Hydrophobic and charged residues in the C-terminal arm of hepatitis C virus RNA-dependent RNA polymerase regulate initiation and elongation

Journal of Virology

Volumn 89, Issue 4, 2015, Pages 2052-2063

  Cherry, Amy L ^c   Dennis, Caitriona A ^a,b   Baron, Andrew ^d   Eisele, Leslie E ^a   Thommes, Pia A ^e   Jaeger, Joachim ^a,b  

^a WADSWORTH CENTER   (United States)

^b Division of Molecular Medicine   (United States)

^c UNIVERSITY OF WORCESTER   (United Kingdom)

^d UNIVERSITY OF LEEDS   (United Kingdom)

^e Euprotec Limited   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

ASPARAGINE; GLUTAMIC ACID; NUCLEOTIDE; PHENYLALANINE; RNA DIRECTED RNA POLYMERASE; URIDINE TRIPHOSPHATE; MUTANT PROTEIN;

AMINO ACID SUBSTITUTION; ARTICLE; BETA LOOP; BINDING AFFINITY; CARBOXY TERMINAL SEQUENCE; CONFORMATION; CONTROLLED STUDY; CRYSTAL STRUCTURE; ENZYME ACTIVE SITE; ENZYME ACTIVITY; HEPATITIS C VIRUS; HUMAN; HUMAN CELL; IN VITRO STUDY; NONHUMAN; PROTEIN STRUCTURE; REPLICON; SITE DIRECTED MUTAGENESIS; STRUCTURE ANALYSIS; TRANSCRIPTION ELONGATION; TRANSCRIPTION INITIATION; VIRUS REPLICATION; CHEMISTRY; ENZYMOLOGY; GENETICS; HEPACIVIRUS; METABOLISM; NUCLEOTIDE SEQUENCE; PHYSIOLOGY; PROTEIN CONFORMATION; X RAY CRYSTALLOGRAPHY;

HEPATITIS C VIRUS;

CRYSTALLOGRAPHY, X-RAY; DNA MUTATIONAL ANALYSIS; HEPACIVIRUS; HUMANS; MUTANT PROTEINS; PROTEIN CONFORMATION; RNA REPLICASE; TRANSCRIPTION ELONGATION, GENETIC; TRANSCRIPTION INITIATION, GENETIC; VIRUS REPLICATION;

EID: 84921657223     PISSN: 0022538X     EISSN: 10985514     Source Type: Journal    
DOI: 10.1128/JVI.01106-14     Document Type: Article

References (47)

