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

Journal of Biological Chemistry

Volumn 289, Issue 10, 2014, Pages 7164-7177

  Brendel, Jutta ^a   Stoll, Britta ^a   Lange, Sita J ^b   Sharma, Kundan ^c   Lenz, Christof ^c,d   Stachler, Aris Edda ^a   Maier, Lisa Katharina ^a   Richter, Hagen ^e   Nickel, Lisa ^f   Schmitz, Ruth A ^f   Randau, Lennart ^e   Allers, Thorsten ^g   Urlaub, Henning ^c,d   Backofen, Rolf ^b   Marchfelder, Anita ^a  

^a UNIVERSITY OF ULM   (Germany)

^b UNIVERSITY OF FREIBURG   (Germany)

^c MAX PLANCK INSTITUTE FOR BIOPHYSICAL CHEMISTRY   (Germany)

^d UNIVERSITY MEDICAL CENTER GÖTTINGEN   (Germany)

^e MAX PLANCK INSTITUTE FOR TERRESTRIAL MICROBIOLOGY   (Germany)

^f UNIVERSITY OF KIEL   (Germany)

^g UNIVERSITY OF NOTTINGHAM   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

BIOCHEMISTRY; BIOLOGY;

HALOFERAX VOLCANII; PALINDROMIC;

PROTEINS;

CAS5 PROTEIN; CAS6 PROTEIN; CAS7 PROTEIN; CELLULAR APOPTOSIS SUSCEPTIBILITY PROTEIN; CLUSTERED REGULATORY INTERSPACED SHORT PALINDROMIC REPEAT DERIVED RNA; PROTEIN VARIANT; RNA; UNCLASSIFIED DRUG;

ARTICLE; BACTERIAL STRAIN; CAS5 GENE; CAS6 GENE; CAS7 GENE; COMPLEX FORMATION; CONTROLLED STUDY; ESCHERICHIA COLI; GENE CLUSTER; GENE DELETION; HALOFERAX VOLCANII; IN VIVO STUDY; MUTATIONAL ANALYSIS; NONHUMAN; PRIORITY JOURNAL; PROTEIN PROTEIN INTERACTION; RNA CLEAVAGE; RNA STABILITY; RNA SYNTHESIS;

ARCHAEA; CAS6; CRISPR/CAS; CRRNA; HALOFERAX VOLCANII; MICROBIOLOGY; MOLECULAR BIOLOGY; MOLECULAR GENETICS; PROTEIN COMPLEXES; TYPE I-B;

AMINO ACID SEQUENCE; ARCHAEAL PROTEINS; CLUSTERED REGULARLY INTERSPACED SHORT PALINDROMIC REPEATS; HALOFERAX VOLCANII; MOLECULAR SEQUENCE DATA; RNA STABILITY; RNA, ARCHAEAL;

EID: 84896773662     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M113.508184     Document Type: Article

References (66)

