PiRNAs, transposon silencing, and germline genome integrity

Mutation Research - Fundamental and Molecular Mechanisms of Mutagenesis

Volumn 714, Issue 1-2, 2011, Pages 95-104

  Castañeda, Julio ^a,b   Genzor, Pavol ^a,b   Bortvin, Alex ^a,b  

^a JOHNS HOPKINS UNIVERSITY   (United States)

^b GEOPHYSICAL LABORATORY   (United States)

Author keywords

DNA methylation; Dnmt; Epigenetic; Germline; Histone modifications; LINE 1; Maelstrom; Mechanism; Mouse; PiRNA; TE; Transposable elements

Indexed keywords

DNA; PIWI INTERACTING RNA; RNA POLYMERASE;

CHROMOSOME STRUCTURE; DNA METHYLATION; EPIGENETICS; FEMALE; GAMETE; GENE EXPRESSION REGULATION; GENE SILENCING; GENOME ANALYSIS; GERM CELL; HISTONE MODIFICATION; HUMAN; MALE; MUTAGENESIS; MUTAGENICITY; PRIORITY JOURNAL; PROGENY; REPRODUCTION; REVIEW; TRANSPOSON;

ANIMALS; DNA TRANSPOSABLE ELEMENTS; DROSOPHILA; EPIGENESIS, GENETIC; GENE SILENCING; GENOMIC INSTABILITY; GERM CELLS; MICE; MUTAGENESIS, INSERTIONAL; RNA, SMALL INTERFERING;

MAMMALIA;

EID: 80051807498     PISSN: 00275107     EISSN: 09218262     Source Type: Journal    
DOI: 10.1016/j.mrfmmm.2011.05.002     Document Type: Review

References (160)

