Crystal structure of the RNA-guided immune surveillance Cascade complex in Escherichia coli

Nature

Volumn 515, Issue 7525, 2014, Pages 147-150

  Zhao, Hongtu ^a,b   Sheng, Gang ^a   Wang, Jiuyu ^a   Wang, Min ^a   Bunkoczi, Gabor ^c   Gong, Weimin ^a   Wei, Zhiyi ^d   Wang, Yanli ^a  

^a INSTITUTE OF BIOPHYSICS   (China)

^b UNIVERSITY OF CHINESE ACADEMY OF SCIENCES   (China)

^c ADDENBROOKE S HOSPITAL   (United Kingdom)

^d SOUTHERN UNIVERSITY OF SCIENCE AND TECHNOLOGY   (China)

Author keywords

[No Author keywords available]

Indexed keywords

DNA; RNA; BACTERIAL RNA; CRISPR ASSOCIATED PROTEIN; MULTIPROTEIN COMPLEX; PROTEIN BINDING; PROTEIN SUBUNIT; RNA BINDING PROTEIN; UNTRANSLATED RNA;

BACTERIUM; CRYSTAL STRUCTURE; DNA; IMMUNE RESPONSE; MOLECULAR ANALYSIS; PROTEIN; RNA;

ARTICLE; BACTERIAL IMMUNITY; BINDING AFFINITY; CARBOXY TERMINAL SEQUENCE; CONFORMATIONAL TRANSITION; CRISPR CAS SYSTEM; CRYOELECTRON MICROSCOPY; CRYSTAL STRUCTURE; ESCHERICHIA COLI; HYDROGEN BOND; NONHUMAN; NUCLEOTIDE REPEAT; PRIORITY JOURNAL; PROTEIN QUATERNARY STRUCTURE; CHEMICAL STRUCTURE; CHEMISTRY; DNA TEMPLATE; GENETICS; IMMUNOLOGY; IMMUNOSURVEILLANCE; METABOLISM; PROTEIN SUBUNIT; X RAY CRYSTALLOGRAPHY;

ARCHAEA; BACTERIA (MICROORGANISMS); ESCHERICHIA COLI;

CRISPR-ASSOCIATED PROTEINS; CRISPR-CAS SYSTEMS; CRYSTALLOGRAPHY, X-RAY; ESCHERICHIA COLI; IMMUNOLOGIC SURVEILLANCE; MODELS, MOLECULAR; MULTIPROTEIN COMPLEXES; PROTEIN BINDING; PROTEIN SUBUNITS; RNA, BACTERIAL; RNA, UNTRANSLATED; RNA-BINDING PROTEINS; TEMPLATES, GENETIC;

EID: 84908445494     PISSN: 00280836     EISSN: 14764687     Source Type: Journal    
DOI: 10.1038/nature13733     Document Type: Article

References (39)

