Replication Vesicles are Load- and Choke-Points in the Hepatitis C Virus Lifecycle

PLoS Pathogens

Volumn 9, Issue 8, 2013, Pages

  Binder, Marco ^a   Sulaimanov, Nurgazy ^b,c   Clausznitzer, Diana ^b   Schulze, Manuel ^b   Hüber, Christian M ^a,e   Lenz, Simon M ^c   Schlöder, Johannes P ^c   Trippler, Martin ^d   Bartenschlager, Ralf ^a   Lohmann, Volker ^a   Kaderali, Lars ^b,c  

^a UNIVERSITY OF HEIDELBERG   (Germany)

^b DRESDEN UNIVERSITY OF TECHNOLOGY   (Germany)

^c UNIVERSITY OF HEIDELBERG   (Germany)

^d UNIVERSITY HOSPITAL ESSEN   (Germany)

^e UNIVERSITY OF CAMBRIDGE   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

HOST FACTOR; NONSTRUCTURAL PROTEIN 4B; NONSTRUCTURAL PROTEIN 5A; VIRUS RNA; VIRUS PROTEIN;

ARTICLE; CALIBRATION; CONTROLLED STUDY; ELECTROPORATION; GENE EXPRESSION; HEPATITIS C VIRUS; HUMAN; HUMAN CELL; LIFE CYCLE; MATHEMATICAL MODEL; NORTHERN BLOTTING; PREDICTION; PROTEIN EXPRESSION; RNA REPLICATION; RNA SYNTHESIS; SENSITIVITY ANALYSIS; SIMULATION; SPECTROPHOTOMETRY; VIRUS GENOME; VIRUS REPLICATION; VIRUS TRANSCRIPTION; BIOLOGICAL MODEL; BIOSYNTHESIS; CELL LINE; GENETICS; HEPACIVIRUS; PHYSIOLOGY; PROTEIN SYNTHESIS;

CELL LINE; HEPACIVIRUS; HUMANS; MODELS, BIOLOGICAL; PROTEIN BIOSYNTHESIS; RNA, VIRAL; VIRAL PROTEINS; VIRUS REPLICATION;

EID: 84883319848     PISSN: 15537366     EISSN: 15537374     Source Type: Journal    
DOI: 10.1371/journal.ppat.1003561     Document Type: Article

References (95)

