Distinct Functions of Argonaute Slicer in siRNA Maturation and Heterochromatin Formation

Molecular Cell

Volumn 63, Issue 2, 2016, Pages 191-205

  Jain, Ruchi ^a   Iglesias, Nahid ^a   Moazed, Danesh ^a  

^a HOWARD HUGHES MEDICAL INSTITUTE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ARGONAUTE 1 PROTEIN; ARGONAUTE PROTEIN; DICER; SINGLE STRANDED RNA; SMALL INTERFERING RNA; ADENOSINE TRIPHOSPHATASE; AGO1 PROTEIN, S POMBE; DCR1 PROTEIN, S POMBE; FUNGAL RNA; HETEROCHROMATIN; HISTONE; RDP1 PROTEIN, S POMBE; RIBONUCLEASE; SCHIZOSACCHAROMYCES POMBE PROTEIN; URA4 PROTEIN, S POMBE;

ANIMAL CELL; ARTICLE; BINDING SITE; CHROMATIN IMMUNOPRECIPITATION; CHROMATIN STRUCTURE; FISSION YEAST; GENE MUTATION; GENE SILENCING; GENE TARGETING; HETEROCHROMATIN; MINICHROMOSOME; NONHUMAN; NORTHERN BLOTTING; NUCLEOTIDE SEQUENCE; PLASMID; PROTEIN FUNCTION; PROTEIN METHYLATION; RNA ANALYSIS; RNA CLEAVAGE; RNA ISOLATION; RNA METHYLATION; RNA SYNTHESIS; SIGNAL TRANSDUCTION; BIOSYNTHESIS; CHROMATIN ASSEMBLY AND DISASSEMBLY; DNA METHYLATION; ENZYMOLOGY; GENE EXPRESSION REGULATION; GENETIC TRANSCRIPTION; GENETICS; METABOLISM; RNA INTERFERENCE; SCHIZOSACCHAROMYCES;

ADENOSINE TRIPHOSPHATASES; ARGONAUTE PROTEINS; CHROMATIN ASSEMBLY AND DISASSEMBLY; DNA METHYLATION; ENDORIBONUCLEASES; GENE EXPRESSION REGULATION, FUNGAL; HETEROCHROMATIN; HISTONES; RNA INTERFERENCE; RNA, FUNGAL; RNA, SMALL INTERFERING; SCHIZOSACCHAROMYCES; SCHIZOSACCHAROMYCES POMBE PROTEINS; TRANSCRIPTION, GENETIC;

EID: 84991106796     PISSN: 10972765     EISSN: 10974164     Source Type: Journal    
DOI: 10.1016/j.molcel.2016.05.039     Document Type: Article

References (71)

