Piwi Modulates Chromatin Accessibility by Regulating Multiple Factors Including Histone H1 to Repress Transposons

Molecular Cell

Volumn 63, Issue 3, 2016, Pages 408-419

  Iwasaki, Yuka W ^a   Murano, Kensaku ^a   Ishizu, Hirotsugu ^b   Shibuya, Aoi ^a   Iyoda, Yumiko ^a   Siomi, Mikiko C ^b   Siomi, Haruhiko ^a   Saito, Kuniaki ^a  

^a KEIO UNIVERSITY SCHOOL OF MEDICINE   (Japan)

^b UNIVERSITY OF TOKYO   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

DEOXYRIBONUCLEASE; GLUTATHIONE TRANSFERASE; HISTONE H1; HISTONE H2A; HISTONE H3; PIWI INTERACTING RNA; RIBONUCLEASE; ARGONAUTE PROTEIN; DROSOPHILA PROTEIN; HETEROCHROMATIN-SPECIFIC NONHISTONE CHROMOSOMAL PROTEIN HP-1; HISTONE; NONHISTONE PROTEIN; PIWI PROTEIN, DROSOPHILA; SMALL INTERFERING RNA; TRANSPOSON;

ANIMAL CELL; ARTICLE; CARBOXY TERMINAL SEQUENCE; CELL DENSITY; CHROMATIN; CONTROLLED STUDY; DROSOPHILA; FEMALE; GENE REPRESSION; IN VITRO STUDY; LONG TERMINAL REPEAT; NONHUMAN; POLYACRYLAMIDE GEL ELECTROPHORESIS; PROMOTER REGION; PROTEIN DEPLETION; PROTEIN EXPRESSION; PROTEIN LOCALIZATION; PROTEIN PROTEIN INTERACTION; RNA SEQUENCE; TRANSPOSON; UPREGULATION; ANIMAL; CELL CULTURE; CHROMATIN ASSEMBLY AND DISASSEMBLY; CYTOLOGY; DNA METHYLATION; DROSOPHILA MELANOGASTER; EPIGENETIC REPRESSION; GENETIC TRANSFECTION; GENETICS; METABOLISM; OVARY; RNA INTERFERENCE;

ANIMALS; ARGONAUTE PROTEINS; CELLS, CULTURED; CHROMATIN ASSEMBLY AND DISASSEMBLY; CHROMOSOMAL PROTEINS, NON-HISTONE; DNA METHYLATION; DNA TRANSPOSABLE ELEMENTS; DROSOPHILA MELANOGASTER; DROSOPHILA PROTEINS; EPIGENETIC REPRESSION; FEMALE; HISTONES; OVARY; RNA INTERFERENCE; RNA, SMALL INTERFERING; TRANSFECTION;

EID: 84978823301     PISSN: 10972765     EISSN: 10974164     Source Type: Journal    
DOI: 10.1016/j.molcel.2016.06.008     Document Type: Article

References (50)

