Antiviral signalling by a cyclic nucleotide activated CRISPR protease.
Bacteria
/ enzymology
Bacteriophages
/ immunology
CRISPR-Associated Proteins
/ metabolism
CRISPR-Cas Systems
/ genetics
Cyclic AMP
/ analogs & derivatives
Enzyme Activation
Gene Expression Regulation, Bacterial
Nucleotides, Cyclic
/ immunology
Operon
Protease La
/ chemistry
RNA, Viral
Sigma Factor
Transcription, Genetic
Journal
Nature
ISSN: 1476-4687
Titre abrégé: Nature
Pays: England
ID NLM: 0410462
Informations de publication
Date de publication:
02 2023
02 2023
Historique:
received:
06
12
2021
accepted:
17
11
2022
pubmed:
25
11
2022
medline:
4
2
2023
entrez:
24
11
2022
Statut:
ppublish
Résumé
CRISPR defence systems such as the well-known DNA-targeting Cas9 and the RNA-targeting type III systems are widespread in prokaryotes
Identifiants
pubmed: 36423657
doi: 10.1038/s41586-022-05571-7
pii: 10.1038/s41586-022-05571-7
doi:
Substances chimiques
CRISPR-Associated Proteins
0
Cyclic AMP
E0399OZS9N
Nucleotides, Cyclic
0
Protease La
EC 3.4.21.53
RNA, Viral
0
Sigma Factor
0
cyclic tetra-adenylate
0
Types de publication
Journal Article
Research Support, Non-U.S. Gov't
Langues
eng
Sous-ensembles de citation
IM
Pagination
168-174Informations de copyright
© 2022. The Author(s), under exclusive licence to Springer Nature Limited.
Références
Makarova, K. S., Wolf, Y. I. & Koonin, E. V. Classification and nomenclature of CRISPR–Cas systems: where from here. CRISPR J. 1, 325–336 (2018).
doi: 10.1089/crispr.2018.0033
Zhu, Y., Klompe, S. E., Vlot, M., van der Oost, J. & Staals, R. H. J. Shooting the messenger: RNA-targetting CRISPR–Cas systems. Biosci. Rep. 38, BSR20170788 (2018).
doi: 10.1042/BSR20170788
Kazlauskiene, M., Kostiuk, G., Venclovas, Č., Tamulaitis, G. & Siksnys, V. A cyclic oligonucleotide signaling pathway in type III CRISPR–Cas systems. Science 357, 605–609 (2017).
doi: 10.1126/science.aao0100
Niewoehner, O. et al. Type III CRISPR–Cas systems produce cyclic oligoadenylate second messengers. Nature 548, 543–548 (2017).
doi: 10.1038/nature23467
Rouillon, C., Athukoralage, J. S., Graham, S., Grüschow, S. & White, M. F. Control of cyclic oligoadenylate synthesis in a type III CRISPR system. eLife 7, e36734 (2018).
doi: 10.7554/eLife.36734
Shmakov, S. A., Makarova, K. S., Wolf, Y. I., Severinov, K. V. & Koonin, E. V. Systematic prediction of genes functionally linked to CRISPR–Cas systems by gene neighborhood analysis. Proc. Natl Acad. Sci. USA 115, E5307–E5316 (2018).
doi: 10.1073/pnas.1803440115
Shah, S. A. et al. Comprehensive search for accessory proteins encoded with archaeal and bacterial type III CRISPR–cas gene cassettes reveals 39 new cas gene families. RNA Biol. 16, 530–542 (2019).
doi: 10.1080/15476286.2018.1483685
Gasiunas, G., Sinkunas, T. & Siksnys, V. Molecular mechanisms of CRISPR-mediated microbial immunity. Cell. Mol. Life Sci. 71, 449–465 (2014).
doi: 10.1007/s00018-013-1438-6
Sasnauskas, G. & Siksnys, V. CRISPR adaptation from a structural perspective. Curr. Opin. Struct. Biol. 65, 17–25 (2020).
doi: 10.1016/j.sbi.2020.05.015
Jiang, F. & Doudna, J. A. CRISPR–Cas9 structures and mechanisms. Annu. Rev. Biophys. 46, 505–529 (2017).
