Structure of yeast Argonaute with guide RNA

Nature

Volumn 486, Issue 7403, 2012, Pages 368-374

  Nakanishi, Kotaro ^a   Weinberg, David E ^b,c   Bartel, David P ^b,c   Patel, Dinshaw J ^a  

^a MEMORIAL SLOAN KETTERING CANCER CENTER   (United States)

^b WHITEHEAD INSTITUTE FOR BIOMEDICAL RESEARCH   (United States)

^c MASSACHUSETTS INSTITUTE OF TECHNOLOGY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ARGONAUTE PROTEIN; GLUTAMIC ACID; GUIDE RNA; HYDROXYL GROUP; NUCLEOTIDE; PHOSPHATE; RIBONUCLEASE H;

ENZYME ACTIVITY; MUTATION; PHOSPHATASE; RNA; YEAST;

AMINO TERMINAL SEQUENCE; ARTICLE; CRYSTAL STRUCTURE; GENE INSERTION; GENE SILENCING; HYDROGEN BOND; KLUYVEROMYCES; NONHUMAN; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; PROTEIN CONFORMATION; PROTEIN DOMAIN; PROTEIN STRUCTURE; RNA CLEAVAGE; RNA INTERFERENCE; SEQUENCE ANALYSIS; YEAST;

ARGONAUTE PROTEINS; BASE SEQUENCE; BIOCATALYSIS; CATALYTIC DOMAIN; CRYSTALLOGRAPHY, X-RAY; EUKARYOTIC CELLS; FUNGAL PROTEINS; KLUYVEROMYCES; MODELS, MOLECULAR; MOLECULAR CONFORMATION; MOLECULAR SEQUENCE DATA; RNA, GUIDE; SACCHAROMYCETALES;

EID: 84862558196     PISSN: 00280836     EISSN: 14764687     Source Type: Journal    
DOI: 10.1038/nature11211     Document Type: Article

References (64)

