Systematic study of the genetic response of a variable virus to the introduction of deleterious mutations in a functional capsid region

Journal of Virology

Volumn 83, Issue 19, 2009, Pages 10140-10151

  Luna, Eva ^a   Rodríguez Huete, Alicia ^a   Rincón, Verónica ^a   Mateo, Roberto ^a,b   Mateu, Mauricio G ^a  

^a UNIVERSIDAD AUTÓNOMA DE MADRID   (Spain)

^b STANFORD UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

AMINO ACID; VIRUS RNA;

AMINO ACID SUBSTITUTION; ARTICLE; CELL CULTURE; DELETION MUTANT; FOOT AND MOUTH DISEASE VIRUS; GENE MUTATION; GENE TARGETING; GENETIC TRANSFECTION; GENETIC VARIABILITY; GENOME; GENOTYPE; NONHUMAN; PRIORITY JOURNAL; PROGENY; PROTEIN INTERACTION; PROTEIN TARGETING; SITE DIRECTED MUTAGENESIS; STEREOCHEMISTRY; SUBSTITUTION LINE; VIRUS CAPSID; VIRUS REPLICATION;

ALANINE; ANIMALS; CAPSID; CELL LINE; CRICETINAE; GENE DELETION; MODELS, MOLECULAR; MOLECULAR CONFORMATION; MUTAGENESIS, SITE-DIRECTED; MUTATION; PROMOTER REGIONS, GENETIC; RNA VIRUSES; RNA, VIRAL; TRANSFECTION; VIRUS ASSEMBLY;

FOOT-AND-MOUTH DISEASE VIRUS; MIRIDAE;

EID: 70349425909     PISSN: 0022538X     EISSN: None     Source Type: Journal    
DOI: 10.1128/JVI.00903-09     Document Type: Article

References (54)

