Impact of HLA-B alleles, epitope binding affinity, functional avidity, and viral coinfection on the immunodominance of virus-specific CTL responses

Journal of Immunology

Volumn 176, Issue 7, 2006, Pages 4094-4101

  Bihl, Florian ^a   Frahm, Nicole ^a   Di Giammarino, Loriana ^a   Sidney, John ^b   John, Mina ^c   Yusim, Karina ^d   Woodberry, Tonia ^e   Sango, Kaori ^a   Hewitt, Hannah S ^a   Henry, Leah ^a   Linde, Caitlyn H ^a   Chisholm III, John V ^a   Zaman, Tauheed M ^f   Pae, Eunice ^g   Mallal, Simon ^c   Walker, Bruce D ^a   Sette, Alessandro ^b   Korber, Bette T ^d   Heckerman, David ^h   Brander, Christian ^a  

^a MASSACHUSETTS GENERAL HOSPITAL   (United States)

^b LA JOLLA INSTITUTE FOR ALLERGY AND IMMUNOLOGY   (United States)

^c MURDOCH UNIVERSITY   (Australia)

^d LOS ALAMOS NATIONAL LABORATORY   (United States)

^e MENZIES SCHOOL OF HEALTH RESEARCH   (Australia)

^f LEMUEL SHATTUCK HOSPITAL   (United States)

^g FENWAY INSTITUTE   (United States)

^h MICROSOFT RESEARCH   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

EPITOPE; HLA A ANTIGEN; HLA B ANTIGEN; HLA C ANTIGEN; PEPTIDE;

ALLELISM; ANTIGEN RECOGNITION; ANTIVIRAL ACTIVITY; ARTICLE; BINDING AFFINITY; CYTOTOXIC T LYMPHOCYTE; ENZYME LINKED IMMUNOSPOT ASSAY; EPITOPE MAPPING; EPSTEIN BARR VIRUS; HLA SYSTEM; HUMAN; HUMAN CELL; HUMAN IMMUNODEFICIENCY VIRUS; IMMUNODOMINANCE; IMMUNOMODULATION; MAJOR CLINICAL STUDY; PEPTIDE ANALYSIS; PRIORITY JOURNAL; RESTRICTION MAPPING; RISK FACTOR; T LYMPHOCYTE ACTIVATION; VIRUS IMMUNITY; VIRUS INFECTION; ACQUIRED IMMUNE DEFICIENCY SYNDROME; ALLELE; AMINO ACID SEQUENCE; CHEMISTRY; GENETICS; HUMAN IMMUNODEFICIENCY VIRUS 1; IMMUNOLOGY; METABOLISM; MOLECULAR GENETICS; VIROLOGY;

ACQUIRED IMMUNODEFICIENCY SYNDROME; ALLELES; AMINO ACID SEQUENCE; EPITOPES, T-LYMPHOCYTE; EPSTEIN-BARR VIRUS INFECTIONS; HERPESVIRUS 4, HUMAN; HIV-1; HLA-A ANTIGENS; HLA-B ANTIGENS; HLA-C ANTIGENS; HUMANS; IMMUNODOMINANT EPITOPES; MOLECULAR SEQUENCE DATA; T-LYMPHOCYTES, CYTOTOXIC;

EID: 33646019589     PISSN: 00221767     EISSN: None     Source Type: Journal    
DOI: 10.4049/jimmunol.176.7.4094     Document Type: Article

References (48)

