A trans-specific polymorphism in ZC3HAV1 is maintained by long-standing balancing selection and may confer susceptibility to multiple sclerosis

Molecular Biology and Evolution

Volumn 29, Issue 6, 2012, Pages 1599-1613

  Cagliani, R ^a   Guerini, F R ^b   Fumagalli, M ^a   Riva, S ^a   Agliardi, C ^b   Galimberti, D ^c   Pozzoli, U ^a   Goris, A ^d   Dubois, B ^d   Fenoglio, C ^c   Forni, D ^a   Sanna, S ^e   Zara, I ^f   Pitzalis, M ^g   Zoledziewska, M ^g   Cucca, F ^e,g   Marini, F ^a   Comi, G P ^c   Scarpini, E ^c   Bresolin, N ^a,c   Clerici, M ^b,c   Sironi, M ^a   more..

^a SCIENTIFIC INSTITUTE   (Italy)

^b IRCCS FONDAZIONE DON CARLO GNOCCHI   (Italy)

^c UNIVERSITY OF MILAN   (Italy)

^d KU LEUVEN UNIVERSITY OF LEUVEN   (Belgium)

^e Milan Unit   (Italy)

^f Parco Tecnologico della Sardegna   (Italy)

^g UNIVERSITY OF SASSARI   (Italy)

Author keywords

Balancing selection; Multiple sclerosis; Trans specific polymorphism; ZC3HAV1

Indexed keywords

ISOPROTEIN; VIRUS PROTEIN; ZINC FINGER PROTEIN;

AMINO ACID SUBSTITUTION; ANIMAL CELL; ARTICLE; CHIMPANZEE; CONTROLLED STUDY; DNA POLYMORPHISM; FEMALE; GENE; GENE MUTATION; GENE SEQUENCE; GENETIC CODE; GENETIC POLYMORPHISM; GENETIC SELECTION; GENETIC SUSCEPTIBILITY; GENETIC VARIABILITY; GENOME; HAPLOTYPE; HUMAN; HUMAN CELL; ITALY; MAJOR CLINICAL STUDY; MAJOR HISTOCOMPATIBILITY COMPLEX; MALE; MULTIPLE SCLEROSIS; NONHUMAN; POLYMERASE CHAIN REACTION; POPULATION GENETICS; RNA SPLICING; SINGLE NUCLEOTIDE POLYMORPHISM; UBIQUITINATION; ZC3HAV1 GENE;

ACEBUTOLOL; ANIMALS; CASE-CONTROL STUDIES; GENE-ENVIRONMENT INTERACTION; GENETIC ASSOCIATION STUDIES; GENETIC PREDISPOSITION TO DISEASE; GENOME, HUMAN; HAPLOTYPES; HUMANS; LINKAGE DISEQUILIBRIUM; MODELS, GENETIC; MULTIPLE SCLEROSIS; ODDS RATIO; PAN TROGLODYTES; PHYLOGENY; POLYMORPHISM, SINGLE NUCLEOTIDE; PROTEIN ISOFORMS; PROTEIN STRUCTURE, TERTIARY; RNA-BINDING PROTEINS; SELECTION, GENETIC; SEQUENCE ANALYSIS, DNA;

PAN; PAN TROGLODYTES; PRIMATES;

EID: 84861385332     PISSN: 07374038     EISSN: 15371719     Source Type: Journal    
DOI: 10.1093/molbev/mss002     Document Type: Article

References (92)

