Multiple sensors ensure guide strand selection in human RNAi pathways

RNA

Volumn 19, Issue 5, 2013, Pages 639-648

  Noland, Cameron L ^a   Doudna, Jennifer A ^a,b  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b LAWRENCE BERKELEY NATIONAL LABORATORY   (United States)

Author keywords

Dicer; PACT; RISC; RNAi; Strand selection; TRBP

Indexed keywords

ARGONAUTE 2 PROTEIN; DICER; DOUBLE STRANDED RNA BINDING PROTEIN; MICRORNA; PROTEIN; PROTEIN ACTIVATOR OF PKR; RNA BINDING PROTEIN; RNA INDUCED SILENCING COMPLEX; SMALL INTERFERING RNA; UNCLASSIFIED DRUG;

5' UNTRANSLATED REGION; ARTICLE; COMPLEX FORMATION; GENE TARGETING; HUMAN; PRIORITY JOURNAL; PROTEIN BINDING; RNA INTERFERENCE; THERMODYNAMICS; TRANSACTIVATION;

ARGONAUTE PROTEINS; CARBOXYPEPTIDASES; DEAD-BOX RNA HELICASES; GENE EXPRESSION REGULATION; GENE SILENCING; HUMANS; MICRORNAS; NUCLEAR RECEPTOR COACTIVATORS; PROTEIN BINDING; RIBONUCLEASE III; RNA INTERFERENCE; RNA, DOUBLE-STRANDED; RNA, SMALL INTERFERING; RNA-BINDING PROTEINS;

EUKARYOTA;

EID: 84876591872     PISSN: 13558382     EISSN: 14699001     Source Type: Journal    
DOI: 10.1261/rna.037424.112     Document Type: Article

References (59)

