Molecular determinants and dynamics of hepatitis C virus secretion

PLoS Pathogens

Volumn 8, Issue 1, 2012, Pages

  Coller, Kelly E ^a   Heaton, Nicholas S ^a   Berger, Kristi L ^a   Cooper, Jacob D ^a   Saunders, Jessica L ^a   Randall, Glenn ^a  

^a UNIVERSITY OF CHICAGO   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

APOLIPOPROTEIN E; CORE PROTEIN; MONTIRELIN; NOCODAZOLE; NONSTRUCTURAL PROTEIN 2; PROTEIN KINASE; SYNAPTOBREVIN 1;

ARTICLE; ENDOPLASMIC RETICULUM; ENDOSOME; GOLGI COMPLEX; HEPATITIS C VIRUS; MICROTUBULE; NONHUMAN; RNA INTERFERENCE; TRANS GOLGI NETWORK; VIRUS CAPSID; VIRUS CORE;

APOLIPOPROTEINS E; BIOLOGICAL TRANSPORT, ACTIVE; CELL LINE; ENDOPLASMIC RETICULUM; GOLGI APPARATUS; HEPACIVIRUS; HUMANS; SECRETORY VESICLES; VESICLE-ASSOCIATED MEMBRANE PROTEIN 1; VIRUS ASSEMBLY; VIRUS RELEASE;

HEPATITIS C VIRUS;

EID: 84857469995     PISSN: 15537366     EISSN: 15537374     Source Type: Journal    
DOI: 10.1371/journal.ppat.1002466     Document Type: Article

References (93)