1. Aygün, O., Mehta, S., Grewal, S.I., HDAC-mediated suppression of histone turnover promotes epigenetic stability of heterochromatin. Nat. Struct. Mol. Biol. 20 (2013), 547–554.
2. 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 410 (2001), 120–124.
3. Bonet-Costa, C., Vilaseca, M., Diema, C., Vujatovic, O., Vaquero, A., Omeñaca, N., Castejón, L., Bernués, J., Giralt, E., Azorín, F., Combined bottom-up and top-down mass spectrometry analyses of the pattern of post-translational modifications of Drosophila melanogaster linker histone H1. J. Proteomics 75 (2012), 4124–4138.
4. Braunschweig, U., Hogan, G.J., Pagie, L., van Steensel, B., Histone H1 binding is inhibited by histone variant H3.3. EMBO J. 28 (2009), 3635–3645.
5. 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 128 (2007), 1089–1103.
6. 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. 21 (2007), 2300–2311.
7. Buenrostro, J.D., Giresi, P.G., Zaba, L.C., Chang, H.Y., Greenleaf, W.J., Transposition of native chromatin for fast and sensitive epigenomic profiling of open chromatin, DNA-binding proteins and nucleosome position. Nat. Methods 10 (2013), 1213–1218.
8. Buenrostro, J.D., Wu, B., Chang, H.Y., Greenleaf, W.J., ATAC-seq: a method for assaying chromatin accessibility genome-wide. Curr. Protoc. Mol. Biol. 109 (2015), 21–29.
9. Bustin, M., Catez, F., Lim, J.H., The dynamics of histone H1 function in chromatin. Mol. Cell 17 (2005), 617–620.
10. Buttinelli, M., Panetta, G., Rhodes, D., Travers, A., The role of histone H1 in chromatin condensation and transcriptional repression. Genetica 106 (1999), 117–124.
11. 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 127 (2000), 503–514.
12. Czech, B., Preall, J.B., McGinn, J., Hannon, G.J., A transcriptome-wide RNAi screen in the Drosophila ovary reveals factors of the germline piRNA pathway. Mol. Cell 50 (2013), 749–761.
13. Dönertas, D., Sienski, G., Brennecke, J., Drosophila Gtsf1 is an essential component of the Piwi-mediated transcriptional silencing complex. Genes Dev. 27 (2013), 1693–1705.
14. Eissenberg, J.C., James, T.C., Foster-Hartnett, D.M., Hartnett, T., Ngan, V., Elgin, S.C.R., Mutation in a heterochromatin-specific chromosomal protein is associated with suppression of position-effect variegation in Drosophila melanogaster. Proc. Natl. Acad. Sci. USA 87 (1990), 9923–9927.
15. Ge, D.T., Zamore, P.D., Small RNA-directed silencing: the fly finds its inner fission yeast?. Curr. Biol. 23 (2013), R318–R320.
16. Goodier, J.L., Kazazian, H.H. Jr., Retrotransposons revisited: the restraint and rehabilitation of parasites. Cell 135 (2008), 23–35.
17. Grewal, S.I., Jia, S., Heterochromatin revisited. Nat. Rev. Genet. 8 (2007), 35–46.
18. 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 315 (2007), 1587–1590.
19. Hale, T.K., Contreras, A., Morrison, A.J., Herrera, R.E., Phosphorylation of the linker histone H1 by CDK regulates its binding to HP1alpha. Mol. Cell 22 (2006), 693–699.
20. Handler, D., Meixner, K., Pizka, M., Lauss, K., Schmied, C., Gruber, F.S., Brennecke, J., The genetic makeup of the Drosophila piRNA pathway. Mol. Cell 50 (2013), 762–777.
21. Ishizu, H., Iwasaki, Y.W., Hirakata, S., Ozaki, H., Iwasaki, W., Siomi, H., Siomi, M.C., Somatic Primary piRNA Biogenesis Driven by cis-Acting RNA Elements and trans-Acting Yb. Cell Rep. 12 (2015), 429–440.
22. Iwasaki, Y.W., Siomi, M.C., Siomi, H., PIWI-Interacting RNA: Its Biogenesis and Functions. Annu. Rev. Biochem. 84 (2015), 405–433.
23. Jacobs, S.A., Khorasanizadeh, S., Structure of HP1 chromodomain bound to a lysine 9-methylated histone H3 tail. Science 295 (2002), 2080–2083.
24. 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 108 (2011), 18760–18765.
25. Klenov, M.S., Lavrov, S.A., Korbut, A.P., Stolyarenko, A.D., Yakushev, E.Y., Reuter, M., Pillai, R.S., Gvozdev, V.A., Impact of nuclear Piwi elimination on chromatin state in Drosophila melanogaster ovaries. Nucleic Acids Res. 42 (2014), 6208–6218.
26. Lachner, M., O'Carroll, D., Rea, S., Mechtler, K., Jenuwein, T., Methylation of histone H3 lysine 9 creates a binding site for HP1 proteins. Nature 410 (2001), 116–120.
27. Laybourn, P.J., Kadonaga, J.T., Role of nucleosomal cores and histone H1 in regulation of transcription by RNA polymerase II. Science 254 (1991), 238–245.
