Silencio/CG9754 connects the piwi-piRNA complex to the cellular heterochromatin machinery

Genes and Development

Volumn 29, Issue 21, 2015, Pages 2258-2271

  Sienski, Grzegorz ^a,b   Batki, Julia ^a   Senti, Kirsten André ^a   Dönertas, Derya ^a   Tirian, Laszlo ^a   Meixner, Katharina ^a   Brennecke, Julius ^a  

^a ERICH SCHMID INSTITUTE OF MATERIALS SCIENCE   (Austria)

^b WHITEHEAD INSTITUTE FOR BIOMEDICAL RESEARCH   (United States)

Author keywords

H3K9 methylation; Heterochromatin formation; piRNA pathway; Piwi; Transcriptional silencing; Transposon silencing

Indexed keywords

ADAPTOR PROTEIN; ARGONAUTE PROTEIN; CARISOPRODOL; DNA; HISTONE METHYLTRANSFERASE; PIWI INTERACTING RNA; PIWI PROTEIN; RNA; SILENCIO PROTEIN; UNCLASSIFIED DRUG; CG9754 PROTEIN, DROSOPHILA; DROSOPHILA PROTEIN; HETEROCHROMATIN; HISTONE; NUCLEAR PROTEIN; PIWI PROTEIN, DROSOPHILA; PROTEIN BINDING; REPRESSOR PROTEIN; SETDB1 PROTEIN, DROSOPHILA; SMALL INTERFERING RNA; SUPPRESSOR OF VARIEGATION 3-9 PROTEIN, DROSOPHILA; TRANSPOSON;

3' UNTRANSLATED REGION; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; BINDING AFFINITY; CHROMATIN IMMUNOPRECIPITATION; CONFORMATIONAL TRANSITION; CONTROLLED STUDY; DROSOPHILA; FEMALE; GENE SILENCING; GENETIC ANALYSIS; GENETIC ASSOCIATION; GENOTYPE; HETEROCHROMATIN; HISTONE METHYLATION; IMMUNOPRECIPITATION; IN VIVO STUDY; INDEL MUTATION; NONHUMAN; OOCYTE DEVELOPMENT; PRIORITY JOURNAL; PROTEIN PROTEIN INTERACTION; SIGNAL TRANSDUCTION; STEADY STATE; TRANSCRIPTION INITIATION; ANIMAL; DROSOPHILA MELANOGASTER; GENE EXPRESSION REGULATION; GENETICS; INSECT GENOME; METABOLISM; METHYLATION; OVARY; PHYSIOLOGY; TRANSPOSON;

ANIMALS; ARGONAUTE PROTEINS; DNA; DNA TRANSPOSABLE ELEMENTS; DROSOPHILA MELANOGASTER; DROSOPHILA PROTEINS; FEMALE; GENE EXPRESSION REGULATION, DEVELOPMENTAL; GENE SILENCING; GENOME, INSECT; HETEROCHROMATIN; HISTONES; METHYLATION; NUCLEAR PROTEINS; OVARY; PROTEIN BINDING; REPRESSOR PROTEINS; RNA; RNA, SMALL INTERFERING;

EID: 84946722434     PISSN: 08909369     EISSN: 15495477     Source Type: Journal    
DOI: 10.1101/gad.271908.115     Document Type: Article

References (68)

