Diverse selective regimes shape genetic diversity at ADAR genes and at their coding targets

References

• Nishikura K. Functions and regulation of RNA editing by ADAR deaminases. Annu Rev Biochem 2010; 79:321-349; PMID:20192758; http://dx.doi.org/10.1146/annurev-biochem-060208-105251
   PubMed Web of Science ®Google Scholar
• Bazak L, Haviv A, Barak M, Jacob-Hirsch J, Deng P, Zhang R, Isaacs FJ, Rechavi G, Li JB, Eisenberg E, et al. A-to-I RNA editing occurs at over a hundred million genomic sites, located in a majority of human genes. Genome Res 2014; 24:365-376; PMID:24347612; http://dx.doi.org/10.1101/gr.164749.113
   PubMed Web of Science ®Google Scholar
• Savva YA, Rieder LE, Reenan RA. The ADAR protein family. Genome Biol 2012; 13:252; PMID:23273215; http://dx.doi.org/10.1186/gb-2012-13-12-252
   PubMed Web of Science ®Google Scholar
• Samuel CE. ADARs: Viruses and innate immunity. Curr Top Microbiol Immunol 2012; 353:163-195; PMID:21809195
   PubMed Web of Science ®Google Scholar
• Slotkin W, Nishikura K. Adenosine-to-inosine RNA editing and human disease. Genome Med 2013; 5:105; PMID:24289319; http://dx.doi.org/10.1186/gm508
   PubMed Web of Science ®Google Scholar
• Rice GI, Kasher PR, Forte GM, Mannion NM, Greenwood SM, Szynkiewicz M, Dickerson JE, Bhaskar SS, Zampini M, Briggs TA, et al. Mutations in ADAR1 cause aicardi-goutieres syndrome associated with a type I interferon signature. Nat Genet 2012; 44:1243-1248; PMID:23001123; http://dx.doi.org/10.1038/ng.2414
   PubMed Web of Science ®Google Scholar
• Daniel C, Silberberg G, Behm M, Ohman M. Alu elements shape the primate transcriptome by cis-regulation of RNA editing. Genome Biol 2014; 15:R28; PMID:24485196; http://dx.doi.org/10.1186/gb-2014-15-2-r28
   PubMed Web of Science ®Google Scholar
• Li JB, Church GM. Deciphering the functions and regulation of brain-enriched A-to-I RNA editing. Nat Neurosci 2013; 16:1518-1522; PMID:24165678; http://dx.doi.org/10.1038/nn.3539
   PubMed Web of Science ®Google Scholar
• Pinto Y, Cohen HY, Levanon EY. Mammalian conserved ADAR targets comprise only a small fragment of the human editosome. Genome Biol 2014; 15:R5; PMID:24393560; http://dx.doi.org/10.1186/gb-2014-15-1-r5
   PubMed Web of Science ®Google Scholar
• Paz-Yaacov N, Levanon EY, Nevo E, Kinar Y, Harmelin A, Jacob-Hirsch J, Amariglio N, Eisenberg E, Rechavi G. Adenosine-to-inosine RNA editing shapes transcriptome diversity in primates. Proc Natl Acad Sci U S A 2010; 107:12174-12179; PMID:20566853; http://dx.doi.org/10.1073/pnas.1006183107
   PubMed Web of Science ®Google Scholar
• Gommans WM, Mullen SP, Maas S. RNA editing: A driving force for adaptive evolution? Bioessays 2009; 31:1137-1145; PMID:19708020; http://dx.doi.org/10.1002/bies.200900045
   PubMedGoogle Scholar
• Xu G, Zhang J. Human coding RNA editing is generally nonadaptive. Proc Natl Acad Sci U S A 2014; 111:3769-3774; PMID:24567376; http://dx.doi.org/10.1073/pnas.1321745111
   PubMedGoogle Scholar
• Wernersson R, Pedersen AG. RevTrans: Multiple alignment of coding DNA from aligned amino acid sequences. Nucleic Acids Res 2003; 31:3537-3539; PMID:12824361; http://dx.doi.org/10.1093/nar/gkg609
   PubMed Web of Science ®Google Scholar
• Kosakovsky Pond SL, Posada D, Gravenor MB, Woelk CH, Frost SD. Automated phylogenetic detection of recombination using a genetic algorithm. Mol Biol Evol 2006; 23:1891-1901; PMID:16818476; http://dx.doi.org/10.1093/molbev/msl051
   PubMedGoogle Scholar
• Kosakovsky Pond SL, Frost SD. Not so different after all: A comparison of methods for detecting amino acid sites under selection. Mol Biol Evol 2005; 22:1208-1222; PMID:15703242; http://dx.doi.org/10.1093/molbev/msi105
