Drosophila microRNAs Are Sorted into Functionally Distinct Argonaute Complexes after Production by Dicer-1

Cell

Volumn 130, Issue 2, 2007, Pages 287-297

  Förstemann, Klaus ^a   Horwich, Michael D ^b   Wee, LiangMeng ^b   Tomari, Yukihide ^b,c   Zamore, Phillip D ^b  

^a UNIVERSITY OF MUNICH   (Germany)

^b UNIVERSITY OF MASSACHUSETTS MEDICAL SCHOOL   (United States)

^c UNIVERSITY OF TOKYO   (Japan)

Author keywords

PROTEINS; RNA

Indexed keywords

ARGONAUTE 1; ARGONAUTE 2; DICER 1; DOUBLE STRANDED RNA; MICRORNA; NUCLEASE; RNA BINDING PROTEIN; SMALL INTERFERING RNA; UNCLASSIFIED DRUG;

ANIMAL CELL; ARTICLE; BINDING SITE; BIOGENESIS; COMPLEX FORMATION; DISSOCIATION; DROSOPHILA MELANOGASTER; ENZYME MECHANISM; GENE EXPRESSION; GENE REPRESSION; NONHUMAN; PRIORITY JOURNAL; PROTEIN RNA BINDING; PROTEIN TARGETING; RNA INTERFERENCE;

EID: 34447291764     PISSN: 00928674     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.cell.2007.05.056     Document Type: Article

References (83)

