Early origin and adaptive evolution of the GW182 protein family, the key component of RNA silencing in animals

References

• Eystathioy T, Chan EKL, Tenenbaum SA, Keene JD, Griffith K, Fritzler MJ. A phosphorylated cytoplasmic autoantigen, GW182, associates with a unique population of human mRNAs within novel cytoplasmic speckles. Mol Biol Cell 2002; 13:1338-51; PMID:11950943; http://dx.doi.org/10.1091/mbc.01-11-0544
   PubMed Web of Science ®Google Scholar
• Braun JE, Huntzinger E, Izaurralde E. The role of GW182 proteins in miRNA-mediated gene silencing. Adv Exp Med Biol 2013; 768:147-63; PMID:23224969
   PubMed Web of Science ®Google Scholar
• Fabian MR, Mathonnet G, Sundermeier T, Mathys H, Zipprich JT, Svitkin YV, Rivas F, Jinek M, Wohlschlegel J, Doudna JA, et al. Mammalian miRNA RISC recruits CAF1 and PABP to affect PABP-dependent deadenylation. Mol Cell 2009; 35:868-80; PMID:19716330; http://dx.doi.org/10.1016/j.molcel.2009.08.004
   PubMed Web of Science ®Google Scholar
• Zekri L, Huntzinger E, Heimstädt S, Izaurralde E. The silencing domain of GW182 interacts with PABPC1 to promote translational repression and degradation of microRNA targets and is required for target release. Mol Cell Biol 2009; 29:6220-31; PMID:19797087; http://dx.doi.org/10.1128/MCB.01081-09
   PubMed Web of Science ®Google Scholar
• Huntzinger E, Braun JE, Heimstädt S, Zekri L, Izaurralde E. Two PABPC1-binding sites in GW182 proteins promote miRNA-mediated gene silencing. EMBO J 2010; 29:4146-60; PMID:21063388; http://dx.doi.org/10.1038/emboj.2010.274
   PubMed Web of Science ®Google Scholar
• Jinek M, Fabian MR, Coyle SM, Sonenberg N, Doudna JA. Structural insights into the human GW182-PABC interaction in microRNA-mediated deadenylation. Nat Struct Mol Biol 2010; 17:238-40; PMID:20098421; http://dx.doi.org/10.1038/nsmb.1768
   PubMed Web of Science ®Google Scholar
• Braun JE, Huntzinger E, Fauser M, Izaurralde E. GW182 proteins directly recruit cytoplasmic deadenylase complexes to miRNA targets. Mol Cell 2011; 44:120-33; PMID:21981923; http://dx.doi.org/10.1016/j.molcel.2011.09.007
   PubMed Web of Science ®Google Scholar
• Chekulaeva M, Mathys H, Zipprich JT, Attig J, Colic M, Parker R, Filipowicz W. miRNA repression involves GW182-mediated recruitment of CCR4-NOT through conserved W-containing motifs. Nat Struct Mol Biol 2011; 18:1218-26; PMID:21984184; http://dx.doi.org/10.1038/nsmb.2166
   PubMed Web of Science ®Google Scholar
• Fabian MR, Cieplak MK, Frank F, Morita M, Green J, Srikumar T, Nagar B, Yamamoto T, Raught B, Duchaine TF, et al. miRNA-mediated deadenylation is orchestrated by GW182 through two conserved motifs that interact with CCR4-NOT. Nat Struct Mol Biol 2011; 18:1211-7; PMID:21984185; http://dx.doi.org/10.1038/nsmb.2149
   PubMed Web of Science ®Google Scholar
• Christie M, Boland A, Huntzinger E, Weichenrieder O, Izaurralde E. Structure of the PAN3 pseudokinase reveals the basis for interactions with the PAN2 deadenylase and the GW182 proteins. Mol Cell 2013; 51:360-73; PMID:23932717; http://dx.doi.org/10.1016/j.molcel.2013.07.011
   PubMed Web of Science ®Google Scholar
