Crystal Structure of Silkworm PIWI-Clade Argonaute Siwi Bound to piRNA

Cell

Volumn 167, Issue 2, 2016, Pages 484-497.e9

  Matsumoto, Naoki ^a   Nishimasu, Hiroshi ^a,b   Sakakibara, Kazuhiro ^a   Nishida, Kazumichi M ^a   Hirano, Takamasa ^c   Ishitani, Ryuichiro ^a   Siomi, Haruhiko ^c   Siomi, Mikiko C ^a   Nureki, Osamu ^a  

^a UNIVERSITY OF TOKYO   (Japan)

^b JAPAN SCIENCE AND TECHNOLOGY AGENCY   (Japan)

^c KEIO UNIVERSITY SCHOOL OF MEDICINE   (Japan)

Author keywords

1U bias; Argonaute; piRNA; PIWI; RNA silencing; Siwi; small RNA; x ray crystallography

Indexed keywords

ARGONAUTE PROTEIN; GUIDE RNA; PHOSPHATE; PIWI INTERACTING RNA; PIWI PROTEIN; SIWI PROTEIN; UNCLASSIFIED DRUG; EIF2C2 PROTEIN, HUMAN; INSECT PROTEIN; SMALL INTERFERING RNA; TRANSPOSON;

ANIMAL CELL; ARTICLE; BOMBYX MORI; CATALYSIS; CRYSTAL STRUCTURE; EUKARYOTE; GENE SILENCING; MOLECULAR RECOGNITION; NONHUMAN; PRIORITY JOURNAL; PROKARYOTE; PROTEIN CLEAVAGE; PROTEIN DOMAIN; PROTEIN RNA BINDING; TRANSPOSON; ANIMAL; BOMBYX; CELL LINE; CHEMISTRY; CONFORMATION; GENETICS; HUMAN; ISOLATION AND PURIFICATION; METABOLISM; X RAY CRYSTALLOGRAPHY;

ANIMALS; ARGONAUTE PROTEINS; BOMBYX; CELL LINE; CRYSTALLOGRAPHY, X-RAY; DNA TRANSPOSABLE ELEMENTS; GENE SILENCING; HUMANS; INSECT PROTEINS; NUCLEIC ACID CONFORMATION; RNA, SMALL INTERFERING;

EID: 84990913683     PISSN: 00928674     EISSN: 10974172     Source Type: Journal    
DOI: 10.1016/j.cell.2016.09.002     Document Type: Article

References (64)

