Rab18 is required for viral assembly of hepatitis C virus through trafficking of the core protein to lipid droplets

Virology

Volumn 462-463, Issue 1, 2014, Pages 166-174

  Dansako, Hiromichi ^a   Hiramoto, Hiroki ^a   Ikeda, Masanori ^a   Wakita, Takaji ^b   Kato, Nobuyuki ^a  

^a OKAYAMA UNIVERSITY   (Japan)

^b NATIONAL INSTITUTE OF INFECTIOUS DISEASES   (Japan)

Author keywords

Core protein; Hepatitis C virus; Lipid droplet; Rab18; RNA replication; Viral assembly

Indexed keywords

CORE PROTEIN; FAT DROPLET; GUANOSINE TRIPHOSPHATASE; PROTEIN RAB18; UNCLASSIFIED DRUG;

ARTICLE; CELL STRAIN; CELL STRAIN HUH 7; CELL STRAIN RSC; CONTROLLED STUDY; ENZYME LOCALIZATION; ENZYME REGULATION; HEPATITIS C; HEPATITIS C VIRUS; HEPATITIS C VIRUS JFH 1; HUMAN; HUMAN CELL; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN LIPID INTERACTION; PROTEIN PROTEIN INTERACTION; PROTEIN TRANSPORT; VIRUS ASSEMBLY; VIRUS CELL INTERACTION; VIRUS INFECTIVITY; VIRUS INHIBITION; VIRUS REPLICATION; VIRUS STRAIN;

CORE PROTEIN; HEPATITIS C VIRUS; LIPID DROPLET; RAB18; RNA REPLICATION; VIRAL ASSEMBLY;

CELL LINE; HEPACIVIRUS; HEPATOCYTES; HOST-PATHOGEN INTERACTIONS; HUMANS; PROTEIN TRANSPORT; RAB GTP-BINDING PROTEINS; VIRAL CORE PROTEINS; VIRUS ASSEMBLY;

EID: 84903737594     PISSN: 00426822     EISSN: 10960341     Source Type: Journal    
DOI: 10.1016/j.virol.2014.05.017     Document Type: Article

References (34)

