Skip to main content

piRNA biogenesis and its functions

Abstract

piRNAs (piwi-interacting RNA) are a novel class of non-coding small single-stranded RNAs with the length of 26–33 nt. The piRNAs play important biological role through the specific interaction with the piwi proteins of the Argonaute family. piRNA function in embryonic development, maintenance of germline DNA integrity, silencing of transposon transcription, suppression of translation, formation of heterochromatin, and epigenetic regulation of sex determination. This review summarizes recent research and progress on biogenesis and function of piRNA in eukaryotic species.

This is a preview of subscription content, access via your institution.

References

  1. Aravin, A.A., Naumova, N.M., Tulin, A.V., Vagin, V.V., Rozovsky, Y.M., and Gvozdev, V.A., Curr. Biol., 2001, vol. 11, pp. 1017–1027.

    CAS  PubMed  Article  Google Scholar 

  2. 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., Nature, 2006, vol. 442, pp. 203–207.

    CAS  PubMed  Google Scholar 

  3. Girard, A., Sachidanandam, R., Hannon, G. J., and Carmell, M.A., Nature, 2006, vol. 442, pp. 199–202.

    PubMed  Google Scholar 

  4. Grivna, S.T., Beyret, E., Wang, Z., and Lin, H., Genes Dev., 2006, vol. 20, pp. 1709–1714.

    CAS  PubMed Central  PubMed  Article  Google Scholar 

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

    CAS  PubMed  Article  Google Scholar 

  6. Ro, S., Park, C., Song, R., Nguyen, D., Jin, J., Sanders, K.M., McCarrey, J.R., and Yan, W., RNA, 2007, vol. 13, pp. 1693–1702.

    CAS  PubMed Central  PubMed  Article  Google Scholar 

  7. Shi, Z., Montgomery, T.A., Qi, Y., and Ruvkun, G., Genome Res., 2013, vol. 23, pp. 497–508.

    CAS  PubMed Central  PubMed  Article  Google Scholar 

  8. Khurana, J.S. and Theurkauf, W.E., Development, 2008, vol. 135, pp. 3–9.

    Google Scholar 

  9. Ghildiyal, M. and Zamore, P.D., Nat. Rev. Genet., 2009, vol. 10, pp. 94–108.

    CAS  PubMed Central  PubMed  Article  Google Scholar 

  10. Malone, C.D. and Hannon, G.J., Cold Spring Harb Symp Quant Biol., 2009, vol. 74, pp. 225–234.

    CAS  PubMed Central  PubMed  Article  Google Scholar 

  11. Senti, K.A. and Brennecke, J., Trends Genet., 2010, vol. 26, pp. 499–509.

    CAS  PubMed  Article  Google Scholar 

  12. 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., Cell, 2007, vol. 129, pp. 69–82.

    CAS  PubMed  Article  Google Scholar 

  13. Kim, V.N., Genes Dev., 2006, vol. 20, pp. 1993–1997.

    CAS  PubMed  Article  Google Scholar 

  14. Sai Lakshmi, S. and Agrawal, S., Nucleic Acids Res., 2008, vol. 36, pp. D173–D177.

    CAS  PubMed Central  PubMed  Article  Google Scholar 

  15. Zhang, Y., Li, J., Chen, R., Dai, A., Luan, D., Ma, T., Hua, D., Chen, G., and Chang, G., Mol. Biol. Rep., 2013, vol. 40, pp. 2799–2807.

    CAS  PubMed  Article  Google Scholar 

  16. Kamminga, L.M., Luteijn, M.J., den Broeder, M.J., Redl, S., Kaaij, L.J., Roovers, E.F., Ladurner, P., Berezikov, E., and Ketting, R.F., EMBO J., 2010, vol. 29, pp. 3688–3700.

    CAS  PubMed Central  PubMed  Article  Google Scholar 

  17. Betel, D., Sheridan, R., Marks, D.S., and Sander, C., PLoS Comput. Biol., 2007, vol. 3, p. e222.

    PubMed Central  PubMed  Article  Google Scholar 

  18. Handler, D., Olivieri, D., Novatchkova, M., Gruber, F.S., Meixner, K., Mechtler, K., Stark, A., Sachidanandam, R., and Brennecke, J., EMBO J., 2011, vol. 30, pp. 3977–3993.