• Chen Y, Boland A, Kuzuoğlu-Öztürk D, Bawankar P, Loh B, Chang C-T, Weichenrieder O, Izaurralde E. A DDX6-CNOT1 complex and W-binding pockets in CNOT9 reveal direct links between miRNA target recognition and silencing. Mol Cell 2014; 54:737-50; PMID:24768540; http://dx.doi.org/10.1016/j.molcel.2014.03.034
   PubMed Web of Science ®Google Scholar
• Mathys H, Basquin J, Ozgur S, Czarnocki-Cieciura M, Bonneau F, Aartse A, Dziembowski A, Nowotny M, Conti E, Filipowicz W. Structural and biochemical insights to the role of the CCR4-NOT complex and DDX6 ATPase in microRNA repression. Mol Cell 2014; 54:751-65; PMID:24768538; http://dx.doi.org/10.1016/j.molcel.2014.03.036
   PubMed Web of Science ®Google Scholar
• Huntzinger E, Izaurralde E. Gene silencing by microRNAs: contributions of translational repression and mRNA decay. Nat Rev Genet 2011; 12:99-110; PMID:21245828; http://dx.doi.org/10.1038/nrg2936
   PubMed Web of Science ®Google Scholar
• Fabian MR, Sonenberg N, Filipowicz W. Regulation of mRNA translation and stability by microRNAs. Annu Rev Biochem 2010; 79:351-79; PMID:20533884; http://dx.doi.org/10.1146/annurev-biochem-060308-103103
   PubMed Web of Science ®Google Scholar
• Behm-Ansmant I, Rehwinkel J, Doerks T, Stark A, Bork P, Izaurralde E. mRNA degradation by miRNAs and GW182 requires both CCR4:NOT deadenylase and DCP1:DCP2 decapping complexes. Genes Dev 2006; 20:1885-98; PMID:16815998; http://dx.doi.org/10.1101/gad.1424106
   PubMed Web of Science ®Google Scholar
• Eulalio A, Tritschler F, Izaurralde E. The GW182 protein family in animal cells: new insights into domains required for miRNA-mediated gene silencing. RNA 2009; 15:1433-42; PMID:19535464; http://dx.doi.org/10.1261/rna.1703809
   PubMed Web of Science ®Google Scholar
• Eulalio A, Tritschler F, Büttner R, Weichenrieder O, Izaurralde E, Truffault V. The RRM domain in GW182 proteins contributes to miRNA-mediated gene silencing. Nucleic Acids Res 2009; 37:2974-83; PMID:19295135; http://dx.doi.org/10.1093/nar/gkp173
   PubMedGoogle Scholar
• Zielezinski A, Karlowski WM. Integrative data analysis indicates an intrinsic disordered domain character of Argonaute-binding motifs. Bioinformatics 2015; 31:332-9; PMID:25304778; http://dx.doi.org/10.1093/bioinformatics/btu666
   PubMedGoogle Scholar
• Till S, Lejeune E, Thermann R, Bortfeld M, Hothorn M, Enderle D, Heinrich C, Hentze MW, Ladurner AG. A conserved motif in Argonaute-interacting proteins mediates functional interactions through the Argonaute PIWI domain. Nat Struct Mol Biol 2007; 14:897-903; PMID:17891150; http://dx.doi.org/10.1038/nsmb1302
   PubMed Web of Science ®Google Scholar
• Moran Y, Praher D, Fredman D, Technau U. The evolution of microRNA pathway protein components in Cnidaria. Mol Biol Evol 2013; 30:2541-52; PMID:24030553; http://dx.doi.org/10.1093/molbev/mst159
   PubMedGoogle Scholar
• Ding L, Spencer A, Morita K, Han M. The developmental timing regulator AIN-1 interacts with miRISCs and may target the argonaute protein ALG-1 to cytoplasmic P bodies in C. elegans. Mol Cell 2005; 19:437-47; PMID:16109369; http://dx.doi.org/10.1016/j.molcel.2005.07.013
   PubMed Web of Science ®Google Scholar
