Skip to main content
Log in

piRNA clusters as a main source of small RNAs in the animal germline

  • Review
  • Published:
Biochemistry (Moscow) Aims and scope Submit manuscript

Abstract

PIWI subfamily Argonaute proteins and small RNAs bound to them (PIWI interacting RNA, piRNA) control mobilization of transposable elements (TE) in the animal germline. piRNAs are generated by distinct genomic regions termed piRNA clusters. piRNA clusters are often extensive loci enriched in damaged fragments of TEs. New TE integration into piRNA clusters causes production of TE-specific piRNAs and repression of cognate sequences. piRNAs are thought to be generated from long single-stranded precursors encoded by piRNA clusters. Special chromatin structures might be essential to distinguish these genomic loci as a source for piRNAs. In this review, we present recent findings on the structural organization of piRNA clusters and piRNA biogenesis in Drosophila and other organisms, which are important for understanding a key epigenetic mechanism that provides defense against TE expansion.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Similar content being viewed by others

References

  1. Siomi, M. C., Sato, K., Pezic, D., and Aravin, A. A. (2011) Nat. Rev. Mol. Cell Biol., 12, 246–258.

    PubMed  CAS  Google Scholar 

  2. Senti, K. A., and Brennecke, J. (2010) Trends Genet., 26, 499–509.

    PubMed  CAS  Google Scholar 

  3. Vagin, V. V., Sigova, A., Li, C., Seitz, H., Gvozdev, V., and Zamore, P. D. (2006) Science, 313, 320–324.

    PubMed  CAS  Google Scholar 

  4. 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.

    PubMed  CAS  Google Scholar 

  5. Saito, K., Nishida, K. M., Mori, T., Kawamura, Y., Miyoshi, K., Nagami, T., Siomi, H., and Siomi, M. C. (2006) Genes Dev., 20, 2214–2222.

    PubMed  CAS  Google Scholar 

  6. Brennecke, J., Aravin, A. A., Stark, A., Dus, M., Kellis, M., Sachidanandam, R., and Hannon, G. J. (2007) Cell, 128, 1089–1103.

    PubMed  CAS  Google Scholar 

  7. Horwich, M. D., Li, C., Matranga, C., Vagin, V., Farley, G., Wang, P., and Zamore, P. D. (2007) Curr. Biol., 17, 1265–1272.

    PubMed  CAS  Google Scholar 

  8. Aravin, A. A., Klenov, M. S., Vagin, V. V., Bantignies, F., Cavalli, G., and Gvozdev, V. A. (2004) Mol. Cell Biol., 24, 6742–6750.

    PubMed  CAS  Google Scholar 

  9. 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., Plasterk, R. H., Hannon, G. J., Draper, B. W., and Ketting, R. F. (2007) Cell, 129, 69–82.

    PubMed  CAS  Google Scholar 

  10. Li, C., Vagin, V. V., Lee, S., Xu, J., Ma, S., Xi, H., Seitz, H., Horwich, M. D., Syrzycka, 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.

    PubMed  CAS  Google Scholar 

  11. Malone, C. D., Brennecke, J., Dus, M., Stark, A., McCombie, W. R., Sachidanandam, R., and Hannon, G. J. (2009) Cell, 137, 522–535.

    PubMed  CAS  Google Scholar 

  12. Lim, A. K., and Kai, T. (2007) Proc. Natl. Acad. Sci. USA, 104, 6714–6719.

    PubMed  CAS  Google Scholar 

  13. Findley, S. D., Tamanaha, M., Clegg, N. J., and Ruohola-Baker, H. (2003) Development, 130, 859–871.

    PubMed  CAS  Google Scholar 

  14. Hall, I. M., Shankaranarayana, G. D., Noma, K., Ayoub, N., Cohen, A., and Grewal, S. I. (2002) Science, 297, 2232–2237.

    PubMed  CAS  Google Scholar 

  15. Onodera, Y., Haag, J. R., Ream, T., Costa Nunes, P., Pontes, O., and Pikaard, C. S. (2005) Cell, 120, 613–622.

    PubMed  CAS  Google Scholar 

  16. 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.

    PubMed  CAS  Google Scholar 

  17. Shpiz, S., Olovnikov, I., Sergeeva, A., Lavrov, S., Abramov, Y., Savitsky, M., and Kalmykova, A. (2011) Nucleic Acids Res., 39, 8703–8711.

