RISC assembly: Coordination between small RNAs and Argonaute proteins

Biochimica et Biophysica Acta - Gene Regulatory Mechanisms

Volumn 1859, Issue 1, 2016, Pages 71-81

  Kobayashi, Hotaka ^a   Tomari, Yukihide ^a  

^a UNIVERSITY OF TOKYO   (Japan)

Author keywords

Argonaute; Chaperone; miRNA; piRNA; RISC; RNA silencing; siRNA; Small RNAs

Indexed keywords

ARGONAUTE PROTEIN; CHAPERONE; MICRORNA; PIWI INTERACTING RNA; RNA INDUCED SILENCING COMPLEX; SMALL INTERFERING RNA; UNTRANSLATED RNA;

BIOGENESIS; CELLULAR DISTRIBUTION; CONFORMATIONAL TRANSITION; GENE SILENCING; HUMAN; NONHUMAN; PRIORITY JOURNAL; PROTEIN ASSEMBLY; PROTEIN RNA BINDING; REVIEW; ANIMAL; CHEMISTRY; CYTOPLASM; GENETICS; RNA INTERFERENCE;

ANIMALS; ARGONAUTE PROTEINS; CYTOPLASM; GENE SILENCING; HUMANS; MICRORNAS; MOLECULAR CHAPERONES; RNA INTERFERENCE; RNA, SMALL INTERFERING; RNA, UNTRANSLATED; RNA-INDUCED SILENCING COMPLEX;

EID: 84953359883     PISSN: 18749399     EISSN: 18764320     Source Type: Journal    
DOI: 10.1016/j.bbagrm.2015.08.007     Document Type: Review

References (204)

1. Carninci P., Kasukawa T., Katayama S., Gough J., Frith M.C., Maeda N., Oyama R., Ravasi T., Lenhard B., Wells C., Kodzius R., Shimokawa K., Bajic V.B., Brenner S.E., Batalov S., Forrest A.R.R., Zavolan M., Davis M.J., Wilming L.G., Aidinis V., et al. The transcriptional landscape of the mammalian genome. Science 2005, 309:1559-1563.
2. Hirose T., Mishima Y., Tomari Y. Elements and machinery of non-coding RNAs: toward their taxonomy. EMBO Rep. 2014, 15:489-507.
3. Peters L., Meister G. Argonaute proteins: mediators of RNA silencing. Mol. Cell 2007, 26:611-623.
4. Hutvagner G., Simard M.J. Argonaute proteins: key players in RNA silencing. Nat. Rev. Mol. Cell Biol. 2008, 9:22-32.
5. Meister G. Argonaute proteins: functional insights and emerging roles. Nat. Rev. Genet. 2013, 14:447-459.
6. Swarts D.C., Makarova K., Wang Y., Nakanishi K., Ketting R.F., Koonin E.V., Patel D.J., van der Oost J. The evolutionary journey of Argonaute proteins. Nat. Struct. Mol. Biol. 2014, 21:743-753.
7. Kim V.N., Han J., Siomi M.C. Biogenesis of small RNAs in animals. Nat. Rev. Mol. Cell Biol. 2009, 10:126-139.
8. Ameres S.L., Zamore P.D. Diversifying microRNA sequence and function. Nat. Rev. Mol. Cell Biol. 2013, 14:475-488.
9. Ha M., Kim V.N. Regulation of microRNA biogenesis. Nat. Rev. Mol. Cell Biol. 2014, 15:509-524.
10. Shenoy A., Blelloch R.H. Regulation of microRNA function in somatic stem cell proliferation and differentiation. Nat. Rev. Mol. Cell Biol. 2014, 15:565-576.
11. Lee R.C., Feinbaum R.L., Ambros V. The C. elegans heterochronic gene lin-4 encodes small RNAs with antisense complementarity to lin-14. Cell 1993, 75:843-854.
12. Kozomara A., Griffiths-Jones S. miRBase: annotating high confidence microRNAs using deep sequencing data. Nucleic Acids Res. 2014, 42:D68-D73.
13. Agarwal V., Bell G.W., Nam J.W., Bartel D.P. Predicting effective microRNA target sites in mammalian mRNAs. Elife 2015, 4:e05005.
14. Lee Y., Jeon K., Lee J.-T., Kim S., Kim V.N. MicroRNA maturation: stepwise processing and subcellular localization. EMBO J. 2002, 21:4663-4670.
15. Lee Y., Kim M., Han J., Yeom K.-H., Lee S., Baek S.H., Kim V.N. MicroRNA genes are transcribed by RNA polymerase II. EMBO J. 2004, 23:4051-4060.
16. Cai X., Hagedorn C.H., Cullen B.R. Human microRNAs are processed from capped, polyadenylated transcripts that can also function as mRNAs. RNA N. Y. N. 2004, 10:1957-1966.
17. Lee Y., Ahn C., Han J., Choi H., Kim J., Yim J., Lee J., Provost P., Rådmark O., Kim S., Kim V.N. The nuclear RNase III Drosha initiates microRNA processing. Nature 2003, 425:415-419.
18. Denli A.M., Tops B.B.J., Plasterk R.H.A., Ketting R.F., Hannon G.J. Processing of primary microRNAs by the Microprocessor complex. Nature 2004, 432:231-235.
19. Gregory R.I., Yan K.-P., Amuthan G., Chendrimada T., Doratotaj B., Cooch N., Shiekhattar R. The Microprocessor complex mediates the genesis of microRNAs. Nature 2004, 432:235-240.
20. Landthaler M., Yalcin A., Tuschl T. The human DiGeorge syndrome critical region gene 8 and its D. melanogaster homolog are required for miRNA biogenesis. Curr. Biol. 2004, 14:2162-2167.
