The piRNA pathway in flies: Highlights and future directions

Current Opinion in Genetics and Development

Volumn 23, Issue 1, 2013, Pages 44-52

  Guzzardo, Paloma M ^a   Muerdter, Felix ^a   Hannon, Gregory J ^a  

^a HOWARD HUGHES MEDICAL INSTITUTE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

HISTONE; PIWI INTERACTING RNA; RIBONUCLEASE; RNA HELICASE;

BOMBYX MORI; CELLULAR DISTRIBUTION; COMPLEX FORMATION; DROSOPHILA MELANOGASTER; EMBRYO DEVELOPMENT; EUCHROMATIN; GENE CLUSTER; GENE LOCUS; GENE SILENCING; GENETIC CONSERVATION; HETEROCHROMATIN; HISTONE METHYLATION; NONHUMAN; PRIORITY JOURNAL; PROTEIN PROCESSING; REVIEW; RNA ANALYSIS; RNA BINDING; RNA SYNTHESIS; RNA TRANSCRIPTION; TRANSPOSON;

ANIMALS; DNA TRANSPOSABLE ELEMENTS; DROSOPHILA MELANOGASTER; DROSOPHILA PROTEINS; FEMALE; GENE SILENCING; GENETIC LOCI; GERM CELLS; OVARY; RNA, SMALL INTERFERING; SIGNAL TRANSDUCTION;

EID: 84877921779     PISSN: 0959437X     EISSN: 18790380     Source Type: Journal    
DOI: 10.1016/j.gde.2012.12.003     Document Type: Review

References (57)

