Transgenerationally inherited piRNAs trigger piRNA biogenesis by changing the chromatin of piRNA clusters and inducing precursor processing

Genes and Development

Volumn 28, Issue 15, 2014, Pages 1667-1680

  Le Thomas, Adrien ^a,b   Stuwe, Evelyn ^a,c   Li, Sisi ^d   Du, Jiamu ^d   Marinov, Georgi ^a   Rozhkov, Nikolay ^e,f   Chen, Yung Chia Ariel ^a   Luo, Yicheng ^a   Sachidanandam, Ravi ^g   Toth, Katalin Fejes ^a   Patel, Dinshaw ^d   Aravin, Alexei A ^a  

^a CALIFORNIA INSTITUTE OF TECHNOLOGY   (United States)

^b SORBONNE UNIVERSITÉ   (France)

^c UNIVERSITY OF REGENSBURG   (Germany)

^d MEMORIAL SLOAN KETTERING CANCER CENTER   (United States)

^e Howard Hughes Medical Institute Cold Spring Harbor Laboratory Cold Spring Harbor   (United States)

^f HOWARD HUGHES MEDICAL INSTITUTE   (United States)

^g MOUNT SINAI SCHOOL OF MEDICINE   (United States)

Author keywords

Epigenetics; H3K9me3; piRNA

Indexed keywords

HETEROCHROMATIN PROTEIN 1; HISTONE H3; LYSINE; PIWI INTERACTING RNA; PROTEIN RHINO; RNA BINDING PROTEIN; SMALL UNTRANSLATED RNA; UNCLASSIFIED DRUG;

ARTICLE; BIOGENESIS; CHROMATIN STRUCTURE; CONTROLLED STUDY; CYTOPLASM; DROSOPHILA MELANOGASTER; ENHANCER REGION; EPIGENETICS; FEMALE; GENETIC TRANSCRIPTION; GENOME; GERM CELL; MALE; NONHUMAN; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; PROTEIN DOMAIN; PROTEIN PROTEIN INTERACTION; RNA PROCESSING; RNA SEQUENCE; TRANSPOSON;

EPIGENETICS; H3K9ME3; PIRNA;

ANIMALS; CHROMATIN; CHROMOSOMAL PROTEINS, NON-HISTONE; DNA METHYLATION; DROSOPHILA; DROSOPHILA PROTEINS; EPIGENESIS, GENETIC; GENE EXPRESSION REGULATION; HISTONES; MULTIGENE FAMILY; PROTEIN BINDING; RNA PRECURSORS; RNA, SMALL UNTRANSLATED; RNA-BINDING PROTEINS; TRANSGENES;

EID: 84905270270     PISSN: 08909369     EISSN: 15495477     Source Type: Journal    
DOI: 10.1101/gad.245514.114     Document Type: Article

References (57)