1. Bernstein E, Caudy AA, Hammond SM, Hannon GJ. 2001. Role for a bidentate ribonuclease in the initiation step of RNA interference. Nature 409: 363-366. (Pubitemid 32151243)
2. Betancur JG, Tomari Y. 2012. Dicer is dispensable for asymmetric RISC loading in mammals. RNA 18: 24-30.
3. Borer PN, Dengler B, Tinoco I, Uhlenbeck OC. 1974. Stability of ribo-nucleic acid double-stranded helices. J Mol Biol 86: 843-853.
4. Chakravarthy S, Sternberg SH, Kellenberger CA, Doudna JA. 2010. Substrate-specific Kinetics of Dicer-catalyzed RNA Processing. J Mol Biol 404: 392-402.
5. Chendrimada TP, Gregory RI, Kumaraswamy E, Norman J, Cooch N, Nishikura K, Shiekhattar R. 2005. TRBP recruits the Dicer complex to Ago2 for microRNA processing and gene silencing. Nature 436: 740-744. (Pubitemid 41117280)
6. Czech B, Zhou R, Erlich Y, Brennecke J, Binari R, Villalta C, Gordon A, Perrimon N, Hannon GJ. 2009. Hierarchical rules for Argonaute loading in Drosophila. Mol Cell 36: 445-456.
7. Dueck A, Ziegler C, Eichner A, Berezikov E, Meister G. 2012. MicroRNAs Associated with the Different Human Argonaute Proteins. Nucleic Acids Res 40: 9850-9862.
8. Elbashir SM, Harborth J, Lendeckel W, Yalcin A, Weber K, Tuschl T. 2001a. Duplexes of 21-nucleotide RNAs mediate RNA interference in cultured mammalian cells. Nature 411: 494-498. (Pubitemid 32494397)
9. Elbashir SM, Lendeckel W, Tuschl T. 2001b. RNA interference is mediated by 21-and 22-nucleotide RNAs. Genes Dev 15: 188-200. (Pubitemid 32107664)
10. Elkayam E, Kuhn C-D, Tocilj A, Haase AD, Greene EM, Hannon GJ, Joshua-Tor L. 2012. The structure of human argonaute-2 in complex with miR-20a. Cell 150: 100-110.
11. ′-nucleotide base-specific recognition of guide RNA by human AGO2. Nature 465: 818-822.
12. Freier SM, Kierzek R, Jaeger JA, Sugimoto N, Caruthers MH, Neilson T, Turner DH. 1986. Improved free-energy parameters for predictions of RNA duplex stability. Proc Natl Acad Sci 83: 9373-9377. (Pubitemid 17223363)
13. Haase AD, Jaskiewicz L, Zhang H, Lainé S, Sack R, Gatignol A, 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. (Pubitemid 41521952)
14. Haley B, Zamore PD. 2004. Kinetic analysis of the RNAi enzyme complex. Nat Struct Mol Biol 11: 599-606. (Pubitemid 38823525)
15. Hu HY, Yan Z, Xu Y, Hu H, Menzel C, Zhou YH, Chen W, Khaitovich P. 2009. Sequence features associated with microRNA strand selection in humans and flies. BMC Genomics 10: 413.
16. Hutvagner G, McLachlan J, Pasquinelli AE, Balint E, Tuschl T, Zamore PD. 2001. A cellular function for the RNA-interference enzyme Dicer in the maturation of the let-7 small temporal RNA. Science 293: 834-838. (Pubitemid 32743968)
17. Iki T, Yoshikawa M, Nishikiori M, Jaudal MC, Matsumoto-Yokoyama E, Mitsuhara I, Meshi T, Ishikawa M. 2010. In vitro assembly of plant RNA-induced silencing complexes facilitated by molecular chaper-one HSP90. Mol Cell 39: 282-291.
18. Iwasaki S, Kobayashi M, Yoda M, Sakaguchi Y, Katsuma S, Suzuki T, Tomari Y. 2010. Hsc70/Hsp90 chaperone machinery mediates ATP-dependent RISC loading of small RNA duplexes. Mol Cell 39: 292-299.
19. Jinek M, Doudna JA. 2009. A three-dimensional view of the molecular machinery of RNA interference. Nature 457: 405-412.
20. Johnston M, Geoffroy M-C, Sobala A, Hay R, Hutvagner G. 2010. HSP90 protein stabilizes unloaded Argonaute complexes and microscopic P-bodies in human cells. Mol Biol Cell 21: 1462-1469.
