Multiple viral ligands naturally presented by different class I molecules in transporter antigen processing-deficient vaccinia virus-infected cells

Journal of Virology

Volumn 86, Issue 1, 2012, Pages 527-541

  Lorente, Elena ^a   Infantes, Susana ^a   Barnea, Eilon ^b   Beer, Ilan ^c   García, Ruth ^a   Lasala, Fátima ^a   Jiménez, Mercedes ^a   Vilches, Carlos ^d   Lemonnier, François A ^e   Admon, Arie ^b   López, Daniel ^a  

^a INSTITUTO DE SALUD CARLOS III   (Spain)

^b TECHNION ISRAEL INSTITUTE OF TECHNOLOGY   (Israel)

^c IBM HAIFA RESEARCH LAB   (Israel)

^d HOSPITAL UNIVERSITARIO PUERTA DE HIERRO   (Spain)

^e INSTITUT PASTEUR   (France)

Author keywords

[No Author keywords available]

Indexed keywords

EPITOPE; HLA A ANTIGEN; HLA A2 ANTIGEN; HLA B ANTIGEN; HLA B27 ANTIGEN; HLA B51 ANTIGEN; HLA C ANTIGEN; MEMBRANE PROTEIN; TRANSPORTER ASSOCIATED WITH ANTIGEN PROCESSING; UNCLASSIFIED DRUG;

ALLELE; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ANTIGEN PRESENTATION; ANTIGEN PURIFICATION; ANTIGEN RECOGNITION; ARTICLE; BINDING AFFINITY; CD8+ T LYMPHOCYTE; CELLULAR IMMUNITY; CONTROLLED STUDY; CYTOTOXIC T LYMPHOCYTE; GENETIC CONSERVATION; HUMAN; HUMAN CELL; HYDROPHOBICITY; IMMUNOGENICITY; IMMUNOLOGICAL MEMORY; LIGAND BINDING; MASS SPECTROMETRY; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN TRANSPORT; VACCINIA; VACCINIA VIRUS; VIRUS PATHOGENESIS;

ANIMALS; ANTIGEN PRESENTATION; ANTIGEN-PRESENTING CELLS; ATP-BINDING CASSETTE TRANSPORTERS; CD8-POSITIVE T-LYMPHOCYTES; CELL LINE; HISTOCOMPATIBILITY ANTIGENS CLASS I; HUMANS; LIGANDS; MICE; MICE, KNOCKOUT; VACCINIA; VACCINIA VIRUS;

COWPOX VIRUS; MUS MUSCULUS; VACCINIA VIRUS; VARIOLA VIRUS;

EID: 84855972135     PISSN: 0022538X     EISSN: 10985514     Source Type: Journal    
DOI: 10.1128/JVI.05737-11     Document Type: Article

References (73)

