Foot-and-mouth disease virus low-fidelity polymerase mutants are attenuated

Archives of Virology

Volumn 159, Issue 10, 2014, Pages 2641-2650

  Xie, Xiaochun ^a   Wang, Haiwei ^a   Zeng, Jianxiong ^a   Li, Chen ^a   Zhou, Guohui ^a   Yang, Decheng ^a   Yu, Li ^a  

^a INSTITUTE OF PLANT PROTECTION   (China)

Author keywords

[No Author keywords available]

Indexed keywords

ANTIVIRUS AGENT; FLUOROURACIL; RIBAVIRIN; RNA DIRECTED RNA POLYMERASE; VIRUS RNA;

ANIMAL; ANTIVIRAL RESISTANCE; BAGG ALBINO MOUSE; BIOSYNTHESIS; CELL LINE; DRUG EFFECTS; ENZYMOLOGY; FOOT AND MOUTH DISEASE; FOOT AND MOUTH DISEASE VIRUS; GENETICS; HAMSTER; MOUSE; MUTATION; MUTATION RATE; NUCLEOTIDE SEQUENCE; PHYSIOLOGY; SEQUENCE ANALYSIS; VIROLOGY; VIRUS REPLICATION;

ANIMALS; ANTIVIRAL AGENTS; BASE SEQUENCE; CELL LINE; CRICETINAE; DRUG RESISTANCE, VIRAL; FLUOROURACIL; FOOT-AND-MOUTH DISEASE; FOOT-AND-MOUTH DISEASE VIRUS; MICE; MICE, INBRED BALB C; MUTATION; MUTATION RATE; RIBAVIRIN; RNA REPLICASE; RNA, VIRAL; SEQUENCE ANALYSIS, RNA; VIRUS REPLICATION;

EID: 84907704014     PISSN: 03048608     EISSN: 14328798     Source Type: Journal    
DOI: 10.1007/s00705-014-2126-z     Document Type: Article

References (47)

