The Biology of CRISPR-Cas: Backward and Forward

Cell

Volumn 172, Issue 6, 2018, Pages 1239-1259

  Hille, Frank ^a,c   Richter, Hagen ^a   Wong, Shi Pey ^a,b,c   Bratovič, Majda ^a,c   Ressel, Sarah ^a   Charpentier, Emmanuelle ^a,b,c  

^a MAX PLANCK INSTITUTE FOR INFECTION BIOLOGY   (Germany)

^b UMEÅ UNIVERSITY   (Sweden)

^c HUMBOLDT UNIVERSITY   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

CRISPR ASSOCIATED PROTEIN; DNA; NUCLEIC ACID; RNA;

BACTERIOPHAGE; BIOGENESIS; CRISPR CAS SYSTEM; DNA INTEGRATION; EVOLUTIONARY ADAPTATION; GENE EXPRESSION; GENETIC SELECTION; HOST PATHOGEN INTERACTION; HUMAN; IMMUNITY; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN PROCESSING; REVIEW; RNA INTERFERENCE; ADAPTIVE IMMUNITY; BACTERIUM; BIOLOGICAL MODEL; BIOLOGY; GENE EXPRESSION REGULATION; GENETICS; PHYSIOLOGY; SIGNAL TRANSDUCTION; TRENDS; VIROLOGY;

ADAPTIVE IMMUNITY; BACTERIA; BACTERIOPHAGES; BIOLOGY; CRISPR-CAS SYSTEMS; GENE EXPRESSION REGULATION, BACTERIAL; MODELS, GENETIC; SIGNAL TRANSDUCTION;

EID: 85043332333     PISSN: 00928674     EISSN: 10974172     Source Type: Journal    
DOI: 10.1016/j.cell.2017.11.032     Document Type: Review

References (230)

1. Abedon, S.T., Spatial vulnerability: bacterial arrangements, microcolonies, and biofilms as responses to low rather than high phage densities. Viruses 4 (2012), 663–687.
2. Abudayyeh, O.O., Gootenberg, J.S., Konermann, S., Joung, J., Slaymaker, I.M., Cox, D.B.T., Shmakov, S., Makarova, K.S., Semenova, E., Minakhin, L., et al. C2c2 is a single-component programmable RNA-guided RNA-targeting CRISPR effector. Science, 353, 2016, aaf5573.
3. Agari, Y., Sakamoto, K., Tamakoshi, M., Oshima, T., Kuramitsu, S., Shinkai, A., Transcription profile of Thermus thermophilus CRISPR systems after phage infection. J. Mol. Biol. 395 (2010), 270–281.
4. 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, 2013, 15.
5. Anders, C., Niewoehner, O., Duerst, A., Jinek, M., Structural basis of PAM-dependent target DNA recognition by the Cas9 endonuclease. Nature 513 (2014), 569–573.
6. Arslan, Z., Wurm, R., Brener, O., Ellinger, P., Nagel-Steger, L., Oesterhelt, F., Schmitt, L., Willbold, D., Wagner, R., Gohlke, H., et al. Double-strand DNA end-binding and sliding of the toroidal CRISPR-associated protein Csn2. Nucleic Acids Res. 41 (2013), 6347–6359.
7. Babu, M., Beloglazova, N., Flick, R., Graham, C., Skarina, T., Nocek, B., Gagarinova, A., Pogoutse, O., Brown, G., Binkowski, A., et al. A dual function of the CRISPR-Cas system in bacterial antivirus immunity and DNA repair. Mol. Microbiol. 79 (2011), 484–502.
8. Barrangou, R., Fremaux, C., Deveau, H., Richards, M., Boyaval, P., Moineau, S., Romero, D.A., Horvath, P., CRISPR provides acquired resistance against viruses in prokaryotes. Science 315 (2007), 1709–1712.
9. Bikard, D., Hatoum-Aslan, A., Mucida, D., Marraffini, L.A., CRISPR interference can prevent natural transformation and virulence acquisition during in vivo bacterial infection. Cell Host Microbe 12 (2012), 177–186.
10. Blosser, T.R., Loeff, L., Westra, E.R., Vlot, M., Künne, T., Sobota, M., Dekker, C., Brouns, S.J.J., Joo, C., Two distinct DNA binding modes guide dual roles of a CRISPR-Cas protein complex. Mol. Cell 58 (2015), 60–70.
11. Bolotin, A., Quinquis, B., Sorokin, A., Ehrlich, S.D., Clustered regularly interspaced short palindrome repeats (CRISPRs) have spacers of extrachromosomal origin. Microbiology 151 (2005), 2551–2561.
12. Bondy-Denomy, J., Pawluk, A., Maxwell, K.L., Davidson, A.R., Bacteriophage genes that inactivate the CRISPR/Cas bacterial immune system. Nature 493 (2013), 429–432.
13. Bondy-Denomy, J., Garcia, B., Strum, S., Du, M., Rollins, M.F., Hidalgo-Reyes, Y., Wiedenheft, B., Maxwell, K.L., Davidson, A.R., Multiple mechanisms for CRISPR-Cas inhibition by anti-CRISPR proteins. Nature 526 (2015), 136–139.
14. Boysen, A., Ellehauge, E., Julien, B., Søgaard-Andersen, L., The DevT protein stimulates synthesis of FruA, a signal transduction protein required for fruiting body morphogenesis in Myxococcus xanthus. J. Bacteriol. 184 (2002), 1540–1546.
15. Brouns, S.J., Jore, M.M., Lundgren, M., Westra, E.R., Slijkhuis, R.J., Snijders, A.P., Dickman, M.J., Makarova, K.S., Koonin, E.V., van der Oost, J., Small CRISPR RNAs guide antiviral defense in prokaryotes. Science 321 (2008), 960–964.
16. Cady, K.C., O'Toole, G.A., Non-identity-mediated CRISPR-bacteriophage interaction mediated via the Csy and Cas3 proteins. J. Bacteriol. 193 (2011), 3433–3445.
17. Carte, J., Wang, R., Li, H., Terns, R.M., Terns, M.P., Cas6 is an endoribonuclease that generates guide RNAs for invader defense in prokaryotes. Genes Dev. 22 (2008), 3489–3496.
18. Carte, J., Pfister, N.T., Compton, M.M., Terns, R.M., Terns, M.P., Binding and cleavage of CRISPR RNA by Cas6. RNA 16 (2010), 2181–2188.
19. Charpentier, E., Richter, H., van der Oost, J., White, M.F., Biogenesis pathways of RNA guides in archaeal and bacterial CRISPR-Cas adaptive immunity. FEMS Microbiol. Rev. 39 (2015), 428–441.
20. Chowdhury, S., Carter, J., Rollins, M.F., Golden, S.M., Jackson, R.N., Hoffmann, C., Nosaka, L., Bondy-Denomy, J., Maxwell, K.L., Davidson, A.R., et al. Structure Reveals Mechanisms of Viral Suppressors that Intercept a CRISPR RNA-Guided Surveillance Complex. Cell 169 (2017), 47–57.
21. Chylinski, K., Le Rhun, A., Charpentier, E., The tracrRNA and Cas9 families of type II CRISPR-Cas immunity systems. RNA Biol. 10 (2013), 726–737.
22. Dagdas, Y.S., Chen, J.S., Sternberg, S.H., Doudna, J.A., Yildiz, A., A conformational checkpoint between DNA binding and cleavage by CRISPR-Cas9. Sci. Adv., 3, 2017, eaao0027.
23. Datsenko, K.A., Pougach, K., Tikhonov, A., Wanner, B.L., Severinov, K., Semenova, E., Molecular memory of prior infections activates the CRISPR/Cas adaptive bacterial immunity system. Nat. Commun., 3, 2012, 945.
