Naturally occurring endo-siRNA silences LINE-1 retrotransposons in human cells through DNA methylation

References

• Brouha B, Schustak J, Badge RM, Lutz-Prigge S, Farley AH, Moran JV, et al. Hot L1s account for the bulk of retrotransposition in the human population. Proc Natl Acad Sci U S A 2003; 100:5280 - 5; http://dx.doi.org/10.1073/pnas.0831042100; PMID: 12682288
   PubMed Web of Science ®Google Scholar
• Beck CR, Collier P, Macfarlane C, Malig M, Kidd JM, Eichler EE, et al. LINE-1 retrotransposition activity in human genomes. Cell 2010; 141:1159 - 70; http://dx.doi.org/10.1016/j.cell.2010.05.021; PMID: 20602998
   PubMed Web of Science ®Google Scholar
• Scott AF, Schmeckpeper BJ, Abdelrazik M, Comey CT, O’Hara B, Rossiter JP, et al. Origin of the human L1 elements: proposed progenitor genes deduced from a consensus DNA sequence. Genomics 1987; 1:113 - 25; http://dx.doi.org/10.1016/0888-7543(87)90003-6; PMID: 3692483
   PubMedGoogle Scholar
• Martin SL, Bushman FD. Nucleic acid chaperone activity of the ORF1 protein from the mouse LINE-1 retrotransposon. Mol Cell Biol 2001; 21:467 - 75; http://dx.doi.org/10.1128/MCB.21.2.467-475.2001; PMID: 11134335
   PubMed Web of Science ®Google Scholar
• Feng Q, Moran JV, Kazazian HH Jr., Boeke JD. Human L1 retrotransposon encodes a conserved endonuclease required for retrotransposition. Cell 1996; 87:905 - 16; http://dx.doi.org/10.1016/S0092-8674(00)81997-2; PMID: 8945517
   PubMed Web of Science ®Google Scholar
• Mathias SL, Scott AF, Kazazian HH Jr., Boeke JD, Gabriel A. Reverse transcriptase encoded by a human transposable element. Science 1991; 254:1808 - 10; http://dx.doi.org/10.1126/science.1722352; PMID: 1722352
   PubMed Web of Science ®Google Scholar
• Moran JV, Holmes SE, Naas TP, DeBerardinis RJ, Boeke JD, Kazazian HH Jr.. High frequency retrotransposition in cultured mammalian cells. Cell 1996; 87:917 - 27; http://dx.doi.org/10.1016/S0092-8674(00)81998-4; PMID: 8945518
   PubMed Web of Science ®Google Scholar
• Goodier JL, Kazazian HH Jr.. Retrotransposons revisited: the restraint and rehabilitation of parasites. Cell 2008; 135:23 - 35; http://dx.doi.org/10.1016/j.cell.2008.09.022; PMID: 18854152
   PubMed Web of Science ®Google Scholar
• Cordaux R, Batzer MA. The impact of retrotransposons on human genome evolution. Nat Rev Genet 2009; 10:691 - 703; http://dx.doi.org/10.1038/nrg2640; PMID: 19763152
   PubMed Web of Science ®Google Scholar
• Esnault C, Maestre J, Heidmann T. Human LINE retrotransposons generate processed pseudogenes. Nat Genet 2000; 24:363 - 7; http://dx.doi.org/10.1038/74184; PMID: 10742098
   PubMed Web of Science ®Google Scholar
• Terai G, Yoshizawa A, Okida H, Asai K, Mituyama T. Discovery of short pseudogenes derived from messenger RNAs. Nucleic Acids Res 2010; 38:1163 - 71; http://dx.doi.org/10.1093/nar/gkp1098; PMID: 19965772
   PubMed Web of Science ®Google Scholar
• Ostertag EM, Kazazian HH Jr.. Biology of mammalian L1 retrotransposons. Annu Rev Genet 2001; 35:501 - 38; http://dx.doi.org/10.1146/annurev.genet.35.102401.091032; PMID: 11700292
   PubMed Web of Science ®Google Scholar
• Belancio VP, Roy-Engel AM, Pochampally RR, Deininger P. Somatic expression of LINE-1 elements in human tissues. Nucleic Acids Res 2010; 38:3909 - 22; http://dx.doi.org/10.1093/nar/gkq132; PMID: 20215437
   PubMed Web of Science ®Google Scholar
• Kano H, Godoy I, Courtney C, Vetter MR, Gerton GL, Ostertag EM, et al. L1 retrotransposition occurs mainly in embryogenesis and creates somatic mosaicism. Genes Dev 2009; 23:1303 - 12; http://dx.doi.org/10.1101/gad.1803909; PMID: 19487571
   PubMed Web of Science ®Google Scholar
