#PAGE_PARAMS# #ADS_HEAD_SCRIPTS# #MICRODATA#

Identification of a Genomic Reservoir for New Genes in Primate Genomes


Tripartite Motif (TRIM) ubiquitin ligases act in the innate immune response against viruses. One of the best characterized members of this family, TRIM5α, serves as a potent retroviral restriction factor with activity against HIV. Here, we characterize what are likely to be the youngest TRIM genes in the human genome. For instance, we have identified 11 TRIM genes that are specific to humans and African apes (chimpanzees, bonobos, and gorillas) and another 7 that are human-specific. Many of these young genes have never been described, and their identification brings the total number of known human TRIM genes to approximately 100. These genes were acquired through segmental duplications, most of which originated from a single locus on chromosome 11. Another polymorphic duplication of this locus has resulted in these genes being copy number variable within the human population, with a Han Chinese woman identified as having 12 additional copies of these TRIM genes compared to other individuals screened in this study. Recently, this locus was annotated as one of 34 “hotspot” regions that are also copy number variable in the genomes of chimpanzees and rhesus macaques. Most of the young TRIM genes originating from this locus are expressed, spliced, and contain signatures of positive natural selection in regions known to determine virus recognition in TRIM5α. However, we find that they do not restrict the same retroviruses as TRIM5α, consistent with the high degree of divergence observed in the regions that control target specificity. We propose that this recombinationally volatile locus serves as a reservoir from which new TRIM genes arise through segmental duplication, allowing primates to continually acquire new antiviral genes that can be selected to target new and evolving pathogens.


Vyšlo v časopise: Identification of a Genomic Reservoir for New Genes in Primate Genomes. PLoS Genet 7(12): e32767. doi:10.1371/journal.pgen.1002388
Kategorie: Research Article
prolekare.web.journal.doi_sk: https://doi.org/10.1371/journal.pgen.1002388

Souhrn

Tripartite Motif (TRIM) ubiquitin ligases act in the innate immune response against viruses. One of the best characterized members of this family, TRIM5α, serves as a potent retroviral restriction factor with activity against HIV. Here, we characterize what are likely to be the youngest TRIM genes in the human genome. For instance, we have identified 11 TRIM genes that are specific to humans and African apes (chimpanzees, bonobos, and gorillas) and another 7 that are human-specific. Many of these young genes have never been described, and their identification brings the total number of known human TRIM genes to approximately 100. These genes were acquired through segmental duplications, most of which originated from a single locus on chromosome 11. Another polymorphic duplication of this locus has resulted in these genes being copy number variable within the human population, with a Han Chinese woman identified as having 12 additional copies of these TRIM genes compared to other individuals screened in this study. Recently, this locus was annotated as one of 34 “hotspot” regions that are also copy number variable in the genomes of chimpanzees and rhesus macaques. Most of the young TRIM genes originating from this locus are expressed, spliced, and contain signatures of positive natural selection in regions known to determine virus recognition in TRIM5α. However, we find that they do not restrict the same retroviruses as TRIM5α, consistent with the high degree of divergence observed in the regions that control target specificity. We propose that this recombinationally volatile locus serves as a reservoir from which new TRIM genes arise through segmental duplication, allowing primates to continually acquire new antiviral genes that can be selected to target new and evolving pathogens.


Zdroje

1. McNabFWRajsbaumRStoyeJPO'GarraA 2011 Tripartite-motif proteins and innate immune regulation. Curr Opin Immunol 23 46 56

2. SardielloMCairoSFontanellaBBallabioAMeroniG 2008 Genomic analysis of the TRIM family reveals two groups of genes with distinct evolutionary properties. BMC Evol Biol 8 225

3. NisoleSStoyeJPSaïbA 2005 TRIM family proteins: retroviral restriction and antiviral defence. Nat Rev Micro 3 799 808

4. PertelTHausmannSMorgerDZügerSGuerraJ 2011 TRIM5 is an innate immune sensor for the retrovirus capsid lattice. Nature 472 361 365

