Study of Sylvilagus rabbit TRIM5 species-specific domain: How ancient endoviruses could have shaped the antiviral repertoire in Lagomorpha

BMC Evolutionary Biology

Volumn 11, Issue 1, 2011, Pages

  De Matos, Ana Lemos ^a,b,c   Van Der Loo, Wessel ^a   Areal, Helena ^a,b   Lanning, Dennis K ^c   Esteves, Pedro J ^a,d  

^a CENTRO DE INVESTIGAÇÃO EM BIODIVERSIDADE E RECURSOS GENÉTICOS   (Portugal)

^b UNIVERSITY OF PORTO   (Portugal)

^c LOYOLA UNIVERSITY CHICAGO   (United States)

^d CESPU   (Portugal)

Author keywords

[No Author keywords available]

Indexed keywords

EVOLUTIONARY BIOLOGY; LAGOMORPH; PRIMATE; PROTEIN; VIRUS;

LAGOMORPHA; LENTIVIRUS; LEPORIDAE; LEPUS; LEPUS CAPENSIS; MAMMALIA; MIRIDAE; ORYCTOLAGUS; ORYCTOLAGUS CUNICULUS; PRIMATES; SYLVILAGUS;

CARRIER PROTEIN;

AMINO ACID SEQUENCE; ANIMAL; ARTICLE; CHEMISTRY; GENETICS; LAGOMORPH; MOLECULAR GENETICS; NUCLEOTIDE SEQUENCE; PHYLOGENY; PROTEIN TERTIARY STRUCTURE; RABBIT; RETROVIRUS; SEQUENCE ALIGNMENT; SPECIES DIFFERENCE; VIROLOGY;

AMINO ACID SEQUENCE; ANIMALS; BASE SEQUENCE; CARRIER PROTEINS; LAGOMORPHA; MOLECULAR SEQUENCE DATA; PHYLOGENY; PROTEIN STRUCTURE, TERTIARY; RABBITS; RETROVIRIDAE; SEQUENCE ALIGNMENT; SPECIES SPECIFICITY;

EID: 80555131036     PISSN: None     EISSN: 14712148     Source Type: Journal    
DOI: 10.1186/1471-2148-11-294     Document Type: Article

References (71)