1. Airaksinen A, Pariente N, Menéndez-Arias L, Domingo E (2003) Curing of foot-and-mouth disease virus from persistently infected cells by ribavirin involves enhanced mutagenesis. Virology 311:339–349
2. Anderson JP, Daifuku R, Loeb LA (2004) Viral error catastrophe by mutagenic nucleosides. Annu Rev Microbiol 58:183–205
3. Baranowski E, Molina N, Núñez JI, Sobrino F, Sáiz M (2003) Recovery of infectious foot-and-mouth disease virus from suckling mice after direct inoculation with in vitro-transcribed RNA. Journal of virology 77:11290–11295
4. Beaucourt S, Borderia AV, Coffey LL, Gnadig NF, Sanz-Ramos M, Beeharry Y, Vignuzzi M (2011) Isolation of fidelity variants of RNA viruses and characterization of virus mutation frequency. J Vis Exp 52:2953
5. Carrillo C, Tulman ER, Delhon G, Lu Z, Carreno A, Vagnozzi A, Kutish GF, Rock DL (2005) Comparative Genomics of Foot-and-Mouth Disease Virus. Journal of virology 79:6487–6504
6. Coffey LL, Beeharry Y, Bordería AV, Blanc H, Vignuzzi M (2011) Arbovirus high fidelity variant loses fitness in mosquitoes and mice. Proceedings of the National Academy of Sciences 108:16038–16043
7. Coffey LL, Vignuzzi M (2011) Host alternation of chikungunya virus increases fitness while restricting population diversity and adaptability to novel selective pressures. Journal of virology 85:1025–1035
8. Crotty S, Cameron CE, Andino R (2001) RNA virus error catastrophe: direct molecular test by using ribavirin. Proceedings of the National Academy of Sciences of the United States of America 98:6895–6900
9. Crotty S, Andino R (2002) Implications of high RNA virus mutation rates: lethal mutagenesis and the antiviral drug ribavirin. Microbes and infection 4:1301–1307
10. Domingo E, Holland J (1997) RNA virus mutations and fitness for survival. Annual Reviews in Microbiology 51:151–178
11. Domingo E, Menéndez-Arias L, Holland JJ (1997) RNA virus fitness. Reviews in medical virology 7:87–96
12. Domingo E, Escarmis C, Baranowski E, Ruiz-Jarabo CM, Carrillo E, Nunez JI, Sobrino F (2003) Evolution of foot-and-mouth disease virus. Virus research 91:47–63
13. Domingo E, Wain-Hobson S (2009) The 30th anniversary of quasispecies. Meeting on ‘Quasispecies: past, present and future’. EMBO Rep 10:444–448
14. Eigen M (1993) Viral quasispecies. SCIENTIFIC AMERICAN-AMERICAN EDITION- 269:32–32
15. Ferrer-Orta C, Arias A, Perez-Luque R, Escarmís 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. Journal of Biological Chemistry 279:47212–47221
16. Ferrer-Orta C, Arias A, Agudo R, Pérez-Luque R, Escarmís C, Domingo E, Verdaguer N (2006) The structure of a protein primer–polymerase complex in the initiation of genome replication. The EMBO journal 25:880–888
17. Ferrer-Orta C, Arias A, Perez-Luque R, Escarmis C, Domingo E, Verdaguer N (2007) Sequential structures provide insights into the fidelity of RNA replication. Proceedings of the National Academy of Sciences of the United States of America 104:9463–9468
18. Garcia-Nunez S, Konig G, Berinstein A, Carrillo E (2010) Differences in the virulence of two strains of Foot-and-Mouth Disease Virus Serotype A with the same spatiotemporal distribution. Virus research 147:149–152
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. Proceedings of the National Academy of Sciences of the United States of America 109:E2294–E2303
20. Goris N, Vandenbussche F, Herr C, Villers J, Stede YV, Clercq KD (2009) Validaion of two real-time RT-PCR methods for foot-and-mouth disease diagnosis: RNA-extraction, matrix effect, uncertainty of measurement and precision. Journal of virological methods 160:157–162
21. Govorkova EA, Ilyushina NA, Marathe BM, McClaren JL, Webster RG (2010) Competitive fitness of oseltamivir-sensitive and-resistant highly pathogenic H5N1 influenza viruses in a ferret model. Journal of virology 84:8042–8050
22. Grubman MJ, Baxt B (1982) Translation of foot-and-mouth disease virion RNA and processing of the primary cleavage products in a rabbit reticulocyte lysate. Virology 116:19–30
23. Grubman MJ, Baxt B (2004) Foot-and-Mouth Disease. Clinical Microbiology Reviews 17:465–493
24. Gutiérrez-Rivas M, Pulido MR, Baranowski E, Sobrino F, Sáiz M (2008) Tolerance to mutations in the foot-and-mouth disease virus integrin-binding RGD region is different in cultured cells and in vivo and depends on the capsid sequence context. Journal of General Virology 89:2531–2539
