Abstract
PIWI proteins interacting with specific type of small RNAs (piRNAs) repress transposable elements in animals. Besides, they have been shown to participate in various cellular processes: in the regulation of heterochromatin formation including telomere structures, in the control of translation and the cell cycle, and in DNA rearrangements. PIWI proteins were first identified by their roles in the self-renewal of germline stem cells. PIWI protein functions are not limited to gonadogenesis, but the role in determining the fate of stem cells is their specific feature conserved throughout the evolution of animals. Molecular mechanisms underlying these processes are far from being understood. This review focuses on the role of PIWI proteins in the control of maintenance and proliferation of germinal stem cells and its relation to the known function of PIWI in transposon repression.
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Malone, C. D., and Hannon, G. J. (2009) Cell, 136, 656–668.
Siomi, M. C., Sato, K., Pezic, D., and Aravin, A. A. (2011) Nat. Rev. Mol. Cell. Biol., 12, 246–258.
Lin, H., and Spradling, A. C. (1997) Development, 124, 2463–2476.
Juliano, C., Wang, J., and Lin, H. (2011) Annu. Rev. Genet., 45, 447–469.
Goodier, J. L., and Kazazian, H. H., Jr. (2008) Cell, 135, 23–35.
Olovnikov, I. A., and Kalmykova, A. I. (2013) Biochemistry (Moscow), 78, 572–584.
Brennecke, J., Aravin, A. A., Stark, A., Dus, M., Kellis, M., Sachidanandam, R., and Hannon, G. J. (2007) Cell, 128, 1089–1103.
Vagin, V. V., Sigova, A., Li, C., Seitz, H., Gvozdev, V., and Zamore, P. D. (2006) Science, 313, 320–324.
Muerdter, F., Olovnikov, I., Molaro, A., Rozhkov, N. V., Czech, B., Gordon, A., Hannon, G. J., and Aravin, A. A. (2012) RNA, 18, 42–52.
Khurana, J. S., Wang, J., Xu, J., Koppetsch, B. S., Thomson, T. C., Nowosielska, A., Li, C., Zamore, P. D., Weng, Z., and Theurkauf, W. E. (2011) Cell, 147, 1551–1563.
De Vanssay, A., Bouge, A. L., Boivin, A., Hermant, C., Teysset, L., Delmarre, V., Antoniewski, C., and Ronsseray, S. (2012) Nature, 490, 112–115.
Klattenhoff, C., Xi, H., Li, C., Lee, S., Xu, J., Khurana, J. S., Zhang, F., Schultz, N., Koppetsch, B. S., Nowosielska, A., Seitz, H., Zamore, P. D., Weng, Z., and Theurkauf, W. E. (2009) Cell, 138, 1137–1149.
Pane, A., Jiang, P., Zhao, D. Y., Singh, M., and Schupbach, T. (2011) EMBO J., 30, 4601–4615.
Gunawardane, L. S., Saito, K., Nishida, K. M., Miyoshi, K., Kawamura, Y., Nagami, T., Siomi, H., and Siomi, M. C. (2007) Science, 315, 1587–1590.
Malone, C. D., Brennecke, J., Dus, M., Stark, A., McCombie, W. R., Sachidanandam, R., and Hannon, G. J. (2009) Cell, 137, 522–535.
Li, C., Vagin, V. V., Lee, S., Xu, J., Ma, S., Xi, H., Seitz, H., Horwich, M. D., Syrzycha, M., Honda, B. M., Kittler, E. L., Zapp, M. L., Klattenhoff, C., Schulz, N., Theurkauf, W. E., Weng, Z., and Zamore, P. D. (2009) Cell, 137, 509–521.
Guzzardo, P. M., Muerdter, F., and Hannon, G. J. (2013) Curr. Opin. Genet. Dev., Epub ahead of print.
Lim, A. K., Tao, L., and Kai, T. (2009) J. Cell. Biol., 186, 333–342.
