyelination in acute lesions. J. Neuropathol. Exp. Neurol. 52:1993;199-204.
44. Redwine J.M., Armstrong R.C. In vivo proliferation of oligodendrocyte progenitors expressing PDGF-alphaR during early remyelination. J. Neurobiol. 37:1998;413-428.
45. Reynolds R., Wilkin G.P. Cellular reaction to an acute demyelinating/remyelinating lesion of the rat brain stem: localisation of GD3 ganglioside immunoreactivity. J. Neurosci. Res. 36:1993;417-434.
46. Richardson W.D., Pringle N., Mosley M.J., Westermark B., Dubois-Dalcq M. A role for platelet-derived growth factor in normal gliogenesis in the central nervous system. Cell. 53:1988;309-319.
47. Scolding N.J., Rayner P.J., Sussman J., Shaw C., Compston D.A.S. A proliferative adult human oligodendrocyte progenitor. NeuroReport. 6:1995;441-445.
48. Shields S.A., Gilson J.M., Blakemore W.F., Franklin R.J.M. Remyelination occurs as extensively but more slowly in old rats compared to young rats following gliotoxin-induced CNS demyelination. Glia. 28:1999;77-83.
49. Sim F.J., Zhao C., Penderis J., Franklin R.J.M. The age-related decrease in CNS remyelination efficiency is attributable to an impairment of both oligodendrocyte progenitor recruitment and differentiation. J. Neurosci. 22:2002;2451-2459.
50. Stidworthy M.F., Genoud S., Suter U., Mantei N., Franklin R.J.M. Quantifying the early stages of remyelination following cuprizone-induced demyelination. Brain Pathol. 13:2003;329-339.
51. Sun T., Pringle N.P., Hardy A.P., Richardson W.D., Smith H.K. Pax6 influences the time and site of origin of glial precursors in the ventral neural tube. Mol. Cell. Neurosci. 12:1998;228-239.
52. Van Heyningen P., Calver A.R., Richardson W.D. Control of progenitor cell number by mitogen supply and demand. Curr. Biol. 11:2001;232-241.
53. Warrington A.E., Asakura K., Bieber A.J., Ciric B., Van K.V., Kaveri S.V., Kyle R.A., Pease L.R., Rodriguez M. Human monoclonal antibodies reactive to oligodendrocytes promote remyelination in a model of multiple sclerosis. Proc. Natl. Acad. Sci.U. S. A. 97:2000;6820-6825.
54. Watanabe M., Toyama Y., Nishiyama A. Differentiation of proliferated NG2-positive glial progenitor cells in a remyelinating lesion. J. Neurosci. Res. 69:2002;826-836.
55. Wolswijk G. Chronic stage multiple sclerosis lesions contain a relatively quiescent population of oligodendrocyte precursor cells. J. Neurosci. 18:1998;601-609.
56. perinatal progenitor cells. J. Cell Biol. 118:1992;889-900.
57. Woodruff R.H., Franklin R.J.M. Demyelination and remyelination of the caudal cerebellar peduncle of adult rats following stereotaxic injections of lysolecithin, ethidium bromide and complement/anti-galactocerebroside - A comparative study. Glia. 25:1999;216-228.
58. Yao D.-L., Liu X., Hudson L.D., Webster H.d. Insulin-like growth factor I treatment reduces demyelination and up-regulates gene expression of myelin-related proteins in experimental autoimmune encephalomyelitis. Proc. Natl. Acad. Sci. U. S. A. 92:1995;6190-6194.