Sequential polymicrobial infections lead to CNS inflammatory disease: Possible involvement of bystander activation in heterologous immunity

Journal of Neuroimmunology

Volumn 188, Issue 1-2, 2007, Pages 22-33

  Tsunoda, Ikuo ^a   Libbey, Jane E ^a   Fujinami, Robert S ^a  

^a UNIVERSITY OF UTAH SCHOOL OF MEDICINE   (United States)

Author keywords

Autoimmunity; CNS demyelinating autoimmune diseases; Experimental autoimmune encephalomyelitis; IL 12; Multiple sclerosis; Theiler's murine encephalomyelitis virus

Indexed keywords

CD3 ANTIGEN; KI 67 ANTIGEN; PROTEOLIPID PROTEIN;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ANTIBODY RESPONSE; ARTICLE; AUTOIMMUNE DISEASE; AUTOIMMUNITY; CELL INFILTRATION; CENTRAL NERVOUS SYSTEM; CENTRAL NERVOUS SYSTEM INFECTION; CONTROLLED STUDY; CYTOMEGALOVIRUS; ENCEPHALOMYELITIS; FEMALE; LYMPHOCYTIC CHORIOMENINGITIS VIRUS; MOUSE; MOUSE STRAIN; MULTIPLE SCLEROSIS; MURINE CYTOMEGALOVIRUS; NONHUMAN; PATHOLOGY; PRIORITY JOURNAL; STATISTICAL SIGNIFICANCE; T LYMPHOCYTE; VACCINIA VIRUS; VIRUS INFECTION;

ANIMALS; AUTOIMMUNE DISEASES OF THE NERVOUS SYSTEM; BYSTANDER EFFECT; CELL PROLIFERATION; CENTRAL NERVOUS SYSTEM INFECTIONS; DISEASE MODELS, ANIMAL; ENCEPHALOMYELITIS, AUTOIMMUNE, EXPERIMENTAL; FEMALE; GENE EXPRESSION REGULATION; IMMUNOLOGIC MEMORY; LYMPHOCYTE ACTIVATION; LYMPHOCYTIC CHORIOMENINGITIS VIRUS; MICE; MUROMEGALOVIRUS; MYELIN PROTEOLIPID PROTEIN; RECOMBINANT PROTEINS; T-LYMPHOCYTES; VACCINIA VIRUS;

EID: 34547107306     PISSN: 01655728     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.jneuroim.2007.05.012     Document Type: Article

References (66)