Castel, S. E., and Martienssen, R. A. (2013) Nat. Rev. Genet., 14, 100–112.
Aravin, A. A., Sachidanandam, R., Bourc’his, D., Schaefer, C., Pezic, D., Toth, K. F., Bestor, T., and Hannon, G. J. (2008) Mol. Cell, 31, 785–799.
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. (2008) Genes Dev., 22, 908–917.
Bortvin, A. (2013) Biochemistry (Moscow), 78, 592–602.
Watanabe, T., Tomizawa, S., Mitsuya, K., Totoki, Y., Yamamoto, Y., Kuramochi-Miyagawa, S., Iida, N., Hoki, Y., Murphy, P. J., Toyoda, A., Gotoh, K., Hiura, H., Arima, T., Fujiyama, A., Sado, T., Shibata, T., Nakano, T., Lin, H., Ichiyanagi, K., Soloway, P. D., and Sasaki, H. (2011) Science, 332, 848–852.
Lee, H. C., Gu, W., Shirayama, M., Youngman, E., Conte, D., Jr., and Mello, C. C. (2012) Cell, 150, 78–87.
Shirayama, M., Seth, M., Lee, H. C., Gu, W., Ishidate, T., Conte, D., Jr., and Mello, C. C. (2012) Cell, 150, 65–77.
Klenov, M. S., Lavrov, S. A., Stolyarenko, A. D., Ryazansky, S. S., Aravin, A. A., Tuschl, T., and Gvozdev, V. A. (2007) Nucleic Acids Res., 35, 5430–5438.
Klenov, M. S., Sokolova, O. A., Yakushev, E. Y., Stolyarenko, A. D., Mikhaleva, E. A., Lavrov, S. A., and Gvozdev, V. A. (2011) Proc. Natl. Acad. Sci. USA, 108, 18760–18765.
Shpiz, S., Olovnikov, I., Sergeeva, A., Lavrov, S., Abramov, Y., Savitsky, M., and Kalmykova, A. (2011) Nucleic Acids Res., 39, 8703–8711.
Wang, S. H., and Elgin, S. C. (2011) Proc. Natl. Acad. Sci. USA, 108, 21164–21169.
Pal-Bhadra, M., Leibovitch, B. A., Gandhi, S. G., Rao, M., Bhadra, U., Birchler, J. A., and Elgin, S. C. (2004) Science, 303, 669–672.
Brower-Toland, B., Findley, S. D., Jiang, L., Liu, L., Yin, H., Dus, M., Zhou, P., Elgin, S. C., and Lin, H. (2007) Genes Dev., 21, 2300–2311.
Yin, H., and Lin, H. (2007) Nature, 450, 304–308.
Grimaud, C., Bantignies, F., Pal-Bhadra, M., Ghana, P., Bhadra, U., and Cavalli, G. (2006) Cell, 124, 957–971.
Kavi, H. H., and Birchler, J. A. (2009) Epigenetics Chromatin, 2, 15.
Ro, S., Park, C., Song, R., Nguyen, D., Jin, J., Sanders, K. M., McCarrey, J. R., and Yan, W. (2007) RNA, 13, 1693–1702.
Ghildiyal, M., Seitz, H., Horwich, M. D., Li, C., Du, T., Lee, S., Xu, J., Kittler, E. L., Zapp, M. L., Weng, Z., and Zamore, P. D. (2008) Science, 320, 1077–1081.
Lee, E. J., Banerjee, S., Zhou, H., Jammalamadaka, A., Arcila, M., Manjunath, B. S., and Kosik, K. S. (2011) RNA, 17, 1090–1099.
Yan, Z., Hu, H. Y., Jiang, X., Maierhofer, V., Neb, E., He, L., Hu, Y., Hu, H., Li, N., Chen, W., and Khaitovich, P. (2011) Nucleic Acids Res., 39, 6596–6607.
