Transcriptional regulator-mediated activation of adaptation genes triggers CRISPR de novo spacer acquisition

Nucleic Acids Research

Volumn 43, Issue 2, 2015, Pages 1044-1055

  Liu, Tao ^a   Li, Yingjun ^a   Wang, Xiaodi ^a   Ye, Qing ^a   Li, Huan ^a   Liang, Yunxiang ^a,b   She, Qunxin ^c   Peng, Nan ^a,b  

^a HUAZHONG AGRICULTURAL UNIVERSITY   (China)

^b Hubei Collaborative Innovation Center for Automotive Components Technology   (China)

^c UNIVERSITY OF COPENHAGEN   (Denmark)

Author keywords

[No Author keywords available]

Indexed keywords

ARCHAEAL DNA; CRISPR ASSOCIATED PROTEIN; TRANSACTIVATOR PROTEIN;

BINDING SITE; CHEMISTRY; CLUSTERED REGULARLY INTERSPACED SHORT PALINDROMIC REPEAT; CRISPR CAS SYSTEM; GENETICS; METABOLISM; PROMOTER REGION; SULFOLOBUS; TRANSCRIPTION INITIATION;

BINDING SITES; CLUSTERED REGULARLY INTERSPACED SHORT PALINDROMIC REPEATS; CRISPR-ASSOCIATED PROTEINS; CRISPR-CAS SYSTEMS; DNA, ARCHAEAL; PROMOTER REGIONS, GENETIC; SULFOLOBUS; TRANS-ACTIVATORS; TRANSCRIPTIONAL ACTIVATION;

EID: 84941035583     PISSN: 03051048     EISSN: 13624962     Source Type: Journal    
DOI: 10.1093/nar/gku1383     Document Type: Article

References (51)

