Roles of Lipoproteins and Apolipoproteins in Particle Formation of Hepatitis C Virus

Trends in Microbiology

Volumn 23, Issue 10, 2015, Pages 618-629

  Fukuhara, Takasuke ^a   Ono, Chikako ^a   Puig Basagoiti, Francesc ^a   Matsuura, Yoshiharu ^a  

^a OSAKA UNIVERSITY   (Japan)

Author keywords

Amphipathic helices; Exchangeable apolipoproteins; Hepato tropism; Lipoprotein

Indexed keywords

APOLIPOPROTEIN A; APOLIPOPROTEIN B; APOLIPOPROTEIN B100; APOLIPOPROTEIN C; APOLIPOPROTEIN E; HIGH DENSITY LIPOPROTEIN; LIPOPROTEIN; LOW DENSITY LIPOPROTEIN; VERY LOW DENSITY LIPOPROTEIN; APOLIPOPROTEIN;

ALPHA HELIX; HEPATITIS C; HEPATITIS C VIRUS; HUMAN; LIFE CYCLE; LIPID METABOLISM; LIPOVIROPARTICLE; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN INTERACTION; PROTEIN TRANSPORT; REVIEW; VIRAL TROPISM; VIRUS ASSEMBLY; VIRUS ENTRY; VIRUS ENVELOPE; VIRUS INFECTIVITY; VIRUS MORPHOGENESIS; VIRUS PARTICLE; VIRUS REPLICATION; CHEMISTRY; HEPACIVIRUS; METABOLISM; VIRION;

APOLIPOPROTEINS; HEPACIVIRUS; LIPOPROTEINS; VIRION; VIRUS ASSEMBLY;

EID: 84943599552     PISSN: 0966842X     EISSN: 18784380     Source Type: Journal    
DOI: 10.1016/j.tim.2015.07.007     Document Type: Review

References (99)

