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The Fundamentals of miRNA Biology: Structure, Biogenesis, and Regulatory Functions

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Abstract

Epigenetic regulation of gene expression plays a key role in controlling many cellular processes. One essential element of such regulation are miRNAs—a class of short non-coding RNAs. The miRNAs were first discovered in 1993, but their active investigation was not started until early 2000s. Recent data show that miRNAs regulate the expression of at least half of human genes. Being involved in regulation of numerous target genes implicated in cell functioning, miRNA activity is critical for normal human development and function, while dysregulation of miRNA is a hallmark of various pathophysiological processes. Current review introduces the reader to the main stages of miRNA life cycle in human cells. The origins of cellular miRNAs, their biogenesis, functions, and regulation of their activity are discussed. The publication is aimed at readers looking for first insights into the intricacies of miRNA biology, but can also serve as a source of reference material for specialists in the area.

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REFERENCES

  1. Lee, R.C., Feinbaum, R.L., and Ambros, V., Cell, 1993, vol. 75, no. 5, pp. 843–854.

    Article  CAS  PubMed  Google Scholar 

  2. Reinhart, B.J., Slack, F.J., Basson, M., Pasquinelli, A.E., Bettinger, J.C., Rougvie, A.E., Horvitz, H.R., and Ruvkun, G., Nature, 2000, vol. 403, no. 6772, pp. 901–906.

    Article  CAS  PubMed  Google Scholar 

  3. Lee, R.C., Ambros, V., Erdmann, V.A., Lee, R.C., Feinbaum, R.L., Ambros, V., Reinhart, B., Wightman, B., Ha, I., Ruvkun, G., Pasquinelli, A.E., Grishok, A., Hutvagner, G., Sharp, P.A., Kent, W.J., et al., Science, 2001, vol. 294, no. 5543, pp. 862–864.

    Article  CAS  PubMed  Google Scholar 

  4. Lagos-Quintana, M., Rauhut, R., Lendeckel, W., Tuschl, T., Elbashir, S.M., Lendeckel, W., Tuschl, T., Hamilton, A.J., Baulcombe, D.C., Hammond, S.M., Bernstein, E., Beach, D., Hannon, G.J., Zamore, P.D., Tuschl, T., et al., Science, 2001, vol. 294, no. 5543, pp. 853–858.

    Article  CAS  PubMed  Google Scholar 

  5. Lau, N.C., Lim, L.P., Weinstein, E.G., Bartel, D.P., Lee, R.C., Feinbaum, R.L., Ambros, V., Wightman, B., Ha, I., Ruvkun, G., Reinhart, B.J., Moss, E.G., Lee, R.C., Ambros, V., and Slack, F.J., et al., Science, 2001, vol. 294, no. 5543, pp. 858–862.

    Article  CAS  PubMed  Google Scholar 

  6. Axtell, M.J., Westholm, J.O., and Lai, E.C., Genome Biol., 2011, vol. 12, no. 4, p. 221.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  7. Griffiths-Jones, S., Saini, H.K., Dongen, S., and Enright, A.J., Nucleic Acids Res., 2008, vol. 36, pp. D154–D158.

  8. Kozomara, A. and Griffiths-Jones, S., Nucleic Acids Res., 2014, vol. 42, Database issue, pp. D68–D73.

  9. Ying, H., Kimmelman, A.C., Lyssiotis, C.A., Hua, S., Chu, G.C., Fletcher-Sananikone, E., Locasale, J.W., Son, J., Zhang, H., Coloff, J.L., Yan, H., Wang, W., Chen, S., Viale, A., and Zheng, H., et al., Cell, 2012, vol. 149, no. 3, pp. 656–670.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  10. Han, B.W., Wang, W., Li, C., Weng, Z., and Zamore, P.D., Science, 2015, vol. 348, no. 6236, pp. 817–821.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  11. Hyun, S., Int. J. Mol. Sci., 2017, vol. 18, no. 5, p. 1028.

  12. Herrmann, A., Priceman, S.J., Swiderski, P., Kujawski, M., Xin, H., Cherryholmes, G.A., Zhang, W., Zhang, C., Lahtz, C., Kowolik, C., Forman, S.J., Kortylewski, M., and Yu, H., J. Clin. Invest., 2014, vol. 124, no. 7, pp. 2977–2987.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  13. Kang, S., Kang, D., Bakhtiar, Ul., Islam, S.M., Je, S., Kim, J.-H., and Song, J.J., Cell. Signal., 2015, vol. 27, no. 6, pp. 1214–1224.

    Article  CAS  PubMed  Google Scholar 

  14. Taft, R.J., Hawkins, P.G., Mattick, J.S., and Morris, K.V., Epigenetics Chromatin, 2011, vol. 4, p. 13.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  15. Ambros, V., Bartel, B., Bartel, D.P., Burge, C.B., Carrington, J.C., Chen, X., Dreyfuss, G., Eddy, S.R., Griffiths-Jones, S., Marshall, M., Matzke, M., Ruvkun, G., and Tuschl, T., RNA, 2003, vol. 9, no. 3, pp. 277–279.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  16. Bartel, D.P., Cell, 2004, vol. 116, no. 2, pp. 281–297.

    Article  CAS  PubMed  Google Scholar 

  17. Fabian, M.R., Sonenberg, N., and Filipowicz, W., Annu. Rev. Biochem., 2010, vol. 79, no. 1, pp. 351–379.

    Article  CAS  PubMed  Google Scholar 

  18. Berezikov, E., Nat. Rev. Genet., 2011, vol. 12, no. 12, pp. 846–860.

    Article  CAS  PubMed  Google Scholar 

  19. Taft, R.J., Pheasant, M., and Mattick, J.S., BioEssays, 2007, vol. 29, no. 3, pp. 288–299.

    Article  CAS  PubMed  Google Scholar 

  20. Grimson, A., Srivastava, M., Fahey, B., Woodcroft, B.J., Chiang, H.R., King, N., Degnan, B.M., Rokhsar, D.S., and Bartel, D.P., Nature, 2008, vol. 455, no. 7217, pp. 1193–1197.

