Hepatitis C virus replication is modulated by the interaction of nonstructural protein NS5B and fatty acid synthase

Journal of Virology

Volumn 87, Issue 9, 2013, Pages 4994-5004

  Huang, Jing Tang ^a,b   Tseng, Ching Ping ^c   Liao, Mei Huei ^a   Lu, Shao Chun ^d   Yeh, Wei Zhou ^a   Sakamoto, Naoya ^e   Chen, Chuan Mu ^b   Cheng, Ju Chien ^a  

^a CHINA MEDICAL UNIVERSITY   (Taiwan)

^b NATIONAL CHUNG HSING UNIVERSITY   (Taiwan)

^c CHANG GUNG UNIVERSITY   (Taiwan)

^d NATIONAL TAIWAN UNIVERSITY   (Taiwan)

^e TOKYO MEDICAL AND DENTAL UNIVERSITY   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

FATTY ACID SYNTHASE; NONSTRUCTURAL PROTEIN 5B; RNA DIRECTED RNA POLYMERASE;

AMINO TERMINAL SEQUENCE; ARTICLE; BINDING AFFINITY; BINDING SITE; CELL LYSATE; CONTROLLED STUDY; ENZYME ACTIVITY; ENZYME ASSAY; HEPATITIS C VIRUS; IMMUNOPRECIPITATION; IN VITRO STUDY; LIPID RAFT; MASS SPECTROMETRY; MATRIX ASSISTED LASER DESORPTION IONIZATION TIME OF FLIGHT MASS SPECTROMETRY; NONHUMAN; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN DETERMINATION; PROTEIN DOMAIN; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN LOCALIZATION; PROTEIN PROTEIN INTERACTION; PROTEOMICS; VIRUS EXPRESSION; VIRUS REPLICATION;

CELL LINE, TUMOR; FATTY ACID SYNTHETASE COMPLEX; HEPACIVIRUS; HEPATITIS C; HUMANS; PROTEIN BINDING; VIRAL NONSTRUCTURAL PROTEINS; VIRUS REPLICATION;

HEPATITIS C VIRUS;

EID: 84876315023     PISSN: 0022538X     EISSN: 10985514     Source Type: Journal    
DOI: 10.1128/JVI.02526-12     Document Type: Article

References (57)

