The stability of secreted, acid-labile H77/JFH-1 hepatitis C virus (HCV) particles is altered by patient isolate genotype 1a p7 sequences

Virology

Volumn 448, Issue , 2014, Pages 117-124

  Atkins, Elizabeth ^a   Tatineni, Ranjitha ^a,c   Li, Hui ^b   Gretch, David ^b   Harris, Mark ^a   Griffin, Stephen ^a,c  

^a UNIVERSITY OF LEEDS   (United Kingdom)

^b UNIVERSITY OF WASHINGTON SCHOOL OF MEDICINE   (United States)

^c INDIAN INSTITUTE OF SCIENCE   (India)

Author keywords

Drug resistance; Ion channel gating; Natural virus variants; Particle acid stability; Viroporin

Indexed keywords

ACID; UNCLASSIFIED DRUG; VIRUS PROTEIN; VIRUS PROTEIN P7;

ACIDITY; AMINO ACID SEQUENCE; ANTIVIRAL SUSCEPTIBILITY; ARTICLE; CELL LEVEL; CONTROLLED STUDY; GENOTYPE; HEPATITIS C; HEPATITIS C VIRUS; HUMAN; MOLECULAR MECHANICS; NONHUMAN; PH MEASUREMENT; PRIORITY JOURNAL; PROTEIN STRUCTURE; VIRAL PHENOMENA AND FUNCTIONS; VIRION; VIROGENESIS; VIRUS GENOME; VIRUS PARTICLE; VIRUS RELEASE; VIRUS SYNTHESIS;

EID: 84886240989     PISSN: 00426822     EISSN: 10960341     Source Type: Journal    
DOI: 10.1016/j.virol.2013.10.003     Document Type: Article

References (40)