• Zhang L, Ding L, Cheung TH, Dong M-Q, Chen J, Sewell AK, Liu X, Yates JR, Han M. Systematic identification of C. elegans miRISC proteins, miRNAs, and mRNA targets by their interactions with GW182 proteins AIN-1 and AIN-2. Mol Cell 2007; 28:598-613; PMID:18042455; http://dx.doi.org/10.1016/j.molcel.2007.09.014
   PubMed Web of Science ®Google Scholar
• Ding XC, Grosshans H. Repression of C. elegans microRNA targets at the initiation level of translation requires GW182 proteins. EMBO J 2009; 28:213-22; PMID:19131968; http://dx.doi.org/10.1038/emboj.2008.275
   PubMed Web of Science ®Google Scholar
• Kuzuoglu-Öztürk D, Huntzinger E, Schmidt S, Izaurralde E. The Caenorhabditis elegans GW182 protein AIN-1 interacts with PAB-1 and subunits of the PAN2-PAN3 and CCR4-NOT deadenylase complexes. Nucleic Acids Res 2012; 40:5651-65; http://dx.doi.org/10.1093/nar/gks218
   PubMed Web of Science ®Google Scholar
• Qiu X-B, Shao Y-M, Miao S, Wang L. The diversity of the DnaJ/Hsp40 family, the crucial partners for Hsp70 chaperones. Cell Mol Life Sci 2006; 63:2560-70; PMID:16952052; http://dx.doi.org/10.1007/s00018-006-6192-6
   PubMed Web of Science ®Google Scholar
• Iwasaki S, Kobayashi M, Yoda M, Sakaguchi Y, Katsuma S, Suzuki T, Tomari Y. Hsc70/Hsp90 chaperone machinery mediates ATP-dependent RISC loading of small RNA duplexes. Mol Cell 2010; 39:292-9; PMID:20605501; http://dx.doi.org/10.1016/j.molcel.2010.05.015
   PubMed Web of Science ®Google Scholar
• Li S, Lian SL, Moser JJ, Fritzler ML, Fritzler MJ, Satoh M, Chan EKL. Identification of GW182 and its novel isoform TNGW1 as translational repressors in Ago2-mediated silencing. J Cell Sci 2008; 121:4134-44; PMID:19056672; http://dx.doi.org/10.1242/jcs.036905
   PubMedGoogle Scholar
• Huminiecki L, Heldin CH. 2R and remodeling of vertebrate signal transduction engine. BMC Biol 2010; 8:146; PMID:21144020; http://dx.doi.org/10.1186/1741-7007-8-146
   PubMedGoogle Scholar
• Makino T, McLysaght A. Ohnologs in the human genome are dosage balanced and frequently associated with disease. Proc Natl Acad Sci U S A 2010; 107:9270-4; PMID:20439718; http://dx.doi.org/10.1073/pnas.0914697107
   PubMed Web of Science ®Google Scholar
• Makino T, McLysaght A, Kawata M. Genome-wide deserts for copy number variation in vertebrates. Nat Commun 2013; 4:2283; PMID:23917329; http://dx.doi.org/10.1038/ncomms3283
   PubMedGoogle Scholar
• Meyer A, Van de Peer Y. From 2R to 3R: evidence for a fish-specific genome duplication (FSGD). BioEssays 2005; 27:937-45; PMID:16108068; http://dx.doi.org/10.1002/bies.20293
   PubMed Web of Science ®Google Scholar
• Hurst LD. The Ka/Ks ratio: diagnosing the form of sequence evolution. Trends Genet 2002; 18:486-7; PMID:12175810; http://dx.doi.org/10.1016/S0168-9525(02)02722-1
   PubMed Web of Science ®Google Scholar
• Karlowski WM, Zielezinski A, Carrère J, Pontier D, Lagrange T, Cooke R. Genome-wide computational identification of WG/GW Argonaute-binding proteins in Arabidopsis. Nucleic Acids Res 2010; 38:4231-45; PMID:20338883; http://dx.doi.org/10.1093/nar/gkq162
   PubMedGoogle Scholar
• Fabian MR, Sonenberg N. The mechanics of miRNA-mediated gene silencing: a look under the hood of miRISC. Nat Struct Mol Biol 2012; 19:586-93; PMID:22664986; http://dx.doi.org/10.1038/nsmb.2296
