Regulation of the hepatitis C virus RNA replicase by endogenous lipid peroxidation

Nature Medicine

Volumn 20, Issue 8, 2014, Pages 927-935

  Yamane, Daisuke ^a,b   McGivern, David R ^a,b   Wauthier, Eliane ^a,b   Yi, Minkyung ^c   Madden, Victoria J ^a   Welsch, Christoph ^d   Antes, Iris ^e   Wen, Yahong ^f   Chugh, Pauline E ^a,b   McGee, Charles E ^a   Widman, Douglas G ^g   Misumi, Ichiro ^a   Bandyopadhyay, Sibali ^h   Kim, Seungtaek ^a,b,i   Shimakami, Tetsuro ^a,b   Oikawa, Tsunekazu ^a,b   Whitmire, Jason K ^a,b   Heise, Mark T ^a,b   Dittmer, Dirk P ^a,b   Kao, C Cheng ^f   Pitson, Stuart M ^j   Merrill, Alfred H ^h   Reid, Lola M ^a,b   Lemon, Stanley M ^a,b   more..

^a UNIVERSITY OF NORTH CAROLINA SCHOOL OF MEDICINE   (United States)

^b UNIVERSITY OF NORTH CAROLINA   (United States)

^c University of Texas Medical Branch School of Medicine   (United States)

^d UNIVERSITY HOSPITAL FRANKFURT   (Germany)

^e Munich Center for Integrated Protein Science   (Germany)

^f INDIANA UNIVERSITY   (United States)

^g IL   (United States)

^h GEORGIA INSTITUTE OF TECHNOLOGY   (United States)

ⁱ Yonsei University College of Medicine   (South Korea)

^j CENTRE FOR CANCER BIOLOGY   (Australia)

more..

Author keywords

[No Author keywords available]

Indexed keywords

ADAPTOR PROTEINS, SIGNAL TRANSDUCING; ANTIVIRAL AGENTS; CELL LINE; CELL MEMBRANE; HEPACIVIRUS; HEPATITIS C; HEPATOCYTES; HUMANS; LIPID PEROXIDATION; OXIDATIVE STRESS; PHOSPHOTRANSFERASES (ALCOHOL GROUP ACCEPTOR); RNA INTERFERENCE; RNA REPLICASE; RNA, SMALL INTERFERING; VIRAL NONSTRUCTURAL PROTEINS; VIRUS REPLICATION;

EID: 84905868112     PISSN: 10788956     EISSN: 1546170X     Source Type: Journal    
DOI: 10.1038/nm.3610     Document Type: Article

References (67)

