Oligodendrocyte progenitor cell susceptibility to injury in multiple sclerosis

American Journal of Pathology

Volumn 183, Issue 2, 2013, Pages 516-525

  Cui, Qiao Ling ^a,b   Kuhlmann, Tanja ^c   Miron, Veronique E ^a   Leong, Soo Yuen ^a   Fang, Jun ^b   Gris, Pavel ^a   Kennedy, Timothy E ^a   Almazan, Guillermina ^b   Antel, Jack ^a  

^a MCGILL UNIVERSITY   (Canada)

^b MCGILL UNIVERSITY   (Canada)

^c UNIVERSITY HOSPITAL MÜNSTER   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

TUMOR NECROSIS FACTOR;

ANIMAL CELL; ARTICLE; CELL COUNT; CELL DEATH; CELL MIGRATION; CELL PROLIFERATION; COCULTURE; CONTROLLED STUDY; DISEASE PREDISPOSITION; EMBRYO; GENE EXPRESSION; HUMAN; HUMAN CELL; HUMAN TISSUE; IN VITRO STUDY; METABOLIC STRESS; MULTIPLE SCLEROSIS; NERVE CELL; NERVE FIBER; NONHUMAN; OLIGODENDROGLIA; PRIORITY JOURNAL; RAT; SPINAL GANGLION; STEM CELL; UPREGULATION; WHITE MATTER;

ADULT; ANIMALS; APOPTOSIS; APOPTOSIS REGULATORY PROTEINS; AXONS; BASIC HELIX-LOOP-HELIX TRANSCRIPTION FACTORS; CELLS, CULTURED; DISEASE SUSCEPTIBILITY; GANGLIA, SPINAL; HUMANS; MULTIPLE SCLEROSIS; MYELIN SHEATH; MYELIN-ASSOCIATED GLYCOPROTEIN; MYELIN-OLIGODENDROCYTE GLYCOPROTEIN; NERVE REGENERATION; NERVE TISSUE PROTEINS; OLIGODENDROGLIA; RATS; STEM CELLS;

EID: 84880610920     PISSN: 00029440     EISSN: 15252191     Source Type: Journal    
DOI: 10.1016/j.ajpath.2013.04.016     Document Type: Article

References (49)