1. Audergon PN, Catania S, Kagansky A, Tong P, Shukla M, Pidoux AL, Allshire RC. 2015. Epigenetics. Restricted epigenetic inheritance of H3K9 methylation. Science 348: 132-135.
2. Aygun O, Mehta S, Grewal SI. 2013. HDAC-mediated suppression of histone turnover promotes epigenetic stability of heterochromatin. Nat Struct Mol Biol 20: 547-554.
3. Ayyanathan K, Lechner MS, Bell P, Maul GG, Schultz DC, Yamada Y, Tanaka K, Torigoe K, Rauscher FJ, III. 2003. Regulated recruitment of HP1 to a euchromatic gene induces mitotically heritable, epigenetic gene silencing: a mammalian cell culture model of gene variegation. Genes Dev 17: 1855-1869.
4. Baron-Benhamou J, Gehring NH, Kulozik AE, Hentze MW. 2004. Using the λN peptide to tether proteins to RNAs. Methods Mol Biol 257: 135-154.
5. Bayne EH, White SA, Kagansky A, Bijos DA, Sanchez-Pulido L, Hoe KL, Kim DU, Park HO, Ponting CP, Rappsilber J, et al. 2010. Stc1: a critical link between RNAi and chromatin modification required for heterochromatin integrity. Cell 140: 666-677.
6. Behm-Ansmant I, Rehwinkel J, Doerks T, Stark A, Bork P, Izaurralde E. 2006. MRNA degradation by miRNAs and GW182 requires both CCR4:NOT deadenylase and DCP1:DCP2 decapping complexes. Genes Dev 20: 1885-1898.
7. Brennecke J, Aravin AA, Stark A, Dus M, Kellis M, Sachidanandam R, Hannon GJ. 2007. Discrete small RNA-generating loci as master regulators of transposon activity in Drosophila. Cell 128: 1089-1103.
8. Brower-Toland B, Riddle NC, Jiang H, Huisinga KL, Elgin SC. 2009. Multiple SET methyltransferases are required to maintain normal heterochromatin domains in the genome of Drosophila melanogaster. Genetics 181: 1303-1319.
9. Buhler M, Verdel A, Moazed D. 2006. Tethering RITS to a nascent transcript initiates RNAi-and heterochromatin-dependent gene silencing. Cell 125: 873-886.
10. Bulut-Karslioglu A, De La Rosa-Velazquez IA, Ramirez F, Barenboim M, Onishi-Seebacher M, Arand J, Galan C, Winter GE, Engist B, Gerle B, et al. 2014. Suv39h-dependent H3K9me3 marks intact retrotransposons and silences LINE elements in mouse embryonic stem cells. Mol Cell 55: 277-290.
11. Castel SE, Martienssen RA. 2013. RNA interference in the nucleus: roles for small RNAs in transcription, epigenetics and beyond. Nat Rev Genet 14: 100-112.
12. Clough E, Moon W, Wang S, Smith K, Hazelrigg T. 2007. Histone methylation is required for oogenesis in Drosophila. Development 134: 157-165.
13. Cox DN, Chao A, Lin H. 2000. piwi encodes a nucleoplasmic factor whose activity modulates the number and division rate of germline stem cells. Development 127: 503-514.
14. Czech B, Preall JB, McGinn J, Hannon GJ. 2013. A transcriptomewide RNAi screen in the Drosophila ovary reveals factors of the germline piRNA pathway. Mol Cell 50: 749-761.
15. Czermin B, Schotta G, Hulsmann BB, Brehm A, Becker PB, Reuter G, Imhof A. 2001. Physical and functional association of SU(VAR)3-9 andHDAC1inDrosophila.EMBORep 2: 915-919.
16. Donertas D, Sienski G, Brennecke J. 2013. Drosophila Gtsf1 is an essential component of the Piwi-mediated transcriptional silencing complex. Genes Dev 27: 1693-1705.
17. Ellermeier C, Higuchi EC, Phadnis N, Holm L, Geelhood JL, Thon G, Smith GR. 2010. RNAi and heterochromatin repress centromeric meiotic recombination. Proc Natl Acad Sci 107: 8701-8705.
18. Fritsch L, Robin P, Mathieu JR, Souidi M, Hinaux H, Rougeulle C, Harel-Bellan A, Ameyar-Zazoua M, Ait-Si-Ali S. 2010. A subset of the histone H3 lysine 9 methyltransferases Suv39h1, G9a, GLP, and SETDB1 participate in a multimeric complex. Mol Cell 37: 46-56.
19. Gokcezade J, Sienski G, Duchek P. 2014. Efficient CRISPR/Cas9 plasmids for rapid and versatile genome editing in Drosophila. G3 (Bethesda) 4: 2279-2282.
20. Hall IM, Shankaranarayana GD, Noma K, Ayoub N, Cohen A, Grewal SI. 2002. Establishment and maintenance of a heterochromatin domain. Science 297: 2232-2237.
21. Handler D, Meixner K, Pizka M, Lauss K, Schmied C, Gruber FS, Brennecke J. 2013. The Genetic Makeup of the Drosophila piRNA Pathway. Mol Cell 50: 762-777.
