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Biochemistry (Moscow)

, Volume 83, Issue 5, pp 483–497 | Cite as

Argonaute Proteins and Mechanisms of RNA Interference in Eukaryotes and Prokaryotes

  • A. V. OlinaEmail author
  • A. V. Kulbachinskiy
  • A. A. Aravin
  • D. M. EsyuninaEmail author
Review

Abstract

Noncoding RNAs play essential roles in genetic regulation in all organisms. In eukaryotic cells, many small non-coding RNAs act in complex with Argonaute proteins and regulate gene expression by recognizing complementary RNA targets. The complexes of Argonaute proteins with small RNAs also play a key role in silencing of mobile genetic elements and, in some cases, viruses. These processes are collectively called RNA interference. RNA interference is a powerful tool for specific gene silencing in both basic research and therapeutic applications. Argonaute proteins are also found in prokaryotic organisms. Recent studies have shown that prokaryotic Argonautes can also cleave their target nucleic acids, in particular DNA. This activity of prokaryotic Argonautes might potentially be used to edit eukaryotic genomes. However, the molecular mechanisms of small nucleic acid biogenesis and the functions of Argonaute proteins, in particular in bacteria and archaea, remain largely unknown. Here we briefly review available data on the RNA interference processes and Argonaute proteins in eukaryotes and prokaryotes.

