Evolution of increased survival in RNA viruses specialized on cancer-derived cells

American Naturalist

Volumn 181, Issue 5, 2013, Pages 585-595

  Brandon Ogbunugafor, C ^a,b   Alto, Barry W ^a,c   Overton, Thomas M ^a,d   Bhushan, Ambika ^a,d   Morales, Nadya M ^a   Turner, Paul E ^a  

^a YALE UNIVERSITY   (United States)

^b HARVARD UNIVERSITY   (United States)

^c UNIVERSITY OF FLORIDA   (United States)

^d HARVARD MEDICAL SCHOOL   (United States)

Author keywords

Experimental evolution; Free living survival; Host parasite interaction; Specialization; Virus

Indexed keywords

CANCER; CYTOLOGY; EVOLUTIONARY BIOLOGY; HOST-PARASITE INTERACTION; RNA; SPECIALIZATION; SURVIVAL; VIRULENCE; VIRUS;

ARTICLE; DIRECTED MOLECULAR EVOLUTION; GENETICS; HELA CELL; HOST PATHOGEN INTERACTION; HUMAN; MDCK CELL; MOLECULAR EVOLUTION; PATHOGENICITY; PHYSIOLOGY; TUMOR CELL LINE; VESICULAR STOMATITIS VIRUS; VIRULENCE;

CELL LINE, TUMOR; DIRECTED MOLECULAR EVOLUTION; EVOLUTION, MOLECULAR; HELA CELLS; HOST-PATHOGEN INTERACTIONS; HUMANS; MADIN DARBY CANINE KIDNEY CELLS; VESICULOVIRUS; VIRULENCE;

RNA VIRUSES; VESICULAR STOMATITIS VIRUS;

EID: 84876360433     PISSN: 00030147     EISSN: None     Source Type: Journal    
DOI: 10.1086/670052     Document Type: Article

References (44)

