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Structure of foot-and-mouth disease virus mutant polymerases with reduced sensitivity to ribavirin.

Ferrer-Orta C, Sierra M, Agudo R, de la Higuera I, Arias A, Pérez-Luque R, Escarmís C, Domingo E, Verdaguer N
J Virol 84 6188-99 (2010)
Related entries: 3klv, 3kmq, 3kms, 3kna

Cited: 44 times
EuropePMC logo PMID: 20392853

Abstract

Passage of poliovirus (PV) or foot-and-mouth disease virus (FMDV) in the presence of ribavirin selected for viruses with decreased sensitivity to R, which included different mutations in their polymerase (3D): G64S located in the finger subdomain in the case of PV and M296I located within loop beta9-alpha11 at the active site in the case of FMDV. To investigate why disparate substitutions were selected in two closely related 3Ds, we constructed FMDVs with a 3D that included either G62S (the equivalent replacement in FMDV of PV G64S), M296I, or both substitutions. G62S, but not M296I, inflicts upon FMDV a strong selective disadvantage which is partially compensated for by the substitution M296I. The corresponding mutant polymerases, 3D(G62S), 3D(M296I), and 3D(G62S-M296I), were analyzed functionally and structurally. G62S in 3D impairs RNA-binding, polymerization, and R monophosphate incorporation activities. The X-ray structures of the 3D(G62S)-RNA, 3D(M296I)-RNA, and 3D(G62S-M296I)-RNA complexes show that although the two positions are separated by 13.1 A, the loops where the replacements reside are tightly connected through an extensive network of interactions that reach the polymerase active site. In particular, G62S seems to restrict the flexibility of loop beta9-alpha11 and, as a consequence, the flexibility of the active site and its ability to bind the RNA template. Thus, a localized change in the finger subdomain of 3D may affect the catalytic domain. The results provide a structural interpretation of why different amino acid substitutions were selected to confer R resistance in closely related viruses and reveal a complex network of intra-3D interactions that can affect the recognition of both the RNA template and incoming nucleotide.

Articles - 3koa mentioned but not cited (5)

  1. A multi-step process of viral adaptation to a mutagenic nucleoside analogue by modulation of transition types leads to extinction-escape. Agudo R, Ferrer-Orta C, Arias A, de la Higuera I, Perales C, Pérez-Luque R, Verdaguer N, Domingo E. PLoS Pathog 6 e1001072 (2010)
  2. Structure of foot-and-mouth disease virus mutant polymerases with reduced sensitivity to ribavirin. Ferrer-Orta C, Sierra M, Agudo R, de la Higuera I, Arias A, Pérez-Luque R, Escarmís C, Domingo E, Verdaguer N. J Virol 84 6188-6199 (2010)
  3. Multifunctionality of a picornavirus polymerase domain: nuclear localization signal and nucleotide recognition. Ferrer-Orta C, de la Higuera I, Caridi F, Sánchez-Aparicio MT, Moreno E, Perales C, Singh K, Sarafianos SG, Sobrino F, Domingo E, Verdaguer N. J Virol 89 6848-6859 (2015)
  4. SARS-CoV-2 structural coverage map reveals viral protein assembly, mimicry, and hijacking mechanisms. O'Donoghue SI, Schafferhans A, Sikta N, Stolte C, Kaur S, Ho BK, Anderson S, Procter JB, Dallago C, Bordin N, Adcock M, Rost B. Mol Syst Biol 17 e10079 (2021)
  5. Evidence for a non-catalytic ion-binding site in multiple RNA-dependent RNA polymerases. Mönttinen HA, Ravantti JJ, Poranen MM. PLoS One 7 e40581 (2012)


Reviews citing this publication (12)

