Viral escape by selection of cytotoxic T cell-resistant variants in influenza a virus pneumonia

Journal of Experimental Medicine

Volumn 191, Issue 11, 2000, Pages 1853-1867

  Price, Graeme E ^a   Ou, Rong ^a   Jiang, Hong ^a   Huang, Lei ^a   Moskophidis, Demetrius ^a  

^a MEDICAL COLLEGE OF GEORGIA   (United States)

Author keywords

CD8+ CTL escape variants; Influenza A virus; Influenza viral pneumonia; T cell receptor transgenic mice; Viral persistence

Indexed keywords

MAJOR HISTOCOMPATIBILITY ANTIGEN CLASS 1;

AMINO ACID SUBSTITUTION; ANIMAL EXPERIMENT; ANIMAL MODEL; ANTIGENIC VARIATION; ARTICLE; CONTROLLED STUDY; CYTOTOXIC T LYMPHOCYTE; GENE MUTATION; IMMUNE RESPONSE; IMMUNITY; IMMUNOCOMPETENCE; INFLUENZA VIRUS A; MOUSE; NONHUMAN; PERSISTENT VIRUS INFECTION; PRIORITY JOURNAL; VIRUS PNEUMONIA;

ANIMALS; ANTIGEN PRESENTATION; ANTIGENIC VARIATION; CELL DIVISION; CELL LINE; CYTOTOXICITY, IMMUNOLOGIC; DISEASE MODELS, ANIMAL; DOGS; EPITOPES, T-LYMPHOCYTE; HOMEODOMAIN PROTEINS; HUMANS; IMMUNOCOMPETENCE; INFLUENZA A VIRUS; INFLUENZA, HUMAN; MICE; MICE, TRANSGENIC; NUCLEOPROTEINS; PEPTIDE FRAGMENTS; PEPTIDES; PNEUMONIA, VIRAL; RNA-BINDING PROTEINS; T-LYMPHOCYTES, CYTOTOXIC; VIRAL CORE PROTEINS; VIRUS LATENCY;

EID: 0034608650     PISSN: 00221007     EISSN: None     Source Type: Journal    
DOI: 10.1084/jem.191.11.1853     Document Type: Article

References (69)