1. Kalyanaraman, B. Teaching the basics of redox biology to medical and graduate students: Oxidants, antioxidants and disease mechanisms. Redox. Biol. 1, 244-257 (2013).
2. Nathan, C. & Cunningham-Bussel, A. Beyond oxidative stress: An immunologist's guide to reactive oxygen species. Nat. Rev. Immunol. 13, 349-361 (2013).
3. Dennery, P.A. Effects of oxidative stress on embryonic development. Birth Defects Res. C Embryo Today 81, 155-162 (2007). (Pubitemid 350086244)
4. Valyi-Nagy, T. & Dermody, T.S. Role of oxidative damage in the pathogenesis of viral infections of the nervous system. Histol. Histopathol. 20, 957-967 (2005). (Pubitemid 40932613)
5. Thomas, D.L. Global control of hepatitis C: Where challenge meets opportunity. Nat. Med. 19, 850-858 (2013).
6. Choi, J. Oxidative stress, endogenous antioxidants, alcohol, and hepatitis C: Pathogenic interactions and therapeutic considerations. Free Radic. Biol. Med. 52, 1135-1150 (2012).
7. Okuda, M. et al. Mitochondrial injury, oxidative stress, and antioxidant gene expression are induced by hepatitis C virus core protein. Gastroenterology 122, 366-375 (2002). (Pubitemid 34116988)
8. Huang, H., Chen, Y. & Ye, J. Inhibition of hepatitis C virus replication by peroxidation of arachidonate and restoration by vitamin E. Proc. Natl. Acad. Sci. USA 104, 18666-18670 (2007). (Pubitemid 350210754)
9. Wakita, T. et al. Production of infectious hepatitis C virus in tissue culture from a cloned viral genome. Nat. Med. 11, 791-796 (2005). (Pubitemid 41021213)
10. Lindenbach, B.D. et al. Complete replication of hepatitis C virus in cell culture. Science 309, 623-626 (2005). (Pubitemid 41033648)
11. Zhong, J. et al. Robust hepatitis C virus infection in vitro. Proc. Natl. Acad. Sci. USA 102, 9294-9299 (2005). (Pubitemid 40923557)
12. Yi, M., Villanueva, R.A., Thomas, D.L., Wakita, T. & Lemon, S.M. Production of infectious genotype 1a hepatitis C virus (Hutchinson strain) in cultured human hepatoma cells. Proc. Natl. Acad. Sci. USA 103, 2310-2315 (2006). (Pubitemid 43271666)
13. Pietschmann, T. et al. Production of infectious genotype 1b virus particles in cell culture and impairment by replication enhancing mutations. PLoS Pathog. 5, e1000475 (2009).
14. Paul, D., Hoppe, S., Saher, G., Krijnse-Locker, J. & Bartenschlager, R. Morphological and biochemical characterization of the membranous hepatitis C virus replication compartment. J. Virol. 87, 10612-10627 (2013).
15. Gosert, R. et al. Identification of the hepatitis C virus RNA replication complex in Huh-7 cells harboring subgenomic replicons. J. Virol. 77, 5487-5492 (2003). (Pubitemid 36460961)
16. Shi, S.T., Lee, K.J., Aizaki, H., Hwang, S.B. & Lai, M.M. Hepatitis C virus RNA replication occurs on a detergent-resistant membrane that cofractionates with caveolin-2. J. Virol. 77, 4160-4168 (2003). (Pubitemid 36350955)
17. Hsu, N.Y. et al. Viral reorganization of the secretory pathway generates distinct organelles for RNA replication. Cell 141, 799-811 (2010).
18. Reiss, S. et al. Recruitment and activation of a lipid kinase by hepatitis C virus NS5A is essential for integrity of the membranous replication compartment. Cell Host Microbe 9, 32-45 (2011).
19. Saxena, V., Lai, C.K., Chao, T.C., Jeng, K.S. & Lai, M.M. Annexin A2 is involved in the formation of hepatitis C virus replication complex on the lipid raft. J. Virol. 86, 4139-4150 (2012).
20. Romero-Brey, I. et al. Three-dimensional architecture and biogenesis of membrane structures associated with hepatitis C virus replication. PLoS Pathog. 8, e1003056 (2012).
21. Miyanari, Y. et al. The lipid droplet is an important organelle for hepatitis C virus production. Nat. Cell Biol. 9, 1089-1097 (2007). (Pubitemid 47338147)
22. Aizaki, H. et al. Critical role of virion-associated cholesterol and sphingolipid in hepatitis C virus infection. J. Virol. 82, 5715-5724 (2008). (Pubitemid 351822247)