1. Levin H.L., Moran J.V. Dynamic interactions between transposable elements and their hosts. Nat Rev Genet 2011, 12:615-627.
2. Malone C.D., Hannon G.J. Small RNAs as guardians of the genome. Cell 2009, 136:656-668.
3. Siomi M.C., Sato K., Pezic D., Aravin A.A. PIWI-interacting small RNAs: the vanguard of genome defence. Nat Rev Mol Cell Biol 2011, 12:246-258.
4. Malone C.D., Brennecke J., Dus M., Stark A., Mccombie W.R., Sachidanandam R., Hannon G.J. Specialized piRNA pathways act in germline and somatic tissues of the Drosophila ovary. Cell 2009, 137:522-535.
5. 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. Collapse of germline piRNAs in the absence of Argonaute3 reveals somatic piRNAs in flies. Cell 2009, 137:509-521.
6. Lécher P., Bucheton A., Pelisson A. Expression of the Drosophila retrovirus gypsy as ultrastructurally detectable particles in the ovaries of flies carrying a permissive flamenco allele. J Gen Virol 1997, 78(Pt 9):2379-2388.
7. Cox D.N., Chao A., Lin H. piwi encodes a nucleoplasmic factor whose activity modulates the number and division rate of germline stem cells. Development (Cambridge, England) 2000, 127:503-514.
8. Harris A.N., Macdonald P.M. Aubergine encodes a Drosophila polar granule component required for pole cell formation and related to eIF2C. Development (Cambridge, England) 2001, 128:2823-2832.
9. Brennecke J., Aravin A.A., Stark A., Dus M., Kellis M., Sachidanandam R., Hannon G.J. Discrete small RNA-generating loci as master regulators of transposon activity in Drosophila. Cell 2007, 128:1089-1103.
10. Gunawardane L.S., Saito K., Nishida K.M., Miyoshi K., Kawamura Y., Nagami T., Siomi H., Siomi M.C. A slicer-mediated mechanism for repeat-associated siRNA 5' end formation in Drosophila. Science (New York, NY) 2007, 315:1587-1590.
11. Ishizu H., Siomi H., Siomi M.C. Biology of PIWI-interacting RNAs: new insights into biogenesis and function inside and outside of germlines. Genes Dev 2012, 26:2361-2373.
12. Niki Y., Yamaguchi T., Mahowald A.P. Establishment of stable cell lines of Drosophila germ-line stem cells. Proc Natl Acad Sci USA 2006, 103:16325-16330.
13. Lau N.C., Robine N., Martin R., Chung W.-J., Niki Y., Berezikov E., Lai E.C. Abundant primary piRNAs, endo-siRNAs, and microRNAs in a Drosophila ovary cell line. Genome Res 2009, 19:1776-1785.
14. Saito K., Inagaki S., Mituyama T., Kawamura Y., Ono Y., Sakota E., Kotani H., Asai K., Siomi H., Siomi M.C. A regulatory circuit for piwi by the large Maf gene traffic jam in Drosophila. Nature 2009, 461:1296-1299.
15. Robine N., Lau N.C., Balla S., Jin Z., Okamura K., Kuramochi-Miyagawa S., Blower M.D., Lai E.C. A broadly conserved pathway generates 3'UTR-directed primary piRNAs. Curr Biol 2009, 19:2066-2076.
16. Khurana J.S., Wang J., Xu J., Koppetsch B.S., Thomson T.C., Nowosielska A., Li C., Zamore P.D., Weng Z., Theurkauf W.E. Adaptation to P element transposon invasion in Drosophila melanogaster. Cell 2011, 147:1551-1563.
17. Robert V., Prud, apos, homme N., Kim A., Bucheton A., Pelisson A. Characterization of the flamenco region of the Drosophila melanogaster genome. Genetics 2001, 158:701-713.
18. Rangan P., Malone C.D., Navarro C., Newbold S.P., Hayes P.S., Sachidanandam R., Hannon G.J., Lehmann R. piRNA production requires heterochromatin formation in Drosophila. Curr Biol 2011, 21:1373-1379.
19. Pane A., Jiang P., Zhao D.Y., Singh M., Schüpbach T. The Cutoff protein regulates piRNA cluster expression and piRNA production in the Drosophila germline. EMBO J 2011, 30:4601-4615.
20. Klattenhoff C., Xi H., Li C., Lee S., Xu J., Khurana J.S., Zhang F., Schultz N., Koppetsch B.S., Nowosielska A., et al. The Drosophila HP1 homolog Rhino is required for transposon silencing and piRNA production by dual-strand clusters. Cell 2009, 138:1137-1149.
