DNA cleavage by CgII and NgoAVII requires interaction between N- and R-proteins and extensive nucleotide hydrolysis

Nucleic Acids Research

Volumn 42, Issue 22, 2014, Pages 13887-13896

  Zaremba, Mindaugas ^a   Toliusis, Paulius ^a   Grigaitis, Rokas ^a   Manakova, Elena ^a   Silanskas, Arunas ^a   Tamulaitiene, Giedre ^a   Szczelkun, Mark D ^b   Siksnys, Virginijus ^a  

^a VILNIUS UNIVERSITY   (Lithuania)

^b UNIVERSITY OF BRISTOL   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

ADENOSINE TRIPHOSPHATASE; ADENOSINE TRIPHOSPHATE; DEAD BOX PROTEIN; DOUBLE STRANDED DNA; HOMODIMER; MONOMER; RESTRICTION ENDONUCLEASE; DNA; NUCLEOTIDE;

ARTICLE; CONTROLLED STUDY; CORYNEBACTERIUM GLUTAMICUM; DNA CLEAVAGE; ENZYME ACTIVITY; ENZYME ANALYSIS; GEL PERMEATION CHROMATOGRAPHY; NEISSERIA GONORRHOEAE; NONHUMAN; PRIORITY JOURNAL; PROTEIN ASSEMBLY; PROTEIN HYDROLYSIS; PROTEIN PROTEIN INTERACTION; STOICHIOMETRY; X RAY CRYSTALLOGRAPHY; CHEMISTRY; ENZYMOLOGY; HYDROLYSIS; ISOLATION AND PURIFICATION; METABOLISM; PROTEIN TERTIARY STRUCTURE;

CORYNEBACTERIUM GLUTAMICUM; NEISSERIA GONORRHOEAE;

ADENOSINE TRIPHOSPHATE; CORYNEBACTERIUM GLUTAMICUM; DEAD-BOX RNA HELICASES; DNA; DNA CLEAVAGE; DNA RESTRICTION ENZYMES; HYDROLYSIS; NEISSERIA GONORRHOEAE; NUCLEOTIDES; PROTEIN STRUCTURE, TERTIARY;

EID: 84927671730     PISSN: 03051048     EISSN: 13624962     Source Type: Journal    
DOI: 10.1093/nar/gku1236     Document Type: Article

References (39)