1. R.B. Tripathi, L.E. Rivers, K.M. Young, F. Jamen, and W.D. Richardson NG2 glia generate new oligodendrocytes but few astrocytes in a murine experimental autoimmune encephalomyelitis model of demyelinating disease J Neurosci 30 2010 16383 16390
2. M. Zawadzka, L.E. Rivers, S.P. Fancy, C. Zhao, R. Tripathi, F. Jamen, K. Young, A. Goncharevich, H. Pohl, M. Rizzi, D.H. Rowitch, N. Kessaris, U. Suter, W.D. Richardson, and R.J. Franklin CNS-resident glial progenitor/stem cells produce Schwann cells as well as oligodendrocytes during repair of CNS demyelination Cell Stem Cell 6 2010 578 590
3. W.M. Carroll, A.R. Jennings, and L.J. Ironside Identification of the adult resting progenitor cell by autoradiographic tracking of oligodendrocyte precursors in experimental CNS demyelination Brain 121 Pt 2 1998 293 302
4. R.J. Franklin, and C. Ffrench-Constant Remyelination in the CNS: from biology to therapy Nat Rev Neurosci 9 2008 839 855
5. J.M. Gensert, and J.E. Goldman Endogenous progenitors remyelinate demyelinated axons in the adult CNS Neuron 19 1997 197 203
6. T. Kuhlmann, V. Miron, Q. Cui, C. Wegner, J. Antel, and W. Bruck Differentiation block of oligodendroglial progenitor cells as a cause for remyelination failure in chronic multiple sclerosis Brain 131 2008 1749 1758
7. J. Antel New directions in multiple sclerosis therapy: matching therapy with pathogenesis Can J Neurol Sci 37 Suppl 2 2010 S42 S48
8. M. Law, A.M. Saindane, Y. Ge, J.S. Babb, G. Johnson, L.J. Mannon, J. Herbert, and R.I. Grossman Microvascular abnormality in relapsing-remitting multiple sclerosis: perfusion MR imaging findings in normal-appearing white matter Radiology 231 2004 645 652
9. H. Lassmann Hypoxia-like tissue injury as a component of multiple sclerosis lesions J Neurol Sci 206 2003 187 191
10. M.T. Fischer, R. Sharma, J.L. Lim, L. Haider, J.M. Frischer, J. Drexhage, D. Mahad, M. Bradl, J. van Horssen, and H. Lassmann NADPH oxidase expression in active multiple sclerosis lesions in relation to oxidative tissue damage and mitochondrial injury Brain 135 2012 886 899
11. H. Lassmann, and J. van Horssen The molecular basis of neurodegeneration in multiple sclerosis FEBS Lett 585 2011 3715 3723
12. A.P. Henderson, M.H. Barnett, J.D. Parratt, and J.W. Prineas Multiple sclerosis: distribution of inflammatory cells in newly forming lesions Ann Neurol 66 2009 739 753
13. J.W. Prineas, E.E. Kwon, E.S. Cho, L.R. Sharer, M.H. Barnett, E.L. Oleszak, B. Hoffman, and B.P. Morgan Immunopathology of secondary-progressive multiple sclerosis Ann Neurol 50 2001 646 657
14. M. Rodriguez, B.W. Scheithauer, G. Forbes, and P.J. Kelly Oligodendrocyte injury is an early event in lesions of multiple sclerosis Mayo Clin Proc 68 1993 627 636
15. D. Mahad, I. Ziabreva, H. Lassmann, and D. Turnbull Mitochondrial defects in acute multiple sclerosis lesions Brain 131 Pt 7 2008 1722 1735
16. R. Dutta, J. McDonough, X. Yin, J. Peterson, A. Chang, T. Torres, T. Gudz, W.B. Macklin, D.A. Lewis, R.J. Fox, R. Rudick, K. Mirnics, and B.D. Trapp Mitochondrial dysfunction as a cause of axonal degeneration in multiple sclerosis patients Ann Neurol 59 2006 478 489
17. J.L. Zambonin, C. Zhao, N. Ohno, G.R. Campbell, S. Engeham, I. Ziabreva, N. Schwarz, S.E. Lee, J.M. Frischer, D.M. Turnbull, B.D. Trapp, H. Lassmann, R.J. Franklin, and D.J. Mahad Increased mitochondrial content in remyelinated axons: implications for multiple sclerosis Brain 134 2011 1901 1913
18. T. Andrews, P. Zhang, and N.R. Bhat TNFalpha potentiates IFNgamma-induced cell death in oligodendrocyte progenitors J Neurosci Res 54 1998 574 583
19. A. Khorchid, G. Fragoso, G. Shore, and G. Almazan Catecholamine-induced oligodendrocyte cell death in culture is developmentally regulated and involves free radical generation and differential activation of caspase-3 Glia 40 2002 283 299
20. H.N. Liu, B.I. Giasson, W.E. Mushynski, and G. Almazan AMPA receptor-mediated toxicity in oligodendrocyte progenitors involves free radical generation and activation of JNK, calpain and caspase 3 J Neurochem 82 2002 398 409
21. G. Fragoso, A.K. Martinez-Bermudez, H.N. Liu, A. Khorchid, S. Chemtob, W.E. Mushynski, and G. Almazan Developmental differences in HO-induced oligodendrocyte cell death: role of glutathione, mitogen-activated protein kinases and caspase 3 J Neurochem 90 2004 392 404
22. I. Ziabreva, G. Campbell, J. Rist, J. Zambonin, J. Rorbach, M.M. Wydro, H. Lassmann, R.J. Franklin, and D. Mahad Injury and differentiation following inhibition of mitochondrial respiratory chain complex IV in rat oligodendrocytes Glia 58 2010 1827 1837
23. W. Bruck, P. Porada, S. Poser, P. Rieckmann, F. Hanefeld, H.A. Kretzschmar, and H. Lassmann Monocyte/macrophage differentiation in early multiple sclerosis lesions Ann Neurol 38 1995 788 796
24. C. Lucchinetti, W. Bruck, J. Parisi, B. Scheithauer, M. Rodriguez, and H. Lassmann Heterogeneity of multiple sclerosis lesions: implications for the pathogenesis of demyelination Ann Neurol 47 2000 707 717
