Cmr3 regulates the suppression on cyclic oligoadenylate synthesis by tag complementarity in a Type III-B CRISPR-Cas system

References

• Barrangou R, Fremaux C, Deveau H, et al. CRISPR provides acquired resistance against viruses in prokaryotes. Science. 2007;315:1709–1712.
   PubMed Web of Science ®Google Scholar
• Marraffini LA, Sontheimer EJ. CRISPR interference limits horizontal gene transfer in staphylococci by targeting DNA. Science. 2008;322:1843–1845.
   PubMed Web of Science ®Google Scholar
• McGinn J, Marraffini LA. Molecular mechanisms of CRISPR-Cas spacer acquisition. Nature Rev Microbiol. 2019;17:7–12.
   PubMed Web of Science ®Google Scholar
• Brouns SJ, Jore MM, Lundgren M, et al. Small CRISPR RNAs guide antiviral defense in prokaryotes. Science. 2008;321:960–964.
   PubMed Web of Science ®Google Scholar
• Carte J, Wang R, Li H, et al. Cas6 is an endoribonuclease that generates guide RNAs for invader defense in prokaryotes. Genes Dev. 2008;22:3489–3496.
   PubMed Web of Science ®Google Scholar
• Mohanraju P, Makarova KS, Zetsche B, et al. Diverse evolutionary roots and mechanistic variations of the CRISPR-Cas systems. Science. 2016;353:aad5147.
   PubMed Web of Science ®Google Scholar
• Koonin EV, Makarova KS, Zhang F. Diversity, classification and evolution of CRISPR-Cas systems. Curr Opin Microbiol. 2017;37:67–78.
   PubMed Web of Science ®Google Scholar
• Chen JS, Ma E, Harrington LB, et al. CRISPR-Cas12a target binding unleashes indiscriminate single-stranded DNase activity. Science. 2018;360:436–439.
   PubMed Web of Science ®Google Scholar
• Gootenberg JS, Abudayyeh OO, Kellner MJ, et al. Multiplexed and portable nucleic acid detection platform with Cas13, Cas12a, and Csm6. Science. 2018;360:439–444.
   PubMed Web of Science ®Google Scholar
• Li SY, Cheng QX, Liu JK, et al. CRISPR-Cas12a has both cis- and trans-cleavage activities on single-stranded DNA. Cell Res. 2018;28:491–493.
   PubMed Web of Science ®Google Scholar
• Abudayyeh OO, Gootenberg JS, Konermann S, et al. C2c2 is a single-component programmable RNA-guided RNA-targeting CRISPR effector. Science. 2016;353:aaf5573.
   PubMed Web of Science ®Google Scholar
• Hale CR, Zhao P, Olson S, et al. RNA-guided RNA cleavage by a CRISPR RNA-Cas protein complex. Cell. 2009;139:945–956.
   PubMed Web of Science ®Google Scholar
• Elmore JR, Sheppard NF, Ramia N, et al. Bipartite recognition of target RNAs activates DNA cleavage by the Type III-B CRISPR-Cas system. Genes Dev. 2016;30:447–459.
   PubMed Web of Science ®Google Scholar
• Estrella MA, Kuo FT, Bailey S. RNA-activated DNA cleavage by the Type III-B CRISPR-Cas effector complex. Genes Dev. 2016;30:460–470.
   PubMed Web of Science ®Google Scholar
• Kazlauskiene M, Tamulaitis G, Kostiuk G, et al. Spatiotemporal control of type III-A CRISPR-Cas immunity: coupling DNA degradation with the target RNA recognition. Mol Cell. 2016;62:295–306.
   PubMed Web of Science ®Google Scholar
• Han W, Li Y, Deng L, et al. A type III-B CRISPR-Cas effector complex mediating massive target DNA destruction. Nucleic Acids Res. 2017;45:1983–1993.
   PubMed Web of Science ®Google Scholar
• Niewoehner O, Garcia-Doval C, Rostol JT, et al. Type III CRISPR-Cas systems produce cyclic oligoadenylate second messengers. Nature. 2017;548:543–548.