    Article  CAS  PubMed  Google Scholar 

  21. Griffiths-Jones, S., Grocock, R.J., Dongen, S., Bateman, A., and Enright, A.J., Nucleic Acids Res., 2006, vol. 34, Database issue, pp. D140–D144.

  22. Umu, S.U., Langseth, H., Bucher-Johannessen, C., Fromm, B., Keller, A., Meese, E., Lauritzen, M., Leithaug, M., Lyle, R., and Rounge, T.B., RNA Biol., 2017, pp. 1–9.

  23. Fromm, B., Billipp, T., Peck, L.E., Johansen, M., Tarver, J.E., King, B.L., Newcomb, J.M., Sempere, L.F., Flatmark, K., Hovig, E., and Peterson, K.J., Annu. Rev. Genet., 2015, vol. 23, no. 49, pp. 213–242.

    Article  CAS  Google Scholar 

  24. Rodriguez, A., Griffiths-Jones, S., Ashurst, J.L., and Bradley, A., Genome Res., 2004, vol. 14, no. 10A, pp. 1902–1910.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  25. Saini, H.K., Enright, A.J., and Griffiths-Jones, S., BMC Genomics, 2008, vol. 9, p. 564.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  26. Campo-Paysaa, F., Simon, M., Cameron, R.A., Peterson, K.J., and Schubert, M., Evol. Dev., 2011, vol. 13, no. 1, pp. 15–27.

    Article  CAS  PubMed  Google Scholar 

  27. Colaiacovo, M., Lamontanara, A., Bernardo, L., Alberici, R., Crosatti, C., Giusti, L., Cattivelli, L., and Faccioli, P., Biol. Direct., 2012, vol. 7, p. 15.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  28. Saini, H.K., Griffiths-Jones, S., and Enright, A.J., Proc. Natl. Acad. Sci. U. S. A., 2007, vol. 104, no. 45, pp. 17719–17724.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  29. Corcoran, D.L., Pandit, K.V., Gordon, B., Bhattacharjee, A., Kaminski, N., and Benos, P.V., PLoS One, 2009, vol. 4, no. 4. e5279.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  30. Ramalingam, P., Palanichamy, J.K., Singh, A., Das, P., Bhagat, M., Kassab, M.A., Sinha, S., and Chattopadhyay, P., RNA, 2014, vol. 20, no. 1, pp. 76–87.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  31. Ozsolak, F., Poling, L.L., Wang, Z., Liu, H., Liu, X.S., Roeder, R.G., Zhang, X., Song, J.S., and Fisher, D.E., Genes Dev., 2008, vol. 22, no. 22, pp. 3172–3183.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  32. Monteys, A.M., Spengler, R.M., Wan, J., Tecedor, L., Lennox, K.A., Xing, Y., and Davidson, B.L., RNA, 2010, vol. 16, no. 3, pp. 495–505.

    Article  PubMed  PubMed Central  Google Scholar 

  33. Baskerville, S. and Bartel, D.P., RNA, 2005, vol. 11, no. 3, pp. 241–247.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  34. Yuan, Z., Sun, X., Liu, H., and Xie, J., PLoS One, 2011, vol. 6, no. 3. e17666.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  35. Friedländer, M.R., Mackowiak, S.D., Li, N., Chen, W., and Rajewsky, N., Nucleic Acids Res., 2012, vol. 40, no. 1, pp. 37–52.

    Article  PubMed  CAS  Google Scholar 

  36. Ender, C., Krek, A., Friedlander, M.R., Beitzinger, M., Weinmann, L., Chen, W., Pfeffer, S., Rajewsky, N., and Meister, G., Mol. Cell, 2008, vol. 32, no. 4, pp. 519–528.

    Article  CAS  PubMed  Google Scholar 

  37. Pederson, T., RNA, 2010, vol. 16, no. 10, pp. 1865–9.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  38. Ono, M., Scott, M.S., Yamada, K., Avolio, F., Barton, G.J., and Lamond, A.I., Nucleic Acids Res., 2011, vol. 39, no. 9, pp. 3879–3891.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  39. Devor, E.J., J. Hered., 2006, vol. 97, no. 2, pp. 186–190.

    Article  CAS  PubMed  Google Scholar 

  40. Lewis, B.P., Shih, I.-H., Jones-Rhoades, M.W., and Bartel, D.P., Cell, 2003, vol. 115, pp. 787–798.

    Article  CAS  PubMed  Google Scholar 

  41. Lim, L.P., Glasner, M.E., Yekta, S., Burge, C.B., and Bartel, D.P., Science, 2003, vol. 299, no. 5612, p. 1540.

    Article  CAS  PubMed  Google Scholar 

  42. Shin, C., Nam, J.-W., Farh, K.K.-H., Chiang, H.R., Shkumatava, A., and Bartel, D.P, Mol. Cell, 2010, vol. 38, no. 6, pp. 789–802.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  43. Farh, K.K.-H, Science, 2005, vol. 310, no. 5755, pp. 1817–1821.

    Article  CAS  PubMed  Google Scholar 

  44. Stark, A., Brennecke, J., Bushati, N., Russell, R.B., and Cohen, S.M., Cell, 2005, vol. 123, no. 6, pp. 1133–1146.

    Article  CAS  PubMed  Google Scholar 

  45. Sood, P., Krek, A., Zavolan, M., Macino, G., and Rajewsky, N., Proc. Natl. Acad. Sci. U. S. A., 2006, vol. 103, no. 8, pp. 2746–2751.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  46. Daugaard, I. and Hansen, T.B., Trends Genet., 2017, vol. 33, no. 3, pp. 208–219.