21. Kanellopoulou C, Muljo SA, Kung AL, Ganesan S, Drapkin R, Jenuwein T, Livingston DM, Rajewsky K. 2005. Dicer-deficient mouse embryonic stem cells are defective in differentiation and cen-tromeric silencing. Genes Dev 19: 489-501. (Pubitemid 40256280)
22. Kawamata T, Seitz H, Tomari Y. 2009. Structural determinants of miRNAs for RISC loading and slicer-independent unwinding. Nat Struct Mol Biol 16: 953-960.
23. Khvorova A, Reynolds A, Jayasena SD. 2003. Functional siRNAs and miRNAs exhibit strand bias. Cell 115: 209-216. (Pubitemid 37329584)
24. Kim K, Lee YS, Carthew RW. 2007. Conversion of pre-RISC to holo-RISC by Ago2 during assembly of RNAi complexes. RNA 13: 22-29. (Pubitemid 46026177)
25. Kok KH, Ng M-HJ, Ching Y-P, Jin D-Y. 2007. Human TRBP and PACT directly interact with each other and associate with dicer to facilitate the production of small interfering RNA. J Biol Chem 282: 17649-17657. (Pubitemid 47100277)
26. Kwak PB, Tomari Y. 2012. The N domain of Argonaute drives duplex unwinding during RISC assembly. Nat Struct Mol Biol 19: 145-151.
27. Lee YS, Nakahara K, Pham JW, Kim K, He Z, Sontheimer EJ, Carthew RW. 2004. Distinct roles for Drosophila Dicer-1 and Dicer-2 in the siRNA/miRNA silencing pathways. Cell 117: 69-81. (Pubitemid 38469899)
28. Lee Y, Hur I, Park S-Y, Kim Y-K, Suh MR, Kim VN. 2006. The role of PACT in the RNA silencing pathway. EMBO J 25: 522-532. (Pubitemid 43237659)
29. Leuschner PJF, Ameres SL, Kueng S, Martinez J. 2006. Cleavage of the siRNA passenger strand during RISC assembly in human cells. EMBO Rep 7: 314-320.
30. Liu Q, Rand TA, Kalidas S, Du F, Kim H-E, Smith DP, Wang X. 2003. R2D2, a bridge between the initiation and effector steps of the Drosophila RNAi pathway. Science 301: 1921-1925. (Pubitemid 37221400)
31. Liu J, Carmell MA, Rivas FV, Marsden CG, Thomson JM, Song J-J, Hammond SM, Joshua-Tor L, Hannon GJ. 2004. Argonaute2 is the catalytic engine of mammalian RNAi. Science 305: 1437-1441. (Pubitemid 39167657)
32. Liu Y, Ye X, Jiang F, Liang C, Chen D, Peng J, Kinch LN, Grishin NV, Liu Q. 2009. C3PO, an endoribonuclease that promotes RNAi by facilitating RISC activation. Science 325: 750-753.
33. Liu Y, Tan H, Tian H, Liang C, Chen S, Liu Q. 2011. Autoantigen La promotes efficient RNAi, antiviral response, and transposon silencing by facilitating multiple-turnover RISC catalysis. Mol Cell 44: 502-508.
34. Liu X, Jin D-Y, McManus MT, Mourelatos Z. 2012. Precursor microRNA-programmed silencing complex assembly pathways in mammals. Mol Cell 46: 507-517.
35. Macrae IJ, Ma E, Zhou M, Robinson CV, Doudna JA. 2008. In vitro re-constitution of the human RISC-loading complex. Proc Natl Acad Sci 105: 512-517. (Pubitemid 351171739)
36. Mathews DH, Sabina J, Zuker M, Turner DH. 1999. Expanded sequence dependence of thermodynamic parameters improves prediction of RNA secondary structure. J Mol Biol 288: 911-940. (Pubitemid 29248642)
37. Matranga C, Tomari Y, Shin C, Bartel DP, Zamore PD. 2005. Passenger-strand cleavage facilitates assembly of siRNA into Ago2-containing RNAi enzyme complexes. Cell 123: 607-620. (Pubitemid 41608464)
38. Meister G, Landthaler M, Patkaniowska A, Dorsett Y, Teng G, Tuschl T. 2004. Human Argonaute2 mediates RNA cleavage targeted by miRNAs and siRNAs. Mol Cell 15: 185-197. (Pubitemid 38950966)
39. Miyoshi T, Takeuchi A, Siomi H, Siomi MC. 2010. A direct role for Hsp90 in pre-RISC formation in Drosophila. Nat Struct Mol Biol 17: 1024-1026.
