Jump to ContentJump to Main Navigation
Show Summary Details
More options …

Cellular and Molecular Biology Letters

Editor-in-Chief: /


IMPACT FACTOR 2016: 1.260
5-year IMPACT FACTOR: 1.506

CiteScore 2016: 1.56

SCImago Journal Rank (SJR) 2016: 0.615
Source Normalized Impact per Paper (SNIP) 2016: 0.470

Online
ISSN
1689-1392
See all formats and pricing
More options …
Volume 15, Issue 1 (Mar 2010)

The telomere-specific non-LTR retrotransposons SART1 and TRAS1 are suppressed by Piwi subfamily proteins in the silkworm, Bombyx mori

Tsuneyuki Tatsuke
  • Laboratory of Silkworm Science, Kyushu University Graduate School of Bioresource and Bioenvironmental Sciences, Hakozaki 6-10-1, Fukuoka, 812-8581, Japan
  • Research Fellow of the Japan Society for the Promotion of Science, Fukuoka, Japan
  • Email
  • Other articles by this author:
  • De Gruyter OnlineGoogle Scholar
/ Kosuke Sakashita
  • Laboratory of Silkworm Science, Kyushu University Graduate School of Bioresource and Bioenvironmental Sciences, Hakozaki 6-10-1, Fukuoka, 812-8581, Japan
  • Email
  • Other articles by this author:
  • De Gruyter OnlineGoogle Scholar
/ Yuki Masaki
  • Laboratory of Silkworm Science, Kyushu University Graduate School of Bioresource and Bioenvironmental Sciences, Hakozaki 6-10-1, Fukuoka, 812-8581, Japan
  • Email
  • Other articles by this author:
  • De Gruyter OnlineGoogle Scholar
/ Jae Lee
  • Laboratory of Silkworm Science, Kyushu University Graduate School of Bioresource and Bioenvironmental Sciences, Hakozaki 6-10-1, Fukuoka, 812-8581, Japan
  • Email
  • Other articles by this author:
  • De Gruyter OnlineGoogle Scholar
/ Yutaka Kawaguchi
  • Laboratory of Silkworm Science, Kyushu University Graduate School of Bioresource and Bioenvironmental Sciences, Hakozaki 6-10-1, Fukuoka, 812-8581, Japan
  • Email
  • Other articles by this author:
  • De Gruyter OnlineGoogle Scholar
/ Takahiro Kusakabe
  • Laboratory of Silkworm Science, Kyushu University Graduate School of Bioresource and Bioenvironmental Sciences, Hakozaki 6-10-1, Fukuoka, 812-8581, Japan
  • Email
  • Other articles by this author:
  • De Gruyter OnlineGoogle Scholar
Published Online: 2009-12-21 | DOI: https://doi.org/10.2478/s11658-009-0038-9

Abstract

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.

Keywords: Bombyx mori; SART1; TRAS1; Telomere; Piwi

  • [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. http://dx.doi.org/10.1038/nrm2632CrossrefGoogle Scholar

  • [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. http://dx.doi.org/10.1101/gad.1454806CrossrefGoogle Scholar

  • [3] Yin, H. and Lin, H. An epigenetic activation role of Piwi and a Piwi-associated piRNA in Drosophila melanogaster. Nature 450 (2007) 304–308. http://dx.doi.org/10.1038/nature06263Web of ScienceCrossrefGoogle Scholar

  • [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. http://dx.doi.org/10.1146/annurev.genet.38.072902.093115CrossrefGoogle Scholar

  • [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. http://dx.doi.org/10.1101/gad.370206CrossrefGoogle Scholar

  • [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. http://dx.doi.org/10.1016/j.cell.2007.01.043CrossrefWeb of ScienceGoogle Scholar

  • [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. http://dx.doi.org/10.1126/science.1140494CrossrefGoogle Scholar

  • [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. http://dx.doi.org/10.1016/j.ibmb.2008.03.007CrossrefWeb of ScienceGoogle Scholar

  • [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. http://dx.doi.org/10.1261/rna.1452209Web of ScienceCrossrefGoogle Scholar

  • [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. http://dx.doi.org/10.1093/nar/gkj507CrossrefGoogle Scholar

  • [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. http://dx.doi.org/10.1007/s10577-005-0990-9CrossrefGoogle Scholar

  • [12] Sasaki, T. and Fujiwara, H. Detection and distribution patterns of telomerase activity in insects. Eur. J. Biochem. 267 (2000) 3025–3031. http://dx.doi.org/10.1046/j.1432-1033.2000.01323.xCrossrefGoogle Scholar

  • [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. http://dx.doi.org/10.1016/j.gene.2006.04.022CrossrefGoogle Scholar

  • [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. Google Scholar

  • [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. Google Scholar

  • [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. http://dx.doi.org/10.1016/j.cell.2007.05.016CrossrefWeb of ScienceGoogle Scholar

  • [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. http://dx.doi.org/10.1073/pnas.0701920104CrossrefGoogle Scholar

  • [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. http://dx.doi.org/10.1261/rna.744307Web of ScienceCrossrefGoogle Scholar

  • [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. http://dx.doi.org/10.1101/gad.12.23.3715CrossrefGoogle Scholar

  • [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. Google Scholar

  • [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. Google Scholar

  • [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. http://dx.doi.org/10.1007/s00427-005-0033-8CrossrefGoogle Scholar