1. Adams, P.D., Afonine, P.V., Bunkóczi, G., Chen, V.B., Davis, I.W., Echols, N., Headd, J.J., Hung, L.W., Kapral, G.J., Grosse-Kunstleve, R.W., et al. PHENIX: a comprehensive Python-based system for macromolecular structure solution. Acta Crystallogr. D Biol. Crystallogr. 66 (2010), 213–221.
2. 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.
3. Chandradoss, S.D., Schirle, N.T., Szczepaniak, M., MacRae, I.J., Joo, C., A dynamic search process underlies microRNA targeting. Cell 162 (2015), 96–107.
4. 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 20 (2014), 773–781.
5. Cowtan, K., The Buccaneer software for automated model building. 1. Tracing protein chains. Acta Crystallogr. D Biol. Crystallogr. 62 (2006), 1002–1011.
6. Czech, B., Hannon, G.J., Small RNA sorting: matchmaking for Argonautes. Nat. Rev. Genet. 12 (2011), 19–31.
7. Czech, B., Hannon, G.J., One loop to rule them all: the ping-pong cycle and piRNA-guided silencing. Trends Biochem. Sci. 41 (2016), 324–337.
8. 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 150 (2012), 100–110.
9. Emsley, P., Cowtan, K., Coot: model-building tools for molecular graphics. Acta Crystallogr. D Biol. Crystallogr. 60 (2004), 2126–2132.
10. Evans, P.R., Murshudov, G.N., How good are my data and what is the resolution?. Acta Crystallogr. D Biol. Crystallogr. 69 (2013), 1204–1214.
11. Faehnle, C.R., Elkayam, E., Haase, A.D., Hannon, G.J., Joshua-Tor, L., The making of a slicer: activation of human Argonaute-1. Cell Rep. 3 (2013), 1901–1909.
12. Feltzin, V.L., Khaladkar, M., Abe, M., Parisi, M., Hendriks, G.J., Kim, J., Bonini, N.M., The exonuclease Nibbler regulates age-associated traits and modulates piRNA length in Drosophila. Aging Cell 14 (2015), 443–452.
13. Frank, F., Sonenberg, N., Nagar, B., Structural basis for 5′-nucleotide base-specific recognition of guide RNA by human AGO2. Nature 465 (2010), 818–822.
14. Ghildiyal, M., Zamore, P.D., Small silencing RNAs: an expanding universe. Nat. Rev. Genet. 10 (2009), 94–108.
15. Gu, S., Jin, L., Huang, Y., Zhang, F., Kay, M.A., Slicing-independent RISC activation requires the argonaute PAZ domain. Curr. Biol. 22 (2012), 1536–1542.
16. 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.
17. 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 348 (2015), 817–821.
18. 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. 12 (2015), 418–428.
19. 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. 17 (2007), 1265–1272.
20. 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 491 (2012), 279–283.
21. Iwasaki, Y.W., Siomi, M.C., Siomi, H., PIWI-interacting RNA: its biogenesis and functions. Annu. Rev. Biochem. 84 (2015), 405–433.
22. Izumi, N., Shoji, K., Sakaguchi, Y., Honda, S., Kirino, Y., Suzuki, T., Katsuma, S., Tomari, Y., Identification and functional analysis of the pre-piRNA 3′ Trimmer in silkworms. Cell 164 (2016), 962–973.
23. Jo, M.H., Shin, S., Jung, S.R., Kim, E., Song, J.J., Hohng, S., Human Argonaute 2 has diverse reaction pathways on target RNAs. Mol. Cell 59 (2015), 117–124.
24. 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 15 (2009), 1258–1264.
25. Kawaoka, S., Izumi, N., Katsuma, S., Tomari, Y., 3′ end formation of PIWI-interacting RNAs in vitro. Mol. Cell 43 (2011), 1015–1022.
26. Kobayashi, H., Tomari, Y., RISC assembly: Coordination between small RNAs and Argonaute proteins. Biochim. Biophys. Acta 1859 (2016), 71–81.
27. Kwak, P.B., Tomari, Y., The N domain of Argonaute drives duplex unwinding during RISC assembly. Nat. Struct. Mol. Biol. 19 (2012), 145–151.
28. Lewis, B.P., Burge, C.B., Bartel, D.P., Conserved seed pairing, often flanked by adenosines, indicates that thousands of human genes are microRNA targets. Cell 120 (2005), 15–20.
29. Malone, C.D., Hannon, G.J., Small RNAs as guardians of the genome. Cell 136 (2009), 656–668.
30. Meister, G., Argonaute proteins: functional insights and emerging roles. Nat. Rev. Genet. 14 (2013), 447–459.
31. 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.
32. Mohn, F., Handler, D., Brennecke, J., Noncoding RNA. piRNA-guided slicing specifies transcripts for Zucchini-dependent, phased piRNA biogenesis. Science 348 (2015), 812–817.
33. Nakanishi, K., Weinberg, D.E., Bartel, D.P., Patel, D.J., Structure of yeast Argonaute with guide RNA. Nature 486 (2012), 368–374.
34. Nakanishi, K., Ascano, M., Gogakos, T., Ishibe-Murakami, S., Serganov, A.A., Briskin, D., Morozov, P., Tuschl, T., Patel, D.J., Eukaryote-specific insertion elements control human ARGONAUTE slicer activity. Cell Rep. 3 (2013), 1893–1900.
35. 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. 10 (2015), 193–203.