5. StremlauMOwensCMPerronMJKiesslingMAutissierP 2004 The cytoplasmic body component TRIM5alpha restricts HIV-1 infection in Old World monkeys. Nature 427 848 853

6. Ganser-PornillosBKChandrasekaranVPornillosOSodroskiJGSundquistWI 2011 Hexagonal assembly of a restricting TRIM5 protein. Proc Natl Acad Sci USA 108 534 539

7. StremlauMPerronMLeeMLiYSongB 2006 Specific recognition and accelerated uncoating of retroviral capsids by the TRIM5alpha restriction factor. Proc Natl Acad Sci USA 103 5514 5519

8. ZhaoGKeDVuTAhnJShahVB 2011 Rhesus TRIM5a Disrupts the HIV-1 Capsid at the Inter- Hexamer Interfaces. PLoS Pathog 7 e1002009 doi:10.1371/journal.ppat.1002009

9. TareenSUEmermanM 2011 Human Trim5α has additional activities that are uncoupled from retroviral capsid recognition. Virology 409 113 120

10. KirmaierAWuFNewmanRMHallLRMorganJS 2010 TRIM5 suppresses cross-species transmission of a primate immunodeficiency virus and selects for emergence of resistant variants in the new species. PLoS Biol 8 e1000462 doi:10.1371/journal.pbio.1000462

11. HatziioannouTPrinciottaMPiatakMYuanFZhangF 2006 Generation of simian-tropic HIV-1 by restriction factor evasion. Science 314 95

12. NewmanRMJohnsonWE 2007 A brief history of TRIM5alpha. AIDS Rev 9 114 125

13. KaiserSMMalikHSEmermanM 2007 Restriction of an Extinct Retrovirus by the Human TRIM5 Antiviral Protein. Science 316 1756 1758

14. KuoR-LZhaoCMalurMKrugRM 2010 Influenza A virus strains that circulate in humans differ in the ability of their NS1 proteins to block the activation of IRF3 and interferon-β transcription. Virology 408 146 158

15. GackMUAlbrechtRAUranoTInnK-SHuangI-C 2009 Influenza A virus NS1 targets the ubiquitin ligase TRIM25 to evade recognition by the host viral RNA sensor RIG-I. Cell Host Microbe 5 439 449

16. ZengWSunLJiangXChenXHouF 2010 Reconstitution of the RIG-I pathway reveals a signaling role of unanchored polyubiquitin chains in innate immunity. Cell 141 315 330

17. PooleEGrovesIMacdonaldAPangYAlcamiA 2009 Identification of TRIM23 as a Cofactor Involved in the Regulation of NF- B by Human Cytomegalovirus. J Virol 83 3581 3590

18. WangJLiuBWangNLeeY-MLiuC 2011 TRIM56 is a virus- and interferon-inducible E3 ubiquitin ligase that restricts pestivirus infection. J Virol 85 3733 3745

19. GeoffroyM-CChelbi-AlixMK 2011 Role of promyelocytic leukemia protein in host antiviral defense. J Interferon Cytokine Res 31 145 158

20. CarthagenaLBergamaschiALunaJMDavidAUchilPD 2009 Human TRIM gene expression in response to interferons. PLoS ONE 4 e4894 doi:10.1371/journal.pone.0004894

21. MeroniGDiez-RouxG 2005 TRIM/RBCC, a novel class of “single protein RING finger” E3 ubiquitin ligases. Bioessays 27 1147 1157

22. MastersSLYaoSWillsonTAZhangJ-GPalmerKR 2006 The SPRY domain of SSB-2 adopts a novel fold that presents conserved Par-4-binding residues. Nat Struct Mol Biol 13 77 84

23. TareenSUSawyerSLMalikHSEmermanM 2009 An expanded clade of rodent Trim5 genes. Virology 385 473 483

24. GokcumenOBabbPLIskowRZhuQShiX 2011 Refinement of primate CNV hotspots identifies candidate genomic regions evolving under positive selection. Genome Biol 12 R52