1. Aravin, A.A., Hannon, G.J., Brennecke, J., The Piwi-piRNA pathway provides an adaptive defense in the transposon arms race. Science 318 (2007), 761–764.
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. Bartel, D.P., MicroRNAs: genomics, biogenesis, mechanism, and function. Cell 116 (2004), 281–297.
4. Bartel, D.P., MicroRNAs: target recognition and regulatory functions. Cell 136 (2009), 215–233.
5. Baum, M., Ngan, V.K., Clarke, L., The centromeric K-type repeat and the central core are together sufficient to establish a functional Schizosaccharomyces pombe centromere. Mol. Biol. Cell 5 (1994), 747–761.
6. Bayne, E.H., White, S.A., Kagansky, A., Bijos, D.A., Sanchez-Pulido, L., Hoe, K.L., Kim, D.U., Park, H.O., Ponting, C.P., Rappsilber, J., Allshire, R.C., Stc1: a critical link between RNAi and chromatin modification required for heterochromatin integrity. Cell 140 (2010), 666–677.
7. Braun, J.E., Huntzinger, E., Izaurralde, E., The role of GW182 proteins in miRNA-mediated gene silencing. Adv. Exp. Med. Biol. 768 (2013), 147–163.
8. 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.
9. Buckley, B.A., Burkhart, K.B., Gu, S.G., Spracklin, G., Kershner, A., Fritz, H., Kimble, J., Fire, A., Kennedy, S., A nuclear Argonaute promotes multigenerational epigenetic inheritance and germline immortality. Nature 489 (2012), 447–451.
10. Bühler, M., Verdel, A., Moazed, D., Tethering RITS to a nascent transcript initiates RNAi- and heterochromatin-dependent gene silencing. Cell 125 (2006), 873–886.
11. Buker, S.M., Iida, T., Bühler, M., Villén, J., Gygi, S.P., Nakayama, J., Moazed, D., Two different Argonaute complexes are required for siRNA generation and heterochromatin assembly in fission yeast. Nat. Struct. Mol. Biol. 14 (2007), 200–207.
12. Buscaino, A., Lejeune, E., Audergon, P., Hamilton, G., Pidoux, A., Allshire, R.C., Distinct roles for Sir2 and RNAi in centromeric heterochromatin nucleation, spreading and maintenance. EMBO J. 32 (2013), 1250–1264.
13. Castel, S.E., Martienssen, R.A., RNA interference in the nucleus: roles for small RNAs in transcription, epigenetics and beyond. Nat. Rev. Genet. 14 (2013), 100–112.
14. Chekulaeva, M., Mathys, H., Zipprich, J.T., Attig, J., Colic, M., Parker, R., Filipowicz, W., miRNA repression involves GW182-mediated recruitment of CCR4-NOT through conserved W-containing motifs. Nat. Struct. Mol. Biol. 18 (2011), 1218–1226.
15. Chen, Q., Yan, M., Cao, Z., Li, X., Zhang, Y., Shi, J., Feng, G.H., Peng, H., Zhang, X., Zhang, Y., et al. Sperm tsRNAs contribute to intergenerational inheritance of an acquired metabolic disorder. Science 351 (2016), 397–400.
16. Colmenares, S.U., Buker, S.M., Buhler, M., Dlakić, M., Moazed, D., Coupling of double-stranded RNA synthesis and siRNA generation in fission yeast RNAi. Mol. Cell 27 (2007), 449–461.
17. Darricarrère, N., Liu, N., Watanabe, T., Lin, H., Function of Piwi, a nuclear Piwi/Argonaute protein, is independent of its slicer activity. Proc. Natl. Acad. Sci. USA 110 (2013), 1297–1302.
18. De Fazio, S., Bartonicek, N., Di Giacomo, M., Abreu-Goodger, C., Sankar, A., Funaya, C., Antony, C., Moreira, P.N., Enright, A.J., O'Carroll, D., The endonuclease activity of Mili fuels piRNA amplification that silences LINE1 elements. Nature 480 (2011), 259–263.
19. Gerace, E.L., Halic, M., Moazed, D., The methyltransferase activity of Clr4Suv39h triggers RNAi independently of histone H3K9 methylation. Mol. Cell 39 (2010), 360–372.
20. Ghildiyal, M., Zamore, P.D., Small silencing RNAs: an expanding universe. Nat. Rev. Genet. 10 (2009), 94–108.
21. Gu, S.G., Pak, J., Guang, S., Maniar, J.M., Kennedy, S., Fire, A., Amplification of siRNA in Caenorhabditis elegans generates a transgenerational sequence-targeted histone H3 lysine 9 methylation footprint. Nat. Genet. 44 (2012), 157–164.
22. Guang, S., Bochner, A.F., Burkhart, K.B., Burton, N., Pavelec, D.M., Kennedy, S., Small regulatory RNAs inhibit RNA polymerase II during the elongation phase of transcription. Nature 465 (2010), 1097–1101.
23. 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.
24. Halic, M., Moazed, D., Dicer-independent primal RNAs trigger RNAi and heterochromatin formation. Cell 140 (2010), 504–516.