   PubMed Web of Science ®Google Scholar
• Makino T, Hokamp K, McLysaght A. The complex relationship of gene duplication and essentiality. Trends Genet 2009; 25:152-5; PMID:19285746; http://dx.doi.org/10.1016/j.tig.2009.03.001
   PubMed Web of Science ®Google Scholar
• Wang Y. Locally duplicated ohnologs evolve faster than nonlocally duplicated ohnologs in Arabidopsis and rice. Genome Biol Evol 2013; 5:362-9; PMID:23362157; http://dx.doi.org/10.1093/gbe/evt016
   PubMedGoogle Scholar
• Parkinson J, Mitreva M, Whitton C, Thomson M, Daub J, Martin J, Schmid R, Hall N, Barrell B, Waterston RH, et al. A transcriptomic analysis of the phylum Nematoda. Nat Genet 2004; 36:1259-67; PMID:15543149; http://dx.doi.org/10.1038/ng1472
   PubMed Web of Science ®Google Scholar
• Maris C, Dominguez C, Allain FH-T. The RNA recognition motif, a plastic RNA-binding platform to regulate post-transcriptional gene expression. FEBS J 2005; 272:2118-31; PMID:15853797; http://dx.doi.org/10.1111/j.1742-4658.2005.04653.x
   PubMed Web of Science ®Google Scholar
• Dinkel H, Van Roey K, Michael S, Davey NE, Weatheritt RJ, Born D, Speck T, Krüger D, Grebnev G, Kuban M, et al. The eukaryotic linear motif resource ELM: 10 years and counting. Nucleic Acids Res 2014; 42:D259-66; PMID:24214962; http://dx.doi.org/10.1093/nar/gkt1047
   PubMed Web of Science ®Google Scholar
• Obbard DJ, Gordon KHJ, Buck AH, Jiggins FM. The evolution of RNAi as a defence against viruses and transposable elements. Philos Trans R Soc Lond B Biol Sci 2009; 364:99-115; PMID:18926973; http://dx.doi.org/10.1098/rstb.2008.0168
   PubMed Web of Science ®Google Scholar
• Ding S-W. RNA-based antiviral immunity. Nat Rev Immunol 2010; 10:632-44; PMID:20706278; http://dx.doi.org/10.1038/nri2824
   PubMed Web of Science ®Google Scholar
• Azevedo J, Garcia D, Pontier D, Ohnesorge S, Yu A, Garcia S, Braun L, Bergdoll M, Hakimi MA, Lagrange T, et al. Argonaute quenching and global changes in Dicer homeostasis caused by a pathogen-encoded GW repeat protein. Genes Dev 2010; 24:904-15; PMID:20439431; http://dx.doi.org/10.1101/gad.1908710
   PubMedGoogle Scholar
• Giner A, Lakatos L, García-Chapa M, López-Moya JJ, Burgyán J. Viral protein inhibits RISC activity by argonaute binding through conserved WG/GW motifs. PLoS Pathog 2010; 6:e1000996; PMID:20657820; http://dx.doi.org/10.1371/journal.ppat.1000996
   PubMed Web of Science ®Google Scholar
• De Ronde D, Pasquier A, Ying S, Butterbach P, Lohuis D, Kormelink R. Analysis of Tomato spotted wilt virus NSs protein indicates the importance of the N-terminal domain for avirulence and RNA silencing suppression. Mol Plant Pathol 2014; 15:185-95; PMID:24103150; http://dx.doi.org/10.1111/mpp.12082
   PubMedGoogle Scholar
• Van Rij RP, Saleh M-C, Berry B, Foo C, Houk A, Antoniewski C, Andino R. The RNA silencing endonuclease Argonaute 2 mediates specific antiviral immunity in Drosophila melanogaster. Genes Dev 2006; 20:2985-95; PMID:17079687; http://dx.doi.org/10.1101/gad.1482006
   PubMed Web of Science ®Google Scholar
• Nayak A, Tassetto M, Kunitomi M, Andino R. Intrinsic Immunity. Berlin, Heidelberg: Springer Berlin Heidelberg; 2013.