1. Ploss A., Evans M.J. Hepatitis C virus host cell entry. Curr. Opin. Virol. 2012, 2:14-19.
2. Fraser C.S., Doudna J.A. Structural and mechanistic insights into hepatitis C viral translation initiation. Nat. Rev. Microbiol. 2007, 5:29-38.
3. Moradpour D., et al. Replication of hepatitis C virus. Nat. Rev. Microbiol. 2007, 5:453-463.
4. Lohmann V., et al. Replication of subgenomic hepatitis C virus RNAs in a hepatoma cell line. Science 1999, 285:110-113.
5. Bartosch B., et al. Infectious hepatitis C virus pseudo-particles containing functional E1-E2 envelope protein complexes. J. Exp. Med. 2003, 197:633-642.
6. Tani H., et al. Replication-competent recombinant vesicular stomatitis virus encoding hepatitis C virus envelope proteins. J. Virol. 2007, 81:8601-8612.
7. Wakita T., et al. Production of infectious hepatitis C virus in tissue culture from a cloned viral genome. Nat. Med. 2005, 11:791-796.
8. Lindenbach B.D., et al. Complete replication of hepatitis C virus in cell culture. Science 2005, 309:623-626.
9. Pileri P., et al. Binding of hepatitis C virus to CD81. Science 1998, 282:938-941.
10. Scarselli E., et al. The human scavenger receptor class B type 1 is a novel candidate receptor for the hepatitis C virus. EMBO J. 2002, 21:5017-5025.
11. Agnello V., et al. Hepatitis C virus and other Flaviviridae viruses enter cells via low density lipoprotein receptor. Proc. Natl. Acad. Sci. U.S.A. 1999, 96:12766-12771.
12. Evans M.J., et al. Claudin-1 is a hepatitis C virus co-receptor required for a late step in entry. Nature 2007, 446:801-805.
13. Ploss A., et al. Human occludin is a hepatitis C virus entry factor required for infection of mouse cells. Nature 2009, 457:882-886.
14. Acton S., et al. Identification of scavenger receptor SR-B1 as a high density lipoprotein receptor. Science 1996, 271:518-520.
15. Yamamoto T., et al. The human LDL receptor: a cysteine-rich protein with multiple sequences in its mRNA. Cell 1984, 39:27-38.
16. Sainz B., et al. Identification of the Niemann-Pick C1-like 1 cholesterol absorption receptor as a new hepatitis C virus entry factor. Nat. Med. 2012, 18:281-285.
17. Miyanari Y., et al. The lipid droplet is an important organelle for hepatitis C virus production. Nat. Cell Biol. 2007, 9:961-969.
18. Herker E., et al. Efficient hepatitis C virus particle formation requires diacylglycerol acyltransferase-1. Nat. Med. 2010, 16:1295-1298.
19. Fukuhara T., Matsuura Y. Role of miR-122 and lipid metabolism in HCV infection. J. Gastroenterol. 2013, 48:169-176.
20. Huang H., et al. Hepatitis C virus production by human hepatocytes dependent on assembly and secretion of very low-density lipoproteins. Proc. Natl. Acad. Sci. U.S.A. 2007, 104:5848-5853.
21. Chang K.S., et al. Human apolipoprotein E is required for infectivity and production of hepatitis C virus in cell culture. J. Virol. 2007, 81:13783-13793.
22. Felmlee D.J., et al. Hepatitis C virus, cholesterol and lipoproteins - impact for the viral life cycle and pathogenesis of liver diseases. Viruses 2013, 5:1292-1324.
23. Thomssen R., et al. Association of hepatitis C virus in human sera with beta-lipoprotein. Med. Microbiol. Immunol. 1992, 181:293-300.
24. Andre P., et al. Characterization of low- and very-low-density hepatitis C virus RNA-containing particles. J. Virol. 2002, 76:6919-6928.
25. Gastaminza P., et al. Differential biophysical properties of infectious intracellular and secreted hepatitis C virus particles. J. Virol. 2006, 80:11074-11081.
26. Gastaminza P., et al. Ultrastructural and biophysical characterization of hepatitis C virus particles produced in cell culture. J. Virol. 2010, 84:10999-11009.
27. Merz A., et al. Biochemical and morphological properties of hepatitis C virus particles and determination of their lipidome. J. Biol. Chem. 2011, 286:3018-3032.
28. Felmlee D.J., et al. Intravascular transfer contributes to postprandial increase in numbers of very-low-density hepatitis C virus particles. Gastroenterology 2010, 139:1774-1783.
