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Not so unique to Primates: The independent adaptive evolution of TRIM5 in Lagomorpha lineage


Autoři: Ana Águeda-Pinto aff001;  Ana Lemos de Matos aff003;  Ana Pinheiro aff001;  Fabiana Neves aff001;  Patrícia de Sousa-Pereira aff001;  Pedro J. Esteves aff001
Působiště autorů: CIBIO/InBio—Centro de Investigação em Biodiversidade e Recursos Genéticos, Universidade do Porto, Campus Agrário de Vairão, Vairão, Portugal aff001;  Departamento de Biologia, Faculdade de Ciências, Universidade do Porto,Porto, Portugal aff002;  Center for Immunotherapy, Vaccines, and Virotherapy (CIVV), The Biodesign Institute, Arizona State University, Tempe, Arizona, United States of America aff003;  CITS—Centro de Investigação em Tecnologias da Saúde, IPSN, CESPU,Gandra, Portugal aff004
Vyšlo v časopise: PLoS ONE 14(12)
Kategorie: Research Article
doi: https://doi.org/10.1371/journal.pone.0226202

Souhrn

The plethora of restriction factors with the ability to inhibit the replication of retroviruses have been widely studied and genetic hallmarks of evolutionary selective pressures in Primates have been well documented. One example is the tripartite motif-containing protein 5 alpha (TRIM5α), a cytoplasmic factor that restricts retroviral infection in a species-specific fashion. In Lagomorphs, similarly to what has been observed in Primates, the specificity of TRIM5 restriction has been assigned to the PRYSPRY domain. In this study, we present the first insight of an intra-genus variability within the Lagomorpha TRIM5 PRYSPRY domain. Remarkably, and considering just the 32 residue-long v1 region of this domain, the deduced amino acid sequences of Daurian pika (Ochotona dauurica) and steppe pika (O. pusilla) evidenced a high divergence when compared to the remaining Ochotona species, presenting values of 44% and 66% of amino acid differences, respectively. The same evolutionary pattern was also observed when comparing the v1 region of two Sylvilagus species members (47% divergence). However, and unexpectedly, the PRYSPRY domain of Lepus species exhibited a great conservation. Our results show a high level of variation in the PRYSPRY domain of Lagomorpha species that belong to the same genus. This suggests that, throughout evolution, the Lagomorpha TRIM5 should have been influenced by constant selective pressures, likely as a result of multiple different retroviral infections.

Klíčová slova:

Hares – Primates – Rabbits – Sequence alignment – Sequence databases – Viral evolution – Pikas


Zdroje

1. Duggal NK, Emerman M. Evolutionary conflicts between viruses and restriction factors shape immunity. Nature Reviews Immunology. 2012;12:687. doi: 10.1038/nri3295 22976433

2. Jern P, Coffin JM. Effects of Retroviruses on Host Genome Function. Annual Review of Genetics. 2008;42(1):709–32. doi: 10.1146/annurev.genet.42.110807.091501 18694346.

3. Chan YK, Gack MU. Viral evasion of intracellular DNA and RNA sensing. Nature Reviews Microbiology. 2016;14:360. doi: 10.1038/nrmicro.2016.45 27174148

4. Hall JC, Rosen A. Type I interferons: crucial participants in disease amplification in autoimmunity. Nature Reviews Rheumatology. 2010;6:40. doi: 10.1038/nrrheum.2009.237 20046205

5. Malim MH, Bieniasz PD. HIV restriction factors and mechanisms of evasion. Cold Spring Harbor perspectives in medicine. 2012;2(5):a006940–a. doi: 10.1101/cshperspect.a006940 22553496.

6. Hatziioannou T, Bieniasz PD. Antiretroviral restriction factors. Current opinion in virology. 2011;1(6):526–32. doi: 10.1016/j.coviro.2011.10.007 22278313.

7. Boso G, Buckler-White A, Kozak CA. Ancient Evolutionary Origin and Positive Selection of the Retroviral Restriction Factor Fv1 in Muroid Rodents. J Virol. 2018;92(18). doi: 10.1128/jvi.00850-18 29976659

8. Pertel T, Hausmann S, Morger D, Züger S, Guerra J, Lascano J, et al. TRIM5 is an innate immune sensor for the retrovirus capsid lattice. Nature. 2011;472(7343):361–5. doi: 10.1038/nature09976 21512573.