1. Abecasis GR, Cookson WO. 2000. GOLD-graphical overview of linkage disequilibrium. Bioinformatics 16:182-183.
2. Adzhubei IA, Schmidt S, Peshkin L, Ramensky VE, Gerasimova A, Bork P, Kondrashov AS, Sunyaev SR. 2010. A method and server for predicting damaging missense mutations. Nat Methods. 7:248-249.
3. Bandelt HJ, Forster P, Rohl A. 1999. Median-joining networks for inferring intraspecific phylogenies. Mol Biol Evol. 16:37-48. (Pubitemid 29024937)
4. Barreiro LB, Quintana-Murci L. 2010. From evolutionary genetics to human immunology: how selection shapes host defence genes. Nat Rev Genet. 11:17-30.
5. Barrett JC, Fry B, Maller J, Daly MJ. 2005. Haploview: analysis and visualization of LD and haplotype maps. Bioinformatics 21:263-265. (Pubitemid 40202029)
6. Bick MJ, Carroll JW, Gao G, Goff SP, Rice CM, MacDonald MR. 2003. Expression of the zinc-finger antiviral protein inhibits alphavirus replication. J Virol. 77:11555-11562. (Pubitemid 37271654)
7. Bromberg Y, Rost B. 2007. SNAP: predict effect of non-synonymous polymorphisms on function. Nucleic Acids Res. 35:3823-3835. (Pubitemid 47244674)
8. Bubb KL, Bovee D, Buckley D, et al. (12 co-authors). 2006. Scan of human genome reveals no new loci under ancient balancing selection. Genetics 173:2165-2177. (Pubitemid 44285693)
9. Cagliani R, Fumagalli M, Biasin M, Piacentini L, Riva S, Pozzoli U, Bonaglia MC, Bresolin N, Clerici M, Sironi M. 2010. Long-term balancing selection maintains trans-specific polymorphisms in the human TRIM5 gene. Hum Genet. 128:577-588.
10. Cagliani R, Fumagalli M, Guerini FR, et al. (17 co-authors). 2011. Identification of a new susceptibility variant for multiple sclerosis in OAS1 by population genetics analysis. Hum Genet. 131:87-97.
11. Cagliani R, Fumagalli M, Riva S, Pozzoli U, Comi GP, Menozzi G, Bresolin N, Sironi M. 2008. The signature of long-standing balancing selection at the human defensin beta-1 promoter. Genome Biol. 9:R143.
12. Calabrese R, Capriotti E, Fariselli P, Martelli PL, Casadio R. 2009. Functional annotations improve the predictive score of human disease-related mutations in proteins. Hum Mutat. 30:1237-1244.
13. Cereda M, Sironi M, Cavalleri M, Pozzoli U. 2011. GeCo + +: a C + + library for genomic features computation and annotation in the presence of variants. Bioinformatics 27:1313-1315.
14. Charlesworth D. 2006. Balancing selection and its effects on sequences in nearby genome regions. PLoS Genet. 2:e64.
15. Chen Z, Chen YZ, Wang XF, Wang C, Yan RX, Zhang Z. 2011. Prediction of ubiquitination sites by using the composition of k-spaced amino acid pairs. PLoS One 6:e22930.
16. Clark AG. 1997. Neutral behavior of shared polymorphism. Proc Natl Acad Sci USA. 94:7730-7734. (Pubitemid 27343718)
17. Claw KG, Tito RY, Stone AC, Verrelli BC. 2010. Haplotype structure and divergence at human and chimpanzee serotonin transporter and receptor genes: implications for behavioral disorder association analyses. Mol Biol Evol. 27:1518-1529.
18. Cooper GM, Stone EA, Asimenos G, NISC Comparative Sequencing Program, Green ED, Batzoglou S, Sidow A. 2005. Distribution and intensity of constraint in mammalian genomic sequence. Genome Res. 15:901-913. (Pubitemid 40994210)
19. Ebers GC. 2008. Environmental factors and multiple sclerosis. Lancet Neurol. 7:268-277. (Pubitemid 351222732)
20. Egloff MP, Malet H, Putics A, et al. (12 co-authors). 2006. Structural and functional basis for ADP-ribose and poly(ADP-ribose) binding by viral macro domains. J Virol. 80:8493-8502. (Pubitemid 44384861)
21. Evans PD, Gilbert SL, Mekel-Bobrov N, Vallender EJ, Anderson JR, Vaez-Azizi LM, Tishkoff SA, Hudson RR, Lahn BT. 2005. Microcephalin, a gene regulating brain size, continues to evolve adaptively in humans. Science 309:1717-1720. (Pubitemid 41285939)
22. Frisse L, Hudson RR, Bartoszewicz A, Wall JD, Donfack J, Di Rienzo A. 2001. Gene conversion and different population histories may explain the contrast between polymorphism and linkage disequilibrium levels. Am J Hum Genet. 69:831-843. (Pubitemid 32868527)