    CAS  PubMed Central  PubMed  Article  Google Scholar 

  19. Sigurdsson, M.I., Smith, A.V., Bjornsson, H.T., and Jonsson, J.J., BMC Genet., 2012, vol. 13, p. 31.

    CAS  PubMed Central  PubMed  Article  Google Scholar 

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

    CAS  PubMed  Article  Google Scholar 

  21. Berninger, P., Jaskiewicz, L., Khorshid, M., and Zavolan, M., BMC Genomics, 2011, vol. 12, p. 46.

    CAS  PubMed Central  PubMed  Article  Google Scholar 

  22. Schwalbe, H., Structure, 2011, vol. 19, pp. 141–142.

    CAS  PubMed  Article  Google Scholar 

  23. Zamore, P.D., EMBO J., 2010, vol. 29, pp. 3219–3221.

    CAS  PubMed Central  PubMed  Article  Google Scholar 

  24. Beyret, E., Liu, N., and Lin, H., Cell Res., 2012, vol. 22, pp. 1429–1439.

    CAS  PubMed Central  PubMed  Article  Google Scholar 

  25. Vagin, V.V., Yu, Y., Jankowska, A., Luo, Y., Wasik, K.A., Malone, C.D., Harrison, E., Rosebrock, A., Wakimoto, B.T., Fagegaltier, D., Muerdter, F., and Hannon, G.J., RNA, 2013, vol. 19, pp. 1064–1077.

    CAS  PubMed  Article  Google Scholar 

  26. Shpiz, S. and Kalmykova, A., Genome Biol., 2009, vol. 10, p. 208.

    PubMed Central  PubMed  Article  Google Scholar 

  27. Liu, G., Lei, B., Li, Y., Tong, K., Ding, Y., Luo, L., Xia, X., Jiang, S., Deng, C., Xiong, Y., and Li, F., PLoS One, 2012, vol. 7, p. e34770.

    CAS  PubMed Central  PubMed  Article  Google Scholar 

  28. Vourekas, A., Zheng, Q., Alexiou, P., Maragkakis, M., Kirino, Y., Gregory, B. D., and Mourelatos, Z., Nat. Struct. Mol. Biol., 2012, vol. 19, pp. 773–781.

    CAS  PubMed Central  PubMed  Article  Google Scholar 

  29. Chuma, S., and Nakano, T., Philos. Trans. R. Soc. Lond. B: Biol. Sci., 2013, vol. 368, p. 20110338.

    Article  Google Scholar 

  30. De Fazio, S., Bartonicek, N., Di Giacomo, M., Abreu-Goodger, C., Sankar, A., Funaya, C., Antony, C., Moreira, P.N., Enright, A.J., and O’Carroll, D., Nature, 2011, vol. 480, pp. 259–263.

    PubMed  Article  Google Scholar 

  31. Pillai, R.S. and Chuma, S., Dev. Growth Differ., 2012, vol. 54, pp. 78–92.

    CAS  PubMed  Article  Google Scholar 

  32. Siomi, M.C., Sato, K., Pezic, D., and Aravin, A.A., Nat. Rev. Mol. Cell Biol., 2011, vol. 12, pp. 246–258.

    CAS  PubMed  Article  Google Scholar 

  33. Khurana, J.S., Xu, J., Weng, Z., and Theurkauf, W.E., PLoS Genet., 2010, vol. 6, p. e1001246.

    CAS  PubMed Central  PubMed  Article  Google Scholar 

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

    CAS  PubMed  Article  Google Scholar 

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

    CAS  PubMed Central  PubMed  Article  Google Scholar 

  36. Snow, P.M., Bieber, A.J., and Goodman, C.S., Cell, 1989, vol. 59, pp. 313–323.

    CAS  PubMed  Article  Google Scholar 

  37. Siomi, M.C., Miyoshi, T., and Siomi, H., Semin. Cell Dev. Biol., 2010, vol. 21, pp. 754–759.

    CAS  PubMed  Article  Google Scholar 

  38. 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., Genes Dev., 2013, vol. 27, pp. 390–399.

    PubMed Central  PubMed  Article  Google Scholar 

  39. Yin, H. and Lin, H., Nature, 2007, vol. 450, pp. 304–308.

    CAS  PubMed  Article  Google Scholar 

  40. Aravin, A.A., Sachidanandam, R., Bourćhis, D., Schaefer, C., Pezic, D., Toth, K.F., Bestor, T., and Hannon, G.J., Mol. Cell, 2008, vol. 31, pp. 785–799.

    CAS  PubMed Central  PubMed  Article  Google Scholar 

  41. Aravin, A.A., Sachidanandam, R., Girard, A., Fejes-Toth, K., and Hannon, G.J., Science, 2007, vol. 316, pp. 744–747.

    CAS  PubMed  Article  Google Scholar 

  42. 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., Genes Dev., 2008, vol. 22, pp. 908–917.