21. Muerdter F., Olovnikov I., Molaro A., Rozhkov N.V., Czech B., Gordon A., Hannon G.J., Aravin A.A. Production of artificial piRNAs in flies and mice. RNA (New York, NY) 2012, 18:42-52.
22. Zhang F., Wang J., Xu J., Zhang Z., Koppetsch B.S., Schultz N., Vreven T., Meignin C., Davis I., Zamore P.D., et al. UAP56 couples piRNA clusters to the perinuclear transposon silencing machinery. Cell 2012, 151:871-884.
23. Ipsaro J.J., Haase A.D., Knott S.R., Joshua-Tor L., Hannon G.J. The structural biochemistry of Zucchini implicates it as a nuclease in piRNA biogenesis. Nature 2012.
24. Nishimasu H., Ishizu H., Saito K., Fukuhara S., Kamatani M.K., Bonnefond L., Matsumoto N., Nishizawa T., Nakanaga K., Aoki J., et al. Structure and function of Zucchini endoribonuclease in piRNA biogenesis. Nature 2012.
25. Huang H., Gao Q., Peng X., Choi S.-Y., Sarma K., Ren H., Morris A.J., Frohman M.A. piRNA-associated germline nuage formation and spermatogenesis require MitoPLD profusogenic mitochondrial-surface lipid signaling. Dev Cell 2011, 20:376-387.
26. Watanabe T., Chuma S., Yamamoto Y., Kuramochi-Miyagawa S., Totoki Y., Toyoda A., Hoki Y., Fujiyama A., Shibata T., Sado T., et al. MITOPLD is a mitochondrial protein essential for nuage formation and piRNA biogenesis in the mouse germline. Dev Cell 2011, 20:364-375.
27. Saito K., Ishizu H., Komai M., Kotani H., Kawamura Y., Nishida K.M., Siomi H., Siomi M.C. Roles for the Yb body components Armitage and Yb in primary piRNA biogenesis in Drosophila. Genes Dev 2010, 24:2493-2498.
28. Handler D., Olivieri D., Novatchkova M., Gruber F.S., Meixner K., Mechtler K., Stark A., Sachidanandam R., Brennecke J. A systematic analysis of Drosophila TUDOR domain-containing proteins identifies Vreteno and the Tdrd12 family as essential primary piRNA pathway factors. EMBO J 2011, 30:3977-3993.
29. Arnoult D., Soares F., Tattoli I., Girardin S.E. Mitochondria in innate immunity. EMBO Rep 2011, 12:901-910.
30. Kawaoka S., Izumi N., Katsuma S., Tomari Y. 3' end formation of PIWI-interacting RNAs in vitro. Mol Cell 2011, 43:1015-1022.
31. Horwich M.D., Li C., Matranga C., Vagin V., Farley G., Wang P., Zamore P.D. The Drosophila RNA methyltransferase, DmHen1, modifies germline piRNAs and single-stranded siRNAs in RISC. Curr Biol 2007, 17:1265-1272.
32. Saito K., Sakaguchi Y., Suzuki T., Suzuki T., Siomi H., Siomi M.C. Pimet, the Drosophila homolog of HEN1, mediates 2'-O-methylation of Piwi-interacting RNAs at their 3' ends. Genes Dev 2007, 21:1603-1608.
33. Olivieri D., Sykora M.M., Sachidanandam R., Mechtler K., Brennecke J. An in vivo RNAi assay identifies major genetic and cellular requirements for primary piRNA biogenesis in Drosophila. EMBO J 2010, 29:3301-3317.
34. Zamparini A.L., Davis M.Y., Malone C.D., Vieira E., Zavadil J., Sachidanandam R., Hannon G.J., Lehmann R. Vreteno, a gonad-specific protein, is essential for germline development and primary piRNA biogenesis in Drosophila. Development (Cambridge, England) 2011, 138:4039-4050.
35. Olivieri D., Senti K.-A., Subramanian S., Sachidanandam R., Brennecke J. The cochaperone shutdown defines a group of biogenesis factors essential for all piRNA populations in Drosophila. Mol Cell 2012, 47:954-969.
36. Preall J.B., Czech B., Guzzardo P.M., Muerdter F., Hannon G.J. shutdown is a component of the Drosophila piRNA biogenesis machinery. RNA (New York, NY) 2012, 18:1446-1457.
37. Xiol J., Cora E., Koglgruber R., Chuma S., Subramanian S., Hosakawa M., Reuter M., Yang Z., Berninger P., Palencia A., et al. A role for Fkbp6 and the chaperone machinery in piRNA amplification and transposon silencing. Mol Cell 2012, 47:970-979.
38. Szakmary A., Reedy M., Qi H., Lin H. The Yb protein defines a novel organelle and regulates male germline stem cell self-renewal in Drosophila melanogaster. J Cell Biol 2009, 185:613-627.