23. Sakamoto, H. et al. Host sphingolipid biosynthesis as a target for hepatitis C virus therapy. Nat. Chem. Biol. 1, 333-337 (2005).
24. Umehara, T. et al. Serine palmitoyltransferase inhibitor suppresses HCV replication in a mouse model. Biochem. Biophys. Res. Commun. 346, 67-73 (2006). (Pubitemid 43884734)
25. Hirata, Y. et al. Self-enhancement of hepatitis C virus replication by promotion of specific sphingolipid biosynthesis. PLoS Pathog. 8, e1002860 (2012).
26. Weng, L. et al. Sphingomyelin activates hepatitis C virus RNA polymerase in a genotype-specific manner. J. Virol. 84, 11761-11770 (2010).
27. Shimakami, T. et al. Protease inhibitor-resistant hepatitis C virus mutants with reduced fitness from impaired production of infectious virus. Gastroenterology 140, 667-675 (2011).
28. Liu, H. et al. Molecular cloning and functional characterization of a novel mammalian sphingosine kinase type 2 isoform. J. Biol. Chem. 275, 19513-19520 (2000). (Pubitemid 30441543)
29. Kapadia, S.B. & Chisari, F.V. Hepatitis C virus RNA replication is regulated by host geranylgeranylation and fatty acids. Proc. Natl. Acad. Sci. USA 102, 2561-2566 (2005). (Pubitemid 40279416)
30. Lindenbach, B.D. et al. Cell culture-grown hepatitis C virus is infectious in vivo and can be recultured in vitro. Proc. Natl. Acad. Sci. USA 103, 3805-3809 (2006). (Pubitemid 43376636)
31. Yanagi, M., Purcell, R.H., Emerson, S.U. & Bukh, J. Transcripts from a single full-length cDNA clone of hepatitis C virus are infectious when directly transfected into liver of a chimpanzee. Proc. Natl. Acad. Sci. USA 94, 8738-8743 (1997). (Pubitemid 27335109)
32. Beard, M.R. et al. An infectious molecular clone of a Japanese genotype 1b hepatitis C virus. Hepatology 30, 316-324 (1999). (Pubitemid 29300603)
33. Andrus, L. et al. Expression of paramyxovirus V proteins promotes replication and spread of hepatitis C virus in cultures of primary human fetal liver cells. Hepatology 54, 1901-1912 (2011).
34. Li, Y.P. et al. Highly efficient full-length hepatitis C virus genotype 1 (strain TN) infectious culture system. Proc. Natl. Acad. Sci. USA 109, 19757-19762 (2012).
35. Bochkov, V.N. et al. Generation and biological activities of oxidized phospholipids. Antioxid. Redox Signal. 12, 1009-1059 (2010).
36. Pizzimenti, S. et al. Interaction of aldehydes derived from lipid peroxidation and membrane proteins. Front. Physiol. 4, 242 (2013).
37. Pitson, S.M. et al. Activation of sphingosine kinase 1 by ERK1/2-mediated phosphorylation. EMBO J. 22, 5491-5500 (2003). (Pubitemid 37279958)
38. Alvarez, S.E. et al. Sphingosine-1-phosphate is a missing cofactor for the E3 ubiquitin ligase TRAF2. Nature 465, 1084-1088 (2010).
39. Hait, N.C. et al. Regulation of histone acetylation in the nucleus by sphingosine-1-phosphate. Science 325, 1254-1257 (2009).
40. Jain, S.K. et al. Oxidative stress in chronic hepatitis C: Not just a feature of late stage disease. J. Hepatol. 36, 805-811 (2002). (Pubitemid 35177411)
41. Yano, M. et al. Comprehensive analysis of the effects of ordinary nutrients on hepatitis C virus RNA replication in cell culture. Antimicrob. Agents Chemother. 51, 2016-2027 (2007). (Pubitemid 46903089)
42. Kohlway, A. et al. Hepatitis C virus RNA replication and virus particle assembly require specific dimerization of the NS4A protein transmembrane domain. J. Virol. 88, 628-642 (2014).
43. Ibrahim, W. et al. Oxidative stress and antioxidant status in mouse liver: Effects of dietary lipid, vitamin E and iron. J. Nutr. 127, 1401-1406 (1997). (Pubitemid 27284011)
44. Lackner, T., Muller, A., Konig, M., Thiel, H.J. & Tautz, N. Persistence of bovine viral diarrhea virus is determined by a cellular cofactor of a viral autoprotease. J. Virol. 79, 9746-9755 (2005). (Pubitemid 41022317)
45. Leivers, A.L. et al. Discovery of selective small molecule type iii phosphatidylinositol 4-kinase α (PI4KIIIα) inhibitors as anti hepatitis C (HCV) agents. J. Med. Chem. 57, 2091-2106 (2014).
