Active site plasticity enables metal-dependent tuning of Cas5d nuclease activity in CRISPR-Cas type I-C system

Nucleic Acids Research

Volumn 42, Issue 6, 2014, Pages 3846-3856

  Punetha, Ankita ^a   Sivathanu, Raveendran ^a   Anand, Baskaran ^a  

^a INDIAN INSTITUTE OF TECHNOLOGY GUWAHATI   (India)

Author keywords

[No Author keywords available]

Indexed keywords

CRISPR ASSOCIATED PROTEIN; DEOXYRIBONUCLEASE; DNA; METAL; PROTEIN CAS5D; PROTEIN CSD1; PROTEIN CSD2; RIBONUCLEASE; RNA; UNCLASSIFIED DRUG;

ARTICLE; CONTROLLED STUDY; CRISPR CAS SYSTEM; ENZYME ACTIVE SITE; ENZYME ACTIVITY; ENZYME SUBSTRATE; HYDROLYSIS; PLASTICITY; PRIORITY JOURNAL; STOICHIOMETRY;

CATALYTIC DOMAIN; CATIONS, DIVALENT; CRISPR-ASSOCIATED PROTEINS; CRISPR-CAS SYSTEMS; ENDODEOXYRIBONUCLEASES; METALS;

EID: 84898952727     PISSN: 03051048     EISSN: 13624962     Source Type: Journal    
DOI: 10.1093/nar/gkt1335     Document Type: Article

References (38)

1. Horvath, P. and Barrangou, R. (2010) CRISPR/Cas, the immune system of bacteria and archaea. Science, 327, 167-170.
2. 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.
3. Wiedenheft, B., Sternberg, S. H. and Doudna, J. A. (2012) RNAguided genetic silencing systems in bacteria and archaea. Nature, 482, 331-338.
4. 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.
5. 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 RNAguided DNA recognition by Cascade. Nat. Struct. Mol. Biol., 18, 529-536.
6. 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.
7. Zhang, J., Rouillon, C., Kerou, M., Reeks, J., Brugger, K., Graham, S., Reimann, J., Cannone, G., Liu, H., Albers, S. V. et al. (2012) Structure and mechanism of the CMR complex for CRISPR-mediated antiviral immunity. Mol. Cell, 45, 303-313.
8. 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.
9. 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.
10. 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.
11. 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.
12. 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.
13. 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.
14. 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.
15. Sashital, D. G., Jinek, M. and Doudna, J. A. (2011) An RNAinduced conformational change required for CRISPR RNA cleavage by the endoribonuclease Cse3. Nat. Struct. Mol. Biol., 18, 680-687.
16. 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.
17. 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.
18. Carte, J., Pfister, N. T., Compton, M. M., Terns, R. M. and Terns, M. P. (2010) Binding and cleavage of CRISPR RNA by Cas6. RNA, 16, 2181-2188.
19. 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.
20. 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.
21. 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.
22. Sinkunas, T., Gasiunas, G., Waghmare, S. P., Dickman, M. J., Barrangou, R., Horvath, P. and Siksnys, V. (2013) In vitro reconstitution of cascade-mediated CRISPR immunity in Streptococcus thermophilus. EMBO J., 32, 385-394.
23. 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 II I. Nature, 471, 602-607.
24. Koo, Y., Ka, D., Kim, E. J., Suh, N. and Bae, E. (2013) Conservation and variability in the structure and function of the Cas5d endoribonuclease in the CRISPR-mediated microbial immune system. J. Mol. Biol., 425, 3799-3810.
25. Pettersen, E. F., Goddard, T. D., Huang, C. C., Couch, G. S., Greenblatt, D. M., Meng, E. C. and Ferrin, T. E. (2004) UCSF Chimera -a visualization system for exploratory research and analysis. J. Comput. Chem., 25, 1605-1612.
26. Jaroszewski, L., Li, Z., Cai, X. H., Weber, C. and Godzik, A. (2011) FFAS server: novel features and applications. Nucleic Acids Res., 39, W38-W44.
27. Cole, C., Barber, J. D. and Barton, G. J. (2008) The Jpred 3 secondary structure prediction server. Nucleic Acids Res., 36, W197-W201.
28. Yang, W., Lee, J. Y. and Nowotny, M. (2006) Making and breaking nucleic acids: two-Mg2+-ion catalysis and substrate specificity. Mol. Cell, 22, 5-13.
29. Maguire, M. E. and Cowan, J. A. (2002) Magnesium chemistry and biochemistry. Biometals, 15, 203-210.
30. Calvin, K. and Li, H. (2008) RNA-splicing endonuclease structure and function. Cell Mol. Life Sci., 65, 1176-1185.
31. Raines, R. T. (1998) Ribonuclease A. Chem. Rev., 98, 1045-1066.
32. Galperin, M. Y. and Koonin, E. V. (2012) Divergence and convergence in enzyme evolution. J. Biol. Chem., 287, 21-28.
33. 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 RNA-guided surveillance complex from a bacterial immune system. Nature, 477, 486-489.
34. 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.
35. Guy, C. P., Majernik, A. I., Chong, J. P. and Bolt, E. L. (2004) A novel nuclease-ATPase (Nar71) from archaea is part of a proposed thermophilic DNA repair system. Nucleic Acids Res., 32, 6176-6186.
36. Vasu, K., Nagamalleswari, E. and Nagaraja, V. (2012) Promiscuous restriction is a cellular defense strategy that confers fitness advantage to bacteria. Proc. Natl Acad. Sci. USA, 109, E1287-E1293.
37. 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.
38. 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.