Effects of messenger RNA structure and other translational control mechanisms on major histocompatibility complex-I mediated antigen presentation

Wiley Interdisciplinary Reviews: RNA

Volumn 6, Issue 2, 2015, Pages 157-171

  Murat, Pierre ^a   Tellam, Judy ^b  

^a UNIVERSITY OF CAMBRIDGE   (United Kingdom)

^b QIMR BERGHOFER MEDICAL RESEARCH INSTITUTE   (Australia)

Author keywords

[No Author keywords available]

Indexed keywords

CELL PROTEIN; DOUBLE STRANDED DNA; DOUBLE STRANDED RNA; GUANINE QUADRUPLEX; LATENCY ASSOCIATED NUCLEAR ANTIGEN; MAJOR HISTOCOMPATIBILITY ANTIGEN CLASS 1; MESSENGER RNA; VIRUS PROTEIN; HLA ANTIGEN CLASS 1;

ANTIGEN PRESENTATION; ANTIGEN RECOGNITION; EPSTEIN BARR VIRUS; GENE CONTROL; GENE TARGETING; GENETIC IDENTIFICATION; HUMAN; IMMUNE EVASION; MAJOR HISTOCOMPATIBILITY COMPLEX; NONHUMAN; OPEN READING FRAME; PRIORITY JOURNAL; PROTEIN MOTIF; REVIEW; RNA STRUCTURE; RNA TRANSLATION; VIRUS REPLICATION; ADAPTIVE IMMUNITY; ANIMAL; BIOSYNTHESIS; CHEMISTRY; CONFORMATION; IMMUNOLOGICAL TOLERANCE; IMMUNOLOGY; METABOLISM; PROTEIN SYNTHESIS; VIRUS;

ADAPTIVE IMMUNITY; ANIMALS; ANTIGEN PRESENTATION; HISTOCOMPATIBILITY ANTIGENS CLASS I; HUMANS; IMMUNE EVASION; IMMUNE TOLERANCE; NUCLEIC ACID CONFORMATION; PROTEIN BIOSYNTHESIS; RNA, MESSENGER; VIRUSES;

EID: 84922967724     PISSN: 17577004     EISSN: 17577012     Source Type: Journal    
DOI: 10.1002/wrna.1262     Document Type: Review

References (74)

