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Quantitative aspects of RNA silencing in metazoans

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Abstract

Small regulatory RNAs (microRNAs, siRNAs, and piRNAs) exhibit several unique features that clearly distinguish them from other known gene regulators. Their genomic organization, mode of action, and proposed biological functions raise specific questions. In this review, we focus on the quantitative aspect of small regulatory RNA biology. The original nature of these small RNAs accelerated the development of novel detection techniques and improved statistical methods and promoted new concepts that may unexpectedly generalize to other gene regulators. Quantification of natural phenomena is at the core of scientific practice, and the unique challenges raised by small regulatory RNAs have prompted many creative innovations by the scientific community.

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References

  1. Ghildiyal, M., and Zamore, P. D. (2009) Nat. Rev. Genet., 10, 94–108.

    Article  PubMed  CAS  Google Scholar 

  2. Kozomara, A., and Griffiths-Jones, S. (2011) Nucleic Acids Res., 39, D152–157.

    Article  PubMed  CAS  Google Scholar 

  3. Jackson, A. L., Bartz, S. R., Schelter, J., Kobayashi, S. V., Burchard, J., Mao, M., Li, B., Cavet, G., and Linsley, P. S. (2003) Nat. Biotechnol., 21, 635–637.

    Article  PubMed  CAS  Google Scholar 

  4. Lim, L. P., Lau, N. C., Garrett-Engele, P., Grimson, A., Schelter, J. M., Castle, J., Bartel, D. P., Linsley, P. S., and Johnson, J. M. (2005) Nature, 433, 769–773.

    Article  PubMed  CAS  Google Scholar 

  5. Lewis, B. P., Burge, C. B., and Bartel, D. P. (2005) Cell, 120, 15–20.

    Article  PubMed  CAS  Google Scholar 

  6. Selbach, M., Schwanhausser, B., Thierfelder, N., Fang, Z., Khanin, R., and Rajewsky, N. (2008) Nature, 455, 58–63.

    Article  PubMed  CAS  Google Scholar 

  7. Baek, D., Villen, J., Shin, C., Camargo, F. D., Gygi, S. P., and Bartel, D. P. (2008) Nature, 455, 64–71.

    Article  PubMed  CAS  Google Scholar 

  8. Friedman, R. C., Farh, K. K., Burge, C. B., and Bartel, D. P. (2009) Genome Res., 19, 92–105.

    Article  PubMed  CAS  Google Scholar 

  9. Hutvagner, G., and Zamore, P. D. (2002) Science, 297, 2056–2060.

    Article  PubMed  CAS  Google Scholar 

  10. Doench, J. G., Petersen, C. P., and Sharp, P. A. (2003) Genes Dev., 17, 438–442.

    Article  PubMed  CAS  Google Scholar 

  11. Meister, G., Landthaler, M., Patkaniowska, A., Dorsett, Y., Teng, G., and Tuschl, T. (2004) Mol. Cell, 15, 185–197.

    Article  PubMed  CAS  Google Scholar 

  12. Liu, J., Carmell, M. A., Rivas, F. V., Marsden, C. G., Thomson, J. M., Song, J. J., Hammond, S. M., Joshua-Tor, L., and Hannon, G. J. (2004) Science, 305, 1437–1441.

    Article  PubMed  CAS  Google Scholar 

  13. Brodersen, P., and Voinnet, O. (2009) Nat. Rev. Mol. Cell Biol., 10, 141–148.

    Article  PubMed  CAS  Google Scholar 

  14. Wilson, D., Charoensawan, V., Kummerfeld, S. K., and Teichmann, S. A. (2008) Nucleic Acids Res., 36, D88–92.

    Article  PubMed  CAS  Google Scholar 

  15. Cook, K. B., Kazan, H., Zuberi, K., Morris, Q., and Hughes, T. R. (2011) Nucleic Acids Res., 39, D301–308.

    Article  PubMed  CAS  Google Scholar 

  16. Yin, H., and Lin, H. (2007) Nature, 450, 304–308.

    Article  PubMed  CAS  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

  20. 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.

