Integrative Functional Genomics of Hepatitis C Virus Infection Identifies Host Dependencies in Complete Viral Replication Cycle

PLoS Pathogens

Volumn 10, Issue 5, 2014, Pages

  Li, Qisheng ^a   Zhang, Yong Yuan ^a   Chiu, Stephan ^a   Hu, Zongyi ^a   Lan, Keng Hsin ^a   Cha, Helen ^a   Sodroski, Catherine ^a   Zhang, Fang ^a   Hsu, Ching Sheng ^a   Thomas, Emmanuel ^a   Liang, T Jake ^a  

^a NATIONAL INSTITUTE OF DIABETES AND DIGESTIVE AND KIDNEY DISEASES   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

DEUBIQUITINASE; SMAD6 PROTEIN; SMALL INTERFERING RNA; VIRUS RECEPTOR;

ARTICLE; BIOINFORMATICS; CONTROLLED STUDY; FUNCTIONAL GENOMICS; GENE EXPRESSION; GENE SILENCING; GENETIC TRANSCRIPTION; GENETIC TRANSFECTION; GENOTYPE; HEPATITIS C; HUMAN; HUMAN CELL; RNA ISOLATION; RNA TRANSLATION; SIGNAL TRANSDUCTION; VIRUS ENTRY; VIRUS REPLICATION; CELL CULTURE; ENZYMOLOGY; GENETICS; GENOMICS; HEPACIVIRUS; HOST PATHOGEN INTERACTION; PHYSIOLOGY; PROCEDURES; SYSTEM ANALYSIS; VIROLOGY; VIRUS ASSEMBLY; VIRUS GENE; VIRUS SHEDDING;

CELLS, CULTURED; GENES, VIRAL; GENOMICS; HEPACIVIRUS; HEPATITIS C; HOST-PATHOGEN INTERACTIONS; HUMANS; RECEPTORS, VIRUS; RNA, SMALL INTERFERING; SYSTEMS INTEGRATION; VIRUS ASSEMBLY; VIRUS INTERNALIZATION; VIRUS REPLICATION; VIRUS SHEDDING;

EID: 84901688047     PISSN: 15537366     EISSN: 15537374     Source Type: Journal    
DOI: 10.1371/journal.ppat.1004163     Document Type: Article

References (70)