25. PerryGHTchindaJMcGrathSDZhangJPickerSR 2006 Hotspots for copy number variation in chimpanzees and humans. Proc Natl Acad Sci USA 103 8006 8011

26. SawyerSLEmermanMMalikHS 2004 Ancient adaptive evolution of the primate antiviral DNA-editing enzyme APOBEC3G. PLoS Biol 2 e275 doi:10.1371/journal.pbio.0020275

27. SawyerSLEmermanMMalikHS 2007 Discordant evolution of the adjacent antiretroviral genes TRIM22 and TRIM5 in mammals. PLoS Pathog 3 e197 doi:10.1371/journal.ppat.0030197

28. SawyerSLWuLIEmermanMMalikHS 2005 Positive selection of primate TRIM5alpha identifies a critical species-specific retroviral restriction domain. Proc Natl Acad Sci USA 102 2832 2837

29. GuptaRKHuéSSchallerTVerschoorEPillayD 2009 Mutation of a single residue renders human tetherin resistant to HIV-1 Vpu-mediated depletion. PLoS Pathog 5 e1000443 doi:10.1371/journal.ppat.1000443

30. LimESMalikHSEmermanM 2010 Ancient adaptive evolution of Tetherin shaped Vpu and Nef functions in human immunodeficiency virus and primate lentiviruses. J Virol 1 38

31. McNattMWZangTHatziioannouTBartlettMFofanaIB 2009 Species-specific activity of HIV-1 Vpu and positive selection of tetherin transmembrane domain variants. PLoS Pathog 5 e1000300 doi:10.1371/journal.ppat.1000300

32. LiuH-LWangY-QLiaoC-HKuangY-QZhengY-T 2005 Adaptive evolution of primate TRIM5alpha, a gene restricting HIV-1 infection. Gene 362 109 116

33. EldeNCChildSJGeballeAPMalikHS 2009 Protein kinase R reveals an evolutionary model for defeating viral mimicry. Nature 457 485 489

34. KernsJAEmermanMMalikHS 2008 Positive selection and increased antiviral activity associated with the PARP-containing isoform of human zinc-finger antiviral protein. PLoS Genet 4 e21 doi:10.1371/journal.pgen.0040021

35. WlasiukGNachmanMW 2010 Adaptation and constraint at Toll-like receptors in primates. Mol Biol Evol 27 2172 2186

36. MicaleLFuscoCAugelloBNapolitanoLMRDermitzakisET 2008 Williams-Beuren syndrome TRIM50 encodes an E3 ubiquitin ligase. Eur J Hum Genet 16 1038 1049

37. CardoneMFLomientoMTetiMGMisceoDRobertoR 2007 Evolutionary history of chromosome 11 featuring four distinct centromere repositioning events in Catarrhini. Genomics 90 35 43

38. ZhangJQinSSaitSNHaleyLLHenryWM 2001 The pericentromeric region of human chromosome 11: evidence for a chromosome-specific duplication. Cytogenet Cell Genet 94 137 141

39. TaylorTDNoguchiHTotokiYToyodaAKurokiY 2006 Human chromosome 11 DNA sequence and analysis including novel gene identification. Nature 440 497 500

40. RedonRIshikawaSFitchKRFeukLPerryGH 2006 Global variation in copy number in the human genome. Nature 444 444 454

41. SchoutenJPMcElgunnCJWaaijerRZwijnenburgDDiepvensF 2002 Relative quantification of 40 nucleic acid sequences by multiplex ligation-dependent probe amplification. Nucleic Acids Res 30 e57

42. ParkHKimJ-IJuYSGokcumenOMillsRE 2010 Discovery of common Asian copy number variants using integrated high-resolution array CGH and massively parallel DNA sequencing. Nat Genet 42 400 405

43. PerryGHBen-DorATsalenkoASampasNRodriguez-RevengaL 2008 The fine-scale and complex architecture of human copy-number variation. Am J Hum Genet 82 685 695