    Article  PubMed  CAS  Google Scholar 

  21. Haase, A. D., Fenoglio, S., Muerdter, F., Guzzardo, P. M., Czech, B., Pappin, D. J., Chen, C., Gordon, A., and Hannon, G. J. (2010) Genes Dev., 24, 2499–2504.

    Article  PubMed  CAS  Google Scholar 

  22. 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.

    Article  PubMed  CAS  Google Scholar 

  23. Qi, H., Watanabe, T., Ku, H. Y., Liu, N., Zhong, M., and Lin, H. (2011) J. Biol. Chem., 286, 3789–3797.

    Article  PubMed  CAS  Google Scholar 

  24. 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.

    Article  PubMed  CAS  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

  26. Olivieri, D., Senti, K. A., Subramanian, S., Sachidanandam, R., and Brennecke, J. (2012) Mol. Cell, 47, 954–969.

    Article  PubMed  CAS  Google Scholar 

  27. Preall, J. B., Czech, B., Guzzardo, P. M., Muerdter, F., and Hannon, G. J. (2012) RNA, 18, 1446–1457.

    Article  PubMed  CAS  Google Scholar 

  28. Matranga, C., Tomari, Y., Shin, C., Bartel, D. P., and Zamore, P. D. (2005) Cell, 123, 607–620.

    Article  PubMed  CAS  Google Scholar 

  29. Rand, T. A., Petersen, S., Du, F., and Wang, X. (2005) Cell, 123, 621–629.

    Article  PubMed  CAS  Google Scholar 

  30. Miyoshi, K., Tsukumo, H., Nagami, T., Siomi, H., and Siomi, M. C. (2005) Genes Dev., 19, 2837–2848.

    Article  PubMed  CAS  Google Scholar 

  31. Kawamata, T., Seitz, H., and Tomari, Y. (2009) Nat. Struct. Mol. Biol., 16, 953–960.

    Article  PubMed  CAS  Google Scholar 

  32. Yoda, M., Kawamata, T., Paroo, Z., Ye, X., Iwasaki, S., Liu, Q., and Tomari, Y. (2010) Nat. Struct. Mol. Biol., 17, 17–23.

    Article  PubMed  CAS  Google Scholar 

  33. Schwarz, D. S., Hutvagner, G., Du, T., Xu, Z., Aronin, N., and Zamore, P. D. (2003) Cell, 115, 199–208.

    Article  PubMed  CAS  Google Scholar 

  34. Khvorova, A., Reynolds, A., and Jayasena, S. D. (2003) Cell, 115, 209–216.

    Article  PubMed  CAS  Google Scholar 

  35. Lagos-Quintana, M., Rauhut, R., Lendeckel, W., and Tuschl, T. (2001) Science, 294, 853–858.

    Article  PubMed  CAS  Google Scholar 

  36. Lau, N. C., Lim, L. P., Weinstein, E. G., and Bartel, D. P. (2001) Science, 294, 858–862.

    Article  PubMed  CAS  Google Scholar 

  37. Lee, R. C., and Ambros, V. (2001) Science, 294, 862–864.

    Article  PubMed  CAS  Google Scholar 

  38. Griffiths-Jones, S., Saini, H. K., van Dongen, S., and Enright, A. J. (2008) Nucleic Acids Res., 36, D154–158.

    Article  PubMed  CAS  Google Scholar 

  39. Ro, S., Park, C., Young, D., Sanders, K. M., and Yan, W. (2007) Nucleic Acids Res., 35, 5944–5953.

    Article  PubMed  CAS  Google Scholar 

  40. DeWit, E., Linsen, S. E., Cuppen, E., and Berezikov, E. (2009) Genome Res., 19, 2064–2074.

    Article  CAS  Google Scholar 

  41. Chiang, H. R., Schoenfeld, L. W., Ruby, J. G., Auyeung, V. C., Spies, N., Baek, D., Johnston, W. K., Russ, C., Luo, S., Babiarz, J. E., Blelloch, R., Schroth, G. P., Nusbaum, C., and Bartel, D. P. (2010) Genes Dev., 24, 992–1009.