1. Liang TJ, Rehermann B, Seeff LB, Hoofnagle JH, (2000) Pathogenesis, natural history, treatment, and prevention of hepatitis C. Annals of internal medicine 132: 296-305.
2. Liang TJ, Ghany MG, (2013) Current and future therapies for hepatitis C virus infection. The New England journal of medicine 368: 1907-1917.
3. 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.
4. 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. Proceedings of the National Academy of Sciences of the United States of America 106: 16410-16415.
5. Randall G, Panis M, Cooper JD, Tellinghuisen TL, Sukhodolets KE, et al. (2007) Cellular cofactors affecting hepatitis C virus infection and replication. Proceedings of the National Academy of Sciences of the United States of America 104: 12884-12889.
6. 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.
7. Moradpour D, Penin F, Rice CM, (2007) Replication of hepatitis C virus. Nature reviews Microbiology 5: 453-463.
8. Ploss A, Evans MJ, (2012) Hepatitis C virus host cell entry. Current opinion in virology 2: 14-19.
9. Bartenschlager R, Penin F, Lohmann V, Andre P, (2011) Assembly of infectious hepatitis C virus particles. Trends in microbiology 19: 95-103.
10. Friedel CC, Haas J, (2011) Virus-host interactomes and global models of virus-infected cells. Trends in microbiology 19: 501-508.
11. Katze MG, Fornek JL, Palermo RE, Walters KA, Korth MJ, (2008) Innate immune modulation by RNA viruses: emerging insights from functional genomics. Nature reviews Immunology 8: 644-654.
12. Panda D, Cherry S, (2012) Cell-based genomic screening: elucidating virus-host interactions. Current opinion in virology 2: 784-792.
13. Berger KL, Cooper JD, Heaton NS, Yoon R, Oakland TE, et al. (2009) Roles for endocytic trafficking and phosphatidylinositol 4-kinase III alpha in hepatitis C virus replication. Proceedings of the National Academy of Sciences of the United States of America 106: 7577-7582.
14. Lupberger J, Zeisel MB, Xiao F, Thumann C, Fofana I, et al. (2011) EGFR and EphA2 are host factors for hepatitis C virus entry and possible targets for antiviral therapy. Nature medicine 17: 589-595.
15. Reiss S, Rebhan I, Backes P, Romero-Brey I, Erfle H, et al. (2011) Recruitment and activation of a lipid kinase by hepatitis C virus NS5A is essential for integrity of the membranous replication compartment. Cell host & microbe 9: 32-45.
16. Bartosch B, Dubuisson J, Cosset FL, (2003) Infectious hepatitis C virus pseudo-particles containing functional E1-E2 envelope protein complexes. The Journal of experimental medicine 197: 633-642.
17. 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.
18. Song Y, Friebe P, Tzima E, Junemann C, Bartenschlager R, et al. (2006) The hepatitis C virus RNA 3′-untranslated region strongly enhances translation directed by the internal ribosome entry site. Journal of virology 80: 11579-11588.
19. Lindenbach BD, Evans MJ, Syder AJ, Wolk B, Tellinghuisen TL, et al. (2005) Complete replication of hepatitis C virus in cell culture. Science 309: 623-626.
20. Wakita T, Pietschmann T, Kato T, Date T, Miyamoto M, et al. (2005) Production of infectious hepatitis C virus in tissue culture from a cloned viral genome. Nature medicine 11: 791-796.
21. Zhong J, Gastaminza P, Cheng G, Kapadia S, Kato T, et al. (2005) Robust hepatitis C virus infection in vitro. Proceedings of the National Academy of Sciences of the United States of America 102: 9294-9299.
22. Steinmann E, Brohm C, Kallis S, Bartenschlager R, Pietschmann T, (2008) Efficient trans-encapsidation of hepatitis C virus RNAs into infectious virus-like particles. Journal of virology 82: 7034-7046.
23. Masaki T, Suzuki R, Saeed M, Mori K, Matsuda M, et al. (2010) Production of infectious hepatitis C virus by using RNA polymerase I-mediated transcription. Journal of virology 84: 5824-5835.
24. Mohr S, Bakal C, Perrimon N, (2010) Genomic screening with RNAi: results and challenges. Annual review of biochemistry 79: 37-64.
25. Sigoillot FD, King RW, (2011) Vigilance and validation: Keys to success in RNAi screening. ACS chemical biology 6: 47-60.
26. Andersen SS, (2000) Spindle assembly and the art of regulating microtubule dynamics by MAPs and Stathmin/Op18. Trends in cell biology 10: 261-267.