1. 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.
2. Lindenbach BD, Meuleman P, Ploss A, Vanwolleghem T, Syder AJ, et al. (2006) Cell culture-grown hepatitis C virus is infectious in vivo and can be recultured in vitro. Proc Natl Acad Sci U S A 103: 3805-3809.
3. 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. Nat Med 11: 791-796.
4. Zhong J, Gastaminza P, Cheng G, Kapadia S, Kato T, et al. (2005) Robust hepatitis C virus infection in vitro. Proc Natl Acad Sci U S A 102: 9294-9299.
5. Bartosch B, Dubuisson J, Cosset FL, (2003) Infectious hepatitis C virus pseudo-particles containing functional E1-E2 envelope protein complexes. J Exp Med 197: 633-642.
6. 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.
7. 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.
8. Bartosch B, Vitelli A, Granier C, Goujon C, Dubuisson J, et al. (2003) Cell entry of hepatitis C virus requires a set of co-receptors that include the CD81 tetraspanin and the SR-B1 scavenger receptor. J Biol Chem 278: 41624-41630.
9. Blanchard E, Belouzard S, Goueslain L, Wakita T, Dubuisson J, et al. (2006) Hepatitis C virus entry depends on clathrin-mediated endocytosis. J Virol 80: 6964-6972.
10. Codran A, Royer C, Jaeck D, Bastien-Valle M, Baumert TF, et al. (2006) Entry of hepatitis C virus pseudotypes into primary human hepatocytes by clathrin-dependent endocytosis. J Gen Virol 87: 2583-2593.
11. 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. J Virol 80: 11571-11578.
12. 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. J Virol 76: 5974-5984.
13. 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.
14. Rouille Y, Helle F, Delgrange D, Roingeard P, Voisset C, et al. (2006) Subcellular localization of hepatitis C virus structural proteins in a cell culture system that efficiently replicates the virus. J Virol 80: 2832-2841.
15. Boulant S, Targett-Adams P, McLauchlan J, (2007) Disrupting the association of hepatitis C virus core protein with lipid droplets correlates with a loss in production of infectious virus. J Gen Virol 88: 2204-2213.
16. Shi ST, Polyak SJ, Tu H, Taylor DR, Gretch DR, et al. (2002) Hepatitis C virus NS5A colocalizes with the core protein on lipid droplets and interacts with apolipoproteins. Virology 292: 198-210.
17. Barba G, Harper F, Harada T, Kohara M, Goulinet S, et al. (1997) Hepatitis C virus core protein shows a cytoplasmic localization and associates to cellular lipid storage droplets. Proc Natl Acad Sci U S A 94: 1200-1205.
18. Moradpour D, Englert C, Wakita T, Wands JR, (1996) Characterization of cell lines allowing tightly regulated expression of hepatitis C virus core protein. Virology 222: 51-63.
19. Ma Y, Yates J, Liang Y, Lemon SM, Yi M, (2008) NS3 helicase domains involved in infectious intracellular hepatitis C virus particle assembly. J Virol 82: 7624-7639.
20. Steinmann E, Penin F, Kallis S, Patel AH, Bartenschlager R, et al. (2007) Hepatitis C virus p7 protein is crucial for assembly and release of infectious virions. PLoS Pathog 3: e103.
21. Jones CT, Murray CL, Eastman DK, Tassello J, Rice CM, (2007) Hepatitis C virus p7 and NS2 proteins are essential for production of infectious virus. J Virol 81: 8374-8383.
22. Stapleford KA, Lindenbach BD, (2011) Hepatitis C virus NS2 coordinates virus particle assembly through physical interactions with the E1-E2 glycoprotein and NS3-NS4A enzyme complexes. J Virol 85: 1706-1717.
23. Jirasko V, Montserret R, Lee JY, Gouttenoire J, Moradpour D, et al. (2010) Structural and functional studies of nonstructural protein 2 of the hepatitis C virus reveal its key role as organizer of virion assembly. PLoS Pathog 6: e1001233.
24. Masaki T, Suzuki R, Murakami K, Aizaki H, Ishii K, et al. (2008) Interaction of hepatitis C virus nonstructural protein 5A with core protein is critical for the production of infectious virus particles. J Virol 82: 7964-76.