24. Deltcheva, E., Chylinski, K., Sharma, C.M., Gonzales, K., Chao, Y., Pirzada, Z.A., Eckert, M.R., Vogel, J., Charpentier, E., CRISPR RNA maturation by trans-encoded small RNA and host factor RNase III. Nature 471 (2011), 602–607.
25. 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 (2013), 1088–1099.
26. Depardieu, F., Didier, J.-P., Bernheim, A., Sherlock, A., Molina, H., Duclos, B., Bikard, D., A Eukaryotic-like Serine/Threonine Kinase Protects Staphylococci against Phages. Cell Host Microbe 20 (2016), 471–481.
27. Deveau, H., Barrangou, R., Garneau, J.E., Labonté, J., Fremaux, C., Boyaval, P., Romero, D.A., Horvath, P., Moineau, S., Phage response to CRISPR-encoded resistance in Streptococcus thermophilus. J. Bacteriol. 190 (2008), 1390–1400.
28. Dillingham, M.S., Kowalczykowski, S.C., RecBCD enzyme and the repair of double-stranded DNA breaks. Microbiol. Mol. Biol. Rev. 72 (2008), 642–671.
29. Dong, D., Ren, K., Qiu, X., Zheng, J., Guo, M., Guan, X., Liu, H., Li, N., Zhang, B., Yang, D., et al. The crystal structure of Cpf1 in complex with CRISPR RNA. Nature 532 (2016), 522–526.
30. Dong, D., Guo, M., Wang, S., Zhu, Y., Wang, S., Xiong, Z., Yang, J., Xu, Z., Huang, Z., Structural basis of CRISPR-SpyCas9 inhibition by an anti-CRISPR protein. Nature 546 (2017), 436–439.
31. Dugar, G., Herbig, A., Förstner, K.U., Heidrich, N., Reinhardt, R., Nieselt, K., Sharma, C.M., High-resolution transcriptome maps reveal strain-specific regulatory features of multiple Campylobacter jejuni isolates. PLoS Genet., 9, 2013, e1003495.
32. Dupuis, M.-È., Villion, M., Magadán, A.H., Moineau, S., CRISPR-Cas and restriction-modification systems are compatible and increase phage resistance. Nat. Commun., 4, 2013, 2087.
33. East-Seletsky, A., O'Connell, M.R., Knight, S.C., Burstein, D., Cate, J.H.D., Tjian, R., Doudna, J.A., Two distinct RNase activities of CRISPR-C2c2 enable guide-RNA processing and RNA detection. Nature 538 (2016), 270–273.
34. East-Seletsky, A., O'Connell, M.R., Burstein, D., Knott, G.J., Doudna, J.A., RNA Targeting by Functionally Orthogonal Type VI-A CRISPR-Cas Enzymes. Mol. Cell 66 (2017), 373–383.
35. Elmore, J.R., Sheppard, N.F., Ramia, N., Deighan, T., Li, H., Terns, R.M., Terns, M.P., Bipartite recognition of target RNAs activates DNA cleavage by the Type III-B CRISPR-Cas system. Genes Dev. 30 (2016), 447–459.
36. Estrella, M.A., Kuo, F.-T., Bailey, S., RNA-activated DNA cleavage by the Type III-B CRISPR-Cas effector complex. Genes Dev. 30 (2016), 460–470.
37. Fagerlund, R.D., Wilkinson, M.E., Klykov, O., Barendregt, A., Pearce, F.G., Kieper, S.N., Maxwell, H.W.R., Capolupo, A., Heck, A.J.R., Krause, K.L., et al. Spacer capture and integration by a type I-F Cas1-Cas2-3 CRISPR adaptation complex. Proc. Natl. Acad. Sci. USA 114 (2017), E5122–E5128.
38. Fineran, P.C., Gerritzen, M.J.H., Suárez-Diez, M., Künne, T., Boekhorst, J., van Hijum, S.A.F.T., Staals, R.H.J., Brouns, S.J.J., Degenerate target sites mediate rapid primed CRISPR adaptation. Proc. Natl. Acad. Sci. USA 111 (2014), E1629–E1638.
39. Fonfara, I., Le Rhun, A., Chylinski, K., Makarova, K.S., Lécrivain, A.-L., Bzdrenga, J., Koonin, E.V., Charpentier, E., Phylogeny of Cas9 determines functional exchangeability of dual-RNA and Cas9 among orthologous type II CRISPR-Cas systems. Nucleic Acids Res. 42 (2014), 2577–2590.
40. Fonfara, I., Richter, H., Bratovič, M., Le Rhun, A., Charpentier, E., The CRISPR-associated DNA-cleaving enzyme Cpf1 also processes precursor CRISPR RNA. Nature 532 (2016), 517–521.
41. Fusco, S., Liguori, R., Limauro, D., Bartolucci, S., She, Q., Contursi, P., Transcriptome analysis of Sulfolobus solfataricus infected with two related fuselloviruses reveals novel insights into the regulation of CRISPR-Cas system. Biochimie 118 (2015), 322–332.
42. Gao, P., Yang, H., Rajashankar, K.R., Huang, Z., Patel, D.J., Type V CRISPR-Cas Cpf1 endonuclease employs a unique mechanism for crRNA-mediated target DNA recognition. Cell Res. 26 (2016), 901–913.
43. Garneau, J.E., Dupuis, M.-È., Villion, M., Romero, D.A., Barrangou, R., Boyaval, P., Fremaux, C., Horvath, P., Magadán, A.H., Moineau, S., The CRISPR/Cas bacterial immune system cleaves bacteriophage and plasmid DNA. Nature 468 (2010), 67–71.
44. Garside, E.L., Schellenberg, M.J., Gesner, E.M., Bonanno, J.B., Sauder, J.M., Burley, S.K., Almo, S.C., Mehta, G., MacMillan, A.M., Cas5d processes pre-crRNA and is a member of a larger family of CRISPR RNA endonucleases. RNA 18 (2012), 2020–2028.
45. Gasiunas, G., Barrangou, R., Horvath, P., Siksnys, V., Cas9-crRNA ribonucleoprotein complex mediates specific DNA cleavage for adaptive immunity in bacteria. Proc. Natl. Acad. Sci. USA 109 (2012), E2579–E2586.
46. 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. Nat. Struct. Mol. Biol. 18 (2011), 688–692.
47. Gleditzsch, D., Müller-Esparza, H., Pausch, P., Sharma, K., Dwarakanath, S., Urlaub, H., Bange, G., Randau, L., Modulating the Cascade architecture of a minimal Type I-F CRISPR-Cas system. Nucleic Acids Res. 44 (2016), 5872–5882.
48. Goldberg, G.W., Jiang, W., Bikard, D., Marraffini, L.A., Conditional tolerance of temperate phages via transcription-dependent CRISPR-Cas targeting. Nature 514 (2014), 633–637.
49. Goldfarb, T., Sberro, H., Weinstock, E., Cohen, O., Doron, S., Charpak-Amikam, Y., Afik, S., Ofir, G., Sorek, R., BREX is a novel phage resistance system widespread in microbial genomes. EMBO J. 34 (2015), 169–183.
50. Goren, M.G., Doron, S., Globus, R., Amitai, G., Sorek, R., Qimron, U., Repeat Size Determination by Two Molecular Rulers in the Type I-E CRISPR Array. Cell Rep. 16 (2016), 2811–2818.
51. Grissa, I., Vergnaud, G., Pourcel, C., The CRISPRdb database and tools to display CRISPRs and to generate dictionaries of spacers and repeats. BMC Bioinformatics, 8, 2007, 172.
52. Gudbergsdottir, S., Deng, L., Chen, Z., Jensen, J.V., Jensen, L.R., She, Q., Garrett, R.A., Dynamic properties of the Sulfolobus CRISPR/Cas and CRISPR/Cmr systems when challenged with vector-borne viral and plasmid genes and protospacers. Mol. Microbiol. 79 (2011), 35–49.
