Non-genotype-specific role of the hepatitis C virus 5′ untranslated region in virus production and in inhibition by interferon

Virology

Volumn 421, Issue 2, 2011, Pages 222-234

  Li, Yi Ping ^a,b   Ramirez, Santseharay ^a,b   Gottwein, Judith M ^a,b   Bukh, Jens ^a,b  

^a Mental Health Services CPH   (Denmark)

^b UNIVERSITY OF COPENHAGEN   (Denmark)

Author keywords

5 terminal nucleotide; Antivirals; Cell culture system; Interaction; Recombinant; RNA virus

Indexed keywords

ADENINE; ALPHA2B INTERFERON; CYTIDINE; NONSTRUCTURAL PROTEIN 2; NONSTRUCTURAL PROTEIN 3;

3' UNTRANSLATED REGION; 5' UNTRANSLATED REGION; ANTIVIRAL ACTIVITY; ARTICLE; CONTROLLED STUDY; GENETIC POLYMORPHISM; GENETIC RECOMBINATION; GENOTYPE; HEPATITIS C VIRUS; HUMAN; HUMAN CELL; IN VITRO STUDY; NONHUMAN; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; TREATMENT RESPONSE; VIROGENESIS; VIRUS INHIBITION; VIRUS VIRULENCE;

5' UNTRANSLATED REGIONS; BASE SEQUENCE; CELL LINE; GENOTYPE; HEPACIVIRUS; HUMANS; INTERFERON-ALPHA; RECOMBINANT PROTEINS; RNA, VIRAL; SEQUENCE ANALYSIS, DNA; VIRAL CORE PROTEINS; VIRUS REPLICATION;

HEPATITIS C VIRUS; RNA VIRUSES;

EID: 80355146825     PISSN: 00426822     EISSN: 10960341     Source Type: Journal    
DOI: 10.1016/j.virol.2011.10.002     Document Type: Article

References (76)