9. Sawyer SL, Wu LI, Emerman M, Malik HS. Positive selection of primate TRIM5α identifies a critical species-specific retroviral restriction domain. Proc Natl Acad Sci U S A. 2005;102(8):2832–7. doi: 10.1073/pnas.0409853102 15689398

10. Han K, Lou DI, Sawyer SL. Identification of a genomic reservoir for new TRIM genes in primate genomes. PLOS Genetics. 2011;7(12):e1002388. doi: 10.1371/journal.pgen.1002388 22144910

11. Goldschmidt V, Ciuffi A, Ortiz M, Brawand D, Muñoz M, Kaessmann H, et al. Antiretroviral Activity of Ancestral TRIM5α. J Virol. 2008;82(5):2089–96. doi: 10.1128/JVI.01828-07 18077724

12. Sawyer SL, Emerman M, Malik HS. Discordant evolution of the adjacent antiretroviral genes TRIM22 and TRIM5 in Mammals. PLOS Pathogens. 2007;3(12):e197. doi: 10.1371/journal.ppat.0030197 18159944

13. Schaller T, Hué S, Towers GJ. An active TRIM5 protein in rabbits indicates a common antiviral ancestor for mammalian TRIM5 proteins. J Virol. 2007;81(21):11713–21. doi: 10.1128/JVI.01468-07 17728224

14. Si Z, Vandegraaff N, O’hUigin C, Song B, Yuan W, Xu C, et al. Evolution of a cytoplasmic tripartite motif (TRIM) protein in cows that restricts retroviral infection. Proceedings of the National Academy of Sciences. 2006;103(19):7454–9. doi: 10.1073/pnas.0600771103 16648259

15. Hron T, Farkašová H, Padhi A, Pačes J, Elleder D. Life history of the oldest Lentivirus: characterization of ELVgv integrations in the dermopteran genome. Molecular Biology and Evolution. 2016;33(10):2659–69. doi: 10.1093/molbev/msw149 27507840

16. de Matos AL, van der Loo W, Areal H, Lanning DK, Esteves PJ. Study of Sylvilagus rabbit TRIM5α species-specific domain: how ancient endoviruses could have shaped the antiviral repertoire in Lagomorpha. BMC Evolutionary Biology. 2011;11(1):294. doi: 10.1186/1471-2148-11-294 21982459

17. Melo-Ferreira J, de Matos AL, Areal H, Lissovsky AA, Carneiro M, Esteves PJ. The phylogeny of pikas (Ochotona) inferred from a multilocus coalescent approach. Mol Phylogenet Evol. 2015;84:240–4. doi: 10.1016/j.ympev.2015.01.004 WOS:000352173500021. 25637497

18. Ge D, Wen Z, Xia L, Zhang Z, Erbajeva M, Huang C, et al. Evolutionary history of Lagomorphs in response to global environmental change. PLOS ONE. 2013;8(4):e59668. doi: 10.1371/journal.pone.0059668 23573205

19. Yap MW, Stoye JP. Apparent effect of rabbit endogenous lentivirus type K acquisition on retrovirus restriction by lagomorph Trim5αs. Philosophical transactions of the Royal Society of London Series B, Biological sciences. 368(1626):20120498–. doi: 10.1098/rstb.2012.0498 23938750.

20. Keckesova Z, Ylinen LMJ, Towers GJ, Gifford RJ, Katzourakis A. Identification of a RELIK orthologue in the European hare (Lepus europaeus) reveals a minimum age of 12 million years for the lagomorph lentiviruses. Virology. 2009;384(1):7–11. doi: 10.1016/j.virol.2008.10.045 19070882

21. Fletcher AJ, Hue S, Schaller T, Pillay D, Towers GJ. Hare TRIM5 alpha restricts divergent retroviruses and exhibits significant sequence variation from closely related Lagomorpha TRIM5 genes. J Virol. 2010;84(23):12463–8. doi: 10.1128/JVI.01514-10 WOS:000283799500037. 20861252