1. Acharya, R., E. Fry, D. Stuart, G. Fox, D. Rowlands, and F. Brown. 1989. The three-dimensional structure of foot-and-mouth disease virus at 2.9 Å resolution. Nature 337:709-716. (Pubitemid 19064726)
2. Baranowski, E., N. Sevilla, N. Verdaguer, C. M. Ruiz-Jarabo, E. Beck, and E. Domingo. 1998. Multiple virulence determinants of foot-and-mouth disease virus in cell culture. J. Virol. 72:6362-6372. (Pubitemid 28323947)
3. Blacklow, S. C., and J. R. Knowles. 1990. How can a catalytic lesion be offset? The energetics of two pseudorevertant triosephosphate isomerases. Biochemistry 29:4099-4108.
4. Bouvier, S. E., and A. R. Poteete. 1996. Second-site reversion of a structural defect in bacteriophage T4 lysozyme. FASEB J. 10:159-163.
5. Brown, K. A., E. E. Howell, and J. Kraut. 1993. Long-range structural effects in a second-site revertant of a mutant dihydrofolate reductase. Proc. Natl. Acad. Sci. USA 90:11753-11756.
6. Burch, C. L., and L. Chao. 1999. Evolution by small steps and rugged landscapes in the RNA virus phi6. Genetics 151:921-927.
7. Chanel-Vos, C., and M. Kielian. 2006. Second-site revertants of a Semliki Forest virus fusion-block mutation reveal the dynamics of a class II membrane fusion protein. J. Virol. 80:6115-6122. (Pubitemid 43849189)
8. Chiu, W., R. M. Burnett, and R. L. Garcea (ed.). 1997. Structural biology of viruses. Oxford University Press, Oxford, United Kingdom.
9. Cimarelli, A., S. Sandin, S. Hoglund, and J. Luban. 2000. Rescue of multiple viral functions by a second-site suppressor of a human immunodeficiency virus type 1 nucleocapsid mutation. J. Virol. 74:4273-4283. (Pubitemid 30214435)
10. Curry, S., C. C. Abrams, E. Fry, J. C. Crowther, G. J. Belsham, D. I. Stuart, and A. M. Q. King. 1995. Viral RNA modulates the acid sensitivity of foot-and-mouth disease virus capsids. J. Virol. 69:430-438. (Pubitemid 24378821)
11. Curry, S., E. Fry, W. Blakemore, R. Abu-Ghazaleh, T. Jackson, A. King, S. Lea, J. Newman, D. Rowlands, and D. Stuart. 1996. Perturbations in the surface structure of A22 Iraq foot-and-mouth disease virus accompanying coupled changes in host cell specificity and antigenicity. Structure 4:135-145. (Pubitemid 126658977)
12. Dam, E., R. Quercia, B. Glass, D. Descamps, O. Launay, X. Duval, H.-G. Kräusslich, A. J. Hance, F. Clavel, et al. 2009. Gag mutations strongly contribute to HIV resistance to protease inhibitors in highly drug-experienced patients besides compensating for fitness loss. PLoS Pathog. 5:e1000345.
13. Deom, C. M., and X. Z. He. 1997. Second-site reversion of a dysfunctional mutation in a conserved region of the tobacco mosaic tobamovirus movement protein. Virology 232:13-18.
14. Desai, P., and S. Person. 1999. Second-site mutations in the N terminus of the major capsid protein (VP5) overcome a block at the maturation cleavage site of the capsid scaffold proteins of herpes simplex virus type 1. Virology 261:357-366. (Pubitemid 29431788)
15. Domingo, E. (ed.). 2006. Quasispecies: concepts and implications for virology. In Current topics in microbiology and immunology series. vol 289. Springer Verlag, Berlin, Germany.
16. Domingo, E., and J. J. Holland. 1997. RNA virus mutations and fitness for survival. Annu. Rev. Microbiol. 51:151-178.
17. Domingo, E., C. Escarmís, L. Menéndez-Arias, and J. J. Holland. 1999. Viral quasispecies and fitness variations, p. 141-161. In E. Domingo, R. G. Webster, and J. J. Holland (ed.), Origin and evolution of viruses. Academic Press, Inc., San Diego, CA.
18. Domingo, E., C. Biebricher, M. Eigen, and J. J. Holland. 2001. Quasi-species and RNA virus evolution: principles and consequences. Landes Bioscience, Austin, TX.
19. Domingo, E., C. M. Ruiz-Jarabo, A. Arias, J. García-Arriaza, and C. Escarmís. 2004. Quasispecies dynamics and evolution of foot-and-mouth disease virus, p. 261-304. In F. Sobrino and E. Domingo (ed.), Foot-and-mouth disease. Current perspectives. Horizon Bioscience, Norfolk, United Kingdom.