21. Han J., Lee Y., Yeom K.-H., Kim Y.-K., Jin H., Kim V.N. The Drosha-DGCR8 complex in primary microRNA processing. Genes Dev. 2004, 18:3016-3027.
22. Han J., Lee Y., Yeom K.-H., Nam J.-W., Heo I., Rhee J.-K., Sohn S.Y., Cho Y., Zhang B.-T., Kim V.N. Molecular basis for the recognition of primary microRNAs by the Drosha-DGCR8 complex. Cell 2006, 125:887-901.
23. Yi R., Qin Y., Macara I.G., Cullen B.R. Exportin-5 mediates the nuclear export of pre-microRNAs and short hairpin RNAs. Genes Dev. 2003, 17:3011-3016.
24. Lund E., Güttinger S., Calado A., Dahlberg J.E., Kutay U. Nuclear export of microRNA precursors. Science 2004, 303:95-98.
25. Bohnsack M.T., Czaplinski K., Gorlich D. Exportin 5 is a RanGTP-dependent dsRNA-binding protein that mediates nuclear export of pre-miRNAs. RNA N. Y. N. 2004, 10:185-191.
26. Zeng Y., Cullen B.R. Structural requirements for pre-microRNA binding and nuclear export by Exportin 5. Nucleic Acids Res. 2004, 32:4776-4785.
27. Maniataki E., Mourelatos Z. A human, ATP-independent, RISC assembly machine fueled by pre-miRNA. Genes Dev. 2005, 19:2979-2990.
28. Gregory R.I., Chendrimada T.P., Cooch N., Shiekhattar R. Human RISC couples microRNA biogenesis and posttranscriptional gene silencing. Cell 2005, 123:631-640.
29. Haase A.D., Jaskiewicz L., Zhang H., Lainé S., Sack R., Gatignol A., Filipowicz W. TRBP, a regulator of cellular PKR and HIV-1 virus expression, interacts with Dicer and functions in RNA silencing. EMBO Rep. 2005, 6:961-967.
30. Lee Y.S., Nakahara K., Pham J.W., Kim K., He Z., Sontheimer E.J., Carthew R.W. Distinct roles for Drosophila Dicer-1 and Dicer-2 in the siRNA/miRNA silencing pathways. Cell 2004, 117:69-81.
31. Förstemann K., Tomari Y., Du T., Vagin V.V., Denli A.M., Bratu D.P., Klattenhoff C., Theurkauf W.E., Zamore P.D. Normal microRNA maturation and germ-line stem cell maintenance requires Loquacious, a double-stranded RNA-binding domain protein. PLoS Biol. 2005, 3:e236.
32. Saito K., Ishizuka A., Siomi H., Siomi M.C. Processing of pre-microRNAs by the Dicer-1-Loquacious complex in Drosophila cells. PLoS Biol. 2005, 3:e235.
33. Jiang F., Ye X., Liu X., Fincher L., McKearin D., Liu Q. Dicer-1 and R3D1-L catalyze microRNA maturation in Drosophila. Genes Dev. 2005, 19:1674-1679.
34. Ghildiyal M., Zamore P.D. Small silencing RNAs: an expanding universe. Nat. Rev. Genet. 2009, 10:94-108.
35. Okamura K., Lai E.C. Endogenous small interfering RNAs in animals. Nat. Rev. Mol. Cell Biol. 2008, 9:673-678.
36. Fire A., Xu S., Montgomery M.K., Kostas S.A., Driver S.E., Mello C.C. Potent and specific genetic interference by double-stranded RNA in Caenorhabditis elegans. Nature 1998, 391:806-811.
37. Ding S.-W., Voinnet O. Antiviral immunity directed by small RNAs. Cell 2007, 130:413-426.
38. Chung W.-J., Okamura K., Martin R., Lai E.C. Endogenous RNA interference provides a somatic defense against Drosophila transposons. Curr. Biol. 2008, 18:795-802.
39. Czech B., Malone C.D., Zhou R., Stark A., Schlingeheyde C., Dus M., Perrimon N., Kellis M., Wohlschlegel J.A., Sachidanandam R., Hannon G.J., Brennecke J. An endogenous small interfering RNA pathway in Drosophila. Nature 2008, 453:798-802.
40. Ghildiyal M., Seitz H., Horwich M.D., Li C., Du T., Lee S., Xu J., Kittler E.L.W., Zapp M.L., Weng Z., Zamore P.D. Endogenous siRNAs derived from transposons and mRNAs in Drosophila somatic cells. Science 2008, 320:1077-1081.
41. Kawamura Y., Saito K., Kin T., Ono Y., Asai K., Sunohara T., Okada T.N., Siomi M.C., Siomi H. Drosophila endogenous small RNAs bind to Argonaute 2 in somatic cells. Nature 2008, 453:793-797.
42. Li Y., Lu J., Han Y., Fan X., Ding S.-W. RNA interference functions as an antiviral immunity mechanism in mammals. Science 2013, 342:231-234.
43. Maillard P.V., Ciaudo C., Marchais A., Li Y., Jay F., Ding S.W., Voinnet O. Antiviral RNA interference in mammalian cells. Science 2013, 342:235-238.
44. Burgess D.J. Small RNAs: antiviral RNAi in mammals. Nat. Rev. Genet. 2013, 14:821.
45. Kole R., Krainer A.R., Altman S. RNA therapeutics: beyond RNA interference and antisense oligonucleotides. Nat. Rev. Drug Discov. 2012, 11:125-140.
46. Provost P., Dishart D., Doucet J., Frendewey D., Samuelsson B., Rådmark O. Ribonuclease activity and RNA binding of recombinant human Dicer. EMBO J. 2002, 21:5864-5874.
