Long-term balancing selection maintains trans-specific polymorphisms in the human TRIM5 gene

Human Genetics

Volumn 128, Issue 6, 2010, Pages 577-588

  Cagliani, R ^a   Fumagalli, M ^a,b   Biasin, M ^c   Piacentini, L ^c   Riva, S ^a   Pozzoli, U ^a   Bonaglia, M C ^a   Bresolin, N ^a,c   Clerici, M ^c,d   Sironi, Manuela ^a  

^a SCIENTIFIC INSTITUTE   (Italy)

^b POLITECNICO DI MILANO   (Italy)

^c UNIVERSITY OF MILAN   (Italy)

^d IRCCS FONDAZIONE DON CARLO GNOCCHI   (Italy)

Author keywords

[No Author keywords available]

Indexed keywords

MESSENGER RNA; TRANSCRIPTION FACTOR; TRIPARTITE MOTIF PROTEIN 5;

ARTICLE; BINDING SITE; CHIMPANZEE; DNA POLYMORPHISM; GENE SEQUENCE; GENE TARGETING; GENETIC ASSOCIATION; GENETIC CODE; GENETIC SUSCEPTIBILITY; GENETIC VARIABILITY; HAPLOTYPE; HUMAN; HUMAN IMMUNODEFICIENCY VIRUS 1 INFECTION; INTRON; MOLECULAR EVOLUTION; NONHUMAN; PRIORITY JOURNAL; RETROVIRUS INFECTION;

ANIMALS; BINDING SITES; CARRIER PROTEINS; EVOLUTION, MOLECULAR; HAPLOTYPES; HUMANS; PAN TROGLODYTES; POLYMORPHISM, GENETIC; SELECTION, GENETIC; TRANSCRIPTION FACTORS;

HUMAN IMMUNODEFICIENCY VIRUS 1; MAMMALIA; PAN; PRIMATES;

EID: 78649316609     PISSN: 03406717     EISSN: 14321203     Source Type: Journal    
DOI: 10.1007/s00439-010-0884-6     Document Type: Article

References (54)

