Evolution of the Retroviral Restriction Gene : Inhibition of Non-MLV Retroviruses
We have followed the evolution of the retroviral restriction gene, Fv1, by functional analysis. We show that Fv1 can recognize and restrict a wider range of retroviruses than previously thought including examples from the gammaretrovirus, lentivirus and foamy virus genera. Nearly every Fv1 tested showed a different pattern of restriction activity. We also identify several hypervariable regions in the coding sequence containing positively selected amino acids that we show to be directly involved in determining restriction specificity. Our results strengthen the analogy between Fv1 and another capsid-binding, retrovirus restriction factor, TRIM5α. Although they share no sequence identity they appear to share a similar design and appear likely to recognise different targets by a mechanism involving multiple weak interactions between a virus-binding domain containing several variable regions and the surface of the viral capsid. We also describe a pattern of constant genetic change, implying that different species of Mus have evolved in the face of ever-changing retroviral threats by viruses of different kinds.
Vyšlo v časopise:
Evolution of the Retroviral Restriction Gene : Inhibition of Non-MLV Retroviruses. PLoS Pathog 10(3): e32767. doi:10.1371/journal.ppat.1003968
Kategorie:
Research Article
prolekare.web.journal.doi_sk:
https://doi.org/10.1371/journal.ppat.1003968
Souhrn
We have followed the evolution of the retroviral restriction gene, Fv1, by functional analysis. We show that Fv1 can recognize and restrict a wider range of retroviruses than previously thought including examples from the gammaretrovirus, lentivirus and foamy virus genera. Nearly every Fv1 tested showed a different pattern of restriction activity. We also identify several hypervariable regions in the coding sequence containing positively selected amino acids that we show to be directly involved in determining restriction specificity. Our results strengthen the analogy between Fv1 and another capsid-binding, retrovirus restriction factor, TRIM5α. Although they share no sequence identity they appear to share a similar design and appear likely to recognise different targets by a mechanism involving multiple weak interactions between a virus-binding domain containing several variable regions and the surface of the viral capsid. We also describe a pattern of constant genetic change, implying that different species of Mus have evolved in the face of ever-changing retroviral threats by viruses of different kinds.
Zdroje
1. ComptonAA, HirschVM, EmermanM (2012) The host restriction factor APOBEC3G and retroviral Vif protein coeveolve due to ongoing genetic conflict. Cell Host and Microbe 11: 91–98.
2. EmermanM, MalikHS (2010) Paleovirology–modern consequences of ancient viruses. PLoS Biol 8: e1000301.
3. MeyersonNR, SawyerSL (2011) Two-stepping through time: mammals and viruses. Trends Microbiol 19: 286–294.
4. SauterD, UnterwegerD, VoglM, UsmaniSM, HeigeleA, et al. (2012) Human tetherin exerts strong selection pressure on the HIV-1 group N Vpu protein. PLoS Pathog 8: e1003093.
5. Goff SP (2007) Retroviridae: The retroviruses and their replication. In: Knipe DM, Griffin DE, Lamb RA, Strauss SE, Howley, Marting MA, Roizman B, editors. Fields Virology. Philadelphia: Lippincott Williams & Wilkins. Chapter 55: : pp1999–2069.
6. FeschotteC, GilbertC (2012) Endogenous viruses: insights into viral evolution and impact on host biology. Nat Rev Genet 13: 283–296.
7. StoyeJP (2012) Studies of endogenous retroviruses reveal a continuing evolutionary saga. Nat Rev Microbiol 10: 395–406.
8. AswadA, KatzourakisA (2012) Paleovirlogy and virally derived immunity. Trends in Ecology and Evolution 27: 627–36.
9. Sanz-RamosM, StoyeJP (2013) Capsid-binding retrovirus restriction factors: discovery, restriction specificity and implications for the development of novel therapeutics. J Gen Virol 94: 2587–98.
10. LillyF (1970) Fv-2: identification and location of a second gene governing the spleen focus response to Friend leukemia virus in mice. J Natl Cancer Inst 45: 163–169.
11. PincusT, HartleyJW, RoweWP (1971) A major genetic locus affecting resistance to infection with murine leukemia viruses. I. Tissue culture studies of naturally occurring viruses. J Exp Med 133: 1219–1233.
