Repurposing endogenous type i CRISPR-Cas systems for programmable gene repression

Nucleic Acids Research

Volumn 43, Issue 1, 2015, Pages 674-681

  Luo, Michelle L ^a   Mullis, Adam S ^a   Leenay, Ryan T ^a   Beisel, Chase L ^a  

^a North Carolina State University   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CRISPR ASSOCIATED PROTEIN;

CELL ENGINEERING; CRISPR CAS SYSTEM; ESCHERICHIA COLI; GENE DELETION; GENETIC TRANSCRIPTION; GENETICS;

CELL ENGINEERING; CRISPR-ASSOCIATED PROTEINS; CRISPR-CAS SYSTEMS; ESCHERICHIA COLI; GENE DELETION; TRANSCRIPTION, GENETIC;

EID: 84941084492     PISSN: 03051048     EISSN: 13624962     Source Type: Journal    
DOI: 10.1093/nar/gku971     Document Type: Article

References (59)

1. Sorek, R., Lawrence, C. M. And Wiedenheft, B. (2013) CRISPR-mediated adaptive immune systems in bacteria and archaea. Annu. Rev. Biochem., 82, 237-266.
2. Barrangou, R., Fremaux, C., Deveau, H., Richards, M., Boyaval, P., Moineau, S., Romero, D. A. And Horvath, P. (2007) CRISPR provides acquired resistance against viruses in prokaryotes. Science, 315, 1709-1712.
3. Makarova, K. S., Haft, D. H., Barrangou, R., Brouns, S. J. J., Charpentier, E., Horvath, P., Moineau, S., Mojica, F. J. M., Wolf, Y. I., Yakunin, A. F. et al. (2011) Evolution and classification of the CRISPR-Cas systems. Nat. Rev. Microbiol., 9, 467-477.
4. Brouns, S. J. J., Jore, M. M., Lundgren, M., Westra, E. R., Slijkhuis, R. J. H., Snijders, A. P. L., Dickman, M. J., Makarova, K. S., Koonin, E. V. And van der Oost, J. (2008) Small CRISPR RNAs guide antiviral defense in prokaryotes. Science, 321, 960-964.
5. Semenova, E., Jore, M. M., Datsenko, K. A., Semenova, A., Westra, E. R., Wanner, B., van der Oost, J., Brouns, S. J. J. And Severinov, K. (2011) Interference by clustered regularly interspaced short palindromic repeat (CRISPR) RNA is governed by a seed sequence. Proc. Natl Acad. Sci. U. S. A., 108, 10098-10103.
6. Deltcheva, E., Chylinski, K., Sharma, C. M., Gonzales, K., Chao, Y., Pirzada, Z. A., Eckert, M. R., Vogel, J. And Charpentier, E. (2011) CRISPR RNA maturation by trans-encoded small RNA and host factor RNase III. Nature, 471, 602-607.
7. Garneau, J. E., Dupuis, M.-E., Villion, M., Romero, D. A., Barrangou, R., Boyaval, P., Fremaux, C., Horvath, P., Magadán, A. H. And Moineau, S. (2010) The CRISPR/Cas bacterial immune system cleaves bacteriophage and plasmid DNA. Nature, 468, 67-71.
8. Hsu, P. D., Lander, E. S. And Zhang, F. (2014) Development and applications of CRISPR-Cas9 for genome engineering. Cell, 157, 1262-1278.
9. Sander, J. D. And Joung, J. K. (2014) CRISPR-Cas systems for editing, regulating and targeting genomes. Nat. Biotechnol., 32, 347-355.
10. Fineran, P. C. And Dy, R. L. (2014) Gene regulation by engineered CRISPR-Cas systems. Curr. Opin. Microbiol., 18, 83-89.
11. Bikard, D. And Marraffini, L. A. (2013) Control of gene expression by CRISPR-Cas systems. F1000prime Rep., 5, 47.
12. Jinek, M., Chylinski, K., Fonfara, I., Hauer, M., Doudna, J. A. And Charpentier, E. (2012) A programmable dual-RNA-guided DNA endonuclease in adaptive bacterial immunity. Science, 337, 816-821.
13. Qi, L. S., Larson, M. H., Gilbert, L. A., Doudna, J. A., Weissman, J. S., Arkin, A. P. And Lim, W. A. (2013) Repurposing CRISPR as an RNA-guided platform for sequence-specific control of gene expression. Cell, 152, 1173-1183.