    PubMed  CAS  Google Scholar 

  18. Sienski, G., Donertas, D., and Brennecke, J. (2012) Cell, 151, 964–980.

    PubMed  CAS  Google Scholar 

  19. Lau, N. C., Robine, N., Martin, R., Chung, W. J., Niki, Y., Berezikov, E., and Lai, E. C. (2009) Genome Res., 19, 1776–1785.

    PubMed  CAS  Google Scholar 

  20. Kawaoka, S., Izumi, N., Katsuma, S., and Tomari, Y. (2011) Mol. Cell, 43, 1015–1022.

    PubMed  CAS  Google Scholar 

  21. Pelisson, A., Song, S. U., Prud’homme, N., Smith, P. A., Bucheton, A., and Corces, V. G. (1994) EMBO J., 13, 4401–4411.

    PubMed  CAS  Google Scholar 

  22. Desset, S., Meignin, C., Dastugue, B., and Vaury, C. (2003) Genetics, 164, 501–509.

    PubMed  CAS  Google Scholar 

  23. Prud’homme, N., Gans, M., Masson, M., Terzian, C., and Bucheton, A. (1995) Genetics, 139, 697–711.

    PubMed  Google Scholar 

  24. Saito, K., Inagaki, S., Mituyama, T., Kawamura, Y., Ono, Y., Sakota, E., Kotani, H., Asai, K., Siomi, H., and Siomi, M. C. (2009) Nature, 461, 1296–1299.

    PubMed  CAS  Google Scholar 

  25. Pelisson, A., Sarot, E., Payen-Groschene, G., and Bucheton, A. (2007) J. Virol., 81, 1951–1960.

    PubMed  CAS  Google Scholar 

  26. Robert, V., Prud’homme, N., Kim, A., Bucheton, A., and Pelisson, A. (2001) Genetics, 158, 701–713.

    PubMed  CAS  Google Scholar 

  27. Kawaoka, S., Mitsutake, H., Kiuchi, T., Kobayashi, M., Yoshikawa, M., Suzuki, Y., Sugano, S., Shimada, T., Kobayashi, J., Tomari, Y., and Katsuma, S. (2012) RNA, 18, 265–273.

    PubMed  CAS  Google Scholar 

  28. Kawaoka, S., Hara, K., Shoji, K., Kobayashi, M., Shimada, T., Sugano, S., Tomari, Y., Suzuki, Y., and Katsuma, S. (2013) Nucleic Acids Res., 41, 1581–1590.

    PubMed  CAS  Google Scholar 

  29. Robine, N., Lau, N. C., Balla, S., Jin, Z., Okamura, K., Kuramochi-Miyagawa, S., Blower, M. D., and Lai, E. C. (2009) Curr. Biol., 19, 2066–2076.

    PubMed  CAS  Google Scholar 

  30. 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.

    PubMed  CAS  Google Scholar 

  31. Aravin, A. A., Hannon, G. J., and Brennecke, J. (2007) Science, 318, 761–764.

    PubMed  CAS  Google Scholar 

  32. Kawaoka, S., Hayashi, N., Suzuki, Y., Abe, H., Sugano, S., Tomari, Y., Shimada, T., and Katsuma, S. (2009) RNA, 15, 1258–1264.

    PubMed  CAS  Google Scholar 

  33. Olovnikov, I., Ryazansky, S., Shpiz, S., Lavrov, S., Abramov, Y., Vaury, C., Jensen, S., and Kalmykova, A. (2013) Nucleic Acids Res., PMID: 23620285; doi: 10.1093/nar/gkt310.

    Google Scholar 

  34. 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.

    PubMed  CAS  Google Scholar 

  35. Olivieri, D., Sykora, M. M., Sachidanandam, R., Mechtler, K., and Brennecke, J. (2010) EMBO J., 29, 3301–3317.

    PubMed  CAS  Google Scholar 

  36. 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.

    PubMed  CAS  Google Scholar 

  37. Ipsaro, J. J., Haase, A. D., Knott, S. R., Joshua-Tor, L., and Hannon, G. J. (2012) Nature, 491, 279–283.

    PubMed  CAS  Google Scholar 

  38. 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.