1. Alotaibi S., Kennedy J., Tellier R., Stephens D., and Banwell B. Epstein-Barr virus in pediatric multiple sclerosis. JAMA 291 (2004) 1875-1879
2. Banwell B.L. Pediatric multiple sclerosis. Curr. Neurol. Neurosci. Rep. 4 (2004) 245-252
3. Barnett L.A., Whitton J.L., Wada Y., and Fujinami R.S. Enhancement of autoimmune disease using recombinant vaccinia virus encoding myelin proteolipid protein [published erratum appears in J. Neuroimmunol. 48:120, 1993]. J. Neuroimmunol. 44 (1993) 15-25
4. Biron C.A. Initial and innate responses to viral infections-pattern setting in immunity or disease. Curr. Opin. Microbiol. 2 (1999) 374-381
5. Biron C.A., Nguyen K.B., Pien G.C., Cousens L.P., and Salazar-Mather T.P. Natural killer cells in antiviral defense: Function and regulation by innate cytokines. Annu. Rev. Immunol. 17 (1999) 189-220
6. Blinzinger K., Hochstein-Mintzel V., and Anzil A.P. Experimental vaccinia virus meningoencephalitis in adult albino mice: Virological, light microscopic and ultrastructural studies. Acta Neuropathol. (Berl) 40 (1977) 193-205
7. Bosse D.C., Campbell Jr. W.G., and Cassell W.A. Light and electron microscopic studies of the pathogenesis of vaccinia virus infection in mouse brain. Proc. Soc. Exp. Biol. Med. 171 (1982) 72-78
8. Chen H.D., Fraire A.E., Joris I., Welsh R.M., and Selin L.K. Specific history of heterologous virus infections determines anti-viral immunity and immunopathology in the lung. Am. J. Pathol. 163 (2003) 1341-1355
9. Cheung K.-S., Li J.K.K., Falletta J.M., Wagner J.L., and Lang D.J. Murine cytomegalovirus infection: hematological, morphological, and functional study of lymphoid cells. Infect. Immun. 33 (1981) 239-249
10. +T cells based on α4 integrin expression. Int. Immunol. 8 (1996) 707-715
11. Constantinescu C.S., Wysocka M., Hilliard B., Ventura E.S., Lavi E., Trinchieri G., and Rostami A. Antibodies against IL-12 prevent superantigen-induced and spontaneous relapses of experimental autoimmune encephalomyelitis. J. Immunol. 161 (1998) 5097-5104
12. Davis L.E. Communicating hydrocephalus in newborn hamsters and cats following vaccinia virus infection. J. Neurosurg. 54 (1981) 767-772
13. Doherty P.C., and Zinkernagel R.M. Enhanced immunological surveillance in mice heterozygous at the H-2 gene complex. Nature 256 (1975) 50-52
14. Eisch A.J., and Mandyam C.D. Beyond BrdU: Basic and clinical implications for analysis of endogenous cell cycle proteins. In: Greer E.V. (Ed). Focus on Stem Cell Research (2004), Nova Science Publisher, Inc, Hauppauge, NY 111-142
15. Fujinami R.S., and Oldstone M.B.A. Amino acid homology between the encephalitogenic site of myelin basic protein and virus: Mechanism for autoimmunity. Science 230 (1985) 1043-1045
16. Ginsberg A.H., and Johnson K.P. Vaccinia virus meningitis in mice after intracerebral inoculation. Infect. Immun. 13 (1976) 1221-1227
17. Gran B., Zhang G.-X., and Rostami A. Role of the IL-12/IL-23 system in the regulation of T-cell responses in central nervous system inflammatory demyelination. Crit. Rev. Immunol. 24 (2004) 111-128
18. Grigoriadis N., and Hadjigeorgiou G.M. Virus-mediated autoimmunity in multiple sclerosis. J. Autoimmun. Dis. 3 (2006) 1
19. Haga I.R., and Bowie A.G. Evasion of innate immunity by vaccinia virus. Parasitology 130 (2005) S11-S25 (Suppl)
20. Inada T., and Mims C.A. Infection of mice with lactic dehydrogenase virus prevents development of experimental allergic encephalomyelitis. J. Neuroimmunol. 11 (1986) 53-56
21. Jee Y., and Matsumoto Y. Two-step activation of T cells, clonal expansion and subsequent Th1 cytokine production, is essential for the development of clinical autoimmune encephalomyelitis. Eur. J. Immunol. 31 (2001) 1800-1812
22. b H chain constant regions are derived from two distinct isotypic genes. Immunogenetics 29 (1989) 92-97
23. Karrer U., Oxenius A., Phillips R., and Klenerman P. Memory T cells: total recall or just a sense of déjà vu?. Nat. Immunol. 2 (2001) 991-993
