The Antiviral Efficacy of HIV-Specific CD8+ T-Cells to a Conserved Epitope is Heavilydependent on the Infecting HIV-1 Isolate

PLoS Pathogens

Volumn 7, Issue 5, 2011, Pages

  Ranasinghe, Srinika R F ^a,d   Kramer, Holger B ^b   Wright, Cynthia ^b   Kessler, Benedikt M ^b   di Gleria, Katalin ^a   Zhang, Yonghong ^a,c   Gillespie, Geraldine M ^a   Blais, Marie Eve ^a   Culshaw, Abigail ^a   Pichulik, Tica ^a   Simmons, Alison ^a   Rowland Jones, Sarah L ^a   McMichael, Andrew J ^a   Dong, Tao ^a  

^a UNIVERSITY OF OXFORD   (United Kingdom)

^b UNIVERSITY OF OXFORD   (United Kingdom)

^c CAPITAL MEDICAL UNIVERSITY   (China)

^d MASSACHUSETTS GENERAL HOSPITAL   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

EPITOPE; HLA B8 ANTIGEN; NEF PROTEIN; VIRUS RNA; GAMMA INTERFERON; HUMAN IMMUNODEFICIENCY VIRUS ANTIGEN; HUMAN IMMUNODEFICIENCY VIRUS VACCINE; PROTEASOME; VIRUS DNA;

ANTIGEN PRESENTATION; ANTIVIRAL ACTIVITY; ARTICLE; CD8+ T LYMPHOCYTE; CLADISTICS; CYTOTOXIC T LYMPHOCYTE; DNA FLANKING REGION; DRUG EFFICACY; FLOW CYTOMETRY; GENETIC VARIABILITY; HUMAN IMMUNODEFICIENCY VIRUS 1; IMMUNE RESPONSE; MOLECULAR RECOGNITION; NONHUMAN; PROTEIN CLEAVAGE; VACCINIA; VIRUS EXPRESSION; VIRUS STRAIN; AMINO ACID SEQUENCE; CHEMISTRY; DNA SEQUENCE; ENZYME LINKED IMMUNOSPOT ASSAY; GENETIC POLYMORPHISM; GENETICS; HUMAN; HUMAN IMMUNODEFICIENCY VIRUS INFECTION; IMMUNOLOGY; METABOLISM; MOLECULAR GENETICS; MUTATION; NUCLEOTIDE SEQUENCE; PHYSIOLOGY; STANDARD; VACCINIA VIRUS; VIROLOGY;

HUMAN IMMUNODEFICIENCY VIRUS 1; VACCINIA VIRUS;

AIDS VACCINES; AMINO ACID SEQUENCE; ANTIGEN PRESENTATION; CONSERVED SEQUENCE; DNA, VIRAL; ENZYME-LINKED IMMUNOSPOT ASSAY; EPITOPES, T-LYMPHOCYTE; HIV ANTIGENS; HIV INFECTIONS; HIV-1; HLA-B8 ANTIGEN; HUMANS; INTERFERON-GAMMA; MOLECULAR SEQUENCE DATA; MUTATION; NEF GENE PRODUCTS, HUMAN IMMUNODEFICIENCY VIRUS; POLYMORPHISM, GENETIC; PROTEASOME ENDOPEPTIDASE COMPLEX; SEQUENCE ANALYSIS, DNA; T-LYMPHOCYTES, CYTOTOXIC; VACCINIA VIRUS;

EID: 79958051220     PISSN: 15537366     EISSN: 15537374     Source Type: Journal    
DOI: 10.1371/journal.ppat.1001341     Document Type: Article

References (65)

