Fulminant lymphocytic choriomeningitis virus-induced inflammation of the cns involves a cytokine-chemokine-cytokine-chemokine cascade

Journal of Immunology

Volumn 182, Issue 2, 2009, Pages 1079-1087

  Christensen, Jeanette E ^a   Simonsen, Stine ^a   Fenger, Christina ^b   Sørensen, Maria R ^a   Moos, Torben ^c   Christensen, Jan P ^a   Finsen, Bente ^b   Thomsen, Allan R ^a  

^a UNIVERSITY OF COPENHAGEN   (Denmark)

^b UNIVERSITY OF SOUTHERN DENMARK   (Denmark)

^c AALBORG UNIVERSITY   (Denmark)

Author keywords

[No Author keywords available]

Indexed keywords

CHEMOKINE; CHEMOKINE RECEPTOR CXCR3; CYTOKINE; GAMMA INTERFERON INDUCIBLE PROTEIN 10; AUTACOID; CXCL10 PROTEIN, MOUSE; GLYCOPROTEIN; GLYCOPROTEIN PEPTIDE 33 41, LYMPHOCYTIC CHORIOMENINGITIS VIRUS; GLYCOPROTEIN PEPTIDE 33-41, LYMPHOCYTIC CHORIOMENINGITIS VIRUS; INTERFERON; PEPTIDE FRAGMENT; VIRUS ANTIGEN; VIRUS PROTEIN;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BONE MARROW; CD8+ T LYMPHOCYTE; CELLULAR IMMUNITY; CHIMERA; CONTROLLED STUDY; FEMALE; LYMPHOCYTIC CHORIOMENINGITIS VIRUS; MICROGLIA; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; VIRUS ENCEPHALITIS; VIRUS IMMUNITY; ANIMAL; BIOSYNTHESIS; C57BL MOUSE; COMPARATIVE STUDY; GENETICS; IMMUNOLOGY; INTRACEREBROVENTRICULAR DRUG ADMINISTRATION; METABOLISM; MOUSE MUTANT; NUDE MOUSE; PATHOLOGY; PHYSIOLOGY; SIGNAL TRANSDUCTION; T LYMPHOCYTE SUBPOPULATION; TRANSGENIC MOUSE; UPREGULATION; VIROLOGY; VIRUS MENINGITIS;

ANIMALS; ANTIGENS, VIRAL; CHEMOKINE CXCL10; CHEMOKINES; CYTOKINES; FEMALE; GLYCOPROTEINS; INFLAMMATION MEDIATORS; INJECTIONS, INTRAVENTRICULAR; INTERFERON TYPE I; LYMPHOCYTIC CHORIOMENINGITIS; LYMPHOCYTIC CHORIOMENINGITIS VIRUS; MICE; MICE, INBRED C57BL; MICE, KNOCKOUT; MICE, NUDE; MICE, TRANSGENIC; PEPTIDE FRAGMENTS; SIGNAL TRANSDUCTION; T-LYMPHOCYTE SUBSETS; UP-REGULATION; VIRAL PROTEINS;

EID: 60549116578     PISSN: 00221767     EISSN: 15506606     Source Type: Journal    
DOI: 10.4049/jimmunol.182.2.1079     Document Type: Article

References (48)