    Article  PubMed  CAS  Google Scholar 

  42. Griffiths-Jones, S., Hui, J. H., Marco, A., and Ronshaugen, M. (2011) EMBO Rep., 12, 172–177.

    Article  PubMed  CAS  Google Scholar 

  43. Okamura, K., Phillips, M. D., Tyler, D. M., Duan, H., Chou, Y. T., and Lai, E. C. (2008) Nat. Struct. Mol. Biol., 15, 354–363.

    Article  PubMed  CAS  Google Scholar 

  44. Okamura, K., Liu, N., and Lai, E. C. (2009) Mol. Cell, 36, 431–444.

    Article  PubMed  CAS  Google Scholar 

  45. Czech, B., Zhou, R., Erlich, Y., Brennecke, J., Binari, R., Villalta, C., Gordon, A., Perrimon, N., and Hannon, G. J. (2009) Mol. Cell, 36, 445–456.

    Article  PubMed  CAS  Google Scholar 

  46. Ghildiyal, M., Xu, J., Seitz, H., Weng, Z., and Zamore, P. D. (2010) RNA, 16, 43–56.

    Article  PubMed  CAS  Google Scholar 

  47. 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.

    Article  PubMed  CAS  Google Scholar 

  48. Kawamura, Y., Saito, K., Kin, T., Ono, Y., Asai, K., Sunohara, T., Okada, T. N., Siomi, M. C., and Siomi, H. (2008) Nature, 453, 793–797.

    Article  PubMed  CAS  Google Scholar 

  49. Tam, O. H., Aravin, A. A., Stein, P., Girard, A., Murchison, E. P., Cheloufi, S., Hodges, E., Anger, M., Sachidanandam, R., Schultz, R. M., and Hannon, G. J. (2008) Nature, 453, 534–538.

    Article  PubMed  CAS  Google Scholar 

  50. Watanabe, T., Totoki, Y., Toyoda, A., Kaneda, M., Kuramochi-Miyagawa, S., Obata, Y., Chiba, H., Kohara, Y., Kono, T., Nakano, T., Surani, M. A., Sakaki, Y., and Sasaki, H. (2008) Nature, 453, 539–543.

    Article  PubMed  CAS  Google Scholar 

  51. Okamura, K., Chung, W. J., Ruby, J. G., Guo, H., Bartel, D. P., and Lai, E. C. (2008) Nature, 453, 803–806.

    Article  PubMed  CAS  Google Scholar 

  52. Czech, B., Malone, C. D., Zhou, R., Stark, A., Schlingeheyde, C., Dus, M., Perrimon, N., Kellis, M., Wohlschlegel, J. A., Sachidanandam, R., Hannon, G. J., and Brennecke, J. (2008) Nature, 453, 798–802.

    Article  PubMed  CAS  Google Scholar 

  53. Sai Lakshmi, S., and Agrawal, S. (2008) Nucleic Acids Res., 36, D173–177.

    Article  PubMed  CAS  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

  55. Lau, N. C., Seto, A. G., Kim, J., Kuramochi-Miyagawa, S., Nakano, T., Bartel, D. P., and Kingston, R. E. (2006) Science, 313, 363–367.

    Article  PubMed  CAS  Google Scholar 

  56. Monteys, A. M., Spengler, R. M., Wan, J., Tecedor, L., Lennox, K. A., Xing, Y., and Davidson, B. L. (2010) RNA, 16, 495–505.

