Strand-specific 5′-O-methylation of siRNA duplexes controls guide strand selection and targeting specificity

RNA

Volumn 14, Issue 2, 2008, Pages 263-274

  Po, Yu Chen ^a,b   Weinmann, Lasse ^b   Gaidatzis, Dimos ^c   Pei, Yi ^a,d   Zavolan, Mihaela ^c   Tuschl, Thomas ^a   Meister, Gunter ^b  

^a ROCKEFELLER UNIVERSITY   (United States)

^b MAX PLANCK INSTITUTE OF BIOCHEMISTRY   (Germany)

^c UNIVERSITY OF BASEL   (Switzerland)

^d MERCK RESEARCH LABORATORIES   (United States)

Author keywords

Gene silencing; Off target effects; RISC; RNA interference; RNAi; siRNA

Indexed keywords

DOUBLE STRANDED RNA; PHOSPHATE; SMALL INTERFERING RNA;

AMINO ACID SEQUENCE; ARTICLE; COMPLEX FORMATION; CONTROLLED STUDY; GENE MUTATION; GENE SILENCING; GENE TARGETING; HUMAN; HUMAN CELL; NONHUMAN; PHOSPHORYLATION; PRIORITY JOURNAL; RNA METHYLATION;

ANIMALS; BASE SEQUENCE; METHYLATION; MOLECULAR SEQUENCE DATA; MUTATION; PHOSPHATES; PHOSPHORYLATION; RNA INTERFERENCE; RNA, SMALL INTERFERING; RNA-INDUCED SILENCING COMPLEX;

EID: 38649099969     PISSN: 13558382     EISSN: 14699001     Source Type: Journal    
DOI: 10.1261/rna.789808     Document Type: Article

References (82)