1. Abedon, S. T., and R. R. Culler. 2007. Optimizing bacteriophage plaque fecundity. Journal of Theoretical Biology 249:582-592.
2. Alto, B. W., and P. E. Turner. 2010. Consequences of host adaptation for performance of vesicular stomatitis virus in novel thermal environments. Evolutionary Ecology 24:299-315.
3. Ausar, S. F., T. R. Foubert, M. H. Hudson, T. S. Vedvick, and C. R. Middaugh. 2006. Conformational stability and disassembly of Nor-walk virus-like particles: effect of pH and temperature. Journal of Biological Chemistry 281:19478-19488.
4. Bonhoeffer, S., R. E. Lenski, and D. Ebert. 1996. The curse of the pharaoh: the evolution of virulence in pathogens with long living propagules. Proceedings of the Royal Society B: Biological Sciences 263:715-721.
5. Bull, J. J. 1994. Perspective: virulence. Evolution 48:1423-1437.
6. Bull, J. J. 2006. Optimality models of phage life history and parallels in disease evolution. Journal of Theoretical Biology 241:928-938.
7. Burch, C. L., and L. Chao. 2000. Evolvability of an RNA virus is determined by its mutational neighbourhood. Nature 406:625-628.
8. Caciagli, P., V. Medina Piles, D. Marian, M. Vecchiati, V. Masenga, G. Mason, T. Falcioni, et al. 2009. Virion stability is important for the circulative transmission of tomato yellow leaf curl sardinia virus by Bemisia tabaci, but virion access to salivary glands does not guarantee transmissibility. Journal of Virology 83:5784-5795.
9. Dennehy, J. J., and P. E. Turner. 2004. Reduced fecundity is the cost of cheating in RNA virus F6. Proceedings of the Royal Society B: Biological Sciences 271:2275-2282.
10. de Paepe, M., and F. Taddei. 2006. Viruses' life history: towards a mechanistic basis of a trade-off between survival and reproduction among phages. PLoS Biology 4:e193.
11. Duffy, S., C. L. Burch, and P. E. Turner. 2007. Evolution of host specificity drives reproductive isolation among RNA viruses. Evolution 61:2614-2622.
12. Duffy, S., P. E. Turner, and C. L. Burch. 2006. Pleiotropic costs of niche expansion in the RNA bacteriophage F6. Genetics 172:751-757.
13. Ebert, D., and J. J. Bull. 2003. Challenging the trade-off model for the evolution of virulence: is virulence management feasible? Trends in Microbiology 11:15-20.
14. Ewald, P. W. 2004. Evolution of virulence. Infectious Disease Clinics of North America 18:1-15.
15. Freshney, R. I. 2000. Culture of animal cells: a manual of basic techniques. 4th ed. Wiley, New York.
16. Gandon, S. 1998. The curse of the pharaoh hypothesis. Proceedings of the Royal Society B: Biological Sciences 265:1545-1552.
17. Gandon, S., P. Agnew, and Y. Michalakis. 2002. Coevolution between parasite virulence and host life-history traits. American Naturalist 160:374-388.
18. 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. Journal of Virology 79:14253-14260.
19. Harrison, R. G. 1912. The cultivation of tissues in extraneous media as a method of morphogenetic study. Anatomical Record 6:181-193.
20. Holland, J. J., J. C. de la Torre, D. K. Clarke, and E. Duarte. 1991. Quantitation of relative fitness and great adaptability of clonal populations of RNA viruses. Journal of Virology 65:2960-2967.
21. Kamo, M., and M. Boots. 2004. The curse of the pharaoh in space: free-living infectious stages and the evolution of virulence in spatially explicit populations. Journal of Theoretical Biology 231:435-441.
22. Kaptur, P. E., M. O. McKenzie, G. W. Wertz, and D. S. Lyles. 1995. Assembly functions of vesicular stomatitis virus matrix protein are not disrupted by mutations at major sites of phosphorylation. Virology 206:894-903.
23. Kennedy, M. A., and R. J. Parks. 2009. Adenovirus virion stability and the viral genome: size matters. Molecular Therapy 17:1664-1666.
24. Lenard, J. 1996. Negative-strand virus M and retrovirus MA proteins: all in a family? Virology 216:289-298.
25. Leschonsky, B., C. Ludwig, K. Bieler, and R. Wagner. 2007. Capsid stability and replication of human immunodeficiency virus type 1 are influenced critically by charge and size of Gag residue 183. Journal of General Virology 88:207-216.
26. Lichty, B. D., A. T Power, D. F. Stojdl, and J. C. Bell. 2004. Vesicular stomatitis virus: re-inventing the bullet. Trends in Molecular Medicine 10:210-216.
27. Halfon, P., H. Khiri, V. Gerolami, M. Bourliere, J. M. Feryn, P. Reynier, A. Gauthier, and G. Cartouzou. 1996. Impact of various handling and storage conditions on quantitative detection of hepatitis C virus RNA. Journal of Hepatology 25:307-311.
28. Lun, X., D. L. Senger, T Alain, A. Oprea, K. Parato, D. F. Stojdl, B. Lichty, et al. 2006. Effects of intravenously administered recombinant vesicular stomatitis virus (VSVDM51) on multifocal and invasive gliomas. Journal of the National Cancer Institute 98:1546-1557.
29. Lyles, D. S., and M. O. McKenzie. 1997. Activity of vesicular stomatitis virus M protein mutants in cell rounding is correlated with the ability to inhibit host gene expression and is not correlated with virus assembly function. Virology 229:77-89.
30. Lyles, D. S., and C. E. Rupprecht. 2007. Rhabdoviridae. Pages 1364-1408 in B. N. Fields, D. M. Knipe, P. M. Howley, D. E. Griffin, R. A. Lamb, M. A. Martin, B. Roizman, et al. Fields' virology. 4th ed. Lippincott, Williams, & Wilkins, Philadelphia.
31. Mateo, R., E. Luna, V. Rincon, and M. G. Mateu. 2008. Engineering viable foot-and-mouth disease viruses with increased thermostability as a step in the development of improved vaccines. Journal of Virology 82:12232-12240.
32. Miralles, R., A. Moya, and S. F. Elena. 1999. Effect of population patchiness and migration rates on the adaptation and divergence of vesicular stomatitis virus quasispecies populations. Journal of General Virology 80:2051-2059.
33. Novella, I. S., D. K. Clarke, J. Quer, E. A. Duarte, C. H. Lee, S. C. Weaver, S. F. Elena, et al. 1995. Extreme fitness differences in mammalian and insect hosts after continuous replication of vesicular stomatitis virus in sandfly cells. Journal of Virology 69: 6805-6809.
34. 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. Journal of Molecular Biology 287:459-465.
35. Ogbunugafor, C. B., S. Basu, N. M. Morales, and P. E. Turner. 2010. Combining mathematics and empirical data to predict emergence of RNA viruses that differ in reservoir use. Philosophical Transactions of the Royal Society B: 365:1919-1930.
36. Remold, S. K., A. Rambaut, and P. E. Turner. 2008. Evolutionary genomics of host adaptation in vesicular stomatitis virus. Molecular Biology and Evolution 25:1138-1147.
37. Rice, W. R. 1989. Analyzing tables of statistical tables. Evolution 43: 223-225.
38. Russell, S. J., and K. Peng. 2007. Viruses as anticancer drugs. Trends in pharmacological sciences 28:326-333.
39. Sanjuán, R., J. M. Cuevas, V. Furio, E. C. Holmes, and A. Moya. 2007. Selection for robustness in mutagenized RNA viruses. PLoS Genetics 3:e93.
40. Skloot, R. L. 2010. The immortal life of Henrietta Lacks. Crown, New York.
41. Stojdl, D. F., B. D. Lichty, B. R. tenOever, J. M. Paterson, A. T. Power, S. Knowles, R. Marius, et al. 2004. VSV strains with defects in their ability to shutdown innate immunity are potent systemic anti-cancer agents. Cancer Cell 4:263-275.
42. Turner, P. E., and S. F. Elena. 2000. Cost of host radiation in an RNA virus. Genetics 156:1465-1470.
43. 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.
44. Walther, B. A., and P. W. Ewald. 2004. Pathogen survival in the external environment and the evolution of virulence. Biological Reviews of the Cambridge Philosophical Society 79:849-869.