• Iskow RC, McCabe MT, Mills RE, Torene S, Pittard WS, Neuwald AF, et al. Natural mutagenesis of human genomes by endogenous retrotransposons. Cell 2010; 141:1253 - 61; http://dx.doi.org/10.1016/j.cell.2010.05.020; PMID: 20603005
   PubMed Web of Science ®Google Scholar
• Yang N, Kazazian HH Jr.. L1 retrotransposition is suppressed by endogenously encoded small interfering RNAs in human cultured cells. Nat Struct Mol Biol 2006; 13:763 - 71; http://dx.doi.org/10.1038/nsmb1141; PMID: 16936727
   PubMed Web of Science ®Google Scholar
• Garcia-Perez JL, Morell M, Scheys JO, Kulpa DA, Morell S, Carter CC, et al. Epigenetic silencing of engineered L1 retrotransposition events in human embryonic carcinoma cells. Nature 2010; 466:769 - 73; http://dx.doi.org/10.1038/nature09209; PMID: 20686575
   PubMed Web of Science ®Google Scholar
• Harris CR, Normart R, Yang Q, Stevenson E, Haffty BG, Ganesan S, et al. Association of nuclear localization of a long interspersed nuclear element-1 protein in breast tumors with poor prognostic outcomes. Genes Cancer 2010; 1:115 - 24; http://dx.doi.org/10.1177/1947601909360812; PMID: 20948976
   PubMedGoogle Scholar
• Roman-Gomez J, Jimenez-Velasco A, Agirre X, Cervantes F, Sanchez J, Garate L, et al. Promoter hypomethylation of the LINE-1 retrotransposable elements activates sense/antisense transcription and marks the progression of chronic myeloid leukemia. Oncogene 2005; 24:7213 - 23; http://dx.doi.org/10.1038/sj.onc.1208866; PMID: 16170379
   PubMed Web of Science ®Google Scholar
• Aporntewan C, Phokaew C, Piriyapongsa J, Ngamphiw C, Ittiwut C, Tongsima S, et al. Hypomethylation of intragenic LINE-1 represses transcription in cancer cells through AGO2. PLoS One 2011; 6:e17934; http://dx.doi.org/10.1371/journal.pone.0017934; PMID: 21423624
   PubMed Web of Science ®Google Scholar
• Wolff EM, Byun HM, Han HF, Sharma S, Nichols PW, Siegmund KD, et al. Hypomethylation of a LINE-1 promoter activates an alternate transcript of the MET oncogene in bladders with cancer. PLoS Genet 2010; 6:e1000917; http://dx.doi.org/10.1371/journal.pgen.1000917; PMID: 20421991
   PubMed Web of Science ®Google Scholar
• Okamura K, Lai EC. Endogenous small interfering RNAs in animals. Nat Rev Mol Cell Biol 2008; 9:673 - 8; http://dx.doi.org/10.1038/nrm2479; PMID: 18719707
   PubMed Web of Science ®Google Scholar
• Kawamura Y, Saito K, Kin T, Ono Y, Asai K, Sunohara T, et al. Drosophila endogenous small RNAs bind to Argonaute 2 in somatic cells. Nature 2008; 453:793 - 7; http://dx.doi.org/10.1038/nature06938; PMID: 18463636
   PubMed Web of Science ®Google Scholar
• Watanabe T, Totoki Y, Toyoda A, Kaneda M, Kuramochi-Miyagawa S, Obata Y, et al. Endogenous siRNAs from naturally formed dsRNAs regulate transcripts in mouse oocytes. Nature 2008; 453:539 - 43; http://dx.doi.org/10.1038/nature06908; PMID: 18404146
   PubMed Web of Science ®Google Scholar
• Lee SH, Eldi P, Cho SY, Rangasamy D. Control of chicken CR1 retrotransposons is independent of Dicer-mediated RNA interference pathway. BMC Biol 2009; 7:53; http://dx.doi.org/10.1186/1741-7007-7-53; PMID: 19691826
   PubMed Web of Science ®Google Scholar
• Nilsen TW. Endo-siRNAs: yet another layer of complexity in RNA silencing. Nat Struct Mol Biol 2008; 15:546 - 8; http://dx.doi.org/10.1038/nsmb0608-546; PMID: 18523465
   PubMed Web of Science ®Google Scholar
• Moazed D. Small RNAs in transcriptional gene silencing and genome defence. Nature 2009; 457:413 - 20; http://dx.doi.org/10.1038/nature07756; PMID: 19158787
   PubMed Web of Science ®Google Scholar
• Bratthauer GL, Cardiff RD, Fanning TG. Expression of LINE-1 retrotransposons in human breast cancer. Cancer 1994; 73:2333 - 6; http://dx.doi.org/10.1002/1097-0142(19940501)73:9<2333::AID-CNCR2820730915>3.0.CO;2-4; PMID: 8168038