1. Bentham M.J., Foster T.L., McCormick C., Griffin S. Mutations in hepatitis C virus p7 reduce both the egress and infectivity of assembled particles via impaired proton channel function. Journal of General Virology 2013, 94:2236-2248.
2. Boo I., teWierik K., Douam F., Lavillette D., Poumbourios P., Drummer H.E. Distinct roles in folding, CD81 receptor binding and viral entry for conserved histidine residues of hepatitis C virus glycoprotein E1 and E2. The Biochemical journal 2012, 443:85-94.
3. Boson B., Granio O., Bartenschlager R., Cosset F.L. A concerted action of hepatitis C virus p7 and nonstructural protein 2 regulates core localization at the endoplasmic reticulum and virus assembly. PLoS Pathogens 2011, 7:e1002144.
4. Clarke D., Griffin S., Beales L., Gelais C.S., Burgess S., Harris M., Rowlands D. Evidence for the formation of a heptameric ion channel complex by the hepatitis C virus p7 protein in vitro. The Journal of Biological Chemistry 2006, 281:37057-37068.
5. Foster T.L., Thompson G.S., Kalverda A.P., Kankanala J., Bentham M., Wetherill L.F., Thompson J., Barker A.M., Clarke D., Noerenberg M., Pearson A.R., Rowlands D.J., Homans S.W., Harris M., Foster R., Griffin S., 2013. Structure-guided design affirms inhibitors of hepatitis C virus p7 as a viable class of antivirals targeting virion release. Hepatology,. [Epub ahead of print]. http://dx.doi.org/10.1002/hep.26685.
6. Foster T.L., Verow M., Wozniak A.L., Bentham M.J., Thompson J., Atkins E., Weinman S.A., Fishwick C., Foster R., Harris M., Griffin S. Resistance mutations define specific antiviral effects for inhibitors of the hepatitis C virus p7 ion channel. Hepatology 2011, 54:79-90.
7. Gastaminza P., Cheng G., Wieland S., Zhong J., Liao W., Chisari F.V. Cellular determinants of hepatitis C virus assembly, maturation, degradation, and secretion. Journal of Virology 2008, 82:2120-2129.
8. Gastaminza P., Kapadia S.B., Chisari F.V. Differential biophysical properties of infectious intracellular and secreted hepatitis C virus particles. Journal of Virology 2006.
9. Gentzsch J., Brohm C., Steinmann E., Friesland M., Menzel N., Vieyres G., Perin P.M., Frentzen A., Kaderali L., Pietschmann T. Hepatitis C virus p7 is critical for capsid assembly and envelopment. PLoS Pathogens 2013, 9:e1003355.
10. Gottwein J.M., Jensen T.B., Mathiesen C.K., Meuleman P., Serre S.B., Lademann J.B., Ghanem L., Scheel T.K., Leroux-Roels G., Bukh J. Development and application of hepatitis C reporter viruses with genotype 1 to 7 core-nonstructural protein 2 (NS2) expressing fluorescent proteins or luciferase in modified JFH1 NS5A. Journal of virology 2011, 85:8913-8928.
11. Griffin S., Stgelais C., Owsianka A.M., Patel A.H., Rowlands D., Harris M. Genotype-dependent sensitivity of hepatitis C virus to inhibitors of the p7 ion channel. Hepatology 2008, 48:1779-1790.
12. Griffin S.D., Beales L.P., Clarke D.S., Worsfold O., Evans S.D., Jaeger J., Harris M.P., Rowlands D.J. The p7 protein of hepatitis C virus forms an ion channel that is blocked by the antiviral drug, Amantadine. FEBS Letters 2003, 535:34-38.
13. Griffin S.D., Harvey R., Clarke D.S., Barclay W.S., Harris M., Rowlands D.J. A conserved basic loop in hepatitis C virus p7 protein is required for amantadine-sensitive ion channel activity in mammalian cells but is dispensable for localization to mitochondria. The Journal of General Virology 2004, 85:451-461.
14. Haid S., Pietschmann T., Pecheur E.I. Low pH-dependent hepatitis C virus membrane fusion depends on E2 integrity, target lipid composition, and density of virus particles. Journal of Biological Chemistry 2009, 284:17657-17667.
15. Jirasko V., Montserret R., Appel N., Janvier A., Eustachi L., Brohm C., Steinmann E., Pietschmann T., Penin F., Bartenschlager R. Structural and functional characterization of nonstructural protein 2 for its role in hepatitis C virus assembly. Journal of Biological Chemistry 2008, 283:28546-28562.
16. Jirasko V., Montserret R., Lee J.Y., Gouttenoire J., Moradpour D., Penin F., Bartenschlager R. Structural and functional studies of nonstructural protein 2 of the hepatitis C virus reveal its key role as organizer of virion assembly. PLoS Pathogens 2010, 6:e1001233.
17. Lavillette D., Bartosch B., Nourrisson D., Verney G., Cosset F.L., Penin F., Pecheur E.I Hepatitis C virus glycoproteins mediate low pH-dependent membrane fusion with liposomes. Journal of Biological Chemistry 2006, 281:3909-3917.
18. Li H., Atkins E., Bruckner J., McArdle S., Qiu W.C., Thomassen L.V., Scott J., Shuhart M.C., Livingston S., Townshend-Bulson L., McMahon B.J., Harris M., Griffin S., Gretch D.R. Genetic and functional heterogeneity of the hepatitis C virus p7 ion channel during natural chronic infection. Virology 2012, 423:30-37.
19. Luik P., Chew C., Aittoniemi J., Chang J., Wentworth P., Dwek R.A., Biggin P.C., Venien-Bryan C., Zitzmann N. The 3-dimensional structure of a hepatitis C virus p7 ion channel by electron microscopy. Proceedings of the National Academy of Sciences of the United States of America 2009, 106:12712-12716.
