RNAi-Dependent and Independent Control of LINE1 Accumulation and Mobility in Mouse Embryonic Stem Cells

PLoS Genetics

Volumn 9, Issue 11, 2013, Pages

  Ciaudo, Constance ^a,b   Jay, Florence ^a,c   Okamoto, Ikuhiro ^b,g   Chen, Chong Jian ^b,d   Sarazin, Alexis ^a   Servant, Nicolas ^d,e,f   Barillot, Emmanuel ^d,e,f   Heard, Edith ^b   Voinnet, Olivier ^a,c  

^a ETH ZURICH   (Switzerland)

^b INSTITUT CURIE   (France)

^c UNIVERSITY OF ZURICH   (Switzerland)

^d INSTITUT CURIE   (France)

^e INSERM U900   (France)

^f PSL RESEARCH UNIVERSITY   (France)

^g KYOTO UNIVERSITY   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

RNA; SMALL INTERFERING RNA;

5' UNTRANSLATED REGION; ARTICLE; BLASTOCYST; CELL DIFFERENTIATION; CELL MOTILITY; CELL PROLIFERATION; EMBRYONIC STEM CELL; GENE MUTATION; GENETIC TRANSCRIPTION; MOUSE; NONHUMAN; RNA DEGRADATION; RNA INTERFERENCE; TRANSPOSON;

5' UNTRANSLATED REGIONS; ANIMALS; ARGONAUTE PROTEINS; CELL DIFFERENTIATION; CELL PROLIFERATION; DEAD-BOX RNA HELICASES; DNA METHYLATION; EMBRYONIC STEM CELLS; GENE EXPRESSION REGULATION, DEVELOPMENTAL; LONG INTERSPERSED NUCLEOTIDE ELEMENTS; MICE; PROMOTER REGIONS, GENETIC; RETROELEMENTS; RIBONUCLEASE III; RNA INTERFERENCE;

EID: 84888209464     PISSN: 15537390     EISSN: 15537404     Source Type: Journal    
DOI: 10.1371/journal.pgen.1003791     Document Type: Article

References (63)

