Targeted gene silencing in mouse germ cells by insertion of a homologous DNA into a piRNA generating locus

Genome Research

Volumn 23, Issue 2, 2013, Pages 292-299

  Yamamoto, Yasuhiro ^a,b   Watanabe, Toshiaki ^c   Hoki, Yuko ^a   Shirane, Kenjiro ^a   Li, Yufeng ^a   Ichiiyanagi, Kenji ^a   Kuramochi Miyagawa, Satomi ^d   Toyoda, Atsushi ^b   Fujiyama, Asao ^b   Oginuma, Masayuki ^b   Suzuki, Hitomi ^b   Sado, Takashi ^a   Nakano, Toru ^b   Sasaki, Hiroyuki ^a  

^a KYUSHU UNIVERSITY   (Japan)

^b NATIONAL INSTITUTE OF GENETICS   (Japan)

^c YALE UNIVERSITY SCHOOL OF MEDICINE   (United States)

^d OSAKA UNIVERSITY   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

DNA FRAGMENT; PIWI INTERACTING RNA;

ANIMAL CELL; ANIMAL EXPERIMENT; ARTICLE; BIOGENESIS; CONTROLLED STUDY; DOWN REGULATION; EMBRYO; GENE INSERTION; GENE LOCUS; GENE REPRESSION; GENE SILENCING; GENE TARGETING; MALE; MOUSE; NONHUMAN; PRIORITY JOURNAL; RETROPOSON; RNA PROCESSING; RNA SEQUENCE; SPERMATOCYTE;

ANIMALS; DNA; GENE EXPRESSION REGULATION; GENE SILENCING; GENE TARGETING; GENES, REPORTER; GENETIC LOCI; GERM CELLS; MALE; MICE; MICE, TRANSGENIC; RNA PROCESSING, POST-TRANSCRIPTIONAL; RNA, SMALL INTERFERING;

EID: 84873385344     PISSN: 10889051     EISSN: 15495469     Source Type: Journal    
DOI: 10.1101/gr.137224.112     Document Type: Article

References (48)