1. Alzhanova D, et al. 2009. Cowpox virus inhibits the transporter associated with antigen processing to evade T cell recognition. Cell Host. Microbe 6:433- 445.
2. Anderson KS, Alexander J, Wei M, Cresswell P. 1993. Intracellular transport of class I MHC molecules in antigen processing mutant cell lines. J. Immunol. 151:3407-3419.
3. Angel Rico MA, et al. 2009. Human respiratory syncytial virus infects and induces activation markers in mouse B lymphocytes. Immunol. Cell Biol. 87:344 -350.
4. Apostolopoulos V, Karanikas V, Haurum JS, McKenzie IF. 1997. Induction of HLA-A2-restricted CTLs to the mucin 1 human breast cancer antigen. J. Immunol. 159:5211-5218.
5. Assarsson E, et al. 2007. A quantitative analysis of the variables affecting the repertoire of T cell specificities recognized after vaccinia virus infection. J. Immunol. 178:7890 -7901.
6. Barnstable CJ, et al. 1978. Production of monoclonal antibodies to group A erythrocytes, HLA and other human cell surface antigens-new tools for genetic analysis. Cell 14:9 -20.
7. Barrett AJ. 2004. Metallopeptidases, p. 231-1047. InA. J. Barrett, N. D. Rawlings, and J. F. Woessner (ed.), Handbook of proteolytic enzymes. Academic Press, London, United Kingdom.
8. Bertoni R, et al. 1997. Human histocompatibility leukocyte antigenbinding supermotifs predict broadly cross-reactive cytotoxic T lymphocyte responses in patients with acute hepatitis. J. Clin. Invest. 100:503-513.
9. Cerundolo V, de la Salle H. 2006. Description of HLA class I- and CD8-deficient patients: insights into the function of cytotoxic T lymphocytes and NK cells in host defense. Semin. Immunol. 18:330 -336.
10. Chen W, Anton LC, Bennink JR, Yewdell JW. 2000. Dissecting the multifactorial causes of immunodominance in class I-restricted T cell responses to viruses. Immunity 12:83-93.
11. Cheuk E, et al. 2002. Human MHC class I transgenic mice deficient for H2 class I expression facilitate identification and characterization of new HLA class I-restricted viral T cell epitopes. J. Immunol. 169:5571-5580.
12. Del Val M, Iborra S, Ramos M, Lázaro S. 2011. Generation of MHC class I ligands in the secretory and vesicular pathways. Cell. Mol. Life Sci. 68: 1543-1552.
13. +T lymphocytes. Mol. Immunol. 39:235-247.
14. Ellis SA, Taylor C, McMichael A. 1982. Recognition of HLA-B27 and related antigen by a monoclonal antibody. Hum. Immunol. 5:49 -59.
15. Eng JK, McCormack Al, Yates JR, III. 1994. An approach to correlate tandem mass spectral data of peptides with amino acid sequences in a protein database. J. Amer. Soc. Mass. Spectrom. 5:976 -989.
16. Fairchild PJ, Wraith DC. 1996. Lowering the tone: mechanisms of im-munodominance among epitopes with low affinity for MHC. Immunol. Today 17:80-85.
17. Fan QR, et al. 1996. Direct binding of a soluble natural killer cell inhibitory receptor to a soluble human leukocyte antigen-CW4 class I major histocompatibility complex molecule. Proc. Natl. Acad. Sci. U. S. A. 93: 7178-7183.
18. Fenner F, Henderson DA, Arita I, Jezek Z, Ladnyi I. 2004. Smallpox and its eradication. WHO, Geneva, Switzerland.
19. Fenteany G, et al. 1995. Inhibition of proteasome activities and subunitspecific amino-terminal threonine modification by lactacystin. Science 268:726-731.
20. Firat H, et al. 1999. H-2 class I knockout, HLA-A2.1-transgenic mice: a versatile animal model for preclinical evaluation of antitumor immunotherapeutic strategies. Eur. J. Immunol. 29:3112-3121.
21. Freed ER, Duma RJ, Escobar MR. 1972. Vaccinia necrosum and its relationship to impaired immunologic responsiveness. Am. J. Med. 52: 411-420.
22. Howell S, Caswell AM, Kenny AJ, Turner AJ. 1993. Membrane peptidases on human osteoblast-like cells in culture: hydrolysis of calcitonin and hormonal regulation of endopeptidase-24.11. Biochem. J. 290: 159-164.
23. Hunt DF, et al. 1992. Characterization of peptides bound to the class I MHCmolecule HLA-A2.1 by mass spectrometry. Science 255:1261-1263.
