Theiler's murine encephalomyelitis virus induced phenotype switch of microglia in vitro

Journal of Neuroimmunology

Volumn 252, Issue 1-2, 2012, Pages 49-55

  Gerhauser, I ^a   Hansmann, F ^a   Puff, C ^a   Kumnok, J ^a   Schaudien, D ^a   Wewetzer, K ^a,b,c   Baumgartner W ^a,b  

^a UNIVERSITY OF VETERINARY MEDICINE HANNOVER   (Germany)

^b CENTER FOR SYSTEMS NEUROSCIENCE   (Germany)

^c HANNOVER MEDICAL SCHOOL   (Germany)

Author keywords

AP 1; Astrocyte; Cytokine; Microglia; NF B; Theiler's murine encephalomyelitis virus

Indexed keywords

GAMMA INTERFERON; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; INTERLEUKIN 1; INTERLEUKIN 10; INTERLEUKIN 12; INTERLEUKIN 2; MESSENGER RNA; NUCLEAR FACTOR KAPPA B P50 SUBUNIT; PROTEIN C FOS; PROTEIN C JUN; TRANSCRIPTION FACTOR AP 1; TRANSCRIPTION FACTOR RELA; TRANSFORMING GROWTH FACTOR BETA1; TUMOR NECROSIS FACTOR; TUMOR NECROSIS FACTOR RECEPTOR 1; TUMOR NECROSIS FACTOR RECEPTOR 2; UNCLASSIFIED DRUG; VIRUS RNA;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; ASTROCYTE; AUTOCRINE EFFECT; CARDIOVIRUS INFECTION; CELL TYPE; CONTROLLED STUDY; ENZYME LINKED IMMUNOSORBENT ASSAY; FEEDBACK SYSTEM; FEMALE; GENE EXPRESSION; IN VITRO STUDY; IN VIVO STUDY; MICROGLIA; MOUSE; MULTIPLE SCLEROSIS; MURINE ENCEPHALOMYELITIS VIRUS; NEWBORN; NONHUMAN; NUCLEOTIDE SEQUENCE; PATHOPHYSIOLOGY; PHENOTYPIC PLASTICITY; PRIORITY JOURNAL; PROTEIN EXPRESSION; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; UPREGULATION; VIRUS CELL INTERACTION; VIRUS LOAD;

ANIMALS; ASTROCYTES; CARDIOVIRUS INFECTIONS; CELLS, CULTURED; CYTOKINES; ENZYME-LINKED IMMUNOSORBENT ASSAY; FEMALE; FLUORESCENT ANTIBODY TECHNIQUE; MICE; MICROGLIA; PHENOTYPE; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; THEILOVIRUS; TRANSCRIPTION FACTORS; UP-REGULATION;

EID: 84867139126     PISSN: 01655728     EISSN: 18728421     Source Type: Journal    
DOI: 10.1016/j.jneuroim.2012.07.018     Document Type: Article

References (65)