1. McMichael A, Mwau M, Hanke T, (2002) HIV T cell vaccines, the importance of clades. Vaccine 20: 1918-1921.
2. Gaschen B, Taylor J, Yusim K, Foley B, Gao F, et al. (2002) Diversity considerations in HIV-1 vaccine selection. Science 296: 2354-2360.
3. Walker B, Korber B, (2001) Immune control of HIV: the obstacles of HLA and viral diversity. Nat Immunol 2: 473-475.
4. McMichael A, Rowland-Jones S, (2001) Cellular immune responses to HIV. Nature 410: 980-987.
5. McMichael AJ, (2006) HIV vaccines. Annu Rev Immunol 24: 227-255.
6. Letourneau S, Im EJ, Mashishi T, Brereton C, Bridgeman A, et al. (2007) Design and pre-clinical evaluation of a universal HIV-1 vaccine. PLoS One 2: e984.
7. Finnefrock AC, Liu X, Opalka DW, Shiver JW, Casimiro DR, et al. (2007) HIV type 1 vaccines for worldwide use: predicting in-clade and cross-clade breadth of immune responses. AIDS Res Hum Retroviruses 23: 1283-1292.
8. Frahm N, Nickle DC, Linde CH, Cohen DE, Zuniga R, et al. (2008) Increased detection of HIV-specific T cell responses by combination of central sequences with comparable immunogenicity. Aids 22: 447-456.
9. Santra S, Korber BT, Muldoon M, Barouch DH, Nabel GJ, et al. (2008) A centralized gene-based HIV-1 vaccine elicits broad cross-clade cellular immune responses in rhesus monkeys. Proc Natl Acad Sci U S A 105: 10489-10494.
10. Allen TM, Altfeld M, (2008) Crippling HIV one mutation at a time. J Exp Med 205: 1003-1007.
11. Streeck H, Frahm N, Walker B, (2009) The role of IFN-gamma Elispot assay in HIV vaccine research. Nat Protoc 4: 461-469.
12. Altfeld M, Addo MM, Shankarappa R, Lee PK, Allen TM, et al. (2003) Enhanced detection of human immunodeficiency virus type 1-specific T-cell responses to highly variable regions by using peptides based on autologous virus sequences. J Virol 77: 7330-7340.
13. Goonetilleke N, Liu MK, Salazar-Gonzalez JF, Ferrari G, Giorgi E, et al. (2009) The first T cell response to transmitted/founder virus contributes to the control of acute viremia in HIV-1 infection. J Exp Med 206: 1253-1272.
14. Lee JK, Stewart-Jones G, Dong T, Harlos K, Di Gleria K, et al. (2004) T cell cross-reactivity and conformational changes during TCR engagement. J Exp Med 200: 1455-1466.
15. Moore CB, John M, James IR, Christiansen FT, Witt CS, et al. (2002) Evidence of HIV-1 adaptation to HLA-restricted immune responses at a population level. Science 296: 1439-1443.
16. Matthews PC, Leslie AJ, Katzourakis A, Crawford H, Payne R, et al. (2009) HLA footprints on human immunodeficiency virus type 1 are associated with interclade polymorphisms and intraclade phylogenetic clustering. J Virol 83: 4605-4615.
17. Bennett M, Ng H, Ali A, Yang O, (2008) Cross-clade detection of HIV-1-specific cytotoxic T lymphocytes does not reflect cross-clade antiviral activity. J Infect Dis 197: 390-397.
18. D'Souza M, Altfeld M, (2008) Measuring HIV-1-specific T cell immunity: how valid are current assays? J Infect Dis 197: 337-339.
19. Le Gall S, Stamegna P, Walker B, (2007) Portable flanking sequences modulate CTL epitope processing. J Clin Invest 117: 3563-3575.
20. Tenzer S, Wee E, Burgevin A, Stewart-Jones G, Friis L, et al. (2009) Antigen processing influences HIV-specific cytotoxic T lymphocyte immunodominance. Nat Immunol 10 (6): 636-46.
21. Zimbwa P, Milicic A, Frater J, Scriba T, Willis A, et al. (2007) Precise identification of a human immunodeficiency virus type 1 antigen processing mutant. J Virol 81: 2031-2038.
22. Allen T, Altfeld M, Yu X, O'Sullivan K, Lichterfeld M, et al. (2004) Selection, transmission, and reversion of an antigen-processing cytotoxic T-lymphocyte escape mutation in human immunodeficiency virus type 1 infection. J Virol 78: 7069-7078.
23. Draenert R, Le Gall S, Pfafferott K, Leslie A, Chetty P, et al. (2004) Immune selection for altered antigen processing leads to cytotoxic T lymphocyte escape in chronic HIV-1 infection. J Exp Med 199: 905-915.