1. Alter H.J., Seeff L.B. Recovery, persistence, and sequelae in hepatitis C virus infection: a perspective on long-term outcom. Semin. Liver Dis. 2000, 20:17-35.
2. Binder M., Quinkert D., Bochkarova O., Klein R., Kezmic N., Bartenschlager R., Lohmann V. Identification of determinants involved in initiation of hepatitis C virus RNA synthesis by using intergenotypic replicase chimeras. J. Virol. 2007, 81:5270-5283.
3. Blight K.J., Norgard E.A. HCV Replicon Systems. Hepatitis C Viruses: Genomes and Molecular Biology 2006, 311-351. Horizon Bioscience, HNorfolk (UK). S.L. Tan (Ed.).
4. Brown E.A., Zhang H., Ping L.H., Lemon S.M. Secondary structure of the 5' nontranslated regions of hepatitis C virus and pestivirus genomic RNAs. Nucleic Acids Res. 1992, 20:5041-5045.
5. Bukh J., Purcell R.H., Miller R.H. Sequence analysis of the 5' noncoding region of hepatitis C virus. Proc. Natl. Acad. Sci. U.S.A. 1992, 89:4942-4946.
6. Bukh J., Meuleman P., Tellier R., Engle R.E., Feinstone S.M., Eder G., Satterfield W.C., Govindarajan S., Krawczynski K., Miller R.H., Leroux-Roels G., Purcell R.H. Challenge pools of hepatitis C virus genotypes 1-6 prototype strains: replication fitness and pathogenicity in chimpanzees and human liver-chimeric mouse models. J. Infect. Dis. 2010, 201:1381-1389.
7. Buratti E., Gerotto M., Pontisso P., Alberti A., Tisminetzky S.G., Baralle F.E. In vivo translational efficiency of different hepatitis C virus 5'-UTRs. FEBS Lett. 1997, 411:275-280.
8. Cai Z., Liang T.J., Luo G. Effects of mutations of the initiation nucleotides on hepatitis C virus RNA replication in the cell. J. Virol. 2004, 78:3633-3643.
9. Chang J., Nicolas E., Marks D., Sander C., Lerro A., Buendia M.A., Xu C., Mason W.S., Moloshok T., Bort R., Zaret K.S., Taylor J.M. miR-122, a mammalian liver-specific microRNA, is processed from hcr mRNA and may downregulate the high affinity cationic amino acid transporter CAT-1. RNA Biol. 2004, 1:106-113.
10. Chinnaswamy S., Murali A., Li P., Fujisaki K., Kao C.C. Regulation of de novo-initiated RNA synthesis in hepatitis C virus RNA-dependent RNA polymerase by intermolecular interactions. J. Virol. 2010, 84:5923-5935.
11. Collier A.J., Tang S., Elliott R.M. Translation efficiencies of the 5' untranslated region from representatives of the six major genotypes of hepatitis C virus using a novel bicistronic reporter assay system. J. Gen. Virol. 1998, 79(Pt 10):2359-2366.
12. Dash S., Prabhu R., Hazari S., Bastian F., Garry R., Zou W., Haque S., Joshi V., Regenstein F.G., Thung S.N. Interferons alpha, beta, gamma each inhibit hepatitis C virus replication at the level of internal ribosome entry site-mediated translation. Liver Int. 2005, 25:580-594.
13. Friebe P., Lohmann V., Krieger N., Bartenschlager R. Sequences in the 5' nontranslated region of hepatitis C virus required for RNA replication. J. Virol. 2001, 75:12047-12057.
14. Gottwein J.M., Bukh J. Cutting the gordian knot-development and biological relevance of hepatitis C virus cell culture systems. Adv. Virus Res. 2008, 71:51-133.
15. Gottwein J.M., Scheel T.K., Hoegh A.M., Lademann J.B., Eugen-Olsen J., Lisby G., Bukh J. Robust hepatitis C genotype 3a cell culture releasing adapted intergenotypic 3a/2a (S52/JFH1) viruses. Gastroenterology 2007, 133:1614-1626.
16. Gottwein J.M., Scheel T.K., Jensen T.B., Lademann J.B., Prentoe J.C., Knudsen M.L., Hoegh A.M., Bukh J. Development and characterization of hepatitis C virus genotype 1-7 cell culture systems: role of CD81 and scavenger receptor class B type I and effect of antiviral drugs. Hepatology 2009, 49:364-377.
17. Gottwein J.M., Scheel T.K., Callendret B., Li Y.P., Eccleston H.B., Engle R.E., Govindarajan S., Satterfield W., Purcell R.H., Walker C.M., Bukh J. Novel infectious cDNA clones of hepatitis C virus genotype 3a (strain S52) and 4a (strain ED43): genetic analyses and in vivo pathogenesis studies. J. Virol. 2010, 84:5277-5293.
18. Gottwein J.M., Scheel T.K., Jensen T.B., Ghanem L., Bukh J. Differential efficacy of protease inhibitors against HCV genotypes 2a, 3a, 5a, and 6a NS3/4A protease recombinant viruses. Gastroenterology 2011, 141:1067-1079.