44. KimJ-IJuYSParkHKimSLeeS 2009 A highly annotated whole-genome sequence of a Korean individual. Nature 460 1011 1015

45. HurstLD 2002 The Ka/Ks ratio: diagnosing the form of sequence evolution. Trends Genet 18 486

46. SchanerPRichardsNWadhwaAAksentijevichIKastnerD 2001 Episodic evolution of pyrin in primates: human mutations recapitulate ancestral amino acid states. Nat Genet 27 318 321

47. MeyersonNRSawyerSL 2011 Two-stepping through time: mammals and viruses. Trends Microbiol 19 286 294

48. ShrinerDNickleDJensenMMullinsJ 2003 Potential impact of recombination on sitewise approaches for detecting positive natural selection. Genet Res 81 115 121

49. PondSLPosadaDGravenorMBWoelkCHFrostSDW 2006 Automated phylogenetic detection of recombination using a genetic algorithm. Mol Biol Evol 23 1891 1901

50. OhAinleMKernsJAMalikHSEmermanM 2006 Adaptive evolution and antiviral activity of the conserved mammalian cytidine deaminase APOBEC3H. J Virol 80 3853 3862

51. YapMWNisoleSStoyeJP 2005 A single amino acid change in the SPRY domain of human Trim5alpha leads to HIV-1 restriction. Curr Biol 15 73 78

52. StremlauMPerronMWelikalaSSodroskiJ 2005 Species-specific variation in the B30.2(SPRY) domain of TRIM5alpha determines the potency of human immunodeficiency virus restriction. J Virol 79 3139 3145

53. Perez-CaballeroDHatziioannouTYangACowanSBieniaszPD 2005 Human tripartite motif 5alpha domains responsible for retrovirus restriction activity and specificity. J Virol 79 8969 8978

54. JohnsonWESawyerSL 2009 Molecular evolution of the antiretroviral TRIM5 gene. Immunogenetics 61 163 176

55. FletcherAJHuéSSchallerTPillayDTowersGJ 2010 Hare TRIM5α restricts divergent retroviruses and exhibits significant sequence variation from closely related lagomorpha TRIM5 genes. J Virol 84 12463 12468

56. MaillardPVEccoGOrtizMTronoD 2010 The specificity of TRIM5 alpha-mediated restriction is influenced by its coiled-coil domain. J Virol 84 5790 5801

57. YohnCTJiangZMcGrathSDHaydenKEKhaitovichP 2005 Lineage-specific expansions of retroviral insertions within the genomes of African great apes but not humans and orangutans. PLoS Biol 3 e110 doi:10.1371/journal.pbio.0030110

58. LanderESLintonLMBirrenBNusbaumCZodyMC 2001 Initial sequencing and analysis of the human genome. Nature 409 860 921

59. SinghRGaihaGWernerLMcKimKMlisanaK 2011 Association of TRIM22 with Type 1 Interferon Response and Viral Control during Primary HIV-1 Infection. Journal of Virology 85 208 216

60. GaoBDuanZXuWXiongS 2009 Tripartite motif-containing 22 inhibits the activity of hepatitis B virus core promoter, which is dependent on nuclear-located RING domain. Hepatology 50 424 433

61. EldinPPaponLOteizaABrocchiELawsonTG 2009 TRIM22 E3 ubiquitin ligase activity is required to mediate antiviral activity against encephalomyocarditis virus. J Gen Virol 90 536 545

62. HanMVDemuthJPMcGrathCLCasolaCHahnMW 2009 Adaptive evolution of young gene duplicates in mammals. Genome Res 19 859 867

63. McEwanWASchallerTYlinenLMHosieMJTowersGJ 2009 Truncation of TRIM5 in the Feliformia explains the absence of retroviral restriction in cells of the domestic cat. J Virol 83 8270 8275

64. BarreiroLBQuintana-MurciL 2010 From evolutionary genetics to human immunology: how selection shapes host defence genes. Nat Rev Genet 11 17 30

65. BayésMMaganoLFRiveraNFloresRPérez JuradoLA 2003 Mutational mechanisms of Williams-Beuren syndrome deletions. Am J Hum Genet 73 131 151