14. Gilbert, L. A., Larson, M. H., Morsut, L., Liu, Z., Brar, G. A., Torres, S. E., Stern-Ginossar, N., Brandman, O., Whitehead, E. H., Doudna, J. A. et al. (2013) CRISPR-mediated modular RNA-guided regulation of transcription in eukaryotes. Cell, 154, 442-451.
15. Perez-Pinera, P., Kocak, D. D., Vockley, C. M., Adler, A. F., Kabadi, A. M., Polstein, L. R., Thakore, P. I., Glass, K. A., Ousterout, D. G., Leong, K. W. et al. (2013) RNA-guided gene activation by CRISPR-Cas9-based transcription factors. Nat. Methods, 10, 973-976.
16. Mali, P., Aach, J., Stranges, P. B., Esvelt, K. M., Moosburner, M., Kosuri, S., Yang, L. And Church, G. M. (2013) CAS9 transcriptional activators for target specificity screening and paired nickases for cooperative genome engineering. Nat. Biotechnol., 31, 833-838.
17. Bikard, D., Jiang, W., Samai, P., Hochschild, A., Zhang, F. And Marraffini, L. A. (2013) Programmable repression and activation of bacterial gene expression using an engineered CRISPR-Cas system. Nucleic Acids Res., 41, 7429-7437.
18. Hale, C. R., Zhao, P., Olson, S., Duff, M. O., Graveley, B. R., Wells, L., Terns, R. M. And Terns, M. P. (2009) RNA-guided RNA cleavage by a CRISPR RNA-Cas protein complex. Cell, 139, 945-956.
19. Zebec, Z., Manica, A., Zhang, J., White, M. F. And Schleper, C. (2014) CRISPR-mediated targeted mRNA degradation in the archaeon Sulfolobus solfataricus. Nucleic Acids Res., 42, 5280-5288.
20. Hale, C. R., Majumdar, S., Elmore, J., Pfister, N., Compton, M., Olson, S., Resch, A. M., Glover, C. V. C. III, Graveley, B. R., Terns, R. M. et al. (2012) Essential features and rational design of CRISPR RNAs that function with the Cas RAMP module complex to cleave RNAs. Mol. Cell, 45, 292-302.
21. 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. (2011) Structural basis for CRISPR RNA-guided DNA recognition by Cascade. Nat. Struct. Mol. Biol., 18, 529-536.
22. Nam, K. H., Haitjema, C., Liu, X., Ding, F., Wang, H., DeLisa, M. P. And Ke, A. (2012) Cas5d protein processes pre-crRNA and assembles into a Cascade-like interference complex in subtype I-C/Dvulg CRISPR-Cas system. Struct. Lond. Engl. 1993, 20, 1574-1584.
23. Westra, E. R., van Erp, P. B. G., Künne, T., Wong, S. P., Staals, R. H. J., Seegers, C. L. C., Bollen, S., Jore, M. M., Semenova, E., Severinov, K. et al. (2012) CRISPR immunity relies on the consecutive binding and degradation of negatively supercoiled invader DNA by Cascade and Cas3. Mol. Cell, 46, 595-605.
24. Sinkunas, T., Gasiunas, G., Fremaux, C., Barrangou, R., Horvath, P. And Siksnys, V. (2011) Cas3 is a single-stranded DNA nuclease and ATP-dependent helicase in the CRISPR/Cas immune system. EMBO J., 30, 1335-1342.
25. Hochstrasser, M. L., Taylor, D. W., Bhat, P., Guegler, C. K., Sternberg, S. H., Nogales, E. And Doudna, J. A. (2014) CasA mediates Cas3-catalyzed target degradation during CRISPR RNA-guided interference. Proc. Natl Acad. Sci. U. S. A., 111, 6618-6623.
26. Jackson, R. N., Lavin, M., Carter, J. And Wiedenheft, B. (2014) Fitting CRISPR-associated Cas3 into the helicase family tree. Curr. Opin. Struct. Biol., 24, 106-114.
27. Brendel, J., Stoll, B., Lange, S. J., Sharma, K., Lenz, C., Stachler, A.-E., Maier, L.-K., Richter, H., Nickel, L., Schmitz, R. A. et al. (2014) A complex of Cas proteins 5, 6, and 7 is required for the biogenesis and stability of clustered regularly interspaced short palindromic repeats (CRISPR)-derived RNAs (crRNAs) in Haloferax volcanii. J. Biol. Chem., 289, 7164-7177.