    CAS  PubMed Central  PubMed  Article  Google Scholar 

  43. Esposito, T., Magliocca, S., Formicola, D., and Gianfrancesco, F., PLoS One, 2011, vol. 6, p. e22727.

    CAS  PubMed Central  PubMed  Article  Google Scholar 

  44. Rajasethupathy, P., Antonov, I., Sheridan, R., Frey, S., Sander, C., Tuschl, T., and Kandel, E.R., Cell, 2012, vol. 149, pp. 693–707.

    CAS  PubMed Central  PubMed  Article  Google Scholar 

  45. 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., Science, 2011, vol. 332, pp. 848–852.

    CAS  PubMed Central  PubMed  Article  Google Scholar 

  46. 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., Cell, 2012, vol. 150, pp. 88–99.

    CAS  PubMed Central  PubMed  Article  Google Scholar 

  47. Landry, C.D., Kandel, E.R., and Rajasethupathy, P., Trends Neurosci., 2013, doi: org/10.1016/j.tins.2013.05.004.

    Google Scholar 

  48. Lee, H.C., Gu, W., Shirayama, M., Youngman, E., Conte, Jr., D., and Mello, C.C., Cell, 2012, vol. 150, pp. 78–87.

    CAS  PubMed Central  PubMed  Article  Google Scholar 

  49. Moazed, D., Cell, 2012, vol. 149, pp. 512–514.

    CAS  PubMed  Article  Google Scholar 

  50. Brower-Toland, B., Findley, S.D., Jiang, L., Liu, L., Yin, H., Dus, M., Zhou, P., Elgin, S.C., and Lin, H., Genes Dev., 2007, vol. 21, pp. 2300–2311.

    CAS  PubMed Central  PubMed  Article  Google Scholar 

  51. Mendez, D.L., Kim, D., Chruszcz, M., Stephens, G.E., Minor, W., Khorasanizadeh, S., and Elgin, S.C., Chembiochem., 2011, vol. 12, pp. 1084–1096.

    CAS  PubMed Central  PubMed  Article  Google Scholar 

  52. Sienski, G., Donertas, D., and Brennecke, J., Cell, 2012, vol. 151, pp. 964–980.

    CAS  PubMed Central  PubMed  Article  Google Scholar 

  53. Juliano, C., Wang, J., and Lin, H., Annu. Rev. Genet., 2011, vol. 45, pp. 447–469.

    CAS  PubMed  Article  Google Scholar 

  54. Fang, W., Wang, X., Bracht, J.R., Nowacki, M., and Landweber, L.F., Cell, 2012, vol. 151, pp. 1243–1255.

    CAS  PubMed Central  PubMed  Article  Google Scholar 

  55. Slanchev, K., Stebler, J., de la Cueva-Mendez, G., and Raz, E., Proc. Natl. Acad. Sci. USA, 2005, vol. 102, pp. 4074–4079.

    CAS  PubMed Central  PubMed  Article  Google Scholar 

  56. Klattenhoff, C. and Theurkauf, W., Development, 2008, vol. 135, pp. 3–9.

    CAS  PubMed  Article  Google Scholar 

  57. Cox, D.N., Chao, A., and Lin, H., Development, 2000, vol. 127, pp. 503–514.

    CAS  PubMed  Google Scholar 

  58. Janic, A., Mendizabal, L., Llamazares, S., Rossell, D., and Gonzalez, C., Science, 2010, vol. 330, pp. 1824–1827.

    CAS  PubMed  Article  Google Scholar 

  59. Sharma, A.K., Nelson, M.C., Brandt, J.E., Wessman, M., Mahmud, N., Weller, K.P., and Hoffman, R., Blood, 2001, vol. 97, pp. 426–434.

    CAS  PubMed  Article  Google Scholar 

  60. Ye, Y., Yin, D.T., Chen, L., Zhou, Q., Shen, R., He, G., Yan, Q., Tong, Z., Issekutz, A.C., Shapiro, C.L., Barsky, S.H., Lin, H., Li, J.J., and Gao, J.X., PLoS One, 2010, vol. 5, p. e13406.

    PubMed Central  PubMed  Article  Google Scholar 

  61. Qiao, D., Zeeman, A.M., Deng, W., Looijenga, L.H., and Lin, H., Oncogene, 2002, vol. 21, pp. 3988–3999.

    CAS  PubMed  Article  Google Scholar 

  62. Wu, Q., Ma, Q., Shehadeh, L.A., Wilson, A., Xia, L., Yu, H., and Webster, K.A., Biochem. Biophys. Res. Commun., 2010, vol. 396, pp. 915–920.

