CTL escape mediated by proteasomal destruction of an HIV-1 cryptic epitope

PLoS Pathogens

Volumn 7, Issue 5, 2011, Pages

  Cardinaud, Sylvain ^a   Consiglieri, Gesa ^b   Bouziat, Romain ^a,c   Urrutia, Alejandra ^a   Graff Dubois, Stéphanie ^a   Fourati, Slim ^d   Malet, Isabelle ^d   Guergnon, Julien ^a   Guihot, Amélie ^a   Katlama, Christine ^d   Autran, Brigitte ^a   van Endert, Peter ^a   Lemonnier, François A ^a,c   Appay, Victor ^a   Schwartz, Olivier ^c   Kloetzel, Peter M ^b   Moris, Arnaud ^a,c  

^a INSERM   (France)

^b CHARITÉ UNIVERSITÄTSMEDIZIN BERLIN   (Germany)

^c INSTITUT PASTEUR   (France)

^d PITIÉ SALPÊTRIÈRE HOSPITAL   (France)

Author keywords

[No Author keywords available]

Indexed keywords

ASPARAGINE; ASPARTIC ACID; EPITOPE; HLA B7 ANTIGEN; PROTEASOME; VIRUS DNA; GAG PROTEIN; HLA B*07 ANTIGEN; HLA-B*07 ANTIGEN; HUMAN IMMUNODEFICIENCY VIRUS ANTIGEN; VIRUS RNA;

ADULT; ALTERNATIVE READING FRAME; ANIMAL CELL; ARTICLE; CLINICAL ARTICLE; CONTROLLED STUDY; CROSS REACTION; CYTOTOXIC T LYMPHOCYTE; DNA POLYMORPHISM; DNA SEQUENCE; EX VIVO STUDY; FEMALE; HUMAN; HUMAN IMMUNODEFICIENCY VIRUS 1; HUMAN IMMUNODEFICIENCY VIRUS INFECTED PATIENT; IN VITRO STUDY; MALE; MASS SPECTROMETRY; MOLECULAR CLONING; NONHUMAN; NUCLEOTIDE SEQUENCE; PERIPHERAL BLOOD MONONUCLEAR CELL; PREVALENCE; PROTEIN DEGRADATION; PROVIRUS; VIRUS STRAIN; AMINO ACID SEQUENCE; ANIMAL; ANTIGEN PRESENTATION; BAGG ALBINO MOUSE; CHEMISTRY; GENETIC POLYMORPHISM; GENETICS; HUMAN IMMUNODEFICIENCY VIRUS INFECTION; IMMUNOLOGY; METABOLISM; MIDDLE AGED; MOLECULAR GENETICS; MOUSE; MUTATION; PHYSIOLOGY; VIROLOGY; VIRUS LOAD;

HUMAN IMMUNODEFICIENCY VIRUS 1;

ADULT; AMINO ACID SEQUENCE; ANIMALS; ANTIGEN PRESENTATION; EPITOPES, T-LYMPHOCYTE; FEMALE; GAG GENE PRODUCTS, HUMAN IMMUNODEFICIENCY VIRUS; HIV ANTIGENS; HIV INFECTIONS; HIV-1; HLA-B7 ANTIGEN; HUMANS; MALE; MICE; MICE, INBRED BALB C; MIDDLE AGED; MOLECULAR SEQUENCE DATA; MUTATION; POLYMORPHISM, GENETIC; PROTEASOME ENDOPEPTIDASE COMPLEX; RNA, VIRAL; SEQUENCE ANALYSIS, DNA; T-LYMPHOCYTES, CYTOTOXIC; VIRAL LOAD; YOUNG ADULT;

EID: 79958071899     PISSN: 15537366     EISSN: 15537374     Source Type: Journal    
DOI: 10.1371/journal.ppat.1002049     Document Type: Article

References (62)