    Article  CAS  PubMed  Google Scholar 

  47. Lee, Y., Kim, M., Han, J., Yeom, K.-H., Lee, S., Baek, S.H., and Kim, V.N., EMBO J., 2004, vol. 23, no. 20, pp. 4051–4060.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  48. Cai, X., Hagedorn, C.H., and Cullen, B.R., RNA, 2004, vol. 10, no. 12, pp. 1957–1966.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  49. Ballarino, M., Pagano, F., Girardi, E., Morlando, M., Cacchiarelli, D., Marchioni, M., Proudfoot, N.J., and Bozzoni, I., Mol. Cell. Biol., 2009, vol. 29, no. 20, pp. 5632–5638.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  50. Borchert, G.M., Lanier, W., and Davidson, B.L., Nat. Struct. Mol. Biol., 2006, vol. 13, no. 12, pp. 1097–1101.

    Article  CAS  PubMed  Google Scholar 

  51. Liang, Y., Ridzon, D., Wong, L., and Chen, C., BMC Genomics, 2007, vol. 8, p. 166.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  52. Chaulk, S.G., Thede, G.L., Kent, O.A., Xu, Z., Gesner, E., Veldhoen, R.A., Khanna, S.K., Goping, I.S., Macmillan, A.M., Mendell, J.T., Young, H., Fahlman, R.P., and Glover, M.J.N., RNA Biol., 2011, vol. 8, no. 6, pp. 1105–1114.

    Article  CAS  PubMed  Google Scholar 

  53. Chakraborty, S., Mehtab, S., Patwardhan, A., and Krishnan, Y., RNA, 2012, vol. 18, no. 5, pp. 1014–1028.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  54. Denli, A.M., Tops, B.B.J., Plasterk, R.H.A., Ketting, R.F., and Hannon, G.J., Nature, 2004, vol. 432, no. 7014, pp. 231–235.

    Article  CAS  PubMed  Google Scholar 

  55. Lee, Y., Ahn, C., Han, J., Choi, H., Kim, J., Yim, J., Lee, J., Provost, P., Rå Dmark, O., Kim, S., and Kim, V.N. Nature, 2003, vol. 425, no. 6956, pp. 415–419.

  56. Roth, B.M., Ishimaru, D., and Hennig, M., J. Biol. Chem., 2013, vol. 288, no. 37, pp. 26785–26799.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  57. Han, J., Lee, Y., Yeom, K.-H., Nam, J.-W., Heo, I., Rhee, J.-K., Sohn, S.Y., Cho, Y., Zhang, B.-T., and Kim, V.N., Cell, 2006, vol. 125, no. 5, pp. 887–901.

    Article  CAS  PubMed  Google Scholar 

  58. Maa, H., Wub, Y., Choia, J.-G., and Wua, H., Proc. Natl. Acad. Sci. U. S. A., 2013, vol. 110, no. 51, pp. 20687–20692.

    Article  CAS  Google Scholar 

  59. Castilla-Llorente, V., Nicastro, G., and Ramos, A., Biochem. Soc. Trans., 2013, vol. 41, no. 4, pp. 861–865.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  60. Chen, C.-Z., Li, L., Lodish, H.F., and Bartel, D.P., Science, 2004, vol. 303, no. 5654, pp. 83–86.

    Article  CAS  PubMed  Google Scholar 

  61. Fang, W. and Bartel, D.P., Mol. Cell, 2015, vol. 60, pp. 131–145.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  62. Auyeung, V.C., Ulitsky, I., McGeary, S.E., and Bartel, D.P., Cell, 2013, vol. 152, no. 4, pp. 844–858.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  63. Nicholson, A.W., Wiley Interdiscip. Rev. RNA, 2014, vol. 5, no. 1, pp. 31–48.

    Article  CAS  PubMed  Google Scholar 

  64. Zeng, Y. and Cullen, B.R., Nucleic Acids Res., 2004, vol. 32, no. 16, pp. 4776–4785.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  65. Lund, E., Guttinger, S., Calado, A., Dahlberg, J.E., and Kutay, U., Science, 2004, vol. 303, no. 5654, pp. 95–98.

    Article  CAS  PubMed  Google Scholar 

  66. Yi, R., Qin, Y., Macara, I.G., and Cullen, B.R., Genes Dev., 2003, vol. 17, no. 24, pp. 3011–3016.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  67. Bartel, D.P., Cell, 2009, vol. 136, no. 2, pp. 215–233.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  68. Park, J.-E., Heo, I., Tian, Y., Simanshu, D.K., Chang, H., Jee, D., Patel, D.J., and Kim, V.N., Nature, 2011, vol. 475, no. 7355, pp. 201–205.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  69. Gu, S., Jin, L., Zhang, Y., Huang, Y., Zhang, F., Valdmanis, P.N., and Kay, M.A., Cell, 2012, vol. 151, no. 4, pp. 900–911.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  70. Zhou, K., Li, F., Repic, A., Brooks, A., Cande, Z., Adams, P., and Doudna, J., Science, 2006, vol. 311, no. 5758, pp. 195–198.

    Article  PubMed  CAS  Google Scholar 

  71. Zhou, K. and Doudna, J.A., Nat. Struct. Mol. Biol., 2007, vol. 14, no. 10, pp. 934–940.

    Article  PubMed  CAS  Google Scholar 

  72. Provost, P., Dishart, D., Doucet, J., Frendewey, D., Samuelsson, B., and Rådmark, O., EMBO J., 2002, vol. 21, no. 21, pp. 5864–5874.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  73. Hammond, S.M., FEBS Lett., 2005, vol. 579, no. 26, pp. 5822–5829.

    Article  CAS  PubMed  Google Scholar 

  74. Zhang, H., Kolb, F.A., Brondani, V., Billy, E., and Filipowicz, W., EMBO J., 2002, vol. 21, no. 21, pp. 5875–5885.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  75. Kawamata, T. and Tomari, Y., Trends Biochem. Sci., 2010, vol. 35, no. 7, pp. 368–376.