1. Rantala M, van de Laar MJ, (2008) Surveillance and epidemiology of hepatitis B and C in Europe- a review. Euro Surveill 13: pii: 18880.
2. Alter MJ, Margolis HS, Krawczynski K, Judson FN, Mares A, et al. (1992) The natural history of community-acquired hepatitis C in the United States. The Sentinel Counties Chronic non-A, non-B Hepatitis Study Team. N Engl J Med 327: 1899-1905.
3. Chen SL, Morgan TR, (2006) The natural history of hepatitis C virus (HCV) infection. Int J Med Sci 3: 47-52.
4. Poynard T, Ratziu V, Benhamou Y, Opolon P, Cacoub P, et al. (2000) Natural history of HCV infection. Baillieres Best Pract Res Clin Gastroenterol 14: 211-228.
5. Moradpour D, Penin F, Rice CM, (2007) Replication of hepatitis C virus. Nat Rev Microbiol 5: 453-463.
6. Romero-Brey I, Merz A, Chiramel A, Lee JY, Chlanda P, et al. (2012) Three-dimensional architecture and biogenesis of membrane structures associated with hepatitis C virus replication. PLoS pathogens 8: e1003056.
7. Gosert R, Egger D, Lohmann V, Bartenschlager R, Blum HE, et al. (2003) Identification of the hepatitis C virus RNA replication complex in Huh-7 cells harboring subgenomic replicons. J Virol 77: 5487-5492.
8. Welsch S, Miller S, Romero-Brey I, Merz A, Bleck CK, et al. (2009) Composition and three-dimensional architecture of the dengue virus replication and assembly sites. Cell Host Microbe 5: 365-375.
9. Bartenschlager R, (2006) Hepatitis C virus molecular clones: from cDNA to infectious virus particles in cell culture. Curr Opin Microbiol 9: 416-422.
10. Quinkert D, Bartenschlager R, Lohmann V, (2005) Quantitative analysis of the hepatitis C virus replication complex. J Virol 79: 13594-13605.
11. Randall RE, Goodbourn S, (2008) Interferons and viruses: an interplay between induction, signalling, antiviral responses and virus countermeasures. J Gen Virol 89: 1-47.
12. Thimme R, Binder M, Bartenschlager R, (2011) Failure of innate and adaptive immune responses in controlling hepatitis C virus infection. FEMS Microbiol Rev 36: 663-83.
13. Lackner T, Muller A, Pankraz A, Becher P, Thiel HJ, et al. (2004) Temporal modulation of an autoprotease is crucial for replication and pathogenicity of an RNA virus. Journal of virology 78: 10765-10775.
14. Neumann AU, Lam NP, Dahari H, Gretch DR, Wiley TE, et al. (1998) Hepatitis C viral dynamics in vivo and the antiviral efficacy of interferon-alpha therapy. Science 282: 103-107.
15. Dahari H, Major M, Zhang X, Mihalik K, Rice CM, et al. (2005) Mathematical modeling of primary hepatitis C infection: noncytolytic clearance and early blockage of virion production. Gastroenterology 128: 1056-1066.
16. Dahari H, Feliu A, Garcia-Retortillo M, Forns X, Neumann AU, (2005) Second hepatitis C replication compartment indicated by viral dynamics during liver transplantation. J Hepatol 42: 491-498.
17. Powers KA, Ribeiro RM, Patel K, Pianko S, Nyberg L, et al. (2006) Kinetics of hepatitis C virus reinfection after liver transplantation. Liver Transpl 12: 207-216.
18. Dahari H, Sainz B Jr, Perelson AS, Uprichard SL, (2009) Modeling subgenomic hepatitis C virus RNA kinetics during treatment with alpha interferon. J Virol 83: 6383-6390.
19. Dixit NM, Layden-Almer JE, Layden TJ, Perelson AS, (2004) Modelling how ribavirin improves interferon response rates in hepatitis C virus infection. Nature 432: 922-924.
20. Snoeck E, Chanu P, Lavielle M, Jacqmin P, Jonsson EN, et al. (2010) A comprehensive hepatitis C viral kinetic model explaining cure. Clin Pharmacol Ther 87: 706-713.
21. Perelson AS, Herrmann E, Micol F, Zeuzem S, (2005) New kinetic models for the hepatitis C virus. Hepatology 42: 749-754.
22. Binder M, Quinkert D, Bochkarova O, Klein R, Kezmic N, et al. (2007) Identification of determinants involved in initiation of hepatitis C virus RNA synthesis by using intergenotypic replicase chimeras. Journal of virology 81: 5270-5283.
23. Lohmann V, Korner F, Koch J, Herian U, Theilmann L, et al. (1999) Replication of subgenomic hepatitis C virus RNAs in a hepatoma cell line. Science 285: 110-113.
24. Dahari H, Ribeiro RM, Rice CM, Perelson AS, (2007) Mathematical modeling of subgenomic hepatitis C virus replication in Huh-7 cells. J Virol 81: 750-760.
25. Mishchenko EL, Bezmaternykh KD, Likhoshvai VA, Ratushny AV, Khlebodarova TM, et al. (2007) Mathematical model for suppression of subgenomic hepatitis C virus RNA replication in cell culture. J Bioinform Comput Biol 5: 593-609.
