Targeting ribosome assembly on the HCV RNA using a small RNA molecule

RNA Biology

Volumn 9, Issue 8, 2012, Pages 1110-1119

  Bhat, Prasanna ^a   Gnanasundram, Sivakumar Vadivel ^a   Mani, Prashant ^b   Ray, Partho Sarothi ^a,c   Sarkar, Debi P ^b   Das, Saumitra ^a  

^a INDIAN INSTITUTE OF SCIENCE   (India)

^b UNIVERSITY OF DELHI   (India)

^c INDIAN INSTITUTE OF SCIENCE EDUCATION AND RESEARCH KOLKATA   (India)

Author keywords

HCV IRES; La autoantigen; Ribosome assembly; Sendai virosome; Translation inhibition

Indexed keywords

CAPPED RNA; LA ANTIGEN; RIBOSOME PROTEIN; RIBOSOME PROTEIN S5; UNCLASSIFIED DRUG; VIROSOME; VIRUS RNA;

5' UNTRANSLATED REGION; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; COLONY FORMATION; CONTROLLED STUDY; FEMALE; HEPATITIS C VIRUS; IN VIVO STUDY; INTERNAL RIBOSOME ENTRY SITE; LIVER CELL; LIVER PARENCHYMA; MEMBRANE FUSION; MOUSE; NONHUMAN; PARAINFLUENZA VIRUS 1; PROTEIN PURIFICATION; REPLICON; RNA REPLICATION; RNA STRUCTURE; RNA TRANSLATION; SMALL RIBOSOMAL SUBUNIT; TRANSLATION INITIATION; VIRAL GENE DELIVERY SYSTEM; VIRUS; VIRUS ASSEMBLY; VIRUS REPLICATION;

HEPATITIS C VIRUS; MUS; SENDAI VIRUS;

EID: 84866624397     PISSN: 15476286     EISSN: 15558584     Source Type: Journal    
DOI: 10.4161/rna.21208     Document Type: Article

References (36)

