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Diverse Small Non-coding RNAs in RNA Interference Pathways

Protocol
Part of the Methods in Molecular Biology book series (MIMB, volume 764)

Abstract

Large numbers of diverse small non-coding RNAs have been discovered and characterized in eukaryotic RNA interference pathways. These small RNAs have distinctive characteristics and are associated with Argonaute family proteins to regulate gene expression and genomes at various levels. These small RNAs include the Dicer-dependent group such as microRNAs (miRNAs) and small interfering RNAs (siRNAs), and the Dicer-independent group such as Piwi-interacting RNAs (piRNAs). This review summarizes the various classes of eukaryotic small RNAs and the general knowledge of their characteristics, biogenesis, and functions, with emphasis on some of the recently identified small RNAs.

Key words

RNAi miRNA siRNA piRNA qiRNA 

Notes

Acknowledgement

This work is supported by funds from the National Institute of Health and Welch Foundation (I-1560) to Y. Liu.

References

  1. 1.
    Ambros, V. (2004) The functions of animal microRNAs. Nature 431, 350–355.PubMedCrossRefGoogle Scholar
  2. 2.
    Buhler, M., and Moazed, D. (2007) Transcription and RNAi in heterochromatic gene silencing. Nat Struct Mol Biol 14, 1041–1048.PubMedCrossRefGoogle Scholar
  3. 3.
    Ghildiyal, M., and Zamore, P. D. (2009) Small silencing RNAs: an expanding universe. Nat Rev Genet 10, 94–108.PubMedCrossRefGoogle Scholar
  4. 4.
    Hannon, G. J. (2002) RNA interference. Nature 418, 244–251.PubMedCrossRefGoogle Scholar
  5. 5.
    Jinek, M., and Doudna, J. A. (2009) A three-dimensional view of the molecular machinery of RNA interference. Nature 457, 405–412.PubMedCrossRefGoogle Scholar
  6. 6.
    Siomi, H., and Siomi, M. C. (2009) On the road to reading the RNA-interference code. Nature 457, 396–404.PubMedCrossRefGoogle Scholar
  7. 7.
    Maiti, M., Lee, H. C., and Liu, Y. (2007) QIP, a putative exonuclease, interacts with the Neurospora argonaute protein and facilitates conversion of duplex siRNA into single strands. Genes Dev 21, 590–600.PubMedCrossRefGoogle Scholar
  8. 8.
    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
  9. 9.
    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
  10. 10.
    Kim, V. N., Han, J., and Siomi, M. C. (2009) Biogenesis of small RNAs in animals. Nat Rev Mol Cell Biol 10, 126–139.PubMedCrossRefGoogle Scholar
  11. 11.
    Chen, X. (2009) Small RNAs and their roles in plant development. Annu Rev Cell Dev Biol 25, 21–44.PubMedCrossRefGoogle Scholar
  12. 12.
    Bartel, D. P. (2004) MicroRNAs: genomics, biogenesis, mechanism, and function. Cell 116, 281–297.PubMedCrossRefGoogle Scholar
  13. 13.
    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. (2003) A uniform system for microRNA annotation. RNA 9, 277–279.PubMedCrossRefGoogle Scholar
  14. 14.
    Lee, R. C., Feinbaum, R. L., and Ambros, V. (1993) The C. elegans heterochromatic gene lin-4 encodes small RNAs with antisense complementarity to lin-14. Cell 75, 843–854.PubMedCrossRefGoogle Scholar
  15. 15.
    Lagos-Quintana, M., Rauhut, R., Lendeckel, W., and Tuschl, T. (2001) Identification of novel genes coding for small expressed RNAs. Science 294, 853–858.PubMedCrossRefGoogle Scholar
  16. 16.
    Lee, R. C., and Ambros, V. (2001) An extensive class of small RNAs in Caenorhabditis elegans. Science 294, 862–864.PubMedCrossRefGoogle Scholar
  17. 17.
