Host alternation of chikungunya virus increases fitness while restricting population diversity and adaptability to novel selective pressures

Journal of Virology

Volumn 85, Issue 2, 2011, Pages 1025-1035

  Coffey, Lark L ^a   Vignuzzi, Marco ^a  

^a CNRS   (France)

Author keywords

[No Author keywords available]

Indexed keywords

AZACITIDINE; FLUOROURACIL; RIBAVIRIN;

ANIMAL CELL; ARTICLE; CELL CYCLE; CHIKUNGUNYA ALPHAVIRUS; CONTROLLED STUDY; EVOLUTIONARY ADAPTATION; FITNESS; GENE SEQUENCE; GENETIC VARIABILITY; HOST CELL; HOST RANGE; HUMAN; HUMAN CELL; INVERTEBRATE; NONHUMAN; PRIORITY JOURNAL; VERTEBRATE; VIRUS NEUTRALIZATION;

ANIMALS; CELL LINE; CERCOPITHECUS AETHIOPS; CHIKUNGUNYA VIRUS; CRICETINAE; GENETIC VARIATION; HOST SPECIFICITY; HUMANS; VIRAL LOAD; VIRULENCE;

ARBOVIRUS; CHIKUNGUNYA VIRUS; INVERTEBRATA; VERTEBRATA;

EID: 78650670077     PISSN: 0022538X     EISSN: 10985514     Source Type: Journal    
DOI: 10.1128/JVI.01918-10     Document Type: Article

References (60)

