Increasing cleavage specificity and activity of restriction endonuclease KpnI

Nucleic Acids Research

Volumn 41, Issue 21, 2013, Pages 9812-9824

  Vasu, Kommireddy ^a   Nagamalleswari, Easa ^a   Zahran, Mai ^b   Imhof, Petra ^c   Xu, Shuang Yong ^d   Zhu, Zhenyu ^d   Chan, Siu Hong ^d   Nagaraja, Valakunja ^a,e  

^a INDIAN INSTITUTE OF SCIENCE   (India)

^b NEW YORK UNIVERSITY   (United States)

^c FREIE UNIVERSITÄT BERLIN   (Germany)

^d NEW ENGLAND BIOLABS   (United States)

^e JAWAHARLAL NEHRU CENTRE FOR ADVANCED SCIENTIFIC RESEARCH   (India)

Author keywords

[No Author keywords available]

Indexed keywords

ASPARTIC ACID; CALCIUM; GLUTAMIC ACID; MAGNESIUM; METAL ION; PROTEIN KPNI; RESTRICTION ENDONUCLEASE; UNCLASSIFIED DRUG;

AMINO ACID SUBSTITUTION; ARTICLE; BINDING SITE; CHEMICAL ANALYSIS; CONTROLLED STUDY; DNA CLEAVAGE; ENZYME ACTIVE SITE; ENZYME ACTIVITY; ENZYME BINDING; ENZYME KINETICS; ENZYME MECHANISM; ENZYME METABOLISM; ENZYME SPECIFICITY; ESCHERICHIA COLI; GENE MUTATION; MOLECULAR DYNAMICS; NONHUMAN; PRIORITY JOURNAL; PROTEIN CLEAVAGE; STRUCTURE ANALYSIS; TURNOVER TIME;

CALCIUM; CATALYTIC DOMAIN; DEOXYRIBONUCLEASES, TYPE II SITE-SPECIFIC; DNA CLEAVAGE; MAGNESIUM; MOLECULAR DYNAMICS SIMULATION; MUTATION; SUBSTRATE SPECIFICITY;

EID: 84890058227     PISSN: 03051048     EISSN: 13624962     Source Type: Journal    
DOI: 10.1093/nar/gkt734     Document Type: Article

References (41)