   PubMed Web of Science ®Google Scholar
• Asch HL, Eliacin E, Fanning TG, Connolly JL, Bratthauer G, Asch BB. Comparative expression of the LINE-1 p40 protein in human breast carcinomas and normal breast tissues. Oncol Res 1996; 8:239 - 47; PMID: 8895199
   PubMed Web of Science ®Google Scholar
• Dmitriev SE, Andreev DE, Terenin IM, Olovnikov IA, Prassolov VS, Merrick WC, et al. Efficient translation initiation directed by the 900-nucleotide-long and GC-rich 5′ untranslated region of the human retrotransposon LINE-1 mRNA is strictly cap dependent rather than internal ribosome entry site mediated. Mol Cell Biol 2007; 27:4685 - 97; http://dx.doi.org/10.1128/MCB.02138-06; PMID: 17470553
   PubMed Web of Science ®Google Scholar
• Leibold DM, Swergold GD, Singer MF, Thayer RE, Dombroski BA, Fanning TG. Translation of LINE-1 DNA elements in vitro and in human cells. Proc Natl Acad Sci U S A 1990; 87:6990 - 4; http://dx.doi.org/10.1073/pnas.87.18.6990; PMID: 1698287
   PubMed Web of Science ®Google Scholar
• Hoffmann MJ, Schulz WA. Causes and consequences of DNA hypomethylation in human cancer. Biochemistry and cell biology 2005; 83:296 - 321
   PubMed Web of Science ®Google Scholar
• Perrin D, Ballestar E, Fraga MF, Frappart L, Esteller M, Guerin JF, et al. Specific hypermethylation of LINE-1 elements during abnormal overgrowth and differentiation of human placenta. Oncogene 2007; 26:2518 - 24; http://dx.doi.org/10.1038/sj.onc.1210039; PMID: 17043645
   PubMed Web of Science ®Google Scholar
• Aravin AA, Sachidanandam R, Bourc’his D, Schaefer C, Pezic D, Toth KF, et al. A piRNA pathway primed by individual transposons is linked to de novo DNA methylation in mice. Mol Cell 2008; 31:785 - 99; http://dx.doi.org/10.1016/j.molcel.2008.09.003; PMID: 18922463
   PubMed Web of Science ®Google Scholar
• Watanabe T, Takeda A, Tsukiyama T, Mise K, Okuno T, Sasaki H, et al. Identification and characterization of two novel classes of small RNAs in the mouse germline: retrotransposon-derived siRNAs in oocytes and germline small RNAs in testes. Genes Dev 2006; 20:1732 - 43; http://dx.doi.org/10.1101/gad.1425706; PMID: 16766679
   PubMed Web of Science ®Google Scholar
• Ghildiyal M, Seitz H, Horwich MD, Li C, Du T, Lee S, et al. Endogenous siRNAs derived from transposons and mRNAs in Drosophila somatic cells. Science 2008; 320:1077 - 81; http://dx.doi.org/10.1126/science.1157396; PMID: 18403677
   PubMed Web of Science ®Google Scholar
• Malone CD, Hannon GJ. Small RNAs as guardians of the genome. Cell 2009; 136:656 - 68; http://dx.doi.org/10.1016/j.cell.2009.01.045; PMID: 19239887
   PubMed Web of Science ®Google Scholar
• Girard A, Hannon GJ. Conserved themes in small-RNA-mediated transposon control. Trends Cell Biol 2008; 18:136 - 48; http://dx.doi.org/10.1016/j.tcb.2008.01.004; PMID: 18282709
   PubMed Web of Science ®Google Scholar
• Speek M. Antisense promoter of human L1 retrotransposon drives transcription of adjacent cellular genes. Mol Cell Biol 2001; 21:1973 - 85; http://dx.doi.org/10.1128/MCB.21.6.1973-1985.2001; PMID: 11238933
   PubMed Web of Science ®Google Scholar
• Czech B, Malone CD, Zhou R, Stark A, Schlingeheyde C, Dus M, et al. An endogenous small interfering RNA pathway in Drosophila. Nature 2008; 453:798 - 802; http://dx.doi.org/10.1038/nature07007; PMID: 18463631
   PubMed Web of Science ®Google Scholar
• Zhou Y, Chen L, Barlogie B, Stephens O, Wu X, Williams DR, et al. High-risk myeloma is associated with global elevation of miRNAs and overexpression of EIF2C2/AGO2. Proc Natl Acad Sci U S A 2010; 107:7904 - 9; http://dx.doi.org/10.1073/pnas.0908441107; PMID: 20385818
   PubMed Web of Science ®Google Scholar