   PubMed Web of Science ®Google Scholar
• Kazlauskiene M, Kostiuk G, Venclovas C, et al. A cyclic oligonucleotide signaling pathway in type III CRISPR-Cas systems. Science. 2017;357:605–609.
   PubMed Web of Science ®Google Scholar
• Rouillon C, Athukoralage JS, Graham S, et al. Control of cyclic oligoadenylate synthesis in a type III CRISPR system. eLife. 2018;7:e36734.
   PubMed Web of Science ®Google Scholar
• Han W, Stella S, Zhang Y, et al. A Type III-B Cmr effector complex catalyzes the synthesis of cyclic oligoadenylate second messengers by cooperative substrate binding. Nucleic Acids Res. 2018;46:10319–10330.
   PubMed Web of Science ®Google Scholar
• Staals RH, Agari Y, Maki-Yonekura S, et al. Structure and activity of the RNA-targeting type III-B CRISPR-Cas complex of thermus thermophilus. Mol Cell. 2013;52:135–145.
   PubMed Web of Science ®Google Scholar
• Tamulaitis G, Kazlauskiene M, Manakova E, et al. Programmable RNA shredding by the type III-A CRISPR-Cas system of streptococcus thermophilus. Mol Cell. 2014;56:506–517.
   PubMed Web of Science ®Google Scholar
• Ramia NF, Spilman M, Tang L, et al. Essential structural and functional roles of the Cmr4 subunit in RNA cleavage by the Cmr CRISPR-Cas complex. Cell Rep. 2014;9:1610–1617.
   PubMed Web of Science ®Google Scholar
• Benda C, Ebert J, Scheltema RA, et al. Structural model of a CRISPR RNA-silencing complex reveals the RNA-target cleavage activity in Cmr4. Mol Cell. 2014;56:43–54.
   PubMed Web of Science ®Google Scholar
• Zhu X, Ye K. Cmr4 is the slicer in the RNA-targeting Cmr CRISPR complex. Nucleic Acids Res. 2015;43:1257–1267.
   PubMed Web of Science ®Google Scholar
• Tamulaitis G, Venclovas C, Siksnys V. Type III CRISPR-Cas immunity: major differences brushed aside. Trends Microbiol. 2017;25:49–61.
   PubMed Web of Science ®Google Scholar
• Deveau H, Barrangou R, Garneau JE, et al. Phage response to CRISPR-encoded resistance in streptococcus thermophilus. J Bacteriol. 2008;190:1390–1400.
   PubMed Web of Science ®Google Scholar
• Gasiunas G, Barrangou R, Horvath P, et al. Cas9-crRNA ribonucleoprotein complex mediates specific DNA cleavage for adaptive immunity in bacteria. Proc Natl Acad Sci U S A. 2012;109:E2579–86.
   PubMed Web of Science ®Google Scholar
• Jinek M, Chylinski K, Fonfara I, et al. A programmable dual-RNA-guided DNA endonuclease in adaptive bacterial immunity. Science. 2012;337:816–821.
   PubMed Web of Science ®Google Scholar
• Zetsche B, Gootenberg JS, Abudayyeh OO, et al. Cpf1 is a single RNA-guided endonuclease of a class 2 CRISPR-Cas system. Cell. 2015;163:759–771.
   PubMed Web of Science ®Google Scholar
• Marraffini LA, Sontheimer EJ. Self versus non-self discrimination during CRISPR RNA-directed immunity. Nature. 2010;463:568–571.
   PubMed Web of Science ®Google Scholar
• Osawa T, Inanaga H, Sato C, et al. Crystal structure of the CRISPR-Cas RNA silencing Cmr complex bound to a target analog. Mol Cell. 2015;58:418–430.
   PubMed Web of Science ®Google Scholar
• Taylor DW, Zhu Y, Staals RH, et al. Structural biology. Structures of the CRISPR-Cmr complex reveal mode of RNA target positioning. Science. 2015;348:581–585.
   PubMedGoogle Scholar
• You L, Ma J, Wang J, et al. Structure Studies of the CRISPR-Csm Complex Reveal Mechanism of Co-transcriptional Interference. Cell. 2019;176:239–53 e16.