24. Infantes S, et al. 2010. Multiple, non-conserved, internal viral ligands naturally presented by HLA-B27 in human respiratory syncytial virusinfected cells. Mol. Cell Proteomics 9:1533-1539.
25. Ishihama Y, Rappsilber J, Andersen JS, Mann M. 2002. Microcolumns with self-assembled particle frits for proteomics. J. Chromatogr. A 979: 233-239.
26. Johnson KL, Ovsyannikova IG, Mason CJ, Bergen HR, III, Poland GA. 2009. Discovery of naturally processed and HLA-presented class I peptides from vaccinia virus infection using mass spectrometry for vaccine development. Vaccine 28:38-47.
27. +T lymphocytes: a topological challenge. Traffic 8:1486 -1494.
28. Kalinke U, Arnold B, Hammerling GJ. 1990. Strong xenogeneic HLA response in transgenic mice after introducing an alpha 3 domain intoHLA B27. Nature 348:642- 644.
29. +T cells shapes the immunodominance hierarchy during boost vaccination. J. Exp. Med. 204:2187-2198.
30. Kennedy R, Poland GA. 2007. T-Cell epitope discovery for variola and vaccinia viruses. Rev. Med. Virol. 17:93-113.
31. Kennedy RB, Ovsyannikova I, Poland GA. 2009. Smallpox vaccines for biodefense. Vaccine 27(Suppl 4):D73-D79.
32. Kennedy RB, Ovsyannikova IG, Jacobson RM, Poland GA. 2009. The immunology of smallpox vaccines. Curr. Opin. Immunol. 21:314 -320.
33. Kondo E, et al. 2004. Identification of novel CTL epitopes of CMV-pp65 presented by a variety of HLA alleles. Blood 103:630-638.
34. Kozlowski S, et al. 1993. Multiple pathways are involved in the extracellular processing of MHC class-I-restricted peptides. J. Immunol. 151: 4033-4044.
35. Lafuente EM, Reche PA. 2009. Prediction of MHC-peptide binding: a systematic and comprehensive overview. Curr. Pharm. Des. 15: 3209-3220.
36. Larsen MV, Nielsen M, Weinzierl A, Lund O. 2006. TAP-independent MHC class I presentation. Curr. Immunol. Rev. 2:233-245.
37. +T cell recognition reveals a proteasome-dependent, transporter associated with antigen processingindependent pathway. J. Exp. Med. 194:1053-1068.
38. Lautscham G, Rickinson A, Blake N. 2003. TAP-independent antigen presentation on MHC class I molecules: lessons from Epstein-Barr virus. Microbes Infect. 5:291-299.
39. Lippincott-Schwartz J, et al. 1990. Microtubule-dependent retrograde transport of proteins into the ER in the presence of brefeldin A suggests an ER recycling pathway. Cell 60:821- 836.
40. López D, Gil-Torregrosa BC, Bergmann C, Del Val M. 2000. Sequential cleavage by metallopeptidases and proteasomes is involved in processing HIV-1 ENV epitope for endogenous MHC class I antigen presentation. J. Immunol. 164:5070-5077.
41. López D, Samino Y, Koszinowski UH, Del Val M. 2001. HIV envelope protein inhibitsMHCclass I presentation of a cytomegalovirus protective epitope. J. Immunol. 167:4238-4244.
42. Lorente E, Garcia R, Lopez D. 2011. Allele-dependent processing pathways generate the endogenous human leukocyte antigen (HLA) class I peptide repertoire in TAP-deficient cells. J. Biol. Chem. 286:38054 -38059.
43. Lorente E, et al. 2011. TAP-independent human histocompatibility complex-Cw1 antigen processing of an HIV envelope protein conserved peptide. AIDS 25:265-269.
44. Lundegaard C, Lund O, Buus S, Nielsen M. 2010. Major histocompatibility complex class I binding predictions as a tool in epitope discovery. Immunology 130:309-318.
45. +T lymphocytes in vivo. J. Immunol. 183:4639-4647.
46. Meyer VS, et al. 2008. Long-term immunity against actual poxviral HLA ligands as identified by differential stable isotope labeling. J. Immunol. 181:6371- 6383.
47. Moss B. 1991. Vaccinia virus: a tool for research and vaccine development. Science 252:1662-1667.
48. Nuchtern JG, Bonifacino JS, Biddison WE, Klausner RD. 1989. Brefeldin A implicates egress from endoplasmic reticulum in class I restricted antigen presentation. Nature 339:223-226.
