Macrophage-depletion induced impairment of experimental CNS remyelination is associated with a reduced oligodendrocyte progenitor cell response and altered growth factor expression

Neurobiology of Disease

Volumn 18, Issue 1, 2005, Pages 166-175

  Kotter, Mark R ^a   Zhao, Chao ^a   Van Rooijen, Nico ^b   Franklin, Robin J M ^a  

^a UNIVERSITY OF CAMBRIDGE   (United Kingdom)

^b VU UNIVERSITY MEDICAL CENTER   (Netherlands)

Author keywords

Demyelination; Growth factors; Inflammation; Macrophages; Oligodendrocyte progenitor cells; Phagocytosis; Regeneration; Remyelination

Indexed keywords

CLODRONIC ACID; FIBROBLAST GROWTH FACTOR 2; GROWTH FACTOR; LIPOSOME; LYSOPHOSPHATIDYLCHOLINE; MESSENGER RNA; MYELIN; MYELIN BASIC PROTEIN; PLATELET DERIVED GROWTH FACTOR A; PLATELET DERIVED GROWTH FACTOR ALPHA RECEPTOR; PLATELET DERIVED GROWTH FACTOR RECEPTOR; SCAVENGER RECEPTOR; SCAVENGER RECEPTOR B; SOMATOMEDIN C; TOXIN; TRANSFORMING GROWTH FACTOR BETA1; UNCLASSIFIED DRUG;

ANIMAL CELL; ANIMAL MODEL; ARTICLE; CENTRAL NERVOUS SYSTEM; CENTRAL NERVOUS SYSTEM DISEASE; CONTROLLED STUDY; DEMYELINATION; FEMALE; IN SITU HYBRIDIZATION; MACROPHAGE; MONOCYTE; NONHUMAN; NUCLEOTIDE SEQUENCE; OLIGODENDROGLIA; PHAGOCYTOSIS; PRIORITY JOURNAL; PROTEIN EXPRESSION; RAT; REMYELINIZATION; STEM CELL; WHITE MATTER;

ANIMALS; CENTRAL NERVOUS SYSTEM; DEMYELINATING DISEASES; DISEASE MODELS, ANIMAL; DOWN-REGULATION; FEMALE; GROWTH SUBSTANCES; MACROPHAGES; MYELIN BASIC PROTEINS; MYELIN SHEATH; NERVE REGENERATION; OLIGODENDROGLIA; PHAGOCYTOSIS; RATS; RATS, SPRAGUE-DAWLEY; RECEPTOR, PLATELET-DERIVED GROWTH FACTOR ALPHA; RECEPTORS, IMMUNOLOGIC; RECEPTORS, SCAVENGER; RNA; STEM CELLS;

EID: 11844253894     PISSN: 09699961     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.nbd.2004.09.019     Document Type: Article

References (85)