23. Fu YX, Li WH. 1993. Statistical tests of neutrality of mutations. Genetics 133:693-709.
24. Fumagalli M, Cagliani R, Pozzoli U, Riva S, Comi GP, Menozzi G, Bresolin N, Sironi M. 2009. Widespread balancing selection and pathogen-driven selection at blood group antigen genes. Genome Res. 19:199-212.
25. Fumagalli M, Pozzoli U, Cagliani R, Comi GP, Bresolin N, Clerici M, Sironi M. 2010. Genome-wide identification of susceptibility alleles for viral infections through a population genetics approach. PLoS Genet. 6:e1000849.
26. Fumagalli M, Pozzoli U, Cagliani R, Comi GP, Riva S, Clerici M, Bresolin N, Sironi M. 2009. Parasites represent a major selective force for interleukin genes and shape the genetic predisposition to autoimmune conditions. J Exp Med. 206: 1395-1408.
27. Gabriel SB, Schaffner SF, Nguyen H, et al. (18 co-authors). 2002. The structure of haplotype blocks in the human genome. Science 296:2225-2229. (Pubitemid 34680308)
28. Gao G, Guo X, Goff SP. 2002. Inhibition of retroviral RNA production by ZAP, a CCCH-type zinc finger protein. Science 297:1703-1706. (Pubitemid 35000785)
29. Garrigan D, Hammer MF. 2006. Reconstructing human origins in the genomic era. Nat Rev Genet. 7:669-680. (Pubitemid 44260003)
30. 1000 Genomes Project Consortium, Durbin RM, Abecasis GR, Altshuler DL, Auton A, Brooks LD, Durbin RM, Gibbs RA, Hurles ME, McVean GA. 2010. A map of human genome variation from population-scale sequencing. Nature 467:1061-1073.
31. Gilad Y, Bustamante CD, Lancet D, Paabo S. 2003. Natural selection on the olfactory receptor gene family in humans and chimpanzees. Am J Hum Genet. 73:489-501. (Pubitemid 37076264)
32. Glazko GV, Nei M. 2003. Estimation of divergence times for major lineages of primate species. Mol Biol Evol. 20:424-434. (Pubitemid 36427177)
33. Gongora R, Figueroa F, Klein J. 1996. The HLA-DRB9 gene and the origin of HLA-DR haplotypes. Hum Immunol. 51:23-31. (Pubitemid 26365653)
34. Gorbalenya AE, Koonin EV, Lai MM. 1991. Putative papain-related thiol proteases of positive-strand RNA viruses. Identification of rubi-and aphthovirus proteases and delineation of a novel conserved domain associated with proteases of rubi-, alpha-and coronaviruses. FEBS Lett. 288:201-205.
35. Grantham R. 1974. Amino acid difference formula to help explain protein evolution. Science 185:862-864.
36. Griffiths RC, Tavare S. 1994. Sampling theory for neutral alleles in a varying environment. Philos Trans R Soc Lond B Biol Sci. 344:403-410.
37. Griffiths RC, Tavare S. 1995. Unrooted genealogical tree probabilities in the infinitely-many-sites model. Math Biosci. 127:77-98.
38. Guo X, Carroll JW, Macdonald MR, Goff SP, Gao G. 2004. The zinc finger antiviral protein directly binds to specific viral mRNAs through the CCCH zinc finger motifs. J Virol. 78:12781-12787. (Pubitemid 39507786)
39. Guo X, Ma J, Sun J, Gao G. 2007. The zinc-finger antiviral protein recruits the RNA processing exosome to degrade the target mRNA. Proc Natl Acad Sci USA. 104:151-156. (Pubitemid 46068000)
40. Gutenkunst RN, Hernandez RD, Williamson SH, Bustamante CD. 2009. Inferring the joint demographic history of multiple populations from multidimensional SNP frequency data. PLoS Genet. 5:e1000695.
41. Hudson RR. 2001. Two-locus sampling distributions and their application. Genetics 159:1805-1817. (Pubitemid 34087616)
42. Kendall MG. 1976. Rank correlation methods. London: Griffin.
43. Kerns JA, Emerman M, Malik HS. 2008. Positive selection and increased antiviral activity associated with the PARPcontaining isoform of human zinc-finger antiviral protein. PLoS Genet. 4:e21.
44. Kumar S, Filipski A, Swarna V, Walker A, Hedges SB. 2005. Placing confidence limits on the molecular age of the human-chimpanzee divergence. Proc Natl Acad Sci USA. 102:18842-18847. (Pubitemid 43050942)
45. Lawlor DA, Ward FE, Ennis PD, Jackson AP, Parham P. 1988. HLA-A and B polymorphisms predate the divergence of humans and chimpanzees. Nature 335:268-271.