• Yang JH, Shao P, Zhou H, Chen YQ, Qu LH. deepBase: a database for deeply annotating and mining deep sequencing data. Nucleic Acids Res 2010; 38:Database issue D123 - 30; http://dx.doi.org/10.1093/nar/gkp943; PMID: 19966272
   PubMedGoogle Scholar
• Kim DH, Villeneuve LM, Morris KV, Rossi JJ. Argonaute-1 directs siRNA-mediated transcriptional gene silencing in human cells. Nat Struct Mol Biol 2006; 13:793 - 7; http://dx.doi.org/10.1038/nsmb1142; PMID: 16936726
   PubMed Web of Science ®Google Scholar
• Bourc’his D, Bestor TH. Meiotic catastrophe and retrotransposon reactivation in male germ cells lacking Dnmt3L. Nature 2004; 431:96 - 9; http://dx.doi.org/10.1038/nature02886; PMID: 15318244
   PubMed Web of Science ®Google Scholar
• Coufal NG, Garcia-Perez JL, Peng GE, Yeo GW, Mu Y, Lovci MT, et al. L1 retrotransposition in human neural progenitor cells. Nature 2009; 460:1127 - 31; http://dx.doi.org/10.1038/nature08248; PMID: 19657334
   PubMed Web of Science ®Google Scholar
• Hata K, Sakaki Y. Identification of critical CpG sites for repression of L1 transcription by DNA methylation. Gene 1997; 189:227 - 34; http://dx.doi.org/10.1016/S0378-1119(96)00856-6; PMID: 9168132
   PubMed Web of Science ®Google Scholar
• Girard A, Sachidanandam R, Hannon GJ, Carmell MA. A germline-specific class of small RNAs binds mammalian Piwi proteins. Nature 2006; 442:199 - 202; PMID: 16751776
   PubMed Web of Science ®Google Scholar
• Rangasamy D. An S/MAR-based L1 retrotransposition cassette mediates sustained levels of insertional mutagenesis without suffering from epigenetic silencing of DNA methylation. Epigenetics 2010; 5:601 - 11; http://dx.doi.org/10.4161/epi.5.7.12647; PMID: 20595816
   PubMed Web of Science ®Google Scholar
• Bock C, Reither S, Mikeska T, Paulsen M, Walter J, Lengauer T. BiQ Analyzer: visualization and quality control for DNA methylation data from bisulfite sequencing. Bioinformatics 2005; 21:4067 - 8; http://dx.doi.org/10.1093/bioinformatics/bti652; PMID: 16141249
   PubMed Web of Science ®Google Scholar
• Rohde C, Zhang Y, Jurkowski TP, Stamerjohanns H, Reinhardt R, Jeltsch A. Bisulfite sequencing Data Presentation and Compilation (BDPC) web server--a useful tool for DNA methylation analysis. Nucleic Acids Res 2008; 36:e34; http://dx.doi.org/10.1093/nar/gkn083; PMID: 18296484
   PubMedGoogle Scholar
• Ellsworth DL, Ellsworth RE, Liebman MN, Hooke JA, Shriver CD. Genomic instability in histologically normal breast tissues: implications for carcinogenesis. Lancet Oncol 2004; 5:753 - 8; http://dx.doi.org/10.1016/S1470-2045(04)01653-5; PMID: 15581548
   PubMed Web of Science ®Google Scholar
• Sunami E, de Maat M, Vu A, Turner RR, Hoon DS. LINE-1 hypomethylation during primary colon cancer progression. PLoS One 2011; 6:e18884; http://dx.doi.org/10.1371/journal.pone.0018884; PMID: 21533144
   PubMed Web of Science ®Google Scholar
• Phokaew C, Kowudtitham S, Subbalekha K, Shuangshoti S, Mutirangura A. LINE-1 methylation patterns of different loci in normal and cancerous cells. Nucleic Acids Res 2008; 36:5704 - 12; http://dx.doi.org/10.1093/nar/gkn571; PMID: 18776216
   PubMed Web of Science ®Google Scholar
• Harris CR, Normart R, Yang Q, Stevenson E, Haffty BG, Ganesan S, et al. Association of nuclear localization of a long interspersed nuclear element-1 protein in breast tumors with poor prognostic outcomes. Genes Cancer 2010; 1:115 - 24; http://dx.doi.org/10.1177/1947601909360812; PMID: 20948976
   PubMedGoogle Scholar
• Rangasamy D, Tremethick DJ, Greaves IK. Gene knockdown by ecdysone-based inducible RNAi in stable mammalian cell lines. Nat Protoc 2008; 3:79 - 88; http://dx.doi.org/10.1038/nprot.2007.456; PMID: 18193024
   PubMed Web of Science ®Google Scholar