Keywords

Argonaute proteins RNA interference small RNAs mobile genetic elements 

Abbreviations

MID

middle domain in Ago proteins

miRISC

microRNA-containing RISC

miRNA

microRNA

PAZ

PIWI-Argonaute-Zwille domain

piRNA

PIWI interacting RNA

PIWI

P-element induced wimpy testis

pri-miPHK

primary miRNA

RISC

RNA-induced silencing complex

siRNA

small interfering RNA

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References

  1. 1.
    Lee, R. C., Feinbaum, R. L., and Ambros, V. (1993) The C. elegans heterochronic gene lin-4 encodes small RNAs with antisense complementarity to lin-14, Cell, 75, 843–854.PubMedCrossRefGoogle Scholar
  2. 2.
    Baulcombe, D. C. (1996) RNA as a target and an initiator of post-transcriptional gene silencing in transgenic plants, Plant Mol. Biol., 32, 79–88.PubMedCrossRefGoogle Scholar
  3. 3.
    Ratcliff, F., Harrison, B. D., and Baulcombe, D. C. (1997) A similarity between viral defense and gene silencing in plants, Science, 276, 1558–1560.PubMedCrossRefGoogle Scholar
  4. 4.
    Fire, A., Xu, S., Montgomery, M. K., Kostas, S. A., Driver, S. E., and Mello, C. C. (1998) Potent and specific genetic interference by double-stranded RNA in Caenorhabditis elegans, Nature, 391, 806–811.PubMedCrossRefGoogle Scholar
  5. 5.
    Hammond, S. M., Bernstein, E., Beach, D., and Hannon, G. J. (2000) An RNA-directed nuclease mediates post-transcriptional gene silencing in Drosophila cells, Nature, 404, 293–296.PubMedCrossRefGoogle Scholar
  6. 6.
    Elbashir, S. M., Lendeckel, W., and Tuschl, T. (2001) RNA interference is mediated by 21-and 22-nucleotide RNAs, Genes Dev., 15, 188–200.PubMedPubMedCentralCrossRefGoogle Scholar
  7. 7.
    Bohmert, K., Camus, I., Bellini, C., Bouchez, D., Caboche, M., and Benning, C. (1998) AGO1 defines a novel locus of Arabidopsis controlling leaf development, Embo J., 17, 170–180.PubMedPubMedCentralCrossRefGoogle Scholar
  8. 8.
    Hutvagner, G., and Simard, M. J. (2008) Argonaute pro-teins: key players in RNA silencing, Nat. Rev. Mol. Cell Biol., 9, 22–32.PubMedCrossRefGoogle Scholar
  9. 9.
    Makarova, K. S., Wolf, Y. I., van der Oost, J., and Koonin, E. V. (2009) Prokaryotic homologs of Argonaute proteins are predicted to function as key components of a novel system of defense against mobile genetic elements, Biol. Direct, 4, 29.PubMedPubMedCentralCrossRefGoogle Scholar
  10. 10.
    Swarts, D. C., Makarova, K., Wang, Y., Nakanishi, K., Ketting, R. F., Koonin, E. V., Patel, D. J., and van der Oost, J. (2014) The evolutionary journey of Argonaute pro-teins, Nat. Struct. Mol. Biol., 21, 743–753.PubMedPubMedCentralCrossRefGoogle Scholar
  11. 11.
    Zaratiegui, M., Irvine, D. V., and Martienssen, R. A. (2007) Noncoding RNAs and gene silencing, Cell, 128, 763–776.PubMedCrossRefGoogle Scholar
  12. 12.
    Carmell, M. A., Xuan, Z., Zhang, M. Q., and Hannon, G. J. (2002) The Argonaute family: tentacles that reach into RNAi, developmental control, stem cell maintenance, and tumorigenesis, Genes Dev., 16, 2733–2742.PubMedCrossRefGoogle Scholar
  13. 13.
    Meister, G. (2013) Argonaute proteins: functional insights and emerging roles, Nat. Rev. Genet., 14, 447–459.PubMedCrossRefGoogle Scholar
  14. 14.
    Schroda, M. (2006) RNA silencing in Chlamydomonas: mechanisms and tools, Curr. Genet., 49, 69–84.PubMedCrossRefGoogle Scholar
  15. 15.
    Zhao, T., Li, G., Mi, S., Li, S., Hannon, G. J., Wang, X. J., and Qi, Y. (2007) A complex system of small RNAs in the unicellular green alga Chlamydomonas reinhardtii, Genes Dev., 21, 1190–1203.PubMedPubMedCentralCrossRefGoogle Scholar
  16. 16.
    Axtell, M. J., Snyder, J. A., and Bartel, D. P. (2007) Common functions for diverse small RNAs of land plants, Plant Cell, 19, 1750–1769.PubMedPubMedCentralCrossRefGoogle Scholar
  17. 17.
    Morel, J. B., Godon, C., Mourrain, P., Beclin, C., Boutet, S., Feuerbach, F., Proux, F., and Vaucheret, H. (2002) Fertile hypomorphic ARGONAUTE (ago1) mutants impaired in post-transcriptional gene silencing and virus resistance, Plant Cell, 14, 629–639.PubMedPubMedCentralCrossRefGoogle Scholar
  18. 18.
    Zhao, K., Zhao, H., Chen, Z., Feng, L., Ren, J., Cai, R., and Xiang, Y. (2015) The Dicer-like, Argonaute and RNA-dependent RNA polymerase gene families in Populus tri-chocarpa: gene structure, gene expression, phylogenetic analysis and evolution, J. Genet., 94, 317–321.Google Scholar
  19. 19.
    Qian, Y., Cheng, Y., Cheng, X., Jiang, H., Zhu, S., and Cheng, B. (2011) Identification and characterization of Dicer-like, Argonaute and RNA-dependent RNA poly-merase gene families in maize, Plant Cell Rep., 30, 1347–1363.Google Scholar
  20. 20.
    Zhai, L., Sun, W., Zhang, K., Jia, H., Liu, L., Liu, Z., Teng, F., and Zhang, Z. (2014) Identification and charac-terization of Argonaute gene family and meiosis-enriched Argonaute during sporogenesis in maize, J. Integr. Plant. Biol., 56, 1042–1052.PubMedCrossRefGoogle Scholar