25. Hammond, S.M., Boettcher, S., Caudy, A.A., Kobayashi, R., Hannon, G.J., Argonaute2, a link between genetic and biochemical analyses of RNAi. Science 293 (2001), 1146–1150.
26. Holoch, D., Moazed, D., RNA-mediated epigenetic regulation of gene expression. Nat. Rev. Genet. 16 (2015), 71–84.
27. Holoch, D., Moazed, D., Small-RNA loading licenses Argonaute for assembly into a transcriptional silencing complex. Nat. Struct. Mol. Biol. 22 (2015), 328–335.
28. Hong, E.J., Villén, J., Gerace, E.L., Gygi, S.P., Moazed, D., A cullin E3 ubiquitin ligase complex associates with Rik1 and the Clr4 histone H3-K9 methyltransferase and is required for RNAi-mediated heterochromatin formation. RNA Biol. 2 (2005), 106–111.
29. Horn, P.J., Bastie, J.N., Peterson, C.L., A Rik1-associated, cullin-dependent E3 ubiquitin ligase is essential for heterochromatin formation. Genes Dev. 19 (2005), 1705–1714.
30. Huntzinger, E., Izaurralde, E., Gene silencing by microRNAs: contributions of translational repression and mRNA decay. Nat. Rev. Genet. 12 (2011), 99–110.
31. Hutvágner, G., Zamore, P.D., RNAi: nature abhors a double-strand. Curr. Opin. Genet. Dev. 12 (2002), 225–232.
32. Irvine, D.V., Zaratiegui, M., Tolia, N.H., Goto, D.B., Chitwood, D.H., Vaughn, M.W., Joshua-Tor, L., Martienssen, R.A., Argonaute slicing is required for heterochromatic silencing and spreading. Science 313 (2006), 1134–1137.
33. Jia, S., Kobayashi, R., Grewal, S.I., Ubiquitin ligase component Cul4 associates with Clr4 histone methyltransferase to assemble heterochromatin. Nat. Cell Biol. 7 (2005), 1007–1013.
34. Kawamata, T., Seitz, H., Tomari, Y., Structural determinants of miRNAs for RISC loading and slicer-independent unwinding. Nat. Struct. Mol. Biol. 16 (2009), 953–960.
35. Kowalik, K.M., Shimada, Y., Flury, V., Stadler, M.B., Batki, J., Bühler, M., The Paf1 complex represses small-RNA-mediated epigenetic gene silencing. Nature 520 (2015), 248–252.
36. Kumar, P., Anaya, J., Mudunuri, S.B., Dutta, A., Meta-analysis of tRNA derived RNA fragments reveals that they are evolutionarily conserved and associate with AGO proteins to recognize specific RNA targets. BMC Biol., 12, 2014, 78.
37. Lee, M., Kim, B., Kim, V.N., Emerging roles of RNA modification: m(6)A and U-tail. Cell 158 (2014), 980–987.
38. Lejeune, E., Allshire, R.C., Common ground: small RNA programming and chromatin modifications. Curr. Opin. Cell Biol. 23 (2011), 258–265.
39. Leuschner, P.J., Ameres, S.L., Kueng, S., Martinez, J., Cleavage of the siRNA passenger strand during RISC assembly in human cells. EMBO Rep. 7 (2006), 314–320.
40. Liu, J., Carmell, M.A., Rivas, F.V., Marsden, C.G., Thomson, J.M., Song, J.J., Hammond, S.M., Joshua-Tor, L., Hannon, G.J., Argonaute2 is the catalytic engine of mammalian RNAi. Science 305 (2004), 1437–1441.
41. Liu, J., Rivas, F.V., Wohlschlegel, J., Yates, J.R. 3rd, Parker, R., Hannon, G.J., A role for the P-body component GW182 in microRNA function. Nat. Cell Biol. 7 (2005), 1261–1266.
42. Ma, J.B., Ye, K., Patel, D.J., Structural basis for overhang-specific small interfering RNA recognition by the PAZ domain. Nature 429 (2004), 318–322.
43. Ma, J.B., Yuan, Y.R., Meister, G., Pei, Y., Tuschl, T., Patel, D.J., Structural basis for 5′-end-specific recognition of guide RNA by the A. fulgidus Piwi protein. Nature 434 (2005), 666–670.
44. Makeyev, E.V., Bamford, D.H., Cellular RNA-dependent RNA polymerase involved in posttranscriptional gene silencing has two distinct activity modes. Mol. Cell 10 (2002), 1417–1427.
45. Malone, C.D., Hannon, G.J., Small RNAs as guardians of the genome. Cell 136 (2009), 656–668.
46. Martienssen, R.A., Maintenance of heterochromatin by RNA interference of tandem repeats. Nat. Genet. 35 (2003), 213–214.
47. Matranga, C., Tomari, Y., Shin, C., Bartel, D.P., Zamore, P.D., Passenger-strand cleavage facilitates assembly of siRNA into Ago2-containing RNAi enzyme complexes. Cell 123 (2005), 607–620.
48. Meister, G., Landthaler, M., Peters, L., Chen, P.Y., Urlaub, H., Lührmann, R., Tuschl, T., Identification of novel argonaute-associated proteins. Curr. Biol. 15 (2005), 2149–2155.
