The cell biology of hepatitis C virus

Microbes and Infection

Volumn 12, Issue 4, 2010, Pages 263-271

  Joyce, Michael A ^a   Tyrrell, D Lorne J ^a  

^a UNIVERSITY OF ALBERTA   (Canada)

Author keywords

Animals; Hepacivirus genetics immunology pathogenicity; Hepatitis C virus; Hepatitis C immunology virology; Host parasite relations; Humans; Interferons immunology metabolism; Signal transduction

Indexed keywords

APOLIPOPROTEIN B; APOLIPOPROTEIN E; FIBRONECTIN; LOW DENSITY LIPOPROTEIN; MALATHION; MITOGEN ACTIVATED PROTEIN KINASE; PROTEIN KINASE B; TRANSFORMING GROWTH FACTOR BETA; VERY LOW DENSITY LIPOPROTEIN;

ADAPTIVE IMMUNITY; APOPTOSIS; CELL STRAIN HEK293; CYTOLOGY; EXTRACELLULAR MATRIX; FOCAL ADHESION; GENE EXPRESSION; GENETIC VARIABILITY; GENOME; GENOTYPE; HEPATITIS C VIRUS; HOST CELL; IMMUNE RESPONSE; INNATE IMMUNITY; LIVER; LIVER CELL; NONHUMAN; PATHOGENESIS; PRIORITY JOURNAL; RNA VIRUS; SHORT SURVEY; SIGNAL TRANSDUCTION; VIRUS ENTRY; VIRUS PARTICLE; VIRUS REPLICATION;

HEPACIVIRUS; HEPATOCYTES; HOST-PATHOGEN INTERACTIONS; HUMANS;

ANIMALIA; HEPATITIS C VIRUS;

EID: 77649274843     PISSN: 12864579     EISSN: 1769714X     Source Type: Journal    
DOI: 10.1016/j.micinf.2009.12.012     Document Type: Short Survey

References (70)

