Limited remyelination in Theiler's murine encephalomyelitis due to insufficient oligodendroglial differentiation of nerve/glial antigen 2 (NG2)-positive putative oligodendroglial progenitor cells

Neuropathology and Applied Neurobiology

Volumn 34, Issue 6, 2008, Pages 603-620

  Ulrich, R ^a   Seeliger, F ^b   Kreutzer, M ^a   Germann, P G ^b   Baumgartner W ^a  

^a UNIVERSITY OF VETERINARY MEDICINE HANNOVER   (Germany)

^b Nycomed   (Germany)

Author keywords

Astrogliosis; Demyelination; Nerve glial antigen 2; Oligodendroglial progenitor cells; Remyelination; Theiler's murine encephalomyelitis

Indexed keywords

2',3' CYCLIC NUCLEOTIDE 3' PHOSPHODIESTERASE; ANTIGEN; GLIAL FIBRILLARY ACIDIC PROTEIN; MESSENGER RNA; MYELIN BASIC PROTEIN; NERVE GLIAL ANTIGEN 2; PLATELET DERIVED GROWTH FACTOR ALPHA RECEPTOR; UNCLASSIFIED DRUG; VIRUS RNA;

ANIMAL CELL; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; ASTROCYTE; AXONAL INJURY; CELL DIFFERENTIATION; CONFOCAL LASER MICROSCOPY; CONTROLLED STUDY; DNA FOOTPRINTING; ELECTRON MICROSCOPY; ENCEPHALOMYELITIS; EXON; FEMALE; IMMUNOFLUORESCENCE; IMMUNOHISTOCHEMISTRY; IMMUNOHISTOLOGY; MOUSE; MULTIPLE SCLEROSIS; MURINE ENCEPHALOMYELITIS VIRUS; NERVE REGENERATION; NONHUMAN; OLIGODENDROGLIA; PRIORITY JOURNAL; PROTEIN LOCALIZATION; REMYELINIZATION; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; STEM CELL;

2',3'-CYCLIC-NUCLEOTIDE PHOSPHODIESTERASES; ANIMALS; ANTIGENS; CARDIOVIRUS INFECTIONS; CELL DIFFERENTIATION; ENCEPHALOMYELITIS; FEMALE; GENE EXPRESSION; IMMUNOHISTOCHEMISTRY; MICE; MICROSCOPY, CONFOCAL; MICROSCOPY, ELECTRON; MICROSCOPY, FLUORESCENCE; MULTIPLE SCLEROSIS; MYELIN BASIC PROTEINS; MYELIN SHEATH; NERVE TISSUE PROTEINS; OLIGODENDROGLIA; PROTEOGLYCANS; RECEPTOR, PLATELET-DERIVED GROWTH FACTOR ALPHA; RNA, MESSENGER; SPINAL CORD; STEM CELLS; THEILOVIRUS;

EID: 56549124821     PISSN: 03051846     EISSN: 13652990     Source Type: Journal    
DOI: 10.1111/j.1365-2990.2008.00956.x     Document Type: Article

References (70)