  21. 21.
    Kapoor, M., Arora, R., Lama, T., Nijhawan, A., Khurana, J. P., Tyagi, A. K., and Kapoor, S. (2008) Genome-wide identification, organization and phylogenetic analysis of Dicer-like, Argonaute and RNA-dependent RNA poly-merase gene families and their expression analysis during reproductive development and stress in rice, BMC Genomics, 9, 451.Google Scholar
  22. 22.
    Drinnenberg, I. A., Weinberg, D. E., Xie, K. T., Mower, J. P., Wolfe, K. H., Fink, G. R., and Bartel, D. P. (2009) RNAi in budding yeast, Science, 326, 544–550.PubMedPubMedCentralCrossRefGoogle Scholar
  23. 23.
    Tolia, N. H., and Joshua-Tor, L. (2007) Slicer and the arg-onautes, Nat. Chem. Biol., 3, 36–43.PubMedCrossRefGoogle Scholar
  24. 24.
    Song, J. J., Smith, S. K., Hannon, G. J., and Joshua-Tor, L. (2004) Crystal structure of Argonaute and its implica-tions for RISC slicer activity, Science, 305, 1434–1437.PubMedCrossRefGoogle Scholar
  25. 25.
    Rivas, F. V., Tolia, N. H., Song, J. J., Aragon, J. P., Liu, J., Hannon, G. J., and JoshuaTor, L. (2005) Purified Argonaute2 and an siRNA form recombinant human RISC, Nat. Struct. Mol. Biol., 12, 340–349.PubMedCrossRefGoogle Scholar
  26. 26.
    Frank, F., Sonenberg, N., and Nagar, B. (2010) Structural basis for 5′-nucleotide base-specific recognition of guide RNA by human AGO2, Nature, 465, 818–822.PubMedCrossRefGoogle Scholar
  27. 27.
    Lau, N. C., Lim, L. P., Weinstein, E. G., and Bartel, D. P. (2001) An abundant class of tiny RNAs with probable regu-latory roles in Caenorhabditis elegans, Science, 294, 858–862.PubMedCrossRefGoogle Scholar
  28. 28.
    Parker, J. S., Roe, S. M., and Barford, D. (2005) Structural insights into mRNA recognition from a PIWI domain–siRNA guide complex, Nature, 434, 663–666.PubMedPubMedCentralCrossRefGoogle Scholar
  29. 29.
    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) Endogenous siRNAs derived from transposons and mRNAs in Drosophila somatic cells, Science, 320, 1077–1081.PubMedPubMedCentralCrossRefGoogle Scholar
  30. 30.
    Miyoshi, T., Ito, K., Murakami, R., and Uchiumi, T. (2016) Structural basis for the recognition of guide RNA and target DNA heteroduplex by Argonaute, Nat. Commun., 7, 11846.PubMedPubMedCentralCrossRefGoogle Scholar
  31. 31.
    Lingel, A., Simon, B., Izaurralde, E., and Sattler, M. (2003) Structure and nucleic-acid binding of the Drosophila Argonaute 2 PAZ domain, Nature, 426, 465–469.PubMedCrossRefGoogle Scholar
  32. 32.
    Yan, K. S., Yan, S., Farooq, A., Han, A., Zeng, L., and Zhou, M. M. (2003) Structure and conserved RNA binding of the PAZ domain, Nature, 426, 468–474.PubMedCrossRefGoogle Scholar
  33. 33.
    Kwak, P. B., and Tomari, Y. (2012) The N domain of Argonaute drives duplex unwinding during RISC assembly, Nat. Struct. Mol. Biol., 19, 145–151.PubMedCrossRefGoogle Scholar
  34. 34.
    Hauptmann, J., Dueck, A., Harlander, S., Pfaff, J., Merkl, R., and Meister, G. (2013) Turning catalytically inactive human Argonaute proteins into active slicer enzymes, Nat. Struct. Mol. Biol., 20, 814–817.PubMedCrossRefGoogle Scholar
  35. 35.
    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) Microarray analysis shows that some microRNAs downregulate large numbers of target mRNAs, Nature, 433, 769–773.PubMedCrossRefGoogle Scholar
  36. 36.
    Chandradoss, S. D., Schirle, N. T., Szczepaniak, M., MacRae, I. J., and Joo, C. (2015) A dynamic search process underlies microRNA targeting, Cell, 162, 96–107.PubMedPubMedCentralCrossRefGoogle Scholar
  37. 37.
    Wang, B., Li, S., Qi, H. H., Chowdhury, D., Shi, Y., and Novina, C. D. (2009) Distinct passenger strand and mRNA cleavage activities of human Argonaute proteins, Nat. Struct. Mol. Biol., 16, 1259–1266.PubMedCrossRefGoogle Scholar
  38. 38.
    Sheng, G., Zhao, H., Wang, J., Rao, Y., Tian, W., Swarts, D. C., van der Oost, J., Patel, D. J., and Wang, Y. (2014) Structure-based cleavage mechanism of Thermus ther-mophilus Argonaute DNA guide strand-mediated DNA tar-get cleavage, Proc. Natl. Acad. Sci. USA, 111, 652–657.PubMedCrossRefGoogle Scholar
  39. 39.
    Tomari, Y., and Zamore, P. D. (2005) Perspective: machines for RNAi, Genes Dev., 19, 517–529.PubMedCrossRefGoogle Scholar
  40. 40.
    Orban, T. I., and Izaurralde, E. (2005) Decay of mRNAs targeted by RISC requires XRN1, the Ski complex, and the exosome, RNA, 11, 459–469.PubMedPubMedCentralCrossRefGoogle Scholar
  41. 41.
    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) Argonaute2 is the cat-alytic engine of mammalian RNAi, Science, 305, 1437–1441.PubMedCrossRefGoogle Scholar
  42. 42.
