The immune response in the CNS in Theiler’s virus induced demyelinating disease switches from an early adaptive response to a chronic innate-like response

Journal of NeuroVirology

Volumn 22, Issue 1, 2016, Pages 66-79

  Gilli, Francesca ^a   Li, Libin ^b,c   Pachner, Andrew R ^a,b  

^a DARTMOUTH MEDICAL SCHOOL   (United States)

^b RUTGERS NEW JERSEY MEDICAL SCHOOL   (United States)

^c GenScript USA Inc   (United States)

Author keywords

CNS infection; Demyelination; MS biomarkers; Neurodegeneration; Neuroinflammation

Indexed keywords

COLONY STIMULATING FACTOR 1; CXCL1 CHEMOKINE; CXCL2 CHEMOKINE; CXCL9 CHEMOKINE; EOTAXIN; EPITHELIAL DERIVED NEUTROPHIL ACTIVATING FACTOR 78; GAMMA INTERFERON; GAMMA INTERFERON INDUCIBLE PROTEIN 10; GRANULOCYTE COLONY STIMULATING FACTOR; GRANULOCYTE MACROPHAGE COLONY STIMULATING FACTOR; INTERLEUKIN 10; INTERLEUKIN 12P40; INTERLEUKIN 12P70; INTERLEUKIN 13; INTERLEUKIN 15; INTERLEUKIN 17; INTERLEUKIN 1ALPHA; INTERLEUKIN 1BETA; INTERLEUKIN 2; INTERLEUKIN 3; INTERLEUKIN 4; INTERLEUKIN 5; INTERLEUKIN 6; INTERLEUKIN 7; INTERLEUKIN 9; MESSENGER RNA; MONOCYTE CHEMOTACTIC PROTEIN 1; TUMOR NECROSIS FACTOR ALPHA; UNINDEXED DRUG; VASCULOTROPIN; CYTOKINE; TOLL LIKE RECEPTOR;

ADAPTIVE IMMUNITY; ANIMAL TISSUE; ARTICLE; CEREBROSPINAL FLUID; CONTROLLED STUDY; CYTOKINE RELEASE; CYTOKINE RESPONSE; DEMYELINATING DISEASE; IMMUNE RESPONSE; IMMUNOASSAY; INNATE IMMUNITY; MALE; MOUSE; NERVOUS SYSTEM INFLAMMATION; NONHUMAN; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN CEREBROSPINAL FLUID LEVEL; REAL TIME POLYMERASE CHAIN REACTION; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; SHAM PROCEDURE; THEILER MURINE ENCEPHALOMYELITIS VIRUS INDUCED DEMYELINATING DISEASE; THEILER'S MURINE ENCEPHALOMYELITIS VIRUS; UPREGULATION; ANIMAL; CARDIOVIRUS INFECTION; CENTRAL NERVOUS SYSTEM; DISEASE COURSE; GENE EXPRESSION REGULATION; GENETICS; GROWTH, DEVELOPMENT AND AGING; HOST PATHOGEN INTERACTION; IMMUNOLOGY; INFLAMMATION; MOLECULAR GENETICS; PATHOGENICITY; THEILOVIRUS; TIME FACTOR; VIROLOGY;

ADAPTIVE IMMUNITY; ANIMALS; CARDIOVIRUS INFECTIONS; CENTRAL NERVOUS SYSTEM; CYTOKINES; DEMYELINATING DISEASES; DISEASE PROGRESSION; GENE EXPRESSION REGULATION; HOST-PATHOGEN INTERACTIONS; IMMUNITY, INNATE; INFLAMMATION; MICE; MOLECULAR SEQUENCE ANNOTATION; REAL-TIME POLYMERASE CHAIN REACTION; RNA, MESSENGER; THEILOVIRUS; TIME FACTORS; TOLL-LIKE RECEPTORS;

EID: 84957848062     PISSN: 13550284     EISSN: 15382443     Source Type: Journal    
DOI: 10.1007/s13365-015-0369-4     Document Type: Article

References (46)