1. Bartel, D. P. MicroRNAs: genomics, biogenesis, mechanism, and function. Cell 116, 281-297 (2004).
2. Meister, G. & Tuschl, T. Mechanisms of gene silencing by double-stranded RNA. Nature 431, 343-349 (2004). (Pubitemid 39265674)
3. Malone, C. D. & Hannon, G. J. Small RNAs as guardians of the genome. Cell 136, 656-668 (2009).
4. Bernstein, E., Caudy, A. A., Hammond, S. M. & Hannon, G. J. Role for a bidentate ribonuclease in the initiation step of RNA interference. Nature 409, 363-366 (2001). (Pubitemid 32151243)
5. Elbashir, S. M., Lendeckel, W.& Tuschl, T.RNA interference ismediated by 21-and 22-nucleotide RNAs. Genes Dev. 15, 188-200 (2001). (Pubitemid 32107664)
6. Hutvágner, G. et al.A cellular function for theRNA-interference enzyme Dicer in the maturation of the let-7 small temporal RNA. Science 293, 834-838 (2001). (Pubitemid 32743968)
7. Matranga, C., Tomari, Y., Shin, C., Bartel, D. P. & Zamore, P. D. Passenger-strand cleavage facilitates assembly of siRNA into Ago2-containing RNAi enzyme complexes. Cell 123, 607-620 (2005). (Pubitemid 41608464)
8. 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, 2837-2848 (2005). (Pubitemid 41739969)
9. Rand, T. A.,Petersen, S.,Du, F.&Wang, X. Argonaute2 cleaves the anti-guide strand of siRNA during RISC activation. Cell 123, 621-629 (2005). (Pubitemid 41608465)
10. Tomari, Y. & Zamore, P. D. Perspective: machines for RNAi. Genes Dev. 19, 517-529 (2005). (Pubitemid 40314984)
11. Carthew, R.W.&Sontheimer, E. J.Origins andmechanisms ofmiRNAsand siRNAs. Cell 136, 642-655 (2009).
12. Song, J. J.,Smith, S. K.,Hannon, G. J.&Joshua-Tor, L. Crystal structure ofArgonaute and its implications for RISC slicer activity. Science 305, 1434-1437 (2004). (Pubitemid 39167656)
13. Yuan, Y. R. et al. Crystal structure of A. aeolicus argonaute, a site-specific DNAguided endoribonuclease, provides insights into RISC-mediated mRNA cleavage. Mol. Cell 19, 405-419 (2005).
14. Liu, J. et al. Argonaute2 is the catalytic engine of mammalian RNAi. Science 305, 1437-1441 (2004). (Pubitemid 39167657)
15. Parker, J. S., Roe, S. M. & Barford, D. Crystal structure of a PIWI protein suggests mechanisms for siRNA recognition and slicer activity. EMBO J. 23, 4727-4737 (2004). (Pubitemid 40069703)
16. Ma, J. B. et al. Structural basis for59-end-specific recognitionofguideRNAby the A. fulgidus Piwi protein. Nature 434, 666-670 (2005).
17. Wang, Y., Sheng, G., Juranek, S., Tuschl, T. & Patel, D. J. Structure of the guidestrand-containing argonaute silencing complex. Nature 456, 209-213 (2008).
18. Wang, Y. et al. Structure of an argonaute silencing complex with a seed-containing guide DNA and target RNA duplex. Nature 456, 921-926 (2008).
19. Wang, Y. et al. Nucleation, propagation and cleavage of target RNAs in Ago silencing complexes. Nature 461, 754-761 (2009).
20. Parker, J. S. How to slice: snapshots of Argonaute in action. Silence 1, 3 (2010).
21. Makarova, K. S., Wolf, Y. I., van der Oost, J. & Koonin, E. V. Prokaryotic homologs of Argonaute proteins are predicted to function as key components of a novel system of defense against mobile genetic elements. Biol. Direct 4, 29 (2009).
22. Meister, G. et al. Identification of novel argonaute-associated proteins. Curr. Biol. 15, 2149-2155 (2005). (Pubitemid 41739749)
23. Lingel, A., Simon, B., Izaurralde, E. & Sattler, M. Structure and nucleic-acid binding of the Drosophila Argonaute 2 PAZ domain. Nature 426, 465-469 (2003). (Pubitemid 37490135)
24. Yan, K. S. et al. Structure and conserved RNA binding of the PAZ domain. Nature 426, 468-474 (2003).
25. Ma, J. B., Ye, K.& Patel, D. J. Structural basis for overhang-specific small interfering RNA recognition by the PAZ domain. Nature 429, 318-322 (2004). (Pubitemid 38684819)
26. Boland, A., Tritschler, F., Heimstadt, S., Izaurralde, E. & Weichenrieder, O. Crystal structure and ligand binding of the MID domain of a eukaryotic Argonaute protein. EMBO Rep. 11, 522-527 (2010).
27. Frank, F., Sonenberg, N.&Nagar, B. Structural basis for59-nucleotide base-specific recognition of guide RNA by human AGO2. Nature 465, 818-822 (2010).
28. Boland, A., Huntzinger, E., Schmidt, S., Izaurralde, E. & Weichenrieder, O. Crystal structure of the MID-PIWI lobe of a eukaryotic Argonaute protein. Proc. Natl Acad. Sci. USA 108, 10466-10471 (2011).
29. Drinnenberg, I. A. et al. RNAi in budding yeast. Science 326, 544-550 (2009).
30. Weinberg, D. E., Nakanishi, K., Patel, D. J. & Bartel, D. P. The inside-out mechanism of Dicers from budding yeasts. Cell 146, 262-276 (2011).
31. Rivas, F. V. et al. PurifiedArgonaute2andan siRNAformrecombinanthuman RISC. Nature Struct. Mol. Biol. 12, 340-349 (2005).
32. Addo-Quaye, C., Eshoo, T. W., Bartel, D. P. & Axtell, M. J. Endogenous siRNA and miRNA targets identified by sequencing of the Arabidopsis degradome. Curr. Biol. 18, 758-762 (2008).
33. German, M. A. et al. Global identification of microRNA-target RNA pairs by parallel analysis of RNA ends. Nature Biotechnol. 26, 941-946 (2008).