26. McLean AK, Luciani F, Tanaka MM, (2010) Trade-offs in resource allocation in the intracellular life-cycle of hepatitis C virus. J Theor Biol 267: 565-572.
27. Nakabayashi J, (2012) A compartmentalization model of hepatitis C virus replication: an appropriate distribution of HCV RNA for the effective replication. J Theor Biol 300: 110-117.
28. Krieger N, Lohmann V, Bartenschlager R, (2001) Enhancement of hepatitis C virus RNA replication by cell culture-adaptive mutations. J Virol 75: 4614-4624.
29. Keum SJ, Park SM, Park JH, Jung JH, Shin EJ, et al. (2012) The specific infectivity of hepatitis C virus changes through its life cycle. Virology 433: 462-470.
30. Lohmann V, Hoffmann S, Herian U, Penin F, Bartenschlager R, (2003) Viral and cellular determinants of hepatitis C virus RNA replication in cell culture. Journal of virology 77: 3007-3019.
31. Blight KJ, McKeating JA, Rice CM, (2002) Highly permissive cell lines for subgenomic and genomic hepatitis C virus RNA replication. Journal of virology 76: 13001-13014.
32. Binder M, Kochs G, Bartenschlager R, Lohmann V, (2007) Hepatitis C virus escape from the interferon regulatory factor 3 pathway by a passive and active evasion strategy. Hepatology 46: 1365-1374.
33. Kato T, Date T, Miyamoto M, Furusaka A, Tokushige K, et al. (2003) Efficient replication of the genotype 2a hepatitis C virus subgenomic replicon. Gastroenterology 125: 1808-1817.
34. Koutsoudakis G, Kaul A, Steinmann E, Kallis S, Lohmann V, et al. (2006) Characterization of the early steps of hepatitis C virus infection by using luciferase reporter viruses. J Virol 80: 5308-5320.
35. Novak JE, Kirkegaard K, (1994) Coupling between genome translation and replication in an RNA virus. Genes & development 8: 1726-1737.
36. Khromykh AA, Sedlak PL, Westaway EG, (2000) cis- and trans-acting elements in flavivirus RNA replication. Journal of virology 74: 3253-3263.
37. Grassmann CW, Isken O, Tautz N, Behrens SE, (2001) Genetic analysis of the pestivirus nonstructural coding region: defects in the NS5A unit can be complemented in trans. Journal of virology 75: 7791-7802.
38. Appel N, Herian U, Bartenschlager R, (2005) Efficient rescue of hepatitis C virus RNA replication by trans-complementation with nonstructural protein 5A. Journal of virology 79: 896-909.
39. Marino S, Hogue IB, Ray CJ, Kirschner DE, (2008) A methodology for performing global uncertainty and sensitivity analysis in systems biology. J Theor Biol 254: 178-196.
40. Saltelli A, Bolado R, (1998) An alternative way to compute Fourier amplitude sensitivity test (FAST). Comput Stat Data Anal 26 (4) (): 445-460 -.
41. Guo JT, Sohn JA, Zhu Q, Seeger C, (2004) Mechanism of the interferon alpha response against hepatitis C virus replicons. Virology 325: 71-81.
42. Pause A, Kukolj G, Bailey M, Brault M, Do F, et al. (2003) An NS3 serine protease inhibitor abrogates replication of subgenomic hepatitis C virus RNA. The Journal of biological chemistry 278: 20374-20380.
43. Windisch MP, Frese M, Kaul A, Trippler M, Lohmann V, et al. (2005) Dissecting the interferon-induced inhibition of hepatitis C virus replication by using a novel host cell line. Journal of virology 79: 13778-13793.
44. Alvisi G, Madan V, Bartenschlager R, (2011) Hepatitis C virus and host cell lipids: an intimate connection. RNA biology 8: 258-269.
45. Navratil V, de Chassey B, Meyniel L, Delmotte S, Gautier C, et al. (2009) VirHostNet: a knowledge base for the management and the analysis of proteome-wide virus-host interaction networks. Nucleic acids research 37: D661-668.
46. Borawski J, Troke P, Puyang X, Gibaja V, Zhao S, et al. (2009) Class III phosphatidylinositol 4-kinase alpha and beta are novel host factor regulators of hepatitis C virus replication. Journal of virology 83: 10058-10074.
47. Tai AW, Benita Y, Peng LF, Kim SS, Sakamoto N, et al. (2009) A functional genomic screen identifies cellular cofactors of hepatitis C virus replication. Cell Host & Microbe 5: 298-307.
48. Li Q, Brass AL, Ng A, Hu Z, Xavier RJ, et al. (2009) A genome-wide genetic screen for host factors required for hepatitis C virus propagation. Proc Natl Acad Sci U S A 106: 16410-16415.
49. Supekova L, Supek F, Lee J, Chen S, Gray N, et al. (2008) Identification of human kinases involved in hepatitis C virus replication by small interference RNA library screening. The Journal of biological chemistry 283: 29-36.