Rajasethupathy, P., Antonov, I., Sheridan, R., Frey, S., Sander, C., Tuschl, T., and Kandel, E. R. (2012) Cell, 149, 693–707.
Cichocki, F., Lenvik, T., Sharma, N., Yun, G., Anderson, S. K., and Miller, J. S. (2010) J. Immunol., 185, 2009–2012.
Khurana, J. S., Xu, J., Weng, Z., and Theurkauf, W. E. (2010) PLoS Genet., 6, e1001246.
Houwing, S., Berezikov, E., and Ketting, R. F. (2008) EMBO J., 27, 2702–2711.
Chalker, D. L., and Yao, M. (2011) Annu. Rev. Genet., 45, 227–246.
Harris, A. N., and Macdonald, P. M. (2001) Development, 128, 2823–2832.
Cox, D. N., Chao, A., Baker, J., Chang, L., Qiao, D., and Lin, H. (1998) Genes Dev., 12, 3715–3727.
Kimble, J. (2011) Cold Spring Harb. Perspect. Biol., 3, a002683.
Spradling, A. C., Fuller, M. T., Braun, R. E., and Yoshida, S. (2011) Cold Spring Harb. Perspect. Biol., 3, a002642.
Kirilly, D., and Xie, T. (2007) Cell Res., 17, 15–25.
Xie, T., Song, X., Jin, Z., Pan, L., Weng, C., Chen, S., and Zhang, N. (2008) Cold Spring Harb. Perspect. Biol., 73, 39–47.
Morrison, S. J., and Spradling, A. S. (2008) Cell, 132, 598–611.
Xie, T., and Spradling, A. C. (1998) Cell, 94, 251–260.
Chen, D., and McKearin, D. (2003) Curr. Biol., 13, 1786–1791.
Cox, D. N., Chao, A., and Lin, H. (2000) Development, 127, 503–514.
Szakmary, A., Cox, D. N., Wang, Z., and Lin, H. (2005) Curr. Biol., 15, 171–178.
King, F. J., Szakmary, A., Cox, D. N., and Lin, H. (2001) Mol. Cell., 7, 497–508.
Chen, D., and McKearin, D. (2005) Curr. Biol., 15, 179–184.
Xia, L., Jia, S., Huang, S., Wang, H., Zhu, Y., Mu, Y., Kan, L., Zheng, W., Wu, D., Li, X., Sun, Q., Meng, A., and Chen, D. (2010) Cell, 143, 978–990.
Casanueva, M. O., and Ferguson, E. L. (2004) Development, 131, 1881–1890.
Rangan, P., Malone, C. D., Navarro, C., Newbold, S. P., Hayes, P. S., Sachidanandam, R., Hannon, G. J., and Lehmann, R. (2011) Curr. Biol., 21, 1373–1379.
Zamparini, A. L., Davis, M. Y., Malone, C. D, Vieira, E., Zavadil, J., Sachidanandam, R., Hannon, G. J., and Lehmann, R. (2011) Development, 138, 4039–4050.
Olivieri, D., Sykora, M. M., Sachidanandam, R., Mechtler, K., and Brennecke, J. (2010) EMBO J., 29, 3301–3317.
Saito, K., Ishizu, H., Komai, M., Kotani, H., Kawamura, Y., Nishida, K. M., Siomi, H., and Siomi, M. C. (2010) Genes Dev., 24, 2493–2498.
Handler, D., Olivieri, D., Novatchkova, M., Gruber, F. S., Meixner, K., Mechtler, K., Stark, A., Sachidanandam, R., and Brennecke, J. (2011) EMBO J., 30, 3977–3993.
Qi, H., Watanabe, T., Ku, H. Y., Liu, N., Zhong, M., and Lin, H. (2011) J. Biol. Chem., 286, 3789–3797.
Szakmary, A., Reedy, M., Qi, H., and Lin, H. (2009) J. Cell Biol., 185, 613–627.