12. RoweWP (1972) Studies of genetic transmission of murine leukemia virus by AKR mice. I. Crosses with Fv-1 n strains of mice. J Exp Med 136: 1272–1285.
13. RoweWP, HartleyJW (1972) Studies of genetic transmission of murine leukemia virus by AKR mice. II. Crosses with Fv-1 b strains of mice. J Exp Med 136: 1286–1301.
14. KozakCA, ChakrabortiA (1996) Single amino acid changes in the murine leukemia virus capsid protein gene define the target of Fv1 resistance. Virology 225: 300–305.
15. HopkinsN, SchindlerJ, HynesR (1977) Six NB-tropic leukemia viruses derived from a B-tropic virus of BALB/c have altered p30. J Virol 21: 309–318.
16. StevensA, BockM, EllisS, LeTissierP, BishopKN, et al. (2004) Retroviral capsid determinants of Fv1 NB- and NR-tropism. J Virol 78: 9592–9598.
17. JolicoeurP, RassartE (1980) Effect of Fv-1 gene product on synthesis of linear and supercoiled viral DNA in cells infected with murine leukemia virus. J Virol 33: 183–195.
18. BestS, Le TissierP, TowersG, StoyeJP (1996) Positional cloning of the mouse retrovirus restriction gene Fv1. Nature 382: 826–829.
19. YapMW, NisoleS, LynchC, StoyeJP (2004) Trim5α protein restricts both HIV-1 and murine leukemia virus. Proc Natl Acad Sci U S A 101: 10786–10791.
20. StremlauM, OwensCM, PerronMJ, KiesslingM, AutisslerP, et al. (2004) The cytoplasmic body component TRIM5α restricts HIV-1 infection in Old World monkeys. Nature 427: 848–853.
21. StremlauM, PerronM, LeeM, LiY, SongB, et al. (2006) Specific recognition and accelerated uncoating of retroviral capsids by the TRIM5a restriction factor. Proc Natl Acad Sci U S A 103: 5514–5519.
22. HilditchL, MatadeenR, GoldstoneDC, RosenthalPB, TaylorIA, et al. (2011) Ordered assembly of murine leukemia virus capsid protein on lipid nanotubes directs specific binding by the restriction factor, Fv1. Proc Natl Acad Sci U S A 108: 5771–5776.
23. YapMW, MortuzaGB, TaylorIA, StoyeJP (2007) The design of artificial retroviral restriction factors. Virology 365: 302–314.
24. OhkuraS, YapMW, SheldonT, StoyeJP (2006) All three variable regions of the TRIM5a B30.2 domain can contribute to the specificity of retrovirus restriction. J Virol 80: 8554–8565.
25. SchallerT, HuéS, TowersGJ (2007) An active TRIM5 protein in rabbits indicates a common antiviral ancestor for mammalian TRIM5 proteins. J Virol 81: 11713–11721.
26. YlinenLMJ, KeckesovaZ, WebbBLJ, GiffordRJM, SmithTPL, et al. (2006) Isolation of an active Lv1 gene from cattle indicates that tripartite motif protein-mediated innate immunity to retroviral infection is widespread among mammals. J Virol 80: 7332–7338.
27. SiZ, VandegraaffN, O'hUiginC, SongB, YuanW, et al. (2006) Evolution of a cytoplasmic tripartite motif (TRIM) protein in cows that restricts retroviral infection. Proc Natl Acad Sci U S A 103: 7454–7459.
28. DiehlWE, StansellE, KaiserSM, EmermanM, HunterE (2008) Identification of Post-entry Restrictions to Mason-Pfizer Monkey Virus Infection in New World Monkey Cells. J Virol 82: 11140–11151.
29. YapMW, LindemannD, StankeN, RehJ, WestphalD, et al. (2008) Restriction of foamy viruses by primate Trim5alpha. J Virol 82: 5429–5439.
30. MortuzaGB, GoldstoneDC, PashleyC, HaireLF, PalmariniM, et al. (2009) Structure of the capsid amino-terminal domain from the betaretrovirus, Jaagsiekte sheep retrovirus. J Mol Biol 386: 1179–1192.