1. Ashraf S.I., McLoon A.L., Sclarsic S.M., and Kunes S. Synaptic protein synthesis associated with memory is regulated by the RISC pathway in Drosophila. Cell 124 (2006) 191-205
2. Aza-Blanc P., Cooper C.L., Wagner K., Batalov S., Deveraux Q.L., and Cooke M.P. Identification of modulators of TRAIL-induced apoptosis via RNAi-based phenotypic screening. Mol. Cell 12 (2003) 627-637
3. Bartel D.P. MicroRNAs: Genomics, biogenesis, mechanism, and function. Cell 116 (2004) 281-297
4. Baumberger N., and Baulcombe D.C. Arabidopsis ARGONAUTE1 is an RNA slicer that selectively recruits microRNAs and short interfering RNAs. Proc. Natl. Acad. Sci. USA 102 (2005) 11928-11933
5. Bernstein E., Caudy A.A., Hammond S.M., and Hannon G.J. Role for a bidentate ribonuclease in the initiation step of RNA interference. Nature 409 (2001) 363-366
6. Bernstein E., Kim S.Y., Carmell M.A., Murchison E.P., Alcorn H., Li M.Z., Mills A.A., Elledge S.J., Anderson K.V., and Hannon G.J. Dicer is essential for mouse development. Nat. Genet. 35 (2003) 215-217
7. Brennecke J., Stark A., Russell R.B., and Cohen S.M. Principles of microRNA-target recognition. PLoS Biol. 3 (2005) e85
8. Brennecke J., Aravin A.A., Stark A., Dus M., Kellis M., Sachidanandam R., and Hannon G.J. Discrete small RNA-generating loci as master regulators of transposon activity in Drosophila. Cell 128 (2007) 1089-1103
9. Davis E., Caiment F., Tordoir X., Cavaille J., Ferguson-Smith A., Cockett N., Georges M., and Charlier C. RNAi-mediated allelic trans-interaction at the imprinted Rtl1/Peg11 locus. Curr. Biol. 15 (2005) 743-749
10. Doench J.G., Petersen C.P., and Sharp P.A. siRNAs can function as miRNAs. Genes Dev. 17 (2003) 438-442
11. Du T., and Zamore P.D. microPrimer: the biogenesis and function of microRNA. Development 132 (2005) 4645-4652
12. Filipowicz W. RNAi: the nuts and bolts of the RISC machine. Cell 122 (2005) 17-20
13. Forstemann K., Tomari Y., Du T., Vagin V.V., Denli A.M., Bratu D.P., Klattenhoff C., Theurkauf W.E., and Zamore P.D. Normal microRNA maturation and germ-line stem cell maintenance requires Loquacious, a double-stranded RNA-binding domain protein. PLoS Biol. 3 (2005) e236
14. Galiana-Arnoux D., Dostert C., Schneemann A., Hoffmann J.A., and Imler J.L. Essential function in vivo for Dicer-2 in host defense against RNA viruses in drosophila. Nat. Immunol. 7 (2006) 590-597
15. Grishok A., Pasquinelli A.E., Conte D., Li N., Parrish S., Ha I., Baillie D.L., Fire A., Ruvkun G., and Mello C.C. Genes and mechanisms related to RNA interference regulate expression of the small temporal RNAs that control C. elegans developmental timing. Cell 106 (2001) 23-34
16. Gunawardane L.S., Saito K., Nishida K.M., Miyoshi K., Kawamura Y., Nagami T., Siomi H., and Siomi M.C. A slicer-mediated mechanism for repeat-associated siRNA 5′ end formation in Drosophila. Science 315 (2007) 1587-1590
17. Haley B., and Zamore P.D. Kinetic analysis of the RNAi enzyme complex. Nat. Struct. Mol. Biol. 11 (2004) 599-606
18. Haley B., Tang G., and Zamore P.D. In vitro analysis of RNA interference in Drosophila melanogaster. Methods 30 (2003) 330-336
19. Hammond S.M., Boettcher S., Caudy A.A., Kobayashi R., and Hannon G.J. Argonaute2, a link between genetic and biochemical analyses of RNAi. Science 293 (2001) 1146-1150
20. Han J., Lee Y., Yeom K.H., Nam J.W., Heo I., Rhee J.K., Sohn S.Y., Cho Y., Zhang B.T., and Kim V.N. Molecular basis for the recognition of primary microRNAs by the Drosha-DGCR8 complex. Cell 125 (2006) 887-901
21. Harfe B.D., McManus M.T., Mansfield J.H., Hornstein E., and Tabin C.J. The RNaseIII enzyme Dicer is required for morphogenesis but not patterning of the vertebrate limb. Proc. Natl. Acad. Sci. USA 102 (2005) 10898-10903