1. P.J. Albrecht, J.C. Murtie, J.K. Ness, J.M. Redwine, J.R. Enterline, R.C. Armstrong, and S.W. Levison Astrocytes produce CNTF during the remyelination phase of viral-induced spinal cord demyelination to stimulate FGF-2 production Neurobiol. Dis. 13 2003 89 101
2. H.A. Arnett, J. Mason, M. Marino, K. Suzuki, G.K. Matsushima, and J.P. Ting TNF alpha promotes proliferation of oligodendrocyte progenitors and remyelination Nat. Neurosci. 4 2001 1116 1122
3. H.A. Arnett, Y. Wang, G.K. Matsushima, K. Suzuki, and J.P. Ting Functional genomic analysis of remyelination reveals importance of inflammation in oligodendrocyte regeneration J. Neurosci. 23 2003 9824 9832
4. B.A. Barres, I.K. Hart, H.S. Coles, J.F. Burne, J.T. Voyvodic, W.D. Richardson, and M.C. Raff Cell death in the oligodendrocyte lineage J. Neurobiol. 23 1992 1221 1230
5. R. Barraclough, D.G. Fernig, P.S. Rudland, and J.A. Smith Synthesis of basic fibroblast growth factor upon differentiation of rat mammary epithelial to myoepithelial-like cells in culture J. Cell Physiol. 144 1990 333 344
6. A.J. Bieber, S. Kerr, and M. Rodriguez Efficient central nervous system remyelination requires T cells Ann. Neurol. 53 2003 680 684
7. A. Bitsch, T. Kuhlmann, C. Da Costa, S. Bunkowski, T. Polak, and W. Bruck Tumour necrosis factor alpha mRNA expression in early multiple sclerosis lesions: correlation with demyelinating activity and oligodendrocyte pathology Glia 29 2000 366 375
8. K.L. Blaschuk, E.E. Frost, and C. Ffrench-Constant The regulation of proliferation and differentiation in oligodendrocyte progenitor cells by alphaV integrins Development 127 2000 1961 1969
9. C.A. Copelman, L.T. Diemel, D. Gveric, N.A. Gregson, and M.L. Cuzner Myelin phagocytosis and remyelination of macrophage-enriched central nervous system aggregate cultures J. Neurosci. Res. 66 2001 1173 1178
10. L.T. Diemel, G. Wolswijk, S.J. Jackson, and M.L. Cuzner Remyelination of cytokine- or antibody-demyelinated CNS aggregate cultures is inhibited by macrophage supplementation Glia 45 2004 278 286
11. M. Eto, H. Yoshikawa, H. Fujimura, I. Naba, H. Sumi-Akamaru, S. Takayasu, H. Itabe, and S. Sakoda The role of CD36 in peripheral nerve remyelination after crush injury Eur. J. Neurosci. 17 2003 2659 2666
12. R.J.M. Franklin Why does remyelination fail in multiple sclerosis? Nat. Rev., Neurosci. 3 2002 705 714
13. R.J.M. Franklin, and G.L. Hinks Understanding CNS remyelination: clues from developmental and regeneration biology J. Neurosci. Res. 58 1999 207 213
14. R.J.M. Franklin, and J.E. Goldman R.A. Lazzarini Remyelination by Endogenous Glia 2004 Elsevier San Diego 173 196
15. E.E. Frost, J.A. Nielsen, T.Q. Le, and R.C. Armstrong PDGF and FGF-2 regulate oligodendrocyte progenitor responses to demyelination J. Neurobiol. 54 2003 457 472
16. M. Fruttiger, L. Karlsson, A.C. Hall, A. Abramsson, A.R. Calver, H. Bostrom, K. Willetts, C.H. Bertold, J.K. Heath, C. Betsholtz, and W.D. Richardson Defective oligodendrocyte development and severe hypomyelination in PDGF-A knockout mice Development 126 1999 457 467
17. J.M. Gensert, and J.E. Goldman Endogenous progenitors remyelinate demyelinated axons in the adult CNS Neuron 19 1997 197 203
18. D.L. Graça, and W.F. Blakemore Delayed remyelination in rat spinal cord following ethidium bromide injection Neuropathol. Appl. Neurobiol. 12 1986 593 605
19. J. Han, D.P. Hajjar, M. Febbraio, and A.C. Nicholson Native and modified low density lipoproteins increase the functional expression of the macrophage class B scavenger receptor, CD36 J. Biol. Chem. 272 1997 21654 21659
20. K.E. Hill, L.V. Zollinger, H.E. Watt, N.G. Carlson, and J.W. Rose Inducible nitric oxide synthase in chronic active multiple sclerosis plaques: distribution, cellular expression and association with myelin damage J. Neuroimmunol. 151 2004 171 179