22. Yap MW, Stoye JP. Apparent effect of rabbit endogenous lentivirus type K acquisition on retrovirus restriction by lagomorph Trim5 alpha s. Philos Trans R Soc B-Biol Sci. 2013;368(1626):11. doi: 10.1098/rstb.2012.0498 WOS:000331222100004. 23938750

23. Song B, Javanbakht H, Perron M, Park DH, Stremlau M, Sodroski J. Retrovirus restriction by TRIM5α variants from Old World and New World Primates. J Virol. 2005;79(7):3930–7. doi: 10.1128/JVI.79.7.3930-3937.2005 15767395

24. Song B, Gold B, O'hUigin C, Javanbakht H, Li X, Stremlau M, et al. The B30.2(SPRY) domain of the retroviral restriction factor TRIM5α exhibits lineage-specific length and sequence variation in primates. J Virol. 2005;79(10):6111–21. doi: 10.1128/JVI.79.10.6111-6121.2005 15857996

25. Soares EA, Menezes AN, Schrago CG, Moreira MAM, Bonvicino CR, Soares MA, et al. Evolution of TRIM5α B30.2 (SPRY) domain in New World primates. Infection, Genetics and Evolution. 2010;10(2):246–53. doi: 10.1016/j.meegid.2009.11.012 19931648

26. Yang H, Ji X, Zhao G, Ning J, Zhao Q, Aiken C, et al. Structural insight into HIV-1 capsid recognition by rhesus TRIM52012.

27. Guindon S, Dufayard JF, Lefort V, Anisimova M, Hordijk W, Gascuel O. New Algorithms and Methods to Estimate Maximum-Likelihood Phylogenies: Assessing the Performance of PhyML 3.0. Syst Biol. 2010;59(3):307–21. doi: 10.1093/sysbio/syq010 WOS:000276528300006. 20525638

28. Wang H-Y, Tang H, Shen CKJ, Wu C-I. Rapidly evolving genes in human. I. The glycophorins and their possible role in evading malaria parasites. Molecular Biology and Evolution. 2003;20(11):1795–804. doi: 10.1093/molbev/msg185 12949139

29. Kosiol C, Vinař T, da Fonseca RR, Hubisz MJ, Bustamante CD, Nielsen R, et al. Patterns of positive selection in six mammalian genomes. PLOS Genetics. 2008;4(8):e1000144. doi: 10.1371/journal.pgen.1000144 18670650

30. Aguileta G, Refrégier G, Yockteng R, Fournier E, Giraud T. Rapidly evolving genes in pathogens: Methods for detecting positive selection and examples among fungi, bacteria, viruses and protists. Infection, Genetics and Evolution. 2009;9(4):656–70. doi: 10.1016/j.meegid.2009.03.010 19442589

31. James LC, Keeble AH, Khan Z, Rhodes DA, Trowsdale J. Structural basis for PRYSPRY-mediated tripartite motif (TRIM) protein function. Proc Natl Acad Sci U S A. 2007;104(15):6200–5. doi: 10.1073/pnas.0609174104 WOS:000245737500021. 17400754

32. Yap MW, Nisole S, Stoye JP. A single amino acid change in the SPRY domain of human TRIM5 alpha leads to HIV-1 restriction. Curr Biol. 2005;15(1):73–8. doi: 10.1016/j.cub.2004.12.042 WOS:000226715000029. 15649369

33. Kumar S, Stecher G, Tamura K. MEGA7: Molecular evolutionary genetics analysis version 7.0 for bigger datasets. Molecular Biology and Evolution. 2016;33(7):1870–4. doi: 10.1093/molbev/msw054 27004904

34. Perelman P, Johnson WE, Roos C, Seuánez HN, Horvath JE, Moreira MAM, et al. A molecular phylogeny of living primates. PLOS Genetics. 2011;7(3):e1001342. doi: 10.1371/journal.pgen.1001342 21436896

35. Diehl WE, Johnson WE, Hunter E. Elevated rate of fixation of endogenous retroviral elements in Haplorhini TRIM5 and TRIM22 genomic sequences: impact on transcriptional regulation. PloS one. 2013;8(3):e58532–e. doi: 10.1371/journal.pone.0058532 23516500.