1. S Asthana S Schmidt S Sunyaev 2005 A limited role for balancing selection Trends Genet 21 30 32 10.1016/j.tig.2004.11.001 1:CAS:528: DC%2BD2MXoslajtg%3D%3D 10.1016/j.tig.2004.11.001 15680511 (Pubitemid 40178846)
2. MJ Bamshad S Mummidi E Gonzalez SS Ahuja DM Dunn WS Watkins S Wooding AC Stone LB Jorde RB Weiss SK Ahuja 2002 A strong signature of balancing selection in the 5′ cis-regulatory region of CCR5 Proc Natl Acad Sci USA 99 10539 10544 10.1073/pnas.162046399 1:CAS:528:DC%2BD38Xmt1Chs7k%3D 10.1073/pnas. 162046399 12149450
3. HJ Bandelt P Forster BC Sykes MB Richards 1995 Mitochondrial portraits of human populations Genetics 141 743 753 1:STN:280:DyaK287gvFKitQ%3D%3D 8647407
4. JC Barrett B Fry J Maller MJ Daly 2005 Haploview: analysis and visualization of LD and haplotype maps Bioinformatics 21 263 265 1:CAS:528:DC%2BD2MXkt1WitQ%3D%3D 10.1093/bioinformatics/bth457 15297300 (Pubitemid 40202029)
5. R Cagliani M Fumagalli S Riva U Pozzoli GP Comi G Menozzi N Bresolin M Sironi 2008 The signature of long-standing balancing selection at the human defensin beta-1 promoter Genome Biol 9 R143 10.1186/gb-2008-9-9-r143 10.1186/gb-2008-9-9-r143 18817538
6. D Charlesworth 2006 Balancing selection and its effects on sequences in nearby genome regions PLoS Genet 2 e64 10.1371/journal.pgen.0020064 10.1371/journal.pgen.0020064 16683038
7. GM Cooper M Brudno EA Stone I Dubchak S Batzoglou A Sidow 2004 Characterization of evolutionary rates and constraints in three mammalian genomes Genome Res 14 539 548 1:CAS:528:DC%2BD2cXjt1yjsbg%3D 10.1101/gr.2034704 15059994 (Pubitemid 38500224)
8. M Emerman HS Malik 2010 Paleovirology-modern consequences of ancient viruses PLoS Biol 8 e1000301 10.1371/journal.pbio.1000301 10.1371/journal.pbio. 1000301 20161719
9. PD Evans SL Gilbert N Mekel-Bobrov EJ Vallender JR Anderson LM Vaez-Azizi SA Tishkoff RR Hudson BT Lahn 2005 Microcephalin, a gene regulating brain size, continues to evolve adaptively in humans Science 309 1717 1720 10.1126/science.1113722 1:CAS:528:DC%2BD2MXpvFCis7o%3D 10.1126/science.1113722 16151009 (Pubitemid 41285939)
10. P Forster R Harding A Torroni H-J Bandelt 1996 Origin and evolution of native American mtDNA variation: a reappraisal Am J Hum Genet 59 935 945 1:CAS:528:DyaK28Xmt1KqsL8%3D 8808611
11. YX Fu WH Li 1993 Statistical tests of neutrality of mutations Genetics 133 693 709 1:STN:280:DyaK3s3gt1Crsw%3D%3D 8454210
12. M Fumagalli R Cagliani U Pozzoli S Riva GP Comi G Menozzi N Bresolin M Sironi 2009 Widespread balancing selection and pathogen-driven selection at blood group antigen genes Genome Res 19 199 212 10.1101/gr.082768.108 1:CAS:528:DC%2BD1MXhvVSjurc%3D 10.1101/gr.082768.108 18997004
13. SB Gabriel SF Schaffner H Nguyen JM Moore J Roy B Blumenstiel J Higgins M DeFelice A Lochner M Faggart SN Liu-Cordero C Rotimi A Adeyemo R Cooper R Ward ES Lander MJ Daly D Altschuler 2002 The structure of haplotype blocks in the human genome Science 296 2225 2229 1:CAS:528:DC%2BD38XkvFGhtrc%3D 10.1126/science.1069424 12029063 (Pubitemid 34680308)
14. GV Glazko M Nei 2003 Estimation of divergence times for major lineages of primate species Mol Biol Evol 20 424 434 1:CAS:528:DC%2BD3sXisFaqsbs%3D 10.1093/molbev/msg050 12644563 (Pubitemid 36427177)
15. V Goldschmidt G Bleiber M May R Martinez M Ortiz A Telenti Swiss HIV cohort study 2006 Role of common human TRIM5α variants in HIV-1 disease progression Retrovirology 3 54 10.1186/1742-4690-3-54 10.1186/1742-4690-3-54 16925802 (Pubitemid 44377740)