1. Anderson R., Harting E., Frey M.S., Leibowitz J.L., Miranda R.C. Theiler's murine encephalomyelitis virus induces rapid necrosis and delayed apoptosis in myelinated mouse cerebellar explant cultures. Brain Res. 2000, 868:259-267.
2. Bottenstein J.E., Sato G.H. Growth of a rat neuroblastoma cell line in serum-free supplemented medium. Proc. Natl. Acad. Sci. U. S. A. 1979, 76:514-517.
3. Bright J.J., Rodriguez M., Sriram S. Differential influence of interleukin-12 in the pathogenesis of autoimmune and virus-induced central nervous system demyelination. J. Virol. 1999, 73:1637-1639.
4. Carpentier P.A., Williams B.R., Miller S.D. Distinct roles of protein kinase R and toll-like receptor 3 in the activation of astrocytes by viral stimuli. Glia 2007, 55:239-252.
5. Chang J.R., Zaczynska E., Katsetos C.D., Platsoucas C.D., Oleszak E.L. Differential expression of TGF-beta, IL-2, and other cytokines in the CNS of Theiler's murine encephalomyelitis virus-infected susceptible and resistant strains of mice. Virology 2000, 278:346-360.
6. Choi S.J., Lee K.H., Park H.S., Kim S.K., Koh C.M., Park J.Y. Differential expression, shedding, cytokine regulation and function of TNFR1 and TNFR2 in human fetal astrocytes. Yonsei Med. J. 2005, 46:818-826.
7. Correa F., Mestre L., Docagne F., Guaza C. Activation of cannabinoid CB2 receptor negatively regulates IL-12p40 production in murine macrophages: role of IL-10 and ERK1/2 kinase signaling. Br. J. Pharmacol. 2005, 145:441-448.
8. Dal Canto M.C., Calenoff M.A., Miller S.D., Vanderlugt C.L. Lymphocytes from mice chronically infected with Theiler's murine encephalomyelitis virus produce demyelination of organotypic cultures after stimulation with the major encephalitogenic epitope of myelin proteolipid protein. Epitope spreading in TMEV infection has functional activity. J. Neuroimmunol. 2000, 104:79-84.
9. Dhandapani K.M., Khan M.M., Wade F.M., Wakade C., Mahesh V.B., Brann D.W. Induction of transforming growth factor-beta1 by basic fibroblast growth factor in rat C6 glioma cells and astrocytes is mediated by MEK/ERK signaling and AP-1 activation. J. Neurosci. Res. 2007, 85:1033-1045.
10. Ding A.H., Nathan C.F., Stuehr D.J. Release of reactive nitrogen intermediates and reactive oxygen intermediates from mouse peritoneal macrophages. Comparison of activating cytokines and evidence for independent production. J. Immunol. 1988, 141:2407-2412.
11. Dopp J.M., Mackenzie-Graham A., Otero G.C., Merrill J.E. Differential expression, cytokine modulation, and specific functions of type-1 and type-2 tumor necrosis factor receptors in rat glia. J. Neuroimmunol. 1997, 75:104-112.
12. Frisk A.L., Baumgärtner W., Gröne A. Dominating interleukin-10 mRNA expression induction in cerebrospinal fluid cells of dogs with natural canine distemper virus induced demyelinating and non-demyelinating CNS lesions. J. Neuroimmunol. 1999, 97:102-109.
13. Gerhauser I., Alldinger S., Ulrich R., Baumgärtner W. Spatio-temporal expression of immediate early genes in the central nervous system of SJL/J mice. Int. J. Dev. Neurosci. 2005, 23:637-649.
14. 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.
15. 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, 66:809-818.
16. Gitlin L., Barchet W., Gilfillan S., Cella M., Beutler B., Flavell R.A., Diamond M.S., Colonna M. Essential role of mda-5 in type I IFN responses to polyriboinosinic:polyribocytidylic acid and encephalomyocarditis picornavirus. Proc. Natl. Acad. Sci. U. S. A. 2006, 103:8459-8464.
17. Gröne A., Alldinger S., Baumgärtner W. Interleukin-1beta, -6, -12 and tumor necrosis factor-alpha expression in brains of dogs with canine distemper virus infection. J. Neuroimmunol. 2000, 110:20-30.
18. Gröne A., Fonfara S., Baumgärtner W. Cell type-dependent cytokine expression after canine distemper virus infection. Viral Immunol. 2002, 15:493-505.
19. Herder V., Hansmann F., Stangel M., Schaudien D., Rohn K., Baumgärtner W., Beineke A. Cuprizone inhibits demyelinating leukomyelitis by reducing immune responses without virus exacerbation in an infectious model of multiple sclerosis. J. Neuroimmunol. 2012, 244:84-93.
20. Inoue A., Koh C.S., Yamazaki M., Yahikozawa H., Ichikawa M., Yagita H., Kim B.S. Suppressive effect on Theiler's murine encephalomyelitis virus-induced demyelinating disease by the administration of anti-IL-12 antibody. J. Immunol. 1998, 161:5586-5593.
