Concerted action at eight phosphodiester bonds by the BcgI restriction endonuclease

Nucleic Acids Research

Volumn 39, Issue 17, 2011, Pages 7630-7640

  Marshall, Jacqueline J T ^a   Smith, Rachel M ^a   Ganguly, Sumita ^a   Halford, Stephen E ^a  

^a UNIVERSITY OF BRISTOL   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

DOUBLE STRANDED DNA; PROTEIN BCGL; TYPE II SITE SPECIFIC DEOXYRIBONUCLEASE; UNCLASSIFIED DRUG;

ARTICLE; BIOACCUMULATION; CHEMICAL BOND; CONTROLLED STUDY; DNA CLEAVAGE; DNA SEQUENCE; DNA STRAND BREAKAGE; ENZYME ACTIVITY; GENE DOSAGE; MOLECULAR RECOGNITION; NONHUMAN; NUCLEOTIDE BINDING SITE; PHOSPHODIESTER BOND; PRIORITY JOURNAL; PROTEIN DNA BINDING; PROTEIN DNA INTERACTION;

DEOXYRIBONUCLEASES, TYPE II SITE-SPECIFIC; DNA; DNA BREAKS, DOUBLE-STRANDED; DNA CLEAVAGE;

EID: 80053195544     PISSN: 03051048     EISSN: 13624962     Source Type: Journal    
DOI: 10.1093/nar/gkr453     Document Type: Article

References (55)