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  2. Ribavirin: a drug active against many viruses with multiple effects on virus replication and propagation. Molecular basis of ribavirin resistance. Beaucourt S, Vignuzzi M. Curr Opin Virol 8 10-15 (2014)
  3. Picornaviral polymerase structure, function, and fidelity modulation. Peersen OB. Virus Res 234 4-20 (2017)
  4. Role of motif B loop in allosteric regulation of RNA-dependent RNA polymerization activity. Garriga D, Ferrer-Orta C, Querol-Audí J, Oliva B, Verdaguer N. J Mol Biol 425 2279-2287 (2013)
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  6. RNA-Dependent RNA Polymerases of Picornaviruses: From the Structure to Regulatory Mechanisms. Ferrer-Orta C, Ferrero D, Verdaguer N. Viruses 7 4438-4460 (2015)
  7. Structural and Functional Basis of the Fidelity of Nucleotide Selection by Flavivirus RNA-Dependent RNA Polymerases. Selisko B, Papageorgiou N, Ferron F, Canard B. Viruses 10 E59 (2018)
  8. The impact of quasispecies dynamics on the use of therapeutics. Perales C, Iranzo J, Manrubia SC, Domingo E. Trends Microbiol 20 595-603 (2012)
  9. Three-dimensional structure of foot-and-mouth disease virus and its biological functions. Han SC, Guo HC, Sun SQ. Arch Virol 160 1-16 (2015)
  10. RNA replication errors and the evolution of virus pathogenicity and virulence. Novella IS, Presloid JB, Taylor RT. Curr Opin Virol 9 143-147 (2014)
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  1. Coxsackievirus B3 mutator strains are attenuated in vivo. Gnädig NF, Beaucourt S, Campagnola G, Bordería AV, Sanz-Ramos M, Gong P, Blanc H, Peersen OB, Vignuzzi M. Proc Natl Acad Sci U S A 109 E2294-303 (2012)
  2. β-d-N4-Hydroxycytidine Is a Potent Anti-alphavirus Compound That Induces a High Level of Mutations in the Viral Genome. Urakova N, Kuznetsova V, Crossman DK, Sokratian A, Guthrie DB, Kolykhalov AA, Lockwood MA, Natchus MG, Crowley MR, Painter GR, Frolova EI, Frolov I. J Virol 92 e01965-17 (2018)
  3. Structure of hepatitis C virus polymerase in complex with primer-template RNA. Mosley RT, Edwards TE, Murakami E, Lam AM, Grice RL, Du J, Sofia MJ, Furman PA, Otto MJ. J Virol 86 6503-6511 (2012)
  4. Alphavirus mutator variants present host-specific defects and attenuation in mammalian and insect models. Rozen-Gagnon K, Stapleford KA, Mongelli V, Blanc H, Failloux AB, Saleh MC, Vignuzzi M. PLoS Pathog 10 e1003877 (2014)
  5. Ribavirin can be mutagenic for arenaviruses. Moreno H, Gallego I, Sevilla N, de la Torre JC, Domingo E, Martín V. J Virol 85 7246-7255 (2011)
  6. Long-range interaction networks in the function and fidelity of poliovirus RNA-dependent RNA polymerase studied by nuclear magnetic resonance. Yang X, Welch JL, Arnold JJ, Boehr DD. Biochemistry 49 9361-9371 (2010)
  7. Extinction of West Nile Virus by Favipiravir through Lethal Mutagenesis. Escribano-Romero E, Jiménez de Oya N, Domingo E, Saiz JC. Antimicrob Agents Chemother 61 e01400-17 (2017)
  8. Enhanced inhibition of foot-and-mouth disease virus by combinations of porcine interferon-α and antiviral agents. Kim SM, Park JH, Lee KN, Kim SK, Ko YJ, Lee HS, Cho IS. Antiviral Res 96 213-220 (2012)
  9. Feasibility of Known RNA Polymerase Inhibitors as Anti-SARS-CoV-2 Drugs. Neogi U, Hill KJ, Ambikan AT, Heng X, Quinn TP, Byrareddy SN, Sönnerborg A, Sarafianos SG, Singh K. Pathogens 9 E320 (2020)
  10. Reduced Chance of Hearing Loss Associated with Therapeutic Drug Monitoring of Aminoglycosides in the Treatment of Multidrug-Resistant Tuberculosis. van Altena R, Dijkstra JA, van der Meer ME, Borjas Howard JF, Kosterink JG, van Soolingen D, van der Werf TS, Alffenaar JW. Antimicrob Agents Chemother 61 e01400-16 (2017)
