The Revolution Continues: Newly Discovered Systems Expand the CRISPR-Cas Toolkit

Molecular Cell

Volumn 68, Issue 1, 2017, Pages 15-25

  Murugan, Karthik ^a   Babu, Kesavan ^b   Sundaresan, Ramya ^b   Rajan, Rakhi ^b   Sashital, Dipali G ^a  

^a IOWA STATE UNIVERSITY   (United States)

^b UNIVERSITY OF OKLAHOMA   (United States)

Author keywords

C2c1; C2c2; Cas12; Cas13; Cas9; Cpf1; CRISPR Cas; genome editing; RNA guided DNA cleavage; RNA guided RNA cleavage

Indexed keywords

CELLULAR APOPTOSIS SUSCEPTIBILITY PROTEIN; GUIDE RNA; NUCLEIC ACID; BACTERIAL PROTEIN; ENDONUCLEASE;

BACTERIOPHAGE; CRISPR CAS SYSTEM; ENZYME ACTIVATION; GENE EDITING; GENE SEQUENCE; GENETIC ENGINEERING; HUMAN; MOLECULAR RECOGNITION; PHYLOGENY; PROKARYOTE; PROTEIN BINDING; PROTEIN CLEAVAGE; REVIEW; STREPTOCOCCUS PYOGENES; BACTERIUM; CHEMISTRY; CLASSIFICATION; CLUSTERED REGULARLY INTERSPACED SHORT PALINDROMIC REPEAT; GENETIC TRANSCRIPTION; GENETICS; GENOME; GROWTH, DEVELOPMENT AND AGING; IMMUNOLOGY; METABOLISM; MOLECULAR MODEL; PROCEDURES; PROTEIN CONFORMATION; PROTEIN DOMAIN; VIROLOGY;

BACTERIA; BACTERIAL PROTEINS; BACTERIOPHAGES; CLUSTERED REGULARLY INTERSPACED SHORT PALINDROMIC REPEATS; CRISPR-CAS SYSTEMS; ENDONUCLEASES; GENE EDITING; GENETIC ENGINEERING; GENOME; HUMANS; MODELS, MOLECULAR; PROTEIN CONFORMATION; PROTEIN DOMAINS; RNA, GUIDE; TRANSCRIPTION, GENETIC;

EID: 85030698228     PISSN: 10972765     EISSN: 10974164     Source Type: Journal    
DOI: 10.1016/j.molcel.2017.09.007     Document Type: Review

References (75)