1. Lawson K.A., Dunn N.R., Roelen B.A., Zeinstra L.M., Davis A.M., Wright C.V., Korving J.P., Hogan B.L. Bmp4 is required for the generation of primordial germ cells in the mouse embryo. Genes Dev. 1999, 13:424-436.
2. Fujiwara T., Dunn N.R., Hogan B.L. Bone morphogenetic protein 4 in the extraembryonic mesoderm is required for allantois development and the localization and survival of primordial germ cells in the mouse. Proc. Natl. Acad. Sci. U.S.A. 2001, 98:13739-13744.
3. Ying Y., Liu X.M., Marble A., Lawson K.A., Zhao G.Q. Requirement of Bmp8b for the generation of primordial germ cells in the mouse. Mol. Endocrinol. 2000, 14:1053-1063.
4. Ying Y., Zhao G.Q. Cooperation of endoderm-derived BMP2 and extraembryonic ectoderm-derived BMP4 in primordial germ cell generation in the mouse. Dev. Biol. 2001, 232:484-492.
5. Seki Y., Yamaji M., Yabuta Y., Sano M., Shigeta M., Matsui Y., Saga Y., Tachibana M., Shinkai Y., Saitou M. Cellular dynamics associated with the genome-wide epigenetic reprogramming in migrating primordial germ cells in mice. Development 2007, 134:2627-2638.
6. Seki Y., Hayashi K., Itoh K., Mizugaki M., Saitou M., Matsui Y. Extensive and orderly reprogramming of genome-wide chromatin modifications associated with specification and early development of germ cells in mice. Dev. Biol. 2005, 278:440-458.
7. Hajkova P., Erhardt S., Lane N., Haaf T., El-Maarri O., Reik W., Walter J., Surani M.A. Epigenetic reprogramming in mouse primordial germ cells. Mech. Dev. 2002, 117:15-23.
8. Surani M.A., Durcova-Hills G., Hajkova P., Hayashi K., Tee W.W. Germ line, stem cells, and epigenetic reprogramming. Cold Spring Harb. Symp. Quant. Biol. 2008, LXXIII:9.
9. Extavour C.G, Akam M. Mechanisms of germ cell specification across the metazoans: epigenesis and preformation. Development 2003, 130:5869-5884.
10. Chaillet J.R., Vogt T.F., Beier D.R., Leder P. Parental-specific methylation of an imprinted transgene is established during gametogenesis and progressively changes during embryogenesis. Cell 1991, 66:77-83.
11. Sapienza C., Peterson A.C., Rossant J., Balling R. Degree of methylation of transgenes is dependent on gamete of origin. Nature 1987, 328:251-254.
12. Reik W., Collick A., Norris M.L., Barton S.C., Surani M.A. Genomic imprinting determines methylation of parental alleles in transgenic mice. Nature 1987, 328:248-251.
13. Monk M., Boubelik M., Lehnert S. Temporal and regional changes in DNA methylation in the embryonic, extraembryonic and germ cell lineages during mouse embryo development. Development 1987, 99:371-382.
14. Kafri T, Ariel M., Brandeis M., Shemer R., Urven L., McCarrey J., Cedar H., Razin A. Developmental pattern of gene-specific DNA methylation in the mouse embryo and germ line. Genes Dev. 1992, 6:705-714.
15. McLaren A. Meiosis and differentiation of mouse germ cells. Symp. Soc. Exp. Biol. 1984, 38:7-23.
16. Obata Y., Kaneko-Ishino T., Koide T., Takai Y., Ueda T., Domeki I., Shiroishi T., Ishino F., Kono T. Disruption of primary imprinting during oocyte growth leads to the modified expression of imprinted genes during embryogenesis. Development 1998, 125:1553-1560.
17. Bennett M.D. The time and duration of meiosis. Philos. Trans. R. Soc. Lond. B: Biol. Sci. 1977, 277:201-226.
18. Hata K., Okano M., Lei H., Li E. Dnmt3L cooperates with the Dnmt3 family of de novo DNA methyltransferases to establish maternal imprints in mice. Development 2002, 129:1983-1993.
19. Bourc'his D., Bestor T.H. Meiotic catastrophe and retrotransposon reactivation in male germ cells lacking Dnmt3L. Nature 2004, 431:96-99.
20. Kaneda M., Okano M., Hata K., Sado T., Tsujimoto N., Li E., Sasaki H. Essential role for de novo DNA methyltransferase Dnmt3a in paternal and maternal imprinting. Nature 2004, 429:900-903.
21. De La Fuente R., Baumann C., Fan T., Schmidtmann A., Dobrinski I., Muegge K. Lsh is required for meiotic chromosome synapsis and retrotransposon silencing in female germ cells. Nat. Cell Biol. 2006, 8:1448-1454.
22. Orgel L.E., Crick F.H. Selfish DNA: the ultimate parasite. Nature 1980, 284:604-607.
23. Lander E.S., Linton L.M., Birren B., Nusbaum C., Zody M.C., Baldwin J., Devon K., Dewar K., Doyle M., FitzHugh W., Funke R., Gage D., Harris K., Heaford A., Howland J., Kann L., Lehoczky J., LeVine R., McEwan P., McKernan K., Meldrim J., Mesirov J.P., Miranda C., Morris W., Naylor J., Raymond C., Rosetti M., Santos R., Sheridan A., Sougnez C., Stange-Thomann N., Stojanovic N., Subramanian A., Wyman D., Rogers J., Sulston J., Ainscough R., Beck S., Bentley D., Burton J., Clee C., Carter N., Coulson A., Deadman R., Deloukas P., Dunham A., Dunham I., Durbin R., French L., Grafham D., Gregory S., Hubbard T., Humphray S., Hunt A., Jones M., Lloyd C., McMurray A., Matthews L., Mercer S., Milne S., Mullikin J.C., Mungall A., Plumb R., Ross M., Shownkeen R., Sims S., Waterston R.H., Wilson R.K., Hillier L.W., McPherson J.D., Marra M.A., Mardis E.R., Fulton L.A., Chinwalla A.T., Pepin K.H., Gish W.R., Chissoe S.L., Wendl M.C., Delehaunty K.D., Miner T.L., Delehaunty A., Kramer J.B., Cook L.L., Fulton R.S., Johnson D.L., Minx P.J., Clifton S.W., Hawkins T., Branscomb E., Predki P., Richardson