1. 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.
2. 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.
3. Sorek,R., Kunin,V. and Hugenholtz,P. (2008) CRISPR-a widespread system that provides acquired resistance against phages in bacteria and archaea. Nat. Rev Microbiol., 6, 181-186.
4. Mojica,F.J., Diez-Villasenor,C., Garcia-Martinez,J. and Soria,E. (2005) Intervening sequences of regularly spaced prokaryotic repeats derive from foreign genetic elements. J. Mol. Evol., 60, 174-182.
5. Kunin,V., Sorek,R. and Hugenholtz,P. (2007) Evolutionary conservation of sequence and secondary structures in CRISPR repeats. Genome Biol., 8, R61.
6. Pourcel,C., Salvignol,G. and Vergnaud,G. (2005) CRISPR elements in Yersinia pestis acquire new repeats by preferential uptake of bacteriophage DNA, and provide additional tools for evolutionary studies. Microbiology, 151, 653-663.
7. Bolotin,A., Quinquis,B., Sorokin,A. and Ehrlich,S.D. (2005) Clustered regularly interspaced short palindrome repeats (CRISPRs) have spacers of extrachromosomal origin. Microbiology, 151, 2551-2561.
8. Shah,S.A., Hansen,N.R. and Garrett,R.A. (2009) Distribution of CRISPR spacer matches in viruses and plasmids of crenarchaeal acidothermophiles and implications for their inhibitory mechanism. Biochem. Soc. Trans., 37, 23-28.
9. 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.
10. Agari,Y., Sakamoto,K., Tamakoshi,M., Oshima,T., Kuramitsu,S. and Shinkai,A. (2010) Transcription profile of Thermus thermophilus CRISPR systems after phage infection. J. Mol. Biol., 395, 270-281.
11. Pougach,K., Semenova,E., Bogdanova,E., Datsenko,K.A., Djordjevic,M.,Wanner,B.L. and Severinov,K. (2010) Transcription, processing and function of CRISPR cassettes in Escherichia coli. Mol. Microbiol., 77, 1367-1379.
12. Haft,D.H., Selengut,J., Mongodin,E.F. and Nelson,K.E. (2005) A guild of 45 CRISPR-associated (Cas) protein families and multiple CRISPR/Cas subtypes exist in prokaryotic genomes. PLoS Comp. Biol., 1, e60.
13. Koonin,E.V. and Makarova,K.S. (2013) CRISPR-Cas: evolution of an RNA-based adaptive immunity system in prokaryotes. RNA Biol., 10, 679-686.
14. 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.
15. Westra,E.R., Swarts,D.C., Staals,R.H., Jore,M.M., Brouns,S.J. and van der Oost,J. (2012) The CRISPRs, they are a-changin': how prokaryotes generate adaptive immunity. Annu. Rev. Genet., 46, 311-339.
16. 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.
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. Yosef,I., Shitrit,D., Goren,M.G., Burstein,D., Pupko,T. and Qimron,U. (2013) DNA motifs determining the efficiency of adaptation into the Escherichia coli CRISPR array. Proc. Natl. Acad. Sci. U.S.A., 110, 14396-14401.
19. Cady,K.C., Bondy-Denomy,J., Heussler,G.E., Davidson,A.R. and O'Toole,G.A. (2012) The CRISPR/Cas adaptive immune system of Pseudomonas aeruginosa mediates resistance to naturally occurring and engineered phages. J. Bacteriol., 194, 5728-5738.
20. Erdmann,S. and Garrett,R.A. (2012) Selective and hyperactive uptake of foreign DNA by adaptive immune systems of an archaeon via two distinct mechanisms. Mol. Microbiol., 85, 1044-1056.
21. Erdmann,S., Le Moine Bauer,S. and Garrett,R.A. (2014) Inter-viral conflicts that exploit host CRISPR immune systems of Sulfolobus. Mol. Microbiol., 91, 900-917.
22. Li,M., Wang,R., Zhao,D. and Xiang,H. (2014) Adaptation of the Haloarcula hispanica CRISPR-Cas system to a purified virus strictly requires a priming process. Nucleic Acids Res., 42, 2483-2492.
23. Li,M., Wang,R. and Xiang,H. (2014) Haloarcula hispanica CRISPR authenticates PAM of a target sequence to prime discriminative adaptation. Nucleic Acids Res., 42, 7226-7235.
24. Richter,C., Dy,R.L., McKenzie,R.E., Watson,B.N., Taylor,C., Chang,J.T., McNeil,M.B., Staals,R.H. and Fineran,P.C. (2014) Priming in the Type I-F CRISPR-Cas system triggers strand-independent spacer acquisition, bi-directionally from the primed protospacer. Nucleic Acids Res. 42, 8516-8526.
25. Datsenko,K.A., Pougach,K., Tikhonov,A., Wanner,B.L., Severinov,K. and Semenova,E. (2012) Molecular memory of prior infections activates the CRISPR/Cas adaptive bacterial immunity system. Nat. Commun., 3, 945.
26. Arslan,Z., Hermanns,V., Wurm,R., Wagner,R. and Pul,U. (2014) Detection and characterization of spacer integration intermediates in type I-E CRISPR-Cas system. Nucleic Acids Res., 42, 7884-7893.
27. Richter,C., Dy,R.L., McKenzie,R.E., Watson,B.N., Taylor,C., Chang,J.T., McNeil,M.B., Staals,R.H. and Fineran,P.C. (2014) Priming in the Type I-F CRISPR-Cas system triggers strand-independent spacer acquisition, bi-directionally from the primed protospacer. Nucleic Acids Res., 42, 8516-8526.