25. Tellinghuisen TL, Foss KL, Treadaway J, (2008) Regulation of hepatitis C virion production via phosphorylation of the NS5A protein. PLoS Pathog 4: e1000032.
26. Appel N, Zayas M, Miller S, Krijnse-Locker J, Schaller T, et al. (2008) Essential role of domain III of nonstructural protein 5A for hepatitis C virus infectious particle assembly. PLoS Pathog 4: e1000035.
27. Hughes M, Griffin S, Harris M, (2009) Domain III of NS5A contributes to both RNA replication and assembly of hepatitis C virus particles. J Gen Virol 90: 1329-1334.
28. Bartenschlager RPF, Lohmann V, André P, (2011) Assembly of infectious hepatitis C virus particles. Trends Microbiol 19: 95-103.
29. Miyanari Y, Atsuzawa K, Usuda N, Watashi K, Hishiki T, et al. (2007) The lipid droplet is an important organelle for hepatitis C virus production. Nat Cell Biol 9: 1089-1097.
30. Lindenbach BD TH-J, Rice CM, (2007) Flaviviruses: the viruses and their replication; In: Knipe DMHP, editors. Philadelphia, Lippincott Williams and Wilkins pp. 1101-1152.
31. Mackenzie JM, Westaway EG, (2001) Assembly and maturation of the flavivirus Kunjin virus appear to occur in the rough endoplasmic reticulum and along the secretory pathway, respectively. J Virol 75: 10787-10799.
32. Chang KS, Jiang J, Cai Z, Luo G, (2007) Human apolipoprotein e is required for infectivity and production of hepatitis C virus in cell culture. J Virol 81: 13783-13793.
33. Jiang J, Luo G, (2009) Apolipoprotein E but not B is required for the formation of infectious hepatitis C virus particles. J Virol 83: 12680-12691.
34. Merz A, Long G, Hiet MS, Brugger B, Chlanda P, et al. (2011) Biochemical and morphological properties of hepatitis C virus particles and determination of their lipidome. J Biol Chem 286: 3018-3032.
35. Gastaminza P, Cheng G, Wieland S, Zhong J, Liao W, et al. (2008) Cellular determinants of hepatitis C virus assembly, maturation, degradation, and secretion. J Virol 82: 2120-2129.
36. 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. Proc Natl Acad Sci U S A 104: 5848-5853.
37. Icard V, Diaz O, Scholtes C, Perrin-Cocon L, Ramiere C, et al. (2009) Secretion of hepatitis C virus envelope glycoproteins depends on assembly of apolipoprotein B positive lipoproteins. PLoS ONE 4: e4233.
38. Diaz O, Delers F, Maynard M, Demignot S, Zoulim F, et al. (2006) Preferential association of Hepatitis C virus with apolipoprotein B48-containing lipoproteins. J Gen Virol 87: 2983-2991.
39. Andre P, Komurian-Pradel F, Deforges S, Perret M, Berland JL, et al. (2002) Characterization of low- and very-low-density hepatitis C virus RNA-containing particles. J Virol 76: 6919-6928.
40. Gastaminza P, Dryden KA, Boyd B, Wood MR, Law M, et al. (2010) Ultrastructural and biophysical characterization of hepatitis C virus particles produced in cell culture. J Virol 84: 10999-11009.
41. 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.
42. Mancone C, Steindler C, Santangelo L, Simonte G, Vlassi C, et al. (2011) Hepatitis C virus production requires apolipoprotein A-I and affects its association with nascent low-density lipoproteins. Gut 60: 378-386.
43. Coller KE, Berger KL, Heaton NS, Cooper JD, Yoon R, et al. (2009) RNA interference and single particle tracking analysis of hepatitis C virus endocytosis. PLoS Pathog 5: e1000702.
44. 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. Proc Natl Acad Sci U S A 106: 7577-7582.
45. Arhel N, Genovesio A, Kim KA, Miko S, Perret E, et al. (2006) Quantitative four-dimensional tracking of cytoplasmic and nuclear HIV-1 complexes. Nat Methods 3: 817-824.
46. Gousset K, Ablan SD, Coren LV, Ono A, Soheilian F, et al. (2008) Real-time visualization of HIV-1 GAG trafficking in infected macrophages. PLoS Pathog 4: e1000015.
47. Turville SG, Aravantinou M, Stossel H, Romani N, Robbiani M, (2008) Resolution of de novo HIV production and trafficking in immature dendritic cells. Nat Methods 5: 75-85.