22. Hutvágner G., and Zamore P.D. A microRNA in a multiple-turnover RNAi enzyme complex. Science 297 (2002) 2056-2060
23. Hutvágner G., McLachlan J., Pasquinelli A.E., Balint E., Tuschl T., and Zamore P.D. A cellular function for the RNA-interference enzyme Dicer in the maturation of the let-7 small temporal RNA. Science 293 (2001) 834-838
24. Jackson A.L., Bartz S.R., Schelter J., Kobayashi S.V., Burchard J., Mao M., Li B., Cavet G., and Linsley P.S. Expression profiling reveals off-target gene regulation by RNAi. Nat. Biotechnol. 21 (2003) 635-637
25. Jackson A.L., Burchard J., Schelter J., Chau B.N., Cleary M., Lim L., and Linsley P.S. Widespread siRNA "off-target" transcript silencing mediated by seed region sequence complementarity. RNA 12 (2006) 1179-1187
26. Jiang F., Ye X., Liu X., Fincher L., McKearin D., and Liu Q. Dicer-1 and R3D1-L catalyze microRNA maturation in Drosophila. Genes Dev. 19 (2005) 1674-1679
27. Kanellopoulou C., Muljo S.A., Kung A.L., Ganesan S., Drapkin R., Jenuwein T., Livingston D.M., and Rajewsky K. Dicer-deficient mouse embryonic stem cells are defective in differentiation and centromeric silencing. Genes Dev. 19 (2005) 489-501
28. Ketting R.F., Fischer S.E., Bernstein E., Sijen T., Hannon G.J., and Plasterk R.H. Dicer functions in RNA interference and in synthesis of small RNA involved in developmental timing in C. elegans. Genes Dev. 15 (2001) 2654-2659
29. Khvorova A., Reynolds A., and Jayasena S.D. Functional siRNAs and miRNAs exhibit strand bias. Cell 115 (2003) 209-216
30. Krek A., Grun D., Poy M.N., Wolf R., Rosenberg L., Epstein E.J., MacMenamin P., da Piedade I., Gunsalus K.C., Stoffel M., and Rajewsky N. Combinatorial microRNA target predictions. Nat. Genet. 37 (2005) 495-500
31. Lai E.C. Micro RNAs are complementary to 3′ UTR sequence motifs that mediate negative post-transcriptional regulation. Nat. Genet. 30 (2002) 363-364
32. Lecellier C.H., Dunoyer P., Arar K., Lehmann-Che J., Eyquem S., Himber C., Saib A., and Voinnet O. A cellular microRNA mediates antiviral defense in human cells. Science 308 (2005) 557-560
33. Lee R.C., Feinbaum R.L., and Ambros V. The C. elegans heterochronic gene lin-4 encodes small RNAs with antisense complementarity to lin-14. Cell 75 (1993) 843-854
34. Lee Y., Ahn C., Han J., Choi H., Kim J., Yim J., Lee J., Provost P., Radmark O., Kim S., and Kim V.N. The nuclear RNase III Drosha initiates microRNA processing. Nature 425 (2003) 415-419
35. Lee Y.S., Nakahara K., Pham J.W., Kim K., He Z., Sontheimer E.J., and Carthew R.W. Distinct roles for Drosophila Dicer-1 and Dicer-2 in the siRNA/miRNA silencing pathways. Cell 117 (2004) 69-81
36. Leuschner P.J., Ameres S.L., Kueng S., and Martinez J. Cleavage of the siRNA passenger strand during RISC assembly in human cells. EMBO Rep. 7 (2006) 314-320
37. Lewis B.P., Burge C.B., and Bartel D.P. Conserved seed pairing, often flanked by adenosines, indicates that thousands of human genes are microRNA targets. Cell 120 (2005) 15-20
38. Lewis B.P., Shih I.H., Jones-Rhoades M.W., Bartel D.P., and Burge C.B. Prediction of mammalian microRNA targets. Cell 115 (2003) 787-798
39. Li X., and Carthew R.W. A microRNA mediates EGF receptor signaling and promotes photoreceptor differentiation in the Drosophila eye. Cell 123 (2005) 1267-1277
40. 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. Microarray analysis shows that some microRNAs downregulate large numbers of target mRNAs. Nature 433 (2005) 769-773