19. Han J.H., Shyamala V., Richman K.H., Brauer M.J., Irvine B., Urdea M.S., Tekamp-Olson P., Kuo G., Choo Q.L., Houghton M. Characterization of the terminal regions of hepatitis C viral RNA: identification of conserved sequences in the 5' untranslated region and poly(A) tails at the 3' end. Proc. Natl. Acad. Sci. U.S.A. 1991, 88:1711-1715.
20. Hazari S., Patil A., Joshi V., Sullivan D.E., Fermin C.D., Garry R.F., Elliott R.M., Dash S. Alpha interferon inhibits translation mediated by the internal ribosome entry site of six different hepatitis C virus genotypes. J. Gen. Virol. 2005, 86:3047-3053.
21. Honda M., Ping L.H., Rijnbrand R.C., Amphlett E., Clarke B., Rowlands D., Lemon S.M. Structural requirements for initiation of translation by internal ribosome entry within genome-length hepatitis C virus RNA. Virology 1996, 222:31-42.
22. Honda M., Beard M.R., Ping L.H., Lemon S.M. A phylogenetically conserved stem-loop structure at the 5' border of the internal ribosome entry site of hepatitis C virus is required for cap-independent viral translation. J. Virol. 1999, 73:1165-1174.
23. Honda M., Rijnbrand R., Abell G., Kim D., Lemon S.M. Natural variation in translational activities of the 5' nontranslated RNAs of hepatitis C virus genotypes 1a and 1b: evidence for a long-range RNA-RNA interaction outside of the internal ribosomal entry site. J. Virol. 1999, 73:4941-4951.
24. Horner S.M., Gale M. Intracellular innate immune cascades and interferon defenses that control hepatitis C virus. J. Interferon Cytokine Res. 2009, 29:489-498.
25. Hwang S.B., Lo S.Y., Ou J.H., Lai M.M. Detection of cellular proteins and viral core protein interacting with the 5' untranslated region of hepatitis C virus RNA. J. Biomed. Sci. 1995, 2:227-236.
26. Jensen T.B., Gottwein J.M., Scheel T.K., Hoegh A.M., Eugen-Olsen J., Bukh J. Highly efficient JFH1-based cell-culture system for hepatitis C virus genotype 5a: failure of homologous neutralizing-antibody treatment to control infection. J. Infect. Dis. 2008, 198:1756-1765.
27. Jopling C.L., Yi M., Lancaster A.M., Lemon S.M., Sarnow P. Modulation of hepatitis C virus RNA abundance by a liver-specific MicroRNA. Science 2005, 309:1577-1581.
28. Jopling C.L., Schutz S., Sarnow P. Position-dependent function for a tandem microRNA miR-122-binding site located in the hepatitis C virus RNA genome. Cell Host Microbe 2008, 4:77-85.
29. Kato T., Furusaka A., Miyamoto M., Date T., Yasui K., Hiramoto J., Nagayama K., Tanaka T., Wakita T. Sequence analysis of hepatitis C virus isolated from a fulminant hepatitis patient. J. Med. Virol. 2001, 64:334-339.
30. Kim Y.K., Kim C.S., Lee S.H., Jang S.K. Domains I and II in the 5' nontranslated region of the HCV genome are required for RNA replication. Biochem. Biophys. Res. Commun. 2002, 290:105-112.
31. Kim Y.K., Lee S.H., Kim C.S., Seol S.K., Jang S.K. Long-range RNA-RNA interaction between the 5' nontranslated region and the core-coding sequences of hepatitis C virus modulates the IRES-dependent translation. RNA 2003, 9:599-606.
32. Koev G., Duncan R.F., Lai M.M. Hepatitis C virus IRES-dependent translation is insensitive to an eIF2alpha-independent mechanism of inhibition by interferon in hepatocyte cell lines. Virology 2002, 297:195-202.
33. Kolykhalov A.A., Agapov E.V., Blight K.J., Mihalik K., Feinstone S.M., Rice C.M. Transmission of hepatitis C by intrahepatic inoculation with transcribed RNA. Science 1997, 277:570-574.
34. Lafuente E., Ramos R., Martinez-Salas E. Long-range RNA-RNA interactions between distant regions of the hepatitis C virus internal ribosome entry site element. J. Gen. Virol. 2002, 83:1113-1121.
35. Lanford R.E., Hildebrandt-Eriksen E.S., Petri A., Persson R., Lindow M., Munk M.E., Kauppinen S., Orum H. Therapeutic silencing of microRNA-122 in primates with chronic hepatitis C virus infection. Science 2010, 327:198-201.
36. Li Y.P., Gottwein J.M., Scheel T.K., Jensen T.B., Bukh J. MicroRNA-122 antagonism against hepatitis C virus genotype 1-6 and reduced efficacy by host RNA insertion or mutations in the HCV 5'UTR. Proc. Natl. Acad. Sci. U.S.A. 2011, 108:4991-4996.
37. Lindenbach B.D., Evans M.J., Syder A.J., Wolk B., Tellinghuisen T.L., Liu C.C., Maruyama T., Hynes R.O., Burton D.R., McKeating J.A., Rice C.M. Complete replication of hepatitis C virus in cell culture. Science 2005, 309:623-626.
