Abstract
Continuous, persistent replication of a wild-type strain of vesicular stomatitis virus in cultured sandfly cells for 10 months profoundly decreased virus replicative fitness in mammalian cells and greatly increased fitness in sandfly cells. After persistent infection of sandfly cells, fitness was over 2,000,000-fold greater than that in mammalian cells, indicating extreme selective differences in the environmental conditions provided by insect and mammalian cells. The sandfly-adapted virus also showed extremely low fitness in mouse brain cells (comparable to that in mammalian cell cultures). It also showed an attenuated phenotype, requiring a nearly millionfold higher intracranial dose than that of its parent clone to kill mice. A single passage of this adapted virus in BHK-21 cells at 37 degrees C restored fitness to near neutrality and also restored mouse neurovirulence. These results clearly illustrate the enormous capacity of RNA viruses to adapt to changing selective environments.
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- Clarke D. K., Duarte E. A., Elena S. F., Moya A., Domingo E., Holland J. The red queen reigns in the kingdom of RNA viruses. Proc Natl Acad Sci U S A. 1994 May 24;91(11):4821–4824. doi: 10.1073/pnas.91.11.4821. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Clarke D. K., Duarte E. A., Moya A., Elena S. F., Domingo E., Holland J. Genetic bottlenecks and population passages cause profound fitness differences in RNA viruses. J Virol. 1993 Jan;67(1):222–228. doi: 10.1128/jvi.67.1.222-228.1993. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Comer J. A., Tesh R. B., Modi G. B., Corn J. L., Nettles V. F. Vesicular stomatitis virus, New Jersey serotype: replication in and transmission by Lutzomyia shannoni (Diptera: Psychodidae). Am J Trop Med Hyg. 1990 May;42(5):483–490. doi: 10.4269/ajtmh.1990.42.483. [DOI] [PubMed] [Google Scholar]
- Comer J. A., Tesh R. B. Phlebotomine sand flies as vectors of vesiculoviruses: a review. Parassitologia. 1991 Dec;33 (Suppl):143–150. [PubMed] [Google Scholar]
- Domingo E., Holland J. J. Complications of RNA heterogeneity for the engineering of virus vaccines and antiviral agents. Genet Eng (N Y) 1992;14:13–31. doi: 10.1007/978-1-4615-3424-2_2. [DOI] [PubMed] [Google Scholar]
- Domingo E. RNA virus evolution and the control of viral disease. Prog Drug Res. 1989;33:93–133. doi: 10.1007/978-3-0348-9146-2_5. [DOI] [PubMed] [Google Scholar]
- Duarte E. A., Clarke D. K., Moya A., Elena S. F., Domingo E., Holland J. Many-trillionfold amplification of single RNA virus particles fails to overcome the Muller's ratchet effect. J Virol. 1993 Jun;67(6):3620–3623. doi: 10.1128/jvi.67.6.3620-3623.1993. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Duarte E. A., Novella I. S., Ledesma S., Clarke D. K., Moya A., Elena S. F., Domingo E., Holland J. J. Subclonal components of consensus fitness in an RNA virus clone. J Virol. 1994 Jul;68(7):4295–4301. doi: 10.1128/jvi.68.7.4295-4301.1994. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Duarte E., Clarke D., Moya A., Domingo E., Holland J. Rapid fitness losses in mammalian RNA virus clones due to Muller's ratchet. Proc Natl Acad Sci U S A. 1992 Jul 1;89(13):6015–6019. doi: 10.1073/pnas.89.13.6015. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Ewald P. W. The evolution of virulence. Sci Am. 1993 Apr;268(4):86–93. doi: 10.1038/scientificamerican0493-86. [DOI] [PubMed] [Google Scholar]
- HURLBUT H. S. West Nile virus infection in arthropods. Am J Trop Med Hyg. 1956 Jan;5(1):76–85. doi: 10.4269/ajtmh.1956.5.76. [DOI] [PubMed] [Google Scholar]
- Holland J. J., de la Torre J. C., Clarke D. K., Duarte E. Quantitation of relative fitness and great adaptability of clonal populations of RNA viruses. J Virol. 1991 Jun;65(6):2960–2967. doi: 10.1128/jvi.65.6.2960-2967.1991. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Khin M. M., Than K. A. Transovarial transmission of dengue 2 virus by Aedes aegypti in nature. Am J Trop Med Hyg. 1983 May;32(3):590–594. doi: 10.4269/ajtmh.1983.32.590. [DOI] [PubMed] [Google Scholar]