1. Aravin A, Gaidatzis D, Pfeffer S, Lagos-Quintana M, Landgraf P, Iovino N, Morris P, Brownstein MJ, Kuramochi-Miyagawa S, Nakano T, et al. 2006. A novel class of small RNAs bind to MILI protein in mouse testes. Nature 442: 203-207.
2. Aravin AA, Hannon GJ, Brennecke J. 2007a. The Piwi-piRNA pathway provides an adaptive defense in the transposon arms race. Science 318: 761-764.
3. Aravin AA, Sachidanandam R, Girard A, Fejes-Toth K, Hannon GJ. 2007b. Developmentally regulated piRNA clusters implicateMILI in transposon control. Science 316: 744-747.
4. Aravin AA, Sachidanandam R, Bourc'his D, Schaefer C, Pezic D, Toth KF, Bestor T, Hannon GJ. 2008. A piRNA pathway primed by individual transposons is linked to de novo DNA methylation in mice. Mol Cell 31: 785-799.
5. Aravin AA, van der HeijdenGW, Castaneda J, Vagin VV, Hannon GJ, Bortvin A. 2009. Cytoplasmic compartmentalization of the fetal piRNA pathway in mice. PLoS Genet 5: e1000764.
6. Assis R, Kondrashov AS. 2009. Rapid repetitive element-mediated expansion of piRNA clusters in mammalian evolution. Proc Natl Acad Sci 106: 7079-7082.
7. Brennecke J, Aravin AA, Stark A, Dus M, Kellis M, Sachidanandam R, Hannon GJ. 2007. Discrete small RNA-generating loci as master regulators of transposon activity in Drosophila. Cell 128: 1089-1103.
8. Carmell MA, Girard A, van de Kant HJ, Bourc'his D, Bestor TH, de Rooij DG, Hannon GJ. 2007. MIWI2 is essential for spermatogenesis and repression of transposons in the mousemale germline. Dev Cell 12: 503-514.
9. Chuma S, Hosokawa M, Tanaka T, Nakatsuji N. 2009. Ultrastructural characterization of spermatogenesis and its evolutionary conservation in the germline: Germinal granules in mammals. Mol Cell Endocrinol 306: 17-23.
10. De Fazio S, Bartonicek N, Di Giacomo M, Abreu-Goodger C, Sankar A, Funaya C, Antony C, Moreira PN, Enright AJ, O'Carroll D. 2011. The endonuclease activity of Mili fuels piRNA amplification that silences LINE1 elements. Nature 480: 259-263.
11. Deng W, Lin H. 2002. miwi, a murine homolog of piwi, encodes a cytoplasmic protein essential for spermatogenesis. Dev Cell 2: 819-830.
12. Fire A, Xu S, Montgomery MK, Kostas SA, Driver SE,Mello CC. 1998. Potent and specific genetic interference by double-stranded RNA in Caenorhabditis elegans. Nature 391: 806-811.
13. Girard A, Hannon GJ. 2008. Conserved themes in small-RNA-mediated transposon control. Trends Cell Biol 18: 136-148.
14. Girard A, Sachidanandam R, Hannon GJ, Carmell MA. 2006. A germlinespecific class of small RNAs binds mammalian Piwi proteins. Nature 442: 199-202.
15. Grivna ST, Beyret E, Wang Z, Lin H. 2006a. A novel class of small RNAs in mouse spermatogenic cells. Genes Dev 20: 1709-1714.
16. Grivna ST, Pyhtila B, Lin H. 2006b. MIWI associates with translational machinery and PIWI-interacting RNAs (piRNAs) in regulating spermatogenesis. Proc Natl Acad Sci 103: 13415-13420.
17. Gunawardane LS, Saito K, Nishida KM, Miyoshi K, Kawamura Y, Nagami T, Siomi H, Siomi MC. 2007. A slicer-mediated mechanism for repeatassociated siRNA 59 end formation in Drosophila. Science 315: 1587-1590.
18. Han JS, Szak ST, Boeke JD. 2004. Transcriptional disruption by the L1 retrotransposon and implications for mammalian transcriptomes. Nature 429: 268-274.
19. Hirasawa R, Chiba H, Kaneda M, Tajima S, Li E, Jaenisch R, Sasaki H. 2008. Maternal and zygotic Dnmt1 are necessary and sufficient for the maintenance of DNA methylation imprints during preimplantation development. Genes Dev 22: 1607-1616.
20. Jiang H, Wong WH. 2008. SeqMap: Mapping massive amount of oligonucleotides to the genome. Bioinformatics 24: 2395-2396.
21. Kawamoto S, Niwa H, Tashiro F, Sano S, Kondoh G, Takeda J, Tabayashi K, Miyazaki J. 2000. A novel reporter mouse strain that expresses enhanced green fluorescent protein upon Cre-mediated recombination. FEBS Lett 470: 263-268.
22. Kawaoka S, Izumi N, Katsuma S, Tomari Y. 2011. 39 end formation of PIWIinteracting RNAs in vitro. Mol Cell 43: 1015-1022.
23. KazazianHHJr. 2004. Mobile elements: Drivers of genome evolution. Science 303: 1626-1632.
24. Khurana JS,Wang J, Xu J, Koppetsch BS, Thomson TC, Nowosielska A, Li C, Zamore PD, Weng Z, Theurkauf WE. 2011. Adaptation to P element transposon invasion in Drosophila melanogaster. Cell 147: 1551-1563.
25. Kim VN, Han J, Siomi MC. 2009. Biogenesis of small RNAs in animals. Nat Rev Mol Cell Biol 10: 126-139.