P., Wenning S., Slezak T., Doggett N., Cheng J.F., Olsen A., Lucas S., Elkin C., Uberbacher E., Frazier M., Gibbs R.A., Muzny D.M., Scherer S.E., Bouck J.B., Sodergren E.J., Worley K.C., Rives C.M., Gorrell J.H., Metzker M.L., Naylor S.L., Kucherlapati R.S., Nelson D.L., Weinstock G.M., Sakaki Y., Fujiyama A., Hattori M., Yada T., Toyoda A., Itoh T., Kawagoe C., Watanabe H., Totoki Y., Taylor T., Weissenbach J., Heilig R., Saurin W., Artiguenave F., Brottier P., Bruls T., Pelletier E., Robert C., Wincker P., Smith D.R., Doucette-Stamm L., Rubenfield M., Weinstock K., Lee H.M., Dubois J., Rosenthal A., Platzer M., Nyakatura G., Taudien S., Rump A., Yang H., Yu J., Wang J., Huang G., Gu J., Hood L., Rowen L., Madan A., Qin S., Davis R.W., Federspiel N.A., Abola A.P., Proctor M.J., Myers R.M., Schmutz J., Dickson M., Grimwood J., Cox D.R., Olson M.V., Kaul R., Shimizu N., Kawasaki K., Minoshima S., Evans G.A., Athanasiou M., Schultz R., Roe B.A., Chen F., Pan H., Ramser J., Lehrach H., Reinhardt R., McCombie W.R., de la Bastide M., Dedhia N., Blocker H., Hornischer K., Nordsiek G., Agarwala R., Aravind L., Bailey J.A., Bateman A., Batzoglou S., Birney E., Bork P., Brown D.G., Burge C.B., Cerutti L., Chen H.C., Church D., Clamp M., Copley R.R., Doerks T., Eddy S.R., Eichler E.E., Furey T.S., Galagan J., Gilbert J.G., Harmon C., Hayashizaki Y., Haussler D., Hermjakob H., Hokamp K., Jang W., Johnson L.S., Jones T.A., Kasif S., Kaspryzk A., Kennedy S., Kent W.J., Kitts P., Koonin E.V., Korf I., Kulp D., Lancet D., Lowe T.M., McLysaght A., Mikkelsen T., Moran J.V., Mulder N., Pollara V.J., Ponting C.P., Schuler G., Schultz J., Slater G., Smit A.F., Stupka E., Szustakowski J., Thierry-Mieg D., Thierry-Mieg J., Wagner L., Wallis J., Wheeler R., Williams A., Wolf Y.I., Wolfe K.H., Yang S.P., Yeh R.F., Collins F., Guyer M.S., Peterson J., Felsenfeld A., Wetterstrand K.A., Patrinos A., Morgan M.J., de Jong P., Catanese J.J., Osoegawa K., Shizuya H., Choi S., Chen Y.J. Initial sequencing and analysis of the human genome. Nature 2001, 409:860-921.
24. Doolittle W.F., Sapienza C. Selfish genes, the phenotype paradigm and genome evolution. Nature 1980, 284:601-603.
25. Bestor T.H, Bourc'his D. Transposon silencing and imprint establishment in mammalian germ cells. Cold Spring Harb. Symp. Quant. Biol. 2004, 69:381-387.
26. Kuramochi-Miyagawa S., Watanabe T., Gotoh K., Totoki Y., Toyoda A., Ikawa M., Asada N., Kojima K., Yamaguchi Y., Ijiri T.W., Hata K., Li E., Matsuda Y., Kimura T., Okabe M., Sakaki Y., Sasaki H., Nakano T. DNA methylation of retrotransposon genes is regulated by Piwi family members MILI and MIWI2 in murine fetal testes. Genes Dev. 2008, 22:908-917.
27. Aravin A.A., Sachidanandam R., Bourc'his D., Schaefer C., Pezic D., Toth K.F., Bestor T., Hannon G.J. A piRNA pathway primed by individual transposons is linked to de novo DNA methylation in mice. Mol. Cell 2008, 31:785-799.
28. Waterston R.H., Lindblad-Toh K., Birney E., Rogers J., Abril J.F., Agarwal P., Agarwala R., Ainscough R., Alexandersson M., An P., Antonarakis S.E., Attwood J., Baertsch R., Bailey J., Barlow K., Beck S., Berry E., Birren B., Bloom T., Bork P., Botcherby M., Bray N., Brent M.R., Brown D.G., Brown S.D., Bult C., Burton J., Butler J., Campbell R.D., Carninci P., Cawley S., Chiaromonte F., Chinwalla A.T., Church D.M., Clamp M., Clee C., Collins F.S., Cook L.L., Copley R.R., Coulson A., Couronne O., Cuff J., Curwen V., Cutts T., Daly M., David R., Davies J., Delehaunty K.D., Deri J., Dermitzakis E.T., Dewey C., Dickens N.J., Diekhans M., Dodge S., Dubchak I., Dunn D.M., Eddy S.R., Elnitski L., Emes R.D., Eswara P., Eyras E., Felsenfeld A., Fewell G.A., Flicek P., Foley K., Frankel W.N., Fulton L.A., Fulton R.S., Furey T.S., Gage D., Gibbs R.A., Glusman G., Gnerre S., Goldman N., Goodstadt L., Grafham D., Graves T.A., Green E.D., Gregory S., Guigo R., Guyer M., Hardison R.C., Haussler D., Hayashizaki Y., Hillier L.W., Hinrichs A., Hlavina W., Holzer T., Hsu F., Hua A., Hubbard T., Hunt A., Jackson I., Jaffe D.B., Johnson L.S., Jones M., Jones T.A., Joy A., Kamal M., Karlsson E.K., Karolchik D., Kasprzyk A., Kawai J., Keibler E., Kells C., Kent W.J., Kirby A., Kolbe D.L., Korf I., Kucherlapati R.S., Kulbokas E.J., Kulp D., Landers T., Leger J.P., Leonard S., Letunic I., Levine R., Li J., Li M., Lloyd C., Lucas S., Ma B., Maglott D.R., Mardis E.R., Matthews L., Mauceli E., Mayer J.H., McCarthy M., McCombie W.R., McLaren S., McLay K., McPherson J.D., Meldrim J., Meredith B., Mesirov J.P., Miller W., Miner T.L., Mongin E., Montgomery K.T., Morgan M., Mott R., Mullikin J.C., Muzny D.M., Nash W.E., Nelson J.O., Nhan M.N., Nicol R., Ning Z., Nusbaum C., O'Connor M.J., Okazaki Y., Oliver K., Overton-Larty E., Pachter L., Parra G., Pepin K.H., Peterson J., Pevzner P., Plumb R., Pohl C.S., Poliakov A., Ponce T.C., Ponting C.P., Potter S., Quail M., Reymond A., Roe B.A., Roskin K.M., Rubin E.M., Rust A.G., Santos R., Sapojnikov V., Schultz B., Schultz J., Schwartz M.S., Schwartz S., Scott C., Seaman S., Searle S., Sharpe T., Sheridan A., Shownkeen R., Sims S., Singer J.B., Slater G., Smit A., Smith D.R., Spencer B., Stabenau A., Stange-Thomann N., Sugnet C., Suyama M., Tesler G., Thompson J., Torrents D., Trevaskis E., Tromp J., Ucla C., Ureta-Vidal A., Vinson J.P., Von Niederhausern A.C., Wade C.M., Wall M., Weber R.J., Weiss R.B., Wendl M.C., West A.P., Wetterstrand K., Wheeler R., Whelan S., Wierzbowski J., Willey D., Williams S., Wilson R.K., Winter E., Worley K.C., Wyman D., Yang S., Yang S.P., Zdobnov E.M., Zody M.C., Lander E.S. Initial sequencing and comparative analysis of the mouse genome. Nature 2002, 420:520-562.