1. Askonas, B.A., A.J. McMichael, and R.G. Webster. 1982. The immune response to influenza viruses and the problem of protection against infection. In Basic and Applied Influenza Research. A.S. Beare, editor. CRC Press, Boca Raton, FL. 159-188.
2. Zinkernagel, R.M. 1993. Immunity to viruses. 3rd ed. In Fundamental Immunology. W.E. Paul, editor. Raven Press Ltd., New York. 1212-1250.
3. Ahmed, R., L.A. Morrison, and D.M. Knipe. 1996. Persistence of viruses. In Fields Virology. Vol. 1. B.N. Fields, D.M. Knipe, and P.M. Howley, editors. 2 vols. Lippincott-Raven Publishers, Philadelphia. 219-249.
4. Hengel, H., and U.H. Kozinowski. 1997. Interference with antigen processing by viruses. Curr. Opin. Immunol. 9:470-476.
5. Marrack, P., and J. Kappler. 1994. Subversion of the immune system. Cell. 76:323-332.
6. McMichael, A.J. 1998. T cell responses and viral escape. Cell. 93:673-676.
7. Moskophidis, D., and R.M. Zinkernagel. 1996. Immunobiology of cytotoxic T-cell resistant virus variants: studies on lymphocytic choriomeningitis virus (LCMV). Semin. Virol. 7:3-11.
8. Ploegh, H.L. 1998. Viral strategies of immune evasion. Science. 280:248-253.
9. Whitton, J.L., and M.B.A. Oldstone. 1996. Immune response to viruses. In Fields Virology. Vol. 1. B.N. Fields, D.M. Knipe, and P.M. Howley, editors. 2 vols. Lippincott-Raven Publishers, Philadelphia. 345-374.
10. Smith, G.L., J.A. Symons, A. Vanderplasschen, and A. Alcami. 1997. Vaccinia virus glycoproteins and immune evasion. Immunol. Rev. 159:137-154.
11. McFadden, G., K. Graham, and M. Barry. 1996. New strategies of immune modulation by DNA viruses. Transplant. Proc. 28:2085-2088.
12. Holland, J. 1993. Replication error, quasispecies populations, and extreme evolution rates of RNA viruses. In Emerging Viruses. S.S. Morse, editor. Oxford University Press, Oxford. 203-218.
13. Lamb, R.A., and R.M. Krug. 1996. Orthomyxoviridae: the viruses and their replication. 3rd ed. In Fields Virology. Vol. 2. B.N. Fields, D.M. Knipe, and P.M. Howley, editors. 2 vols. Lippincott-Raven Publishers, Philadelphia. 1353-1395.
14. Kilbourne, E.D. 1987. Influenza. Plenum Medical Book Co., New York. 359.
15. Ada, G.L., and P.D. Jones. 1986. The immune response to influenza infection. Curr. Top. Microbiol. Immunol. 128:1-54.
16. + T-cell mechanisms in the control of respiratory virus infections. Immunol. Rev. 159:105-117.
17. Gerhard, W., K. Mozdzanowska, M. Furchner, G. Washko, and K. Maiese. 1997. Role of the B-cell response in recovery of mice from primary influenza virus infection. Immunol. Rev. 159:95-103.
18. Lukacher, A.E., V.L. Braciale, and T.J. Braciale. 1984. In vivo effector function of influenza virus-specific cytotoxic T lymphocyte clones is highly specific. J. Exp. Med. 160:814-826.
19. McMichael, A. 1994. Cytotoxic T lymphocytes specific for influenza virus. Curr. Top. Microbiol. Immunol. 189:75-91.
20. Graham, M.B., and T.J. Braciale. 1997. Resistance to and recovery from lethal influenza virus infection in B lymphocyte-deficient mice. J. Exp. Med. 186:2063-2068.
21. Palese, P., and J.F. Young. 1982. Variation of influenza A, influenza B, and influenza C viruses. Science. 215:1468-1474.
22. Yewdell, J.W., R.G. Webster, and W.U. Gerhard. 1979. Antigenic variation in three distinct determinants of an influenza type A haemagglutinin molecule. Nature. 279:246-248.
23. Webster, R.G., W.G. Laver, G.M. Air, and G.C. Schild. 1982. Molecular mechanisms of variation in influenza viruses. Nature. 296:115-121.
24. Wiley, D.C., I.A. Wilson, and J.J. Skehel. 1981. Structural identification of the antibody-binding sites of Hong-Kong influenza hemagglutinin and their involvement in antigenic variation. Nature: 289:373-378.
25. Webster, K.G., W.J. Bean, O.T. Gorman, T.M. Chambers, and Y. Kawaoka. 1992. Evolution and ecology of influenza A viruses. Microbiol. Rev. 56:152-179.
26. Smith, F.I., and P. Palese. 1989. Variation in influenza virus genes: epidemiological, pathogenic, and evolutionary consequences. In The Influenza Viruses. K.M. Krug, editor. Plenum Press. New York/London. 319-360.
27. Gorman, O.T., W.J. Bean, and R.G. Webster. 1992. Evolutionary processes in influenza viruses-divergence, rapid evolution, and stasis. Curr. Top. Microbiol. Immunol. 176:75-97.