22. Hayashi R, Handler D, Ish-Horowicz D, Brennecke J. 2014. The exon junction complex is required for definition and excision of neighboring introns in Drosophila. Genes Dev 28: 1772-1785.
23. Huang XA, Yin H, Sweeney S, Raha D, Snyder M, Lin H. 2013. A major epigenetic programming mechanism guided by piRNAs. Dev Cell 24: 502-516.
24. Ishida M, Shimojo H, Hayashi A, Kawaguchi R, Ohtani Y, Uegaki K, Nishimura Y, Nakayama J. 2012. Intrinsic nucleic acidbinding activity of Chp1 chromodomain is required for heterochromatic gene silencing. Mol Cell 47: 228-241.
25. Jayaprakash AD, Jabado O, Brown BD, Sachidanandam R. 2011. Identification and remediation of biases in the activity of RNA ligases in small-RNA deep sequencing. Nucleic Acids Res 39: e141.
26. Jinek M, Chylinski K, Fonfara I, Hauer M, Doudna JA, Charpentier E. 2012.Aprogrammable dual-RNA-guidedDNAendonuclease in adaptive bacterial immunity. Science 337: 816-821.
27. Jonas S, Izaurralde E. 2015. Towards a molecular understanding of microRNA-mediated gene silencing. Nat Rev Genet 16: 421-433.
28. Kato Y, Kato M, Tachibana M, Shinkai Y, Yamaguchi M. 2008. Characterization of Drosophila G9a in vivo and identification of genetic interactants. Genes Cells 13: 703-722.
29. Kowalik KM, Shimada Y, Flury V, Stadler MB, Batki J, Buhler M. 2015. The Paf1 complex represses small-RNA-mediated epigenetic gene silencing. Nature 520: 248-252.
30. Lachner M, O’Carroll D, Rea S, Mechtler K, Jenuwein T. 2001. Methylation of histone H3 lysine 9 creates a binding site for HP1 proteins. Nature 410: 116-120.
31. Lee TI, Johnstone SE, Young RA. 2006. Chromatin immunoprecipitation and microarray-based analysis of protein location. Nat Protoc 1: 729-748.
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 Y, Danzer JR, Alvarez P, Belmont AS, Wallrath LL. 2003. Effects of tethering HP1 to euchromatic regions of the Drosophila genome. Development 130: 1817-1824.
34. Markstein M, Pitsouli C, Villalta C, Celniker SE, Perrimon N. 2008. Exploiting position effects and the gypsy retrovirus insulator to engineer precisely expressed transgenes. Nat Genet 40: 476-483.
35. Matsui T, Leung D, Miyashita H, Maksakova IA, Miyachi H, Kimura H, Tachibana M, Lorincz MC, Shinkai Y. 2010. Proviral silencing in embryonic stem cells requires the histone methyltransferase ESET. Nature 464: 927-931.
36. Mohn F, Sienski G, Handler D, Brennecke J. 2014. The rhino-deadlock-cutoff complex licenses noncanonical transcription of dual-strand piRNA clusters in Drosophila. Cell 157: 1364-1379.
37. Muerdter F, Guzzardo PM, Gillis J, Luo Y, Yu Y, Chen C, Fekete R, Hannon GJ. 2013. A genome-wide RNAi screen draws a genetic framework for transposon control and primary piRNA biogenesis in Drosophila. Mol Cell 50: 736-748.
38. Nakayama J, Rice JC, Strahl BD, Allis CD, Grewal SI. 2001. Role of histone H3 lysine 9 methylation in epigenetic control of heterochromatin assembly. Science 292: 110-113.
39. Ni JQ, Liu LP, Binari R, Hardy R, Shim HS, Cavallaro A, Booker M, Pfeiffer BD, Markstein M, Wang H, et al. 2009. A Drosophila resource of transgenic RNAi lines for neurogenetics. Genetics 182: 1089-1100.
40. Niki Y, Yamaguchi T, Mahowald AP. 2006. Establishment of stable cell lines of Drosophila germ-line stem cells. Proc Natl Acad Sci 103: 16325-16330.
41. Noma K, Sugiyama T, Cam H, Verdel A, Zofall M, Jia S, Moazed D, Grewal SI. 2004. RITS acts in cis to promote RNA interference-mediated transcriptional and post-transcriptional silencing. Nat Genet 36: 1174-1180.
42. Ohtani H, Iwasaki YW, Shibuya A, Siomi H, Siomi MC, Saito K. 2013. DmGTSF1 is necessary for Piwi-piRISC-mediated transcriptional transposon silencing in the Drosophila ovary. Genes Dev 27: 1656-1661.
43. Olivieri D, Senti KA, Subramanian S, Sachidanandam R, Brennecke J. 2012. The cochaperone shutdown defines a group of biogenesis factors essential for all piRNA populations in Drosophila. Mol Cell 47: 954-969.
44. Pezic D, Manakov SA, Sachidanandam R, Aravin AA. 2014. piRNApathway targets active LINE1 elements to establish the repressive H3K9me3 mark in germ cells. Genes Dev 28: 1410-1428.
45. Post C, Clark JP, Sytnikova YA, Chirn GW, Lau NC. 2014. The capacity of target silencing by Drosophila PIWI and piRNAs. RNA 20: 1977-1986.