16. RC Griffiths S Tavare 1994 Sampling theory for neutral alleles in a varying environment Philos Trans R Soc Lond B Biol Sci 344 403 410 10.1098/rstb.1994.0079 1:STN:280:DyaK2M%2FpvVyqtg%3D%3D 10.1098/rstb.1994.0079 7800710
17. RC Griffiths S Tavare 1995 Unrooted genealogical tree probabilities in the infinitely-many-sites model Math Biosci 127 77 98 1:STN:280: DyaK2M3lt1Ojug%3D%3D 10.1016/0025-5564(94)00044-Z 7734858
18. T Heinemeyer E Wingender I Reuter H Hermjakob AE Kel OV Kel EV Ignatieva EA Ananko OA Podkolodnaya FA Kolpakov NL Podkolodny NA Kolchanov 1998 Databases on transcriptional regulation: TRANSFAC, TRRD and COMPEL Nucleic Acids Res 26 362 367 1:CAS:528:DyaK1cXovVCktQ%3D%3D 10.1093/nar/26.1.362 9399875 (Pubitemid 28295292)
19. RR Hudson M Kreitman M Aguade 1987 A test of neutral molecular evolution based on nucleotide data Genetics 116 153 159 1:CAS:528:DyaL2sXktlCgsLk%3D 3110004
20. H Javanbakht P An B Gold DC Petersen C O'Huigin GW Nelson SJ O'Brien GD Kirk R Detels S Buchbinder S Donfield S Shulenin B Song MJ Perron M Stremlau J Sodroski M Dean C Winkler 2006 Effects of human TRIM5α polymorphisms on antiretroviral function and susceptibility to human immunodeficiency virus infection Virology 354 15 27 10.1016/j.virol.2006.06.031 1:CAS:528: DC%2BD28XhtVWqtLrI 10.1016/j.virol.2006.06.031 16887163 (Pubitemid 44468115)
21. WE Johnson SL Sawyer 2009 Molecular evolution of the antiretroviral TRIM5 gene Immunogenetics 61 163 176 10.1007/s00251-009-0358-y 1:CAS:528: DC%2BD1MXis1Kju7w%3D 10.1007/s00251-009-0358-y 19238338
22. IK Jordan IB Rogozin GV Glazko EV Koonin 2003 Origin of a substantial fraction of human regulatory sequences from transposable elements Trends Genet 19 68 72 1:CAS:528:DC%2BD3sXkvVyitg%3D%3D 10.1016/S0168-9525(02)00006-9 12547512 (Pubitemid 36120660)
23. SM Kaiser HS Malik M Emerman 2007 Restriction of an extinct retrovirus by the human TRIM5α antiviral protein Science 316 1756 1758 10.1126/science.1140579 1:CAS:528:DC%2BD2sXms1Wgsb0%3D 10.1126/science.1140579 17588933 (Pubitemid 46988552)
24. S Karlin SF Altschul 1990 Methods for assessing the statistical significance of molecular sequence features by using general scoring schemes Proc Natl Acad Sci USA 87 2264 2268 1:CAS:528:DyaK3cXhslGhsbo%3D 10.1073/pnas.87.6.2264 2315319
25. S Karlin SF Altschul 1993 Applications and statistics for multiple high-scoring segments in molecular sequences Proc Natl Acad Sci USA 90 5873 5877 1:CAS:528:DyaK3sXks1Ohs70%3D 10.1073/pnas.90.12.5873 8390686
26. X Liu Y Fu Z Liu B Lin Y Xie Y Liu Y Xu J Lin X Fan M Dong K Zeng CI Wu A Xu 2006 An ancient balanced polymorphism in a regulatory region of human major histocompatibility complex is retained in Chinese minorities but lost worldwide Am J Hum Genet 78 393 400 10.1086/500593 1:CAS:528:DC%2BD28XitVWqt7c%3D 10.1086/500593 16465617 (Pubitemid 43291222)
27. DA Loisel MV Rockman GA Wray J Altmann SC Alberts 2006 Ancient polymorphism and functional variation in the primate MHC-DQA1 5' cis-regulatory region Proc Natl Acad Sci USA 103 16331 16336 10.1073/pnas.0607662103 1:CAS:528:DC%2BD28Xht1WmsLrE 10.1073/pnas.0607662103 17053068 (Pubitemid 44715196)
28. GT Marth E Czabarka J Murvai ST Sherry 2004 The allele frequency spectrum in genome-wide human variation data reveals signals of differential demographic history in three large world populations Genetics 166 351 372 1:CAS:528:DC%2BD2cXivFKjtbw%3D 10.1534/genetics.166.1.351 15020430 (Pubitemid 38364726)