    PubMed  CAS  Google Scholar 

  39. Voigt, F., Reuter, M., Kasaruho, A., Schulz, E. C., Pillai, R. S., and Barabas, O. (2012) RNA, 18, 2128–2134.

    PubMed  CAS  Google Scholar 

  40. Pane, A., Wehr, K., and Schupbach, T. (2007) Dev. Cell, 12, 851–862.

    PubMed  CAS  Google Scholar 

  41. 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.

    PubMed  CAS  Google Scholar 

  42. Anand, A., and Kai, T. (2012) EMBO J., 31, 870–882.

    PubMed  CAS  Google Scholar 

  43. Zhang, Z., Xu, J., Koppetsch, B. S., Wang, J., Tipping, C., Ma, S., Weng, Z., Theurkauf, W. E., and Zamore, P. D. (2011) Mol. Cell, 44, 572–584.

    PubMed  CAS  Google Scholar 

  44. Patil, V. S., and Kai, T. (2010) Curr. Biol., 20, 724–730.

    PubMed  CAS  Google Scholar 

  45. Siomi, M. C., Mannen, T., and Siomi, H. (2010) Genes Dev., 24, 636–646.

    PubMed  CAS  Google Scholar 

  46. Brennecke, J., Malone, C. D., Aravin, A. A., Sachidanandam, R., Stark, A., and Hannon, G. J. (2008) Science, 322, 1387–1392.

    PubMed  CAS  Google Scholar 

  47. Bucheton, A. (1990) Trends Genet., 6, 16–21.

    PubMed  CAS  Google Scholar 

  48. Kidwell, M. G., Kidwell, J. F., and Sved, J. A. (1977) Genetics, 86, 813–833.

    PubMed  CAS  Google Scholar 

  49. 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.

    PubMed  CAS  Google Scholar 

  50. Grentzinger, T., Armenise, C., Brun, C., Mugat, B., Serrano, V., Pelisson, A., and Chambeyron, S. (2012) Genome Res., 22, 1877–1888.

    PubMed  CAS  Google Scholar 

  51. Jensen, S., Gassama, M. P., and Heidmann, T. (1999) Nat. Genet., 21, 209–212.

    PubMed  CAS  Google Scholar 

  52. De Vanssay, A., Bouge, A. L., Boivin, A., Hermant, C., Teysset, L., Delmarre, V., Antoniewski, C., and Ronsseray, S. (2012) Nature, 490, 112–115.

    PubMed  Google Scholar 

  53. Ronsseray, S., Josse, T., Boivin, A., and Anxolabehere, D. (2003) Genetica, 117, 327–335.

    PubMed  CAS  Google Scholar 

  54. Pardue, M. L., and DeBaryshe, P. G. (2003) Annu. Rev. Genet., 37, 485–511.

    PubMed  CAS  Google Scholar 

  55. Shpiz, S., and Kalmykova, A. (2012) in Reviews on Selected Topics of Telomere Biology (Li, B., ed.) Intech, Rijeka, pp. 31–56.

  56. Todeschini, A. L., Teysset, L., Delmarre, V., and Ronsseray, S. (2010) PLoS One, 5, e11032.

    PubMed  Google Scholar 

  57. Nagao, A., Mituyama, T., Huang, H., Chen, D., Siomi, M. C., and Siomi, H. (2010) RNA, 16, 2503–2515.

    PubMed  CAS  Google Scholar 

  58. Cox, D. N., Chao, A., and Lin, H. (2000) Development, 127, 503–514.

    PubMed  CAS  Google Scholar 

  59. Kibanov, M. V., Egorova, K. S., Ryazansky, S. S., Sokolova, O. A., Kotov, A. A., Olenkina, O. M., Stolyarenko, A. D., Gvozdev, V. A., and Olenina, L. V. (2011) Mol. Biol. Cell, 22, 3410–3419.

    PubMed  CAS  Google Scholar 

  60. Nishida, K. M., Saito, K., Mori, T., Kawamura, Y., Nagami-Okada, T., Inagaki, S., Siomi, H., and Siomi, M. C. (2007) RNA, 13, 1911–1922.

    PubMed  CAS  Google Scholar 

  61. Aravin, A. A., Naumova, N. M., Tulin, A. V., Vagin, V. V., Rozovsky, Y. M., and Gvozdev, V. A. (2001) Curr. Biol., 11, 1017–1027.