   Google Scholar
• Van Mierlo JT, Overheul GJ, Obadia B, van Cleef KWR, Webster CL, Saleh M-C, Obbard DJ, van Rij RP. Novel Drosophila viruses encode host-specific suppressors of RNAi. PLoS Pathog 2014; 10:e1004256; PMID:25032815; http://dx.doi.org/10.1371/journal.ppat.1004256
   PubMedGoogle Scholar
• Obbard DJ, Jiggins FM, Halligan DL, Little TJ. Natural selection drives extremely rapid evolution in antiviral RNAi genes. Curr Biol 2006; 16:580-5; PMID:16546082; http://dx.doi.org/10.1016/j.cub.2006.01.065
   PubMed Web of Science ®Google Scholar
• Kolaczkowski B, Hupalo DN, Kern AD. Recurrent adaptation in RNA interference genes across the Drosophila phylogeny. Mol Biol Evol 2011; 28:1033-42; PMID:20971974; http://dx.doi.org/10.1093/molbev/msq284
   PubMedGoogle Scholar
• Obbard DJ, Jiggins FM, Bradshaw NJ, Little TJ. Recent and recurrent selective sweeps of the antiviral RNAi gene Argonaute-2 in three species of Drosophila. Mol Biol Evol 2011; 28:1043-56; PMID:20978039; http://dx.doi.org/10.1093/molbev/msq280
   PubMedGoogle Scholar
• Aqil M, Naqvi AR, Bano AS, Jameel S. The HIV-1 Nef Protein Binds Argonaute-2 and Functions as a Viral Suppressor of RNA Interference. PLoS One 2013; 8:e74472; PMID:24023945; http://dx.doi.org/10.1371/journal.pone.0074472
   PubMed Web of Science ®Google Scholar
• Altschul SF, Madden TL, Schäffer AA, Zhang J, Zhang Z, Miller W, Lipman DJ. Gapped BLAST and PSI-BLAST: a new generation of protein database search programs. Nucleic Acids Res 1997; 25:3389-402; PMID:9254694; http://dx.doi.org/10.1093/nar/25.17.3389
   PubMed Web of Science ®Google Scholar
• Consortium U. Activities at the Universal Protein Resource (UniProt). Nucleic Acids Res 2014; 42:D191-8; PMID:24253303; http://dx.doi.org/10.1093/nar/gkt1140
   PubMed Web of Science ®Google Scholar
• Finn RD, Bateman A, Clements J, Coggill P, Eberhardt RY, Eddy SR, Heger A, Hetherington K, Holm L, Mistry J, et al. Pfam: the protein families database. Nucleic Acids Res 2014; 42:D222-30; PMID:24288371; http://dx.doi.org/10.1093/nar/gkt1223
   PubMed Web of Science ®Google Scholar
• Eddy SR. Accelerated Profile HMM Searches. PLoS Comput Biol 2011; 7:e1002195; PMID:22039361; http://dx.doi.org/10.1371/journal.pcbi.1002195
   PubMed Web of Science ®Google Scholar
• Hunter S, Jones P, Mitchell A, Apweiler R, Attwood TK, Bateman A, Bernard T, Binns D, Bork P, Burge S, et al. InterPro in 2011: new developments in the family and domain prediction database. Nucleic Acids Res 2012; 40:D306-12; PMID:22096229; http://dx.doi.org/10.1093/nar/gkr948
   PubMed Web of Science ®Google Scholar
• Letunic I, Doerks T, Bork P. SMART 7: recent updates to the protein domain annotation resource. Nucleic Acids Res 2012; 40:D302-5; PMID:22053084; http://dx.doi.org/10.1093/nar/gkr931