1. Wang YE, Li B, Carlson JM, Streeck H, Gladden AD, et al. (2009) Protective HLA class I alleles that restrict acute-phase CD8+ T-cell responses are associated with viral escape mutations located in highly conserved regions of human immunodeficiency virus type 1. J Virol 83: 1845-1855.
2. 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.
3. Koup RA, Safrit JT, Cao Y, Andrews CA, Leod GM, et al. (1994) Temporal association of cellular immune responses with the initial control of viremia in primary human immunodeficiency virus type 1 syndrome. J Virol 68: 4650-4655.
4. Kiepiela P, Leslie AJ, Honeyborne I, Ramduth D, Thobakgale C, et al. (2004) Dominant influence of HLA-B in mediating the potential co-evolution of HIV and HLA. Nature 432: 769-775.
5. 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.
6. Brumme ZL, John M, Carlson JM, Brumme CJ, Chan D, et al. (2009) HLA-associated immune escape pathways in HIV-1 subtype B Gag, Pol and Nef proteins. PLoS One 4: e6687.
7. Duda A, Lee-Turner L, Fox J, Robinson N, Dustan S, et al. (2009) HLA-associated clinical progression correlates with epitope reversion rates in early human immunodeficiency virus infection. J Virol 83: 1228-1239.
8. Goulder PJ, Brander C, Tang Y, Tremblay C, Colbert RA, et al. (2001) Evolution and transmission of stable CTL escape mutations in HIV infection. Nature 412: 334-338.
9. 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.
10. Koizumi H, Hashimoto M, Fujiwara M, Murakoshi H, Chikata T, et al. (2010) Different in vivo effects of HIV-1 immunodominant epitope-specific CTLs on selection of escape mutant viruses. J Virol 84: 5508-19.
11. Philips RE, Rowland-Jones S, Nixon DF, Gotch FM, Edwards JP, et al. (1991) Human immunodeficiency virus genetic variation that can escape cytotoxic T cell recognition. Nature 354: 453-459.
12. Borrow P, Lewicki H, Wei X, Horwitz MS, Peffer N, et al. (1997) 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.
13. Goulder PJ, Phillips RE, Colbert RA, McAdam S, Ogg G, et al. (1997) Late escape from an immunodominant cytotoxic T-lymphocyte response associated with progression to AIDS. Nat Med 3: 212-217.
14. Goulder PJ, Watkins DI, (2004) HIV and SIV CTL escape: implications for vaccine design. Nat Rev Immunol 4: 630-640.
15. 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: 636-646.
16. Draenert R, Le Gall S, Pfafferott KJ, Leslie AJ, 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.
17. Le Gall S, Stamegna P, Walker BD, (2007) Portable flanking sequences modulate CTL epitope processing. J Clin Invest 117: 3563-3575.
18. Milicic A, Price DA, Zimbwa P, Booth BL, Brown HL, et al. (2005) CD8+ T cell epitope-flanking mutations disrupt proteasomal processing of HIV-1 Nef. J Immunol 175: 4618-4626.
19. Zimbwa P, Milicic A, Frater J, Scriba TJ, Willis A, et al. (2007) Precise identification of a human immunodeficiency virus type 1 antigen processing mutant. J Virol 81: 2031-2038.
20. 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.
21. Schubert U, Anton LC, Gibbs J, Norbury CC, Yewdell JW, et al. (2000) Rapid degradation of a large fraction of newly synthesized proteins by proteasomes. Nature 404: 770-774.
22. Casartelli N, Guivel-Benhassine F, Bouziat R, Brandler S, Schwartz O, et al. (2010) The antiviral factor APOBEC3G improves CTL recognition of cultured HIV-infected T cells. J Exp Med 207: 39-49.
23. Cardinaud S, Starck SR, Chandra P, Shastri N, (2010) The synthesis of truncated polypeptides for immune surveillance and viral evasion. PLoS One 5: e8692.
24. Cardinaud S, Bouziat R, Rohrlich PS, Tourdot S, Weiss L, et al. (2009) Design of a HIV-1-derived HLA-B07.02-restricted polyepitope construct. Aids 23: 1945-1954.
25. Ho O, Green WR, (2006) Alternative translational products and cryptic T cell epitopes: expecting the unexpected. J Immunol 177: 8283-8289.
