Respiratory syncytial virus nucleoprotein-specific cytotoxic T-cell epitopes in a South African population of diverse HLA types are conserved in circulating field strains

Journal of Virology

Volumn 77, Issue 13, 2003, Pages 7319-7329

  Venter, Marietjie ^a   Rock, Michael ^b   Puren, Adrian J ^a   Tiemessen, Caroline T ^a   Crowe Jr , James E ^b,c  

^a NATIONAL INSTITUTE FOR COMMUNICABLE DISEASES   (South Africa)

^b VANDERBILT UNIVERSITY SCHOOL OF MEDICINE   (United States)

^c VANDERBILT UNIVERSITY MEDICAL CENTER   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

EPITOPE; GAMMA INTERFERON; HLA B ANTIGEN; VIRUS NUCLEOPROTEIN;

ADULT; ARTICLE; CYTOLYSIS; CYTOTOXIC T LYMPHOCYTE; GENETIC VARIABILITY; GENOTYPE; HLA SYSTEM; HUMAN; HUMAN CELL; MEMORY CELL; NONHUMAN; NORMAL HUMAN; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; RESPIRATORY SYNCYTIAL PNEUMOVIRUS; RESPIRATORY TRACT INFECTION; SOUTH AFRICA; VIRUS STRAIN;

AMINO ACID SEQUENCE; BASE SEQUENCE; DNA PRIMERS; EPITOPES; HLA ANTIGENS; HUMANS; INTERFERON TYPE II; MOLECULAR SEQUENCE DATA; POPULATION SURVEILLANCE; SEQUENCE HOMOLOGY, AMINO ACID; T-LYMPHOCYTES, CYTOTOXIC; VIRAL PROTEINS;

EID: 0038129484     PISSN: 0022538X     EISSN: None     Source Type: Journal    
DOI: 10.1128/JVI.77.13.7319-7329.2003     Document Type: Article

References (51)