   PubMed Web of Science ®Google Scholar
• Sigrist CJA, de Castro E, Cerutti L, Cuche BA, Hulo N, Bridge A, Bougueleret L, Xenarios I. New and continuing developments at PROSITE. Nucleic Acids Res 2013; 41:D344-7; PMID:23161676; http://dx.doi.org/10.1093/nar/gks1067
   PubMed Web of Science ®Google Scholar
• Wallace IM, O'Sullivan O, Higgins DG, Notredame C. M-Coffee: combining multiple sequence alignment methods with T-Coffee. Nucleic Acids Res 2006; 34:1692-9; PMID:16556910; http://dx.doi.org/10.1093/nar/gkl091
   PubMed Web of Science ®Google Scholar
• Felsenstein J. PHYLIP -Phylogeny inference package (Version 3.2). Cladistics 1989; 5:164-66.
   Google Scholar
• Guindon S, Dufayard J-F, Lefort V, Anisimova M, Hordijk W, Gascuel O. New algorithms and methods to estimate maximum-likelihood phylogenies: assessing the performance of PhyML 3.0. Syst Biol 2010; 59:307-21; PMID:20525638; http://dx.doi.org/10.1093/sysbio/syq010
   PubMed Web of Science ®Google Scholar
• Abascal F, Zardoya R, Posada D. ProtTest: selection of best-fit models of protein evolution. Bioinformatics 2005; 21:2104-5; PMID:15647292; http://dx.doi.org/10.1093/bioinformatics/bti263
   PubMed Web of Science ®Google Scholar
• Anisimova M, Gascuel O. Approximate likelihood-ratio test for branches: A fast, accurate, and powerful alternative. Syst Biol 2006; 55:539-52; PMID:16785212; http://dx.doi.org/10.1080/10635150600755453
   PubMed Web of Science ®Google Scholar
• Huelsenbeck JP, Ronquist F, Nielsen R, Bollback JP. Bayesian inference of phylogeny and its impact on evolutionary biology. Science (80- ) 2001; 294:2310-4; http://dx.doi.org/10.1126/science.1065889
   PubMed Web of Science ®Google Scholar
• Ronquist F, Huelsenbeck JP. MrBayes 3: Bayesian phylogenetic inference under mixed models. Bioinformatics 2003; 19:1572-4; PMID:12912839; http://dx.doi.org/10.1093/bioinformatics/btg180
   PubMed Web of Science ®Google Scholar
• Suyama M, Torrents D, Bork P. PAL2NAL: robust conversion of protein sequence alignments into the corresponding codon alignments. Nucleic Acids Res 2006; 34:W609-12; PMID:16845082; http://dx.doi.org/10.1093/nar/gkl315
   PubMed Web of Science ®Google Scholar
• Zhang Z, Li J, Zhao X-Q, Wang J, Wong GK-S, Yu J. KaKs_Calculator: calculating Ka and Ks through model selection and model averaging. Genomics Proteomics Bioinformatics 2006; 4:259-63; PMID:17531802; http://dx.doi.org/10.1016/S1672-0229(07)60007-2
   PubMedGoogle Scholar
• Yang Z. PAML: a program package for phylogenetic analysis by maximum likelihood. Comput Appl Biosci CABIOS 1997; 13:555-6.
   PubMedGoogle Scholar
• Sidow A. Sequence first. Ask questions later. Cell 2002; 111:13-6; PMID:12372296; http://dx.doi.org/10.1016/S0092-8674(02)01003-6
   PubMedGoogle Scholar