1. Al-Attar, S., Westra, E. R., van der Oost, J., and Brouns, S. J. (2011) Clustered regularly interspaced short palindromic repeats (CRISPRs). The hallmark of an ingenious antiviral defense mechanism in prokaryotes. Biol. Chem. 392, 277-289
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. 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
4. Garneau, J. E., Dupuis, M.È., 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
5. Garrett, R. A., Vestergaard, G., and Shah, S. A. (2011) Archaeal CRISPRbased immune systems. Exchangeable functional modules. Trends Microbiol. 19, 549-556
6. Marchfelder, A., Fischer, S., Brendel, J., Stoll, B., Maier, L. K., Jäger, D., Prasse, D., Plagens, A., Schmitz, R. A., and Randau, L. (2012) Small RNAs for defence and regulation in archaea. Extremophiles 16, 685-696
7. 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
8. 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., van der Oost, J., and Koonin, E. V. (2011) Evolution and classification of the CRISPR-Cas systems. Nat. Rev. Microbiol. 9, 467-477
9. Charpentier, E., van der Oost, J., and White, M. F. (2013) crRNA biogenesis. in CRISPR-Cas Systems (Barrangou, R., and van der Oost, J. eds) pp. 115-144, Springer-Verlag, Berlin
10. Carte, J., Pfister, N. T., Compton, M. M., Terns, R. M., and Terns, M. P. (2010) Binding and cleavage of CRISPRRNAby Cas6.RNA16, 2181-2188
11. Carte, J., Wang, R., Li, H., Terns, R. M., and Terns, M. P. (2008) Cas6 is an endoribonuclease that generates guide RNAs for invader defense in prokaryotes. Genes Dev. 22, 3489-3496
12. Li, M., Liu, H., Han, J., Liu, J., Wang, R., Zhao, D., Zhou, J., and Xiang, H. (2013) Characterization of CRISPR RNA biogenesis and Cas6 cleavagemediated inhibition of a provirus in the haloarchaeon Haloferax mediterranei. J. Bacteriol. 195, 867-875
13. Nickel, L., Weidenbach, K., Jäger, D., Backofen, R., Lange, S. J., Heidrich, N., and Schmitz, R. A. (2013) Two CRISPR-Cas systems in Methanosarcina mazei strain Gö1 display common processing features despite belonging to different types I and III. RNA Biol. 10, 779-791
14. Reeks, J., Naismith, J. H., and White, M. F. (2013) CRISPR interference. A structural perspective. Biochem. J. 453, 155-166
15. Reeks, J., Sokolowski, R. D., Graham, S., Liu, H., Naismith, J. H., and White, M. F. (2013) Structure of a dimeric crenarchaeal Cas6 enzyme with an atypical active site for CRISPR RNA processing. Biochem. J. 452, 223-230
16. Richter, H., Zoephel, J., Schermuly, J., Maticzka, D., Backofen, R., and Randau, L. (2012) Characterization of CRISPR RNA processing in Clostridium thermocellum and Methanococcus maripaludis. Nucleic Acids Res. 40, 9887-9896
17. Shao, Y., and Li, H. (2013) Recognition and cleavage of a nonstructured CRISPR RNA by its processing endoribonuclease Cas6. Structure 21, 385-393
18. 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 Comput. Biol. 1, e60
19. Voss, B., Georg, J., Schön, V., Ude, S., and Hess, W. R. (2009) Biocomputational prediction of non-coding RNAs in model cyanobacteria. BMC Genomics 10, 123
20. 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
21. Haurwitz, R. E., Jinek, M., Wiedenheft, B., Zhou, K., and Doudna, J. A. (2010) Sequence-and structure-specific RNA processing by a CRISPR endonuclease. Science 329, 1355-1358
22. Lintner, N. G., Kerou, M., Brumfield, S. K., Graham, S., Liu, H., Naismith, J. H., Sdano, M., Peng, N., She, Q., Copié, V., Young, M. J., White, M. F., and Lawrence, C. M. (2011) Structural and functional characterization of an archaeal clustered regularly interspaced short palindromic repeat (CRISPR)-associated complex for antiviral defense (CASCADE), J. Biol. Chem. 286, 21643-21656
23. Maier, L. K., Lange, S. J., Stoll, B., Haas, K. A., Fischer, S., Fischer, E., Duchardt-Ferner, E., Wöhnert, J., Backofen, R., and Marchfelder, A. (2013) Essential requirements for the detection and degradation of invaders by the Haloferax volcanii CRISPR/Cas system I-B. RNA Biol. 10, 865-874