    Llave, C., Kasschau, K. D., Rector, M. A., and Carrington, J. C. (2002) Endogenous and silencing-associated small RNAs in plants. Plant Cell 14, 1605–1619.PubMedCrossRefGoogle Scholar
  18. 18.
    Molnar, A., Schwach, F., Studholme, D. J., Thuenemann, E. C., and Baulcombe, D. C. (2007) miRNAs control gene expression in the single-cell alga Chlamydomonas reinhardtii. Nature 447, 1126–1129.PubMedCrossRefGoogle Scholar
  19. 19.
    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.PubMedCrossRefGoogle Scholar
  20. 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. (2008) Early origins and evolution of microRNAs and Piwi-interacting RNAs in animals. Nature 455, 1193–1197.PubMedCrossRefGoogle Scholar
  21. 21.
    Lee, H. C., Li, L., Gu, W., Xue, Z., Crosthwaite, S. K., Pertsemlidis, A., Lewis, Z. A., Freitag, M., Selker, E. U., Mello, C. C., and Liu, Y. (2010) Diverse pathways generate microRNA-like RNAs and Dicer-independent small interfering RNAs in fungi. Mol Cell 38, 803–814.Google Scholar
  22. 22.
    Griffiths-Jones, S., Saini, H. K., van Dongen, S., and Enright, A. J. (2008) miRBase: tools for microRNA genomics. Nucl Acids Res 36, D154–158.PubMedCrossRefGoogle Scholar
  23. 23.
    Reinhart, B. J., Slack, F. J., Basson, M., Pasquinelli, A. E., Bettinger, J. C., Rougvie, A. E., Horvitz, H. R., and Ruvkun, G. (2000) The 21-nucleotide let-7 RNA regulates developmental timing in Caenorhabditis elegans. Nature 403, 901–906.PubMedCrossRefGoogle Scholar
  24. 24.
    Kim, V. N. (2005) MicroRNA biogenesis: coordinated cropping and dicing. Nat Rev Mol Cell Biol 6, 376–385.PubMedCrossRefGoogle Scholar
  25. 25.
    Voinnet, O. (2009) Origin, biogenesis, and activity of plant microRNAs. Cell 136, 669–687.PubMedCrossRefGoogle Scholar
  26. 26.
    Lee, Y., Kim, M., Han, J., Yeom, K. H., Lee, S., Baek, S. H., and Kim, V. N. (2004) MicroRNA genes are transcribed by RNA polymerase II. EMBO J 23, 4051–4060.PubMedCrossRefGoogle Scholar
  27. 27.
    Cai, X., Hagedorn, C. H., and Cullen, B. R. (2004) Human microRNAs are processed from capped, polyadenylated transcripts that can also function as mRNAs. RNA 10, 1957–1966.PubMedCrossRefGoogle Scholar
  28. 28.
    Lee, Y., Ahn, C., Han, J., Choi, H., Kim, J., Yim, J., Lee, J., Provost, P., Radmark, O., Kim, S., and Kim, V. N. (2003) The nuclear RNase III Drosha initiates microRNA processing. Nature 425, 415–419.PubMedCrossRefGoogle Scholar
  29. 29.
    Han, J., Lee, Y., Yeom, K. H., Kim, Y. K., Jin, H., and Kim, V. N. (2004) The Drosha-DGCR8 complex in primary microRNA processing. Genes Dev 18, 3016–3027.PubMedCrossRefGoogle Scholar
  30. 30.
    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
  31. 31.
    Landthaler, M., Yalcin, A., and Tuschl, T. (2004) The human DiGeorge syndrome critical region gene 8 and Its D. melanogaster homolog are required for miRNA biogenesis. Curr Biol 14, 2162–2167.PubMedCrossRefGoogle Scholar
  32. 32.
    Carthew, R. W., and Sontheimer, E. J. (2009) Origins and mechanisms of miRNAs and siRNAs. Cell 136, 642–655.PubMedCrossRefGoogle Scholar
  33. 33.
    Barringhaus, K. G., and Zamore, P. D. (2009) MicroRNAs: regulating a change of heart. Circulation 119, 2217–2224.PubMedCrossRefGoogle Scholar
  34. 34.
    Reinhart, B. J., Weinstein, E. G., Rhoades, M. W., Bartel, B., and Bartel, D. P. (2002) MicroRNAs in plants. Genes Dev 16, 1616–1626.PubMedCrossRefGoogle Scholar
  35. 35.
    Zhang, B., Pan, X., and Stellwag, E. J. (2008) Identification of soybean microRNAs and their targets. Planta 229, 161–182.PubMedCrossRefGoogle Scholar
  36. 36.