1. Medawar, P. B. 1948. Immunity to homologous grafted skin, III: the fate of skin homografts transplanted to the brain, to subcutanous tissue, and to anterior chamber of the eye. Br. J. Exp. Pathol. 29: 58-69.
2. Engelhardt, B., and R. M. Ransohoff. 2005. The ins and outs of T-lymphocyte trafficking to the CNS: anatomical sites and molecular mechanisms. Trends Immunol. 26: 485-495.
3. Carson, M. J., J. M. Doose, B. Melchior, C. D. Schmid, and C. C. Ploix. 2006. CNS immune privilege: hiding in plain sight. Immunol. Rev. 213: 48-65.
4. Matyszak, M. K., and V. H. Perry. 1996. The potential role of dendritic cells in immune-mediated inflammatory diseases in the central nervous system. Neuroscience 74: 599-608.
5. Hickey, W. F. 2001. Basic principles of immunological surveillance of the normal central nervous system. Glia 36: 118-124.
6. Butcher, E. C. 1991. Leukocyte-endothelial cell recognition: three (or more) steps to specificity and diversity. Cell 67: 1033-1036.
7. Thomsen, A. R., A. Nansen, A. N. Madsen, C. Bartholdy, and J. P. Christensen. 2003. Regulation of T cell migration during viral infection: role of adhesion molecules and chemokines. Immunol. Lett. 85: 119-127.
8. Franciotta, D., G. Martino, E. Zardini, R. Furlan, R. Bergamaschi, L. Andreoni, and V. Cosi. 2001. Serum and CSF levels of MCP-1 and IP-10 in multiple sclerosis patients with acute and stable disease and undergoing immunomodulatory therapies. J. Neuroimmunol. 115: 192-198.
9. Sorensen, T. L., M. Tani, J. Jensen, V. Pierce, C. Lucchinetti, V. A. Folcik, S. Qin, J. Rottman, F. Sellebjerg, R. M. Strieter, et al. 1999. Expression of specific chemokines and chemokine receptors in the central nervous system of multiple sclerosis patients. J. Clin. Invest. 103: 807-815.
10. + T cells are increased in multiple sclerosis and their ligands MIP-1α and IP-10 are expressed in demyelinating brain lesions. Proc. Natl. Acad. Sci. USA 96: 6873-6878.
11. Sorensen, T. L., C. Trebst, P. Kivisakk, K. L. Klaege, A. Majmudar, R. Ravid, H. Lassmann, D. B. Olsen, R. M. Strieter, R. M. Ransohoff, and F. Sellebjerg. 2002. Multiple sclerosis: a study of CXCL10 and CXCR3 co-localization in the inflamed central nervous system. J. Neuroimmunol. 127: 59-68.
12. Hsieh, M. F., S. L. Lai, J. P. Chen, J. M. Sung, Y. L. Lin, B. A. Wu-Hsieh, C. Gerard, A. Luster, and F. Liao. 2006. Both CXCR3 and CXCL10/IFN-inducible protein 10 are required for resistance to primary infection by dengue virus. J. Immunol. 177: 1855-1863.
13. + T-cell recruitment and control of West Nile virus encephalitis. J. Virol. 79: 11457-11466.
14. Bergmann, C. C., T. E. Lane, and S. A. Stohlman. 2006. Coronavirus infection of the central nervous system: host-virus stand-off. Nat. Rev. Microbiol. 4: 121-132.
15. Christensen, J. E., A. Nansen, T. Moos, B. Lu, C. Gerard, J. P. Christensen, and A. R. Thomsen. 2004. Efficient T-cell surveillance of the CNS requires expression of the CXC chemokine receptor 3. J. Neurosci. 24: 4849-4858.
16. + effector T cells involved in immune surveillance of the lymphocytic choriomeningitis virus-infected central nervous system. J. Immunol. 176: 4235-4243.
17. + T cell-mediated inflammation in the central nervous system of virus-infected mice. J. Immunol. 175: 1767-1775.
18. Hotchin, J., and H. Weigand. 1961. The effects of pretreatment with x-rays on the pathogenesis of lymphocytic choriomeningitis in mice, I: host survival, virus multiplication and leukocytosis. J. Immunol. 87: 675-681.
19. Cole, G. A., N. Nathanson, and R. A. Prendergast. 1972. Requirement for theta-bearing cells in lymphocytic choriomeningitis virus-induced central nervous system disease. Nature 238: 335-337.
20. + immune T cells. Cell Immunol. 107: 8-14.
21. + T cells. Immunol. Today 11: 55-59.
22. + T cells in cell-mediated immunity to LCMV: studies in MHC class I and class II deficient mice. Scand. J. Immunol. 40: 373-382.
23. Pircher, H., K. Burki, R. Lang, H. Hengartner, and R. M. Zinkernagel. 1989. Tolerance induction in double specific T-cell receptor transgenic mice varies with antigen. Nature 342: 559-561.
24. Christoffersen, P. J., M. Volkert, and J. Rygaard. 1976. Immunological unresponsiveness of nude mice to LCM virus infection. Acta Pathol. Microbiol. Scand. 84C: 520-523.
25. Blattman, J. N., R. Antia, D. J. Sourdive, X. Wang, S. M. Kaech, K. Murali-Krishna, J. D. Altman, and R. Ahmed. 2002. Estimating the precursor frequency of naive antigen-specific CD8 T cells. J. Exp. Med. 195: 657-664.
26. Pfaffl, M. W. 2001. A new mathematical model for relative quantification in real-time RT-PCR. Nucleic Acids Res. 29: e45.