29. M Nei WH Li 1979 Mathematical model for studying genetic variation in terms of restriction endonucleases Proc Natl Acad Sci USA 76 5269 5273 1:CAS:528:DyaL3cXitVWn 10.1073/pnas.76.10.5269 291943 (Pubitemid 10236121)
30. RM Newman L Hall M Connole GL Chen S Sato E Yuste W Diehl E Hunter A Kaur GM Miller WE Johnson 2006 Balancing selection and the evolution of functional polymorphism in Old World monkey TRIM5α Proc Natl Acad Sci USA 103 19134 19139 10.1073/pnas.0605838103 1:CAS:528:DC%2BD28XhtlertbvL 10.1073/pnas. 0605838103 17142324 (Pubitemid 350010634)
31. R Development Core Team (2008) R: a language and environment for statistical computing, Vienna, Austria
32. S Sawyer 1989 Statistical tests for detecting gene conversion Mol Biol Evol 6 526 538 1:CAS:528:DyaL1MXlvFWhtb4%3D 2677599
33. SL Sawyer LI Wu JM Akey M Emerman HS Malik 2006 High-frequency persistence of an impaired allele of the retroviral defense gene TRIM5α in humans Curr Biol 16 95 100 10.1016/j.cub.2005.11.045 1:CAS:528: DC%2BD28XksVahuw%3D%3D 10.1016/j.cub.2005.11.045 16401428 (Pubitemid 43049892)
34. SL Sawyer M Emerman HS Malik 2007 Discordant evolution of the adjacent antiretroviral genes TRIM22 and TRIM5 in mammals PLoS Pathog 3 e197 10.1371/journal.ppat.0030197 10.1371/journal.ppat.0030197 18159944
35. SF Schaffner C Foo S Gabriel D Reich MJ Daly D Altshuler 2005 Calibrating a coalescent simulation of human genome sequence variation Genome Res 15 1576 1583 10.1101/gr.3709305 1:CAS:528:DC%2BD2MXhtF2itb7E 10.1101/gr.3709305 16251467 (Pubitemid 41545011)
36. S Sewram R Singh E Kormuth L Werner K Mlisana SS Karim T Ndung'u 2009 CAPRISA Acute Infection Study Team Human TRIM5alpha expression levels and reduced susceptibility to HIV-1 infection J Infect Dis 199 1657 1663 10.1086/598861 1:CAS:528:DC%2BD1MXmvVOmurs%3D 10.1086/598861 19388851
37. B Song B Gold C O'Huigin H Javanbakht X Li M Stremlau C Winkler M Dean J Sodroski 2005 The B30.2(SPRY) domain of the retroviral restriction factor TRIM5alpha exhibits lineage-specific length and sequence variation in primates J Virol 79 6111 6121 10.1128/JVI.79.10.6111-6121.2005 1:CAS:528: DC%2BD2MXkt1WitLo%3D 10.1128/JVI.79.10.6111-6121.2005 15857996 (Pubitemid 40617216)
38. EC Speelmon D Livingston-Rosanoff SS Li Q Vu J Bui DE Geraghty LP Zhao MJ McElrath 2006 Genetic association of the antiviral restriction factor TRIM5α with human immunodeficiency virus type 1 infection J Virol 80 2463 2471 10.1128/JVI.80.5.2463-2471.2006 1:CAS:528:DC%2BD28XhvFyhtLk%3D 10.1128/JVI.80.5.2463-2471.2006 16474153 (Pubitemid 43271552)
39. M Stephens P Scheet 2005 Accounting for decay of linkage disequilibrium in haplotype inference and missing-data imputation Am J Hum Genet 76 449 462 10.1086/428594 1:CAS:528:DC%2BD2MXhsFKrsbg%3D 10.1086/428594 15700229 (Pubitemid 40250525)
40. M Stephens NJ Smith P Donnelly 2001 A new statistical method for haplotype reconstruction from population data Am J Hum Genet 68 978 989 10.1086/319501 1:STN:280:DC%2BD3M3kslWgsA%3D%3D 10.1086/319501 11254454 (Pubitemid 32289743)
41. M Stremlau CM Owens MJ Perron M Kiessling P Autissier J Sodroski 2004 The cytoplasmic body component TRIM5α restricts HIV-1 infection in Old World monkeys Nature 427 848 853 10.1038/nature02343 1:CAS:528:DC%2BD2cXhsFCisLo%3D 10.1038/nature02343 14985764 (Pubitemid 38297747)
