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Research Paper

A seed motif for target RNA capture enables efficient immune defence by a type III-B CRISPR-Cas system

, , , , , , , ORCID Icon & ORCID Icon show all
Pages 1166-1178 | Received 21 Feb 2019, Accepted 06 May 2019, Published online: 26 May 2019

References

  • Horvath P, Barrangou R. CRISPR/Cas, the immune system of bacteria and archaea. Science. 2010;327:167–170.
  • Barrangou R, Marraffini LA. CRISPR-Cas systems: prokaryotes upgrade to adaptive immunity. Mol Cell. 2014;54:234–244.
  • van der Oost J, Westra ER, Jackson RN, et al. Unravelling the structural and mechanistic basis of CRISPR-Cas systems. Nat Rev Microbiol. 2014;12:479–492.
  • Mohanraju P, Makarova KS, Zetsche B, et al. Diverse evolutionary roots and mechanistic variations of the CRISPR-Cas systems. Science. 2016;353:aad5147.
  • Makarova KS, Zhang F, Koonin EV. SnapShot: class 1 CRISPR-Cas systems. Cell. 2017;168(946–946):e941.
  • Makarova KS, Zhang F, Koonin EV. SnapShot: class 2 CRISPR-Cas systems. Cell. 2017;168(328–328):e321.
  • Rollie C, Schneider S, Brinkmann AS, et al. Intrinsic sequence specificity of the Cas1 integrase directs new spacer acquisition. Elife. 2015;4:e08716.
  • Arslan Z, Hermanns V, Wurm R, et al. Detection and characterization of spacer integration intermediates in type I-E CRISPR-Cas system. Nucleic Acids Res. 2014;42:7884–7893.
  • Silas S, Mohr G, Sidote DJ, et al. Direct CRISPR spacer acquisition from RNA by a natural reverse transcriptase-Cas1 fusion protein. Science. 2016;351:aad4234.
  • Xiao Y, Ng S, Nam KH, et al. How type II CRISPR-Cas establish immunity through Cas1-Cas2-mediated spacer integration. Nature. 2017;550:137–141.
  • Bhaya D, Davison M, Barrangou R. CRISPR-Cas systems in bacteria and archaea: versatile small RNAs for adaptive defense and regulation. Annu Rev Genet. 2011;45:273–297.
  • Charpentier E, Richter H, van der Oost J, et al. Biogenesis pathways of RNA guides in archaeal and bacterial CRISPR-Cas adaptive immunity. FEMS Microbiol Rev. 2015;39:428–441.
  • Brouns SJ, Jore MM, Lundgren M, et al. Small CRISPR RNAs guide antiviral defense in prokaryotes. Science. 2008;321:960–964.
  • Plagens A, Richter H, Charpentier E, et al. DNA and RNA interference mechanisms by CRISPR-Cas surveillance complexes. FEMS Microbiol Rev. 2015;39:442–463.
  • Anders C, Niewoehner O, Duerst A, et al. Structural basis of PAM-dependent target DNA recognition by the Cas9 endonuclease. Nature. 2014;513:569–573.
  • Westra ER, Semenova E, Datsenko KA, et al. Type I-E CRISPR-cas systems discriminate target from non-target DNA through base pairing-independent PAM recognition. PLoS Genet. 2013;9:e1003742.
  • Mojica FJ, Diez-Villasenor C, Garcia-Martinez J, et al. Short motif sequences determine the targets of the prokaryotic CRISPR defence system. Microbiology. 2009;155:733–740.
  • 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.
  • Zhang J, Rouillon C, Kerou M, et al. Structure and mechanism of the CMR complex for CRISPR-mediated antiviral immunity. Mol Cell. 2012;45:303–313.
  • Zebec Z, Manica A, Zhang J, et al. CRISPR-mediated targeted mRNA degradation in the archaeon Sulfolobus solfataricus. Nucleic Acids Res. 2014;42:5280–5288.
  • Peng W, Feng M, Feng X, et al. An archaeal CRISPR type III-B system exhibiting distinctive RNA targeting features and mediating dual RNA and DNA interference. Nucleic Acids Res. 2015;43:406–417.
  • Zhang J, Graham S, Tello A, et al. Multiple nucleic acid cleavage modes in divergent type III CRISPR systems. Nucleic Acids Res. 2016;44:1789–1799.