   PubMed Web of Science ®Google Scholar
• Lindblad-Toh K, Garber M, Zuk O, Lin MF, Parker BJ, Washietl S, Kheradpour P, Ernst J, Jordan G, Mauceli E, et al. A high-resolution map of human evolutionary constraint using 29 mammals. Nature 2011; 478:476-482; PMID:21993624; http://dx.doi.org/10.1038/nature10530
   PubMed Web of Science ®Google Scholar
• Yang Z. PAML: A program package for phylogenetic analysis by maximum likelihood. Comput Appl Biosci 1997; 13:555-556; PMID:9367129
   PubMedGoogle Scholar
• Yang Z. PAML 4: Phylogenetic analysis by maximum likelihood. Mol Biol Evol 2007; 24:1586-1591; PMID:17483113; http://dx.doi.org/10.1093/molbev/msm088
   PubMed Web of Science ®Google Scholar
• Anisimova M, Bielawski JP, Yang Z. Accuracy and power of bayes prediction of amino acid sites under positive selection. Mol Biol Evol 2002; 19:950-958; PMID:12032251; http://dx.doi.org/10.1093/oxfordjournals.molbev.a004152
   PubMed Web of Science ®Google Scholar
• Yang Z, Wong WS, Nielsen R. Bayes empirical bayes inference of amino acid sites under positive selection. Mol Biol Evol 2005; 22:1107-1118; PMID:15689528; http://dx.doi.org/10.1093/molbev/msi097
   PubMed Web of Science ®Google Scholar
• Murrell B, Wertheim JO, Moola S, Weighill T, Scheffler K, Kosakovsky Pond SL. Detecting individual sites subject to episodic diversifying selection. PLoS Genet 2012; 8:e1002764; PMID:22807683; http://dx.doi.org/10.1371/journal.pgen.1002764
   PubMed Web of Science ®Google Scholar
• Yang Z, Nielsen R. Synonymous and nonsynonymous rate variation in nuclear genes of mammals. J Mol Evol 1998; 46:409-418; PMID:9541535; http://dx.doi.org/10.1007/PL00006320
   PubMed Web of Science ®Google Scholar
• Kosakovsky Pond SL, Murrell B, Fourment M, Frost SD, Delport W, Scheffler K. A random effects branch-site model for detecting episodic diversifying selection. Mol Biol Evol 2011; 28:3033-3043; PMID:21670087; http://dx.doi.org/10.1093/molbev/msr125
   PubMedGoogle Scholar
• Zhang J, Nielsen R, Yang Z. Evaluation of an improved branch-site likelihood method for detecting positive selection at the molecular level. Mol Biol Evol 2005; 22:2472-2479; PMID:16107592; http://dx.doi.org/10.1093/molbev/msi237
   PubMed Web of Science ®Google Scholar
• Anisimova M, Yang Z. Multiple hypothesis testing to detect lineages under positive selection that affects only a few sites. Mol Biol Evol 2007; 24:1219-1228; PMID:17339634; http://dx.doi.org/10.1093/molbev/msm042
   PubMedGoogle Scholar
• 1000 Genomes Project Consortium, Durbin RM, Abecasis GR, Altshuler DL, Auton A, Brooks LD, Durbin RM, Gibbs RA, Hurles ME, McVean GA. A map of human genome variation from population-scale sequencing. Nature 2010; 467:1061-1073; PMID:20981092; http://dx.doi.org/10.1038/nature09534
   PubMed Web of Science ®Google Scholar
• Auton A, Fledel-Alon A, Pfeifer S, Venn O, Segurel L, Street T, Leffler EM, Bowden R, Aneas I, Broxholme J, et al. A fine-scale chimpanzee genetic map from population sequencing. Science 2012; 336:193-198; PMID:22422862; http://dx.doi.org/10.1126/science.1216872
   PubMedGoogle Scholar
• Quach H, Wilson D, Laval G, Patin E, Manry J, Guibert J, Barreiro LB, Nerrienet E, Verschoor E, Gessain A, et al. Different selective pressures shape the evolution of toll-like receptors in human and african great ape populations. Hum Mol Genet 2013; 22:4829-4840; PMID:23851028; http://dx.doi.org/10.1093/hmg/ddt335
   PubMedGoogle Scholar