53. Gunderson, F.F., Cianciotto, N.P., The CRISPR-associated gene cas2 of Legionella pneumophila is required for intracellular infection of amoebae. MBio, 4, 2013 e00074–13.
54. Gunderson, F.F., Mallama, C.A., Fairbairn, S.G., Cianciotto, N.P., Nuclease activity of Legionella pneumophila Cas2 promotes intracellular infection of amoebal host cells. Infect. Immun. 83 (2015), 1008–1018.
55. Guo, T.W., Bartesaghi, A., Yang, H., Falconieri, V., Rao, P., Merk, A., Eng, E.T., Raczkowski, A.M., Fox, T., Earl, L.A., et al. Cryo-EM Structures Reveal Mechanism and Inhibition of DNA Targeting by a CRISPR-Cas Surveillance Complex. Cell 171 (2017), 414–426.
56. Haft, D.H., Selengut, J., Mongodin, E.F., Nelson, K.E., A guild of 45 CRISPR-associated (Cas) protein families and multiple CRISPR/Cas subtypes exist in prokaryotic genomes. PLoS Comput. Biol., 1, 2005, e60.
57. Hall, A.R., Scanlan, P.D., Morgan, A.D., Buckling, A., Host-parasite coevolutionary arms races give way to fluctuating selection. Ecol. Lett. 14 (2011), 635–642.
58. Hatoum-Aslan, A., Maniv, I., Marraffini, L.A., 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. USA 108 (2011), 21218–21222.
59. 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 (2013), 27888–27897.
60. 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 (2014), 310–317.
61. Haurwitz, R.E., Jinek, M., Wiedenheft, B., Zhou, K., Doudna, J.A., Sequence- and structure-specific RNA processing by a CRISPR endonuclease. Science 329 (2010), 1355–1358.
62. Hayes, R.P., Xiao, Y., Ding, F., van Erp, P.B.G., Rajashankar, K., Bailey, S., Wiedenheft, B., Ke, A., Structural basis for promiscuous PAM recognition in type I-E Cascade from E. coli. Nature 530 (2016), 499–503.
63. 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 (2016), 1902–1913.
64. Heler, R., Samai, P., Modell, J.W., Weiner, C., Goldberg, G.W., Bikard, D., Marraffini, L.A., Cas9 specifies functional viral targets during CRISPR-Cas adaptation. Nature 519 (2015), 199–202.
65. Heussler, G.E., Cady, K.C., Koeppen, K., Bhuju, S., Stanton, B.A., O'Toole, G.A., Clustered Regularly Interspaced Short Palindromic Repeat-Dependent, Biofilm-Specific Death of Pseudomonas aeruginosa Mediated by Increased Expression of Phage-Related Genes. MBio, 6, 2015 e00129–15.
66. Hirano, H., Gootenberg, J.S., Horii, T., Abudayyeh, O.O., Kimura, M., Hsu, P.D., Nakane, T., Ishitani, R., Hatada, I., Zhang, F., et al. Structure and Engineering of Francisella novicida Cas9. Cell 164 (2016), 950–961.
67. Hochstrasser, M.L., Taylor, D.W., Bhat, P., Guegler, C.K., Sternberg, S.H., Nogales, E., Doudna, J.A., CasA mediates Cas3-catalyzed target degradation during CRISPR RNA-guided interference. Proc. Natl. Acad. Sci. USA 111 (2014), 6618–6623.
68. Hochstrasser, M.L., Taylor, D.W., Kornfeld, J.E., Nogales, E., Doudna, J.A., DNA Targeting by a Minimal CRISPR RNA-Guided Cascade. Mol. Cell 63 (2016), 840–851.
69. Hooton, S.P.T., Connerton, I.F., Campylobacter jejuni acquire new host-derived CRISPR spacers when in association with bacteriophages harboring a CRISPR-like Cas4 protein. Front. Microbiol., 5, 2015, 744.
70. Høyland-Kroghsbo, N.M., Paczkowski, J., Mukherjee, S., Broniewski, J., Westra, E., Bondy-Denomy, J., Bassler, B.L., Quorum sensing controls the Pseudomonas aeruginosa CRISPR-Cas adaptive immune system. Proc. Natl. Acad. Sci. USA 114 (2017), 131–135.
71. Huo, Y., Nam, K.H., Ding, F., Lee, H., Wu, L., Xiao, Y., Farchione, M.D. Jr., Zhou, S., Rajashankar, K., Kurinov, I., et al. Structures of CRISPR Cas3 offer mechanistic insights into Cascade-activated DNA unwinding and degradation. Nat. Struct. Mol. Biol. 21 (2014), 771–777.
72. Iranzo, J., Lobkovsky, A.E., Wolf, Y.I., Koonin, E.V., Evolutionary dynamics of the prokaryotic adaptive immunity system CRISPR-Cas in an explicit ecological context. J. Bacteriol. 195 (2013), 3834–3844.
73. Ishino, Y., Shinagawa, H., Makino, K., Amemura, M., Nakata, A., Nucleotide sequence of the iap gene, responsible for alkaline phosphatase isozyme conversion in Escherichia coli, and identification of the gene product. J. Bacteriol. 169 (1987), 5429–5433.
74. Jackson, R.N., Golden, S.M., van Erp, P.B.G., Carter, J., Westra, E.R., Brouns, S.J.J., van der Oost, J., Terwilliger, T.C., Read, R.J., Wiedenheft, B., Structural biology. Crystal structure of the CRISPR RNA-guided surveillance complex from Escherichia coli. Science 345 (2014), 1473–1479.
75. Jansen, R., Embden, J.D., Gaastra, W., Schouls, L.M., Identification of genes that are associated with DNA repeats in prokaryotes. Mol. Microbiol. 43 (2002), 1565–1575.
76. Jiang, F., Doudna, J.A., CRISPR-Cas9 Structures and Mechanisms. Annu. Rev. Biophys. 46 (2017), 505–529.
77. Jiang, W., Maniv, I., Arain, F., Wang, Y., Levin, B.R., Marraffini, L.A., Dealing with the evolutionary downside of CRISPR immunity: bacteria and beneficial plasmids. PLoS Genet., 9, 2013, e1003844.
78. Jiang, F., Zhou, K., Ma, L., Gressel, S., Doudna, J.A., STRUCTURAL BIOLOGY. A Cas9-guide RNA complex preorganized for target DNA recognition. Science 348 (2015), 1477–1481.
79. Jiang, F., Taylor, D.W., Chen, J.S., Kornfeld, J.E., Zhou, K., Thompson, A.J., Nogales, E., Doudna, J.A., Structures of a CRISPR-Cas9 R-loop complex primed for DNA cleavage. Science 351 (2016), 867–871.
80. Jiang, W., Samai, P., Marraffini, L.A., Degradation of Phage Transcripts by CRISPR-Associated RNases Enables Type III CRISPR-Cas Immunity. Cell 164 (2016), 710–721.
81. Jinek, M., Chylinski, K., Fonfara, I., Hauer, M., Doudna, J.A., Charpentier, E., A programmable dual-RNA-guided DNA endonuclease in adaptive bacterial immunity. Science 337 (2012), 816–821.
82. Jinek, M., Jiang, F., Taylor, D.W., Sternberg, S.H., Kaya, E., Ma, E., Anders, C., Hauer, M., Zhou, K., Lin, S., et al. Structures of Cas9 endonucleases reveal RNA-mediated conformational activation. Science, 343, 2014, 1247997.
83. Jore, M.M., Lundgren, M., van Duijn, E., Bultema, J.B., Westra, E.R., Waghmare, S.P., Wiedenheft, B., Pul, U., Wurm, R., Wagner, R., et al. Structural basis for CRISPR RNA-guided DNA recognition by Cascade. Nat. Struct. Mol. Biol. 18 (2011), 529–536.