34. Elbashir, S. M.,Martinez, J., Patkaniowska, A., Lendeckel, W.& Tuschl, T. Functional anatomyof siRNAs formediating efficientRNAi in Drosophilamelanogasterembryo lysate. EMBO J. 20, 6877-6888 (2001). (Pubitemid 33134217)
35. Haley, B. & Zamore, P. D. Kinetic analysis of the RNAi enzyme complex. Nature Struct. Mol. Biol. 11, 599-606 (2004). (Pubitemid 38823525)
36. Martinez, J. & Tuschl, T. RISC is a 59 phosphomonoester-producing RNA endonuclease. Genes Dev. 18, 975-980 (2004).
37. Ameres, S. L., Martinez, J. & Schroeder, R. Molecular basis for target RNA recognition and cleavage by human RISC. Cell 130, 101-112 (2007). (Pubitemid 47031315)
38. 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 130, 287-297 (2007). (Pubitemid 47086327)
39. Frazão, C. et al. Unravelling the dynamics of RNA degradation by ribonuclease II and its RNA-bound complex. Nature 443, 110-114 (2006). (Pubitemid 44344058)
40. Parker, J. S., Roe, S. M. & Barford, D. Structural insights into mRNA recognition from a PIWI domain-siRNA guide complex. Nature 434, 663-666 (2005). (Pubitemid 40488560)
41. Pan, Y. & MacKerell, A. D. Jr. Altered structural fluctuations in duplex RNA versus DNA: a conformational switch involving base pair opening. Nucleic Acids Res. 31, 7131-7140 (2003). (Pubitemid 38016159)
42. Schwarz, D. S., Hutvágner, G., Haley, B. & Zamore, P. D. Evidence that siRNAs function as guides, not primers, in the Drosophila and human RNAi pathways. Mol. Cell 10, 537-548 (2002). (Pubitemid 35284172)
43. Chiu, Y. L. & Rana, T. M. siRNA function in RNAi: a chemical modification analysis. RNA 9, 1034-1048 (2003). (Pubitemid 37093614)
44. Parker, J. S., Parizotto, E. A., Wang, M., Roe, S. M. & Barford, D. Enhancement of the seed-target recognition step in RNA silencing by a PIWI/MID domain protein. Mol. Cell 33, 204-214 (2009).
45. Mallory, A. C. et al. MicroRNA control of PHABULOSA in leaf development: importance of pairing to the microRNA 59 region. EMBO J. 23, 3356-3364 (2004). (Pubitemid 39209159)
46. Nowotny, M., Gaidamakov, S. A., Crouch, R. J. & Yang, W. Crystal structures of RNase H bound to an RNA/DNA hybrid: substrate specificity and metaldependent catalysis. Cell 121, 1005-1016 (2005). (Pubitemid 40884393)
47. Hall, T. M. Structure and function of argonaute proteins. Structure 13, 1403-1408 (2005). (Pubitemid 41427580)
48. Nowotny, M. Retroviral integrase superfamily: the structural perspective. EMBO Rep. 10, 144-151 (2009).
49. Schirle, N. T. & Macrae, I. J. The crystal structure of human Argonaute2. Science http://dx.doi.org/10.1126/science.1221551 (26 April 2012).
50. Otwinowski, Z. & Minor, W. Processing of X-ray diffraction data collected in oscillation mode. Meth. Enzymol. 276, 307-326 (1997). (Pubitemid 27085611)
51. Pape, T. & Schneider, T. R. HKL2MAP: a graphical user interface for phasing with SHELX programs. J. Appl. Crystallogr. 37, 843-844 (2004).
52. McCoy, A. J. et al.Phaser crystallographic software. J.Appl. Crystallogr.40, 658-674 (2007). (Pubitemid 47080256)
53. Collaborative Computational Project. The CCP4 suite: programs for protein crystallography. Acta Crystallogr. 50, 760-763 (1994).
54. Jones, T. A., Zou, J. Y., Cowan,S. W.&Kjeldgaard, M.Improved methods for building proteinmodels in electron densitymaps and the location of errors in thesemodels. Acta Crystallogr. A 47, 110-119 (1991).
55. Adams, P. D. et al. PHENIX: building new software for automated crystallographic structure determination. Acta Crystallogr. 58, 1948-1954 (2002). (Pubitemid 35337293)
56. Vagin, A. & Teplyakov, A. An approach to multi-copy search in molecular replacement. Acta Crystallogr. 56, 1622-1624 (2000). (Pubitemid 32040020)
57. Brünger, A. T. et al. Crystallography & NMR system: a new software suite for macromolecular structure determination. Acta Crystallogr. 54, 905-921 (1998).
58. DeLano, W. L. & Lam, J. W. PyMOL: A communications tool for computational models. Abstracts of Papers of the American Chemical Society 230 (2005).
59. Grimson, A. et al. Early origins and evolution of microRNAs and Piwi-interacting RNAs in animals. Nature 455, 1193-1197 (2008).
60. Jeong, H. et al. Genome sequences of Escherichia coli B strains REL606 and BL21(DE3). J. Mol. Biol. 394, 644-652 (2009).
61. Gietz, R. D.& Schiestl, R. H. High-efficiency yeast transformation using the LiAc/SS carrier DNA/PEG method. Nature Protocols 2, 31-34 (2007). (Pubitemid 47040065)
62. Mumberg, D., Muller, R. & Funk, M. Yeast vectors for the controlled expression of heterologous proteins in different genetic backgrounds. Gene 156, 119-122 (1995).
63. Sikorski, R. S. & Hieter, P. A system of shuttle vectors and yeast host strains designed for efficient manipulation of DNA in Saccharomyces cerevisiae. Genetics 122, 19-27 (1989).
64. Longtine, M. S. et al. Additional modules for versatile and economical PCR-based gene deletion and modification in Saccharomyces cerevisiae. Yeast 14, 953-961 (1998). (Pubitemid 28328001)