1. Beck CR, Garcia-Perez JL, Badge RM, Moran J V, (2011) LINE-1 elements in structural variation and disease. Annu Rev Genomics Hum Genet 12: 187-215.
2. Zaratiegui M, Irvine D V, Martienssen R, (2007) Noncoding RNAs and gene silencing. Cell 128: 763-776.
3. Aravin AA, Sachidanandam R, Bourc'his D, Schaefer C, Pezic D, et al. (2008) A piRNA pathway primed by individual transposons is linked to de novo DNA methylation in mice. Mol Cell 31: 785-799.
4. Smith ZD, Chan MM, Mikkelsen TS, Gu H, Gnirke A, et al. (2012) A unique regulatory phase of DNA methylation in the early mammalian embryo. Nature 484: 339-344.
5. Howlett SK, Reik W, (1991) Methylation levels of maternal and paternal genomes during preimplantation development. Development 113: 119-127.
6. Packer AI, Manova K, Bachvarova RF, (1993) A Discrete LINE-1 Transcript in Mouse Blastocysts. Dev Biol 157: 281-283.
7. Kano H, Godoy I, Courtney C, Vetter MR, Gerton GL, et al. (2009) L1 retrotransposition occurs mainly in embryogenesis and creates somatic mosaicism. Genes Dev 23: 1303-1312.
8. Teixeira FK, Heredia F, Sarazin A, Roudier F, Boccara M, et al. (2009) A role for RNAi in the selective correction of DNA methylation defects. Science 323: 1600-1604.
9. Slotkin RK, Vaughn M, Borges F, Tanurdzić M, Becker JD, et al. (2009) Epigenetic reprogramming and small RNA silencing of transposable elements in pollen. Cell 136: 461-472.
10. Bernstein E, Caudy AA, Hammond SM, Hannon GJ, (2001) Role for a bidentate ribonuclease in the initiation step of RNA interference. Nature 409: 363-366.
11. Stark GR, Kerr IM, Williams BR, Silverman RH, Schreiber RD, (1998) How cells respond to interferons. Annu Rev Biochem 67: 227-264.
12. Watanabe T, Totoki Y, Toyoda A, Kaneda M, Kuramochi-Miyagawa S, et al. (2008) Endogenous siRNAs from naturally formed dsRNAs regulate transcripts in mouse oocytes. Nature 453: 539-543.
13. Babiarz JE, Ruby JG, Wang Y, Bartel DP, Blelloch R, (2008) Mouse ES cells express endogenous shRNAs, siRNAs, and other Microprocessor-independent, Dicer-dependent small RNAs. Genes Dev 22: 2773-2785.
14. Arand J, Spieler D, Karius T, Branco MR, Meilinger D, et al. (2012) In Vivo Control of CpG and Non-CpG DNA Methylation by DNA Methyltransferases. PLoS Genet 8: e1002750.
15. Chow JC, Ciaudo C, Fazzari MJ, Mise N, Servant N, et al. (2010) LINE-1 activity in facultative heterochromatin formation during X chromosome inactivation. Cell 141: 956-969.
16. Weng A, Magnuson T, Storb U, (1995) Strain-specific transgene methylation occurs early in mouse development and can be recapitulated in embryonic stem cells. Development 121: 2853-2859.
17. Kanellopoulou C, Muljo SA, Kung AL, Ganesan S, Drapkin R, et al. (2005) Dicer-deficient mouse embryonic stem cells are defective in differentiation and centromeric silencing. Genes Dev 19: 489-501.
18. Calabrese JM, Seila AC, Yeo GW, Sharp P a, (2007) RNA sequence analysis defines Dicer's role in mouse embryonic stem cells. PNAS 104: 18097-18102.
19. Mätlik K, Redik K, Speek M, (2006) L1 antisense promoter drives tissue-specific transcription of human genes. J Biomed Biotech 2006: 1-16.
20. Yang N, Kazazian HH, (2006) L1 retrotransposition is suppressed by endogenously encoded small interfering RNAs in human cultured cells. Nat Struct Mol Biol 13: 763-771.
21. Kazazian H (2011) Mobile DNA: Finding Treasure in Junk. 1st ed. FT Press Science.
22. Murchison EP, Partridge JF, Tam OH, Cheloufi S, Hannon GJ, (2005) Characterization of Dicer-deficient murine embryonic stem cells. PNAS 102: 12135-12140.
23. Tay Y, Zhang J, Thomson AM, Lim B, Rigoutsos I, (2008) MicroRNAs to Nanog, Oct4 and Sox2 coding regions modulate embryonic stem cell differentiation. Nature 455: 1124-1128.
24. Chen C, Servant N, Toedling J, Sarazin A, Marchais A, et al. (2012) ncPRO-seq: a tool for annotation and profiling analysis of ncRNAs from small RNA-seq. Bioinformatics 28: 3-5.
25. Goodier JL, Ostertag EM, Du K, Kazazian HH, (2001) A novel active L1 retrotransposon subfamily in the mouse. Genome Res 11: 1677-1685.
26. Ip J, Canham P, Choo KHA, Inaba Y, Jacobs Sa, et al. (2012) Normal DNA Methylation Dynamics in DICER1-Deficient Mouse Embryonic Stem Cells. PLoS Genet 8: e1002919.
27. Tsumura A, Hayakawa T, Kumaki Y, Takebayashi S, Sakaue M, et al. (2006) Maintenance of self-renewal ability of mouse embryonic stem cells in the absence of DNA methyltransferases Dnmt1, Dnmt3a and Dnmt3b. Genes Cells 11: 805-814.
28. Ostertag EM, Kazazian HHJ, (2001) BIOLOGY OF MAMMALIAN L1 RETROTRANSPOSONS. Annual review of genetics 35: 501-538.
29. Naas TP, DeBerardinis RJ, Moran J V, Ostertag EM, Kingsmore SF, et al. (1998) An actively retrotransposing, novel subfamily of mouse L1 elements. The EMBO journal 17: 590-597.
30. Prak ET, Dodson AW, Farkash EA, Kazazian HH Jr, (2003) Tracking an embryonic L1 retrotransposition event. PNAS 100: 1832-1837.
31. Ostertag EM, Prak ET, DeBerardinis RJ, Moran JV, Kazazian HH, (2000) Determination of L1 retrotransposition kinetics in cultured cells. NAR 28: 1418-1423.
32. Ostertag EM, DeBerardinis RJ, Goodier JL, Zhang Y, Yang N, et al. (2002) A mouse model of human L1 retrotransposition. Nat Genet 32: 655-660.