1. Saito I, Miyamura T, Ohbayashi A, Harada H, Katayama T, Kikuchi S, et al. Hepatitis C virus infection is associated with the development of hepatocellular carcinoma. Proc Natl Acad Sci U S A 1990; 87:6547-9; PMID:2168552; http://dx.doi.org/10.1073/pnas.87.17.6547.
2. Hoofnagle JH. Hepatitis C: the clinical spectrum of disease. Hepatology 1997; 26(Suppl 1):15S-20S; PMID:9305658; http://dx.doi.org/10.1002/hep. 510260703.
3. Iwasaki Y, Ikeda H, Araki Y, Osawa T, Kita K, Ando M, et al. Limitation of combination therapy of interferon and ribavirin for older patients with chronic hepatitis C. Hepatology 2006; 43:54-63; PMID:16374855; http://dx.doi.org/10.1002/hep.20984.
4. Kato N, Hijikata M, Ootsuyama Y, Nakagawa M, Ohkoshi S, Sugimura T, et al. Molecular cloning of the human hepatitis C virus genome from Japanese patients with non-A, non-B hepatitis. Proc Natl Acad Sci U S A 1990; 87:9524-8; PMID:2175903; http://dx.doi.org/10.1073/pnas.87.24.9524.
5. Pudi R, Abhiman S, Srinivasan N, Das S. Hepatitis C virus internal ribosome entry site-mediated translation is stimulated by specific interaction of independent regions of human La autoantigen. J Biol Chem 2003; 278:12231-40; PMID:12540850; http://dx.doi.org/10.1074/jbc.M210287200.
6. Otto GA, Puglisi JD. The pathway of HCV IRES-mediated translation initiation. Cell 2004; 119:369- 80; PMID:15507208; http://dx.doi.org/10.1016/j. cell.2004.09.038.
7. Kieft JS, Zhou K, Jubin R, Doudna JA. Mechanism of ribosome recruitment by hepatitis C IRES RNA. RNA 2001; 7:194-206; PMID:11233977; http://dx.doi.org/10.1017/S1355838201001790.
8. Lukavsky PJ. Structure and function of HCV IRES domains. Virus Res 2009; 139:166-71; PMID:18638512; http://dx.doi.org/10.1016/j.virusres.2008.06.004.
9. Pestova TV, Hellen CU, Shatsky IN. Canonical eukaryotic initiation factors determine initiation of translation by internal ribosomal entry. Mol Cell Biol 1996; 16:6859-69; PMID:8943341.
10. Ray PS, Das S. Inhibition of hepatitis C virus IRES-mediated translation by small RNAs analogous to stemloop structures of the 5'-untranslated region. Nucleic Acids Res 2004; 32:1678-87; PMID:15020704; http://dx.doi.org/10.1093/ nar/gkh328.
11. Rabl J, Leibundgut M, Ataide SF, Haag A, Ban N. Crystal structure of the eukaryotic 40S ribosomal subunit in complex with initiation factor 1. Science 2011; 331:730-6; PMID:21205638; http://dx.doi.org/10.1126/science.1198308.
12. Berry KE, Waghray S, Mortimer SA, Bai Y, Doudna JA. Crystal structure of the HCV IRES central domain reveals strategy for start-codon positioning. Structure 2011; 19:1456-66; PMID:22000514; http://dx.doi.org/10.1016/j.str.2011. 08.002.
13. Domitrovich AM, Diebel KW, Ali N, Sarker S, Siddiqui A. Role of La autoantigen and polypyrimidine tract-binding protein in HCV replication. Virology 2005; 335:72-86; PMID:15823607; http://dx.doi.org/10.1016/j.virol.2005. 02.009.
14. Paek KY, Kim CS, Park SM, Kim JH, Jang SK. RNA-binding protein hnRNP D modulates internal ribosome entry site-dependent translation of hepatitis C virus RNA. J Virol 2008; 82:12082-93; PMID:18842733; http://dx.doi.org/10.1128/ JVI.01405-08.
15. Fontanes V, Raychaudhuri S, Dasgupta A. A cell-permeable peptide inhibits hepatitis C virus replication by sequestering IRES transacting factors. Virology 2009; 394:82-90; PMID:19740508; http://dx.doi.org/10.1016/j.virol.2009. 08.012.
16. Romero-López C, Sánchez-Luque FJ, Berzal-Herranz A. Targets and tools: recent advances in the development of anti-HCV nucleic acids. Infect Disord Drug Targets 2006; 6:121-45; PMID:16789875; http://dx.doi.org/10.2174/ 187152606784112182.
17. Kikuchi K, Umehara T, Fukuda K, Hwang J, Kuno A, Hasegawa T, et al. RNA aptamers targeted to domain II of hepatitis C virus IRES that bind to its apical loop region. J Biochem 2003; 133:263-70; PMID:12761160; http://dx.doi.org/10. 1093/jb/mvg036.
18. Subramanian N, Mani P, Roy S, Gnanasundram SV, Sarkar DP, Das S. Targeted delivery of hepatitis C virus-specific short hairpin RNA in mouse liver using Sendai virosomes. J Gen Virol 2009; 90:1812-9; PMID:19297606; http://dx.doi.org/10.1099/vir.0.010579-0.