1. Aaskov, J., K. Buzacott, H. M. Thu, K. Lowry, and E. C. Holmes. 2006.Long-term transmission of defective RNA viruses in humans and Aedes mosquitoes. Science 311:236-238.
2. Agapov, E. V., I. A. Razumov, I. V. Frolov, A. A. Kolykhalov, S. V. Netesov, and V. B. Loktev. 1994. Localization of four antigenic sites involved in Venezuelan equine encephalomyelitis virus protection. Arch. Virol. 139: 173-181.
3. Borderia, A. V., R. Lorenzo-Redondo, M. Pernas, C. Casado, T. Alvaro, E. Domingo, and C. Lopez-Galindez. 2010. Initial fitness recovery of HIV-1 is associated with quasispecies heterogeneity and can occur without modifications in the consensus sequence. PLoS One 5:e10319.
4. Ciota, A. T., A. O. Lovelace, Y. Jia, L. J. Davis, D. S. Young, and L. D.Kramer. 2008. Characterization of mosquito-adapted West Nile virus.J. Gen. Virol. 89:1633-1642.
5. Ciota, A. T., K. A. Ngo, A. O. Lovelace, A. F. Payne, Y. Zhou, P. Y. Shi, and L. D. Kramer. 2007. Role of the mutant spectrum in adaptation and replication of West Nile virus. J. Gen. Virol. 88:865-874.
6. Coffey, L. L., N. Vasilakis, A. C. Brault, A. M. Powers, F. Tripet, and S. C.Weaver. 2008. Arbovirus evolution in vivo is constrained by host alternation.Proc. Natl. Acad. Sci. U. S. A. 105:6970-6975.
7. Cooper, L. A., and T. W. Scott. 2001. Differential evolution of eastern equine encephalitis virus populations in response to host cell type. Genetics 157: 1403-1412.
8. Craig, S., H. M. Thu, K. Lowry, X. F. Wang, E. C. Holmes, and J. Aaskov. 2003. Diverse dengue type 2 virus populations contain recombinant and both parental viruses in a single mosquito host. J. Virol. 77:4463-4467.
9. Crotty, S., and R. Andino. 2002. Implications of high RNA virus mutation rates: lethal mutagenesis and the antiviral drug ribavirin. Microbes Infect.4:1301-1307.
10. Domingo, E., and J. J. Holland. 1997. RNA virus mutations and fitness for survival. Annu. Rev. Microbiol. 51:151-178.
11. Drake, J. W., and J. J. Holland. 1999. Mutation rates among RNA viruses.Proc. Natl. Acad. Sci. U. S. A. 96:13910-13913.
12. Eigen, M. 1996. On the nature of virus quasispecies. Trends Microbiol.4:216-218.
13. Eigen, M. 1971. Self organization of matter and the evolution of biological macromolecules. Naturwissenschaften 58:465-523.
14. Farci, P., and R. H. Purcell. 2000. Clinical significance of hepatitis C virus genotypes and quasispecies. Semin. Liver Dis. 20:103-126.
15. Farci, P., A. Shimoda, A. Coiana, G. Diaz, G. Peddis, J. C. Melpolder, A. Strazzera, D. Y. Chien, S. J. Munoz, A. Balestrieri, R. H. Purcell, and H. J.Alter. 2000. The outcome of acute hepatitis C predicted by the evolution of the viral quasispecies. Science 288:339-344.
16. Fitzpatrick, K. A ., E. R. Deardorff, K. Pesko, D. E. Brackney, B. Zhang, E. Bedrick, P. Y. Shi, and G. D. Ebel. 2010. Population variation of West Nile virus confers a host-specific fitness benefit in mosquitoes. Virology 404:89-95.
17. Greene, I. P., E. Wang, E. R. Deardorff, R. Milleron, E. Domingo, and S. C. Weaver. 2005. Effect of alternating passage on adaptation of Sindbis virus to vertebrate and invertebrate cells. J. Virol. 79:14253-14260.
18. Holmes, E. C. 2009. The evolution and emergence of RNA viruses. Oxford University Press, New York, NY.
19. Holmes, E. C., and S. S. Twiddy. 2003. The origin, emergence and evolutionary genetics of dengue virus. Infect. Genet. Evol. 3:19-28.
20. Jerzak, G., K. A. Bernard, L. D. Kramer, and G. D. Ebel. 2005. Genetic variation in West Nile virus from naturally infected mosquitoes and birds suggests quasispecies structure and strong purifying selection. J. Gen. Virol. 86:2175-2183.
21. Jerzak, G. V., K. Bernard, L. D. Kramer, P. Y. Shi, and G. D. Ebel. 2007. The West Nile virus mutant spectrum is host-dependant and a determinant of mortality in mice. Virology 360:469-476.
22. Jerzak, G. V., I. Brown, P. Y. Shi, L. D. Kramer, and G. D. Ebel. 2008. Genetic diversity and purifying selection in West Nile virus po pulations are maintained during host switching. Virology 374:256-260.