    Yu, B., Yang, Z., Li, J., Minakhina, S., Yang, M., Padgett, R. W., Steward, R., and Chen, X. (2005) Methylation as a crucial step in plant microRNA biogenesis. Science 307, 932–935.PubMedCrossRefGoogle Scholar
  37. 37.
    Felippes, F. F., Schneeberger, K., Dezulian, T., Huson, D. H., and Weigel, D. (2008) Evolution of Arabidopsis thaliana microRNAs from random sequences. RNA 14, 2455–2459.PubMedCrossRefGoogle Scholar
  38. 38.
    Brodersen, P., Sakvarelidze-Achard, L., Bruun-Rasmussen, M., Dunoyer, P., Yamamoto, Y. Y., Sieburth, L., and Voinnet, O. (2008) Widespread translational inhibition by plant miRNAs and siRNAs. Science 320, 1185–1190.PubMedCrossRefGoogle Scholar
  39. 39.
    Siomi, H., and Siomi, M. C. (2007) Expanding RNA physiology: microRNAs in a unicellular organism. Genes Dev 21, 1153–1156.PubMedCrossRefGoogle Scholar
  40. 40.
    Odling-Smee, L. (2007) Complex set of RNAs found in simple green algae. Nature 447, 518.PubMedCrossRefGoogle Scholar
  41. 41.
    Napoli, C., Lemieux, C., and Jorgensen, R. (1990) Introduction of a chimeric chalcone synthase gene into Petunia results in reversible co-suppression of homologous genes in trans. Plant Cell 2, 279–289.PubMedCrossRefGoogle Scholar
  42. 42.
    Romano, N., and Macino, G. (1992) Quelling: transient inactivation of gene expression in Neurospora crassa by transformation with homologous sequences. Mol Microbiol 6, 3343–3353.PubMedCrossRefGoogle Scholar
  43. 43.
    Carmell, M. A., and Hannon, G. J. (2004) RNase III enzymes and the initiation of gene silencing. Nat Struct Mol Biol 11, 214–218.PubMedCrossRefGoogle Scholar
  44. 44.
    Cecere, G., and Cogoni, C. (2009) Quelling targets the rDNA locus and functions in rDNA copy number control. BMC Microbiol 9, 44.PubMedCrossRefGoogle Scholar
  45. 45.
    Catalanotto, C., Pallotta, M., ReFalo, P., Sachs, M. S., Vayssie, L., Macino, G., and Cogoni, C. (2004) Redundancy of the two dicer genes in transgene-induced posttranscriptional gene silencing in Neurospora crassa. Mol Cell Biol 24, 2536–2545.PubMedCrossRefGoogle Scholar
  46. 46.
    Catalanotto, C., Nolan, T., and Cogoni, C. (2006) Homology effects in Neurospora crassa. FEMS Microbiol Lett 254, 182–189.PubMedCrossRefGoogle Scholar
  47. 47.
    Freitag, M., Lee, D. W., Kothe, G. O., Pratt, R. J., Aramayo, R., and Selker, E. U. (2004) DNA methylation is independent of RNA interference in Neurospora. Science 304, 1939.PubMedCrossRefGoogle Scholar
  48. 48.
    Chicas, A., Forrest, E. C., Sepich, S., Cogoni, C., and Macino, G. (2005) Small interfering RNAs that trigger posttranscriptional gene silencing are not required for the histone H3 Lys9 methylation necessary for transgenic tandem repeat stabilization in Neurospora crassa. Mol Cell Biol 25, 3793–3801.PubMedCrossRefGoogle Scholar
  49. 49.
    Castanotto, D., and Rossi, J. J. (2009) The promises and pitfalls of RNA-interference-based therapeutics. Nature 457, 426–433.PubMedCrossRefGoogle Scholar
  50. 50.
    Siomi, M. C. (2009) Short interfering RNA-mediated gene silencing; towards successful application in human patients. Adv Drug Deliv Rev 61, 668–671.PubMedCrossRefGoogle Scholar
  51. 51.
    Jackson, A. L., and Linsley, P. S. (2010) Recognizing and avoiding siRNA off-target effects for target identification and therapeutic application. Nat Rev Drug Discov 9, 57–67.PubMedCrossRefGoogle Scholar
  52. 52.
    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 diversification of small RNA pathways in plants. PLoS Biol 2, E104.PubMedCrossRefGoogle Scholar
  53. 53.
