Rapid Evolution of PARP Genes Suggests a Broad Role for ADP-Ribosylation in Host-Virus Conflicts

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The outcome of viral infections is determined by the repertoire and specificity of the antiviral genes in a particular animal species. The identification of candidate immunity genes and mechanisms is a key step in describing this repertoire. Despite advances in genome sequencing, identification of antiviral genes has largely remained dependent on demonstration of their activity against candidate viruses. However, antiviral proteins that directly interact with viral targets or antagonists also bear signatures of recurrent evolutionary adaptation, which can be used to identify candidate antivirals. Here, we find that five out of seventeen genes that contain a domain that can catalyze the post-translational addition ADP-ribose to proteins bear such signatures of recurrent genetic innovation. In particular, we find that all the genes that encode both ADP-ribose addition (via PARP domains) as well as recognition and/or removal (via macro domains) activities have evolved under extremely strong diversifying selection in mammals. Furthermore, such genes have undergone multiple episodes of gene duplications and losses throughout mammalian evolution. Combined with the knowledge that some viruses also encode macro domains to counteract host immunity, our evolutionary analyses therefore implicate ADP-ribosylation as an underappreciated key step in antiviral defense in mammalian genomes.

Vyšlo v časopise: Rapid Evolution of PARP Genes Suggests a Broad Role for ADP-Ribosylation in Host-Virus Conflicts. PLoS Genet 10(5): e32767. doi:10.1371/journal.pgen.1004403
Kategorie: Research Article
prolekare.web.journal.doi_sk: https://doi.org/10.1371/journal.pgen.1004403

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Zdroje

1. SalomonD, OrthK (2013) What pathogens have taught us about posttranslational modifications. Cell Host Microbe 14: 269–279.

2. AdhyaD, BasuA (2010) Epigenetic modulation of host: new insights into immune evasion by viruses. J Biosci 35: 647–663.

3. IsaacsonMK, PloeghHL (2009) Ubiquitination, ubiquitin-like modifiers, and deubiquitination in viral infection. Cell Host Microbe 5: 559–570.

4. HottigerMO, HassaPO, LuscherB, SchulerH, Koch-NolteF (2010) Toward a unified nomenclature for mammalian ADP-ribosyltransferases. Trends Biochem Sci 35: 208–219.

5. ZieglerM (2000) New functions of a long-known molecule. Emerging roles of NAD in cellular signaling. Eur J Biochem 267: 1550–1564.

6. GibsonBA, KrausWL (2012) New insights into the molecular and cellular functions of poly(ADP-ribose) and PARPs. Nat Rev Mol Cell Biol 13: 411–424.

7. HassaPO, HottigerMO (2008) The diverse biological roles of mammalian PARPS, a small but powerful family of poly-ADP-ribose polymerases. Front Biosci 13: 3046–3082.

8. SchreiberV, DantzerF, AmeJC, de MurciaG (2006) Poly(ADP-ribose): novel functions for an old molecule. Nat Rev Mol Cell Biol 7: 517–528.

9. CitarelliM, TeotiaS, LambRS (2010) Evolutionary history of the poly(ADP-ribose) polymerase gene family in eukaryotes. BMC Evol Biol 10: 308.

10. OttoH, RechePA, BazanF, DittmarK, HaagF, et al. (2005) In silico characterization of the family of PARP-like poly(ADP-ribosyl)transferases (pARTs). BMC Genomics 6: 139.

11. VyasS, Chesarone-CataldoM, TodorovaT, HuangYH, ChangP (2013) A systematic analysis of the PARP protein family identifies new functions critical for cell physiology. Nat Commun 4: 2240.

12. FeijsKL, VerheugdP, LuscherB (2013) Expanding functions of intracellular resident mono-ADP-ribosylation in cell physiology. FEBS J 280: 3519–3529.

13. LeungA, TodorovaT, AndoY, ChangP (2012) Poly(ADP-ribose) regulates post-transcriptional gene regulation in the cytoplasm. RNA Biol 9: 542–548.