    CAS  PubMed Central  PubMed  Article  Google Scholar 

  63. Cheng, J., Guo, J.M., Xiao, B.X., Miao, Y., Jiang, Z., Zhou, H., and Li, Q.N., Clin. Chim. Acta, 2011, vol. 412, pp. 1621–1625.

    CAS  PubMed  Article  Google Scholar 

  64. Cheng, J., Deng, H., Xiao, B., Zhou, H., Zhou, F., Shen, Z., and Guo, J., Cancer Lett., 2012, vol. 315, pp. 12–17.

    CAS  PubMed  Article  Google Scholar 

  65. Cui, L., Lou, Y., Zhang, X., Zhou, H., Deng, H., Song, H., Yu, X., Xiao, B., Wang, W., and Guo, J., Clin. Biochem., 2011, vol. 44, pp. 1050–1057.

    CAS  PubMed  Article  Google Scholar 

  66. Pek, J.W. and Kai, T., Cell Div., 2011, vol. 6, p. 6.

    CAS  PubMed Central  PubMed  Article  Google Scholar 

  67. Huang, G., Hu, H., Xue, X., Shen, S., Gao, E., Guo, G., Shen, X., and Zhang, X., Clin. Transl. Oncol., 2013, vol. 15, pp. 563–568.

    CAS  PubMed  Article  Google Scholar 

  68. Law, P.T., Qin, H., Ching, A.K., Lai, K.P., Co, N.N., He, M., Lung, R.W., Chan, A.W., Chan, T.F., and Wong, N., J. Hepatol., 2013, vol. 58, pp. 1165–1173.

    CAS  PubMed  Article  Google Scholar 

  69. Wu, Q., Luo, Y., Lu, R., Lau, N., Lai, E.C., Li, W.X., and Ding, S.W., Proc. Natl. Acad. Sci. USA, 2010, vol. 107, pp. 1606–1611.

    CAS  PubMed Central  PubMed  Article  Google Scholar 

  70. Hess, A.M., Prasad, A.N., Ptitsyn, A., Ebel, G.D., Olson, K.E., Barbacioru, C., Monighetti, C., and Campbell, C.L., BMC Microbiol., 2011, vol. 11, p. 45.

    CAS  PubMed Central  PubMed  Article  Google Scholar 

  71. Brackney, D.E., Scott, J.C., Sagawa, F., Woodward, J.E., Miller, N.A., Schilkey, F.D., Mudge, J., Wilusz, J., Olson, K.E., Blair, C.D., and Ebel, G.D., PLoS Negl. Trop. Dis., 2010, vol. 4, p. e856.

    PubMed Central  PubMed  Article  Google Scholar 

  72. Scott, J.C., Brackney, D.E., Campbell, C.L., Bondu-Hawkins, V., Hjelle, B., Ebel, G.D., Olson, K.E., and Blair, C.D., PLoS Negl. Trop. Dis., 2010, vol. 4, p. e848.

    PubMed Central  PubMed  Article  Google Scholar 

  73. Leger, P., Lara, E., Jagla, B., Sismeiro, O., Mansuroglu, Z., Coppee, J.Y., Bonnefoy, E., and Bouloy, M., J. Virol., 2013, vol. 87, p. 1631–1648.

    CAS  PubMed Central  PubMed  Article  Google Scholar 

  74. Morazzani, E.M., Wiley, M.R., Murreddu, M.G., Adelman, Z.N., and Myles, K.M., PLoS Pathog., 2012, vol. 8, p. e1002470.

    CAS  PubMed Central  PubMed  Article  Google Scholar 

  75. Vodovar, N., Bronkhorst, A.W., van Cleef, K.W., Miesen, P., Blanc, H., van Rij, R.P., and Saleh, M.C., PLoS One, 2012, vol. 7, p. e30861.

    CAS  PubMed Central  PubMed  Article  Google Scholar 

  76. Lucas, K.J., Myles, K.M., and Raikhel, A.S., Trends Parasitol., 2013, vol. 29, pp. 295–303.

    CAS  PubMed  Article  Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Yong Huang.

Additional information

The article is published in the original.

Rights and permissions

Reprints and Permissions

About this article

Verify currency and authenticity via CrossMark

Cite this article

Huang, Y., Bai, J.Y. & Ren, H.T. piRNA biogenesis and its functions. Russ J Bioorg Chem 40, 293–299 (2014). https://doi.org/10.1134/S1068162014030169

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1134/S1068162014030169

Keywords

  • piRNA
  • regulation
  • function
  • cancer