Theiler's murine encephalomyelitis virus preferentially infects immature stages of the murine oligodendrocyte precursor cell line BO-1 and blocks oligodendrocytic differentiation in vitro

Brain Research

Volumn 1327, Issue , 2010, Pages 24-37

  Pringproa, Kidsadagon ^a,b   Rohn, Karl ^a   Kummerfeld, Maren ^a   Wewetzer, Konstantin ^a,c   Baumgärtner, Wolfgang ^a,b  

^a UNIVERSITY OF VETERINARY MEDICINE HANNOVER   (Germany)

^b CENTER FOR SYSTEMS NEUROSCIENCE   (Germany)

^c HANNOVER MEDICAL SCHOOL   (Germany)

Author keywords

Oligodendrocyte; OPC; TMEV

Indexed keywords

2',3' CYCLIC NUCLEOTIDE 3' PHOSPHODIESTERASE; RETINOIC ACID;

ANIMAL CELL; ARTICLE; CELL DIFFERENTIATION; CELL PROLIFERATION; CONTROLLED STUDY; DEMYELINATION; IN VITRO STUDY; INFECTION SENSITIVITY; MOUSE; MURINE ENCEPHALOMYELITIS VIRUS; NONHUMAN; OLIGODENDROGLIA; PHENOTYPE; PRIORITY JOURNAL; REMYELINIZATION; RNA VIRUS INFECTION; STEM CELL; VIRUS PATHOGENESIS;

ANALYSIS OF VARIANCE; ANIMALS; ANIMALS, NEWBORN; BROMODEOXYURIDINE; CARDIOVIRUS INFECTIONS; CELL DIFFERENTIATION; CELL LINE, TRANSFORMED; CELL PROLIFERATION; CRICETINAE; CULTURE MEDIA, CONDITIONED; DISEASE MODELS, ANIMAL; GANGLIOSIDES; IN SITU NICK-END LABELING; MICE; MICROSCOPY, ELECTRON, SCANNING; OLIGODENDROGLIA; PLAQUE ASSAY; POLIOMYELITIS; THEILOVIRUS; VIRAL PROTEINS;

ANIMALIA; MURINAE; THEILER'S ENCEPHALOMYELITIS VIRUS;

EID: 77950352612     PISSN: 00068993     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.brainres.2010.02.068     Document Type: Article

References (55)