25. B. Ranscht, P.A. Clapshaw, J. Price, M. Noble, and W. Seifert Development of oligodendrocytes and Schwann cells studied with a monoclonal antibody against galactocerebroside Proc Natl Acad Sci U S A 79 1982 2709 2713
26. F. Ruffini, N. Arbour, M. Blain, A. Olivier, and J.P. Antel Distinctive properties of human adult brain-derived myelin progenitor cells Am J Pathol 165 2004 2167 2175
27. G.S. Eisenbarth, F.S. Walsh, and M. Nirenberg Monoclonal antibody to a plasma membrane antigen of neurons Proc Natl Acad Sci U S A 76 1979 4913 4917
28. I. Sommer, and M. Schachner Monoclonal antibodies (O1 to O4) to oligodendrocyte cell surfaces: an immunocytological study in the central nervous system Dev Biol 83 1981 311 327
29. F.J. Sim, J.K. Lang, B. Waldau, N.S. Roy, T.E. Schwartz, W.H. Pilcher, K.J. Chandross, S. Natesan, J.E. Merrill, and S.A. Goldman Complementary patterns of gene expression by human oligodendrocyte progenitors and their environment predict determinants of progenitor maintenance and differentiation Ann Neurol 59 2006 763 779
30. G. Fragoso, J.D. Haines, J. Roberston, L. Pedraza, W.E. Mushynski, and G. Almazan p38 mitogen-activated protein kinase is required for central nervous system myelination Glia 55 2007 1531 1541
31. S.C. Zhang, B. Ge, and I.D. Duncan Adult brain retains the potential to generate oligodendroglial progenitors with extensive myelination capacity Proc Natl Acad Sci U S A 96 1999 4089 4094
32. A. Williams, G. Piaton, M.S. Aigrot, A. Belhadi, M. Theaudin, F. Petermann, J.L. Thomas, B. Zalc, and C. Lubetzki Semaphorin 3A and 3F: key players in myelin repair in multiple sclerosis? Brain 130 2007 2554 2565
33. M.S. Windrem, M.C. Nunes, W.K. Rashbaum, T.H. Schwartz, R.A. Goodman, G. McKhann 2nd, N.S. Roy, and S.A. Goldman Fetal and adult human oligodendrocyte progenitor cell isolates myelinate the congenitally dysmyelinated brain Nat Med 10 2004 93 97
34. M.S. Windrem, S.J. Schanz, M. Guo, G.F. Tian, V. Washco, N. Stanwood, M. Rasband, N.S. Roy, M. Nedergaard, L.A. Havton, S. Wang, and S.A. Goldman Neonatal chimerization with human glial progenitor cells can both remyelinate and rescue the otherwise lethally hypomyelinated shiverer mouse Cell Stem Cell 2 2008 553 565
35. W. Bruck, M. Schmied, G. Suchanek, Y. Bruck, H. Breitschopf, S. Poser, S. Piddlesden, and H. Lassmann Oligodendrocytes in the early course of multiple sclerosis Ann Neurol 35 1994 65 73
36. M.P. Targett, J. Sussman, N. Scolding, M.T. O'Leary, D.A. Compston, and W.F. Blakemore Failure to achieve remyelination of demyelinated rat axons following transplantation of glial cells obtained from the adult human brain Neuropathol Appl Neurobiol 22 1996 199 206
37. H.S. Keirstead, and W.F. Blakemore Identification of post-mitotic oligodendrocytes incapable of remyelination within the demyelinated adult spinal cord J Neuropathol Exp Neurol 56 1997 1191 1201
38. W.F. Blakemore, and K.A. Irvine Endogenous or exogenous oligodendrocytes for remyelination J Neurol Sci 265 2008 43 46
39. Q.L. Cui, G. Fragoso, V.E. Miron, P.J. Darlington, W.E. Mushynski, J. Antel, and G. Almazan Response of human oligodendrocyte progenitors to growth factors and axon signals J Neuropathol Exp Neurol 69 2010 930 944
40. D. Dewar, S.M. Underhill, and M.P. Goldberg Oligodendrocytes and ischemic brain injury J Cereb Blood Flow Metab 23 2003 263 274
41. B. Gerstner, C. Buhrer, C. Rheinlander, O. Polley, A. Schuller, M. Berns, M. Obladen, and U. Felderhoff-Mueser Maturation-dependent oligodendrocyte apoptosis caused by hyperoxia J Neurosci Res 84 2006 306 315
42. B. Gerstner, T.M. DeSilva, K. Genz, A. Armstrong, F. Brehmer, R.L. Neve, U. Felderhoff-Mueser, J.J. Volpe, and P.A. Rosenberg Hyperoxia causes maturation-dependent cell death in the developing white matter J Neurosci 28 2008 1236 1245
43. H. Le-Niculescu, E. Bonfoco, Y. Kasuya, F.X. Claret, D.R. Green, and M. Karin Withdrawal of survival factors results in activation of the JNK pathway in neuronal cells leading to Fas ligand induction and cell death Mol Cell Biol 19 1999 751 763
44. R. Caricchio, L. D'Adamio, and P.L. Cohen Fas, ceramide and serum withdrawal induce apoptosis via a common pathway in a type II Jurkat cell line Cell Death Differ 9 2002 574 580
45. L.Y. Yu, M. Saarma, and U. Arumae Death receptors and caspases but not mitochondria are activated in the GDNF- or BDNF-deprived dopaminergic neurons J Neurosci 28 2008 7467 7475
46. F.M. Hofman, D.R. Hinton, K. Johnson, and J.E. Merrill Tumor necrosis factor identified in multiple sclerosis brain J Exp Med 170 1989 607 612
47. P. Dowling, G. Shang, S. Raval, J. Menonna, S. Cook, and W. Husar Involvement of the CD95 (APO-1/Fas) receptor/ligand system in multiple sclerosis brain J Exp Med 184 1996 1513 1518
48. K. Wosik, J. Antel, T. Kuhlmann, W. Bruck, B. Massie, and J. Nalbantoglu Oligodendrocyte injury in multiple sclerosis: a role for p53 J Neurochem 85 2003 635 644
49. S.K. Ludwin Chronic demyelination inhibits remyelination in the central nervous system. An analysis of contributing factors Lab Invest 43 1980 382 387