    Article  PubMed  Google Scholar 

  57. Newman, M. A., Thomson, J. M., and Hammond, S. M. (2008) RNA, 14, 1539–1549.

    Article  PubMed  CAS  Google Scholar 

  58. Viswanathan, S. R., Daley, G. Q., and Gregory, R. I. (2008) Science, 320, 97–100.

    Article  PubMed  CAS  Google Scholar 

  59. Heo, I., Joo, C., Cho, J., Ha, M., Han, J., and Kim, V. N. (2008) Mol. Cell, 32, 276–284.

    Article  PubMed  CAS  Google Scholar 

  60. Rybak, A., Fuchs, H., Smirnova, L., Brandt, C., Pohl, E. E., Nitsch, R., and Wulczyn, F. G. (2008) Nat. Cell Biol., 10, 987–993.

    Article  PubMed  CAS  Google Scholar 

  61. Heo, I., Joo, C., Kim, Y. K., Ha, M., Yoon, M. J., Cho, J., Yeom, K. H., Han, J., and Kim, V. N. (2009) Cell, 138, 696–708.

    Article  PubMed  CAS  Google Scholar 

  62. Hagan, J. P., Piskounova, E., and Gregory, R. I. (2009) Nat. Struct. Mol. Biol., 16, 1021–1025.

    Article  PubMed  CAS  Google Scholar 

  63. Thornton, J. E., Chang, H. M., Piskounova, E., and Gregory, R. I. (2012) RNA, 18, 1875–1885.

    Article  PubMed  CAS  Google Scholar 

  64. Lehrbach, N. J., Armisen, J., Lightfoot, H. L., Murfitt, K. J., Bugaut, A., Balasubramanian, S., and Miska, E. A. (2009) Nat. Struct. Mol. Biol., 16, 1016–1020.

    Article  PubMed  CAS  Google Scholar 

  65. Heo, I., Ha, M., Lim, J., Yoon, M. J., Park, J. E., Kwon, S. C., Chang, H., and Kim, V. N. (2012) Cell, 151, 521–532.

    Article  PubMed  CAS  Google Scholar 

  66. Katoh, T., Sakaguchi, Y., Miyauchi, K., Suzuki, T., Kashiwabara, S., Baba, T., and Suzuki, T. (2009) Genes Dev., 23, 433–438.

    Article  PubMed  CAS  Google Scholar 

  67. Burroughs, A. M., Ando, Y., de Hoon, M. J., Tomaru, Y., Nishibu, T., Ukekawa, R., Funakoshi, T., Kurokawa, T., Suzuki, H., Hayashizaki, Y., and Daub, C. O. (2010) Genome Res., 20, 1398–1410.

    Article  PubMed  CAS  Google Scholar 

  68. Ameres, S. L., Horwich, M. D., Hung, J. H., Xu, J., Ghildiyal, M., Weng, Z., and Zamore, P. D. (2010) Science, 328, 1534–1539.

    Article  PubMed  CAS  Google Scholar 

  69. Chatterjee, S., and Großhans, H. (2009) Nature, 461, 546–549.

    Article  PubMed  CAS  Google Scholar 

  70. Das, S. K., Sokhi, U. K., Bhutia, S. K., Azab, B., Su, Z. Z., Sarkar, D., and Fisher, P. B. (2010) Proc. Natl. Acad. Sci. USA, 107, 11948–11953.

    Article  PubMed  CAS  Google Scholar 

  71. 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. J., Luo, S., Schroth, G. P., Carrington, J. C., Bartel, D. P., and Mello, C. C. (2008) Mol. Cell, 31, 67–78.

    Article  PubMed  CAS  Google Scholar 

  72. 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.

    Article  PubMed  CAS  Google Scholar 

  73. Sarot, E., Payen-Groschene, G., Bucheton, A., and Pelisson, A. (2004) Genetics, 166, 1313–1321.

    Article  PubMed  CAS  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

  75. Aravin, A. A., Sachidanandam, R., Girard, A., Fejes-Toth, K., and Hannon, G. J. (2007) Science, 316, 744–747.

    Article  PubMed  CAS  Google Scholar 

  76. 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.