1. Retrotransposons, endogenous retroviruses, and the evolution of retroelements. Boeke JD, Stoye JP, Retroviruses CSHL Press, New York, Coffin JM, Hughes SH, Varmus HE, 1997 343 435
2. Retroviral taxonomy, protein structures, sequences, and genetic maps. Petropoulos C, Retroviruses CSHL Press, New York, Coffin JM, Hughes SH, Varmus HE, 1997 757 805
3. The evolution, distribution and diversity of endogenous retroviruses. Gifford R, Tristem M, Virus Genes 2003 26 291 315 10.1023/A:1024455415443 12876457 (Pubitemid 36903218)
4. Discovery and analysis of the first endogenous lentivirus. Katzourakis A, Tristem M, Pybus OG, Gifford RJ, Proc Natl Acad Sci USA 2007 104 6261 6265 10.1073/pnas.0700471104 17384150 (Pubitemid 47186082)
5. Identification of a RELIK orthologue in the European hare (Lepus europaeus) reveals a minimum age of 12 million years for the lagomorph lentiviruses. Keckesova Z, Ylinen LMJ, Towers GJ, Gifford RJ, Katzourakis A, Virology 2009 384 7 11 10.1016/j.virol.2008.10.045 19070882
6. Sharing of endogenous lentiviral gene fragments among leporid lineages separated for more than 12 million years. van der Loo W, Abrantes J, Esteves PJ, J Virol 2009 83 2386 2388 10.1128/JVI.01116-08 19109386
7. The cytoplasmic body component TRIM5 restricts HIV-1 infection in Old World monkeys. Stremlau M, Owens CM, Perron MJ, Kiessling M, Autissier P, Sodroski J, Nature 2004 427 848 853 10.1038/nature02343 14985764 (Pubitemid 38297747)
8. Cyclophilin A retrotransposition into TRIM5 explains owl monkey resistance to HIV-1. Sayah DM, Sokolskaja E, Berthoux L, Luban J, Nature 2004 430 569 573 10.1038/nature02777 15243629 (Pubitemid 38998631)
9. TRIM family proteins: retroviral restriction and antiviral defence. Nisole S, Stoye JP, Sab A, Nat Rev Microbiol 2005 3 799 808 10.1038/nrmicro1248 16175175 (Pubitemid 41518740)
10. TRIM family proteins and their emerging roles in innate immunity. Ozato K, Shin D-M, Chang T-H, Morse HC, Nat Rev Immunol 2008 8 849 860 10.1038/nri2413 18836477
11. The tripartite motif family identifies cell compartments. Reymond A, Meroni G, Fantozzi A, Merla G, Cairo S, Luzi L, Riganelli D, Zanaria E, Messali S, Cainarca S, Guffanti A, Minucci S, Pelicci PG, Ballabio A, EMBO J 2001 20 2140 2151 10.1093/emboj/20.9.2140 11331580 (Pubitemid 32410584)
12. Ubiquitination of E3 ubiquitin ligase TRIM5 and its potential role. Yamauchi K, Wada K, Tanji K, Tanaka M, Kamitani T, FEBS J 2008 275 1540 1555 10.1111/j.1742-4658.2008.06313.x 18312418 (Pubitemid 351388800)
13. The contribution of RING and B-box 2 domains to retroviral restriction mediated by monkey TRIM5alpha. Javanbakht H, Diaz-Griffero F, Stremlau M, Si Z, Sodroski J, J Biol Chem 2005 280 26933 26940 10.1074/jbc.M502145200 15897199 (Pubitemid 41040729)
14. Functional interplay between the B-BOX 2 and the B30.2 (SPRY) domains of TRIM5 Li X, Song B, Xiang SH, Sodroski J, Virology 2007 366 234 244 10.1016/j.virol.2007.04.022 17543365 (Pubitemid 47398911)
15. The TRIM5alpha B-box 2 domain promotes cooperative binding to the retroviral capsid by mediating higher-order self-association. Li X, Sodroski J, J Virol 2008 82 11495 11502 10.1128/JVI.01548-08 18799578
16. Characterization of TRIM5 trimerization and its contribution to human immunodeficiency virus capsid binding. Javanbakht H, Yuan W, Yeung DF, Song B, Diaz-Griffero F, Li Y, Li X, Stremlau M, Sodroski J, Virology 2006 353 234 246 10.1016/j.virol.2006.05.017 16808955 (Pubitemid 44308489)
17. A single amino acid change in the SPRY domain of human Trim5 leads to HIV-1 restriction. Yap MW, Nisole S, Stoye JP, Curr Biol 2005 15 73 78 10.1016/j.cub.2004.12.042 15649369 (Pubitemid 40084706)
18. Species-specific variation in the B30.2 (SPRY) domain of TRIM5 determines the potency of Human Immunodeficiency Virus restriction. Stremlau M, Perron M, Welikala S, Sodroski J, J Virol 2005 79 3139 3145 10.1128/JVI.79.5.3139-3145. 2005 15709033 (Pubitemid 40270592)