24. + T cell memory: lifelong persistence of encephalitogenic T cell clones in healthy immune repertoires. J. Immunol. 175 (2005) 69-81
25. Kissler S., Anderton S.M., and Wraith D.C. Antigen-presenting cell activation: a link between infection and autoimmunity?. J. Autoimmun. 16 (2001) 303-308
26. Kosugi I., Kawasaki H., Arai Y., and Tsutsui Y. Innate immune responses to cytomegalovirus infection in the developing mouse brain and their evasion by virus-infected neurons. Am. J. Pathol. 161 (2002) 919-928
27. Kriesel J.D., and Sibley W.A. The case for rhinoviruses in the pathogenesis of multiple sclerosis. Mult. Scler. 11 (2005) 1-4
28. Libbey J.E., and Fujinami R.S. Are virus infections triggers for autoimmune disease?. Clin. Microbiol. Newsl. 24 (2002) 73-76
29. Lois C., and Alvarez-Buylla A. Proliferating subventricular zone cells in the adult mammalian forebrain can differentiate into neurons and glia. Proc. Natl. Acad. Sci. U. S. A. 90 (1993) 2074-2077
30. Lussier G. Effect of antithymocyte serum of murine cytomegalovirus emcephalitis in weanling mice. Rev. Can. Biol. 34 (1975) 1-10
31. Martin R.M., Brady J.L., and Lew A.M. The need for IgG2c specific antiserum when isotyping antibodies from C57BL/6 and NOD mice. J. Immunol. Methods 212 (1998) 187-192
32. Martin R.M., and Lew A.M. Is IgG2a a good Th1 marker in mice?. Immunol. Today 19 (1998) 49
33. Mason D.Y., Cordell J., Brown M., Pallesen G., Ralfkiaer E., Rothbard J., Crumpton M., and Gatter K.C. Detection of T cells in paraffin wax embedded tissue using antibodies against a peptide sequence from the CD3 antigen. J. Clin. Pathol. 42 (1989) 1194-1200
34. McCoy L., Tsunoda I., and Fujinami R.S. Multiple sclerosis and virus induced immune responses: Autoimmunity can be primed by molecular mimicry and augmented by bystander activation. Autoimmunity 39 (2006) 9-19
35. Monteyne P., Bihl F., Levillayer F., Brahic M., and Bureau J.-F. The Th1/Th2 balance does not account for the difference of susceptibility of mouse strains to Theiler's virus persistent infection. J. Immunol. 162 (1999) 7330-7334
36. Morshead C.M., Reynolds B.A., Craig C.G., McBurney M.W., Staines W.A., Morassutti D., Weiss S., and van der Kooy D. Neural stem cells in the adult mammalian forebrain: a relatively quiescent subpopulation of subependymal cells. Neuron 13 (1994) 1071-1082
37. Ohmori K., Hong Y., Fujiwara M., and Matsumoto Y. In situ demonstration of proliferating cells in the rat central nervous system during experimental autoimmune encephalomyelitis. Evidence suggesting that most infiltrating T cells do not proliferate in the target organ. Lab. Invest. 66 (1992) 54-62
38. Oldstone M.B.A., Tishon A., Geckeler R., Lewicki H., and Whitton J.L. A common antiviral cytotoxic T-lymphocyte epitope for diverse major histocompatibility complex haplotypes: implications for vaccination. Proc. Natl. Acad. Sci. U. S. A. 89 (1992) 2752-2755
39. Olson J.K., Eagar T.N., and Miller S.D. Functional activation of myelin-specific T cells by virus-induced molecular mimicry. J. Immunol. 169 (2002) 2719-2726
40. Petro T.M. Disparate expression of IL-12 by SJL/J and B10.S macrophages during Theiler's virus infection is associated with activity of TLR7 and mitogen-activated protein kinases. Microb. Infect. 7 (2005) 224-232
41. Razvi E.S., Jiang Z., Woda B.A., and Welsh R.M. Lymphocyte apoptosis during the silencing of the immune response to acute viral infections in normal, lpr, and Bcl-2-transgenic mice. Am. J. Pathol. 147 (1995) 79-91
42. Segal B.M., and Shevach E.M. IL-12 unmasks latent autoimmune disease in resistant mice. J. Exp. Med. 184 (1996) 771-775
43. Soekawa M., Morita C., Moriguchi R., and Nakamura M. Neurovirulence of vaccinia viruses for mice. Zentralbl. Bakteriol. [Orig. A] 226 (1974) 434-442
44. Takács K., Chandler P., and Altmann D.M. Relapsing and remitting experimental allergic encephalomyelitis: a focused response to the encephalitogenic peptide rather than epitope spread. Eur. J. Immunol. 27 (1997) 2927-2934