84. Ka, D., Lee, H., Jung, Y.-D., Kim, K., Seok, C., Suh, N., Bae, E., Crystal Structure of Streptococcus pyogenes Cas1 and Its Interaction with Csn2 in the Type II CRISPR-Cas System. Structure 24 (2016), 70–79.
85. Kaiser, D., Robinson, M., Kroos, L., Myxobacteria, polarity, and multicellular morphogenesis. Cold Spring Harb. Perspect. Biol., 2, 2010, a000380.
86. Kasman, L.M., Kasman, A., Westwater, C., Dolan, J., Schmidt, M.G., Norris, J.S., Overcoming the phage replication threshold: a mathematical model with implications for phage therapy. J. Virol. 76 (2002), 5557–5564.
87. Kazlauskiene, M., Tamulaitis, G., Kostiuk, G., Venclovas, Č., Siksnys, V., Spatiotemporal Control of Type III-A CRISPR-Cas Immunity: Coupling DNA Degradation with the Target RNA Recognition. Mol. Cell 62 (2016), 295–306.
88. Kazlauskiene, M., Kostiuk, G., Venclovas, Č., Tamulaitis, G., Siksnys, V., A cyclic oligonucleotide signaling pathway in type III CRISPR-Cas systems. Science 357 (2017), 605–609.
89. Kim, D., Kim, J., Hur, J.K., Been, K.W., Yoon, S.H., Kim, J.-S., Genome-wide analysis reveals specificities of Cpf1 endonucleases in human cells. Nat. Biotechnol. 34 (2016), 863–868.
90. Kim, H.K., Song, M., Lee, J., Menon, A.V., Jung, S., Kang, Y.-M., Choi, J.W., Woo, E., Koh, H.C., Nam, J.-W., Kim, H., In vivo high-throughput profiling of CRISPR-Cpf1 activity. Nat. Methods 14 (2017), 153–159.
91. Kleinstiver, B.P., Tsai, S.Q., Prew, M.S., Nguyen, N.T., Welch, M.M., Lopez, J.M., McCaw, Z.R., Aryee, M.J., Joung, J.K., Genome-wide specificities of CRISPR-Cas Cpf1 nucleases in human cells. Nat. Biotechnol. 34 (2016), 869–874.
92. Komor, A.C., Badran, A.H., Liu, D.R., CRISPR-Based Technologies for the Manipulation of Eukaryotic Genomes. Cell 168 (2017), 20–36.
93. Koonin, E.V., Makarova, K.S., CRISPR-Cas: evolution of an RNA-based adaptive immunity system in prokaryotes. RNA Biol. 10 (2013), 679–686.
94. Koonin, E.V., Makarova, K.S., Zhang, F., Diversity, classification and evolution of CRISPR-Cas systems. Curr. Opin. Microbiol. 37 (2017), 67–78.
95. Koskella, B., Brockhurst, M.A., Bacteria-phage coevolution as a driver of ecological and evolutionary processes in microbial communities. FEMS Microbiol. Rev. 38 (2014), 916–931.
96. Kunin, V., Sorek, R., Hugenholtz, P., Evolutionary conservation of sequence and secondary structures in CRISPR repeats. Genome Biol., 8, 2007, R61.
97. Künne, T., Kieper, S.N., Bannenberg, J.W., Vogel, A.I.M., Miellet, W.R., Klein, M., Depken, M., Suarez-Diez, M., Brouns, S.J.J., Cas3-Derived Target DNA Degradation Fragments Fuel Primed CRISPR Adaptation. Mol. Cell 63 (2016), 852–864.
98. Labrie, S.J., Samson, J.E., Moineau, S., Bacteriophage resistance mechanisms. Nat. Rev. Microbiol. 8 (2010), 317–327.
99. Lenski, R.E., Coevolution of bacteria and phage: are there endless cycles of bacterial defenses and phage counterdefenses?. J. Theor. Biol. 108 (1984), 319–325.
100. Lenski, R.E., Levin, B.R., Constraints on the Coevolution of Bacteria and Virulent Phage: A Model, Some Experiments, and Predictions for Natural Communities. Am. Nat. 125 (1985), 585–602.
101. Levin, B.R., Moineau, S., Bushman, M., Barrangou, R., The population and evolutionary dynamics of phage and bacteria with CRISPR-mediated immunity. PLoS Genet., 9, 2013, e1003312.
102. Levy, A., Goren, M.G., Yosef, I., Auster, O., Manor, M., Amitai, G., Edgar, R., Qimron, U., Sorek, R., CRISPR adaptation biases explain preference for acquisition of foreign DNA. Nature 520 (2015), 505–510.
103. Li, M., Wang, R., Zhao, D., Xiang, H., Adaptation of the Haloarcula hispanica CRISPR-Cas system to a purified virus strictly requires a priming process. Nucleic Acids Res. 42 (2014), 2483–2492.
104. Li, R., Fang, L., Tan, S., Yu, M., Li, X., He, S., Wei, Y., Li, G., Jiang, J., Wu, M., Type I CRISPR-Cas targets endogenous genes and regulates virulence to evade mammalian host immunity. Cell Res. 26 (2016), 1273–1287.
105. Liu, L., Chen, P., Wang, M., Li, X., Wang, J., Yin, M., Wang, Y., C2c1-sgRNA Complex Structure Reveals RNA-Guided DNA Cleavage Mechanism. Mol. Cell 65 (2017), 310–322.
106. Liu, L., Li, X., Wang, J., Wang, M., Chen, P., Yin, M., Li, J., Sheng, G., Wang, Y., Two Distant Catalytic Sites Are Responsible for C2c2 RNase Activities. Cell 168 (2017), 121–134.
107. Liu, L., Li, X., Ma, J., Li, Z., You, L., Wang, J., Wang, M., Zhang, X., Wang, Y., The Molecular Architecture for RNA-Guided RNA Cleavage by Cas13a. Cell 170 (2017), 714–726.
108. Louwen, R., Horst-Kreft, D., de Boer, A.G., van der Graaf, L., de Knegt, G., Hamersma, M., Heikema, A.P., Timms, A.R., Jacobs, B.C., Wagenaar, J.A., et al. A novel link between Campylobacter jejuni bacteriophage defence, virulence and Guillain-Barré syndrome. Eur. J. Clin. Microbiol. Infect. Dis. 32 (2013), 207–226.
109. Makarova, K.S., Grishin, N.V., Shabalina, S.A., Wolf, Y.I., Koonin, E.V., A putative RNA-interference-based immune system in prokaryotes: computational analysis of the predicted enzymatic machinery, functional analogies with eukaryotic RNAi, and hypothetical mechanisms of action. Biol. Direct, 1, 2006, 7.
110. Makarova, K.S., Haft, D.H., Barrangou, R., Brouns, S.J., Charpentier, E., Horvath, P., Moineau, S., Mojica, F.J., Wolf, Y.I., Yakunin, A.F., et al. Evolution and classification of the CRISPR-Cas systems. Nat. Rev. Microbiol. 9 (2011), 467–477.
111. Makarova, K.S., Wolf, Y.I., Koonin, E.V., The basic building blocks and evolution of CRISPR-CAS systems. Biochem. Soc. Trans. 41 (2013), 1392–1400.
112. Makarova, K.S., Wolf, Y.I., Alkhnbashi, O.S., Costa, F., Shah, S.A., Saunders, S.J., Barrangou, R., Brouns, S.J.J., Charpentier, E., Haft, D.H., et al. An updated evolutionary classification of CRISPR-Cas systems. Nat. Rev. Microbiol. 13 (2015), 722–736.