46. Li B, Krishnan VG, Mort ME, Xin F, Kamati KK, Cooper DN, Mooney SD, Radivojac P. 2009. Automated inference of molecular mechanisms of disease from amino acid substitutions. Bioinformatics 25:2744-2750.
47. Marth GT, Czabarka E, Murvai J, Sherry ST. 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. (Pubitemid 38364726)
48. Mayer WE, Jonker M, Klein D, Ivanyi P, van Seventer G, Klein J. 1988. Nucleotide sequences of chimpanzee MHC class I alleles: evidence for trans-species mode of evolution. EMBO J. 7:2765-2774.
49. McDonald WI, Compston A, Edan G, et al. (16 co-authors). 2001. Recommended diagnostic criteria for multiple sclerosis: guidelines from the international panel on the diagnosis of multiple sclerosis. Ann Neurol. 50:121-127.
50. McIntire JJ, Umetsu SE, Macaubas C, et al. (13 co-authors). 2003. Immunology: hepatitis A virus link to atopic disease. Nature 425:576. (Pubitemid 37280135)
51. McVean G, Awadalla P, Fearnhead P. 2002. A coalescent-based method for detecting and estimating recombination from gene sequences. Genetics 160:1231-1241. (Pubitemid 34263482)
52. Morin PA, Moore JJ, Chakraborty R, Jin L, Goodall J, Woodruff DS. 1994. Kin selection, social structure, gene flow, and the evolution of chimpanzees. Science 265:1193-1201. (Pubitemid 24291977)
53. Muller S, Moller P, Bick MJ, Wurr S, Becker S, Gunther S, Kummerer BM. 2007. Inhibition of filovirus replication by the zinc finger antiviral protein. J Virol. 81:2391-2400.
54. Nachman MW, Crowell SL. 2000. Estimate of the mutation rate per nucleotide in humans. Genetics 156:297-304.
55. Nei M, Li WH. 1979. Mathematical model for studying genetic variation in terms of restriction endonucleases. Proc Natl Acad Sci USA. 76:5269-5273. (Pubitemid 10236121)
56. Neuvonen M, Ahola T. 2009. Differential activities of cellular and viral macro domain proteins in binding of ADP-ribose metabolites. J Mol Biol. 385:212-225.
57. Ng PC, Henikoff S. 2003. SIFT: predicting amino acid changes that affect protein function. Nucleic Acids Res. 31:3812-3814. (Pubitemid 37442253)
58. O'Brien M, Lonergan R, Costelloe L, et al. (12 co-authors). 2010. OAS1: a multiple sclerosis susceptibility gene that influences disease severity. Neurology 75:411-418.
59. Ouararhni K, Hadj-Slimane R, Ait-Si-Ali S, Robin P, Mietton F, Harel-Bellan A, Dimitrov S, Hamiche A. 2006. The histone variant mH2A1.1 interferes with transcription by down-regulating PARP-1 enzymatic activity. Genes Dev. 20:3324-3336. (Pubitemid 44904853)
60. Poser CM. 2006. Revisions to the 2001 McDonald diagnostic criteria. Ann Neurol. 59:727-728.
61. Pritchard JK, Stephens M, Donnelly P. 2000. Inference of population structure using multilocus genotype data. Genetics 155:945-959. (Pubitemid 30397141)
62. Prugnolle F, Manica A, Charpentier M, Guegan JF, Guernier V, Balloux F. 2005. Pathogen-driven selection and worldwide HLA class I diversity. Curr Biol. 15:1022-1027. (Pubitemid 40772149)
63. Pugliatti M, Rosati G, Carton H, Riise T, Drulovic J, Vecsei L, Milanov I. 2006. The epidemiology of multiple sclerosis in Europe. Eur J Neurol. 13:700-722. (Pubitemid 44143944)
64. Purcell S, Neale B, Todd-Brown K, et al. (11 co-authors). 2007. PLINK: a tool set for whole-genome association and population-based linkage analyses. Am J Hum Genet. 81:559-575. (Pubitemid 47330214)
65. R Development Core Team. 2008. R: a language and environment for statistical computing. Vienna (Austria): R Foundation for Statistical Computing.
66. Radivojac P, Vacic V, Haynes C, Cocklin RR, Mohan A, Heyen JW, Goebl MG, Iakoucheva LM. 2010. Identification, analysis, and prediction of protein ubiquitination sites. Proteins 78:365-380.
67. Ray N, Wegmann D, Fagundes NJ, Wang S, Ruiz-Linares A, Excoffier L. 2010. A statistical evaluation of models for the initial settlement of the American continent emphasizes the importance of gene flow with Asia. Mol Biol Evol. 27:337-345.
68. Romanoski CE, Lee S, Kim MJ, et al. (13 co-authors). 2010. Systems genetics analysis of gene-by-environment interactions in human cells. Am J Hum Genet. 86:399-410.
69. Salkind NJ, editor. 2007. Encyclopedia of measurement and statistics. Thousand Oaks (CA): Sage Publications.