48. Mire CE DD, Delos SE, White JM, Whitt MA, (2009) Glycoprotein-dependent acidification of vesicular stomatitis virus enhances release of matrix protein. J Virol 83: 12139-12150.
49. Das SC PD, Nayak D, Pattnaik AK, (2009) Biarsenical labeling of vesicular stomatitis virus encoding tetracysteine-tagged m protein allows dynamic imaging of m protein and virus uncoating in infected cells. J Virol 83: 2611-2622.
50. Hadlock KG, Lanford RE, Perkins S, Rowe J, Yang Q, et al. (2000) Human monoclonal antibodies that inhibit binding of hepatitis C virus E2 protein to CD81 and recognize conserved conformational epitopes. J Virol 74: 10407-10416.
51. Popescu CI, Callens N, Trinel D, Roingeard P, Moradpour D, et al. (2011) NS2 Protein of Hepatitis C Virus Interacts with Structural and Non-Structural Proteins towards Virus Assembly. PLoS Pathog 7: e1001278.
52. 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.
53. Wacker I, Kaether C, Kromer A, Migala A, Almers W, et al. (1997) Microtubule-dependent transport of secretory vesicles visualized in real time with a GFP-tagged secretory protein. J Cell Sci 110 (Pt 13): 1453-1463.
54. Welte MA, (2004) Bidirectional transport along microtubules. Curr Biol 14: R525-537.
55. Boulant S, Douglas MW, Moody L, Budkowska A, Targett-Adams P, et al. (2008) Hepatitis C Virus Core Protein Induces Lipid Droplet Redistribution in a Microtubule- and Dynein-Dependent Manner. Traffic 9: 1268-1282.
56. Knight ZA, Gonzalez B, Feldman ME, Zunder ER, Goldenberg DD, et al. (2006) A pharmacological map of the PI3-K family defines a role for p110alpha in insulin signaling. Cell 125: 733-747.
57. Toth B, Balla A, Ma H, Knight ZA, Shokat KM, et al. (2006) Phosphatidylinositol 4-kinase IIIbeta regulates the transport of ceramide between the endoplasmic reticulum and Golgi. J Biol Chem 281: 36369-36377.
58. Mensenkamp AR, Jong MC, van Goor H, van Luyn MJ, Bloks V, et al. (1999) Apolipoprotein E participates in the regulation of very low density lipoprotein-triglyceride secretion by the liver. J Biol Chem 274: 35711-35718.
59. 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.
60. Nielsen SU, Bassendine MF, Burt AD, Martin C, Pumeechockchai W, et al. (2006) Association between hepatitis C virus and very-low-density lipoprotein (VLDL)/LDL analyzed in iodixanol density gradients. J Virol 80: 2418-2428.
61. Hishiki T, Shimizu Y, Tobita R, Sugiyama K, Ogawa K, et al. (2010) Infectivity of hepatitis C virus is influenced by association with apolipoprotein E isoforms. J Virol 84: 12048-12057.
62. Owen DM, Huang H, Ye J, Gale M Jr, (2009) Apolipoprotein E on hepatitis C virion facilitates infection through interaction with low-density lipoprotein receptor. Virology 394: 99-108.
63. Cun W JJ, 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. J Virol 84: 11532-11541.
64. Fazio S, Linton MF, Hasty AH, Swift LL, (1999) Recycling of apolipoprotein E in mouse liver. J Biol Chem 274: 8247-8253.
65. Fazio S, Linton MF, Swift LL, (2000) The cell biology and physiologic relevance of ApoE recycling. Trends Cardiovasc Med 10: 23-30.
66. Hamilton RL, Wong JS, Guo LS, Krisans S, Havel RJ, (1990) Apolipoprotein E localization in rat hepatocytes by immunogold labeling of cryothin sections. J Lipid Res 31: 1589-1603.
67. Gusarova V SJ, Sullivan ML, Watkins SC, Brodsky JL, Fisher EA, (2007) Golgi-associated maturation of very low density lipoproteins involves conformational changes in apolipoprotein B, but is not dependent on apolipoprotein E. J Biochem 282: 19453-19462.
68. Ullrich O RS, Urbé S, Zerial M, Parton RG, (1996) Rab11 regulates recycling through the pericentriolar recycling endosome. J Cell Biol 135: 913-924.
69. Casanova JE, Wang X, Kumar R, Bhartur SG, Navarre J, et al. (1999) Association of Rab25 and Rab11a with the apical recycling system of polarized Madin-Darby canine kidney cells. Mol Biol Cell 10: 47-61.
70. Chen W FY, Chen D, Wandinger-Ness A, (1998) Rab11 is required for trans-golgi network-to-plasma membrane transport and a preferential target for GDP dissociation inhibitor. Mol Biol Cell 9: 3241-3257.