47. Zhang H., Kolb F.A., Brondani V., Billy E., Filipowicz W. Human Dicer preferentially cleaves dsRNAs at their termini without a requirement for ATP. EMBO J. 2002, 21:5875-5885.
48. Pham J.W., Pellino J.L., Lee Y.S., Carthew R.W., Sontheimer E.J. A Dicer-2-dependent 80s complex cleaves targeted mRNAs during RNAi in Drosophila. Cell 2004, 117:83-94.
49. Aravin A.A., Hannon G.J., Brennecke J. The Piwi-piRNA pathway provides an adaptive defense in the transposon arms race. Science 2007, 318:761-764.
50. Malone C.D., Hannon G.J. Small RNAs as guardians of the genome. Cell 2009, 136:656-668.
51. 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.
52. Ross R.J., Weiner M.M., Lin H. PIWI proteins and PIWI-interacting RNAs in the soma. Nature 2014, 505:353-359.
53. Weick E.-M., Miska E.A. piRNAs: from biogenesis to function. Dev. Camb. Engl. 2014, 141:3458-3471.
54. Aravin A.A., Lagos-Quintana M., Yalcin A., Zavolan M., Marks D., Snyder B., Gaasterland T., Meyer J., Tuschl T. The small RNA profile during Drosophila melanogaster development. Dev. Cell 2003, 5:337-350.
55. 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.
56. Li X.Z., Roy C.K., Dong X., Bolcun-Filas E., Wang J., Han B.W., Xu J., Moore M.J., Schimenti J.C., Weng Z., Zamore P.D. An ancient transcription factor initiates the burst of piRNA production during early meiosis in mouse testes. Mol. Cell 2013, 50:67-81.
57. Klattenhoff C., Xi H., Li C., Lee S., Xu J., Khurana J.S., Zhang F., Schultz N., Koppetsch B.S., Nowosielska A., Seitz H., Zamore P.D., Weng Z., Theurkauf W.E. The Drosophila HP1 homolog Rhino is required for transposon silencing and piRNA production by dual-strand clusters. Cell 2009, 138:1137-1149.
58. 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.
59. Zhang Z., Wang J., Schultz N., Zhang F., Parhad S.S., Tu S., Vreven T., Zamore P.D., Weng Z., Theurkauf W.E. The HP1 homolog rhino anchors a nuclear complex that suppresses piRNA precursor splicing. Cell 2014, 157:1353-1363.
60. Mohn F., Sienski G., Handler D., Brennecke J. The rhino-deadlock-cutoff complex licenses noncanonical transcription of dual-strand piRNA clusters in Drosophila. Cell 2014, 157:1364-1379.
61. Zhang F., Wang J., Xu J., Zhang Z., Koppetsch B.S., Schultz N., Vreven T., Meignin C., Davis I., Zamore P.D., Weng Z., Theurkauf W.E. UAP56 couples piRNA clusters to the perinuclear transposon silencing machinery. Cell 2012, 151:871-884.
62. 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.
63. Watanabe T., Chuma S., Yamamoto Y., Kuramochi-Miyagawa S., Totoki Y., Toyoda A., Hoki Y., Fujiyama A., Shibata T., Sado T., Noce T., Nakano T., Nakatsuji N., Lin H., Sasaki H. MITOPLD is a mitochondrial protein essential for nuage formation and piRNA biogenesis in the mouse germline. Dev. Cell 2011, 20:364-375.
64. Nishimasu H., Ishizu H., Saito K., Fukuhara S., Kamatani M.K., Bonnefond L., Matsumoto N., Nishizawa T., Nakanaga K., Aoki J., Ishitani R., Siomi H., Siomi M.C., Nureki O. Structure and function of Zucchini endoribonuclease in piRNA biogenesis. Nature 2012, 491:284-287.
65. 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, 491:279-283.
66. 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 2007, 315:1587-1590.
67. 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.
68. Kirino Y., Mourelatos Z. The mouse homolog of HEN1 is a potential methylase for Piwi-interacting RNAs. RNA N. Y. N. 2007, 13:1397-1401.
69. Kawaoka S., Izumi N., Katsuma S., Tomari Y. 3' end formation of PIWI-interacting RNAs in vitro. Mol. Cell 2011, 43:1015-1022.
70. Schirle N.T., MacRae I.J. The crystal structure of human Argonaute2. Science 2012, 336:1037-1040.
71. Nakanishi K., Weinberg D.E., Bartel D.P., Patel D.J. Structure of yeast Argonaute with guide RNA. Nature 2012, 486:368-374.
72. Elkayam E., Kuhn C.-D., Tocilj A., Haase A.D., Greene E.M., Hannon G.J., Joshua-Tor L. The structure of human argonaute-2 in complex with miR-20a. Cell 2012, 150:100-110.
73. Meister G., Landthaler M., Patkaniowska A., Dorsett Y., Teng G., Tuschl T. Human Argonaute2 mediates RNA cleavage targeted by miRNAs and siRNAs. Mol. Cell 2004, 15:185-197.
74. 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 2004, 305:1437-1441.
75. Tritschler F., Huntzinger E., Izaurralde E. Role of GW182 proteins and PABPC1 in the miRNA pathway: a sense of déjà vu. Nat. Rev. Mol. Cell Biol. 2010, 11:379-384.
76. Huntzinger E., Izaurralde E. Gene silencing by microRNAs: contributions of translational repression and mRNA decay. Nat. Rev. Genet. 2011, 12:99-110.