113. Mandin, P., Repoila, F., Vergassola, M., Geissmann, T., Cossart, P., Identification of new noncoding RNAs in Listeria monocytogenes and prediction of mRNA targets. Nucleic Acids Res. 35 (2007), 962–974.
114. Manica, A., Zebec, Z., Teichmann, D., Schleper, C., In vivo activity of CRISPR-mediated virus defence in a hyperthermophilic archaeon. Mol. Microbiol. 80 (2011), 481–491.
115. Marraffini, L.A., Sontheimer, E.J., CRISPR interference limits horizontal gene transfer in staphylococci by targeting DNA. Science 322 (2008), 1843–1845.
116. Marraffini, L.A., Sontheimer, E.J., Self versus non-self discrimination during CRISPR RNA-directed immunity. Nature 463 (2010), 568–571.
117. McGinn, J., Marraffini, L.A., CRISPR-Cas Systems Optimize Their Immune Response by Specifying the Site of Spacer Integration. Mol. Cell 64 (2016), 616–623.
118. Mekler, V., Minakhin, L., Severinov, K., Mechanism of duplex DNA destabilization by RNA-guided Cas9 nuclease during target interrogation. Proc. Natl. Acad. Sci. USA 114 (2017), 5443–5448.
119. Modell, J.W., Jiang, W., Marraffini, L.A., CRISPR-Cas systems exploit viral DNA injection to establish and maintain adaptive immunity. Nature 544 (2017), 101–104.
120. Mohanraju, P., Makarova, K.S., Zetsche, B., Zhang, F., Koonin, E.V., van der Oost, J., Diverse evolutionary roots and mechanistic variations of the CRISPR-Cas systems. Science, 353, 2016, aad5147.
121. Mojica, F.J., Díez-Villaseñor, C., García-Martínez, J., Soria, E., Intervening sequences of regularly spaced prokaryotic repeats derive from foreign genetic elements. J. Mol. Evol. 60 (2005), 174–182.
122. Mojica, F.J., Díez-Villaseñor, C., García-Martínez, J., Almendros, C., Short motif sequences determine the targets of the prokaryotic CRISPR defence system. Microbiology 155 (2009), 733–740.
123. 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 (2013), 22184–22192.
124. Mulepati, S., Héroux, A., Bailey, S., Structural biology. Crystal structure of a CRISPR RNA-guided surveillance complex bound to a ssDNA target. Science 345 (2014), 1479–1484.
125. Nam, K.H., Haitjema, C., Liu, X., Ding, F., Wang, H., DeLisa, M.P., Ke, A., Cas5d protein processes pre-crRNA and assembles into a cascade-like interference complex in subtype I-C/Dvulg CRISPR-Cas system. Structure 20 (2012), 1574–1584.
126. Niewoehner, O., Jinek, M., Structural basis for the endoribonuclease activity of the type III-A CRISPR-associated protein Csm6. RNA 22 (2016), 318–329.
127. Niewoehner, O., Garcia-Doval, C., Rostøl, J.T., Berk, C., Schwede, F., Bigler, L., Hall, J., Marraffini, L.A., Jinek, M., Type III CRISPR-Cas systems produce cyclic oligoadenylate second messengers. Nature 548 (2017), 543–548.
128. Nishimasu, H., Ran, F.A., Hsu, P.D., Konermann, S., Shehata, S.I., Dohmae, N., Ishitani, R., Zhang, F., Nureki, O., Crystal structure of Cas9 in complex with guide RNA and target DNA. Cell 156 (2014), 935–949.
129. Nishimasu, H., Cong, L., Yan, W.X., Ran, F.A., Zetsche, B., Li, Y., Kurabayashi, A., Ishitani, R., Zhang, F., Nureki, O., Crystal Structure of Staphylococcus aureus Cas9. Cell 162 (2015), 1113–1126.
130. Nuñez, J.K., Kranzusch, P.J., Noeske, J., Wright, A.V., Davies, C.W., Doudna, J.A., Cas1-Cas2 complex formation mediates spacer acquisition during CRISPR-Cas adaptive immunity. Nat. Struct. Mol. Biol. 21 (2014), 528–534.
131. Nuñez, J.K., Lee, A.S.Y., Engelman, A., Doudna, J.A., Integrase-mediated spacer acquisition during CRISPR-Cas adaptive immunity. Nature 519 (2015), 193–198.
132. Nuñez, J.K., Bai, L., Harrington, L.B., Hinder, T.L., Doudna, J.A., CRISPR Immunological Memory Requires a Host Factor for Specificity. Mol. Cell 62 (2016), 824–833.
133. Olovnikov, I., Chan, K., Sachidanandam, R., Newman, D.K., Aravin, A.A., Bacterial argonaute samples the transcriptome to identify foreign DNA. Mol. Cell 51 (2013), 594–605.
134. Osawa, T., Inanaga, H., Sato, C., Numata, T., Crystal structure of the CRISPR-Cas RNA silencing Cmr complex bound to a target analog. Mol. Cell 58 (2015), 418–430.
135. Paez-Espino, D., Sharon, I., Morovic, W., Stahl, B., Thomas, B.C., Barrangou, R., Banfield, J.F., CRISPR immunity drives rapid phage genome evolution in Streptococcus thermophilus. MBio, 6, 2015 e00262–15.
136. Patterson, A.G., Jackson, S.A., Taylor, C., Evans, G.B., Salmond, G.P.C., Przybilski, R., Staals, R.H.J., Fineran, P.C., Quorum Sensing Controls Adaptive Immunity through the Regulation of Multiple CRISPR-Cas Systems. Mol. Cell 64 (2016), 1102–1108.
137. Patterson, A.G., Yevstigneyeva, M.S., Fineran, P.C., Regulation of CRISPR-Cas adaptive immune systems. Curr. Opin. Microbiol. 37 (2017), 1–7.
138. Pausch, P., Müller-Esparza, H., Gleditzsch, D., Altegoer, F., Randau, L., Bange, G., Structural Variation of Type I-F CRISPR RNA Guided DNA Surveillance. Mol. Cell 67 (2017), 622–632.
139. Pawluk, A., Bondy-Denomy, J., Cheung, V.H.W., Maxwell, K.L., Davidson, A.R., A new group of phage anti-CRISPR genes inhibits the type I-E CRISPR-Cas system of Pseudomonas aeruginosa. MBio, 5, 2014 e00896–14.
140. Pawluk, A., Staals, R.H.J., Taylor, C., Watson, B.N.J., Saha, S., Fineran, P.C., Maxwell, K.L., Davidson, A.R., Inactivation of CRISPR-Cas systems by anti-CRISPR proteins in diverse bacterial species. Nat. Microbiol., 1, 2016, 16085.
141. Pawluk, A., Amrani, N., Zhang, Y., Garcia, B., Hidalgo-Reyes, Y., Lee, J., Edraki, A., Shah, M., Sontheimer, E.J., Maxwell, K.L., Davidson, A.R., Naturally Occurring Off-Switches for CRISPR-Cas9. Cell 167 (2016), 1829–1838.
142. Peng, R., Xu, Y., Zhu, T., Li, N., Qi, J., Chai, Y., Wu, M., Zhang, X., Shi, Y., Wang, P., et al. Alternate binding modes of anti-CRISPR viral suppressors AcrF1/2 to Csy surveillance complex revealed by cryo-EM structures. Cell Res. 27 (2017), 853–864.
143. Perez-Rodriguez, R., Haitjema, C., Huang, Q., Nam, K.H., Bernardis, S., Ke, A., DeLisa, M.P., Envelope stress is a trigger of CRISPR RNA-mediated DNA silencing in Escherichia coli. Mol. Microbiol. 79 (2011), 584–599.
144. Plagens, A., Tjaden, B., Hagemann, A., Randau, L., Hensel, R., Characterization of the CRISPR/Cas subtype I-A system of the hyperthermophilic crenarchaeon Thermoproteus tenax. J. Bacteriol. 194 (2012), 2491–2500.