39. Megosh H.B., Cox D.N., Campbell C., Lin H. The role of PIWI and the miRNA machinery in Drosophila germline determination. Curr Biol 2006, 16:1884-1894.
40. Brennecke J., Malone C.D., Aravin A.A., Sachidanandam R., Stark A., Hannon G.J. An epigenetic role for maternally inherited piRNAs in transposon silencing. Science (New York, NY) 2008, 322:1387-1392.
41. Grentzinger T., Armenise C., Brun C., Mugat B., Serrano V., Pelisson A., Chambeyron S. piRNA-mediated transgenerational inheritance of an acquired trait. Genome Res 2012, 22:1877-1888.
42. Klenov M.S., Sokolova O.A., Yakushev E.Y., Stolyarenko A.D., Mikhaleva E.A., Lavrov S.A., Gvozdev V.A. Separation of stem cell maintenance and transposon silencing functions of Piwi protein. Proc Natl Acad Sci USA 2011, 108:18760-18765.
43. Huisinga K., Elgin S. Small RNA-directed heterochromatin formation in the context of development: what flies might learn from fission yeast. Biochim Biophys Acta 2008, 1789:3-16.
44. Aravin A.A., Sachidanandam R., Girard A., Fejes Toth K., Hannon G.J. Developmentally regulated piRNA clusters implicate MILI in transposon control. Science (New York, NY) 2007, 316:744-747.
45. Aravin A.A., Bourc'his D. Small RNA guides for de novo DNA methylation in mammalian germ cells. Genes Dev 2008, 22:970-975.
46. Klenov M.S., Lavrov S.A., Stolyarenko A.D., Ryazansky S.S., Aravin A.A., Tuschl T., Gvozdev V.A. Repeat-associated siRNAs cause chromatin silencing of retrotransposons in the Drosophila melanogaster germline. Nucleic Acids Res 2007, 35:5430-5438.
47. Wang S.H., Elgin S.C.R. Drosophila Piwi functions downstream of piRNA production mediating a chromatin-based transposon silencing mechanism in female germ line. Proc Natl Acad Sci USA 2011, 108:21164-21169.
48. Shpiz S., Olovnikov I., Sergeeva A., Lavrov S., Abramov Y., Savitsky M., Kalmykova A. Mechanism of the piRNA-mediated silencing of Drosophila telomeric retrotransposons. Nucleic Acids Res 2011, 39:8703-8711.
49. Sienski G., Dönertas D., Brennecke J Transcriptional silencing of transposons by Piwi and Maelstrom and its impact on chromatin state and gene expression. Cell 2012, 151:964-980.
50. Findley S.D., Tamanaha M., Clegg N.J., Ruohola-Baker H. Maelstrom, a Drosophila spindle-class gene, encodes a protein that colocalizes with Vasa and RDE1/AGO1 homolog, Aubergine, in nuage. Development (Cambridge, England) 2003, 130:859-871.
51. Lim A.K., Kai T. Unique germ-line organelle, nuage, functions to repress selfish genetic elements in Drosophila melanogaster. Proc Natl Acad Sci USA 2007, 104:6714-6719.
52. Lachner M., apos O., Carroll D., Rea S., Mechtler K., Jenuwein T. Methylation of histone H3 lysine 9 creates a binding site for HP1 proteins. Nature 2001, 410:116-120.
53. Bannister A.J., Zegerman P., Partridge J.F., Miska E.A., Thomas J.O., Allshire R.C., Kouzarides T. Selective recognition of methylated lysine 9 on histone H3 by the HP1 chromo domain. Nature 2001, 410:120-124.
54. Brower-Toland B., Findley S.D., Jiang L., Liu L., Yin H., Dus M., Zhou P., Elgin S.C.R., Lin H. Drosophila PIWI associates with chromatin and interacts directly with HP1a. Genes Dev 2007, 21:2300-2311.
55. de Vanssay A., Bougé A.-L., Boivin A., Hermant C., Teysset L., Delmarre V., Antoniewski C., Ronsseray S. Paramutation in Drosophila linked to emergence of a piRNA-producing locus. Nature 2012, 490:112-115.
56. Haynes K., Caudy A., Collins L., Elgin S. Element 1360 and RNAi components contribute to HP1-dependent silencing of a pericentric reporter. Curr Biol 2006, 16:2222-2227.
57. Pal-Bhadra M. Heterochromatic silencing and HP1 localization in Drosophila are dependent on the RNAi machinery. Science (New York, NY) 2004, 303:669-672.