1. Ada, G. L., and P. D. Jones. 1987. The cell-mediated and humoral responses to influenza virus infection in the mouse lung. Adv. Exp. Med. Biol. 216B:1033-1042.
2. Alansari, H., and L. N. Potgieter. 1994. Nucleotide and predicted amino acid sequence analysis of the ovine respiratory syncytial virus non-structural 1C and 1B genes and the small hydrophobic protein gene. J. Gen. Virol. 75(Pt 2):401-404.
3. Altfeld, M. A., A. Trocha, R. L. Eldridge, E. S. Rosenberg, M. N. Phillips, M. M. Addo, R. P. Sekaly, S. A. Kalams, S. A. Burchett, K. McIntosh, B. D. Walker, and P. J. Goulder. 2000. Identification of dominant optimal HLA-B60- and HLA-B61-restricted cytotoxic T-lymphocyte (CTL) epitopes: rapid characterization of CTL responses by enzyme-linked immunospot assay. J. Virol. 74:8541-8549.
4. Altman, J. D., P. A. Moss, P. J. 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. (Erratum 280:1821, 1998.)
5. Apolloni, A., D. Moss, R. Stumm, S. Burrows, A. Suhrbier, I. Misko, C. Schmidt, and T. Sculley. 1992. Sequence variation of cytotoxic T cell epitopes in different isolates of Epstein-Barr virus. Eur. J. Immunol. 22:183-189.
6. Bangham, C. R., P. J. Openshaw, L. A. Ball, A. M. King, G. W. Wertz, and B. A. Askonas. 1986. Human and murine cytotoxic T cells specific to respiratory syncytial virus recognize the viral nucleoprotein (N), but not the major glycoprotein (G), expressed by vaccinia virus recombinants. J. Immunol. 137:3973-3977.
7. Barouch, D. H., J. Kunstman, M. J. Kuroda, J. E. Schmitz, S. Santra, F. W. Peyerl, G. R. Krivulka, K. Beaudry, M. A. Lifton, D. A. Gorgone, D. C. Montefiori, M. G. Lewis, S. M. Wolinsky, and N. L. Letvin. 2002. Eventual AIDS vaccine failure in a rhesus monkey by viral escape from cytotoxic T lymphocytes. Nature 415:335-339.
8. Barr, J., P. Chambers, C. R. Pringle, and A. J. Easton. 1991. Sequence of the major nucleocapsid protein gene of pneumonia virus of mice: sequence comparisons suggest structural homology between nucleocapsid proteins of pneumoviruses, paramyxoviruses, rhabdoviruses and filoviruses. J. Gen. Virol. 72(Pt 3):677-685.
9. Bednarek, M. A., S. Y. Sauma, M. C. Gammon, G. Porter, S. Tamhankar, A. R. Williamson, and H. J. Zweerink. 1991. The minimum peptide epitope from the influenza virus matrix protein. Extra and intracellular loading of HLA-A2. J. Immunol. 147:4047-4053.
10. Bertoletti, A., A. Sette, F. V. Chisari, A. Penna, M. Levrero, 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.
11. Boon, A. C., G. de Mutsert, Y. M. Graus, R. A. Fouchier, K. Sintnicolaas, A. D. Osterhaus, and G. F. Rimmelzwaan. 2002. Sequence variation in a newly identified HLA-B35-restricted epitope in the influenza A virus nucleoprotein associated with escape from cytotoxic T lymphocytes. J. Virol. 76:2567-2572.
12. Brandenburg, A. H., L. de Waal, H. H. Timmerman, P. Hoogerhout, R. L. de Swart, and A. D. Osterhaus. 2000. HLA class I-restricted cytotoxic T cell epitopes of the respiratory, syncytial virus fusion protein. J. Virol. 74:10240-10244.
13. Buchholz, U. J., S. Finke, and K. K. Conzelmann. 1999. Generation of bovine respiratory syncytial virus (BRSV) from cDNA: BRSV NS2 is not essential for virus replication in tissue culture, and the human RSV leader region acts as a functional BRSV genome promoter. J. Virol. 73:251-259.
14. Cannon, M. J., and C. R. Bangham. 1989. Recognition of respiratory syncytial virus fusion protein by mouse cytotoxic T cell clones and a human cytotoxic T cell line. J. Gen. Virol. 70:79-87.
15. 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.
16. Cannon, M. J., E. J. Stott, G. Taylor, and B. A. Askonas. 1987. Clearance of persistent respiratory, syncytial virus infections in immunodeficient mice following transfer of primed T cells. Immunology 62:133-138.
17. Cherrie, A. H., K. Anderson, G. W. Wertz, and P. J. Openshaw. 1992. Human cytotoxic T cells stimulated by antigen on dendritic cells recognize the N, SH, F, M, 22K, and 1b proteins of respiratory syncytial virus. J. Virol. 66:2102-2110.
