The Cas6e ribonuclease is not required for interference and adaptation by the E. Colitype I-E CRISPR-Cas system

Nucleic Acids Research

Volumn 43, Issue 12, 2015, Pages 6049-6061

  Semenova, Ekaterina ^a   Kuznedelov, Konstantin ^a   Datsenko, Kirill A ^a,b   Boudry, Pierre M ^a,c   Savitskaya, Ekaterina E ^d,e   Medvedeva, Sofia ^d,f   Beloglazova, Natalia ^g   Logacheva, Maria ^h,i   Yakunin, Alexander F ^g   Severinov, Konstantin ^a,d,e,f,j  

^a RUTGERS UNIVERSITY   (United States)

^b PURDUE UNIVERSITY   (United States)

^c INSTITUT PASTEUR   (France)

^d SKOLKOVO INSTITUTE OF SCIENCE AND TECHNOLOGY   (Russian Federation)

^e INSTITUTE OF MOLECULAR GENETICS   (Russian Federation)

^f INSTITUTE OF GENE BIOLOGY   (Russian Federation)

^g UNIVERSITY OF TORONTO   (Canada)

^h MOSCOW STATE UNIVERSITY   (Russian Federation)

ⁱ PIROGOV RUSSIAN NATIONAL RESEARCH MEDICAL UNIVERSITY   (Russian Federation)

^j PETER THE GREAT ST PETERSBURG POLYTECHNIC UNIVERSITY   (Russian Federation)

more..

Author keywords

[No Author keywords available]

Indexed keywords

DOUBLE STRANDED DNA; ENDORIBONUCLEASE CAS6E; NUCLEASE; RIBONUCLEASE; UNCLASSIFIED DRUG; CRISPR ASSOCIATED PROTEIN; RNA;

ARTICLE; BACTERIAL CELL; BACTERIAL STRAIN; CONTROLLED STUDY; CRISPR CAS SYSTEM; ENTEROBACTERIA PHAGE T5; ESCHERICHIA COLI; GENETIC TRANSCRIPTION; HIGH THROUGHPUT SEQUENCING; MOLECULAR PROBE; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; SIMPLE SEQUENCE REPEAT; BACTERIOPHAGE; ENZYMOLOGY; GENETICS; METABOLISM; PHYSIOLOGY; PLASMID; TRANSCRIPTION TERMINATION;

BACTERIOPHAGES; CRISPR-ASSOCIATED PROTEINS; CRISPR-CAS SYSTEMS; ENDORIBONUCLEASES; ESCHERICHIA COLI; PLASMIDS; RNA; TRANSCRIPTION TERMINATION, GENETIC;

EID: 84942156327     PISSN: 03051048     EISSN: 13624962     Source Type: Journal    
DOI: 10.1093/nar/gkv546     Document Type: Article

References (76)

