An active immune defense with a minimal CRISPR (clustered regularly interspaced short palindromic repeats) RNA and without the Cas6 protein

Journal of Biological Chemistry

Volumn 290, Issue 7, 2015, Pages 4192-4201

  Maier, Lisa Katharina ^a   Stachler, Aris Edda ^a   Saunders, Sita J ^b   Backofen, Rolf ^b   Marchfelder, Anita ^a  

^a UNIVERSITY OF ULM   (Germany)

^b UNIVERSITY OF FREIBURG   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

BIOCHEMISTRY; BIOLOGY;

IMMUNE DEFENSE; PALINDROMIC;

NUCLEIC ACIDS;

BACTERIAL PROTEIN; BACTERIAL RNA; CAS6B PROTEIN; UNCLASSIFIED DRUG; ARCHAEAL PROTEIN; ARCHAEAL RNA;

ARTICLE; BACTERIAL IMMUNITY; BACTERIAL STRAIN; CLUSTERED REGULARLY INTERSPACED SHORT PALINDROMIC REPEAT; CONTROLLED STUDY; DOWN REGULATION; HALOFERAX VOLCANII; MOLECULAR INTERACTION; MUTATION; NONHUMAN; PLASMID; PROTEIN DEGRADATION; PROTEIN EXPRESSION; PROTEIN FUNCTION; RNA ANALYSIS; RNA INTERFERENCE; RNA SEQUENCE; UPREGULATION; CRISPR CAS SYSTEM; GENE EXPRESSION REGULATION; GENETIC ENGINEERING; GENETICS; HIGH THROUGHPUT SEQUENCING; IMMUNOLOGY; NORTHERN BLOTTING;

ARCHAEAL PROTEINS; BLOTTING, NORTHERN; CLUSTERED REGULARLY INTERSPACED SHORT PALINDROMIC REPEATS; CRISPR-CAS SYSTEMS; GENE EXPRESSION REGULATION, ARCHAEAL; GENETIC ENGINEERING; HALOFERAX VOLCANII; HIGH-THROUGHPUT NUCLEOTIDE SEQUENCING; PLASMIDS; RNA INTERFERENCE; RNA, ARCHAEAL;

EID: 84922767032     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M114.617506     Document Type: Article

References (56)