1. Ulrich R, Baumgärtner W, Gerhauser I, Seeliger F, Haist V, Deschl U, Alldinger S. MMP-12, MMP-3, and TIMP-1 are markedly upregulated in chronic demyelinating theiler murine encephalomyelitis. J Neuropathol Exp Neurol 2006 65 : 783 93
2. Gerhauser I, Alldinger S, Baumgärtner W. Ets-1 represents a pivotal transcription factor for viral clearance, inflammation, and demyelination in a mouse model of multiple sclerosis. J Neuroimmunol 2007 188 : 86 94
3. Welsh CJR, Tonks P, Borrow P, Nash AA. Theiler's virus- an experimental-model of virus-induced demyelination. Autoimmunity 1990 6 : 105 12
4. Rodriguez M. Effectors of demyelination and remyelination in the CNS: implications for multiple sclerosis. Brain Pathol 2007 17 : 219 29
5. Gerhauser I, Ulrich R, Alldinger S, Baumgärtner W. Induction of activator protein-1 and nuclear factor-kappaB as a prerequisite for disease development in susceptible SJL/J mice after theiler murine encephalomyelitis. J Neuropathol Exp Neurol 2007 66 : 809 18
6. McGavern DB, Murray PD, Rodriguez M. Quantitation of spinal cord demyelination, remyelination, atrophy, and axonal loss in a model of progressive neurologic injury. J Neurosci Res 1999 58 : 492 504
7. Njenga MK, Coenen MJ, DeCuir N, Yeh HY, Rodriguez M. Short-term treatment with interferon-alpha/beta promotes remyelination, whereas long-term treatment aggravates demyelination in a murine model of multiple sclerosis. J Neurosci Res 2000 59 : 661 70
8. Zoecklein LJ, Pavelko KD, Gamez J, Papke L, McGavern DB, Ure DR, Njenga MK, Johnson AJ, Nakane S, Rodriguez M. Direct comparison of demyelinating disease induced by the Daniel's strain and BeAn strain of Theiler's murine encephalomyelitis virus. Brain Pathol 2003 13 : 291 308
9. Dalcanto MC, Lipton HL. Primary demyelination in Theiler's virus-infection - ultrastructural study. Lab Invest 1975 33 : 626 37
10. Dalcanto MC, Barbano RL. Remyelination during remission in Theiler's virus-infection. Am J Pathol 1984 116 : 30 45
11. Dalcanto MC, Lipton HL. Schwann-cell remyelination and recurrent demyelination in the central nervous-system of mice infected with attenuated Theiler's virus. Am J Pathol 1980 98 : 101 22
12. Miller DJ, RiveraQuinones C, Njenga MK, Leibowitz J, Rodriguez M. Spontaneous CNS remyelination in beta(2) microglobulin-deficient mice following virus-induced demyelination. J Neurosci 1995 15 : 8345 52
13. Murray PD, McGavern DB, Sathornsumetee S, Rodriguez M. Spontaneous remyelination following extensive demyelination is associated with improved neurological function in a viral model of multiple sclerosis. Brain 2001 124 : 1403 16
14. Rodriguez M, Lennon VA, Benveniste EN, Merrill JE. Remyelination by oligodendrocytes stimulated by antiserum to spinal-cord. J Neuropathol Exp Neurol 1987 46 : 84 95
15. Rodriguez M, Lennon VA, Miller DJ. Immunoglobulins reactive with myelin basic-protein promote remyelination in the central-nervous-system. Ann Neurol 1995 38 : 340 1
16. Njenga MK, Murray PD, McGavern D, Lin XQ, Drescher KM, Rodriguez M. Absence of spontaneous central nervous system remyelination in class II-deficient mice infected with Theiler's virus. J Neuropathol Exp Neurol 1999 58 : 78 91
17. Reynolds R, Dawson M, Papadopoulos D, Polito A, Di Bello IC, Pham-Dinh D, Levine J. The response of NG2-expressing oligodendrocyte progenitors to demyelination in MOG-EAE and MS. J Neurocytol 2002 31 : 523 36
18. Lucchinetti C, Bruck W, Parisi J, Scheithauer B, Rodriguez M, Lassmann H. A quantitative analysis of oligodendrocytes in multiple sclerosis lesions - a study of 113 cases. Brain 1999 122 : 2279 95
19. Patrikios P, Stadelmann C, Kutzelnigg A, Rauschka H, Schmidbauer M, Laursen H, Sorensen PS, Bruck W, Lucchinetti C, Lassmann H. Remyelination is extensive in a subset of multiple sclerosis patients. Brain 2006 129 : 3165 72
20. Ludwin SK. Central-nervous-system remyelination - studies in chronically damaged tissue. Ann Neurol 1994 36 : S143 S5
21. Chang A, Nishiyama A, Peterson J, Prineas J, Trapp BD. NG2-positive oligodendrocyte progenitor cells in adult human brain and multiple sclerosis lesions. J Neurosci 2000 20 : 6404 12
22. Raine CS, Cross AH. Axonal dystrophy as a consequence of long-term demyelination. Lab Invest 1989 60 : 714 25
23. Di Bello IC, Dawson MRL, Levine JM, Reynolds R. Generation of oligodendroglial progenitors in acute inflammatory demyelinating lesions of the rat brain stem is associated with demyelination rather than inflammation. J Neurocytol 1999 28 : 365 81
