Conflicting selective forces affect T cell receptor contacts in an immunodominant human immunodeficiency virus epitope

Nature Immunology

Volumn 7, Issue 2, 2006, Pages 179-189

  Iversen, Astrid K N ^a   Stewart Jones, Guillaume ^b   Learn, Gerald H ^c   Christie, Natasha ^d   Sylvester Hviid, Christina ^e   Armitage, Andrew E ^a   Kaul, Rupert ^d   Beattie, Tara ^a   Lee, Jean K ^a   Li, Yanping ^a   Chotiyarnwong, Pojchong ^b   Dong, Tao ^a   Xu, Xiaoning ^a   Luscher, Mark A ^d   MacDonald, Kelly ^d   Ullum, Henrik ^f   Klarlund Pedersen, Bente ^f   Skinhøj, Peter ^f   Fugger, Lars ^a,g   Buus, Søren ^e   Mullins, James I ^c   Jones, E Yvonne ^b   van der Merwe, P Anton ^h   McMichael, Andrew J ^a   more..

^a JOHN RADCLIFFE HOSPITAL   (United Kingdom)

^b UNIVERSITY OF OXFORD   (United Kingdom)

^c UNIVERSITY OF WASHINGTON   (United States)

^d UNIVERSITY OF TORONTO   (Canada)

^e UNIVERSITY OF COPENHAGEN   (Denmark)

^f Rigshospitalet   (Denmark)

^g AARHUS UNIVERSITY HOSPITAL   (Denmark)

^h UNIVERSITY OF OXFORD   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

AMINO ACID; DIDANOSINE; EPITOPE; HLA A2 ANTIGEN; LAMIVUDINE; RITONAVIR; T LYMPHOCYTE RECEPTOR; VIRUS RNA; ZIDOVUDINE;

ANTIGEN BINDING; ARTICLE; BINDING AFFINITY; CELL SELECTION; CLINICAL ARTICLE; CONTROLLED STUDY; CORRELATION ANALYSIS; CYTOTOXIC T LYMPHOCYTE; DISEASE COURSE; ENZYME LINKED IMMUNOSPOT ASSAY; FEMALE; GENE MUTATION; GENETIC VARIABILITY; HIGHLY ACTIVE ANTIRETROVIRAL THERAPY; HUMAN; HUMAN CELL; HUMAN IMMUNODEFICIENCY VIRUS; HUMAN IMMUNODEFICIENCY VIRUS INFECTION; IN VIVO STUDY; INFECTION CONTROL; MOLECULAR CLONING; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; VIRUS LOAD; VIRUS REPLICATION; WILD TYPE;

ADULT; AMINO ACID SEQUENCE; CRYSTALLOGRAPHY, X-RAY; EVOLUTION, MOLECULAR; FEMALE; GENE PRODUCTS, GAG; HIV ANTIGENS; HIV INFECTIONS; HIV-1; HLA-A2 ANTIGEN; HUMANS; IMMUNODOMINANT EPITOPES; MODELS, MOLECULAR; MOLECULAR SEQUENCE DATA; MULTIPROTEIN COMPLEXES; MUTATION; PEPTIDE FRAGMENTS; PHYLOGENY; RECEPTORS, ANTIGEN, T-CELL; SELECTION (GENETICS); T-LYMPHOCYTES, CYTOTOXIC; VARIATION (GENETICS); VIREMIA;

EID: 31344452079     PISSN: 15292908     EISSN: 15292916     Source Type: Journal    
DOI: 10.1038/ni1298     Document Type: Article

References (64)