1. 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.
2. 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.
3. 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.
4. Borges, A.L., Davidson, A.R., Bondy-Denomy, J., The discovery, mechanisms, and evolutionary impact of anti-CRISPRs. Annu Rev Virol, 2017, 10.1146/annurev-virology-101416-041616 Published online July 27, 2017.
5. Burstein, D., Harrington, L.B., Strutt, S.C., Probst, A.J., Anantharaman, K., Thomas, B.C., Doudna, J.A., Banfield, J.F., New CRISPR-Cas systems from uncultivated microbes. Nature 542 (2017), 237–241.
6. Chen, J.S., Dagdas, Y.S., Kleinstiver, B.P., Welch, M.M., Harrington, L.B., Sternberg, S.H., Joung, J.K., Yildiz, A., Doudna, J.A., Enhanced proofreading governs CRISPR-Cas9 targeting accuracy. bioRxiv, 2017, 10.1101/160036.
7. 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, o0027.
8. 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.
9. 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.
10. Doudna, J.A., Charpentier, E., Genome editing. The new frontier of genome engineering with CRISPR-Cas9. Science, 346, 2014, 1258096.
11. 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.
12. 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.e3.
13. 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.
14. 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.
15. 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.
16. Gogleva, A.A., Gelfand, M.S., Artamonova, I.I., Comparative analysis of CRISPR cassettes from the human gut metagenomic contigs. BMC Genomics, 15, 2014, 202.
17. Gootenberg, J.S., Abudayyeh, O.O., Lee, J.W., Essletzbichler, P., Dy, A.J., Joung, J., Verdine, V., Donghia, N., Daringer, N.M., Freije, C.A., et al. Nucleic acid detection with CRISPR-Cas13a/C2c2. Science 356 (2017), 438–442.
18. Gorski, S.A., Vogel, J., Doudna, J.A., RNA-based recognition and targeting: sowing the seeds of specificity. Nat. Rev. Mol. Cell Biol. 18 (2017), 215–228.
19. 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.
20. Hille, F., Charpentier, E., CRISPR-Cas: biology, mechanisms and relevance. Philos. Trans. R. Soc. Lond. B Biol. Sci., 371, 2016, 10.1098/rstb.2015.0496.
21. Hochstrasser, M.L., Doudna, J.A., Cutting it close: CRISPR-associated endoribonuclease structure and function. Trends Biochem. Sci. 40 (2015), 58–66.
22. Hsu, P.D., Lander, E.S., Zhang, F., Development and applications of CRISPR-Cas9 for genome engineering. Cell 157 (2014), 1262–1278.
23. Hur, J.K., Kim, K., Been, K.W., Baek, G., Ye, S., Hur, J.W., Ryu, S.-M., Lee, Y.S., Kim, J.-S., Targeted mutagenesis in mice by electroporation of Cpf1 ribonucleoproteins. Nat. Biotechnol. 34 (2016), 807–808.
24. Jackson, R.N., Wiedenheft, B., A conserved structural chassis for mounting versatile CRISPR RNA-guided immune responses. Mol. Cell 58 (2015), 722–728.
25. Jackson, R.N., Golden, S.M., van Erp, P.B., Carter, J., Westra, E.R., Brouns, S.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.
26. Jackson, S.A., McKenzie, R.E., Fagerlund, R.D., Kieper, S.N., Fineran, P.C., Brouns, S.J.J., CRISPR-Cas: adapting to change. Science, 356, 2017, 10.1126/science.aal5056.
27. Jiang, F., Doudna, J.A., CRISPR-Cas9 structures and mechanisms. Annu. Rev. Biophys. 46 (2017), 505–529.
28. 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.
29. 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.
30. 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.
31. 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.
32. 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.
33. 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.
34. Kleinstiver, B.P., Pattanayak, V., Prew, M.S., Tsai, S.Q., Nguyen, N.T., Zheng, Z., Joung, J.K., High-fidelity CRISPR-Cas9 nucleases with no detectable genome-wide off-target effects. Nature 529 (2016), 490–495.
35. 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.
36. Koonin, E.V., Makarova, K.S., Zhang, F., Diversity, classification and evolution of CRISPR-Cas systems. Curr. Opin. Microbiol. 37 (2017), 67–78.
37. Kuscu, C., Arslan, S., Singh, R., Thorpe, J., Adli, M., Genome-wide analysis reveals characteristics of off-target sites bound by the Cas9 endonuclease. Nat. Biotechnol. 32 (2014), 677–683.
38. 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.
39. 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.e10.
40. 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.e12.
41. 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.