1. Pingoud, A., Fuxreiter, M., Pingoud, V. and Wende, W. (2005) Type II restriction endonucleases: structure and mechanism. Cell. Mol. Life Sci., 62, 685-707.
2. Aravind, L., Makarova, K.S. and Koonin, E.V. (2000) Survey and summary: holliday junction resolvases and related nucleases: identification of new families, phyletic distribution and evolutionary trajectories. Nucleic Acids Res., 28, 3417-3432.
3. 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.
4. Saravanan, M., Bujnicki, J.M., Cymerman, I.A., Rao, D.N. and Nagaraja, V. (2004) Type II restriction endonuclease R.KpnI is a member of the HNH nuclease superfamily. Nucleic Acids Res., 32, 6129-6135.
5. Miyazono, K.I., Watanabe, M., Kosinski, J., Ishikawa, K., Kamo, M., Sawasaki, T., Nagata, K., Bujnicki, J.M., Endo, Y., Tanokura, M. et al. (2007) Novel protein fold discovered in the PabI family of restriction enzymes. Nucleic Acids Res., 35, 1908-1918.
6. Bujnicki, J.M., Radlinska, M. and Rychlewski, L. (2001) Polyphyletic evolution of type II restriction enzymes revisited: two independent sources of second-hand folds revealed. Trends Biochem. Sci., 26, 9-11.
7. Orlowski, J. and Bujnicki, J.M. (2008) Structural and evolutionary classification of Type II restriction enzymes based on theoretical and experimental analyses. Nucleic Acids Res., 36, 3552-3569.
8. Pommer, A.J., Cal, S., Keeble, A.H., Walker, D., Evans, S.J., Kühlmann, U.C., Cooper, A., Connolly, B.A., Hemmings, A.M., Moore, G.R. et al. (2001) Mechanism and cleavage specificity of the H-N-H endonuclease colicin E9. J. Mol. Biol., 314, 735-749.
9. Biertümpfel, C., Yang, W. and Suck, D. (2007) Crystal structure of T4 endonuclease VII resolving a Holliday junction. Nature, 449, 616-620.
10. Keeble, A.H., Hemmings, A.M., James, R., Moore, G.R. and Kleanthous, C. (2002) Multistep binding of transition metals to the H-N-H endonuclease toxin colicin E9. Biochemistry, 41, 10234-10244.
11. Pommer, A.J., Kühlmann, U.C., Cooper, A., Hemmings, A.M., Moore, G.R., James, R. and Kleanthous, C. (1999) Homing in on the role of transition metals in the HNH motif of colicin endonucleases. J. Biol. Chem., 274, 27153-27160.
12. Yang, W. (2008) An equivalent metal ion in one-and two-metalion catalysis. Nat. Struct. Mol. Biol., 15, 1228-1231.
13. Wittmayer, P.K. and Raines, R.T. (1996) Substrate binding and turnover by the highly specific I-PpoI endonuclease. Biochemistry, 35, 1076-1083.
14. Ku, W.Y., Liu, Y.W., Hsu, Y.C., Liao, C.-C., Liang, P.-H., Yuan, H.S. and Chak, K.-F. (2002) The zinc ion in the HNH motif of the endonuclease domain of colicin E7 is not required for DNA binding but is essential for DNA hydrolysis. Nucleic Acids Res., 30, 1670-1678.
15. Galburt, E.A., Chevalier, B., Tang, W., Jurica, M.S., Flick, K.E., Monnat, R.J. and Stoddard, B.L. (1999) A novel endonuclease mechanism directly visualized for I-PpoI. Nat. Struct. Biol., 6, 1096-1099.
16. Drouin, M., Lucas, P., Otis, C., Lemieux, C. and Turmel, M. (2000) Biochemical characterization of I-CmoeI reveals that this H-N-H homing endonuclease shares functional similarities with H-N-H colicins. Nucleic Acids Res., 28, 4566-4572.
17. Chan, S.-H., Opitz, L., Higgins, L., O'loane, D. and Xu, S.-Y. (2010) Cofactor requirement of HpyAV restriction endonuclease. PLoS One, 5, e9071.
18. Kriukiene, E. (2006) Domain organization and metal ion requirement of the Type IIS restriction endonuclease MnlI. FEBS Lett., 580, 6115-6122.
19. Vasu, K., Saravanan, M. and Nagaraja, V. (2011) Endonuclease Active Site Plasticity Allows DNA Cleavage with Diverse Alkaline Earth and Transition Metal Ions. ACS Chem. Biol., 6, 934-942.
20. Wei, H., Therrien, C., Blanchard, A., Guan, S. and Zhu, Z. (2008) The Fidelity Index provides a systematic quantitation of star activity of DNA restriction endonucleases. Nucleic Acids Res., 36, e50-e50.