40. Murchison EP, Partridge JF, Tam OH, Cheloufi S, Hannon GJ. 2005. Characterization of Dicer-deficient murine embryonic stem cells. Proc Natl Acad Sci 102: 12135-12140. (Pubitemid 41291141)
41. Noland CL, Ma E, Doudna JA. 2011. SiRNA Repositioning for Guide Strand Selection by Human Dicer Complexes. Mol Cell 43: 110-121.
42. Okamura K, Liu N, Lai EC. 2009. Distinct mechanisms for microRNA strand selection by Drosophila Argonautes. Mol Cell 36: 431-444.
43. ′ ends of siRNA. RNA 11: 512-516. (Pubitemid 40397184)
44. Pare JM, Tahbaz N, López-Orozco J, LaPointe P, Lasko P, Hobman TC. 2009. Hsp90 regulates the function of Argonaute 2 and its recruitment to stress granules and P-bodies. Mol Biol Cell 20: 3273-3284.
45. Provost P, Dishart D, Doucet J, Frendewey D, Samuelsson B, Rådmark O. 2002. Ribonuclease activity and RNA binding of recom-binant human Dicer. EMBO J 21: 5864-5874. (Pubitemid 35315284)
46. Rand TA, Petersen S, Du F, Wang X. 2005. Argonaute2 cleaves the anti-guide strand of siRNA during RISC activation. Cell 123: 621-629. (Pubitemid 41608465)
47. Rivas FV, Tolia NH, Song J-J, Aragon JP, Liu J, Hannon GJ, Joshua-Tor L. 2005. Purified Argonaute2 and an siRNA form recombinant human RISC. Nat Struct Mol Biol 12: 340-349. (Pubitemid 43093089)
48. Schwarz DS, Hutvagner G, Du T, Xu Z, Aronin N, Zamore PD. 2003. Asymmetry in the assembly of the RNAi enzyme complex. Cell 115: 199-208. (Pubitemid 37329583)
49. Tian Y, Simanshu DK, Ascano M, Diaz-Avalos R, Park AY, Juranek SA, Rice WJ, Yin Q, Robinson CV, Tuschl T, et al. 2011. Multimeric assembly and biochemical characterization of the Trax-translin endo-nuclease complex. Nat Struct Mol Biol 18: 658-664.
50. Tinoco I, Borer PN, Dengler B, Levin MD, Uhlenbeck OC, Crothers DM, Bralla J. 1973. Improved estimation of secondary structure in ribonucleic acids. Nat New Biol 246: 40-41.
51. Tomari Y, Matranga C, Haley B, Martinez N, Zamore PD. 2004. A protein sensor for siRNA asymmetry. Science 306: 1377-1380. (Pubitemid 39532515)
52. Tomari Y, Du T, Zamore PD. 2007. Sorting of Drosophila small silencing RNAs. Cell 130: 299-308. (Pubitemid 47086328)
53. Wang Y, Juranek S, Li H, Sheng G, Tuschl T, Patel DJ. 2008. Structure of an argonaute silencing complex with a seed-containing guide DNA and target RNA duplex. Nature 456: 921-926.
54. Wang B, Li S, Qi HH, Chowdhury D, Shi Y, Novina CD. 2009. Distinct passenger strand and mRNA cleavage activities of human Argonaute proteins. Nat Struct Mol Biol 16: 1259-1266.
55. Wang D, Zhang Z, O'Loughlin E, Lee T, Houel S, O'Carroll D, Tarakhovsky A, Ahn NG, Yi R. 2012. Quantitative functions of Argonaute proteins in mammalian development. Genes Dev 26: 693-704.
56. Xia T, SantaLucia J, Burkard ME, Kierzek R, Schroeder SJ, Jiao X, Cox C, Turner DH. 1998. Thermodynamic parameters for an expanded nearest-neighbor model for formation of RNA duplexes with Watson-Crick base pairs. Biochemistry 37: 14719-14735. (Pubitemid 28487580)
57. Ye X, Huang N, Liu Y, Paroo Z, Huerta C, Li P, Chen S, Liu Q, Zhang H. 2011. Structure of C3PO and mechanism of human RISC activation. Nat Struct Mol Biol 18: 650-657.
58. Yoda M, Kawamata T, Paroo Z, Ye X, Iwasaki S, Liu Q, Tomari Y. 2010. ATP-dependent human RISC assembly pathways. Nat Struct Mol Biol 17: 17-23.
59. Zhang H, Kolb FA, Brondani V, Billy E, Filipowicz W. 2002. Human Dicer preferentially cleaves dsRNAs at their termini without a requirement for ATP. EMBO J 21: 5875-5885. (Pubitemid 35315285)