• Grossman SR, Andersen KG, Shlyakhter I, Tabrizi S, Winnicki S, Yen A, Park DJ, Griesemer D, Karlsson EK, Wong SH, et al. Identifying recent adaptations in large-scale genomic data. Cell 2013; 152:703-713; PMID:23415221; http://dx.doi.org/10.1016/j.cell.2013.01.035
   PubMed Web of Science ®Google Scholar
• Forni D, Cagliani R, Tresoldi C, Pozzoli U, De Gioia L, Filippi G, Riva S, Menozzi G, Colleoni M, Biasin M, et al. An evolutionary analysis of antigen processing and presentation across different timescales reveals pervasive selection. PLoS Genet 2014; 10:e1004189; PMID:24675550; http://dx.doi.org/10.1371/journal.pgen.1004189
   PubMed Web of Science ®Google Scholar
• Forni D, Cagliani R, Pozzoli U, Colleoni M, Riva S, Biasin M, Filippi G, De Gioia L, Gnudi F, Comi GP, et al. A 175 million year history of T cell regulatory molecules reveals widespread selection, with adaptive evolution of disease alleles. Immunity 2013; 38:1129-1141; PMID:23707475; http://dx.doi.org/10.1016/j.immuni.2013.04.008
   PubMedGoogle Scholar
• Barreiro LB, Ben-Ali M, Quach H, Laval G, Patin E, Pickrell JK, Bouchier C, Tichit M, Neyrolles O, Gicquel B, et al. Evolutionary dynamics of human toll-like receptors and their different contributions to host defense. PLoS Genet 2009; 5:e1000562; PMID:19609346; http://dx.doi.org/10.1371/journal.pgen.1000562
   PubMed Web of Science ®Google Scholar
• Fagny M, Patin E, Enard D, Barreiro LB, Quintana-Murci L, Laval G. Exploring the occurrence of classic selective sweeps in humans using whole-genome sequencing data sets. Mol Biol Evol 2014; 31:1850-68; PMID:24694833; http://dx.doi.org\10.1093/molbev/msu118
   PubMed Web of Science ®Google Scholar
• Zeng K, Fu YX, Shi S, Wu CI. Statistical tests for detecting positive selection by utilizing high-frequency variants. Genetics 2006; 174:1431-1439; PMID:16951063; http://dx.doi.org/10.1534/genetics.106.061432
   PubMedGoogle Scholar
• Fairfax BP, Humburg P, Makino S, Naranbhai V, Wong D, Lau E, Jostins L, Plant K, Andrews R, McGee C, et al. Innate immune activity conditions the effect of regulatory variants upon monocyte gene expression. Science 2014; 343:1246949; PMID:24604202; http://dx.doi.org/10.1126/science.1246949
   PubMed Web of Science ®Google Scholar
• Ramaswami G, Li JB. RADAR: A rigorously annotated database of A-to-I RNA editing. Nucleic Acids Res 2014; 42:D109-13; PMID:24163250; http://dx.doi.org/10.1093/nar/gkt996
   PubMed Web of Science ®Google Scholar
• Wang J, Duncan D, Shi Z, Zhang B. WEB-based GEne SeT AnaLysis toolkit (WebGestalt): Update 2013. Nucleic Acids Res 2013; 41:W77-83; PMID:23703215; http://dx.doi.org/10.1093/nar/gkt439
   PubMed Web of Science ®Google Scholar
• Athanasiadis A, Placido D, Maas S, Brown BA,2nd, Lowenhaupt K, Rich A. The crystal structure of the zbeta domain of the RNA-editing enzyme ADAR1 reveals distinct conserved surfaces among Z-domains. J Mol Biol 2005; 351:496-507; PMID:16023667; http://dx.doi.org/10.1016/j.jmb.2005.06.028
   PubMedGoogle Scholar
• Athanasiadis A. Zalpha-domains: At the intersection between RNA editing and innate immunity. Semin Cell Dev Biol 2012; 23:275-280; PMID:22085847; http://dx.doi.org/10.1016/j.semcdb.2011.11.001
   PubMedGoogle Scholar
• Poulsen H, Nilsson J, Damgaard CK, Egebjerg J, Kjems J. CRM1 mediates the export of ADAR1 through a nuclear export signal within the Z-DNA binding domain. Mol Cell Biol 2001; 21:7862-7871; PMID:11604520; http://dx.doi.org/10.1128/MCB.21.22.7862-7871.2001
   PubMed Web of Science ®Google Scholar
• Strehblow A, Hallegger M, Jantsch MF. Nucleocytoplasmic distribution of human RNA-editing enzyme ADAR1 is modulated by double-stranded RNA-binding domains, a leucine-rich export signal, and a putative dimerization domain. Mol Biol Cell 2002; 13:3822-3835; PMID:12429827; http://dx.doi.org/10.1091/mbc.E02-03-0161