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2. Bhaya, D., Davison, M. and Barrangou, R. (2011) CRISPR-Cas systems in bacteria and archaea: versatile small RNAs for adaptive defense and regulation. Annu. Rev. Genet., 45, 273-297.
3. 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.
4. van der Oost, J., Jore, M.M., Westra, E.R., Lundgren, M. and Brouns, S.J. (2009) CRISPR-based adaptive and heritable immunity in prokaryotes. Trends Biochem. Sci., 34, 401-407.
5. 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. and van der Oost, J. (2008) Small CRISPR RNAs guide antiviral defense in prokaryotes. Science, 321, 960-964.
6. 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. (2011) Evolution and classification of the CRISPR-Cas systems. Nat. Rev. Microbiol., 9, 467-477.
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9. Westra, E.R., Semenova, E., Datsenko, K.A., Jackson, R.N., Wiedenheft, B., Severinov, K. and Brouns, S.J. (2013) Type I-E CRISPR-cas systems discriminate target from non-target DNA through base pairing-independent PAM recognition. PLoS Genet., 9, e1003742.
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12. Mulepati, S., Heroux, A. and Bailey, S. (2014) Crystal structure of a CRISPR RNA-guided surveillance complex bound to a ssDNA target. Science, 345, 1479-1484.
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14. Sashital, D.G., Jinek, M. and Doudna, J.A. (2011) An RNA-induced conformational change required for CRISPR RNA cleavage by the endoribonuclease Cse3. Nat. Struct. Mol. Biol., 18, 680-687.
15. Westra, E.R., van Erp, P.B., Kunne, T., Wong, S.P., Staals, R.H., Seegers, C.L., 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.
16. Mulepati, S. and Bailey, S. (2013) In vitro reconstitution of an Escherichia coli RNA-guided immune system reveals unidirectional, ATP-dependent degradation of DNA target. J. Biol. Chem., 288, 22184-22192.
17. Yosef, I., Goren, M.G. and Qimron, U. (2012) Proteins and DNA elements essential for the CRISPR adaptation process in Escherichia coli. Nucleic Acids Res., 40, 5569-5576.
18. Datsenko, K.A., Pougach, K., Tikhonov, A., Wanner, B.L., Severinov, K. and Semenova, E. (2012) Prior encounters dramatically stimulate adaptive bacterial CRISPR immune response to viruses. Nat. Commun., 3, 945.
19. Swarts, D.C., Mosterd, C., van Passel, M.W. and Brouns, S.J. (2012) CRISPR interference directs strand specific spacer acquisition. PLoS One, 7, e35888.
20. Fineran, P.C., Gerritzen, M.J., Suárez-Diez, M., Künne, T., Boekhorst, J., van Hijum, S.A., Staals, R.H. and Brouns, S.J. (2014) Degenerate target sites mediate rapid primed CRISPR adaptation. Proc. Natl. Acad. Sci. U.S.A., 111, 1629-1638.
21. Pougach, K., Semenova, E., Bogdanova, E., Datsenko, K.A., Djordjevic, M., Wanner, B.L. and Severinov, K. (2010) Transcription, transcript processing and function of E. coli CRISPR locus. Mol Microbiol, 77, 1367-1379.
22. Maier, L.K., Stachler, A.E., Saunders, S.J., Backofen, R. and Marchfelder, A. (2015) An active immune defense with a minimal CRISPR (Clustered Regularly Interspaced Short Palindromic Repeats) RNA and without the Cas6 Protein. J. Biol. Chem., 290, 4192-4201.
23. Beloglazova, N., Kuznedelov, K., Flick, R., Datsenko, K.A., Brown, G., Popovic, A., Lemak, S., Semenova, E., Severinov, K. and Yakunin, A.F. (2015) CRISPR RNA binding and DNA targeting by purified Cascade complexes from Escherichia coli. Nucleic Acids Res., 43, 530-543.
24. 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.
25. Pougach, K. and Severinov, K. (2012) Use of semi-quantitative Northern blot analysis to determine relative quantities of bacterial CRISPR transcripts. Methods Mol. Biol, 905, 73-86.
26. Pages, H., Aboyoun, P, Gentleman, R. and DebRoy, S. (2012) R package version 2.24.1.
27. Krzywinski, M., Schein, J., Birol, I., Connors, J., Gascoyne, R., Horsman, D., Jones, S.J. and Marra, M.A. (2009) Circos: an information aesthetic for comparative genomics. Genome Res., 19, 1639-1645.
28. Farnham, PJ. and Platt, T. (1980) A model for transcription termination suggested by studies on the trp attenuator in vitro using base analogs. Cell, 20, 739-748.
29. Celesnik, H., Deana, A. and Belasco, J.G. (2007) Initiation of RNA decay in Escherichia coli by 5' pyrophosphate removal. Mol. Cell, 27: 79-90.
30. Severinov, K. and Goldfarb, A. (1994) Topology of the product binding site in RNA polymerase revealed by transcript slippage at the phage lambda PL promoter. J. Biol. Chem., 269, 31701-31705.