29. Mc C.B. The origin and behavior of mutable loci in maize. Proc. Natl. Acad. Sci. U.S.A. 1950, 36:344-355.
30. Feschotte C., Pritham E.J. DNA transposons and the evolution of eukaryotic genomes. Annu. Rev. Genet. 2007, 41:331-368.
31. Eickbush T.H., Jamburuthugoda V.K. The diversity of retrotransposons and the properties of their reverse transcriptases. Virus Res. 2008, 134:221-234.
32. Havecker E.R., Gao X., Voytas D.F. The diversity of LTR retrotransposons. Genome Biol. 2004, 5:225.
33. McCarthy E.M., McDonald J.F. Long terminal repeat retrotransposons of Mus musculus. Genome Biol. 2004, 5:R14.
34. Babushok D.V., Kazazian H.H. Progress in understanding the biology of the human mutagen, LINE-1. Hum. Mutat. 2007, 28:527-539.
35. Belancio V.P., Deininger P.L., Roy-Engel A.M. LINE dancing in the human genome: transposable elements and disease. Genome Med. 2009, 1:97.
36. Wagner A. Transposable elements as genomic diseases. Mol. Biosyst. 2009, 5:32-35.
37. Harris C.R., Normart R., Yang Q., Stevenson E., Haffty B.G., Ganesan S., Cordon-Cardo C., Levine A.J., Tang L.H. 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.
38. Mirabello L., Savage S.A., Korde L., Gadalla S.M., Greene M.H. LINE-1 methylation is inherited in familial testicular cancer kindreds. BMC Med. Genet. 2010, 11:77.
39. Muotri A.R., Marchetto M.C., Coufal N.G., Oefner R., Yeo G., Nakashima K., Gage F.H. L1 retrotransposition in neurons is modulated by MeCP2. Nature 2010, 468:443-446.
40. Muotri A.R., Chu V.T., Marchetto M.C., Deng W., Moran J.V., Gage F.H. Somatic mosaicism in neuronal precursor cells mediated by L1 retrotransposition. Nature 2005, 435:903-910.
41. van den Hurk J.A., Meij I.C., Seleme M.C., Kano H., Nikopoulos K., Hoefsloot L.H., Sistermans E.A., de Wijs I.J., Mukhopadhyay A., Plomp A.S., de Jong P.T., Kazazian H.H., Cremers F.P. L1 retrotransposition can occur early in human embryonic development. Hum. Mol. Genet. 2007, 16:1587-1592.
42. Kano H., Godoy I., Courtney C., Vetter M.R., Gerton G.L., Ostertag E.M., Kazazian H.H. L1 retrotransposition occurs mainly in embryogenesis and creates somatic mosaicism. Genes Dev. 2009, 23:1303-1312.
43. Coufal N.G., Garcia-Perez J.L., Peng G.E., Yeo G.W., Mu Y., Lovci M.T., Morell M., O'Shea K.S., Moran J.V., Gage F.H. L1 retrotransposition in human neural progenitor cells. Nature 2009, 460:1127-1131.
44. Cost G.J., Feng Q., Jacquier A., Boeke J.D. Human L1 element target-primed reverse transcription in vitro. EMBO J. 2002, 21:5899-5910.
45. Dmitriev S.E., Andreev D.E., Terenin I.M., Olovnikov I.A., Prassolov V.S., Merrick W.C., Shatsky I.N. 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.
46. Han J.S. Non-long terminal repeat (non-LTR) retrotransposons: mechanisms, recent developments, and unanswered questions. Mob. DNA 2010, 1:15.
47. Gasior S.L, Wakeman T.P., Xu B., Deininger P.L. The human LINE-1 retrotransposon creates DNA double-strand breaks. J. Mol. Biol. 2006, 357:1383-1393.
48. Dombroski B.A., Mathias S.L., Nanthakumar E., Scott A.F., Kazazian H.H. Isolation of an active human transposable element. Science 1991, 254:1805-1808.
49. Johnson K.J., Springer N.M., Bielinsky A.K., Largaespada D.A., Ross J.A. Developmental origins of cancer. Cancer Res. 2009, 69:6375-6377.
50. Holmes S.E., Singer M.F., Swergold G.D. Studies on p40, the leucine zipper motif-containing protein encoded by the first open reading frame of an active human LINE-1 transposable element. J. Biol. Chem. 1992, 267:19765-19768.
51. Martin S.L, Branciforte D., Keller D., Bain D.L. Trimeric structure for an essential protein in L1 retrotransposition. Proc. Natl. Acad. Sci. U.S.A. 2003, 100:13815-13820.
52. Januszyk K., Li P.W., Villareal V., Branciforte D., Wu H., Xie Y., Feigon J., Loo J.A., Martin S.L., Clubb R.T. Identification and solution structure of a highly conserved C-terminal domain within ORF1p required for retrotransposition of long interspersed nuclear element-1. J. Biol. Chem. 2007, 282:24893-24904.
53. Kolosha V.O., Martin S.L. High-affinity, non-sequence-specific RNA binding by the open reading frame 1 (ORF1) protein from long interspersed nuclear element 1 (LINE-1). J. Biol. Chem. 2003, 278:8112-8117.
54. Khazina E, Weichenrieder O. Non-LTR retrotransposons encode noncanonical RRM domains in their first open reading frame. Proc. Natl. Acad. Sci. U.S.A. 2009, 106:731-736.
55. Kulpa D.A., Moran J.V. Cis-preferential LINE-1 reverse transcriptase activity in ribonucleoprotein particles. Nat. Struct. Mol. Biol. 2006, 13:655-660.
56. Hohjoh H., Singer M.F. Cytoplasmic ribonucleoprotein complexes containing human LINE-1 protein and RNA. EMBO J. 1996, 15:630-639.