1. McMichael, A. & Klenerman, P. HIV/AIDS. HLA leaves its footprints on HIV. Science 296, 1410-1411 (2002).
2. Moore, C.B. et al. Evidence of HIV-1 adaptation to HLA-restricted immune responses at a population level. Science 296, 1439-1443 (2002).
3. Brander, C. & Walker, B.D. Gradual adaptation of HIV to human host populations: Good or bad news? Nat Med. 9, 1359-1362 (2003).
4. Allen, T.M. et al. Tat-specific cytotoxic T lymphocytes select for SIV escape variants during resolution of primary viraemia. Nature 407, 386-390 (2000).
5. Borrow, P. et al. Antiviral pressure exerted by HIV-1-specific cytotoxic T lymphocytes (CTLs) during primary infection demonstrated by rapid selection of CTL escape virus. Nat. Med. 3, 205-211 (1997).
6. Price, D.A. et al. Positive selection of HIV-1 cytotoxic T lymphocyte escape variants during primary infection. Proc. Natl. Acad. Sci. USA 94, 1890-1895 (1997).
7. Jamieson, B.D. et al. Epitope escape mutation and decay of human immunodeficiency virus type 1-specific CTL responses. J. Immunol. 171, 5372-5379 (2003).
8. Kelleher, A.D. et al. Clustered mutations in HIV-1 gag are consistently required for escape from HLA-B27-restricted cytotoxic T lymphocyte responses. J. Exp. Med. 193, 375-386 (2001).
9. Leslie, A.J. et al. HIV evolution: CTL escape mutation and reversion after transmission. Nat. Med. 10, 282-289 (2004).
10. Altfeld, M. et al. Influence of HLA-857 on clinical presentation and viral control during acute HIV-1 infection. AIDS 17, 2581-2591 (2003).
11. Goulder, P.J. et al. Late escape from an immunodominant cytotoxic T -lymphocyte response associated with progression to AIDS. Nat. Med. 3, 212-217 (1997).
12. Altfeld, M. et al. The majority of currently circulating human immunodeficiency virus type 1 clades B viruses fail to prime cytotoxic T-lymphocyte responses against an otherwise immunodominant HLA-A2-restricted epitome: Implications for vaccine design. J. Virol. 79, 5000-5005 (2005).
13. Goulder, P.J. et al. Evolution and transmission of stable CTL escape mutations in HIV infection. Nature 412, 334-338 (2001).
14. Browning, M. & Krausa, P. Genetic diversity of HLA-A2: Evolutionary and functional significance. Immunol. Today 17, 165-170 (1996).
15. Johnson, R.P. et al. HIV-1 gag-specific cytotoxic T lymphocytes recognize multiple highly conserved epitopes. Fine specificity of the gag-specific response defined by using unstimulated peripheral blood mononuclear cells and cloned effector cells. J. Immunol. 147, 1512-1521 (1991).
16. Tsomides, T.J. et al. Naturally processed viral peptides recognized by cytotoxic T lymphocytes on cells chronically infected by human immunodeficiency virus type 1. J. Exp. Med. 180, 1283-1293 (1994).
17. HIV Sequence Compendium 2003 (eds. Leitner, T. et al.) LA-UR 04-7420 (Theoretical Biology and Biophysics Group, Los Alamos National Laboratory, New Mexico, USA, 2004).
18. Ogg, G.S. et al. Quantitation of HIV-1-specific cytotoxic T lymphocytes and plasma load of viral RNA. Science 279, 2103-2106 (1998).
19. Goulder, P.J. et al. Substantial differences in specificity of HIV-specific cytotoxic T cells in acute and chronic HIV infection. J. Exp. Med. 193, 181-194 (2001).
20. Ogg, G.S. et al. Longitudinal phenotypic analysis of human immunodeficiency virus type 1-specific cytotoxic T lymphocytes: correlation with disease progression. J. Virol. 73, 9153-9160 (1999).
21. Yang, Z. PAML: A program package for phylogenetic analysis by maximum likelihood. Comput. Appl. Biosci. 13, 555-556 (1997).
22. Goulder, P.J. et al. 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 (2001).