77. Kawamata T., Tomari Y. Making RISC. Trends Biochem. Sci. 2010, 35:368-376.
78. Schwarz D.S., Hutvágner G., Du T., Xu Z., Aronin N., Zamore P.D. Asymmetry in the assembly of the RNAi enzyme complex. Cell 2003, 115:199-208.
79. Khvorova A., Reynolds A., Jayasena S.D. Functional siRNAs and miRNAs exhibit strand bias. Cell 2003, 115:209-216.
80. Tomari Y., Matranga C., Haley B., Martinez N., Zamore P.D. A protein sensor for siRNA asymmetry. Science 2004, 306:1377-1380.
81. Liu Q., Rand T.A., Kalidas S., Du F., Kim H.-E., Smith D.P., Wang X. R2D2, a bridge between the initiation and effector steps of the Drosophila RNAi pathway. Science 2003, 301:1921-1925.
82. Tomari Y., Du T., Haley B., Schwarz D.S., Bennett R., Cook H.A., Koppetsch B.S., Theurkauf W.E., Zamore P.D. RISC assembly defects in the Drosophila RNAi mutant armitage. Cell 2004, 116:831-841.
83. Tomari Y., Du T., Zamore P.D. Sorting of Drosophila small silencing RNAs. Cell 2007, 130:299-308.
84. Liu X., Jiang F., Kalidas S., Smith D., Liu Q. Dicer-2 and R2D2 coordinately bind siRNA to promote assembly of the siRISC complexes. RNA N. Y. N. 2006, 12:1514-1520.
85. Martinez J., Patkaniowska A., Urlaub H., Lührmann R., Tuschl T. Single-stranded antisense siRNAs guide target RNA cleavage in RNAi. Cell 2002, 110:563-574.
86. Kanellopoulou C., Muljo S.A., Kung A.L., Ganesan S., Drapkin R., Jenuwein T., Livingston D.M., Rajewsky K. Dicer-deficient mouse embryonic stem cells are defective in differentiation and centromeric silencing. Genes Dev. 2005, 19:489-501.
87. Murchison E.P., Partridge J.F., Tam O.H., Cheloufi S., Hannon G.J. Characterization of Dicer-deficient murine embryonic stem cells. Proc. Natl. Acad. Sci. U. S. A. 2005, 102:12135-12140.
88. Betancur J.G., Tomari Y. Dicer is dispensable for asymmetric RISC loading in mammals. RNA N. Y. N. 2012, 18:24-30.
89. Kim Y., Yeo J., Lee J.H., Cho J., Seo D., Kim J.-S., Kim V.N. Deletion of human tarbp2 reveals cellular microRNA targets and cell-cycle function of TRBP. Cell Rep. 2014, 9:1061-1074.
90. Parker J.S., Roe S.M., Barford D. Structural insights into mRNA recognition from a PIWI domain-siRNA guide complex. Nature 2005, 434:663-666.
91. 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 2005, 434:666-670.
92. Suzuki H.I., Katsura A., Yasuda T., Ueno T., Mano H., Sugimoto K., Miyazono K. Small-RNA asymmetry is directly driven by mammalian Argonautes. Nat. Struct. Mol. Biol. 2015, 22:512-521.
93. Yoda M., Kawamata T., Paroo Z., Ye X., Iwasaki S., Liu Q., Tomari Y. ATP-dependent human RISC assembly pathways. Nat. Struct. Mol. Biol. 2010, 17:17-23.
94. Kawamata T., Seitz H., Tomari Y. Structural determinants of miRNAs for RISC loading and slicer-independent unwinding. Nat. Struct. Mol. Biol. 2009, 16:953-960.
95. Okamura K., Liu N., Lai E.C. Distinct mechanisms for microRNA strand selection by Drosophila Argonautes. Mol. Cell 2009, 36:431-444.
96. Czech B., Zhou R., Erlich Y., Brennecke J., Binari R., Villalta C., Gordon A., Perrimon N., Hannon G.J. Hierarchical rules for Argonaute loading in Drosophila. Mol. Cell 2009, 36:445-456.
97. Ghildiyal M., Xu J., Seitz H., Weng Z., Zamore P.D. Sorting of Drosophila small silencing RNAs partitions microRNA* strands into the RNA interference pathway. RNA N. Y. N. 2010, 16:43-56.
98. Mi S., Cai T., Hu Y., Chen Y., Hodges E., Ni F., Wu L., Li S., Zhou H., Long C., Chen S., Hannon G.J., Qi Y. Sorting of small RNAs into Arabidopsis argonaute complexes is directed by the 5' terminal nucleotide. Cell 2008, 133:116-127.
99. Montgomery T.A., Howell M.D., Cuperus J.T., Li D., Hansen J.E., Alexander A.L., Chapman E.J., Fahlgren N., Allen E., Carrington J.C. Specificity of ARGONAUTE7-miR390 interaction and dual functionality in TAS3 trans-acting siRNA formation. Cell 2008, 133:128-141.
100. Takeda A., Iwasaki S., Watanabe T., Utsumi M., Watanabe Y. The mechanism selecting the guide strand from small RNA duplexes is different among argonaute proteins. Plant Cell Physiol. 2008, 49:493-500.
101. Endo Y., Iwakawa H., Tomari Y. Arabidopsis ARGONAUTE7 selects miR390 through multiple checkpoints during RISC assembly. EMBO Rep. 2013, 14:652-658.
102. Kwak P.B., Tomari Y. The N domain of Argonaute drives duplex unwinding during RISC assembly. Nat. Struct. Mol. Biol. 2012, 19:145-151.
103. Wang Y., Juranek S., Li H., Sheng G., Wardle G.S., Tuschl T., Patel D.J. Nucleation, propagation and cleavage of target RNAs in Ago silencing complexes. Nature 2009, 461:754-761.