28. Doherty, P.C., W. Allan, M. Eichelberger, and S.R. Carding. 1992. Roles of αβ and γδ T cell subsets in viral immunity. Annu. Rev. Immunol. 10:123-151.
29. Townsend, A.R.M., and H. Bodmer. 1989. Antigen recognition by class-I restricted T lymphocytes. Annu. Rev. Immunol. 7:601-624.
30. Mamalaki, C., T. Norton, Y. Tanaka, A.R. Townsend, P. Chandler, E. Simpson, and D. Kioussis. 1992. Thymic depletion and peripheral activation of class I major histocompatibility complex-restricted T cells by soluble peptide in T-cell receptor transgenic mice. Proc. Natl. Acad Sci. USA. 89: 11342-11346.
31. Mamalaki, C., J. Elliott, T. Norton, N. Yannoutsos, A.R. Townsend, P. Chandler, E. Simpson, and D. Kioussis. 1993. Positive and negative selection in transgenic mice expressing a T-cell receptor specific for influenza nucleoprotein and endogenous superantigen. Dev. Immunol. 3:159-174.
32. Corbella, P., D. Moskophidis, E. Spanopoulou, C. Mamalaki, M. Tolaini, A. Itano, D. Lans, D. Baltimore, E. Robey, and D. Kioussis. 1994. Functional commitment to helper T cell lineage precedes positive selection and is independent of T cell receptor MHC specificity. Immunity. 1:269-276.
33. Spanopoulou, E., C.A. Roman, L.M. Corcoran, M.S. Schlissel, D.P. Silver, D. Nemazee, M.C. Nussenzweig, S.A. Shinton, R.R. Hardy, and D. Baltimore. 1994. Functional immunoglobulin transgenes guide ordered B-cell differentiation in Rag-1-deficient mice. Genes Dev. 8:1030-1042.
34. Barrett, T., and S.C. Inglis. 1985. Growth, purification and titration of influenza viruses. In Virology: A Practical Approach. B.W.J. Mahy, editor. IRL Press, Oxford. 119-150.
35. Thompson, W.R. 1947. The use of moving averages and interpolation to estimate median effective dose. Bacteriol. Rev. 11:115-147.
36. Vitiello, A., L. Yuan, R.W. Chesnut, J. Sidney, S. Southwood, P. Farness, M.R. Jackson, P.A. Peterson, and A. Sette. 1996. Immunodominance analysis of CTL responses to influenza PR8 virus reveals two new dominant and subdominant Kb-restricted epitopes. J. Immunol. 157:5555-5562.
37. 51Cr-labelled allogeneic target cells in vitro: inhibition by isoantibody and by drugs. Immunology. 14:181-196.
38. Pewe, L., G.L. Wu, E.M. Barnett, R.F. Castro, and S. Perlman. 1996. Cytotoxic T cell-resistant variants are selected in a virus-induced demyelinating disease. Immunity. 5:253-262.
39. Powis, S.J., A.R.M. Townsend, E.V. Deverson, J. Bastin, G.W. Butcher, and J.C. Howard. 1991. Restoration of antigen presentation to the mutant cell line RMA-S by an MHC-linked transporter. Nature. 354:528-531.
40. Schumacher, T.M.N., M.-T. Heemels, J.J. Neefjes, J.M. Kast, C.J.M. Melief, and H.L. Ploegh. 1990. Direct binding of peptide to empty MHC class I molecules on intact cells in vitro. Cell. 62:563-567.
41. Altman, J.D, P.A. Reay, and M.M. Davis. 1993. Formation of functional peptide complexes of class II major histocompatibility complex proteins from subunits produced in Escherichia coli. Proc. Natl. Acad. Sci. USA. 90:10330-10334.
42. Altman, J.D., P.A.H. Moss, P.J.R. Goulder, D.H. Barouch, M.G. McHeyzer-Williams, J.I. Bell, A.J. McMichael, and M.M. Davis. 1996. Phenotypic analysis of antigen-specific T lymphocytes. Science. 274:94-96.
43. + T cells in primary and secondary influenza pneumonia. Immunity. 8:683-691.
44. Murali-Krishna, K., J.D. Altman, M. Suresh, D.J.D Sourdive, A.J. Zajac, J.D. Miller, J. Slansky, and R. Ahmed. 1998. Counting antigen-specific CD8 T cells: a reevaluation of bystander activation during viral infection. Immunity. 8:177-187.
45. Pircher, H., D. Moskophidis, U. Rohrer, K. Bürki, H. Hengartner, and R.M. Zinkernagel. 1990. Viral escape by selection of cytotoxic T cell-resistant virus variants in vivo. Nature. 346:629-633.
46. Shaw, A.S., and M.L. Dustin. 1997. Making the T cell receptor go the distance: a topological view of T cell activation. Immunity. 6:361-369.
47. Townsend, A.R., and J.J. Skehel. 1984. The influenza A virus nucleoprotein gene controls the induction of both subtype specific and cross-reactive cytotoxic T cells. J. Exp. Med. 160:552-563.