28. Richter, C., Gristwood, T., Clulow, J. S. And Fineran, P. C. (2012) In vivo protein interactions and complex formation in the Pectobacterium atrosepticum subtype I-F CRISPR/Cas system. PloS One, 7, e49549.
29. Wiedenheft, B., van Duijn, E., Bultema, J. B., Bultema, J., Waghmare, S. P., Waghmare, S., Zhou, K., Barendregt, A., Westphal, W., Heck, A. J. R. et al. (2011) RNA-guided complex from a bacterial immune system enhances target recognition through seed sequence interactions. Proc. Natl Acad. Sci. U. S. A., 108, 10092-10097.
30. Datsenko, K. A. And Wanner, B. L. (2000) One-step inactivation of chromosomal genes in Escherichia coli K-12 using PCR products. Proc. Natl Acad. Sci. U. S. A., 97, 6640-6645.
31. Court, D. L., Swaminathan, S., Yu, D., Wilson, H., Baker, T., Bubunenko, M., Sawitzke, J. And Sharan, S. K. (2003) Mini-lambda: A tractable system for chromosome and BAC engineering. Gene, 315, 63-69.
32. Cherepanov, P. P. And Wackernagel, W. (1995) Gene disruption in Escherichia coli: TcR and KmR cassettes with the option of Flp-catalyzed excision of the antibiotic-resistance determinant. Gene, 158, 9-14.
33. Zaslaver, A., Bren, A., Ronen, M., Itzkovitz, S., Kikoin, I., Shavit, S., Liebermeister, W., Surette, M. G. And Alon, U. (2006) A comprehensive library of fluorescent transcriptional reporters for Escherichia coli. Nat. Methods, 3, 623-628.
34. Afroz, T., Biliouris, K., Kaznessis, Y. And Beisel, C. L. (2014) Bacterial sugar utilization gives rise to distinct single-cell behaviours. Mol. Microbiol., 93, 1093-1103.
35. Gomaa, A. A., Klumpe, H. E., Luo, M. L., Selle, K., Barrangou, R. And Beisel, C. L. (2014) Programmable removal of bacterial strains by use of genome-targeting CRISPR-Cas systems. mBio, 5, e00928-e00913.
36. Stead, M. B., Agrawal, A., Bowden, K. E., Nasir, R., Mohanty, B. K., Meagher, R. B. And Kushner, S. R. (2012) RNAsnapTM: A rapid, quantitative and inexpensive, method for isolating total RNA from bacteria. Nucleic Acids Res., 40, e156.
37. Pul, U., Wurm, R., Arslan, Z., Geissen, R., Hofmann, N. And Wagner, R. (2010) Identification and characterization of E. coli CRISPR-cas promoters and their silencing by H-NS. Mol. Microbiol., 75, 1495-1512.
38. Westra, E. R., Pul, U., Heidrich, N., Jore, M. M., Lundgren, M., Stratmann, T., Wurm, R., Raine, A., Mescher, M., Van Heereveld, L. et al. (2010) H-NS-mediated repression of CRISPR-based immunity in Escherichia coli K12 can be relieved by the transcription activator LeuO. Mol. Microbiol., 77, 1380-1393.
39. Kovacic, R. T. (1987) The 0C closed complexes between Escherichia coli RNA polymerase and two promoters, T7-A3 and lacUV5. J. Biol. Chem., 262, 13654-13661.
40. Hussein, R. And Lim, H. N. (2011) Disruption of small RNA signaling caused by competition for Hfq. Proc. Natl Acad. Sci. U. S. A., 108, 1110-1115.
41. Gross, J. And Englesberg, E. (1959) Determination of the order of mutational sites governing L-arabinose utilization in Escherichia coli B/r bv transduction with phage Plbt. Virology, 9, 314-331.
42. Power, J. (1967) The L-rhamnose genetic system in Escherichia coli K-12. Genetics, 55, 557-568.
43. Lawlis, V. B., Dennis, M. S., Chen, E. Y., Smith, D. H. And Henner, D. J. (1984) Cloning and sequencing of the xylose isomerase and xylulose kinase genes of Escherichia coli. Appl. Environ. Microbiol., 47, 15-21.
44. Beckwith, J. R. (1967) Regulation of the lac operon. Recent studies on the regulation of lactose metabolism in Escherichia coli support the operon model. Science, 156, 597-604.