21. G.L. Hinks, and R.J.M. Franklin 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
22. G.L. Hinks, and R.J.M. Franklin Delayed changes in growth factor gene expression during slow remyelination in the CNS of aged rats Mol. Cell. Neurosci. 16 2000 542 556
23. S. Hu, W.S. Sheng, P.K. Peterson, and C.C. Chao Cytokine modulation of murine microglial cell superoxide production Glia 13 1995 45 50
24. I. Huitinga, N. van Rooijen, C.J. de Groot, B.M. Uitdehaag, and C.D. Dijkstra Suppression of experimental allergic encephalomyelitis in Lewis rats after elimination of macrophages J. Exp. Med. 172 1990 1025 1033
25. J. Husemann, and S.C. Silverstein Expression of scavenger receptor class B, type 1, by astrocytes and vascular smooth muscle cells in normal adult mouse and human brain and in Alzheimer's disease brain Am. J. Pathol. 158 2001 825 832
26. J. Husemann, J.D. Loike, R. Anankov, M. Febbraio, and S.C. Silverstein Scavenger receptors in neurobiology and neuropathology: their role on microglia and other cells of the nervous system Glia 40 2002 195 205
27. J. Hsieh, J.B. Aimone, B.K. Kaspar, T. Kuwabara, K. Nakashima, and F.H. Gage IGF-I instructs multipotent adult neural progenitor cells to become oligodendrocytes J. Cell. Biol. 164 2004 111 122
28. R.R. Ji, Q. Zhang, X. Zhang, F. Piehl, T. Reilly, R.F. Pettersson, and T. Hokfelt Prominent expression of bFGF in dorsal root ganglia after axotomy Eur. J. Neurosci. 7 1995 2458 2468
29. C.A. Jordan, V.L. Friedrich Jr., F. de Ferra, D.G. Weismiller, K.V. Holmes, and M. Dubois-Dalcq Differential exon expression in myelin basic protein transcripts during central nervous system (CNS) remyelination Cell. Mol. Neurobiol. 10 1990 3 18
30. M.R. Kotter, A. Setzu, F.J. Sim, N. van Rooijen, and R.J.M. Franklin Macrophage depletion impairs oligodendrocyte remyelination following lysolecithin-induced demyelination Glia 35 2001 204 212
31. H. Lassmann, M. Schmied, K. Vass, and W.F. Hickey Bone marrow derived elements and resident microglia in brain inflammation Glia 7 1993 19 24
32. H. Lassmann, W. Bruck, C. Lucchinetti, and M. Rodriguez Remyelination in multiple sclerosis Mult. Scler. 3 1997 133 136
33. H. Lassmann, W. Bruck, and C. Lucchinetti Heterogeneity of multiple sclerosis pathogenesis: implications for diagnosis and therapy Trends Mol. Med. 7 2001 115 121
34. J.M. Levine, and R. Reynolds Activation and proliferation of endogenous oligodendrocyte precursor cells during ethidium bromide-induced demyelination Exp. Neurol. 160 1999 333 347
35. Y.M. Li, S. Arkins, R.H. McCusker Jr., S.M. Donovan, Q. Liu, S. Jayaraman, R. Dantzer, and K.W. Kelley Macrophages synthesize and secrete a 25-kilodalton protein that binds insulin-like growth factor-I J. Immunol. 156 1996 64 72
36. A.J. Loughlin, C.A. Copelman, A. Hall, T. Armer, B.C. Young, D.N. Landon, and M.L. Cuzner Myelination and remyelination of aggregate rat brain cell cultures enriched with macrophages J. Neurosci. Res. 47 1997 384 392
37. S.K. Ludwin Chronic demyelination inhibits remyelination in the central nervous system. An analysis of contributing factors Lab. Invest. 43 1980 382 387
38. S.K. Ludwin, and N.H. Sternberger An immunohistochemical study of myelin proteins during remyelination in the central nervous system Acta Neuropathol. (Berl) 63 1984 240 248
39. J.L. Marin-Teva, I. Dusart, C. Colin, A. Gervais, N. van Rooijen, and M. Mallat Microglia promote the death of developing Purkinje cells Neuron 41 2004 535 547
40. J.L. Mason, P. Ye, K. Suzuki, A.J. D'Ercole, and G.K. Matsushima Insulin-like growth factor-1 inhibits mature oligodendrocyte apoptosis during primary demyelination J. Neurosci. 20 2000 5703 5708
41. J.L. Mason, K. Suzuki, D.D. Chaplin, and G.K. Matsushima Interleukin-1beta promotes repair of the CNS J. Neurosci. 21 2001 7046 7052
