Adaptive Gene Amplification As an Intermediate Step in the Expansion of Virus Host Range

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The spread of microbes from animals to humans has been responsible for most recently emerging human infectious diseases, including AIDS, bird flu, and SARS. Therefore, understanding the evolutionary and molecular mechanisms underlying cross-species transmission is of critical importance for public health. After entering a new host cell, the success of a virus depends on its ability to overcome antiviral factors in the cell, such as protein kinase R (PKR). To investigate the process of virus transmission between species, we employed a recombinant vaccinia virus (VVΔEΔK+RhTRS1) expressing the rhesus cytomegalovirus PKR antagonist RhTRS1. This protein inhibits some African green monkey (AGM) PKRs; however, it does not inhibit human or rhesus variants of PKR. Serial passaging VVΔEΔK+RhTRS1 in RhTRS1-resistant AGM cells resulted in rhtrs1 duplication in the viral genome, which improved VVΔEΔK+RhTRS1 replication in AGM cells. Remarkably, rhtrs1 duplication also enhanced virus replication in human and rhesus cells. In contrast, passage of VVΔEΔK+RhTRS1 in human cells, without prior adaptation in AGM cells, did not improve VVΔEΔK+RhTRS1 replication. These results support the hypothesis that amplification of a weak viral antagonist of a host defense protein in one species may enable cross-species transmission into new hosts that are nonpermissive to the initial virus.

Vyšlo v časopise: Adaptive Gene Amplification As an Intermediate Step in the Expansion of Virus Host Range. PLoS Pathog 10(3): e32767. doi:10.1371/journal.ppat.1004002
Kategorie: Research Article
prolekare.web.journal.doi_sk: https://doi.org/10.1371/journal.ppat.1004002

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Zdroje

1. YamadaA (2004) [Zoonoses]. Uirusu 54: 17–22.

2. MahyBW (2000) The global threat of emerging infectious diseases. Isr Med Assoc J 2 Suppl: 23–26.

3. BengisRG, LeightonFA, FischerJR, ArtoisM, MornerT, et al. (2004) The role of wildlife in emerging and re-emerging zoonoses. Rev Sci Tech 23: 497–511.

4. ParrishCR, HolmesEC, MorensDM, ParkEC, BurkeDS, et al. (2008) Cross-species virus transmission and the emergence of new epidemic diseases. Microbiol Mol Biol Rev 72: 457–470.

5. ChuaKB (2003) Nipah virus outbreak in Malaysia. J Clin Virol 26: 265–275.

6. Daszak P, Plowright R, Epstein JH, Pulliam J, Abdul Rahman S, et al.. (2006) The emergence of Nipah and Hendra virus: pathogen dynamics across a wildlife-livestock-human continuum. In: Collinge RS, editors. Disease ecology: community structure and pathogen dynamics. Oxford, United Kingdom: Oxford University Press. pp. 186–201.

7. SharpPM, HahnBH (2011) Origins of HIV and the AIDS pandemic. Cold Spring Harb Perspect Med 1 (1) a006841.

8. StremlauM, OwensCM, PerronMJ, KiesslingM, AutissierP, et al. (2004) The cytoplasmic body component TRIM5alpha restricts HIV-1 infection in Old World monkeys. Nature 427: 848–853.

9. SadlerAJ, WilliamsBR (2007) Structure and function of the protein kinase R. Curr Top Microbiol Immunol 316: 253–292.

10. Mohr IJ, Pe'ery T, Mathews MB (2007) Protein synthesis and translational control during viral infection. In: Mathews MB, Sonenberg N, Hershey JWB, editors. Translational control in biology and medicine. Cold Spring Harbor, NY: Cold Spring Harbor Laboratory Press. pp. 545–599.

11. DaughertyMD, MalikHS (2012) Rules of engagement: molecular insights from host-virus arms races. Annu Rev Genet 46: 677–700.

12. EldeNC, ChildSJ, GeballeAP, MalikHS (2009) Protein kinase R reveals an evolutionary model for defeating viral mimicry. Nature 457: 485–489.

13. RothenburgS, SeoEJ, GibbsJS, DeverTE, DittmarK (2009) Rapid evolution of protein kinase PKR alters sensitivity to viral inhibitors. Nat Struct Mol Biol 16: 63–70.

14. BrownCJ, ToddKM, RosenzweigRF (1998) Multiple duplications of yeast hexose transport genes in response to selection in a glucose-limited environment. Mol Biol Evol 15: 931–942.

15. GonzalezE, KulkarniH, BolivarH, ManganoA, SanchezR, et al. (2005) The influence of CCL3L1 gene-containing segmental duplications on HIV-1/AIDS susceptibility. Science 307: 1434–1440.

16. RothJR, AnderssonDI (2004) Amplification-mutagenesis–how growth under selection contributes to the origin of genetic diversity and explains the phenomenon of adaptive mutation. Res Microbiol 155: 342–351.

17. EldeNC, ChildSJ, EickbushMT, KitzmanJO, RogersKS, et al. (2012) Poxviruses deploy genomic accordions to adapt rapidly against host antiviral defenses. Cell 150: 831–841.

18. SlabaughM, RosemanN, DavisR, MathewsC (1988) Vaccinia virus-encoded ribonucleotide reductase: sequence conservation of the gene for the small subunit and its amplification in hydroxyurea-resistant mutants. J Virol 62: 519–527.

