EIF2A mediates translation of hepatitis C viral mRNA under stress conditions

EMBO Journal

Volumn 30, Issue 12, 2011, Pages 2454-2464

  Kim, Joon Hyun ^a   Park, Sung Mi ^a   Park, Ji Hoon ^a   Keum, Sun Ju ^a   Jang, Sung Key ^a  

^a Pohang University of Science and Technology (POSTECH)   (South Korea)

Author keywords

eIF2A; HCV; IRES; stress; translation

Indexed keywords

INITIATION FACTOR 2ALPHA; MESSENGER RNA; METHIONINE TRANSFER RNA; VIRUS RNA;

ARTICLE; HEPATITIS C; HEPATITIS C VIRUS; INTERNAL RIBOSOME ENTRY SITE; NONHUMAN; PRIORITY JOURNAL; PROTEIN DOMAIN; PROTEIN FUNCTION; RNA TRANSLATION; STRESS;

CELL LINE, TUMOR; EUKARYOTIC INITIATION FACTOR-2; HELA CELLS; HEPACIVIRUS; HEPATITIS C; HUMANS; MUTAGENESIS, INSERTIONAL; PROTEIN BIOSYNTHESIS; PROTEIN INTERACTION DOMAINS AND MOTIFS; PROTEIN INTERACTION MAPPING; RIBOSOME SUBUNITS, SMALL, EUKARYOTIC; RNA, MESSENGER; RNA, VIRAL; STRESS, PHYSIOLOGICAL;

EUKARYOTA; HEPATITIS C VIRUS;

EID: 79958804665     PISSN: 02614189     EISSN: 14602075     Source Type: Journal    
DOI: 10.1038/emboj.2011.146     Document Type: Article

References (48)