  11. Involvement of a joker mutation in a polymerase-independent lethal mutagenesis escape mechanism. Agudo R, de la Higuera I, Arias A, Grande-Pérez A, Domingo E. Virology 494 257-266 (2016)
  12. The crystal structure of a cardiovirus RNA-dependent RNA polymerase reveals an unusual conformation of the polymerase active site. 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. J Virol 88 5595-5607 (2014)
  13. Inhibitors of foot and mouth disease virus targeting a novel pocket of the RNA-dependent RNA polymerase. Durk RC, Singh K, Cornelison CA, Rai DK, Matzek KB, Leslie MD, Schafer E, Marchand B, Adedeji A, Michailidis E, Dorst CA, Moran J, Pautler C, Rodriguez LL, McIntosh MA, Rieder E, Sarafianos SG. PLoS One 5 e15049 (2010)
  14. Residues Arg283, Arg285, and Ile287 in the nucleotide binding pocket of bovine viral diarrhea virus NS5B RNA polymerase affect catalysis and fidelity. Curti E, Jaeger J. J Virol 87 199-207 (2013)
  15. Influence of mutagenesis and viral load on the sustained low-level replication of an RNA virus. Perales C, Agudo R, Manrubia SC, Domingo E. J Mol Biol 407 60-78 (2011)
  16. Both cis and trans Activities of Foot-and-Mouth Disease Virus 3D Polymerase Are Essential for Viral RNA Replication. Herod MR, Ferrer-Orta C, Loundras EA, Ward JC, Verdaguer N, Rowlands DJ, Stonehouse NJ. J Virol 90 6864-6883 (2016)
  17. Molecular and Functional Bases of Selection against a Mutation Bias in an RNA Virus. de la Higuera I, Ferrer-Orta C, de Ávila AI, Perales C, Sierra M, Singh K, Sarafianos SG, Dehouck Y, Bastolla U, Verdaguer N, Domingo E. Genome Biol Evol 9 1212-1228 (2017)
  18. Surface for catalysis by poliovirus RNA-dependent RNA polymerase. Wang J, Lyle JM, Bullitt E. J Mol Biol 425 2529-2540 (2013)
  19. Molecular dissection of a viral quasispecies under mutagenic treatment: positive correlation between fitness loss and mutational load. Arias A, Isabel de Ávila A, Sanz-Ramos M, Agudo R, Escarmís C, Domingo E. J Gen Virol 94 817-830 (2013)
  20. Mutagenesis-mediated decrease of pathogenicity as a feature of the mutant spectrum of a viral population. Sanz-Ramos M, Rodríguez-Calvo T, Sevilla N. PLoS One 7 e39941 (2012)
  21. Inhibition of viral RNA-dependent RNA polymerases with clinically relevant nucleotide analogs. Maheden K, Todd B, Gordon CJ, Tchesnokov EP, Götte M. Enzymes 49 315-354 (2021)
  22. Characterization of susceptibility variants of poliovirus grown in the presence of favipiravir. Daikoku T, Mizuguchi M, Obita T, Yokoyama T, Yoshida Y, Takemoto M, Shiraki K. J Microbiol Immunol Infect 51 581-586 (2018)
  23. Repeated exposure to 5D9, an inhibitor of 3D polymerase, effectively limits the replication of foot-and-mouth disease virus in host cells. Rai DK, Schafer EA, Singh K, McIntosh MA, Sarafianos SG, Rieder E. Antiviral Res 98 380-385 (2013)
  24. Evaluation of anti-HIV-1 mutagenic nucleoside analogues. Vivet-Boudou V, Isel C, El Safadi Y, Smyth RP, Laumond G, Moog C, Paillart JC, Marquet R. J Biol Chem 290 371-383 (2015)
  25. Changes in protein domains outside the catalytic site of the bacteriophage Qβ replicase reduce the mutagenic effect of 5-azacytidine. Cabanillas L, Sanjuán R, Lázaro E. J Virol 88 10480-10487 (2014)
  26. Contribution of a Multifunctional Polymerase Region of Foot-and-Mouth Disease Virus to Lethal Mutagenesis. de la Higuera I, Ferrer-Orta C, Moreno E, de Ávila AI, Soria ME, Singh K, Caridi F, Sobrino F, Sarafianos SG, Perales C, Verdaguer N, Domingo E. J Virol 92 e01119-18 (2018)
  27. Directed Evolution of Seneca Valley Virus in Tumorsphere and Monolayer Cell Cultures of a Small-Cell Lung Cancer Model. Waqqar S, Lee K, Lawley B, Bilton T, Quiñones-Mateu ME, Bostina M, Burga LN. Cancers (Basel) 15 2541 (2023)


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