    Okamura, K., Phillips, M. D., Tyler, D. M., Duan, H., Chou, Y. T., and Lai, E. C. (2008) The regulatory activity of microRNA* species has substantial influence on microRNA and 3′ UTR evolution, Nat. Struct. Mol. Biol., 15, 354–363.PubMedPubMedCentralCrossRefGoogle Scholar
  43. 43.
    Babiarz, J. E., Ruby, J. G., Wang, Y., Bartel, D. P., and Blelloch, R. (2008) Mouse ES cells express endogenous shRNAs, siRNAs, and other Microprocessor-independent, Dicer-dependent small RNAs, Genes Dev., 22, 2773–2785.PubMedGoogle Scholar
  44. 44.
    Xie, Z., Johansen, L. K., Gustafson, A. M., Kasschau, K. D., Lellis, A. D., Zilberman, D., Jacobsen, S. E., and Carrington, J. C. (2004) Genetic and functional diversifi-cation of small RNA pathways in plants, PLoS Biol., 2, E104.PubMedPubMedCentralCrossRefGoogle Scholar
  45. 45.
    Lu, C., Kulkarni, K., Souret, F. F., MuthuValliappan, R., Tej, S. S., Poethig, R. S., Henderson, I. R., Jacobsen, S. E., Wang, W., Green, P. J., and Meyers, B. C. (2006) MicroRNAs and other small RNAs enriched in the Arabidopsis RNA-dependent RNA polymerase-2 mutant, Genome Res., 16, 1276–1288.PubMedPubMedCentralCrossRefGoogle Scholar
  46. 46.
    Kasschau, K. D., Fahlgren, N., Chapman, E. J., Sullivan, C. M., Cumbie, J. S., Givan, S. A., and Carrington, J. C. (2007) Genome-wide profiling and analysis of Arabidopsis siRNAs, PLoS Biol., 5, e57.PubMedPubMedCentralCrossRefGoogle Scholar
  47. 47.
    Chapman, E. J., and Carrington, J. C. (2007) Specialization and evolution of endogenous small RNA pathways, Nat. Rev. Genet., 8, 884–896.PubMedCrossRefGoogle Scholar
  48. 48.
    Zhang, H., Kolb, F. A., Jaskiewicz, L., Westhof, E., and Filipowicz, W. (2004) Single processing center models for human Dicer and bacterial RNase III, Cell, 118, 57–68.PubMedCrossRefGoogle Scholar
  49. 49.
    Macrae, I. J., Zhou, K., Li, F., Repic, A., Brooks, A. N., Cande, W. Z., Adams, P. D., and Doudna, J. A. (2006) Structural basis for double-stranded RNA processing by Dicer, Science, 311, 195–198.PubMedCrossRefGoogle Scholar
  50. 50.
    Schwarz, D. S., Hutvagner, G., Du, T., Xu, Z., Aronin, N., and Zamore, P. D. (2003) Asymmetry in the assembly of the RNAi enzyme complex, Cell, 115, 199–208.PubMedCrossRefGoogle Scholar
  51. 51.
    Ambros, V. (2003) MicroRNA pathways in flies and worms: growth, death, fat, stress, and timing, Cell, 113, 673–676.PubMedCrossRefGoogle Scholar
  52. 52.
    Bartel, D. P. (2004) MicroRNAs: genomics, biogenesis, mechanism, and function, Cell, 116, 281–297.PubMedCrossRefPubMedCentralGoogle Scholar
  53. 53.
    Cullen, B. R. (2004) Transcription and processing of human microRNA precursors, Mol. Cell, 16, 861–865.PubMedCrossRefGoogle Scholar
  54. 54.
    Saini, H. K., Griffiths-Jones, S., and Enright, A. J. (2007) Genomic analysis of human microRNA transcripts, Proc. Natl. Acad. Sci. USA, 104, 17719–17724.PubMedPubMedCentralCrossRefGoogle Scholar
  55. 55.
    Lee, Y., Jeon, K., Lee, J. T., Kim, S., and Kim, V. N. (2002) MicroRNA maturation: stepwise processing and subcellu-lar localization, EMBO J., 21, 4663–4670.PubMedPubMedCentralCrossRefGoogle Scholar
  56. 56.
    Han, J., Lee, Y., Yeom, K. H., Kim, Y. K., Jin, H., and Kim, V. N. (2004) The Drosha–DGCR8 complex in pri-mary microRNA processing, Genes Dev., 18, 3016–3027.PubMedPubMedCentralCrossRefGoogle Scholar
  57. 57.
    Denli, A. M., Tops, B. B., Plasterk, R. H., Ketting, R. F., and Hannon, G. J. (2004) Processing of primary microRNAs by the Microprocessor complex, Nature, 432, 231–235.PubMedCrossRefGoogle Scholar
  58. 58.
    Gregory, R. I., Yan, K. P., Amuthan, G., Chendrimada, T., Doratotaj, B., Cooch, N., and Shiekhattar, R. (2004) The Microprocessor complex mediates the genesis of microRNAs, Nature, 432, 235–240.PubMedCrossRefGoogle Scholar
  59. 59.
    Lee, Y., Han, J., Yeom, K. H., Jin, H., and Kim, V. N. (2006) Drosha in primary microRNA processing, Cold Spring Harb. Symp. Quant. Biol., 71, 51–57.PubMedCrossRefGoogle Scholar
  60. 60.
    Lund, E., and Dahlberg, J. E. (2006) Substrate selectivity of exportin 5 and Dicer in the biogenesis of microRNAs, Cold Spring Harb. Symp. Quant. Biol., 71, 59–66.PubMedCrossRefGoogle Scholar
  61. 61.
    Hutvagner, G., McLachlan, J., Pasquinelli, A. E., Balint, E., Tuschl, T., and Zamore, P. D. (2001) A cellular function for the RNA-interference enzyme Dicer in the maturation of the let-7 small temporal RNA, Science, 293, 834–838.PubMedCrossRefGoogle Scholar
  62. 62.
    Grishok, A., Pasquinelli, A. E., Conte, D., Li, N., Parrish, S., Ha, I., Baillie, D. L., Fire, A., Ruvkun, G., and Mello, C. C. (2001) Genes and mechanisms related to RNA inter-ference regulate expression of the small temporal RNAs that control C. elegans developmental timing, Cell, 106, 23–34.PubMedCrossRefGoogle Scholar
  63. 63.