14. SeoGJ, KincaidRP, PhanaksriT, BurkeJM, PareJM, et al. (2013) Reciprocal inhibition between intracellular antiviral signaling and the RNAi machinery in mammalian cells. Cell Host Microbe 14: 435–445.

15. RosenthalF, FeijsKL, FrugierE, BonalliM, ForstAH, et al. (2013) Macrodomain-containing proteins are new mono-ADP-ribosylhydrolases. Nat Struct Mol Biol 20: 502–507.

16. JankeviciusG, HasslerM, GoliaB, RybinV, ZachariasM, et al. (2013) A family of macrodomain proteins reverses cellular mono-ADP-ribosylation. Nat Struct Mol Biol 20: 508–514.

17. ChildSJ, FrankeCA, HrubyDE (1988) Inhibition of vaccinia virus replication by nicotinamide: evidence for ADP-ribosylation of viral proteins. Virus Res 9: 119–132.

18. LiZ, YamauchiY, KamakuraM, MurayamaT, GoshimaF, et al. (2012) Herpes simplex virus requires poly(ADP-ribose) polymerase activity for efficient replication and induces extracellular signal-related kinase-dependent phosphorylation and ICP0-dependent nuclear localization of tankyrase 1. J Virol 86: 492–503.

19. FeijsKL, ForstAH, VerheugdP, LuscherB (2013) Macrodomain-containing proteins: regulating new intracellular functions of mono(ADP-ribosyl)ation. Nat Rev Mol Cell Biol 14: 443–451.

20. ParkE, GriffinDE (2009) The nsP3 macro domain is important for Sindbis virus replication in neurons and neurovirulence in mice. Virology 388: 305–314.

21. KuriT, ErikssonKK, PuticsA, ZustR, SnijderEJ, et al. (2011) The ADP-ribose-1''-monophosphatase domains of severe acute respiratory syndrome coronavirus and human coronavirus 229E mediate resistance to antiviral interferon responses. J Gen Virol 92: 1899–1905.

22. SchogginsJW, RiceCM (2011) Interferon-stimulated genes and their antiviral effector functions. Curr Opin Virol 1: 519–525.

23. GaoG, GuoX, GoffSP (2002) Inhibition of retroviral RNA production by ZAP, a CCCH-type zinc finger protein. Science 297: 1703–1706.

24. MullerS, MollerP, BickMJ, WurrS, BeckerS, et al. (2007) Inhibition of filovirus replication by the zinc finger antiviral protein. J Virol 81: 2391–2400.

25. BickMJ, CarrollJW, GaoG, GoffSP, RiceCM, et al. (2003) Expression of the zinc-finger antiviral protein inhibits alphavirus replication. J Virol 77: 11555–11562.

26. MaoR, NieH, CaiD, ZhangJ, LiuH, et al. (2013) Inhibition of hepatitis B virus replication by the host zinc finger antiviral protein. PLoS Pathog 9: e1003494.

27. GuoX, CarrollJW, MacdonaldMR, GoffSP, GaoG (2004) The zinc finger antiviral protein directly binds to specific viral mRNAs through the CCCH zinc finger motifs. J Virol 78: 12781–12787.

28. GuoX, MaJ, SunJ, GaoG (2007) The zinc-finger antiviral protein recruits the RNA processing exosome to degrade the target mRNA. Proc Natl Acad Sci U S A 104: 151–156.

29. LeungAK, VyasS, RoodJE, BhutkarA, SharpPA, et al. (2011) Poly(ADP-ribose) regulates stress responses and microRNA activity in the cytoplasm. Mol Cell 42: 489–499.

30. TemperaI, DengZ, AtanasiuC, ChenCJ, D'ErmeM, et al. (2010) Regulation of Epstein-Barr virus OriP replication by poly(ADP-ribose) polymerase 1. J Virol 84: 4988–4997.