19. KondrashovFA (2012) Gene duplication as a mechanism of genomic adaptation to a changing environment. Proc Biol Sci 279: 5048–5057.

20. ChildSJ, BrennanG, BragginJE, GeballeAP (2012) Species specificity of protein kinase r antagonism by cytomegalovirus TRS1 genes. J Virol 86: 3880–3889.

21. SlabaughMB, RosemanNA, MathewsCK (1989) Amplification of the ribonucleotide reductase small subunit gene: analysis of novel joints and the mechanism of gene duplication in vaccinia virus. Nucleic Acids Res 17: 7073–7088.

22. ChildSJ, BrennanG, BragginJE, GeballeAP (2012) Species specificity of protein kinase r antagonism by cytomegalovirus TRS1 genes. J Virol 86: 3880–3889.

23. GarciaMA, MeursEF, EstebanM (2007) The dsRNA protein kinase PKR: virus and cell control. Biochimie 89: 799–811.

24. JonesKE, PatelNG, LevyMA, StoreygardA, BalkD, et al. (2008) Global trends in emerging infectious diseases. Nature 451: 990–993.

25. BaylissCD, ConditRC (1993) Temperature-sensitive mutants in the vaccinia virus A18R gene increase double-stranded RNA synthesis as a result of aberrant viral transcription. Virology 194: 254–262.

26. CresawnSG, PrinsC, LatnerDR, ConditRC (2007) Mapping and phenotypic analysis of spontaneous isatin-beta-thiosemicarbazone resistant mutants of vaccinia virus. Virology 363: 319–332.

27. RehmKE, ConnorRF, JonesGJ, YimbuK, RoperRL (2010) Vaccinia virus A35R inhibits MHC class II antigen presentation. Virology 397: 176–186.

28. RehmKE, RoperRL (2011) Deletion of the A35 gene from Modified Vaccinia Virus Ankara increases immunogenicity and isotype switching. Vaccine 29: 3276–3283.

29. TalloczyZ, JiangW, VirginHW, LeibDA, ScheunerD, et al. (2002) Regulation of starvation- and virus-induced autophagy by the eIF2alpha kinase signaling pathway. Proc Natl Acad Sci U S A 99: 190–195.

30. LuB, NakamuraT, InouyeK, LiJ, TangY, et al. (2012) Novel role of PKR in inflammasome activation and HMGB1 release. Nature 488: 670–674 nature11290.

31. HettEC, SlaterLH, MarkKG, KawateT, MonksBG, et al. (2013) Chemical genetics reveals a kinase-independent role for protein kinase R in pyroptosis. Nat Chem Biol 9: 398–405 nchembio.1236 [pii];10.1038/nchembio.1236 [doi].

32. ChildSJ, HakkiM, De NiroKL, GeballeAP (2004) Evasion of cellular antiviral responses by human cytomegalovirus TRS1 and IRS1. J Virol 78: 197–205.

33. TartagliaJ, PerkusME, TaylorJ, NortonEK, AudonnetJC, et al. (1992) NYVAC: a highly attenuated strain of vaccinia virus. Virology 188: 217–232.

34. BeattieE, PaolettiE, TartagliaJ (1995) Distinct patterns of IFN sensitivity observed in cells infected with vaccinia K3L- and E3L- mutant viruses. Virology 210: 254–263.

35. BeattieE, TartagliaJ, PaolettiE (1991) Vaccinia virus-encoded eIF-2 alpha homolog abrogates the antiviral effect of interferon. Virology 183: 419–422.

36. RahmanMM, LiuJ, ChanWM, RothenburgS, McFaddenG (2013) Myxoma Virus Protein M029 Is a Dual Function Immunomodulator that Inhibits PKR and Also Conscripts RHA/DHX9 to Promote Expanded Host Tropism and Viral Replication. PLoS Pathog 9: e1003465.

37. MarshallEE, BierleCJ, BruneW, GeballeAP (2009) Essential role for either TRS1 or IRS1 in human cytomegalovirus replication. J Virol 83: 4112–4120.

38. ChennaR, SugawaraH, KoikeT, LopezR, GibsonTJ, et al. (2003) Multiple sequence alignment with the Clustal series of programs. Nucleic Acids Res 31: 3497–3500.

39. EspositoJ, ConditR, ObijeskiJ (1981) The preparation of orthopoxvirus DNA. J Virol Methods 2: 175–179.

40. SimpsonJT, WongK, JackmanSD, ScheinJE, JonesSJ, et al. (2009) ABySS: a parallel assembler for short read sequence data. Genome Res 19: 1117–1123.

41. LiH, DurbinR (2009) Fast and accurate short read alignment with Burrows-Wheeler transform. Bioinformatics 25: 1754–1760 btp324.

42. McKennaA, HannaM, BanksE, SivachenkoA, CibulskisK, et al. (2010) The Genome Analysis Toolkit: a MapReduce framework for analyzing next-generation DNA sequencing data. Genome Res 20: 1297–1303.

43. LiH, DurbinR (2010) Fast and accurate long-read alignment with Burrows-Wheeler transform. Bioinformatics 26: 589–595.

44. KurtzS, PhillippyA, DelcherAL, SmootM, ShumwayM, et al. (2004) Versatile and open software for comparing large genomes. Genome Biol 5: R12 10.1186/gb-2004-5-2-r12 [doi];gb-2004-5-2-r12 [pii].