41. Lingel A., Simon B., Izaurralde E., and Sattler M. Structure and nucleic-acid binding of the Drosophila Argonaute 2 PAZ domain. Nature 426 (2003) 465-469
42. Liu Q., Rand T.A., Kalidas S., Du F., Kim H.E., Smith D.P., and Wang X. R2D2, a bridge between the initiation and effector steps of the Drosophila RNAi pathway. Science 301 (2003) 1921-1925
43. 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. Argonaute2 is the catalytic engine of mammalian RNAi. Science 305 (2004) 1437-1441
44. Liu X., Jiang F., Kalidas S., Smith D., and Liu Q. Dicer-2 and R2D2 coordinately bind siRNA to promote assembly of the siRISC complexes. RNA 12 (2006) 1514-1520
45. Ma J.B., Ye K., and Patel D.J. Structural basis for overhang-specific small interfering RNA recognition by the PAZ domain. Nature 429 (2004) 318-322
46. Ma J.B., Yuan Y.R., Meister G., Pei Y., Tuschl T., and Patel D.J. Structural basis for 5′-end-specific recognition of guide RNA by the A. fulgidus Piwi protein. Nature 434 (2005) 666-670
47. Mansfield J.H., Harfe B.D., Nissen R., Obenauer J., Srineel J., Chaudhuri A., Farzan-Kashani R., Zuker M., Pasquinelli A.E., Ruvkun G., et al. MicroRNA-responsive 'sensor' transgenes uncover Hox-like and other developmentally regulated patterns of vertebrate microRNA expression. Nat. Genet. 36 (2004) 1079-1083
48. Matranga C., Tomari Y., Shin C., Bartel D.P., and Zamore P.D. Passenger-strand cleavage facilitates assembly of siRNA into Ago2-containing RNAi enzyme complexes. Cell 123 (2005) 607-620
49. Meister G., Landthaler M., Patkaniowska A., Dorsett Y., Teng G., and Tuschl T. Human Argonaute2 mediates RNA cleavage targeted by miRNAs and siRNAs. Mol. Cell 15 (2004) 185-197
50. Miyoshi K., Tsukumo H., Nagami T., Siomi H., and Siomi M.C. Slicer function of Drosophila Argonautes and its involvement in RISC formation. Genes Dev. 19 (2005) 2837-2848
51. Nykanen A., Haley B., and Zamore P.D. ATP requirements and small interfering RNA structure in the RNA interference pathway. Cell 107 (2001) 309-321
52. Okamura K., Ishizuka A., Siomi H., and Siomi M.C. Distinct roles for Argonaute proteins in small RNA-directed RNA cleavage pathways. Genes Dev. 18 (2004) 1655-1666
53. Parker J.S., Roe S.M., and Barford D. Crystal structure of a PIWI protein suggests mechanisms for siRNA recognition and slicer activity. EMBO J. 23 (2004) 4727-4737
54. Parker J.S., Roe S.M., and Barford D. Structural insights into mRNA recognition from a PIWI domain-siRNA guide complex. Nature 434 (2005) 663-666
55. Pham J.W., Pellino J.L., Lee Y.S., Carthew R.W., and Sontheimer E.J. A Dicer-2-dependent 80s complex cleaves targeted mRNAs during RNAi in Drosophila. Cell 117 (2004) 83-94
56. Poy M.N., Eliasson L., Krutzfeldt J., Kuwajima S., Ma X., Macdonald P.E., Pfeffer S., Tuschl T., Rajewsky N., Rorsman P., and Stoffel M. A pancreatic islet-specific microRNA regulates insulin secretion. Nature 432 (2004) 226-230
57. Preall J.B., He Z., Gorra J.M., and Sontheimer E.J. Short interfering RNA strand selection is independent of dsRNA processing polarity during RNAi in Drosophila. Curr. Biol. 16 (2006) 530-535
58. Qi Y., Denli A.M., and Hannon G.J. Biochemical specialization within Arabidopsis RNA silencing pathways. Mol. Cell 19 (2005) 421-428
59. Rajewsky N., and Socci N.D. Computational identification of microRNA targets. Dev. Biol. 267 (2004) 529-535
60. Rand T.A., Ginalski K., Grishin N.V., and Wang X. Biochemical identification of Argonaute 2 as the sole protein required for RNA-induced silencing complex activity. Proc. Natl. Acad. Sci. USA 101 (2004) 14385-14389
61. Rand T.A., Petersen S., Du F., and Wang X. Argonaute2 cleaves the anti-guide strand of siRNA during RISC activation. Cell 123 (2005) 621-629