1. Bartel, D.P. 2004. MicroRNAs: Genomics, biogenesis, mechanism, and function. Cell 116: 281-297.
2. Birmingham, A., Anderson, E.M., Reynolds, A., Ilsley-Tyree, D., Leake, D., Fedorov, Y., Baskerville, S., Maksimova, E., Robinson, K., Karpilow, J., et al. 2006. 3′-UTR seed matches, but not overall identity, are associated with RNAi off-targets. Nat. Methods 3: 199-204.
3. Carmell, M.A., Xuan, Z., Zhang, M.Q., and Hannon, G.J. 2002. The Argonaute family: Tentacles that reach into RNAi, developmental control, stem cell maintenance, and tumorigenesis. Genes & Dev. 16: 2733-2742.
4. Chendrimada, T.P., Gregory, R.I., Kumaraswamy, E., Norman, J., Cooch, N., Nishikura, K., and Shiekhattar, R. 2005. TRBP recruits the Dicer complex to Ago2 for microRNA processing and gene silencing. Nature 436: 740-744.
5. Dorsett, Y. and Tuschl, T. 2004. siRNAs: Applications in functional genomics and potential as therapeutics. Nat. Rev. Drug Discov. 3: 318-329.
6. Ebhardt, H.A., Thi, E.P., Wang, M.B., and Unrau, P.J. 2005. Extensive 3′ modification of plant small RNAs is modulated by helper component-proteinase expression. Proc. Natl. Acad. Sci. 102: 13398-13403.
7. Echeverri, C.J. and Perrimon, N. 2006. High-throughput RNAi screening in cultured cells: A user's guide. Nat. Rev. Genet. 7: 373-384.
8. Elbashir, S.M., Lendeckel, W., and Tuschl, T. 2001. RNA interference is mediated by 21 and 22 nt RNAs. Genes & Dev. 15: 188-200.
9. Elmén, J., Thonberg, H., Ljungberg, K., Frieden, M., Westergaard, M., Xu, Y., Wahren, B., Liang, Z., Ørum, H., Koch, T., et al. 2005. Locked nucleic acid (LNA) mediated improvements in siRNA stability and functionality. Nucleic Acids Res. 33: 439-447. doi: 10.1093/nar/gki193.
10. Filipowicz, W. 2005. RNAi: The nuts and bolts of the RISC machine. Cell 122: 17-20.
11. Filipowicz, W., Jaskiewicz, L., Kolb, F.A., and Pillai, R.S. 2005. Posttranscriptional gene silencing by siRNAs and miRNAs. Curr. Opin. Struct. Biol. 15: 331-341.
12. Förstemann, K., Tomari, Y., Du, T., Vagin, V.V., Denli, A.M., Bratu, D.P., Klattenhoff, C., Theurkauf, W.E., and Zamore, P.D. 2005. Normal microRNA maturation and germ-line stem cell maintenance requires Loquacious, a double-stranded RNA-binding domain protein. PLoS Biol. 3: e236. doi: 10.1371/journal.pbio.0030236.
13. Fuchs, F. and Boutros, M. 2006. Cellular phenotyping by RNAi. Brief Funct. Genomic Proteomic 5: 52-56.
14. Gentleman, R.C., Carey, V.J., Bates, D.M., Bolstad, B., Dettling, M., Dudoit, S., Ellis, B., Gautier, L., Ge, Y., Gentry, J., et al. 2004. Bioconductor: Open software development for computational biology and bioinformatics. Genome Biol. 5: R80. doi: 10.1186/gb-2004-5-10- r80.
15. Gregory, R.I., Chendrimada, T.P., Cooch, N., and Shiekhattar, R. 2005. Human RISC couples microRNA biogenesis and posttranscriptional gene silencing. Cell 123: 631-640.
16. Grimm, D., Streetz, K.L., Jopling, C.L., Storm, T.A., Pandey, K., Davis, C.R., Marion, P., Salazar, F., and Kay, M.A. 2006. Fatality in mice due to oversaturation of cellular microRNA/short hairpin RNA pathways. Nature 441: 537-541.
17. Haase, A.D., Jaskiewicz, L., Zhang, H., Laine, S., Sack, R., Gatignol, A., and Filipowicz, W. 2005. TRBP, a regulator of cellular PKR and HIV-1 virus expression, interacts with Dicer and functions in RNA silencing. EMBO Rep. 6: 961-967.
18. Hammond, S.M., Boettcher, S., Caudy, A.A., Kobayashi, R., and Hannon, G.J. 2001. Argonaute2, a link between genetic and biochemical analyses of RNAi. Science 293: 1146-1150.
19. Harborth, J., Elbashir, S.M., Vandenburgh, K., Manninga, H., Scaringe, S.A., Weber, K., and Tuschl, T. 2003. Sequence, chemical, and structural variation of small interfering RNAs and short hairpin RNAs and the effect on mammalian gene silencing. Antisense Nucleic Acid Drug Dev. 13: 83-105.