24. Wiedenheft, B., van Duijn, E., Bultema, J. B., Waghmare, S. P., Zhou, K., Barendregt, A., Westphal, W., Heck, A., Boekema, E. J., Dickman, M. J., and Doudna, J. A. (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
25. 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
26. Sternberg, S. H., Haurwitz, R. E., and Doudna, J. A. (2012) Mechanism of substrate selection by a highly specific CRISPR endoribonuclease. RNA 18, 661-672
27. Gesner, E. M., Schellenberg, M. J., Garside, E. L., George, M. M., and Macmillan, A. M. (2011) Recognition and maturation of effector RNAs in a CRISPR interference pathway. Nat. Struct. Mol. Biol. 18, 688-692
28. Reeks, J., Graham, S., Anderson, L., Liu, H., White, M. F., and Naismith, J. H. (2013) Structure of the archaeal Cascade subunit Csa5. Relating the small subunits of CRISPR effector complexes. RNA Biol. 10, 762-769
29. Juranek, S., Eban, T., Altuvia, Y., Brown, M., Morozov, P., Tuschl, T., and Margalit, H. (2012) A genome-wide view of the expression and processing patterns of Thermus thermophilus HB8 CRISPR RNAs. RNA. 18, 783-794
30. Hatoum-Aslan, A., Maniv, I., and Marraffini, L. A. (2011) 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. U.S.A. 108, 21218-21222
31. 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
32. Wang, R., Preamplume, G., Terns, M. P., Terns, R. M., and Li, H. (2011) Interaction of the Cas6 riboendonuclease with CRISPR RNAs. Recognition and cleavage. Structure 19, 257-264
33. Garside, E. L., Schellenberg, M. J., Gesner, E. M., Bonanno, J. B., Sauder, J. M., Burley, S. K., Almo, S. C., Mehta, G., and MacMillan, A. M. (2012) Cas5d processes pre-crRNA and is a member of a larger family of CRISPR RNA endonucleases. RNA 18, 2020-2028
34. 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. Structure 20, 1574-1584
35. 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
36. Westra, E. R., van Erp, P. B., Künne, T., Wong, S. P., Staals, R. H., Seegers, C. L., Bollen, S., Jore, M. M., Semenova, E., Severinov, K., de Vos, W. M., Dame, R. T., de Vries, R., Brouns, S. J., and van der Oost, J. (2012) CRISPR immunity relies on the consecutive binding and degradation of negatively supercoiled invader DNA by Cascade and Cas3. Mol. Cell. 46, 595-605
37. Kunin, V., Sorek, R., and Hugenholtz, P. (2007) Evolutionary conservation of sequence and secondary structures in CRISPR repeats. Genome Biol. 8, R61
38. Wang, R., Zheng, H., Preamplume, G., Shao, Y., and Li, H. (2012) The impact of CRISPR repeat sequence on structures of a Cas6 protein-RNA complex. Protein Sci. 21, 405-417
39. Lange, S. J., Alkhnbashi, O. S., Rose, D., Will, S., and Backofen, R. (2013) CRISPRmap. An automated classification of repeat conservation in prokaryotic adaptive immune systems. Nucleic Acids Res. 41, 8034-8044
40. Maier, L. K., Fischer, S., Stoll, B., Brendel, J., Pfeiffer, F., Dyall-Smith, M., and Marchfelder, A. (2012) The immune system of halophilic archaea. Mob. Genet. Elements 2, 228-232
41. Maier, L. K., Stoll, B., Brendel, J., Fischer, S., Pfeiffer, F., Dyall-Smith, M., and Marchfelder, A. (2013) The ring of confidence. A haloarchaeal CRISPR/Cas system. Biochem. Soc. Trans. 41, 374-378
42. Fischer, S., Maier, L. K., Stoll, B., Brendel, J., Fischer, E., Pfeiffer, F., Dyall-Smith, M., and Marchfelder, A. (2012) An archaeal immune system can detect multiple protospacer adjacent motifs (PAMs) to target invader DNA. J. Biol. Chem. 287, 33351-33363
43. Allers, T., Barak, S., Liddell, S., Wardell, K., and Mevarech, M. (2010) Improved strains and plasmid vectors for conditional overexpression of His-tagged proteins in Haloferax volcanii. Appl. Environ. Microbiol. 76, 1759-1769
44. Miller, J. H. (1972) Experiments in Molecular Genetics, Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NY
45. Fröls, S., Dyall-Smith, M., and Pfeifer, F. (2012) Biofilm formation by haloarchaea. Environ. Microbiol. 14, 3159-3174
