The telomere-specific non-LTR retrotransposons SART 1 and TRAS1 are suppressed by PIWI subfamily proteins in the silkworm, Bombyx mori

• Autorzy: Tatsuke T , Sakashita K. , Masaki Y. , Lee J.M. , Kawaguchi Y. , Kusakabe T.
• Języki publikacji: EN

Abstrakty

EN

The telomere structures in Bombyx mori are thought to be maintained mainly by the transposition of the specialized telomeric retroelements SART and TRAS. The silkworm genome has telomeric TTAGG repeats and telomerase, but this telomerase displays little or no activity. Here, we report that the transcription of the telomeric retroelements SART1 and TRAS1 is suppressed by the silkworm Piwi subfamily proteins BmAgo3 and Siwi. The silkworm Piwi subfamily was found to be expressed predominantly in the gonads and early embryo, as in other model organisms, but in BmN4 cultured cells, these proteins formed granules that were separate from the nuage, which is a different behaviour pattern. The expression of TRAS1 was increased in BmN4 cells when BmAgo3 or Siwi were silenced by RNAi. Our results suggest that B. mori Piwi proteins are involved in regulating the transposition of telomeric retroelements, and that the functional piRNA pathway is conserved in BmN4 cultured cells.

Słowa kluczowe

EN

telomere; retrotransposon; SART1 protein; TRAS1 antibody; protein; silkworm; Bombyx mori; Piwi subfamily; RNA interference

• Wydawca: -
• Czasopismo: Cellular and Molecular Biology Letters
• Rocznik: 2010
• Tom: 15
• Numer: 1
• Opis fizyczny: p.118-133,fig.,ref.

Twórcy

autor

Tatsuke T

• Kyushu University Graduate School of Bioresource and Bioenvironmental Sciences, Hakozaki 6-10-1, Fukuoka 812-8581, Japan

autor

Sakashita K.

autor

Masaki Y.

autor

Lee J.M.

autor

Kawaguchi Y.

autor

Kusakabe T.