38. Lu M., Wiese M., Roggendorf M. Selection of genetic variants of the 5' noncoding region of hepatitis C virus occurs only in patients responding to interferon alpha therapy. J. Med. Virol. 1999, 59:146-153.
39. Luo G., Hamatake R.K., Mathis D.M., Racela J., Rigat K.L., Lemm J., Colonno R.J. De novo initiation of RNA synthesis by the RNA-dependent RNA polymerase (NS5B) of hepatitis C virus. J. Virol. 2000, 74:851-863.
40. Luo G., Xin S., Cai Z. Role of the 5'-proximal stem-loop structure of the 5' untranslated region in replication and translation of hepatitis C virus RNA. J. Virol. 2003, 77:3312-3318.
41. Machlin E.S., Sarnow P., Sagan S.M. Masking the 5' terminal nucleotides of the hepatitis C virus genome by an unconventional microRNA-target RNA complex. Proc. Natl. Acad. Sci. U.S.A. 2011, 108:3193-3198.
42. Manns M.P., Foster G.R., Rockstroh J.K., Zeuzem S., Zoulim F., Houghton M. The way forward in HCV treatment-finding the right path. Nat. Rev. Drug Discov. 2007, 6:991-1000.
43. Moradpour D., Penin F., Rice C.M. Replication of hepatitis C virus. Nat. Rev. Microbiol. 2007, 5:453-463.
44. Motazakker M., Preikschat P., Elliott J., Smith C.A., Mills P.R., Oien K., Spence E., Elliott R.M., McCruden E.A. Translation efficiencies of the 5'-untranslated region of genotypes 1a and 3a in hepatitis C infected patients. J. Med. Virol. 2007, 79:259-269.
45. Murphy D., Chamerland J., Dandavino R., Sablonm E. A new genotype of hepatitis C virus orginating from central Africa. Hepatology 2007, 46:623A.
46. Parsons J., Castaldi M.P., Dutta S., Dibrov S.M., Wyles D.L., Hermann T. Conformational inhibition of the hepatitis C virus internal ribosome entry site RNA. Nat. Chem. Biol. 2009, 5:823-825.
47. Paulsen R.B., Seth P.P., Swayze E.E., Griffey R.H., Skalicky J.J., Cheatham T.E., Davis D.R. Inhibitor-induced structural change in the HCV IRES domain IIa RNA. Proc. Natl. Acad. Sci. U.S.A. 2010, 107:7263-7268.
48. Pawlotsky J.M. The nature of interferon-alpha resistance in hepatitis C virus infection. Curr. Opin. Infect. Dis. 2003, 16:587-592.
49. Poynard T., Yuen M.F., Ratziu V., Lai C.L. Viral hepatitis. Lancet 2003, 362:2095-2100.
50. Prentoe J., Jensen T.B., Meuleman P., Serre S.B., Scheel T.K., Leroux-Roels G., Gottwein J.M., Bukh J. Hypervariable region 1 differentially impacts viability of hepatitis C genotype 1-6 strains and impairs virus neutralization. J. Virol. 2011, 85:2224-2234.
51. Reusken C.B., Dalebout T.J., Eerligh P., Bredenbeek P.J., Spaan W.J. Analysis of hepatitis C virus/classical swine fever virus chimeric 5'NTRs: sequences within the hepatitis C virus IRES are required for viral RNA replication. J. Gen. Virol. 2003, 84:1761-1769.
52. Reynolds J.E., Kaminski A., Kettinen H.J., Grace K., Clarke B.E., Carroll A.R., Rowlands D.J., Jackson R.J. Unique features of internal initiation of hepatitis C virus RNA translation. EMBO J. 1995, 14:6010-6020.
53. Romero-Lopez C., Berzal-Herranz A. A long-range RNA-RNA interaction between the 5' and 3' ends of the HCV genome. RNA 2009, 15:1740-1752.
54. Ross R.S., Viazov S.O., Holtzer C.D., Beyou A., Monnet A., Mazure C., Roggendorf M. Genotyping of hepatitis C virus isolates using CLIP sequencing. J. Clin. Microbiol. 2000, 38:3581-3584.
55. Saito T., Owen D.M., Jiang F., Marcotrigiano J., Gale M. Innate immunity induced by composition-dependent RIG-I recognition of hepatitis C virus RNA. Nature 2008, 454:523-527.
56. Sakai A., Takikawa S., Thimme R., Meunier J.C., Spangenberg H.C., Govindarajan S., Farci P., Emerson S.U., Chisari F.V., Purcell R.H., Bukh J. In vivo study of the HC-TN strain of hepatitis C virus recovered from a patient with fulminant hepatitis: RNA transcripts of a molecular clone (pHC-TN) are infectious in chimpanzees but not in Huh7.5 cells. J. Virol. 2007, 81:7208-7219.
57. Scheel T.K., Gottwein J.M., Jensen T.B., Prentoe J.C., Hoegh A.M., Alter H.J., Eugen-Olsen J., Bukh J. Development of JFH1-based cell culture systems for hepatitis C virus genotype 4a and evidence for cross-genotype neutralization. Proc. Natl. Acad. Sci. U.S.A. 2008, 105:997-1002.
58. Scheel T.K., Gottwein J.M., Carlsen T.H., Li Y.P., Jensen T.B., Spengler U., Weis N., Bukh J. Efficient culture adaptation of hepatitis C virus recombinants with genotype-specific core-NS2 by using previously identified mutations. J. Virol. 2011, 85:2891-2906.