23. Knight, R. L., K. L. Schultz, R. J. Kent, M. Venkatesan, and D. E. Griffin. 2009. Role of N-linked glycosylation for Sindbis virus infection and replication in vertebrate and invertebrate systems. J. Virol. 83:5640-5647.
24. Lanciotti, R. S., O. L. Kosoy, J. J. Laven, A. J. Panella, J. O. Velez, A. J. Lambert, and G. L. Campbell. 2007. Chikungunya virus in US travelers returning from India, 2006. Emerg. Infect. Dis. 13:764-767.
25. Noppornpanth, S., T. X. Lien, Y. Poovorawan, S. L. Smits, A. D. Osterhaus, and B. L. Haagmans. 2006. Identification of a natural ly occurring recombinant genotype 2/6 hepatitis C virus. J. Virol. 80:7569-7577.
26. Novella, I. S., D. K. Clarke, J. Quer, E. A. Duarte, C. H. Lee, S. C. Weaver, S. F. Elena, A. Moya, E. Domingo, and J. J. Holland. 1995. Extreme fitness differences in mammalian and insect hosts after continuous replication of vesicular stomatitis virus in sandfly cells. J. Virol. 69:6805-6809.
27. Novella, I. S., and B. E. Ebendick-Corpus. 2004. Molecular basis of fitness loss and fitness recovery in vesicular stomatitis virus. J. Mol. Biol. 342:1423-1430.
28. Novella, I. S., C. L. Hershey, C. Escarmis, E. Domingo, and J. J. Holland. 1999. Lack of evolutionary stasis during alternating replication of an arbovirus in insect and mammalian cells. J. Mol. Biol. 287:459-465.
29. Ogbunugafor, C. B., J. B. Pease, and P. E. Turner. 2010. On the possible role of robustness in the evolution of infectious diseases. Chaos 20:026108.
30. Pfeiffer, J. K., and K. Kirkegaard. 2005. Increased fidelity reduces poliovirus fitness and virulence under selective pressure in mice. PLoS Pathog. 1:e11.
31. Pfeiffer, J. K., and K. Kirkegaard. 2003. A single mutation in poliovirus RNA-dependent RNA polymerase confers resistance to mutagenic nucleotide analogs via increased fidelity. Proc. Natl. Acad. Sci. U. S. A. 100:7289-7294.
32. Powers, A. M., and C. H. Logue. 2007. Changing patterns of chikungunya virus: re-emergence of a zoonotic arbovirus. J. Gen. Virol. 88:2363-2377.
33. Racaniello, V. R. 2007. Picornaviridae: the viruses and their replication, p. 797. In B. N. Fields, D. M. Knipe, P. M. Howley, and D. E. Griffin (ed.), Fields virology, vol. 1, 5th ed. Lippincott Williams & Wilkins, Philadelphia,PA.
34. Ravichandran, R., and M. Manian. 2008. Ribavirin therapy for Chikungunya arthritis. J. Infect. Dev. Ctries. 2:140-142.
35. Rosenblum, C. I., and V. Stollar. 1999. SVMPA, a mutant of Sindbis virus resistant to mycophenolic acid and ribavirin, shows an increased sensitivity tochick interferon. Virology 259:228-233.
36. Sanjuan, R., M. R. Nebot, N. Chirico, L. M. Mansky, and R. Belshaw. 2010. Viral mutation rates. J. Virol. 84:9733-9748.
37. Sanz-Ramos, M., F. Diaz-San Segundo, C. Escarmis, E. Domingo, and N. Sevilla. 2008. Hidden virulence determinants in a viral quasispecies in vivo. J. Virol. 82:10465-10476.
38. Scholle, F., Y. A. Girard, Q. Zhao, S. Higgs, and P. W. Mason. 2004.trans-Packaged West Nile virus-like particles: infectious properties in vitro and in infected mosquito vectors. J. Virol. 78:11605-11614.
39. Schuffenecker, I., I. Iteman, A. Michault, S. Murri, L. Frangeul, M. C. Vaney, R. Lavenir, N. Pardigon, J. M. Reynes, F. Pettinelli, L. Biscornet, L. Diancourt, S. Michel, S. Duquerroy, G. Guigon, M. P. Frenkiel, A. C. Brehin,N. Cubito, P. Despres, F. Kunst, F. A. Rey, H. Zeller, and S. Brisse. 2006. Genome microevolution of chikungunya viruses causing the Indian Ocean outbreak. PLoS Med. 3:e263.
40. Shabman, R. S., T. E. Morrison, C. Moore, L. White, M. S. Suthar, L.Hueston, N. Rulli, B. Lidbury, J. P. Ting, S. Mahalingam, and M. T. Heise. 2007. Differential induction of type I interferon responses in myeloid dendritic cells by mosquito and mammalian-cell-derived alphaviruses. J. Virol. 81:237-247.
41. Sierra, M., A. Airaksinen, C. Gonzalez-Lopez, R. Agudo, A. Arias, and E.Domingo. 2007. Foot-and-mouth disease virus mutant with decreased sensitivity to ribavirin: implications for error catastrophe. J. Virol. 81:2012-2024.