1. Wilson, G.G. and Murray, N.E. (1991) Restriction and modification systems. Annu. Rev. Genet., 25, 585-627. (Pubitemid 21903734)
2. Roberts, R.J., Belfort, M., Bestor, T., Bhagwat, A.S., Bickle, T.A., Bitinaite, J., Blumenthal, R.M., Degtyarev, S.K., 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. (Pubitemid 36437486)
3. 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.
4. Dryden, D.T., Murray, N.E. and Rao, D.N. (2001) Nucleoside triphosphate-dependent restriction enzymes. Nucleic Acids Res., 29, 3728-3741. (Pubitemid 32910515)
5. Bourniquel, A.A. and Bickle, T.A. (2002) Complex restriction enzymes: NTP-driven molecular motors. Biochimie, 84, 1047-1059. (Pubitemid 36253730)
6. Roberts, R.J. and Halford, S.E. (1993) Type II restriction endonucleases. In Linn, S.M., Lloyd, R.S. and Roberts, R.J. (eds), Nucleases. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NY, pp. 35-88.
7. Aggarwal, A.K. (1995) Structure and function of restriction endonucleases. Curr. Opin. Struct. Biol., 5, 11-19.
8. Perona, J.J. (2002) Type II restriction endonucleases. Methods, 28, 353-364. (Pubitemid 35373848)
9. Cheng, X. and Roberts, R.J. (2001) AdoMet-dependent methylation, DNA methyltransferases and base flipping. Nucleic Acids Res., 29, 3784-3795. (Pubitemid 32910519)
10. Kong, H., Roemer, S.E., Waite-Rees, P.A., Benner, J.S., Wilson, G.G. and Nwankwo, D.O. (1994) Characterization of BcgI, a new kind of restriction-modification system. J. Biol. Chem., 269, 683-690. (Pubitemid 24026713)
11. Kong, H. (1998) Analyzing the functional organization of a novel restriction modification system, the BcgI system. J. Mol. Biol., 279, 823-832. (Pubitemid 28284697)
12. Janulaitis, A., Petrusyte, M., Maneliene, Z., Klimasauskas, S. and Butkus, V. (1992) Purification and properties of the Eco57I restriction endonuclease and methylase-prototypes of a new class. Nucleic Acids Res., 20, 6043-6049.
13. Piekarowicz, A., Golaszewska, M., Sunday, A.O., Siwinska, M. and Stein, D.C. (1999) The HaeIV restriction modification system of Haemophilus aegyptius is encoded by a single polypeptide. J. Mol. Biol., 293, 1055-1065.
14. Cesnaviciene, E.E., Petrusyte, M.M., Kazlauskiene, R.R., Maneliene, Z., Timinskas, A., Lubys, A. and Janulaitis, A. (2001) Characterization of AloI, a restriction-modification System of a new type. J. Mol. Biol., 314, 205-216. (Pubitemid 33105087)
15. Morgan, R.D., Bhatia, T.K., Lovasco, L. and Davis, T.B. (2008) MmeI: a minimal Type II restriction-modification system that only modifies one DNA strand for host protection. Nucleic Acids Res., 36, 6558-6570.
16. 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.
17. Aggarwal, A.K. and Wah, D.A. (1998) Novel site-specific DNA endonucleases. Curr. Opin. Struct. Biol., 8, 19-25. (Pubitemid 28107911)
18. Bath, A.J., Milsom, S.E., Gormley, N.A. and Halford, S.E. (2002) Many type IIs restriction endonucleases interact with two recognition sites before cleaving DNA. J. Biol. Chem., 277, 4024-4033. (Pubitemid 34968658)
19. Chan, S.H., Stoddard, B.L. and Xu, S.Y. (2011) Natural and engineered nicking endonucleases-from cleavage mechanism to engineering of strand-specificity. Nucleic Acids Res., 39, 1-18.
20. Marshall, J.J.T. and Halford, S.E. (2010) The Type IIB restriction endonucleases. Biochem. Soc. Trans., 38, 410-416.
21. Vitkute, J., Maneliene, Z., Petrusyte, M. and Janulaitis, A. (1997) BplI, a new BcgI-like restriction endonuclease, which recognizes a symmetric sequence. Nucleic Acids Res., 25, 4444-4446. (Pubitemid 27500752)
22. Kwiatek, A. and Piekarowicz, A. (2007) The restriction endonuclease R.NmeDI from Neisseria meningitidis that recognizes a palindromic sequence and cuts the DNA on both sides of the recognition sequence. Nucleic Acids Res., 35, 6539-6546. (Pubitemid 350111621)
23. Kong, H., Morgan, R.D., Maunus, R.E. and Schildkraut, I. (1993) A unique restriction endonuclease, BcgI, from Bacillus coagulans. Nucleic Acids Res., 21, 987-991. (Pubitemid 23153008)
24. Kennedy, A.K., Haniford, D.B. and Mizuuchi, K. (2000) Single active site catalysis of the successive phosphoryl transfer steps by DNA transposases: insights from phosphorothioate stereoselectivity. Cell, 101, 295-305.
25. Jinek, M. and Doudna, J.A. (2009) A three-dimensional view of the molecular machinery of RNA interference. Nature, 457, 405-412.
26. Halford, S.E., Welsh, A.J. and Szczelkun, M.D. (2004) Enzyme-mediated DNA-looping. Annu. Rev. Biophys. Biomol. Struct., 33, 1-24.
27. Wentzell, L.M., Nobbs, T.J. and Halford, S.E. (1995) The SfiI restriction endonuclease makes a four-strand DNA break at two copies of its recognition sequence. J. Mol. Biol., 248, 581-595.
28. Mucke, M., Kruger, D.H. and Reuter, M. (2003) Diversity of Type II restriction endonucleases that require two DNA recognition sites. Nucleic Acids Res., 31, 6079-6084. (Pubitemid 37442335)
29. Gowers, D.M., Bellamy, S.R.W. and Halford, S.E. (2004) One recognition sequence, seven restriction enzymes, five reaction mechanisms. Nucleic Acids Res., 32, 3469-3479. (Pubitemid 39117464)
30. Gemmen, G.J., Millin, R. and Smith, D.E. (2006) Tension-dependent DNA cleavage by restriction endonucleases: Two-site enzymes are "switched off" at low force. Proc. Natl Acad. Sci. USA, 103, 11555-11560. (Pubitemid 44182490)