57. Hohjoh H., Singer M.F. Sequence-specific single-strand RNA binding protein encoded by the human LINE-1 retrotransposon. EMBO J. 1997, 16:6034-6043.
58. Wei W., Gilbert N., Ooi S.L., Lawler J.F., Ostertag E.M., Kazazian H.H., Boeke J.D., Moran J.V. Human L1 retrotransposition: cis preference versus trans complementation. Mol. Cell. Biol. 2001, 21:1429-1439.
59. Kulpa D.A., Moran J.V. Ribonucleoprotein particle formation is necessary but not sufficient for LINE-1 retrotransposition. Hum. Mol. Genet. 2005, 14:3237-3248.
60. Martin S.L., Li J., Weisz J.A. Deletion analysis defines distinct functional domains for protein-protein and nucleic acid interactions in the ORF1 protein of mouse LINE-1. J. Mol. Biol. 2000, 304:11-20.
61. Martin S.L., Bushman F.D. Nucleic acid chaperone activity of the ORF1 protein from the mouse LINE-1 retrotransposon. Mol. Cell. Biol. 2001, 21:467-475.
62. Feng Q., Moran J.V., Kazazian H.H., Boeke J.D. Human L1 retrotransposon encodes a conserved endonuclease required for retrotransposition. Cell 1996, 87:905-916.
63. Mathias S.L., Scott A.F., Kazazian H.H., Boeke J.D., Gabriel A. Reverse transcriptase encoded by a human transposable element. Science 1991, 254:1808-1810.
64. Goodier J.L., Mandal P.K., Zhang L., Kazazian H.H. Discrete subcellular partitioning of human retrotransposon RNAs despite a common mechanism of genome insertion. Hum. Mol. Genet. 2010, 19:1712-1725.
65. Wallace N., Wagstaff B.J., Deininger P.L., Roy-Engel A.M. LINE-1 ORF1 protein enhances Alu SINE retrotransposition. Gene 2008, 419:1-6.
66. Huda A., Marino-Ramirez L., Jordan I.K. Epigenetic histone modifications of human transposable elements: genome defense versus exaptation. Mob. DNA 2010, 1:2.
67. Huda A., Marino-Ramirez L., Landsman D., Jordan I.K. Repetitive DNA elements, nucleosome binding and human gene expression. Gene 2009, 436:12-22.
68. Nur I, Pascale E., Furano A.V. The left end of rat L1 (L1Rn, long interspersed repeated) DNA which is a CpG island can function as a promoter. Nucleic Acids Res. 1988, 16:9233-9251.
69. Goyal R., Reinhardt R., Jeltsch A. Accuracy of DNA methylation pattern preservation by the Dnmt1 methyltransferase. Nucleic Acids Res. 2006, 34:1182-1188.
70. Brown K.D., Robertson K.D. DNMT1 knockout delivers a strong blow to genome stability and cell viability. Nat. Genet. 2007, 39:289-290.
71. Esteve P.O., Chin H.G., Benner J., Feehery G.R., Samaranayake M., Horwitz G.A., Jacobsen S.E., Pradhan S. Regulation of DNMT1 stability through SET7-mediated lysine methylation in mammalian cells. Proc. Natl. Acad. Sci. U.S.A. 2009, 106:5076-5081.
72. Kato Y., Kaneda M., Hata K., Kumaki K., Hisano M., Kohara Y., Okano M., Li E., Nozaki M., Sasaki H. Role of the Dnmt3 family in de novo methylation of imprinted and repetitive sequences during male germ cell development in the mouse. Hum. Mol. Genet. 2007, 16:2272-2280.
73. Gowher H., Liebert K., Hermann A., Xu G., Jeltsch A. Mechanism of stimulation of catalytic activity of Dnmt3A and Dnmt3B DNA-(cytosine-C5)-methyltransferases by Dnmt3L. J. Biol. Chem. 2005, 280:13341-13348.
74. Liang G., Chan M.F., Tomigahara Y., Tsai Y.C., Gonzales F.A., Li E., Laird P.W., Jones P.A. Cooperativity between DNA methyltransferases in the maintenance methylation of repetitive elements. Mol. Cell. Biol. 2002, 22:480-491.
75. Glass J.L., Fazzari M.J., Ferguson-Smith A.C., Greally J.M. CG dinucleotide periodicities recognized by the Dnmt3a-Dnmt3L complex are distinctive at retroelements and imprinted domains. Mamm. Genome 2009, 20:633-643.
76. Jia D., Jurkowska R.Z., Zhang X., Jeltsch A., Cheng X. Structure of Dnmt3a bound to Dnmt3L suggests a model for de novo DNA methylation. Nature 2007, 449:248-251.
77. Zilberman D., Gehring M., Tran R.K., Ballinger T., Henikoff S. Genome-wide analysis of Arabidopsis thaliana DNA methylation uncovers an interdependence between methylation and transcription. Nat. Genet. 2007, 39:61-69.
78. Gendrel A.V., Colot V. Arabidopsis epigenetics: when RNA meets chromatin. Curr. Opin. Plant Biol. 2005, 8:142-147.
79. Ross J.P., Suetake I., Tajima S., Molloy P.L. Recombinant mammalian DNA methyltransferase activity on model transcriptional gene silencing short RNA:DNA heteroduplex substrates. Biochem. J. 2010, 432:323-332.
80. Ooi S.K., Qiu C., Bernstein E., Li K., Jia D., Yang Z., Erdjument-Bromage H., Tempst P., Lin S.P., Allis C.D., Cheng X., Bestor T.H. DNMT3L connects unmethylated lysine 4 of histone H3 to de novo methylation of DNA. Nature 2007, 448:714-717.
81. Hu J.L., Zhou B.O., Zhang R.R., Zhang K.L., Zhou J.Q., Xu G.L. The N-terminus of histone H3 is required for de novo DNA methylation in chromatin. Proc. Natl. Acad. Sci. U.S.A. 2009, 106:22187-22192.
82. Garcia-Perez J.L., Morell M., Scheys J.O., Kulpa D.A., Morell S., Carter C.C., Hammer G.D., Collins K.L., O'Shea K.S., Menendez P., Moran J.V. Epigenetic silencing of engineered L1 retrotransposition events in human embryonic carcinoma cells. Nature 2010, 466:769-773.
83. Chew Y.C., West J.T., Kratzer S.J., Ilvarsonn A.M., Eissenberg J.C., Dave B.J., Klinkebiel D., Christman J.K., Zempleni J. Biotinylation of histones represses transposable elements in human and mouse cells and cell lines and in Drosophila melanogaster. J. Nutr. 2008, 138:2316-2322.