49. Omura S, et al. 1991. Lactacystin, a novel microbial metabolite, induces neuritogenesis of neuroblastoma cells. J. Antibiot. (Tokyo) 44:113-116.
50. Oseroff C, et al. 2005. HLA class I-restricted responses to vaccinia recognize a broad array of proteins mainly involved in virulence and viral gene regulation. Proc. Natl. Acad. Sci. U. S. A. 102:13980 -13985.
51. Parham P, Bodmer WF. 1978. Monoclonal antibody to a human histocompatibility alloantigen, HLA-A2. Nature 276:397-399.
52. Pascolo S, et al. 1997. HLA-A2.1-restricted education and cytolytic activity of CD8(+) T lymphocytes from beta2 microglobulin (beta2m) HLA-A2.1 monochain transgenic H-2Db beta2m double knockout mice. J. Exp. Med. 185:2043-2051.
53. Pasquetto V, et al. 2005. HLA-A*0201, HLA-A*1101, and HLA-B*0702 transgenic mice recognize numerous poxvirus determinants from a wide variety of viral gene products. J. Immunol. 175:5504 -5515.
54. Rammensee HG, Bachmann J, Emmerich NPN, Bachor OA, Stevanovic S. 1999. SYFPEITHI: database for MHC ligands and peptide motifs. Immunogenetics 50:213-219.
55. Rawlings ND, Barrett AJ. 1995. Evolutionary families of metallopeptidases. Methods Enzymol. 248:183-228.
56. Redfield RR, et al. 1987. Disseminated vaccinia in a military recruit with human immunodeficiency virus (HIV) disease. N. Engl. J. Med. 316: 673-676.
57. Salter RD, Cresswell P. 1986. Impaired assembly and transport of HLA-A and -B antigens in a mutant TxB cell hybrid. EMBO J. 5:943-949.
58. 3+group is physiologically presented by major histocompatibility class I molecules. J. Biol. Chem. 279:1151-1160.
59. Saric T, et al. 2002. An IFN-γ-induced aminopeptidase in the ER, ERAP1, trims precursors to MHC class I-presented peptides. Nat. Immunol. 3:1169 -1176.
60. Schramm B, Locker JK. 2005. Cytoplasmic organization of POXvirus DNA replication. Traffic 6:839-846.
61. Serwold T, González F, Kim J, Jacob R, Shastri N. 2002. ERAAP customizes peptides for MHC class I molecules in the endoplasmic reticulum. Nature 419:480-483.
62. Slee EA, et al. 1996. Benzyloxycarbonyl-Val-Ala-Asp (OMe) fluoromethylketone (Z-VAD.FMK) inhibits apoptosis by blocking the processing of CPP32. Biochem. J. 315:21-24.
63. Spies T, DeMars R. 1991. Restored expression of major histocompatibility class I molecules by gene transfer of a putative peptide transporter. Nature 351:323-324.
64. Thornberry NA. 1994. Interleukin-1 beta converting enzyme. Methods Enzymol. 244:615-631.
65. Umezawa H. 1976. Structures and activities of protease inhibitors of microbial origin. Methods Enzymol. 45:678-695.
66. Villadangos JA, Galocha B, Lopez de Castro JA. 1994. Unusual topology of an HLA-B27 allospecific T cell epitope lacking peptide specificity. J. Immunol. 152:2317-2323.
67. Wang M, et al. 2007. CTL epitopes for influenza A including the H5N1 bird flu; genome-, pathogen-, and HLA-wide screening. Vaccine 25: 2823-2831.
68. Weihofen A, Binns K, Lemberg MK, Ashman K, Martoglio B. 2002. Identification of signal peptide peptidase, a presenilin-type aspartic protease. Science 296:2215-2218.
69. Weihofen A, Lemberg MK, Ploegh HL, Bogyo M, Martoglio B. 2000. Release of signal peptide fragments into the cytosol requires cleavage in the transmembrane region by a protease activity that is specifically blocked by a novel cysteine protease inhibitor. J. Biol. Chem. 275: 30951-30956.
70. Weinzierl AO, et al. 2008. Features of TAP-independent MHC class I ligands revealed by quantitative mass spectrometry. Eur. J. Immunol. 38:1503-1510.
71. Yewdell JW, Bennink JR. 1989. Brefeldin A specifically inhibits presentation of protein antigens to cytotoxic T lymphocytes. Science 244: 1072-1075.
72. York IA, et al. 2002. The ER aminopeptidase ERAP1 enhances or limits antigen presentation by trimming epitopes to 8-9 residues. Nat. Immunol. 3:1177-1184.
73. York IA, Goldberg AL, Mo XY, Rock KL. 1999. Proteolysis and class I major histocompatibility complex antigen presentation. Immunol. Rev. 172:49-66.