66. LupskiJRStankiewiczP 2005 Genomic Disorders: Molecular Mechanisms for Rearrangements and Conveyed Phenotypes. PLoS Genet 1 e49 doi:10.1371/journal.pgen.0010049

67. PerryGHDominyNJClawKGLeeASFieglerH 2007 Diet and the evolution of human amylase gene copy number variation. Nat Genet 39 1256 1260

68. KentWJSugnetCWFureyTSRoskinKMPringleTH 2002 The Human Genome Browser at UCSC. Genome Res 12 996 1006

69. KentWJ 2002 BLAT—The BLAST-Like Alignment Tool. Genome Res 12 656 664

70. TamuraKPetersonDPetersonNStecherGNeiM 2011 MEGA5: Molecular Evolutionary Genetics Analysis using Maximum Likelihood, Evolutionary Distance, and Maximum Parsimony Methods. Mol Biol Evol in press

71. DelportWPoonAFYFrostSDWKosakovsky PondSL 2010 Datamonkey 2010: a suite of phylogenetic analysis tools for evolutionary biology. Bioinformatics 26 2455 2457

72. YangZ 1997 PAML: a program package for phylogenetic analysis by maximum likelihood. Comput Appl Biosci 13 555 556

73. AnisimovaMBielawskiJPYangZ 2001 Accuracy and power of the likelihood ratio test in detecting adaptive molecular evolution. Mol Biol Evol 18 1585 1592

74. YamashitaMEmermanM 2004 Capsid is a dominant determinant of retrovirus infectivity in nondividing cells. J Virol 78 5670 5678

75. BockMBishopKNTowersGStoyeJP 2000 Use of a transient assay for studying the genetic determinants of Fv1 restriction. J Virol 74 7422 7430

76. BarrazaRAPoeschlaEM 2008 Human gene therapy vectors derived from feline lentiviruses. Vet Immunol Immunopathol 123 23 31

77. LoewenNBarrazaRWhitwamTSaenzDTKemlerI 2003 FIV Vectors. Methods Mol Biol 229 251 271

78. PerelmanPJohnsonWERoosCSeuánezHNHorvathJE 2011 A molecular phylogeny of living primates. PLoS Genet 7 e1001342 doi:10.1371/journal.pgen.1001342

79. HedgesSB 2002 The origin and evolution of model organisms. Nat Rev Genet 3 838 849

80. ParkEYKwonO-BJeongB-CYiJ-SLeeCS 2010 Crystal structure of PRY-SPRY domain of human TRIM72. Proteins 78 790 795

81. CuffJAClampMESiddiquiASFinlayMBartonGJ 1998 JPred: a consensus secondary structure prediction server. Bioinformatics 14 892 893

82. JamesLCKeebleAHKhanZRhodesDATrowsdaleJ 2007 Structural basis for PRYSPRY-mediated tripartite motif (TRIM) protein function. Proc Natl Acad Sci USA 104 6200 6205

83. GrütterCBriandCCapitaniGMittlPREPapinS 2006 Structure of the PRYSPRY-domain: implications for autoinflammatory diseases. FEBS Lett 580 99 106

84. SongBJavanbakhtHPerronMParkDHStremlauM 2005 Retrovirus restriction by TRIM5alpha variants from Old World and New World primates. J Virol 79 3930 3937

Štítky
Genetika Reprodukčná medicína

Článok vyšiel v časopise

PLOS Genetics


2011 Číslo 12
Najčítanejšie tento týždeň
Najčítanejšie v tomto čísle
Kurzy

Zvýšte si kvalifikáciu online z pohodlia domova

Získaná hemofilie - Povědomí o nemoci a její diagnostika
nový kurz

Eozinofilní granulomatóza s polyangiitidou
Autori: doc. MUDr. Martina Doubková, Ph.D.

Všetky kurzy
Prihlásenie
Zabudnuté heslo

Zadajte e-mailovú adresu, s ktorou ste vytvárali účet. Budú Vám na ňu zasielané informácie k nastaveniu nového hesla.

Prihlásenie

Nemáte účet?  Registrujte sa

#ADS_BOTTOM_SCRIPTS#