46. Ragunathan K, Jih G, Moazed D. 2015. Epigenetics. Epigenetic inheritance uncoupled from sequence-specific recruitment. Science 348: 1258699.
47. Rangan P, Malone CD, Navarro C, Newbold SP, Hayes PS, Sachidanandam R, Hannon GJ, Lehmann R. 2011. piRNA production requires heterochromatin formation in Drosophila. Curr Biol 21: 1373-1379.
48. Rea S, Eisenhaber F, O’Carroll D, Strahl BD, Sun ZW, Schmid M, Opravil S, Mechtler K, Ponting CP, Allis CD, et al. 2000. Regulation of chromatin structure by site-specific histone H3 methyltransferases. Nature 406: 593-599.
49. Robine N, Lau NC, Balla S, Jin Z, Okamura K, Kuramochi-Miyagawa S, Blower MD, Lai EC. 2009. A broadly conserved pathway generates 3’UTR-directed primary piRNAs. Curr Biol 19: 2066-2076.
50. Rowe HM, Jakobsson J, Mesnard D, Rougemont J, Reynard S, Aktas T, Maillard PV, Layard-Liesching H, Verp S, Marquis J, et al. 2010. KAP1 controls endogenous retroviruses in embryonic stem cells. Nature 463: 237-240.
51. Rozhkov NV, Hammell M, Hannon GJ. 2013. Multiple roles for Piwi in silencing Drosophila transposons. Genes Dev 27: 400-412.
52. Saito K, Inagaki S, Mituyama T, Kawamura Y, Ono Y, Sakota E, Kotani H, Asai K, Siomi H, Siomi MC. 2009. A regulatory circuit for piwi by the large Maf gene traffic jam in Drosophila. Nature 461: 1296-1299.
53. Saito K, Ishizu H, Komai M, Kotani H, Kawamura Y, Nishida KM, Siomi H, Siomi MC. 2010. Roles for the Yb body components Armitage and Yb in primary piRNA biogenesis in Drosophila. Genes Dev 24: 2493-2498.
54. Sarot E, Payen-Groschene G, Bucheton A, Pelisson A. 2004. Evidence for a piwi-dependent RNA silencing of the gypsy endogenous retrovirus by the Drosophila melanogaster flamenco gene. Genetics 166: 1313-1321.
55. Schotta G, Ebert A, Krauss V, Fischer A, Hoffmann J, Rea S, Jenuwein T, Dorn R, Reuter G. 2002. Central role of Drosophila SU (VAR)3-9 in histone H3-K9 methylation and heterochromatic gene silencing. EMBO J 21: 1121-1131.
56. Senti KA, Jurczak D, Sachidanandam R, Brennecke J. 2015. piRNA-guided slicing of transposon transcripts enforces their transcriptional silencing via specifying the nuclear piRNA repertoire. Genes Dev 29: 1747-1762.
57. Sienski G, Donertas 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.
58. Stabell M, Eskeland R, Bjorkmo M, Larsson J, Aalen RB, Imhof A, Lambertsson A. 2006.
59. The Drosophila G9a gene encodes a multi-catalytic histone methyltransferase required for normal development. Nucleic Acids Res 34: 4609-4621.
60. Sugiyama T, Cam HP, Sugiyama R, Noma K, Zofall M, Kobayashi R, Grewal SI. 2007. SHREC, an effector complex for heterochromatic transcriptional silencing. Cell 128: 491-504.
61. Sun FL, Cuaycong MH, Elgin SC. 2001. Long-range nucleosome ordering is associated with gene silencing in Drosophila melanogaster pericentric heterochromatin. Mol Cell Biol 21: 2867-2879.
62. Towbin BD, Gonzalez-Aguilera C, Sack R, Gaidatzis D, Kalck V, Meister P, Askjaer P, Gasser SM. 2012. Step-wise methylation of histone H3K9 positions heterochromatin at the nuclear periphery. Cell 150: 934-947.
63. Tschiersch B, Hofmann A, Krauss V, Dorn R, Korge G, Reuter G. 1994. The protein encoded by the Drosophila position-effect variegation suppressor gene Su(var)3-9 combines domains of antagonistic regulators of homeotic gene complexes. EMBO J 13: 3822-3831.
64. Verdel A, Jia S, Gerber S, Sugiyama T, Gygi S, Grewal SI, Moazed D. 2004. RNAi-mediated targeting of heterochromatin by the RITS complex. Science 303: 672-676.
65. Volpe TA, Kidner C, Hall IM, Teng G, Grewal SI, Martienssen RA. 2002. Regulation of heterochromatic silencing and histone H3 lysine-9 methylation by RNAi. Science 297: 1833-1837.
66. Wang SH, Elgin SC. 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.
67. Yamada T, Fischle W, Sugiyama T, Allis CD, Grewal SI. 2005. The nucleation and maintenance of heterochromatin by a histone deacetylase in fission yeast. Mol Cell 20: 173-185.
68. Yu Y, Gu J, Jin Y, Luo Y, Preall JB, Ma J, Czech B, Hannon GJ. 2015. Panoramix enforces piRNA-dependent cotranscriptional silencing. Science 350: 339-342.