The epigenetic regulation of transposable elements by PIWI-interacting RNAs in Drosophila

Genes and Genetic Systems

Volumn 88, Issue 1, 2013, Pages 9-17

  Saito, Kuniaki ^a  

^a KEIO UNIVERSITY SCHOOL OF MEDICINE   (Japan)

Author keywords

Drosophila; Hybrid dysgenesis; PiRNAs; PIWI proteins; Transposable elements

Indexed keywords

ARGONAUTE 3 PROTEIN; ARGONAUTE PROTEIN; PIWI INTERACTING RNA; SMALL UNTRANSLATED RNA; UNCLASSIFIED DRUG;

AUBERGINE; BIOGENESIS; DNA METHYLATION; DROSOPHILA; EPIGENETICS; EVOLUTIONARY ADAPTATION; GENE REPRESSION; GENE SILENCING; GENOME ANALYSIS; GENOMIC INSTABILITY; GERM CELL; HETEROCHROMATIN; HISTONE METHYLATION; HYBRID DYSGENESIS; INSECT GENOME; NONHUMAN; PROTEIN EXPRESSION; REVIEW; SCHIZOSACCHAROMYCES POMBE; TETRAHYMENA; TRANSPOSON;

EID: 84877898486     PISSN: 13417568     EISSN: 18805779     Source Type: Journal    
DOI: 10.1266/ggs.88.9     Document Type: Review

References (76)

