Structure-function relationships underlying the replication fidelity of viral RNA-dependent RNA polymerases

Journal of Virology

Volumn 89, Issue 1, 2015, Pages 275-286

  Campagnola, Grace ^a   McDonald, Seth ^a   Beaucourt, Stéphanie ^b   Vignuzzi, Marco ^b   Peersen, Olve B ^a  

^a Department of Environmental and Radiological Health Sciences   (United States)

^b INSTITUT PASTEUR   (France)

Author keywords

[No Author keywords available]

Indexed keywords

ELONGATION FACTOR; RNA DIRECTED RNA POLYMERASE; MUTANT PROTEIN; VIRUS RNA;

AMINO TERMINAL SEQUENCE; ARTICLE; CHEMICAL ANALYSIS; CONSENSUS SEQUENCE; COXSACKIE VIRUS B3; CRYSTAL STRUCTURE; ENTEROVIRUS 71; ENZYME ACTIVE SITE; ENZYME STRUCTURE; FLOW KINETICS; IN VIVO STUDY; MICHAELIS MENTEN KINETICS; MOLECULAR DYNAMICS; NONHUMAN; NUCLEAR MAGNETIC RESONANCE; POLIOMYELITIS VIRUS; PROTEIN DOMAIN; PROTEIN FUNCTION; PROTEIN MOTIF; RNA TRANSLATION; TISSUE CULTURE; VIROGENESIS; VIRUS GENOME; VIRUS MORPHOLOGY; VIRUS MUTATION; VIRUS REPLICATION; CHEMICAL STRUCTURE; ENTEROVIRUS B; ENZYMOLOGY; GENETICS; HUMAN; KINETICS; METABOLISM; NUCLEOTIDE SEQUENCE; PHYSIOLOGY; PROTEIN CONFORMATION; PROTEIN TERTIARY STRUCTURE; X RAY CRYSTALLOGRAPHY;

COXSACKIEVIRUS; POLIOVIRUS; RNA VIRUSES;

CRYSTALLOGRAPHY, X-RAY; DNA MUTATIONAL ANALYSIS; ENTEROVIRUS B, HUMAN; HUMANS; KINETICS; MODELS, MOLECULAR; MUTANT PROTEINS; PROTEIN CONFORMATION; PROTEIN STRUCTURE, TERTIARY; RNA REPLICASE; RNA, VIRAL; VIRUS REPLICATION;

EID: 84919427801     PISSN: 0022538X     EISSN: 10985514     Source Type: Journal    
DOI: 10.1128/JVI.01574-14     Document Type: Article

References (48)