27. Roohvand F, Maillard P, Lavergne JP, Boulant S, Walic M, et al. (2009) Initiation of hepatitis C virus infection requires the dynamic microtubule network: role of the viral nucleocapsid protein. The Journal of biological chemistry 284: 13778-13791.
28. Wolk B, Buchele B, Moradpour D, Rice CM, (2008) A dynamic view of hepatitis C virus replication complexes. Journal of virology 82: 10519-10531.
29. 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.
30. Vaillancourt FH, Pilote L, Cartier M, Lippens J, Liuzzi M, et al. (2009) Identification of a lipid kinase as a host factor involved in hepatitis C virus RNA replication. Virology 387: 5-10.
31. Hinson ER, Cresswell P, (2009) The antiviral protein, viperin, localizes to lipid droplets via its N-terminal amphipathic alpha-helix. Proceedings of the National Academy of Sciences of the United States of America 106: 20452-20457.
32. Helbig KJ, Eyre NS, Yip E, Narayana S, Li K, et al. (2011) The antiviral protein viperin inhibits hepatitis C virus replication via interaction with nonstructural protein 5A. Hepatology 54: 1506-1517.
33. Sainz B Jr, Barretto N, Martin DN, Hiraga N, Imamura M, et al. (2012) Identification of the Niemann-Pick C1-like 1 cholesterol absorption receptor as a new hepatitis C virus entry factor. Nature medicine 18: 281-285.
34. Barrowman J, Bhandari D, Reinisch K, Ferro-Novick S, (2010) TRAPP complexes in membrane traffic: convergence through a common Rab. Nature reviews Molecular cell biology 11: 759-763.
35. Pileri P, Uematsu Y, Campagnoli S, Galli G, Falugi F, et al. (1998) Binding of hepatitis C virus to CD81. Science 282: 938-941.
36. Evans MJ, von Hahn T, Tscherne DM, Syder AJ, Panis M, et al. (2007) Claudin-1 is a hepatitis C virus co-receptor required for a late step in entry. Nature 446: 801-805.
37. Ploss A, Evans MJ, Gaysinskaya VA, Panis M, You H, et al. (2009) Human occludin is a hepatitis C virus entry factor required for infection of mouse cells. Nature 457: 882-886.
38. Mercer J, Helenius A, (2009) Virus entry by macropinocytosis. Nature cell biology 11: 510-520.
39. Brazzoli M, Bianchi A, Filippini S, Weiner A, Zhu Q, et al. (2008) CD81 is a central regulator of cellular events required for hepatitis C virus infection of human hepatocytes. Journal of virology 82: 8316-8329.
40. Li Z, Vance DE, (2008) Phosphatidylcholine and choline homeostasis. Journal of lipid research 49: 1187-1194.
41. Haid S, Pietschmann T, Pecheur EI, (2009) Low pH-dependent hepatitis C virus membrane fusion depends on E2 integrity, target lipid composition, and density of virus particles. The Journal of biological chemistry 284: 17657-17667.
42. Blanchard E, Belouzard S, Goueslain L, Wakita T, Dubuisson J, et al. (2006) Hepatitis C virus entry depends on clathrin-mediated endocytosis. Journal of virology 80: 6964-6972.
43. Meertens L, Bertaux C, Dragic T, (2006) Hepatitis C virus entry requires a critical postinternalization step and delivery to early endosomes via clathrin-coated vesicles. Journal of virology 80: 11571-11578.
44. Sun X, Yau VK, Briggs BJ, Whittaker GR, (2005) Role of clathrin-mediated endocytosis during vesicular stomatitis virus entry into host cells. Virology 338: 53-60.
45. Riento K, Ridley AJ, (2003) Rocks: multifunctional kinases in cell behaviour. Nature reviews Molecular cell biology 4: 446-456.
46. Goldenberg NM, Grinstein S, Silverman M, (2007) Golgi-bound Rab34 is a novel member of the secretory pathway. Molecular biology of the cell 18: 4762-4771.
47. Coyne CB, Shen L, Turner JR, Bergelson JM, (2007) Coxsackievirus entry across epithelial tight junctions requires occludin and the small GTPases Rab34 and Rab5. Cell host & microbe 2: 181-192.
48. Trotard M, Lepere-Douard C, Regeard M, Piquet-Pellorce C, Lavillette D, et al. (2009) Kinases required in hepatitis C virus entry and replication highlighted by small interference RNA screening. FASEB journal: official publication of the Federation of American Societies for Experimental Biology 23: 3780-3789.
49. Syed GH, Amako Y, Siddiqui A, (2010) Hepatitis C virus hijacks host lipid metabolism. Trends in endocrinology and metabolism: TEM 21: 33-40.