1. 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.
2. Aravin, A., Gaidatzis, D., Pfeffer, S., Lagos-Quintana, M., Landgraf, P., Iovino, N., Morris, P., Brownstein, M. J., Kuramochi-Miyagawa, S., Nakano, T., et al. (2006) A novel class of small RNAs bind to MILI protein in mouse testes. Nature 442, 203-207.
3. Aravin, A. A., Sachidanandam, R., Girard, A., Fejes-Toth, K., and Hannon, G. J. (2007) Developmentally regulated piRNA clusters implicate MILI in transposon control. Science 316, 744-747.
4. 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 individual transposons is linked to de novo DNA methylation in mice. Mol. Cell 31, 785-799.
5. Biemont, C., and Vieira, C. (2006) Genetics: junk DNA as an evolutionary force. Nature 443, 521-524.
6. 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 transpo son activity in Drosophila. Cell 128, 1089-1103.
7. 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.
8. Brookfield, J. F., Montgomery, E., and Langley, C. H. (1984) Apparent absence of transposable elements related to the P elements of D. Melanogaster in other species of Drosophila. Nature 310, 330-332.
9. Bucheton, A., Paro, R., Sang, H. M., Pelisson, A., and Finnegan, D. J. (1984) The molecular basis of I-R hybrid dysgenesis in Drosophila melanogaster: identification, cloning, and properties of the I factor. Cell 38, 153-163.
10. Callinan, P. A., and Batzer, M. A. (2006) Retrotransposable elements and human disease. Genome Dyn. 1, 104-115.
11. Carmell, M. A., Girard, A., van de Kant, H. J., Bourc'his, D., Bestor, T. H., de Rooij, D. G., and Hannon, G. J. (2007) MIWI2 is essential for spermatogenesis and repression of transposons in the mouse male germline. Dev. Cell 12, 503-514.
12. Chambeyron, S., Popkova, A., Payen-Groschene, G., Brun, C., Laouini, D., Pelisson, A., and Bucheton, A. (2008) piRNA-mediated nuclear accumulation of retrotransposon transcripts in the Drosophila female germline. Proc. Natl. Acad. Sci. USA 105, 14964-14969.
13. Cox, D. N., Chao, A., Baker, J., Chang, L., Qiao, D., and Lin, H. (1998) A novel class of evolutionarily conserved genes defined by piwi are essential for stem cell self-renewal. Genes Dev. 12, 3715-3727.
14. Cox, D. N., Chao, A., and Lin, H. (2000) piwi encodes a nucleoplasmic factor whose activity modulates the number and division rate of germline stem cells. Development 127, 503-514.
15. Czech, B., Malone, C. D., Zhou, R., Stark, A., Schlingeheyde, C., Dus, M., Perrimon, N., Kellis, M., Wohlschlegel, J. A., Sachidanandam, R., et al. (2008) An endogenous small interfering RNA pathway in Drosophila. Nature 453, 798-802.
16. Daniels, S. B., Peterson, K. R., Strausbaugh, L. D., Kidwell, M. G., and Chovnick, A. (1990) Evidence for horizontal transmission of the P transposable element between Drosophila species. Genetics 124, 339-355.
17. Darricarrere, N., Liu, N., Watanabe, T., and Lin, H. (2013) Function of Piwi, a nuclear Piwi/Argonaute protein, is independent of its slicer activity. Proc. Natl. Acad. Sci. USA 110, 1297-1302.
18. Deshpande, G., Calhoun, G., and Schedl, P. (2005) Drosophila argonaute-2 is required early in embryogenesis for the assembly of centric/centromeric heterochromatin, nuclear division, nuclear migration, and germ-cell formation. Genes Dev. 19, 1680-1685.
19. Desset, S., Buchon, N., Meignin, C., Coiffet, M., and Vaury, C. (2008) In Drosophila melanogaster the COM locus directs the somatic silencing of two retrotransposons through both Piwi-dependent and -independent pathways. PLoS ONE 3, e1526.
20. Eissenberg, J. C., James, T. C., Foster-Hartnett, D. M., Hartnett, T., Ngan, V., and Elgin, S. C. (1990) Mutation in a heterochromatin-specific chromosomal protein is associated with suppression of position-effect variegation in Drosophila melanogaster. Proc. Natl. Acad. Sci. USA 87, 9923-9927.
21. Finnegan, D. J. (2012) Retrotransposons. Curr. Biol. 22, R432-R437.
22. Ghildiyal, M., and Zamore, P. D. (2009) Small silencing RNAs: an expanding universe. Nat. Rev. Genet. 10, 94-108.
23. 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.
24. Gogvadze, E., and Buzdin, A. (2009) Retroelements and their impact on genome evolution and functioning. Cell. Mol. Life Sci. 66, 3727-3742.
25. Grewal, S. I. (2010) RNAi-dependent formation of heterochromatin and its diverse functions. Curr. Opin. Genet. Dev. 20, 134-141.