46. Fischer, S., Benz, J., Späth, B., Maier, L.-K., Straub, J., Granzow, M., Raabe, M., Urlaub, H., Hoffmann, J., Brutschy, B., Allers, T., Soppa, J., and Marchfelder, A. (2010) The archaeal Lsm protein binds to small RNAs. J. Biol. Chem. 285, 34429-34438
47. Allers, T., Ngo, H. P., Mevarech, M., and Lloyd, R. G. (2004) Development of additional selectable markers for the halophilic archaeon Haloferax volcanii based on the leuB and trpA genes. Appl. Environ. Microbiol. 70, 943-953
48. Cline, S. W., Schalkwyk, L. C., and Doolittle, W. F. (1989) Transformation of the archaebacterium Halobacterium volcanii with genomic DNA. J. Bacteriol. 171, 4987-4991
49. Nieuwlandt, D. T., Palmer, J. R., Armbruster, D. T., Kuo, Y.-P., Oda, W., and Daniels, C. J. (1995) A rapid procedure for the isolation of RNA from Haloferax volcanii. in Archaea. A Laboratory Manual (Robb, F. T., Place, A. R., Sowers, K. R., Schreier, H. J., DasSarma, S., and Fleischmann, E. M., eds) p. 161, Cold Spring Harbor Press, Cold Spring Harbor, NY
50. Stroud, A., Liddell, S., and Allers, T. (2012) Genetic and biochemical identification of a novel single-stranded DNA-binding complex in Haloferax volcanii. Front. Microbiol. 3, 224
51. Shevchenko, A., Wilm, M., Vorm, O., and Mann, M. (1996) Mass spectrometric sequencing of proteins silver-stained polyacrylamide gels. Anal. Chem. 68, 850-858
52. Pfeiffer, F., Broicher, A., Gillich, T., Klee, K., Mejía, J., Rampp, M., and Oesterhelt, D. (2008) Genome information management and integrated data analysis with HaloLex. Arch. Microbiol. 190, 281-299
53. Cox, J., and Mann, M. (2008) MaxQuant enables high peptide identification rates, individualized p.p.b.-range mass accuracies and proteome-wide protein quantification. Nat. Biotechnol. 26, 1367-1372
54. Kelley, L. A., and Sternberg, M. J. (2009) Protein structure prediction on the Web. A case study using the Phyre server. Nat. Protoc. 4, 363-371
55. 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
56. Needleman, S. B., and Wunsch, C. D. (1970) A general method applicable to the search for similarities in the amino acid sequence of two proteins. J. Mol. Biol. 48, 443-453
57. Schwanhäusser, B., Busse, D., Li, N., Dittmar, G., Schuchhardt, J., Wolf, J., Chen, W., and Selbach, M. (2011) Global quantification of mammalian gene expression control. Nature 473, 337-342
58. 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., Beijer, M. R., Barendregt, A., Zhou, K., Snijders, A. P., Dickman, M. J., Doudna, J. A., Boekema, E. J., Heck, A. J., van der Oost, J., and Brouns, S. J. (2011) Structural basis for CRISPR RNA-guided DNA recognition by Cascade. Nat. Struct. Mol. Biol. 18, 529-536
59. Makarova, K. S., Aravind, L., Wolf, Y. I., and Koonin, E. V. (2011) Unification of Cas protein families and a simple scenario for the origin and evolution of CRISPR-Cas systems. Biol. Direct 6, 38
60. 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
61. Wiedenheft, B., Lander, G. C., Zhou, K., Jore, M. M., Brouns, S. J., van der Oost, J., Doudna, J. A., and Nogales, E. (2011) Structures of the RNAguided surveillance complex from a bacterial immune system. Nature 477, 486-489
62. 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
63. 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., and Heck, A. J. (2012) Native tandem and ion mobility mass spectrometry highlight structural and modular similarities in clustered-regularly-interspaced short-palindromic-repeats (CRISPR)-associated protein complexes from Escherichia coli and Pseudomonas aeruginosa. Mol. Cell Proteomics 11, 1430-1441
64. Wiedenheft, B., Sternberg, S. H., and Doudna, J. A. (2012) RNA-guided genetic silencing systems in bacteria and archaea. Nature 482, 331-338
65. Randau, L. (2012) RNA processing in the minimal organism Nanoarchaeum equitans. Genome Biol. 13, R63
66. Scholz, I., Lange, S. J., Hein, S., Hess, W. R., and Backofen, R. (2013) CRISPR-Cas systems in the cyanobacterium Synechocystis sp. PCC6803 exhibit distinct processing pathways involving at least two Cas6 and a Cmr2 protein. PLoS One 8, e56470