1. Lindenbach BD, Rice CM. 2005. Unravelling hepatitis C virus replication from genome to function. Nature 436:933-938.
2. Egger D, Wolk B, Gosert R, Bianchi L, Blum HE, Moradpour D, Bienz K. 2002. Expression of hepatitis C virus proteins induces distinct membrane alterations including a candidate viral replication complex. J. Virol. 76:5974-5984.
3. Moradpour D, Penin F, Rice CM. 2007. Replication of hepatitis C virus. Nat. Rev. Microbiol. 5:453-463.
4. Samuel D, Feray C. 2000. Recurrent hepatitis C after liver transplantation: clinical and therapeutical issues. J. Viral Hepat. 7:87-92.
5. Thomson BJ, Finch RG. 2005. Hepatitis C virus infection. Clin. Microbiol. Infect. 11:86-94.
6. Poenisch M, Bartenschlager R. 2010. New insights into structure and replication of the hepatitis C virus and clinical implications. Semin. Liver Dis. 30:333-347.
7. Hwang SJ, Lee SD. 2011. Hepatic steatosis and hepatitis C: still unhappy bedfellows? J. Gastroenterol. Hepatol. 26(Suppl. 1):96-101.
8. Negro F. 2010. Abnormalities of lipid metabolism in hepatitis C virus infection. Gut 59:1279-1287.
9. 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.
10. Liu S, McCormick KD, Zhao W, Zhao T, Fan D, Wang T. 2012. Human apolipoprotein E peptides inhibit hepatitis C virus entry by blocking virus binding. Hepatology 56:484-491.
11. Mancone C, Steindler C, Santangelo L, Simonte G, Vlassi C, Longo MA, D'Offizi G, Di Giacomo C, Pucillo LP, Amicone L, Tripodi M, Alonzi T. 2011. Hepatitis C virus production requires apolipoprotein A-I and affects its association with nascent low-density lipoproteins. Gut 60:378-386.
12. Gastaminza P, Cheng G, Wieland S, Zhong J, Liao W, Chisari FV. 2008. Cellular determinants of hepatitis C virus assembly, maturation, degradation, and secretion. J. Virol. 82:2120-2129.
13. Huang H, Sun F, Owen DM, Li W, Chen Y, Gale M, Jr., Ye J. 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.
14. Kapadia SB, Chisari FV. 2005. Hepatitis C virus RNA replication is regulated by host geranylgeranylation and fatty acids. Proc. Natl. Acad. Sci. U. S. A. 102:2561-2566.
15. Wang C, Gale M, Jr, Keller BC, Huang H, Brown MS, Goldstein JL, Ye J. 2005. Identification of FBL2 as a geranylgeranylated cellular protein required for hepatitis C virus RNA replication. Mol. Cell 18:425-434.
16. Ye J, Wang C, Sumpter R, Jr, Brown MS, Goldstein JL, Gale M, Jr. 2003. Disruption of hepatitisCvirusRNAreplication through inhibition of host protein geranylgeranylation. Proc. Natl. Acad. Sci. U. S. A. 100:15865-15870.
17. Su AI, Pezacki JP, Wodicka L, Brideau AD, Supekova L, Thimme R, Wieland S, Bukh J, Purcell RH, Schultz PG, Chisari FV. 2002. Genomic analysis of the host response to hepatitis C virus infection. Proc. Natl. Acad. Sci. U. S. A. 99:15669-15674.
18. Yang W, Hood BL, Chadwick SL, Liu S, Watkins SC, Luo G, Conrads TP, Wang T. 2008. Fatty acid synthase is up-regulated during hepatitis C virus infection and regulates hepatitis C virus entry and production. Hepatology 48:1396-1403.
19. Choi J, Lee KJ, Zheng Y, Yamaga AK, Lai MM, Ou JH. 2004. Reactive oxygen species suppress hepatitis C virus RNA replication in human hepatoma cells. Hepatology 39:81-89.
20. Cheng JC, Chang MF, Chang SC. 1999. Specific interaction between the hepatitis C virus NS5B RNA polymerase and the 3' end of the viral RNA. J. Virol. 73:7044-7049.
21. Weng LP, Wu CC, Hsu BL, Chi LM, Liang Y, Tseng CP, Hsieh LL, Yu JS. 2008. Secretome-based identification of Mac-2 binding protein as a potential oral cancer marker involved in cell growth and motility. J. Proteome Res. 7:3765-3775.
22. Craggs JK, Ball JK, Thomson BJ, Irving WL, Grabowska AM. 2001. Development of a strand-specific RT-PCR based assay to detect the replicative form of hepatitis C virus RNA. J. Virol. Methods 94:111-120.