50. Demirov D, Gabriel G, Schneider C, Hohenberg H, Ludwig S, (2012) Interaction of influenza A virus matrix protein with RACK1 is required for virus release. Cellular microbiology 14: 774-789.
51. Gallina A, Rossi F, Milanesi G, (2001) Rack1 binds HIV-1 Nef and can act as a Nef-protein kinase C adaptor. Virology 283: 7-18.
52. Nilsson J, Sengupta J, Frank J, Nissen P, (2004) Regulation of eukaryotic translation by the RACK1 protein: a platform for signalling molecules on the ribosome. EMBO reports 5: 1137-1141.
53. Benga WJ, Krieger SE, Dimitrova M, Zeisel MB, Parnot M, et al. (2010) Apolipoprotein E interacts with hepatitis C virus nonstructural protein 5A and determines assembly of infectious particles. Hepatology 51: 43-53.
54. Cun W, Jiang J, Luo G, (2010) The C-terminal alpha-helix domain of apolipoprotein E is required for interaction with nonstructural protein 5A and assembly of hepatitis C virus. Journal of virology 84: 11532-11541.
55. Huang H, Sun F, Owen DM, Li W, Chen Y, et al. (2007) Hepatitis C virus production by human hepatocytes dependent on assembly and secretion of very low-density lipoproteins. Proceedings of the National Academy of Sciences of the United States of America 104: 5848-5853.
56. Herker E, Harris C, Hernandez C, Carpentier A, Kaehlcke K, et al. (2010) Efficient hepatitis C virus particle formation requires diacylglycerol acyltransferase-1. Nature medicine 16: 1295-1298.
57. Li Q, Pene V, Krishnamurthy S, Cha H, Liang TJ, (2013) Hepatitis C virus infection activates an innate pathway involving IKK-alpha in lipogenesis and viral assembly. Nature medicine 19: 722-729.
58. Gastaminza P, Kapadia SB, Chisari FV, (2006) Differential biophysical properties of infectious intracellular and secreted hepatitis C virus particles. Journal of virology 80: 11074-11081.
59. Coller KE, Heaton NS, Berger KL, Cooper JD, Saunders JL, et al. (2012) Molecular determinants and dynamics of hepatitis C virus secretion. PLoS pathogens 8: e1002466.
60. Shintani Y, Fujie H, Miyoshi H, Tsutsumi T, Tsukamoto K, et al. (2004) Hepatitis C virus infection and diabetes: direct involvement of the virus in the development of insulin resistance. Gastroenterology 126: 840-848.
61. Li Q, Ali MA, Cohen JI, (2006) Insulin degrading enzyme is a cellular receptor mediating varicella-zoster virus infection and cell-to-cell spread. Cell 127: 305-316.
62. Timpe JM, Stamataki Z, Jennings A, Hu K, Farquhar MJ, et al. (2008) Hepatitis C virus cell-cell transmission in hepatoma cells in the presence of neutralizing antibodies. Hepatology 47: 17-24.
63. Melotte V, Qu X, Ongenaert M, van Criekinge W, de Bruine AP, et al. (2010) The N-myc downstream regulated gene (NDRG) family: diverse functions, multiple applications. FASEB journal: official publication of the Federation of American Societies for Experimental Biology 24: 4153-4166.
64. Kachhap SK, Faith D, Qian DZ, Shabbeer S, Galloway NL, et al. (2007) The N-Myc down regulated Gene1 (NDRG1) Is a Rab4a effector involved in vesicular recycling of E-cadherin. PloS one 2: e844.
65. Hagist S, Sultmann H, Millonig G, Hebling U, Kieslich D, et al. (2009) In vitro-targeted gene identification in patients with hepatitis C using a genome-wide microarray technology. Hepatology 49: 378-386.
66. Kato T, Matsumura T, Heller T, Saito S, Sapp RK, et al. (2007) Production of infectious hepatitis C virus of various genotypes in cell cultures. Journal of virology 81: 4405-4411.
67. Gottwein JM, Scheel TK, Jensen TB, Lademann JB, Prentoe JC, et al. (2009) 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 49: 364-377.
68. Gottwein JM, Jensen TB, Mathiesen CK, Meuleman P, Serre SB, et al. (2011) Development and application of hepatitis C reporter viruses with genotype 1 to 7 core-nonstructural protein 2 (NS2) expressing fluorescent proteins or luciferase in modified JFH1 NS5A. Journal of virology 85: 8913-8928.
69. Matsumura T, Hu Z, Kato T, Dreux M, Zhang YY, et al. (2009) Amphipathic DNA polymers inhibit hepatitis C virus infection by blocking viral entry. Gastroenterology 137: 673-681.
70. Lavillette D, Tarr AW, Voisset C, Donot P, Bartosch B, et al. (2005) Characterization of host-range and cell entry properties of the major genotypes and subtypes of hepatitis C virus. Hepatology 41: 265-274.