36. Nishimasu, H., Ishizu, H., Saito, K., Fukuhara, S., Kamatani, M.K., Bonnefond, L., Matsumoto, N., Nishizawa, T., Nakanaga, K., Aoki, J., et al. Structure and function of Zucchini endoribonuclease in piRNA biogenesis. Nature 491 (2012), 284–287.
37. Okamura, K., Lai, E.C., Endogenous small interfering RNAs in animals. Nat. Rev. Mol. Cell Biol. 9 (2008), 673–678.
38. Park, J.H., Shin, C., Slicer-independent mechanism drives small-RNA strand separation during human RISC assembly. Nucleic Acids Res. 43 (2015), 9418–9433.
39. 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. 20 (2006), 2214–2222.
40. 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. 21 (2007), 1603–1608.
41. Salomon, W.E., Jolly, S.M., Moore, M.J., Zamore, P.D., Serebrov, V., Single-molecule imaging reveals that Argonaute reshapes the binding properties of its nucleic acid guides. Cell 162 (2015), 84–95.
42. Schirle, N.T., MacRae, I.J., The crystal structure of human Argonaute2. Science 336 (2012), 1037–1040.
43. Schirle, N.T., Sheu-Gruttadauria, J., MacRae, I.J., Structural basis for microRNA targeting. Science 346 (2014), 608–613.
44. Schirle, N.T., Sheu-Gruttadauria, J., Chandradoss, S.D., Joo, C., MacRae, I.J., Water-mediated recognition of t1-adenosine anchors Argonaute2 to microRNA targets. eLife, 4, 2015, e07646.
45. Schürmann, N., Trabuco, L.G., Bender, C., Russell, R.B., Grimm, D., Molecular dissection of human Argonaute proteins by DNA shuffling. Nat. Struct. Mol. Biol. 20 (2013), 818–826.
46. Sheng, G., Zhao, H., Wang, J., Rao, Y., Tian, W., Swarts, D.C., van der Oost, J., Patel, D.J., Wang, Y., Structure-based cleavage mechanism of Thermus thermophilus Argonaute DNA guide strand-mediated DNA target cleavage. Proc. Natl. Acad. Sci. USA 111 (2014), 652–657.
47. Simon, B., Kirkpatrick, J.P., Eckhardt, S., Reuter, M., Rocha, E.A., Andrade-Navarro, M.A., Sehr, P., Pillai, R.S., Carlomagno, T., Recognition of 2′-O-methylated 3′-end of piRNA by the PAZ domain of a Piwi protein. Structure 19 (2011), 172–180.
48. Siomi, H., Siomi, M.C., On the road to reading the RNA-interference code. Nature 457 (2009), 396–404.
49. 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.
50. Tang, W., Tu, S., Lee, H.C., Weng, Z., Mello, C.C., The RNase PARN-1 trims piRNA 3′ ends to promote transcriptome surveillance in C. elegans. Cell 164 (2016), 974–984.
51. Terwilliger, T.C., Maximum-likelihood density modification. Acta Crystallogr. D Biol. Crystallogr. 56 (2000), 965–972.
52. Tian, Y., Simanshu, D.K., Ma, J.B., Patel, D.J., Structural basis for piRNA 2′-O-methylated 3′-end recognition by Piwi PAZ (Piwi/Argonaute/Zwille) domains. Proc. Natl. Acad. Sci. USA 108 (2011), 903–910.
53. Vagin, A., Teplyakov, A., Molecular replacement with MOLREP. Acta Crystallogr. D Biol. Crystallogr. 66 (2010), 22–25.
54. Wang, Y., Sheng, G., Juranek, S., Tuschl, T., Patel, D.J., Structure of the guide-strand-containing argonaute silencing complex. Nature 456 (2008), 209–213.
55. Wang, Y., Juranek, S., Li, H., Sheng, G., Tuschl, T., Patel, D.J., Structure of an argonaute silencing complex with a seed-containing guide DNA and target RNA duplex. Nature 456 (2008), 921–926.
56. 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 461 (2009), 754–761.
57. 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 56 (2014), 708–716.
58. Wang, H., Ma, Z., Niu, K., Xiao, Y., Wu, X., Pan, C., Zhao, Y., Wang, K., Zhang, Y., Liu, N., Antagonistic roles of Nibbler and Hen1 in modulating piRNA 3′ ends in Drosophila. Development 143 (2016), 530–539.
59. Waterman, D.G., Winter, G., Parkhurst, J.M., Fuentes-Montero, L., Hattne, J., Brewster, A., Sauter, N.K., Evans, G., Rosenstrom, P., The DIALS framework for integration software. CCP4 Newsletter 49 (2013), 16–19.
60. Weick, E.M., Miska, E.A., piRNAs: from biogenesis to function. Development 141 (2014), 3458–3471.
61. Xiol, J., Spinelli, P., Laussmann, M.A., Homolka, D., Yang, Z., Cora, E., Couté, Y., Conn, S., Kadlec, J., Sachidanandam, R., et al. RNA clamping by Vasa assembles a piRNA amplifier complex on transposon transcripts. Cell 157 (2014), 1698–1711.
62. Yao, C., Sasaki, H.M., Ueda, T., Tomari, Y., Tadakuma, H., Single-molecule analysis of the target cleavage reaction by the Drosophila RNAi enzyme complex. Mol. Cell 59 (2015), 125–132.
63. Yuan, Y.R., Pei, Y., Ma, J.B., Kuryavyi, V., Zhadina, M., Meister, G., Chen, H.Y., Dauter, Z., Tuschl, T., Patel, D.J., Crystal structure of A. aeolicus argonaute, a site-specific DNA-guided endoribonuclease, provides insights into RISC-mediated mRNA cleavage. Mol. Cell 19 (2005), 405–419.
64. Zeng, L., Zhang, Q., Yan, K., Zhou, M.M., Structural insights into piRNA recognition by the human PIWI-like 1 PAZ domain. Proteins 79 (2011), 2004–2009.