  76. Nakanishi, K., Wiley Interdiscip. Rev. RNA, 2016, vol. 7, no. 5, pp. 637–660.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  77. Schirle, N.T. and Macrae, I.J., Science, 2012, vol. 336, no. 6084, pp. 1037–1040.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  78. Elkayam, E., Kuhn, C.-D., Tocilj, A., Haase, A.D., Greene, E.M., Hannon, G.J., and Joshua-Tor, L., Cell, 2012, vol. 150, no. 1, pp. 100–110.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  79. Jiang, H., Sheong, F.K., Zhu, L., Gao, X., Bernauer, J., Huang, X., PLOS Comput. Biol., vol. 11, no. 7. e1004404.

  80. Jinek, M. and Doudna, J.A., Nature, 2009, vol. 457.

  81. Swarts, D.C., Makarova, K., Wang, Y., Nakanishi, K., Ketting, R.F., Koonin, E.V., Patel, D.J., and Van der Oost, J., Nat. Struct. Mol. Biol., 2014, vol. 21, no. 9, pp. 743–753.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  82. Faehnle, C.R., Elkayam, E., Haase, A.D., Hannon, G.J., Joshua-Tor, L., and Keck, W.M., Cell Rep., 2013, vol. 3, no. 6, pp. 1901–1909.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  83. Dueck, A., Ziegler, C., Eichner, A., Berezikov, E., and Meister, G., Nucleic Acids Res., 2012, vol. 40, no. 19, pp. 9850–9862.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  84. Iwasaki, S., Kobayashi, M., Yoda, M., Sakaguchi, Y., Katsuma, S., Suzuki, T., and Tomari, Y., 2010, Mol. Cell, vol. 39, no. 2, pp. 292–299.

  85. Iwasaki, S., Sasaki, H.M., Sakaguchi, Y., Suzuki, T., Tadakuma, H., and Tomari, Y., Nature, 2015, vol. 521, no. 7553, pp. 533–536.

    Article  CAS  PubMed  Google Scholar 

  86. Miyoshi, T., Takeuchi, A., Siomi, H., and Siomi, M.C., Nat. Struct. Mol. Biol., 2010, vol. 17, no. 8, pp. 1024–1026.

    Article  CAS  PubMed  Google Scholar 

  87. Khvorova, A., Reynolds, A., Jayasena, S.D., Bartel, D.P., Aronin, N., Zamore, P.D., Rappsilber, J., Mann, M., Dreyfuss, G., and Mello, C.C., et al., Cell, 2003, vol. 115, no. 2, pp. 209–216.

    Article  CAS  PubMed  Google Scholar 

  88. Schwarz, D.S., Hutvagner, G., Du, T., Xu, Z., Aronin, N., and Zamore, P.D., Cell, 2003, vol. 115, no. 2, pp. 199–208.

    Article  CAS  PubMed  Google Scholar 

  89. Suzuki, H.I., Katsura, A., Yasuda, T., Ueno, T., Mano, H., Sugimoto, K., and Miyazono, K., Nat. Struct. Mol. Biol., 2015, vol. 22, no. 7, pp. 512–521.

    Article  CAS  PubMed  Google Scholar 

  90. Nakanishi, K., Weinberg, D.E., Bartel, D.P., and Patel, D.J., Nature, 2012, vol. 486, no. 7403, pp. 368–374.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  91. Kwak, P.B. and Tomari, Y., Nat. Struct. Mol. Biol., 2012, vol. 19, no. 2.

  92. Yang, J.-S. and Lai, E.C., Mol. Cell, 2011, vol. 43, no. 6, pp. 892–903.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  93. Berezikov, E., Chung, W.-J., Willis, J., Cuppen, E., and Lai, E.C., Mol. Cell, 2007, vol. 28, no. 2, pp. 328–336.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  94. Ruby, J.G., Jan, C.H., and Bartel, D.P., Nature, 2007, vol. 448, no. 7149, pp. 83–86.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  95. Okamura, K., Hagen, J.W., Duan, H., Tyler, D.M., and Lai, E.C., Cell, 2007, vol. 130, no. 1, pp. 89–100.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  96. Rasmussen, K.D., Simmini, S., Abreu-Goodger, C., Bartonicek, N., Giacomo, M.Di., Bilbao-Cortes, D., Horos, R., Lindern, M., Von Enright, A.J., and O’Carroll, D., J. Exp. Med., 2010, vol. 207, no. 7, pp. 1351–1358.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  97. Cheloufi, S., Santos, C.O.Dos., Chong, M.M.W., and Hannon, G.J., Nature, 2010, vol. 465, no. 7298, pp. 584–589.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  98. Cifuentes, D., Xue, H., Taylor, D.W., Patnode, H., Mishima, Y., Cheloufi, S., Ma, E., Mane, S., Hannon, G.J., Lawson, N.D., Wolfe, S.A., and Giraldez, A.J., Science, 2010, vol. 328, no. 5986, pp. 1694–1698.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  99. Yoda, M., Cifuentes, D., Izumi, N., Sakaguchi, Y., Suzuki, T., Giraldez, A.J., and Tomari, Y., Cell Rep., vol. 5, no. 3, pp. 715–726.

  100. Kim, Y.-K., Kim, B., and Kim, V.N., Proc. Natl. Acad. Sci. U. S. A., 2016, vol. 113, no. 13, pp. E1881–E1889.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  101. Martinez, I., Hayes, K.E., Barr, J.A., Harold, A.D., Xie, M., Bukhari, S.I.A., Vasudevan, S., Steitz, J.A., and DiMaio, D., Proc. Natl. Acad. Sci. U. S. A., 2017, vol. 114, no. 25, pp. E4961–E4970.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  102. Bernstein, E., Kim, S.Y., Carmell, M.A., Murchison, E.P., Alcorn, H., Li, M.Z., Mills, A.A., Elledge, S.J., Anderson, K.V., and Hannon, G.J., Nat. Genet., 2003, vol. 35, no. 3, pp. 215–217.