1. Hong Z, Cameron CE, Walker MP, Castro C, Yao N, Lau JYN, Zhong W. 2001. A novel mechanism to ensure terminal initiation by hepatitis C virus NS5B polymerase. Virology 285:6-11. http://dx.doi.org/10.1006/viro.2001.0948.
2. Kao CC, Singh P, Eckert DJ. 2001. De novo initiation of viral RNAdependent RNA synthesis. Virology 287:251-260. http://dx.doi.org/10.1006/viro.2001.1039.
3. Jin Z, Leveque V, Ma H, Johnson KA, Klumpp K. 2012. Assembly, purification, and pre-steady-state kinetic analysis of active RNAdependent RNA polymerase elongation complex. J Biol Chem 287: 10674-10683. http://dx.doi.org/10.1074/jbc.M111.325530.
4. Ago H, Adachi T, Yoshida A, Yamamoto M, Habuka N, Yatsunami K, Miyano M. 1999. Crystal structure of the RNA-dependent RNA polymerase of hepatitis C virus. Structure 7:1417-1426. http://dx.doi.org/10.1016/S0969-2126(00)80031-3.
5. Lesburg CA, Cable MB, Ferrari E, Hong Z, Mannarino AF, Weber PC. 1999. Crystal structure of the RNA-dependent RNA polymerase from hepatitis C virus reveals a fully encircled active site. Nat Struct Biol 6:937-934. http://dx.doi.org/10.1038/13305.
6. Bressanelli S, Tomei L, Rey FA, De Francesco R. 2002. Structural analysis of the hepatitis C virus RNA polymerase in complex with ribonucleotides. J Virol 76:3482-3492. http://dx.doi.org/10.1128/JVI.76.7.3482-3492.2002.
7. O'Farrell D, Trowbridge R, Rowlands D, Jager J. 2003. Substrate complexes of hepatitis C virus RNA polymerase (HCV-J4): structural evidence for nucleotide import and de novo initiation. J Mol Biol 326:1025-1035. http://dx.doi.org/10.1016/S0022-2836(02)01439-0.
8. Butcher SJ, Grimes JM, Makeyev EV, Bamford DH, Stuart DI. 2001. A mechanism for initiation RNA-dependent RNA polymerisation. Nature 410:235-240. http://dx.doi.org/10.1038/35065653.
9. Tao Y, Farsetta DL, Nibert ML, Harrison SC. 2002. RNA synthesis in a cage-structural studies of reovirus polymerase lambda3. Cell 111:733-745. http://dx.doi.org/10.1016/S0092-8674(02)01110-8.
10. Ng KK, Cherney MM, Vazquez AL, Machin A, Alonso JM, Parra F, James MN. 2002. Crystal structures of active and inactive conformations of a caliciviral RNA-dependent RNA polymerase. J Biol Chem 277:1381-1387. http://dx.doi.org/10.1074/jbc.M109261200.
11. Ferrer-Orta C, Arias A, Perez-Luque R, Escarmis C, Domingo E, Verdaguer N. 2004. Structure of foot-and-mouth disease virus RNA-dependent RNA polymerase and its complex with a template-primer RNA. J Biol Chem 279:47212-47221. http://dx.doi.org/10.1074/jbc.M405465200.
12. Love RA, Maegley KA, Yu X, Ferre RA, Lingardo LK, Diehl W, Parge HE, Dragovich PS, Fuhrman SA. 2004. The crystal structure of the RNA-dependent RNA polymerase from human rhinovirus: a dual function target for common cold antiviral therapy. Structure 12:1533-1544. http://dx.doi.org/10.1016/j.str.2004.05.024.
13. Choi KH, Groarke JM, Young DC, Kuhn RJ, Smith JL, Pevear DC, Rossmann MG. 2004. The structure of the RNA-dependent RNA polymerase from bovine viral diarrhea virus establishes the role of GTP in de novo initiation. Proc Natl Acad Sci USA 101:4425-4430. http://dx.doi.org/10.1073/pnas.0400660101.
14. Biswal BK, Cherney MM, Wang M, Chan L, Yannopoulos CG, Bilimoria D, Nicolas O, Bedard J, James MNG. 2005. Crystal structures of the RNA-dependent RNA polymerase genotype 2a of hepatitis C virus reveal two conformations and suggest mechanisms of inhibition by nonnucleoside inhibitors. J Biol Chem 280:18202-18210. http://dx.doi.org/10.1074/jbc.M413410200.
15. Fullerton SWB, Blaschke M, Coutard B, Gebhardt J, Gorbalenya A, Canard B, Tucker PA, Rohayem J. 2007. Structural and functional characterization of sapovirus RNA-dependent RNA polymerase. J Virol 81: 1858-1871. http://dx.doi.org/10.1128/JVI.01462-06.
16. Ng KK, Pendas-Franco N, Rojo J, Boga JA, Machin A, Alonso JM, Parra F. 2004. Crystal structure of Norwalk virus polymerase reveals the carboxyl terminus in the active site cleft. J Biol Chem 279:16638-16645. http://dx.doi.org/10.1074/jbc.M400584200.