104. 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 2005, 123:607-620.
105. Rand T.A., Petersen S., Du F., Wang X. Argonaute2 cleaves the anti-guide strand of siRNA during RISC activation. Cell 2005, 123:621-629.
106. Miyoshi K., Tsukumo H., Nagami T., Siomi H., Siomi M.C. Slicer function of Drosophila Argonautes and its involvement in RISC formation. Genes Dev. 2005, 19:2837-2848.
107. Shin C. Cleavage of the star strand facilitates assembly of some microRNAs into Ago2-containing silencing complexes in mammals. Mol. Cells 2008, 26:308-313.
108. Liu Y., Ye X., Jiang F., Liang C., Chen D., Peng J., Kinch L.N., Grishin N.V., Liu Q. C3PO, an endoribonuclease that promotes RNAi by facilitating RISC activation. Science 2009, 325:750-753.
109. Ye X., Huang N., Liu Y., Paroo Z., Huerta C., Li P., Chen S., Liu Q., Zhang H. Structure of C3PO and mechanism of human RISC activation. Nat. Struct. Mol. Biol. 2011, 18:650-657.
110. Kawamata T., Yoda M., Tomari Y. Multilayer checkpoints for microRNA authenticity during RISC assembly. EMBO Rep. 2011, 12:944-949.
111. Lewis B.P., Shih I.-hun., Jones-Rhoades M.W., Bartel D.P., Burge C.B. Prediction of mammalian microRNA targets. Cell 2003, 115:787-798.
112. Doench J.G., Sharp P.A. Specificity of microRNA target selection in translational repression. Genes Dev. 2004, 18:504-511.
113. Brennecke J., Stark A., Russell R.B., Cohen S.M. Principles of microRNA-target recognition. PLoS Biol. 2005, 3:e85.
114. Grimson A., Farh K.K.-H., Johnston W.K., Garrett-Engele P., Lim L.P., Bartel D.P. MicroRNA targeting specificity in mammals: determinants beyond seed pairing. Mol. Cell 2007, 27:91-105.
115. Gu S., Jin L., Huang Y., Zhang F., Kay M.A. Slicing-independent RISC activation requires the argonaute PAZ domain. Curr. Biol. 2012, 22:1536-1542.
116. 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.
117. Ameres S.L., Horwich M.D., Hung J.-H., Xu J., Ghildiyal M., Weng Z., Zamore P.D. Target RNA-directed trimming and tailing of small silencing RNAs. Science 2010, 328:1534-1539.
118. Ameres S.L., Hung J.-H., Xu J., Weng Z., Zamore P.D. Target RNA-directed tailing and trimming purifies the sorting of endo-siRNAs between the two Drosophila Argonaute proteins. RNA N. Y. N. 2011, 17:54-63.
119. Park W., Li J., Song R., Messing J., Chen X. CARPEL FACTORY, a Dicer homolog, and HEN1, a novel protein, act in microRNA metabolism in Arabidopsis thaliana. Curr. Biol. 2002, 12:1484-1495.
120. Yu B., Yang Z., Li J., Minakhina S., Yang M., Padgett R.W., Steward R., Chen X. Methylation as a crucial step in plant microRNA biogenesis. Science 2005, 307:932-935.
121. Li J., Yang Z., Yu B., Liu J., Chen X. Methylation protects miRNAs and siRNAs from a 3'-end uridylation activity in Arabidopsis. Curr. Biol. 2005, 15:1501-1507.
122. Yang Z., Ebright Y.W., Yu B., Chen X. HEN1 recognizes 21-24nt small RNA duplexes and deposits a methyl group onto the 2' OH of the 3' terminal nucleotide. Nucleic Acids Res. 2006, 34:667-675.
123. Pham J.W., Sontheimer E.J. Molecular requirements for RNA-induced silencing complex assembly in the Drosophila RNA interference pathway. J. Biol. Chem. 2005, 280:39278-39283.
124. Iki T., Yoshikawa M., Nishikiori M., Jaudal M.C., Matsumoto-Yokoyama E., Mitsuhara I., Meshi T., Ishikawa M. In vitro assembly of plant RNA-induced silencing complexes facilitated by molecular chaperone HSP90. Mol. Cell 2010, 39:282-291.
125. Iwasaki S., Kobayashi M., Yoda M., Sakaguchi Y., Katsuma S., Suzuki T., Tomari Y. Hsc70/Hsp90 chaperone machinery mediates ATP-dependent RISC loading of small RNA duplexes. Mol. Cell 2010, 39:292-299.
126. Johnston M., Geoffroy M.-C., Sobala A., Hay R., Hutvagner G. HSP90 protein stabilizes unloaded argonaute complexes and microscopic P-bodies in human cells. Mol. Biol. Cell 2010, 21:1462-1469.
127. Miyoshi T., Takeuchi A., Siomi H., Siomi M.C. A direct role for Hsp90 in pre-RISC formation in Drosophila. Nat. Struct. Mol. Biol. 2010, 17:1024-1026.
128. Iki T., Yoshikawa M., Meshi T., Ishikawa M. Cyclophilin 40 facilitates HSP90-mediated RISC assembly in plants. EMBO J. 2012, 31:267-278.
129. Pare J.M., LaPointe P., Hobman T.C. Hsp90 cochaperones p23 and FKBP4 physically interact with hAgo2 and activate RNA interference-mediated silencing in mammalian cells. Mol. Biol. Cell 2013, 24:2303-2310.
130. Martinez N.J., Chang H.-M., Borrajo J.de R., Gregory R.I. The co-chaperones Fkbp4/5 control Argonaute2 expression and facilitate RISC assembly. RNA N. Y. N. 2013, 19:1583-1593.