26. Grivna, S. T., Beyret, E., Wang, Z., and Lin, H. (2006a) A novel class of small RNAs in mouse spermatogenic cells. Genes Dev. 20, 1709-1714.
27. Grivna, S. T., Pyhtila, B., and Lin, H. (2006b) MIWI associates with translational machinery and PIWI-interacting RNAs (piRNAs) in regulating spermatogenesis. Proc. Natl. Acad. Sci. USA 103, 13415-13420.
28. 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.
29. Hancks, D. C., and Kazazian, H. H. Jr. (2012) Active human retrotransposons: variation and disease. Curr. Opin. Genet. Dev. 22, 191-203.
30. Harris, A. N., and Macdonald, P. M. (2001) Aubergine encodes a Drosophila polar granule component required for pole cell formation and related to eIF2C. Development 128, 2823-2832.
31. Hiraizumi, Y. (1971) Spontaneous recombination in Drosophila melanogaster males. Proc. Natl. Acad. Sci. USA 68, 268-270.
32. Ichiyanagi, K. (2013) Epigenetic regulation of transcription and possible functions of mammalian short interspersed elements, SINEs. Genes Genet. Syst. 88, 19-29.
33. Ishizu, H., Siomi, H., and Siomi, M. C. (2012) Biology of PIWIinteracting RNAs: new insights into biogenesis and function inside and outside of germlines. Genes Dev. 26, 2361- 2373.
34. Ito, H. (2013) Small RNAs and regulation of transposons in plants. Genes Genet. Syst. 88, 3-7.
35. Juliano, C., Wang, J., and Lin, H. (2011) Uniting germline and stem cells: the function of Piwi proteins and the piRNA pathway in diverse organisms. Annu. Rev. Genet. 45, 447-469.
36. Kapitonov, V. V., and Jurka, J. (2003) Molecular paleontology of transposable elements in the Drosophila melanogaster genome. Proc. Natl. Acad. Sci. USA 100, 6569-6574.
37. Kawamura, Y., Saito, K., Kin, T., Ono, Y., Asai, K., Sunohara, T., Okada, T. N., Siomi, M. C., and Siomi, H. (2008) Drosophila endogenous small RNAs bind to Argonaute 2 in somatic cells. Nature 453, 793-797.
38. Khurana, J. S., and Theurkauf, W. (2010) piRNAs, transposon silencing, and Drosophila germline development. J. Cell Biol. 191, 905-913.
39. Khurana, J. S., Wang, J., Xu, J., Koppetsch, B. S., Thomson, T. C., Nowosielska, A., Li, C., Zamore, P. D., Weng, Z., and Theurkauf, W. E. (2011) Adaptation to P element transposon invasion in Drosophila melanogaster. Cell 147, 1551-1563.
40. Kidwell, M. G., Kidwell, J. F., and Sved, J. A. (1977) Hybrid dysgenesis in Drosophila melanogaster: A syndrome of aberrant traits including mutation, sterility and male recombination. Genetics 86, 813-833.
41. Klattenhoff, C., Xi, H., Li, C., Lee, S., Xu, J., Khurana, J. S., Zhang, F., Schultz, N., Koppetsch, B. S., Nowosielska, A., et al. (2009) The Drosophila HP1 homolog Rhino is required for transposon silencing and piRNA production by dualstrand clusters. Cell 138, 1137-1149.
42. Klenov, M. S., Sokolova, O. A., Yakushev, E. Y., Stolyarenko, A. D., Mikhaleva, E. A., Lavrov, S. A., and Gvozdev, V. A. (2011) Separation of stem cell maintenance and transposon silencing functions of Piwi protein. Proc. Natl. Acad. Sci. USA 108, 18760-18765.
43. Kuramochi-Miyagawa, S., Watanabe, T., Gotoh, K., Totoki, Y., Toyoda, A., Ikawa, M., Asada, N., Kojima, K., Yamaguchi, Y., Ijiri, T. W., et al. (2008) DNA methylation of retrotransposon genes is regulated by Piwi family members MILI and MIWI2 in murine fetal testes. Genes Dev. 22, 908-917.
44. Lander, E. S., Linton, L.M., Birren, B., Nusbaum, C., Zody, M. C., Baldwin, J., Devon, K., Dewar, K., Doyle, M., FitzHugh, W., et al. (2001) Initial sequencing and analysis of the human genome. Nature 409, 860-921.
45. 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.
46. Lau, N. C., Robine, N., Martin, R., Chung, W. J., Niki, Y., Berezikov, E., and Lai, E. C. (2009) Abundant primary piRNAs, endo-siRNAs, and microRNAs in a Drosophila ovary cell line. Genome Res. 19, 1776-1785.
47. Levin, H. L., and Moran, J. V. (2011) Dynamic interactions between transposable elements and their hosts. Nat. Rev. Genet. 12, 615-627.
48. Li, C., Vagin, V. V., Lee, S., Xu, J., Ma, S., Xi, H., Seitz, H., Horwich, M. D., Syrzycka, M., Honda, B. M., et al. (2009) Collapse of germline piRNAs in the absence of Argonaute3 reveals somatic piRNAs in flies. Cell 137, 509-521.
49. Malone, C. D., and Hannon, G. J. (2009) Small RNAs as guardians of the genome. Cell 136, 656-668.
50. Moazed, D. (2009) Small RNAs in transcriptional gene silencing and genome defence. Nature 457, 413-420.
