Major histocompatibility complex-dependent cytotoxic T lymphocyte repertoire and functional avidity contribute to strain-specific disease susceptibility after murine respiratory syncytial virus infection

Journal of Virology

Volumn 85, Issue 19, 2011, Pages 10135-10143

  Jessen, Birthe ^a   Faller, Simone ^a   Krempl, Christine D ^b   Ehl, Stephan ^a  

^a UNIVERSITY OF FREIBURG   (Germany)

^b UNIVERSITY OF WÜRZBURG   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

EPITOPE;

ALLELE; ANIMAL CELL; ANIMAL TISSUE; ARTICLE; BAGG ALBINO MOUSE; BINDING AFFINITY; C57BL 6 MOUSE; CD8+ T LYMPHOCYTE; CELLULAR IMMUNITY; CONGENIC STRAIN; CONTROLLED STUDY; CYTOLYSIS; CYTOTOXIC T LYMPHOCYTE; DISEASE PREDISPOSITION; GENETIC SUSCEPTIBILITY; IMMUNOPATHOLOGY; MAJOR HISTOCOMPATIBILITY COMPLEX; MATING; MOUSE; MOUSE STRAIN; NONHUMAN; PNEUMONIA; PRIORITY JOURNAL; RESPIRATORY SYNCYTIAL PNEUMOVIRUS; RESPIRATORY SYNCYTIAL VIRUS INFECTION; T CELL DEPLETION; T LYMPHOCYTE ACTIVATION; VIRUS MUTANT; WEIGHT REDUCTION;

ANIMALS; DISEASE MODELS, ANIMAL; DISEASE SUSCEPTIBILITY; EPITOPES, T-LYMPHOCYTE; H-2 ANTIGENS; MICE; MICE, INBRED BALB C; MICE, INBRED C57BL; RESPIRATORY SYNCYTIAL VIRUS INFECTIONS; RESPIRATORY SYNCYTIAL VIRUSES; RODENT DISEASES; T-LYMPHOCYTES, CYTOTOXIC;

MURINAE; MUS; RESPIRATORY SYNCYTIAL VIRUS; RICE STRIPE VIRUS;

EID: 80053934256     PISSN: 0022538X     EISSN: 10985514     Source Type: Journal    
DOI: 10.1128/JVI.00816-11     Document Type: Article

References (57)