1. Alter M.J., Margolis H.S., Krawczynski K., Judson F.N., Mares A., Alexander W.J., Hu P.Y., Miller J.K., Gerber M.A., Sampliner R.E., et al., The Sentinel Counties Chronic non-A, non-B Hepatitis Study Team. The natural history of community-acquired hepatitis C in the United States. N. Engl. J. Med. 327 (1992) 1899-1905
2. Timm J., and Roggendorf M. Sequence diversity of hepatitis C virus: implications for immune control and therapy. World J. Gastroenterol. 13 (2007) 4808-4817
3. Buratti E., Tisminetzky S., Zotti M., and Baralle F.E. Functional analysis of the interaction between HCV 5′UTR and putative subunits of eukaryotic translation initiation factor eIF3. Nucleic Acids Res. 26 (1998) 3179-3187
4. Jopling C.L., Norman K.L., and Sarnow P. Positive and negative modulation of viral and cellular mRNAs by liver-specific microRNA miR-122. Cold Spring Harb. Symp. Quant. Biol. 71 (2006) 369-376
5. Song Y., Friebe P., Tzima E., Junemann C., Bartenschlager R., and Niepmann M. The hepatitis C virus RNA 3′-untranslated region strongly enhances translation directed by the internal ribosome entry site. J. Virol. 80 (2006) 11579-11588
6. Friebe P., Boudet J., Simorre J.P., and Bartenschlager R. Kissing-loop interaction in the 3′ end of the hepatitis C virus genome essential for RNA replication. J. Virol. 79 (2005) 380-392
7. Diviney S., Tuplin A., Struthers M., Armstrong V., Elliott R.M., Simmonds P., and Evans D.J. A hepatitis C virus cis-acting replication element forms a long-range RNA-RNA interaction with upstream RNA sequences in NS5B. J. Virol. 82 (2008) 9008-9022
8. Yu K.L., Jang S.I., and You J.C. Identification of in vivo interaction between hepatitis C virus core protein and 5′ and 3′ UTR RNA. Virus Res. 145 (2009) 285-292
9. Lai C.K., Jeng K.S., Machida K., and Lai M.M. Association of hepatitis C virus replication complexes with microtubules and actin filaments is dependent on the interaction of NS3 and NS5A. J. Virol. 82 (2008) 8838-8848
10. Wolk B., Buchele B., Moradpour D., and Rice C.M. A dynamic view of hepatitis C virus replication complexes. J. Virol. 82 (2008) 10519-10531
11. Targett-Adams P., Boulant S., and McLauchlan J. Visualization of double-stranded RNA in cells supporting hepatitis C virus RNA replication. J. Virol. 82 (2008) 2182-2195
12. Elazar M., Liu P., Rice C.M., and Glenn J.S. An N-terminal amphipathic helix in hepatitis C virus (HCV) NS4B mediates membrane association, correct localization of replication complex proteins, and HCV RNA replication. J. Virol. 78 (2004) 11393-11400
13. Gastaminza P., Cheng G., Wieland S., Zhong J., Liao W., and Chisari F.V. Cellular determinants of hepatitis C virus assembly, maturation, degradation, and secretion. J. Virol. 82 (2008) 2120-2129
14. Hijikata M., Kato N., Ootsuyama Y., Nakagawa M., and Shimotohno K. Gene mapping of the putative structural region of the hepatitis C virus genome by in vitro processing analysis. Proc. Natl. Acad. Sci. U.S.A 88 (1991) 5547-5551
15. Miyanari Y., Atsuzawa K., Usuda N., Watashi K., Hishiki T., Zayas M., Bartenschlager R., Wakita T., Hijikata M., and Shimotohno K. The lipid droplet is an important organelle for hepatitis C virus production. Nat. Cell. Biol. 9 (2007) 1089-1097
16. Nakai K., Okamoto T., Kimura-Someya T., Ishii K., Lim C.K., Tani H., Matsuo E., Abe T., Mori Y., Suzuki T., Miyamura T., Nunberg J.H., Moriishi K., and Matsuura Y. Oligomerization of hepatitis C virus core protein is crucial for interaction with the cytoplasmic domain of E1 envelope protein. J. Virol. 80 (2006) 11265-11273
17. Murray C.L., Jones C.T., Tassello J., and Rice C.M. Alanine scanning of the hepatitis C virus core protein reveals numerous residues essential for production of infectious virus. J. Virol. 81 (2007) 10220-10231
18. Deleersnyder V., Pillez A., Wychowski C., Blight K., Xu J., Hahn Y.S., Rice C.M., and Dubuisson J. Formation of native hepatitis C virus glycoprotein complexes. J. Virol. 71 (1997) 697-704