42. Marraffini, L.A., CRISPR-Cas immunity in prokaryotes. Nature 526 (2015), 55–61.
43. Mojica, F.J.M., 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.
44. Niewoehner, O., Jinek, M., Structural basis for the endoribonuclease activity of the type III-A CRISPR-associated protein Csm6. RNA 22 (2016), 318–329.
45. 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.
46. 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.
47. O'Connell, M.R., Oakes, B.L., Sternberg, S.H., East-Seletsky, A., Kaplan, M., Doudna, J.A., Programmable RNA recognition and cleavage by CRISPR/Cas9. Nature 516 (2014), 263–266.
48. 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.
49. Shao, S., Zhang, W., Hu, H., Xue, B., Qin, J., Sun, C., Sun, Y., Wei, W., Sun, Y., Long-term dual-color tracking of genomic loci by modified sgRNAs of the CRISPR/Cas9 system. Nucleic Acids Res., 44, 2016, e86.
50. 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.
51. 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.
52. Singh, D., Sternberg, S.H., Fei, J., Doudna, J.A., Ha, T., Real-time observation of DNA recognition and rejection by the RNA-guided endonuclease Cas9. Nat. Commun., 7, 2016, 12778.
53. Slaymaker, I.M., Gao, L., Zetsche, B., Scott, D.A., Yan, W.X., Zhang, F., Rationally engineered Cas9 nucleases with improved specificity. Science 351 (2016), 84–88.
54. 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.e7.
55. Sorek, R., Lawrence, C.M., Wiedenheft, B., CRISPR-mediated adaptive immune systems in bacteria and archaea. Annu. Rev. Biochem. 82 (2013), 237–266.
56. Stella, S., Alcón, P., Montoya, G., Structure of the Cpf1 endonuclease R-loop complex after target DNA cleavage. Nature 546 (2017), 559–563.
57. 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.
58. Sternberg, S.H., LaFrance, B., Kaplan, M., Doudna, J.A., Conformational control of DNA target cleavage by CRISPR-Cas9. Nature 527 (2015), 110–113.
59. Sternberg, S.H., Richter, H., Charpentier, E., Qimron, U., Adaptation in CRISPR-Cas systems. Mol. Cell 61 (2016), 797–808.
60. Swarts, D.C., Makarova, K., Wang, Y., Nakanishi, K., Ketting, R.F., Koonin, E.V., Patel, D.J., van der Oost, J., The evolutionary journey of Argonaute proteins. Nat. Struct. Mol. Biol. 21 (2014), 743–753.
61. 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.e4.
62. Szczelkun, M.D., Tikhomirova, M.S., Sinkunas, T., Gasiunas, G., Karvelis, T., Pschera, P., Siksnys, V., Seidel, R., Direct observation of R-loop formation by single RNA-guided Cas9 and Cascade effector complexes. Proc. Natl. Acad. Sci. USA 111 (2014), 9798–9803.
63. Tamulaitis, G., Venclovas, Č., Siksnys, V., Type III CRISPR-Cas immunity: major differences brushed aside. Trends Microbiol. 25 (2017), 49–61.
64. Tang, X., Lowder, L.G., Zhang, T., Malzahn, A.A., Zheng, X., Voytas, D.F., Zhong, Z., Chen, Y., Ren, Q., Li, Q., et al. A CRISPR-Cpf1 system for efficient genome editing and transcriptional repression in plants. Nat Plants, 3, 2017, 17018.
65. Tsai, S.Q., Joung, J.K., Defining and improving the genome-wide specificities of CRISPR-Cas9 nucleases. Nat. Rev. Genet. 17 (2016), 300–312.
66. Wang, H., La Russa, M., Qi, L.S., CRISPR/Cas9 in genome editing and beyond. Annu. Rev. Biochem. 85 (2016), 227–264.
67. Wu, X., Scott, D.A., Kriz, A.J., Chiu, A.C., Hsu, P.D., Dadon, D.B., Cheng, A.W., Trevino, A.E., Konermann, S., Chen, S., et al. Genome-wide binding of the CRISPR endonuclease Cas9 in mammalian cells. Nat. Biotechnol. 32 (2014), 670–676.
68. Wu, D., Guan, X., Zhu, Y., Ren, K., Huang, Z., Structural basis of stringent PAM recognition by CRISPR-C2c1 in complex with sgRNA. Cell Res. 27 (2017), 705–708.
69. 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.
70. 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.e12.
71. 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.
72. Zetsche, B., Heidenreich, M., Mohanraju, P., Fedorova, I., Kneppers, J., DeGennaro, E.M., Winblad, N., Choudhury, S.R., Abudayyeh, O.O., Gootenberg, J.S., et al. Multiplex gene editing by CRISPR-Cpf1 using a single crRNA array. Nat. Biotechnol. 35 (2017), 31–34.
73. Zhang, X., Wang, J., Cheng, Q., Zheng, X., Zhao, G., Wang, J., Multiplex gene regulation by CRISPR-ddCpf1. Cell Discov., 3, 2017, 17018.
74. 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.
75. Zhong, G., Wang, H., Li, Y., Tran, M.H., Farzan, M., Cpf1 proteins excise CRISPR RNAs from mRNA transcripts in mammalian cells. Nat. Chem. Biol. 13 (2017), 839–841.