    Bernstein, E., Caudy, A. A., Hammond, S. M., and Hannon, G. J. (2001) Role for a bidentate ribonuclease in the initiation step of RNA interference, Nature, 409, 363–366.PubMedCrossRefGoogle Scholar
  64. 64.
    Kawamata, T., and Tomari, Y. (2010) Making RISC, Trends Biochem. Sci., 35, 368–376.PubMedCrossRefGoogle Scholar
  65. 65.
    Meijer, H. A., Smith, E. M., and Bushell, M. (2014) Regulation of miRNA strand selection: follow the leader? Biochem. Soc. Trans., 42, 1135–1140.PubMedCrossRefGoogle Scholar
  66. 66.
    MacRae, I. J., Ma, E., Zhou, M., Robinson, C. V., and Doudna, J. A. (2008) In vitro reconstitution of the human RISC-loading complex, Proc. Natl. Acad. Sci. USA, 105, 512–517.PubMedPubMedCentralCrossRefGoogle Scholar
  67. 67.
    Eamens, A. L., Smith, N. A., Curtin, S. J., Wang, M. B., and Waterhouse, P. M. (2009) The Arabidopsis thaliana double-stranded RNA binding protein DRB1 directs guide strand selection from microRNA duplexes, RNA, 15, 2219–2235.PubMedPubMedCentralCrossRefGoogle Scholar
  68. 68.
    Khvorova, A., Reynolds, A., and Jayasena, S. D. (2003) Functional siRNAs and miRNAs exhibit strand bias, Cell, 115, 209–216.PubMedCrossRefGoogle Scholar
  69. 69.
    Montgomery, T. A., Howell, M. D., Cuperus, J. T., Li, D., Hansen, J. E., Alexander, A. L., Chapman, E. J., Fahlgren, N., Allen, E., and Carrington, J. C. (2008) Specificity of ARGONAUTE7–miR390 interaction and dual function-ality in TAS3 trans-acting siRNA formation, Cell, 133, 128–141.PubMedCrossRefGoogle Scholar
  70. 70.
    Takeda, A., Iwasaki, S., Watanabe, T., Utsumi, M., and Watanabe, Y. (2008) The mechanism selecting the guide strand from small RNA duplexes is different among arg-onaute proteins, Plant Cell Physiol., 49, 493–500.PubMedCrossRefGoogle Scholar
  71. 71.
    Tomari, Y., Du, T., and Zamore, P. D. (2007) Sorting of Drosophila small silencing RNAs, Cell, 130, 299–308.PubMedPubMedCentralCrossRefGoogle Scholar
  72. 72.
    Czech, B., Zhou, R., Erlich, Y., Brennecke, J., Binari, R., Villalta, C., Gordon, A., Perrimon, N., and Hannon, G. J. (2009) Hierarchical rules for Argonaute loading in Drosophila, Mol. Cell, 36, 445–456.PubMedPubMedCentralCrossRefGoogle Scholar
  73. 73.
    Zhu, H., Hu, F., Wang, R., Zhou, X., Sze, S. H., Liou, L. W., Barefoot, A., Dickman, M., and Zhang, X. (2011) Arabidopsis Argonaute10 specifically sequesters miR166/165 to regulate shoot apical meristem develop-ment, Cell, 145, 242–256.PubMedPubMedCentralCrossRefGoogle Scholar
  74. 74.
    Aravin, A. A., Lagos-Quintana, M., Yalcin, A., Zavolan, M., Marks, D., Snyder, B., Gaasterland, T., Meyer, J., and Tuschl, T. (2003) The small RNA profile during Drosophila melanogaster development, Dev. Cell, 5, 337–350.PubMedCrossRefGoogle Scholar
  75. 75.
    Girard, A., Sachidanandam, R., Hannon, G. J., and Carmell, M. A. (2006) A germline-specific class of small RNAs binds mammalian Piwi proteins, Nature, 442, 199–202.PubMedGoogle Scholar
  76. 76.
    Brennecke, J., Malone, C. D., Aravin, A. A., Sachidanandam, R., Stark, A., and Hannon, G. J. (2008) An epigenetic role for maternally inherited piRNAs in transposon silencing, Science, 322, 1387–1392.PubMedPubMedCentralCrossRefGoogle Scholar
  77. 77.
    Aravin, A. A., Naumova, N. M., Tulin, A. V., Vagin, V. V., Rozovsky, Y. M., and Gvozdev, V. A. (2001) Double-stranded RNA-mediated silencing of genomic tandem repeats and transposable elements in the D. melanogaster germline, Curr. Biol., 11, 1017–1027.PubMedCrossRefGoogle Scholar
  78. 78.
    Aravin, A. A., Hannon, G. J., and Brennecke, J. (2007) The Piwi-piRNA pathway provides an adaptive defense in the transposon arms race, Science, 318, 761–764.PubMedCrossRefGoogle Scholar
  79. 79.
    Aravin, A. A., Sachidanandam, R., Bourc’his, D., Schaefer, C., Pezic, D., Toth, K. F., Bestor, T., and Hannon, G. J. (2008) A piRNA pathway primed by indi-vidual transposons is linked to de novo DNA methylation in mice, Mol. Cell, 31, 785–799.PubMedPubMedCentralCrossRefGoogle Scholar
  80. 80.
    Brennecke, J., Aravin, A. A., Stark, A., Dus, M., Kellis, M., Sachidanandam, R., and Hannon, G. J. (2007) Discrete small RNA-generating loci as master regulators of transposon activity in Drosophila, Cell, 128, 1089–1103.PubMedCrossRefGoogle Scholar
  81. 81.
    Muerdter, F., Olovnikov, I., Molaro, A., Rozhkov, N. V., Czech, B., Gordon, A., Hannon, G. J., and Aravin, A. A. (2012) Production of artificial piRNAs in flies and mice, RNA, 18, 42–52.PubMedPubMedCentralCrossRefGoogle Scholar
  82. 82.
    Andersen, P. R., Tirian, L., Vunjak, M., and Brennecke, J. (2017) A heterochromatin-dependent transcription machinery drives piRNA expression, Nature, 549, 54–59.PubMedPubMedCentralCrossRefGoogle Scholar
  83. 83.
    Ipsaro, J. J., Haase, A. D., Knott, S. R., Joshua-Tor, L., and Hannon, G. J. (2012) The structural biochemistry of Zucchini implicates it as a nuclease in piRNA biogenesis, Nature, 491, 279–283.PubMedPubMedCentralCrossRefGoogle Scholar