1. Adams SL, Safer B, Anderson WF, Merrick WC (1975) Eukaryotic initiation complex formation. Evidence for two distinct pathways. J Biol Chem 250: 9083-9089
2. 0 noncoding region of the hepatitis C virus RNA genome and its functional requirement in internal initiation of translation. J Virol 69: 6367-6375
3. Benali-Furet NL, Chami M, Houel L, De Giorgi F, Vernejoul F, Lagorce D, Buscail L, Bartenschlager R, Ichas F, Rizzuto R, Paterlini-Brechot P (2005) Hepatitis C virus core triggers apopto-sis in liver cells by inducing ER stress and ER calcium depletion. Oncogene 24: 4921-4933 (Pubitemid 41129096)
4. Boehringer D, Thermann R, Ostareck-Lederer A, Lewis JD, Stark H (2005) Structure of the hepatitis C virus IRES bound to the human 80S ribosome: remodeling of the HCV IRES. Structure 13: 1695-1706 (Pubitemid 41571833)
5. Choi SK, Lee JH, Zoll WL, Merrick WC, Dever TE (1998) Promotion of met-tRNAiMet binding to ribosomes by yIF2, a bacterial IF2 homolog in yeast. Science 280: 1757-1760 (Pubitemid 28283500)
6. Dmitriev SE, Terenin IM, Andreev DE, Ivanov PA, Dunaevsky JE, Merrick WC, Shatsky IN (2010) GTP-independent tRNA delivery to the ribosomal P-site by a novel eukaryotic translation factor. J Biol Chem 285: 26779-26787
7. Farrell PJ, Balkow K, Hunt T, Jackson RJ, Trachsel H (1977) Phosphorylation of initiation factor elF-2 and the control of reticulocyte protein synthesis. Cell 11 : 187-200 (Pubitemid 8126067)
8. Gale Jr MJ, Korth MJ, Tang NM, Tan SL, Hopkins DA, Dever TE, Polyak SJ, Gretch DR, Katze MG (1997) Evidence that hepatitis C virus resistance to interferon is mediated through repression of the PKR protein kinase by the nonstructural 5A protein. Virology 230: 217-227 (Pubitemid 27211852)
9. Garaigorta U, Chisari FV (2009) Hepatitis C virus blocks interferon effector function by inducing protein kinase R phosphorylation. Cell Host Microbe 6: 513-522
10. Garcia MA, Gil J, Ventoso I, Guerra S, Domingo E, Rivas C, Esteban M (2006) Impact of protein kinase PKR in cell biology: from antiviral to antiproliferative action. Microbiol Mol Biol Rev 70: 1032-1060 (Pubitemid 44958263)
11. Grentzmann G, Ingram JA, Kelly PJ, Gesteland RF, Atkins JF (1998) A dual-luciferase reporter system for studying recoding signals. RNA 4: 479-486 (Pubitemid 28160788)
12. 0 border of the internal ribosomal entry site of hepatitis C virus. J Virol 72: 8782-8788 (Pubitemid 28471821)
13. Holcik M, Sonenberg N (2005) Translational control in stress and apoptosis. Nat Rev Mol Cell Biol 6: 318-327 (Pubitemid 40516898)
14. Jackson RJ, Hellen CU, Pestova TV (2010) The mechanism of eukaryotic translation initiation and principles of its regulation. Nat Rev Mol Cell Biol 11 : 113-127
15. Jubin R, Vantuno NE, Kieft JS, Murray MG, Doudna JA, Lau JY, Baroudy BM (2000) Hepatitis C virus internal ribosome entry site (IRES) stem loop IIId contains a phylogenetically conserved GGG triplet essential for translation and IRES folding. J Virol 74: 10430-10437
16. Kang JI, Kwon SN, Park SH, Kim YK, Choi SY, Kim JP, Ahn BY (2009) PKR protein kinase is activated by hepatitis C virus and inhibits viral replication through translational control. Virus Res 142: 51-56
17. Kieft JS, Zhou K, Jubin R, Doudna JA (2001) Mechanism of ribosome recruitment by hepatitis C IRES RNA. RNA 7: 194-206 (Pubitemid 33590503)
18. Kim CS, Jung JH, Wakita T, Yoon SK, Jang SK (2007) Monitoring the antiviral effect of alpha interferon on individual cells. J Virol 81 : 8814-8820 (Pubitemid 47242854)
19. Kim JH, Paek KY, Ha SH, Cho S, Choi K, Kim CS, Ryu SH, Jang SK (2004) A cellular RNA-binding protein enhances internal riboso-mal entry site-dependent translation through an interaction downstream of the hepatitis C virus polyprotein initiation codon. Mol Cell Biol 24: 7878-7890 (Pubitemid 39167439)
20. Kolupaeva VG, Pestova TV, Hellen CU (2000) An enzymatic foot-printing analysis of the interaction of 40S ribosomal subunits with the internal ribosomal entry site of hepatitis C virus. J Virol 74: 6242-6250 (Pubitemid 30429788)
21. Komar AA, Gross SR, Barth-Baus D, Strachan R, Hensold JO, Goss Kinzy T, Merrick WC (2005) Novel characteristics of the biological properties of the yeast Saccharomyces cerevisiae eukaryotic initiation factor 2A. J Biol Chem 280: 15601-15611 (Pubitemid 40616677)
22. Lancaster AM, Jan E, Sarnow P (2006) Initiation factor-independent translation mediated by the hepatitis C virus internal ribosome entry site. RNA 12: 894-902
23. Lukavsky PJ (2009) Structure and function of HCV IRES domains. Virus Res 139: 166-171
24. Lukavsky PJ, Otto GA, Lancaster AM, Sarnow P, Puglisi JD (2000) Structures of two RNA domains essential for hepatitis C virus internal ribosome entry site function. Nat Struct Biol 7: 1105-1110