Bibliografia

• 1. Kim, V.N., Han, J. and Siomi, M.C. Biogenesis of small RNAs in animals. Nat. Rev. Mol. Cell Biol. 10 (2009) 126-139.
• 2. Saito, K., Nishida, K.M., Mori, T., Kawamura, Y., Miyoshi, K., Nagami, T., Siomi, H. and Siomi, M.C. Specific association of Piwi with rasiRNAs derived from retrotransposon and heterochromatic regions in the Drosophila genome. Genes Dev. 20 (2006) 2214-2222.
• 3. Yin, H. and Lin, H. An epigenetic activation role of Piwi and a Piwiassociated piRNA in Drosophila melanogaster. Nature 450 (2007) 304-308.
• 4. Pardue, M.L. and DeBaryshe, P.G. Retrotransposons provide an evolutionarily robust non-telomerase mechanism to maintain telomeres. Annu. Rev. Genet. 37 (2003) 485-511.
• 5. Savitsky, M., Kwon, D., Georgiev, P., Kalmykova, A. and Gvozdev, V. Telomere elongation is under the control of the RNAi-based mechanism in the Drosophila germline. Genes Dev. 20 (2006) 345-354.
• 6. Brennecke, J., Aravin, A.A., Stark, A., Dus, M., Kellis, M., Sachidanandam, R. and Hannon, G.J. Discrete small RNA-generating loci as master regulators of transposon activity in Drosophila. Cell 128 (2007) 1089-1103.
• 7. Gunawardane, L.S., Saito, K., Nishida, K.M., Miyoshi, K., Kawamura, Y., Nagami, T., Siomi, H. and Siomi, M.C. A slicer-mediated mechanism for repeat-associated siRNA 5' end formation in Drosophila. Science 315 (2007) 1587-1590.
• 8. Kawaoka, S., Hayashi, N., Katsuma, S., Kishino, H., Kohara, Y., Mita, K., and Shimada, T. Bombyx small RNAs: Genomic defense system against transposons in the silkworm, Bombyx mori. Insect Biochem. Mol. Biol. 38 (2008) 1058-1065.
• 9. Kawaoka, S., Hayashi, N., Suzuki, Y., Abe, H., Sugano, S., Tomari, Y., Shimada, T. and Katsuma, S. The Bombyx ovary-derived cell line endogenously expresses PIWI/PIWI-interacting RNA complexes. RNA 15 (2009) 1258-1264.
• 10. Tsukioka, H., Takahashi, M., Mon, H., Okano, K., Mita, K., Shimada, T., Lee, J.M., Kawaguchi, Y., Koga, K. and Kusakabe, T. Role of the silkworm argonaute2 homolog gene in double-strand break repair of extrachromosomal DNA. Nucleic Acids Res. 34 (2006) 1092-1101.
• 11. Fujiwara, H., Osanai, M., Matsumoto, T. and Kojima, K.K. Telomerespecific non-LTR retrotransposons and telomere maintenance in the silkworm, Bombyx mori. Chromosome Res. 13 (2005) 455-467.
• 12. Sasaki, T. and Fujiwara, H. Detection and distribution patterns of telomerase activity in insects. Eur. J. Biochem. 267 (2000) 3025-3031.
• 13. Osanai, M., Kojima, K.K., Futahashi, R., Yaguchi, S. and Fujiwara, H. Identification and characterization of the telomerase reverse transcriptase of Bombyx mori (silkworm) and Tribolium castaneum (flour beetle). Gene 376 (2006) 281-289.
• 14. Mitsunobu, H., Sakashita, K., Mon, H., Yoshida, H., Lee, J.M., Kawaguchi, Y., Koga, K.,and Kusakabe, T. Construction of gateway-based destination vectors for detecting subcellular localization of proteins in the silkworm, Bombyx mori. J. Insect Biotech. Seric. 75 (2006) 141-145.
• 15. Maeda, T., Kusakabe, T., Lee, J.M., Miyagawa, Y., Kawaguchi, Y. and Koga, K. Efficient nonviral gene transfer mediated by polyethyleneimine in an insect cell line. J. Insect Biotech. Seric. 74 (2005) 21-26.
• 16. Kiriakidou, M., Tan, G.S., Lamprinaki, S., De Planell-Saguer, M., Nelson, P.T. and Mourelatos, Z. An mRNA m7G cap binding-like motif within human Ago2 represses translation. Cell 129 (2007) 1141-1151.
• 17. Lim, A.K. and Kai, T. Unique germ-line organelle, nuage, functions to repress selfish genetic elements in Drosophila melanogaster. Proc. Natl. Acad. Sci. U S A 104 (2007) 6714-6719.
• 18. Nishida, K.M., Saito, K., Mori, T., Kawamura, Y., Nagami-Okada, T., Inagaki, S., Siomi, H. and Siomi, M.C. Gene silencing mechanisms mediated by Aubergine piRNA complexes in Drosophila male gonad. RNA 13 (2007) 1911-1922.
• 19. Cox, D.N., Chao, A., Baker, J., Chang, L., Qiao, D. and Lin, H. A novel class of evolutionarily conserved genes defined by piwi are essential for stem cell self-renewal. Genes Dev. 12 (1998) 3715-3727.
• 20. Harris, A.N. and Macdonald, P.M. Aubergine encodes a Drosophila polar granule component required for pole cell formation and related to eIF2C. Development 128 (2001) 2823-2832.
• 21. Cox, D.N., Chao, A. and Lin, H. piwi encodes a nucleoplasmic factor whose activity modulates the number and division rate of germline stem cells. Development 127 (2000) 503-514.
• 22. Nakao, H., Hatakeyama, M., Lee, J.M., Shimoda, M. and Kanda, T. Expression pattern of Bombyx vasa-like (BmVLG) protein and its implications in germ cell development. Dev. Genes Evol. 216 (2006) 94-99.
• 23. Tomoyasu, Y., Miller, T., Tomita, S., Schoppmeier, M., Grossmann, D. and Bucher, G. Exploring systemic RNA interference in insects: a genome-wide survey for RNAi genes in Tribolium. Genome Biol. 9 (2008) R10.
• 24. 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. and Nakano, T. DNA methylation of retrotransposon genes is regulated by Piwi family members MILI and MIWI2 in murine fetal testes. Genes Dev. 22 (2008) 908-917.
• 25. Aravin, A.A., Sachidanandam, R., Bourc'his, D., Schaefer, C., Pezic, D., Toth, K.F., Bestor, T. and Hannon, G.J. A piRNA pathway primed by individual transposons is linked to de novo DNA methylation in mice. Mol. Cell 31 (2008) 785-799.
• 26. Anzai, T., Takahashi, H. and Fujiwara, H. Sequence-specific recognition and cleavage of telomeric repeat (TTAGG)(n) by endonuclease of non-long terminal repeat retrotransposon TRAS1. Mol. Cell Biol. 21 (2001) 100-108.
• 27. Okazaki, S., Ishikawa, H. and Fujiwara, H. Structural analysis of TRAS1, a novel family of telomeric repeat-associated retrotransposons in the silkworm, Bombyx mori. Mol. Cell Biol. 15 (1995) 4545-4552.
• 28. Takahashi, H. and Fujiwara, H. Transcription analysis of the telomeric repeat-specific retrotransposons TRAS1 and SART1 of the silkworm Bombyx mori. Nucleic Acids Res. 27 (1999) 2015-2021.
• 29. Takahashi, H. and Fujiwara, H. Transplantation of target site specificity by swapping the endonuclease domains of two LINEs. EMBO J. 21 (2002) 408-417.
• 30. Takahashi, H., Okazaki, S. and Fujiwara, H. A new family of site-specific retrotransposons, SART1, is inserted into telomeric repeats of the silkworm, Bombyx mori. Nucleic Acids Res. 25 (1997) 1578-1584.
• 31. Pal-Bhadra, M., Bhadra, U. and Birchler, J.A. RNAi related mechanisms affect both transcriptional and posttranscriptional transgene silencing in Drosophila. Mol. Cell 9 (2002) 315-327.