20. Ellard, F. M., J. Drew, W. Blakemore, D. I. Stuart, and A. M. Q. King. 1999. Evidence for the role of His-142 of protein 1C in the acid-induced disassembly of foot-and-mouth disease virus capsids. J. Gen. Virol. 80:1911-1918.
21. Fry, E. E., S. M. Lea, T. Jackson, J. W. Newman, F. M. Ellard, W. E. Blakemore, R. Abu-Ghazaleh, A. Samuel, A. M. King, and D. I. Stuart. 1999. The structure and function of a foot-and-mouth disease virus-oligosaccharide receptor complex. EMBO J. 18:543-554.
22. Jarvik, J., and D. Botstein. 1975. Conditional-lethal mutations that suppress genetic defects in morphogenesis by altering structural proteins. Proc. Natl. Acad. Sci. USA 72:2738-2742.
23. Joerger, A. C., M. D. Allen, and A. R. Fersht. 2004. Crystal structure of a superstable mutant of human p53 core domain. Insights into the mechanism of rescuing oncogenic mutations. J. Biol. Chem. 279:1291-1296.
24. Kim, H.-W., T. J. Shen, D. P. Sun, N. T. Ho, M. Madrid, M. F. Tam, M. Zou, P. F. Cottam, and C. Ho. 1994. Restoring allosterism with compensatory mutations in hemoglobin. Proc. Natl. Acad. Sci. USA 91:11547-11551.
25. Klig, L. S., D. L. Oxender, D. L., and C. Yanofsky. 1988. Second-site revertants of Escherichia coli trp repressor mutants. Genetics 120:651-655.
26. Lea, S., J. Hernández, W. Blakemore, E. Brocchi, S. Curry, E. Domingo, E. Fry, R. Abu-Ghazaleh, A. M. Q. King, J. Newman, D. Stuart, and M. G. Mateu. 1994. The structure and antigenicity of a serotype C foot-and-mouth disease virus. Structure 2:123-139. (Pubitemid 124002014)
27. Mahy, B. W. J. (ed.). 2005. Foot-and-mouth disease virus. In Current topics in microbiology and immunology series, vol.288. Springer Verlag, Berlin, Germany.
28. Mateo, R., A. Díaz, E. Baranowski, and M. G. Mateu. 2003. Complete alanine scanning of intersubunit interfaces in a foot-and-mouth disease virus capsid reveals critical contributions of many side chains to particle stability and viral function. J. Biol. Chem. 278:41019-41027.
29. Mateo, R., and M. G. Mateu. 2007. Deterministic, compensatory mutational events in the capsid of foot-and-mouth disease virus in response to the introduction of mutations found in viruses from persistent infections. J. Virol. 81:1879-1887. (Pubitemid 46214460)
30. Mateo, R., E. Luna, V. Rincón, and M. G. Mateu. 2008. Engineering viable foot-and-mouth disease viruses with increased thermostability as a step in the development of improved vaccines. J. Virol. 82:12232-12240.
31. Mateu, M. G. 1995. Antibody recognition of picornaviruses and escape from neutralization: a structural view. Virus Res. 38:1-24.
32. Mateu, M. G., and N. Verdaguer. 2004. Functional and structural aspects of the interaction of foot-and-mouth disease virus with antibodies, p. 223-260. In F. Sobrino and E. Domingo (ed.), Foot and mouth disease: current perspectives. Horizon Bioscience, Norfolk, United Kingdom.
33. Nijhuis, M., R. Schuurman, D. de Jong, J. Erickson, E. Gustchina, J. Albert, P. Schipper, S. Gulnik, and C. A. Boucher. 1999. Increased fitness of drug-resistant HIV-1 protease as a result of acquisition of compensatory mutations during suboptimal therapy. AIDS 13:2349-2359.
34. Nikolova, P. V., K. B. Wong, B. DeDecker, J. Henckel, and A. R. Fersht. 2000. Mechanism of rescue of common p53 cancer mutations by second-site suppressor mutations. EMBO J. 19:370-378. (Pubitemid 30072607)
35. Novella, I. S., and B. E. Ebendick-Corpus. 2004. Molecular basis of fitness losses and fitness recovery in vesicular stomatitis virus. J. Mol. Biol. 342:1423-1430.
36. Olivares, I., V. Sánchez-Merino, M. A. Martínez, E. Domingo, C. López-Galíndez, and L. Menéndez-Arias. 1999. Second-site reversion of a human immunodeficiency virus type 1 reverse transcriptase mutant that restores enzyme function and replication capacity. J. Virol. 73:6293-6298. (Pubitemid 29327805)