doi: 10.1146/annurev-biophys-062215-010822
Jinek, M. et al. A programmable dual-RNA-guided DNA endonuclease in adaptive bacterial immunity. Science 337, 816–821 (2012).
doi: 10.1126/science.1225829
Athukoralage, J. S. & White, M. F. Cyclic oligoadenylate signalling and regulation by ring nucleases during type III CRISPR defence. RNA 27, 855–867 (2021).
doi: 10.1261/rna.078739.121
Jia, N., Jones, R., Sukenick, G. & Patel, D. J. Second messenger cA4 formation within the composite Csm1 Palm pocket of type III-A CRISPR–Cas Csm complex and its release path. Mol. Cell 75, 933–943.e6 (2019).
doi: 10.1016/j.molcel.2019.06.013
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).
doi: 10.3389/fgene.2014.00102
Lau, R. K. et al. Structure and mechanism of a cyclic trinucleotide-activated bacterial endonuclease mediating bacteriophage immunity. Mol. Cell 77, 723–733.e6 (2020).
doi: 10.1016/j.molcel.2019.12.010
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).
doi: 10.1016/j.jmb.2010.11.019
McMahon, S. A. et al. Structure and mechanism of a type III CRISPR defence DNA nuclease activated by cyclic oligoadenylate. Nat. Commun. 11, 500 (2020).
doi: 10.1038/s41467-019-14222-x
Rostøl, J. T. et al. The Card1 nuclease provides defence during type III CRISPR immunity. Nature 590, 624–629 (2021).
doi: 10.1038/s41586-021-03206-x
Garcia-Doval, C. et al. Activation and self-inactivation mechanisms of the cyclic oligoadenylate-dependent CRISPR ribonuclease Csm6. Nat. Commun. 11, 1596 (2020).
doi: 10.1038/s41467-020-15334-5
Lawrence, C. M., Charbonneau, A. & Gauvin, C. Cyclic tetra‐adenylate (cA
Meeske, A. J., Nakandakari-Higa, S. & Marraffini, L. A. Cas13-induced cellular dormancy prevents the rise of CRISPR-resistant bacteriophage. Nature 570, 241–245 (2019).
doi: 10.1038/s41586-019-1257-5
Burroughs, A. M., Zhang, D., Schäffer, D. E., Iyer, L. M. & Aravind, L. Comparative genomic analyses reveal a vast, novel network of nucleotide-centric systems in biological conflicts, immunity and signaling. Nucleic Acids Res. 43, 10633–10654 (2015).
doi: 10.1093/nar/gkv1267
Lowey, B. et al. CBASS immunity uses CARF-related effectors to sense 3′-5′- and 2′-5′-linked cyclic oligonucleotide signals and protect bacteria from phage infection. Cell 182, 38–49.e17 (2020).
doi: 10.1016/j.cell.2020.05.019
Makarova, K. S. et al. Evolutionary and functional classification of the CARF domain superfamily, key sensors in prokaryotic antivirus defense. Nucleic Acids Res. 48, 8828–8847 (2020).
doi: 10.1093/nar/gkaa635
Zwart, P. H. et al. Automated structure solution with the PHENIX suite. Methods Mol. Biol. 426, 419–435 (2008).
doi: 10.1007/978-1-60327-058-8_28
Chen, V. B. et al. MolProbity: all-atom structure validation for macromolecular crystallography. Acta Crystallogr. D 66, 12–21 (2010).
doi: 10.1107/S0907444909042073
Chung, I. Y. & Paetzel, M. Crystal structures of yellowtail ascites virus VP4 protease: trapping an internal cleavage site trans acyl–enzyme complex in a native Ser/Lys dyad active site. J. Biol. Chem. 288, 13068–13081 (2013).
doi: 10.1074/jbc.M112.386953
Krogh, A., Larsson, B., von Heijne, G. & Sonnhammer, E. L. L. Predicting transmembrane protein topology with a hidden markov model: application to complete genomes. J. Mol. Biol. 305, 567–580 (2001).
doi: 10.1006/jmbi.2000.4315
Fatma, S., Chakravarti, A., Zeng, X. & Huang, R. H. Molecular mechanisms of the CdnG–Cap5 antiphage defense system employing 3′, 2′-cGAMP as the second messenger. Nat. Commun. 12, 6381 (2021).