  • Deng L, Garrett RA, Shah SA, et al. A novel interference mechanism by a type IIIB CRISPR-Cmr module in Sulfolobus. Mol Microbiol. 2013;87:1088–1099.
  • Goldberg GW, Jiang W, Bikard D, et al. Conditional tolerance of temperate phages via transcription-dependent CRISPR-Cas targeting. Nature. 2014;514:633–637.
  • Samai P, Pyenson N, Jiang W, et al. Co-transcriptional DNA and RNA cleavage during Type III CRISPR-Cas immunity. Cell. 2015;161:1164–1174.
  • 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.
  • 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.
  • 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.
  • Liu TY, Iavarone AT, Doudna JA. RNA and DNA targeting by a reconstituted thermus thermophilus Type III-A CRISPR-Cas system. PLoS One. 2017;12:e0170552.
  • 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.
  • Marraffini LA, Sontheimer EJ. Self versus non-self discrimination during CRISPR RNA-directed immunity. Nature. 2010;463:568–571.
  • Jackson RN, Wiedenheft B. A conserved structural chassis for mounting versatile CRISPR RNA-guided immune responses. Mol Cell. 2015;58:722–728.
  • Kazlauskiene M, Kostiuk G, Venclovas C, et al. A cyclic oligonucleotide signaling pathway in type III CRISPR-Cas systems. Science. 2017;357:605–609.
  • Niewoehner O, Garcia-Doval C, Rostol JT, et al. Type III CRISPR-Cas systems produce cyclic oligoadenylate second messengers. Nature. 2017;548:543–548.
  • 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.
  • Rouillon C, Athukoralage JS, Graham S, et al. Control of cyclic oligoadenylate synthesis in a type III CRISPR system. Elife. 2018;7:e36734.
  • Wang L, Mo CY, Wasserman MR, et al. Dynamics of Cas10 govern discrimination between self and non-self in Type III CRISPR-Cas immunity. Mol Cell. 2019;73(278–290):e4.
  • You L, Ma J, Wang J, et al. Structure studies of the CRISPR-Csm complex reveal mechanism of co-transcriptional interference. Cell. 2019;176(239–253):e16.
  • Athukoralage JS, Rouillon C, Graham S, et al. Ring nucleases deactivate type III CRISPR ribonucleases by degrading cyclic oligoadenylate. Nature. 2018;562:277–280.
  • Gorski SA, Vogel J, Doudna JA. RNA-based recognition and targeting: sowing the seeds of specificity. Nat Rev Mol Cell Biol. 2017;18:215–228.
  • Bartel DP. MicroRNAs: target recognition and regulatory functions. Cell. 2009;136:215–233.
  • Kunne T, Swarts DC, Brouns SJ. Planting the seed: target recognition of short guide RNAs. Trends Microbiol. 2014;22:74–83.
  • Semenova E, Jore MM, Datsenko KA, et al. Interference by clustered regularly interspaced short palindromic repeat (CRISPR) RNA is governed by a seed sequence. Proc Natl Acad Sci U S A. 2011;108:10098–10103.
  • Wiedenheft B, van Duijn E, Bultema JB, et al. RNA-guided complex from a bacterial immune system enhances target recognition through seed sequence interactions. Proc Natl Acad Sci U S A. 2011;108:10092–10097.
  • Sternberg SH, Redding S, Jinek M, et al. DNA interrogation by the CRISPR RNA-guided endonuclease Cas9. Nature. 2014;507:62–67.
  • Blosser TR, Loeff L, Westra ER, et al. Two distinct DNA binding modes guide dual roles of a CRISPR-Cas protein complex. Mol Cell. 2015;58:60–70.
  • Lim Y, Bak SY, Sung K, et al. Structural roles of guide RNAs in the nuclease activity of Cas9 endonuclease. Nat Commun. 2016;7:13350.
  • Swarts DC, van der Oost J, Jinek M. Structural basis for guide RNA processing and seed-dependent DNA targeting by CRISPR-Cas12a. Mol Cell. 2017;66(221–233):e224.