19. Op De Beeck A., Voisset C., Bartosch B., Ciczora Y., Cocquerel L., Keck Z., Foung S., Cosset F.L., and Dubuisson J. Characterization of functional hepatitis C virus envelope glycoproteins. J. Virol. 78 (2004) 2994-3002
20. Brohm C., Steinmann E., Friesland M., Lorenz I.C., Patel A., Penin F., Bartenschlager R., and Pietschmann T. Characterization of determinants important for hepatitis C virus p7 function in morphogenesis using trans-complementation. J. Virol. (2009)
21. Schregel V., Jacobi S., Penin F., and Tautz N. Hepatitis C virus NS2 is a protease stimulated by cofactor domains in NS3. Proc. Natl. Acad. Sci. U.S.A 106 (2009) 5342-5347
22. Yi M., Ma Y., Yates J., and Lemon S.M. Trans-complementation of an NS2 defect in a late step in hepatitis C virus (HCV) particle assembly and maturation. PLoS Pathog. 5 (2009) e1000403
23. Steinkuhler C., Urbani A., Tomei L., Biasiol G., Sardana M., Bianchi E., Pessi A., and De Francesco R. Activity of purified hepatitis C virus protease NS3 on peptide substrates. J. Virol. 70 (1996) 6694-6700
24. Wolk B., Sansonno D., Krausslich H.G., Dammacco F., Rice C.M., Blum H.E., and Moradpour D. Subcellular localization, stability, and trans-cleavage competence of the hepatitis C virus NS3-NS4A complex expressed in tetracycline-regulated cell lines. J. Virol. 74 (2000) 2293-2304
25. Beran R.K., Lindenbach B.D., and Pyle A.M. The NS4A protein of hepatitis C virus promotes RNA-coupled ATP hydrolysis by the NS3 helicase. J. Virol. 83 (2009) 3268-3275
26. Mercer D.F., Schiller D.E., Elliott J.F., Douglas D.N., Hao C., Rinfret A., Addison W.R., Fischer K.P., Churchill T.A., Lakey J.R., Tyrrell D.L., and Kneteman N.M. Hepatitis C virus replication in mice with chimeric human livers. Nat. Med. 7 (2001) 927-933
27. Gondeau C., Pichard-Garcia L., and Maurel P. Cellular models for the screening and development of anti-hepatitis C virus agents. Pharmacol. Ther. 124 (2009) 1-22
28. Wakita T., Pietschmann T., Kato T., Date T., Miyamoto M., Zhao Z., Murthy K., Habermann A., Krausslich H.G., Mizokami M., Bartenschlager R., and Liang T.J. Production of infectious hepatitis C virus in tissue culture from a cloned viral genome. Nat. Med. 11 (2005) 791-796
29. 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., and Rice C.M. Complete replication of hepatitis C virus in cell culture. Science 309 (2005) 623-626
30. Bradley D., McCaustland K., Krawczynski K., Spelbring J., Humphrey C., and Cook E.H. Hepatitis C virus: buoyant density of the factor VIII-derived isolate in sucrose. J. Med. Virol. 34 (1991) 206-208
31. Andre P., Komurian-Pradel F., Deforges S., Perret M., Berland J.L., Sodoyer M., Pol S., Brechot C., Paranhos-Baccala G., and Lotteau V. Characterization of low- and very-low-density hepatitis C virus RNA-containing particles. J. Virol. 76 (2002) 6919-6928
32. Owen D.M., Huang H., Ye J., and Gale Jr. M. Apolipoprotein E on hepatitis C virion facilitates infection through interaction with low-density lipoprotein receptor. Virology (2009)
33. Germi R., Crance J.M., Garin D., Guimet J., Lortat-Jacob H., Ruigrok R.W., Zarski J.P., and Drouet E. Cellular glycosaminoglycans and low density lipoprotein receptor are involved in hepatitis C virus adsorption. J. Med. Virol. 68 (2002) 206-215
34. Meuleman P., Hesselgesser J., Paulson M., Vanwolleghem T., Desombere I., Reiser H., and Leroux-Roels G. Anti-CD81 antibodies can prevent a hepatitis C virus infection in vivo. Hepatology 48 (2008) 1761-1768
35. Scarselli E., Ansuini H., Cerino R., Roccasecca R.M., Acali S., Filocamo G., Traboni C., Nicosia A., Cortese R., and Vitelli A. The human scavenger receptor class B type I is a novel candidate receptor for the hepatitis C virus. Embo. J. 21 (2002) 5017-5025