1. Roberts, R. J., Belfort, M., Bestor, T., Bhagwat, A. S., Bickle, T. A., Bitinaite, J., Blumenthal, R. M., Degtyarev, S., Dryden, D. T. F., Dybvig, K. et al. (2003) A nomenclature for restriction enzymes, DNA methyltransferases, homing endonucleases and their genes. Nucleic Acids Res., 31, 1805-1812.
2. Schafer, A., Kalinowski, J. and Puhler, A. (1994) Increased fertility of Corynebacterium glutamicum recipients in intergeneric matings with Escherichia coli after stress exposure. Appl. Environ. Microbiol., 60, 756-759.
3. Schafer, A., Schwarzer, A., Kalinowski, J. and Puhler, A. (1994) Cloning and characterization of a DNA region encoding a stress-sensitive restriction system from Corynebacterium glutamicum ATCC 13032 and analysis of its role in intergeneric conjugation with Escherichia coli. J. Bacteriol., 176, 7309-7319.
4. Dang, T. N., Zhang, L., Zollner, S., Srinivasan, U., Abbas, K., Marrs, C. F. and Foxman, B. (2013) Uropathogenic Escherichia coli are less likely than paired fecal E. coli to have CRISPR loci. Infect. Genet. Evol., 19, 212-218.
5. Frunzke, J., Bramkamp, M., Schweitzer, J. E. and Bott, M. (2008) Population Heterogeneity in Corynebacterium glutamicum ATCC 13032 caused by prophage CGP3. J. Bacteriol., 190, 5111-5119.
6. Nanda, A. M., Heyer, A., Kramer, C., Grunberger, A., Kohlheyer, D. and Frunzke, J. (2014) Analysis of SOS-induced spontaneous prophage induction in Corynebacterium glutamicum at the single-cell level. J. Bacteriol., 196, 180-188.
7. Xu, S. Y., Nugent, R. L., Kasamkattil, J., Fomenkov, A., Gupta, Y., Aggarwal, A., Wang, X., Li, Z., Zheng, Y. and Morgan, R. (2012) Characterization of type II and III restriction-modification systems from Bacillus cereus strains ATCC 10987 and ATCC 14579. J. Bacteriol., 194, 49-60.
8. Roberts, R. J., Vincze, T., Posfai, J. and Macelis, D. (2010) REBASE-a database for DNA restriction and modification: enzymes, genes and genomes. Nucleic Acids Res., 38, D234-D236.
9. Tamulaitiene, G., Silanskas, A., Grazulis, S., Zaremba, M. and Siksnys, V. (2014) Crystal structure of the R-protein of the multisubunit ATP-dependent restriction endonuclease NgoAVII. Nucleic Acids Res.
10. Grazulis, S., Manakova, E., Roessle, M., Bochtler, M., Tamulaitiene, G., Huber, R. and Siksnys, V. (2005) Structure of the metal-independent restriction enzyme BfiI reveals fusion of a specific DNA-binding domain with a nonspecific nuclease. Proc. Natl. Acad. Sci. U. S. A., 102, 15797-15802.
11. Sasnauskas, G., Halford, S. E. and Siksnys, V. (2003) How the BfiI restriction enzyme uses one active site to cut two DNA strands. Proc. Natl. Acad. Sci. U. S. A., 100, 6410-6415.
12. Sapranauskas, R., Sasnauskas, G., Lagunavicius, A., Vilkaitis, G., Lubys, A. and Siksnys, V. (2000) Novel subtype of type IIs restriction enzymes. BfiI endonuclease exhibits similarities to the EDTA-resistant nuclease Nuc of Salmonella typhimurium. J. Biol. Chem., 275, 30878-30885.
13. Hu, Y., Li, T., Yang, Z., Zhang, B. and Li, Y. (2008) Phage resistance of Corynebacterium crenatum conferred by the restriction and modification system cglI. Sheng Wu Gong Cheng Xue Bao, 24, 760-765.
14. Iyer, L. M., Abhiman, S. and Aravind, L. (2008) MutL homologs in restriction-modification systems and the origin of eukaryotic MORC ATPases. Biol. Direct, 3, 8.
15. Singleton, M. R., Dillingham, M. S. and Wigley, D. B. (2007) Structure and mechanism of helicases and nucleic acid translocases. Annu. Rev. Biochem., 76, 23-50.
16. Stein, D. C., Gunn, J. S., Radlinska, M. and Piekarowicz, A. (1995) Restriction and modification systems of Neisseria gonorrhoeae. Gene, 157, 19-22.
17. Schafer, A., Tauch, A., Droste, N., Puhler, A. and Kalinowski, J. (1997) The Corynebacterium glutamicum cglIM gene encoding a 5-cytosine methyltransferase enzyme confers a specific DNA methylation pattern in an McrBC-deficient Escherichia coli strain. Gene, 203, 95-101.
18. Zheng, L., Baumann, U. and Reymond, J. L. (2004) An efficient one-step site-directed and site-saturation mutagenesis protocol. Nucleic Acids Res., 32, e115.
19. Petoukhov, M. V., Konarev, P. V., Kikhney, A. G. and Svergun, D. (2007) ATSAS 2.1-towards automated and web-supported small-angle scattering data analysis. J. Appl. Crystallogr., 40, s223-s228.