21. Jin Y.H., Mohindru M., Kang M.H., Fuller A.C., Kang B., Gallo D., Kim B.S. Differential virus replication, cytokine production, and antigen-presenting function by microglia from susceptible and resistant mice infected with Theiler's virus. J. Virol. 2007, 81:11690-11702.
22. Jin Y.H., Hou W., Kim S.J., Fuller A.C., Kang B., Goings G., Miller S.D., Kim B.S. Type I interferon signals control Theiler's virus infection site, cellular infiltration and T cell stimulation in the CNS. J. Neuroimmunol. 2010, 226:27-37.
23. Karin M., Liu Z., Zandi E. AP-1 function and regulation. Curr. Opin. Cell Biol. 1997, 9:240-246.
24. Katz-Levy Y., Neville K.L., Padilla J., Rahbe S., Begolka W.S., Girvin A.M., Olson J.K., Vanderlugt C.L., Miller S.D. Temporal development of autoreactive Th1 responses and endogenous presentation of self myelin epitopes by central nervous system-resident APCs in Theiler's virus-infected mice. J. Immunol. 2000, 165:5304-5314.
25. Kigerl K.A., Gensel J.C., Ankeny D.P., Alexander J.K., Donnelly D.J., Popovich P.G. Identification of two distinct macrophage subsets with divergent effects causing either neurotoxicity or regeneration in the injured mouse spinal cord. J. Neurosci. 2009, 29:13435-13444.
26. Kim H.J., Ifergan I., Antel J.P., Seguin R., Duddy M., Lapierre Y., Jalili F., Bar-Or A. Type 2 monocyte and microglia differentiation mediated by glatiramer acetate therapy in patients with multiple sclerosis. J. Immunol. 2004, 172:7144-7153.
27. Kim B.S., Palma J.P., Kwon D., Fuller A.C. Innate immune response induced by Theiler's murine encephalomyelitis virus infection. Immunol. Res. 2005, 31:1-12.
28. Kohno T., Brewer M.T., Baker S.L., Schwartz P.E., King M.W., Hale K.K., Squires C.H., Thompson R.C., Vannice J.L. A second tumor necrosis factor receptor gene product can shed a naturally occurring tumor necrosis factor inhibitor. Proc. Natl. Acad. Sci. U. S. A. 1990, 87:8331-8335.
29. Kummerfeld M., Meens J., Haas L., Baumgärtner W., Beineke A. Generation and characterization of a polyclonal antibody for the detection of Theiler's murine encephalomyelitis virus by light and electron microscopy. J. Virol. Methods 2009, 160:185-188.
30. Kummerfeld M., Seehusen F., Klein S., Ulrich R., Kreutzer R., Gerhauser I., Herder V., Baumgärtner W., Beineke A. Periventricular demyelination and axonal pathology is associated with subependymal virus spread in a murine model for multiple sclerosis. Intervirology 2012, 10.1159/000336563.
31. Kumnok J., Ulrich R., Wewetzer K., Rohn K., Hansmann F., Baumgärtner W., Alldinger S. Differential transcription of matrix-metalloproteinase genes in primary mouse astrocytes and microglia infected with Theiler's murine encephalomyelitis virus. J. Neurovirol. 2008, 14:205-217.
32. Kuno R., Wang J., Kawanokuchi J., Takeuchi H., Mizuno T., Suzumura A. Autocrine activation of microglia by tumor necrosis factor-alpha. J. Neuroimmunol. 2005, 162:89-96.
33. Kuno R., Yoshida Y., Nitta A., Nabeshima T., Wang J., Sonobe Y., Kawanokuchi J., Takeuchi H., Mizuno T., Suzumura A. The role of TNF-alpha and its receptors in the production of NGF and GDNF by astrocytes. Brain Res. 2006, 1116:12-18.
34. Lipton H.L. Theilers virus-infection in mice-unusual biphasic disease process leading to demyelination. Infect. Immun. 1975, 11:1147-1155.
35. Mantovani A., Sica A., Sozzani S., Allavena P., Vecchi A., Locati M. The chemokine system in diverse forms of macrophage activation and polarization. Trends Immunol. 2004, 25:677-686.
36. Markus S., Failing K., Baumgärtner W. Increased expression of pro-inflammatory cytokines and lack of up-regulation of anti-inflammatory cytokines in early distemper CNS lesions. J. Neuroimmunol. 2002, 125:30-41.
37. McCoy M.K., Tansey M.G. TNF signaling inhibition in the CNS: implications for normal brain function and neurodegenerative disease. J. Neuroinflammation 2008, 5:45.
38. Miller S.D., Olson J.K., Croxford J.L. Multiple pathways to induction of virus-induced autoimmune demyelination: lessons from Theiler's virus infection. J. Autoimmun. 2001, 16:219-227.
39. Oleszak E.L., Chang J.R., Friedman H., Katsetos C.D., Platsoucas C.D. Theiler's virus infection: a model for multiple sclerosis. Clin. Microbiol. Rev. 2004, 17:174-207.
40. Olson J.K., Girvin A.M., Miller S.D. Direct activation of innate and antigen-presenting functions of microglia following infection with Theiler's virus. J. Virol. 2001, 75:9780-9789.
