Novel mutations in a tissue culture-adapted hepatitis c virus strain improve infectious-virus stability and markedly enhance infection kinetics

Journal of Virology

Volumn 85, Issue 8, 2011, Pages 3978-3985

  Pokrovskii, Maria V ^a   Bush, Caroline O ^a   Beran, Rudolf K F ^a   Robinson, Margaret F ^a   Cheng, Guofeng ^a   Tirunagari, Neeraj ^a   Fenaux, Martijn ^a   Greenstein, Andrew E ^a   Zhong, Weidong ^a   Delaney IV, William E ^a   Paulson, Matthew S ^a  

^a GILEAD SCIENCES   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

NONSTRUCTURAL PROTEIN 3; NONSTRUCTURAL PROTEIN 4A; VIRUS PROTEIN;

ADAPTATION; AMINO ACID SUBSTITUTION; ARTICLE; CONTROLLED STUDY; HEPATITIS C VIRUS; NONHUMAN; PHENOTYPE; PRIORITY JOURNAL; THERMOSTABILITY; TISSUE CULTURE; VIROGENESIS; VIRUS ASSEMBLY; VIRUS INFECTIVITY; VIRUS MUTATION; VIRUS PARTICLE; VIRUS RELEASE; VIRUS REPLICATION;

CELL LINE; DNA MUTATIONAL ANALYSIS; HEPACIVIRUS; HUMANS; MUTATION; MUTATION, MISSENSE; SERIAL PASSAGE; VIRAL CORE PROTEINS; VIRAL LOAD; VIRAL NONSTRUCTURAL PROTEINS; VIRUS CULTIVATION; VIRUS REPLICATION;

HEPATITIS C VIRUS;

EID: 79952822301     PISSN: 0022538X     EISSN: 10985514     Source Type: Journal    
DOI: 10.1128/JVI.01760-10     Document Type: Article

References (47)