51. Mochizuki, K. (2012) Developmentally programmed, RNAdirected genome rearrangement in Tetrahymena. Dev. Growth Differ. 54, 108-119.
52. Negre, N., Brown, C. D., Ma, L., Bristow, C. A., Miller, S. W., Wagner, U., Kheradpour, P., Eaton, M. L., Loriaux, P., Sealfon, R., et al. (2011) A cis-regulatory map of the Drosophila genome. Nature 471, 527-531.
53. Nishida, K. M., Saito, K., Mori, T., Kawamura, Y., Nagami-Okada, T., Inagaki, S., Siomi, H., and Siomi, M. C. (2007) Gene silencing mechanisms mediated by Aubergine piRNA complexes in Drosophila male gonad. RNA 13, 1911-1922.
54. Okamura, K., Ishizuka, A., Siomi, H., and Siomi, M. C. (2004) Distinct roles for Argonaute proteins in small RNA-directed RNA cleavage pathways. Genes Dev. 18, 1655-1666.
55. 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.
56. Pelisson, A., Song, S. U., Prud'homme, N., Smith, P. A., Bucheton, A., and Corces, V. G. (1994) Gypsy transposition correlates with the production of a retroviral envelope-like protein under the tissue-specific control of the Drosophila flamenco gene. EMBO J. 13, 4401-4411.
57. Pillai, R. S., and Chuma, S. (2012) piRNAs and their involvement in male germline development in mice. Dev. Growth Differ. 54, 78-92.
58. Robine, N., Lau, N. C., Balla, S., Jin, Z., Okamura, K., Kuramochi-Miyagawa, S., Blower, M. D., and Lai, E. C. (2009) A broadly conserved pathway generates 3′UTRdirected primary piRNAs. Curr. Biol. 19, 2066-2076.
59. Rongo, C., and Lehmann, R. (1996) Regulated synthesis, transport and assembly of the Drosophila germ plasm. Trends Genet. 12, 102-109.
60. Rubin, G. M., Kidwell, M. G., and Bingham, P. M. (1982) The molecular basis of P-M hybrid dysgenesis: the nature of induced mutations. Cell 29, 987-994.
61. Saito, K., and Siomi, M. C. (2010) Small RNA-mediated quiescence of transposable elements in animals. Dev. Cell 19, 687-697.
62. 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.
63. Saito, K., Inagaki, S., Mituyama, T., Kawamura, Y., Ono, Y., Sakota, E., Kotani, H., Asai, K., Siomi, H., and Siomi, M. C. (2009) A regulatory circuit for piwi by the large Maf gene traffic jam in Drosophila. Nature 461, 1296-1299.
64. Saito, K., Ishizu, H., Komai, M., Kotani, H., Kawamura, Y., Nishida, K. M., Siomi, H., and Siomi, M. C. (2010) Roles for the Yb body components Armitage and Yb in primary piRNA biogenesis in Drosophila. Genes Dev. 24, 2493-2498.
65. Sashital, D. G., and Doudna, J. A. (2010) Structural insights into RNA interference. Curr. Opin. Struct. Biol. 20, 90-97.
66. Senti, K. A., and Brennecke, J. (2010) The piRNA pathway: a fly's perspective on the guardian of the genome. Trends Genet. 26, 499-509.
67. Shpiz, S., Olovnikov, I., Sergeeva, A., Lavrov, S., Abramov, Y., Savitsky, M., and Kalmykova, A. (2011) Mechanism of the piRNA-mediated silencing of Drosophila telomeric retrotransposons. Nucleic Acids Res. 39, 8703-8711.
68. Sienski, G., Donertas, D., and Brennecke, J. (2012) Transcriptional silencing of transposons by Piwi and maelstrom and its impact on chromatin state and gene expression. Cell 151, 964-980.
69. Siomi, M. C., Sato, K., Pezic, D., and Aravin, A. A. (2011) PIWIinteracting small RNAs: the vanguard of genome defence. Nat. Rev. Mol. Cell Biol. 12, 246-258.
70. Slotkin, R. K., and Martienssen, R. (2007) Transposable elements and the epigenetic regulation of the genome. Nat. Rev. Genet. 8, 272-285.
71. 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.
72. Wang, S. H., and Elgin, S. C. (2011) Drosophila Piwi functions downstream of piRNA production mediating a chromatinbased transposon silencing mechanism in female germ line. Proc. Natl. Acad. Sci. USA 108, 21164-21169.
73. 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.
74. Watanabe, T., Tomizawa, S., Mitsuya, K., Totoki, Y., Yamamoto, Y., Kuramochi-Miyagawa, S., Iida, N., Hoki, Y., Murphy, P. J., Toyoda, A., et al. (2011) Role for piRNAs and noncoding RNA in de novo DNA methylation of the imprinted mouse Rasgrf1 locus. Science 332, 848-852.
75. Williams, R. W., and Rubin, G. M. (2002) ARGONAUTE1 is required for efficient RNA interference in Drosophila embryos. Proc. Natl. Acad. Sci. USA 99, 6889-6894.
76. Yin, H., and Lin, H. (2007) An epigenetic activation role of Piwi and a Piwi-associated piRNA in Drosophila melanogaster. Nature 450, 304-308.