33. Xie Y, Rosser JM, Thompson TL, Boeke JD, An W, (2011) Characterization of L1 retrotransposition with high-throughput dual-luciferase assays. NAR 39: e16.
34. Xiao S, Xie D, Cao X, Yu P, Xing X, et al. (2012) Comparative epigenomic annotation of regulatory DNA. Cell 149: 1381-1392.
35. Dueck A, Ziegler C, Eichner A, Berezikov E, Meister G, (2012) microRNAs associated with the different human Argonaute proteins. NAR 40: 9850-9862.
36. Ciaudo C, Bourdet A, Cohen-Tannoudji M, Dietz HC, Rougeulle C, et al. (2006) Nuclear mRNA degradation pathway(s) are implicated in Xist regulation and X chromosome inactivation. PLoS Genet 2: e94.
37. Wang Y, Medvid R, Melton C, Jaenisch R, Blelloch R, (2007) DGCR8 is essential for microRNA biogenesis and silencing of embryonic stem cell self-renewal. Nat Genet 39: 380-385.
38. Su H, Trombly MI, Chen J, Wang X, (2009) Essential and overlapping functions for mammalian Argonautes in microRNA silencing. Genes Dev 23: 304-317.
39. Wang D, Zhang Z, O'Loughlin E, Lee T, Houel S, et al. (2012) Quantitative functions of Argonaute proteins in mammalian development. Genes Dev 26: 693-704.
40. Smibert P, Yang J-S, Azzam G, Liu J-L, Lai EC, (2013) Homeostatic control of Argonaute stability by microRNA availability. NSMB pp. 1-9.
41. Derrien B, Baumberger N, Schepetilnikov M, Viotti C, Cillia J De, (2012) Degradation of the antiviral component ARGONAUTE1 by the autophagy pathway. PNAS 109: 15942-15946.
42. Johnston M, Geoffroy M, Sobala A, Hay R, Hutvagner G, (2010) HSP90 Protein Stabilizes Unloaded Argonaute Complexes and Microscopic P-bodies in Human Cells. Mol Biol Cell 21: 1462-1469.
43. Gy I, Gasciolli V, Lauressergues D, Morel J-B, Gombert J, et al. (2007) Arabidopsis FIERY1, XRN2, and XRN3 are endogenous RNA silencing suppressors. The Plant cell 19: 3451-3461.
44. Yamanaka S, Mehta S, Reyes-Turcu FE, Zhuang F, Fuchs RT, et al. (2013) RNAi triggered by specialized machinery silences developmental genes and retrotransposons. Nature 493: 557-560.
45. Swergold GD, (1990) Identification, Characterization, and Cell Specificity of a Human LINE-1 Promoter. Mol Cell Biol 10: 6718-6729.
46. Houseley J, Tollervey D, (2009) The many pathways of RNA degradation. Cell 136: 763-776.
47. Rosenbloom KR, Sloan C a, Malladi VS, Dreszer TR, Learned K, et al. (2012) ENCODE Data in the UCSC Genome Browser: year 5 update. NAR 41: 56-63.
48. Fagegaltier D, Bouge AL, Berry B, Poisot E, Sismeiro O, et al. (2009) The endogenous siRNA pathway is involved in heterochromatin formation in Drosophila. PNAS 106: 21258-21263.
49. Moreno AB, Martínez de Alba AE, Bardou F, Crespi MD, Vaucheret H, et al. (2013) Cytoplasmic and nuclear quality control and turnover of single-stranded RNA modulate post-transcriptional gene silencing in plants. NAR 41: 4699-4708.
50. Tam OH, Aravin AA, Stein P, Girard A, Murchison EP, et al. (2008) Pseudogene-derived small interfering RNAs regulate gene expression in mouse oocytes. Nature 453: 534-538.
51. Hu Q, Tanasa B, Trabucchi M, Li W, Zhang J, et al. (2012) DICER- and AGO3-dependent generation of retinoic acid-induced DR2 Alu RNAs regulates human stem cell proliferation. NSMB 19: 1168-1175.
52. Paddison PJ, Caudy A a, Hannon GJ, (2002) Stable suppression of gene expression by RNAi in mammalian cells. PNAS 99: 1443-1448.
53. Billy E, Brondani V, Zhang H, Müller U, Filipowicz W, (2001) Specific interference with gene expression induced by long, double-stranded RNA in mouse embryonal teratocarcinoma cell lines. PNAS 98: 11443-14428.
54. Maillart P, Ciaudo C, Marchais A, Li Y, Jay F, et al. (2013) Antiviral RNA interference in mammalian cells. In press.
55. Hooper M, Hardy K, Handyside A, Hunter S, Monk M, (1987) HPRT-deficient (Lesch-Nyhan) mouse embryos derived from germline colonization by cultured cells. Nature 326: 292-295.
56. Meister G, Landthaler M, Patkaniowska A, Dorsett Y, Teng G, et al. (2004) Human Argonaute2 mediates RNA cleavage targeted by miRNAs and siRNAs. Mol Cell 15: 185-197.
57. Bernstein E, Kim SY, Carmell M a, Murchison EP, Alcorn H, et al. (2003) Dicer is essential for mouse development. Nat Genet 35: 215-217.
58. Vooijs M, Jonkers J, Berns a, (2001) A highly efficient ligand-regulated Cre recombinase mouse line shows that LoxP recombination is position dependent. EMBO reports 2: 292-297.
59. Penny GD, Kay GF, Sheardown SA, Rastan S, Brockdorff N, et al. (1996) Requirement for Xist in X chromosome inactivation. Nature 379: 131-137.
60. Landthaler M, Gaidatzis D, Rothballer A, Chen PY, Soll SJ, et al. (2008) Molecular characterization of human Argonaute-containing ribonucleoprotein complexes and their bound target mRNAs. RNA 14: 2580-2596.
61. Henderson IR, Chan SR, Cao X, Johnson L, Jacobsen SE, (2010) Accurate sodium bisulfite sequencing in plants. Epigenetics 5: 47-49.
62. Gruntman E, Qi Y, Slotkin RK, Roeder T, Martienssen Ra, et al. (2008) Kismeth: analyzer of plant methylation states through bisulfite sequencing. BMC bioinformatics 9: 371.
63. Rohde C, Zhang Y, Reinhardt R, Jeltsch A, (2010) BISMA-fast and accurate bisulfite sequencing data analysis of individual clones from unique and repetitive sequences. BMC bioinformatics 11: 230.