1. Ahlgren S.C., Wallace H., Bishop J., Neophytou C., and Raff M.C. Effects of thyroid hormone on embryonic oligodendrocyte precursor cell development in vivo and in vitro. Mol. Cell. Neurosci. 9 (1997) 420-432
2. Aubert C., Chamorro M., and Brahic M. Identification of Theiler's virus infected cells in the central nervous system of the mouse during demyelinating disease. Microb. Pathog. 3 (1987) 319-326
3. Baas D., Bourbeau D., Sarlieve L.L., Ittel M.E., Dussault J.H., and Puymirat J. Oligodendrocyte maturation and progenitor cell proliferation are independently regulated by thyroid hormone. Glia. 19 (1997) 324-332
4. Barkhof F., Bruck W., De Groot C.J., Bergers E., Hulshof S., Geurts J., Polman C.H., and van der Valk P. Remyelinated lesions in multiple sclerosis: magnetic resonance image appearance. Arch. Neurol. 60 (2003) 1073-1081
5. Barres B.A., Lazar M.A., and Raff M.C. A novel role for thyroid hormone, glucocorticoids and retinoic acid in timing oligodendrocyte development. Development 120 (1994) 1097-1108
6. Baumgärtner W., Krakowka S., and Gorham J.R. Canine parainfluenza virus-induced encephalitis in ferrets. J. Comp. Path. 100 (1989) 67-76
7. Bihl F., Pena-Rossi C., Guenet J.L., Brahic M., and Bureau J.F. The Shiverer mutation affects the persistence of Theiler's virus in the central nervous system. J. Virol. 71 (1997) 5025-5030
8. Caselli E., Galvan M., Santoni F., Alvarez S., de Lera A.R., Ivanova D., Gronemeyer H., Caruso A., Guidoboni M., Cassai E., Dolcetti R., and Di Luca D. Retinoic acid analogues inhibit human herpesvirus 8 replication. Antivir. Ther. 13 (2008) 199-209
9. Causey O.R., and Theiler M. Virus antibody survey on sera of residents of the Amazon valley in Brazil. Am. J. Trop. Med. Hyg. 7 (1958) 36-41
10. Dal Canto M.C., and Lipton H.L. Schwann cell remyelination and recurrent demyelination in the central nervous system of mice infected with attenuated Theiler's virus. Am. J. Pathol. 98 (1980) 101-122
11. Dal Canto M.C., and Lipton H.L. Ultrastructural immunohistochemical localization of virus in acute and chronic demyelinating Theiler's virus infection. Am. J. Pathol. 106 (1982) 20-29
12. Dal Canto M.C., Kim B.S., Miller S.D., and Melvold R.W. Theiler's murine encephalomyelitis virus (TMEV)-induced demyelination: a model for human multiple sclerosis. Methods 10 (1996) 453-461
13. de Castro F., and Bribian A. The molecular orchestra of the migration of oligodendrocyte precursors during development. Brain Res. Brain Res. Rev. 49 (2005) 227-241
14. de Vellis J. Developmental and hormonal regulation of gene expression in oligodendrocytes. Ann. N. Y. Acad. Sci. 605 (1990) 81-89
15. Fanarraga M.L., Sommer I., and Griffiths I.R. O-2A progenitors of the mouse optic nerve exhibit a developmental pattern of antigen expression different from the rat. Glia 15 (1995) 95-104
16. Franklin R.J., and Ffrench-Constant C. Remyelination in the CNS: from biology to therapy. Nat. Rev. Neurosci. 9 (2008) 839-855
17. Franklin R.J., and Kotter M.R. The biology of CNS remyelination: the key to therapeutic advances. J Neurol. 255 (2008) 19-25
18. Graves M.C., Bologa L., Siegel L., and Londe H. Theiler's virus in brain cell cultures: lysis of neurons and oligodendrocytes and persistence in astrocytes and macrophages. J. Neurosci. Res. 15 (1986) 491-501
19. Hao X., Kim T.S., and Braciale T.J. Differential response of respiratory dendritic cell subsets to influenza virus infection. J. Virol. 82 (2008) 4908-4919
20. + T cells directed against a viral peptide contribute to loss of motor function by disrupting axonal transport in a viral model of fulminant demyelination. J. Neuroimmunol. 188 (2007) 13-21
21. Jelachich M.L., and Lipton H.L. Theiler's murine encephalomyelitis virus kills restrictive but not permissive cells by apoptosis. J. Virol. 70 (1996) 6856-6861
22. Kuhlmann T., Miron V., Cuo Q., Wegner C., Antel J., and Bruck W. Differentiation block of oligodendroglial progenitor cells as a cause for remyelination failure in chronic multiple sclerosis. Brain 131 (2008) 1749-1758
23. Kummerfeld M., Meens J., Haas L., Baumgärtner W., and Beineke A. Generation and characterization of a polyclonal antibody for the detection of Theilers murine encephalomyelitis virus by light and electron microscopy. J. Virol. Methods 160 (2009) 185-188
24. Kumnok J., Ulrich R., Wewetzer K., Rohn K., Hansmann F., Baumgärtner W., and Alldinger S. Differential transcription of matrix-metalloproteinase genes in primary mouse astrocytes and microglia infected with Theiler's murine encephalomyelitis virus. J. Neurovirol. 14 (2008) 205-217
25. Lipton H.L., Twaddle G., and Jelachich M.L. The predominant virus antigen burden is present in macrophages in Theiler's murine encephalomyelitis virus-induced demyelinating disease. J. Virol. 69 (1995) 2525-2533
26. Lipton H.L., Kumar A.S., and Trottier M. Theiler's virus persistence in the central nervous system of mice is associated with continuous viral replication and a difference in outcome of infection of infiltrating macrophages versus oligodendrocytes. Virus Res. 111 (2005) 214-223
27. Maeda Y., Yamaguchi T., Hijikata Y., Morita Y., Tanaka M., Hirase C., Takai S., Tatsumi Y., and Kanamaru A. All-trans retinoic acid attacks reverse transcriptase resulting in inhibition of HIV-1 replication. Hematology 12 (2007) 263-266
28. McGavern D.B., Murray P.D., and Rodriguez M. Quantitation of spinal cord demyelination, remyelination, atrophy, and axonal loss in a model of progressive neurologic injury. J. Neurosci. Res. 58 (1999) 492-504