71. Bruce EA, Digard P, Stuart AD, (2010) The Rab11 pathway is required for influenza A virus budding and filament formation. J Virol 84: 5848-5859.
72. Rowe RK, Suszko JW, Pekosz A, (2008) Roles for the recycling endosome, Rab8, and Rab11 in hantavirus release from epithelial cells. Virology 382: 239-249.
73. Chambers R, Takimoto T, (2010) Trafficking of Sendai virus nucleocapsids is mediated by intracellular vesicles. PLoS One 5: e10994.
74. Söllner T BM, Whiteheart SW, Scheller RH, Rothman JE, (1993) A protein assembly-disassembly pathway in vitro that may correspond to sequential steps of synaptic vesicle docking, activation, and fusion. Cell 75: 409-418.
75. Murray CL, Jones CT, Rice CM, (2008) Architects of assembly: roles of Flaviviridae non-structural proteins in virion morphogenesis. Nat Rev Microbiol 6: 699-708.
76. Ma Y, Anantpadma M, Timpe JM, Shanmugam S, Singh SM, et al. (2011) Hepatitis C virus NS2 protein serves as a scaffold for virus assembly by interacting with both structural and nonstructural proteins. J Virol 85: 86-97.
77. Bamberger MJLM, (1990) Possible role of the Golgi apparatus in the assembly of very low density lipoprotein. Proc Natl Acad Sci U S A 87: 2390-2394.
78. Tran K T-TG, DeLong CJ, Cui Z, Shan J, Burton L, Jamieson JC, Yao Z, (2002) Intracellular assembly of very low density lipoproteins containing apolipoprotein B100 in rat hepatoma McA-RH7777 cells. J Biol Chem 277: 31187-31200.
79. Bonifacino JS L-SJ, (2003) Coat proteins: shaping membrane transport. Nat Rev Mol Cell Biol 4: 409-414.
80. Amako Y SG, Siddiqui A, (2011) Protein kinase D negatively regulates hepatitis C virus maturation through phosphorylation of oxysterol binding protein and ceramide transfer protein. J Biol Chem doi:10.1074/jbc.M110.182097.
81. Borawski J TP, Puyang X, Gibaja V, Zhao S, Mickanin C, et al. (2009) Class III phosphatidylinositol 4-kinase alpha and beta are novel host factor regulators of hepatitis C virus replication. J Virol 83: 10058-10074.
82. 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 J 23: 3780-3789.
83. Folsch H, (2005) The building blocks for basolateral vesicles in polarized epithelial cells. Trends Cell Biol 15: 222-228.
84. Li Q BA, Ng A, Hu Z, Xavier RJ, Liang TJ, Elledge SJ, (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.
85. Lai CK, Jeng KS, Machida K, Lai MM, (2010) Hepatitis C virus egress and release depend on endosomal trafficking of core protein. J Virol 84: 11590-11598.
86. Egea G, Lazaro-Dieguez F, Vilella M, (2006) Actin dynamics at the Golgi complex in mammalian cells. Curr Opin Cell Biol 18: 168-178.
87. Smith GA, Enquist LW, (2002) Break ins and break outs: viral interactions with the cytoskeleton of Mammalian cells. Annu Rev Cell Dev Biol 18: 135-161.
88. Boson B, Granio O, Bartenschlager R, Cosset FL, (2011) A concerted action of hepatitis C virus p7 and nonstructural protein 2 regulates core localization at the endoplasmic reticulum and virus assembly. PLoS Pathog 7: e1002144.
89. 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.
90. Witteveldt J, Evans MJ, Bitzegeio J, Koutsoudakis G, Owsianka AM, et al. (2009) CD81 is dispensable for hepatitis C virus cell-to-cell transmission in hepatoma cells. J Gen Virol 90: 48-58.
91. Mateu G, Donis RO, Wakita T, Bukh J, Grakoui A, (2008) Intragenotypic JFH1 based recombinant hepatitis C virus produces high levels of infectious particles but causes increased cell death. Virology 376: 397-407.
92. Martin BR GB, Adams SR, Tsien RY, (2005) Mammalian cell-based optimization of the biarsenical-binding tetracysteine motif for improved fluorescence and affinity. Nat Biotechnol 23: 1308-1314.
93. Randall G, Chen L, Panis M, Fischer AK, Lindenbach BD, et al. (2006) Silencing of USP18 potentiates the antiviral activity of interferon against hepatitis C virus infection. Gastroenterology 131: 1584-1591.