29. Shimizu Y., et al. Lipoprotein lipase and hepatic triglyceride lipase reduce the infectivity of hepatitis C virus (HCV) through their catalytic activities on HCV-associated lipoproteins. Virology 2010, 407:152-159.
30. Aizaki H., et al. Critical role of virion-associated cholesterol and sphingolipid in hepatitis C virus infection. J. Virol. 2008, 82:5715-5724.
31. Yamamoto M., et al. Structural requirements of virion-associated cholesterol for infectivity, buoyant density and apolipoprotein association of hepatitis C virus. J. Gen. Virol. 2011, 92:2082-2087.
32. Andreo U., et al. Lipoprotein lipase mediates hepatitis C virus (HCV) cell entry and inhibits HCV infection. Cell. Microbiol. 2007, 9:2445-2456.
33. Catanese M.T., et al. Ultrastructural analysis of hepatitis C virus particles. Proc. Natl. Acad. Sci. U.S.A. 2013, 110:9505-9510.
34. Diaz O., et al. Preferential association of hepatitis C virus with apolipoprotein B48-containing lipoproteins. J. Gen. Virol. 2006, 87:2983-2991.
35. Meunier J.C., et al. Apolipoprotein C1 association with hepatitis C virus. J. Virol. 2008, 82:9647-9656.
36. Fukuhara T., et al. Amphipathic α-helices in apolipoproteins are crucial to the formation of infectious hepatitis C virus particles. PLoS Pathog. 2014, 10:e1004534.
37. Dreux M., et al. The exchangeable apolipoprotein ApoC-1 promotes membrane fusion of hepatitis C virus. J. Biol. Chem. 2007, 282:32357-32369.
38. Zaidi N., et al. Lipogenesis and lipolysis: the pathways exploited by the cancer cells to acquire fatty acids. Prog. Lipid Res. 2013, 52:585-589.
39. Shimizu Y., et al. Lipoprotein component associated with hepatitis C virus is essential for virus infectivity. Curr. Opin. Virol. 2011, 1:19-26.
40. Maillard P., et al. Lipoprotein lipase inhibits hepatitis C virus (HCV) infection by blocking virus cell entry. PLoS ONE 2011, 6:e26637.
41. Owen D.M., et al. Apolipoprotein E on hepatitis C virion facilitates infection through interaction with low-density lipoprotein receptor. Virology 2009, 394:99-108.
42. Jiang J., et al. Hepatitis C virus attachment mediated by apolipoprotein E binding to cell surface heparan sulfate. J. Virol. 2012, 86:7256-7267.
43. Lefevre M., et al. Syndecan 4 is involved in mediating HCV entry through interaction with lipoviral particle-associated apolipoprotein E. PLoS ONE 2014, 9:e95550.
44. Bankwitz D., et al. Role of hypervariable region 1 for the interplay of hepatitis C virus with entry factors and lipoproteins. J. Virol. 2014, 88:12644-12655.
45. Prentoe J., et al. Hypervariable region 1 deletion and required adaptive envelope mutations confer decreased dependency on scavenger receptor class B type 1 and low-density lipoprotein receptor for hepatitis C virus. J. Virol. 2014, 88:1725-1739.
46. Barretto N., et al. Determining the involvement and therapeutic implications of host cellular factors in hepatitis C virus cell-to-cell spread. J. Virol. 2014, 88:5050-5061.
47. Hueging K., et al. Apolipoprotein E codetermines tissue tropism of hepatitis C virus and is cruicial for viral cell-to-cell transmission by contributing to a postenvelopment step of assembly. J. Virol. 2014, 88:1433-1446.
48. Gastaminza P., et al. Cellular determinants of hepatitis C virus assembly, maturation, degradation, and secretion. J. Virol. 2008, 82:2120-2129.
49. Jiang J., Luo G. Apolipoprotein E but not B is required for the formation of infectious hepatitis C virus particles. J. Virol. 2009, 83:12680-12691.
50. Steinmann E., Pietschmann T. Hepatitis C virus: from molecular virology to antiviral therapy. Cell culture systems for hepatitis C virus. Curr. Top. Microbiol. Immunol. 2013, 369:17-48.
51. Mancone C., et al. Hepatitis C virus production requires apolipoprotein A-1 and affects its association with nascent low-density lipoproteins. Gut 2011, 60:378-386.