    Katiyar-Agarwal, S., Morgan, R., Dahlbeck, D., Borsani, O., Villegas, A., Jr., Zhu, J. K., Staskawicz, B. J., and Jin, H. (2006) A pathogen-inducible endogenous siRNA in plant immunity. Proc Natl Acad Sci USA 103, 18002–18007.PubMedCrossRefGoogle Scholar
  54. 54.
    Borsani, O., Zhu, J., Verslues, P. E., Sunkar, R., and Zhu, J. K. (2005) Endogenous siRNAs derived from a pair of natural cis-antisense transcripts regulate salt tolerance in Arabidopsis. Cell 123, 1279–1291.PubMedCrossRefGoogle Scholar
  55. 55.
    Katiyar-Agarwal, S., Gao, S., Vivian-Smith, A., and Jin, H. (2007) A novel class of bacteria-induced small RNAs in Arabidopsis. Genes Dev 21, 3123–3134.PubMedCrossRefGoogle Scholar
  56. 56.
    Vazquez, F., Vaucheret, H., Rajagopalan, R., Lepers, C., Gasciolli, V., Mallory, A. C., Hilbert, J. L., Bartel, D. P., and Crete, P. (2004) Endogenous trans-acting siRNAs regulate the accumulation of Arabidopsis mRNAs. Mol Cell 16, 69–79.PubMedCrossRefGoogle Scholar
  57. 57.
    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.PubMedCrossRefGoogle Scholar
  58. 58.
    Okamura, K., Balla, S., Martin, R., Liu, N., and Lai, E. C. (2008) Two distinct mechanisms generate endogenous siRNAs from bidirectional transcription in Drosophila melanogaster. Nat Struct Mol Biol 15, 581–590.PubMedCrossRefGoogle Scholar
  59. 59.
    Okamura, K., Chung, W. J., Ruby, J. G., Guo, H., Bartel, D. P., and Lai, E. C. (2008) The Drosophila hairpin RNA pathway generates endogenous short interfering RNAs. Nature 453, 803–806.PubMedCrossRefGoogle Scholar
  60. 60.
    Chung, W. J., Okamura, K., Martin, R., and Lai, E. C. (2008) Endogenous RNA interference provides a somatic defense against Drosophila transposons. Curr Biol 18, 795–802.PubMedCrossRefGoogle Scholar
  61. 61.
    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) Pseudogene-derived small interfering RNAs regulate gene expression in mouse oocytes. Nature 453, 534–538.PubMedCrossRefGoogle Scholar
  62. 62.
    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) An endogenous small interfering RNA pathway in Drosophila. Nature 453, 798–802.PubMedCrossRefGoogle Scholar
  63. 63.
    Ruby, J. G., Jan, C., Player, C., Axtell, M. J., Lee, W., Nusbaum, C., Ge, H., and Bartel, D. P. (2006) Large-scale sequencing reveals 21U-RNAs and additional microRNAs and endogenous siRNAs in C. elegans. Cell 127, 1193–1207.PubMedCrossRefGoogle Scholar
  64. 64.
    Gent, J. I., Lamm, A. T., Pavelec, D. M., Maniar, J. M., Parameswaran, P., Tao, L., Kennedy, S., and Fire, A. Z. (2010) Distinct phases of siRNA synthesis in an endogenous RNAi pathway in C. elegans Soma. Mol Cell 37, 593–595.CrossRefGoogle Scholar
  65. 65.
    Vasale, J. J., Gu, W., Thivierge, C., Batista, P. J., Claycomb, J. M., Youngman, E. M., Duchaine, T. F., Mello, C. C., and Conte, D., Jr. (2010) Sequential rounds of RNA-dependent RNA transcription drive endogenous small-RNA biogenesis in the ERGO-1/Argonaute pathway. Proc Natl Acad Sci USA 107, 3582–3587.PubMedCrossRefGoogle Scholar
  66. 66.
    Halic, M., and Moazed, D. (2009) 22G-RNAs in transposon silencing and centromere function. Mol Cell 36, 170–171.PubMedCrossRefGoogle Scholar
  67. 67.
    Gu, W., Shirayama, M., Conte, D., Jr., Vasale, J., Batista, P. J., Claycomb, J. M., Moresco, J. J., Youngman, E. M., Keys, J., Stoltz, M. J., Chen, C. C., Chaves, D. A., Duan, S., Kasschau, K. D., Fahlgren, N., Yates, J. R., 3rd, Mitani, S., Carrington, J. C., and Mello, C. C. (2009) Distinct argonaute-mediated 22G-RNA pathways direct genome surveillance in the C. elegans germline. Mol Cell 36, 231–244.PubMedCrossRefGoogle Scholar
  68. 68.