doi: 10.1038/s41467-021-26738-2
Jiang, K. et al. Structural basis of formation of the microtubule minus-end-regulating CAMSAP–katanin complex. Structure 26, 375–382.e4 (2018).
doi: 10.1016/j.str.2017.12.017
Saha, C. K., Sanches Pires, R., Brolin, H., Delannoy, M. & Atkinson, G. C. FlaGs and webFlaGs: discovering novel biology through the analysis of gene neighbourhood conservation. Bioinformatics 37, 1312–1314 (2021).
doi: 10.1093/bioinformatics/btaa788
Zimmermann, L. et al. A completely reimplemented MPI bioinformatics toolkit with a new HHpred server at its core. J. Mol. Biol. 430, 2237–2243 (2018).
doi: 10.1016/j.jmb.2017.12.007
Jumper, J. et al. Highly accurate protein structure prediction with AlphaFold. Nature 596, 583–589 (2021).
doi: 10.1038/s41586-021-03819-2
Holm, L. & Rosenström, P. Dali server: conservation mapping in 3D. Nucleic Acids Res. 38, W545–W549 (2010).
doi: 10.1093/nar/gkq366
Simanshu, D. K., Yamaguchi, Y., Park, J.-H., Inouye, M. & Patel, D. J. Structural basis of mRNA recognition and cleavage by toxin MazF and its regulation by antitoxin MazE in Bacillus subtilis. Mol. Cell 52, 447–458 (2013).
doi: 10.1016/j.molcel.2013.09.006
Hogrel, G. et al. Cyclic nucleotide-induced helical structure activates a TIR immune effector. Nature 608, 808–812 (2022).
doi: 10.1038/s41586-022-05070-9
Paget, M. S. Bacterial sigma factors and anti-sigma factors: structure, function and distribution. Biomolecules 5, 1245–1265 (2015).
doi: 10.3390/biom5031245
Sineva, E., Savkina, M. & Ades, S. E. Themes and variations in gene regulation by extracytoplasmic function (ECF) sigma factors. Curr. Opin. Microbiol. 36, 128–137 (2017).
doi: 10.1016/j.mib.2017.05.004
Krissinel, E. & Henrick, K. Inference of macromolecular assemblies from crystalline state. J. Mol. Biol. 372, 774–797 (2007).
doi: 10.1016/j.jmb.2007.05.022
Schuster, C. F. & Bertram, R. Toxin–antitoxin systems are ubiquitous and versatile modulators of prokaryotic cell fate. FEMS Microbiol. Lett. 340, 73–85 (2013).
doi: 10.1111/1574-6968.12074
Walsh, P. N. & Ahmad, S. S. Proteases in blood clotting. Essays Biochem. 38, 95–112 (2002).
doi: 10.1042/bse0380095
Brown, M. S., Ye, J., Rawson, R. B. & Goldstein, J. L. Regulated intramembrane proteolysis: a control mechanism conserved from bacteria to humans. Cell 100, 391–398 (2000).
doi: 10.1016/S0092-8674(00)80675-3
Fei, X., Bell, T. A., Barkow, S. R., Baker, T. A. & Sauer, R. T. Structural basis of ClpXP recognition and unfolding of ssrA-tagged substrates. eLife 9, e61496 (2020).
doi: 10.7554/eLife.61496
Hu, C. et al. Craspase is a CRISPR RNA-guided, RNA-activated protease. Science 377, 1278–1285 (2022).
doi: 10.1126/science.add5064
van Beljouw, S. P. B. et al. The gRAMP CRISPR–Cas effector is an RNA endonuclease complexed with a caspase-like peptidase. Science 373, 1349–1353 (2021).
doi: 10.1126/science.abk2718
Kato, K. et al. RNA-triggered protein cleavage and cell growth arrest by the type III-E CRISPR nuclease-protease. Science 378, 882–889 (2022).
doi: 10.1126/science.add7347
Strecker, J. et al. RNA-activated protein cleavage with a CRISPR-associated endopeptidase. Science 378, 874–881 (2022).