   PubMed Web of Science ®Google Scholar
• Anderson P, Kedersha N. RNA granules: Post-transcriptional and epigenetic modulators of gene expression. Nat Rev Mol Cell Biol 2009; 10:430-436; PMID:19461665; http://dx.doi.org/10.1038/nrm2694
   PubMed Web of Science ®Google Scholar
• Masliah G, Barraud P, Allain FH. RNA recognition by double-stranded RNA binding domains: A matter of shape and sequence. Cell Mol Life Sci 2013; 70:1875-1895; PMID:22918483
   PubMed Web of Science ®Google Scholar
• Barraud P, Banerjee S, Mohamed WI, Jantsch MF, Allain FH. A bimodular nuclear localization signal assembled via an extended double-stranded RNA-binding domain acts as an RNA-sensing signal for transportin 1. Proc Natl Acad Sci U S A 2014; 111:E1852-61; PMID:24753571; http://dx.doi.org/10.1073/pnas.1323698111
   PubMed Web of Science ®Google Scholar
• ENCODE Project Consortium, Bernstein BE, Birney E, Dunham I, Green ED, Gunter C, Snyder M. An integrated encyclopedia of DNA elements in the human genome. Nature 2012; 489:57-74; PMID:22955616; http://dx.doi.org/10.1038/nature11247
   PubMed Web of Science ®Google Scholar
• Enard D, Messer PW, Petrov DA. Genome-wide signals of positive selection in human evolution. Genome Res 2014; 24:885-95; PMID:24619126; http://dx.doi.org\10.1101/gr.164822.113
   PubMed Web of Science ®Google Scholar
• Fraser HB. Gene expression drives local adaptation in humans. Genome Res 2013; 23:1089-1096; PMID:23539138; http://dx.doi.org/10.1101/gr.152710.112
   PubMed Web of Science ®Google Scholar
• Tomaselli S, Locatelli F, Gallo A. The RNA editing enzymes ADARs: Mechanism of action and human disease. Cell Tissue Res 2014; 356:527-532; PMID:24770896; http://dx.doi.org/10.1007/s00441-014-1863-3
   PubMedGoogle Scholar
• Chen JY, Peng Z, Zhang R, Yang XZ, Tan BC, Fang H, Liu CJ, Shi M, Ye ZQ, Zhang YE, et al. RNA editome in rhesus macaque shaped by purifying selection. PLoS Genet 2014; 10:e1004274; PMID:24722121; http://dx.doi.org/10.1371/journal.pgen.1004274
   PubMed Web of Science ®Google Scholar
• Yeo J, Goodman RA, Schirle NT, David SS, Beal PA. RNA editing changes the lesion specificity for the DNA repair enzyme NEIL1. Proc Natl Acad Sci U S A 2010; 107:20715-20719; PMID:21068368; http://dx.doi.org/10.1073/pnas.1009231107
   PubMed Web of Science ®Google Scholar
• Bahn JH, Lee JH, Li G, Greer C, Peng G, Xiao X. Accurate identification of A-to-I RNA editing in human by transcriptome sequencing. Genome Res 2012; 22:142-150; PMID:21960545; http://dx.doi.org/10.1101/gr.124107.111
   PubMed Web of Science ®Google Scholar
• Doria M, Neri F, Gallo A, Farace MG, Michienzi A. Editing of HIV-1 RNA by the double-stranded RNA deaminase ADAR1 stimulates viral infection. Nucleic Acids Res 2009; 37:5848-5858; PMID:19651874; http://dx.doi.org/10.1093/nar/gkp604
   PubMed Web of Science ®Google Scholar
• Doria M, Tomaselli S, Neri F, Ciafre SA, Farace MG, Michienzi A, Gallo A. ADAR2 editing enzyme is a novel human immunodeficiency virus-1 proviral factor. J Gen Virol 2011; 92:1228-1232; PMID:21289159; http://dx.doi.org/10.1099/vir.0.028043-0
   PubMedGoogle Scholar
• Phuphuakrat A, Kraiwong R, Boonarkart C, Lauhakirti D, Lee TH, Auewarakul P. Double-stranded RNA adenosine deaminases enhance expression of human immunodeficiency virus type 1 proteins. J Virol 2008; 82:10864-10872; PMID:18753201; http://dx.doi.org/10.1128/JVI.00238-08
   PubMed Web of Science ®Google Scholar