42. J.L. Mason, S. Xuan, I. Dragatsis, A. Efstratiadis, and J.E. Goldman Insulin-like growth factor (IGF) signaling through type 1 IGF receptor plays an important role in remyelination J. Neurosci. 23 2003 7710 7718
43. B.A. Masters, H. Werner, C.T. Roberts Jr., D. LeRoith, and M.K. Raizada Insulin-like growth factor I (IGF-I) receptors and IGF-I action in oligodendrocytes from rat brains Regul. Pept. 33 1991 117 131
44. R.D. McKinnon, C. Smith, T. Behar, T. Smith, and M. Dubois-Dalcq Distinct effects of bFGF and PDGF on oligodendrocyte progenitor cells Glia 7 1993 245 254
45. J.E. Merrill, and R.P. Zimmerman Natural and induced cytotoxicity of oligodendrocytes by microglia is inhibitable by TGF beta Glia 4 1991 327 331
46. R. Milner, G. Edwards, C. Streuli, and C. Ffrench-Constant A role in migration for the alpha V beta 1 integrin expressed on oligodendrocyte precursors J. Neurosci. 16 1996 7240 7252
47. P. Morell, C.V. Barrett, J.L. Mason, A.D. Toews, J.D. Hostettler, G.W. Knapp, and G.K. Matsushima Gene expression in brain during cuprizone-induced demyelination and remyelination Mol. Cell. Neurosci. 12 1998 220 227
48. R.V. Mueller, T.K. Hunt, A. Tokunaga, and E.M. Spencer The effect of insulinlike growth factor I on wound healing variables and macrophages in rats Arch. Surg. 129 1994 262 265
49. C.F. Nathan Secretory products of macrophages J. Clin. Invest. 79 1987 319 326
50. S.L. O'Donnell, T.J. Frederick, J.K. Krady, S.J. Vannucci, and T.L. Wood IGF-I and microglia/macrophage proliferation in the ischemic mouse brain Glia 39 2002 85 97
51. S.S. Ousman, and S. David Lysophosphatidylcholine induces rapid recruitment and activation of macrophages in the adult mouse spinal cord Glia 30 2000 92 104
52. R.B. Panek, and E.N. Benveniste Class II MHC gene expression in microglia. Regulation by the cytokines IFN-gamma, TNF-alpha, and TGF-beta J. Immunol. 154 1995 2846 2854
53. R.A. Pollock, and W.D. Richardson The alternative-splice isoforms of the PDGF A-chain differ in their ability to associate with the extracellular matrix and to bind heparin in vitro Growth Factors 7 1992 267 277
54. J.W. Prineas, and F. Connell Remyelination in multiple sclerosis Ann. Neurol. 5 1979 22 31
55. J.W. Prineas, R.O. Barnard, T. Revesz, E.E. Kwon, L. Sharer, and E.S. Cho Multiple sclerosis: pathology of recurrent lesions Brain 116 1993 681 693
56. J. Prineas, W. McDonald, and R.J.M. Franklin Demyelinating diseases D.I. Graham P.L. Lantos Greenfield's Neuropathology 2002 Arnold London 471 550
57. C.S. Raine The Norton Lecture: a review of the oligodendrocyte in the multiple sclerosis lesion J. Neuroimmunol. 77 1997 135 152
58. C.S. Raine, and E. Wu Multiple sclerosis: remyelination in acute lesions J. Neuropathol. Exp. Neurol. 52 1993 199 204
59. J.M. Redwine, and R.C. Armstrong In vivo proliferation of oligodendrocyte progenitors expressing PDGFalphaR during early remyelination J. Neurobiol. 37 1998 413 428
60. S. Robinson, and R.H. Miller Contact with central nervous system myelin inhibits oligodendrocyte progenitor maturation Dev. Biol. 216 1999 359 368
61. S. Robinson, M. Tani, R.M. Strieter, R.M. Ransohoff, and R.H. Miller The chemokine growth-regulated oncogene-alpha promotes spinal cord oligodendrocyte precursor proliferation J. Neurosci. 18 1998 10457 10463
62. J.W. Rose, K.E. Hill, H.E. Watt, and N.G. Carlson Inflammatory cell expression of cyclooxygenase-2 in the multiple sclerosis lesion J. Neuroimmunol. 149 2004 40 49
63. B.A. Scheven, and N.J. Hamilton Stimulation of macrophage growth and multinucleated cell formation in rat bone marrow cultures by insulin-like growth factor I Biochem. Biophys. Res. Commun. 174 1991 647 653
64. N. Schuster, H. Bender, A. Philippi, S. Subramaniam, J. Strelau, Z. Wang, and K. Krieglstein TGF-beta induces cell death in the oligodendroglial cell line OLI-neu Glia 40 2002 95 108