   PubMed Web of Science ®Google Scholar
• Jia N, Mo CY, Wang C, et al. Type III-A CRISPR-Cas Csm complexes: assembly, periodic RNA cleavage, DNase activity regulation, and autoimmunity. Mol Cell. 2018;73:264–73 e5.
   PubMed Web of Science ®Google Scholar
• Golovanov IB, Zhenodarova SM, Ivanitskii GR. Structure-property correlation and prediction of melting temperature of RNA duplexes. Doklady biological sciences: proceedings of the Academy of Sciences of the USSR. Bio sci Sect. 2001;380:504–507.
   Google Scholar
• Meeske AJ, Marraffini LA. RNA guide complementarity prevents self-targeting in type VI CRISPR systems. Mol Cell. 2018;71:791–801 e3.
   PubMed Web of Science ®Google Scholar
• Lasa I, Toledo-Arana A, Dobin A, et al. Genome-wide antisense transcription drives mRNA processing in bacteria. Proc Natl Acad Sci U S A. 2011;108:20172–20177.
   PubMed Web of Science ®Google Scholar
• Lillestol RK, Shah SA, Brugger K, et al. CRISPR families of the crenarchaeal genus sulfolobus: bidirectional transcription and dynamic properties. Mol Microbiol. 2009;72:259–272.
   PubMed Web of Science ®Google Scholar
• Pyenson NC, Gayvert K, Varble A, et al. Broad targeting specificity during bacterial type III CRISPR-Cas immunity constrains viral escape. Cell Host Microbe. 2017;22:343–53 e3.
   PubMed Web of Science ®Google Scholar
• Silas S, Lucas-Elio P, Jackson SA, et al. Type III CRISPR-Cas systems can provide redundancy to counteract viral escape from type I systems. eLife. 2017;6:e27601.
   PubMed Web of Science ®Google Scholar
• Gleditzsch D, Pausch P, Muller-Esparza H, et al. PAM identification by CRISPR-Cas effector complexes: diversified mechanisms and structures. Rna Biol. 2018;16:1–14.
   Web of Science ®Google Scholar
• Hale CR, Cocozaki A, Li H, et al. Target RNA capture and cleavage by the Cmr type III-B CRISPR-Cas effector complex. Genes Dev. 2014;28:2432–2443.
   PubMed Web of Science ®Google Scholar
• Li Y, Zhang Y, Lin J, et al. Cmr1 enables efficient RNA and DNA interference of a III-B CRISPR-Cas system by binding to target RNA and crRNA. Nucleic Acids Res. 2017;45:11305–11314.
   PubMed Web of Science ®Google Scholar
• Mogila I, Kazlauskiene M, Valinskyte S, et al. Genetic dissection of the type III-A CRISPR-Cas system csm complex reveals roles of individual subunits. Cell Rep. 2019;26:2753–65 e4.
   PubMed Web of Science ®Google Scholar
• Peng N, Deng L, Mei Y, et al. A synthetic arabinose-inducible promoter confers high levels of recombinant protein expression in hyperthermophilic archaeon sulfolobus islandicus. Appl Environ Microbiol. 2012;78:5630–5637.
   PubMed Web of Science ®Google Scholar
• Warrens AN, Jones MD, Lechler RI. Splicing by overlap extension by PCR using asymmetric amplification: an improved technique for the generation of hybrid proteins of immunological interest. Gene. 1997;186:29–35.
   PubMed Web of Science ®Google Scholar
• Peng N, Han W, Li Y, et al. Genetic technologies for extremely thermophilic microorganisms of sulfolobus, the only genetically tractable genus of crenarchaea. Sci China Life Sci. 2017;60:370–385.
   PubMed Web of Science ®Google Scholar
• Zhang J, White MF. Expression and purification of the CMR (Type III-B) complex in sulfolobus solfataricus. Methods Mol Biol. 2015;1311:185–194.
   PubMedGoogle Scholar
• Robert X, Gouet P. Deciphering key features in protein structures with the new ENDscript server. Nucleic Acids Res. 2014;42:W320–4.
   PubMed Web of Science ®Google Scholar