84. Zempleni J., Chew Y.C., Bao B., Pestinger V., Wijeratne S.S. Repression of transposable elements by histone biotinylation. J. Nutr. 2009, 139:2389-2392.
85. Brunmeir R., Lagger S., Simboeck E., Sawicka A., Egger G., Hagelkruys A., Zhang Y., Matthias P., Miller W.J., Seiser C. Epigenetic regulation of a murine retrotransposon by a dual histone modification mark. PLoS Genet. 2010, 6:e1000927.
86. Questa J.I., Walbot V., Casati P. Mutator transposon activation after UV-B involves chromatin remodeling. Epigenetics 2010, 5:352-363.
87. Sridhar V.V., Kapoor A., Zhang K., Zhu J., Zhou T., Hasegawa P.M., Bressan R.A., Zhu J.K. Control of DNA methylation and heterochromatic silencing by histone H2B deubiquitination. Nature 2007, 447:735-738.
88. Aravin A.A., Naumova N.M., Tulin A.V., Vagin V.V., Rozovsky Y.M., Gvozdev V.A. Double-stranded RNA-mediated silencing of genomic tandem repeats and transposable elements in the D. melanogaster germline. Curr. Biol. 2001, 11:1017-1027.
89. Sarot E., Payen-Groschene G., Bucheton A., Pelisson A. Evidence for a piwi-dependent RNA silencing of the gypsy endogenous retrovirus by the Drosophila melanogaster flamenco gene. Genetics 2004, 166:1313-1321.
90. Aravin A.A., Lagos-Quintana M., Yalcin A., Zavolan M., Marks D., Snyder B., Gaasterland T., Meyer J., Tuschl T. The small RNA profile during Drosophila melanogaster development. Dev. Cell 2003, 5:337-350.
91. Aravin A., Gaidatzis D., Pfeffer S., Lagos-Quintana M., Landgraf P., Iovino N., Morris P., Brownstein M.J., Kuramochi-Miyagawa S., Nakano T., Chien M., Russo J.J., Ju J., Sheridan R., Sander C., Zavolan M., Tuschl T. A novel class of small RNAs bind to MILI protein in mouse testes. Nature 2006, 442:203-207.
92. Girard A., Sachidanandam R., Hannon G.J., Carmell M.A. A germline-specific class of small RNAs binds mammalian Piwi proteins. Nature 2006, 442:199-202.
93. Grivna S.T., Beyret E., Wang Z., Lin H. A novel class of small RNAs in mouse spermatogenic cells. Genes Dev. 2006, 20:1709-1714.
94. Lau N.C., Seto A.G., Kim J., Kuramochi-Miyagawa S., Nakano T., Bartel D.P., Kingston R.E. Characterization of the piRNA complex from rat testes. Science 2006, 313:363-367.
95. Vagin V.V., Sigova A., Li C., Seitz H., Gvozdev V., Zamore P.D. A distinct small RNA pathway silences selfish genetic elements in the germline. Science 2006, 313:320-324.
96. Brennecke J., Aravin A.A., Stark A., Dus M., Kellis M., Sachidanandam R., Hannon G.J. Discrete small RNA-generating loci as master regulators of transposon activity in Drosophila. Cell 2007, 128:1089-1103.
97. Malone C.D., Brennecke J., Dus M., Stark A., McCombie W.R., Sachidanandam R., Hannon G.J. Specialized piRNA pathways act in germline and somatic tissues of the Drosophila ovary. Cell 2009, 137:522-535.
98. Li C., Vagin V.V., Lee S., Xu J., Ma S., Xi H., Seitz H., Horwich M.D., Syrzycka M., Honda B.M., Kittler E.L., Zapp M.L., Klattenhoff C., Schulz N., Theurkauf W.E., Weng Z., Zamore P.D. Collapse of germline piRNAs in the absence of Argonaute3 reveals somatic piRNAs in flies. Cell 2009, 137:509-521.
99. Saito K., Ishizu H., Komai M., Kotani H., Kawamura Y., Nishida K.M., Siomi H., Siomi M.C. Roles for the Yb body components Armitage and Yb in primary piRNA biogenesis in Drosophila. Genes Dev. 2010, 24:2493-2498.
100. Haase A.D., Fenoglio S., Muerdter F., Guzzardo P.M., Czech B., Pappin D.J., Chen C., Gordon A., Hannon G.J. Probing the initiation and effector phases of the somatic piRNA pathway in Drosophila. Genes Dev. 2010, 24:2499-2504.
101. Olivieri D., Sykora M.M., Sachidanandam R., Mechtler K., Brennecke J. An in vivo RNAi assay identifies major genetic and cellular requirements for primary piRNA biogenesis in Drosophila. EMBO J. 2010, 29:3301-3317.
102. Qi H., Watanabe T., Ku H.Y., Liu N., Zhong M., Lin H. The Yb body, a major site for piRNA biogenesis and a gateway for Piwi expression and transport to the nucleus in somatic cells. J. Biol. Chem. 2010, 286:3789-3797.
103. Pane A, Wehr K., Schupbach T. Zucchini and squash encode two putative nucleases required for rasiRNA production in the Drosophila germline. Dev. Cell 2007, 12:851-862.
104. Szakmary A., Reedy M., Qi H., Lin H. The Yb protein defines a novel organelle and regulates male germline stem cell self-renewal in Drosophila melanogaster. J. Cell Biol. 2009, 185:613-627.
105. Thomson T., Liu N., Arkov A., Lehmann R., Lasko P. Isolation of new polar granule components in Drosophila reveals P body and ER associated proteins. Mech. Dev. 2008, 125:865-873.
106. Lau N.C., Robine N., Martin R., Chung W.J., Niki Y., Berezikov E., Lai E.C. Abundant primary piRNAs, endo-siRNAs, and microRNAs in a Drosophila ovary cell line. Genome Res. 2009, 19:1776-1785.
107. Brennecke J, Malone C.D., Aravin A.A., Sachidanandam R., Stark A., Hannon G.J. An epigenetic role for maternally inherited piRNAs in transposon silencing. Science 2008, 322:1387-1392.
108. Lim A.K., Tao L., Kai T. piRNAs mediate posttranscriptional retroelement silencing and localization to pi-bodies in the Drosophila germline. J. Cell Biol. 2009, 186:333-342.
