Phosphate and R2D2 Restrict the Substrate Specificity of Dicer-2, an ATP-Driven Ribonuclease

Molecular Cell

Volumn 42, Issue 2, 2011, Pages 172-184

  Cenik, Elif Sarinay ^a   Fukunaga, Ryuya ^a   Lu, Gang ^b   Dutcher, Robert ^b   Wang, Yeming ^b   Tanaka Hall, Traci M ^b   Zamore, Phillip D ^a  

^a UNIVERSITY OF MASSACHUSETTS MEDICAL SCHOOL   (United States)

^b NATIONAL INSTITUTE OF ENVIRONMENTAL HEALTH SCIENCES   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ADENOSINE DIPHOSPHATE; ADENOSINE TRIPHOSPHATE; BINDING PROTEIN; DICER; DICER 2; DOUBLE STRANDED RNA; MICRORNA; PHOSPHATE; R2D2 PROTEIN; RIBONUCLEASE III; RNA; SMALL INTERFERING RNA; UNCLASSIFIED DRUG;

AMINO TERMINAL SEQUENCE; ARTICLE; CARBOXY TERMINAL SEQUENCE; PROTEIN CLEAVAGE; PROTEIN HYDROLYSIS; PROTEIN PURIFICATION; RNA CLEAVAGE;

ADENOSINE DIPHOSPHATE; ADENOSINE TRIPHOSPHATE; ANIMALS; DROSOPHILA MELANOGASTER; DROSOPHILA PROTEINS; HYDROLYSIS; KINETICS; MICRORNAS; MODELS, BIOLOGICAL; PHOSPHATES; RIBONUCLEASE III; RNA HELICASES; RNA PROCESSING, POST-TRANSCRIPTIONAL; RNA, DOUBLE-STRANDED; RNA, SMALL INTERFERING; RNA-BINDING PROTEINS; SUBSTRATE SPECIFICITY;

EID: 79954630841     PISSN: 10972765     EISSN: 10974164     Source Type: Journal    
DOI: 10.1016/j.molcel.2011.03.002     Document Type: Article

References (73)