26. Saulquin X, Scotet E, Trautmann L, Peyrat MA, Halary F, et al. (2002) +1 Frameshifting as a novel mechanism to generate a cryptic cytotoxic T lymphocyte epitope derived from human interleukin 10. J Exp Med 195: 353-358.
27. Wang RF, Parkhurst MR, Kawakami Y, Robbins PF, Rosenberg SA, (1996) Utilization of an alternative open reading frame of a normal gene in generating a novel human cancer antigen. J Exp Med 183: 1131-1140.
28. Godet Y, Moreau-Aubry A, Guilloux Y, Vignard V, Khammari A, et al. (2008) MELOE-1 is a new antigen overexpressed in melanomas and involved in adoptive T cell transfer efficiency. J Exp Med 205: 2673-2682.
29. Bullock TN, Eisenlohr LC, (1996) Ribosomal scanning past the primary initiation codon as a mechanism for expression of CTL epitopes encoded in alternative reading frames. J Exp Med 184: 1319-1329.
30. Mayrand SM, Schwarz DA, Green WR, (1998) An alternative translational reading frame encodes an immunodominant retroviral CTL determinant expressed by an immunodeficiency-causing retrovirus. J Immunol 160: 39-50.
31. Maness NJ, Valentine LE, May GE, Reed J, Piaskowski SM, et al. (2007) AIDS virus specific CD8+ T lymphocytes against an immunodominant cryptic epitope select for viral escape. J Exp Med 204: 2505-2512.
32. Cardinaud S, Moris A, Fevrier M, Rohrlich PS, Weiss L, et al. (2004) Identification of cryptic MHC I-restricted epitopes encoded by HIV-1 alternative reading frames. J Exp Med 199: 1053-1063.
33. Bansal A, Carlson J, Yan J, Akinsiku OT, Schaefer M, et al. (2010) CD8 T cell response and evolutionary pressure to HIV-1 cryptic epitopes derived from antisense transcription. J Exp Med 207: 51-59, S51-53.
34. Berger CT, Carlson JM, Brumme CJ, Hartman KL, Brumme ZL, et al. (2010) Viral adaptation to immune selection pressure by HLA class I-restricted CTL responses targeting epitopes in HIV frameshift sequences. J Exp Med 207: 61-75, S61-12.
35. Schweighardt B, Wrin T, Meiklejohn DA, Spotts G, Petropoulos CJ, et al. (2010) Immune escape mutations detected within HIV-1 epitopes associated with viral control during treatment interruption. J Acquir Immune Defic Syndr 53: 36-46.
36. Garrison KE, Champiat S, York VA, Agrawal AT, Kallas EG, et al. (2009) Transcriptional errors in human immunodeficiency virus type 1 generate targets for T-cell responses. Clin Vaccine Immunol 16: 1369-1371.
37. Rohrlich PS, Cardinaud S, Firat H, Lamari M, Briand P, et al. (2003) HLA-B*0702 transgenic, H-2K(b)D(b) double-knockout mice: phenotypical and functional characterization in response to influenza virus. Int Immunol 15: 765-772.
38. Kloetzel PM, (2001) Antigen processing by the proteasome. Nat Rev Mol Cell Biol 2: 179-187.
39. Falk K, Rotzschke O, Stevanovic S, Jung G, Rammensee HG, (1991) Allele-specific motifs revealed by sequencing of self-peptides eluted from MHC molecules. Nature 351: 290-296.
40. Rammensee H, Bachmann J, Emmerich NP, Bachor OA, Stevanovic S, (1999) SYFPEITHI: database for MHC ligands and peptide motifs. Immunogenetics 50: 213-219.
41. Lauvau G, Kakimi K, Niedermann G, Ostankovitch M, Yotnda P, et al. (1999) Human transporters associated with antigen processing (TAPs) select epitope precursor peptides for processing in the endoplasmic reticulum and presentation to T cells. J Exp Med 190: 1227-1240.
42. Serwold T, Gaw S, Shastri N, (2001) ER aminopeptidases generate a unique pool of peptides for MHC class I molecules. Nat Immunol 2: 644-651.
43. Saric T, Beninga J, Graef CI, Akopian TN, Rock KL, et al. (2001) Major histocompatibility complex class I-presented antigenic peptides are degraded in cytosolic extracts primarily by thimet oligopeptidase. J Biol Chem 276: 36474-36481.