1. Arikawa E QG, Han Y, Pan H, Yang J (2011) RT2 Profiler™ PCR arrays: pathway-focused gene expression profiling with qRT-PCR. SABiosciences
2. Begolka WS, Vanderlugt CL, Rahbe SM, Miller SD (1998) Differential expression of inflammatory cytokines parallels progression of central nervous system pathology in two clinically distinct models of multiple sclerosis. J Immunol 161:4437–4446
3. Chang JR, Zaczynska E, Katsetos CD, Platsoucas CD, Oleszak EL (2000) 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 278:346–360
4. Chastain EM, Duncan DS, Rodgers JM, Miller SD (2011) The role of antigen presenting cells in multiple sclerosis. Biochim Biophys Acta 1812:265–274
5. Croxford JL, Olson JK, Miller SD (2002) Epitope spreading and molecular mimicry as triggers of autoimmunity in the Theiler’s virus-induced demyelinating disease model of multiple sclerosis. Autoimmun Rev 1:251–260
6. Cunningham LA, Wetzel M, Rosenberg GA (2005) Multiple roles for MMPs and TIMPs in cerebral ischemia. Glia 50:329–339
7. da Silva FAFG, da Silva IDCG, Gonçalves GA, de Almeida FA, de Noronha SAAC, de Noronha SMR, Nakamura MU (2014) Viscum album modulates apoptotic related genes in melanoma tumor of mice. Am J Mol Biol 4:49–58
8. Dal Canto MC, Lipton HL (1975) Primary demyelination in Theiler’s virus infection. An ultrastructural study. Lab Investig 33:626–637
9. Elgert KD (2009) Immunology: understanding the immune system. Wiley
10. Elliott R, Li F, Dragomir I, Chua MM, Gregory BD, Weiss SR (2013) Analysis of the host transcriptome from demyelinating spinal cord of murine coronavirus-infected mice. PLoS One 8:e75346
11. Fainardi E, Castellazzi M, Bellini T, Manfrinato MC, Baldi E, Casetta I, Paolino E, Granieri E, Dallocchio F (2006) Cerebrospinal fluid and serum levels and intrathecal production of active matrix metalloproteinase-9 (MMP-9) as markers of disease activity in patients with multiple sclerosis. Mult Scler 12:294–301
12. Fang L, Huber-Abel F, Teuchert M, Hendrich C, Dorst J, Schattauer D, Zettlmeissel H, Wlaschek M, Scharffetter-Kochanek K, Tumani H, Ludolph AC, Brettschneider J (2009) Linking neuron and skin: matrix metalloproteinases in amyotrophic lateral sclerosis (ALS). J Neurol Sci 285:62–66
13. Gentilini D, Perino A, Vigano P, Chiodo I, Cucinella G, Vignali M, Di Blasio AM, Busacca M (2011) Gene expression profiling of peripheral blood mononuclear cells in endometriosis identifies genes altered in non-gynaecologic chronic inflammatory diseases. Hum Reprod 26:3109–3117
14. Gonzalez-Navajas JM, Lee J, David M, Raz E (2012) Immunomodulatory functions of type I interferons. Nat Rev Immunol 12:125–135
15. Gragnani A, Cezillo MV, da Silva ID, de Noronha SM, Correa-Noronha SA, Ferreira LM (2014) Gene expression profile of cytokines and receptors of inflammation from cultured keratinocytes of burned patients. Burns 40:947–956
16. Heneka MT, Kummer MP, Latz E (2014) Innate immune activation in neurodegenerative disease. Nat Rev Immunol 14:463–477
17. Huang X, Yang Y (2010) Targeting the TLR9-MyD88 pathway in the regulation of adaptive immune responses. Expert Opin Ther Targets 14:787–796
18. Kandagaddala LD, Kang MJ, Chung BC, Patterson TA, Kwon OS (2012) Expression and activation of matrix metalloproteinase-9 and NADPH oxidase in tissues and plasma of experimental autoimmune encephalomyelitis in mice. Exp Toxicol Pathol 64:109–114
19. Lehnardt S (2010) Innate immunity and neuroinflammation in the CNS: the role of microglia in Toll-like receptor-mediated neuronal injury. Glia 58:253–263
20. Li L, Narayan K, Pak E, Pachner AR (2006) Intrathecal antibody production in a mouse model of Lyme neuroborreliosis. J Neuroimmunol 173:56–68
21. Lipton HL (1975) Theiler’s virus infection in mice: an unusual biphasic disease process leading to demyelination. Infect Immun 11:1147–1155
22. Lipton HL, Dal Canto MC (1976) Theiler’s virus-induced demyelination: prevention by immunosuppression. Science 192:62–64
23. Lorenzl S, Albers DS, LeWitt PA, Chirichigno JW, Hilgenberg SL, Cudkowicz ME, Beal MF (2003) Tissue inhibitors of matrix metalloproteinases are elevated in cerebrospinal fluid of neurodegenerative diseases. J Neurol Sci 207:71–76