1. 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 2011, 17:54-63.
2. Auesukaree C., Homma T., Tochio H., Shirakawa M., Kaneko Y., Harashima S. Intracellular phosphate serves as a signal for the regulation of the PHO pathway in Saccharomyces cerevisiae. J. Biol. Chem. 2004, 279:17289-17294.
3. Bass B.L. Double-stranded RNA as a template for gene silencing. Cell 2000, 101:235-238.
4. Beran R.K., Bruno M.M., Bowers H.A., Jankowsky E., Pyle A.M. Robust translocation along a molecular monorail: the NS3 helicase from hepatitis C virus traverses unusually large disruptions in its track. J. Mol. Biol. 2006, 358:974-982.
5. Bernstein E., Caudy A.A., Hammond S.M., Hannon G.J. Role for a bidentate ribonuclease in the initiation step of RNA interference. Nature 2001, 409:363-366.
6. Bianco P.R., Kowalczykowski S.C. Translocation step size and mechanism of the RecBC DNA helicase. Nature 2000, 405:368-372.
7. Bowers H.A., Maroney P.A., Fairman M.E., Kastner B., Lührmann R., Nilsen T.W., Jankowsky E. Discriminatory RNP remodeling by the DEAD-box protein DED1. RNA 2006, 12:903-912.
8. Burt C.T., Glonek T., Bárány M. Analysis of phosphate metabolites, the intracellular pH, and the state of adenosine triphosphate in intact muscle by phosphorus nuclear magnetic resonance. J. Biol. Chem. 1976, 251:2584-2591.
9. Cerutti L., Mian N., Bateman A. Domains in gene silencing and cell differentiation proteins: the novel PAZ domain and redefinition of the Piwi domain. Trends Biochem. Sci. 2000, 25:481-482.
10. Chakravarthy S., Sternberg S.H., Kellenberger C.A., Doudna J.A. Substrate-specific kinetics of Dicer-catalyzed RNA processing. J. Mol. Biol. 2010, 404:392-402.
11. 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 2007, 27:449-461.
12. Czech B., Malone C.D., Zhou R., Stark A., Schlingeheyde C., Dus M., Perrimon N., Kellis M., Wohlschlegel J.A., Sachidanandam R., et al. An endogenous small interfering RNA pathway in Drosophila. Nature 2008, 453:798-802.
13. Denli A.M., Tops B.B., Plasterk R.H., Ketting R.F., Hannon G.J. Processing of primary microRNAs by the Microprocessor complex. Nature 2004, 432:231-235.
14. Dumont S., Cheng W., Serebrov V., Beran R.K., Tinoco I.J., Pyle A.M., Bustamante C. RNA translocation and unwinding mechanism of HCV NS3 helicase and its coordination by ATP. Nature 2006, 439:105-108.
15. Erecińska M., Stubbs M., Miyata Y., Ditre C.M. Regulation of cellular metabolism by intracellular phosphate. Biochim. Biophys. Acta 1977, 462:20-35.
16. Förstemann K., Horwich M.D., Wee L., Tomari Y., Zamore P.D. Drosophila microRNAs are sorted into functionally distinct argonaute complexes after production by dicer-1. Cell 2007, 130:287-297.
17. 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.
18. Franks T.M., Singh G., Lykke-Andersen J. Upf1 ATPase-dependent mRNP disassembly is required for completion of nonsense- mediated mRNA decay. Cell 2010, 143:938-950.
19. Gan J., Tropea J.E., Austin B.P., Court D.L., Waugh D.S., Ji X. Structural insight into the mechanism of double-stranded RNA processing by ribonuclease III. Cell 2006, 124:355-366.
20. Ghildiyal M., Seitz H., Horwich M.D., Li C., Du T., Lee S., Xu J., Kittler E.L., Zapp M.L., Weng Z., Zamore P.D. Endogenous siRNAs derived from transposons and mRNAs in Drosophila somatic cells. Science 2008, 320:1077-1081.
21. 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.
22. Haley B., Tang G., Zamore P.D. In vitro analysis of RNA interference in Drosophila melanogaster. Methods 2003, 30:330-336.
23. Halls C., Mohr S., Del Campo M., Yang Q., Jankowsky E., Lambowitz A.M. Involvement of DEAD-box proteins in group I and group II intron splicing. Biochemical characterization of Mss116p, ATP hydrolysis-dependent and -independent mechanisms, and general RNA chaperone activity. J. Mol. Biol. 2007, 365:835-855.
24. 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.
25. 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.
26. Hartig J.V., Esslinger S., Böttcher R., Saito K., Förstemann K. Endo-siRNAs depend on a new isoform of loquacious and target artificially introduced, high-copy sequences. EMBO J. 2009, 28:2932-2944.
27. Hartig J.V., Förstemann K. Loqs-PD and R2D2 define independent pathways for RISC generation in Drosophila. Nucleic Acids Res 2011, Published online January 17, 2011.
28. 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.
29. 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.
30. Ketting R.F., Fischer S.E., Bernstein E., Sijen T., Hannon G.J., Plasterk R.H. Dicer functions in RNA interference and in synthesis of small RNA involved in developmental timing in C. elegans. Genes Dev. 2001, 15:2654-2659.
31. Kini H.K., Walton S.P. In vitro binding of single-stranded RNA by human Dicer. FEBS Lett. 2007, 581:5611-5616.
32. 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.
33. 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.
34. Lingel A., Simon B., Izaurralde E., Sattler M. Structure and nucleic-acid binding of the Drosophila Argonaute 2 PAZ domain. Nature 2003, 426:465-469.
35. Lingel A., Simon B., Izaurralde E., Sattler M. Nucleic acid 3′-end recognition by the Argonaute2 PAZ domain. Nat. Struct. Mol. Biol. 2004, 11:576-577.
36. 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.
37. 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 2006, 12:1514-1520.
38. Lu W.P., Fei L. A logarithmic approximation to initial rates of enzyme reactions. Anal. Biochem. 2003, 316:58-65.
39. Ma E., MacRae I.J., Kirsch J.F., Doudna J.A. Autoinhibition of human dicer by its internal helicase domain. J. Mol. Biol. 2008, 380:237-243.