20. Horwich, M.D., Li, C., Matranga, C., Vagin, V., Farley, G., Wang, P., and Zamore, P.D. 2007. The Drosophila RNA methyltransferase, DmHen1, modifies germline piRNAs and single-stranded siRNAs in RISC. Curr. Biol. 17: 1265-1272.
21. Hutvágner, G. and Zamore, P.D. 2002. A microRNA in a multiple-turnover RNAi enzyme complex. Science 297: 2056-2060.
22. Jackson, A.L., Bartz, S.R., Schelter, J., Kobayashi, S.V., Burchard, J., Mao, M., Li, B., Cavet, G., and Linsley, P.S. 2003. Expression profiling reveals off-target gene regulation by RNAi. Nat. Biotechnol. 21: 635-637.
23. Jackson, A.L., Burchard, J., Leake, D., Reynolds, A., Schelter, J., Guo, J., Johnson, J.M., Lim, L., Karpilow, J., Nichols, K., et al. 2006a. Position-specific chemical modification of siRNAs reduces "off-target" transcript silencing. RNA 12: 1197-1205.
24. Jackson, A.L., Burchard, J., Schelter, J., Chau, B.N., Cleary, M., Lim, L., and Linsley, P.S. 2006b. Widespread siRNA "off-target" transcript silencing mediated by seed region sequence complementarity. RNA 12: 1179-1187.
25. Jiang, F., Ye, X., Liu, X., Fincher, L., McKearin, D., and Liu, Q. 2005. Dicer-1 and R3D1-L catalyze microRNA maturation in Drosophila. Genes & Dev. 19: 1674-1679.
26. Khvorova, A., Reynolds, A., and Jayasena, S.D. 2003. Functional siRNAs and miRNAs exhibit strand bias. Cell 115: 209-216.
27. Kirino, Y. and Mourelatos, Z. 2007. Mouse Piwi-interacting RNAs are 2′-O-methylated at their 3′ termini. Nat. Struct. Mol. Biol. 14: 347-348.
28. Krausz, E. 2007. High-content siRNA screening. Mol. Biosyst. 3: 232-240.
29. Lai, E.C. 2002. Micro RNAs are complementary to 3′-UTR sequence motifs that mediate negative post-transcriptional regulation. Nat. Genet. 30: 363-364.
30. Lau, N.C., Lim, L.P., Weinstein, E.G., and Bartel, D.P. 2001. An abundant class of tiny RNAs with probable regulatory roles in Caenorhabditis elegans.. Science 294: 858-862.
31. Lee, Y., Hur, I., Park, S.Y., Kim, Y.K., Suh, M.R., and Kim, V.N. 2006. The role of PACT in the RNA silencing pathway. EMBO J. 25: 522-532.
32. Leuschner, P.J., Ameres, S.L., Kueng, S., and Martinez, J. 2006. Cleavage of the siRNA passenger strand during RISC assembly in human cells. EMBO Rep. 7: 314-320.
33. Lewis, B.P., Shih, I., Jones-Rhoades, M.W., Bartel, D.P., and Burge, C.B. 2003. Prediction of mammalian microRNA targets. Cell 115: 787-798.
34. Lim, L.P., Lau, N.C., Garrett-Engele, P., Grimson, A., Schelter, J.M., Castle, J., Bartel, D.P., Linsley, P.S., and Johnson, J.M. 2005. Microarray analysis shows that some microRNAs downregulate large numbers of target mRNAs. Nature 433: 769-773.
35. Lin, X., Ruan, X., Anderson, M.G., McDowell, J.A., Kroeger, P.E., Fesik, S.W., and Shen, Y. 2005. siRNA-mediated off-target gene silencing triggered by a 7 nt complementation. Nucleic Acids Res. 33: 4527-4535. doi: 10.1093/nar/gki762.
36. Lingel, A., Simon, B., Izaurralde, E., and Sattler, M. 2004. Nucleic acid 3′-end recognition by the Argonaute2 PAZ domain. Nat. Struct. Mol. Biol. 11: 576-577.
37. Linsley, P.S., Schelter, J., Burchard, J., Kibukawa, M., Martin, M.M., Bartz, S.R., Johnson, J.M., Cummins, J.M., Raymond, C.K., Dai, H., et al. 2007. Transcripts targeted by the microRNA-16 family cooperatively regulate cell cycle progression. Mol. Cell. Biol. 27: 2240-2252.
38. Liu, Q., Rand, T.A., Kalidas, S., Du, F., Kim, H.E., Smith, D.P., and Wang, X. 2003. R2D2, a bridge between the initiation and effector steps of the Drosophila RNAi pathway. Science 301: 1921-1925.
39. Liu, J., Carmell, M.A., Rivas, F.V., Marsden, C.G., Thomson, J.M., Song, J.J., Hammond, S.M., Joshua-Tor, L., and Hannon, G.J. 2004. Argonaute2 is the catalytic engine of mammalian RNAi. Science 305: 1437-1441.