21. Chandrashekaran, S., Saravanan, M., Radha, D.R. and Nagaraja, V. (2004) Ca2+-mediated site-specific DNA cleavage and suppression of promiscuous activity of KpnI restriction endonuclease. J. Biol. Chem., 279, 49736-49740.
22. 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, E1287-93.
23. Khersonsky, O. and Tawfik, D.S. (2010) Enzyme promiscuity: a mechanistic and evolutionary perspective. Annu. Rev. Biochem., 79, 471-505.
24. Rockah-Shmuel, L. and Tawfik, D.S. (2012) Evolutionary transitions to new DNA methyltransferases through target site expansion and shrinkage. Nucleic Acids Res., 40, 11627-11637.
25. Vasu, K., Saravanan, M., Rajendra, B.V.R.N. and Nagaraja, V. (2010) Generation of a manganese specific restriction endonuclease with nicking activity. Biochemistry, 49, 8425-8433.
26. Saravanan, M., Vasu, K. and Nagaraja, V. (2008) Evolution of sequence specificity in a restriction endonuclease by a point mutation. Proc. Natl Acad. Sci. USA, 105, 10344-10347.
27. Nagamalleswari, E., Vasu, K. and Nagaraja, V. (2012) Ca 2+binding to the ExDxD motif regulates the DNA cleavage specificity of a promiscuous endonuclease. Biochemistry, 51, 8939-8949.
28. Chiu, J., March, P.E., Lee, R. and Tillett, D. (2004) Site-directed, Ligase-Independent Mutagenesis (SLIM): a single-tube methodology approaching 100% efficiency in 4 h. Nucleic Acids Res., 32, e174-e174.
29. Saravanan, M., Vasu, K., Kanakaraj, R., Rao, D.N. and Nagaraja, V. (2007) R.KpnI, an HNH superfamily REase, exhibits differential discrimination at non-canonical sequences in the presence of Ca2+and Mg2. Nucleic Acids Res., 35, 2777-2786.
30. Jorgensen, W.L., Chandrasekhar, J., Madura, J.D., Impey, R.W. and Klein, M.L. (1983) Comparison of simple potential functions for simulating liquid water. J. Chem. Phys., 79, 926-935.
31. Phillips, J.C., Braun, R., Wang, W., Gumbart, J., Tajkhorshid, E., Villa, E., Chipot, C., Skeel, R.D., Kalé, L. and Schulten, K. (2005) Scalable molecular dynamics with NAMD. J. Comput. Chem., 26, 1781-1802.
32. MacKerell, A.D., Banavali, N. and Foloppe, N. (2001) Development and current status of the CHARMM force field for nucleic acids. Biopolymers, 56, 257-265.
33. Darden, T., York, D. and Pedersen, L. (1993) Particle mesh Ewald: An N log(N) method for Ewald sums in large systems. J. Chem. Phys., 98, 10089-10092.
34. Evans, D.J. and Holian, B.L. (1985) The Nose-Hoover thermostat. J. Chem. Phys., 83, 4069-4074.
35. Yang, W. (2010) Nucleases: diversity of structure, function and mechanism. Quart. Rev. Biophys., 44, 1-93.
36. Etzkorn, C. and Horton, N.C. (2004) Ca2+ binding in the active site of HincII: implications for the catalytic mechanism. Biochemistry, 43, 13256-13270.
37. Babu, C.S., Dudev, T., Casareno, R., Cowan, J.A. and Lim, C. (2003) A combined experimental and theoretical study of divalent metal ion selectivity and function in proteins: application to E. coli ribonuclease H1. J. Am. Chem. Soc., 125, 9318-9328.
38. Tari, L.W., Matte, A., Pugazhenthi, U., Goldie, H. and Delbaere, L.T.J. (1996) Snapshot of an enzyme reaction intermediate in the structure of the ATP-Mg2+-oxalate ternary complex of Escherichia coli PEP carboxykinase. Nat. Struct. Biol., 3, 355-363.
39. Lesser, D., KURPIEWSKI, M. and Jen-Jacobson, L. (1990) The energetic basis of specificity in the Eco RI endonuclease-DNA interaction. Science, 250, 776-786.
40. Vanamee, E.S., Viadiu, H., Chan, S.-H., Ummat, A., Hartline, A.M., Xu, S.-Y. and Aggarwal, A.K. (2011) Asymmetric DNA recognition by the OkrAI endonuclease, an isoschizomer of BamHI. Nucleic Acids Res., 39, 712-719.
41. Lam, S.Y., Yeung, R.C.Y., Yu, T.-H., Sze, K.-H. and Wong, K.-B. (2011) A rigidifying salt-bridge favors the activity of thermophilic enzyme at high temperatures at the expense of low-temperature activity. PLoS Biol., 9, e1001027.