23. Cheng JC, Yeh YJ, Tseng CP, Hsu SD, Chang YL, Sakamoto N, Huang HD. 2012. Let-7b is a novel regulator of hepatitis C virus replication. Cell. Mol. Life Sci. 69:2621-2633.
24. Wakita T, Pietschmann T, Kato T, Date T, Miyamoto M, Zhao Z, Murthy K, Habermann A, Krausslich HG, Mizokami M, Bartenschlager R, Liang TJ. 2005. Production of infectious hepatitis C virus in tissue culture from a cloned viral genome. Nat. Med. 11:791-796.
25. Gao L, Aizaki H, He JW, Lai MM. 2004. Interactions between viral nonstructural proteins and host protein hVAP-33 mediate the formation of hepatitis C virus RNA replication complex on lipid raft. J. Virol. 78:3480-3488.
26. Quinkert D, Bartenschlager R, Lohmann V. 2005. Quantitative analysis of the hepatitis C virus replication complex. J. Virol. 79:13594-13605.
27. Lahser FC, Malcolm BA. 2004. A continuous nonradioactive assay for RNA-dependent RNA polymerase activity. Anal. Biochem. 325:247-254.
28. Mosley RT, Edwards TE, Murakami E, Lam AM, Grice RL, Du J, Sofia MJ, Furman PA, Otto MJ. 2012. Structure of hepatitis C virus polymerase in complex with primer-template RNA. J. Virol. 86:6503-6511.
29. Shi ST, Lee KJ, Aizaki H, Hwang SB, Lai MM. 2003. Hepatitis C virus RNA replication occurs on a detergent-resistant membrane that cofractionates with caveolin-2. J. Virol. 77:4160-4168.
30. Kuhajda FP, Pizer ES, Li JN, Mani NS, Frehywot GL, Townsend CA. 2000. Synthesis and antitumor activity of an inhibitor of fatty acid synthase. Proc. Natl. Acad. Sci. U. S. A. 97:3450-3454.
31. Kridel SJ, Axelrod F, Rozenkrantz N, Smith JW. 2004. Orlistat is a novel inhibitor of fatty acid synthase with antitumor activity. Cancer Res. 64:2070-2075.
32. Migliaccio G, Tomassini JE, Carroll SS, Tomei L, Altamura S, Bhat B, Bartholomew L, Bosserman MR, Ceccacci A, Colwell LF, Cortese R, De Francesco R, Eldrup AB, Getty KL, Hou XS, LaFemina RL, Ludmerer SW, MacCoss M, McMasters DR, Stahlhut MW, Olsen DB, Hazuda DJ, Flores OA. 2003. Characterization of resistance to non-obligate chainterminating ribonucleoside analogs that inhibit hepatitis C virus replication in vitro. J. Biol. Chem. 278:49164-49170.
33. Ahlquist P, Noueiry AO, Lee WM, Kushner DB, Dye BT. 2003. Host factors in positive-strand RNA virus genome replication. J. Virol. 77:8181-8186.
34. Moriishi K, Matsuura Y. 2007. Host factors involved in the replication of hepatitis C virus. Rev. Med. Virol. 17:343-354.
35. Alvisi G, Madan V, Bartenschlager R. 2011. Hepatitis C virus and host cell lipids: an intimate connection. RNA Biol. 8:258-269.
36. Jayakumar A, Tai MH, Huang WY, al-Feel W, Hsu M, Abu-Elheiga L, Chirala SS, Wakil SJ. 1995. Human fatty acid synthase: properties and molecular cloning. Proc. Natl. Acad. Sci. U. S. A. 92:8695-8699.
37. Fujino T, Nakamuta M, Yada R, Aoyagi Y, Yasutake K, Kohjima M, Fukuizumi K, Yoshimoto T, Harada N, Yada M, Kato M, Kotoh K, Taketomi A, Maehara Y, Nakashima M, Enjoji M. 2010. Expression profile of lipid metabolism-associated genes in hepatitis C virus-infected human liver. Hepatol. Res. 40:923-929.
38. Aragones G, Alonso-Villaverde C, Oliveras-Ferraros C, Beltran-Debon R, Rull A, Rodriguez-Sanabria F, Camps J, Martin AV, Menendez JA, Joven J. 2010. Infection with HIV and HCV enhances the release of fatty acid synthase into circulation: evidence for a novel indicator of viral infection. BMC Gastroenterol. 10:92. doi:10.1186/1471-230X-10-92.
39. Joven J, Espinel E, Rull A, Beltran-Debon R, Aragones G, Rodriguez-Gallego E, Camps J, Pedro-Botet J, Sans T, Menendez JA, Alonso-Villaverde C. 2011. Serum fatty acid synthase concentration is increased in patients with hepatitis viral infection and may assist in the prediction of liver steatosis. J. Clin. Virol. 51:199-201.