24. Milicic A, Price D, Zimbwa P, Booth B, Brown H, et al. (2005) CD8+ T cell epitope-flanking mutations disrupt proteasomal processing of HIV-1 Nef. J Immunol 175: 4618-4626.
25. Yokomaku Y, Miura H, Tomiyama H, Kawana-Tachikawa A, Takiguchi M, et al. (2004) 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.
26. Seifert U, Liermann H, Racanelli V, Halenius A, Wiese M, et al. (2004) Hepatitis C virus mutation affects proteasomal epitope processing. J Clin Invest 114: 250-259.
27. Kimura Y, Gushima T, Rawale S, Kaumaya P, Walker C, (2005) Escape mutations alter proteasome processing of major histocompatibility complex class I-restricted epitopes in persistent hepatitis C virus infection. J Virol 79: 4870-4876.
28. Kawashima Y, Pfafferott K, Frater J, Matthews P, Payne R, et al. (2009) Adaptation of HIV-1 to human leukocyte antigen class I. Nature 458: 641-645.
29. Loffredo JT, Burwitz BJ, Rakasz EG, Spencer SP, Stephany JJ, et al. (2007) The antiviral efficacy of simian immunodeficiency virus-specific CD8+ T cells is unrelated to epitope specificity and is abrogated by viral escape. J Virol 81: 2624-2634.
30. Yang OO, Kalams SA, Trocha A, Cao H, Luster A, et al. (1997) Suppression of human immunodeficiency virus type 1 replication by CD8+ cells: evidence for HLA class I-restricted triggering of cytolytic and noncytolytic mechanisms. J Virol 71: 3120-3128.
31. Collins KL, Chen BK, Kalams SA, Walker BD, Baltimore D, (1998) HIV-1 Nef protein protects infected primary cells against killing by cytotoxic T lymphocytes. Nature 391: 397-401.
32. Ali A, Realegeno S, Yang OO, Lewis MJ, (2009) Simultaneous assessment of CD4 and MHC-I downregulation by Nef primary isolates in the context of infection. J Virol Methods 161: 297-304.
33. Lewis MJ, Balamurugan A, Ohno A, Kilpatrick S, Ng HL, et al. (2008) Functional adaptation of Nef to the immune milieu of HIV-1 infection in vivo. J Immunol 180: 4075-4081.
34. Kessler B, Glas R, Ploegh H, (2002) MHC class I antigen processing regulated by cytosolic proteolysis-short cuts that alter peptide generation. Mol Immunol 39: 171-179.
35. Seifert U, Maranon C, Shmueli A, Desoutter JF, Wesoloski L, et al. (2003) An essential role for tripeptidyl peptidase in the generation of an MHC class I epitope. Nat Immunol 4: 375-379.
36. Kloetzel P, (2004) Generation of major histocompatibility complex class I antigens: functional interplay between proteasomes and TPPII. Nat Immunol 5: 661-669.
37. Yewdell J, Reits E, Neefjes J, (2003) Making sense of mass destruction: quantitating MHC class I antigen presentation. Nat Rev Immunol 3: 952-961.
38. Lucchiari-Hartz M, Lindo V, Hitziger N, Gaedicke S, Saveanu L, et al. (2003) Differential proteasomal processing of hydrophobic and hydrophilic protein regions: contribution to cytotoxic T lymphocyte epitope clustering in HIV-1-Nef. Proc Natl Acad Sci U S A 100: 7755-7760.
39. Mo AX, van Lelyveld SF, Craiu A, Rock KL, (2000) Sequences that flank subdominant and cryptic epitopes influence the proteolytic generation of MHC class I-presented peptides. J Immunol 164: 4003-4010.
40. Cascio P, Hilton C, Kisselev AF, Rock KL, Goldberg AL, (2001) 26S proteasomes and immunoproteasomes produce mainly N-extended versions of an antigenic peptide. EMBO J 20: 2357-2366.
41. Kessler BM, Glas R, Ploegh HL, (2002) MHC class I antigen processing regulated by cytosolic proteolysis-short cuts that alter peptide generation. Mol Immunol 39: 171-179.
42. Gaczynska M, Rock KL, Spies T, Goldberg AL, (1994) Peptidase activities of proteasomes are differentially regulated by the major histocompatibility complex-encoded genes for LMP2 and LMP7. Proc Natl Acad Sci U S A 91: 9213-9217.
43. Altfeld M, Allen T, Yu X, Johnston M, Agrawal D, et al. (2002) HIV-1 superinfection despite broad CD8+ T-cell responses containing replication of the primary virus. Nature 420: 434-439.
44. McElrath M, De Rosa S, Moodie Z, Dubey S, Kierstead L, et al. (2008) HIV-1 vaccine-induced immunity in the test-of-concept Step Study: a case-cohort analysis. Lancet 372: 1894-1905.