28. Diez-Villasenor,C., Guzman,N.M., Almendros,C., Garcia-Martinez,J. and Mojica,F.J. (2013) CRISPR-spacer integration reporter plasmids reveal distinct genuine acquisition specificities among CRISPR-Cas I-E variants of Escherichia coli. RNA Biol., 10, 792-802.
29. Fineran,P.C., Gerritzen,M.J., Suarez-Diez,M., Kunne,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.
30. Hynes,A.P., Villion,M. and Moineau,S. (2014) Adaptation in bacterial CRISPR-Cas immunity can be driven by defective phages. Nat. Commun., 5, 4399.
31. Heler,R., Marraffini,L.A. and Bikard,D. (2014) Adapting to new threats: the generation of memory by CRISPR-Cas immune systems. Mol. Microbiol., 93, 1-9.
32. Deng,L., Kenchappa,C.S., Peng,X., She,Q. and Garrett,R.A. (2012) Modulation of CRISPR locus transcription by the repeat-binding protein Cbp1 in Sulfolobus. Nucleic Acids Res., 40, 2470-2480.
33. Shinkai,A., Kira,S., Nakagawa,N., Kashihara,A., Kuramitsu,S. and Yokoyama,S. (2007) Transcription activation mediated by a cyclic AMP receptor protein from Thermus thermophilus HB8. J. Bacteriol., 189, 3891-3901.
34. 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.
35. 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.
36. Medina-Aparicio,L., Rebollar-Flores,J.E., Gallego-Hernandez,A.L., Vazquez,A., Olvera,L., Gutierrez-Rios,R.M., Calva,E. and Hernandez-Lucas,I. (2011) The CRISPR/Cas immune system is an operon regulated by LeuO, H-NS, and leucine-responsive regulatory protein in Salmonella enterica serovar Typhi. J. Bacteriol., 193, 2396-2407.
37. Deng,L., Garrett,R.A., Shah,S.A., Peng,X. and She,Q. (2013) A novel interference mechanism by a type IIIB CRISPR-Cmr module in Sulfolobus. Mol. Microbiol., 87, 1088-1099.
38. Peng,W., Li,H., Hallstrom,S., Peng,N., Liang,Y.X. and She,Q. (2013) Genetic determinants of PAM-dependent DNA targeting and pre-crRNA processing in Sulfolobus islandicus. RNA Biol., 10, 738-748.
39. Gudbergsdottir,S., Deng,L., Chen,Z., Jensen,J.V., Jensen,L.R., She,Q. and Garrett,R.A. (2011) 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, 35-49.
40. Deng,L., Zhu,H., Chen,Z., Liang,Y.X. and She,Q. (2009) Unmarked gene deletion and host-vector system for the hyperthermophilic crenarchaeon Sulfolobus islandicus. Extremophiles, 13, 735-746.
41. Peng,N., Deng,L., Mei,Y., Jiang,D., Hu,Y., Awayez,M., Liang,Y. and She,Q. (2012) A synthetic arabinose-inducible promoter confers high levels of recombinant protein expression in hyperthermophilic archaeon Sulfolobus islandicus. Appl. Environ. Microbiol., 78, 5630-5637.
42. Abella,M., Rodriguez,S., Paytubi,S., Campoy,S., White,M.F. and Barbe,J. (2007) The Sulfolobus solfataricus radA paralogue sso0777 is DNA damage inducible and positively regulated by the Sta1 protein. Nucleic Acids Res., 35, 6788-6797.
43. Samson,R.Y., Xu,Y., Gadelha,C., Stone,T.A., Faqiri,J.N., Li,D., Qin,N., Pu,F., Liang,Y.X., She,Q. et al. (2013) Specificity and function of archaeal DNA replication initiator proteins. Cell Rep., 3, 485-496.
44. Zhang,C., Guo,L., Deng,L., Wu,Y., Liang,Y., Huang,L. and She,Q. (2010) Revealing the essentiality of multiple archaeal pcna genes using a mutant propagation assay based on an improved knockout method. Microbiology, 156, 3386-3397.
45. Ao,X., Li,Y., Wang,F., Feng,M., Lin,Y., Zhao,S., Liang,Y. and Peng,N. (2013) The Sulfolobus initiator element is an important contributor to promoter strength. J. Bacteriol., 195, 5216-5222.
46. Garrett,R.A., Vestergaard,G. and Shah,S.A. (2011) Archaeal CRISPR-based immune systems: exchangeable functional modules. Trends Microbiol., 19, 549-556.
47. Manica,A., Zebec,Z., Teichmann,D. and Schleper,C. (2011) In vivo activity of CRISPR-mediated virus defence in a hyperthermophilic archaeon. Mol. Microbiol., 80, 481-491.
48. Quax,T.E., Voet,M., Sismeiro,O., Dillies,M.A., Jagla,B., Coppee,J.Y., Sezonov,G., Forterre,P., van der Oost,J., Lavigne,R. et al. (2013) Massive activation of archaeal defense genes during viral infection. J. Virol., 87, 8419-8428.
49. Lintner,N.G., Frankel,K.A., Tsutakawa,S.E., Alsbury,D.L., Copie,V., Young,M.J., Tainer,J.A. and Lawrence,C.M. (2011) The structure of the CRISPR-associated protein Csa3 provides insight into the regulation of the CRISPR/Cas system. J. Mol. Biol., 405, 939-955.
50. Peng,N., Xia,Q., Chen,Z., Liang,Y.X. and She,Q. (2009) An upstream activation element exerting differential transcriptional activation on an archaeal promoter. Mol. Microbiol., 74, 928-939.
51. Shah,S.A., Erdmann,S., Mojica,F.J. and Garrett,R.A. (2013) Protospacer recognition motifs: mixed identities and functional diversity. RNA Biol., 10, 891-899.