27. Lambertsen, K. L., R. Gregersen, N. Drojdahl, T. Owens, and B. Finsen. 2001. A specific and sensitive method for visualization of tumor necrosis factor in the murine central nervous system. Brain Res. 7: 175-191.
28. Kerr, I. M., and R. E. Brown. 1978. pppA2′p5′A2′ p5′ A: an inhibitor of protein synthesis synthesized with an enzyme fraction from interferon-treated cells. Proc. Natl. Acad. Sci. USA 75: 256-260.
29. Zhou, A., J. Paranjape, T. L. Brown, H. Nie, S. Naik, B. Dong, A. Chang, B. Trapp, R. Fairchild, C. Colmenares, and R. H. Silverman. 1997. Interferon action and apoptosis are defective in mice devoid of 2′,5′- oligoadenylate-dependent RNase L. EMBO J. 16: 6355-6363.
30. + T cells increase during viral infection and migrate to sites of infection. Eur. J. Immunol. 30: 1797-1806.
31. Nansen, A., J. P. Christensen, C. Ropke, O. Marker, A. Scheynius, and A. R. Thomsen. 1998. Role of interferon-γ in the pathogenesis of LCMV-induced meningitis: unimpaired leucocyte recruitment, but deficient macrophage activation in interferon-γ knock-out mice. J. Neuroimmunol. 86: 202-212.
32. Madsen, A. N., A. Nansen, J. P. Christensen, and A. R. Thomsen. 2003. Role of macrophage inflammatory protein-1α in T-cell-mediated immunity to viral infection. J. Virol. 77: 12378-12384.
33. Christen, U., D. B. McGavern, A. D. Luster, M. G. von Herrath, and M. B. Oldstone. 2003. Among CXCR3 chemokines, IFN-γ-inducible protein of 10 kDa (CXC chemokine ligand (CXCL) 10) but not monokine induced by IFN-γ (CXCL9) imprints a pattern for the subsequent development of autoimmune disease. J. Immunol. 171: 6838-6845.
34. Prakash, A., E. Smith, C. K. Lee, and D. E. Levy. 2005. Tissue-specific positive feedback requirements for production of type I interferon following virus infection. J. Biol. Chem. 280: 18651-18657.
35. Asensio, V. C., C. Kincaid, and I. L. Campbell. 1999. Chemokines and the inflammatory response to viral infection in the central nervous system with a focus on lymphocytic choriomeningitis virus. J. Neurovirol. 5: 65-75.
36. Thomsen, A. R., M. Volkert, and O. Marker. 1979. The timing of the immune response in relation to virus growth determines the outcome of the LCM infection. Acta Pathol. Microbiol. Scand. 87C: 47-54.
37. Kawai, T., and S. Akira. 2006. Innate immune recognition of viral infection. Nat. Immunol. 7: 131-137.
38. Prinz, M., H. Schmidt, A. Mildner, K. P. Knobeloch, U. K. Hanisch, J. Raasch, D. Merkler, C. Detje, I. Gutcher, J. Mages, et al. 2008. Distinct and nonredundant in vivo functions of IFNAR on myeloid cells limit autoimmunity in the central nervous system. Immunity 28: 675-686.
39. Teige, I., A. Treschow, A. Teige, R. Mattsson, V. Navikas, T. Leanderson, R. Holmdahl, and S. Issazadeh-Navikas. 2003. IFN-β gene deletion leads to augmented and chronic demyelinating experimental autoimmune encephalomyelitis. J. Immunol. 170: 4776-4784.
40. Ousman, S. S., J. Wang, and I. L. Campbell. 2005. Differential regulation of interferon regulatory factor (IRF)-7 and IRF-9 gene expression in the central nervous system during viral infection. J. Virol. 79: 7514-7527.
41. McKimmie, C. S., N. Johnson, A. R. Fooks, and J. K. Fazakerley. 2005. Viruses selectively upregulate Toll-like receptors in the central nervous system. Biochem. Biophys. Res. Commun. 336: 925-933.
42. Asensio, V. C., and I. L. Campbell. 1997. Chemokine gene expression in the brains of mice with lymphocytic choriomeningitis. J. Virol. 71: 7832-7840.
43. Doherty, P. C., and R. M. Zinkernagel. 1974. T-cell-mediated immunopathology in viral infections. Transplant. Rev. 19: 89-120.
44. Kagi, D., B. Ledermann, K. Burki, P. Seiler, B. Odermatt, K. J. Olsen, E. R. Podack, R. M. Zinkernagel, and H. Hengartner. 1994. Cytotoxicity mediated by T cells and natural killer cells is greatly impaired in perforin-deficient mice. Nature 369: 31-37.
45. + T cells mediate fatal lymphocytic choriomeningitis despite impaired cytokine production. J. Virol. 80: 1222-1230.
46. Delhaye, S., S. Paul, G. Blakqori, M. Minet, F. Weber, P. Staeheli, and T. Michiels. 2006. Neurons produce type I interferon during viral encephalitis. Proc. Natl. Acad. Sci. USA 103: 7835-7840.
47. Carpentier, P. A., M. T. Getts, and S. D. Miller. 2008. Pro-inflammatory functions of astrocytes correlate with viral clearance and strain-dependent protection from TMEV-induced demyelinating disease. Virology 375: 24-36.
48. Zhou, S., A. Halle, E. A. Kurt-Jones, A. M. Cerny, E. Porpiglia, M. Rogers, D. T. Golenbock, and R. W. Finberg. 2008. Lymphocytic Choriomeningitis Virus (LCMV) infection of CNS glial cells results in TLR2-MyD88/Mal-dependent inflammatory responses. J. Neuroimmunol. 194: 70-82.