    Article  PubMed  CAS  Google Scholar 

  77. 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.

    Article  PubMed  CAS  Google Scholar 

  78. 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.

    Article  PubMed  CAS  Google Scholar 

  79. Rouget, C., Papin, C., Boureux, A., Meunier, A. C., Franco, B., Robine, N., Lai, E. C., Pelisson, A., and Simonelig, M. (2010) Nature, 467, 1128–1132.

    Article  PubMed  CAS  Google Scholar 

  80. Rajasethupathy, P., Antonov, I., Sheridan, R., Frey, S., Sander, C., Tuschl, T., and Kandel, E. R. (2012) Cell, 149, 693–707.

    Article  PubMed  CAS  Google Scholar 

  81. Chung, W. J., Okamura, K., Martin, R., and Lai, E. C. (2008) Curr. Biol., 18, 795–802.

    Article  PubMed  CAS  Google Scholar 

  82. 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.

    Article  PubMed  CAS  Google Scholar 

  83. 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.

    Article  PubMed  CAS  Google Scholar 

  84. Rozhkov, N. V., Schostak, N. G., Zelentsova, E. S., Yushenova, I. A., Zatsepina, O. G., and Evgen’ev, M. B. (2013) Mol. Biol. Evol., 30, 397–408.

    Article  PubMed  CAS  Google Scholar 

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

    PubMed  Google Scholar 

  86. 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 

  87. Pall, G. S., Codony-Servat, C., Byrne, J., Ritchie, L., and Hamilton, A. (2007) Nucleic Acids Res., 35, e60.

    Article  PubMed  CAS  Google Scholar 

  88. Pall, G. S., and Hamilton, A. J. (2008) Nat. Protoc., 3, 1077–1084.

    Article  PubMed  CAS  Google Scholar 

  89. Tang, F., Hajkova, P., Barton, S. C., Lao, K., and Surani, M. A. (2006) Nucleic Acids Res., 34, e9.

    Article  PubMed  CAS  Google Scholar 

  90. Benes, V., and Castoldi, M. (2010) Methods, 50, 244–249.

    Article  PubMed  CAS  Google Scholar 

  91. Seitz, H., Ghildiyal, M., and Zamore, P. D. (2008) Curr. Biol., 18, 147–151.

    Article  PubMed  CAS  Google Scholar 

  92. Livak, K. J., and Schmittgen, T. D. (2001) Methods, 25, 402–408.

    Article  PubMed  CAS  Google Scholar 

  93. Derveaux, S., Vandesompele, J., and Hellemans, J. (2010) Methods, 50, 227–230.

    Article  PubMed  CAS  Google Scholar 

  94. Han, L., Wen, Z., Lynn, R. C., Baudet, M. L., Holt, C. E., Sasaki, Y., Bassell, G. J., and Zheng, J. Q. (2011) Mol. Brain, 4, 40.

    Article  PubMed  CAS  Google Scholar 

  95. Yin, J. Q., Zhao, R. C., and Morris, K. V. (2008) Trends Biotechnol., 26, 70–76.

    Article  PubMed  CAS  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

  97. Fahlgren, N., Sullivan, C. M., Kasschau, K. D., Chapman, E. J., Cumbie, J. S., Montgomery, T. A., Gilbert, S. D., Dasenko, M., Backman, T. W., Givan, S. A., and Carrington, J. C. (2009) RNA, 15, 992–1002.

    Article  PubMed  CAS  Google Scholar 

  98. Dabney, A., Storey, J. D., and with assistance from Gregory R. Warnes (2011) Q-Value: Q-Value Estimation for False Discovery Rate Control. R package version 1.26.0.