  • [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. http://dx.doi.org/10.1186/gb-2008-9-1-r10Web of ScienceGoogle Scholar

  • [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. http://dx.doi.org/10.1101/gad.1640708Web of ScienceCrossrefGoogle Scholar

  • [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. http://dx.doi.org/10.1016/j.molcel.2008.09.003Web of ScienceCrossrefGoogle Scholar

  • [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. http://dx.doi.org/10.1128/MCB.21.1.100-108.2001CrossrefGoogle Scholar

  • [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. Google Scholar

  • [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. http://dx.doi.org/10.1093/nar/27.9.2015CrossrefGoogle Scholar

  • [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. http://dx.doi.org/10.1093/emboj/21.3.408CrossrefGoogle Scholar

  • [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. http://dx.doi.org/10.1093/nar/25.8.1578CrossrefGoogle Scholar

  • [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. http://dx.doi.org/10.1016/S1097-2765(02)00440-9CrossrefGoogle Scholar

About the article

Published Online: 2009-12-21

Published in Print: 2010-03-01


Citation Information: Cellular and Molecular Biology Letters, ISSN (Online) 1689-1392, DOI: https://doi.org/10.2478/s11658-009-0038-9.

Export Citation

© 2009 University of Wrocław, Poland. This work is licensed under the Creative Commons Attribution-NonCommercial-NoDerivatives 3.0 License. BY-NC-ND 3.0

Citing Articles

Here you can find all Crossref-listed publications in which this article is cited. If you would like to receive automatic email messages as soon as this article is cited in other publications, simply activate the “Citation Alert” on the top of this page.

[1]
Anandrao Ashok Patil, Tsuneyuki Tatsuke, Hiroaki Mon, Jae Man Lee, Daisuke Morokuma, Masato Hino, and Takahiro Kusakabe
Biochemical and Biophysical Research Communications, 2017
[2]
Sergey Y. Morozov, Ekaterina A. Lazareva, and Andrey G. Solovyev
PeerJ, 2017, Volume 5, Page e3673
[3]
Shozo Honda, Phillipe Loher, Keisuke Morichika, Megumi Shigematsu, Takuya Kawamura, Yoriko Kirino, Isidore Rigoutsos, and Yohei Kirino
Scientific Reports, 2017, Volume 7, Number 1
[4]
Anandrao Ashok Patil, Tsuneyuki Tatsuke, Hiroaki Mon, Jae Man Lee, Daisuke Morokuma, Masato Hino, and Takahiro Kusakabe
Biochemical and Biophysical Research Communications, 2017, Volume 490, Number 2, Page 134
[5]
Zhiqing Li, Daojun Cheng, Hiroaki Mon, Li Zhu, Jian Xu, Tsuneyuki Tatsuke, Jae Man Lee, Qingyou Xia, Takahiro Kusakabe, and Roberto Mantovani
PLoS ONE, 2013, Volume 8, Number 1, Page e52320
[6]
Tsuneyuki Tatsuke, Li Zhu, Zhiqing Li, Hitoshi Mitsunobu, Kaito Yoshimura, Hiroaki Mon, Jae Man Lee, Takahiro Kusakabe, and Axel Imhof
PLoS ONE, 2014, Volume 9, Number 3, Page e92313
[7]
Ekaterina Lazareva, Alexander Lezzhov, Nikita Vassetzky, Andrey Solovyev, and Sergey Morozov
Frontiers in Microbiology, 2015, Volume 6
[8]
Robyn S.M. Lim and Toshie Kai
Seminars in Cell & Developmental Biology, 2015, Volume 47-48, Page 17
[9]
Li Zhu, Tsuneyuki Tatsuke, Jian Xu, Zhiqing Li, Hiroaki Mon, Jae Man Lee, and Takahiro Kusakabe
Insect Biochemistry and Molecular Biology, 2015, Volume 64, Page 78
[10]
Yudai Nagata, Jae Man Lee, Hiroaki Mon, Shigeo Imanishi, Sun Mee Hong, Shoji Komatsu, Yuji Oshima, and Takahiro Kusakabe
Biotechnology Letters, 2013, Volume 35, Number 7, Page 1009
[11]
L. Zhu, Y. Masaki, T. Tatsuke, Z. Li, H. Mon, J. Xu, J. M. Lee, and T. Kusakabe
Insect Molecular Biology, 2013, Volume 22, Number 3, Page 320
[12]
Li Zhu, Tsuneyuki Tatsuke, Zhiqing Li, Hiroaki Mon, Jian Xu, Jae Man Lee, and Takahiro Kusakabe
Applied Entomology and Zoology, 2012, Volume 47, Number 3, Page 207
[13]
Zhiqing Li, Tsuneyuki Tatsuke, Kosuke Sakashita, Li Zhu, Jian Xu, Hiroaki Mon, Jae Man Lee, and Takahiro Kusakabe
Molecular Biology Reports, 2012, Volume 39, Number 5, Page 5575
[14]
Isao Kobayashi, Haruna Tsukioka, Natuo Kômoto, Keiro Uchino, Hideki Sezutsu, Toshiki Tamura, Takahiro Kusakabe, and Shuichiro Tomita
Insect Biochemistry and Molecular Biology, 2012, Volume 42, Number 2, Page 148

Comments (0)

Please log in or register to comment.
Log in