doi: 10.1126/science.add7450
Tunyasuvunakool, K. et al. Highly accurate protein structure prediction for the human proteome. Nature 596, 590–596 (2021).
doi: 10.1038/s41586-021-03828-1
Robert, X. & Gouet, P. Deciphering key features in protein structures with the new ENDscript server. Nucleic Acids Res. 42, W320–W324 (2014).
doi: 10.1093/nar/gku316
Liu, H. & Naismith, J. H. An efficient one-step site-directed deletion, insertion, single and multiple-site plasmid mutagenesis protocol. BMC Biotechnol. 8, 91 (2008).
doi: 10.1186/1472-6750-8-91
Rouillon, C., Athukoralage, J. S., Graham, S., Grüschow, S. & White, M. F. Investigation of the cyclic oligoadenylate signaling pathway of type III CRISPR systems. Methods Enzymol. 616, 191–218 (2019).
doi: 10.1016/bs.mie.2018.10.020
Cianci, M. et al. P13, the EMBL macromolecular crystallography beamline at the low-emittance PETRA III ring for high-and low-energy phasing with variable beam focusing. J. Synchrotron Radiat. 24, 323–332 (2017).
doi: 10.1107/S1600577516016465
Kabsch, W. Automatic-indexing of rotation diffraction patterns. J. Appl. Crystallogr. 21, 67–72 (1988).
doi: 10.1107/S0021889887009737
Liebschner, D. et al. Macromolecular structure determination using X-rays, neutrons and electrons: recent developments in Phenix. Acta Crystallogr. D Struct. Biol. 75, 861–877 (2019).
doi: 10.1107/S2059798319011471
Emsley, P. & Cowtan, K. Coot: model-building tools for molecular graphics. Acta Crystallogr. D 60, 2126–2132 (2004).
doi: 10.1107/S0907444904019158
Williams, C. J. et al. MolProbity: more and better reference data for improved all‐atom structure validation. Protein Sci. 27, 293–315 (2018).
doi: 10.1002/pro.3330
McCoy, A. J. et al. Phaser crystallographic software. J. Appl. Crystallogr. 40, 658–674 (2007).
doi: 10.1107/S0021889807021206
Blanchet, C. E. et al. Versatile sample environments and automation for biological solution X-ray scattering experiments at the P12 beamline (PETRA III, DESY). J. Appl. Crystallogr. 48, 431–443 (2015).
doi: 10.1107/S160057671500254X
Graewert, M. A. et al. Adding size exclusion chromatography (SEC) and light scattering (LS) devices to obtain high-quality small angle X-ray scattering (SAXS) data. Crystals 10, 975 (2020).
doi: 10.3390/cryst10110975
Franke, D., Kikhney, A. G. & Svergun, D. I. Automated acquisition and analysis of small angle X-ray scattering data. Nucl. Instrum. Methods Phys. Res. A 689, 52–59 (2012).
doi: 10.1016/j.nima.2012.06.008
Konarev, P. V., Volkov, V. V., Sokolova, A. V., Koch, M. H. J. & Svergun, D. I. PRIMUS: a Windows PC-based system for small-angle scattering data analysis. J. Appl. Crystallogr. 36, 1277–1282 (2003).
doi: 10.1107/S0021889803012779
Manalastas-Cantos, K. et al. ATSAS 3.0: expanded functionality and new tools for small-angle scattering data analysis. J. Appl. Crystallogr. 54, 343–355 (2021).
doi: 10.1107/S1600576720013412
Svergun, D., Barberato, C. & Koch, M. H. J. CRYSOL—a program to evaluate X-ray solution scattering of biological macromolecules from atomic coordinates. J. Appl. Crystallogr. 28, 768–773 (1995).
doi: 10.1107/S0021889895007047
Franke, D. & Svergun, D. I. DAMMIF, a program for rapid ab-initio shape determination in small-angle scattering. J. Appl. Crystallogr. 42, 342–346 (2009).
doi: 10.1107/S0021889809000338
Svergun, D. I. Restoring low resolution structure of biological macromolecules from solution scattering using simulated annealing. Biophys. J. 76, 2879–2886 (1999).