    PubMed  CAS  Google Scholar 

  62. Bozzetti, M. P., Massari, S., Finelli, P., Meggio, F., Pinna, L. A., Boldyreff, B., Issinger, O. G., Palumbo, G., Ciriaco, C., Bonaccorsi, S., et al. (1995) Proc. Natl. Acad. Sci. USA, 92, 6067–6071.

    PubMed  CAS  Google Scholar 

  63. Gell, S. L., and Reenan, R. A. (2012) Genetics, 193, 771–784.

    PubMed  Google Scholar 

  64. Kalmykova, A. I., Klenov, M. S., and Gvozdev, V. A. (2005) Nucleic Acids Res., 33, 2052–2059.

    PubMed  CAS  Google Scholar 

  65. 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.

    PubMed  CAS  Google Scholar 

  66. Zhang, F., Wang, J., Xu, J., Zhang, Z., Koppetsch, B. S., Schultz, N., Vreven, T., Meignin, C., Davis, I., Zamore, P. D., Weng, Z., and Theurkauf, W. E. (2012) Cell, 151, 871–884.

    PubMed  CAS  Google Scholar 

  67. Zofall, M., and Grewal, S. I. (2006) Cold Spring Harb. Symp. Quant. Biol., 71, 487–496.

    PubMed  CAS  Google Scholar 

  68. Volpe, T. A., Kidner, C., Hall, I. M., Teng, G., Grewal, S. I., and Martienssen, R. A. (2002) Science, 297, 1833–1837.

    PubMed  CAS  Google Scholar 

  69. Verdel, A., Jia, S., Gerber, S., Sugiyama, T., Gygi, S., Grewal, S. I., and Moazed, D. (2004) Science, 303, 672–676.

    PubMed  CAS  Google Scholar 

  70. Motamedi, M. R., Verdel, A., Colmenares, S. U., Gerber, S. A., Gygi, S. P., and Moazed, D. (2004) Cell, 119, 789–802.

    PubMed  CAS  Google Scholar 

  71. Sugiyama, T., Cam, H., Verdel, A., Moazed, D., and Grewal, S. I. (2005) Proc. Natl. Acad. Sci. USA, 102, 152–157.

    PubMed  CAS  Google Scholar 

  72. Zofall, M., and Grewal, S. I. (2006) Mol. Cell, 22, 681–692.

    PubMed  CAS  Google Scholar 

  73. Halic, M., and Moazed, D. (2010) Cell, 140, 504–516.

    PubMed  CAS  Google Scholar 

  74. Clough, E., Moon, W., Wang, S., Smith, K., and Hazelrigg, T. (2007) Development, 134, 157–165.

    PubMed  CAS  Google Scholar 

  75. Yoon, J., Lee, K. S., Park, J. S., Yu, K., Paik, S. G., and Kang, Y. K. (2008) PLoS One, 3, e2234.

    PubMed  Google Scholar 

  76. Tschiersch, B., Hofmann, A., Krauss, V., Dorn, R., Korge, G., and Reuter, G. (1994) EMBO J., 13, 3822–3831.

    PubMed  CAS  Google Scholar 

  77. 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.

    PubMed  CAS  Google Scholar 

  78. Ushijima, Y., Inoue, Y. H., Konishi, T., Kitazawa, D., Yoshida, H., Shimaji, K., Kimura, H., and Yamaguchi, M. (2012) Chromosome Res., 20, 319–331.

    PubMed  CAS  Google Scholar 

  79. Moshkovich, N., and Lei, E. P. (2010) PLoS Genet., 6, e1000880.

    PubMed  Google Scholar 

  80. Fanti, L., Giovinazzo, G., Berloco, M., and Pimpinelli, S. (1998) Mol. Cell, 2, 527–538.

    PubMed  CAS  Google Scholar 

  81. Volpe, A. M., Horowitz, H., Grafer, C. M., Jackson, S. M., and Berg, C. A. (2001) Genetics, 159, 1117–1134.

    PubMed  CAS  Google Scholar 

  82. Pane, A., Jiang, P., Zhao, D. Y., Singh, M., and Schupbach, T. (2011) EMBO J., 30, 4601–4615.

    PubMed  CAS  Google Scholar 

  83. Chen, Y., Pane, A., and Schupbach, T. (2007) Curr. Biol., 17, 637–642.

    PubMed  CAS  Google Scholar 

  84. Kawaoka, S., Arai, Y., Kadota, K., Suzuki, Y., Hara, K., Sugano, S., Shimizu, K., Tomari, Y., Shimada, T., and Katsuma, S. (2011) RNA, 17, 1401–1407.