65. Y. Shinar, and F.A. McMorris Developing oligodendroglia express mRNA for insulin-like growth factor-I, a regulator of oligodendrocyte development J. Neurosci. Res. 42 1995 516 527
66. F.C. Silberstein, R. De Simone, G. Levi, and F. Aloisi Cytokine-regulated expression of platelet-derived growth factor gene and protein in cultured human astrocytes J. Neurochem. 66 1996 1409 1417
67. F.J. Sim, G.L. Hinks, and R.J.M. Franklin The re-expression of the homeodomain transcription factor Gtx during remyelination of experimentally induced demyelinating lesions in young and old rat brain Neuroscience 100 2000 131 139
68. F.J. Sim, C. Zhao, W.W. Li, A. Lakatos, and R.J.M. Franklin Expression of the POU-domain transcription factors SCIP/Oct-6 and Brn-2 is associated with Schwann cell but not oligodendrocyte remyelination of the CNS Mol. Cell. Neurosci. 20 2002 669 682
69. F.J. Sim, C. Zhao, J. Penderis, and R.J.M. Franklin 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
70. C. Sunderkotter, T. Nikolic, M.J. Dillon, N. van Rooijen, M. Stehling, D.A. Drevets, and P.J. Leenen Subpopulations of mouse blood monocytes differ in maturation stage and inflammatory response J. Immunol. 172 2004 4410 4417
71. A. Suzumura, M. Sawada, H. Yamamoto, and T. Marunouchi Transforming growth factor-beta suppresses activation and proliferation of microglia in vitro J. Immunol. 151 1993 2150 2158
72. M. Ueda, A.E. Becker, N. Kasayuki, A. Kojima, Y. Morita, and S. Tanaka In situ detection of platelet-derived growth factor-A and -B chain mRNA in human coronary arteries after percutaneous transluminal coronary angioplasty Am. J. Pathol. 149 1996 831 843
73. N. van Rooijen The liposome-mediated macrophage 'suicide' technique J. Immunol. Methods 124 1989 1 6
74. N. van Rooijen, and A. Sanders Liposome mediated depletion of macrophages: mechanism of action, preparation of liposomes and applications J. Immunol. Methods 174 1994 83 93
75. N. van Rooijen, N. Kors, E.M. vd, and C.D. Dijkstra Depletion and repopulation of macrophages in spleen and liver of rat after intravenous treatment with liposome-encapsulated dichloromethylene diphosphonate Cell. Tissue Res. 260 1990 215 222
76. N. van Rooijen, J. Bakker, and A. Sanders Transient suppression of macrophage functions by liposome-encapsulated drugs Trends. Biotechnol. 15 1997 178 185
77. J.M. Vela, E. Molina-Holgado, A. Arevalo-Martin, G. Almazan, and C. Guaza Interleukin-1 regulates proliferation and differentiation of oligodendrocyte progenitor cells Mol. Cell. Neurosci. 20 2002 489 502
78. M. Watanabe, Y. Toyama, and A. Nishiyama Differentiation of proliferated NG2-positive glial progenitor cells in a remyelinating lesion J. Neurosci. Res. 69 2002 826 836
79. G. Wolswijk Oligodendrocyte precursor cells in the demyelinated multiple sclerosis spinal cord Brain 125 2002 338 349
80. R.H. Woodruff, and R.J.M. Franklin 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
81. R.H. Woodruff, and R.J.M. Franklin The expression of myelin protein mRNAs during remyelination of lysolecithin-induced demyelination Neuropathol. Appl. Neurobiol. 25 1999 226 235
82. R.H. Woodruff, M. Fruttiger, W.D. Richardson, and R.J.M. Franklin Platelet-derived growth factor regulates oligodendrocyte progenitor numbers in adult CNS and their response following CNS demyelination Mol. Cell. Neurosci. 25 2004 252 262
83. B.G. Xiao, X.F. Bai, G.X. Zhang, and H. Link Transforming growth factor-beta1 induces apoptosis of rat microglia without relation to bcl-2 oncoprotein expression Neurosci. Lett. 226 1997 71 74
84. P. Ye, and A.J. D'Ercole Insulin-like growth factor I protects oligodendrocytes from tumor necrosis factor-alpha-induced injury Endocrinology 140 1999 3063 3072
85. C. Yu, M. Takeda, and B. Soliven Regulation of cell cycle proteins by TNF-alpha and TGF-beta in cells of oligodendroglial lineage J. Neuroimmunol. 108 2000 2 10