18. Chiba, Y., Y. Higashidate, K. Suga, K. Honjo, H. Tsutsumi, and P. L. Ogra. 1989. Development of cell-mediated cytotoxic immunity to respiratory syncytial virus in human infants following naturally acquired infection. J. Med. Virol. 28:133-139.
19. Collins, P. L., K. Anderson, S. J. Langer, and G. W. Wertz. 1985. Correct sequence for the major nucleocapsid protein mRNA of respiratory syncytial virus. Virology 146:69-77.
20. Collins, P. L., K. McIntosh, and R. M. Chanock. 1996. Respiratory syncytial virus, p. 1313-1351. In B. N. Fields, D. M. Knipe, P. M. Howley, and R. M. Chanock (ed.), Fields virology, 3rd ed. Lippincott Raven Press, Philadelphia, Pa.
21. Goulder, P. J., M. M. Addo, M. A. Altfeld, E. S. Rosenberg, Y. Tang, U. Govender, N. Mngqundaniso, K. Annamalai, T. U. Vogel, M. Hammond, M. Bunce, H. M. Coovadia, and B. D. Walker. 2001. Rapid definition of five novel HLA-A*3002-restricted human immunodeficiency virus-specific cytotoxic T-lymphocyte epitopes by Elispot and intracellular cytokine staining assays. J. Virol. 75:1339-1347.
22. Goulder, P. J., C. Brander, K. Annamalai, N. Mngqundaniso, U. Govender, Y. Tang, S. He, K. E. Hartman, C. A. O'Callaghan, G. S. Ogg, M. A. Altfeld, E. S. Rosenberg, H. Cao, S. A. Kalams, M. Hammond, M. Bunce, S. I. Pelton, S. A. Burchett, K. McIntosh, H. M. Coovadia, and B. D. Walker. 2000. Differential narrow focusing of immunodominant human immunodeficiency virus gag-specific cytotoxic T-lymphocyte responses in infected African and caucasoid adults and children. J. Virol. 74:5679-5690.
23. Goulder, P. J., C. Brander, Y. Tang, C. Tremblay, R. A. Colbert, M. M. Addo, E. S. Rosenberg, T. Nguyen, R. Allen, A. Trocha, M. Altfeld, S. He, M. Bunce, R. Funkhouser, S. I. Pelton, S. K. Burchett, K. McIntosh, B. T. Korber, and B. D. Walker. 2001. Evolution and transmission of stable CTL escape mutations in HIV infection. Nature 412:334-338.
24. Goulder, P. J., F. Lechner, P. Klenerman, K. McIntosh, and B. D. Walker. 2000. Characterization of a novel respiratory syncytial virus-specific human cytotoxic T-lymphocyte epitope. J. Virol. 74:7694-7697.
25. Graham, B. S. 1996. Immunological determinants of disease caused by respiratory syncytial virus. Trends Microbiol. 4:290-293.
26. Hammond, M. G., E. D. du Toit, A. Sanchez-Mazas, M. Andrien, M. Coluzzi, M. de Pablo, G. de Stefano, C. Kaplan, L. J. Kennedy, L. Louie, and F. Migot. 1997. HLA in sub-Saharan Africa, p. 345-353. In D. Charon (ed.), Proceedings of the 12th International Histocompatibility Workshop and Conference. SSAF report, Paris, France.
27. Johnson, P. R., and P. L. Collins. 1989. The 1B (NS2), 1C (NS1) and N proteins of human respiratory syncytial virus (RSV) of antigenic subgroups A and B: sequence conservation and divergence within RSV genomic RNA. J. Gen. Virol. 70(Pt 6):1539-1547.
28. Karron, R. A., D. A. Buonagurio, A. F. Georgiu, S. S. Whitehead, J. E. Adamus, M. L. Clements-Mann, D. O. Harris, V. B. Randolph, S. A. Udem, B. R. Murphy, and M. S. Sidhu. 1997. Respiratory syncytial virus (RSV) SH and G proteins are not essential for viral replication in vitro: clinical evaluation and molecular characterization of a cold-passaged, attenuated RSV subgroup B mutant. Proc. Natl. Acad. Sci. USA 94:13961-13966.
29. 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.
30. Kumar, S., K. Tamura, I. B. Jakobsen, and M. Nei. 2001. MEGA2: molecular evolutionary genetics analysis software. Bioinformatics 17:1244-1245.
31. Lalvani, A., T. Dong, G. Ogg, A. A. Patham, H. Newell, A. V. Hill, A. J. McMichael, and S. Rowland-Jones. 1997. Optimization of a peptide-based protocol employing IL-7 for in vitro restimulation of human cytotoxic T lymphocyte precursors. J. Immunol. Methods 210:65-77.
32. Larsen, L. E., A. Uttenthal, P. Arctander, K. Tjornehoj, B. Viuff, C. Rontved, L. Ronsholt, S. Alexandersen, and M. Blixenkrone-Moller. 1998. Serological and genetic characterisation of bovine respiratory syncytial virus (BRSV) indicates that Danish isolates belong to the intermediate subgroup: no evidence of a selective effect on the variability of G protein nucleotide sequence by prior cell culture adaption and passages in cell culture or calves. Vet. Microbiol. 62:265-279.