1. Adams PD, Afonine PV, Bunkóczi G, Chen VB, Davis IW, Echols N, Headd JJ, Hung LW, Kapral GJ, Grosse-Kunstleve RW, et al. 2010. PHENIX: a comprehensive Python-based system for macromolecular structure solution. Acta Crystallogr D Biol Crystallogr 66: 213-221.
2. Alekseyenko AA, Gorchakov AA, Kharchenko PV, Kuroda MI. 2014. Reciprocal interactions of human C10orf12 and C17orf96 with PRC2 revealed by BioTAP-XL cross-linking and affinity purification. Proc Natl Acad Sci 111: 2488-2493.
3. Aravin A, Hannon G, Brennecke J. 2007a. The Piwi-piRNA pathway provides an adaptive defense in the transposon arms race. Science 318: 761-764.
4. Aravin A, Sachidanandam R, Girard A, Fejes-Toth K, Hannon G. 2007b. Developmentally regulated piRNA clusters implicate MILI in transposon control. Science 316: 744-747.
5. Aravin AA, Sachidanandam R, Bourc'his D, Schaefer C, Pezic D, Toth KF, Bestor T, Hannon GJ. 2008. A piRNA pathway primed by individual transposons is linked to de novo DNA methylation in mice. Mol Cell 31: 785-799.
6. Brennecke J, Aravin A, Stark A, Dus M, Kellis M, Sachidanandam R, Hannon G. 2007. Discrete small RNA-generating loci as master regulators of transposon activity in Drosophila. Cell 128: 1089-1103.
7. Brennecke J, Malone C, Aravin A, Sachidanandam R, Stark A, Hannon G. 2008. An epigenetic role for maternally inherited piRNAs in transposon silencing. Science, 322: 1387-1392.
8. Chen Y, Pane A, Schüpbach T. 2007. Cutoff and aubergine mutations result in retrotransposon upregulation and checkpoint activation in Drosophila. Curr Biol 17: 637-642.
9. Czech B, Malone CD, Zhou R, Stark A, Schlingeheyde C, Dus M, Perrimon N, Kellis M, Wohlschlegel JA, Sachidanandam R, et al. 2008. An endogenous small interfering RNA pathway in Drosophila. Nature 453: 798-802.
10. de Vanssay A, Bougé A-L, Boivin A, Hermant C, Teysset L, Delmarre V, Antoniewski C, Ronsseray S. 2012. Paramutation in Drosophila linked to emergence of a piRNA-producing locus. Nature 490: 112-115.
11. Dorer DR, Henikoff S. 1997. Transgene repeat arrays interact with distant heterochromatin and cause silencing in cis and trans. Genetics 147: 1181-1190.
12. Emsley P, Lohkamp B, Scott WG, Cowtan K. 2010. Features and development of Coot. Acta Crystallogr D Biol Crystallogr 66: 486-501.
13. Ghildiyal M, Zamore P. 2009. Small silencing RNAs: an expanding universe. Nat Rev Genet 10: 94-108.
14. Grewal SI. 2010. RNAi-dependent formation of heterochromatin and its diverse functions. Curr Opin Genet Dev 20: 134-141.
15. Grewal S, Jia S. 2007. Heterochromatin revisited. Nat Rev Genet 8: 35-46.
16. Gunawardane LS, Saito K, Nishida KM, Miyoshi K, Kawamura Y, Nagami T, Siomi H, Siomi MC. 2007. A slicer-mediated mechanism for repeat-associated siRNA 59 end formation in Drosophila. Science 315: 1587-1590.
17. Harris AN, Macdonald PM. 2001. Aubergine encodes a Drosophila polar granule component required for pole cell formation and related to eIF2C. Development 128: 2823-2832.
18. Jacobs SA, Khorasanizadeh S. 2002. Structure of HP1 chromodomain bound to a lysine 9-methylated histone H3 tail. Science 295: 2080-2083.
19. Jiao X, Xiang S, Oh C, Martin CE, Tong L, Kiledjian M. 2010. Identification of a quality-control mechanism for mRNA 59-end capping. Nature 467: 608-611.
20. Jiao X, Chang JH, Kilic T, Tong L, Kiledjian M. 2013. A mammalian pre-mRNA 59 end capping quality control mechanism and an unexpected link of capping to pre-mRNA processing. Mol Cell 50: 104-115.
21. Johnson DS, Mortazavi A, Myers RM, Wold B. 2007. Genomewide mapping of in vivo protein-DNA interactions. Science 316: 1497-1502.
22. Josse T, Teysset L, Todeschini A-L, Sidor C, Anxolabéhère D, Ronsseray S. 2007. Telomeric trans-silencing: an epigenetic repression combining RNA silencing and heterochromatin formation. PLoS Genet 3: 1633-1643.
23. Kalmykova AI, Klenov MS, Gvozdev VA. 2005. Argonaute protein PIWI controls mobilization of retrotransposons in the Drosophila male germline. Nucleic Acids Res 33: 2052-2059.
24. Kelleher E, Edelman N, Barbash D. 2012. Drosophila interspecific hybrids phenocopy piRNA-pathway mutants. PLoS Biol 10: e1001428.
25. Kim M, Krogan NJ, Vasiljeva L, Rando OJ, Nedea E, Greenblatt JF, Buratowski S. 2004. The yeast Rat1 exonuclease promotes transcription termination by RNA polymerase II. Nature 432: 517-522.
26. Kim V, Han J, Siomi M. 2009. Biogenesis of small RNAs in animals. Nat Rev Mol Cell Biol 10: 126-139.
27. Klattenhoff C, Xi H, Li C, Lee S, Xu J, Khurana J, Zhang F, Schultz N, Koppetsch B, Nowosielska A, et al. 2009. The Drosophila HP1 homolog Rhino is required for transposon silencing and piRNA production by dual-strand clusters. Cell 138: 1137-1149.
28. Langmead B, Trapnell C, Pop M, Salzberg SL. 2009. Ultrafast and memory-efficient alignment of short DNA sequences to the human genome. Genome Biol 10: R25.
29. Laskowski RA, Moss DS, Thornton JM. 1993. Main-chain bond lengths and bond angles in protein structures. J Mol Biol 231: 1049-1067.
