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

Epigenetics

Volumn 7, Issue 7, 2012, Pages 758-771

  Chen, Long ^a   Dahlstrom, Jane E ^a,b,c   Lee, Sung Hun ^a   Rangasamy, Danny ^a  

^a Biology and Environment   (Australia)

^b CANBERRA HOSPITAL   (Australia)

^c The Australian National University   (Australia)

Author keywords

Endogenous small RNAs; Human cancer cells; Retrotransposons; RNAi pathway

Indexed keywords

DNA; LONG INTERSPERSED NUCLEAR ELEMENT 1; NUCLEIC ACID BINDING PROTEIN; SMALL INTERFERING RNA; UNCLASSIFIED DRUG;

ARTICLE; BREAST CANCER; BREAST CELL; CANCER CELL; DNA METHYLATION; HUMAN; HUMAN CELL; PROTEIN EXPRESSION; RNA ANALYSIS; TRANSPOSON;

EID: 84863799077     PISSN: 15592294     EISSN: 15592308     Source Type: Journal    
DOI: 10.4161/epi.20706     Document Type: Article

References (55)

1. 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 USA 2003; 100:5280-5285; PMID:12682288; http://dx.doi.org/10.1073/pnas.0831042100.
2. Beck CR, Collier P, Macfarlane C, Malig M, Kidd JM, Eichler EE, et al. LINE-1 retrotransposition activity in human genomes. Cell 2010; 141:1159-1170; PMID:20602998; http://dx.doi.org/10.1016/j.cell.2010.05.021.
3. 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; 1:113-125; PMID:3692483; http://dx.doi.org/10.1016/0888-7543(87)90003-6.
4. Martin SL, Bushman FD. Nucleic acid chaperone activity of the ORF1 protein from the mouse LINE-1 retrotransposon. Mol Cell Biol 2001; 21:467-475; PMID:11134335; http://dx.doi.org/10.1128/MCB.21.2.467-75.2001.
5. Feng Q, Moran JV, Kazazian HH Jr, Boeke JD. Human L1 retrotransposon encodes a conserved endonuclease required for retrotransposition. Cell 1996; 87:905-916; PMID:8945517; http://dx.doi.org/10.1016/S0092-8674(00)81997-2.
6. Mathias SL, Scott AF, Kazazian HH Jr, Boeke JD, Gabriel A. Reverse transcriptase encoded by a human transposable element. Science 1991; 254:1808-1810; PMID:1722352; http://dx.doi.org/10.1126/science.1722352.
7. Moran JV, Holmes SE, Naas TP, DeBerardinis RJ, Boeke JD, Kazazian HH Jr. High frequency retrotransposition in cultured mammalian cells. Cell 1996; 87:917-927; PMID:8945518; http://dx.doi.org/10.1016/S0092-8674(00)81998-4.
8. Goodier JL, Kazazian HH Jr. Retrotransposons revisited: the restraint and rehabilitation of parasites. Cell 2008; 135:23-35; PMID:18854152; http://dx.doi.org/10.1016/j.cell.2008.09.022.
9. Cordaux R, Batzer MA. The impact of retrotransposons on human genome evolution. Nat Rev Genet 2009; 10:691-703; PMID:19763152; http://dx.doi.org/10.1038/nrg2640.
10. Esnault C, Maestre J, Heidmann T. Human LINE retrotransposons generate processed pseudogenes. Nat Genet 2000; 24:363-367; PMID:10742098; http://dx.doi.org/10.1038/74184.
11. Terai G, Yoshizawa A, Okida H, Asai K, Mituyama T. Discovery of short pseudogenes derived from messenger RNAs. Nucleic Acids Res 2010; 38:1163-1171; PMID:19965772; http://dx.doi.org/10.1093/nar/gkp1098.
12. Ostertag EM, Kazazian HH Jr. Biology of mammalian L1 retrotransposons. Annu Rev Genet 2001; 35:501-538; PMID:11700292; http://dx.doi.org/10.1146/annurev.genet.35.102401.091032.
13. Belancio VP, Roy-Engel AM, Pochampally RR, Deininger P. Somatic expression of LINE-1 elements in human tissues. Nucleic Acids Res 2010; 38:3909-3922; PMID:20215437; http://dx.doi.org/10.1093/nar/gkq132.
14. 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; 23:1303-1312; PMID:19487571; http://dx.doi.org/10.1101/gad.1803909.
15. Iskow RC, McCabe MT, Mills RE, Torene S, Pittard WS, Neuwald AF, et al. Natural mutagenesis of human genomes by endogenous retrotransposons. Cell 2010; 141:1253-1261; PMID:20603005; http://dx.doi.org/10.1016/j.cell.2010.05.020.
16. Yang N, Kazazian HH Jr. L1 retrotransposition is suppressed by endogenously encoded small interfering RNAs in human cultured cells. Nat Struct Mol Biol 2006; 13:763-771; PMID:16936727; http://dx.doi.org/10.1038/nsmb1141.
17. 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; 466:769-773; PMID:20686575; http://dx.doi.org/10.1038/nature09209.
18. 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; 1:115-124; PMID:20948976; http://dx.doi.org/10.1177/1947601909360812.
19. 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; 24:7213-7223; PMID:16170379; http://dx.doi.org/10.1038/sj.onc.1208866.
20. 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; 6:17934;PMID:21423624; http://dx.doi.org/10.1371/journal.pone.0017934.
21. 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; 6:1000917; PMID:20421991; http://dx.doi.org/10.1371/journal.pgen.1000917.
22. Okamura K, Lai EC. Endogenous small interfering RNAs in animals. Nat Rev Mol Cell Biol 2008; 9:673-678; PMID:18719707; http://dx.doi.org/10.1038/nrm2479.
23. 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; 453:793-797; PMID:18463636; http://dx.doi.org/10.1038/nature06938.
24. 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; 453:539-543; PMID:18404146; http://dx.doi.org/10.1038/nature06908.