    Claycomb, J. M., Batista, P. J., Pang, K. M., Gu, W., Vasale, J. J., van Wolfswinkel, J. C., Chaves, D. A., Shirayama, M., Mitani, S., Ketting, R. F., Conte, D., Jr., and Mello, C. C. (2009) The argonaute CSR-1 and its 22G-RNA cofactors are required for holocentric chromosome segregation. Cell 139, 123–134.PubMedCrossRefGoogle Scholar
  69. 69.
    van Wolfswinkel, J. C., Claycomb, J. M., Batista, P. J., Mello, C. C., Berezikov, E., and Ketting, R. F. (2009) CDE-1 affects chromosome segregation through uridylation of CSR-1-bound siRNAs. Cell 139, 135–148.PubMedCrossRefGoogle Scholar
  70. 70.
    Lee, H. C., Chang, S. S., Choudhary, S., Aalto, A. P., Maiti, M., Bamford, D. H., and Liu, Y. (2009) qiRNA is a new type of small interfering RNA induced by DNA damage. Nature 459, 274–277.PubMedCrossRefGoogle Scholar
  71. 71.
    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
  72. 72.
    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) A novel class of small RNAs bind to MILI protein in mouse testes. Nature 442, 203–207.PubMedGoogle Scholar
  73. 73.
    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
  74. 74.
    Grivna, S. T., Beyret, E., Wang, Z., and Lin, H. (2006) A novel class of small RNAs in mouse spermatogenic cells. Genes Dev 20, 1709–1714.PubMedCrossRefGoogle Scholar
  75. 75.
    Batista, P. J., Ruby, J. G., Claycomb, J. M., Chiang, R., Fahlgren, N., Kasschau, K. D., Chaves, D. A., Gu, W., Vasale, J. J., Duan, S., Conte, D., Jr., Luo, S., Schroth, G. P., Carrington, J. C., Bartel, D. P., and Mello, C. C. (2008) PRG-1 and 21U-RNAs interact to form the piRNA complex required for fertility in C. elegans. Mol Cell 31, 67–78.PubMedCrossRefGoogle Scholar
  76. 76.
    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) Piwi and piRNAs act upstream of an endogenous siRNA pathway to suppress Tc3 transposon mobility in the Caenorhabditis elegans germline. Mol Cell 31, 79–90.PubMedCrossRefGoogle Scholar
  77. 77.
    Lau, N. C., Seto, A. G., Kim, J., Kuramochi-Miyagawa, S., Nakano, T., Bartel, D. P., and Kingston, R. E. (2006) Characterization of the piRNA complex from rat testes. Science 313, 363–367.PubMedCrossRefGoogle Scholar
  78. 78.
    Vagin, V. V., Sigova, A., Li, C., Seitz, H., Gvozdev, V., and Zamore, P. D. (2006) A distinct small RNA pathway silences selfish genetic elements in the germline. Science 313, 320–324.PubMedCrossRefGoogle Scholar
  79. 79.
    Lin, H. (2007) piRNAs in the germ line. Science 316, 397.PubMedCrossRefGoogle Scholar
  80. 80.
    Thomson, T., and Lin, H. (2009) The biogenesis and function of PIWI proteins and piRNAs: progress and prospect. Annu Rev Cell Dev Biol 25, 355–376.PubMedCrossRefGoogle Scholar
  81. 81.
    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
  82. 82.
    Malone, C. D., and Hannon, G. J. (2009) Small RNAs as guardians of the genome. Cell 136, 656–668.PubMedCrossRefGoogle Scholar
  83. 83.
    Girard, A., and Hannon, G. J. (2008) Conserved themes in small-RNA-mediated transposon control. Trends Cell Biol 18, 136–148.PubMedCrossRefGoogle Scholar
  84. 84.
    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
  85. 85.
    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.PubMedCrossRefGoogle Scholar
  86. 86.
    Xu, M., You, Y., Hunsicker, P., Hori, T., Small, C., Griswold, M. D., and Hecht, N. B. (2008) Mice deficient for a small cluster of Piwi-interacting RNAs implicate Piwi-interacting RNAs in transposon control. Biol Reprod 79, 51–57.PubMedCrossRefGoogle Scholar
  87. 87.
    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