131. Iwasaki S., Sasaki H.M., Sakaguchi Y., Suzuki T., Tadakuma H., Tomari Y. Defining fundamental steps in the assembly of the Drosophila RNAi enzyme complex. Nature 2015, 521:533-536.
132. Ye R., Wang W., Iki T., Liu C., Wu Y., Ishikawa M., Zhou X., Qi Y. Cytoplasmic assembly and selective nuclear import of Arabidopsis Argonaute4/siRNA complexes. Mol. Cell 2012, 46:859-870.
133. Woehrer S.L., Aronica L., Suhren J.H., Busch C.J.-L., Noto T., Mochizuki K. A Tetrahymena Hsp90 co-chaperone promotes siRNA loading by ATP-dependent and ATP-independent mechanisms. EMBO J. 2015, 34:559-577.
134. Smith D.F., Toft D.O. Minireview: the intersection of steroid receptors with molecular chaperones: observations and questions. Mol. Endocrinol. 2008, 22:2229-2240.
135. Taipale M., Jarosz D.F., Lindquist S. HSP90 at the hub of protein homeostasis: emerging mechanistic insights. Nat. Rev. Mol. Cell Biol. 2010, 11:515-528.
136. Li J., Soroka J., Buchner J. The Hsp90 chaperone machinery: conformational dynamics and regulation by co-chaperones. Biochim. Biophys. Acta 2012, 1823:624-635.
137. 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. 2005, 12:340-349.
138. 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.
139. Xiol J., Cora E., Koglgruber R., Chuma S., Subramanian S., Hosokawa M., Reuter M., Yang Z., Berninger P., Palencia A., Benes V., Penninger J., Sachidanandam R., Pillai R.S. A role for Fkbp6 and the chaperone machinery in piRNA amplification and transposon silencing. Mol. Cell 2012, 47:970-979.
140. Izumi N., Kawaoka S., Yasuhara S., Suzuki Y., Sugano S., Katsuma S., Tomari Y. Hsp90 facilitates accurate loading of precursor piRNAs into PIWI proteins. RNA N. Y. N. 2013, 19:896-901.
141. Girard A., Sachidanandam R., Hannon G.J., Carmell M.A. A germline-specific class of small RNAs binds mammalian Piwi proteins. Nature 2006, 442:199-202.
142. Aravin A., Gaidatzis D., Pfeffer S., Lagos-Quintana M., Landgraf P., Iovino N., Morris P., Brownstein M.J., Kuramochi-Miyagawa S., Nakano T., Chien M., Russo J.J., Ju J., Sheridan R., Sander C., Zavolan M., Tuschl T. A novel class of small RNAs bind to MILI protein in mouse testes. Nature 2006, 442:203-207.
143. Vagin V.V., Sigova A., Li C., Seitz H., Gvozdev V., Zamore P.D. A distinct small RNA pathway silences selfish genetic elements in the germline. Science 2006, 313:320-324.
144. Nishida K.M., Saito K., Mori T., Kawamura Y., Nagami-Okada T., Inagaki S., Siomi H., Siomi M.C. Gene silencing mechanisms mediated by Aubergine piRNA complexes in Drosophila male gonad. RNA N. Y. N. 2007, 13:1911-1922.
145. Aravin A.A., Sachidanandam R., Bourc'his D., Schaefer C., Pezic D., Toth K.F., Bestor T., Hannon G.J. A piRNA pathway primed by individual transposons is linked to de novo DNA methylation in mice. Mol. Cell 2008, 31:785-799.
146. Li C., Vagin V.V., Lee S., Xu J., Ma S., Xi H., Seitz H., Horwich M.D., Syrzycka M., Honda B.M., Kittler E.L.W., Zapp M.L., Klattenhoff C., Schulz N., Theurkauf W.E., Weng Z., Zamore P.D. Collapse of germline piRNAs in the absence of Argonaute3 reveals somatic piRNAs in flies. Cell 2009, 137:509-521.
147. 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.
148. 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.
149. Nagao A., Mituyama T., Huang H., Chen D., Siomi M.C., Siomi H. Biogenesis pathways of piRNAs loaded onto AGO3 in the Drosophila testis. RNA N. Y. N. 2010, 16:2503-2515.
150. Cox D.N., Chao A., Baker J., Chang L., Qiao D., Lin H. A novel class of evolutionarily conserved genes defined by piwi are essential for stem cell self-renewal. Genes Dev. 1998, 12:3715-3727.
151. 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 2000, 127:503-514.
152. Saito K., Nishida K.M., Mori T., Kawamura Y., Miyoshi K., Nagami T., Siomi H., Siomi M.C. Specific association of Piwi with rasiRNAs derived from retrotransposon and heterochromatic regions in the Drosophila genome. Genes Dev. 2006, 20:2214-2222.
153. Mohn F., Handler D., Brennecke J. Noncoding RNA piRNA-guided slicing specifies transcripts for Zucchini-dependent, phased piRNA biogenesis. Science 2015, 348:812-817.
154. Han B.W., Wang W., Li C., Weng Z., Zamore P.D. Noncoding RNA piRNA-guided transposon cleavage initiates Zucchini-dependent, phased piRNA production. Science 2015, 348:817-821.
155. Homolka D., Pandey R.R., Goriaux C., Brasset E., Vaury C., Sachidanandam R., Fauvarque M.-O., Pillai R.S. PIWI slicing and RNA elements in precursors instruct directional primary piRNA biogenesis. Cell Rep. 2015, 12:418-428.
156. Kawaoka S., Hayashi N., Suzuki Y., Abe H., Sugano S., Tomari Y., Shimada T., Katsuma S. The Bombyx ovary-derived cell line endogenously expresses PIWI/PIWI-interacting RNA complexes. RNA N. Y. N. 2009, 15:1258-1264.