46. Oikawa, T. et al. Sal-like protein 4 (SALL4), a stem cell biomarker in liver cancers. Hepatology 57, 1469-1483 (2013).
47. Schmelzer, E. et al. Human hepatic stem cells from fetal and postnatal donors. J. Exp. Med. 204, 1973-1987 (2007). (Pubitemid 47236331)
48. Wang, Y. et al. Paracrine signals from mesenchymal cell populations govern the expansion and differentiation of human hepatic stem cells to adult liver fates. Hepatology 52, 1443-1454 (2010).
49. Kubota, H. & Reid, L.M. Clonogenic hepatoblasts, common precursors for hepatocytic and biliary lineages, are lacking classical major histocompatibility complex class I antigen. Proc. Natl. Acad. Sci. USA 97, 12132-12137 (2000).
50. Ma, Y., Yates, J., Liang, Y., Lemon, S.M. & Yi, M. NS3 helicase domains involved in infectious intracellular hepatitis C virus particle assembly. J. Virol. 82, 7624-7639 (2008). (Pubitemid 352031229)
51. Yanagi, M., Purcell, R.H., Emerson, S.U. & Bukh, J. Transcripts from a single full-length cDNA clone of hepatitis C virus are infectious when directly transfected into the liver of a chimpanzee. Proc. Natl. Acad. Sci. USA 94, 8738-8743 (1997). (Pubitemid 27335109)
52. Shimakami, T. et al. Stabilization of hepatitis C virus RNA by an Ago2-miR-122 complex. Proc. Natl. Acad. Sci. USA 109, 941-946 (2012).
53. Date, T. et al. Novel cell culture-adapted genotype 2a hepatitis C virus infectious clone. J. Virol. 86, 10805-10820 (2012).
54. Saeed, M. et al. Efficient replication of genotype 3a and 4a hepatitis C virus replicons in human hepatoma cells. Antimicrob. Agents Chemother. 56, 5365-5373 (2012).
55. Timpe, J.M. et al. Hepatitis C virus cell-cell transmission in hepatoma cells in the presence of neutralizing antibodies. Hepatology 47, 17-24 (2008). (Pubitemid 351171037)
56. Kannan, R.P., Hensley, L.L., Evers, L.E., Lemon, S.M. & McGivern, D.R. Hepatitis C virus infection causes cell cycle arrest at the level of initiation of mitosis. J. Virol. 85, 7989-8001 (2011).
57. Puneet, P. et al. SphK1 regulates proinflammatory responses associated with endotoxin and polymicrobial sepsis. Science 328, 1290-1294 (2010).
58. Dansako, H. et al. 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. 9, e1003345 (2013).
59. Shaner, R.L. et al. Quantitative analysis of sphingolipids for lipidomics using triple quadrupole and quadrupole linear ion trap mass spectrometers. J. Lipid Res. 50, 1692-1707 (2009).
60. Sullards, M.C., Liu, Y., Chen, Y. & Merrill, A.H. Jr. Analysis of mammalian sphingolipids by liquid chromatography tandem mass spectrometry (LC-MS/MS) and tissue imaging mass spectrometry (TIMS). Biochim. Biophys. Acta 1811, 838-853 (2011).
61. Reynolds, E.S. The use of lead citrate at high pH as an electron-opaque stain in electron microscopy. J. Cell Biol. 17, 208-212 (1963).
62. Papin, J.F., Vahrson, W. & Dittmer, D.P. SYBR green-based real-time quantitative PCR assay for detection of West Nile Virus circumvents false-negative results due to strain variability. J. Clin. Microbiol. 42, 1511-1518 (2004). (Pubitemid 38500789)
63. Gurukumar, K.R. et al. Development of real time PCR for detection and quantitation of Dengue Viruses. Virol. J. 6, 10 (2009).
64. Qu, L. et al. Disruption of TLR3 signaling due to cleavage of TRIF by the hepatitis A virus protease-polymerase processing intermediate, 3CD. PLoS Pathog. 7, e1002169 (2011).
65. Ahmed, R., Salmi, A., Butler, L.D., Chiller, J.M. & Oldstone, M.B. Selection of genetic variants of lymphocytic choriomeningitis virus in spleens of persistently infected mice. Role in suppression of cytotoxic T lymphocyte response and viral persistence. J. Exp. Med. 160, 521-540 (1984). (Pubitemid 14052514)
66. Bartenschlager, R., Lohmann, V. & Penin, F. The molecular and structural basis of advanced antiviral therapy for hepatitis C virus infection. Nat. Rev. Microbiol. 11, 482-496 (2013).
67. Humphrey, W., Dalke, A. & Schulten, K. VMD: Visual molecular dynamics. J. Mol. Graph. 14, 33-38, 27-28 (1996). (Pubitemid 26152973)