24. Godfraind C, Friedrich VL, Holmes KV, Duboisdalcq M. Invivo analysis of glial-cell phenotypes during a viral demyelinating disease in mice. J Cell Biol 1989 109 : 2405 16
25. Jordan C, Friedrich V, Duboisdalcq M. Insitu hybridization analysis of myelin gene transcripts in developing mouse spinal-cord. J Neurosci 1989 9 : 248 57
26. Mason JL, Jones JJ, Taniike M, Morell P, Suzuki K, Matsushima GK. Mature oligodendrocyte apoptosis precedes IGF-1 production and oligodendrocyte progenitor accumulation and differentiation during demyelination/remyelination. J Neurosci Res 2000 61 : 251 62
27. Matsushima GK, Morell P. The neurotoxicant, cuprizone, as a model to study demyelination and remyelination in the central nervous system. Brain Pathol 2001 11 : 107 16
28. Morell P, Barrett CV, Mason JL, Toews AD, Hostettler JD, Knapp GW, Matsushima GK. Gene expression in brain during Cuprizone-induced demyelination and remyelination. Mol Cell Neurosci 1998 12 : 220 7
29. Redwine JM, Armstrong RC. In vivo proliferation of oligodendrocyte progenitors expressing PDGF alpha R during early remyelination. J Neurobiol 1998 37 : 413 28
30. Woodruff RH, Franklin RJM. The expression of myelin protein mRNAs during remyelination of lysolecithin-induced demyelination. Neuropathol Appl Neurobiol 1999 25 : 226 35
31. Woodruff RH, Franklin RJM. 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 1999 25 : 216 28
32. Gensert JM, Goldman JE. Endogenous progenitors remyelinate demyelinated axons in the adult CNS. Neuron 1997 19 : 197 203
33. Baumann N, Pham-Dinh D. Biology of oligodendrocyte and myelin in the mammalian central nervous system. Physiol Rev 2001 81 : 871 927
34. Stangel M, Hartung HP. Remyelinating strategies for the treatment of multiple sclerosis. Prog Neurobiol 2002 68 : 361 76
35. Scolding N, Franklin R, Stevens S, Heldin CH, Compston A, Newcombe J. Oligodendrocyte progenitors are present in the normal adult human CNS and in the lesions of multiple sclerosis. Brain 1998 121 : 2221 8
36. Wolswijk G. Oligodendrocyte precursor cells in the demyelinated multiple sclerosis spinal cord. Brain 2002 125 : 338 49
37. Ulrich R, Gerhauser I, Seeliger F, Baumgartner W, Alldinger S. Matrix metalloproteinases and their inhibitors in the developing mouse brain and spinal cord: a reverse transcription quantitative polymerase chain reaction study. Dev Neurosci 2005 27 : 408 18
38. Klapdor K, Dulfer BG, Hammann A, VanderStaay FJ. A low-cost method to analyse footprint patterns. J Neurosci Methods 1997 75 : 49 54
39. McGavern DB, Zoecklein L, Drescher KM, Rodriguez M. Quantitative assessment of neurologic deficits in a chronic progressive murine model of CNS demyelination. Exp Neurol 1999 158 : 171 81
40. Baumgärtner W, Krakowka S, Blakeslee JR. Persistent infection of Vero cells by paramyxoviruses - a morphological and immunoelectron microscopic investigation. Intervirology 1987 27 : 218 23
41. Seeliger F, Hess O, Probsting M, Kleinschmidt S, Woehrmann T, Germann PG, Baumgartner W. Confocal laser scanning analysis of an equine oral mast cell tumor with atypical expression of tyrosine kinase receptor C-KIT. Vet Pathol 2007 44 : 225 8
42. Jiang YH, Henderson D, Blackstad M, Chen A, Miller RF, Verfaillie CM. Neuroectodermal differentiation from mouse multipotent adult progenitor cells. Proc Natl Acad Sci USA 2003 100 : 11854 60
43. Li SH, Lee RKK, Chen PW, Lu CH, Wang SH, Hwu YM. Differential expression and distribution of alternatively spliced transcripts of PDGF-A and of PDGF receptor-alpha in mouse reproductive tissues. Life Sci 2005 77 : 2412 24
44. Vandesompele J, De Preter K, Pattyn F, Poppe B, Van Roy N, De Paepe A, Speleman F. Accurate normalization of real-time quantitative RT-PCR data by geometric averaging of multiple internal control genes. Genome Biol 2002 3 : RESEARCH0034
45. Lassmann H, Bruck W, Lucchinetti CF. The immunopathology of multiple sclerosis: an overview. Brain Pathol 2007 17 : 210 18
46. Ozden S, Aubert C, Gonzalezdunia D, Brahic M. Insitu analysis of proteolipid protein gene transcripts during persistent Theiler's virus-infection. J Histochem Cytochem 1991 39 : 1305 9
47. Yamada M, Zurbriggen A, Fujinami RS. The relationship between viral-RNA, myelin-specific messenger-RNAs, and demyelination in central-nervous-system disease during Theiler's virus-infection. Am J Pathol 1990 137 : 1467 79