42. M Stremlau M Perron M Lee Y Li B Song H Javanbakht F Diaz-Griffero DJ Anderson WI Sundquist J Sodroski 2006 Specific recognition and accelerated uncoating of retroviral capsids by the TRIM5α restriction factor Proc Natl Acad Sci USA 103 5514 5519 10.1073/pnas.0509996103 1:CAS:528: DC%2BD28Xjslejs70%3D 10.1073/pnas.0509996103 16540544
43. F Tajima 1989 Statistical method for testing the neutral mutation hypothesis by DNA polymorphism Genetics 123 585 595 1:CAS:528: DyaK3cXhslentA%3D%3D 2513255
44. Z Tan AM Shon C Ober 2005 Evidence of balancing selection at the HLA-G promoter region Hum Mol Genet 14 3619 3628 10.1093/hmg/ddi389 1:CAS:528:DC%2BD2MXht1GgsrvN 10.1093/hmg/ddi389 16236759 (Pubitemid 41754663)
45. SU Tareen SL Sawyer HS Malik M Emerman 2009 An expanded clade of rodent Trim5 genes Virology 385 473 483 10.1016/j.virol.2008.12.018 1:CAS:528:DC%2BD1MXisFOnt7s%3D 10.1016/j.virol.2008.12.018 19147168
46. K Thornton 2003 Libsequence: a C++ class library for evolutionary genetic analysis Bioinformatics 19 2325 2327 1:CAS:528:DC%2BD3sXpvVSjurc%3D 10.1093/bioinformatics/btg316 14630667 (Pubitemid 37483994)
47. SA Tishkoff BC Verrelli 2003 Patterns of human genetic diversity: implications for human evolutionary history and disease Annu Rev Genomics Hum Genet 4 293 340 10.1146/annurev.genom.4.070802.110226 1:CAS:528: DC%2BD3sXptFWmtbk%3D 10.1146/annurev.genom.4.070802.110226 14527305 (Pubitemid 37392927)
48. LN van de Lagemaat JR Landry DL Mager P Medstrand 2003 Transposable elements in mammals promote regulatory variation and diversification of genes with specialized functions Trends Genet 19 530 536 10.1016/j.tig.2003.08.004 14550626 (Pubitemid 37204911)
49. D van Manen MA Rits C Beugeling K van Dort H Schuitemaker NA Kootstra 2008 The effect of Trim5 polymorphisms on the clinical course of HIV-1 infection PLoS Pathog 4 e18 10.1371/journal.ppat.0040018 10.1371/journal.ppat.0040018 18248091 (Pubitemid 351340720)
50. CA Virgen Z Kratovac PD Bieniasz T Hatziioannou 2008 Independent genesis of chimeric TRIM5-cyclophilin proteins in two primate species Proc Natl Acad Sci USA 105 3563 3568 10.1073/pnas.0709258105 1:CAS:528:DC%2BD1cXjtlaltb8%3D 10.1073/pnas.0709258105 18287034 (Pubitemid 351723592)
51. BF Voight AM Adams LA Frisse Y Qian RR Hudson A Di Rienzo 2005 Interrogating multiple aspects of variation in a full resequencing data set to infer human population size changes Proc Natl Acad Sci USA 102 18508 18513 10.1073/pnas.0507325102 1:CAS:528:DC%2BD28Xpt1Oj 10.1073/pnas.0507325102 16352722 (Pubitemid 43011256)
52. GA Watterson 1975 On the number of segregating sites in genetical models without recombination Theor Popul Biol 7 256 276 1:STN:280:DyaE2M7pvFSquw%3D%3D 10.1016/0040-5809(75)90020-9 1145509
53. SI Wright B Charlesworth 2004 The HKA test revisited: a maximum-likelihood-ratio test of the standard neutral model Genetics 168 1071 1076 10.1534/genetics.104.026500 10.1534/genetics.104.026500 15514076 (Pubitemid 39491480)
54. G Zogopoulos KC Ha F Naqib S Moore H Kim A Montpetit F Robidoux P Laflamme M Cotterchio C Greenwood SW Scherer B Zanke TJ Hudson GD Bader S Gallinger 2007 Germ-line DNA copy number variation frequencies in a large North American population Hum Genet 122 345 353 10.1007/s00439-007-0404-5 1:CAS:528:DC%2BD2sXhtFyqsrrP 10.1007/s00439-007-0404-5 17638019 (Pubitemid 47616542)