    Article  CAS  PubMed  Google Scholar 

  103. Davis, T.H., Cuellar, T.L., Koch, S.M., Barker, A.J., Harfe, B.D., McManus, M.T., and Ullian, E.M., J. Neurosci., 2008, vol. 28, no. 17, pp. 4322–4330.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  104. Babiarz, J.E., Hsu, R., Melton, C., Thomas, M., Ullian, E.M., and Blelloch, R., RNA, 2011, vol. 17, no. 8, pp. 1489–1501.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  105. Chong, M.M.W., Zhang, G., Cheloufi, S., Neubert, T.A., Hannon, G.J., and Littman, D.R., Genes Dev., 2010, vol. 24, no. 17, pp. 1951–1960.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  106. Ambros, V., Nature, 2004, vol. 431, no. 7006, pp. 350–355.

    Article  CAS  PubMed  Google Scholar 

  107. Kloosterman, W.P. and Plasterk, R.H.A., Dev. Cell, 2006, vol. 11, no. 4, pp. 441–450.

    Article  CAS  PubMed  Google Scholar 

  108. Bartel, D.P., Cell, 2018, vol. 173.

  109. Almeida, M.I., Reis, R.M., and Calin, G.A., Mutat. Res. Mol. Mech. Mutagen., 2011, vol. 717, nos. 1–2, pp. 1–8.

    Article  CAS  Google Scholar 

  110. Bartel, D.P. and Chen, C.-Z., Nat. Rev. Genet., 2004, vol. 5, no. 5, pp. 396–400.

    Article  CAS  PubMed  Google Scholar 

  111. Selbach, M., Schwanhausser, B., Thierfelder, N., Fang, Z., Khanin, R., and Rajewsky, N., Nature, 2008, vol. 455, no. 7209, pp. 58–63.

    Article  CAS  PubMed  Google Scholar 

  112. Baek, D., Villén, J., Shin, C., Camargo, F.D., Gygi, S.P., and Bartel, D.P., Nature, 2008, vol. 455, no. 7209, pp. 64–71.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  113. Mukherji, S., Ebert, M.S., Zheng, G.X., Tsang, J.S., Sharp, P.A., and Van Oudenaarden, A. Nat. Genet., vol. 43, no. 9, pp. 854–859.

  114. Fang, Z. and Rajewsky, N., PLoS One, 2011, vol. 6, no. 3. e18067.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  115. Bagga, S., Bracht, J., Hunter, S., Massirer, K., Holtz, J., Eachus, R., and Pasquinelli, A.E., Cell, 2005, vol. 122, pp. 553–563.

    Article  CAS  PubMed  Google Scholar 

  116. Leoni, G. and Tramontano, A., Nucleic Acids Res., 2016, vol. 44, no. 9. e82.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  117. Afonso-Grunz, F. and Muller, S., Cell. Mol. Life Sci., 2015, vol. 72, no. 16, pp. 3127–3141.

    Article  CAS  PubMed  Google Scholar 

  118. Lewis, B.P., Burge, C.B., and Bartel, D.P., Cell, 2005, vol. 120, no. 1, pp. 15–20.

    Article  CAS  PubMed  Google Scholar 

  119. Friedman, R.C., Farh, K.K.-H., Burge, C.B., and Bartel, D.P., Genome Res., 2009, vol. 19, no. 1, pp. 92–105.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  120. Royo, F., Zuñiga-Garcia, P., Sanchez-Mosquera, P., Egia, A., Perez, A., Loizaga, A., Arceo, R., Lacasa, I., Rabade, A., Arrieta, E., Bilbao, R., Unda, M., Carracedo, A., and Falcon-Perez, J.M., J. Extracell. Vesicles, 2016, vol. 5, p. 29497.

    Article  PubMed  CAS  Google Scholar 

  121. Garcia, D.M., Baek, D., Shin, C., Bell, G.W., Grimson, A., and Bartel, D.P., Nat. Struct. Mol. Biol., 2011, vol. 18, no. 10, pp. 1139–1146.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  122. Grimson, A., Nat. Methods, 2010, vol. 7, no. 10, pp. 795–797.

    Article  CAS  PubMed  Google Scholar 

  123. Chi, S.W., Hannon, G.J., and Darnell, R.B., Nat. Struct. Mol. Biol., 2012, vol. 19, no. 3, pp. 321–327.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  124. Helwak, A., Kudla, G., Dudnakova, T., and Tollervey, D., Cell, 2013, vol. 153, no. 3, pp. 654–665.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  125. Moore, M.J., Scheel, T.K.H., Luna, J.M., Park, C.Y., Fak, J.J., Nishiuchi, E., Rice, C.M., and Darnell, R.B., Nat. Commun., 2015, vol. 6, p. 8864.

    Article  CAS  PubMed  Google Scholar 

  126. Loeb, G.B., Khan, A.A., Canner, D., Hiatt, J.B., Shendure, J., Darnell, R.B., Leslie, C.S., and Rudensky, A.Y., Mol. Cell, 2012, vol. 48, no. 5, pp. 760–770.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  127. Hafner, M., Lianoglou, S., Tuschl, T., and Betel, D., Methods, 2012, vol. 58, no. 2, pp. 94–105.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  128. Martin, H.C., Wani, S., Steptoe, A.L., Krishnan, K., Nones, K., Nourbakhsh, E., Vlassov, A., Grimmond, S.M., and Cloonan, N., Genome Biol., 2014, vol. 15, no. 3, p. R51.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  129. 129. Grimson, A., Farh, K.K.-H., Johnston, W.K., Garrett-Engele, P., Lim, L.P., and Bartel, D.P., Mol. Cell, 2007, vol. 27, no. 1, pp. 91–105.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  130. Valencia-Sanchez, M.A., Genes Dev., 2006, vol. 20, no. 5, pp. 515–524.