37. Olivares, I., M. Gutiérrez-Rivas, C. López-Galíndez, and L. Menéndez-Arias. 2004. Tryptophan scanning mutagenesis of aromatic residues within the polymerase domain of HIV-1 reverse transcriptase: critical role of Phe-130 for p51 function and second-site revertant restoring viral replication capacity. Virology 324:400-411. (Pubitemid 38797856)
38. Ono, A., M. Huang, and E. O. Freed. 1997. Characterization of human immunodeficiency virus type 1 matrix revertants: effects on virus assembly, Gag processing, and Env incorporation into virions. J. Virol. 71:4409-4418.
39. Pazhanisamy, S., C. M. Stuver, A. B. Cullinan, N. Margolin, B. G. Rao, and D. J. Livingston. 1996. Kinetic characterization of human immunodeficiency virus type-1 protease-resistant variants. J. Biol. Chem. 271:17979-17985.
40. Pelemans, H., R. Esnouf, K. L. Min, M. Parniak, E. De Clercq, and J. Balzarini. 2001. Mutations at amino acid positions 63, 189, and 396 of human immunodeficiency virus type 1 reverse transcriptase (RT) partially restore the DNA polymerase activity of a Trp229Tyr mutant RT. Virology 287:143-150. (Pubitemid 32778246)
41. Poon, A., and L. Chao. 2005. The rate of compensatory mutation in the DNA bacteriophage ΦX174. Genetics 170:989-999. (Pubitemid 41105458)
42. Poteete, A. R., D. Rennell, S. E. Bouvier, and L. W. Hardy. 1997. Alteration of T4 lysozyme structure by second-site reversion of deleterious mutations. Protein Sci. 6:2418-2425.
43. Reguera, J., A. Carreira, L. Riolobos, J. M. Almendral, and M. G. Mateu. 2004. Role of interfacial amino acid residues in assembly, stability and conformation of a spherical virus capsid. Proc. Natl. Acad. Sci. USA 101:2724-2729.
44. Rueckert, R. R. 1996. Picornaviridae: the viruses and their replication, p. 609-654. In B. N. Fields, D. M. Knipe, and P. M. Howley (ed.), Fields virology, 3rd ed. Lippincott-Raven Publishers, Philadelphia, PA.
45. Sayle, R. A., and E. J. Milner-White. 1995. RasMol: biomolecular graphics for all. Trends Biochem. Sci. 20:374-376.
46. Sobrino, F., and E. Domingo (ed.). 2004. Foot and Mouth Disease: current perspectives. Horizon Bioscience, Norfolk, United Kingdom.
47. Sobrino, F., M. Dávila, J. Ortín, and E. Domingo. 1983. Multiple genetic variants arise in the course of replication of foot-and-mouth disease virus in cell culture. Virology 128:310-318.
48. Tachedjian, G., H. E. Aronson, and S. P. Goff. 2000. Analysis of mutations and suppressors affecting interactions between the subunits of the HIV type 1 reverse transcriptase. Proc. Natl. Acad. Sci. USA 97:6334-6339.
49. Thompson, J. R., S. Doun, and K. L. Perry. 2006. Compensatory capsid protein mutations in cucumber mosaic virus confer systematic infectivity in squash (Cucurbita pepo). J. Virol. 80:7740-7743.
50. Vriend, G. 1990. Whatif: a molecular modeling and drug design program. J. Mol. Graph. 8:52-56.
51. Warner, S. C., P. Desai, and S. Person. 2000. Second-site mutations encoding residues 34 and 78 of the major capsid protein (VP5) of herpes simplex virus type 1 are important for overcoming a blocked maturation cleavage site of the capsid scaffold proteins. Virology 278:217-226.
52. Wray, J. W., W. A. Baase, J. D. Lindstrom, L. H. Weaver, A. R. Poteete, and B. W. Matthews. 1999. Structural analysis of a non-contiguous second-site revertant in T4 lysozyme show that increasing the rigidity of a protein can enhance its stability. J. Mol. Biol. 292:1111-1120.
53. Wu, T. D., C. A. Schiffer, M. J. Gonzales, J. Taylor, R. Kantor, S. Chou, D. Israelski, A. R. Zolopa, W. F. Fessel, and R. W. Shafer. 2003. Mutation patterns and structural correlates in human immunodeficiency virus type 1 protease following different protease inhibitor treatments. J. Virol. 77:4836-4847.
54. Yuan, T. T., and C. Shih. 2000. A frequent, naturally occurring mutation (P130T) of human hepatitis B virus core antigen is compensatory for immature secretion phenotype of another frequent variant (I97L). J. Virol. 74:4929-4932.