70. Sanna S, Pitzalis M, Zoledziewska M, et al. (41 co-authors). 2010. Variants within the immunoregulatory CBLB gene are associated with multiple sclerosis. Nat Genet. 42:495-497.
71. Schaffner SF, Foo C, Gabriel S, Reich D, Daly MJ, Altshuler D. 2005. Calibrating a coalescent simulation of human genome sequence variation. Genome Res. 15:1576-1583. (Pubitemid 41545011)
72. Sironi M, Clerici M. 2010. The hygiene hypothesis: an evolutionary perspective. Microbes Infect. 12:421-427.
73. Stephens M, Scheet P. 2005. Accounting for decay of linkage disequilibrium in haplotype inference and missing-data imputation. Am J Hum Genet. 76:449-462. (Pubitemid 40250525)
74. Stephens M, Smith NJ, Donnelly P. 2001. A new statistical method for haplotype reconstruction from population data. Am J Hum Genet. 68:978-989. (Pubitemid 32289743)
75. Stone AC, Griffiths RC, Zegura SL, Hammer MF. 2002. High levels of Y-chromosome nucleotide diversity in the genus pan. Proc Natl Acad Sci USA. 99:43-48. (Pubitemid 34060313)
76. Sunyaev S, Ramensky V, Koch I, Lathe W 3rd, Kondrashov AS, Bork P. 2001. Prediction of deleterious human alleles. Hum Mol Genet. 10:591-597. (Pubitemid 32229363)
77. Tajima F. 1989. Statistical method for testing the neutral mutation hypothesis by DNA polymorphism. Genetics 123:585-595. (Pubitemid 19274682)
78. Tan J, Vonrhein C, Smart OS, Bricogne G, Bollati M, Kusov Y, Hansen G, Mesters JR, Schmidt CL, Hilgenfeld R. 2009. The SARSunique domain (SUD) of SARS coronavirus contains two macrodomains that bind G-quadruplexes. PLoS Pathog. 5:e1000428.
79. Thomas PD, Kejariwal A. 2004. Coding single-nucleotide polymorphisms associated with complex vs. mendelian disease: evolutionary evidence for differences in molecular effects. Proc Natl Acad Sci USA. 101:15398-15403. (Pubitemid 39441553)
80. Thomson G. 1995. Mapping disease genes: family-based association studies. Am J Hum Genet. 57:487-498.
81. Thomson R, Pritchard JK, Shen P, Oefner PJ, Feldman MW. 2000. Recent common ancestry of human Y chromosomes: evidence from DNA sequence data. Proc Natl Acad Sci USA. 97: 7360-7365. (Pubitemid 30431468)
82. Thornton K. 2003. Libsequence: a C + + class library for evolutionary genetic analysis. Bioinformatics 19:2325-2327. (Pubitemid 37483994)
83. Tishkoff SA, Verrelli BC. 2003. Patterns of human genetic diversity: implications for human evolutionary history and disease. Annu Rev Genomics Hum Genet. 4:293-340. (Pubitemid 37392927)
84. Verrelli BC, Lewis CM Jr, Stone AC, Perry GH. 2008. Different selective pressures shape the molecular evolution of color vision in chimpanzee and human populations. Mol Biol Evol. 25:2735-2743.
85. Verrelli BC, Tishkoff SA, Stone AC, Touchman JW. 2006. Contrasting histories of G6PD molecular evolution and malarial resistance in humans and chimpanzees. Mol Biol Evol. 23:1592-1601. (Pubitemid 44297417)
86. Voight BF, Adams AM, Frisse LA, Qian Y, Hudson RR, Di Rienzo A. 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. (Pubitemid 43011256)
87. Watterson GA. 1975. On the number of segregating sites in genetical models without recombination. Theor Popul Biol. 7:256-276.
88. Wittke-Thompson JK, Pluzhnikov A, Cox NJ. 2005. Rational inferences about departures from Hardy-Weinberg equilibrium. Am J Hum Genet. 76:967-986. (Pubitemid 40705433)
89. Wiuf C, Zhao K, Innan H, Nordborg M. 2004. The probability and chromosomal extent of trans-specific polymorphism. Genetics 168:2363-2372. (Pubitemid 40066368)
90. Wright SI, Charlesworth B. 2004. The HKA test revisited: a maximumlikelihood-ratio test of the standard neutral model. Genetics 168:1071-1076. (Pubitemid 39491480)
91. Yu N, Jensen-Seaman MI, Chemnick L, Kidd JR, Deinard AS, Ryder O, Kidd KK, Li WH. 2003. Low nucleotide diversity in chimpanzees and bonobos. Genetics 164:1511-1518. (Pubitemid 37102212)
92. Zhang Y, Burke CW, Ryman KD, Klimstra WB. 2007. Identification and characterization of interferon-induced proteins that inhibit alphavirus replication. J Virol. 81:11246-11255. (Pubitemid 47536097)