48. Jordan CA, Friedrich VL, Godfraind C, Cardellechio CB, Holmes KV, Duboisdalcq M. Expression of viral and myelin gene transcripts in a murine CNS demyelinating disease caused by a coronavirus. Glia 1989 2 : 318 29
49. Franklin RJM. Why does remyelination fail in multiple sclerosis? Nat Rev Neurosci 2002 3 : 705 14
50. Mason JL, Toews A, Hostettler JD, Morell P, Suzuki K, Goldman JE, Matsushima GK. Oligodendrocytes and progenitors become progressively depleted within chronically demyelinated lesions. Am J Pathol 2004 164 : 1673 82
51. Wolswijk G. Chronic stage multiple sclerosis lesions contain a relatively quiescent population of oligodendrocyte precursor cells. J Neurosci 1998 18 : 601 9
52. Kuhlmann T, Remington L, Cognet I, Bourbonniere L, Zehntner S, Guilhot F, Herman A, Guay-Giroux A, Antel JP, Owens T, Gauchat JF. Continued administration of ciliary neurotrophic factor protects mice from inflammatory pathology in experimental autoimmune encephalomyelitis. Am J Pathol 2006 169 : 584 98
53. Alonso G. NG2 proteoglycan-expressing cells of the adult rat brain: possible involvement in the formation of glial scar astrocytes following stab wound. Glia 2005 49 : 318 38
54. Tang XF, Davies JE, Davies SJA. Changes in distribution, cell associations, and protein expression levels of NG2, neurocan, phosphacan, brevican, versican V2, and tenascin-C during acute to chronic maturation of spinal cord scar tissue. J Neurosci Res 2003 71 : 427 44
55. Prayoonwiwat N, Rodriguez M. The potential for oligodendrocyte proliferation during demyelinating disease. J Neuropathol Exp Neurol 1993 52 : 55 63
56. Kotter MR, Li WW, Zhao C, Franklin RJM. Myelin impairs CNS remyelination by inhibiting oligodendrocyte precursor cell differentiation. J Neurosci 2006 26 : 328 32
57. Keirstead HS, Levine JM, Blakemore WF. Response of the oligodendrocyte progenitor cell population (defined by NG2 labelling) to demyelination of the adult spinal cord. Glia 1998 22 : 161 70
58. Ye P, Bagnell R, D'Ercole AJ. Mouse NG2(+) oligodendrocyte precursors express mRNA for proteolipid protein but not its DM-20 variant: a study of laser microdissection-captured NG2(+) cells. J Neurosci 2003 23 : 4401 5
59. Linington C, Engelhardt B, Kapocs G, Lassman H. Induction of persistently demyelinated lesions in the rat following the repeated adoptive transfer of encephalitogenic T-cells and demyelinating antibody. J Neuroimmunol 1992 40 : 219 24
60. Nagasato K, Farris RW, DuboisDalcq M, Voskuhl RR. Exon 2 containing myelin basic protein (MBP) transcripts are expressed in lesions of experimental allergic encephalomyelitis (EAE). J Neuroimmunol 1997 72 : 21 5
61. Jordan CA, Friedrich VL, Deferra F, Weismiller DG, Holmes KV, Duboisdalcq M. Differential exon expression in myelin basic-protein transcripts during central-nervous-system (CNS) Remyelination. Cell Mol Neurobiol 1990 10 : 3 17
62. Fawcett JW, Asher RA. The glial scar and central nervous system repair. Brain Res Bull 1999 49 : 377 91
63. Titeux M, Galou M, Gomes FCA, Dormont D, Neto VM, Paulin D. Differences in the activation of the GFAP gene promoter by prion and viral infections. Mol Brain Res 2002 109 : 119 27
64. Levine JM, Stincone F, Lee YS. Development and differentiation of glial precursor cells in the rat cerebellum. Glia 1993 7 : 307 21
65. Pringproa K, Kumnok J, Ulrich R, Baumgärtner W, Wewetzer K. In vitro characterization of a murine oligodendrocyte precursor cell line (BO-1) following spontaneous immortalization. Int J Dev Neurosci 2008 26 : 283 91.
66. Tsunoda I, Kuang LQ, Libbey JE, Fujinami RS. Axonal injury heralds virus-induced demyelination. Am J Pathol 2003 162 : 1259 69
67. Tsunoda I, Tanaka T, Saijoh Y, Fujinami RS. Targeting inflammatory demyelinating lesions to sites of Wallerian degeneration. Am J Pathol 2007 171 : 1563 75
68. McGavern DB, Murray PD, Rivera-Quinones C, Schmelzer JD, Low PA, Rodriguez M. Axonal loss results in spinal-cord atrophy, electrophysiological abnormalities and neurological deficits following demyelination in a chronic inflammatory model of multiple sclerosis. Brain 2000 123 : 519 31
69. Mi S, Miller RH, Lee X, Scott ML, Shulag-Morskaya S, Shao ZH, Chang JF, Thill G, Levesque M, Zhang MD, Hession C, Sah D, Trapp B, He ZG, Jung V, McCoy JM, Pepinsky RB. LINGO-1 negatively regulates myelination by oligodendrocytes. Nat Neurosci 2005 8 : 745 51
70. John GR, Shankar SL, Shafit-Zagardo B, Massimi A, Lee SC, Raine CS, Brosnan CF. Multiple sclerosis: re-expression of a developmental pathway that restricts oligodendrocyte maturation. Nat Med 2002 8 : 1115 21