23. Brander, C. et al. Lack of strong immune selection pressure by the immunodominant, HLA-A*0201-restricted cytotoxic T lymphocyte response in chronic human immunodeficiency virus-1 infection. J. Clin. Invest. 101, 2559-2566 (1998).
24. Sette, A. et al. The relationship between class I binding affinity and immunogenicity of potential cytotoxic T cell epitopes. J. Immunol. 153, 5586-5592 (1994).
25. Lee, J.K. et al. T cell cross-reactivity and conformational changes during TcR engagement. J. Exp. Med. 200, 1455-1466 (2004).
26. van der Merwe, P.A. & Davis, S.J. Molecular interactions mediating T cell antigen recognition. Annu. Rev. Immunol. 21, 659-684 (2003).
27. Madden, D.R., Garboczi, D.N. & Wiley, D.C. The antigenic identity of peptide-MHC complexes: A comparison of the conformations of five viral peptides presented by HLA-A2. Cell 75, 693-708 (1993).
28. Ding, Y.H. et al. Two human T cell receptors bind in a similar diagonal mode to the HLA-A2/Tax peptide complex using different TCR amino acids. Immunity 8, 403-411 (1998).
29. Garboczi, D.N. et al. Structure of the complex between human T-cell receptor, viral peptide and HLA-A2. Nature 384, 134-141 (1996).
30. Stewart-Jones, G.B., McMichael, A.J., Bell, J.I., Stuart, D.I. & Jones, E.Y. A structural basis for immunodominant human T cell receptor recognition. Nat. Immunol. 4, 657-663 (2003).
31. Edwards, C.T., Pfafferott, K.J., Goulder, P.J., Phillips, R.E. & Holmes, E.C. Intrapatient escape in the A*0201-restricted epitope SLYNTVATL drives evolution of human immunodeficiency virus type 1 at the population level. J. Virol. 79, 9363-9366 (2005).
32. Feeney, M.E. et al. Immune escape precedes breakthrough human immunodeficiency virus type 1 viremia and broadening of the cytotoxic T-lymphocyte response in an HLA-B27-positive long-term-nonprogressing child. J. Virol. 78, 8927-8930 (2004).
33. Goulder, P.J. et al. Combined structural and immunological refinement of HIV-1 HLA-B8-restricted cytotoxic T lymphocyte epitopes. Eur. J. Immunol. 27, 1515-1521 (1997).
34. Yokomaku, Y. et al. Impaired processing and presentation of cytotoxic-T-lymphocyte (CTL) epitopes are major escape mechanisms from CTL immune/pressure in human immunodeficiency virus type 1 infection. J. Virol. 78, 1324-1332 (2004).
35. Matano, T. et al. Cytotoxic T lymphocyte-based control of simian immunodeficiency virus replication in a preclinical AIDS vaccine trial. J. Exp. Med. 199, 1709-1718 (2004).
36. Friedrich, T.C. et al. Reversion of CTL escape-variant immunodeficiency viruses in vivo. Nat. Med. 10, 275-281 (2004).
37. Kan-Mitchell, J. et al. The HIV-1 HLA-A2-SLYNTVATL is a help-independent CTL epitope. J. Immunol. 172, 5249-5261 (2004).
38. Sun, J.C. & Bevan, M.J. Defective CD8 T cell memory following acute infection without CD4 T cell help. Science 300, 339-342 (2003).
39. Shedlock, D.J. & Shen, H. Requirement for CD4 T cell help in generating functional CD8 T cell memory. Science 300, 337-339 (2003).
40. Krogsgaard, M. et al. Evidence that structural rearrangements and/or flexibility during TCR binding can contribute to T cell activation. Mol. Cell 12, 1367-1378 (2003).
41. Iversen, A.K. et al. Cervical human immunodeficiency virus type 1 shedding is associated with genital beta-chemokine secretion. J. Infect Dis. 178, 1334-1342 (1998).
42. Iversen, A.K. et al. Distinct determinants of human immunodeficiency virus type 1 RNA and DNA loads in vaginal and cervical secretions. J. Infect Dis. 177, 1214-1220 (1998).
