Type III CRISPR-Cas systems produce cyclic oligoadenylate second messengers

Nature

Volumn 548, Issue 7669, 2017, Pages 543-548

  Niewoehner, Ole ^a   Garcia Doval, Carmela ^a   Rostøl, Jakob T ^b   Berk, Christian ^c   Schwede, Frank ^d   Bigler, Laurent ^a   Hall, Jonathan ^c   Marraffini, Luciano A ^b   Jinek, Martin ^a  

^a UNIVERSITY OF ZURICH   (Switzerland)

^b ROCKEFELLER UNIVERSITY   (United States)

^c ETH ZURICH   (Switzerland)

^d BIOLOG Life Science Institute   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

ADENOSINE TRIPHOSPHATE; CRISPR ASSOCIATED PROTEIN; CRISPR ASSOCIATED PROTEIN CSM6; RIBONUCLEASE; UNCLASSIFIED DRUG;

CHEMICAL BONDING; GENE EXPRESSION; IMMUNE RESPONSE; IMMUNITY; PROKARYOTE; PROTEIN; RNA;

ARTICLE; CLUSTERED REGULARLY INTERSPACED SHORT PALINDROMIC REPEAT; CRISPR CAS SYSTEM; ENZYME ACTIVITY; INNATE IMMUNITY; NONHUMAN; PRIORITY JOURNAL; RNA BINDING; RNA CLEAVAGE; SECOND MESSENGER; STAPHYLOCOCCUS EPIDERMIDIS; ALLOSTERISM; DIFFUSION; ENZYME ACTIVATION; ENZYMOLOGY; EURYARCHAEOTA; GENETICS; METABOLISM; PHYSIOLOGY; PROTEIN DOMAIN; THERMUS THERMOPHILUS;

MAMMALIA; PROKARYOTA;

ALLOSTERIC REGULATION; CRISPR-ASSOCIATED PROTEINS; CRISPR-CAS SYSTEMS; DIFFUSION; ENZYME ACTIVATION; EURYARCHAEOTA; IMMUNITY, INNATE; PROTEIN DOMAINS; RIBONUCLEASES; SECOND MESSENGER SYSTEMS; THERMUS THERMOPHILUS;

EID: 85028735202     PISSN: 00280836     EISSN: 14764687     Source Type: Journal    
DOI: 10.1038/nature23467     Document Type: Article

References (41)