145. Plagens, A., Tripp, V., Daume, M., Sharma, K., Klingl, A., Hrle, A., Conti, E., Urlaub, H., Randau, L., In vitro assembly and activity of an archaeal CRISPR-Cas type I-A Cascade interference complex. Nucleic Acids Res. 42 (2014), 5125–5138.
146. Pourcel, C., Salvignol, G., Vergnaud, G., CRISPR elements in Yersinia pestis acquire new repeats by preferential uptake of bacteriophage DNA, and provide additional tools for evolutionary studies. Microbiology 151 (2005), 653–663.
147. Price, V.J., Huo, W., Sharifi, A., Palmer, K.L., CRISPR-Cas and Restriction-Modification Act Additively against Conjugative Antibiotic Resistance Plasmid Transfer in Enterococcus faecalis. mSphere, 1, 2016 e00064–16.
148. Pyenson, N.C., Gayvert, K., Varble, A., Elemento, O., Marraffini, L.A., Broad Targeting Specificity during Bacterial Type III CRISPR-Cas Immunity Constrains Viral Escape. Cell Host Microbe 22 (2017), 343–353.
149. Quax, T.E.F., Voet, M., Sismeiro, O., Dillies, M.-A., Jagla, B., Coppée, J.-Y., Sezonov, G., Forterre, P., van der Oost, J., Lavigne, R., Prangishvili, D., Massive activation of archaeal defense genes during viral infection. J. Virol. 87 (2013), 8419–8428.
150. Rauch, B.J., Silvis, M.R., Hultquist, J.F., Waters, C.S., McGregor, M.J., Krogan, N.J., Bondy-Denomy, J., Inhibition of CRISPR-Cas9 with Bacteriophage Proteins. Cell 168 (2017), 150–158.
151. Redding, S., Sternberg, S.H., Marshall, M., Gibb, B., Bhat, P., Guegler, C.K., Wiedenheft, B., Doudna, J.A., Greene, E.C., Surveillance and Processing of Foreign DNA by the Escherichia coli CRISPR-Cas System. Cell 163 (2015), 854–865.
152. Reeks, J., Sokolowski, R.D., Graham, S., Liu, H., Naismith, J.H., White, M.F., Structure of a dimeric crenarchaeal Cas6 enzyme with an atypical active site for CRISPR RNA processing. Biochem. J. 452 (2013), 223–230.
153. Richter, C., Chang, J.T., Fineran, P.C., Function and regulation of clustered regularly interspaced short palindromic repeats (CRISPR) / CRISPR associated (Cas) systems. Viruses 4 (2012), 2291–2311.
154. Richter, H., Zoephel, J., Schermuly, J., Maticzka, D., Backofen, R., Randau, L., Characterization of CRISPR RNA processing in Clostridium thermocellum and Methanococcus maripaludis. Nucleic Acids Res. 40 (2012), 9887–9896.
155. Richter, H., Lange, S.J., Backofen, R., Randau, L., Comparative analysis ofCas6b processing and CRISPR RNA stability. RNA Biol. 10 (2013), 700–707.
156. Richter, C., Dy, R.L., McKenzie, R.E., Watson, B.N.J., Taylor, C., Chang, J.T., McNeil, M.B., Staals, R.H.J., Fineran, P.C., Priming in the Type I-F CRISPR-Cas system triggers strand-independent spacer acquisition, bi-directionally from the primed protospacer. Nucleic Acids Res. 42 (2014), 8516–8526.
157. Richter, H., Rompf, J., Wiegel, J., Rau, K., Randau, L., Fragmentation of the CRISPR-Cas Type I-B signature protein Cas8b. Biochim. Biophys. Acta 1861:11 Pt B (2017), 2993–3000.
158. Rollins, M.F., Chowdhury, S., Carter, J., Golden, S.M., Wilkinson, R.A., Bondy-Denomy, J., Lander, G.C., Wiedenheft, B., Cas1 and the Csy complex are opposing regulators of Cas2/3 nuclease activity. Proc. Natl. Acad. Sci. USA 114 (2017), E5113–E5121.
159. Samai, P., Pyenson, N., Jiang, W., Goldberg, G.W., Hatoum-Aslan, A., Marraffini, L.A., Co-transcriptional DNA and RNA Cleavage during Type III CRISPR-Cas Immunity. Cell 161 (2015), 1164–1174.
160. Sampson, T.R., Saroj, S.D., Llewellyn, A.C., Tzeng, Y.-L., Weiss, D.S., A CRISPR/Cas system mediates bacterial innate immune evasion and virulence. Nature 497 (2013), 254–257.
161. Sapranauskas, R., Gasiunas, G., Fremaux, C., Barrangou, R., Horvath, P., Siksnys, V., The Streptococcus thermophilus CRISPR/Cas system provides immunity in Escherichia coli. Nucleic Acids Res. 39 (2011), 9275–9282.
162. Sashital, D.G., Jinek, M., Doudna, J.A., An RNA-induced conformational change required for CRISPR RNA cleavage by the endoribonuclease Cse3. Nat. Struct. Mol. Biol. 18 (2011), 680–687.
163. Savitskaya, E., Semenova, E., Dedkov, V., Metlitskaya, A., Severinov, K., High-throughput analysis of type I-E CRISPR/Cas spacer acquisition in E. coli. RNA Biol. 10 (2013), 716–725.
164. Seed, K.D., Lazinski, D.W., Calderwood, S.B., Camilli, A., A bacteriophage encodes its own CRISPR/Cas adaptive response to evade host innate immunity. Nature 494 (2013), 489–491.
165. Sefcikova, J., Roth, M., Yu, G., Li, H., Cas6 processes tight and relaxed repeat RNA via multiple mechanisms: A hypothesis. BioEssays, 39, 2017, 1700019.
166. Semenova, E., Jore, M.M., Datsenko, K.A., Semenova, A., Westra, E.R., Wanner, B., van der Oost, J., Brouns, S.J., Severinov, K., Interference by clustered regularly interspaced short palindromic repeat (CRISPR) RNA is governed by a seed sequence. Proc. Natl. Acad. Sci. USA 108 (2011), 10098–10103.
167. Shao, Y., Li, H., Recognition and cleavage of a nonstructured CRISPR RNA by its processing endoribonuclease Cas6. Structure 21 (2013), 385–393.
168. Shao, Y., Richter, H., Sun, S., Sharma, K., Urlaub, H., Randau, L., Li, H., A Non-Stem-Loop CRISPR RNA Is Processed by Dual Binding Cas6. Structure 24 (2016), 547–554.
169. Sheppard, N.F., Glover, C.V.C. 3rd, Terns, R.M., Terns, M.P., The CRISPR-associated Csx1 protein of Pyrococcus furiosus is an adenosine-specific endoribonuclease. RNA 22 (2016), 216–224.
170. Shin, J., Jiang, F., Liu, J.J., Bray, N.L., Rauch, B.J., Baik, S.H., Nogales, E., Bondy-Denomy, J., Corn, J.E., Doudna, J.A., Disabling Cas9 by an anti-CRISPR DNA mimic. Sci. Adv., 3, 2017, e1701620.
171. Shipman, S.L., Nivala, J., Macklis, J.D., Church, G.M., Molecular recordings by directed CRISPR spacer acquisition. Science, 353, 2016, aaf1175.
172. Shmakov, S., Savitskaya, E., Semenova, E., Logacheva, M.D., Datsenko, K.A., Severinov, K., Pervasive generation of oppositely oriented spacers during CRISPR adaptation. Nucleic Acids Res. 42 (2014), 5907–5916.