36. Cormier E.G., Tsamis F., Kajumo F., Durso R.J., Gardner J.P., and Dragic T. CD81 is an entry coreceptor for hepatitis C virus. Proc. Natl. Acad. Sci. U.S.A. 101 (2004) 7270-7274
37. Evans M.J., von Hahn T., Tscherne D.M., Syder A.J., Panis M., Wolk B., Hatziioannou T., McKeating J.A., Bieniasz P.D., and Rice C.M. Claudin-1 is a hepatitis C virus co-receptor required for a late step in entry. Nature 446 (2007) 801-805
38. Ploss A., Evans M.J., Gaysinskaya V.A., Panis M., You H., de Jong Y.P., and Rice C.M. Human occludin is a hepatitis C virus entry factor required for infection of mouse cells. Nature 457 (2009) 882-886
39. Brazzoli M., Bianchi A., Filippini S., Weiner A., Zhu Q., Pizza M., and Crotta S. CD81 is a central regulator of cellular events required for hepatitis C virus infection of human hepatocytes. J. Virol. 82 (2008) 8316-8329
40. Blanchard E., Belouzard S., Goueslain L., Wakita T., Dubuisson J., Wychowski C., and Rouille Y. Hepatitis C virus entry depends on clathrin-mediated endocytosis. J. Virol. 80 (2006) 6964-6972
41. Timpe J.M., Stamataki Z., Jennings A., Hu K., Farquhar M.J., Harris H.J., Schwarz A., Desombere I., Roels G.L., Balfe P., and McKeating J.A. Hepatitis C virus cell-cell transmission in hepatoma cells in the presence of neutralizing antibodies. Hepatology 47 (2008) 17-24
42. Schwarz A.K., Grove J., Hu K., Mee C.J., Balfe P., and McKeating J.A. Hepatoma cell density promotes claudin-1 and scavenger receptor BI expression and hepatitis C virus internalization. J. Virol. 83 (2009) 12407-12414
43. Lavillette D., Pecheur E.I., Donot P., Fresquet J., Molle J., Corbau R., Dreux M., Penin F., and Cosset F.L. Characterization of fusion determinants points to the involvement of three discrete regions of both E1 and E2 glycoproteins in the membrane fusion process of hepatitis C virus. J. Virol. 81 (2007) 8752-8765
44. Haid S., Pietschmann T., and Pecheur E.I. Low pH-dependent hepatitis C virus membrane fusion depends on E2 integrity, target lipid composition, and density of virus particles. J. Biol. Chem. 284 (2009) 17657-17667
45. Berger K.L., Cooper J.D., Heaton N.S., Yoon R., Oakland T.E., Jordan T.X., Mateu G., Grakoui A., and Randall G. Roles for endocytic trafficking and phosphatidylinositol 4-kinase III alpha in hepatitis C virus replication. Proc. Natl. Acad. Sci. U.S.A 106 (2009) 7577-7582
46. Li Q., Brass A.L., Ng A., Hu Z., Xavier R.J., Liang T.J., and Elledge S.J. A genome-wide genetic screen for host factors required for hepatitis C virus propagation. Proc. Natl. Acad. Sci. U.S.A 106 (2009) 16410-16415
47. Stone M., Jia S., Heo W.D., Meyer T., and Konan K.V. Participation of rab5, an early endosome protein, in hepatitis C virus RNA replication machinery. J. Virol. 81 (2007) 4551-4563
48. Aligo J., Jia S., Manna D., and Konan K.V. Formation and function of hepatitis C virus replication complexes require residues in the carboxy-terminal domain of NS4B protein. Virology 393 (2009) 68-83
49. Sklan E.H., Serrano R.L., Einav S., Pfeffer S.R., Lambright D.G., and Glenn J.S. TBC1D20 is a Rab1 GTPase-activating protein that mediates hepatitis C virus replication. J. Biol. Chem. 282 (2007) 36354-36361
50. Hamamoto I., Nishimura Y., Okamoto T., Aizaki H., Liu M., Mori Y., Abe T., Suzuki T., Lai M.M., Miyamura T., Moriishi K., and Matsuura Y. Human VAP-B is involved in hepatitis C virus replication through interaction with NS5A and NS5B. J. Virol. 79 (2005) 13473-13482
51. Kukihara H., Moriishi K., Taguwa S., Tani H., Abe T., Mori Y., Suzuki T., Fukuhara T., Taketomi A., Maehara Y., and Matsuura Y. Human VAP-C negatively regulates hepatitis C virus propagation. J. Virol. 83 (2009) 7959-7969
52. Prosser D.C., Tran D., Gougeon P.Y., Verly C., and Ngsee J.K. FFAT rescues VAPA-mediated inhibition of ER-to-Golgi transport and VAPB-mediated ER aggregation. J. Cell. Sci. 121 (2008) 3052-3061