45. Theil D.J., Tsunoda I., Libbey J.E., Derfuss T.J., and Fujinami R.S. Alterations in cytokine but not chemokine mRNA expression during three distinct Theiler's virus infections. J. Neuroimmunol. 104 (2000) 22-30
46. Theil D.J., Tsunoda I., Rodriguez F., Whitton J.L., and Fujinami R.S. Viruses can silently prime for and trigger central nervous system autoimmune disease. J. Neurovirol. 7 (2001) 220-227
47. Tsunoda I., and Fujinami R.S. Theiler's murine encephalomyelitis virus. In: Ahmed R., and Chen I. (Eds). Persistent Viral Infections (1999), John Wiley & Sons, Ltd, England 517-536
48. Tsunoda I., McCright I.J., Kuang L.-Q., Zurbriggen A., and Fujinami R.S. Hydrocephalus in mice infected with a Theiler's murine encephalomyelitis virus variant. J. Neuropathol. Exp. Neurol. 56 (1997) 1302-1313
49. Tsunoda I., Kuang L.-Q., Tolley N.D., Whitton J.L., and Fujinami R.S. Enhancement of experimental allergic encephalomyelitis (EAE) by DNA immunization with myelin proteolipid protein (PLP) plasmid DNA. J. Neuropathol. Exp. Neurol. 57 (1998) 758-767
50. Tsunoda I., Tolley N.D., Theil D.J., Whitton J.L., Kobayashi H., and Fujinami R.S. Exacerbation of viral and autoimmune animal models for multiple sclerosis by bacterial DNA. Brain Pathol. 9 (1999) 481-493
51. S mouse strains. Brain Pathol. 10 (2000) 402-418
52. Tsunoda I., Wada Y., Libbey J.E., Cannon T.S., Whitby F.G., and Fujinami R.S. Prolonged gray matter disease without demyelination caused by Theiler's murine encephalomyelitis virus with a mutation in VP2 puff B. J. Virol. 75 (2001) 7494-7505
53. +cytotoxic T cells during Theiler's murine encephalomyelitis virus infection: Implications for autoimmunity. J. Virol. 76 (2002) 12834-12844
54. Tsunoda I., Kuang L.-Q., Libbey J.E., and Fujinami R.S. Axonal injury heralds virus-induced demyelination. Am. J. Pathol. 162 (2003) 1259-1269
55. Tsunoda I., Kuang L.-Q., Igenge I.Z.M., and Fujinami R.S. Converting relapsing remitting to secondary progressive experimental allergic encephalomyelitis (EAE) by ultraviolet B irradiation. J. Neuroimmunol. 160 (2005) 122-134
56. Tsunoda I., Libbey J.E., Kuang L.-Q., Terry E.J., and Fujinami R.S. Massive apoptosis in lymphoid organs in animal models for primary and secondary progressive multiple sclerosis. Am. J. Pathol. 167 (2005) 1631-1646
57. Tsunoda I., Tanaka T., Terry E.J., and Fujinami R.S. Contrasting roles for axonal degeneration in an autoimmune versus viral model for multiple sclerosis: When can axonal injury be beneficial?. Am. J. Pathol. 170 (2007) 214-226
58. Tsutsui Y., Kashiwai A., Kawamura N., Aiba-Masago S., and Kosugi I. Prolonged infection of mouse brain neurons with murine cytomegalovirus after pre- and perinatal infection. Arch. Virol. 140 (1995) 1725-1736
59. Tuft S. Polymicrobial infection and the eye. Br. J. Ophthalmol. 90 (2006) 257-258
60. van Pesch V., van Eyll O., and Michiels T. The leader protein of Theiler's virus inhibits immediate-early alpha/beta interferon production. J. Virol. 75 (2001) 7811-7817
61. von Herrath M.G., Fujinami R.S., and Whitton J.L. Microorganisms and autoimmunity: making the barren field fertile?. Nat. Rev. Microbiol. 1 (2003) 151-157
62. Wang L.-Y., and Fujinami R.S. Enhancement of EAE and induction of autoantibodies to T-cell epitopes in mice infected with a recombinant vaccinia virus encoding myelin proteolipid protein. J. Neuroimmunol. 75 (1997) 75-83
63. Welsh R.M., and Selin L.K. No one is naive: the significance of heterologous T-cell immunity. Nat. Rev. Immunol. 2 (2002) 417-426
64. Willenborg D.O., and Staykova M.A. Cytokines in the pathogenesis and therapy of autoimmune encephalomyelitis and multiple sclerosis. Adv. Exp. Med. Biol. 520 (2003) 96-119
65. Xu R., Johnson A.J., Liggitt D., and Bevan M.J. Cellular and humoral immunity against vaccinia virus infection of mice. J. Immunol. 172 (2004) 6265-6271
66. Yoshida H., Sumichika H., Hamano S., He X., Minamishima Y., Kimura G., and Nomoto K. Induction of apoptosis of T cells by infecting mice with murine cytomegalovirus. J. Virol. 69 (1995) 4769-4775