1. Ferrer-Orta C, Arias A, Escarmis C, Verdaguer N. 2006. A comparison of viral RNA-dependent RNA polymerases. Curr Opin Struct Biol 16:27-34. http://dx.doi.org/10.1016/j.sbi.2005.12.002.
2. Ng KK, Arnold JJ, Cameron CE. 2008. Structure-function relationships among RNA-dependent RNA polymerases. Curr Top Microbiol Immunol 320:137-156. http://dx.doi.org/10.1007/978-3-540-75157-1_7.
3. Lescar J, Canard B. 2009. RNA-dependent RNA polymerases from flaviviruses and Picornaviridae. Curr Opin Struct Biol 19:759-767. http://dx.doi.org/10.1016/j.sbi.2009.10.011.
4. Mosley RT, Edwards TE, Murakami E, Lam AM, Grice RL, Du J, Sofia MJ, Furman PA, Otto MJ. 2012. Structure of HCV polymerase in complex with primer-template RNA. J Virol 86:6503-6511. http://dx.doi.org/10.1128/JVI.00386-12.
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 6:937-943. http://dx.doi.org/10.1038/13305.
6. 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 theRNApolymerase domain of the West Nile virus non-structural protein 5. J Biol Chem. 282: 10678-10689. http://dx.doi.org/10.1074/jbc.M607273200.
7. Yap TL, Xu T, Chen YL, Malet H, Egloff MP, Canard B, Vasudevan SG, Lescar J. 2007. Crystal structure of the dengue virus RNA-dependentRNA polymerase catalytic domain at 1.85-angstrom resolution. J Virol 81: 4753-4765. http://dx.doi.org/10.1128/JVI.02283-06.
8. Lu G, Gong P. 2013. Crystal structure of the full-length Japanese encephalitis virus NS5 reveals a conserved methyltransferase-polymerase interface. PLoS Pathog 9:e1003549. http://dx.doi.org/10.1371/journal.ppat.1003549.
9. 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.
10. Gong P, Kortus MG, Nix JC, Davis RE, Peersen OB. 2013. Structures of coxsackievirus, rhinovirus, and poliovirus polymerase elongation complexes solved by engineering RNA mediated crystal contacts. PLoS One 8:e60272. http://dx.doi.org/10.1371/journal.pone.0060272.
11. Zamyatkin DF, Parra F, Alonso JM, Harki DA, Peterson BR, Grochulski P, Ng KK. 2008. Structural insights into mechanisms of catalysis and inhibition in Norwalk virus polymerase. J Biol Chem 283:7705-7712. http://dx.doi.org/10.1074/jbc.M709563200.
12. Salas-Rojas M, Galvez-Romero G, Anton-Palma B, Acevedo R, Blanco-Favela F, Aguilar-Setien A. 2014. The coelomic fluid of the sea urchin Tripneustes depressus shows antiviral activity against Suid herpesvirus type 1 (SHV-1) and rabies virus (RV). Fish Shellfish Immunol 36:158-163. http://dx.doi.org/10.1016/j.fsi.2013.10.025.
13. Acevedo A, Brodsky L, Andino R. 2014. Mutational and fitness landscapes of an RNA virus revealed through population sequencing. Nature 505:686-690. http://dx.doi.org/10.1038/nature12861.
14. Lauring AS, Frydman J, Andino R. 2013. The role of mutational robustness in RNA virus evolution. Nat Rev Microbiol 11:327-336. http://dx.doi.org/10.1038/nrmicro3003.
15. Graci JD, Gnadig NF, Galarraga JE, Castro C, Vignuzzi M, Cameron CE. 2012. Mutational robustness of an RNA virus influences sensitivity to lethal mutagenesis. J Virol 86:2869-2873. http://dx.doi.org/10.1128/JVI.05712-11.
16. Borderia AV, Stapleford KA, Vignuzzi M. 2011. RNA virus population diversity: implications for inter-species transmission. Curr Opin Virol 1:643-648. http://dx.doi.org/10.1016/j.coviro.2011.09.012.
17. Pfeiffer JK, Kirkegaard K. 2005. Increased fidelity reduces poliovirus fitness and virulence under selective pressure in mice. PLoS Pathog 1:e11. http://dx.doi.org/10.1371/journal.ppat.0010011.
18. Pfeiffer JK, Kirkegaard K. 2006. Bottleneck-mediated quasispecies restriction during spread of an RNA virus from inoculation site to brain. Proc Natl Acad Sci USA 103:5520-5525. http://dx.doi.org/10.1073/pnas.0600834103.