  84. 84.
    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) Structure and function of Zucchini endoribonuclease in piRNA biogene-sis, Nature, 491, 284–287.PubMedCrossRefGoogle Scholar
  85. 85.
    Kawaoka, S., Izumi, N., Katsuma, S., and Tomari, Y. (2011) 3′ end formation of PIWI-interacting RNAs in vitro, Mol. Cell, 43, 1015–1022.PubMedCrossRefGoogle Scholar
  86. 86.
    Siomi, M. C., Sato, K., Pezic, D., and Aravin, A. A. (2011) PIWI-interacting small RNAs: the vanguard of genome defence, Nat. Rev. Mol. Cell Biol., 12, 246–258.PubMedCrossRefGoogle Scholar
  87. 87.
    Law, J. A., and Jacobsen, S. E. (2010) Establishing, main-taining and modifying DNA methylation patterns in plants and animals, Nat. Rev. Genet., 11, 204–220.PubMedPubMedCentralCrossRefGoogle Scholar
  88. 88.
    Rogers, K., and Chen, X. (2013) Biogenesis, turnover, and mode of action of plant microRNAs, Plant Cell, 25, 2383–2399.PubMedPubMedCentralCrossRefGoogle Scholar
  89. 89.
    Wei, W., Ba, Z., Gao, M., Wu, Y., Ma, Y., Amiard, S., White, C. I., Rendtlew Danielsen, J. M., Yang, Y. G., and Qi, Y. (2012) A role for small RNAs in DNA double-strand break repair, Cell, 149, 101–112.PubMedCrossRefGoogle Scholar
  90. 90.
    Ba, Z., and Qi, Y. (2013) Small RNAs: emerging key play-ers in DNA double-strand break repair, Sci. China Life Sci., 56, 933–936.PubMedCrossRefGoogle Scholar
  91. 91.
    Ameyar-Zazoua, M., Rachez, C., Souidi, M., Robin, P., Fritsch, L., Young, R., Morozova, N., Fenouil, R., Descostes, N., Andrau, J. C., Mathieu, J., Hamiche, A., Ait-Si-Ali, S., Muchardt, C., Batsche, E., and Harel-Bellan, A. (2012) Argonaute proteins couple chromatin silencing to alternative splicing, Nat. Struct. Mol. Biol., 19, 998–1004.PubMedCrossRefGoogle Scholar
  92. 92.
    Hendrickson, D. G., Hogan, D. J., McCullough, H. L., Myers, J. W., Herschlag, D., Ferrell, J. E., and Brown, P. O. (2009) Concordant regulation of translation and mRNA abundance for hundreds of targets of a human microRNA, PLoS Biol., 7, e1000238.PubMedPubMedCentralCrossRefGoogle Scholar
  93. 93.
    Guo, H., Ingolia, N. T., Weissman, J. S., and Bartel, D. P. (2010) Mammalian microRNAs predominantly act to decrease target mRNA levels, Nature, 466, 835–840.PubMedPubMedCentralCrossRefGoogle Scholar
  94. 94.
    Rissland, O. S., and Lai, E. C. (2011) RNA silencing in Monterey, Development, 138, 3093–3102.PubMedCrossRefGoogle Scholar
  95. 95.
    Arribas-Layton, M., Wu, D., Lykke-Andersen, J., and Song, H. (2013) Structural and functional control of the eukaryotic mRNA decapping machinery, Biochim. Biophys. Acta, 1829, 580–589.PubMedCrossRefGoogle Scholar
  96. 96.
    Hutvagner, G., and Zamore, P. D. (2002) A microRNA in a multiple-turnover RNAi enzyme complex, Science, 297, 2056–2060.PubMedCrossRefGoogle Scholar
  97. 97.
    Wu, G., Park, M. Y., Conway, S. R., Wang, J. W., Weigel, D., and Poethig, R. S. (2009) The sequential action of miR156 and miR172 regulates developmental timing in Arabidopsis, Cell, 138, 750–759.PubMedPubMedCentralCrossRefGoogle Scholar
  98. 98.
    Eulalio, A., Huntzinger, E., Nishihara, T., Rehwinkel, J., Fauser, M., and Izaurralde, E. (2009) Deadenylation is a widespread effect of miRNA regulation, RNA, 15, 21–32.PubMedPubMedCentralCrossRefGoogle Scholar
  99. 99.
    Wakiyama, M., Takimoto, K., Ohara, O., and Yokoyama, S. (2007) Let-7 microRNA-mediated mRNA deadenyla-tion and translational repression in a mammalian cell-free system, Genes Dev., 21, 1857–1862.PubMedPubMedCentralCrossRefGoogle Scholar
  100. 100.
    Valencia-Sanchez, M. A., Liu, J., Hannon, G. J., and Parker, R. (2006) Control of translation and mRNA degra-dation by miRNAs and siRNAs, Genes Dev., 20, 515–524.PubMedCrossRefGoogle Scholar
  101. 101.
    Iwakawa, H. O., and Tomari, Y. (2015) The functions of microRNAs: mRNA decay and translational repression, Trends Cell Biol., 25, 651–665.PubMedCrossRefGoogle Scholar
  102. 102.
    Wilczynska, A., and Bushell, M. (2015) The complexity of miRNA-mediated repression, Cell Death Differ., 22, 22–33.PubMedCrossRefGoogle Scholar
  103. 103.
    Fukao, A., Mishima, Y., Takizawa, N., Oka, S., Imataka, H., Pelletier, J., Sonenberg, N., Thoma, C., and Fujiwara, T. (2014) MicroRNAs trigger dissociation of eIF4AI and eIF4AII from target mRNAs in humans, Mol. Cell, 56, 79–89.PubMedCrossRefGoogle Scholar
  104. 104.
    Bazzini, A. A., Lee, M. T., and Giraldez, A. J. (2012) Ribosome profiling shows that miR-430 reduces transla-tion before causing mRNA decay in zebrafish, Science, 336, 233–237.PubMedPubMedCentralCrossRefGoogle Scholar
  105. 105.
    Bethune, J., Artus-Revel, C. G., and Filipowicz, W. (2012) Kinetic analysis reveals successive steps leading to miRNA-mediated silencing in mammalian cells, EMBO Rep., 13, 716–723.PubMedPubMedCentralCrossRefGoogle Scholar