26. Klattenhoff C, Theurkauf W. 2008. Biogenesis and germline functions of piRNAs. Development 135: 3-9.
27. Kotaja N, Lin H, Parvinen M, Sassone-Corsi P. 2006. Interplay of PIWI/Argonaute protein MIWI and kinesin KIF17b in chromatoid bodies of male germ cells. J Cell Sci 119: 2819-2825.
28. Kuramochi-Miyagawa S, Kimura T, Yomogida K, Kuroiwa A, Tadokoro Y, Fujita Y, Sato M, Matsuda Y, Nakano T. 2001. Two mouse piwi-related genes: miwi and mili. Mech Dev 108: 121-133.
29. Kuramochi-Miyagawa S, Kimura T, Ijiri TW, Isobe T, Asada N, Fujita Y, Ikawa M, Iwai N, Okabe M, DengW, et al. 2004. Mili, a mammalian member of piwi family gene, is essential for spermatogenesis. Development 131: 839-849.
30. Kuramochi-Miyagawa S,Watanabe T, Gotoh K, Totoki Y, Toyoda A, Ikawa M, Asada N, Kojima K, Yamaguchi Y, Ijiri TW, et al. 2008. DNA methylation of retrotransposon genes is regulated by Piwi family members MILI and MIWI2 in murine fetal testes. Genes Dev 22: 908-917.
31. Lau NC, Seto AG, Kim J, Kuramochi-Miyagawa S, Nakano T, Bartel DP, Kingston RE. 2006. Characterization of the piRNA complex from rat testes. Science 313: 363-367.
32. Lim AK, Tao L, Kai T. 2009. piRNAs mediate posttranscriptional retroelement silencing and localization to pi-bodies in the Drosophila germline. J Cell Biol 186: 333-342.
33. Liu J, Valencia-Sanchez MA, Hannon GJ, Parker R. 2005. MicroRNAdependent localization of targeted mRNAs to mammalian P-bodies. Nat Cell Biol 7: 719-723.
34. Lund E, Sheets MD, Imboden SB, Dahlberg JE. 2011. Limiting Ago protein restricts RNAi and microRNA biogenesis during early development in Xenopus laevis. Genes Dev 25: 1121-1131.
35. Muerdter F, Olovnikov I, Molaro A, Rozhkov NV, Czech B, Gordon A, Hannon GJ, Aravin AA. 2011. Production of artificial piRNAs in flies and mice. RNA 18: 42-52.
36. Oginuma M, Hirata T, Saga Y. 2008. Identification of presomitic mesoderm (PSM)-specific Mesp1 enhancer and generation of a PSM-specific Mesp1/Mesp2-null mouse using BAC-based rescue technology. Mech Dev 125: 432-440.
37. Pillai RS, Chuma S. 2012. piRNAs and their involvement in male germline development in mice. Dev Growth Differ 54: 78-92.
38. Reuter M, Berninger P, Chuma S, Shah H, Hosokawa M, Funaya C, Antony C, Sachidanandam R, Pillai RS. 2011. Miwi catalysis is required for piRNA amplification-independent LINE1 transposon silencing. Nature 480: 264-267.
39. Siomi MC, Sato K, Pezic D, Aravin AA. 2011. PIWI-interacting small RNAs: The vanguard of genome defence. Nat Rev Mol Cell Biol 12: 246-258.
40. Suzuki A, Tsuda M, Saga Y. 2007. Functional redundancy among Nanos proteins and a distinct role of Nanos2 during male germ cell development. Development 134: 77-83.
41. Vagin VV, Sigova A, Li C, Seitz H, Gvozdev V, Zamore PD. 2006. A distinct small RNA pathway silences selfish genetic elements in the germline. Science 313: 320-324.
42. Wang YL, Liu W, Sun YJ, Kwon J, Setsuie R, Osaka H, Noda M, Aoki S, Yoshikawa Y, Wada K. 2006. Overexpression of ubiquitin carboxylterminal hydrolase L1 arrests spermatogenesis in transgenic mice. Mol Reprod Dev 73: 40-49.
43. Watanabe T, Takeda A, Tsukiyama T, Mise K, Okuno T, Sasaki H, Minami N, Imai H. 2006. 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 20: 1732-1743.
44. Watanabe T, Totoki Y, Sasaki H, Minami N, Imai H. 2007. Analysis of small RNA profiles during development. Methods Enzymol 427: 155-169.
45. Watanabe T, Tomizawa S, Mitsuya K, Totoki Y, Yamamoto Y, Kuramochi-Miyagawa S, Iida N, Hoki Y, Murphy PJ, Toyoda A, et al. 2011. Role for piRNAs and noncoding RNA in de novo DNA methylation of the imprinted mouse Rasgrf1 locus. Science 332: 848-852.
46. Waterston RH, Lindblad-Toh K, Birney E, Rogers J, Abril JF, Agarwal P, Agarwala R, Ainscough R, Alexandersson M, An P, et al. 2002. Initial sequencing and comparative analysis of the mouse genome. Nature 420: 520-562.
47. Xu M, You Y, Hunsicker P, Hori T, Small C, Griswold MD, Hecht NB. 2008. Mice deficient for a small cluster of Piwi-interacting RNAs implicate Piwi-interacting RNAs in transposon control. Biol Reprod 79: 51-57.
48. Zambrowicz BP, Imamoto A, Fiering S, Herzenberg LA, Kerr WG, Soriano P. 1997. Disruption of overlapping transcripts in the ROSA b geo 26 gene trap strain leads to widespread expression of b-galactosidase in mouse embryos and hematopoietic cells. Proc Natl Acad Sci 94: 3789-3794.