  88. 88.
    Watanabe, T., Takeda, A., Tsukiyama, T., Mise, K., Okuno, T., Sasaki, H., Minami, N., and Imai, H. (2006) Identification and characterization of two novel classes of small RNAs in the mouse germline: retrotransposon-derived siRNAs in oocytes and germline small RNAs in testes. Genes Dev 20, 1732–1743.PubMedCrossRefGoogle Scholar
  89. 89.
    Saito, K., Nishida, K. M., Mori, T., Kawamura, Y., Miyoshi, K., Nagami, T., Siomi, H., and Siomi, M. C. (2006) Specific association of Piwi with rasiRNAs derived from retrotransposon and heterochromatic regions in the Drosophila genome. Genes Dev 20, 2214–2222.PubMedCrossRefGoogle Scholar
  90. 90.
    Kawaoka, S., Hayashi, N., Katsuma, S., Kishino, H., Kohara, Y., Mita, K., and Shimada, T. (2008) Bombyx small RNAs: genomic defense system against transposons in the silkworm, Bombyx mori. Insect Biochem Mol Biol 38, 1058–1065.PubMedCrossRefGoogle Scholar
  91. 91.
    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) A role for Piwi and piRNAs in germ cell maintenance and transposon silencing in Zebrafish. Cell 129, 69–82.PubMedCrossRefGoogle Scholar
  92. 92.
    Houwing, S., Berezikov, E., and Ketting, R. F. (2008) Zili is required for germ cell differentiation and meiosis in zebrafish. EMBO J 27, 2702–2711.PubMedCrossRefGoogle Scholar
  93. 93.
    Ro, S., Park, C., Song, R., Nguyen, D., Jin, J., Sanders, K. M., McCarrey, J. R., and Yan, W. (2007) Cloning and expression profiling of testis-expressed piRNA-like RNAs. RNA 13, 1693–1702.PubMedCrossRefGoogle Scholar
  94. 94.
    Gunawardane, L. S., Saito, K., Nishida, K. M., Miyoshi, K., Kawamura, Y., Nagami, T., Siomi, H., and Siomi, M. C. (2007) A slicer-mediated mechanism for repeat-associated siRNA 5' end formation in Drosophila. Science 315, 1587–1590.PubMedCrossRefGoogle Scholar
  95. 95.
    Malone, C. D., Brennecke, J., Dus, M., Stark, A., McCombie, W. R., Sachidanandam, R., and Hannon, G. J. (2009) Specialized piRNA pathways act in germline and somatic tissues of the Drosophila ovary. Cell 137, 522–535.PubMedCrossRefGoogle Scholar
  96. 96.
    Li, C., Vagin, V. V., Lee, S., Xu, J., Ma, S., Xi, H., Seitz, H., Horwich, M. D., Syrzycka, M., Honda, B. M., Kittler, E. L., Zapp, M. L., Klattenhoff, C., Schulz, N., Theurkauf, W. E., Weng, Z., and Zamore, P. D. (2009) Collapse of germline piRNAs in the absence of argonaute3 reveals somatic piRNAs in flies. Cell 137, 509–521.PubMedCrossRefGoogle Scholar
  97. 97.
    Sijen, T., Fleenor, J., Simmer, F., Thijssen, K. L., Parrish, S., Timmons, L., Plasterk, R. H., and Fire, A. (2001) On the role of RNA amplification in dsRNA-triggered gene silencing. Cell 107, 465–476.PubMedCrossRefGoogle Scholar
  98. 98.
    Aoki, K., Moriguchi, H., Yoshioka, T., Okawa, K., and Tabara, H. (2007) In vitro analyses of the production and activity of secondary small interfering RNAs in C. elegans. EMBO J 26, 5007–5019.PubMedCrossRefGoogle Scholar
  99. 99.
    Pak, J., and Fire, A. (2007) Distinct populations of primary and secondary effectors during RNAi in C. elegans. Science 315, 241–244.PubMedCrossRefGoogle Scholar
  100. 100.
    Sijen, T., Steiner, F. A., Thijssen, K. L., and Plasterk, R. H. (2007) Secondary siRNAs result from unprimed RNA synthesis and form a distinct class. Science 315, 244–247.PubMedCrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media, LLC 2011

Authors and Affiliations

  1. 1.Department of PhysiologyThe University of Texas Southwestern Medical CenterDallasUSA

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