• Biswas N, Wang T, Ding M, Tumne A, Chen Y, Wang Q, Gupta P. ADAR1 is a novel multi targeted anti-HIV-1 cellular protein. Virology 2012; 422:265-277; PMID:22104209; http://dx.doi.org/10.1016/j.virol.2011.10.024
   PubMedGoogle Scholar
• Sawyer SL, Elde NC. A cross-species view on viruses. Curr Opin Virol 2012; 2:561-568; PMID:22835485; http://dx.doi.org/10.1016/j.coviro.2012.07.003
   PubMed Web of Science ®Google Scholar
• Kantaputra PN, Chinadet W, Ohazama A, Kono M. Dyschromatosis symmetrica hereditaria with long hair on the forearms, hypo/hyperpigmented hair, and dental anomalies: Report of a novel ADAR1 mutation. Am J Med Genet A 2012; 158A:2258-2265; PMID:22821605; http://dx.doi.org/10.1002/ajmg.a.35488
   PubMedGoogle Scholar
• Sharma R, Wang Y, Zhou P, Steinman RA, Wang Q. An essential role of RNA editing enzyme ADAR1 in mouse skin. J Dermatol Sci 2011; 64:70-72; PMID:21788117; http://dx.doi.org/10.1016/j.jdermsci.2011.06.013
   PubMedGoogle Scholar
• Vilella AJ, Severin J, Ureta-Vidal A, Heng L, Durbin R, Birney E. EnsemblCompara GeneTrees: Complete, duplication-aware phylogenetic trees in vertebrates. Genome Res 2009; 19:327-335; PMID:19029536; http://dx.doi.org/10.1101/gr.073585.107
   PubMed Web of Science ®Google Scholar
• Guindon S, Delsuc F, Dufayard JF, Gascuel O. Estimating maximum likelihood phylogenies with PhyML. Methods Mol Biol 2009; 537:113-137; PMID:19378142; http://dx.doi.org/10.1007/978-1-59745-251-9_6
   PubMedGoogle Scholar
• Darriba D, Taboada GL, Doallo R, Posada D. ProtTest 3: Fast selection of best-fit models of protein evolution. Bioinformatics 2011; 27:1164-1165; PMID:21335321; http://dx.doi.org/10.1093/bioinformatics/btr088
   PubMed Web of Science ®Google Scholar
• Delport W, Poon AF, Frost SD, Kosakovsky Pond SL. Datamonkey 2010: A suite of phylogenetic analysis tools for evolutionary biology. Bioinformatics 2010; 26:2455-2457; PMID:20671151; http://dx.doi.org/10.1093/bioinformatics/btq429
   PubMed Web of Science ®Google Scholar
• Wilson DJ, Hernandez RD, Andolfatto P, Przeworski M. A population genetics-phylogenetics approach to inferring natural selection in coding sequences. PLoS Genet 2011; 7:e1002395; PMID:22144911; http://dx.doi.org/10.1371/journal.pgen.1002395
   PubMedGoogle Scholar
• Cereda M, Sironi M, Cavalleri M, Pozzoli U. GeCo++: A C++ library for genomic features computation and annotation in the presence of variants. Bioinformatics 2011; 27:1313-1315; PMID:21398667; http://dx.doi.org/10.1093/bioinformatics/btr123
   PubMedGoogle Scholar
• Thornton K. Libsequence: A C++ class library for evolutionary genetic analysis. Bioinformatics 2003; 19:2325-2327; PMID:14630667; http://dx.doi.org/10.1093/bioinformatics/btg316
   PubMed Web of Science ®Google Scholar
• Wright S. Genetical structure of populations. Nature 1950;166:247-249; PMID:15439261; http://dx.doi.org/10.1038/166247a0
   PubMed Web of Science ®Google Scholar
• Fay JC, Wu CI. Hitchhiking under positive darwinian selection. Genetics 2000; 155:1405-1413; PMID:10880498
   PubMed Web of Science ®Google Scholar
• Johnson AD, Handsaker RE, Pulit SL, Nizzari MM, O'Donnell CJ, de Bakker PI. SNAP: A web-based tool for identification and annotation of proxy SNPs using HapMap. Bioinformatics 2008; 24:2938-2939; PMID:18974171; http://dx.doi.org/10.1093/bioinformatics/btn564
   PubMed Web of Science ®Google Scholar
• Cooper GM, Stone EA, Asimenos G, NISC Comparative Sequencing Program, Green ED, Batzoglou S, Sidow A. Distribution and intensity of constraint in mammalian genomic sequence. Genome Res 2005; 15:901-913; PMID:15965027; http://dx.doi.org/10.1101/gr.3577405
   PubMed Web of Science ®Google Scholar