24. Lorenzl S, Narr S, Angele B, Krell HW, Gregorio J, Kiaei M, Pfister HW, Beal MF (2006) The matrix metalloproteinases inhibitor Ro 28-2653 [correction of Ro 26-2853] extends survival in transgenic ALS mice. Exp Neurol 200:166–171
25. Mack CL, Vanderlugt-Castaneda CL, Neville KL, Miller SD (2003) Microglia are activated to become competent antigen presenting and effector cells in the inflammatory environment of the Theiler’s virus model of multiple sclerosis. J Neuroimmunol 144:68–79
26. Martinez NE, Karlsson F, Sato F, Kawai E, Omura S, Minagar A, Grisham MB, Tsunoda I (2014) Protective and detrimental roles for regulatory T cells in a viral model for multiple sclerosis. Brain Pathol
27. Mecha M, Carrillo-Salinas FJ, Mestre L, Feliu A, Guaza C (2013) Viral models of multiple sclerosis: neurodegeneration and demyelination in mice infected with Theiler’s virus. Prog Neurobiol 101–102:46–64
28. Miller SD, Vanderlugt CL, Begolka WS, Pao W, Yauch RL, Neville KL, Katz-Levy Y, Carrizosa A, Kim BS (1997) Persistent infection with Theiler’s virus leads to CNS autoimmunity via epitope spreading. Nat Med 3:1133–1136
29. Mogensen TH, Melchjorsen J, Larsen CS, Paludan SR (2010) Innate immune recognition and activation during HIV infection. Retrovirology 7:54
30. Murray PD, Krivacic K, Chernosky A, Wei T, Ransohoff RM, Rodriguez M (2000) Biphasic and regionally-restricted chemokine expression in the central nervous system in the Theiler’s virus model of multiple sclerosis. J Neurovirol 6(Suppl 1):S44–S52
31. Olson JK, Girvin AM, Miller SD (2001) Direct activation of innate and antigen-presenting functions of microglia following infection with Theiler’s virus. J Virol 75:9780–9789
32. Olson JK, Miller SD (2004) Microglia initiate central nervous system innate and adaptive immune responses through multiple TLRs. J Immunol 173:3916–3924
33. Olson JK, Miller SD (2009) The innate immune response affects the development of the autoimmune response in Theiler’s virus-induced demyelinating disease. J Immunol 182:5712–5722
34. Pachner AR, Brady J, Narayan K (2007a) Antibody-secreting cells in the central nervous system in an animal model of MS: phenotype, association with disability, and in vitro production of antibody. J Neuroimmunol 190:112–120
35. Pachner AR, Li L, Lagunoff D (2011) Plasma cells in the central nervous system in the Theiler’s virus model of multiple sclerosis. J Neuroimmunol 232:35–40
36. Pachner AR, Li L, Narayan K (2007b) Intrathecal antibody production in an animal model of multiple sclerosis. J Neuroimmunol 185:57–63
37. Raddatz BB, Hansmann F, Spitzbarth I, Kalkuhl A, Deschl U, Baumgartner W, Ulrich R (2014) Transcriptomic meta-analysis of multiple sclerosis and its experimental models. PLoS One 9:e86643
38. Richards MH, Getts MT, Podojil JR, Jin YH, Kim BS, Miller SD (2011) Virus expanded regulatory T cells control disease severity in the Theiler’s virus mouse model of MS. J Autoimmun 36:142–154
39. Rosenberg GA (2002) Matrix metalloproteinases in neuroinflammation. Glia 39:279–291
40. Sato S, Reiner SL, Jensen MA, Roos RP (1997) Central nervous system cytokine mRNA expression following Theiler’s murine encephalomyelitis virus infection. J Neuroimmunol 76:213–223
41. Sorgeloos F, Jha BK, Silverman RH, Michiels T (2013) Evasion of antiviral innate immunity by Theiler’s virus L* protein through direct inhibition of RNase L. PLoS Pathog 9:e1003474
42. Stavrou S, Feng Z, Lemon SM, Roos RP (2010) Different strains of Theiler’s murine encephalomyelitis virus antagonize different sites in the type I interferon pathway. J Virol 84:9181–9189
43. Stomrud E, Bjorkqvist M, Janciauskiene S, Minthon L, Hansson O (2010) Alterations of matrix metalloproteinases in the healthy elderly with increased risk of prodromal Alzheimer’s disease. Alzheimers Res Ther 2:20
44. Tsunoda I, Iwasaki Y, Terunuma H, Sako K, Ohara Y (1996) A comparative study of acute and chronic diseases induced by two subgroups of Theiler’s murine encephalomyelitis virus. Acta Neuropathol 91:595–602
45. Ulrich R, Kalkuhl A, Deschl U, Baumgartner W (2010) Machine learning approach identifies new pathways associated with demyelination in a viral model of multiple sclerosis. J Cell Mol Med 14:434–448
46. Virgin HW, Wherry EJ, Ahmed R (2009) Redefining chronic viral infection. Cell 138:30–50