59. Scheel T.K., Gottwein J.M., Mikkelsen L.S., Jensen T.B., Bukh J. Recombinant HCV variants with NS5A from genotypes 1-7 have different sensitivities to an NS5A inhibitor but not interferon-alpha. Gastroenterology 2011, 140:1032-1042.
60. Shi S.T., Lai M.M.C. HCV 5' and 3'UTR: when translation meets replication. Hepatitis C Viruses: Genomes and Molecular Biology 2006, 49-87. Horizon Bioscience, Norfolk, UK. S.L. Tan (Ed.).
61. Simmonds P., Bukh J., Combet C., Deleage G., Enomoto N., Feinstone S., Halfon P., Inchauspe G., Kuiken C., Maertens G., Mizokami M., Murphy D.G., Okamoto H., Pawlotsky J.M., Penin F., Sablon E., Shin I., Stuyver L.J., Thiel H.J., Viazov S., Weiner A.J., Widell A. Consensus proposals for a unified system of nomenclature of hepatitis C virus genotypes. Hepatology 2005, 42:962-973.
62. Soler M., Pellerin M., Malnou C.E., Dhumeaux D., Kean K.M., Pawlotsky J.M. Quasispecies heterogeneity and constraints on the evolution of the 5' noncoding region of hepatitis C virus (HCV): relationship with HCV resistance to interferon-alpha therapy. Virology 2002, 298:160-173.
63. Song Y., Friebe P., Tzima E., Junemann C., Bartenschlager R., Niepmann M. The hepatitis C virus RNA 3'-untranslated region strongly enhances translation directed by the internal ribosome entry site. J. Virol. 2006, 80:11579-11588.
64. Sumpter R., Loo Y.M., Foy E., Li K., Yoneyama M., Fujita T., Lemon S.M., Gale M. Regulating intracellular antiviral defense and permissiveness to hepatitis C virus RNA replication through a cellular RNA helicase, RIG-I. J. Virol. 2005, 79:2689-2699.
65. Takeda Y., Okoshi S., Suzuki K., Yano M., Gangemi J.D., Jay G., Asakura H., Aoyagi Y. Effect of interferon alpha and cell cycle progression on translation mediated by the hepatitis C virus 5' untranslated region: a study using a transgenic mouse model. J. Viral Hepat. 2004, 11:33-44.
66. Tanaka Y., Shimoike T., Ishii K., Suzuki R., Suzuki T., Ushijima H., Matsuura Y., Miyamura T. Selective binding of hepatitis C virus core protein to synthetic oligonucleotides corresponding to the 5' untranslated region of the viral genome. Virology 2000, 270:229-236.
67. Tsukiyama-Kohara K., Iizuka N., Kohara M., Nomoto A. Internal ribosome entry site within hepatitis C virus RNA. J. Virol. 1992, 66:1476-1483.
68. Wakita T., Pietschmann T., Kato T., Date T., Miyamoto M., Zhao Z., Murthy K., Habermann A., Krausslich H.G., Mizokami M., Bartenschlager R., Liang T.J. Production of infectious hepatitis C virus in tissue culture from a cloned viral genome. Nat. Med. 2005, 11:791-796.
69. Wang C., Sarnow P., Siddiqui A. Translation of human hepatitis C virus RNA in cultured cells is mediated by an internal ribosome-binding mechanism. J. Virol. 1993, 67:3338-3344.
70. Yanagi M., Purcell R.H., Emerson S.U., Bukh J. Transcripts from a single full-length cDNA clone of hepatitis C virus are infectious when directly transfected into the liver of a chimpanzee. Proc. Natl. Acad. Sci. U.S.A. 1997, 94:8738-8743.
71. Yu K.L., Jang S.I., You J.C. Identification of in vivo interaction between hepatitis C virus core protein and 5' and 3' UTR RNA. Virus Res. 2009, 145:285-292.
72. Zeuzem S. Heterogeneous virologic response rates to interferon-based therapy in patients with chronic hepatitis C: who responds less well?. Ann. Intern. Med. 2004, 140:370-381.
73. Zeuzem S. Interferon-based therapy for chronic hepatitis C: current and future perspectives. Nat. Clin. Pract. Gastroenterol. Hepatol. 2008, 5:610-622.
74. Zhong W., Ferrari E., Lesburg C.A., Maag D., Ghosh S.K., Cameron C.E., Lau J.Y., Hong Z. Template/primer requirements and single nucleotide incorporation by hepatitis C virus nonstructural protein 5B polymerase. J. Virol. 2000, 74:9134-9143.
75. Zhong W., Uss A.S., Ferrari E., Lau J.Y., Hong Z. De novo initiation of RNA synthesis by hepatitis C virus nonstructural protein 5B polymerase. J. Virol. 2000, 74:2017-2022.
76. Zhong J., Gastaminza P., Cheng G., Kapadia S., Kato T., Burton D.R., Wieland S.F., Uprichard S.L., Wakita T., Chisari F.V. Robust hepatitis C virus infection in vitro. Proc. Natl. Acad. Sci. U.S.A. 2005, 102:9294-9299.