25. Knowles NJ, Samuel AR (2003) Molecular epidemiology of foot-and-mouth disease virus. Virus research 91:65–80
26. Lauring AS, Andino R (2010) Quasispecies theory and the behavior of RNA viruses. PLoS pathogens 6:e1001005
27. Levi LI, Gnädig NF, Beaucourt S, McPherson MJ, Baron B, Arnold JJ, Vignuzzi M (2010) Fidelity variants of RNA dependent RNA polymerases uncover an indirect, mutagenic activity of amiloride compounds. PLoS pathogens 6:e1001163
28. Liu X, Yang X, Lee CA, Moustafa IM, Smidansky ED, Lum D, Arnold JJ, Cameron CE, Boehr DD (2013) Vaccine-derived mutation in motif D of poliovirus RNA-dependent RNA polymerase lowers nucleotide incorporation fidelity. The Journal of biological chemistry 288:32753–32765
29. Loeb LA, Mullins JI (2000) Perspective-Lethal Mutagenesis of HIV by Mutagenic Ribonucleoside Analogs. AIDS research and human retroviruses 16:1–3
30. Martín V, Grande-Pérez A, Domingo E (2008) No evidence of selection for mutational robustness during lethal mutagenesis of lymphocytic choriomeningitis virus. Virology 378:185–192
31. Mason PW, Grubman MJ, Baxt B (2003) Molecular basis of pathogenesis of FMDV. Virus research 91:9–32
32. Melo EC, Saraiva V, Astudillo V (2002) Review of the status of foot and mouth disease in countries of South America and approaches to control and eradication. Rev sci tech Off int Epiz 21:429–436
33. Pfeiffer JK, Kirkegaard K (2003) A single mutation in poliovirus RNA-dependent RNA polymerase confers resistance to mutagenic nucleotide analogs via increased fidelity. Proceedings of the National Academy of Sciences of the United States of America 100:7289–7294
34. Pfeiffer JK, Kirkegaard K (2005) Increased fidelity reduces poliovirus fitness and virulence under selective pressure in mice. PLoS pathogens 1:e11
35. Reed LJ, Muech H (1938) A simple method of estimating fifty per cent endpoints. Am J Epidemiol 27:493–497
36. Rodriguez-Pulido M, Sobrino F, Saiz M (2001) Inoculation of newborn mice with non-coding regions of foot-and-mouth disease virus RNA can induce a rapid, solid and wide-range protection against viral infection. Antiviral Research 92:500–504
37. Ruiz-Jarabo CM, Ly C, Domingo E, Torre JCdl (2003) Lethal mutagenesis of the prototypic arenavirus lymphocytic choriomeningitis virus (LCMV). Virology 308:37–47
38. Schaaper RM (1998) Antimutator mutants in bacteriophage T4 and Escherichia coli. Genetics 148:1579–1585
39. Shaw AE, Reid SM, Ebert K, Hutchings GH, Ferris NP, King DP (2007) Implementation of a one-step real-time RT-PCR protocol for diagnosis of foot-and-mouth disease. Journal of virological methods 143:81–85
40. Sierra M, Airaksinen A, González-López C, Agudo R, Arias A, Domingo E (2007) Foot-and-mouth disease virus mutant with decreased sensitivity to ribavirin: implications for error catastrophe. Journal of virology 81:2012–2024
41. Sobrino F, Saiz M, Jimenez-clavero MA, Nunez JI, Rosas MF, Baranowski E, Ley V (2001) Foot-and-mouth disease virus: a long known virus, but a current threat. Vet Res 32:1–30
42. Vignuzzi M, Stone JK, Arnold JJ, Cameron CE, Andino R (2005) Quasispecies diversity determines pathogenesis through cooperative interactions in a viral population. Nature 439:344–348
43. Vignuzzi M, Wendt E, Andino R (2008) Engineering attenuated virus vaccines by controlling replication fidelity. Nature medicine 14:154–161
44. Wang H, Zhao L, Li W, Zhou G, Yu L (2011) Identification of a conformational epitope on the VP1 GH Loop of type Asia1 foot-and-mouth disease virus defined by a protective monoclonal antibody. Veterinary microbiology 148:189–199
45. Weeks SA, Lee CA, Zhao Y, Smidansky ED, August A, Arnold JJ, Cameron CE (2012) A Polymerase mechanism-based strategy for viral attenuation and vaccine development. The Journal of biological chemistry 287:31618–31622
46. Zeng J, Wang H, Xie X, Yang D, Zhou G, Yu L (2013) An increased replication fidelity mutant of foot-and-mouth disease virus retains fitness in vitro and virulence in vivo. Antiviral Res 100:1–7
47. Zeng J, Wang H, Xie X, Li C, Zhou G, Yang D, Yu L (2014) Ribavirin-Resistant Variants of Foot-and-Mouth Disease Virus: The Effect of Restricted Quasispecies Diversity on Viral Virulence. J Virol: JVI. 03513-03594