173. Shmakov, S., Abudayyeh, O.O., Makarova, K.S., Wolf, Y.I., Gootenberg, J.S., Semenova, E., Minakhin, L., Joung, J., Konermann, S., Severinov, K., et al. Discovery and Functional Characterization of Diverse Class 2 CRISPR-Cas Systems. Mol. Cell 60 (2015), 385–397.
174. Shmakov, S., Smargon, A., Scott, D., Cox, D., Pyzocha, N., Yan, W., Abudayyeh, O.O., Gootenberg, J.S., Makarova, K.S., Wolf, Y.I., et al. Diversity and evolution of class 2 CRISPR-Cas systems. Nat. Rev. Microbiol. 15 (2017), 169–182.
175. Silas, S., Mohr, G., Sidote, D.J., Markham, L.M., Sanchez-Amat, A., Bhaya, D., Lambowitz, A.M., Fire, A.Z., Direct CRISPR spacer acquisition from RNA by a natural reverse transcriptase-Cas1 fusion protein. Science, 351, 2016, aad4234.
176. Sinkunas, T., Gasiunas, G., Waghmare, S.P., Dickman, M.J., Barrangou, R., Horvath, P., Siksnys, V., In vitro reconstitution of Cascade-mediated CRISPR immunity in Streptococcus thermophilus. EMBO J. 32 (2013), 385–394.
177. Siringan, P., Connerton, P.L., Cummings, N.J., Connerton, I.F., Alternative bacteriophage life cycles: the carrier state of Campylobacter jejuni. Open Biol., 4, 2014, 130200.
178. Smargon, A.A., Cox, D.B.T., Pyzocha, N.K., Zheng, K., Slaymaker, I.M., Gootenberg, J.S., Abudayyeh, O.A., Essletzbichler, P., Shmakov, S., Makarova, K.S., et al. Cas13b Is a Type VI-B CRISPR-Associated RNA-Guided RNase Differentially Regulated by Accessory Proteins Csx27 and Csx28. Mol. Cell 65 (2017), 618–630.
179. Smith, G.R., How RecBCD enzyme and Chi promote DNA break repair and recombination: a molecular biologist's view. Microbiol. Mol. Biol. Rev. 76 (2012), 217–228.
180. Sontheimer, E.J., Davidson, A.R., Inhibition of CRISPR-Cas systems by mobile genetic elements. Curr. Opin. Microbiol. 37 (2017), 120–127.
181. Staals, R.H.J., Zhu, Y., Taylor, D.W., Kornfeld, J.E., Sharma, K., Barendregt, A., Koehorst, J.J., Vlot, M., Neupane, N., Varossieau, K., et al. RNA targeting by the type III-A CRISPR-Cas Csm complex of Thermus thermophilus. Mol. Cell 56 (2014), 518–530.
182. Staals, R.H.J., Jackson, S.A., Biswas, A., Brouns, S.J.J., Brown, C.M., Fineran, P.C., Interference-driven spacer acquisition is dominant over naive and primed adaptation in a native CRISPR-Cas system. Nat. Commun., 7, 2016, 12853.
183. Stella, S., Alcón, P., Montoya, G., Structure of the Cpf1 endonuclease R-loop complex after target DNA cleavage. Nature 546 (2017), 559–563.
184. Stern, A., Keren, L., Wurtzel, O., Amitai, G., Sorek, R., Self-targeting by CRISPR: gene regulation or autoimmunity?. Trends Genet. 26 (2010), 335–340.
185. Sternberg, S.H., Redding, S., Jinek, M., Greene, E.C., Doudna, J.A., DNA interrogation by the CRISPR RNA-guided endonuclease Cas9. Nature 507 (2014), 62–67.
186. Sternberg, S.H., LaFrance, B., Kaplan, M., Doudna, J.A., Conformational control of DNA target cleavage by CRISPR-Cas9. Nature 527 (2015), 110–113.
187. Swarts, D.C., Mosterd, C., van Passel, M.W., Brouns, S.J., CRISPR interference directs strand specific spacer acquisition. PLoS ONE, 7, 2012, e35888.
188. Swarts, D.C., Jore, M.M., Westra, E.R., Zhu, Y., Janssen, J.H., Snijders, A.P., Wang, Y., Patel, D.J., Berenguer, J., Brouns, S.J.J., van der Oost, J., DNA-guided DNA interference by a prokaryotic Argonaute. Nature 507 (2014), 258–261.
189. Swarts, D.C., Koehorst, J.J., Westra, E.R., Schaap, P.J., van der Oost, J., Effects of Argonaute on Gene Expression in Thermus thermophilus. PLoS ONE, 10, 2015, e0124880.
190. Swarts, D.C., van der Oost, J., Jinek, M., Structural Basis for Guide RNA Processing and Seed-Dependent DNA Targeting by CRISPR-Cas12a. Mol. Cell 66 (2017), 221–233.
191. Tamulaitis, G., Kazlauskiene, M., Manakova, E., Venclovas, Č., Nwokeoji, A.O., Dickman, M.J., Horvath, P., Siksnys, V., Programmable RNA shredding by the type III-A CRISPR-Cas system of Streptococcus thermophilus. Mol. Cell 56 (2014), 506–517.
192. Taylor, D.W., Zhu, Y., Staals, R.H.J., Kornfeld, J.E., Shinkai, A., van der Oost, J., Nogales, E., Doudna, J.A., Structural biology. Structures of the CRISPR-Cmr complex reveal mode of RNA target positioning. Science 348 (2015), 581–585.
193. Thöny-Meyer, L., Kaiser, D., devRS, an autoregulated and essential genetic locus for fruiting body development in Myxococcus xanthus. J. Bacteriol. 175 (1993), 7450–7462.
194. Toledo-Arana, A., Dussurget, O., Nikitas, G., Sesto, N., Guet-Revillet, H., Balestrino, D., Loh, E., Gripenland, J., Tiensuu, T., Vaitkevicius, K., et al. The Listeria transcriptional landscape from saprophytism to virulence. Nature 459 (2009), 950–956.
195. Touchon, M., Charpentier, S., Clermont, O., Rocha, E.P., Denamur, E., Branger, C., CRISPR distribution within the Escherichia coli species is not suggestive of immunity-associated diversifying selection. J. Bacteriol. 193 (2011), 2460–2467.
196. Vale, P.F., Lafforgue, G., Gatchitch, F., Gardan, R., Moineau, S., Gandon, S., Costs of CRISPR-Cas-mediated resistance in Streptococcus thermophilus. Proc. Biol. Sci., 282, 2015 20151270.
197. van der Oost, J., Westra, E.R., Jackson, R.N., Wiedenheft, B., Unravelling the structural and mechanistic basis of CRISPR-Cas systems. Nat. Rev. Microbiol. 12 (2014), 479–492.
198. van Houte, S., Ekroth, A.K., Broniewski, J.M., Chabas, H., Ashby, B., Bondy-Denomy, J., Gandon, S., Boots, M., Paterson, S., Buckling, A., Westra, E.R., The diversity-generating benefits of a prokaryotic adaptive immune system. Nature 532 (2016), 385–388.
199. Vercoe, R.B., Chang, J.T., Dy, R.L., Taylor, C., Gristwood, T., Clulow, J.S., Richter, C., Przybilski, R., Pitman, A.R., Fineran, P.C., Cytotoxic chromosomal targeting by CRISPR/Cas systems can reshape bacterial genomes and expel or remodel pathogenicity islands. PLoS Genet., 9, 2013, e1003454.
200. Viswanathan, P., Murphy, K., Julien, B., Garza, A.G., Kroos, L., Regulation of dev, an operon that includes genes essential for Myxococcus xanthus development and CRISPR-associated genes and repeats. J. Bacteriol. 189 (2007), 3738–3750.