1. Wiedenheft, B., Sternberg, S. H. & Doudna, J. A. RNA-guided genetic silencing systems in bacteria and archaea. Nature 482, 331-338 (2012).
2. Barrangou, R. et al. CRISPR provides acquired resistance against viruses in prokaryotes. Science 315, 1709-1712 (2007).
3. Garneau, J. E. et al. The CRISPR/Cas bacterial immune system cleaves bacteriophage and plasmid DNA. Nature 468, 67-71 (2010).
4. Andersson, A. F. & Banfield, J. F. Virus population dynamics and acquired virus resistance in natural microbial communities. Science 320, 1047-1050 (2008).
5. Jansen, R., Embden, J. D., Gaastra, W. & Schouls, L. M. Identification of genes that are associated with DNA repeats in prokaryotes. Mol. Microbiol. 43, 1565-1575 (2002).
6. van der Oost, J., Jore, M. M., Westra, E. R., Lundgren, M. & Brouns, S. J. CRISPR-based adaptive and heritable immunity in prokaryotes. Trends Biochem. Sci. 34, 401-407 (2009).
7. Westra, E. R. et al. The CRISPRs, they are a-changin': how prokaryotes generate adaptive immunity. Annu. Rev. Genet. 46, 311-339 (2012).
8. van der Oost, J., Westra, E. R., Jackson, R. N. & Wiedenheft, B. Unravelling the structural and mechanistic basis of CRISPR-Cas systems. Nature Rev. Microbiol. 12, 479-492 (2014).
9. Makarova, K. S., Wolf, Y. I. & Koonin, E. V. The basic building blocks and evolution of CRISPR-cas systems. Biochem. Soc. Trans. 41, 1392-1400 (2013).
10. Wiedenheft, B. et al. Structures of the RNA-guided surveillance complex from a bacterial immune system. Nature 477, 486-489 (2011).
11. Jore, M. M. et al. Structural basis for CRISPR RNA-guided DNA recognition by Cascade. Nature Struct. Mol. Biol. 18, 529-536 (2011).
12. Reeks, J., Naismith, J. H. & White, M. F. CRISPR interference: a structural perspective. Biochem. J. 453, 155-166 (2013).
13. Brouns, S. J. et al. Small CRISPR RNAs guide antiviral defense in prokaryotes. Science 321, 960-964 (2008).
14. Sashital, D. G., Jinek, M. & Doudna, J. A. An RNA-induced conformational change required for CRISPR RNA cleavage by the endoribonuclease Cse3. Nature Struct. Mol. Biol. 18, 680-687 (2011).
15. Gesner, E. M., Schellenberg, M. J., Garside, E. L., George, M. M. & Macmillan, A. M. Recognition and maturation of effector RNAs in a CRISPR interference pathway. Nature Struct. Mol. Biol. 18, 688-692 (2011).
16. Haurwitz, R. E., Jinek, M., Wiedenheft, B., Zhou, K. & Doudna, J. A. Sequence- and structure-specific RNA processing by a CRISPR endonuclease. Science 329, 1355-1358 (2010).
17. Nam, K. H. et al. Cas5d protein processes pre-crRNA and assembles into a cascade-like interference complex in subtype I-C/Dvulg CRISPR-Cas system. Structure 20, 1574-1584 (2012).
18. Lintner, N. G. et al. Structural and functional characterization of an archaeal clustered regularly interspaced short palindromic repeat (CRISPR)-associated complex forantiviraldefense (CASCADE). J. Biol. Chem. 286, 21643-21656 (2011).
19. Hrle, A. et al. Structure and RNA-binding properties of the type III-A CRISPR-associated protein Csm3. RNA Biol. 10, 1670-1678 (2013).
20. Wiedenheft, B. et al. RNA-guided complex from a bacterial immune system enhances target recognition through seed sequence interactions. Proc. Natl Acad. Sci. USA 108, 10092-10097 (2011).
21. Semenova, E. et al. Interference by clustered regularly interspaced short palindromic repeat (CRISPR) RNA is governed by a seed sequence. Proc. Natl Acad. Sci. USA 108, 10098-10103 (2011).
22. Künne, T., Swarts, D. C. & Brouns, S. J. Planting the seed: target recognition of short guide RNAs. Trends Microbiol. 22, 74-83 (2014).
23. Sashital, D. G., Wiedenheft, B. & Doudna, J. A. Mechanism of foreign DNA selection in a bacterial adaptive immune system. Mol. Cell 46, 606-615 (2012).
24. Hochstrasser, M. L. et al. CasA mediates Cas3-catalyzed target degradation during CRISPR RNA-guided interference. Proc. Natl Acad. Sci. USA 111, 6618-6623 (2014).
25. Wang, Y., Sheng, G., Juranek, S., Tuschl, T. & Patel, D. J. Structure of the guide-strand- containing argonaute silencing complex. Nature 456, 209-213 (2008).
26. Westra, E. R. et al. CRISPR immunity relies on the consecutive binding and degradation of negatively supercoiled invader DNA by Cascade and Cas3. Mol. Cell 46, 595-605 (2012).
27. Mulepati, S. & Bailey, S. In vitro reconstitution of an Escherichia coli RNA-guided immune system reveals unidirectional, ATP-dependent degradation of DNA target. J. Biol. Chem. 288, 22184-22192 (2013).
28. Sinkunas, T. et al. In vitro reconstitution of Cascade-mediated CRISPR immunity in Streptococcus thermophilus. EMBO J. 32, 385-394 (2013).
29. Jackson, R. N., Lavin, M., Carter, J. & Wiedenheft, B. Fitting CRISPR-associated Cas3 into the helicase family tree. Curr. Opin. Struct. Biol. 24, 106-114 (2014).
30. Sinkunas, T. et al. Cas3 is a single-stranded DNA nuclease and ATP-dependent helicase in the CRISPR/Cas immune system. EMBO J. 30, 1335-1342 (2011).
31. Battye, T. G., Kontogiannis, L., Johnson, O., Powell, H. R. & Leslie, A. G. iMOSFLM: a new graphical interface for diffraction-image processing with MOSFLM. Acta Crystallogr. D 67, 271-281 (2011).
32. Otwinowski, Z. & Minor, W. Processing of X-Ray diffraction data collected in oscillation mode. Methods Enzymol. 276, 307-326 (1997).
33. Xiong, Y. From electron microscopy to X-ray crystallography: molecular-replacement case studies. Acta Crystallogr. D 64, 76-82 (2008).
34. McCoy, A. J. et al. Phaser crystallographic software. J. Appl. Crystallogr. 40, 658-674 (2007).
35. Terwilliger, T. C. Maximum-likelihood density modification. Acta Crystallogr. D 56, 965-972 (2000).
36. Adams, P. D. et al. PHENIX: building new software for automated crystallographic structure determination. Acta Crystallogr. D 58, 1948-1954 (2002).
37. Emsley, P. & Cowtan, K. Coot: model-building tools for molecular graphics. Acta Crystallogr. D 60, 2126-2132 (2004).
38. Chen, V. B. et al. MolProbity: all-atom structure validation for macromolecular crystallography. Acta Crystallogr. D 66, 12-21 (2010).
39. Laskowski, R. A., MacArthur, M. W., Moss, D. S. & Thornton, J. M. PROCHECK: a program to check the stereochemical quality of protein structures. J. Appl. Crystallogr. 26, 283-291 (1993).