DNA methylation of retrotransposon genes is regulated by Piwi family members MILI and MIWI2 in murine fetal testes

Genes and Development

Volumn 22, Issue 7, 2008, Pages 908-917

  Kuramochi Miyagawa, Satomi ^a   Watanabe, Toshiaki ^b   Gotoh, Kengo ^a   Totoki, Yasushi ^c   Toyoda, Atsushi ^c   Ikawa, Masahito ^d   Asada, Noriko ^a   Kojima, Kanako ^a   Yamaguchi, Yuka ^a   Ijiri, Takashi W ^e   Hata, Kenichiro ^b   Li, En ^f   Matsuda, Yoichi ^e   Kimura, Tohru ^a   Okabe, Masaru ^d   Sakaki, Yoshiyuki ^c   Sasaki, Hiroyuki ^b   Nakano, Toru ^a,f  

^a OSAKA UNIVERSITY   (Japan)

^b NATIONAL INSTITUTE OF GENETICS   (Japan)

^c RIKEN YOKOHAMA INSTITUTE   (Japan)

^d OSAKA UNIVERSITY   (Japan)

^e HOKKAIDO UNIVERSITY   (Japan)

^f NOVARTIS INSTITUTES FOR BIOMEDICAL RESEARCH   (United States)

Author keywords

DNA methylation; piRNA; Piwi; Retrotransposon; Spermatogenesis

Indexed keywords

CELL DNA; PIWI PROTEIN; PROTEIN MILI; PROTEIN MIWI 2; UNCLASSIFIED DRUG;

ANIMAL CELL; ARTICLE; CONTROLLED STUDY; DNA METHYLATION; DROSOPHILA; FETUS CELL; FETUS DEVELOPMENT; GENE CONTROL; GENE EXPRESSION; GENE MUTATION; GENE REGULATORY NETWORK; GERM CELL; LONG INTERSPERSED REPEAT; MALE; MOUSE; NONHUMAN; NUCLEOTIDE SEQUENCE; NULL ALLELE; ONCOGENE; PRIORITY JOURNAL; PROTEIN INTERACTION; RETROPOSON; RNA ANALYSIS; TESTIS DEVELOPMENT; TRANSPOSON; WILD TYPE;

ANIMALS; BLOTTING, NORTHERN; CLUSTER ANALYSIS; CPG ISLANDS; DNA METHYLATION; FEMALE; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION, DEVELOPMENTAL; GENOTYPE; IMMUNOPRECIPITATION; MALE; MICE; MICE, KNOCKOUT; OLIGONUCLEOTIDE ARRAY SEQUENCE ANALYSIS; PROTEIN BINDING; PROTEINS; RETROELEMENTS; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; RNA, UNTRANSLATED; TESTIS;

INTRACISTERNAL A-PARTICLES; MURINAE;

EID: 41649116098     PISSN: 08909369     EISSN: 15495477     Source Type: Journal    
DOI: 10.1101/gad.1640708     Document Type: Article

References (35)