45. Altfeld M, Allen TM, (2006) Hitting HIV where it hurts: an alternative approach to HIV vaccine design. Trends Immunol 27: 504-510.
46. Goepfert PA, Lumm W, Farmer P, Matthews P, Prendergast A, et al. (2008) Transmission of HIV-1 Gag immune escape mutations is associated with reduced viral load in linked recipients. J Exp Med 205: 1009-1017.
47. Kiepiela P, Ngumbela K, Thobakgale C, Ramduth D, Honeyborne I, et al. (2007) CD8+ T-cell responses to different HIV proteins have discordant associations with viral load. Nat Med 13: 46-53.
48. Lichterfeld M, Yu X, Le Gall S, Altfeld M, (2005) Immunodominance of HIV-1-specific CD8(+) T-cell responses in acute HIV-1 infection: at the crossroads of viral and host genetics. Trends Immunol 26: 166-171.
49. Altfeld M, Kalife E, Qi Y, Streeck H, Lichterfeld M, et al. (2006) HLA Alleles Associated with Delayed Progression to AIDS Contribute Strongly to the Initial CD8(+) T Cell Response against HIV-1. PLoS Med 3: e403.
50. Price D, Goulder P, Klenerman P, Sewell A, Easterbrook P, et al. (1997) Positive selection of HIV-1 cytotoxic T lymphocyte escape variants during primary infection. Proc Natl Acad Sci U S A 94: 1890-1895.
51. Yang OO, Sarkis PT, Ali A, Harlow JD, Brander C, et al. (2003) Determinant of HIV-1 mutational escape from cytotoxic T lymphocytes. J Exp Med 197: 1365-1375.
52. Lubong Sabado R, Kavanagh D, Kaufmann D, Fru K, Babcock E, et al. (2009) In vitro priming recapitulates in vivo HIV-1 specific T cell responses, revealing rapid loss of virus reactive CD4 T cells in acute HIV-1 infection. PLoS One 4: e4256.
53. Streeck H, Jolin J, Qi Y, Yassine-Diab B, Johnson R, et al. (2009) HIV-1-specific CD8+ T cell responses during primary infection are major determinants of the viral set point and loss of CD4+ T cells. J Virol 83 (15): 7641-8.
54. Kloetzel PM, (2001) Antigen processing by the proteasome. Nat Rev Mol Cell Biol 2: 179-187.
55. Kloetzel PM, Ossendorp F, (2004) Proteasome and peptidase function in MHC-class-I-mediated antigen presentation. Curr Opin Immunol 16: 76-81.
56. Yewdell J, (2005) Immunoproteasomes: regulating the regulator. Proc Natl Acad Sci U S A 102: 9089-9090.
57. Kisselev A, Akopian T, Woo K, Goldberg A, (1999) The sizes of peptides generated from protein by mammalian 26 and 20 S proteasomes. Implications for understanding the degradative mechanism and antigen presentation. J Biol Chem 274: 3363-3371.
58. Cascio P, Hilton C, Kisselev A, Rock K, Goldberg A, (2001) 26S proteasomes and immunoproteasomes produce mainly N-extended versions of an antigenic peptide. EMBO J 20: 2357-2366.
59. Samino Y, López D, Guil S, Saveanu L, van Endert P, et al. (2006) A long N-terminal-extended nested set of abundant and antigenic major histocompatibility complex class I natural ligands from HIV envelope protein. J Biol Chem 281: 6358-6365.
60. Reits E, Griekspoor A, Neijssen J, Groothuis T, Jalink K, et al. (2003) Peptide diffusion, protection, and degradation in nuclear and cytoplasmic compartments before antigen presentation by MHC class I. Immunity 18: 97-108.
61. Choppin J, Cohen W, Bianco A, Briand J, Connan F, et al. (2001) Characteristics of HIV-1 Nef regions containing multiple CD8+ T cell epitopes: wealth of HLA-binding motifs and sensitivity to proteasome degradation. J Immunol 166: 6164-6169.
62. Dong T, Stewart-Jones G, Chen N, Easterbrook P, Xu X, et al. (2004) HIV-specific cytotoxic T cells from long-term survivors select a unique T cell receptor. J Exp Med 200: 1547-1557.
63. Dong T, Stewart-Jones G, Chen N, Easterbrook P, Xu X, et al. (2004) HIV-specific cytotoxic T cells from long-term survivors select a unique T cell receptor. J Exp Med 200: 1547-1557.
64. Groettrup M, Soza A, Eggers M, Kuehn L, Dick T, et al. (1996) A role for the proteasome regulator PA28alpha in antigen presentation. Nature 381: 166-168.
65. Xu D, Suenaga N, Edelmann M, Fridman R, Muschel R, et al. (2008) Novel MMP-9 substrates in cancer cells revealed by a label-free quantitative proteomics approach. Mol Cell Proteomics 7: 2215-2228.