1. Burrows SR, Moss DJ, Khanna R. Understanding human T-cell-mediated immunoregulation through herpesviruses. Immunol Cell Biol 2011, 89:352-358.
2. Blum JS, Wearsch PA, Cresswell P. Pathways of antigen processing. Annu Rev Immunol 2013, 31:443-473.
3. Ploegh HL. Viral strategies of immune evasion. Science 1998, 280:248-253.
4. Elliott T, Williams A. The optimization of peptide cargo bound to MHC class I molecules by the peptide-loading complex. Immunol Rev 2005, 207:89-99.
5. Hansen TH, Bouvier M. MHC class I antigen presentation: learning from viral evasion strategies. Nat Rev Immunol 2009, 9:503-513.
6. Khanna R, Burrows SR. Role of cytotoxic T lymphocytes in Epstein-Barr virus-associated diseases. Annu Rev Microbiol 2000, 54:19-48.
7. Murat P, Zhong J, Lekieffre L, Cowieson NP, Clancy JL, Preiss T, Balasubramanian S, Khanna R, Tellam J. G-quadruplexes regulate Epstein-Barr virus-encoded nuclear antigen 1 mRNA translation. Nat Chem Biol 2014, 10:358-364.
8. Tellam J, Fogg MH, Rist M, Connolly G, Tscharke D, Webb N, Heslop L, Wang F, Khanna R. Influence of translation efficiency of homologous viral proteins on the endogenous presentation of CD8+ T cell epitopes. J Exp Med 2007, 204:525-532.
9. Tellam J, Smith C, Rist M, Webb N, Cooper L, Vuocolo T, Connolly G, Tscharke DC, Devoy MP, Khanna R. Regulation of protein translation through mRNA structure influences MHC class I loading and T cell recognition. Proc Natl Acad Sci USA 2008, 105:9319-9324.
10. Tellam JT, Lekieffre L, Zhong J, Lynn DJ, Khanna R. Messenger RNA Sequence Rather than Protein Sequence Determines the Level of Self-synthesis and Antigen Presentation of the EBV-encoded Antigen, EBNA1. PLoS Pathog 2012, 8:e1003112.
11. Yin Y, Manoury B, Fahraeus R. Self-inhibition of synthesis and antigen presentation by Epstein-Barr virus-encoded EBNA1. Science 2003, 301:1371-1374.
12. Cresswell P, Bangia N, Dick T, Diedrich G. The nature of the MHC class I peptide loading complex. Immunol Rev 1999, 172:21-28.
13. Rock KL, Gramm C, Rothstein L, Clark K, Stein R, Dick L, Hwang D, Goldberg AL. Inhibitors of the proteasome block the degradation of most cell proteins and the generation of peptides presented on MHC class I molecules. Cell 1994, 78:761-771.
14. Baumeister W, Walz J, Zuhl F, Seemuller E. The proteasome: paradigm of a self-compartmentalizing protease. Cell 1998, 92:367-380.
15. Levitskaya J, Sharipo A, Leonchiks A, Ciechanover A, Masucci MG. Inhibition of ubiquitin/proteasome-dependent protein degradation by the Gly-Ala repeat domain of the Epstein-Barr virus nuclear antigen 1. Proc Natl Acad Sci USA 1997, 94:12616-12621.
16. Farrell HE, Davis-Poynter NJ. From sabotage to camouflage: viral evasion of cytotoxic T lymphocyte and natural killer cell-mediated immunity. Semin Cell Dev Biol 1998, 9:369-378.
17. Fruh K, Gruhler A, Krishna RM, Schoenhals GJ. A comparison of viral immune escape strategies targeting the MHC class I assembly pathway. Immunol Rev 1999, 168:157-166.
18. Andersson M, Paabo S, Nilsson T, Peterson PA. Impaired intracellular transport of class I MHC antigens as a possible means for adenoviruses to evade immune surveillance. Cell 1985, 43:215-222.
19. Li L, Muzahim Y, Bouvier M. Crystal structure of adenovirus E3-19K bound to HLA-A2 reveals mechanism for immunomodulation. Nat struct Mol Biol 2012, 19:1176-1181.
20. Hegde NR, Chevalier MS, Wisner TW, Denton MC, Shire K, Frappier L, Johnson DC. The role of BiP in endoplasmic reticulum-associated degradation of major histocompatibility complex class I heavy chain induced by cytomegalovirus proteins. J Biol Chem 2006, 281:20910-20919.