40. Liu, X., Jiang, F., Kalidas, S., Smith, D., and Liu, Q. 2006. Dicer-2 and R2D2 coordinately bind siRNA to promote assembly of the siRISC complexes. RNA 12: 1514-1520.
41. Ma, J.B., Ye, K., and Patel, D.J. 2004. Structural basis for overhang-specific small interfering RNA recognition by the PAZ domain. Nature 429: 318-322.
42. Ma, J.B., Yuan, Y.R., Meister, G., Pei, Y., Tuschl, T., and Patel, D.J. 2005. Structural basis for 5′-end-specific recognition of guide RNA by the A. fulgidus Piwi protein. Nature 434: 666-670.
43. Maniataki, E. and Mourelatos, Z. 2005. A human, ATP-independent, RISC assembly machine fueled by pre-miRNA. Genes & Dev. 19: 2979-2990.
44. Martinez, J., Patkaniowska, A., Urlaub, H., Lührmann, R., and Tuschl, T. 2002a. Single-stranded anti-sense siRNAs guide target RNA cleavage in RNAi. Cell 110: 563-574.
45. Martinez, L.A., Naguibneva, I., Lehrmann, H., Vervisch, A., Tchenio, T., Lozano, G., and Harel-Bellan, A. 2002b. Synthetic small inhibiting RNAs: efficient tools to inactivate oncogenic mutations and restore p53 pathways. Proc. Natl. Acad. Sci. 99: 14849-14854.
46. Matranga, C., Tomari, Y., Shin, C., Bartel, D.P., and Zamore, P.D. 2005. Passenger-strand cleavage facilitates assembly of siRNA into Ago2-containing RNAi enzyme complexes. Cell 123: 607-620.
47. Meister, G. and Tuschl, T. 2004. Mechanisms of gene silencing by double-stranded RNA. Nature 431: 343-349.
48. Meister, G., Landthaler, M., Patkaniowska, A., Dorsett, Y., Teng, G., and Tuschl, T. 2004. Human Argonaute2 mediates RNA cleavage targeted by miRNAs and siRNAs. Mol. Cell 15: 185-197.
49. Meister, G., Landthaler, M., Peters, L., Chen, P.Y., Urlaub, H., Luhrmann, R., and Tuschl, T. 2005. Identification of novel Argonaute-associated proteins. Curr. Biol. 15: 2149-2155.
50. Miyoshi, K., Tsukumo, H., Nagami, T., Siomi, H., and Siomi, M.C. 2005. Slicer function of Drosophila Argonautes and its involvement in RISC formation. Genes & Dev. 19: 2837-2848.
51. Nykänen, A., Haley, B., and Zamore, P.D. 2001. ATP requirements and small interfering RNA structure in the RNA interference pathway. Cell 107: 309-321.
52. Ohara, T., Sakaguchi, Y., Suzuki, T., Ueda, H., and Miyauchi, K. 2007. The 39 termini of mouse Piwi-interacting RNAs are 2′-O-methylated. Nat. Struct. Mol. Biol. 14: 349-350.
53. Parker, J.S., Roe, S.M., and Barford, D. 2004. Crystal structure of a PIWI protein suggests mechanisms for siRNA recognition and slicer activity. EMBO J. 23: 4727-4737.
54. Parker, J.S., Roe, S.M., and Barford, D. 2005. Structural insights into mRNA recognition from a PIWI domain-siRNA guide complex. Nature 434: 663-666.
55. Pei, Y. and Tuschl, T. 2006. On the art of identifying effective and specific siRNAs. Na. Methods 3: 670-676.
56. Pelisson, A., Sarot, E., Payen-Groschene, G., and Bucheton, A. 2007. A novel repeat-associated small interfering RNA-mediated silencing pathway downregulates complementary sense gypsy transcripts in somatic cells of the Drosophila ovary. J. Virol. 81: 1951-1960.
57. Peters, L. and Meister, G. 2007. Argonaute proteins: Mediators of RNA silencing. Mol. Cell 26: 611-623.
58. Preall, J.B. and Sontheimer, E.J. 2005. RNAi: RISC gets loaded. Cell 123: 543-545.
59. Rajewsky, N. and Socci, N.D. 2004. Computational identification of microRNA targets. Dev. Biol. 267: 529-535.
60. Rand, T.A., Ginalski, K., Grishin, N.V., and Wang, X. 2004. Biochemical identification of Argonaute 2 as the sole protein required for RNA-induced silencing complex activity. Proc. Natl. Acad. Sci. 101: 14385-14389.
61. Rand, T.A., Petersen, S., Du, F., and Wang, X. 2005. Argonaute2 cleaves the anti-guide strand of siRNA during RISC activation. Cell 123: 621-629.