    Article  CAS  PubMed  Google Scholar 

  131. Chou, C.H., Chang, N.W., Shrestha, S., Hsu, S.Da., Lin, Y.L., Lee, W.H., Yang, C.D., Hong, H.C., Wei, T.Y., Tu, S.J., Tsai, T.R., Ho, S.Y., Jian, T.Y., Wu, H.Y., and Chen, P.R., et al., Nucleic Acids Res., 2016, vol. 44, no. D1, pp. D239–D247.

  132. Gam, J.J., Babb, J., and Weiss, R., Nat. Commun., 2018, vol. 9, no. 1, p. 2430.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  133. Jens, M. and Rajewsky, N., Nat. Rev. Genet., 2015, vol. 16, no. 2, pp. 113–126.

    Article  CAS  PubMed  Google Scholar 

  134. Guo, L., Zhao, Y., Yang, S., Zhang, H., and Chen, F., Biomed. Res. Int., 2014, vol. 2014, pp. 1–8.

    Google Scholar 

  135. Rong, D., Sun, H., Li, Z., Liu, S., Dong, C., Fu, K., Tang, W., and Cao, H., Oncotarget, 2017, vol. 8, pp. 73271–73281.

  136. Yao, B., Li, S., and Chan, E.K.L., Ten Years Prog. GW/P Body Res., Adv. Exp. Med. Biol., 2013, vol. 768, pp. 71–96.

    Article  CAS  PubMed  Google Scholar 

  137. Huntzinger, E., Kuzuoğlu-Öztürk, D., Braun, J.E., Eulalio, A., Wohlbold, L., and Izaurralde, E., Nucleic Acids Res., 2013, vol. 41, no. 2, pp. 978–994.

    Article  CAS  PubMed  Google Scholar 

  138. Collart, M.A. and Panasenko, O.O., Gene, 2012, vol. 492, no. 1, pp. 42–53.

    Article  CAS  PubMed  Google Scholar 

  139. Wolf, J. and Passmore, L.A., Biochem. Soc. Trans., 2014, vol. 42, no. 1, pp. 184–187.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  140. Presnyak, V. and Coller, J., Biochim. Biophys. Acta,Gene Regul. Mech., 2013, vol. 1829, no. 8, pp. 817–823.

    CAS  Google Scholar 

  141. Morozova, N., Zinovyev, A., Nonne, N., Pritchard, L.-L., Gorban, A.N., and Harel-Bellan, A., RNA, 2012, vol. 18, no. 9, pp. 1635–1655.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  142. Wilczynska, A. and Bushell, M., Cell Death Differ., 2015, vol. 22, no. 1, pp. 22–33.

    Article  CAS  PubMed  Google Scholar 

  143. Fukaya, T. and Tomari, Y., Mol. Cell, 2012, vol. 48, pp. 825–836.

    Article  CAS  PubMed  Google Scholar 

  144. Larsson, O. and Nadon, R., Translation, 2013, vol. 1, no. 1, e24557.

  145. Fabian, M.R., Mathonnet, G., Sundermeier, T., Mathys, H., Zipprich, J.T., Svitkin, Y.V., Rivas, F., Jinek, M., Wohlschlegel, J., Doudna, J.A., Chen, C.Y.A., Shyu, A.Bin., Yates, J.R., Hannon, G.J., Filipowicz, W., et al., Mol. Cell, 2009, vol. 35, no. 6, pp. 868–880.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  146. Djuranovic, S., Nahvi, A., and Green, R., Science, 2012, vol. 336, no. 6078, pp. 237–240.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  147. Eichhorn, S.W., Guo, H., Mcgeary, S.E., Rodriguez-Mias, R.A., Shin, C., Baek, D., Hsu, S.-H., Ghoshal, K., Villen, J., and Bartel, D.P., Mol. Cell, 2014, vol. 56, no. 1, pp. 104–115.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  148. Meijer, H.A., Kong, Y.W., Lu, W.T., Wilczynska, A., Spriggs, R.V., Robinson, S.W., Godfrey, J.D., Willis, A.E., and Bushell, M., Science, 2013, vol. 340, no. 6128, pp. 82–85.

    Article  CAS  PubMed  Google Scholar 

  149. Rehwinkel, J., RNA, 2005, vol. 11, no. 11, pp. 1640–1647.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  150. Fukaya, T. and Tomari, Y., EMBO J., 2011, vol. 30426, pp. 4998–5009.

    Article  CAS  Google Scholar 

  151. Yang, Z. and Wang, L., Cell Biosci., 2011, vol. 1, no. 1, p. 31.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  152. Finnegan, E.F. and Pasquinelli, A.E., Crit. Rev. Biochem. Mol. Biol., 2013, vol. 48, no. 1, pp. 51–68.

    Article  CAS  PubMed  Google Scholar 

  153. Eiring, A.M., Harb, J.G., Neviani, P., Garton, C., Oaks, J.J., Spizzo, R., Liu, S., Schwind, S., Santhanam, R., Hickey, C.J., Becker, H., Chandler, J.C., Andino, R., Cortes, J., Hokland, P., et al., Cell, 2010, vol. 140, no. 5, pp. 652–665.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  154. Pitchiaya, S., Heinicke, L.A., Park, J.I., Cameron, E.L., and Walter, N.G., Cell Rep., vol. 19, no. 3, pp. 630–642.