48. + memory T cells by viral variants. J. Exp. Med. 190: 1319-1328.
49. Borrow, P., and G.M. Shaw. 1998. Cytotoxic T-lymphocyte escape viral variants: how important are they in viral evasion of immune clearance in vivo? Immunol. Rev. 164:37-51.
50. Lewicki, H.A., M.G. Von Herrath, C.F. Evans, J.L. Whitton, and M.B. Oldstone. 1995. CTL escape viral variants. II. Biologic activity in vivo. Virology. 211:443-450.
51. Tashiro, M., and R. Rott. 1996. The role of proteolytic cleavage of viral glycoproteins in the pathogenesis of influenza virus infections. Semin. Virol. 7:237-243.
52. Steinhauer, D.A. 1999. Role of hemagglutinin cleavage for the pathogenicity of influenza virus. Virology. 258:1-20.
53. + T cells clear influenza virus by perform or Fas-dependent processes. J. Immunol. 159:5197-5200.
54. Young, A.C., W. Zhang, J.C. Sacchettini, and S.G. Nathenson. 1994. The three-dimensional structure of H-2Db at 2.4 Å resolution: implications for antigen-determinant selection. Cell. 76:39-50.
55. + T lymphocytes. Immunol. Rev. 151:31-49.
56. Yewdell, J.W., L. Eisenlohr, J.H. Cox, F. Esquevel, R.W. Anderson, C.K. Lapham, R. French, and J.R. Bennink. 1993. Processing and presentation of viral proteins to MHC class I-restricted T lymphocytes. In Viruses and the Cellular Immune Response. D.B. Thomas, editor. Marcel Dekker, Inc., New York. 31-48.
57. Gileadi, U., A. Gallimore, P. Van der Bruggen, and V. Cerundolo. 1999. Effect of epitope flanking residues on the presentation of N-terminal cytotoxic T lymphocyte epitopes. Eur. J. Immunol. 29:2213-2222.
58. Klenerman, P., S. Rowland-Jones, S. McAdam, J. Edwards, S. Daenke, D. Lalloo, B. Koppe, W. Rosenberg, D. Boyd, A. Edwards, et al. 1994. Cytotoxic T-cell activity antagonized by naturally occurring HIV-1 Gag variants. Nature. 369:403-407.
59. Bertoletti, A., A. Sette, F.V. Chisari, A. Penna, M. Levreto, M. De Carli, F. Fiaccadori, and C. Ferrari. 1994. Natural variants of cytotoxic epitopes are T-cell receptor antagonists for antiviral cytotoxic T cells. Nature. 369:407-410.
60. Klenerman, P., and R.M. Zinkernagel. 1998. Original antigenic sin impairs cytotoxic T lymphocyte responses to viruses bearing variant epitopes. Nature. 394:482-485.
61. + cytotoxic T cells to virus clearance or pathologic manifestations of influenza virus infection in a T cell receptor transgenic mouse model. J. Exp. Med. 188:223-232.
62. Williams, O., Y. Tanaka, M. Bix, M. Murdjeva, D. Littman, and D. Kioussis. 1996. Inhibition of thymocyte negative selection by T cell receptor antagonist peptides. Eur. J. Immunol. 26:532-538.
63. Smyth, L.A., O. Williams, D.J. Huby, T. Nordon, O. Acuto, S.C. Ley, and D. Kioussis. 1998. Altered peptide ligands induce quantitatively but not qualitatively different intracellular signals in primary thymocytes. Proc. Natl. Acad. Sci. USA. 95: 8193-8198.
64. Parker, C.E., and K.G. Gould. 1996. Influenza A virus - a model for viral antigen presentation to cytotoxic T-lymphocytes. Semin. Virol. 7:61-73.
65. Rocha, E., N.J. Cox, R.A. Black, M.W. Harmon, C.J. Harrison, and A.P. Kendal. 1991. Antigenic and genetic-variation in influenza A (H1N1) virus isolates recovered from a persistently infected immunodeficient child. J. Virol. 65: 2340-2350.
66. Yewdell, J.W., J.R. Beninnk, G.L. Smith, and B. Moss. 1985. Influenza A virus nucleoprotein is a major target antigen for cross-reactive anti-influenza A virus cytotoxic T lymphocytes. Proc. Natl. Acad. Sci. USA. 82:1785-1789.
67. Couch, R.B., J.A. Englund, and E. Whimbey. 1997. Respiratory virus infections in immunocompetent and immunocompromised persons. Am. J. Med. 102:2-9.
68. Koenig, S., A.J. Conley, Y.A. Brewah, G.M. Jones, S. Leath, L.J. Boots, V. Davey, G. Pantaleo, J.F. Demarest, C. Carter, et al. 1995. Transfer of HIV-1-specific cytotoxic T lymphocytes to an AIDS patient leads to selection for mutant HIV variants and subsequent disease progression. Nat. Med. 1:330-336.
69. Mortara, L., F. Letournuer, H. Gras-Masse, A. Venet, J.-G. Guillet, and I. Bourgault-Villada. 1998. Selection of virus variants and emergence of virus escape mutants after immunization with an epitope vaccine. J. Virol. 72:1403-1410.