62. Rivas, F.V., Tolia, N.H., Song, J.J., Aragon, J.P., Liu, J., Hannon, G.J., and Joshua-Tor, L. 2005. Purified Argonaute2 and an siRNA form recombinant human RISC. Nat. Struct. Mol. Biol. 12: 340-349.
63. Robb, G.B. and Rana, T.M. 2007. RNA helicase A interacts with RISC in human cells and functions in RISC loading. Mol. Cell 26: 523-537.
64. Root, D.E., Hacohen, N., Hahn, W.C., Lander, E.S., and Sabatini, D.M. 2006. Genome-scale loss-of-function screening with a lentiviral RNAi library. Nat. Methods 3: 715-719.
65. Saito, K., Ishizuka, A., Siomi, H., and Siomi, M.C. 2005. Processing of pre-microRNAs by the Dicer-1-Loquacious complex in Drosophila cells. PLoS Biol. 3: e235. doi: 10.1371/journal.pbio.0030235.
66. Saito, K., Sakaguchi, Y., Suzuki, T., Siomi, H., and Siomi, M.C. 2007. Pimet, the Drosophila homolog of HEN1, mediates 2′-O-methylation of Piwi- interacting RNAs at their 39 ends. Genes & Dev. 21: 1603-1608.
67. Schwarz, D.S., Hutvágner, G., Du, T., Xu, Z., Aronin, N., and Zamore, P.D. 2003. Asymmetry in the assembly of the RNAi enzyme complex. Cell 115: 199-208.
68. Song, J.J. and Joshua-Tor, L. 2006. Argonaute and RNA - Getting into the groove. Curr. Opin. Struct. Biol. 16: 5-11.
69. Song, J.J., Liu, J., Tolia, N.H., Schneiderman, J., Smith, S.K., Martienssen, R.A., Hannon, G.J., and Joshua-Tor, L. 2003. The crystal structure of the Argonaute2 PAZ domain reveals an RNA binding motif in RNAi effector complexes. Nat. Struct. Biol. 10: 1026-1032.
70. Song, J.J., Smith, S.K., Hannon, G.J., and Joshua-Tor, L. 2004. Crystal structure of Argonaute and its implications for RISC slicer activity. Science 305: 1434-1437.
71. Stark, A., Brennecke, J., Russell, R.B., and Cohen, S.M. 2003. Identification of Drosophila microRNA targets. PLoS Biol. 1: 397-409. doi: 10.1371/journal.pbio.0000060.
72. Tomari, Y., Du, T., Haley, B., Schwarz, D.S., Bennett, R., Cook, H.A., Koppetsch, B.S., Theurkauf, W.E., and Zamore, P.D. 2004a. RISC assembly defects in the Drosophila RNAi mutant armitage. Cell 116: 831-841.
73. Tomari, Y., Matranga, C., Haley, B., Martinez, N., and Zamore, P.D. 2004b. A protein sensor for siRNA asymmetry. Science 306: 1377-1380.
74. Tomari, Y. and Zamore, P.D. 2005. Perspective: Machines for RNAi. Genes & Dev. 19: 517-529.
75. Tuschl, T., Zamore, P.D., Lehmann, R., Bartel, D.P., and Sharp, P.A. 1999. Targeted mRNA degradation by double-stranded RNA in vitro. Genes & Dev. 13: 3191-3197.
76. Vagin, V.V., Sigova, A., Li, C., Seitz, H., Gvozdev, V., and Zamore, P.D. 2006. A distinct small RNA pathway silences selfish genetic elements in the germline. Science 313: 320-324.
77. Weitzer, S. and Martinez, J. 2007. The human RNA kinase hClp1 is active on 3′ transfer RNA exons and short interfering RNAs. Nature 447: 222-226.
78. Wu, Z., Irizarry, R.A., Gentleman, R., Martinez-Murillo, F., and Spencer, F. 2004. A model-based background adjustment for oligonucleotide expression arrays. J. Am. Stat. Assoc. 99: 909-917.
79. Yan, K.S., Yan, S., Farooq, A., Han, A., Zeng, L., and Zhou, M.M. 2003. Structure and conserved RNA binding of the PAZ domain. Nature 426: 468-474.
80. Yu, B., Yang, Z., Li, J., Minakhina, S., Yang, M., Padgett, R.W., Steward, R., and Chen, X. 2005. Methylation as a crucial step in plant microRNA biogenesis. Science 307: 932-935.
81. Yuan, Y.R., Pei, Y., Ma, J.B., Kuryavyi, V., Zhadina, M., Meister, G., Chen, H.Y., Dauter, Z., Tuschl, T., and Patel, D.J. 2005. Crystal structure of A. aeolicus Argonaute, a site-specific DNA-guided endoribonuclease, provides insights into RISC-mediated mRNA cleavage. Mol. Cell 19: 405-419.
82. Yuan, Y.R., Pei, Y., Chen, H.Y., Tuschl, T., and Patel, D.J. 2006. A potential protein-RNA recognition event along the RISC-loading pathway from the structure of A. aeolicus Argonaute with externally bound siRNA. Structure 14: 1557-1565.