  155. Pong, S.K. and Gullerova, M., FEBS Lett., 2018, vol. 592, no. 17, pp. 2973–2986.

    Article  CAS  PubMed  Google Scholar 

  156. Czech, B. and Hannon, G.J., Nat. Rev. Genet., 2011, vol. 12, no. 1, pp. 19–31.

    Article  CAS  PubMed  Google Scholar 

  157. Rybak-Wolf, A., Jens, M., Murakawa, Y., Herzog, M., Landthaler, M., and Rajewsky, N., Cell, 2014, pp. 1153–1167.

  158. Burger, K. and Gullerova, M., Nat. Rev. Mol. Cell Biol., 2015, vol. 16, no. 7, pp. 417–430.

    Article  CAS  PubMed  Google Scholar 

  159. Davis-Dusenbery, B.N. and Hata, A., J. Biochem., 2010, vol. 148, no. 4, pp. 381–392.

    CAS  PubMed  PubMed Central  Google Scholar 

  160. Ha, M. and Kim, V.N., Nat. Rev. Mol. Cell Biol., 2014, vol. 15, no. 8, pp. 509–524.

    Article  CAS  PubMed  Google Scholar 

  161. Lee, H., Han, S., Kwon, C.S., and Lee, D., Protein Cell, 2016, vol. 7, no. 2, pp. 100–113.

    Article  CAS  PubMed  Google Scholar 

  162. Kim, B., Ha, M., Loeff, L., Chang, H., Simanshu, D.K., Li, S., Fareh, M., Patel, D.J., Joo, C., and Kim, N., EMBO J., 2015, vol. 34, pp. 1801–1815.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  163. Fernandez, N., Cordiner, R.A., Young, R.S., Hug, N., Macias, S., and Cáceres, J.F., Nat. Commun., 2017, vol. 8, p. 15114.

  164. Guo, L. and Chen, F., Gene, 2014, vol. 544, no. 1, pp. 1–7.

    Article  CAS  PubMed  Google Scholar 

  165. 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., Genes Dev., 2010, vol. 24, no. 10, pp. 992–1009.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  166. Kim, B., Jeong, K., and Kim, V.N., Mol. Cell, 2017, vol. 66, no. 2, pp. 258– 269.

    Article  CAS  PubMed  Google Scholar 

  167. Humphreys, D.T., Hynes, C.J., Patel, H.R., Wei, G.H., Cannon, L., Fatkin, D., Suter, C.M., Clancy, J.L., and Preiss, T., PLoS One, 2012, vol. 7, no. 2. e30933.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  168. Starega-Roslan, J., Krol., J., Koscianska, E., Kozlowski, P., Szlachcic, W.J., Sobczak, K., and Krzyzosiak, W.J., Nucleic Acids Res., 2011, vol. 39, no. 1, pp. 257–268.

    Article  CAS  PubMed  Google Scholar 

  169. Juvvuna, P.K., Khandelia, P., Lee, L.M., and Makeyev, E.V., Nucleic Acids Res., 2012, vol. 40, no. 14, pp. 6808–6820.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  170. Liu, X., Zheng, Q., Vrettos, N., Maragkakis, M., Alexiou, P., Gregory, B.D., and Mourelatos, Z., Mol. Cell, 2014, vol. 55, pp. 868–879.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  171. Heale, B.S.E., Keegan, L.P., and O’Connell, M.A., Adv. Exp. Med. Biol., 2010, vol. 700, pp. 76–84.

    Article  CAS  PubMed  Google Scholar 

  172. Morin, R.D., O’Connor, M.D., Griffith, M., Kuchenbauer, F., Delaney, A., Prabhu, A.-L., Zhao, Y., McDonald, H., Zeng, T., Hirst, M., Eaves, C.J., and Marra, M.A., Genome Res., 2008, vol. 18, no. 4, pp. 610–621.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  173. Lee, L.W., Zhang, S., Etheridge, A., Ma, L., Martin, D., Galas, D., and Wang, K., RNA, 2010, vol. 16, no. 11, pp. 2170–2180.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  174. Li, L., Song, Y., Shi, X., Liu, J., Xiong, S., Chen, W., Fu, Q., Huang, Z., Gu, N., and Zhang, R., Genome Res, 2018, vol. 28, no. 1, pp. 132–143.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  175. Yang, J.-S., Phillips, M.D., Betel, D., Mu, P., Ventura, A., Siepel, A.C., Chen, K.C., and Lai, E.C., RNA, 2011, vol. 17, no. 2, pp. 312–326.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  176. Almeida, M.I., Nicoloso, M.S., Zeng, L., Ivan, C., Spizzo, R., Gafà, R., Xiao, L., Zhang, X., Vannini, I., Fanini, F., Fabbri, M., Lanza, G., Reis, R.M., Zweidler-McKay, P.A., and Calin, G.A., Gastroenterology, 2012, vol. 142, no. 4, pp. 886– 896.

    Article  CAS  PubMed  Google Scholar 

  177. Yang, X., Du, W.W., Li, H., Liu, F., Khorshidi, A., Rutnam, Z.J., and Yang, B.B., Nucleic Acids Res., 2013, vol. 41, no. 21, pp. 9688–9704.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  178. Kato, M., Chen, X., Inukai, S., Zhao, H., and Slack, F.J., RNA, 2011, vol. 17, no. 10, pp. 1804–1820.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  179. Potla, R., Singh, I.S., Atamas, S.P., and Hasday, J.D., RNA, 2015, vol. 21, no. 7, pp. 1261–1273.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  180. Guo, L. and Lu, Z., PLoS One, 2010, vol. 5, no. 6.

  181. Kang, S.-M., Choi, J.-W., Hong, S.-H., and Lee, H.-J., Int. J. Mol. Sci., 2013, vol. 14, no. 7, pp. 13231–13240.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  182. Meijer, H.A., Smith, E.M., and Bushell, M., Biochem. Soc. Trans., 2014, vol. 42, no. 4, pp. 1135–1140.

    Article  CAS  PubMed  Google Scholar 

  183. Grimm, D., Wang, L., Lee, J.S., Schurmann, N., Gu, S., Börner, K., Storm, T.A., and Kay, M.A., J. Clin. Invest., 2010, vol. 120, no. 9, pp. 3106–3119.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  184. Hansen, T.B., Veno, M.T., Jensen, T.I., Schaefer, A., Damgaard, C.K., and Kjems, J., Nat. Commun., 2016, vol. 7, p. 11538.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  185. Stagsted, L.V.W., Daugaard, I., and Hansen, T.B., BioEssays, 2017, vol. 39, no. 4, p. 1600239.