    Google Scholar 

  99. Srivastava, S., and Chen, L. (2010) Nucleic Acids Res., 38, e170.

    Article  PubMed  CAS  Google Scholar 

  100. Langmead, B., Hansen, K. D., and Leek, J. T. (2010) Genome Biol., 11, R83.

    Article  PubMed  Google Scholar 

  101. Anders, S., and Huber, W. (2010) Genome Biol., 11, R106.

    Article  PubMed  CAS  Google Scholar 

  102. Robinson, M. D., McCarthy, D. J., and Smyth, G. K. (2010) Bioinformatics, 26, 139–140.

    Article  PubMed  CAS  Google Scholar 

  103. Tuschl, T., Zamore, P. D., Lehmann, R., Bartel, D. P., and Sharp, P. A. (1999) Genes Dev., 13, 3191–3197.

    Article  PubMed  CAS  Google Scholar 

  104. Haley, B., and Zamore, P. D. (2004) Nat. Struct. Mol. Biol., 11, 599–606.

    Article  PubMed  CAS  Google Scholar 

  105. Yang, D., Lu, H., and Erickson, J. W. (2000) Curr. Biol., 10, 1191–1200.

    Article  PubMed  CAS  Google Scholar 

  106. Mathonnet, G., Fabian, M. R., Svitkin, Y. V., Parsyan, A., Huck, L., Murata, T., Biffo, S., Merrick, W. C., Darzynkiewicz, E., Pillai, R. S., Filipowicz, W., Duchaine, T. F., and Sonenberg, N. (2007) Science, 317, 1764–1767.

    Article  PubMed  CAS  Google Scholar 

  107. Wakiyama, M., Takimoto, K., Ohara, O., and Yokoyama, S. (2007) Genes Dev., 21, 1857–1862.

    Article  PubMed  CAS  Google Scholar 

  108. Thermann, R., and Hentze, M. W. (2007) Nature, 447, 875–878.

    Article  PubMed  CAS  Google Scholar 

  109. Iwasaki, S., Kawamata, T., and Tomari, Y. (2009) Mol. Cell, 34, 58–67.

    Article  PubMed  CAS  Google Scholar 

  110. Aleman, L. M., Doench, J., and Sharp, P. A. (2007) RNA, 13, 385–395.

    Article  PubMed  CAS  Google Scholar 

  111. Fabian, M. R., Sonenberg, N., and Filipowicz, W. (2010) Annu. Rev. Biochem., 79, 351–379.

    Article  PubMed  CAS  Google Scholar 

  112. Chen, P. Y., Manninga, H., Slanchev, K., Chien, M., Russo, J. J., Ju, J., Sheridan, R., John, B., Marks, D. S., Gaidatzis, D., Sander, C., Zavolan, M., and Tuschl, T. (2005) Genes Dev., 19, 1288–1293.

    Article  PubMed  CAS  Google Scholar 

  113. Giraldez, A. J., Mishima, Y., Rihel, J., Grocock, R. J., Van Dongen, S., Inoue, K., Enright, A. J., and Schier, A. F. (2006) Science, 312, 75–79.

    Article  PubMed  CAS  Google Scholar 

  114. Bazzini, A. A., Lee, M. T., and Giraldez, A. J. (2012) Science, 336, 233–237.

    Article  PubMed  CAS  Google Scholar 

  115. Goljanek-Whysall, K., Pais, H., Rathjen, T., Sweetman, D., Dalmay, T., and Munsterberg, A. (2012) J. Cell Sci., 125, 3590–3600.

    Article  PubMed  CAS  Google Scholar 

  116. Ciaudo, C., Servant, N., Cognat, V., Sarazin, A., Kieffer, E., Viville, S., Colot, V., Barillot, E., Heard, E., and Voinnet, O. (2009) PLoS Genet., 5, e1000620.

