Fidelity Variants of RNA Dependent RNA polymerases uncover an indirect, mutagenic activity of amiloride compounds

PLoS Pathogens

Volumn 6, Issue 10, 2010, Pages

  Levi, Laura I ^a   Gnädig, Nina F ^a   Beaucourt, Stéphanie ^a   McPherson, Malia J ^a   Baron, Bruno ^b   Arnold, Jamie J ^c   Vignuzzi, Marco ^a  

^a CNRS   (France)

^b INSTITUT PASTEUR   (France)

^c PENNSYLVANIA STATE UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

AMILORIDE; ION; MAGNESIUM; MANGANESE; MUTAGENIC AGENT; RNA DIRECTED RNA POLYMERASE; ANTIVIRUS AGENT; DNA DIRECTED RNA POLYMERASE; DRUG DERIVATIVE; RNA; VIRUS RNA;

ANTIVIRAL ACTIVITY; ANTIVIRAL RESISTANCE; ARTICLE; CONCENTRATION (PARAMETERS); COXSACKIE VIRUS B3; DRUG TARGETING; GENE REPLICATION; MUTAGENESIS; MUTAGENIC ACTIVITY; MUTATION RATE; NONHUMAN; POLIOMYELITIS VIRUS; RNA VIRUS; VIRUS GENE; VIRUS ISOLATION; VIRUS MUTATION; VIRUS REPLICATION; WILD TYPE; ANIMAL; CERCOPITHECUS; DNA TEMPLATE; DRUG EFFECT; ENTEROVIRUS; GENETIC TRANSCRIPTION; GENETIC VARIABILITY; GENETICS; HELA CELL; HUMAN; METABOLISM; NUCLEOTIDE SEQUENCE; VERO CELL;

COXSACKIEVIRUS; POLIOVIRUS;

AMILORIDE; ANIMALS; ANTIVIRAL AGENTS; BASE SEQUENCE; CERCOPITHECUS AETHIOPS; DNA-DIRECTED RNA POLYMERASES; ENTEROVIRUS; GENETIC VARIATION; HELA CELLS; HUMANS; MUTAGENESIS; MUTAGENS; RNA; RNA, VIRAL; TEMPLATES, GENETIC; TRANSCRIPTION, GENETIC; VERO CELLS;

EID: 78449244303     PISSN: 15537366     EISSN: 15537374     Source Type: Journal    
DOI: 10.1371/journal.ppat.1001163     Document Type: Article

References (41)