30. Lau NC, Robine N, Martin R, Chung WJ, Niki Y, Berezikov E, Lai EC. 2009. Abundant primary piRNAs, endo-siRNAs, and microRNAs in a Drosophila ovary cell line. Genome Res 19: 1776-1785.
31. Lemaitre B, Ronsseray S, Coen D. 1993. Maternal repression of the P element promoter in the germline of Drosophilamelanogaster: a model for the P cytotype. Genetics 135: 149-160.
32. Le Thomas A, Rogers AK, Webster A, Marinov GK, Liao SE, Perkins EM, Hur JK, Aravin AA, Toth KF. 2013. Piwi induces piRNA-guided transcriptional silencing and establishment of a repressive chromatin state. Genes Dev 27: 390-399.
33. Li C, Vagin VV, Lee S, Xu J, Ma S, Xi H, Seitz H, Horwich MD, Syrzycka M, Honda BM, et al. 2009. Collapse of germline piRNAs in the absence of Argonaute3 reveals somatic piRNAs in flies. Cell 137: 509-521.
34. Malone CD, Brennecke J, Dus M, Stark A, McCombie WR, Sachidanandam R, Hannon GJ. 2009. Specialized piRNA pathways act in germline and somatic tissues of the Drosophila ovary. Cell 137: 522-535.
35. McCoy AJ. 2007. Solving structures of protein complexes by molecular replacement with Phaser. Acta Crystallogr D Biol Crystallogr 63: 32-41.
36. Megosh H, Cox D, Campbell C, Lin H. 2006. The role of PIWI and the miRNA machinery in Drosophila germline determination. Curr Biol 16: 1884-1894.
37. Mortazavi A, Williams BA, McCue K, Schaeffer L, Wold B. 2008. Mapping and quantifying mammalian transcriptomes by RNA-seq. Nat Methods 5: 621-628.
38. Moshkovich N, Lei E. 2010. HP1 recruitment in the absence of argonaute proteins in Drosophila. PLoS Genet 6: e1000880.
39. Muerdter F, Olovnikov I, Molaro A, Rozhkov N, Czech B, Gordon A, Hannon G, Aravin A. 2012. Production of artificial piRNAs in flies and mice. RNA 18: 42-52.
40. Olovnikov IA, Kalmykova AI. 2013. piRNA clusters as a main source of small RNAs in the animal germline. Biochemistry (Mosc) 78: 572-584.
41. Otwinowski Z, Minor W. 1997. Processing of X-ray diffraction data collected in oscillation mode. Methods Enzymol 276: 307-326.
42. Pane A, Jiang P, Zhao DY, Singh M, Schupbach T. 2011. The Cutoff protein regulates piRNA cluster expression and piRNA production in the Drosophila germline. EMBO J 30: 4601-4615.
43. Rangan P, Malone C, Navarro C, Newbold S, Hayes P, Sachidanandam R, Hannon G, Lehmann R. 2011. piRNA production requires heterochromatin formation in Drosophila. Curr Biol 21: 1373-1379.
44. Roche SE, Rio DC. 1998. Trans-silencing by P elements inserted in subtelomeric heterochromatin involves the Drosophila Polycomb group gene, Enhancer of zeste. Genetics 149: 1839-1855.
45. Ronsseray S, Boivin A, Anxolabehere D. 2001. P-element repression in Drosophila melanogaster by variegating clusters of P-lacZ-white transgenes. Genetics 159: 1631-1642.
46. Ronsseray S, Josse T, Boivin A, Anxolabehere D. 2003. Telomeric transgenes and trans-silencing in Drosophila. Genetica 117: 327-335.
47. Rozhkov N, Hammell M, Hannon G. 2013. Multiple roles for Piwi in silencing Drosophila transposons. Genes Dev 27: 400-412.
48. Sanchez P, Daniels KJ, Park YN, Soll DR. 2014. Generating a battery of monoclonal antibodies against native green fluorescent protein for immunostaining, FACS, IP, and ChIP using a unique adjuvant. Monoclon Antib Immunodiagn Immunother 33: 80-88.
49. Shpiz S, Olovnikov I, Sergeeva A, Lavrov S, Abramov Y, Savitsky M, Kalmykova A. 2011. Mechanism of the piRNA-mediated silencing of Drosophila telomeric retrotransposons. Nucleic Acids Res 39: 8703-8711.
50. Shpiz S, Ryazansky S, Olovnikov I, Abramov Y, Kalmykova A. 2014. Euchromatic transposon insertions trigger production of novel Pi- and endo-siRNAs at the target sites in the Drosophila germline. PLoS Genet 10: e1004138.
51. Sienski G, Dönertas D, Brennecke J. 2012. Transcriptional silencing of transposons by piwi and maelstrom and its impact on chromatin state and gene expression. Cell 151: 964-980.
52. Siomi MC, Sato K, Pezic D, Aravin AA. 2011. PIWI-interacting small RNAs: the vanguard of genome defence. Nat Rev Mol Cell Biol 12: 246-258.
53. Todeschini A-LL, Teysset L, Delmarre V, Ronsseray S. 2010. The epigenetic trans-silencing effect in Drosophila involves maternally- transmitted small RNAs whose production depends on the piRNA pathway and HP1. PLoS ONE 5: e11032.
54. Wang S, Elgin S. 2011. Drosophila Piwi functions downstream of piRNA production mediating a chromatin-based transposon silencing mechanism in female germ line. Proc Natl Acad Sci 108: 21164-21169.
55. Xue Y, Bai X, Lee I, Kallstrom G, Ho J, Brown J, Stevens A, Johnson AW. 2000. Saccharomyces cerevisiae RAI1 (YGL246c) is homologous to human DOM3Z and encodes a protein that binds the nuclear exoribonuclease Rat1p. Mol Cell Biol 20: 4006-4015.
56. Zhang F, Wang J, Xu J, Zhang Z, Koppetsch B, Schultz N, Vreven T, Meignin C, Davis I, Zamore P, et al. 2012. UAP56 couples piRNA clusters to the perinuclear transposon silencing machinery. Cell 151: 871-884.
57. Zofall M, Grewal SI. 2006. Swi6/HP1 recruits a JmjC domain protein to facilitate transcription of heterochromatic repeats. Mol Cell 22: 681-692.