    Article  PubMed  CAS  Google Scholar 

  117. Bethune, J., Artus-Revel, C. G., and Filipowicz, W. (2012) EMBO Rep., 13, 716–723.

    Article  PubMed  CAS  Google Scholar 

  118. Krol, J., Busskamp, V., Markiewicz, I., Stadler, M. B., Ribi, S., Richter, J., Duebel, J., Bicker, S., Fehling, H. J., Schubeler, D., Oertner, T. G., Schratt, G., Bibel, M., Roska, B., and Filipowicz, W. (2010) Cell, 141, 618–631.

    Article  PubMed  CAS  Google Scholar 

  119. Zeng, Y., Yi, R., and Cullen, B. R. (2003) Proc. Natl. Acad. Sci. USA, 100, 9779–9784.

    Article  PubMed  CAS  Google Scholar 

  120. Yekta, S., Shih, I. H., and Bartel, D. P. (2004) Science, 304, 594–596.

    Article  PubMed  CAS  Google Scholar 

  121. Mullokandov, G., Baccarini, A., Ruzo, A., Jayaprakash, A. D., Tung, N., Israelow, B., Evans, M. J., Sachidanandam, R., and Brown, B. D. (2012) Nat. Methods, 9, 840–846.

    Article  PubMed  CAS  Google Scholar 

  122. Patzel, V., Rutz, S., Dietrich, I., Koberle, C., Scheffold, A., and Kaufmann, S. H. (2005) Nat. Biotechnol., 23, 1440–1444.

    Article  PubMed  CAS  Google Scholar 

  123. Westerhout, E. M., and Berkhout, B. (2007) Nucleic Acids Res., 35, 4322–4330.

    Article  PubMed  CAS  Google Scholar 

  124. Shao, Y., Chan, C. Y., Maliyekkel, A., Lawrence, C. E., Roninson, I. B., and Ding, Y. (2007) RNA, 13, 1631–1640.

    Article  PubMed  CAS  Google Scholar 

  125. Tafer, H., Ameres, S. L., Obernosterer, G., Gebeshuber, C. A., Schroeder, R., Martinez, J., and Hofacker, I. L. (2008) Nat. Biotechnol., 26, 578–583.

    Article  PubMed  CAS  Google Scholar 

  126. Larsson, E., Sander, C., and Marks, D. (2010) Mol. Syst. Biol., 6, 433.

    PubMed  CAS  Google Scholar 

  127. Addo-Quaye, C., Eshoo, T. W., Bartel, D. P., and Axtell, M. J. (2008) Curr. Biol., 18, 758–762.

    Article  PubMed  CAS  Google Scholar 

  128. Wightman, B., Ha, I., and Ruvkun, G. (1993) Cell, 75, 855–862.

    Article  PubMed  CAS  Google Scholar 

  129. Bagga, S., Bracht, J., Hunter, S., Massirer, K., Holtz, J., Eachus, R., and Pasquinelli, A. E. (2005) Cell, 122, 553–563.

    Article  PubMed  CAS  Google Scholar 

  130. Khan, A. A., Betel, D., Miller, M. L., Sander, C., Leslie, C. S., and Marks, D. S. (2009) Nat. Biotechnol., 27, 549–555.

    Article  PubMed  CAS  Google Scholar 

  131. Nakahara, K., Kim, K., Sciulli, C., Dowd, S. R., Minden, J. S., and Carthew, R. W. (2005) Proc. Natl. Acad. Sci. USA, 102, 12023–12028.

    Article  PubMed  CAS  Google Scholar 

  132. Guo, H., Ingolia, N. T., Weissman, J. S., and Bartel, D. P. (2010) Nature, 466, 835–840.

    Article  PubMed  CAS  Google Scholar 

  133. Bonaldi, T., Straub, T., Cox, J., Kumar, C., Becker, P. B., and Mann, M. (2008) Mol. Cell, 31, 762–772.

    Article  PubMed  CAS  Google Scholar 

  134. Snijder, B., and Pelkmans, L. (2011) Nat. Rev. Mol. Cell Biol., 12, 119–125.

    Article  PubMed  CAS  Google Scholar 

  135. Mukherji, S., Ebert, M. S., Zheng, G. X., Tsang, J. S., Sharp, P. A., and van Oudenaarden, A. (2011) Nat. Genet., 43, 854–859.