1. Aravin, A., Gaidatzis, D., Pfeffer, S., Lagos-Quintana, M., Landgraf, P., Iovino, N., Morris, P., Brownstein, M.J., 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, A.A., Sachidanandam, R., Girard, A., Fejes-Toth, K., and Hannon, G.J. 2007. Developmentally regulated piRNA clusters implicate MILI in transposon control. Science 316: 744-747.
3. Bellve, A.R., Cavicchia, J.C., Millette, C.F., O'Brien, D.A., Bhatnagar, Y.M., and Dym, M. 1977. Spermatogenic cells of the prepuberal mouse. Isolation and morphological characterization. J. Cell Biol. 74: 68-85.
4. Bourc'his, D. and Bestor, T.H. 2004. Meiotic catastrophe and retrotransposon reactivation in male germ cells lacking Dnmt3L. Nature 431: 96-99.
5. Brennecke, J., Aravin, A.A., Stark, A., Dus, M., Kellis, M., Sachidanandam, R., and Hannon, G.J. 2007. Discrete small RNA-generating loci as master regulators of transposon activity in Drosophila. Cell 128: 1089-1103.
6. Carmell, M.A., Girard, A., van de Kant, H.J., Bourc'his, D., Bestor, T.H., de Rooij, D.G., and Hannon, G.J. 2007. MIWI2 is essential for spermatogenesis and repression of transposons in the mouse male germline. Dev. Cell 12: 503-514.
7. Cox, D.N., Chao, A., Baker, J., Chang, L., Qiao, D., and Lin, H. 1998. A novel class of evolutionarily conserved genes defined by piwi are essential for stem cell self-renewal. Genes & Dev. 12: 3715-3727.
8. Girard, A., Sachidanandam, R., Hannon, G.J., and Carmell, M.A. 2006. A germline-specific class of small RNAs binds mammalian Piwi proteins. Nature 442: 199-202.
9. Grivna, S.T., Beyret, E., Wang, Z., and Lin, H. 2006. A novel class of small RNAs in mouse spermatogenic cells. Genes & Dev. 20: 1709-1714.
10. Gunawardane, L.S., Saito, K., Nishida, K.M., Miyoshi, K., Kawamura, Y., Nagami, T., Siomi, H., and Siomi, M.C. 2007. A slicer-mediated mechanism for repeat-associated siRNA 5′ end formation in Drosophila. Science 315: 1587-1590.
11. Hata, K., Kusumi, M., Yokomine, T., Li, E., and Sasaki, H. 2006. Meiotic and epigenetic aberrations in Dnmt3L-deficient male germ cells. Mol. Reprod. Dev. 73: 116-122.
12. Houwing, S., Kamminga, L.M., Berezikov, E., Cronembold, D., Girard, A., van den Elst, H., Filippov, D.V., Blaser, H., Raz, E., Moens, C.B., et al. 2007. A role for Piwi and piRNAs in germ cell maintenance and transposon silencing in zebrafish. Cell 129: 69-82.
13. Ishihara, H., Tanaka, I., Wan, H., Nojima, K., and Yoshida, K. 2004. Retrotransposition of limited deletion type of intracisternal A-particle elements in the myeloid leukemia Clls of C3H/He mice. J. Radiat. Res. (Tokyo) 45: 25-32.
14. Kalmykova, A.I., Klenov, M.S., and Gvozdev, V.A. 2005. Argonaute protein PIWI controls mobilization of retrotransposons in the Drosophila male germline. Nucleic Acids Res. 33: 2052-2059.
15. Kato, Y., Kaneda, M., Hata, K., Kumaki, K., Hisano, M., Kohara, Y., Okano, M., Li, E., Nozaki, M., and Sasaki, H. 2007. 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. 16: 2272-2280.
16. Kuramochi-Miyagawa, S., Kimura, T., Yomogida, K., Kuroiwa, A., Tadokoro, Y., Fujita, Y., Sato, M., Matsuda, Y., and Nakano, T. 2001. Two mouse piwi-related genes: miwi and mili. Mech. Dev. 108: 121-133.
17. Kuramochi-Miyagawa, S., Kimura, T., Ijiri, T.W., Isobe, T., Asada, N., Fujita, Y., Ikawa, M., Iwai, N., Okabe, M., Deng, W., et al. 2004. Mili, a mammalian member of piwi family gene, is essential for spermatogenesis. Development 131: 839-849.