31. Marshall, J.J., Gowers, D.M. and Halford, S.E. (2007) Restriction endonucleases that bridge and excise two recognition sites from DNA. J. Mol. Biol., 367, 419-431. (Pubitemid 46295428)
32. Welsh, A.J., Halford, S.E. and Scott, D.J. (2004) Analysis of type II restriction endonucleases that interact with two recognition sites. In Pingoud, A. (ed.), Nucleic Acids and Molecular Biology, Restriction Endonucleases, Vol. 14. Springer, Berlin, pp. 297-317.
33. Krüger, D.H., Barcak, G.J., Reuter, M. and Smith, H.O. (1988) EcoRII can be activated to cleave refractory DNA recognition sites. Nucleic Acids Res., 16, 3997-4008.
34. Embleton, M.L., Siksnys, V. and Halford, S.E. (2001) DNA cleavage reactions by type II restriction enzymes that require two copies of their recognition sites. J. Mol. Biol., 311, 503-514. (Pubitemid 32816585)
35. Nobbs, T.J., Szczelkun, M.D., Wentzell, L.M. and Halford, S.E. (1998) DNA excision by the SfiI restriction endonuclease. J. Mol. Biol., 281, 419-432. (Pubitemid 28372120)
36. Siksnys, V., Grazulis, S. and Huber, R. (2004) Structure and function of the tetrameric restriction enzymes. In Pingoud, A. (ed.), Nucleic Acids and Molecular Biology, Restriction Endonucleases, Vol. 14. Springer, Berlin, pp. 237-259.
37. Zaremba, M., Sasnauskas, G., Urbanke, C. and Siksnys, V. (2005) Conversion of the tetrameric restriction endonuclease Bse634I into a dimer: Oligomeric structure-stability-function correlations. J. Mol. Biol., 348, 459-478. (Pubitemid 40462109)
38. Zaremba, M., Owsicka, A., Tamulaitis, G., Sasnauskas, G., Shlyakhtenko, L.S., Lushnikov, A.Y., Lyubchenko, Y.L., Laurens, N., van den Broek, B., Wuite, G.J.L. et al. (2010) DNA synapsis through transient tetramerization triggers cleavage by Ecl18kI restriction enzyme. Nucleic Acids Res., 38, 7142-7154.
39. Kong, H. and Smith, C.L. (1997) Substrate DNA and cofactor regulate the activities of a multi-functional restriction-modification enzyme, BcgI. Nucleic Acids Res., 25, 3687-3692. (Pubitemid 27390189)
40. Kong, H. and Smith, C.L. (1998) Does BcgI, a unique restriction endonuclease, require two recognition sites for cleavage? Biol. Chem., 379, 605-609. (Pubitemid 28209944)
41. Jurenaite-Urbanaviciene, S., Serksnaite, J., Kriukiene, E., Giedriene, J., Venclovas, C. and Lubys, A. (2007) Generation of DNA cleavage specificities of type II restriction endonucleases by reassortment of target recognition domains. Proc. Natl Acad. Sci. USA, 104, 10358-10363. (Pubitemid 47185670)
42. Vipond, I.B., Baldwin, G.S., Oram, M., Erskine, S.G., Wentzell, L.M., Szczelkun, M.D., Nobbs, T.J. and Halford, S.E. (1995) A general assay for restriction endonucleases and other DNA-modifying enzymes with plasmid substrates. Mol. Biotechnol., 4, 259-268.
43. Gill, S.C. and von Hippel, P.H. (1989) Calculation of protein extinction coefficients from amino acid sequence data. Anal. Biochem., 182, 319-326. (Pubitemid 19277112)
44. Bellamy, S.R., Milsom, S.E., Kovacheva, Y.S., Sessions, R.B. and Halford, S.E. (2007) A switch in the mechanism of communication between the two DNA-binding sites in the SfiI restriction endonuclease. J. Mol. Biol., 373, 1169-1183. (Pubitemid 47539481)
45. Sanders, K.L., Catto, L.E., Bellamy, S.R.W. and Halford, S.E. (2009) Targeting individual subunits of the FokI restriction endonuclease to specific DNA strands. Nucleic Acids Res., 37, 2105-2115.
46. Sambrook, J. and Russell, D.W. (2001) Molecular Cloning: A Laboratory Manual. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NY.
47. MacRae, I.J. and Doudna, J.A. (2007) Ribonuclease revisited: structural insights into ribonuclease III family enzymes. Curr. Opin. Struct. Biol., 17, 138-145. (Pubitemid 46240810)
48. 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 III. Nature, 471, 602-607.
49. Blaszczyk, J., Tropea, J.E., Bubunenko, M., Routzahn, K.M., Waugh, D.S., Court, D.L. and Ji, X. (2001) Crystallographic and modeling studies of RNase III suggest a mechanism for double-stranded RNA cleavage. Structure, 9, 1225-1236. (Pubitemid 34025056)
50. Sasnauskas, G., Zakrys, L., Zaremba, M., Cosstick, R., Gaynor, J.W., Halford, S.E. and Siksnys, V. (2010) A novel mechanism for the scission of double-stranded DNA: BfiI cuts both 30-50 and 50-30 strands by rotating a single active site. Nucleic Acids Res., 38, 2399-2410.
51. Gormley, N.A., Hillberg, A.L. and Halford, S.E. (2002) The Type IIs restriction endonuclease BspMI is a tetramer that acts concertedly at two copies of an asymmetric DNA sequence. J. Biol. Chem., 277, 4034-4041. (Pubitemid 34968659)
52. Kingston, I.J., Gormley, N.A. and Halford, S.E. (2003) DNA supercoiling enables the Type IIS restriction enzyme BspMI to recognize the relative orientation of two DNA sequences. Nucleic Acids Res., 31, 5221-5228. (Pubitemid 37441889)
53. Bitinaite, J., Wah, D.A., Aggarwal, A.K. and Schildkraut, I. (1998) FokI dimerization is required for DNA cleavage. Proc. Natl Acad. Sci. USA, 95, 10570-10575. (Pubitemid 28413108)
54. Catto, L.E., Ganguly, S., Milsom, S.E., Welsh, A.J. and Halford, S.E. (2006) Protein assembly and DNA looping by the FokI restriction endonuclease. Nucleic Acids Res., 34, 1711-1720.
55. Sears, L.E., Zhou, B., Aliotta, J.M., Morgan, R.D. and Kong, H. (1996) BaeI, another unusual BcgI-like restriction endonuclease. Nucleic Acids Res., 24, 3590-3592. (Pubitemid 26315772)