Evolutionary History and Attenuation of Myxoma Virus on Two Continents

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The attenuation of myxoma virus (MYXV) following its introduction as a biological control into the European rabbit populations of Australia and Europe is the canonical study of the evolution of virulence. However, the evolutionary genetics of this profound change in host-pathogen relationship is unknown. We describe the genome-scale evolution of MYXV covering a range of virulence grades sampled over 49 years from the parallel Australian and European epidemics, including the high-virulence progenitor strains released in the early 1950s. MYXV evolved rapidly over the sampling period, exhibiting one of the highest nucleotide substitution rates ever reported for a double-stranded DNA virus, and indicative of a relatively high mutation rate and/or a continually changing selective environment. Our comparative sequence data reveal that changes in virulence involved multiple genes, likely losses of gene function due to insertion-deletion events, and no mutations common to specific virulence grades. Hence, despite the similarity in selection pressures there are multiple genetic routes to attain either highly virulent or attenuated phenotypes in MYXV, resulting in convergence for phenotype but not genotype.

Vyšlo v časopise: Evolutionary History and Attenuation of Myxoma Virus on Two Continents. PLoS Pathog 8(10): e32767. doi:10.1371/journal.ppat.1002950
Kategorie: Research Article
prolekare.web.journal.doi_sk: https://doi.org/10.1371/journal.ppat.1002950

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Zdroje

1. Fenner F, Ratcliffe FN (1965) Myxomatosis. Cambridge: Cambridge University Press.

2. FennerF, DayMF, WoodroofeGM (1956) Epidemiological consequences of the mechanical transmission of myxomatosis by mosquitoes. J Hyg (Camb) 54: 284–303.

3. FennerF, MarshallID (1957) A comparison of the virulence for European rabbits (Oryctolagus cuniculus) of strains of myxoma virus recovered in the field in Australia, Europe and America. J Hyg (Camb) 55: 149–191.

4. DayMF, FennerF, WoodroofeGM, McIntyreGA (1956) Further studies on the mechanism of mosquito transmission of myxomatosis in the European rabbit. J Hyg (Camb) 54: 258–283.

5. FennerF (1983) Biological control as exemplified by smallpox eradication and myxomatosis. Proc Royal Soc Lond B 218: 259–285.

6. MarshallID, DouglasGW (1961) Studies in the epidemiology of infectious myxomatosis of rabbits. VIII. Further observations on changes in the innate resistance of Australian wild rabbits exposed to myxomatosis. J Hyg (Camb) 59: 117–122.

7. MarshallID, FennerF (1959) Studies in the epidemiology of infectious myxomatosis of rabbits. V. Changes in the innate resistance of wild rabbits between 1951 and 1959. J Hyg (Camb) 56: 288–302.

8. BestSM, KerrPJ (2000) Coevolution of host and virus: the pathogenesis of virulent and attenuated strains of myxoma virus in resistant and susceptible European rabbits. Virology 267: 36–48.

9. KerrPJ, McFaddenG (2002) The immune response to myxoma virus. Viral Immunol 15: 229–246.

10. AndersonRM, MayRM (1982) Coevolution of hosts and parasites. Parasitol 85: 411–426.

11. BullJJ (1994) Virulence. Evolution 48: 1423–1437.

12. MackinnonMJ, GandonS, ReadAF (2008) Virulence evolution in response to vaccination: The case of malaria. Vaccine 26: C42–C52.

13. ReadAF (1994) The evolution of virulence. Trends Microbiol 2: 73–76.

14. DwyerG, LevinSA, ButtelL (1990) A simulation model of the population dynamics and evolution of myxomatosis. Ecol Monog 60: 423–447.

15. BootsM, HudsonPJ, SasakiA (2004) Large shifts in pathogen virulence relate to host population structure. Science 303: 842–845.

16. CameronC, Hota-MitchellS, ChenL, BarrettJ, CaoJ-X, et al. (1999) The complete DNA sequence of myxoma virus. Virology 264: 298–318.

17. StanfordMM, WerdenSJ, McFaddenG (2007) Myxoma virus in the European rabbit: interactions between the virus and its susceptible host. Vet Res 38: 299–318.

18. MoralesM, RamirezMA, CanoMJ, ParragaM, CastillaJ, et al. (2009) Genome comparison of a nonpathogenic myxoma virus field strain with its ancestor, the virulent Lausanne strain. J Virol 83: 2397–2403.

19. DrummondAJ, RambautA (2007) BEAST: Bayesian evolutionary analysis by sampling trees. BMC Evol Biol 7: 214–221.

20. KerrPJ, JacksonRJ, RobinsonAJ, SwanJ, SilversL, et al. (1999) Infertility in female rabbits (Oryctolagus cuniculus) alloimmunized with the rabbit zona pellucida protein ZPB either as a purified recombinant protein or expressed by recombinant myxoma virus. Biol Reprod 61: 606–613.

21. DouglasGW (1962) The Glenfield strain of myxoma virus. Its use in Victoria. J Agri (Victoria) 60: 511–515.

22. SaintKM, FrenchN, KerrPJ (2001) Genetic variation in Australian isolates of myxoma virus: an evolutionary and epidemiological study. Arch Virol 146: 1105–1123.

23. WerdenSJ, McFaddenG (2008) The role of cell signaling in poxvirus tropism: the case of the M-T5 host range protein of myxoma virus. Biochim Biophys Acta 1784: 228–237.