1. Abe K., Ikeda M., Dansako H., Naka K., Kato N. Cell culture-adaptive NS3 mutations required for the robust replication of genome-length hepatitis C virus RNA. Virus Res. 2007, 125:88-97.
2. Ariumi Y., Kuroki M., Abe K., Dansako H., Ikeda M., Wakita T., Kato N. DDX3 DEAD-box RNA helicase is required for hepatitis C virus RNA replication. J. Virol. 2007, 81:13922-13926.
3. Ariumi Y., Kuroki M., Dansako H., Abe K., Ikeda M., Wakita T., Kato N. The DNA damage sensors ataxia-telangiectasia mutated kinase and checkpoint kinase 2 are required for hepatitis C virus RNA replication. J. Virol. 2008, 82:9639-9646.
4. Blight K.J., McKeating J.A., Rice C.M. Highly permissive cell lines for subgenomic and genomic hepatitis C virus RNA replication. J. Virol. 2002, 76:13001-13014.
5. Boulant S., Douglas M.W., Moody L., Budkowska A., Targett-Adams P., McLauchlan J. Hepatitis C virus core protein induces lipid droplet redistribution in a microtubule- and dynein-dependent manner. Traffic 2008, 9:1268-1282.
6. Brasaemle D.L., Dolios G., Shapiro L., Wang R. Proteomic analysis of proteins associated with lipid droplets of basal and lipolytically stimulated 3T3-L1 adipocytes. J. Biol. Chem. 2004, 279:46835-46842.
7. Choo Q.L., Kuo G., Weiner A.J., Overby L.R., Bradley D.W., Houghton M. Isolation of a cDNA clone derived from a blood-borne non-A, non-B viral-hepatitis genome. Science 1989, 244:359-362.
8. Counihan N.A., Rawlinson S.M., Lindenbach B.D. Trafficking of hepatitis C virus core protein during virus particle assembly. PLoS Pathog. 2011, 7:e1002302.
9. Dansako H., Ikeda M., Abe K., Mori K., Takemoto K., Ariumi Y., Kato N. A new living cell-based assay system for monitoring genome-length hepatitis C virus RNA replication. Virus Res. 2008, 137:72-79.
10. Dansako H., Ikeda M., Ariumi Y., Wakita T., Kato N. Double-stranded RNA-induced interferon-beta and inflammatory cytokine production modulated by hepatitis C virus serine proteases derived from patients with hepatic diseases. Arch. Virol. 2009, 154:801-810.
11. Dansako H., Ikeda M., Kato N. Limited suppression of the interferon-beta production by hepatitis C virus serine protease in cultured human hepatocytes. FEBS J. 2007, 274:4161-4176.
12. Dansako H., Naganuma A., Nakamura T., Ikeda F., Nozaki A., Kato N. Differential activation of interferon-inducible genes by hepatitis C virus core protein mediated by the interferon stimulated response element. Virus Res. 2003, 97:17-30.
13. Dansako H., Naka K., Ikeda M., Kato N. Hepatitis C virus proteins exhibit conflicting effects on the interferon system in human hepatocyte cells. Biochem. Biophys. Res. Commun. 2005, 336:458-468.
14. Dansako H., Yamane D., Welsch C., McGivern D.R., Hu F.Y., Kato N., Lemon S.M. Class A scavenger receptor 1 (MSR1) restricts hepatitis C virus replication by mediating Toll-like receptor 3 recognition of viral RNAs produced in neighboring cells. PLoS Pathog. 2013, 9:e1003345.
15. Dejgaard S.Y., Murshid A., Erman A., Kizilay O., Verbich D., Lodge R., Dejgaard K., Ly-Hartig T.B., Pepperkok R., Simpson J.C., Presley J.F. Rab18 and Rab43 have key roles in ER-Golgi trafficking. J. Cell Sci. 2008, 121:2768-2781.
16. Hickenbottom S.J., Kimmel A.R., Londos C., Hurley J.H. Structure of a lipid droplet protein: the PAT family member TIP47. Structure 2004, 12:1199-1207.
17. Hope R.G., Murphy D.J., McLauchlan J. The domains required to direct core proteins of hepatitis C virus and GB virus-B to lipid droplets share common features with plant oleosin proteins. J. Biol. Chem. 2002, 277:4261-4270.
18. Hutagalung A.H., Novick P.J. Role of Rab GTPases in membrane traffic and cell physiology. Physiol. Rev. 2011, 91:119-149.
19. Ikeda M., Abe K., Dansako H., Nakamura T., Naka K., Kato N. Efficient replication of a full-length hepatitis C virus genome, strain O, in cell culture, and development of a luciferase reporter system. Biochem. Biophys. Res. Commun. 2005, 329:1350-1359.
20. Ikeda M., Abe K., Yamada M., Dansako H., Naka K., Kato N. Different anti-HCV profiles of statins and their potential for combination therapy with interferon. Hepatology 2006, 44:117-125.
21. Kato N. Molecular virology of hepatitis C virus. Acta Med. Okayama 2001, 55:133-159.
22. Kato N., Mori K., Abe K., Dansako H., Kuroki M., Ariumi Y., Wakita T., Ikeda M. Efficient replication systems for hepatitis C virus using a new human hepatoma cell line. Virus Res. 2009, 146:41-50.
23. Kato N., Sugiyama K., Namba K., Dansako H., Nakamura T., Takami M., Naka K., Nozaki A., Shimotohno K. Establishment of a hepatitis C virus subgenomic replicon derived from human hepatocytes infected in vitro. Biochem. Biophys. Res. Commun. 2003, 306:756-766.
24. Kenworthy R., Lambert D., Yang F., Wang N., Chen Z., Zhu Haizhen, Zhu F., Liu C., Li K., Tang H. Short-hairpin RNAs delivered by lentiviral vector transduction trigger RIG-I-mediated IFN activation. Nucleic Acids Res. 2009, 37:6587-6599.
25. Mannova P., Fang R.H., Wang H., Deng B., McIntosh M.W., Hanash S.M., Beretta L. Modification of host lipid raft proteome upon hepatitis C virus replication. Mol. Cell. Proteomics 2006, 5:2319-2325.
26. Matto M., Rice C.M., Aroeti B., Glenn J.S. Hepatitis C virus core protein associates with detergent-resistant membranes distinct from classical plasma membrane rafts. J. Virol. 2004, 78:12047-12053.
27. Miyanari Y., Atsuzawa K., Usuda N., Watashi K., Hishiki T., Zayas M., Bartenschlager R., Wakita T., Hijikata M., Shimotohno K. The lipid droplet is an important organelle for hepatitis C virus production. Nat. Cell Biol. 2007, 9:1089-1097.
28. Ohkoshi S., Kojima H., Tawaraya H., Miyajima T., Kamimura T., Asakura H., Satoh A., Hirose S., Hijikata M., Kato N., Shimotohno K. Prevalence of antibody against non-A, non-B hepatitis-virus in Japanese patients with hepatocellular-carcinoma. Jpn. J. Cancer Res. 1990, 81:550-553.
29. Ohsaki Y., Maeda T., Maeda M., Tauchi-Sato K., Fujimoto T. Recruitment of TIP47 to lipid droplets is controlled by the putative hydrophobic cleft. Biochem. Biophys. Res. Commun. 2006, 347:279-287.
30. Ozeki S., Cheng J.L., Tauchi-Sato K., Hatano N., Taniguchi H., Fujimoto T. Rab18 localizes to lipid droplets and induces their close apposition to the endoplasmic reticulum-derived membrane. J. Cell Sci. 2005, 118:2601-2611.
31. Salloum S., Wang H., Ferguson C., Parton R.G., Tai A.W. Rab18 binds to hepatitis C virus NS5A and promotes interaction between sites of viral replication and lipid droplets. PLoS Pathog. 2013, 9:e1003513.
32. Shavinskaya A., Boulant S., Penin F., McLauchlan J., Bartenschlager R. The lipid droplet binding domain of hepatitis C virus core protein is a major determinant for efficient virus assembly. J. Biol. Chem. 2007, 282:37158-37169.
33. Shi S.T., Lee K.J., Aizaki H., Hwang S.B., Lai M.M.C. Hepatitis C virus RNA replication occurs on a detergent-resistant membrane that coffactionates with caveolin-2. J. Virol. 2003, 77:4160-4168.
34. Targett-Adams P., Boulant S., McLauchlan J. Visualization of double-stranded RNA in cells supporting hepatitis C virus RNA replication. J. Virol. 2008, 82:2182-2195.