  • Jinek M, Chylinski K, Fonfara I, et al. A programmable dual-RNA-guided DNA endonuclease in adaptive bacterial immunity. Science. 2012;337:816–821.
  • Abudayyeh OO, Gootenberg JS, Konermann S, et al. C2c2 is a single-component programmable RNA-guided RNA-targeting CRISPR effector. Science. 2016;353:aaf5573.
  • Liu L, Li X, Wang J, et al. Two distant catalytic sites are responsible for C2c2 RNase activities. Cell. 2017;168(121–134):e112.
  • Smargon AA, Cox DB, Pyzocha NK, et al. Cas13b is a type VI-B CRISPR-associated RNA-guided RNase differentially regulated by accessory proteins Csx27 and Csx28. Mol Cell. 2017;65(618–630):e617.
  • Maniv I, Jiang W, Bikard D, et al. Impact of different target sequences on Type III CRISPR-Cas immunity. J Bacteriol. 2016;198:941–950.
  • 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.
  • 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.
  • Gudbergsdottir S, Deng L, Chen Z, et al. Dynamic properties of the Sulfolobus CRISPR/Cas and CRISPR/Cmr systems when challenged with vector-borne viral and plasmid genes and protospacers. Mol Microbiol. 2011;79:35–49.
  • Spilman M, Cocozaki A, Hale C, et al. Structure of an RNA silencing complex of the CRISPR-Cas immune system. Mol Cell. 2013;52:146–152.
  • Staals RHJ, 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.
  • 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.
  • Hale CR, Zhao P, Olson S, et al. RNA-guided RNA cleavage by a CRISPR RNA-Cas protein complex. Cell. 2009;139:945–956.
  • 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.
  • 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;22:343–353.e3.
  • Hatoum-Aslan A, Maniv I, Marraffini LA. Mature clustered, regularly interspaced, short palindromic repeats RNA (crRNA) length is measured by a ruler mechanism anchored at the precursor processing site. Proc Natl Acad Sci U S A. 2011;108:21218–21222.
  • Staals RH, Zhu Y, Taylor DW, et al. RNA targeting by the type III-A CRISPR-Cas Csm complex of thermus thermophilus. Mol Cell. 2014;56:518–530.
  • Hatoum-Aslan A, Samai P, Maniv I, et al. A ruler protein in a complex for antiviral defense determines the length of small interfering CRISPR RNAs. J Biol Chem. 2013;288:27888–27897.
  • Walker FC, Chou-Zheng L, Dunkle JA, et al. Molecular determinants for CRISPR RNA maturation in the Cas10-Csm complex and roles for non-Cas nucleases. Nucleic Acids Res. 2017;45:2112–2123.
  • 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.
  • Brennecke J, Stark A, Russell RB, et al. Principles of microRNA-target recognition. PLoS Biol. 2005;3:e85.
  • Storz G, Vogel J, Wassarman KM. Regulation by small RNAs in bacteria: expanding frontiers. Mol Cell. 2011;43:880–891.
  • Bandyra KJ, Said N, Pfeiffer V, et al. The seed region of a small RNA drives the controlled destruction of the target mRNA by the endoribonuclease RNase E. Mol Cell. 2012;47:943–953.
  • Deng L, Zhu H, Chen Z, et al. Unmarked gene deletion and host-vector system for the hyperthermophilic crenarchaeon Sulfolobus islandicus. Extremophiles. 2009;13:735–746.
  • Li Y, Pan S, Zhang Y, et al. Harnessing Type I and Type III CRISPR-Cas systems for genome editing. Nucleic Acids Res. 2016;44:e34.
  • 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.
  • Peng N, Xia Q, Chen Z, et al. An upstream activation element exerting differential transcriptional activation on an archaeal promoter. Mol Microbiol. 2009;74:928–939.

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