24. MossmanK, Fong LeeS, BarryM, BoshkovL, McFaddenG (1996) Disruption of M-T5, a novel myxoma virus gene member of the poxvirus host range superfamily, results in dramatic attenuation of myxomatosis in infected European rabbits. J Virol 70: 4394–4410.

25. CollinN, GuérinJ-L, DrexlerI, BlaniéS, GelfiJ, et al. (2005) The poxviral scrapin MV-LAP requires a myxoma viral infection context to efficiently downregulate MHC-I molecules. Virology 343: 171–178.

26. GuérinJ-L, GelfiJ, BouillierS, DelverdierM, BellangerF-A, et al. (2002) Myxoma virus leukemia-associated protein is responsible for major histocompatibility complex class 1 and Fas-CD95 down-regulation and defines scrapins, a new group of surface cellular receptor abductor proteins. J Virol 76: 2912–2923.

27. BarteeE, McCormackA, FrühH (2006) Quantitative membrane proteomics reveals new cellular targets of viral immune modulators. PLoS Pathog 2: E107.

28. MansouriM, BarteeE, GouveiaK, Hovey NerenbergBT, et al. (2003) The PHD/LAP-domain protein M153R of myxoma virus is a ubiquitin ligase that induces the rapid internalization and lysosomal destruction of CD4. J Virol 77: 1427–1440.

29. BlaniéS, GelfiJ, BertagnoliS, Camus-BouclainvilleC (2010) MNF, an ankyrin repeat protein of myxoma virus, is part of a native cellular SCF complex during viral infection. Virol J 7: 56.

30. Camus-BouclainvilleC, FietteL, BouchihaS, PignoletB, CounorD, et al. (2004) A virulence factor of myxoma virus colocalizes with NF-kappaB in the nucleus and interferes with inflammation. J Virol 78: 2510–2516.

31. DuffyS, ShackeltonLA, HolmesEC (2008) Rates of evolutionary change in viruses: Patterns and determinants. Nat Rev Genet 9: 267–276.

32. FirthC, KitchenA, ShapiroB, SuchardMA, HolmesEC, et al. (2010) Using time-structured data to estimate evolutionary rates of double-stranded DNA viruses. Mol Biol Evol 27: 2038–2051.

33. McGeochDJ, GathererD (2005) Integrating reptilian herpesviruses into the family Herpesviridae. J Virol 79: 725–731.

34. SanjuánR, NebotMR, ChiricoN, ManskyLM, BelshawR (2010) Viral mutation rates. J Virol 84: 9733–9748.

35. KerrPJ, MerchantJC, SilversL, HoodG, RobinsonAJ (2003) Monitoring the spread of myxoma virus in rabbit populations in the southern tablelands of New South Wales, Australia. II. Selection of a virus strain that was transmissible and could be monitored by polymerase chain reaction. Epidemiol Infect 130: 123–133.

36. KerrPJ, PerkinsHD, InglisB, StaggR, McLaughlinE, et al. (2004) Expression of rabbit IL-4 by recombinant myxoma viruses enhances virulence and overcomes genetic resistance to myxomatosis. Virology 324: 117–128.

37. Mead-BriggsAR, VaughanJA (1975) The differential transmissibility of myxoma virus strains of differing virulence grades by the rabbit flea Spilopsyllus cuniculi (Dale). J Hyg (Camb) 75: 237–247.

38. KerrPJ, HoneJ, PerrinL, FrenchN, WilliamsCK (2010) Molecular and serological analysis of the epidemiology of myxoma virus in rabbits. Vet Microbiol 143: 167–178.

39. BraultAC, Huang CY-H, LangevinSA, KinneyRM, BowenRA, et al. (2007) A single positively selected West Nile viral mutation confers increased avian virogenesis in American crows. Nat Genet 39: 1162–1166.

40. BaigentSJ, McCauleyJW (2003) Influenza type A in humans, mammals and birds: determinants of virus virulence, host-range and interspecies transmission. Bioessays 25: 657–671.

41. FenyöEM, AlbertJ, AsjöB (1989) Replicative capacity, cytopathic effect and cell tropism of HIV. AIDS 3: S5–12.

42. ConnorRI, HoDD (1994) Human immunodeficiency virus type 1 variants with increased replicative capacity develop during the asymptomatic stage before disease progression. J Virol 68: 4400–4408.

43. KimataJT, KullerL, AndersonDB, DaileyP, OverbaughJ (1999) Emerging cytopathic and antigenic simian immunodeficiency virus variants influence AIDS progression. Nat Med 5: 535–541.

44. Holmes EC (2009) The Evolution and Emergence of RNA viruses. Oxford: Oxford University Press.

45. PopM, PhillippyA, DelcherAL, SalzbergSL (2004) Comparative genome assembly. Briefings Bioinformat 5: 237–248.

46. MartinDP, LemeyP, LottM, MoultonV, PosadaD, et al. (2010) RDP3: a flexible and fast computer program for analyzing recombination. Bioinformatics 26: 2462.

47. Swofford DL (2003) PAUP*. Phylogenetic Analysis Using Parsimony (*and other methods). Version 4. Sunderland, Mass: Sinauer Associates.

48. MosesA (1911) O virus do myxoma dos coelhos. Mem Inst Osw Cruz 3: 46–53.

49. RussellRJ, RobbinsSJ (1989) Cloning and molecular characterization of the myxoma virus genome. Virology 170: 147–159.

50. BermanD, KerrPJ, Stagg R. van LeeuwenBH, GonzalezT (2006) Should the 40-year-old practice of releasing virulent myxoma virus to control rabbits (Oryctolagus cuniculus) be continued? Wildl Res 33: 549–556.