19. Pudi R, Abhiman S, Srinivasan N, Das S. Hepatitis C virus internal ribosome entry site-mediated translation is stimulated by specific interaction of independent regions of human La autoantigen. J Biol Chem 2003; 278:12231-40; PMID:12540850; http://dx.doi.org/10.1074/jbc.M210287200.
20. Domitrovich AM, Diebel KW, Ali N, Sarker S, Siddiqui A. Role of La autoantigen and polypyrimidine tract-binding protein in HCV replication. Virology 2005; 335:72-86; PMID:15823607; http://dx.doi.org/10.1016/j.virol.2005. 02.009.
21. Fukushi S, Okada M, Stahl J, Kageyama T, Hoshino FB, Katayama K. Ribosomal protein S5 interacts with the internal ribosomal entry site of hepatitis C virus. J Biol Chem 2001; 276:20824-6; PMID:11331271; http://dx.doi.org/10.1074/jbc.C100206200.
22. Brummelkamp TR, Bernards R, Agami R. A system for stable expression of short interfering RNAs in mammalian cells. Science 2002; 296:550-3; PMID:11910072; http://dx.doi.org/10.1126/science.1068999.
23. Kato T, Date T, Miyamoto M, Sugiyama M, Tanaka Y, Orito E, et al. Detection of anti-hepatitis C virus effects of interferon and ribavirin by a sensitive replicon system. J Clin Microbiol 2005; 43:5679-84; PMID:16272504; http://dx.doi.org/10.1128/JCM.43.11.5679-5684.2005.
24. Wang C, Le SY, Ali N, Siddiqui A. An RNA pseudoknot is an essential structural element of the internal ribosome entry site located within the hepatitis C virus 5′ noncoding region. RNA 1995; 1:526-37; PMID:7489514.
25. Spahn CM, Kieft JS, Grassucci RA, Penczek PA, Zhou K, Doudna JA, et al. Hepatitis C virus IRES RNA-induced changes in the conformation of the 40s ribosomal subunit. Science 2001; 291:1959-62; PMID:11239155; http://dx.doi.org/10.1126/science.1058409.
26. Boehringer D, Thermann R, Ostareck-Lederer A, Lewis JD, Stark H. Structure of the hepatitis C virus IRES bound to the human 80S ribosome: remodeling of the HCV IRES. Structure 2005; 13:1695-706; PMID:16271893.
27. Landry DM, Hertz MI, Thompson SR. RPS25 is essential for translation initiation by the Dicistroviridae and hepatitis C viral IRESs. Genes Dev 2009; 23:2753-64; PMID:19952110; http://dx.doi.org/10.1101/gad.1832209.
28. Pudi R, Ramamurthy SS, Das S. A peptide derived from RNA recognition motif 2 of human la protein binds to hepatitis C virus internal ribosome entry site, prevents ribosomal assembly, and inhibits internal initiation of translation. J Virol 2005; 79:9842-53; PMID:16014945; http://dx.doi.org/10.1128/ JVI.79.15.9842-9853.2005.
29. Lanford RE, Hildebrandt-Eriksen ES, Petri A, Persson R, Lindow M, Munk ME, et al. Therapeutic silencing of microRNA-122 in primates with chronic hepatitis C virus infection. Science 2010; 327:198-201; PMID:19965718; http://dx.doi.org/10.1126/science.1178178.
30. Ramani K, Hassan Q, Venkaiah B, Hasnain SE, Sarkar DP. Site-specific gene delivery in vivo through engineered Sendai viral envelopes. Proc Natl Acad Sci U S A 1998; 95:11886-90; PMID:9751760; http://dx.doi.org/10.1073/pnas.95.20. 11886.
31. Yi M, Ma Y, Yates J, Lemon SM. Compensatory mutations in E1, p7, NS2, and NS3 enhance yields of cell culture-infectious intergenotypic chimeric hepatitis C virus. J Virol 2007; 81:629-38; PMID:17079282; http://dx.doi.org/10.1128/JVI. 01890-06.
32. Ray PS, Das S. La autoantigen is required for the internal ribosome entry site-mediated translation of Coxsackievirus B3 RNA. Nucleic Acids Res 2002; 30:4500-8; PMID:12384597; http://dx.doi.org/10.1093/nar/gkf583.
33. Frese M, Barth K, Kaul A, Lohmann V, Schwärzle V, Bartenschlager R. Hepatitis C virus RNA replication is resistant to tumour necrosis factor-alpha. J Gen Virol 2003; 84:1253-9; PMID:12692291; http://dx.doi.org/10.1099/vir.0. 18997-0.
34. Hellman LM, Fried MG. Electrophoretic mobility shift assay (EMSA) for detecting protein-nucleic acid interactions. Nat Protoc 2007; 2:1849-61; PMID:17703195; http://dx.doi.org/10.1038/nprot.2007.249.
35. Wakita T, Pietschmann T, Kato T, Date T, Miyamoto M, Zhao Z, et al. Production of infectious hepatitis C virus in tissue culture from a cloned viral genome. Nat Med 2005; 11:791-6; PMID:15951748; http://dx.doi.org/10.1038/ nm1268.
36. Frese M, Barth K, Kaul A, Lohmann V, Schwärzle V, Bartenschlager R. Hepatitis C virus RNA replication is resistant to tumour necrosis factor-alpha. J Gen Virol 2003; 84:1253-9; PMID:12692291; http://dx.doi.org/10.1099/vir.0. 18997-0.