    PubMed  CAS  Google Scholar 

  85. Kawaoka, S., Hayashi, N., Katsuma, S., Kishino, H., Kohara, Y., Mita, K., and Shimada, T. (2008) Insect Biochem. Mol. Biol., 38, 1058–1065.

    PubMed  CAS  Google Scholar 

  86. Kawaoka, S., Minami, K., Katsuma, S., Mita, K., and Shimada, T. (2008) Biochem. Biophys. Res. Commun., 367, 755–760.

    PubMed  CAS  Google Scholar 

  87. Arensburger, P., Hice, R. H., Wright, J. A., Craig, N. L., and Atkinson, P. W. (2011) BMC Genomics, 12, 606.

    PubMed  CAS  Google Scholar 

  88. Morazzani, E. M., Wiley, M. R., Murreddu, M. G., Adelman, Z. N., and Myles, K. M. (2012) PLoS Pathog., 8, e1002470.

    PubMed  CAS  Google Scholar 

  89. Campbell, C. L., Black, W. C. T., Hess, A. M., and Foy, B. D. (2008) BMC Genomics, 9, 425.

    PubMed  Google Scholar 

  90. Van der Heijden, G. W., and Bortvin, A. (2009) Epigenetics, 4, 76–79.

    PubMed  Google Scholar 

  91. 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) Dev. Cell, 12, 503–514.

    PubMed  CAS  Google Scholar 

  92. Rozhkov, N. V., Aravin, A. A., Zelentsova, E. S., Schostak, N. G., Sachidanandam, R., McCombie, W. R., Hannon, G. J., and Evgen’ev, M. B. (2010) RNA, 16, 1634–1645.

    PubMed  CAS  Google Scholar 

  93. Aravin, A. A., and Bourc’his, D. (2008) Genes Dev., 22, 970–975.

    PubMed  CAS  Google Scholar 

  94. Aravin, A., Gaidatzis, D., Pfeffer, S., Lagos-Quintana, M., Landgraf, P., Iovino, N., Morris, P., Brownstein, M. J., Kuramochi-Miyagawa, S., Nakano, T., Chien, M., Russo, J. J., Ju, J., Sheridan, R., Sander, C., Zavolan, M., and Tuschl, T. (2006) Nature, 442, 203–207.

    PubMed  CAS  Google Scholar 

  95. 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.

    PubMed  CAS  Google Scholar 

  96. Kuramochi-Miyagawa, S., Kimura, T., Yomogida, K., Kuroiwa, A., Tadokoro, Y., Fujita, Y., Sato, M., Matsuda, Y., and Nakano, T. (2001) Mech. Dev., 108, 121–133.

    PubMed  CAS  Google Scholar 

  97. Kuramochi-Miyagawa, S., Kimura, T., Ijiri, T. W., Isobe, T., Asada, N., Fujita, Y., Ikawa, M., Iwai, N., Okabe, M., Deng, W., Lin, H., Matsuda, Y., and Nakano, T. (2004) Development, 131, 839–849.

    PubMed  CAS  Google Scholar 

  98. Deng, W., and Lin, H. (2002) Dev. Cell, 2, 819–830.

    PubMed  CAS  Google Scholar 

  99. Girard, A., Sachidanandam, R., Hannon, G. J., and Carmell, M. A. (2006) Nature, 442, 199–202.

    PubMed  Google Scholar 

  100. Das, P. P., Bagijn, M. P., Goldstein, L. D., Woolford, J. R., Lehrbach, N. J., Sapetschnig, A., Buhecha, H. R., Gilchrist, M. J., Howe, K. L., Stark, R., Matthews, N., Berezikov, E., Ketting, R. F., Tavare, S., and Miska, E. A. (2008) Mol. Cell, 31, 79–90.

    PubMed  CAS  Google Scholar 

  101. Batista, P. J., Ruby, J. G., Claycomb, J. M., Chiang, R., Fahlgren, N., Kasschau, K. D., Chaves, D. A., Gu, W., Vasale, J. J., Duan, S., Conte, D., Jr., Luo, S., Schroth, G. P., Carrington, J. C., Bartel, D. P., and Mello, C. C. (2008) Mol. Cell, 31, 67–78.