157. Cora E., Pandey R.R., Xiol J., Taylor J., Sachidanandam R., McCarthy A.A., Pillai R.S. The MID-PIWI module of Piwi proteins specifies nucleotide- and strand-biases of piRNAs. RNA N. Y. N. 2014, 20:773-781.
158. Wang W., Yoshikawa M., Han B.W., Izumi N., Tomari Y., Weng Z., Zamore P.D. The initial uridine of primary piRNAs does not create the tenth adenine that is the hallmark of secondary piRNAs. Mol. Cell 2014, 56:708-716.
159. Schirle N.T., Sheu-Gruttadauria J., MacRae I.J. Structural basis for microRNA targeting. Science 2014, 346:608-613.
160. Gibbings D., Voinnet O. Control of RNA silencing and localization by endolysosomes. Trends Cell Biol. 2010, 20:491-501.
161. Kim Y.J., Maizel A., Chen X. Traffic into silence: endomembranes and post-transcriptional RNA silencing. EMBO J. 2014, 33:968-980.
162. Cikaluk D.E., Tahbaz N., Hendricks L.C., DiMattia G.E., Hansen D., Pilgrim D., Hobman T.C. GERp95, a membrane-associated protein that belongs to a family of proteins involved in stem cell differentiation. Mol. Biol. Cell 1999, 10:3357-3372.
163. Tahbaz N., Carmichael J.B., Hobman T.C. GERp95 belongs to a family of signal-transducing proteins and requires Hsp90 activity for stability and Golgi localization. J. Biol. Chem. 2001, 276:43294-43299.
164. Sen G.L., Blau H.M. Argonaute 2/RISC resides in sites of mammalian mRNA decay known as cytoplasmic bodies. Nat. Cell Biol. 2005, 7:633-636.
165. Liu J., Valencia-Sanchez M.A., Hannon G.J., Parker R. MicroRNA-dependent localization of targeted mRNAs to mammalian P-bodies. Nat. Cell Biol. 2005, 7:719-723.
166. Pillai R.S., Bhattacharyya S.N., Artus C.G., Zoller T., Cougot N., Basyuk E., Bertrand E., Filipowicz W. Inhibition of translational initiation by Let-7 microRNA in human cells. Science 2005, 309:1573-1576.
167. Liu J., Rivas F.V., Wohlschlegel J., Yates J.R., Parker R., Hannon G.J. A role for the P-body component GW182 in microRNA function. Nat. Cell Biol. 2005, 7:1261-1266.
168. Jakymiw A., Lian S., Eystathioy T., Li S., Satoh M., Hamel J.C., Fritzler M.J., Chan E.K.L. Disruption of GW bodies impairs mammalian RNA interference. Nat. Cell Biol. 2005, 7:1267-1274.
169. Chu C., Rana T.M. Translation repression in human cells by microRNA-induced gene silencing requires RCK/p54. PLoS Biol. 2006, 4:e210.
170. Leung A.K.L., Calabrese J.M., Sharp P.A. Quantitative analysis of Argonaute protein reveals microRNA-dependent localization to stress granules. Proc. Natl. Acad. Sci. U. S. A. 2006, 103:18125-18130.
171. Eulalio A., Behm-Ansmant I., Schweizer D., Izaurralde E. P-body formation is a consequence, not the cause, of RNA-mediated gene silencing. Mol. Cell. Biol. 2007, 27:3970-3981.
172. Siomi M.C., Siomi H. Characterization of endogenous human Argonautes and their miRNA partners in RNA silencing. Nucleic Acids Symp. Ser. 2008, 2004:59-60.
173. Jagannath A., Wood M.J.A. Localization of double-stranded small interfering RNA to cytoplasmic processing bodies is Ago2 dependent and results in up-regulation of GW182 and Argonaute-2. Mol. Biol. Cell 2009, 20:521-529.
174. Gibbings D.J., Ciaudo C., Erhardt M., Voinnet O. Multivesicular bodies associate with components of miRNA effector complexes and modulate miRNA activity. Nat. Cell Biol. 2009, 11:1143-1149.
175. Lee Y.S., Pressman S., Andress A.P., Kim K., White J.L., Cassidy J.J., Li X., Lubell K., Lim D.H., Cho I.S., Nakahara K., Preall J.B., Bellare P., Sontheimer E.J., Carthew R.W. Silencing by small RNAs is linked to endosomal trafficking. Nat. Cell Biol. 2009, 11:1150-1156.
176. Harris D.A., Kim K., Nakahara K., Vásquez-Doorman C., Carthew R.W. Cargo sorting to lysosome-related organelles regulates siRNA-mediated gene silencing. J. Cell Biol. 2011, 194:77-87.
177. Gibbings D., Leblanc P., Jay F., Pontier D., Michel F., Schwab Y., Alais S., Lagrange T., Voinnet O. Human prion protein binds Argonaute and promotes accumulation of microRNA effector complexes. Nat. Struct. Mol. Biol. 2012, 19:517-524. S1.
178. Gibbings D., Mostowy S., Jay F., Schwab Y., Cossart P., Voinnet O. Selective autophagy degrades DICER and AGO2 and regulates miRNA activity. Nat. Cell Biol. 2012, 14:1314-1321.
179. Stalder L., Heusermann W., Sokol L., Trojer D., Wirz J., Hean J., Fritzsche A., Aeschimann F., Pfanzagl V., Basselet P., Weiler J., Hintersteiner M., Morrissey D.V., Meisner-Kober N.C. The rough endoplasmatic reticulum is a central nucleation site of siRNA-mediated RNA silencing. EMBO J. 2013, 32:1115-1127.