31. OhsakiE, UedaK, SakakibaraS, DoE, YadaK, et al. (2004) Poly(ADP-ribose) polymerase 1 binds to Kaposi's sarcoma-associated herpesvirus (KSHV) terminal repeat sequence and modulates KSHV replication in latency. J Virol 78: 9936–9946.

32. BuenoMT, ReyesD, ValdesL, SahebaA, UriasE, et al. (2013) Poly(ADP-ribose) polymerase 1 promotes transcriptional repression of integrated retroviruses. J Virol 87: 2496–2507.

33. AtashevaS, AkhrymukM, FrolovaEI, FrolovI (2012) New PARP gene with an anti-alphavirus function. J Virol 86: 8147–8160.

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

35. MitchellPS, PatzinaC, EmermanM, HallerO, MalikHS, et al. (2012) Evolution-guided identification of antiviral specificity determinants in the broadly acting interferon-induced innate immunity factor MxA. Cell Host Microbe 12: 598–604.

36. SawyerSL, WuLI, EmermanM, MalikHS (2005) Positive selection of primate TRIM5alpha identifies a critical species-specific retroviral restriction domain. Proc Natl Acad Sci U S A 102: 2832–2837.

37. KernsJA, EmermanM, MalikHS (2008) Positive selection and increased antiviral activity associated with the PARP-containing isoform of human zinc-finger antiviral protein. PLoS Genet 4: e21.

38. SawyerSL, EmermanM, MalikHS (2007) Discordant evolution of the adjacent antiretroviral genes TRIM22 and TRIM5 in mammals. PLoS Pathog 3: e197.

39. MunkC, WillemsenA, BravoIG (2012) An ancient history of gene duplications, fusions and losses in the evolution of APOBEC3 mutators in mammals. BMC Evol Biol 12: 71.

40. YangZ (2007) PAML 4: phylogenetic analysis by maximum likelihood. Mol Biol Evol 24: 1586–1591.

41. PondSL, FrostSD, MuseSV (2005) HyPhy: hypothesis testing using phylogenies. Bioinformatics 21: 676–679.

42. Kosakovsky PondSL, MurrellB, FourmentM, FrostSD, DelportW, et al. (2011) A random effects branch-site model for detecting episodic diversifying selection. Mol Biol Evol 28: 3033–3043.

43. WongWS, YangZ, GoldmanN, NielsenR (2004) Accuracy and power of statistical methods for detecting adaptive evolution in protein coding sequences and for identifying positively selected sites. Genetics 168: 1041–1051.

44. van ZonA, MossinkMH, ScheperRJ, SonneveldP, WiemerEA (2003) The vault complex. Cell Mol Life Sci 60: 1828–1837.

45. BergerW, SteinerE, GruschM, ElblingL, MickscheM (2009) Vaults and the major vault protein: novel roles in signal pathway regulation and immunity. Cell Mol Life Sci 66: 43–61.

46. ColeC, BarberJD, BartonGJ (2008) The Jpred 3 secondary structure prediction server. Nucleic Acids Res 36: W197–201.

47. BarkauskaiteE, JankeviciusG, LadurnerAG, AhelI, TiminszkyG (2013) The recognition and removal of cellular poly(ADP-ribose) signals. FEBS J 280: 3491–3507.

48. ForstAH, KarlbergT, HerzogN, ThorsellAG, GrossA, et al. (2013) Recognition of mono-ADP-ribosylated ARTD10 substrates by ARTD8 macrodomains. Structure 21: 462–475.

49. HolbournKP, ShoneCC, AcharyaKR (2006) A family of killer toxins. Exploring the mechanism of ADP-ribosylating toxins. FEBS J 273: 4579–4593.

50. JuszczynskiP, KutokJL, LiC, MitraJ, AguiarRC, et al. (2006) BAL1 and BBAP are regulated by a gamma interferon-responsive bidirectional promoter and are overexpressed in diffuse large B-cell lymphomas with a prominent inflammatory infiltrate. Mol Cell Biol 26: 5348–5359.

51. SchogginsJW, WilsonSJ, PanisM, MurphyMY, JonesCT, et al. (2011) A diverse range of gene products are effectors of the type I interferon antiviral response. Nature 472: 481–485.