31. GoldstoneDC, FlowerTG, BallNJ, Sanz-RamosM, WYM, et al. (2013) A unique spumavirus Gag N-terminal domain with functional properties of orthoretroviral matrix and capsid. PLoS Pathog 5: e1003376 doi:1003310.1001371/journal.ppat.1003376
32. SawyerSL, WuLI, EmermanM, MalikHS (2005) Positive selection of primate TRIM5a identifies a critical species-specific retroviral restriction domain. Proc Natl Acad Sci U S A 102: 102.
33. HanK, LouDI, SawyerSL (2011) Identification of a genomic reservoir for new TRIM genes in primate genomes. PLoS Genet 7: e1002388.
34. GoldschmidtV, CiuffiA, OrtizM, BrawandD, MunozM, et al. (2008) Antiretroviral activity of ancestral TRIM5alpha. J Virol 82: 2089–2096.
35. JohnsonWE, SawyerSL (2009) Molecular evolution of the antiretroviral TRIM5 gene. Immunogenetics 61: 163–178.
36. KaiserSM, MalikHS, EmermanM (2007) Restriction of an extinct retrovirus by the human TRIM5a antiviral protein. Science 316: 1756–1758.
37. Perez-CaballeroD, SollSJ, BieniaszPD (2008) Evidence for restriction of ancient primate gammaretroviruses by APOBEC3 but not TRIM5a proteins. PLoS Pathogens 4: e1000181.
38. YapMW, StoyeJP (2013) Apparent effect of rabbit endogenous lentivirus type K acquisition on retrovirus restriction by lagomorph Trim5αs. Philos Trans R Soc Lond B Biol Sci 368 doi: 10.1098/rstb.2012.0498
39. QiCF, BonhommeF, Buckler-WhiteA, BucklerC, OrthA, et al. (1998) Molecular phylogeny of Fv1. Mamm Genome 9: 1049–1055.
40. YanY, Buckler-WhiteA, WollenbergK, KozakCA (2009) Origin, antiviral function and evidence for positive selection of the gammaretrovirus restriction gene Fv1 in the genus Mus. Proc Natl Acad Sci U S A 106: 3259–3263.
41. KozakCA, O'NeillRR (1987) Diverse wild mouse origins of xenotropic, mink cell focus-forming, and two types of ecotropic proviral genes. J Virol 61: 3082–3088.
42. TomonagaK, CoffinJM (1999) Structures of endogenous nonecotropic murine leukemia virus (MLV) long terminal repeats in wild mice: implication for evolution of MLVs. J Virol 73: 4327–4340.
43. Ellis SA (2000) Evolutionary and functional studies of the mouse retrovirus restriction gene, Fv1. PhD thesis, University of London.
44. GuénetJ-L, BonhommeF (2003) Wild mice: an ever-increasing contribution to a popular mammalian model. Trends in Genetics 19: 24–31.
45. BishopKN, MortuzaGB, HowellS, YapMW, StoyeJP, et al. (2006) Characterization of an amino-terminal dimerization domain from retroviral restriction factor Fv1. J Virol 80: 8225–8235.
46. CravenRC, Leure-duPreeAE, R. A. WeldonJ, WillsJW (1995) Genetic analysis of the major homology region of the Rous Sarcoma Virus Gag protein. J Virol 69: 4213–4227.
47. BénitL, de ParsevalN, CasellaJ-F, CallebautI, CordonnierA, et al. (1997) Cloning of a new murine endogenous retrovirus, MuERV-L, with strong similarity to the human HERV-L element and a gag coding sequence closely related to the Fv1 restriction gene. J Virol 71: 5652–5657.
48. BishopKN, BockM, TowersG, StoyeJP (2001) Identification of the regions of Fv1 necessary for MLV restriction. J Virol 75: 5182–5188.
49. LundriganBL, JansaSA, TuckerPK (2002) Phylogenetic relationships in the genus Mus, based on paterrnally, maternally and biparentally inherited characters. Syst Biol 51: 410–431.
50. ChevretP, JenkinsP, CatzeflisF (2003) Evolutionary systematics of the Indian mouse Mus famulus Bonhote, 1898: molecular (DNA/DNA hybridization and 12S rRNA sequences) and morphological evidence. Zoological Journal of the Linnean Society 137: 385–401.