19. Retrovirus resistance factors Ref1 and Lv1 are species-specific variants of TRIM5alpha. Hatziioannou T, Perez-Caballero D, Yang A, Cowan S, Bieniasz PD, Proc Natl Acad Sci USA 2004 101 10774 10779 10.1073/pnas.0402361101 15249685 (Pubitemid 38955818)
20. The human and African green monkey TRIM5alpha genes encode Ref1 and Lv1 retroviral restriction factor activities. Keckesova Z, Ylinen LM, Towers GJ, Proc Natl Acad Sci USA 2004 101 10780 10785 10.1073/pnas.0402474101 15249687 (Pubitemid 38955819)
21. Trim5alpha protein restricts both HIV-1 and murine leukemia virus. Yap MW, Nisole S, Lynch C, Stoye JP, Proc Natl Acad Sci USA 2004 101 10786 10791 10.1073/pnas.0402876101 15249690 (Pubitemid 38955820)
22. TRIM5alpha mediates the postentry block to N-tropic murine leukemia viruses in human cells. Perron MJ, Stremlau M, Song B, Ulm W, Mulligan RC, Sodroski J, Proc Natl Acad Sci USA 2004 101 11827 11832 10.1073/pnas.0403364101 15280539 (Pubitemid 39095379)
23. Removal of arginine 332 allows human TRIM5alpha to bind human immunodeficiency virus capsids and to restrict infection. Li Y, Li X, Stremlau M, Lee M, Sodrosky J, J Virol 2006 80 6738 6744 10.1128/JVI.00270-06 16809279 (Pubitemid 44025173)
24. TRIM5alpha selectively binds a restriction-sensitive retroviral capsid. Sebastian S, Luban J, Retrovirology 2005 2 40 10.1186/1742-4690-2-40 15967037 (Pubitemid 41522422)
25. The B30.2 (SPRY) domain of the retroviral restriction factor TRIM5alpha exhibits lineage-specific length and sequence variation in primates. Song B, Gold B, O'hUigin C, Javanbakht H, Li X, Stremlau M, Winkler C, Dean M, Sodroski J, J Virol 2005 79 6111 6121 10.1128/JVI.79.10.6111-6121.2005 15857996 (Pubitemid 40617216)
26. Structural basis for PRYSPRY-mediated tripartite motif (TRIM) protein function. James LC, Keeble AH, Khan Z, Rhodes DA, Trowsdale J, Proc Natl Acad Sci USA 2007 104 6200 6205 10.1073/pnas.0609174104 17400754 (Pubitemid 47186072)
27. Human TRIM5 has additional activities that are uncoupled from retroviral capsid recognition. Tareen SU, Emerman M, Virology 2011 409 113 120 10.1016/j.virol.2010.09.018 21035162
28. TRIM5 is an innate immune sensor for the retrovirus capsid lattice. Pertel T, Hausmann S, Morger D, Züger S, Guerra J, Lascano J, Reinhard C, Santoni FA, Uchil PD, Chatel L, Bisiaux A, Albert ML, Strambio-De-Castillia C, Mothes W, Pizzato M, Grütter MG, Luban J, Nature 2011 472 361 365 10.1038/nature09976 21512573
29. Hexagonal assembly of a restricting TRIM5alpha protein. Ganser-Pornillos BK, Chandrasekaran V, Pornillos O, Sodroski JG, Sundquist WI, Yeager M, Proc Natl Acad Sci USA 2011 108 534 539 10.1073/pnas.1013426108 21187419
30. Rhesus TRIM5 disrupts the HIV-1 capsid at the inter-hexamer interfaces. Zhao G, Ke D, Vu T, Ahn J, Shah VB, Yang R, Aiken C, Charlton LM, Gronenborn AM, Zhang P, PLoS Pathog 2011 7 1002009 10.1371/journal.ppat.1002009 21455494
31. Positive selection of primate TRIM5 identifies a critical species-specific retroviral restriction domain. Sawyer SL, Wu LI, Emerman M, Malik HS, Proc Natl Acad Sci USA 2005 102 2832 2837 10.1073/pnas.0409853102 15689398 (Pubitemid 40299877)
32. Molecular evolution of the antiretroviral TRIM5 gene. Johnson WE, Sawyer SL, Immunogenetics 2009 61 163 176 10.1007/s00251-009-0358-y 19238338
33. Evolution of TRIM5 B30.2 (SPRY) domain in New World primates. Soares EA, Menezes AN, Schrago CG, Moreira MAM, Bonvicino CR, Soares MA, Seuánez HN, Infect Genet Evol 2010 10 246 253 10.1016/j.meegid.2009.11.012 19931648
34. Balancing selection and the evolution of functional polymorphism in Old World monkey TRIM5 Newman RM, Hall L, Connole M, Chen G-L, Sato S, Yuste E, Diehl W, Hunter E, Kaur A, Miller GM, Johnson WE, Proc Natl Acad Sci USA 2006 103 19134 19139 10.1073/pnas.0605838103 17142324 (Pubitemid 350010634)