20. Ma Y., Anantpadma M., Timpe J.M., Shanmugam S., Singh S.M., Lemon S.M., Yi M. Hepatitis C virus NS2 protein serves as a scaffold for virus assembly by interacting with both structural and nonstructural proteins. Journal of virology 2011, 85:86-97.
21. Mohl B.P., Tedbury P.R., Griffin S., Harris M. Hepatitis C virus-induced autophagy is independent of the unfolded protein response. Journal of virology 2012, 86:10724-10732.
22. OuYang B., Xie S., Berardi M.J., Zhao X., Dev J., Yu W., Sun B., Chou J.J. Unusual architecture of the p7 channel from hepatitis C virus. Nature 2013, 498:521-525.
23. Pavlovic D., Neville D.C., Argaud O., Blumberg B., Dwek R.A., Fischer W.B., Zitzmann N. The hepatitis C virus p7 protein forms an ion channel that is inhibited by long-alkyl-chain iminosugar derivatives. Proceedings of the National Academy of Sciences of the United States of America 2003, 100:6104-6108.
24. Perez-Berna A.J., Guillen J., Moreno M.R., Bernabeu A., Pabst G., Laggner P., Villalain J. Identification of the membrane-active regions of hepatitis C virus p7 protein: biophysical characterization of the loop region. Journal of Biological Chemistry 2008, 283:8089-8101.
25. Pinto L.H., Dieckmann G.R., Gandhi C.S., Papworth C.G., Braman J., Shaughnessy M.A., Lear J.D., Lamb R.A., DeGrado W.F. A functionally defined model for the M2 proton channel of influenza A virus suggests a mechanism for its ion selectivity. Proceedings of the National Academy of Sciences of the United States of America 1997, 94:11301-11306.
26. Popescu C.I., Callens N., Trinel D., Roingeard P., Moradpour D., Descamps V., Duverlie G., Penin F., Heliot L., Rouille Y., Dubuisson J. NS2 protein of hepatitis C virus interacts with structural and non-structural proteins towards virus assembly. PLoS Pathogens 2011, 7:e1001278.
27. Premkumar A., Wilson L., Ewart G.D., Gage P.W. Cation-selective ion channels formed by p7 of hepatitis C virus are blocked by hexamethylene amiloride. FEBS Letters 2004, 557:99-103.
28. Saunier B., Triyatni M., Ulianich L., Maruvada P., Yen P., Kohn L.D. Role of the asialoglycoprotein receptor in binding and entry of hepatitis C virus structural proteins in cultured human hepatocytes. Journal of Virology 2003, 77:546-559.
29. Stapleford K.A., Lindenbach B.D. Hepatitis C virus NS2 coordinates virus particle assembly through physical interactions with the E1-E2 glycoprotein and NS3-NS4A enzyme complexes. Journal of Virology 2011, 85:1706-1717.
30. Steinhauer D.A., Wharton S.A., Skehel J.J., Wiley D.C., Hay A.J. Amantadine selection of a mutant influenza virus containing an acid-stable hemagglutinin glycoprotein: evidence for virus-specific regulation of the pH of glycoprotein transport vesicles. Proceedings of the National Academy of Sciences of the United States of America 1991, 88:11525-11529.
31. Steinmann E., Whitfield T., Kallis S., Dwek R.A., Zitzmann N., Pietschmann T., Bartenschlager R. Antiviral effects of amantadine and iminosugar derivatives against hepatitis C virus. Hepatology 2007, 46:330-338.
32. StGelais C., Foster T.L., Verow M., Atkins E., Fishwick C.W., Rowlands D., Harris M., Griffin S. Determinants of hepatitis C virus p7 ion channel function and drug sensitivity identified in vitro. Journal of Virology 2009, 83:7970-7981.
33. StGelais C., Tuthill T.J., Clarke D.S., Rowlands D.J., Harris M., Griffin S. Inhibition of hepatitis C virus p7 membrane channels in a liposome-based assay system. Antiviral Research 2007, 76:48-58.
34. Tedbury P., Welbourn S., Pause A., King B., Griffin S., Harris M. The subcellular localization of the hepatitis C virus non-structural protein NS2 is regulated by an ion channel-independent function of the p7 protein. Journal of General Virology 2011, 92:819-830.
35. Tscherne D.M., Jones C.T., Evans M.J., Lindenbach B.D., McKeating J.A., Rice C.M. Time- and temperature-dependent activation of hepatitis C virus for low-pH-triggered entry. Journal of Virology 2006, 80:1734-1741.
36. Vieyres G., Brohm C., Friesland M., Gentzsch J., Wolk B., Roingeard P., Steinmann E., Pietschmann T. Subcellular localization and function of an epitope-tagged p7 viroporin in hepatitis C virus-producing cells. Journal of Virology 2013, 87:1664-1678.
37. Wakita T., Pietschmann T., Kato T., Date T., Miyamoto M., Zhao Z., Murthy K., Habermann A., Krausslich H.G., Mizokami M., Bartenschlager R., Liang T.J. Production of infectious hepatitis C virus in tissue culture from a cloned viral genome. Nature Medicine 2005, 11:791-796.
38. Wetherill L.F., Holmes K.K., Verow M., Muller M., Howell G., Harris M., Fishwick C., Stonehouse N., Foster R., Blair G.E., Griffin S., Macdonald A. High-risk human papillomavirus E5 oncoprotein displays channel-forming activity sensitive to small-molecule inhibitors. Journal of Virology 2012, 86:5341-5351.
39. Wozniak A.L., Griffin S., Rowlands D., Harris M., Yi M., Lemon S.M., Weinman S.A. Intracellular proton conductance of the hepatitis C virus p7 protein and its contribution to infectious virus production. PLoS Pathogens 2010, 6:e1001087.
40. Yi M., Ma Y., Yates J., Lemon S.M. Compensatory mutations in E1, p7, NS2, and NS3 enhance yields of cell culture-infectious intergenotypic chimeric hepatitis C virus. Journal of Virology 2007, 81:629-638.