41. Pahl H.L. Activators and target genes of Rel/NF-kappaB transcription factors. Oncogene 1999, 18:6853-6866.
42. Palma J.P., Kim B.S. The scope and activation mechanisms of chemokine gene expression in primary astrocytes following infection with Theiler's virus. J. Neuroimmunol. 2004, 149:121-129.
43. Palma J.P., Yauch R.L., Kang H.K., Lee H.G., Kim B.S. Preferential induction of IL-10 in APC correlates with a switch from Th1 to Th2 response following infection with a low pathogenic variant of Theiler's virus. J. Immunol. 2002, 168:4221-4230.
44. Palma J.P., Kwon D., Clipstone N.A., 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. 2003, 77:6322-6331.
45. Pullen L.C., Miller S.D., Dal Canto M.C., Van der Meide P.H., Kim B.S. Alteration in the level of interferon-gamma results in acceleration of Theiler's virus-induced demyelinating disease. J. Neuroimmunol. 1994, 55:143-152.
46. Qi Y., Dal Canto M.C. Effect of Theiler's murine encephalomyelitis virus and cytokines on cultured oligodendrocytes and astrocytes. J. Neurosci. Res. 1996, 45:364-374.
47. Rubio N., Rojo P., Torres C. Overexpression of basal c-fos and c-jun but not of ras oncogenes after Theiler's murine encephalomyelitis virus infection of glial cells. J. Neurovirol. 1996, 2:167-174.
48. Sato S., Reiner S.L., Jensen M.A., Roos R.P. Central nervous system cytokine mRNA expression following Theiler's murine encephalomyelitis virus infection. J. Neuroimmunol. 1997, 76:213-223.
49. Sato F., Tanaka H., Hasanovic F., Tsunoda I. Theiler's virus infection: pathophysiology of demyelination and neurodegeneration. Pathophysiology 2011, 18:31-41.
50. Schmitz T., Chew L.J. Cytokines and myelination in the central nervous system. ScientificWorldJournal 2008, 8:1119-1147.
51. Sica A., Schioppa T., Mantovani A., Allavena P. Tumour-associated macrophages are a distinct M2 polarised population promoting tumour progression: potential targets of anti-cancer therapy. Eur. J. Cancer 2006, 42:717-727.
52. So E.Y., Kim B.S. Theiler's virus infection induces TLR3-dependent upregulation of TLR2 critical for proinflammatory cytokine production. Glia 2009, 57:1216-1226.
53. So E.Y., Kang M.H., Kim B.S. Induction of chemokine and cytokine genes in astrocytes following infection with Theiler's murine encephalomyelitis virus is mediated by the Toll-like receptor 3. Glia 2006, 53:858-867.
54. Stohlman S.A., Hinton D.R. Viral induced demyelination. Brain Pathol. 2001, 11:92-106.
55. Tompkins S.M., Fuller K.G., Miller S.D. Theiler's virus-mediated autoimmunity: local presentation of CNS antigens and epitope spreading. Ann. N. Y. Acad. Sci. 2002, 958:26-38.
56. Trottier M., Schlitt B.P., Kung A.Y., Lipton H.L. Transition from acute to persistent Theiler's virus infection requires active viral replication that drives proinflammatory cytokine expression and chronic demyelinating disease. J. Virol. 2004, 78:12480-12488.
57. Ulrich R., Gerhauser I., Seeliger F., Baumgärtner 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, 27:408-418.
58. 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, 65:783-793.
59. Ulrich R., Seeliger F., Kreutzer M., Germann P.G., 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. 2008, 34:603-620.
60. Van Zee K.J., Kohno T., Fischer E., Rock C.S., Moldawer L.L., Lowry S.F. Tumor necrosis factor soluble receptors circulate during experimental and clinical inflammation and can protect against excessive tumor necrosis factor alpha in vitro and in vivo. Proc. Natl. Acad. Sci. U. S. A. 1992, 89:4845-4849.
61. 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).
62. Veroni C., Gabriele L., Canini I., Castiello L., Coccia E., Remoli M.E., Columba-Cabezas S., Arico E., Aloisi F., Agresti C. Activation of TNF receptor 2 in microglia promotes induction of anti-inflammatory pathways. Mol. Cell. Neurosci. 2010, 45:234-244.
63. Waetzig V., Czeloth K., Hidding U., Mielke K., Kanzow M., Brecht S., Goetz M., Lucius R., Herdegen T., Hanisch U.K. c-Jun N-terminal kinases (JNKs) mediate pro-inflammatory actions of microglia. Glia 2005, 50:235-246.
64. Zheng L., Calenoff M.A., 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. 2001, 118:256-267.
65. Zhu C., Gagnidze K., Gemberling J.H., Plevy S.E. Characterization of an activation protein-1-binding site in the murine interleukin-12 p40 promoter. Demonstration of novel functional elements by a reductionist approach. J. Biol. Chem. 2001, 276:18519-18528.