44. van Endert PM, Riganelli D, Greco G, Fleischhauer K, Sidney J, et al. (1995) The peptide-binding motif for the human transporter associated with antigen processing. J Exp Med 182: 1883-1895.
45. 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.
46. Moris A, Nobile C, Buseyne F, Porrot F, Abastado JP, et al. (2004) DC-SIGN promotes exogenous MHC-I-restricted HIV-1 antigen presentation. Blood 103: 2648-2654.
47. Ossendorp F, Eggers M, Neisig A, Ruppert T, Groettrup M, et al. (1996) A single residue exchange within a viral CTL epitope alters proteasome-mediated degradation resulting in lack of antigen presentation. Immunity 5: 115-124.
48. Chapiro J, Claverol S, Piette F, Ma W, Stroobant V, et al. (2006) Destructive cleavage of antigenic peptides either by the immunoproteasome or by the standard proteasome results in differential antigen presentation. J Immunol 176: 1053-1061.
49. Gavioli R, Gallerani E, Fortini C, Fabris M, Bottoni A, et al. (2004) HIV-1 tat protein modulates the generation of cytotoxic T cell epitopes by modifying proteasome composition and enzymatic activity. J Immunol 173: 3838-3843.
50. Toes RE, Nussbaum AK, Degermann S, Schirle M, Emmerich NP, et al. (2001) Discrete cleavage motifs of constitutive and immunoproteasomes revealed by quantitative analysis of cleavage products. J Exp Med 194: 1-12.
51. Kuckelkorn U, Ferreira EA, Drung I, Liewer U, Kloetzel PM, et al. (2002) The effect of the interferon-gamma-inducible processing machinery on the generation of a naturally tumor-associated human cytotoxic T lymphocyte epitope within a wild-type and mutant p53 sequence context. Eur J Immunol 32: 1368-1375.
52. Schwab SR, Li KC, Kang C, Shastri N, (2003) Constitutive display of cryptic translation products by MHC class I molecules. Science 301: 1367-1371.
53. Watts JM, Dang KK, Gorelick RJ, Leonard CW, Bess JW Jr, et al. (2009) Architecture and secondary structure of an entire HIV-1 RNA genome. Nature 460: 711-716.
54. Allen TM, Altfeld M, Geer SC, Kalife ET, Moore C, et al. (2005) Selective escape from CD8+ T-cell responses represents a major driving force of human immunodeficiency virus type 1 (HIV-1) sequence diversity and reveals constraints on HIV-1 evolution. J Virol 79: 13239-13249.
55. Parcej D, Tampe R, (2010) ABC proteins in antigen translocation and viral inhibition. Nat Chem Biol 6: 572-580.
56. Basler M, Youhnovski N, Van Den Broek M, Przybylski M, Groettrup M, (2004) Immunoproteasomes down-regulate presentation of a subdominant T cell epitope from lymphocytic choriomeningitis virus. J Immunol 173: 3925-3934.
57. Almeida JR, Price DA, Papagno L, Arkoub ZA, Sauce D, et al. (2007) Superior control of HIV-1 replication by CD8+ T cells is reflected by their avidity, polyfunctionality, and clonal turnover. J Exp Med 204: 2473-2485.
58. Maness NJ, Wilson NA, Reed JS, Piaskowski SM, Sacha JB, et al. (2010) Robust, vaccine-induced CD8(+) T lymphocyte response against an out-of-frame epitope. J Immunol 184: 67-72.
59. Martinez V, Costagliola D, Bonduelle O, N'go N, Schnuriger A, et al. (2005) Combination of HIV-1-specific CD4 Th1 cell responses and IgG2 antibodies is the best predictor for persistence of long-term nonprogression. J Infect Dis 191: 2053-2063.
60. Bunce M, O'Neill CM, Barnardo MC, Krausa P, Browning MJ, et al. (1995) Phototyping: comprehensive DNA typing for HLA-A, B, C, DRB1, DRB3, DRB4, DRB5 & DQB1 by PCR with 144 primer mixes utilizing sequence-specific primers (PCR-SSP). Tissue Antigens 46: 355-367.
61. Dunbar SA, (2006) Applications of Luminex xMAP technology for rapid, high-throughput multiplexed nucleic acid detection. Clin Chim Acta 363: 71-82.
62. Moris A, Pajot A, Blanchet F, Guivel-Benhassine F, Salcedo M, et al. (2006) Dendritic cells and HIV-specific CD4+ T cells: HIV antigen presentation, T-cell activation, and viral transfer. Blood 108: 1643-1651.