  106. 106.
    Djuranovic, S., Nahvi, A., and Green, R. (2012) miRNA-mediated gene silencing by translational repression fol-lowed by mRNA deadenylation and decay, Science, 336, 237–240.PubMedPubMedCentralCrossRefGoogle Scholar
  107. 107.
    Braun, J. E., Huntzinger, E., Fauser, M., and Izaurralde, E. (2011) GW182 proteins directly recruit cytoplasmic deadenylase complexes to miRNA targets, Mol. Cell, 44, 120–133.PubMedCrossRefGoogle Scholar
  108. 108.
    Mathys, H., Basquin, J., Ozgur, S., Czarnocki-Cieciura, M., Bonneau, F., Aartse, A., Dziembowski, A., Nowotny, M., Conti, E., and Filipowicz, W. (2014) Structural and biochemical insights to the role of the CCR4–NOT com-plex and DDX6 ATPase in microRNA repression, Mol. Cell, 54, 751–765.PubMedCrossRefGoogle Scholar
  109. 109.
    Braun, J. E., Huntzinger, E., and Izaurralde, E. (2013) The role of GW182 proteins in miRNA-mediated gene silencing, Adv. Exp. Med. Biol., 768, 147–163.PubMedCrossRefGoogle Scholar
  110. 110.
    Verdel, A., Jia, S., Gerber, S., Sugiyama, T., Gygi, S., Grewal, S. I., and Moazed, D. (2004) RNAi-mediated tar-geting of heterochromatin by the RITS complex, Science, 303, 672–676.PubMedPubMedCentralCrossRefGoogle Scholar
  111. 111.
    Jih, G., Iglesias, N., Currie, M. A., Bhanu, N. V., Paulo, J. A., Gygi, S. P., Garcia, B. A., and Moazed, D. (2017) Unique roles for histone H3K9me states in RNAi and her-itable silencing of transcription, Nature, 547, 463–467.PubMedPubMedCentralCrossRefGoogle Scholar
  112. 112.
    Lan, F., Zaratiegui, M., Villen, J., Vaughn, M. W., Verdel, A., Huarte, M., Shi, Y., Gygi, S. P., Moazed, D., Martienssen, R. A., and Shi, Y. (2007) S. pombe LSD1 homologs regulate heterochromatin propagation and euchromatic gene transcription, Mol. Cell, 26, 89–101.PubMedCrossRefGoogle Scholar
  113. 113.
    Sienski, G., Donertas, D., and Brennecke, J. (2012) Transcriptional silencing of transposons by Piwi and mael-strom and its impact on chromatin state and gene expres-sion, Cell, 151, 964–980.PubMedPubMedCentralCrossRefGoogle Scholar
  114. 114.
    Le Thomas, A., Rogers, A. K., Webster, A., Marinov, G. K., Liao, S. E., Perkins, E. M., Hur, J. K., Aravin, A. A., and Toth, K. F. (2013) Piwi induces piRNA-guided tran-scriptional silencing and establishment of a repressive chromatin state, Genes Dev., 27, 390–399.PubMedPubMedCentralCrossRefGoogle Scholar
  115. 115.
    Chen, Y. A., and Aravin, A. A. (2015) Non-coding RNAs in transcriptional regulation: the review for current molec-ular biology reports, Curr. Mol. Biol. Rep., 1, 10–18.PubMedPubMedCentralCrossRefGoogle Scholar
  116. 116.
    Fang, X., and Qi, Y. (2016) RNAi in plants: an Argonaute-centered view, Plant Cell, 28, 272–285.PubMedPubMedCentralCrossRefGoogle Scholar
  117. 117.
    He, X. J., Hsu, Y. F., Zhu, S., Wierzbicki, A. T., Pontes, O., Pikaard, C. S., Liu, H. L., Wang, C. S., Jin, H., and Zhu, J. K. (2009) An effector of RNA-directed DNA methylation in Arabidopsis is an ARGONAUTE 4-and RNA-binding protein, Cell, 137, 498–508.PubMedPubMedCentralCrossRefGoogle Scholar
  118. 118.
    Haag, J. R., Ream, T. S., Marasco, M., Nicora, C. D., Norbeck, A. D., Pasa-Tolic, L., and Pikaard, C. S. (2012) In vitro transcription activities of Pol IV, Pol V, and RDR2 reveal coupling of Pol IV and RDR2 for dsRNA synthesis in plant RNA silencing, Mol. Cell, 48, 811–818.Google Scholar
  119. 119.
    Pontier, D., Yahubyan, G., Vega, D., Bulski, A., Saez-Vasquez, J., Hakimi, M. A., Lerbs-Mache, S., Colot, V., and Lagrange, T. (2005) Reinforcement of silencing at transposons and highly repeated sequences requires the concerted action of two distinct RNA polymerases IV in Arabidopsis, Genes Dev., 19, 2030–2040.PubMedPubMedCentralCrossRefGoogle Scholar
  120. 120.
    Mosher, R. A., Schwach, F., Studholme, D., and Baulcombe, D. C. (2008) PolIVb influences RNA-direct-ed DNA methylation independently of its role in siRNA biogenesis, Proc. Natl. Acad. Sci. USA, 105, 3145–3150.PubMedPubMedCentralCrossRefGoogle Scholar
  121. 121.
    Wierzbicki, A. T., Haag, J. R., and Pikaard, C. S. (2008) Noncoding transcription by RNA polymerase Pol IVb/Pol V mediates transcriptional silencing of overlap-ping and adjacent genes, Cell, 135, 635–648.PubMedPubMedCentralCrossRefGoogle Scholar
  122. 122.
    Wierzbicki, A. T., Ream, T. S., Haag, J. R., and Pikaard, C. S. (2009) RNA polymerase V transcription guides ARGONAUTE4 to chromatin, Nat. Genet., 41, 630–634.PubMedPubMedCentralCrossRefGoogle Scholar
  123. 123.
    Cao, X., and Jacobsen, S. E. (2002) Role of the Arabidopsis DRM methyltransferases in de novo DNA methylation and gene silencing, Curr. Biol., 12, 1138–1144.PubMedCrossRefGoogle Scholar
  124. 124.