52. Segrest J.P., et al. The amphipathic helix in the exchangeable apolipoproteins: a review of secondary structure and function. J. Lipid Res. 1992, 33:141-166.
53. Lindenbach B. Hepatitis C virus: from molecular virology to antiviral therapy. Virion assembly and release. Curr. Top. Microbiol. Immunol. 2013, 369:199-218.
54. Bartenschlager R., et al. Assembly of infectious hepatitis C virus particles. Trends Microbiol. 2011, 19:95-103.
55. Lee J., et al. Apolipoprotein E likely contributes to a maturation step of infectious hepatitis C virus particles and interacts with viral envelope glycoproteins. J. Virol. 2014, 88:12422-12437.
56. da Costa D., et al. Reconstitution of the entire hepatitis C virus life cycle in nonhepatic cells. J. Virol. 2012, 86:11919-11925.
57. Hussain M.M., et al. Microsomal triglyceride transfer protein and its role in apoB-lipoprotein assembly. J. Lipid Res. 2003, 44:22-32.
58. Jammart B., et al. Very-low-density lipoprotein (VLDL)-producing and hepatitis C virus-replicating HepG2 cells secrete no more lipoviroparticles than VLDL-deficient Huh7.5 cells. J. Virol. 2013, 87:5065-5080.
59. Icard V., et al. Secretion of hepatitis C virus envelope glycoproteins depends on assembly of apolipoprotein B positive lipoproteins. PLoS ONE 2009, 4:e4233.
60. Pecheur E.I., et al. Morphological characterization and fusion properties of triglyceride-rich lipoproteins obtained from cells transduced with hepatitis C virus glycoproteins. J. Biol. Chem. 2010, 285:25802-25811.
61. Segrest J.P., et al. ApoB-100 has a pentapartite structure composed of three amphipathic α-helical domains alternating with two amphipathic β-strand domains. Arterioscler. Thromb. 1994, 14:1674-1685.
62. Mei X., Atkinson D. Crystal structure of C-terminal truncated apolipoprotein A-1 reveals the assembly of high density lipoprotein (HDL) by dimerization. J. Biol. Chem. 2011, 286:38570-38582.
63. Rozek A., et al. Conformation of human apolipoprotein C-1 in a lipid-mimetic environment determined by CD and NMR spectroscopy. Biochemistry 1999, 38:14475-14484.
64. Chen J., et al. Topology of human apolipoprotein E3 uniquely regulates its diverse biological functions. Proc. Natl. Acad. Sci. U.S.A. 2011, 108:14813-14818.
65. Saito H., et al. Contribution of domain structure and lipid interaction to the functionality of exchangeable human apolipoproteins. Prog. Lipid Res. 2004, 43:350-380.
66. Boyer A., et al. The association of hepatitis C virus glycoproteins with apolipoproteins E and B early in assembly is conserved in lipoviral particles. J. Biol. Chem. 2014, 289:18904-18913.
67. Lee J.Y., et al. Apolipoprotein E likely contributes to a maturation step of infectious hepaititis C virus particles and interacts with viral envelope glycoproteins. J. Virol. 2014, 88:12422-12437.
68. Schaefer E.J., et al. Human chylomicron apolipoprotein metabolism. Biochem. Biophys. Res. Commun. 1978, 80:405-412.
69. Lin C., et al. Apolipoprotein J, a glucose-upregulated molecular chaperone, stabilizes core and NS5A to promote infectious hepatitis C virus virion production. J. Hepatol. 2014, 61:984-993.
70. Pan M., et al. The late addition of core lipids to nascent apolipoprotein B100, resulting in the assembly and secretion of triglyceride-rich lipoproteins, is independent of both microsomal triglyceride transfer protein activity and new triglyceride synthesis. J. Biol. Chem. 2002, 277:4413-4421.
71. Tiwari S., Siddiqi S.A. Intracellular traficking and secretion of very low density lipoproteins. Arterioscler. Thromb. Vasc. Biol. 2012, 32:1079-1086.
72. Tran K., et al. Intracellular assembly of very low density lipoproteins containing apolipoprotein B100 in rat hepatoma McA-RH7777 cells. J. Biol. Chem. 2002, 277:31187-31200.
73. Swift L.L. Role of the Golgi apparatus in the phosphorylation of apolipoprotein B. J. Biol. Chem. 1996, 271:31491-31495.