35. Long-term balancing selection maintains trans-specific polymorphisms in the human TRIM5 gene. Cagliani R, Fumagalli M, Biasin M, Piacentini L, Riva S, Pozzoli U, Bonaglia MC, Bresolin N, Clerici M, Sironi M, Human Genet 2010 128 577 588 10.1007/s00439-010-0884-6
36. Evolution of a cytoplasmic tripartite motif (TRIM) protein in cows that restricts retroviral infection. Si Z, Vandegraaff N, O'hUigin C, Song B, Yuan W, Xu C, Perron M, Li X, Marasco WA, Engelman A, Dean M, Sodroski J, Proc Natl Acad Sci USA 2006 103 7454 7459 10.1073/pnas.0600771103 16648259 (Pubitemid 43727854)
37. Discordant evolution of the adjacent antiretroviral genes TRIM22 and TRIM5 in mammals. Sawyer SL, Emerman M, Malik HS, PLoS Pathog 2007 3 197 10.1371/journal.ppat.0030197 18159944
38. An active TRIM5 protein in rabbits indicates a common antiviral ancestor for mammalian TRIM5 proteins. Schaller T, Hué S, Towers GJ, J Virol 2007 81 11713 11721 10.1128/JVI.01468-07 17728224 (Pubitemid 47623803)
39. An expanded clade of rodent Trim5 genes. Tareen SU, Sawyer SL, Malik HS, Emerman M, Virology 2009 385 473 483 10.1016/j.virol.2008.12.018 19147168
40. Hare TRIM5 restricts divergent retroviruses and exhibits significant sequence variation from closely related Lagomorpha TRIM5 genes. Fletcher AJ, Hué S, Schaller T, Pillay D, Towers GJ, J Virol 2010 84 12463 12468 10.1128/JVI.01514-10 20861252
41. A molecular supermatrix of the rabbits and hares (Leporidae) allows for the identification of five intercontinental exchanges during the Miocene. Matthee CA, van Vuuren BJ, Bell D, Robinson TJ, Syst Biol 2004 53 433 447 10.1080/10635150490445715 15503672 (Pubitemid 38946907)
42. Pikas, hares and rabbits (Lagomorpha). Matthee CA, The timetree of life Oxford University Press, New York, NY, Hedges SB, Kumar S, 2009 487 489
43. Inferring divergence times within pikas (Ochotona spp.) using mtDNA and relaxed molecular dating techniques. Lanier HC, Olson LE, Mol Phylogenet Evol 2009 53 1 12 10.1016/j.ympev.2009.05.035 19501176
44. The evolutionary history of the European rabbit (Oryctolagus cuniculus): major patterns of population differentiation and geographic expansion inferred from protein polymorphism. Ferrand N, Branco M, Phylogeography of Southern European Refugia Springer, The Netherlands, Weiss S, Ferrand N, 2007 207 235
45. Genetic variation at chemokine receptor CCR5 in leporids: alteration at the 2nd extracellular domain by gene conversion with CCR2 in Oryctolagus, but not in Sylvilagus and Lepus species. Carmo CR, Esteves PJ, Ferrand N, van der Loo W, Immunogenetics 2006 58 494 501 10.1007/s00251-006-0095-4 16596402 (Pubitemid 43830115)
46. A shared unusual genetic change at the chemokine receptor type 5 between Oryctolagus, Bunolagus and Pentalagus. Abrantes J, Carmo CR, Matthee CA, Yamada F, van der Loo W, Esteves PJ, Conserv Genet 2011 12 325 330 10.1007/s10592-009- 9990-1
47. H) in Leporids: an unusual case of transspecies polymorphism. Esteves PJ, Lanning D, Ferrand N, Knight KL, Zhai SK, van der Loo W, Immunogenetics 2005 57 874 882 10.1007/s00251-005-0022-0 16247606 (Pubitemid 41817946)
48. Phylogenomics of primates and their ancestral populations. Siepel A, Genome Res 2009 19 1929 1941 10.1101/gr.084228.108 19801602
49. Evolution of the primate lineage leading to modern humans: phylogenetic and demographic inferences from DNA sequences. Takahata N, Satta Y, Proc Natl Acad Sci USA 1997 94 4811 4815 10.1073/pnas.94.9.4811 9114074 (Pubitemid 27194326)
50. Simple methods for estimating the numbers of synonymous and nonsynonymous nucleotide substitutions. Nei M, Gojobori T, Mol Biol Evol 1986 3 418 426 3444411 (Pubitemid 16010523)
51. Constructing primate phylogenies from ancient retrovirus sequences. Johnson WE, Coffin JM, Proc Natl Acad Sci USA 1999 96 10254 10260 10.1073/pnas.96.18.10254 10468595 (Pubitemid 29422545)