1. 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
2. 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
3. Barrangou, R., and Marraffini, L. A. (2014) CRISPR-Cas systems: prokaryotes upgrade to adaptive immunity. Mol. Cell 54, 234-244
4. Terns, M. P., and Terns, R. M. (2011) CRISPR-based adaptive immune systems. Curr. Opin. Microbiol. 14, 321-327
5. 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
6. Bikard, D., and Marraffini, L. A. (2013) Control of gene expression by CRISPR-Cas systems. 1000Prime 10.12703/P5-47
7. 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
8. Mojica, F. J., Díez-Villaseñor, C., García-Martínez, J., and Almendros, C. (2009) Short motif sequences determine the targets of the prokaryotic CRISPR defence system. Microbiology 155, 733-740
9. Charpentier, E., van der Oost, J., and White, M. F. (2013) in CRISPR-Cas Systems (Barrangou, R., and van der Oost, J., eds) pp. 115-144, Springer- Verlag, Berlin
10. 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
11. Vestergaard, G., Garrett, R. A., and Shah, S. A. (2014) CRISPR adaptive immune systems of Archaea. RNA Biol. 11, 156-167
12. Reeks, J., Naismith, J. H., and White, M. F. (2013) CRISPR interference: a structural perspective. Biochem. J. 453, 155-166
13. 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
14. 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
15. 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
16. 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
17. 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
18. Wiedenheft, B., van Duijn, E., Bultema, J. B., Bultema, J., Waghmare, S. P., Waghmare, S., Zhou, K., Barendregt, A., Westphal, W., Heck, A. J., Heck, A., Boekema, E. J., Boekema, E., Dickman, M. J., Dickman, M., 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
19. Künne, T., Swarts, D. C., and Brouns, S. J. (2014) Planting the seed: target recognition of short guide RNAs. Trends Microbiol. 22, 74-83
20. 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
21. 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
22. Brendel, J., Stoll, B., Lange, S. J., Sharma, K., Lenz, C., Stachler, A. E., Maier, L. K., Richter, H., Nickel, L., Schmitz, R. A., Randau, L., Allers, T., Urlaub, H., Backofen, R., and Marchfelder, A. (2014) A complex of Cas proteins 5, 6, and 7 is required for the biogenesis and stability of crRNAs in Haloferax volcanii. J. Biol. Chem. 289, 7164-7177
23. Hartmann, R. K., Gössringer, M., Späth, B., Fischer, S., and Marchfelder, A. (2009) The making of tRNAs and more-RNase P and tRNase Z. Prog. Mol. Biol. Transl. Sci. 85, 319-368
24. 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
25. Miller, J. H. (1972) Experiments in Molecular Genetics, Cold Spring Harbour Laboratory Press, Cold Spring Harbor, NY
26. Delmas, S., Shunburne, L., Ngo, H. P., and Allers, T. (2009) Mre11-Rad50 promotes rapid repair of DNA damage in the polyploid archaeon Haloferax volcanii by restraining homologous recombination. PLoS Genet. 5, e1000552
27. 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
28. 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
29. 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
30. Stoll, B. (2013) Biology II, Ulm University, Ulm, Germany
31. Norais, C., Hawkins, M., Hartman, A. L., Eisen, J. A., Myllykallio, H., and Allers, T. (2007) Genetic and physical mapping ofDNAreplication origins in Haloferax volcanii. PLoS Genet. 3, e77
32. 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
33. Cock, P. J., Fields, C. J., Goto, N., Heuer, M. L., and Rice, P. M. (2010) The Sanger FASTQ file format for sequences with quality scores, and the Solexa/ Illumina FASTQ variants. Nucleic Acids Res. 38, 1767-1771
34. Hoffmann, S., Otto, C., Kurtz, S., Sharma, C. M., Khaitovich, P., Vogel, J., Stadler, P. F., and Hackermüller, J. (2009) Fast mapping of short sequences with mismatches, insertions and deletions using index structures. PLoS Comput. Biol. 5, e1000502
35. Robinson, J. T., Thorvaldsdóttir, H., Winckler, W., Guttman, M., Lander, E. S., Getz, G., and Mesirov, J. P. (2011) Integrative genomics viewer. Nat. Biotechnol. 29, 24-26
36. Hölzle, A., Fischer, S., Heyer, R., Schütz, S., Zacharias, M., Walther, P., Allers, T., and Marchfelder, A. (2008) Maturation of the 5S rRNA 5' end is catalyzed in vitro by the endonuclease tRNase Z in the archaeon H. volcanii. RNA 14, 928-937
37. Hölzle, A., Stoll, B., Schnattinger, T., Schöning, U., Tjaden, B., and Marchfelder, A. (2012) tRNA-like elements in Haloferax volcanii. Biochimie 94, 940-946
38. Gopalan, V., Vioque, A., and Altman, S. (2002) RNase P: variations and uses. J. Biol. Chem. 277, 6759-6762
39. Schierling, K., Rösch, S., Rupprecht, R., Schiffer, S., and Marchfelder, A. (2002) tRNA 3' end maturation in archaea has eukaryotic features: the RNase Z from Haloferax volcanii. J. Mol. Biol. 316, 895-902
40. 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
41. 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
42. 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
43. Mulepati, S., Héroux, A., and Bailey, S. (2014) Crystal structure of a CRISPR RNA-guided surveillance complex bound to a ssDNA target. Science 345, 1479-1484
44. 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
45. 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
46. 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
47. 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
48. Goren, M. G., Yosef, I., Auster, O., and Qimron, U. (2012) Experimental definition of a clustered regularly interspaced short palindromic duplicon in Escherichia coli. J. Mol. Biol. 423, 14-16
49. 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
50. Sinkunas, T., Gasiunas, G., Waghmare, S. P., Dickman, M. J., Barrangou, R., Horvath, P., and Siksnys, V. (2013) In vitro reconstitution of Cascademediated CRISPR immunity in Streptococcus thermophilus. EMBO J. 32, 385-394
51. Dupuis, M. E., and Moineau, S. (2013) in CRISPR-Cas Systems (Barrangou, R., and van der Oost, J., eds) pp. 171-200, Springer-Verlag, Berlin
52. Almendros, C., Guzmán, N. M., Díez-Villaseñor, C., García-Martínez, J., and Mojica, F. J. (2012) Target motifs affecting natural immunity by a constitutive CRISPR-Cas system in Escherichia coli. PLoS One 7, e50797
53. 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
54. 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
55. 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
56. 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