1. Sette, A., and J. Fikes. 2003. Epitope-based vaccines: an update on epitope identification, vaccine design and delivery. Curr. Opin. Immunol 15: 461-470.
2. Brander, C., K. E. Hartman, A. K. Trocha, N. G. Jones, R. P. Johnson, B. Korber, P. Wentworth, S. P. Buchbinder, S. Wolinsky, B. D. Walker, and S. A. Kalams. 1998. Lack of strong immune selection pressure by the immunodominant, HLA-A*0201 restricted CTL response in chronic HIV-1 infection. J. Clin. Invest. 101: 2559-2566.
3. 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: 1797-1780.
4. Day, C. L., A. K. Shea, M. A. Altfeld, D. P. Olson, S. P. Buchbinder, F. M. Hecht, E. S. Rosenberg, B. D. Walker, and S. A. Kalams. 2001. Relative dominance of epitope-specific cytotoxic T-lymphocyte responses in human immunodeficiency virus type 1-infected persons with shared HLA alleles. J. Virol. 75: 6279-6291.
5. + T cells at the levels of T cell repertoire and presentation of viral antigens. J. Exp. Med. 193: 1319-1326.
6. Brander, C., and Y. Riviere. 2002. Early and late cytotoxic T lymphocyte responses in HIV infection. AIDS 16: S97-S103.
7. Altfeld, M., T. M. Allen, E. T. Kalife, N. Frahm, M. M. Addo, B. R. Mothe, A. Rathod, L. L. Reyor, J. Harlow, X. G. Yu, et al. 2005. The majority of currently circulating human immunodeficiency virus type 1 clade B viruses fail to prime cytotoxic T-lymphocyte responses against an otherwise immunodominant HLA-A2-restricted epitope: implications for vaccine design. J. Virol. 79: 5000-5005.
8. + T cell responses to influenza A virus: roles for cross-presentation and lysis-independent immunodomination. J. Immunol. 173: 5021-5027.
9. Probst, H. C., K. Tschannen, A. Gallimore, M. Martinic, M. Basler, T. Dumrese, E. Y. Jones, and M. F. van den Broek. 2003. Immunodominance of an antiviral cytotoxic T cell response is shaped by the kinetics of viral protein expression. J. Immunol. 171: 5415-5422.
10. Welsh, R. M., L. K. Selin, and E. Szomolanyi-Tsuda. 2004. Immunological memory to viral infections. Annu. Rev. Immunol 22: 711-743.
11. Sette, A., A. Vitiello, B. Reherman, P. Fowler, R. Nayersina, W. M. Kast, C. J. Melief, C. Oseroff, L. Yuan, J. Ruppert, et al. 1994. The relationship between class 1 binding affinity and immunogenicity of potential cytotoxic T cell epitopes. J. Immunol. 153: 5586-5592.
12. Wentworth, P. A., A. Vitiello, J. Sidney, E. Keogh, R. W. Chesnut, H. Grey, and A. Sette. 1996. Differences and similarities in the A2.1-restricted cytotoxic T cell repertoire in humans and human leukocyte antigen-transgenic mice. Eur. J. Immunol. 26: 97-101.
13. Alexander, J., C. Oseroff, J. Sidney, P. Wentworth, E. Keogh, G. Hermanson, F. V. Chisari, R. T. Kubo, H. M. Grey, and A. Sette. 1997. Derivation of HLA-A11/Kb transgenic mice: functional CTL repertoire and recognition of human A11-restricted CTL epitopes. J. Immunol. 159: 4753-4761.
14. Boggiano, C., R. Moya, C. Pinilla, F. Bihl, C. Brander, J. Sidney, A. Sette, and S. E. Blondelle. 2005. Discovery and characterization of highly immunogenic and broadly recognized mimics of the HIV-1 CTL epitope Gag77-85. Eur. J. Immunol. 35: 1428-1437.
15. Ogg, G. S., X. Jin, S. Bonhoeffer, P. R. Dunbar, M. A. Nowak, S. Monard, J. P. Segal, Y. Cao, S. L. Rowland-Jones, V. Cerundolo, et al. 1998. Quantitation of HIV-1-specific cytotoxic T lymphocytes and plasma load of viral RNA. Science 279: 2103-2106.
16. Kiepiela, P., A. J. Leslie, I. Honeyborne, D. Ramduth, C. Thobakgale, S. Chetty, P. Rathnavalu, C. Moore, K. J. Pfafferott, L. Hilton, et al. 2004. Revolutionary influences of HIV and HLA: the dominant role of HLA-B. Nature 432: 769-774.