33. McMichael, A. 1994. Cytotoxic T lymphocytes specific for influenza virus. Curr. Top. Microbiol. Immunol. 189:75-91.
34. Murali-Krishna, K., J. D. Altman, M. Suresh, D. Sourdive, A. Zajac, and R. Ahmed. 1998. In vivo dynamics of anti-viral CD8 T cell responses to different epitopes. An evaluation of bystander activation in primary and secondary responses to viral infection. Adv. Exp. Med. Biol. 452:123-142.
35. Oldstone, M. B. 1997. How viruses escape from cytotoxic T lymphocytes: molecular parameters and players. Virology 234:179-185.
36. 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.
37. Parker, K. C., M. A. Bednarek, and J. E. Coligan. 1994. Scheme for ranking potential HLA-A2 binding peptides based on independent binding of individual peptide side-chains. J. Immunol. 152:163-175.
38. Price, D. A., P. J. Goulder, P. Klenerman, A. K. Sewell, P. J. Easterbrook, M. Troop, C. R. Bangham, and R. E. Phillips. 1997. Positive selection of HIV-1 cytotoxic T lymphocyte escape variants during primary infection. Proc. Natl. Acad. Sci. USA 94:1890-1895.
39. Price, G. E., R. Ou, H. Jiang, L. Huang, and D. Moskophidis. 2000. Viral escape by selection of cytotoxic T cell-resistant variants in influenza A virus pneumonia. J. Exp. Med. 191:1853-1867.
40. Rammensee, H., J. Bachmann, N. P. Emmerich, O. A. Bachor, and S. Stevanovic. 1999. SYFPEITHI: database for MHC ligands and peptide motifs. Immunogenetics 50:213-219.
41. Shin, H.-J., K. T. Cameron, J. A. Jacobs, E. A. Turpin, D. A. Halvorson, S. M. Goyal, K. V. Nagaraja, M. C. Kumar, D. C. Lauer, B. S. Seal, and M. K. Njenga. 2002. Molecular epidemiology of subgroup C avian pneumoviruses isolated in the United States and comparison with subgroup A and B viruses. J. Clin. Microbiol. 40:1687-1693.
42. Thompson, J. D., T. J. Gibson, F. Plewniak, F. Jeanmougin, and D. G. Higgins. 1997. The CLUSTAL_X windows interface: flexible strategies for multiple sequence alignment aided by quality analysis tools. Nucleic Acids Res. 25:4876-4882.
43. Valarcher, J. F., H. Bourhy, A. Lavenu, N. Bourges-Abella, M. Roth, O. Andreoletti, P. Ave, and F. Schelcher. 2001. Persistent infection of B lymphocytes by bovine respiratory syncytial virus. Virology 291:55-67.
44. van den Hoogen, B. G., T. M. Bestebroer, A. D. Osterhaus, and R. A. Fouchier. 2002. Analysis of the genomic sequence of a human metapneumovirus. Virology 295:119-132.
45. Venter, M., M. Collinson, and B. D. Schoub. 2002. Molecular epidemiological analysis of community circulating respiratory syncytial virus in rural South Africa: comparison of viruses and genotypes responsible for different disease manifestations. J. Med. Virol. 68:452-461.
46. Venter, M., S. A. Madhi, C. T. Tiemessen, and B. D. Schoub. 2001. Genetic diversity and molecular epidemiology of respiratory syncytial virus over four consecutive seasons in South Africa: identification of new subgroup A and B genotypes. J. Gen. Virol. 82:2117-2124.
47. Voeten, J. T., T. M. Bestebroer, N. J. Nieuwkoop, R. A. Fouchier, A. D. Osterhaus, and G. F. Rimmelzwaan. 2000. Antigenic drift in the influenza A virus (H3N2) nucleoprotein and escape from recognition by cytotoxic T lymphocytes. J. Virol. 74:6800-6807.
48. Walker, B. D., C. Flexner, K. Birch-Limberger, L. Fisher, T. J. Paradis, A. Aldovini, R. Young, B. Moss, and R. T. Schooley. 1989. Long-term culture and fine specificity of human cytotoxic T-lymphocyte clones reactive with human immunodeficiency virus type 1. Proc. Natl. Acad. Sci. USA 86:9514-9518.
49. Walsh, E., and B. Graham. 1999. Respiratory syncytial viruses, p. 161-203. In Viral infections of the respiratory tract, vol. 27. Marcel Dekker, Inc., New York, N.Y.
50. Weber, M. W., E. K. Mulholland, and B. M. Greenwood. 1998. Respiratory syncytial virus infection in tropical and developing countries. Trop. Med. Int. Health 3:268-280.
51. Yellen-Shaw, A. J., E. J. Wherry, G. C. Dubois, and L. C. Eisenlohr. 1997. Point mutation flanking a CTL epitope ablates in vitro and in vivo recognition of a full-length viral protein. J. Immunol. 158:3227-3234.