    Article  CAS  Google Scholar 

  186. Smibert, P., Yang, J.-S., Azzam, G., Liu, J.-L., and Lai, E.C., Nat. Struct. Mol. Biol., 2013, vol. 20, no. 7, pp. 789–795.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  187. Martinez, N.J. and Gregory, R.I., RNA, 2013, vol. 19, no. 5, pp. 605–612.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  188. Janas, M.M., Wang, B., Harris, A.S., Aguiar, M., Shaffer, J.M., Subrahmanyam, Y.V.B.K., Behlke, M.A., Wucherpfennig, K.W., Gygi, S.P., Gagnon, E., and Novina, C.D., RNA, 2012, vol. 18, no. 11, pp. 2041–2055.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  189. Stalder, L., Heusermann, W., Sokol., L., Trojer, D., Wirz, J., Hean, J., Fritzsche, A., Aeschimann, F., Pfanzagl, V., Basselet, P., Weiler, J., Hintersteiner, M., Morrissey, D.V., and Meisner-Kober, N.C., EMBO J., 2013, vol. 32, no. 8, pp. 1115–1127.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  190. Flores, O., Kennedy, E.M., Skalsky, R.L., and Cullen, B.R., Nucleic Acids Res., 2014, vol. 42, no. 7, pp. 4332–4347.

  191. Zealy, R.W., Wrenn, S.P., Davila, S., Min, K.W., and Yoon, J.H., Wiley Interdiscip. Rev. RNA, 2017, vol. 8, no. 5, pp. 1–8.

    Article  CAS  Google Scholar 

  192. Ciafrè, S.A. and Galardi, S., RNA Biol., 2013, vol. 10, no. 6, pp. 935–942.

    Article  PubMed  CAS  Google Scholar 

  193. Kartha, R.V. and Subramanian, S., Front. Genet., 2014, vol. 5, pp. 1–9.

    Article  CAS  Google Scholar 

  194. Memczak, S., Jens, M., Elefsinioti, A., Torti, F., Krueger, J., Rybak, A., Maier, L., Mackowiak, S.D., Gregersen, L.H., Munschauer, M., Loewer, A., Ziebold, U., Landthaler, M., Kocks, C., Le Noble, F., et al., Nature, 2013, vol. 495, no. 7441, pp. 333–338.

    Article  CAS  PubMed  Google Scholar 

  195. Denzler, R., Agarwal, V., Stefano, J., Bartel, D.P., and Stoffel, M., Mol. Cell, 2014, vol. 54, no. 5, pp. 766–776.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  196. Thomson, D.W. and Dinger, M.E., Nat. Rev. Genet., 2016, vol. 17, no. 5, pp. 272–283.

    Article  CAS  PubMed  Google Scholar 

  197. Gantier, M.P., McCoy, C.E., Rusinova, I., Saulep, D., Wang, D., Xu, D., Irving, A.T., Behlke, M.A., Hertzog, P.J., Mackay, F., and Williams, B.R.G., Nucleic Acids Res., 2011, vol. 39, no. 13, pp. 5692–5703.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  198. 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., Cell, 2010, vol. 141, no. 4, pp. 618–631.

  199. Okamura, K., Phillips, M.D., Tyler, D.M., Duan, H., Chou, Y., and Lai, E.C., Nat. Struct. Mol. Biol., 2008, vol. 15, no. 4, pp. 354–363.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  200. Avril-Sassen, S., Goldstein, L.D., Stingl, J., Blenkiron, C., Quesne, J.Le., Spiteri, I., Karagavriilidou, K., Watson, C.J., Tavare, S., Miska, E.A., and Caldas, C., BMC Genomics, 2009, vol. 10, no. 1, p. 548.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  201. Kato, M., Lencastre, A., Pincus, Z., and Slack, F.J., Genome Biol., 2009, vol. 10, no. 5, p. R54.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  202. Chatterjee, S., Fasler, M., Büssing, I., and Großhans, H., Dev. Cell, 2011, vol. 20, no. 3, pp. 388–396.

    Article  CAS  PubMed  Google Scholar 

  203. Bitetti, A., Mallory, A.C., Golini, E., Carrieri, C., Carreño Gutiérrez, H., Perlas, E., Pérez-Rico, Y.A., Tocchini-Valentini, G.P., Enright, A.J., Norton, W.H.J., Mandillo, S., O’Carroll, D., and Shkumatava, A., Nat. Struct. Mol. Biol., 2018.

  204. Ameres, S.L., Horwich, M.D., Hung, J.-H., Xu, J., Ghildiyal, M., Weng, Z., and Zamore, P.D., Science, 2010, vol. 328, no. 5985, pp. 1534–1539.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  205. Shukla, S., Bjerke, G.A., Muhlrad, D., Yi, R., and Parker, R., Mol. Cell, 2019, vol. 73, no. 6, pp. 1204– 1216.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

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Funding

The work was partially supported by the Russian Science Foundation, project no. 16-15-00124; P.P. Laktionov acknowledges financial support within the framework of the Russian state budget project no. AAAA-A17-117020210024-8 to the ICBFM SB RAS.

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  1. Institute of Chemical Biology and Fundamental Medicine, Siberian Branch, Russian Academy of Sciences, 630090, Novosibirsk, Russia

    I. A. Zaporozhchenko, E. Yu. Rykova & P. P. Laktionov

  2. Meshalkin National Medical Research Center, Ministry of Healthcare of the Russian Federation, 630055, Novosibirsk, Russia

    I. A. Zaporozhchenko, E. Yu. Rykova & P. P. Laktionov

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  1. I. A. Zaporozhchenko
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Translated by N. Onishchenko

Abbreviations: RISC, RNA-induced silencing complex.

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Zaporozhchenko, I.A., Rykova, E.Y. & Laktionov, P.P. The Fundamentals of miRNA Biology: Structure, Biogenesis, and Regulatory Functions. Russ J Bioorg Chem 46, 1–13 (2020). https://doi.org/10.1134/S106816202001015X

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