21. Coscoy L, Ganem D. Kaposi's sarcoma-associated herpesvirus encodes two proteins that block cell surface display of MHC class I chains by enhancing their endocytosis. Proc Natl Acad Sci USA 2000, 97:8051-8056.
22. Fruh K, Ahn K, Djaballah H, Sempe P, van Endert PM, Tampe R, Peterson PA, Yang Y. A viral inhibitor of peptide transporters for antigen presentation. Nature 1995, 375:415-418.
23. Hill A, Jugovic P, York I, Russ G, Bennink J, Yewdell J, Ploegh H, Johnson D. Herpes simplex virus turns off the TAP to evade host immunity. Nature 1995, 375:411-415.
24. Ahn K, Gruhler A, Galocha B, Jones TR, Wiertz EJ, Ploegh HL, Peterson PA, Yang Y, Fruh K. The ER-luminal domain of the HCMV glycoprotein US6 inhibits peptide translocation by TAP. Immunity 1997, 6:613-621.
25. Lehner PJ, Karttunen JT, Wilkinson GW, Cresswell P. The human cytomegalovirus US6 glycoprotein inhibits transporter associated with antigen processing-dependent peptide translocation. Proc Natl Acad Sci USA 1997, 94:6904-6909.
26. Hislop AD, Ressing ME, van Leeuwen D, Pudney VA, Horst D, Koppers-Lalic D, Croft NP, Neefjes JJ, Rickinson AB, Wiertz EJ. A CD8+ T cell immune evasion protein specific to Epstein-Barr virus and its close relatives in Old World primates. J Exp Med 2007, 204:1863-1873.
27. Zaldumbide A, Ossevoort M, Wiertz EJ, Hoeben RC. In cis inhibition of antigen processing by the latency-associated nuclear antigen I of Kaposi sarcoma herpes virus. Mol Immunol 2007, 44:1352-1360.
28. Sadasivan B, Lehner PJ, Ortmann B, Spies T, Cresswell P. Roles for calreticulin and a novel glycoprotein, tapasin, in the interaction of MHC class I molecules with TAP. Immunity 1996, 5:103-114.
29. Bennett EM, Bennink JR, Yewdell JW, Brodsky FM. Cutting edge: adenovirus E19 has two mechanisms for affecting class I MHC expression. J Immunol 1999, 162:5049-5052.
30. Khanna R, Moss D, Gandhi M. Technology insight: applications of emerging immunotherapeutic strategies for Epstein-Barr virus-associated malignancies. Nat Clin Pract Oncol 2005, 2:138-149.
31. Blake N. Immune evasion by gammaherpesvirus genome maintenance proteins. J Gen Virol 2010, 91:829-846.
32. Sharipo A, Imreh M, Leonchiks A, Imreh S, Masucci MG. A minimal glycine-alanine repeat prevents the interaction of ubiquitinated I kappaB α with the proteasome: a new mechanism for selective inhibition of proteolysis. Nat Med 1998, 4:939-944.
33. Levitskaya J, Coram M, Levitsky V, Imreh S, Steigerwald-Mullen PM, Klein G, Kurilla MG, Masucci MG. Inhibition of antigen processing by the internal repeat region of the Epstein-Barr virus nuclear antigen-1. Nature 1995, 375:685-688.
34. Daskalogianni C, Apcher S, Candeias MM, Naski N, Calvo F, Fahraeus R. Gly-Ala repeats induce position- and substrate-specific regulation of 26 S proteasome-dependent partial processing. J Biol Chem 2008, 283:30090-30100.
35. Yewdell JW, Reits E, Neefjes J. Making sense of mass destruction: quantitating MHC class I antigen presentation. Nat Rev Immunol 2003, 3:952-961.
36. Colbert JD, Farfan-Arribas DJ, Rock KL. Substrate-induced protein stabilization reveals a predominant contribution from mature proteins to peptides presented on MHC class I. J Immunol 2013, 191:5410-5419.
37. Rock KL, Farfan-Arribas DJ, Colbert JD, Goldberg AL. Re-examining class-I presentation and the DRiP hypothesis. Trends Immunol 2014, 35:144-152.