45. Plagens, A., Tripp, V., Daume, M., Sharma, K., Klingl, A., Hrle, A., Conti, E., Urlaub, H. And Randau, L. (2014) In vitro assembly and activity of an archaeal CRISPR-Cas type I-A Cascade interference complex. Nucleic Acids Res., 42, 5125-5138.
46. Esvelt, K. M., Mali, P., Braff, J. L., Moosburner, M., Yaung, S. J. And Church, G. M. (2013) Orthogonal Cas9 proteins for RNA-guided gene regulation and editing. Nat. Methods, 10, 1116-1121.
47. Grissa, I., Vergnaud, G. And Pourcel, C. (2007) The CRISPRdb database and tools to display CRISPRs and to generate dictionaries of spacers and repeats. BMC Bioinformatics, 8, 172.
48. Jiang, W., Bikard, D., Cox, D., Zhang, F. And Marraffini, L. A. (2013) RNA-guided editing of bacterial genomes using CRISPR-Cas systems. Nat. Biotechnol., 31, 233-239.
49. Nishimasu, H., Ran, F. A., Hsu, P. D., Konermann, S., Shehata, S. I., Dohmae, N., Ishitani, R., Zhang, F. And Nureki, O. (2014) Crystal structure of Cas9 in complex with guide RNA and target DNA. Cell, 156, 935-949.
50. Fu, Y., Foden, J. A., Khayter, C., Maeder, M. L., Reyon, D., Joung, J. K. And Sander, J. D. (2013) High-frequency off-target mutagenesis induced by CRISPR-Cas nucleases in human cells. Nat. Biotechnol., 31, 822-826.
51. Pattanayak, V., Lin, S., Guilinger, J. P., Ma, E., Doudna, J. A. And Liu, D. R. (2013) High-throughput profiling of off-target DNA cleavage reveals RNA-programmed Cas9 nuclease specificity. Nat. Biotechnol., 31, 839-843.
52. Hsu, P. D., Scott, D. A., Weinstein, J. A., Ran, F. A., Konermann, S., Agarwala, V., Li, Y., Fine, E. J., Wu, X., Shalem, O. et al. (2013) DNA targeting specificity of RNA-guided Cas9 nucleases. Nat. Biotechnol., 31, 827-832.
53. Kuscu, C., Arslan, S., Singh, R., Thorpe, J. And Adli, M. (2014) Genome-wide analysis reveals characteristics of off-target sites bound by the Cas9 endonuclease. Nat. Biotechnol., 32, 677-683.
54. Fineran, P. C., Gerritzen, M. J. H., Suárez-Diez, M., Künne, T., Boekhorst, J., van Hijum, S. A. F. T., Staals, R. H. J. And Brouns, S. J. J. (2014) Degenerate target sites mediate rapid primed CRISPR adaptation. Proc. Natl Acad. Sci. U. S. A., 111, E1629-E1638.
55. Smith, C., Gore, A., Yan, W., Abalde-Atristain, L., Li, Z., He, C., Wang, Y., Brodsky, R. A., Zhang, K., Cheng, L. et al. (2014) Whole-genome sequencing analysis reveals high specificity of CRISPR/Cas9 and TALEN-based genome editing in human iPSCs. Cell Stem Cell, 15, 12-13.
56. Veres, A., Gosis, B. S., Ding, Q., Collins, R., Ragavendran, A., Brand, H., Erdin, S., Talkowski, M. E. And Musunuru, K. (2014) Low incidence of off-target mutations in individual CRISPR-Cas9 and TALEN targeted human stem cell clones detected by whole-genome sequencing. Cell Stem Cell, 15, 27-30.
57. Stern, A., Keren, L., Wurtzel, O., Amitai, G. And Sorek, R. (2010) Self-targeting by CRISPR: gene regulation or autoimmunity Trends Genet., 26, 335-340.
58. Sampson, T. R., Napier, B. A., Schroeder, M. R., Louwen, R., Zhao, J., Chin, C.-Y., Ratner, H. K., Llewellyn, A. C., Jones, C. L., Laroui, H. et al. (2014) A CRISPR-Cas system enhances envelope integrity mediating antibiotic resistance and inflammasome evasion. Proc. Natl Acad. Sci. U. S. A., 111, 11163-11168.
59. Sampson, T. R., Saroj, S. D., Llewellyn, A. C., Tzeng, Y.-L. And Weiss, D. S. (2013) A CRISPR/Cas system mediates bacterial innate immune evasion and virulence. Nature, 497, 254-257.