42. Smith, D. R., A. P. Adams, J. L. Kenney, E. Wang, and S. C. Weaver. 2008. Venezuelan equine encephalitis virus in the mosquito vector Aedes taeniorhynchus: infection initiated by a small number of susceptible epithelial cells and a population bottleneck. Virology 372:176-186.
43. Smith, D. R., P. V. Aguilar, L. L. Coffey, G. D. Gromowski, E. Wang, and S. C. Weaver. 2006. Venezuelan equine encephalitis virus transmission and effect on pathogenesis. Emerg. Infect. Dis. 12:1190-1196.
44. Strauss, J. H., and E. G. Strauss. 1994. The alphaviruses: gene expression, replication, and evolution. Microbiol. Rev. 58:491-562.
45. Tamura, K., J. Dudley, M. Nei, and S. Kumar. 2007. MEGA4: Molecular Evolutionary Genetics Analysis (MEGA) software version 4.0. Mol. Biol. Evol. 24:1596-1599.
46. Tsetsarkin, K. A., D. L. Vanlandingham, C. E. McGee, and S. Higgs. 2007.A single mutation in chikungunya virus affects vector specificity and epidemicpotential. PLoS Pathog. 3:e201.
47. Tsiang, M., S. S. Monroe, and S. Schlesinger. 1985. Studies of defective interfering RNAs of Sindbis virus with and without tRNAAsp sequences att heir 5& termini. J. Virol. 4:38-44.
48. Turner, P. E., and S. F. Elena. 2000. Cost of host radiation in an RNA virus. Genetics 156:1465-1470.
49. Turner, P. E., N. M. Morales, B. W. Alto, and S. K. Remold. 2010. Role of evolved host breadth in the initial emergence of an RNA virus. Evolution 64:3273-3286.
50. Vanlandingham, D. L., B. S. Schneider, K. Klingler, J. Fair, D. Beasley, J.Huang, P. Hamilton, and S. Higgs. 2004. Real-time reverse transcriptasepolymerase chain reaction quantification of West Nile virus transmitted by Culex pipiens quinquefasciatus. Am. J. Trop. Med. Hyg. 71:120-123.
51. Vasilakis, N., E. R. Deardorff, J. L. Kenney, S. L. Rossi, K. A. Hanley, and S. C. Weaver. 2009. Mosquitoes put the brake on arbovirus evolution: experimental evolution reveals slower mutation accumulation in mosquito than vertebrate cells. PLoS Pathog. 5:e1000467.
52. Vignuzzi, M., J. K. Stone, J. J. Arnold, C. E. Cameron, and R. Andino. 2006.Quasispecies diversity determines pathogenesis through cooperative interactions in a viral population. Nature 439:344-348.
53. Vrati, S., C. A. Fernon, L. Dalgarno, and R. C. Weir. 1988. Location of a major antigenic site involved in Ross River virus neutralization. Virology162:346-353.
54. Wang, E., H. Ni, R. Xu, A. D. Barrett, S. J. Watowich, D. J. Gubler, and S. C. Weaver. 2000. Evolutionary relationships of endemic/epidemic and sylvatic dengue viruses. J. Virol. 74:3227-3234.
55. Wang, W. K., S. R. Lin, C. M. Lee, C. C. King, and S. C. Chang. 2002. Dengue type 3 virus in plasma is a population of closely related genomes:quasispecies. J. Virol. 76:4662-4665.
56. Weaver, S. C., A. C. Brault, W. Kang, and J. J. Holland. 1999. Genetic and fitness changes accompanying adaptation of an arbovirus to vertebrate and invertebrate cells. J. Virol. 73:4316-4326.
57. Wittke, V., T. E. Robb, H. M. Thu, A. Nisalak, S. Nimmannitya, S. Kalayanrooj, D. W. Vaughn, T. P. Endy, E. C. Holmes, and J. G. Aaskov. 2002. Extinction and rapid emergence of strains of dengue 3 virus during an interepidemic period. Virology 301:148-156.
58. Wolinsky, S. M., B. T. Korber, A. U. Neumann, M. Daniels, K. J. Kunstman, A. J. Whetsell, M. R. Furtado, Y. Cao, D. D. Ho, and J. T. Safrit. 1996. Adaptive evolution of human immunodeficiency virus-type 1 during the natural course of infection. Science 272:537-542.
59. Young, K. C., K. L. Lindsay, K. J. Lee, W. C. Liu, J. W. He, S. L. Milstein, and M. M. Lai. 2003. Identification of a ribavirin-resistant NS5B mutation of hepatitis C virus during ribavirin monotherapy. Hepatology 38:869-878.
60. Zhu, T., H. Mo, N. Wang, D. S. Nam, Y. Cao, R. A. Koup, and D. D. Ho. 1993. Genotypic and phenotypic characterization of HIV-1 patients with primary infection. Science 261:1179-1181.