51. BockM, BishopKN, TowersG, StoyeJP (2000) Use of a transient assay for studying the genetic determinants of Fv1 restriction. J Virol 74: 7422–7430.
52. SloanRD, WainbergMD (2011) The role of unintegrated DNA in HIV infection. Retrovirology 8: 52.
53. YuSF, BaldwinDN, GwynnSR, YendapalliS, LinialML (1996) Human Foamy Virus replication: a pathway distinct from that of retroviruses and hepadnaviruses. Science 271: 1579–1582.
54. SayahDM, SokolskajaE, BerthouxL, LubanJ (2004) Cyclophilin A retrotransposition into TRIM5 explains owl monkey resistance to HIV-1. Nature 430: 569–573.
55. SongB, GoldB, O'hUiginC, JavanbakhtM, LiX, et al. (2005) The B30.2(SPRY) domain of retroviral restriction factor TRIM5a exhibits lineage-specific length and sequence variation in primates. J Virol 79: 6111–6121.
56. Perez-CaballeroD, HatziioannouT, YangA, CowanS, BieniaszPD (2005) Human tripartite motif 5α domains responsible for retrovirus restriction activity and specificity. J Virol 79: 8969–8978.
57. LiX, SodroskiJ (2008) The TRIM5{alpha} B-box 2 Domain Promotes Cooperative Binding to the Retroviral Capsid by Mediating Higher-order Self-association. J Virol 82: 11495–11502.
58. BestS, Le TissierPR, StoyeJP (1997) Endogenous retroviruses and the evolution of resistance to retroviral infection. Trends Microbiol 4: 313–318.
59. BénitL, LallemandJ-B, CasellaJ-F, PhilippeH, HeidmannT (1999) ERV-L elements: a family of endogenous retrovirus-like elements active through the evolution of mammals. J Virol 73: 3301–3308.
60. BamunusingheD, LiuQ, LuX, OlerA, KozakCA (2013) Endogenous gammaretrovirus acquisition in Mus musculus subspecies carrying functional variants of the XPR1 virus receptor. J Virol 87: 9845–9855.
61. OdakaT, IkedaH, YoshikuraH, MoriwakiK, SuzukiS (1981) Fv-4: gene controlling resistance to NB-tropic Friend murine leukemia virus. Distribution in wild mice, introduction into genetic background of BALB/c mice, and mapping of chromosomes. J Natl Cancer Inst 67: 1123–1127.
62. KozakCA (2013) Evolution of different antiviral strategies in wild mice exposed to different gammaretroviruses. Curr Opin Virol 3: 657–63.
63. LinialML (2000) Why aren't foamy viruses pathogenic? Trends Micribiol 8: 284–289.
64. ChoudharyA, GalvinTA, WilliamsDK, BerenJ, BryantMA, et al. (2013) Influence of naturally occurring simian foamy viruses (SFVs) on SIV disease progression in the rhesus macaque (Macaca mulatta) model. Viruses 5: 1414–1430.
65. LanderMR, ChattopadhyaySK (1984) A Mus dunni cell line that lacks sequences closely related to endogenous murine leukemia viruses and can be infected by ecotropic, amphotropic, xenotropic and mink cell focus-forming viruses. J Virol 52: 695–698.
66. GoldstoneDC, YapMW, RobertsonLE, HaireLF, TaylorWR, et al. (2010) Structural and functional analysis of prehistoric lentiviruses uncovers an ancient molecular interface. Cell Host Microbe 8: 248–259.
67. IkedaY, CollinsMK, RadcliffePA, MitrophanousKA, TakeuchiY (2002) Gene transduction efficiency in cells of different species by HIV and EIAV vectors. Gene Therapy 9: 932–938.
68. SerhanF, PenaudM, PetitC, Leste-LasserreT, TrajcevskiS, et al. (2004) Early detection of a two-long-terminal-repeat junction molecule in the cytoplasm of recombinant murine leukemia virus-infected cells. J Virol 78: 6190–6199.
69. LabudaD, SinnettD, RicherC, DeragonJ-M, StrikerG (1991) Evolution of mouse B1 repeats: 7SL RNA folding pattern conserved. J Mol Evol 32: 405–414.
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Hygiena a epidemiológia Infekčné lekárstvo LaboratóriumČlánok vyšiel v časopise
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