43. Iversen, A. K. et al. Presence of multiple HIV subtypes and a high frequency of subtype chimeric viruses in heterosexually infected women. J. Acquir. Immune Defic. Syndr. 22, 325-332 (1999).
44. Brander, C. et al. Efficient processing of the immunodominant, HLA-A*0201-restricted human immunodeficiency virus type 1 cytotoxic T-lymphocyte epitope despite multiple variations in the epitope flanking sequences. J. Virol. 73, 10191-10198 (1999).
45. Goulder, P.J. et al. Mother-to-child transmission of HIV infection and CTL escape through HLA-A2-SLYNTVATL epitope sequence variation. Immunol. Lett. 79, 109-116 (2001).
46. Goulder, P.J. et al. Patterns of immunodominance in HIV-1-specific cytotoxic T lymphocyte responses in two human histocompatibility leukocyte antigens (HLA)-identical siblings with HLA-A*0201 are influenced by epitope mutation. J. Exp. Med. 185, 1423-1433 (1997).
47. Sylvester-Hvid, C. et al. Establishment of a quantitative ELISA capable of determining peptide - MHC class I interaction. Tissue Antigens 59, 251-258 (2002).
48. Dong, T. et al. An HLA-B35-restricted epitope modified at an anchor residue results in an antagonist peptide. Eur. J. Immunol. 26, 335-339 (1996).
49. Garboczi, D.N., Madden, D.R. & Wiley, D.C. Five viral peptide-HLA-A2 co-crystals. Simultaneous space group determination and X-ray data collection. J. Mol. Biol. 239, 581-587 (1994).
50. Willcox, B.E. et al. TCR binding to peptide-MHC stabilizes a flexible recognition interface. Immunity 10, 357-365 (1999).
51. Parham, P. & Brodsky, F.M. Partial purification and some properties of BB7.2. A cytotoxic monoclonal antibody with specificity for HLA-A2 and a variant of HLA-A28. Hum. Immunol. 3, 277-299 (1981).
52. Otwinowski, Z. & Minor, W. Processing of X-ray diffraction data collected in oscillation mode. Methods Enzymol. 276, 307-326 (1997).
53. Thompson, J.D., Higgins, D.G. & Gibson, T.J. CLUSTAL W: Improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice. Nucleic Acids Res. 22, 4673-4680 (1994).
54. Maddison, W.P. & Maddison, D.R. MacClade - Analysis of Phylogeny and Character Evolution - Version 4, (Sinauer Associates, Inc., Sunderland, MA, 2001).
55. Learn, G.H., Jr. et al. Maintaining the integrity of human immunodeficiency virus sequence databases. J. Virol. 70, 5720-5730 (1996).
56. Rose, P.P. & Korber, B.T. Detecting hypermutations in viral sequences with an emphasis on G → A hypermutation. Bioinformatics 16, 400-401 (2000).
57. Iversen, A.K. Genital HIV shedding in women. AIDS Patient Care STDS 13, 695-701 (1999).
58. Huelsenbeck, J.P. & Crandall, K.A. Phylogeny estimation and hypothesis testing using maximum likelihood. Annu. Rev. Ecol. Syst 28, 437-466 (1997).
59. Posada, D. & Crandall, K.A. MODELTEST: Testing the model of DNA substitution. Bioinformatics 14, 817-818 (1998).
60. Swofford, D.L. PAUP* 4.0: Phylogenetic Analysis Using Parsimony (*and Other Methods) 4.0b2a edn. (Sinauer Associates, Sunderland, Massachusetts, 1999).
61. Akaike, H. A new look at statistical model identification. IEEE Trans. Autom. Contr. 19, 716-723 (1974).
62. Yang, Z. Maximum likelihood estimation on large phylogenies and analysis of adaptive evolution in human influenza virus A. J. Mol. Evol. 51, 423-432 (2000).
63. Nielsen, R. & Yang, Z. Likelihood models for detecting positively selected amino acid sites and applications to the HIV-1 envelope gene. Genetics 148, 929-936 (1998).
64. Hill, C.P., Worthylake, D., Bancroft, D.P., Christensen, A.M. & Sundquist, W.I. Crystal structures of the trimeric human immunodeficiency virus type 1 matrix protein: Implications for membrane association and assembly. Proc. Natl Acad. Sci. USA 93, 3099-3104 (1996).