62. Reinhart B.J., Slack F.J., Basson M., Pasquinelli A.E., Bettinger J.C., Rougvie A.E., Horvitz H.R., and Ruvkun G. The 21-nucleotide let-7 RNA regulates developmental timing in Caenorhabditis elegans. Nature 403 (2000) 901-906
63. Rivas F.V., Tolia N.H., Song J.J., Aragon J.P., Liu J., Hannon G.J., and Joshua-Tor L. Purified Argonaute2 and an siRNA form recombinant human RISC. Nat. Struct. Mol. Biol. 12 (2005) 340-349
64. Saito K., Ishizuka A., Siomi H., and Siomi M.C. Processing of pre-microRNAs by the Dicer-1-Loquacious complex in Drosophila cells. PLoS Biol. 3 (2005) e235
65. Saito K., Nishida K.M., Mori T., Kawamura Y., Miyoshi K., Nagami T., Siomi H., and 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
66. Schratt G.M., Tuebing F., Nigh E.A., Kane C.G., Sabatini M.E., Kiebler M., and Greenberg M.E. A brain-specific microRNA regulates dendritic spine development. Nature 439 (2006) 283-289
67. Schwarz D.S., Hutvágner G., Du T., Xu Z., Aronin N., and Zamore P.D. Asymmetry in the assembly of the RNAi enzyme complex. Cell 115 (2003) 199-208
68. Song J.J., Liu J., Tolia N.H., Schneiderman J., Smith S.K., Martienssen R.A., Hannon G.J., and Joshua-Tor L. The crystal structure of the Argonaute2 PAZ domain reveals an RNA binding motif in RNAi effector complexes. Nat. Struct. Biol. 10 (2003) 1026-1032
69. Song J.J., Smith S.K., Hannon G.J., and Joshua-Tor L. Crystal structure of Argonaute and its implications for RISC slicer activity. Science 305 (2004) 1434-1437
70. Stark A., Brennecke J., Russel R.B., and Cohen S.M. Identification of Drosophila microRNA targets. PLoS Biol. 1 (2003) 1-13
71. Steller H., and Pirrotta V. A transposable P vector that confers selectable G418 resistance to Drosophila larvae. EMBO J. 4 (1985) 167-171
72. Tabara H., Sarkissian M., Kelly W.G., Fleenor J., Grishok A., Timmons L., Fire A., and Mello C.C. The rde-1 gene, RNA interference, and transposon silencing in C. elegans. Cell 99 (1999) 123-132
73. Teleman A.A., Maitra S., and Cohen S.M. Drosophila lacking microRNA miR-278 are defective in energy homeostasis. Genes Dev. 20 (2006) 417-422
74. Tomari Y., and Zamore P.D. Perspective: machines for RNAi. Genes Dev. 19 (2005) 517-529
75. Tomari Y., Matranga C., Haley B., Martinez N., and Zamore P.D. A protein sensor for siRNA asymmetry. Science 306 (2004) 1377-1380
76. Tomari Y., Du T., Haley B., Schwarz D.S., Bennett R., Cook H.A., Koppetsch B.S., Theurkauf W.E., and Zamore P.D. RISC assembly defects in the Drosophila RNAi mutant armitage. Cell 116 (2004) 831-841
77. Tomari Y., Du T., and Zamore P.D. Sorting of Drosophila small silencing RNAs. Cell 130 (2007) 299-308 this issue
78. Vagin V.V., Sigova A., Li C., Seitz H., Gvozdev V., and Zamore P.D. A distinct small RNA pathway silences selfish genetic elements in the germline. Science 313 (2006) 320-324
79. Wang X.H., Aliyari R., Li W.X., Li H.W., Kim K., Carthew R., Atkinson P., and Ding S.W. RNA interference directs innate immunity against viruses in adult Drosophila. Science 312 (2006) 452-454
80. Yan K.S., Yan S., Farooq A., Han A., Zeng L., and Zhou M.M. Structure and conserved RNA binding of the PAZ domain. Nature 426 (2003) 468-474
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. 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
82. Yekta S., Shih I.H., and Bartel D.P. MicroRNA-directed cleavage of HOXB8 mRNA. Science 304 (2004) 594-596
83. Zeng Y., Wagner E.J., and Cullen B.R. Technique: Both natural and designed micro RNAs can inhibit the expression of cognate mRNAs when expressed in human cells. Mol. Cell 9 (2002) 1327-1333