17. Bihl, F. K., E. Loggi, J. V. Chisholm III, H. S. Hewitt, L. M. Henry, C. Linde, T. J. Suscovich, J. T. Wong, N. Frahm, P. Andreone, and C. Brander. 2005. Simultaneous assessment of cytotoxic T lymphocyte responses against multiple viral infections by combined usage of optimal epitope matrices, anti-CD3 mAb T-cell expansion and "RecycleSpot". J Transl. Med. 3: 20.
18. Frahm, N., B. T. Korber, C. M. Adams, J. J. Szinger, R. Draenert, M. M. Addo, M. E. Feeney, K. Yusim, K. Sango, N. V. Brown, et al. 2004. Consistent cytotoxic-T-lymphocyte targeting of immunodominant regions in human immunodeficiency virus across multiple ethnicities. J. Virol. 78: 2187-2200.
19. Woodberry, T., L. Henry, T. Suscovich, J. K. Davis, N. Frahm, B. Walker, D. T. Scadden, F. Z. Wang, and C. Brander. 2005. Differential targeting and shifts in the immunodominance of EBV specific CD8 and CD4 T cell responses from acute to persistent infection. J. Infect. Dis.. 192:1513-1524.
20. Frahm, N., P. Goulder, and C. Brander. 2002. Total assessment of HIV specific CTL responses: epitope clustering, processing preferences and the impact of HIV sequence heterogeneity. In HIV Molecular Immunology Database. C. B. B. Korber, B. Walker, R. Koup, J. Moore, B. Haynes, and G. Meyers, eds. Los Alamos National Laboratory: Theoretical Biology and Biophysics, Los Alamos, NM.
21. Rickinson, A. B., and D. J. Moss. 1997. Human cytotoxic T lymphocyte responses to Epstein-Barr virus infection. Annu. Rev. Immunol. 15: 405-431.
22. Frahm, N., S. Adams, P. Kiepiela, C. H. Linde, H. S. Hewitt, M. Lichterfeld, K. Sango, N. V. Brown, E. Pae, A. G. Wurcel, et al. 2005. HLA-B63 presents HLA-B57/B58-restricted cytotoxic T-lymphocyte epitopes and is associated with low human immunodeficiency virus load. J. Virol. 79: 10218-10225.
23. Woodberry, T., T. J. Suscovich, L. M. Henry, M. August, M. T. Waring, A. Kaur, C. Hess, J. L. Kutok, J. C. Aster, F. Wang, et al. 2005. aEb7 (CD103) expression identifies a highly active, tonsil-resident effector-memory CTL population. J. Immunol. 175: 4355-4362.
24. Trautmann, L., M. Rimbert, K. Echasserieau, X. Saulquin, B. Neveu, J. Dechanet, V. Cerundolo, and M. Bonneville. 2005. Selection of T cell clones expressing high-affinity public TCRs within Human cytomegalovirus-specific CD8 T cell responses. J. Immunol. 175: 6123-6132.
25. Sidney, J., S. Southwood, and A. Seite. 2005. Classification of A1- and A24-supertype molecules by analysis of their MHC-peptide binding repertoires. Immunogenetics 1-16.
26. Sette, A., and J. Sidney. 1999. Nine major HLA class I supertypes account for the vast preponderance of HLA-A and -B polymorphism. Immunogenetics 50: 201-212.
27. Yusim, K., C. Kesmir, B. Gaschen, M. M. Addo, M. Altfeld, S. Brunak, A. Chigaev, V. Detours, and B. T. Korber. 2002. Clustering patterns of cytotoxic T-lymphocyte epitopes in human immunodeficiency virus type 1 (HIV-1) proteins reveal imprints of immune evasion on HIV-1 global variation. J. Virol. 76: 8757-8768.
28. Gaschen, B., J. Taylor, K. Yusim, B. Foley, F. Gao, D. Lang, V. Novitsky, B. Haynes, B. H. Hahn, T. Bhattacharya, and B. Korber. 2002. Diversity considerations in HIV-1 vaccine selection. Science 296: 2354-2360.
29. Leslie, A. J., K. J. Pfafferott, P. Chetty, R. Draenert, M. M. Addo, M. Feeney, Y. Tang, E. C. Holmes, T. Allen, J. G. Prado, et al. 2004. HIV evolution: CTL escape mutation and reversion after transmission. Nat. Med. 10: 282-289.
30. Goulder, P. J., C. Brander, Y. Tang, C. Tremblay, R. A. Colbert, M. M. Addo, E. S. Rosenberg, T. Nguyen, R. Allen, A. Trocha, et al. 2001. Evolution and transmission of stable CTL escape mutations in HIV infection. Nature 412: 334-338.