19. Gnadig NF, Beaucourt S, Campagnola G, Borderia AV, Sanz-Ramos M, Gong P, Blanc H, Peersen OB, Vignuzzi M. 2012. Coxsackievirus B3 mutator strains are attenuated in vivo. Proc Natl Acad Sci USA 109: E2294-E2303. http://dx.doi.org/10.1073/pnas.1204022109.
20. Arnold JJ, Vignuzzi M, Stone JK, Andino R, Cameron CE. 2005. Remote site control of an active site fidelity checkpoint in a viral RNA-dependent RNA polymerase. J Biol Chem 280:25706-25716. http://dx.doi.org/10.1074/jbc.M503444200.
21. Meng T, Kwang J. 2014. Attenuation of human enterovirus 71 highreplication-fidelity variants in AG129 mice. J Virol 88:5803-5815. http://dx.doi.org/10.1128/JVI.00289-14.
22. Coffey LL, Beeharry Y, Borderia AV, Blanc H, Vignuzzi M. 2011. Arbovirus high fidelity variant loses fitness in mosquitoes and mice. Proc Natl Acad Sci USA 108:16038-16043. http://dx.doi.org/10.1073/pnas.1111650108.
23. Rozen-Gagnon K, Stapleford KA, Mongelli V, Blanc H, Failloux AB, Saleh MC, Vignuzzi M. 2014. Alphavirus mutator variants present hostspecific defects and attenuation in mammalian and insect models. PLoS Pathog 10:e1003877. http://dx.doi.org/10.1371/journal.ppat.1003877.
24. Yang X, Welch JL, Arnold JJ, Boehr DD. 2010. Long-range interaction networks in the function and fidelity of poliovirus RNA-dependent RNA polymerase studied by nuclear magnetic resonance. Biochemistry 49: 9361-9371. http://dx.doi.org/10.1021/bi100833r.
25. Moustafa IM, Shen H, Morton B, Colina CM, Cameron CE. 2011. Molecular dynamics simulations of viral RNA polymerases link conserved and correlated motions of functional elements to fidelity. J Mol Biol 410: 159-181. http://dx.doi.org/10.1016/j.jmb.2011.04.078.
26. Gohara DW, Ha CS, Kumar S, Ghosh B, Arnold JJ, Wisniewski TJ, Cameron CE. 1999. Production of "authentic" poliovirus RNAdependent RNA polymerase (3D(pol)) by ubiquitin-protease-mediated cleavage in Escherichia coli. Protein Expr Purif 17:128-138. http://dx.doi.org/10.1006/prep.1999.1100.
27. Campagnola G, Weygandt M, Scoggin K, Peersen O. 2008. Crystal structure of coxsackievirus B3 3Dpol highlights the functional importance of residue 5 in picornavirus polymerases. J Virol 82:9458-9464. http://dx.doi.org/10.1128/JVI.00647-08.
28. Thompson AA, Peersen OB. 2004. Structural basis for proteolysisdependent activation of the poliovirus RNA-dependent RNA polymerase. EMBO J 23:3462-3471. http://dx.doi.org/10.1038/sj.emboj.7600357.
29. Gong P, Campagnola G, Peersen OB. 2009. A quantitative stopped-flow fluorescence assay for measuring polymerase elongation rates. Anal Biochem 391:45-55. http://dx.doi.org/10.1016/j.ab.2009.04.035.
30. Hobdey SE, Kempf BJ, Steil BP, Barton DJ, Peersen OB. 2010. Poliovirus polymerase residue 5 plays a critical role in elongation complex stability. J Virol 84:8072-8084. http://dx.doi.org/10.1128/JVI.02147-09.
31. Morin A, Eisenbraun B, Key J, Sanschagrin PC, Timony MA, Ottaviano M, Sliz P. 2013. Collaboration gets the most out of software. eLife 2:e01456. http://dx.doi.org/10.7554/eLife.01456.
32. Pfeiffer JK, Kirkegaard K. 2003. A single mutation in poliovirus RNAdependent RNA polymerase confers resistance to mutagenic nucleotide analogs via increased fidelity. Proc Natl Acad Sci USA 100:7289-7294. http://dx.doi.org/10.1073/pnas.1232294100.
33. Korboukh VK, Lee CA, Acevedo A, Vignuzzi M, Xiao Y, Arnold JJ, Hemperly S, Graci JD, August A, Andino R, Cameron CE. 2014. RNA virus population diversity: an optimum for maximal fitness and virulence. J Biol Chem 289:29531-29544. http://dx.doi.org/10.1074/jbc.M114.592303.