38. Cardinaud S, Starck SR, Chandra P, Shastri N. The synthesis of truncated polypeptides for immune surveillance and viral evasion. PLoS One 2010, 5:e8692.
39. Cristillo AD, Mortimer JR, Barrette IH, Lillicrap TP, Forsdyke DR. Double-stranded RNA as a not-self alarm signal: to evade, most viruses purine-load their RNAs, but some (HTLV-1, Epstein-Barr) pyrimidine-load. J Theor Biol 2001, 208:475-491.
40. Thorley-Lawson DA, Miyashita EM, Khan G. Epstein-Barr virus and the B cell: that's all it takes. Trends Microbiol 1996, 4:204-208.
41. Karlin S, Blaisdell BE, Mocarski ES, Brendel V. A method to identify distinctive charge configurations in protein sequences, with application to human herpesvirus polypeptides. J Mol Biol 1988, 205:165-177.
42. Parkinson GN, Lee MP, Neidle S. Crystal structure of parallel quadruplexes from human telomeric DNA. Nature 2002, 417:876-880.
43. Balasubramanian S, Hurley LH, Neidle S. Targeting G-quadruplexes in gene promoters: a novel anticancer strategy? Nat Rev Drug Discov 2011, 10:261-275.
44. Neidle S, Parkinson G. Telomere maintenance as a target for anticancer drug discovery. Nat Rev Drug Discov 2002, 1:383-393.
45. Rodriguez R, Miller KM, Forment JV, Bradshaw CR, Nikan M, Britton S, Oelschlaegel T, Xhemalce B, Balasubramanian S, Jackson SP. Small-molecule-induced DNA damage identifies alternative DNA structures in human genes. Nat Chem Biol 2012, 8:301-310.
46. Rainbow L, Platt GM, Simpson GR, Sarid R, Gao SJ, Stoiber H, Herrington CS, Moore PS, Schulz TF. The 222- to 234-kilodalton latent nuclear protein (LNA) of Kaposi's sarcoma-associated herpesvirus (human herpesvirus 8) is encoded by orf73 and is a component of the latency-associated nuclear antigen. J Virol 1997, 71:5915-5921.
47. Larocca D, Chao LA, Seto MH, Brunck TK. Human T-cell leukemia virus minus strand transcription in infected T-cells. Biochem Biophys Res Commun 1989, 163:1006-1013.
48. Cook LB, Elemans M, Rowan AG, Asquith B. HTLV-1: persistence and pathogenesis. Virology 2013, 435:131-140.
49. Norseen J, Johnson FB, Lieberman PM. Role for G-quadruplex RNA binding by Epstein-Barr virus nuclear antigen 1 in DNA replication and metaphase chromosome attachment. J Virol 2009, 83:10336-10346.
50. Liu Y, Wimmer E, Paul AV. Cis-acting RNA elements in human and animal plus-strand RNA viruses. Biochim Biophys Acta 2009, 1789:495-517.
51. Andino R, Rieckhof GE, Baltimore D. A functional ribonucleoprotein complex forms around the 5' end of poliovirus RNA. Cell 1990, 63:369-380.
52. Andino R, Rieckhof GE, Achacoso PL, Baltimore D. Poliovirus RNA synthesis utilizes an RNP complex formed around the 5′-end of viral RNA. EMBO J 1993, 12:3587-3598.
53. Deitz SB, Dodd DA, Cooper S, Parham P, Kirkegaard K. MHC I-dependent antigen presentation is inhibited by poliovirus protein 3A. Proc Natl Acad Sci USA 2000, 97:13790-13795.
54. Zhou Z, Mogensen MM, Powell PP, Curry S, Wileman T. Foot-and-mouth disease virus 3C protease induces fragmentation of the Golgi compartment and blocks intra-Golgi transport. J Virol 2013, 87:11721-11729.
55. Starck SR, Shastri N. Non-conventional sources of peptides presented by MHC class I. Cell Mol Life Sci 2011, 68:1471-1479.
56. Jacks T, Power MD, Masiarz FR, Luciw PA, Barr PJ, Varmus HE. Characterization of ribosomal frameshifting in HIV-1 gag-pol expression. Nature 1988, 331:280-283.
57. Mayrand SM, Schwarz DA, Green WR. An alternative translational reading frame encodes an immunodominant retroviral CTL determinant expressed by an immunodeficiency-causing retrovirus. J Immunol 1998, 160:39-50.