49. Miyoshi, K., Tsukumo, H., Nagami, T., Siomi, H., Siomi, M.C., Slicer function of Drosophila Argonautes and its involvement in RISC formation. Genes Dev. 19 (2005), 2837–2848.
50. Motamedi, M.R., Verdel, A., Colmenares, S.U., Gerber, S.A., Gygi, S.P., Moazed, D., Two RNAi complexes, RITS and RDRC, physically interact and localize to noncoding centromeric RNAs. Cell 119 (2004), 789–802.
51. 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.
52. Pak, J., Maniar, J.M., Mello, C.C., Fire, A., Protection from feed-forward amplification in an amplified RNAi mechanism. Cell 151 (2012), 885–899.
53. Partridge, J.F., Scott, K.S., Bannister, A.J., Kouzarides, T., Allshire, R.C., cis-acting DNA from fission yeast centromeres mediates histone H3 methylation and recruitment of silencing factors and cohesin to an ectopic site. Curr. Biol. 12 (2002), 1652–1660.
54. Provost, P., Silverstein, R.A., Dishart, D., Walfridsson, J., Djupedal, I., Kniola, B., Wright, A., Samuelsson, B., Radmark, O., Ekwall, K., Dicer is required for chromosome segregation and gene silencing in fission yeast cells. Proc. Natl. Acad. Sci. USA 99 (2002), 16648–16653.
55. Rand, T.A., Petersen, S., Du, F., Wang, X., Argonaute2 cleaves the anti-guide strand of siRNA during RISC activation. Cell 123 (2005), 621–629.
56. 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.
57. Rehwinkel, J., Behm-Ansmant, I., Gatfield, D., Izaurralde, E., A crucial role for GW182 and the DCP1:DCP2 decapping complex in miRNA-mediated gene silencing. RNA 11 (2005), 1640–1647.
58. Reinhart, B.J., Bartel, D.P., Small RNAs correspond to centromere heterochromatic repeats. Science, 297, 2002, 1831.
59. Reuter, M., Berninger, P., Chuma, S., Shah, H., Hosokawa, M., Funaya, C., Antony, C., Sachidanandam, R., Pillai, R.S., Miwi catalysis is required for piRNA amplification-independent LINE1 transposon silencing. Nature 480 (2011), 264–267.
60. Rivas, F.V., Tolia, N.H., Song, J.J., Aragon, J.P., Liu, J., Hannon, G.J., Joshua-Tor, L., Purified Argonaute2 and an siRNA form recombinant human RISC. Nat. Struct. Mol. Biol. 12 (2005), 340–349.
61. Senti, K.A., Brennecke, J., The piRNA pathway: a fly's perspective on the guardian of the genome. Trends Genet. 26 (2010), 499–509.
62. Sharma, U., Conine, C.C., Shea, J.M., Boskovic, A., Derr, A.G., Bing, X.Y., Belleannee, C., Kucukural, A., Serra, R.W., Sun, F., et al. Biogenesis and function of tRNA fragments during sperm maturation and fertilization in mammals. Science 351 (2016), 391–396.
63. Shirayama, M., Seth, M., Lee, H.C., Gu, W., Ishidate, T., Conte, D. Jr., Mello, C.C., piRNAs initiate an epigenetic memory of nonself RNA in the C. elegans germline. Cell 150 (2012), 65–77.
64. Siomi, M.C., Sato, K., Pezic, D., Aravin, A.A., PIWI-interacting small RNAs: the vanguard of genome defence. Nat. Rev. Mol. Cell Biol. 12 (2011), 246–258.
65. Song, J.J., Smith, S.K., Hannon, G.J., Joshua-Tor, L., Crystal structure of Argonaute and its implications for RISC slicer activity. Science 305 (2004), 1434–1437.
66. Verdel, A., Jia, S., Gerber, S., Sugiyama, T., Gygi, S., Grewal, S.I., Moazed, D., RNAi-mediated targeting of heterochromatin by the RITS complex. Science 303 (2004), 672–676.
67. Volpe, T.A., Kidner, C., Hall, I.M., Teng, G., Grewal, S.I., Martienssen, R.A., Regulation of heterochromatic silencing and histone H3 lysine-9 methylation by RNAi. Science 297 (2002), 1833–1837.
68. Wong, K.H., Jin, Y., Moqtaderi, Z., Multiplex Illumina sequencing using DNA barcoding. Curr. Protoc. Mol. Biol., 7, 2013 Unit 7.11.
69. Yu, R., Jih, G., Iglesias, N., Moazed, D., Determinants of heterochromatic siRNA biogenesis and function. Mol. Cell 53 (2014), 262–276.
70. Zekri, L., Huntzinger, E., Heimstädt, S., Izaurralde, E., The silencing domain of GW182 interacts with PABPC1 to promote translational repression and degradation of microRNA targets and is required for target release. Mol. Cell. Biol. 29 (2009), 6220–6231.
71. Zhang, K., Mosch, K., Fischle, W., Grewal, S.I., Roles of the Clr4 methyltransferase complex in nucleation, spreading and maintenance of heterochromatin. Nat. Struct. Mol. Biol. 15 (2008), 381–388.