doi: 10.1016/S0006-3495(99)77443-6
Volkov, V. V. & Dmitri, I. S. Uniqueness of ab initio shape determination in small-angle scattering. J. Appl. Crystallogr. 36, 860–864 (2003).
doi: 10.1107/S0021889803000268
Kozin, M. B. & Svergun, D. I. Automated matching of high- and low-resolution structural models. J. Appl. Crystallogr. 34, 33–41 (2001).
doi: 10.1107/S0021889800014126
Petoukhov, M. V. et al. New developments in the ATSAS program package for small-angle scattering data analysis. J. Appl. Crystallogr. 45, 342–350 (2012).
doi: 10.1107/S0021889812007662
Milov, A., Salikohov, K. & Shirov, M. Application of Endor in electron-spin echo for paramagnetic center space distribution in solids. Fizika Tverdogo Tela 23, 975–982 (1981).
Pannier, M., Veit, S., Godt, A., Jeschke, G. & Spiess, H. W. Dead-time free measurement of dipole–dipole interactions between electron spins. J. Magn. Reson. 142, 331–340 (2000).
doi: 10.1006/jmre.1999.1944
Larsen, R. G. & Singel, D. J. Double electron–electron resonance spin–echo modulation: spectroscopic measurement of electron spin pair separations in orientationally disordered solids. J. Chem. Phys. 98, 5134–5146 (1993).
doi: 10.1063/1.464916
Worswick, S. G., Spencer, J. A., Jeschke, G. & Kuprov, I. Deep neural network processing of DEER data. Sci. Adv. 4, eaat5218 (2018).
doi: 10.1126/sciadv.aat5218
Fábregas Ibáñez, L., Jeschke, G. & Stoll, S. DeerLab: a comprehensive software package for analyzing dipolar electron paramagnetic resonance spectroscopy data. Magn. Reson. 1, 209–224 (2020).
doi: 10.5194/mr-1-209-2020
Jeschke, G., Chechik, V., Ionita, P. & Godt, A. DeerAnalysis2006—a comprehensive software package for analyzing pulsed ELDOR data. Appl. Magn. Reson. 30, 473–498 (2006).
doi: 10.1007/BF03166213
Mirdita, M. et al. ColabFold: making protein folding accessible to all. Nat. Methods 19, 679–682 (2022).
doi: 10.1038/s41592-022-01488-1
Cha, S. S. et al. Crystal structure of Lon protease: molecular architecture of gated entry to a sequestered degradation chamber. EMBO J. 29, 3520–3530 (2010).
doi: 10.1038/emboj.2010.226
Chung, I. Y. W. & Paetzel, M. Crystal structure of a viral protease intramolecular acyl-enzyme complex. J. Biol. Chem. 286, 12475–12482 (2011).
Léa, M. C. et al. Bacterial RadA is a DnaB-type helicase interacting with RecA to promote bidirectional D-loop extension. Nat. Commun. 8, 15638 (2017).
Zorzini, V. et al. Substrate recognition and activity regulation of the Escherichia coli mRNA endonuclease MazF. J. Biol. Chem. 291, 10950–10960 (2016).
doi: 10.1074/jbc.M116.715912
Hagelueken, G., Ward, R., Naismith, J. H. & Schiemann, O. MtsslWizard: in silico spin-labeling and generation of distance distributions in PyMOL. Appl. Magn. Reson. 42, 377–391 (2012).
doi: 10.1007/s00723-012-0314-0
Campagne, S., Marsh, M. E., Capitani, G., Vorholt, J. A. & Allain, F. H. T. Structural basis for −10 promoter element melting by environmentally induced sigma factors. Nat. Struct. Mol. Biol. 21, 269–276 (2014).
doi: 10.1038/nsmb.2777
Lane, W. J. & Darst, S. A. The structural basis for promoter −35 element recognition by the group IV σ factors. PLoS Biol. 4, e269 (2006).
doi: 10.1371/journal.pbio.0040269
Li, L., Fang, C., Zhuang, N., Wang, T. & Zhang, Y. Structural basis for transcription initiation by bacterial ECF σ factors. Nat. Commun. 10, 1153 (2019).
doi: 10.1038/s41467-019-09096-y