201. Vorontsova, D., Datsenko, K.A., Medvedeva, S., Bondy-Denomy, J., Savitskaya, E.E., Pougach, K., Logacheva, M., Wiedenheft, B., Davidson, A.R., Severinov, K., Semenova, E., Foreign DNA acquisition by the I-F CRISPR-Cas system requires all components of the interference machinery. Nucleic Acids Res. 43 (2015), 10848–10860.
202. Wallace, R.A., Black, W.P., Yang, X., Yang, Z., A CRISPR with roles in Myxococcus xanthus development and exopolysaccharide production. J. Bacteriol. 196 (2014), 4036–4043.
203. Wang, J., Li, J., Zhao, H., Sheng, G., Wang, M., Yin, M., Wang, Y., Structural and Mechanistic Basis of PAM-Dependent Spacer Acquisition in CRISPR-Cas Systems. Cell 163 (2015), 840–853.
204. Wei, Y., Terns, R.M., Terns, M.P., Cas9 function and host genome sampling in Type II-A CRISPR-Cas adaptation. Genes Dev. 29 (2015), 356–361.
205. Weinberger, A.D., Wolf, Y.I., Lobkovsky, A.E., Gilmore, M.S., Koonin, E.V., Viral diversity threshold for adaptive immunity in prokaryotes. MBio, 3, 2012 e00456–12.
206. Weissman, J.L., Holmes, R., Barrangou, R., Moineau, S., Fagan, W.F., Levin, B.R., Johnson, P.L., Immune Loss as a Driver of Coexistence During Host-Phage Coevolution. bioRxiv, 2017, 10.1101/105908.
207. Westra, E.R., Nilges, B., van Erp, P.B., van der Oost, J., Dame, R.T., Brouns, S.J., Cascade-mediated binding and bending of negatively supercoiled DNA. RNA Biol. 9 (2012), 1134–1138.
208. Westra, E.R., Buckling, A., Fineran, P.C., CRISPR-Cas systems: beyond adaptive immunity. Nat. Rev. Microbiol. 12 (2014), 317–326.
209. Westra, E.R., Dowling, A.J., Broniewski, J.M., van Houte, S., Evolution and Ecology of CRISPR. Annu. Rev. Ecol. Evol. Syst. 47 (2016), 307–331.
210. Wiedenheft, B., Lander, G.C., Zhou, K., Jore, M.M., Brouns, S.J.J., van der Oost, J., Doudna, J.A., Nogales, E., Structures of the RNA-guided surveillance complex from a bacterial immune system. Nature 477 (2011), 486–489.
211. Wiedenheft, B., van Duijn, E., Bultema, J.B., Waghmare, S.P., Zhou, K., Barendregt, A., Westphal, W., Heck, A.J., Boekema, E.J., Dickman, M.J., Doudna, J.A., RNA-guided complex from a bacterial immune system enhances target recognition through seed sequence interactions. Proc. Natl. Acad. Sci. USA 108 (2011), 10092–10097.
212. Wigley, D.B., Bacterial DNA repair: recent insights into the mechanism of RecBCD, AddAB and AdnAB. Nat. Rev. Microbiol. 11 (2013), 9–13.
213. Wright, A.V., Doudna, J.A., Protecting genome integrity during CRISPR immune adaptation. Nat. Struct. Mol. Biol. 23 (2016), 876–883.
214. Wright, A.V., Nuñez, J.K., Doudna, J.A., Biology and Applications of CRISPR Systems: Harnessing Nature's Toolbox for Genome Engineering. Cell 164 (2016), 29–44.
215. Wright, A.V., Liu, J.-J., Knott, G.J., Doxzen, K.W., Nogales, E., Doudna, J.A., Structures of the CRISPR genome integration complex. Science 357 (2017), 1113–1118.
216. Xiao, Y., Luo, M., Hayes, R.P., Kim, J., Ng, S., Ding, F., Liao, M., Ke, A., Structure Basis for Directional R-loop Formation and Substrate Handover Mechanisms in Type I CRISPR-Cas System. Cell 170 (2017), 48–60.
217. Xiao, Y., Ng, S., Nam, K.H., Ke, A., How type II CRISPR-Cas establish immunity through Cas1-Cas2-mediated spacer integration. Nature 550 (2017), 137–141.
218. Xue, C., Whitis, N.R., Sashital, D.G., Conformational Control of Cascade Interference and Priming Activities in CRISPR Immunity. Mol. Cell 64 (2016), 826–834.
219. Yamada, M., Watanabe, Y., Gootenberg, J.S., Hirano, H., Ran, F.A., Nakane, T., Ishitani, R., Zhang, F., Nishimasu, H., Nureki, O., Crystal Structure of the Minimal Cas9 from Campylobacter jejuni Reveals the Molecular Diversity in the CRISPR-Cas9 Systems. Mol. Cell 65 (2017), 1109–1121.
220. Yamano, T., Nishimasu, H., Zetsche, B., Hirano, H., Slaymaker, I.M., Li, Y., Fedorova, I., Nakane, T., Makarova, K.S., Koonin, E.V., et al. Crystal Structure of Cpf1 in Complex with Guide RNA and Target DNA. Cell 165 (2016), 949–962.
221. Yang, H., Patel, D.J., Inhibition Mechanism of an Anti-CRISPR Suppressor AcrIIA4 Targeting SpyCas9. Mol. Cell 67 (2017), 117–127.
222. Yang, H., Gao, P., Rajashankar, K.R., Patel, D.J., PAM-Dependent Target DNA Recognition and Cleavage by C2c1 CRISPR-Cas Endonuclease. Cell 167 (2016), 1814–1828.
223. Yoganand, K.N.R., Sivathanu, R., Nimkar, S., Anand, B., Asymmetric positioning of Cas1-2 complex and Integration Host Factor induced DNA bending guide the unidirectional homing of protospacer in CRISPR-Cas type I-E system. Nucleic Acids Res. 45 (2017), 367–381.
224. Yosef, I., Goren, M.G., Qimron, U., Proteins and DNA elements essential for the CRISPR adaptation process in Escherichia coli. Nucleic Acids Res. 40 (2012), 5569–5576.
225. Young, J.C., Dill, B.D., Pan, C., Hettich, R.L., Banfield, J.F., Shah, M., Fremaux, C., Horvath, P., Barrangou, R., Verberkmoes, N.C., Phage-induced expression of CRISPR-associated proteins is revealed by shotgun proteomics in Streptococcus thermophilus. PLoS ONE, 7, 2012, e38077.
226. Zegans, M.E., Wagner, J.C., Cady, K.C., Murphy, D.M., Hammond, J.H., O'Toole, G.A., Interaction between bacteriophage DMS3 and host CRISPR region inhibits group behaviors of Pseudomonas aeruginosa. J. Bacteriol. 191 (2009), 210–219.
227. Zetsche, B., Gootenberg, J.S., Abudayyeh, O.O., Slaymaker, I.M., Makarova, K.S., Essletzbichler, P., Volz, S.E., Joung, J., van der Oost, J., Regev, A., et al. Cpf1 is a single RNA-guided endonuclease of a class 2 CRISPR-Cas system. Cell 163 (2015), 759–771.
228. Zhang, J., Kasciukovic, T., White, M.F., The CRISPR associated protein Cas4 Is a 5′ to 3′ DNA exonuclease with an iron-sulfur cluster. PLoS ONE, 7, 2012, e47232.
229. Zhang, Y., Heidrich, N., Ampattu, B.J., Gunderson, C.W., Seifert, H.S., Schoen, C., Vogel, J., Sontheimer, E.J., Processing-independent CRISPR RNAs limit natural transformation in Neisseria meningitidis. Mol. Cell 50 (2013), 488–503.
230. Zhao, H., Sheng, G., Wang, J., Wang, M., Bunkoczi, G., Gong, W., Wei, Z., Wang, Y., Crystal structure of the RNA-guided immune surveillance Cascade complex in Escherichia coli. Nature 515 (2014), 147–150.