1. Amanatidou, V., S. Apostolakis, and D. A. Spandidos. 2009. Genetic diversity of the host and severe respiratory syncytial virus-induced lower respiratory tract infection. Pediatr. Infect. Dis. J. 28:135-410.
2. Aung, S., J. A. Rutigliano, and B. S. Graham. 2001. Alternative mechanisms of respiratory syncytial virus clearance in perforin knockout mice lead to enhanced disease. J. Virol. 75:9918-9924.
3. Billam, P., et al. 2011. T cell receptor clonotype influences epitope hierarchy in the CD8+ T cell response to respiratory syncytial virus infection. J. Biol. Chem. 286:4829-4841.
4. Brandt, C. D., et al. 1973. Epidemiology of respiratory syncytial virus infection in Washington, D.C. 3. Composite analysis of eleven consecutive yearly epidemics. Am. J. Epidemiol. 98:355-364.
5. Cannon, M. J., P. J. Openshaw, and B. A. Askonas. 1988. Cytotoxic T cells clear virus but augment lung pathology in mice infected with respiratory syncytial virus. J. Exp. Med. 168:1163-1168.
6. Carrington, M., et al. 1999. HLA and HIV-1: heterozygote advantage and B*35-Cw*04 disadvantage. Science 283:1748-1752.
7. Chavez-Bueno, S., A. Mejias, H. S. Jafri, and O. Ramilo. 2005. Respiratory syncytial virus: old challenges and new approaches. Pediatr. Ann. 34:62-68.
8. Choi, E. H., H. J. Lee, T. Yoo, and S. J. Chanock. 2002. A common haplotype of interleukin-4 gene IL4 is associated with severe respiratory syncytial virus disease in Korean children. J. Infect. Dis. 186:1207-1211.
9. Crowe, C. R., et al. 2009. Critical role of IL-17RA in immunopathology of influenza infection. J. Immunol. 183:5301-5310.
10. de Saint Basile, G., G. Menasche, and A. Fischer. 2010. Molecular mechanisms of biogenesis and exocytosis of cytotoxic granules. Nat. Rev. Immunol. 10:568-579.
11. El Saleeby, C. M., J. Suzich, M. E. Conley, and J. P. DeVincenzo. 2004. Quantitative effects of palivizumab and donor-derived T cells on chronic respiratory syncytial virus infection, lung disease, and fusion glycoprotein amino acid sequences in a patient before and after bone marrow transplantation. Clin. Infect. Dis. 39:e17-e20.
12. Fishaut, M., D. Tubergen, and K. McIntosh. 1980. Cellular response to respiratory viruses with particular reference to children with disorders of cell-mediated immunity. J. Pediatr. 96:179-186.
13. Fulton, R. B., D. K. Meyerholz, and S. M. Varga. 2010. Foxp3+ CD4 regulatory T cells limit pulmonary immunopathology by modulating the CD8 T cell response during respiratory syncytial virus infection. J. Immunol. 185:2382-2392.
14. Graham, B. S., L. A. Bunton, P. F. Wright, and D. T. Karzon. 1991. Role of T lymphocyte subsets in the pathogenesis of primary infection and rechallenge with respiratory syncytial virus in mice. J. Clin. Invest. 88:1026-1033.
15. Graham, B. S., T. R. Johnson, and R. S. Peebles. 2000. Immune-mediated disease pathogenesis in respiratory syncytial virus infection. Immunopharmacology 48:237-247.
16. Graham, B. S., M. D. Perkins, P. F. Wright, and D. T. Karzon. 1988. Primary respiratory syncytial virus infection in mice. J. Med. Virol. 26:153-162.
17. Hall, C. B. 1999. Respiratory syncytial virus: a continuing culprit and conundrum. J. Pediatr. 135:2-7.
18. Hall, C. B., et al. 1986. Respiratory syncytial viral infection in children with compromised immune function. N. Engl. J. Med. 315:77-81.
19. Hull, J., A. Thomson, and D. Kwiatkowski. 2000. Association of respiratory syncytial virus bronchiolitis with the interleukin 8 gene region in UK families. Thorax 55:1023-1027.
20. Hussell, T., et al. 1998. Host genetic determinants of vaccine-induced eosinophilia during respiratory syncytial virus infection. J. Immunol. 161:6215-6222.
21. Inoue, Y., et al. 2007. CD14-550 C/T, which is related to the serum level of soluble CD14, is associated with the development of respiratory syncytial virus bronchiolitis in the Japanese population. J. Infect. Dis. 195:1618-1624.
22. Isaacs, D., C. J. Taylor, A. Ting, and A. J. McMichael. 1989. HLA class I antigens in severe RSV bronchiolitis. Tissue Antigens 34:210-212.
23. Janssen, R., et al. 2007. Genetic susceptibility to respiratory syncytial virus bronchiolitis is predominantly associated with innate immune genes. J. Infect. Dis. 196:826-834.
24. Johnson, T. R., S. M. Varga, T. J. Braciale, and B. S. Graham. 2004. Vbeta14(+) T cells mediate the vaccine-enhanced disease induced by immunization with respiratory syncytial virus (RSV) G glycoprotein but not with formalin-inactivated RSV. J. Virol. 78:8753-8760.
25. Jordan, M. B., D. Hildeman, J. Kappler, and P. Marrack. 2004. An animal model of hemophagocytic lymphohistiocytosis (HLH): CD8+ T cells and interferon gamma are essential for the disorder. Blood 104:735-743.
26. Kappler, J. W., U. Staerz, J. White, and P. C. Marrack. 1988. Self-tolerance eliminates T cells specific for Mls-modified products of the major histocompatibility complex. Nature 332:35-40.
27. Kaslow, R. A., et al. 1996. Influence of combinations of human major histocompatibility complex genes on the course of HIV-1 infection. Nat. Med. 2:405-411.
28. Kuball, J., et al. 2009. Increasing functional avidity of TCR-redirected T cells by removing defined N-glycosylation sites in the TCR constant domain. J. Exp. Med. 206:463-475.
29. Kulkarni, A. B., et al. 1995. Cytotoxic T cells specific for a single peptide on the M2 protein of respiratory syncytial virus are the sole mediators of resistance induced by immunization with M2 encoded by a recombinant vaccinia virus. J. Virol. 69:1261-2364.