109. Rouget C., Papin C., Boureux A., Meunier A.C., Franco B., Robine N., Lai E.C., Pelisson A., Simonelig M. Maternal mRNA deadenylation and decay by the piRNA pathway in the early Drosophila embryo. Nature 2010, 467:1128-1132.
110. Trelogan S.A., Martin S.L. Tightly regulated, developmentally specific expression of the first open reading frame from LINE-1 during mouse embryogenesis. Proc. Natl. Acad. Sci. U.S.A. 1995, 92:1520-1524.
111. Aravin A.A, van der Heijden G.W., Castaneda J., Vagin V.V., Hannon G.J., Bortvin A. Cytoplasmic compartmentalization of the fetal piRNA pathway in mice. PLoS Genet. 2009, 5:e1000764.
112. Soper S.F., van der Heijden G.W., Hardiman T.C., Goodheart M., Martin S.L., de Boer P., Bortvin A. Mouse maelstrom, a component of nuage, is essential for spermatogenesis and transposon repression in meiosis. Dev. Cell 2008, 15:285-297.
113. Ma L, Buchold G.M., Greenbaum M.P., Roy A., Burns K.H., Zhu H., Han D.Y., Harris R.A., Coarfa C., Gunaratne P.H., Yan W., Matzuk M.M. GASZ is essential for male meiosis and suppression of retrotransposon expression in the male germline. PLoS Genet. 2009, 5:e1000635.
114. Shoji M., Tanaka T., Hosokawa M., Reuter M., Stark A., Kato Y., Kondoh G., Okawa K., Chujo T., Suzuki T., Hata K., Martin S.L., Noce T., Kuramochi-Miyagawa S., Nakano T., Sasaki H., Pillai R.S., Nakatsuji N., Chuma S. The TDRD9-MIWI2 complex is essential for piRNA-mediated retrotransposon silencing in the mouse male germline. Dev. Cell 2009, 17:775-787.
115. Kuramochi-Miyagawa S., Kimura T., Yomogida K., Kuroiwa A., Tadokoro Y., Fujita Y., Sato M., Matsuda Y., Nakano T. Two mouse piwi-related genes: miwi and mili. Mech. Dev. 2001, 108:121-133.
116. Frost R.J., Hamra F.K., Richardson J.A., Qi X., Bassel-Duby R., Olson E.N. MOV10L1 is necessary for protection of spermatocytes against retrotransposons by Piwi-interacting RNAs. Proc. Natl. Acad. Sci. U.S.A. 2010, 107:11847-11852.
117. Zheng K., Xiol J., Reuter M., Eckardt S., Leu N.A., McLaughlin K.J., Stark A., Sachidanandam R., Pillai R.S., Wang P.J. Mouse MOV10L1 associates with Piwi proteins and is an essential component of the Piwi-interacting RNA (piRNA) pathway. Proc. Natl. Acad. Sci. U.S.A. 2010, 107:11841-11846.
118. Yan W., Rajkovic A., Viveiros M.M., Burns K.H., Eppig J.J., Matzuk M.M. Identification of Gasz, an evolutionarily conserved gene expressed exclusively in germ cells and encoding a protein with four ankyrin repeats, a sterile-alpha motif, and a basic leucine zipper. Mol. Endocrinol. 2002, 16:1168-1184.
119. Reuter M, Chuma S., Tanaka T., Franz T., Stark A., Pillai R.S. Loss of the Mili-interacting Tudor domain-containing protein-1 activates transposons and alters the Mili-associated small RNA profile. Nat. Struct. Mol. Biol. 2009, 16:639-646.
120. Wang J., Saxe J.P., Tanaka T., Chuma S., Lin H. Mili interacts with tudor domain-containing protein 1 in regulating spermatogenesis. Curr. Biol. 2009, 19:640-644.
121. Halic M., Moazed D. Dicer-independent primal RNAs trigger RNAi and heterochromatin formation. Cell 2010, 140:504-516.
122. Kuramochi-Miyagawa S., Kimura T., Ijiri T.W., Isobe T., Asada N., Fujita Y., Ikawa M., Iwai N., Okabe M., Deng W., Lin H., Matsuda Y., Nakano T. Mili, a mammalian member of piwi family gene, is essential for spermatogenesis. Development 2004, 131:839-849.
123. Carmell M.A, Girard A., van de Kant H.J., Bourc'his D., Bestor T.H., de Rooij D.G., Hannon G.J. MIWI2 is essential for spermatogenesis and repression of transposons in the mouse male germline. Dev. Cell 2007, 12:503-514.
124. Ma J.B., Yuan Y.R., Meister G., Pei Y., Tuschl T., Patel D.J. Structural basis for 5'-end-specific recognition of guide RNA by the A. fulgidus Piwi protein. Nature 2005, 434:666-670.
125. Parker J.S, Roe S.M., Barford D. Structural insights into mRNA recognition from a PIWI domain-siRNA guide complex. Nature 2005, 434:663-666.
126. Teixeira D., Parker R. Analysis of P-body assembly in Saccharomyces cerevisiae. Mol. Biol. Cell 2007, 18:2274-2287.
127. Parker R., Sheth U. P bodies and the control of mRNA translation and degradation. Mol. Cell 2007, 25:635-646.
128. Wassenegger M. RNA-directed DNA methylation. Plant Mol. Biol. 2000, 43:203-220.
129. Mathieu O., Bender J. RNA-directed DNA methylation. J. Cell Sci. 2004, 117:4881-4888.
130. Gao Z., Liu H.L., Daxinger L., Pontes O., He X., Qian W., Lin H., Xie M., Lorkovic Z.J., Zhang S., Miki D., Zhan X., Pontier D., Lagrange T., Jin H., Matzke A.J., Matzke M., Pikaard C.S., Zhu J.K. An RNA polymerase II- and AGO4-associated protein acts in RNA-directed DNA methylation. Nature 2010, 465:106-109.
131. Matzke M., Kanno T., Huettel B., Daxinger L., Matzke A.J. Targets of RNA-directed DNA methylation. Curr. Opin. Plant Biol. 2007, 10:512-519.
132. Kuramochi-Miyagawa S., Watanabe T., Gotoh K., Takamatsu K., Chuma S., Kojima-Kita K., Shiromoto Y., Asada N., Toyoda A., Fujiyama A., Totoki Y., Shibata T., Kimura T., Nakatsuji N., Noce T., Sasaki H., Nakano T. MVH in piRNA processing and gene silencing of retrotransposons. Genes Dev. 2010, 24:887-892.
133. Tanaka S.S., Toyooka Y., Akasu R., Katoh-Fukui Y., Nakahara Y., Suzuki R., Yokoyama M., Noce T. The mouse homolog of Drosophila Vasa is required for the development of male germ cells. Genes Dev. 2000, 14:841-853.