40. Ma J.B., Ye K., Patel D.J. Structural basis for overhang-specific small interfering RNA recognition by the PAZ domain. Nature 2004, 429:318-322.
41. MacRae I.J., Zhou K., Doudna J.A. Structural determinants of RNA recognition and cleavage by Dicer. Nat. Struct. Mol. Biol. 2007, 14:934-940.
42. Macrae I.J., Zhou K., Li F., Repic A., Brooks A.N., Cande W.Z., Adams P.D., Doudna J.A. Structural basis for double-stranded RNA processing by Dicer. Science 2006, 311:195-198.
43. Matranga C., Pyle A.M. The double stranded RNA-dependent ATPase DRH-3: insight into its role in RNA silencing in Caenorhabditis elegans. J. Biol. Chem. 2010, 285:25363-25371.
44. Miyoshi K., Miyoshi T., Hartig J.V., Siomi H., Siomi M.C. Molecular mechanisms that funnel RNA precursors into endogenous small-interfering RNA and microRNA biogenesis pathways in Drosophila. RNA 2010, 16:506-515.
45. Moore M.J., Query C.C. Joining of RNAs by splinted ligation. Methods Enzymol. 2000, 317:109-123.
46. Moore M.J., Sharp P.A. Evidence for two active sites in the spliceosome provided by stereochemistry of pre-mRNA splicing. Nature 1993, 365:364-368.
47. Myong S., Cui S., Cornish P.V., Kirchhofer A., Gack M.U., Jung J.U., Hopfner K.P., Ha T. Cytosolic viral sensor RIG-I is a 5′-triphosphate-dependent translocase on double-stranded RNA. Science 2009, 323:1070-1074.
48. Nakamura M., Ando R., Nakazawa T., Yudazono T., Tsutsumi N., Hatanaka N., Ohgake T., Hanaoka F., Eki T. Dicer-related drh-3 gene functions in germ-line development by maintenance of chromosomal integrity in Caenorhabditis elegans. Genes Cells 2007, 12:997-1010.
49. Nykänen A., Haley B., Zamore P.D. ATP requirements and small interfering RNA structure in the RNA interference pathway. Cell 2001, 107:309-321.
50. Okamura K., Balla S., Martin R., Liu N., Lai E.C. Two distinct mechanisms generate endogenous siRNAs from bidirectional transcription in Drosophila melanogaster. Nat. Struct. Mol. Biol. 2008, 15:581-590.
51. Okamura K., Chung W.J., Ruby J.G., Guo H., Bartel D.P., Lai E.C. The Drosophila hairpin RNA pathway generates endogenous short interfering RNAs. Nature 2008, 453:803-806.
52. Patel S.S., Donmez I. Mechanisms of helicases. J. Biol. Chem. 2006, 281:18265-18268.
53. 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.
54. 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.
55. Pyle A.M. Translocation and unwinding mechanisms of RNA and DNA helicases. Annu. Rev. Biophys. 2008, 37:317-336.
56. Rivera M.A., Blackburn E.H. Processive utilization of the human telomerase template: lack of a requirement for template switching. J. Biol. Chem. 2004, 279:53770-53781.
57. Rose S.D., Kim D.H., Amarzguioui M., Heidel J.D., Collingwood M.A., Davis M.E., Rossi J.J., Behlke M.A. Functional polarity is introduced by Dicer processing of short substrate RNAs. Nucleic Acids Res. 2005, 33:4140-4156.
58. 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.
59. Seidel R., Bloom J.G., Dekker C., Szczelkun M.D. Motor step size and ATP coupling efficiency of the dsDNA translocase EcoR124I. EMBO J. 2008, 27:1388-1398.
60. Song J.J., Liu J., Tolia N.H., Schneiderman J., Smith S.K., Martienssen R.A., Hannon G.J., Joshua-Tor L. The crystal structure of the Argonaute2 PAZ domain reveals an RNA binding motif in RNAi effector complexes. Nat. Struct. Biol. 2003, 10:1026-1032.
61. Takeshita D., Zenno S., Lee W.C., Nagata K., Saigo K., Tanokura M. Homodimeric structure and double-stranded RNA cleavage activity of the C-terminal RNase III domain of human dicer. J. Mol. Biol. 2007, 374:106-120.
62. Tam O.H., Aravin A.A., Stein P., Girard A., Murchison E.P., Cheloufi S., Hodges E., Anger M., Sachidanandam R., Schultz R.M., Hannon G.J. Pseudogene-derived small interfering RNAs regulate gene expression in mouse oocytes. Nature 2008, 453:534-538.
63. Tomari Y., Du T., Zamore P.D. Sorting of Drosophila small silencing RNAs. Cell 2007, 130:299-308.
64. Tomari Y., Matranga C., Haley B., Martinez N., Zamore P.D. A protein sensor for siRNA asymmetry. Science 2004, 306:1377-1380.
65. Watanabe T., Totoki Y., Toyoda A., Kaneda M., Kuramochi-Miyagawa S., Obata Y., Chiba H., Kohara Y., Kono T., Nakano T., et al. Endogenous siRNAs from naturally formed dsRNAs regulate transcripts in mouse oocytes. Nature 2008, 453:539-543.
66. Welker N.C., Pavelec D.M., Nix D.A., Duchaine T.F., Kennedy S., Bass B.L. Dicer's helicase domain is required for accumulation of some, but not all, C. elegans endogenous siRNAs. RNA 2010, 16:893-903.
67. Yan K.S., Yan S., Farooq A., Han A., Zeng L., Zhou M.M. Structure and conserved RNA binding of the PAZ domain. Nature 2003, 426:468-474.
68. Yang N., Kazazian H.H.J. L1 retrotransposition is suppressed by endogenously encoded small interfering RNAs in human cultured cells. Nat. Struct. Mol. Biol. 2006, 13:763-771.
69. Ye X., Paroo Z., Liu Q. Functional anatomy of the Drosophila microRNA-generating enzyme. J. Biol. Chem. 2007, 282:28373-28378.
70. Zamore P.D., Tuschl T., Sharp P.A., Bartel D.P. RNAi: double-stranded RNA directs the ATP-dependent cleavage of mRNA at 21 to 23 nucleotide intervals. Cell 2000, 101:25-33.
71. 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.
72. Zhang H., Kolb F.A., Jaskiewicz L., Westhof E., Filipowicz W. Single processing center models for human Dicer and bacterial RNase III. Cell 2004, 118:57-68.
73. Zhou R., Czech B., Brennecke J., Sachidanandam R., Wohlschlegel J.A., Perrimon N., Hannon G.J. Processing of Drosophila endo-siRNAs depends on a specific Loquacious isoform. RNA 2009, 15:1886-1895.