29. Michiels T., Jarousse N., and Brahic M. Analysis of the leader and capsid coding regions of persistent and neurovirulent strains of Theiler's virus. Virology 214 (1995) 550-558
30. Ohara Y., Konno H., Iwasaki Y., Yamamoto T., Terunuma H., and Suzuki H. Cytotropism of Theiler's murine encephalomyelitis viruses on oligodendrocyte-enriched cultures. Arch. Virol. 114 (1990) 293-298
31. Oldstone M.B.A., Sinha Y.N., Blount P., Tishon A., Rodriguez M., von Wedel R., and Lampert P.W. Virus-induced alterations in homeostasis: alterations in differentiated functions of infected cells in vivo. Science 218 (1982) 1125-1127
32. Oleszak E.L., Chang J.R., Friedman H., Katsetos C.D., and Platsoucas C.D. Theiler's virus infection: a model for multiple sclerosis. Clin. Microbiol. Rev. 17 (2004) 174-207
33. O'Shea H., Crang J., Tonks P., Nash A.A., and Fazakerley J.K. The PI capsid region of Theiler's virus controls replication in mouse glial cell cultures. Arch. Virol. 142 (1997) 1521-1535
34. Palma J.P., Kwon D., Clipstone N.A., and Kim B.S. Infection with Theiler's murine encephalomyelitis virus directly induces proinflammatory cytokines in primary astrocytes via NF-kappaB activation: potential role for the initiation of demyelinating disease. J. Virol. 77 (2003) 6322-6331
35. Patrikios P., Stadelmann C., Kutzelnigg A., Rauschka H., Schmidbauer M., Laursen H., Sorensen P.S., Bruck W., Lucchinetti C., and Lassmann H. Remyelination is extensive in a subset of multiple sclerosis patients. Brain 129 (2006) 3165-3172
36. Pevear D.C., Calenoff M., Rozhon E., and Lipton H.L. Analysis of the complete nucleotide sequence of the picornavirus Theiler's murine encephalomyelitis virus indicates that it is closely related to cardioviruses. J. Virol. 61 (1987) 1507-1516
37. Pombo P.M., Barettino D., Ibarrola N., Vega S., and Rodriguez-Pena A. Stimulation of the myelin basic protein gene expression by 9-cis-retinoic acid and thyroid hormone: activation in the context of its native promoter. Brain Res. Mol. Brain Res. 64 (1999) 92-100
38. Pozner R.G., Berria M.I., Negrotto S., Schattner M., and Gomez R.M. Differential astrocyte response to Theiler's murine encephalomyelitis virus infection. Intervirology 48 (2005) 279-284
39. Prayoonwiwat N., and Rodriguez M. The potential for oligodendrocyte proliferation during demyelinating disease. J. Neuropathol. Exp. Neurol. 52 (1993) 55-63
40. Prineas J.W., and Connell F. Remyelination in multiple sclerosis. Ann. Neurol. 5 (1979) 22-31
41. Pringproa K., Kumnok J., Ulrich R., Baumgärtner W., and Wewetzer K. In vitro characterization of a murine oligodendrocyte precursor cell line (BO-1) following spontaneous immortalization. Int. J. Dev. Neurosci. 26 (2008) 283-291
42. Qi Y., and Dal Canto M.C. Effect of Theiler's murine encephalomyelitis virus and cytokines on cultured oligodendrocytes and astrocytes. J. Neurosci. Res. 45 (1996) 364-374
43. Raff M.C., Miller R.H., and Noble M. A glial progenitor cell that develops in vitro into an astrocyte or an oligodendrocyte depending on culture medium. Nature 303 (1983) 390-396
44. Raff M.C., Williams B.P., and Miller R.H. The in vitro differentiation of a bipotential glial progenitor cell. EMBO J. 3 (1984) 1857-1864
45. Rodriguez M., Leibowitz J.L., and Lampert P.W. Persistent infection of oligodendrocytes in Theiler's virus-induced encephalomyelitis. Ann. Neurol. 13 (1983) 426-433
46. Rodriguez M., Oleszak E., and Leibowitz J. Theiler's murine encephalomyelitis: a model of demyelination and persistence of virus. Crit. Rev. Immunol. 7 (1987) 325-365
47. Techangamsuwan S., Imbschweiler I., Kreutzer R., Kreutzer M., Baumgärtner W., and Wewetzer K. Similar behaviour and primate-like properties of adult canine Schwann cells and olfactory ensheathing cells in long-term culture. Brain Res. 1240 (2008) 31-38
48. Tokumoto Y.M., Durand B., and Raff M.C. An analysis of the early events when oligodendrocyte precursor cells are triggered to differentiate by thyroid hormone, retinoic acid, or PDGF withdrawal. Dev. Biol. 213 (1999) 327-339
49. Trottier C., Chabot S., Mann K.K., Colombo M., Chatterjee A., Miller Jr. W.H., and Ward B.J. Retinoids inhibit measles virus in vitro via nuclear retinoid receptor signaling pathways. Antiviral Res. 80 (2008) 45-53
50. Tsunoda I., and Fujinami R.S. Inside-out versus outside-in models for virus induced demyelination: axonal damage triggering demyelination. Springer Semin. Immunopathol. 24 (2002) 105-125
51. + T-cell clones following virus infection. J. Virol. 79 (2005) 14640-14646
52. Ulrich R., Seeliger F., Kreutzer M., Germann P.G., and Baumgärtner W. Limited remyelination in Theiler's murine encephalomyelitis due to insufficient oligodendroglial differentiation of nerve/glial antigen 2 (NG2)-positive putative oligodendroglial progenitor cells. Neuropathol. Appl. Neurobiol. 34 (2008) 603-620
53. Ulrich, R., Kalkuhl, A., Deschl, U., Baumgärtner, W., in press. Machine learning approach identifies new pathways associated with demyelination in a viral model of multiple sclerosis. J Cell Mol Med. doi:10.1111/j.1582-4934.2008.00646.x.
54. Welsh C.J., Steelman A.J., Mi W., Young C.R., Storts R., Welsh Jr. T.H., and Meagher M.W. Neuroimmune interactions in a model of multiple sclerosis. Ann. N. Y. Acad. Sci. 1153 (2009) 209-219
55. Zheng L., Calenoff M.A., and Dal Canto M.C. Astrocytes, not microglia, are the main cells responsible for viral persistence in Theiler's murine encephalomyelitis virus infection leading to demyelination. J. Neuroimmunol. 118 (2001) 256-267