18. Lander, E.S., Linton, L.M., Birren, B., Nusbaum, C., Zody, M.C., Baldwin, J., Devon, K., Dewar, K., Doyle, M., FitzHugh, W., et al. 2001. Initial sequencing and analysis of the human genome. Nature 409: 860-921.
19. Lane, N., Dean, W., Erhardt, S., Hajkova, P., Surani, A., Walter, J., and Reik, W. 2003. Resistance of IAPs to methylation reprogramming may provide a mechanism for epigenetic inheritance in the mouse. Genesis 35: 88-93.
20. Lau, N.C., Seto, A.G., Kim, J., Kuramochi-Miyagawa, S., Nakano, T., Bartel, D.P., and Kingston, R.E. 2006. Characterization of the piRNA complex from rat testes. Science 313: 363-367.
21. Meistrich, M.L. 1993. Cell and molecular biology of the testis. Oxford University Press, New York.
22. Moussian, B., Schoof, H., Haecker, A., Jurgens, G., and Laux, T. 1998. Role of the ZWILLE gene in the regulation of central shoot meristem cell fate during Arabidopsis embryogenesis. EMBO J. 17: 1799-1809.
23. Nolan, T., Braccini, L., Azzalin, G., De Toni, A., Macino, G., and Cogoni, C. 2005. The post-transcriptional gene silencing machinery functions independently of DNA methylation to repress a LINE1-like retrotransposon in Neurospora crassa. Nucleic Acids Res. 33: 1564-1573.
24. Peters, L. and Meister, G. 2007. Argonaute proteins: Mediators of RNA silencing. Mol. Cell 26: 611-623.
25. Reddien, P.W., Oviedo, N.J., Jennings, J.R., Jenkin, J.C., and Sanchez Alvarado, A. 2005. SMEDWI-2 is a PIWI-like protein that regulates planarian stem cells. Science 310: 1327-1330.
26. Saito, K., Nishida, K.M., Mori, T., Kawamura, Y., Miyoshi, K., Nagami, T., Siomi, H., and Siomi, M.C. 2006. Specific association of Piwi with rasiRNAs derived from retrotransposon and heterochromatic regions in the Drosophila genome. Genes & Dev. 20: 2214-2222.
27. Sakai, Y., Suetake, I., Shinozaki, F., Yamashina, S., and Tajima, S. 2004. Co-expression of de novo DNA methyltransferases Dnmt3a2 and Dnmt3L in gonocytes of mouse embryos. Brain Res. Gene Expr. Patterns 5: 231-237.
28. Sarot, E., Payen-Groschene, G., Bucheton, A., and Pelisson, A. 2004. Evidence for a piwi-dependent RNA silencing of the gypsy endogenous retrovirus by the Drosophila melanogaster flamenco gene. Genetics 166: 1313-1321.
29. Shi, H., Ullu, E., and Tschudi, C. 2004. Function of the Trypanosome Argonaute 1 protein in RNA interference requires the N-terminal RGG domain and arginine 735 in the Piwi domain. J. Biol. Chem. 279: 49889-49893.
30. Tanaka, S.S., Toyooka, Y., Akasu, R., Katoh-Fukui, Y., Nakahara, Y., Suzuki, R., Yokoyama, M., and Noce, T. 2000. The mouse homolog of Drosophila Vasa is required for the development of male germ cells. Genes & Dev. 14: 841-853.
31. Walsh, C.P., Chaillet, J.R., and Bestor, T.H. 1998. Transcription of IAP endogenous retroviruses is constrained by cytosine methylation. Nat. Genet. 20: 116-117.
32. Watanabe, T., Takeda, A., Tsukiyama, T., Mise, K., Okuno, T., Sasaki, H., Minami, N., and 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.
33. Webster, K.E., O'Bryan, M.K., Fletcher, S., Crewther, P.E., Aapola, U., Craig, J., Harrison, D.K., Aung, H., Phutikanit, N., Lyle, R., et al. 2005. Meiotic and epigenetic defects in Dnmt3L-knockout mouse spermatogenesis. Proc. Natl. Acad. Sci. 102: 4068-4073.
34. Yoshimizu, T., Sugiyama, N., De Felice, M., Yeom, Y.I., Ohbo, K., Masuko, K., Obinata, M., Abe, K., Scholer, H.R., and Matsui, Y. 1999. Germline-specific expression of the Oct-4/green fluorescent protein (GFP) transgene in mice. Dev. Growth Differ. 41: 675-684.
35. Zaratiegui, M., Irvine, D.V., and Martienssen, R.A. 2007. Noncoding RNAs and gene silencing. Cell 128: 763-776.