17. Malet H, Egloff MP, Selisko B, Butcher RE, Wright PJ, Roberts M, Gruez A, Sulzenbacher G, Vonrhein C, Bricogne G, Mackenzie JM, Khromykh AA, Davidson AD, Canard B. 2007. Crystal structure of the RNA polymerase domain of the West Nile virus non-structural protein 5. J Biol Chem 282: 10678-10689. http://dx.doi.org/10.1074/jbc.M607273200.
18. Yap TL, Xu T, Chen Y-L, Malet H, Egloff M-P, Canard B, Vasudevan SG, Lescar J. 2007. Crystal structure of the dengue virus RNA-dependent RNA polymerase catalytic domain at 1.85-angstrom resolution. J Virol 81:4753-4765. http://dx.doi.org/10.1128/JVI.02283-06.
19. Campagnola G, Weygandt M, Scoggin K, Peersen O. 2008. Crystal structure of coxsackievirus B3 3Dpol highlights functional importance of residue 5 in picornaviral polymerases. J Virol 82:9458-9464. http://dx.doi.org/10.1128/JVI.00647-08.
20. Gong P, Peersen OB. 2010. Structural basis for active site closure by the poliovirus RNA-dependent RNA polymerase. Proc Natl Acad Sci USA 107:22505-22510. http://dx.doi.org/10.1073/pnas.1007626107.
21. Alam I, Lee JH, Cho KJ, Han KR, Yang JM, Chung MS, Kim KH. 2012. Crystal structures of murine norovirus-1 RNA-dependent RNA polymerase in complex with 2-thiouridine or ribavirin. Virology 426:143-151. http://dx.doi.org/10.1016/j.virol.2012.01.016.
22. Takeshita D, Tomita K. 2012. Molecular basis for RNA polymerization by Qβ replicase. Nat Struct Mol Biol 19:229-237. http://dx.doi.org/10.1038/nsmb.2204.
23. Wright S, Poranen MM, Bamford DH, Stuart DI, Grimes JM. 2012. Noncatalytic ions direct the RNA-dependentRNApolymerase of bacterial double-stranded RNA virus ϕ6 from de novo initiation to elongation. J Virol 86:2837-2849. http://dx.doi.org/10.1128/JVI.05168-11.
24. Noble CG, Lim SP, Chen YL, Liew CW, Yap L, Lescar J, Shi P-Y. 2013. Conformational flexibility of the dengue virus RNA-dependent RNA polymerase revealed by a complex with an inhibitor. J Virol 87:5291-5295. http://dx.doi.org/10.1128/JVI.00045-13.
25. Bahar MW, Sarin LP, Graham SC, Pang J, Bamford DH, Stuart DI, Grimes JM. 2013. Structure of a VP1-VP3 complex suggests how birnaviruses package the VP1 polymerase. J Virol 87:3229-3236. http://dx.doi.org/10.1128/JVI.02939-12.
26. Chinnaswamy S, Yarbrough I, Palaninathan S, Ranjith-Kumar CT, Vijayaraghavan V, Demeler B, Lemon SM, Sacchettini JC, Kao CC. 2008. A locking mechanism regulates RNA synthesis and host protein interaction by the hepatitis C virus polymerase. J Biol Chem 283:20535-20546. http://dx.doi.org/10.1074/jbc.M801490200.
27. Adachi T, Ago H, Habuka N, Okuda K, Komatsu M, Ikeda S, Yatsunami K. 2002. The essential role of C-terminal residues in regulating the activity of hepatitis C virus RNA-dependent RNA polymerase. Biochim Biophys Acta 1601:38-48. http://dx.doi.org/10.1016/S1570-9639(02)00433-8.
28. Cheney IW, Naim S, Lai VCH, Dempsey S, Bellows D, Walker MP, Shim JH, Horscroft N, Hong Z, Zhong W. 2002. Mutations in NS5B polymerase of hepatitis C virus: impacts on in vitro enzymatic activity and viral RNA replication in the subgenomic replicon cell culture. Virology 297:298-306. http://dx.doi.org/10.1006/viro.2002.1461.
29. Leveque VJ-P, Johnson RB, Parsons S, Ren J, Xie C, Zhang F, Wang QM. 2003. Identification of a C-terminal regulatory motif in hepatitis C virus RNA-dependent RNA polymerase: structural and biochemical analysis. J Virol 77:9020-9028. http://dx.doi.org/10.1128/JVI.77.16.9020-9028.2003.
30. Ranjith-Kumar CT, Gutshall L, Sarisky RT, Kao CC. 2003. Multiple interactions within the hepatitis C virus RNA polymerase repress primerdependent RNA synthesis. J Mol Biol 330:675-685. http://dx.doi.org/10.1016/S0022-2836(03)00613-2.
31. Nakabayashi H, Taketa K, Miyano K, Yamane T, Sato J. 1982. Growth of human hepatoma cells lines with differentiated functions in chemically defined medium. Cancer Res 42:3858-3863.