53. Farhan H., Weiss M., Tani K., Kaufman R.J., and Hauri H.P. Adaptation of endoplasmic reticulum exit sites to acute and chronic increases in cargo load. Embo. J. 27 (2008) 2043-2054
54. Piodi A., Chouteau P., Lerat H., Hezode C., and Pawlotsky J.M. Morphological changes in intracellular lipid droplets induced by different hepatitis C virus genotype core sequences and relationship with steatosis. Hepatology 48 (2008) 16-27
55. Olofsson S.O., Bostrom P., Andersson L., Rutberg M., Perman J., and Boren J. Lipid droplets as dynamic organelles connecting storage and efflux of lipids. Biochim. Biophys. Acta 1791 (2009) 448-458
56. Yao H., and Ye J. Long chain acyl-CoA synthetase 3-mediated phosphatidylcholine synthesis is required for assembly of very low density lipoproteins in human hepatoma Huh7 cells. J. Biol. Chem. 283 (2008) 849-854
57. Gale Jr. M., and Foy E.M. Evasion of intracellular host defence by hepatitis C virus. Nature 436 (2005) 939-945
58. Bigger C.B., Brasky K.M., and Lanford R.E. DNA microarray analysis of chimpanzee liver during acute resolving hepatitis C virus infection. J. Virol. 75 (2001) 7059-7066
59. Walters K.A., Joyce M.A., Thompson J.C., Smith M.W., Yeh M.M., Proll S., Zhu L.F., Gao T.J., Kneteman N.M., Tyrrell D.L., and Katze M.G. Host-specific response to HCV infection in the chimeric SCID-beige/Alb-uPA mouse model: role of the innate antiviral immune response. PLoS Pathog. 2 (2006) e59
60. Meylan E., Curran J., Hofmann K., Moradpour D., Binder M., Bartenschlager R., and Tschopp J. Cardif is an adaptor protein in the RIG-I antiviral pathway and is targeted by hepatitis C virus. Nature 437 (2005) 1167-1172
61. Lin W., Kim S.S., Yeung E., Kamegaya Y., Blackard J.T., Kim K.A., Holtzman M.J., and Chung R.T. Hepatitis C virus core protein blocks interferon signaling by interaction with the STAT1 SH2 domain. J. Virol. 80 (2006) 9226-9235
62. Loo Y.M., Owen D.M., Li K., Erickson A.K., Johnson C.L., Fish P.M., Carney D.S., Wang T., Ishida H., Yoneyama M., Fujita T., Saito T., Lee W.M., Hagedorn C.H., Lau D.T., Weinman S.A., Lemon S.M., and Gale Jr. M. Viral and therapeutic control of IFN-beta promoter stimulator 1 during hepatitis C virus infection. Proc. Natl. Acad. Sci. U.S.A 103 (2006) 6001-6006
63. Joyce M.A., Walters K.A., Lamb S.E., Yeh M.M., Zhu L.F., Kneteman N., Doyle J.S., Katze M.G., and Tyrrell D.L. HCV induces oxidative and ER stress, and sensitizes infected cells to apoptosis in SCID/Alb-uPA mice. PLoS Pathog. 5 (2009) e1000291
64. Nelson D.R. The immunopathogenesis of hepatitis C virus infection. Clin. Liver Dis. 5 (2001) 931-953
65. Walters K.A., Syder A.J., Lederer S.L., Diamond D.L., Paeper B., Rice C.M., and Katze M.G. Genomic analysis reveals a potential role for cell cycle perturbation in HCV-mediated apoptosis of cultured hepatocytes. PLoS Pathog. 5 (2009) e1000269
66. de Chassey B., Navratil V., Tafforeau L., Hiet M.S., Aublin-Gex A., Agaugue S., Meiffren G., Pradezynski F., Faria B.F., Chantier T., Le Breton M., Pellet J., Davoust N., Mangeot P.E., Chaboud A., Penin F., Jacob Y., Vidalain P.O., Vidal M., Andre P., Rabourdin-Combe C., and Lotteau V. Hepatitis C virus infection protein network. Mol. Syst. Biol. 4 (2008) 230
67. Wang D., Long J., Dai F., Liang M., Feng X.H., and Lin X. BCL6 represses Smad signaling in transforming growth factor-beta resistance. Cancer Res. 68 (2008) 783-789
68. Reilly S.M., and Lee C.H. PPAR delta as a therapeutic target in metabolic disease. FEBS Lett. 582 (2008) 26-31
69. Arbouzova N.I., Bach E.A., and Zeidler M.P. Ken & barbie selectively regulates the expression of a subset of Jak/STAT pathway target genes. Curr. Biol. 16 (2006) 80-88
70. Godoy P., Hengstler J.G., Ilkavets I., Meyer C., Bachmann A., Muller A., Tuschl G., Mueller S.O., and Dooley S. Extracellular matrix modulates sensitivity of hepatocytes to fibroblastoid dedifferentiation and transforming growth factor beta-induced apoptosis. Hepatology 49 (2009) 2031-2043