36. Stremlau M, Perron M, Lee M, Li Y, Song B, Javanbakht H, et al. Specific recognition and accelerated uncoating of retroviral capsids by the TRIM5α restriction factor. Proceedings of the National Academy of Sciences. 2006;103(14):5514–9. doi: 10.1073/pnas.0509996103 16540544

37. McCarthy KR, Kirmaier A, Autissier P, Johnson WE. Evolutionary and functional analysis of old world primate TRIM5 reveals the ancient emergence of primate lentiviruses and convergent evolution targeting a conserved capsid interface. PLoS pathogens. 2015;11(8):e1005085–e. doi: 10.1371/journal.ppat.1005085 26291613.

38. Kratovac Z, Virgen CA, Bibollet-Ruche F, Hahn BH, Bieniasz PD, Hatziioannou T. Primate lentivirus capsid sensitivity to TRIM5 proteins. J Virol. 2008;82(13):6772–7. doi: 10.1128/JVI.00410-08 18417575

39. Johnson WE, Sawyer SL. Molecular evolution of the antiretroviral TRIM5 gene. Immunogenetics. 2009;61(3):163–76. doi: 10.1007/s00251-009-0358-y 19238338

40. Li Y-L, Chandrasekaran V, Carter SD, Woodward CL, Christensen DE, Dryden KA, et al. Primate TRIM5 proteins form hexagonal nets on HIV-1 capsids. eLife. 2016;5:e16269. doi: 10.7554/eLife.16269 27253068.

41. Javanbakht H, An P, Gold B, Petersen DC, O'Huigin C, Nelson GW, et al. Effects of human TRIM5α polymorphisms on antiretroviral function and susceptibility to human immunodeficiency virus infection. Virology. 2006;354(1):15–27. doi: 10.1016/j.virol.2006.06.031 16887163

42. Kovalskyy DB, Ivanov DN. Recognition of the hiv capsid by the TRIM5 alpha restriction factor is mediated by a subset of pre-existing conformations of the TRIM5 alpha SPRY domain. Biochemistry. 2014;53(9):1466–76. doi: 10.1021/bi4014962 WOS:000332913600009. 24506064

43. Katzourakis A, Tristem M, Pybus OG, Gifford RJ. Discovery and analysis of the first endogenous lentivirus. Proceedings of the National Academy of Sciences. 2007;104(15):6261–5. doi: 10.1073/pnas.0700471104 17384150

44. Chuong EB, Elde NC, Feschotte C. Regulatory evolution of innate immunity through co-option of endogenous retroviruses. Science. 2016;351(6277):1083–7. doi: 10.1126/science.aad5497 26941318

45. Patel MR, Emerman M, Malik HS. Paleovirology—ghosts and gifts of viruses past. Current Opinion in Virology. 2011;1(4):304–9. doi: 10.1016/j.coviro.2011.06.007 22003379

46. Rivas-Carrillo SD, Pettersson ME, Rubin C-J, Jern P. Whole-genome comparison of endogenous retrovirus segregation across wild and domestic host species populations. Proceedings of the National Academy of Sciences. 2018;115(43):11012–7. doi: 10.1073/pnas.1815056115 30297425

47. Hayward A, Cornwallis CK, Jern P. Pan-vertebrate comparative genomics unmasks retrovirus macroevolution. Proceedings of the National Academy of Sciences. 2015;112(2):464–9. doi: 10.1073/pnas.1414980112 25535393

48. de Matos AL, de Sousa-Pereira P, Lissovsky AA, van der Loo W, Melo-Ferreira J, Cui J, et al. Endogenization of mouse mammary tumor virus (MMTV)-like elements in genomes of pikas (Ochotona sp.). Virus Res. 2015;210:22–6. doi: 10.1016/j.virusres.2015.06.021 WOS:000365455500004. 26151606

49. Neves F, Abrantes J, Esteves PJ. Evolution of CCL11: genetic characterization in lagomorphs and evidence of positive and purifying selection in mammals. Innate Immunity. 2016;22(5):336–43. doi: 10.1177/1753425916647471 27189425.