32. Friebe P, Lohmann V, Krieger N, Bartenschlager R. 2001. Sequences in the 5' nontranslated region of hepatitis C virus required for RNA replication. J Virol 75:12047-12057. http://dx.doi.org/10.1128/JVI.75.24.12047-12057.2001.
33. Otwinowski Z, Minor W. 1997. Processing of X-ray diffraction data collected in oscillation mode. Methods Enzymol 276:307-326.
34. CCP4. 1994. The CCP4 Suite: programs for protein crystallography. Acta Crystallogr D Biol Crystallogr 50:760-763. http://dx.doi.org/10.1107/S0907444994003112.
35. Zwart PH, Afonine PV, Grosse-Kunstleve RW, Hung LW, Ioerger TR, McCoy AJ, McKee E, Moriarty NW, Read RJ, Sacchettini JC, Sauter NK, Storoni LC, Terwilliger TC, Adams PD. 2008. Automated structure solution with the PHENIX suite. Methods Mol Biol 426:419-435. http://dx.doi.org/10.1007/978-1-60327-058-8_28.
36. Laskowski RA, MacArthur MW, Moss DS, Thornton JM. 1993. PROCHECK: a program to check the stereochemical quality of protein structures. J Appl Crystallogr 26:283-291. http://dx.doi.org/10.1107/S0021889892009944.
37. Schuck P. 2000. Size-distribution analysis of macromolecules by sedimentation velocity ultracentrifugation and Lamm equation modeling. Biophys J 78:1606-1619. http://dx.doi.org/10.1016/S0006-3495(00)76713-0.
38. Doublié S, Tabor S, Long AM, Richardson CC, Ellenberger T. 1998. Crystal structure of a bacteriophage T7 DNA replication complex. Nature 391:251-258. http://dx.doi.org/10.1038/34593.
39. Huang H, Chopra R, Verdine GL, Harrison SC. 1998. Structure of a covalently trapped catalytic complex of HIV reverse transcriptase: implications for drug resistance. Science 282:1669-1675. http://dx.doi.org/10.1126/science.282.5394.1669.
40. Tuplin A, Evans DJ, Simmonds P. 2004. Detailed mapping of RNA secondary structures in core and NS5B-encoding region sequences of hepatitis C virus by RNase cleavage and novel bioinformatic prediction methods. J Gen Virol 85:3037-3047. http://dx.doi.org/10.1099/vir.0.80141-0.
41. You S, Stump DD, Branch AD, Rice CM. 2004. A cis-acting replication element in the sequence encoding the NS5B RNA-dependent RNA polymerase is required for hepatitis C virus RNA replication. J Virol 78:1352-1366. http://dx.doi.org/10.1128/JVI.78.3.1352-1366.2004.
42. Lee H, Shin H, Wimmer E, Paul AV. 2004. cis-Acting RNA signals in the NS5B C-terminal coding sequence of the hepatitis C virus genome. J Virol 78:10865-10877. http://dx.doi.org/10.1128/JVI.78.20.10865-10877.2004.
43. Smith DB, Simmonds P. 1997. Characteristics of nucleotide substitution in the hepatitis C virus genome: constraints on sequence change in coding regions at both ends of the genome. J Mol Evol 45:238-246. http://dx.doi.org/10.1007/PL00006226.
44. Ferron F, Bussetta C, Dutartre H, Canard B. 2005. The modeled structure of the RNA dependent RNA polymerase of GBV-C virus suggests a role for motif E in Flaviviridae RNA polymerases. BMC Bioinformatics 6:255. http://dx.doi.org/10.1186/1471-2105-6-255.
45. Harrus D, Ahmed-El-Sayed N, Simister PC, Miller S, Triconnet M, Hagedorn CH, Mahias K, Rey FA, Astier-Gin T, Bressanelli S. 2010. Further insights into the roles of GTP and the C terminus of the hepatitis C virus polymerase in the initiation of RNA synthesis. J Biol Chem 285: 32906-32918. http://dx.doi.org/10.1074/jbc.M110.151316.
46. Vives-Adrian L, Lujan C, Oliva B, van der Linden L, Selisko B, Coutard B, Canard B, van Kuppeveld FJ, Ferrer-Orta C, Verdaguer N. 2014. The crystal structure of a cardiovirus RNA-dependent RNA polymerase reveals an unusual conformation of the polymerase active site. J Virol 88: 5595-5607. http://dx.doi.org/10.1128/JVI.03502-13.
47. Boyce SE, Tirunagari N, Niedziela-Majka A, Perry J, Wong M, Kan E, Lagpacan L, Barauskas O, Hung M, Fenaux M, Appleby T, Watkins WJ, Schmitz U, Sakowicz R. 2014. Structural and regulatory elements of HCV NS5B polymerase-β-loop and C-terminal tail-are required for activity of allosteric thumb site II inhibitors. PLoS One 9:e84808. http://dx.doi.org/10.1371/journal.pone.0084808.