52. MedzhitovR, SchneiderDS, SoaresMP (2012) Disease tolerance as a defense strategy. Science 335: 936–941.

53. LanglandJO, CameronJM, HeckMC, JancovichJK, JacobsBL (2006) Inhibition of PKR by RNA and DNA viruses. Virus Res 119: 100–110.

54. MeylanE, CurranJ, HofmannK, MoradpourD, BinderM, et al. (2005) Cardif is an adaptor protein in the RIG-I antiviral pathway and is targeted by hepatitis C virus. Nature 437: 1167–1172.

55. YangY, LiangY, QuL, ChenZ, YiM, et al. (2007) Disruption of innate immunity due to mitochondrial targeting of a picornaviral protease precursor. Proc Natl Acad Sci U S A 104: 7253–7258.

56. MukherjeeA, MoroskySA, Delorme-AxfordE, Dybdahl-SissokoN, ObersteMS, et al. (2011) The coxsackievirus B 3C protease cleaves MAVS and TRIF to attenuate host type I interferon and apoptotic signaling. PLoS Pathog 7: e1001311.

57. DrahosJ, RacanielloVR (2009) Cleavage of IPS-1 in cells infected with human rhinovirus. J Virol 83: 11581–11587.

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

59. PatelMR, LooYM, HornerSM, GaleMJr, MalikHS (2012) Convergent evolution of escape from hepaciviral antagonism in primates. PLoS Biol 10: e1001282.

60. BeckhamCJ, ParkerR (2008) P bodies, stress granules, and viral life cycles. Cell Host Microbe 3: 206–212.

61. AguiarRC, YakushijinY, KharbandaS, SalgiaR, FletcherJA, et al. (2000) BAL is a novel risk-related gene in diffuse large B-cell lymphomas that enhances cellular migration. Blood 96: 4328–4334.

62. ChoSH, RaybuckA, WeiM, EricksonJ, NamKT, et al. (2013) B cell-intrinsic and -extrinsic regulation of antibody responses by PARP14, an intracellular (ADP-ribosyl)transferase. J Immunol 191: 3169–3178.

63. Drummond AJ, Ashton B, Buxton S, Cheung M, Cooper A, et al.. (2011) Geneious v5.0. Available from www.geneious.com.

64. ComeronJM (1999) K-Estimator: calculation of the number of nucleotide substitutions per site and the confidence intervals. Bioinformatics 15: 763–764.

65. AltschulSF, MaddenTL, SchafferAA, ZhangJ, ZhangZ, et al. (1997) Gapped BLAST and PSI-BLAST: a new generation of protein database search programs. Nucleic Acids Res 25: 3389–3402.

66. SonnhammerEL, DurbinR (1995) A dot-matrix program with dynamic threshold control suited for genomic DNA and protein sequence analysis. Gene 167: GC1–10.

67. ZhouL, PerteaM, DelcherAL, FloreaL (2009) Sim4cc: a cross-species spliced alignment program. Nucleic Acids Res 37: e80.

68. LarkinMA, BlackshieldsG, BrownNP, ChennaR, McGettiganPA, et al. (2007) Clustal W and Clustal X version 2.0. Bioinformatics 23: 2947–2948.

69. GuindonS, DufayardJF, LefortV, AnisimovaM, HordijkW, et al. (2010) New algorithms and methods to estimate maximum-likelihood phylogenies: assessing the performance of PhyML 3.0. Syst Biol 59: 307–321.

70. AbascalF, ZardoyaR, PosadaD (2005) ProtTest: selection of best-fit models of protein evolution. Bioinformatics 21: 2104–2105.

71. TamuraK, StecherG, PetersonD, FilipskiA, KumarS (2013) MEGA6: Molecular Evolutionary Genetics Analysis Version 6.0. Mol Biol Evol 30: 2725–2729.

72. Delano WL (2006) The PyMOL molecular graphics system. v.0.99. Delano Scientific.