1. Bartenschlager, R. 2006. Hepatitis C virus molecular clones: from cDNA to infectious virus particles in cell culture. Curr. Opin. Microbiol. 9:416-422.
2. Bartenschlager, R., and T. Pietschmann. 2005. Efficient hepatitis C virus cell culture system: what a difference the host cell makes. Proc. Natl. Acad. Sci. U. S. A. 102:9739-9740.
3. Bungyoku, Y., et al. 2009. Efficient production of infectious hepatitis C virus with adaptive mutations in cultured hepatoma cells. J. Gen. Virol. 90:1681-1691.
4. Delgrange, D., et al. 2007. Robust production of infectious viral particles in Huh-7 cells by introducing mutations in hepatitis C virus structural proteins. J. Gen. Virol. 88:2495-2503.
5. Deng, L., et al. 2008. Hepatitis C virus infection induces apoptosis through a Bax-triggered, mitochondrion-mediated, caspase 3-dependent pathway. J. Virol. 82:10375-10385. (Pubitemid 352691171)
6. Dentzer, T. G., I. C. Lorenz, M. J. Evans, and C. M. Rice. 2009. Determinants of the hepatitis C virus nonstructural protein 2 protease domain required for production of infectious virus. J. Virol. 83:12702-12713.
7. Eisenberg, D. C., and D. M. Crothers. 1979. Physical chemistry with applications to life sciences. Addison Wesley Longman, Reading, MA.
8. Farquhar, M. J., et al. 2008. Protein kinase A-dependent step(s) in hepatitis C virus entry and infectivity. J. Virol. 82:8797-8811.
9. Gottwein, J. M., et al. 2007. Robust hepatitis C genotype 3a cell culture releasing adapted intergenotypic 3a/2a (S52/JFH1) viruses. Gastroenterology 133:1614-1626. (Pubitemid 350029736)
10. Gottwein, J. M., et al. 2009. Development and characterization of hepatitis C virus genotype 1-7 cell culture systems: role of CD81 and scavenger receptor class B type I and effect of antiviral drugs. Hepatology 49:364-377.
11. Gouttenoire, J., F. Penin, and D. Moradpour. 2010. Hepatitis C virus nonstructural protein 4B: a journey into unexplored territory. Rev. Med. Virol. 20:117-129.
12. Jirasko, V., et al. 2008. Structural and functional characterization of nonstructural protein 2 for its role in hepatitis C virus assembly. J. Biol. Chem. 283:28546-28562.
13. Jones, C. T., C. L. Murray, D. K. Eastman, J. Tassello, and C. M. Rice. 2007. Hepatitis C virus p7 and NS2 proteins are essential for production of infectious virus. J. Virol. 81:8374-8383.
14. Jones, D. M., A. H. Patel, P. Targett-Adams, and J. McLauchlan. 2009. The hepatitis C virus NS4B protein can trans-complement viral RNA replication and modulates production of infectious virus. J. Virol. 83:2163-2177.
15. Kato, T., et al. 2008. Hepatitis C virus JFH-1 strain infection in chimpanzees is associated with low pathogenicity and emergence of an adaptive mutation. Hepatology 48:732-740.
16. Kato, T., et al. 2007. Production of infectious hepatitis C virus of various genotypes in cell cultures. J. Virol. 81:4405-4411. (Pubitemid 46668637)
17. Kaul, A., I. Woerz, P. Meuleman, G. Leroux-Roels, and R. Bartenschlager. 2007. Cell culture adaptation of hepatitis C virus and in vivo viability of an adapted variant. J. Virol. 81:13168-13179.
18. Kaul, A., I. Worz, and R. Bartenschlager. 2009. Adaptation of the hepatitis C virus to cell culture. Methods Mol. Biol. 510:361-372.
19. Klein, K. C., S. R. Dellos, and J. R. Lingappa. 2005. Identification of residues in the hepatitis C virus core protein that are critical for capsid assembly in a cell-free system. J. Virol. 79:6814-6826.
20. Koutsoudakis, G., E. Herrmann, S. Kallis, R. Bartenschlager, and T. Pietschmann. 2007. The level of CD81 cell surface expression is a key determinant for productive entry of hepatitis C virus into host cells. J. Virol. 81:588-598. (Pubitemid 46067886)
21. Lindenbach, B. D. 2009. Measuring HCV infectivity produced in cell culture and in vivo. Methods Mol. Biol. 510:329-336.
22. Lindenbach, B. D., et al. 2005. Complete replication of hepatitis C virus in cell culture. Science 309:623-626. (Pubitemid 41033648)
23. Lindenbach, B. D., et al. 2006. Cell culture-grown hepatitis C virus is infectious in vivo and can be recultured in vitro. Proc. Natl. Acad. Sci. U. S. A. 103:3805-3809.
24. Lohmann, V., et al. 1999. Replication of subgenomic hepatitis C virus RNAs in a hepatoma cell line. Science 285:110-113. (Pubitemid 29307577)
25. Masaki, T., et al. 2008. Interaction of hepatitis C virus nonstructural protein 5A with core protein is critical for the production of infectious virus particles. J. Virol. 82:7964-7976.