74. Sundaram M., Yao Z. Intrahepatic role of exchangeable apolipoproteins in lipoprotein assembly and secretion. Arterioscler. Thromb. Vasc. Biol. 2012, 32:1073-1078.
75. -/- mice is regulated by LPL activity and involves proteoglycans and SR-B1. J. Lipid Res. 2008, 49:1553-1561.
76. Coller K.E., et al. Molecular determinants and dynamics of hepatitis C virus secretion. PLoS Pathog. 2012, 8:e1002466.
77. Falkowska E., et al. Hepatitis C virus envelope glycoprotein E2 glycans modulate entry, CD81 binding and neutralization. J. Virol. 2007, 81:8072-8079.
78. Albecka A., et al. Role of low-density lipoprotein receptor in the hepatitis C virus life cycle. Hepatology 2011, 55:998-1007.
79. Maillard P., et al. The interaction of natural hepatitis C virus with human scavenger receptor SR-BI/Cla 1 is mediated by ApoB-containing lipoproteins. FASEB J. 2006, 20:735-737.
80. Dao Thi V.L., et al. Characterization of hepatitis C virus particle subpopulations reveals multiple usage of the scavenger receptor BI for entry steps. J. Biol. Chem. 2012, 287:31242-31257.
81. Ding Q., et al. The impact of hepatitis C virus entry on viral tropism. Cell Host Microbe 2014, 16:562-568.
82. Long G., et al. Mouse hepatic cells support assembly of infectious hepatitis C virus particles. Gastroenterology 2011, 141:1057-1066.
83. Frentzen A., et al. Cell entry, efficient RNA replication, and production of infectious hepatitis C virus progeny in mouse liver-derived cells. Hepatology 2014, 59:78-88.
84. Rocha-Perugini V., et al. The CD81 partner EWI-2wint inhibits hepatitis C virus entry. PLoS ONE 2008, 3:e1866.
85. Fukuhara T., et al. Expression of microRNA miR-122 facilitates an efficient replication in nonhepatic cells upon infection with hepatitis C virus. J. Virol. 2012, 86:7918-7933.
86. Kupershmidt I., et al. Ontology-based meta-analysis of global collections of high-throughput public data. PLoS ONE 2010, 5:e13066.
87. Fletcher N.F., et al. Hepatitis C virus infects the endothelial cells of the blood-brain barrier. Gastroenterology 2012, 142:634-643.
88. Gumber S.C., Chopra S. Hepatitis C: a multifaceted disease, review of extrahepatic manifestations. Ann. Intern. Med. 1995, 123:615-620.
89. Jacobson I.M., et al. Telaprevir for previously untreated chronic hepatitis C virus infection. N. Engl. J. Med. 2011, 364:2405-2416.
90. Sulkowski M.S., et al. Daclatasvir plus sofosbuvir for previously treated or untreated chronic HCV infection. N. Engl. J. Med. 2014, 370:211-221.
91. Sarrazin C., Zeuzem S. Resistance to direct antiviral agents in patients with hepatitis C virus infection. Gastroenterology 2010, 138:447-462.
92. Chan K., et al. Cost effectiveness of direct-acting antiviral therapy for treatment-naive patients with chronic HCV genotype 1 infection in the veterans health administration. Clin. Gastroenterol. Hepatol. 2013, 11:1503-1510.
93. Bassendine M.F., et al. HCV and the hepatic lipid pathway as a potential treatment target. J. Hepatol. 2011, 55:1428-1440.
94. Ikeda M., et al. Different anti-HCV profiles of statins and their potential for combination therapy with interferon. Hepatology 2006, 44:117-125.
95. Zhu Q., et al. Statin therapy improves response to interferon alfa and ribavirin in chronic hepatitis C: a systematic review and meta-analysis. Antiviral Res. 2013, 98:373-379.
96. Bader T., et al. A randomized controlled trial adding fluvastatin to peginterferon and ribavirin for naive genotype 1 hepatitis C patients. J. Viral Hepat. 2013, 20:622-627.
97. Forde K.A., et al. Do statins reduce hepatitis C RNA titers during routine clinical use?. World J. Gastroenterol. 2009, 15:5020-5027.
98. Bocchetta S., et al. Up-regulation of the ATP-binding cassette transporter A1 inhibits hepatitis C virus infection. PLoS ONE 2014, 9:e92140.
99. Cheng G., et al. A virocidal amphipathic (-helical peptide that inhibits hepatitis C virus infection in vitro. Proc. Natl. Acad. Sci. U.S.A. 2008, 105:3088-3093.