34. Ward CD, Stokes MA, Flanegan JB. 1988. Direct measurement of the poliovirus RNA polymerase error frequency in vitro. J Virol 62:558-562.
35. Lauring AS, Acevedo A, Cooper SB, Andino R. 2012. Codon usage determines the mutational robustness, evolutionary capacity, and virulence of an RNA virus. Cell Host Microbe 12:623-632. http://dx.doi.org/10.1016/j.chom.2012.10.008.
36. Yang X, Smidansky ED, Maksimchuk KR, Lum D, Welch JL, Arnold JJ, Cameron CE, Boehr DD. 2012. Motif D of viral RNA-dependent RNA polymerases determines efficiency and fidelity of nucleotide addition. Structure 20:1519-1527. http://dx.doi.org/10.1016/j.str.2012.06.012.
37. Shen H, Sun H, Li G. 2012. What is the role of motif D in the nucleotide incorporation catalyzed by the RNA-dependent RNA polymerase from poliovirus?. PLoS Comput Biol 8:e1002851. http://dx.doi.org/10.1371/journal.pcbi.1002851.
38. Castro C, Smidansky ED, Arnold JJ, Maksimchuk KR, Moustafa I, Uchida A, Gotte M, Konigsberg W, Cameron CE. 2009. Nucleic acid polymerases use a general acid for nucleotidyl transfer. Nat Struct Mol Biol 16:212-218. http://dx.doi.org/10.1038/nsmb.1540.
39. 2+. Biochemistry 43:5126-5137. http://dx.doi.org/10.1021/bi035212y.
40. Kortus MG, Kempf BJ, Haworth KG, Barton DJ, Peersen OB. 2012. A template RNA entry channel in the fingers domain of the poliovirus polymerase. J Mol Biol 417:263-278. http://dx.doi.org/10.1016/j.jmb.2012.01.049.
41. Weeks SA, Lee CA, Zhao Y, Smidansky ED, August A, Arnold J J, Cameron CE. 2012. A polymerase mechanism-based strategy for viral attenuation and vaccine development. J Biol Chem 287:31618-31622. http://dx.doi.org/10.1074/jbc.C112.401471.
42. Crotty S, Cameron CE, Andino R. 2001. RNA virus error catastrophe: direct molecular test by using ribavirin. Proc Natl Acad SciUS A 98:6895-6900. http://dx.doi.org/10.1073/pnas.111085598.
43. Sadeghipour S, Bek EJ, McMinn PC. 2013. Ribavirin-resistant mutants of human enterovirus 71 express a high replication fidelity phenotype during growth in cell culture. J Virol 87:1759-1769. http://dx.doi.org/10.1128/JVI.02139-12.
44. Arias A, Arnold JJ, Sierra M, Smidansky ED, Domingo E, Cameron CE. 2008. Determinants of RNA-dependent RNA polymerase (in)fidelity revealed by kinetic analysis of the polymerase encoded by a foot-and-mouth disease virus mutant with reduced sensitivity to ribavirin. J Virol 82: 12346-12355. http://dx.doi.org/10.1128/JVI.01297-08.
45. Sierra M, Airaksinen A, Gonzalez-Lopez C, Agudo R, Arias A, Domingo E. 2007. Foot-and-mouth disease virus mutant with decreased sensitivity to ribavirin: implications for error catastrophe. J Virol 81:2012-2024. http://dx.doi.org/10.1128/JVI.01606-06.
46. Pugachev KV, Guirakhoo F, Ocran SW, Mitchell F, Parsons M, Penal C, Girakhoo S, Pougatcheva SO, Arroyo J, Trent DW, Monath TP. 2004. High fidelity of yellow fever virus RNA polymerase. J Virol 78:1032-1038. http://dx.doi.org/10.1128/JVI.78.2.1032-1038.2004.
47. Jin Z, Deval J, Johnson KA, Swinney DC. 2011. Characterization of the elongation complex of dengue virus RNA polymerase: assembly, kinetics of nucleotide incorporation, and fidelity. J Biol Chem 286:2067-2077. http://dx.doi.org/10.1074/jbc.M110.162685.
48. Van Slyke GA, Ciota AT, Willsey GG, Jaeger J, Shi PY, Kramer LD. 2012. Point mutations in the West Nile virus (Flaviviridae; Flavivirus) RNA-dependent RNA polymerase alter viral fitness in a host-dependent manner in vitro and in vivo. Virology 427:18-24. http://dx.doi.org/10.1016/j.virol.2012.01.036.