28. Le Thomas, A., Rogers, A.K., Webster, A., Marinov, G.K., Liao, S.E., Perkins, E.M., Hur, J.K., Aravin, A.A., Tóth, K.F., Piwi induces piRNA-guided transcriptional silencing and establishment of a repressive chromatin state. Genes Dev. 27 (2013), 390–399.
29. Li, G., Reinberg, D., Chromatin higher-order structures and gene regulation. Curr. Opin. Genet. Dev. 21 (2011), 175–186.
30. Lu, X., Wontakal, S.N., Kavi, H., Kim, B.J., Guzzardo, P.M., Emelyanov, A.V., Xu, N., Hannon, G.J., Zavadil, J., Fyodorov, D.V., Skoultchi, A.I., Drosophila H1 regulates the genetic activity of heterochromatin by recruitment of Su(var)3-9. Science 340 (2013), 78–81.
31. Misteli, T., Gunjan, A., Hock, R., Bustin, M., Brown, D.T., Dynamic binding of histone H1 to chromatin in living cells. Nature 408 (2000), 877–881.
32. Muerdter, F., Guzzardo, P.M., Gillis, J., Luo, Y., Yu, Y., Chen, C., Fekete, R., Hannon, G.J., A genome-wide RNAi screen draws a genetic framework for transposon control and primary piRNA biogenesis in Drosophila. Mol. Cell 50 (2013), 736–748.
33. Nakayama, J., Rice, J.C., Strahl, B.D., Allis, C.D., Grewal, S.I., Role of histone H3 lysine 9 methylation in epigenetic control of heterochromatin assembly. Science 292 (2001), 110–113.
34. Nielsen, A.L., Oulad-Abdelghani, M., Ortiz, J.A., Remboutsika, E., Chambon, P., Losson, R., Heterochromatin formation in mammalian cells: interaction between histones and HP1 proteins. Mol. Cell 7 (2001), 729–739.
35. Niki, Y., Yamaguchi, T., Mahowald, A.P., Establishment of stable cell lines of Drosophila germ-line stem cells. Proc. Natl. Acad. Sci. USA 103 (2006), 16325–16330.
36. Ohtani, H., Iwasaki, Y.W., Shibuya, A., Siomi, H., Siomi, M.C., Saito, K., DmGTSF1 is necessary for Piwi-piRISC-mediated transcriptional transposon silencing in the Drosophila ovary. Genes Dev. 27 (2013), 1656–1661.
37. Pennings, S., Meersseman, G., Bradbury, E.M., Linker histones H1 and H5 prevent the mobility of positioned nucleosomes. Proc. Natl. Acad. Sci. USA 91 (1994), 10275–10279.
38. Post, C., Clark, J.P., Sytnikova, Y.A., Chirn, G.W., Lau, N.C., The capacity of target silencing by Drosophila PIWI and piRNAs. RNA 20 (2014), 1977–1986.
39. Rea, S., Eisenhaber, F., O'Carroll, D., Strahl, B.D., Sun, Z.W., Schmid, M., Opravil, S., Mechtler, K., Ponting, C.P., Allis, C.D., Jenuwein, T., Regulation of chromatin structure by site-specific histone H3 methyltransferases. Nature 406 (2000), 593–599.
40. Rozhkov, N.V., Hammell, M., Hannon, G.J., Multiple roles for Piwi in silencing Drosophila transposons. Genes Dev. 27 (2013), 400–412.
41. 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 461 (2009), 1296–1299.
42. 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. 24 (2010), 2493–2498.
43. Schotta, G., Ebert, A., Krauss, V., Fischer, A., Hoffmann, J., Rea, S., Jenuwein, T., Dorn, R., Reuter, G., Central role of Drosophila SU(VAR)3-9 in histone H3-K9 methylation and heterochromatic gene silencing. EMBO J. 21 (2002), 1121–1131.
44. Sienski, G., Dönertas, D., Brennecke, J., Transcriptional silencing of transposons by Piwi and maelstrom and its impact on chromatin state and gene expression. Cell 151 (2012), 964–980.
45. Sienski, G., Batki, J., Senti, K.A., Dönertas, D., Tirian, L., Meixner, K., Brennecke, J., Silencio/CG9754 connects the Piwi-piRNA complex to the cellular heterochromatin machinery. Genes Dev. 29 (2015), 2258–2271.
46. Vujatovic, O., Zaragoza, K., Vaquero, A., Reina, O., Bernués, J., Azorín, F., Drosophila melanogaster linker histone dH1 is required for transposon silencing and to preserve genome integrity. Nucleic Acids Res. 40 (2012), 5402–5414.
47. Wang, S.H., Elgin, S.C., Drosophila Piwi functions downstream of piRNA production mediating a chromatin-based transposon silencing mechanism in female germ line. Proc. Natl. Acad. Sci. USA 108 (2011), 21164–21169.
48. Yu, Y., Gu, J., Jin, Y., Luo, Y., Preall, J.B., Ma, J., Czech, B., Hannon, G.J., Panoramix enforces piRNA-dependent cotranscriptional silencing. Science 350 (2015), 339–342.
49. Zhou, B.R., Feng, H., Kato, H., Dai, L., Yang, Y., Zhou, Y., Bai, Y., Structural insights into the histone H1-nucleosome complex. Proc. Natl. Acad. Sci. USA 110 (2013), 19390–19395.
50. Zhou, B.R., Jiang, J., Feng, H., Ghirlando, R., Xiao, T.S., Bai, Y., Structural mechanisms of nucleosome recognition by linker histones. Mol. Cell 59 (2015), 628–638.