31. van Duijn, E., Barbu, I.M., Barendregt, A., Jore, M.M., Wiedenheft, B., Lundgren, M., Westra, E.R., Brouns, S.J., Doudna, J.A., van der Oost, J. et al. (2012) Native tandem and ion mobility mass spectrometry highlight structural and modular similarities in clustered-regularly-interspaced shot-palindromic-repeats (CRISPR)-associated protein complexes from Escherichia coli and Pseudomonas aeruginosa. Mol. Cell. Proteomics, 11, 1430-14341.
32. Savitskaya, E., Semenova, E., Dedkov, V., Metlitskaya, A. and Severinov, K. (2013) High-throughput analysis of type I-E CRISPR/Cas spacer acquisition in E. coli. RNA Biol., 10, 716-725.
33. Shmakov, S., Savitskaya, E., Semenova, E., Datsenko, K.A. and Severinov, K. (2014) Pervasive generation of oppositely-oriented spacers during CRISPR adaptation. Nucleic Acids Res., 42, 5907-5916.
34. Torres, M., Condon, C., Balada, J.M., Squires, C. and Squires, C.L. (2001) Ribosomal protein S4 is a transcription factor with properties remarkably similar to NusA, a protein involved in both non-ribosomal and ribosomal RNA antitermination. EMBO J., 20, 3811-3820.
35. Chylinski, K., Le Rhun, A. and Charpentier, E. (2013) The tracrRNA and Cas9 families of type II CRISPR-Cas immunity systems. RNA Biol. 10, 726-737.
36. Staals, R.H., Zhu, Y., Taylor, D.W., Kornfeld, J.E., Sharma, K., Barendregt, A., Koehorst, J.J., Vlot, M., Neupane, N., Varossieau, K. et al. (2014) RNA targeting by the type III-A CRISPR-Cas Csm complex of Thermus thermophilus. Mol. Cell, 56, 518-530.
37. Hale, C.R., Cocozaki, A., Li, H., Terns, R.M. and Terns, M.P. (2014) Target RNA capture and cleavage by the Cmr type III-B CRISPR-Cas effector complex. Genes Dev., 28, 2432-2443.
38. Konermann, S., Brigham, M.D., Trevino, A.E., Joung, J., Abudayyeh, O.O., Barcena, C., Hsu, P.D., Habib, N., Gootenberg, J.S., Nishimasu, H. et al. Genome-scale transcriptional activation by an engineered CRISPR-Cas9 complex. Nature, 517, 583-588.
39. Makarova, K.S., Grishin, N.V., Shabalina, S.A., Wolf, Y.I. and Koonin, E.V. (2006) 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, 7.
40. Bhaya, D., Davison, M. and Barrangou, R. (2011) CRISPR-Cas systems in bacteria and archaea: versatile small RNAs for adaptive defense and regulation. Annu. Rev. Genet., 45, 273-297.
41. 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.
42. van der Oost, J., Jore, M.M., Westra, E.R., Lundgren, M. and Brouns, S.J. (2009) CRISPR-based adaptive and heritable immunity in prokaryotes. Trends Biochem. Sci., 34, 401-407.
43. 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. and van der Oost, J. (2008) Small CRISPR RNAs guide antiviral defense in prokaryotes. Science, 321, 960-964.
44. 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. (2011) Evolution and classification of the CRISPR-Cas systems. Nat. Rev. Microbiol., 9, 467-477.
45. 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.
46. Semenova, E., Jore, M.M., Datsenko, K.A., Semenova, A., Westra, E.R., Wanner, B., van der Oost, J., Brouns, S.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.
47. Westra, E.R., Semenova, E., Datsenko, K.A., Jackson, R.N., Wiedenheft, B., Severinov, K. and Brouns, S.J. (2013) Type I-E CRISPR-cas systems discriminate target from non-target DNA through base pairing-independent PAM recognition. PLoS Genet., 9, e1003742.
48. Sashital, D.G., Wiedenheft, B. and Doudna, J.A. (2012) Mechanism of foreign DNA selection in a bacterial adaptive immune system. Mol. Cell, 46, 606-615.
49. 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. and Wiedenheft, B. (2014) Crystal structure of the CRISPR RNA-guided surveillance complex from Escherichia coli. Science, 345, 1473-1479.
50. Mulepati, S., Heroux, A. and Bailey, S. (2014) Crystal structure of a CRISPR RNA-guided surveillance complex bound to a ssDNA target. Science, 345, 1479-1484.
51. Zhao, H., Sheng, G., Wang, J., Wang, M., Bunkoczi, G., Gong, W., Wei, Z. and Wang, Y. (2014) Crystal structure of the RNA-guided immune surveillance Cascade complex in Escherichia coli. Nature, 515, 147-150.
52. Sashital, D.G., Jinek, M. and Doudna, J.A. (2011) An RNA-induced conformational change required for CRISPR RNA cleavage by the endoribonuclease Cse3. Nat. Struct. Mol. Biol., 18, 680-687.
53. Westra, E.R., van Erp, P.B., Kunne, T., Wong, S.P., Staals, R.H., Seegers, C.L., 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.
54. Mulepati, S. and Bailey, S. (2013) In vitro reconstitution of an Escherichia coli RNA-guided immune system reveals unidirectional, ATP-dependent degradation of DNA target. J. Biol. Chem., 288, 22184-22192.