50. de Sousa-Pereira P, Abrantes J, Baldauf H-M, Keppler OT, Esteves PJ. Evolutionary study of leporid CD4 reveals a hotspot of genetic variability within the D2 domain. Immunogenetics. 2016;68(6):477–82. doi: 10.1007/s00251-016-0909-y 26979977

51. Pinheiro A, Woof JM, Almeida T, Abrantes J, Alves PC, Gortázar C, et al. Leporid immunoglobulin G shows evidence of strong selective pressure on the hinge and CH3 domains. Open biology. 2014;4(9):140088. doi: 10.1098/rsob.140088 25185680

52. de Matos AL, McFadden G, Esteves PJ. Evolution of viral sensing RIG-I-like receptor genes in Leporidae genera Oryctolagus, Sylvilagus, and Lepus. Immunogenetics. 2014;66(1):43–52. doi: 10.1007/s00251-013-0740-7 WOS:000329096900006. 24220721

53. Hall TA, editor BioEdit: a user-friendly biological sequence alignment editor and analysis program for Windows 95/98/NT. Nucleic acids symposium series; 1999: [London]: Information Retrieval Ltd., c1979–c2000.

54. Thompson JD, Higgins DG, Gibson TJ. CLUSTAL-W—improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice. Nucleic Acids Res. 1994;22(22):4673–80. doi: 10.1093/nar/22.22.4673 WOS:A1994PU19900018. 7984417

55. Posada D. jModelTest: Phylogenetic Model Averaging. Molecular Biology and Evolution. 2008;25(7):1253–6. doi: 10.1093/molbev/msn083 18397919

56. Posada D, Crandall KA. The effect of recombination on the accuracy of phylogeny estimation. Journal of Molecular Evolution. 2002;54(3):396–402. doi: 10.1007/s00239-001-0034-9 11847565

57. Martin DP, Lemey P, Lott M, Moulton V, Posada D, Lefeuvre P. RDP3: a flexible and fast computer program for analyzing recombination. Bioinformatics. 2010;26(19):2462–+. doi: 10.1093/bioinformatics/btq467 WOS:000282170000017. 20798170

58. Yang Z. PAML 4: Phylogenetic Analysis by Maximum Likelihood. Molecular Biology and Evolution. 2007;24(8):1586–91. doi: 10.1093/molbev/msm088 17483113

59. Yang Z, Wong WSW, Nielsen R. Bayes Empirical Bayes inference of amino acid sites under positive selection. Molecular Biology and Evolution. 2005;22(4):1107–18. doi: 10.1093/molbev/msi097 15689528

60. Pond SLK, Frost SDW. Datamonkey: rapid detection of selective pressure on individual sites of codon alignments. Bioinformatics. 2005;21(10):2531–3. doi: 10.1093/bioinformatics/bti320 15713735

61. Delport W, Poon AFY, Frost SDW, Kosakovsky Pond SL. Datamonkey 2010: a suite of phylogenetic analysis tools for evolutionary biology. Bioinformatics. 2010;26(19):2455–7. doi: 10.1093/bioinformatics/btq429 20671151

62. Kosakovsky Pond SL, Frost SDW. Not so different after all: a comparison of methods for detecting amino acid sites under selection. Molecular Biology and Evolution. 2005;22(5):1208–22. doi: 10.1093/molbev/msi105 15703242

63. Murrell B, Wertheim JO, Moola S, Weighill T, Scheffler K, Kosakovsky Pond SL. Detecting individual sites subject to episodic diversifying selection. PLOS Genetics. 2012;8(7):e1002764. doi: 10.1371/journal.pgen.1002764 22807683

64. Murrell B, Moola S, Mabona A, Weighill T, Sheward D, Kosakovsky Pond SL, et al. FUBAR: a fast, unconstrained Bayesian AppRoximation for inferring selection. Molecular Biology and Evolution. 2013;30(5):1196–205. doi: 10.1093/molbev/mst030 23420840

65. de Matos AL, Liu J, McFadden G, Esteves PJ. Evolution and divergence of the mammalian SAMD9/SAMD9L gene family. Bmc Evolutionary Biology. 2013;13:16. doi: 10.1186/1471-2148-13-16 WOS:000320538300001.

66. Librado P, Rozas J. DnaSP v5: a software for comprehensive analysis of DNA polymorphism data. Bioinformatics. 2009;25(11):1451–2. doi: 10.1093/bioinformatics/btp187 19346325


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