1. Mohanraju, P. et al. Diverse evolutionary roots and mechanistic variations of the CRISPR-Cas systems. Science 353, aad5147 (2016).
2. Marraffini, L. A. CRISPR-Cas immunity in prokaryotes. Nature 526, 55-61 (2015).
3. Sorek, R., Lawrence, C. M. & Wiedenheft, B. CRISPR-mediated adaptive immune systems in bacteria and archaea. Annu. Rev. Biochem. 82, 237-266 (2013).
4. Koonin, E. V., Makarova, K. S. & Zhang, F. Diversity, classification and evolution of CRISPR-Cas systems. Curr. Opin. Microbiol. 37, 67-78 (2017).
5. Makarova, K. S. et al. An updated evolutionary classification of CRISPR-Cas systems. Nat. Rev. Microbiol. 13, 722-736 (2015).
6. Samai, P. et al. Co-transcriptional DNA and RNA cleavage during Type III CRISPR-Cas immunity. Cell 161, 1164-1174 (2015).
7. Goldberg, G. W., Jiang, W., Bikard, D. & Marraffini, L. A. Conditional tolerance of temperate phages via transcription-dependent CRISPR-Cas targeting. Nature 514, 633-637 (2014).
8. Deng, L., Garrett, R. A., Shah, S. A., Peng, X. & She, Q. A novel interference mechanism by a type IIIB CRISPR-Cmr module in Sulfolobus. Mol. Microbiol. 87, 1088-1099 (2013).
9. Elmore, J. R. et al. Bipartite recognition of target RNAs activates DNA cleavage by the type III-B CRISPR-Cas system. Genes Dev. 30, 447-459 (2016).
10. Estrella, M. A., Kuo, F.-T. & Bailey, S. RNA-Activated DNA cleavage by the type III-B CRISPR-Cas effector complex. Genes Dev. 30, 460-470 (2016).
11. Kazlauskiene, M., Tamulaitis, G., Kostiuk, G., Venclovas, . & Siksnys, V. Spatiotemporal control of type III-A CRISPR-Cas immunity: coupling DNA degradation with the target RNA recognition. Mol. Cell 62, 295-306 (2016).
12. Tamulaitis, G., Venclovas, . & Siksnys, V. Type III CRISPR-Cas immunity: major differences brushed aside. Trends Microbiol. 25, 49-61 (2017).
13. Makarova, K. S., Anantharaman, V., Grishin, N. V., Koonin, E. V. & Aravind, L. CARF and WYL domains: ligand-binding regulators of prokaryotic defense systems. Front. Genet. 5, 102 (2014).
14. Anantharaman, V., Makarova, K. S., Burroughs, A. M., Koonin, E. V. & Aravind, L. Comprehensive analysis of the HEPN superfamily: identification of novel roles in intra-genomic conflicts, defense, pathogenesis and RNA processing. Biol. Direct 8, 15 (2013).
15. Hatoum-Aslan, A., Maniv, I., Samai, P. & Marraffini, L. A. Genetic characterization of antiplasmid immunity through a type III-A CRISPR-Cas system. J. Bacteriol. 196, 310-317 (2014).
16. Jiang, W., Samai, P. & Marraffini, L. A. Degradation of phage transcripts by CRISPR-Associated RNases enables type III CRISPR-Cas immunity. Cell 164, 710-721 (2016).
17. Niewoehner, O. & Jinek, M. Structural basis for the endoribonuclease activity of the type III-A CRISPR-Associated protein Csm6. RNA 22, 318-329 (2016).
18. Sheppard, N. F., Glover, C. V. C., III, Terns, R. M. & Terns, M. P. The CRISPRassociated Csx1 protein of Pyrococcus furiosus is an adenosine-specific endoribonuclease. RNA 22, 216-224 (2016).
19. Staals, R. H. J. et al. RNA targeting by the type III-A CRISPR-Cas Csm complex of Thermus thermophilus. Mol. Cell 56, 518-530 (2014).
20. Tamulaitis, G. et al. Programmable RNA shredding by the type III-A CRISPR-Cas system of Streptococcus thermophilus. Mol. Cell 56, 506-517 (2014).
21. Hatoum-Aslan, A., Samai, P., Maniv, I., Jiang, W. & Marraffini, L. A. A ruler protein in a complex for antiviral defense determines the length of small interfering CRISPR RNAs. J. Biol. Chem. 288, 27888-27897 (2013).
22. Burroughs, A. M., Zhang, D., Schäffer, D. E., Iyer, L. M. & Aravind, L. Comparative genomic analyses reveal a vast, novel network of nucleotidecentric systems in biological conflicts, immunity and signaling. Nucleic Acids Res. 43, 10633-10654 (2015).
23. Yan, X., Guo, W. & Yuan, Y. A. Crystal structures of CRISPR-Associated Csx3 reveal a manganese-dependent deadenylation exoribonuclease. RNA Biol. 12, 749-760 (2015).
24. Topuzlu, E. & Lawrence, C. M. Recognition of a pseudo-symmetric RNA tetranucleotide by Csx3, a new member of the CRISPR associated Rossmann fold superfamily. RNA Biol. 13, 254-257 (2016).
25. Carroll, S. S. et al. Activation of RNase L by 2? ,5?-oligoadenylates. Kinetic characterization. J. Biol. Chem. 272, 19193-19198 (1997).
26. Prischi, F., Nowak, P. R., Carrara, M. & Ali, M. M. U. Phosphoregulation of Ire1 RNase splicing activity. Nat. Commun. 5, 3554 (2014).
27. Staals, R. H. J. et al. Structure and activity of the RNA-targeting Type III-B CRISPR-Cas complex of Thermus thermophilus. Mol. Cell 52, 135-145 (2013).
28. Hale, C. R., Cocozaki, A., Li, H., Terns, R. M. & Terns, M. P. Target RNA capture and cleavage by the Cmr type III-B CRISPR-Cas effector complex. Genes Dev. 28, 2432-2443 (2014).
29. Makarova, K. S. et al. Evolution and classification of the CRISPR-Cas systems. Nat. Rev. Microbiol. 9, 467-477 (2011).
30. Osawa, T., Inanaga, H. & Numata, T. Crystal structure of the Cmr2-Cmr3 subcomplex in the CRISPR-Cas RNA silencing effector complex. J. Mol. Biol. 425, 3811-3823 (2013).
31. Kalia, D. et al. Nucleotide, c-di-GMP, c-di-AMP, cGMP, cAMP, (p)ppGpp signaling in bacteria and implications in pathogenesis. Chem. Soc. Rev. 42, 305-341 (2013).
32. Hornung, V., Hartmann, R., Ablasser, A. & Hopfner, K.-P. OAS proteins and cGAS: unifying concepts in sensing and responding to cytosolic nucleic acids. Nat. Rev. Immunol. 14, 521-528 (2014).
33. East-Seletsky, A. et al. Two distinct RNase activities of CRISPR-C2c2 enable guide-RNA processing and RNA detection. Nature 538, 270-273 (2016).
34. He, F., Vestergaard, G., Peng, W., She, Q. & Peng, X. CRISPR-Cas type I-A Cascade complex couples viral infection surveillance to host transcriptional regulation in the dependence of Csa3b. Nucleic Acids Res. 45, 1902-1913 (2017).
35. Lintner, N. G. et al. The structure of the CRISPR-Associated protein Csa3 provides insight into the regulation of the CRISPR/Cas system. J. Mol. Biol. 405, 939-955 (2011).
36. Geertsma, E. R. FX cloning: a simple and robust high-throughput cloning method for protein expression. Methods Mol. Biol. 1116, 153-164 (2014).
37. Kreiswirth, B. N. et al. The toxic shock syndrome exotoxin structural gene is not detectably transmitted by a prophage. Nature 305, 709-712 (1983).
38. Krissinel, E. & Henrick, K. Secondary-structure matching (SSM), a new tool for fast protein structure alignment in three dimensions. Acta Crystallogr. D 60, 2256-2268 (2004).
39. Sievers, F. et al. Fast, scalable generation of high-quality protein multiple sequence alignments using Clustal Omega. Mol. Syst. Biol. 7, 539 (2011).
40. Gouet, P., Courcelle, E., Stuart, D. I. & Métoz, F. ESPript: analysis of multiple sequence alignments in PostScript. Bioinformatics 15, 305-308 (1999).
41. Kelley, L. A., Mezulis, S., Yates, C. M., Wass, M. N. & Sternberg, M. J. E. The Phyre2 web portal for protein modeling, prediction and analysis. Nat. Protocols 10, 845-858 (2015).