26. Mateu, G., R. O. Donis, T. Wakita, J. Bukh, and A. Grakoui. 2008. Intragenotypic JFH1 based recombinant hepatitis C virus produces high levels of infectious particles but causes increased cell death. Virology 376:397-407.
27. Murray, C. L., C. T. Jones, J. Tassello, and C. M. Rice. 2007. Alanine scanning of the hepatitis C virus core protein reveals numerous residues essential for production of infectious virus. J. Virol. 81:10220-10231.
28. Nakai, K., et al. 2006. Oligomerization of hepatitis C virus core protein is crucial for interaction with the cytoplasmic domain of E1 envelope protein. J. Virol. 80:11265-11273. (Pubitemid 44706566)
29. Paintsil, E., H. He, C. Peters, B. D. Lindenbach, and R. Heimer. 2010. Survival of hepatitis C virus in syringes: implication for transmission among injection drug users. J. Infect. Dis. 202:984-990.
30. Paulson, M. S., et al. 2009. Comparison of HCV NS3 protease and NS5B polymerase inhibitor activity in 1a, 1b and 2a replicons and 2a infectious virus. Antiviral Res. 83:135-142.
31. Phan, T., R. K. Beran, C. Peters, I. C. Lorenz, and B. D. Lindenbach. 2009. Hepatitis C virus NS2 protein contributes to virus particle assembly via opposing epistatic interactions with the E1-E2 glycoprotein and NS3-NS4A enzyme complexes. J. Virol. 83:8379-8395.
32. Pietschmann, T., et al. 2006. Construction and characterization of infectious intragenotypic and intergenotypic hepatitis C virus chimeras. Proc. Natl. Acad. Sci. U. S. A. 103:7408-7413.
33. Podevin, P., A. Carpentier, V. Pene, L. Aoudjehane, M. Carriere, S. Zaidi, C. Hernandez, V. Calle, J. F. Meritet, O. Scatton, M. Dreux, F. L. Cosset, T. Wakita, R. Bartenschlager, S. Demignot, F. Conti, A. R. Rosenberg, and Y. Calmus. 2010. Production of infectious hepatitis C virus in primary cultures of human adult hepatocytes. Gastroenterology 139:1355-1364.
34. Qu, L., L. K. McMullan, and C. M. Rice. 2001. Isolation and characterization of noncytopathic pestivirus mutants reveals a role for nonstructural protein NS4B in viral cytopathogenicity. J. Virol. 75:10651-10662.
35. Reed, L. J., and H. Muench. 1938. A simple method of estimating 50 percent end-points. Am. J. Hyg. 27:493-497.
36. Russell, R. S., et al. 2008. Advantages of a single-cycle production assay to study cell culture-adaptive mutations of hepatitis C virus. Proc. Natl. Acad. Sci. U. S. A. 105:4370-4375.
37. Scheel, T. K., et al. 2008. Development of JFH1-based cell culture systems for hepatitis C virus genotype 4a and evidence for cross-genotype neutralization. Proc. Natl. Acad. Sci. U. S. A. 105:997-1002.
38. Sekine-Osajima, Y., et al. 2008. Development of plaque assays for hepatitis C virus-JFH1 strain and isolation of mutants with enhanced cytopathogenicity and replication capacity. Virology 371:71-85.
39. Song, H., et al. 2010. Thermal stability and inactivation of hepatitis C virus grown in cell culture. Virol. J. 7:40.
40. Stapleford, K. A., and B. Lindenbach. 2011. Hepatitis C virus NS2 coordinates virus particle assembly through physical interactions with the E1-E2 glycoprotein and NS3-NS4A enzyme complexes. J. Virol. 85:1706-1717.
41. Wakita, T., et al. 2005. Production of infectious hepatitis C virus in tissue culture from a cloned viral genome. Nat. Med. 11:791-796.
42. Welbourn, S., et al. 2009. Investigation of a role for lysine residues in non-structural proteins 2 and 2/3 of the hepatitis C virus for their degradation and virus assembly. J. Gen. Virol. 90:1071-1080.
43. Yang, H., and W. E. Delaney IV. 2006. A novel fluorescence-based protease assay using the endogenous NS3/4A protease activity present in the total cell lysates of HCV replicon cells. J. Clin. Virol. 36:S109.
44. Yi, M., Y. Ma, J. Yates, and S. M. Lemon. 2007. Compensatory mutations in E1, p7, NS2, and NS3 enhance yields of cell culture-infectious intergenotypic chimeric hepatitis C virus. J. Virol. 81:629-638.
45. Yi, M., Y. Ma, J. Yates, and S. M. Lemon. 2009. Trans-complementation of an NS2 defect in a late step in hepatitis C virus (HCV) particle assembly and maturation. PLoS Pathog. 5:e1000403.
46. Zhong, J., et al. 2005. Robust hepatitis C virus infection in vitro. Proc. Natl. Acad. Sci. U. S. A. 102:9294-9299.
47. Zhong, J., et al. 2006. Persistent hepatitis C virus infection in vitro: coevolution of virus and host. J. Virol. 80:11082-11093. (Pubitemid 44706549)