52. Paleovirology-Modern consequences of ancient viruses. Emerman M, Malik HS, PLoS Biol 2010 8 1000301 10.1371/journal.pbio.1000301 20161719
53. Positive selection and increased antiviral activity associated with the PARP-containing isoform of human zinc-finger antiviral protein. Kerns JA, Emerman M, Malik HS, PLoS Genet 2008 4 21 10.1371/journal.pgen.0040021 18225958 (Pubitemid 351230882)
54. Protein kinase R reveals an evolutionary model for defeating viral mimicry. Elde NC, Child SJ, Geballe AP, Malik HS, Nature 2009 457 485 489 10.1038/nature07529 19043403
55. Restriction of an extinct retrovirus by the human TRIM5 antiviral protein. Kaiser SM, Malik HS, Emerman M, Science 2007 316 1756 1758 10.1126/science.1140579 17588933 (Pubitemid 46988552)
56. Structural and functional analysis of prehistoric lentiviruses uncovers an ancient molecular interface. Goldstone DC, Yap MW, Robertson LE, Haire LF, Taylor WR, Katzourakis A, Stoye JP, Taylor IA, Cell Host Microbe 2010 8 248 259 10.1016/j.chom.2010.08.006 20833376
57. Crystal structure of human cyclophilin A bound to the amino-terminal domain of HIV-1 capsid. Gamble TR, Vajdos FF, Yoo S, Worthylake DK, Houseweart M, Sundquist WI, Hill CP, Cell 1996 87 1285 1294 10.1016/S0092-8674(00)81823-1 8980234 (Pubitemid 27010111)
58. Human immunodeficiency virus type 1 Gag protein binds to cyclophilins A and B. Luban J, Bossolt KL, Franke EK, Kalpana GV, Goff SP, Cell 1993 73 1067 1078 10.1016/0092-8674(93)90637-6 8513493 (Pubitemid 23180482)
59. First-strand cDNA synthesis primed with oligo(dT). Krug MS, Berger SL, Methods Enzymol 1987 152 316 325 2443800
60. Genetic algorithm approaches for the phylogenetic analysis of large biological sequence datasets under the maximum likelihood criterion. Zwickl DJ, PhD thesis University of Texas, Austin 2006
61. jModelTest: Phylogenetic Model Averaging. Posada D, Mol Biol Evol 2008 25 1253 1256 10.1093/molbev/msn083 18397919 (Pubitemid 351882013)
62. The rapid generation of mutation data matrices from protein sequences. Jones DT, Taylor WR, Thornton JM, CABIOS 1992 8 275 282 1633570
63. ProtTest: Selection of best-fit models of protein evolution. Abascal F, Zardoya R, Posada D, Bioinformatics 2005 21 2104 2105 10.1093/bioinformatics/ bti263 15647292 (Pubitemid 40668057)
64. PAL: An object-oriented programming library for molecular evolution and phylogenetics. Drummond A, Strimmer K, Bioinformatics 2001 17 662 663 10.1093/bioinformatics/17.7.662 11448888 (Pubitemid 32707592)
65. A simple, fast, and accurate algorithm to estimate large phylogenies by maximum likelihood. Guindon S, Gascuel O, Syst Biol 2003 52 696 704 10.1080/10635150390235520 14530136 (Pubitemid 37365050)
66. A sliding window-based method to detect selective constraints in protein-coding genes and its application to RNA viruses. Fares MA, Elena SF, Ortiz J, Moya A, Barrio E, J Mol Evol 2002 55 509 521 10.1007/s00239-002-2346-9 12399925 (Pubitemid 35222930)
67. Not so different after all: a comparison of methods for detecting amino acid sites under selection. Kosakovsky Pond SL, Frost SD, Mol Biol Evol 2005 22 1208 1222 10.1093/molbev/msi105 15703242 (Pubitemid 40577758)
68. Datamonkey: rapid detection of selective pressure on individual sites of codon alignments. Kosakovsky Pond SL, Frost SD, Bioinformatics 2005 21 2531 2533 10.1093/bioinformatics/bti320 15713735 (Pubitemid 40731616)
69. MEGA5: Molecular Evolutionary Genetics Analysis using Maximum Likelihood, Evolutionary Distance, and Maximum Parsimony Methods. Tamura K, Peterson D, Peterson N, Stecher G, Nei M, Kumar S, Mol Biol Evol 2011 28 2731 2739 10.1093/molbev/msr121 21546353
70. Determination of window size for analysing DNA sequences. Tajima F, J Mol Evol 1991 33 470 473 10.1007/BF02103140 1960744
71. DnaSP v5: A software for comprehensive analysis of DNA polymorphism data. Librado P, Rozas J, Bioinformatics 2009 25 1451 1452 10.1093/bioinformatics/ btp187 19346325