30. Kulkarni, A. B., M. Connors, C. Y. Firestone, H. C. Morse III, and B. R. Murphy. 1993. The cytolytic activity of pulmonary CD8+ lymphocytes, induced by infection with a vaccinia virus recombinant expressing the M2 protein of respiratory syncytial virus (RSV), correlates with resistance to RSV infection in mice. J. Virol. 67:1044-1049.
31. Leist, T., A. Althage, E. Haenseler, H. Hengartner, and R. M. Zinkernagel. 1989. Major histocompatibility complex-linked susceptibility or resistance to disease caused by a noncytopathic virus varies with the disease parameter evaluated. J. Exp. Med. 170:269-277.
32. Lukens, M. V., et al. 2006. Characterization of the CD8+ T cell responses directed against respiratory syncytial virus during primary and secondary infection in C57BL/6 mice. Virology 352:157-168.
33. Mejias, A., et al. 2004. Anti-respiratory syncytial virus (RSV) neutralizing antibody decreases lung inflammation, airway obstruction, and airway hyperresponsiveness in a murine RSV model. Antimicrob. Agents Chemother. 48:1811-2182.
34. Messaoudi, I., J. A. Guevara Patino, R. Dyall, J. LeMaoult, and J. Nikolich-Zugich. 2002. Direct link between MHC polymorphism, T cell avidity, and diversity in immune defense. Science 298:1797-1800.
35. Miyairi, I., and J. P. DeVincenzo. 2008. Human genetic factors and respiratory syncytial virus disease severity. Clin. Microbiol. Rev. 21:686-703.
36. Moskophidis, D., et al. 1995. Role of virus and host variables in virus persistence or immunopathological disease caused by a non-cytolytic virus. J. Gen. Virol. 76(Pt. 2):381-391.
37. Neumann-Haefelin, C., et al. 2006. Dominant influence of an HLA-B27 restricted CD8+ T cell response in mediating HCV clearance and evolution. Hepatology 43:563-572.
38. Nicholas, J. A., K. L. Rubino, M. E. Levely, E. G. Adams, and P. L. Collins. 1990. Cytolytic T-lymphocyte responses to respiratory syncytial virus: effector cell phenotype and target proteins. J. Virol. 64:4232-4241.
39. Openshaw, P. J., K. Anderson, G. W. Wertz, and B. A. Askonas. 1990. The 22,000-kilodalton protein of respiratory syncytial virus is a major target for Kd-restricted cytotoxic T lymphocytes from mice primed by infection. J. Virol. 64:1683-1689.
40. Ostler, T., T. Hussell, C. D. Surh, P. Openshaw, and S. Ehl. 2001. Long-term persistence and reactivation of T cell memory in the lung of mice infected with respiratory syncytial virus. Eur. J. Immunol. 31:2574-2582.
41. Ostler, T., et al. 2001. An improved protocol for measuring cytotoxic T cell activity in anatomic compartments with low cell numbers. J. Immunol. Methods 257:155-161.
42. Pachlopnik Schmid, J., et al. 2009. Neutralization of IFNgamma defeats haemophagocytosis in LCMV-infected perforin- and Rab27a-deficient mice. EMBO Mol. Med. 1:112-124.
43. Pereyra, F., et al. 2010. The major genetic determinants of HIV-1 control affect HLA class I peptide presentation. Science 330:1551-1557.
44. Prince, G. A., R. L. Horswood, J. Berndt, S. C. Suffin, and R. M. Chanock. 1979. Respiratory syncytial virus infection in inbred mice. Infect. Immun. 26:764-766.
45. Puthothu, B., M. Krueger, J. Forster, and A. Heinzmann. 2006. Association between severe respiratory syncytial virus infection and IL13/IL4 haplotypes. J. Infect. Dis. 193:438-441.
46. Ruckwardt, T. J., K. L. Bonaparte, M. C. Nason, and B. S. Graham. 2009. Regulatory T cells promote early influx of CD8+ T cells in the lungs of respiratory syncytial virus-infected mice and diminish immunodominance disparities. J. Virol. 83:3019-3028.
47. Ruckwardt, T. J., et al. 2010. Responses against a subdominant CD8+ T cell epitope protect against immunopathology caused by a dominant epitope. J. Immunol. 185:4673-4680.
48. Rutigliano, J. A., M. T. Rock, A. K. Johnson, J. E. Crowe, Jr., and B. S. Graham. 2005. Identification of an H-2D(b)-restricted CD8+ cytotoxic T lymphocyte epitope in the matrix protein of respiratory syncytial virus. Virology 337:335-343.
49. Rutigliano, J. A., T. J. Ruckwardt, J. E. Martin, and B. S. Graham. 2007. Relative dominance of epitope-specific CD8+ T cell responses in an F1 hybrid mouse model of respiratory syncytial virus infection. Virology 362: 314-319.
50. Slifka, M. K., and J. L. Whitton. 2001. Functional avidity maturation of CD8(+) T cells without selection of higher affinity TCR. Nat. Immunol. 2:711-717.
51. Stark, J. M., et al. 2002. Genetic susceptibility to respiratory syncytial virus infection in inbred mice. J. Med. Virol. 67:92-100.
52. Tal, G., et al. 2004. Association between common Toll-like receptor 4 mutations and severe respiratory syncytial virus disease. J. Infect. Dis. 189:2057-2063.
53. Trachtenberg, E., et al. 2003. Advantage of rare HLA supertype in HIV disease progression. Nat. Med. 9:928-935.
54. Tregoning, J. S., et al. 2010. Genetic susceptibility to the delayed sequelae of neonatal respiratory syncytial virus infection is MHC dependent. J. Immunol. 185:5384-5391.
55. Vallbracht, S., et al. 2007. Influence of a single viral epitope on T cell response and disease after infection of mice with respiratory syncytial virus. J. Immunol. 179:8264-8273.
56. Vallbracht, S., H. Unsold, and S. Ehl. 2006. Functional impairment of cytotoxic T cells in the lung airways following respiratory virus infections. Eur. J. Immunol. 36:1434-1442.
57. Zeng, R., C. Li, N. Li, L. Wei, and Y. Cui. 2011. The role of cytokines and chemokines in severe respiratory syncytial virus infection and subsequent asthma. Cytokine 53:1-7.