55. Yosef, I., Goren, M.G. and Qimron, U. (2012) Proteins and DNA elements essential for the CRISPR adaptation process in Escherichia coli. Nucleic Acids Res., 40, 5569-5576.
56. Datsenko, K.A., Pougach, K., Tikhonov, A., Wanner, B.L., Severinov, K. and Semenova, E. (2012) Prior encounters dramatically stimulate adaptive bacterial CRISPR immune response to viruses. Nat. Commun., 3, 945.
57. Swarts, D.C., Mosterd, C., van Passel, M.W. and Brouns, S.J. (2012) CRISPR interference directs strand specific spacer acquisition. PLoS One, 7, e35888.
58. Fineran, P.C., Gerritzen, M.J., Suárez-Diez, M., Künne, T., Boekhorst, J., van Hijum, S.A., Staals, R.H. and Brouns, S.J. (2014) Degenerate target sites mediate rapid primed CRISPR adaptation. Proc. Natl. Acad. Sci. U.S.A., 111, 1629-1638.
59. Pougach, K., Semenova, E., Bogdanova, E., Datsenko, K.A., Djordjevic, M., Wanner, B.L. and Severinov, K. (2010) Transcription, transcript processing and function of E. coli CRISPR locus. Mol Microbiol, 77, 1367-1379.
60. Maier, L.K., Stachler, A.E., Saunders, S.J., Backofen, R. and Marchfelder, A. (2015) An active immune defense with a minimal CRISPR (Clustered Regularly Interspaced Short Palindromic Repeats) RNA and without the Cas6 Protein. J. Biol. Chem., 290, 4192-4201.
61. Beloglazova, N., Kuznedelov, K., Flick, R., Datsenko, K.A., Brown, G., Popovic, A., Lemak, S., Semenova, E., Severinov, K. and Yakunin, A.F. (2015) CRISPR RNA binding and DNA targeting by purified Cascade complexes from Escherichia coli. Nucleic Acids Res., 43, 530-543.
62. 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.
63. Pougach, K. and Severinov, K. (2012) Use of semi-quantitative Northern blot analysis to determine relative quantities of bacterial CRISPR transcripts. Methods Mol. Biol, 905, 73-86.
64. Pages, H., Aboyoun, P, Gentleman, R. and DebRoy, S. (2012) R package version 2.24.1.
65. Krzywinski, M., Schein, J., Birol, I., Connors, J., Gascoyne, R., Horsman, D., Jones, S.J. and Marra, M.A. (2009) Circos: an information aesthetic for comparative genomics. Genome Res., 19, 1639-1645.
66. Farnham, PJ. and Platt, T. (1980) A model for transcription termination suggested by studies on the trp attenuator in vitro using base analogs. Cell, 20, 739-748.
67. Celesnik, H., Deana, A. and Belasco, J.G. (2007) Initiation of RNA decay in Escherichia coli by 5' pyrophosphate removal. Mol. Cell, 27: 79-90.
68. Severinov, K. and Goldfarb, A. (1994) Topology of the product binding site in RNA polymerase revealed by transcript slippage at the phage lambda PL promoter. J. Biol. Chem., 269, 31701-31705.
69. van Duijn, E., Barbu, I.M., Barendregt, A., Jore, M.M., Wiedenheft, B., Lundgren, M., Westra, E.R., Brouns, S.J., Doudna, J.A., van der Oost, J. et al. (2012) Native tandem and ion mobility mass spectrometry highlight structural and modular similarities in clustered-regularly-interspaced shot-palindromic-repeats (CRISPR)-associated protein complexes from Escherichia coli and Pseudomonas aeruginosa. Mol. Cell. Proteomics, 11, 1430-14341.
70. Savitskaya, E., Semenova, E., Dedkov, V., Metlitskaya, A. and Severinov, K. (2013) High-throughput analysis of type I-E CRISPR/Cas spacer acquisition in E. coli. RNA Biol., 10, 716-725.
71. Shmakov, S., Savitskaya, E., Semenova, E., Datsenko, K.A. and Severinov, K. (2014) Pervasive generation of oppositely-oriented spacers during CRISPR adaptation. Nucleic Acids Res., 42, 5907-5916.
72. Torres, M., Condon, C., Balada, J.M., Squires, C. and Squires, C.L. (2001) Ribosomal protein S4 is a transcription factor with properties remarkably similar to NusA, a protein involved in both non-ribosomal and ribosomal RNA antitermination. EMBO J., 20, 3811-3820.
73. Chylinski, K., Le Rhun, A. and Charpentier, E. (2013) The tracrRNA and Cas9 families of type II CRISPR-Cas immunity systems. RNA Biol. 10, 726-737.
74. Staals, R.H., Zhu, Y., Taylor, D.W., Kornfeld, J.E., Sharma, K., Barendregt, A., Koehorst, J.J., Vlot, M., Neupane, N., Varossieau, K. et al. (2014) RNA targeting by the type III-A CRISPR-Cas Csm complex of Thermus thermophilus. Mol. Cell, 56, 518-530.
75. Hale, C.R., Cocozaki, A., Li, H., Terns, R.M. and Terns, M.P. (2014) Target RNA capture and cleavage by the Cmr type III-B CRISPR-Cas effector complex. Genes Dev., 28, 2432-2443.
76. Konermann, S., Brigham, M.D., Trevino, A.E., Joung, J., Abudayyeh, O.O., Barcena, C., Hsu, P.D., Habib, N., Gootenberg, J.S., Nishimasu, H. et al. Genome-scale transcriptional activation by an engineered CRISPR-Cas9 complex. Nature, 517, 583-588.