    Barrangou, R., and Horvath, P. (2017) A decade of discov-ery: CRISPR functions and applications, Nat. Microbiol., 2, 17092.PubMedCrossRefGoogle Scholar
  125. 125.
    Koonin, E. V., Makarova, K. S., and Zhang, F. (2017) Diversity, classification and evolution of CRISPR–Cas systems, Curr. Opin. Microbiol., 37, 67–78.PubMedCrossRefPubMedCentralGoogle Scholar
  126. 126.
    Koonin, E. V. (2017) Evolution of RNA-and DNA-guid-ed antivirus defense systems in prokaryotes and eukary-otes: common ancestry vs convergence, Biol. Direct, 12, 5.PubMedPubMedCentralCrossRefGoogle Scholar
  127. 127.
    Olovnikov, I., Chan, K., Sachidanandam, R., Newman, D. K., and Aravin, A. A. (2013) Bacterial argonaute sam-ples the transcriptome to identify foreign DNA, Mol. Cell, 51, 594–605.PubMedCrossRefGoogle Scholar
  128. 128.
    Swarts, D. C., Jore, M. M., Westra, E. R., Zhu, Y., Janssen, J. H., Snijders, A. P., Wang, Y., Patel, D. J., Berenguer, J., Brouns, S. J. J., and van der Oost, J. (2014) DNA-guided DNA interference by a prokaryotic Argonaute, Nature, 507, 258–261.PubMedPubMedCentralCrossRefGoogle Scholar
  129. 129.
    Shabalina, S. A., and Koonin, E. V. (2008) Origins and evolution of eukaryotic RNA interference, Trends Ecol. Evol., 23, 578–587.PubMedPubMedCentralCrossRefGoogle Scholar
  130. 130.
    Koonin, E. V., Makarova, K. S., and Wolf, Y. I. (2017) Evolutionary genomics of defense systems in Archaea and bacteria, Annu. Rev. Microbiol., 71, 233–261.PubMedPubMedCentralCrossRefGoogle Scholar
  131. 131.
    Burroughs, A. M., Iyer, L. M., and Aravind, L. (2013) Two novel PIWI families: roles in inter-genomic conflicts in bacteria and Mediator-dependent modulation of tran-scription in eukaryotes, Biol. Direct, 8, 13.PubMedPubMedCentralCrossRefGoogle Scholar
  132. 132.
    Ma, J. B., Yuan, Y. R., Meister, G., Pei, Y., Tuschl, T., and Patel, D. J. (2005) Structural basis for 5′-end-specific recognition of guide RNA by the A. fulgidus Piwi protein, Nature, 434, 666–670.PubMedPubMedCentralCrossRefGoogle Scholar
  133. 133.
    Yuan, Y. R., Pei, Y., Ma, J. B., Kuryavyi, V., Zhadina, M., Meister, G., Chen, H. Y., Dauter, Z., Tuschl, T., and Patel, D. J. (2005) Crystal structure of A. aeolicus argonaute, a site-specific DNA-guided endoribonuclease, provides insights into RISC-mediated mRNA cleavage, Mol. Cell, 19, 405–419.PubMedPubMedCentralCrossRefGoogle Scholar
  134. 134.
    Swarts, D. C., Hegge, J. W., Hinojo, I., Shiimori, M., Ellis, M. A., Dumrongkulraksa, J., Terns, R. M., Terns, M. P., and van der Oost, J. (2015) Argonaute of the archaeon Pyrococcus furiosus is a DNA-guided nuclease that targets cognate DNA, Nucleic Acids Res., 43, 5120–5129.PubMedPubMedCentralCrossRefGoogle Scholar
  135. 135.
    Matsumoto, N., Nishimasu, H., Sakakibara, K., Nishida, K. M., Hirano, T., Ishitani, R., Siomi, H., Siomi, M. C., and Nureki, O. (2016) Crystal structure of silkworm PIWI-clade Argonaute Siwi bound to piRNA, Cell, 167, 484–497 e489.PubMedCrossRefGoogle Scholar
  136. 136.
    Swarts, D. C., Szczepaniak, M., Sheng, G., Chandradoss, S. D., Zhu, Y., Timmers, E. M., Zhang, Y., Zhao, H., Lou, J., Wang, Y., Joo, C., and van der Oost, J. (2017) Autonomous generation and loading of DNA guides by bacterial Argonaute, Mol. Cell, 65, 985–998 e986.PubMedPubMedCentralCrossRefGoogle Scholar
  137. 137.
    Zander, A., Holzmeister, P., Klose, D., Tinnefeld, P., and Grohmann, D. (2014) Single-molecule FRET supports the two-state model of Argonaute action, RNA Biology, 11, 45–56.PubMedCrossRefGoogle Scholar
  138. 138.
    Zander, A., Willkomm, S., Ofer, S., van Wolferen, M., Egert, L., Buchmeier, S., Stockl, S., Tinnefeld, P., Schneider, S., Klingl, A., Albers, S. V., Werner, F., and Grohmann, D. (2017) Guide-independent DNA cleavage by archaeal Argonaute from Methanocaldococcus jan-naschii, Nat. Microbiol., 2, 17034.PubMedCrossRefGoogle Scholar
  139. 139.
    Kaya, E., Doxzen, K. W., Knoll, K. R., Wilson, R. C., Strutt, S. C., Kranzusch, P. J., and Doudna, J. A. (2016) A bacterial Argonaute with noncanonical guide RNA speci-ficity, Proc. Natl. Acad. Sci. USA, 113, 4057–4062.PubMedPubMedCentralCrossRefGoogle Scholar
  140. 140.
    Doxzen, K. W., and Doudna, J. A. (2017) DNA recogni-tion by an RNA-guided bacterial Argonaute, PloS One, 12, e0177097.PubMedPubMedCentralCrossRefGoogle Scholar
  141. 141.
    Hegge, J. W., Swarts, D. C., and van der Oost, J. (2017) Prokaryotic Argonaute proteins: novel genome-editing tools? Nat. Rev. Microbiol., 16, 5–11.PubMedCrossRefGoogle Scholar

Copyright information

© Pleiades Publishing, Ltd. 2018

Authors and Affiliations

  1. 1.Institute of Molecular GeneticsRussian Academy of SciencesMoscowRussia
  2. 2.California Institute of TechnologyDivision of BiologyPasadenaUSA

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