25. Merrick WC, Anderson WF (1975) Purification and characterization of homogeneous protein synthesis initiation factor M1 from rabbit reticulocytes. J Biol Chem 250: 1197-1206
26. Paek KY, Kim CS, Park SM, Kim JH, Jang SK (2008) RNA-binding protein hnRNP D modulates internal ribosome entry site-dependent translation of hepatitis C virus RNA. J Virol 82: 12082-12093
27. Pestova TV, de Breyne S, Pisarev AV, Abaeva IS, Hellen CU (2008) eIF2-dependent and eIF2-independent modes of initiation on the CSFV IRES: a common role of domain II. EMBO J 27: 1060-1072 (Pubitemid 351508158)
28. Pestova TV, Hellen CU (2005) Reconstitution of eukaryotic translation elongation in vitro following initiation by internal ribosomal entry. Methods 36: 261-269 (Pubitemid 41074957)
29. Pisarev AV, Shirokikh NE, Hellen CU (2005) Translation initiation by factor-independent binding of eukaryotic ribosomes to internal ribosomal entry sites. C R Biol 328: 589-605 (Pubitemid 40903694)
30. Reineke LC, Merrick WC (2009) Characterization of the functional role of nucleotides within the URE2 IRES element and the requirements for eIF2A-mediated repression. RNA 15: 2264-2277
31. Robert F, Kapp LD, Khan SN, Acker MG, Kolitz S, Kazemi S, Kaufman RJ, Merrick WC, Koromilas AE, Lorsch JR, Pelletier J (2006) Initiation of protein synthesis by hepatitis C virus is refractory to reduced eIF2.GTP.Met-tRNA(i) (Met) ternary complex availability. Mol Biol Cell 17: 4632-4644 (Pubitemid 44665734)
32. Roll-Mecak A, Cao C, Dever TE, Burley SK (2000) X-ray structures of the universal translation initiation factor IF2/eIF5B: conforma-tional changes on GDP and GTP binding. Cell 103: 781-792
33. Samuel CE (2001) Antiviral actions of interferons. Clin Microbiol Rev 14: 778-809 (Pubitemid 32979631)
34. Schmitt E, Naveau M, Mechulam Y (2010) Eukaryotic and archaeal translation initiation factor 2: a heterotrimeric tRNA carrier. FEBS Lett 584: 405-412
35. Shimoike T, Koyama C, Murakami K, Suzuki R, Matsuura Y, Miyamura T, Suzuki T (2006) Down-regulation of the internal ribosome entry site (IRES)-mediated translation of the hepatitis C virus: critical role of binding of the stem-loop IIId domain of IRES and the viral core protein. Virology 345: 434-445 (Pubitemid 43189902)
36. Siridechadilok B, Fraser CS, Hall RJ, Doudna JA, Nogales E (2005) Structural roles for human translation factor eIF3 in initiation of protein synthesis. Science 310 : 1513-1515 (Pubitemid 41746350)
37. 0 nontranslated regions of hepatitis C virus and classical swine fever virus RNAs. J Virol 72: 4775-4782 (Pubitemid 28215653)
38. Skabkin MA, Skabkina OV, Dhote V, Komar AA, Hellen CU, Pestova TV (2010) Activities of ligatin and MCT-1/DENR in eukaryotic translation initiation and ribosomal recycling. Genes Dev 24: 1787-1801
39. 0 non-coding region: implications for secondary structure, virus detection and typing. The International HCV Collaborative Study Group. J Gen Virol 76(Part 7): 1749-1761
40. Spahn CM, Kieft JS, Grassucci RA, Penczek PA, Zhou K, Doudna JA, Frank J (2001) Hepatitis C virus IRES RNA-induced changes in the conformation of the 40s ribosomal subunit. Science 291: 1959-1962 (Pubitemid 32216995)
41. Tardif KD, Mori K, Siddiqui A (2002) Hepatitis C virus subgenomic replicons induce endoplasmic reticulum stress activating an intracellular signaling pathway. J Virol 76: 7453-7459 (Pubitemid 34760967)
42. Taylor DR, Shi ST, Romano PR, Barber GN, Lai MM (1999) Inhibition of the interferon-inducible protein kinase PKR by HCV E2 protein. Science 285: 107-110 (Pubitemid 29307576)
43. Terenin IM, Dmitriev SE, Andreev DE, Shatsky IN (2008) Eukaryotic translation initiation machinery can operate in a bacterial-like mode without eIF2. Nat Struct Mol Biol 15: 836-841
44. Ventoso I, Sanz MA, Molina S, Berlanga JJ, Carrasco L, Esteban M (2006) Translational resistance of late alphavirus mRNA to eIF2alpha phosphorylation: a strategy to overcome the antiviral effect of protein kinase PKR. Genes Dev 20: 87-100 (Pubitemid 43042670)
45. Wakita T, Pietschmann T, Kato T, Date T, Miyamoto M, Zhao Z, Murthy K, Habermann A, Krausslich HG, Mizokami M, Bartenschlager R, Liang TJ (2005) Production of infectious hepatitis C virus in tissue culture from a cloned viral genome. Nat Med 11 : 791-796 (Pubitemid 41021213)
46. 0 UTR RNA. Virus Res 145: 285-292
47. Zhong J, Gastaminza P, Cheng G, Kapadia S, Kato T, Burton DR, Wieland SF, Uprichard SL, Wakita T, Chisari FV (2005) Robust hepatitis C virus infection in vitro. Proc Natl Acad Sci USA 102: 9294-9299 (Pubitemid 40923557)
48. Zoll WL, Horton LE, Komar AA, Hensold JO, Merrick WC (2002) Characterization of mammalian eIF2A and identification of the yeast homolog. J Biol Chem 277: 37079-37087