40. Woodhouse SD, Narayan R, Latham S, Lee S, Antrobus R, Gangadharan B, Luo S, Schroth GP, Klenerman P, Zitzmann N. 2010. Transcriptome sequencing, microarray, and proteomic analyses reveal cellular and metabolic impact of hepatitis C virus infection in vitro. Hepatology 52:443-453.
41. Miyanari Y, Atsuzawa K, Usuda N, Watashi K, Hishiki T, Zayas M, Bartenschlager R, Wakita T, Hijikata M, Shimotohno K. 2007. The lipid droplet is an important organelle for hepatitis C virus production. Nat. Cell Biol. 9:1089-1097.
42. Ueno K. 2000. Involvement of fatty acid synthase in axonal development in mouse embryos. Genes Cells 5:859-869.
43. Yu GY, Lee KJ, Gao L, Lai MM. 2006. Palmitoylation and polymerization of hepatitis C virus NS4B protein. J. Virol. 80:6013-6023.
44. Jackel-Cram C, Babiuk LA, Liu Q. 2007. Up-regulation of fatty acid synthase promoter by hepatitis C virus core protein: genotype-3a core has a stronger effect than genotype-1b core. J. Hepatol. 46:999-1008.
45. Oem JK, Jackel-Cram C, Li YP, Zhou Y, Zhong J, Shimano H, Babiuk LA, Liu Q. 2008. Activation of sterol regulatory element-binding protein 1c and fatty acid synthase transcription by hepatitis C virus non-structural protein 2. J. Gen. Virol. 89:1225-1230.
46. Park CY, Jun HJ, Wakita T, Cheong JH, Hwang SB. 2009. Hepatitis C virus nonstructural 4B protein modulates sterol regulatory elementbinding protein signaling via the AKT pathway. J. Biol. Chem. 284:9237-9246.
47. Jackel-Cram C, Qiao L, Xiang Z, Brownlie R, Zhou Y, Babiuk L, Liu Q. 2010. Hepatitis C virus genotype-3a core protein enhances sterol regulatory element-binding protein-1 activity through the phosphoinositide 3-kinase-Akt-2 pathway. J. Gen. Virol. 91:1388-1395.
48. Foo NC, Yen TS. 2000. Activation of promoters for cellular lipogenic genes by hepatitis B virus large surface protein. Virology 269:420-425.
49. Li Y, Webster-Cyriaque J, Tomlinson CC, Yohe M, Kenney S. 2004. Fatty acid synthase expression is induced by the Epstein-Barr virus immediate-early protein BRLF1 and is required for lytic viral gene expression. J. Virol. 78:4197-4206.
50. Munger J, Bennett BD, Parikh A, Feng XJ, McArdle J, Rabitz HA, Shenk T, Rabinowitz JD. 2008. Systems-level metabolic flux profiling identifies fatty acid synthesis as a target for antiviral therapy. Nat. Biotechnol. 26:1179-1186.
51. Heaton NS, Perera R, Berger KL, Khadka S, Lacount DJ, Kuhn RJ, Randall G. 2010. Dengue virus nonstructural protein 3 redistributes fatty acid synthase to sites of viral replication and increases cellular fatty acid synthesis. Proc. Natl. Acad. Sci. U. S. A. 107:17345-17350.
52. Miyanari Y, Hijikata M, Yamaji M, Hosaka M, Takahashi H, Shimotohno K. 2003. Hepatitis C virus non-structural proteins in the probable membranous compartment function in viral genome replication. J. Biol. Chem. 278:50301-50308.
53. Menendez JA, Lupu R. 2007. Fatty acid synthase and the lipogenic phenotype in cancer pathogenesis. Nat. Rev. Cancer 7:763-777.
54. Wu JM, Skill NJ, Maluccio MA. 2010. Evidence of aberrant lipid metabolism in hepatitis C and hepatocellular carcinoma. HPB (Oxford) 12:625-636.
55. Di Vizio D, Adam RM, Kim J, Kim R, Sotgia F, Williams T, Demichelis F, Solomon KR, Loda M, Rubin MA, Lisanti MP, Freeman MR. 2008. Caveolin-1 interacts with a lipid raft-associated population of fatty acid synthase. Cell Cycle 7:2257-2267.
56. Cokakli M, Erdal E, Nart D, Yilmaz F, Sagol O, Kilic M, Karademir S, Atabey N. 2009. Differential expression of Caveolin-1 in hepatocellular carcinoma: correlation with differentiation state, motility and invasion. BMC Cancer 9:65. doi:10.1186/1471-2407-9-65.
57. Tse EY, Ko FC, Tung EK, Chan LK, Lee TK, Ngan ES, Man K, Wong AS, Ng IO, Yam JW. 2012. Caveolin-1 overexpression is associated with hepatocellular carcinoma tumourigenesis and metastasis. J. Pathol. 226:645-653.