1. Horisberger JD (1998) Amiloride-sensitive Na channels. Curr Opin Cell Biol 10: 443-449.
2. Nakayama S, Nomura H (1995) Mechanisms of intracellular Mg2+ regulation affected by amiloride and ouabain in the guinea-pig taenia caeci. J Physiol (488(Pt 1): 1-12.
3. Wilson L, Gage P, Ewart G (2006) Hexamethylene amiloride blocks E protein ion channels and inhibits coronavirus replication. Virology 353: 294-306.
4. Premkumar A, Horan CR, Gage PW (2005) Dengue virus M protein C-terminal peptide (DVM-C) forms ion channels. J Membr Biol 204: 33-38.
5. Ewart GD, Mills K, Cox GB, Gage PW (2002) Amiloride derivatives block ion channel activity and enhancement of virus-like particle budding caused by HIV-1 protein Vpu. Eur Biophys J 31: 26-35.
6. Premkumar A, Wilson L, Ewart GD, Gage PW (2004) Cation-selective ion channels formed by p7 of hepatitis C virus are blocked by hexamethylene amiloride. FEBS Lett 557: 99-103.
7. Gazina EV, Harrison DN, Jefferies M, Tan H, Williams D, et al. (2005) Ion transport blockers inhibit human rhinovirus 2 release. Antiviral Res 67: 98-106.
8. Harrison DN, Gazina EV, Purcell DF, Anderson DA, Petrou S (2008) Amiloride derivatives inhibit coxsackievirus B3 RNA replication. J Virol 82: 1465-1473.
9. Loeb LA, Essigmann JM, Kazazi F, Zhang J, Rose KD, et al. (1999) Lethal mutagenesis of HIV with mutagenic nucleoside analogs. Proc Natl Acad SciUS A 96: 1492-1497.
10. Crotty S, Cameron C, Andino R (2002) Ribavirin's antiviral mechanism of action: lethal mutagenesis? J Mol Med 80: 86-95.
11. Airaksinen A, Pariente N, Menendez-Arias L, Domingo E (2003) Curing of footand- mouth disease virus from persistently infected cells by ribavirin involves enhanced mutagenesis. Virology 311: 339-349.
12. Pariente N, Sierra S, Lowenstein PR, Domingo E (2001) Efficient virus extinction by combinations of a mutagen and antiviral inhibitors. J Virol 75: 9723-9730.
13. Ruiz-Jarabo CM, Ly C, Domingo E, de la Torre JC (2003) Lethal mutagenesis of the prototypic arenavirus lymphocytic choriomeningitis virus (LCMV). Virology 308: 37-47.
14. 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 U S A 100: 7289-7294.
15. 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.
16. Pfeiffer JK, Kirkegaard K (2005) Increased fidelity reduces poliovirus fitness and virulence under selective pressure in mice. PLoS Pathog 1: e11.
17. Vignuzzi M, Stone JK, Arnold JJ, Cameron CE, Andino R (2006) Quasispecies diversity determines pathogenesis through cooperative interactions in a viral population. Nature 439: 344-348.
18. Vignuzzi M, Wendt E, Andino R (2008) Engineering attenuated virus vaccines by controlling replication fidelity. Nat Med 14: 154-161.
19. Crotty S, Maag D, Arnold JJ, Zhong W, Lau JY, et al. (2000) The broad-spectrum antiviral ribonucleoside ribavirin is an RNA virus mutagen. Nat Med 6: 1375-1379.
20. Jackson-Grusby L, Laird PW, Magge SN, Moeller BJ, Jaenisch R (1997) Mutagenicity of 5-aza-29-deoxycytidine is mediated by the mammalian DNA methyltransferase. Proc Natl Acad Sci U S A 94: 4681-4685.
21. Arnold JJ, Cameron CE (2000) Poliovirus RNA-dependent RNA polymerase (3D(pol)). Assembly of stable, elongation-competent complexes by using a symmetrical primer-template substrate (sym/sub). J Biol Chem 275: 5329-5336.
22. Uetani T, Matsubara T, Nomura H, Murohara T, Nakayama S (2003) Ca2+- dependent modulation of intracellular Mg2+ concentration with amiloride and KB-R7943 in pig carotid artery. J Biol Chem 278: 47491-47497.
23. Steitz TA (1998) A mechanism for all polymerases. Nature 391: 231-232.
24. Korneeva VS, Cameron CE (2007) Structure-function relationships of the viral RNA-dependent RNA polymerase: fidelity, replication speed, and initiation mechanism determined by a residue in the ribose-binding pocket. J Biol Chem 282: 16135-16145.
25. Ferrer-Orta C, Arias A, Perez-Luque R, Escarmis C, Domingo E, et al. (2007) Sequential structures provide insights into the fidelity of RNA replication. Proc Natl Acad Sci U S A 104: 9463-9468.
26. Arias A, Arnold JJ, Sierra M, Smidansky ED, Domingo E, et al. (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.
27. Crotty S, Gohara D, Gilligan DK, Karelsky S, Cameron CE, et al. (2003) Manganese-dependent polioviruses caused by mutations within the viral polymerase. J Virol 77: 5378-5388.
28. Arnold JJ, Cameron CE (2004) Poliovirus RNA-dependent RNA polymerase (3Dpol): pre-steady-state kinetic analysis of ribonucleotide incorporation in the presence of Mg2+. Biochemistry 43: 5126-5137.
29. Arnold JJ, Gohara DW, Cameron CE (2004) Poliovirus RNA-dependent RNA polymerase (3Dpol): pre-steady-state kinetic analysis of ribonucleotide incorporation in the presence of Mn2+. Biochemistry 43: 5138-5148.
30. Lanford RE, Chavez D, Guerra B, Lau JY, Hong Z, et al. (2001) Ribavirin induces error-prone replication of GB virus B in primary tamarin hepatocytes. J Virol 75: 8074-8081.
31. Severson WE, Schmaljohn CS, Javadian A, Jonsson CB (2003) Ribavirin causes error catastrophe during Hantaan virus replication. J Virol 77: 481-488.
32. Cuevas JM, Gonzalez-Candelas F, Moya A, Sanjuan R (2009) The effect of ribavirin on the mutation rate and spectrum of Hepatitis C virus in vivo. J Virol 83: 5760-5764.
33. Graci JD, Harki DA, Korneeva VS, Edathil JP, Too K, et al. (2007) Lethal mutagenesis of poliovirus mediated by a mutagenic pyrimidine analogue. J Virol 81: 11256-11266.
34. Graci JD, Too K, Smidansky ED, Edathil JP, Barr EW, et al. (2008) Lethal mutagenesis of picornaviruses with N-6-modified purine nucleoside analogues. Antimicrob Agents Chemother 52: 971-979.
35. Moriyama K, Suzuki T, Negishi K, Graci JD, Thompson CN, et al. (2008) Effects of introduction of hydrophobic group on ribavirin base on mutation induction and anti-RNA viral activity. J Med Chem 51: 159-166.
36. 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.
37. Gruez A, Selisko B, Roberts M, Bricogne G, Bussetta C, et al. (2008) The crystal structure of coxsackievirus B3 RNA-dependent RNA polymerase in complex with its protein primer VPg confirms the existence of a second VPg binding site on Picornaviridae polymerases. J Virol 82: 9577-9590.
38. Thompson AA, Peersen OB (2004) Structural basis for proteolysis-dependent activation of the poliovirus RNA-dependent RNA polymerase. EMBO J 23: 3462-3471.
39. Arnold JJ, Bernal A, Uche U, Sterner DE, Butt TR, et al. (2006) Small ubiquitinlike modifying protein isopeptidase assay based on poliovirus RNA polymerase activity. Anal Biochem 350: 214-221.
40. Studier FW (2005) Protein production by auto-induction in high density shaking cultures. Protein Expr Purif 41: 207-234.
41. Castro C, Smidansky E, Maksimchuk KR, Arnold JJ, Korneeva VS, et al. (2007) Two proton transfers in the transition state for nucleotidyl transfer catalyzed by RNA- and DNA-dependent RNA and DNA polymerases. Proc Natl Acad Sci U S A 104: 4267-4272.