134. Vagin V.V., Wohlschlegel J., Qu J., Jonsson Z., Huang X., Chuma S., Girard A., Sachidanandam R., Hannon G.J., Aravin A.A. Proteomic analysis of murine Piwi proteins reveals a role for arginine methylation in specifying interaction with Tudor family members. Genes Dev. 2009, 23:1749-1762.
135. Chen C., Jin J., James D.A., Adams-Cioaba M.A., Park J.G., Guo Y., Tenaglia E., Xu C., Gish G., Min J., Pawson T. Mouse Piwi interactome identifies binding mechanism of Tdrkh Tudor domain to arginine methylated Miwi. Proc. Natl. Acad. Sci. U.S.A. 2009, 106:20336-20341.
136. Biessmann H., Valgeirsdottir K., Lofsky A., Chin C., Ginther B., Levis R.W., Pardue M.L. HeT-A, a transposable element specifically involved in "healing" broken chromosome ends in Drosophila melanogaster. Mol. Cell. Biol. 1992, 12:3910-3918.
137. Levis R.W, Ganesan R., Houtchens K., Tolar L.A., Sheen F.M. Transposons in place of telomeric repeats at a Drosophila telomere. Cell 1993, 75:1083-1093.
138. Fugmann S.D. The origins of the Rag genes-from transposition to V(D)J recombination. Semin. Immunol. 2010, 22:10-16.
139. Chalker D.L. Transposons that clean up after themselves. Genome Biol. 2009, 10:224.
140. Finnegan D.J. Genome dynamics: transposition and the single cell. Curr. Biol. 2009, 19:R555-558.
141. Nowacki M., Higgins B.P., Maquilan G.M., Swart E.C., Doak T.G., Landweber L.F. A functional role for transposases in a large eukaryotic genome. Science 2009, 324:935-938.
142. McVicker G., Green P. Genomic signatures of germline gene expression. Genome Res. 2010, 20:1503-1511.
143. Kvikstad E.M., Makova K.D. The (r)evolution of SINE versus LINE distributions in primate genomes: sex chromosomes are important. Genome Res. 2010, 20:600-613.
144. Beraldi R., Pittoggi C., Sciamanna I., Mattei E., Spadafora C. Expression of LINE-1 retroposons is essential for murine preimplantation development. Mol. Reprod. Dev. 2006, 73:279-287.
145. Sciamanna I., Barberi L., Martire A., Pittoggi C., Beraldi R., Giordano R., Magnano A.R., Hogdson C., Spadafora C. Sperm endogenous reverse transcriptase as mediator of new genetic information. Biochem. Biophys. Res. Commun. 2003, 312:1039-1046.
146. Pittoggi C., Sciamanna I., Mattei E., Beraldi R., Lobascio A.M., Mai A., Quaglia M.G., Lorenzini R., Spadafora C. Role of endogenous reverse transcriptase in murine early embryo development. Mol. Reprod. Dev. 2003, 66:225-236.
147. Dupuy A.J. Current applications of transposons in mouse genetics. Methods Enzymol. 2010, 477:53-70.
148. Rubin G.M., Spradling A.C. Genetic transformation of Drosophila with transposable element vectors. Science 1982, 218:348-353.
149. Spradling A.C., Rubin G.M. Transposition of cloned P elements into Drosophila germ line chromosomes. Science 1982, 218:341-347.
150. Spradling A.C., Stern D., Beaton A., Rhem E.J., Laverty T., Mozden N., Misra S., Rubin G.M. The Berkeley Drosophila Genome Project gene disruption project: Single P-element insertions mutating 25% of vital Drosophila genes. Genetics 1999, 153:135-177.
151. Lin H., Spradling A.C. A novel group of pumilio mutations affects the asymmetric division of germline stem cells in the Drosophila ovary. Development 1997, 124:2463-2476.
152. Ivics Z., Hackett P.B., Plasterk R.H., Izsvak Z. Molecular reconstruction of Sleeping Beauty, a Tc1-like transposon from fish, and its transposition in human cells. Cell 1997, 91:501-510.
153. Dupuy A.J, Akagi K., Largaespada D.A., Copeland N.G., Jenkins N.A. Mammalian mutagenesis using a highly mobile somatic Sleeping Beauty transposon system. Nature 2005, 436:221-226.
154. Dupuy A.J., Rogers L.M., Kim J., Nannapaneni K., Starr T.K., Liu P., Largaespada D.A., Scheetz T.E., Jenkins N.A., Copeland N.G. A modified sleeping beauty transposon system that can be used to model a wide variety of human cancers in mice. Cancer Res. 2009, 69:8150-8156.
155. Largaespada D.A. Transposon-mediated mutagenesis of somatic cells in the mouse for cancer gene identification. Methods 2009, 49:282-286.
156. Kitada K., Keng V.W., Takeda J., Horie K. Generating mutant rats using the Sleeping Beauty transposon system. Methods 2009, 49:236-242.
157. Liu L., Liu H., Visner G., Fletcher B.S. Sleeping Beauty-mediated eNOS gene therapy attenuates monocrotaline-induced pulmonary hypertension in rats. FASEB J. 2006, 20:2594-2596.
158. Chuma S., Hosokawa M., Kitamura K., Kasai S., Fujioka M., Hiyoshi M., Takamune K., Noce T., Nakatsuji N. Tdrd1/Mtr-1, a tudor-related gene, is essential for male germ-cell differentiation and nuage/germinal granule formation in mice. Proc. Natl. Acad. Sci. U.S.A. 2006, 103:15894-15899.
159. Watanabe T, Totoki Y., Toyoda A., Kaneda M., Kuramochi-Miyagawa S., Obata Y., Chiba H., Kohara Y., Kono T., Nakano T., Surani M.A., Sakaki Y., Sasaki H. Endogenous siRNAs from naturally formed dsRNAs regulate transcripts in mouse oocytes. Nature 2008, 453:539-543.
160. Tam O.H., Aravin A.A., Stein P., Girard A., Murchison E.P., Cheloufi S., Hodges E., Anger M., Sachidanandam R., Schultz R.M., Hannon G.J. Pseudogene-derived small interfering RNAs regulate gene expression in mouse oocytes. Nature 2008, 453:534-538.