- Mudd J. A., Leavitt R. W., Kingsbury D. T., Holland J. J. Natural selection of mutants of vesicular stomatitis virus by cultured cells of Drosophila melanogaster. J Gen Virol. 1973 Sep;20(3):341–351. doi: 10.1099/0022-1317-20-3-341. [DOI] [PubMed] [Google Scholar]
- Nichol S. T. Genetic diversity of enzootic isolates of vesicular stomatitis virus New Jersey. J Virol. 1988 Feb;62(2):572–579. doi: 10.1128/jvi.62.2.572-579.1988. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Nichol S. T., Rowe J. E., Fitch W. M. Punctuated equilibrium and positive Darwinian evolution in vesicular stomatitis virus. Proc Natl Acad Sci U S A. 1993 Nov 15;90(22):10424–10428. doi: 10.1073/pnas.90.22.10424. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Novella I. S., Duarte E. A., Elena S. F., Moya A., Domingo E., Holland J. J. Exponential increases of RNA virus fitness during large population transmissions. Proc Natl Acad Sci U S A. 1995 Jun 20;92(13):5841–5844. doi: 10.1073/pnas.92.13.5841. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Novella I. S., Elena S. F., Moya A., Domingo E., Holland J. J. Size of genetic bottlenecks leading to virus fitness loss is determined by mean initial population fitness. J Virol. 1995 May;69(5):2869–2872. doi: 10.1128/jvi.69.5.2869-2872.1995. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Peleg J. Growth of viruses in arthropod cell cultures: applications. I. Attenuation of Semliki Forest (SF) virus in continuously cultured Aedes aegypti mosquito cells (Peleg) as a step in production of vaccines. Curr Top Microbiol Immunol. 1971;55:155–161. doi: 10.1007/978-3-642-65224-0_26. [DOI] [PubMed] [Google Scholar]
- Rosen L., Shroyer D. A., Tesh R. B., Freier J. E., Lien J. C. Transovarial transmission of dengue viruses by mosquitoes: Aedes albopictus and Aedes aegypti. Am J Trop Med Hyg. 1983 Sep;32(5):1108–1119. doi: 10.4269/ajtmh.1983.32.1108. [DOI] [PubMed] [Google Scholar]
- Schaffer P. A., Scherer W. F. Stability of virulence and plaque size of Venezuelan encephalitis virus with passage in Mosquitoes (Aedes aegypti). Am J Epidemiol. 1971 Jan;93(1):68–74. doi: 10.1093/oxfordjournals.aje.a121229. [DOI] [PubMed] [Google Scholar]
- Schwartz R. H. The value of synthetic peptides as vaccines for eliciting T-cell immunity. Curr Top Microbiol Immunol. 1986;130:79–85. doi: 10.1007/978-3-642-71440-5_7. [DOI] [PubMed] [Google Scholar]
- Singh K. R. Propagation of arboviruses in Singh's Aedes cell lines. I. Growth of arboviruses in Aedes albopictus and A. aegypti cell lines. Curr Top Microbiol Immunol. 1971;55:127–133. doi: 10.1007/978-3-642-65224-0_20. [DOI] [PubMed] [Google Scholar]
- Taylor W. P., Marshall I. D. Adaptation studies with Ross River virus: laboratory mice and cell cultures. J Gen Virol. 1975 Jul;28(1):59–72. doi: 10.1099/0022-1317-28-1-59. [DOI] [PubMed] [Google Scholar]
- Taylor W. P., Marshall I. D. Adaptation studies with Ross River virus: retention of field level virulence. J Gen Virol. 1975 Jul;28(1):73–83. doi: 10.1099/0022-1317-28-1-73. [DOI] [PubMed] [Google Scholar]
- Tesh R. B., Chaniotis B. N., Johnson K. M. Vesicular stomatitis virus (Indiana serotype): transovarial transmission by phlebotomine sandlies. Science. 1972 Mar 31;175(4029):1477–1479. doi: 10.1126/science.175.4029.1477. [DOI] [PubMed] [Google Scholar]
- Tesh R. B., Modi G. B. Development of a continuous cell line from the sand fly Lutzomyia longipalpis (Diptera: Psychodidae), and its susceptibility to infection with arboviruses. J Med Entomol. 1983 Mar 30;20(2):199–202. doi: 10.1093/jmedent/20.2.199. [DOI] [PubMed] [Google Scholar]
- Tesh R. B., Peralta P. H., Johnson K. M. Ecologic studies of vesicular stomatitis virus. I. Prevalence of infection among animals and humans living in an area of endemic VSV activity. Am J Epidemiol. 1969 Sep;90(3):255–261. doi: 10.1093/oxfordjournals.aje.a121068. [DOI] [PubMed] [Google Scholar]