180. Antoniou A., Baptista M., Carney N., Hanley J.G. PICK1 links Argonaute 2 to endosomes in neuronal dendrites and regulates miRNA activity. EMBO Rep. 2014, 15:548-556.
181. Zhang X., Zuo X., Yang B., Li Z., Xue Y., Zhou Y., Huang J., Zhao X., Zhou J., Yan Y., Zhang H., Guo P., Sun H., Guo L., Zhang Y., Fu X.-D. MicroRNA directly enhances mitochondrial translation during muscle differentiation. Cell 2014, 158:607-619.
182. Li S., Liu L., Zhuang X., Yu Y., Liu X., Cui X., Ji L., Pan Z., Cao X., Mo B., Zhang F., Raikhel N., Jiang L., Chen X. MicroRNAs inhibit the translation of target mRNAs on the endoplasmic reticulum in Arabidopsis. Cell 2013, 153:562-574.
183. 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.
184. 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.
185. Qi H., Watanabe T., Ku H.-Y., Liu N., Zhong M., Lin H. The Yb body, a major site for Piwi-associated RNA biogenesis and a gateway for Piwi expression and transport to the nucleus in somatic cells. J. Biol. Chem. 2011, 286:3789-3797.
186. Murota Y., Ishizu H., Nakagawa S., Iwasaki Y.W., Shibata S., Kamatani M.K., Saito K., Okano H., Siomi H., Siomi M.C. Yb integrates piRNA intermediates and processing factors into perinuclear bodies to enhance piRISC assembly. Cell Rep. 2014, 8:103-113.
187. 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. 2015, 12:429-440.
188. al-Mukhtar K.A., Webb A.C. An ultrastructural study of primordial germ cells, oogonia and early oocytes in Xenopus laevis. J. Embryol. Exp. Morphol. 1971, 26:195-217.
189. Eddy E.M. Germ plasm and the differentiation of the germ cell line. Int. Rev. Cytol. 1975, 43:229-280.
190. Snee M.J., Macdonald P.M. Live imaging of nuage and polar granules: evidence against a precursor-product relationship and a novel role for Oskar in stabilization of polar granule components. J. Cell Sci. 2004, 117:2109-2120.
191. Lim A.K., Kai T. Unique germ-line organelle, nuage, functions to repress selfish genetic elements in Drosophila melanogaster. Proc. Natl. Acad. Sci. U. S. A. 2007, 104:6714-6719.
192. Liang L., Diehl-Jones W., Lasko P. Localization of vasa protein to the Drosophila pole plasm is independent of its RNA-binding and helicase activities. Dev. Camb. Engl. 1994, 120:1201-1211.
193. 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. Dev. Camb. Engl. 2003, 130:859-871.
194. 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.
195. Xiol J., Spinelli P., Laussmann M.A., Homolka D., Yang Z., Cora E., Couté Y., Conn S., Kadlec J., Sachidanandam R., Kaksonen M., Cusack S., Ephrussi A., Pillai R.S. RNA clamping by Vasa assembles a piRNA amplifier complex on transposon transcripts. Cell 2014, 157:1698-1711.
196. Nishida K.M., Iwasaki Y.W., Murota Y., Nagao A., Mannen T., Kato Y., Siomi H., Siomi M.C. Respective functions of two distinct Siwi complexes assembled during PIWI-interacting RNA biogenesis in Bombyx germ cells. Cell Rep. 2015, 10:193-203.
197. Aravin A.A., van der Heijden G.W., Castañeda J., Vagin V.V., Hannon G.J., Bortvin A. Cytoplasmic compartmentalization of the fetal piRNA pathway in mice. PLoS Genet. 2009, 5:e1000764.
198. Fujiwara Y., Komiya T., Kawabata H., Sato M., Fujimoto H., Furusawa M., Noce T. Isolation of a DEAD-family protein gene that encodes a murine homolog of Drosophila vasa and its specific expression in germ cell lineage. Proc. Natl. Acad. Sci. U. S. A. 1994, 91:12258-12262.
199. Toyooka Y., Tsunekawa N., Takahashi Y., Matsui Y., Satoh M., Noce T. Expression and intracellular localization of mouse Vasa-homologue protein during germ cell development. Mech. Dev. 2000, 93:139-149.
200. Kuramochi-Miyagawa S., Kimura T., Ijiri T.W., Isobe T., Asada N., Fujita Y., Ikawa M., Iwai N., Okabe M., Deng W., Lin H., Matsuda Y., Nakano T. Mili, a mammalian member of piwi family gene, is essential for spermatogenesis. Dev. Camb. Engl. 2004, 131:839-849.
201. Costa Y., Speed R.M., Gautier P., Semple C.A., Maratou K., Turner J.M.A., Cooke H.J. Mouse MAELSTROM: the link between meiotic silencing of unsynapsed chromatin and microRNA pathway?. Hum. Mol. Genet. 2006, 15:2324-2334.
202. Liu L., Qi H., Wang J., Lin H. PAPI, a novel TUDOR-domain protein, complexes with AGO3, ME31B and TRAL in the nuage to silence transposition. Dev. Camb. Engl. 2011, 138:1863-1873.
203. Honda S., Kirino Y., Maragkakis M., Alexiou P., Ohtaki A., Murali R., Mourelatos Z., Kirino Y. Mitochondrial protein BmPAPI modulates the length of mature piRNAs. RNA N. Y. N. 2013, 19:1405-1418.
204. Saxe J.P., Chen M., Zhao H., Lin H. Tdrkh is essential for spermatogenesis and participates in primary piRNA biogenesis in the germline. EMBO J. 2013, 32:1869-1885.