50. Booker M, Samsonova AA, Kwon Y, Flockhart I, Mohr SE, et al. (2011) False negative rates in Drosophila cell-based RNAi screens: a case study. BMC genomics 12: 50.
51. de Chassey B, Navratil V, Tafforeau L, Hiet MS, Aublin-Gex A, et al. (2008) Hepatitis C virus infection protein network. Molecular systems biology 4: 230.
52. Bauhofer O, Ruggieri A, Schmid B, Schirmacher P, Bartenschlager R, (2012) Persistence of HCV in quiescent hepatic cells under conditions of an interferon-induced antiviral response. Gastroenterology 143: 429-438 e428.
53. Su AI, Pezacki JP, Wodicka L, Brideau AD, Supekova L, et al. (2002) Genomic analysis of the host response to hepatitis C virus infection. Proceedings of the National Academy of Sciences of the United States of America 99: 15669-15674.
54. Thimme R, Bukh J, Spangenberg HC, Wieland S, Pemberton J, et al. (2002) Viral and immunological determinants of hepatitis C virus clearance, persistence, and disease. Proceedings of the National Academy of Sciences of the United States of America 99: 15661-15668.
55. Thimme R, Binder M, Bartenschlager R, (2012) Failure of innate and adaptive immune responses in controlling hepatitis C virus infection. FEMS microbiology reviews 36: 663-683.
56. Kaul A, Stauffer S, Berger C, Pertel T, Schmitt J, et al. (2009) Essential role of cyclophilin A for hepatitis C virus replication and virus production and possible link to polyprotein cleavage kinetics. PLoS pathogens 5: e1000546.
57. Ghany MG, Nelson DR, Strader DB, Thomas DL, Seeff LB, (2011) An update on treatment of genotype 1 chronic hepatitis C virus infection: 2011 practice guideline by the American Association for the Study of Liver Diseases. Hepatology 54: 1433-1444.
58. Rong L, Dahari H, Ribeiro RM, Perelson AS, (2010) Rapid emergence of protease inhibitor resistance in hepatitis C virus. Science translational medicine 2: 30ra32.
59. Thompson AJ, Locarnini SA, Beard MR, (2011) Resistance to anti-HCV protease inhibitors. Current opinion in virology 1: 599-606.
60. Targett-Adams P, Graham EJ, Middleton J, Palmer A, Shaw SM, et al. (2011) Small molecules targeting hepatitis C virus-encoded NS5A cause subcellular redistribution of their target: insights into compound modes of action. Journal of virology 85: 6353-6368.
61. Pawlotsky JM, (2012) New antiviral agents for hepatitis C. F1000 biology reports 4: 5.
62. Sarrazin C, Hezode C, Zeuzem S, Pawlotsky JM, (2012) Antiviral strategies in hepatitis C virus infection. J Hepatol 56 Suppl 1: S88-100.
63. Egger D, Wolk B, Gosert R, Bianchi L, Blum HE, et al. (2002) Expression of hepatitis C virus proteins induces distinct membrane alterations including a candidate viral replication complex. Journal of virology 76: 5974-5984.
64. Padmanabhan P, Dixit NM, (2011) Mathematical model of viral kinetics in vitro estimates the number of E2-CD81 complexes necessary for hepatitis C virus entry. PLoS computational biology 7: e1002307.
65. Koutsoudakis G, Herrmann E, Kallis S, Bartenschlager R, Pietschmann T, (2007) The level of CD81 cell surface expression is a key determinant for productive entry of hepatitis C virus into host cells. Journal of virology 81: 588-598.
66. Long G, Hiet MS, Windisch MP, Lee JY, Lohmann V, et al. (2011) Mouse hepatic cells support assembly of infectious hepatitis C virus particles. Gastroenterology 141: 1057-1066.
67. Metz P, Dazert E, Ruggieri A, Mazur J, Kaderali L, et al. (2012) Identification of type I and type II interferon-induced effectors controlling hepatitis C virus replication. Hepatology 56: 2082-2093.
68. Schoggins JW, Wilson SJ, Panis M, Murphy MY, Jones CT, et al. (2011) A diverse range of gene products are effectors of the type I interferon antiviral response. Nature 472: 481-485.
69. Tautz N, Meyers G, Thiel HJ, (1998) Pathogenesis of mucosal disease, a deadly disease of cattle caused by a pestivirus. Clinical and diagnostic virology 10: 121-127.
70. Becher P, Tautz N, (2011) RNA recombination in pestiviruses: cellular RNA sequences in viral genomes highlight the role of host factors for viral persistence and lethal disease. RNA biology 8: 216-224.
71. Frolov I, Agapov E, Hoffman TA Jr, Pragai BM, Lippa M, et al. (1999) Selection of RNA replicons capable of persistent noncytopathic replication in mammalian cells. Journal of virology 73: 3854-3865.
72. Guedj J, Dahari H, Perelson AS, (2011) Understanding the nature of early HCV RNA blips and the use of mathematical modeling of viral kinetics during IFN-based therapy. Proceedings of the National Academy of Sciences of the United States of America 108: E302 author reply E303.