    Article  PubMed  CAS  Google Scholar 

  136. Huang, L., Mollet, S., Souquere, S., Le Roy, F., Ernoult-Lange, M., Pierron, G., Dautry, F., and Weil, D. (2011) J. Biol. Chem., 286, 24219–24230.

    Article  PubMed  CAS  Google Scholar 

  137. Taft, R. J., Pheasant, M., and Mattick, J. S. (2007) Bioessays, 29, 288–299.

    Article  PubMed  CAS  Google Scholar 

  138. Heimberg, A. M., Sempere, L. F., Moy, V. N., Donoghue, P. C., and Peterson, K. J. (2008) Proc. Natl. Acad. Sci. USA, 105, 2946–2950.

    Article  PubMed  CAS  Google Scholar 

  139. Cacchiarelli, D., Santoni, D., and Bozzoni, I. (2008) RNA Biol., 5, 120–122.

    Article  PubMed  CAS  Google Scholar 

  140. Berezikov, E. (2011) Nat. Rev. Genet., 12, 846–860.

    Article  PubMed  CAS  Google Scholar 

  141. Aburomia, R., Khaner, O., and Sidow, A. (2003) J. Struct. Funct. Genom., 3, 45–52.

    Article  CAS  Google Scholar 

  142. Technau, U. (2008) Nature, 455, 1184–1185.

    Article  PubMed  CAS  Google Scholar 

  143. Valentine, J. W., Collins, A. G., and Meyer, C. P. (1994) Paleobiology, 20, 131–142.

    Google Scholar 

  144. Bell, G., and Mooers, A. O. (1997) Biol. J. Linn Soc., 60, 345–363.

    Article  Google Scholar 

  145. Glansdorff, N., Xu, Y., and Labedan, B. (2009) Res. Microbiol., 160, 522–528.

    Article  PubMed  CAS  Google Scholar 

  146. Lee, R. C., Feinbaum, R. L., and Ambros, V. (1993) Cell, 75, 843–854.

    Article  PubMed  CAS  Google Scholar 

  147. Sandelin, A., Alkema, W., Engstrom, P., Wasserman, W. W., and Lenhard, B. (2004) Nucleic Acids Res., 32, D91–94.

    Article  PubMed  CAS  Google Scholar 

  148. Schmidt, D., Wilson, M. D., Ballester, B., Schwalie, P. C., Brown, G. D., Marshall, A., Kutter, C., Watt, S., Martinez-Jimenez, C. P., Mackay, S., Talianidis, I., Flicek, P., and Odom, D. T. (2010) Science, 328, 1036–1040.

    Article  PubMed  CAS  Google Scholar 

  149. Bartel, D. P., and Chen, C. Z. (2004) Nat. Rev. Genet., 5, 396–400.

    Article  PubMed  CAS  Google Scholar 

  150. Seitz, H. (2009) Curr. Biol., 19, 870–873.

    Article  PubMed  CAS  Google Scholar 

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  1. A. M. Sergeeva

    Present address: Institute of Molecular Genetics, Russian Academy of Sciences, pl. Kurchatova 2, 123182, Moscow, Russia

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  1. IGH du CNRS (UPR 1142), 141 rue de la Cardonille, 34396, Montpellier, France

    A. M. Sergeeva, N. Pinzón Restrepo & H. Seitz

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Published in Russian in Biokhimiya, 2013, Vol. 78, No. 6, pp. 795–810.

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Sergeeva, A.M., Pinzón Restrepo, N. & Seitz, H. Quantitative aspects of RNA silencing in metazoans. Biochemistry Moscow 78, 613–626 (2013). https://doi.org/10.1134/S0006297913060072

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