20. Svergun, D. (1992) Determination of the regularization parameter in indirect-transform methods using perceptual criteria. J. Appl. Crystallogr., 25, 495-503.
21. Fischer, H., de Oliveira Neto, M., Napolitano, H. B., Polikarpov, I. and Craievich, A. F. (2010) Determination of the molecular weight of proteins in solution from a single small-angle X-ray scattering measurement on a relative scale. J. Appl. Crystallogr., 43, 101-109.
22. Tamulaitis, G., Mucke, M. and Siksnys, V. (2006) Biochemical and mutational analysis of EcoRII functional domains reveals evolutionary links between restriction enzymes. FEBS Lett., 580, 1665-1671.
23. Peakman, L. J., Antognozzi, M., Bickle, T. A., Janscak, P. and Szczelkun, M. D. (2003) S-adenosyl methionine prevents promiscuous DNA cleavage by the EcoP1I type III restriction enzyme. J. Mol. Biol., 333, 321-335.
24. Cordin, O., Banroques, J., Tanner, N. K. and Linder, P. (2006) The DEAD-box protein family of RNA helicases. Gene, 367, 17-37.
25. Fairman-Williams, M. E., Guenther, U. P. and Jankowsky, E. (2010) SF1 and SF2 helicases: family matters. Curr. Opin. Struct. Biol., 20, 313-324.
26. Szczelkun, M. D. (2013) Roles for helicases as ATP-dependent molecular switches. Adv. Exp. Med. Biol., 767, 225-244.
27. Obarska-Kosinska, A., Taylor, J. E., Callow, P., Orlowski, J., Bujnicki, J. M. and Kneale, G. G. (2008) HsdR subunit of the type I restriction-modification enzyme EcoR124I: biophysical characterisation and structural modelling. J. Mol. Biol., 376, 438-452.
28. Sisakova, E., Stanley, L. K., Weiserova, M. and Szczelkun, M. D. (2008) A RecB-family nuclease motif in the Type I restriction endonuclease EcoR124I. Nucleic Acids Res., 36, 3939-3949.
29. Janscak, P., Sandmeier, U., Szczelkun, M. D. and Bickle, T. A. (2001) Subunit assembly and mode of DNA cleavage of the type III restriction endonucleases EcoP1I and EcoP15I. J. Mol. Biol., 306, 417-431.
30. 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.
31. Seidel, R., Bloom, J. G., Dekker, C. and Szczelkun, M. D. (2008) Motor step size and ATP coupling efficiency of the dsDNA translocase EcoR124I. EMBO J., 27, 1388-1398.
32. Stanley, L. K., Seidel, R., van der Scheer, C., Dekker, N. H., Szczelkun, M. D. and Dekker, C. (2006) When a helicase is not a helicase: dsDNA tracking by the motor protein EcoR124I. EMBO J., 25, 2230-2239.
33. Schwarz, F. W., Toth, J., van Aelst, K., Cui, G., Clausing, S., Szczelkun, M. D. and Seidel, R. (2013) The helicase-like domains of type III restriction enzymes trigger long-range diffusion along DNA. Science, 340, 353-356.
34. Lagunavicius, A., Sasnauskas, G., Halford, S. E. and Siksnys, V. (2003) The metal-independent type IIs restriction enzyme BfiI is a dimer that binds two DNA sites but has only one catalytic centre. J. Mol. Biol., 326, 1051-1064.
35. Golovenko, D., Manakova, E., Zakrys, L., Zaremba, M., Sasnauskas, G., Grazulis, S. and Siksnys, V. (2014) Structural insight into the specificity of the B3 DNA-binding domains provided by the co-crystal structure of the C-terminal fragment of BfiI restriction enzyme. Nucleic Acids Res., 42, 4113-4122.
36. Vitkute, J., Maneliene, Z., Petrusyte, M. and Janulaitis, A. (1998) BfiI, a restriction endonuclease from Bacillus firmus S8120, which recognizes the novel non-palindromic sequence 5'-ACTGGG (N) 5/4-3'. Nucleic Acids Res., 26, 3348-3349.
37. van Aelst, K., Toth, J., Ramanathan, S. P., Schwarz, F. W., Seidel, R. and Szczelkun, M. D. (2010) Type III restriction enzymes cleave DNA by long-range interaction between sites in both head-to-head and tail-to-tail inverted repeat. Proc. Natl. Acad. Sci. U. S. A., 107, 9123-9128.
38. Smith, R. M., Diffin, F. M., Savery, N. J., Josephsen, J. and Szczelkun, M. D. (2009) DNA cleavage and methylation specificity of the single polypeptide restriction-modification enzyme LlaGI. Nucleic Acids Res., 37, 7206-7218.
39. Butterer, A., Pernstich, C., Smith, R. M., Sobott, F., Szczelkun, M. D. and Toth, J. (2014) Type III restriction endonucleases are heterotrimeric: comprising one helicase-nuclease subunit and a dimeric methyltransferase that binds only one specific DNA. Nucleic Acids Res., 42, 5139-5150.