31. + T cell responses from primary to persistent phases of Epstein-Barr virus infection. J. Exp. Med. 195: 893-905.
32. Frahm, N., P. Kiepiela, S. Adams, C. H. Linde, H. S. Hewitt, K. Sango, M. E. Feeney, C. Moore, M. M. Addo, M. Lichterfeld, et al. 2006. Control of HIV replication by cytotoxic T lymphocytes targeting subdominant CTL epitopes. Nat. Immunol. 7:173-180.
33. O'Brien, S. J., X. Gao, and M. Carrington. 2001. HLA and AIDS: a cautionary tale. Trends Mol. Med. 7: 379-381.
34. Hunziker, I. P., A. Cerny, and W. J. Pichler. 1998. Who is right? Or, how to judge the disagreement about HLA restriction of Nef peptides. AIDS Res. Hum. Retroviruses 14: 921-924.
35. Selin, L. K., S. R. Nahill, and R. M. Welsh. 1994. Cross-reactivities in memory cytotoxic T lymphocyte recognition of heterologous viruses. J. Exp. Med. 179: 1933-1943.
36. Selin, L. K., K. Vergilis, R. M. Welsh, and S. R. Nahill. 1996. Reduction of otherwise remarkably stable virus-specific cytotoxic T lymphocyte memory by heterologous viral infections. J. Exp. Med. 183: 2489-2499.
37. Price, D. A., J. M. Brenchley, L. E. Ruff, M. R. Betts, B. J. Hill, M. Roederer, R. Koup, S. A. Migueles, E. Gostick, L. Wooldridge, et al. 2005. Competition for antigen shapes clonal dominance in CD8 T cell populations specific for persistent DNA viruses. J. Exp. Med. 202: 1349-1361.
38. Chen, J. L., G. Stewart-Jones, G. Bossi, N. M. Lissin, L. Wooldridge, E. M. Choi, G. Held, P. R. Dunbar, R. M. Esnouf, M. Sami, et al. 2005. Structural and kinetic basis for heightened immunogenicity of T cell vaccines. J. Exp. Med. 201: 1243-1255.
39. Boon, A. C., G. De Mutsert, R. A. Fouchier, K. Sintnicolaas, A. D. Osterhaus, and G. F. Rimmelzwaan. 2004. Preferential HLA usage in the influenza virus-specific CTL response. J. Immunol. 172: 4435-4443.
40. Marsh, S. G. E., P. Parham, and L. D. Barber. 2000. The HLA Facts Book. Academic, New York.
41. Brander, C., P. O'Connor, T. Suscovich, G. Jones, Y. Lee, D. Kedes, D. Ganem, J. Martin, D. Osmond, S. Southwood, et al. 2001. Definition of an optimal CTL epitope against the latently expressed KSHV kaposin protein. J. Infect. Dis. 184: 119-126.
42. Cerny, A., J. G. McHutchison, C. Pasquinelli, M. E. Brown, M. A. Brothers, B. Grabscheid, P. Fowler, M. Houghton, and F. V. Chisari. 1995. Cytotoxic T lymphocytes response to hepatitis C virus-derived peptides containing the HLA A2.1 binding motif. J. Clin. Invest. 95: 521-530.
43. Altfeld, M., B. Livingston, N. Reshamwala, T. Nguyen, M. Addo, M. Shea, M. Newman, J. Fikes, J. Sidney, P. Wentworth, et al. 2001. Identification of novel HLA-A2-restricted HIV-1-specific CTL epitopes predicted by the HLA-A2 supertype peptide-binding motif. J. Virol. 75: 1301-1311.
44. + T-cell epitopes specific for immediate-early transactivator Rta of Epstein-Barr virus. Hum. Immunol. 66: 483-493.
45. Frahm, N., K. Yusim, S. Adams, J. Sidney, P. Hraber, H. S. Hewitt, C. H. Linde, T. Woodberry, L. Henry, J. Listgarten, et al. 2006. Extensive HLA class I allele promiscuity among viral cytotoxic T lymphocyte (CTL) epitopes. Submitted for publication.
46. Frahm, N., P. Goulder, and C. Brander. 2003. Broad HIV-1 specific CTL responses reveal extensive HLA class I binding promiscuity of HIV-derived, optimally defined CTL epitopes. In HIV Molecular Immunology Database. C. B. B. Korber, B. Walker, R. Koup, J. Moore, B. Haynes, and G. Meyers, eds. Los Alamos National Laboratory: Theoretical Biology and Biophysics, Los Alamos, NM.
47. + T-cell populations with differing cytolytic activities. J. Virol. 75: 7399-7409.
48. + T-cell responses is dramatically modified by DNA immunization and is regulated by gamma interferon. J. Virol. 76: 4251-4259.