25. 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; PMID:19691826; http://dx.doi.org/10.1186/1741-7007-7-53.
26. Nilsen TW. Endo-siRNAs: yet another layer of complexity in RNA silencing. Nat Struct Mol Biol 2008; 15:546-548; PMID:18523465; http://dx.doi.org/10.1038/nsmb0608-546.
27. Moazed D. Small RNAs in transcriptional gene silencing and genome defence. Nature 2009; 457:413-420; PMID:19158787; http://dx.doi.org/10.1038/nature07756.
28. Bratthauer GL, Cardiff RD, Fanning TG. Expression of LINE-1 retrotransposons in human breast cancer. Cancer 1994; 73:2333-2336; PMID:8168038; http://dx.doi.org/10.1002/1097-0142(19940501)73:92333::AIDCNCR2820730915 3.0.CO;2-4.
29. 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; 8:239-247; PMID:8895199.
30. 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; 27:4685-4697; PMID:17470553; http://dx.doi.org/10.1128/MCB.02138-06.
31. 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 USA 1990; 87:6990-6994; PMID:1698287; http://dx.doi.org/10.1073/pnas.87.18.6990.
32. Hoffmann MJ, Schulz WA. Causes and consequences of DNA hypomethylation in human cancer. Biochemistry and cell biology 2005; 83:296-321.
33. 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; 26:2518-2524; PMID:17043645; http://dx.doi.org/10.1038/sj.onc.1210039.
34. 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; 31:785-799; PMID:18922463; http://dx.doi.org/10.1016/j.molcel.2008.09.003.
35. 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; 20:1732-1743; PMID:16766679; http://dx.doi.org/10.1101/gad.1425706.
36. 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; 320:1077-1081; PMID:18403677; http://dx.doi.org/10.1126/science.1157396.
37. Malone CD, Hannon GJ. Small RNAs as guardians of the genome. Cell 2009; 136:656-668; PMID:19239887; http://dx.doi.org/10.1016/j.cell.2009.01.045.
38. Girard A, Hannon GJ. Conserved themes in small- RNA-mediated transposon control. Trends Cell Biol 2008; 18:136-148; PMID:18282709; http://dx.doi.org/10.1016/j.tcb.2008.01.004.
39. Speek M. Antisense promoter of human L1 retrotransposon drives transcription of adjacent cellular genes. Mol Cell Biol 2001; 21:1973-1985; PMID:11238933; http://dx.doi.org/10.1128/MCB.21.6.1973-85.2001.
40. 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; PMID:18463631; http://dx.doi.org/10.1038/nature07007.
41. 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 USA 2010; 107:7904-7909; PMID:20385818; http://dx.doi.org/10.1073/pnas.0908441107.
42. Yang JH, Shao P, Zhou H, Chen YQ, Qu LH. Deep-Base: a database for deeply annotating and mining deep sequencing data. Nucleic Acids Res 2010; 38:123-130; PMID:19966272; http://dx.doi.org/10.1093/nar/gkp943.
43. Kim DH, Villeneuve LM, Morris KV, Rossi JJ. Argonaute-1 directs siRNA-mediated transcriptional gene silencing in human cells. Nat Struct Mol Biol 2006; 13:793-797; PMID:16936726; http://dx.doi.org/10.1038/nsmb1142.
44. Bourc'his D, Bestor TH. Meiotic catastrophe and retrotransposon reactivation in male germ cells lacking Dnmt3L. Nature 2004; 431:96-99; PMID:15318244; http://dx.doi.org/10.1038/nature02886
45. Coufal NG, Garcia-Perez JL, Peng GE, Yeo GW, Mu Y, Lovci MT, et al. L1 retrotransposition in human neural progenitor cells. Nature 2009; 460:1127-1131; PMID:19657334; http://dx.doi.org/10.1038/nature08248.
46. Hata K, Sakaki Y. Identification of critical CpG sites for repression of L1 transcription by DNA methylation. Gene 1997; 189:227-234; PMID:9168132; http://dx.doi.org/10.1016/S0378-1119(96)00856-6.
47. 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.
48. 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; 5:601-611; PMID:20595816; http://dx.doi.org/10.4161/epi.5.7.12647.
49. 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; 21:4067-4068; PMID:16141249; http://dx.doi.org/10.1093/bioinformatics/bti652.
50. 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; 36:34; PMID:18296484; http://dx.doi.org/10.1093/nar/gkn083.
51. Ellsworth DL, Ellsworth RE, Liebman MN, Hooke JA, Shriver CD. Genomic instability in histologically normal breast tissues: implications for carcinogenesis. Lancet Oncol 2004; 5:753-758; PMID:15581548; http://dx.doi.org/10.1016/S1470-2045(04)01653-5.
52. Sunami E, de Maat M, Vu A, Turner RR, Hoon DS. LINE-1 hypomethylation during primary colon cancer progression. PLoS One 2011; 6:18884; PMID:21533144; http://dx.doi.org/10.1371/journal.pone.0018884.
53. 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; 36:5704-5712; PMID:18776216; http://dx.doi.org/10.1093/nar/gkn571.
54. 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; 1:115-124; PMID:20948976; http://dx.doi.org/10.1177/1947601909360812.
55. Rangasamy D, Tremethick DJ, Greaves IK. Gene knockdown by ecdysone-based inducible RNAi in stable mammalian cell lines. Nat Protoc 2008; 3:79-88; PMID:18193024; http://dx.doi.org/10.1038/nprot.2007.456