58. Maness NJ, Valentine LE, May GE, Reed J, Piaskowski SM, Soma T, Furlott J, Rakasz EG, Friedrich TC, Price DA, et al. AIDS virus specific CD8+ T lymphocytes against an immunodominant cryptic epitope select for viral escape. J Exp Med 2007, 204:2505-2512.
59. Maness NJ, Walsh AD, Piaskowski SM, Furlott J, Kolar HL, Bean AT, Wilson NA, Watkins DI. CD8+ T cell recognition of cryptic epitopes is a ubiquitous feature of AIDS virus infection. J Virol 2010, 84:11569-11574.
60. Berger CT, Carlson JM, Brumme CJ, Hartman KL, Brumme ZL, Henry LM, Rosato PC, Piechocka-Trocha A, Brockman MA, Harrigan PR, et al. Viral adaptation to immune selection pressure by HLA class I-restricted CTL responses targeting epitopes in HIV frameshift sequences. J Exp Med 2010, 207:61-75.
61. Starck SR, Jiang VV, Pavon-Eternod M, Prasad S, McCarthy B, Pan T, Shastri N. Leucine-tRNA initiates at CUG start codons for protein synthesis and presentation by MHC class I. Science 2012, 336:1719-1723.
62. Maness NJ, Wilson NA, Reed JS, Piaskowski SM, Sacha JB, Walsh AD, Thoryk E, Heidecker GJ, Citron MP, Liang X, et al. Robust, vaccine-induced CD8(+) T lymphocyte response against an out-of-frame epitope. J Immunol 2010, 184:67-72.
63. Chen W, Calvo PA, Malide D, Gibbs J, Schubert U, Bacik I, Basta S, O'Neill R, Schickli J, Palese P, et al. A novel influenza A virus mitochondrial protein that induces cell death. Nat Med 2001, 7:1306-1312.
64. Zamarin D, Ortigoza MB, Palese P. Influenza A virus PB1-F2 protein contributes to viral pathogenesis in mice. J Virol 2006, 80:7976-7983.
65. Moss WN, Priore SF, Turner DH. Identification of potential conserved RNA secondary structure throughout influenza A coding regions. RNA 2011, 17:991-1011.
66. McAuley JL, Chipuk JE, Boyd KL, Van De Velde N, Green DR, McCullers JA. PB1-F2 proteins from H5N1 and 20 century pandemic influenza viruses cause immunopathology. PLoS Pathog 2010, 6:e1001014.
67. Conenello GM, Zamarin D, Perrone LA, Tumpey T, Palese P. A single mutation in the PB1-F2 of H5N1 (HK/97) and 1918 influenza A viruses contributes to increased virulence. PLoS Pathog 2007, 3:1414-1421.
68. Conenello GM, Tisoncik JR, Rosenzweig E, Varga ZT, Palese P, Katze MG. A single N66S mutation in the PB1-F2 protein of influenza A virus increases virulence by inhibiting the early interferon response in vivo. J Virol 2011, 85:652-662.
69. Varga ZT, Ramos I, Hai R, Schmolke M, Garcia-Sastre A, Fernandez-Sesma A, Palese P. The influenza virus protein PB1-F2 inhibits the induction of type I interferon at the level of the MAVS adaptor protein. PLoS Pathog 2011, 7:e1002067.
70. Schmolke M, Manicassamy B, Pena L, Sutton T, Hai R, Varga ZT, Hale BG, Steel J, Perez DR, Garcia-Sastre A. Differential contribution of PB1-F2 to the virulence of highly pathogenic H5N1 influenza A virus in mammalian and avian species. PLoS Pathog 2011, 7:e1002186.
71. Brakier-Gingras L, Charbonneau J, Butcher SE. Targeting frameshifting in the human immunodeficiency virus. Expert Opin Ther Targets 2012, 16:249-258.
72. Howard MT, Gesteland RF, Atkins JF. Efficient stimulation of site-specific ribosome frameshifting by antisense oligonucleotides. RNA 2004, 10:1653-1661.
73. Yu CH, Noteborn MH, Olsthoorn RC. Stimulation of ribosomal frameshifting by antisense LNA. Nucleic Acids Res 2010, 38:8277-8283.
74. Ofori LO, Hilimire TA, Bennett RP, Brown NW Jr, Smith HC, Miller BL. High-affinity recognition of HIV-1 frameshift-stimulating RNA alters frameshifting in vitro and interferes with HIV-1 infectivity. J Med Chem 2014, 57:723-732.