    PubMed  CAS  Google Scholar 

  102. Lee, H. C., Gu, W., Shirayama, M., Youngman, E., Conte, D., Jr., and Mello, C. C. (2012) Cell, 150, 78–87.

    PubMed  CAS  Google Scholar 

  103. Shirayama, M., Seth, M., Lee, H. C., Gu, W., Ishidate, T., Conte, D., Jr., and Mello, C. C. (2012) Cell, 150, 65–77.

    PubMed  CAS  Google Scholar 

  104. Bagijn, M. P., Goldstein, L. D., Sapetschnig, A., Weick, E. M., Bouasker, S., Lehrbach, N. J., Simard, M. J., and Miska, E. A. (2012) Science, 337, 574–578.

    PubMed  CAS  Google Scholar 

  105. Ashe, A., Sapetschnig, A., Weick, E. M., Mitchell, J., Bagijn, M. P., Cording, A. C., Doebley, A. L., Goldstein, L. D., Lehrbach, N. J., Le Pen, J., Pintacuda, G., Sakaguchi, A., Sarkies, P., Ahmed, S., and Miska, E. A. (2012) Cell, 150, 88–99.

    PubMed  CAS  Google Scholar 

  106. Ruby, J. G., Jan, C., Player, C., Axtell, M. J., Lee, W., Nusbaum, C., Ge, H., and Bartel, D. P. (2006) Cell, 127, 1193–1207.

    PubMed  CAS  Google Scholar 

  107. Cecere, G., Zheng, G. X., Mansisidor, A. R., Klymko, K. E., and Grishok, A. (2012) Mol. Cell, 47, 734–745.

    PubMed  CAS  Google Scholar 

  108. Gu, W., Lee, H. C., Chaves, D., Youngman, E. M., Pazour, G. J., Conte, D., Jr., and Mello, C. C. (2012) Cell, 151, 1488–1500.

    PubMed  CAS  Google Scholar 

  109. Bushati, N., Stark, A., Brennecke, J., and Cohen, S. M. (2008) Curr. Biol., 18, 501–506.

    PubMed  CAS  Google Scholar 

  110. Mochizuki, K., Fine, N. A., Fujisawa, T., and Gorovsky, M. A. (2002) Cell, 110, 689–699.

    PubMed  CAS  Google Scholar 

  111. Bouhouche, K., Gout, J. F., Kapusta, A., Betermier, M., and Meyer, E. (2011) Nucleic Acids Res., 39, 4249–4264.

    PubMed  CAS  Google Scholar 

  112. Hobson, D. J., Wei, W., Steinmetz, L. M., and Svejstrup, J. Q. (2012) Mol. Cell, 48, 365–374.

    PubMed  CAS  Google Scholar 

  113. Maxwell, P. H., Belote, J. M., and Levis, R. W. (2006) Nucleic Acids Res., 34, 5498–5507.

    PubMed  CAS  Google Scholar 

  114. Minchiotti, G., Contursi, C., and Di Nocera, P. P. (1997) J. Mol. Biol., 267, 37–46.

    PubMed  CAS  Google Scholar 

  115. Shpiz, S., Kwon, D., Rozovsky, Y., and Kalmykova, A. (2009) Nucleic Acids Res., 37, 268–278.

    PubMed  CAS  Google Scholar 

  116. Speek, M. (2001) Mol. Cell. Biol., 21, 1973–1985.

    PubMed  CAS  Google Scholar 

  117. Klattenhoff, C., Bratu, D. P., McGinnis-Schultz, N., Koppetsch, B. S., Cook, H. A., and Theurkauf, W. E. (2007) Dev. Cell, 12, 45–55.

    PubMed  CAS  Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to A. I. Kalmykova.

Additional information

Original Russian Text © I. A. Olovnikov, A. I. Kalmykova, 2013, published in Biokhimiya, 2013, Vol. 78, No. 6, pp. 747–762.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Olovnikov, I.A., Kalmykova, A.I. piRNA clusters as a main source of small RNAs in the animal germline. Biochemistry Moscow 78, 572–584 (2013). https://doi.org/10.1134/S0006297913060035

Download citation

  • Received:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1134/S0006297913060035

Key words

Navigation