73. Schaller T, Appel N, Koutsoudakis G, Kallis S, Lohmann V, et al. (2007) Analysis of hepatitis C virus superinfection exclusion by using novel fluorochrome gene-tagged viral genomes. Journal of virology 81: 4591-4603.
74. Huang da W, Sherman BT, Lempicki RA, (2009) Systematic and integrative analysis of large gene lists using DAVID bioinformatics resources. Nature protocols 4: 44-57.
75. Huang da W, Sherman BT, Lempicki RA, (2009) Bioinformatics enrichment tools: paths toward the comprehensive functional analysis of large gene lists. Nucleic acids research 37: 1-13.
76. Wang C, Pflugheber J, Sumpter R Jr, Sodora DL, Hui D, et al. (2003) Alpha interferon induces distinct translational control programs to suppress hepatitis C virus RNA replication. J Virol 77: 3898-3912.
77. Oh JW, Ito T, Lai MM, (1999) A recombinant hepatitis C virus RNA-dependent RNA polymerase capable of copying the full-length viral RNA. J Virol 73: 7694-7702.
78. Ma H, Leveque V, De Witte A, Li W, Hendricks T, et al. (2005) Inhibition of native hepatitis C virus replicase by nucleotide and non-nucleoside inhibitors. Virology 332: 8-15.
79. Thompson JF, Hayes LS, Lloyd DB, (1991) Modulation of firefly luciferase stability and impact on studies of gene regulation. Gene 103: 171-177.
80. Leclerc GM, Boockfor FR, Faught WJ, Frawley LS, (2000) Development of a destabilized firefly luciferase enzyme for measurement of gene expression. BioTechniques 29: 590-591, 594-596, 598 passim.
81. Pause A, Kukolj G, Bailey M, Brault M, Do F, et al. (2003) An NS3 serine protease inhibitor abrogates replication of subgenomic hepatitis C virus RNA. J Biol Chem 278: 20374-20380.
82. Pietschmann T, Lohmann V, Rutter G, Kurpanek K, Bartenschlager R, (2001) Characterization of cell lines carrying self-replicating hepatitis C virus RNAs. J Virol 75: 1252-1264.
83. Bock HG (1981) Numerical Treatment of inverse problems in chemical reaction kinetics. In: Ebert KH, Deuflhard P, Jäger W, editors. Modelling of Chemical Reaction Systems. Berlin, Heidelberg, New York: Springer. pp. 102-125.
84. Bock HG, (1987) Randwertproblemmethoden zur Parameteridentifizierung in Systemen nichtlinearer Differentialgleichungen. Bonner Mathematische Schriften 183Bonn.
85. Bock HG, Kostina EA, Schlöder JP, (2007) Numerical Methods for Parameter Estimation in Nonlinear Differential Algebraic Equations. GAMM Mitteilungen 30: 376-408.
86. Rodriguez-Fernandez M, Banga JR, (2010) SensSB: a software toolbox for the development and sensitivity analysis of systems biology models. Bioinformatics 26: 1675-1676.
87. Daniels BC, Chen YJ, Sethna JP, Gutenkunst RN, Myers CR, (2008) Sloppiness, robustness, and evolvability in systems biology. Current opinion in biotechnology 19: 389-395.
88. Gutenkunst RN, Waterfall JJ, Casey FP, Brown KS, Myers CR, et al. (2007) Universally sloppy parameter sensitivities in systems biology models. PLoS computational biology 3: 1871-1878.
89. Saltelli A, Chan K, Scott EM (2000) Sensitivity analysis. Chichester; New York: Wiley. xv, 475 p. p.
90. Mohd-Ismail NK, Deng L, Sukumaran SK, Yu VC, Hotta H, et al. (2009) The hepatitis C virus core protein contains a BH3 domain that regulates apoptosis through specific interaction with human Mcl-1. Journal of virology 83: 9993-10006.
91. Drouet C, Bouillet L, Csopaki F, Colomb MG, (1999) Hepatitis C virus NS3 serine protease interacts with the serpin C1 inhibitor. FEBS letters 458: 415-418.
92. Prikhod'ko EA, Prikhod'ko GG, Siegel RM, Thompson P, Major ME, et al. (2004) The NS3 protein of hepatitis C virus induces caspase-8-mediated apoptosis independent of its protease or helicase activities. Virology 329: 53-67.
93. Street A, Macdonald A, Crowder K, Harris M, (2004) The Hepatitis C virus NS5A protein activates a phosphoinositide 3-kinase-dependent survival signaling cascade. The Journal of biological chemistry 279: 12232-12241.
94. He Y, Nakao H, Tan SL, Polyak SJ, Neddermann P, et al. (2002) Subversion of cell signaling pathways by hepatitis C virus nonstructural 5A protein via interaction with Grb2 and P85 phosphatidylinositol 3-kinase. Journal of virology 76: 9207-9217.
95. Domitrovich AM, Felmlee DJ, Siddiqui A, (2005) Hepatitis C virus nonstructural proteins inhibit apolipoprotein B100 secretion. The Journal of biological chemistry 280: 39802-39808.