King, F. J., and Lin, H. (1999) Development, 126, 1833–1844.
Ipsaro, J. J., Haase, A. D., Knott, S. R., Joshua-Tor, L., and Hannon, G. J. (2012) Nature, 491, 279–283.
Nishimasu, H., Ishizu, H., Saito, K., Fukuhara, S., Kamatani, M. K., Bonnefond, L., Matsumoto, N., Nishizawa, T., Nakanaga, K., Aoki, J., Ishitani, R., Siomi, H., Siomi, M. C., and Nureki, O. (2012) Nature, 491, 284–287.
Pane, A., Wehr, K., and Schupbach, T. (2007) Dev. Cell, 12, 851–862.
Le Thomas, A., Rogers, A. K., Webster, A., Marinov, G. K., Liao, S. E., Perkins, E. M., Hur, J. K., Aravin, A. A., and Toth, K. F. (2013) Genes Dev., 27, 390–399.
Sun, H., Li, D., Chen, S., Liu, Y., Liao, X., Deng, W., Li, N., Zeng, M., Tao, D., and Ma, Y. (2010) J. Biol. Chem., 285, 4243–4250.
Zhang, K., Lu, Y., Yang, P., Li, C., Sun, H., Tao, D., Liu, Y., Zhang, S., and Ma, Y. (2012) PLoS One, 7, e41973.
Gangaraju, V. K., Yin, H., Weiner, M. M., Wang, J., Huang, X. A., and Lin, H. (2011) Nat. Genet., 43, 153–158.
Megosh, H. B., Cox, D. N., Campbell, C., and Lin, H. (2006) Curr. Biol., 16, 1884–1894.
Pek, J. W., and Kai, T. (2011) Curr. Biol., 21, 39–44.
Lazzaro, F., Giannattasio, M., Puddu, F., Granata, M., Pellicioli, A., Plevani, P., and Muzi-Falconi, M. (2009) DNA Repair (Amst.), 8, 1055–1067.
Chen, L., Shen, R., Ye, Y., Pu, X. A., Liu, X., Duan, W., Wen, J., Zimmerer, J., Wang, Y., Liu, Y., Lasky, L. C., Heerema, N. A., Perrotti, D., Ozato, K., Kuramochi-Miyagawa, S., Nakano, T., Yates, A. J., Carson, W. E., 3rd, Lin, H., Barsky, S. H., and Gao, J. X. (2007) PLoS ONE, 2, e293.
Lee, J. H., Schutte, D., Wulf, G., Fuzesi, L., Radzun, H. J., Schweyer, S., Engel, W., and Nayernia, K. (2006) Hum. Mol. Genet., 15, 201–211.
Liu, X., Sun, Y., Guo, J., Ma, H., Li, J., Dong, B., Jin, G., Zhang, J., Wu, J., Meng, L., and Shou, C. (2006) Int. J. Cancer, 118, 1922–1929.
Suzuki, R., Honda, S., and Kirino, Y. (2012) Front. Genet., 3, 204.
Janic, A., Mendizabal, L., Llamazares, S., Rossell, D., and Gonzalez, C. (2010) Science, 330, 1824–1827.
Siddiqi, S., Terry, M., and Matushansky, I. (2012) PLoS ONE, 7, e33711.
Chenais, B. (2013) Biochim. Biophys. Acta, 1835, 28–35.
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Original Russian Text © E. Y. Yakushev, O. A. Sokolova, V. A. Gvozdev, M. S. Klenov, 2013, published in Biokhimiya, 2013, Vol. 78, No. 6, pp. 763–770.
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Yakushev, E.Y., Sokolova, O.A., Gvozdev, V.A. et al. Multifunctionality of PIWI proteins in control of germline stem cell fate. Biochemistry Moscow 78, 585–591 (2013). https://doi.org/10.1134/S0006297913060047
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DOI: https://doi.org/10.1134/S0006297913060047