Advantage of being a dimer for Serratia marcescens endonuclease

Journal of Physical Chemistry B

Volumn 113, Issue 2, 2009, Pages 511-521

  Chen, Chuanying ^a   Krause, Kurt ^b   Pettitt, B Montgomery ^a  

^a University of Houston   (United States)

^b UNIVERSITY OF OTAGO   (New Zealand)

Author keywords

[No Author keywords available]

Indexed keywords

BINDING ENERGY; COORDINATION REACTIONS; DNA; DYNAMICS; ELECTROSTATICS; GENES; MOLECULAR DYNAMICS; NUCLEIC ACIDS;

ACTIVE SITES; AQUEOUS SOLUTIONS; DIMER COMPLEXES; ELECTROSTATIC BINDINGS; ENDONUCLEASE; MOLECULAR-DYNAMICS SIMULATIONS; SERRATIA MARCESCENS; WATER CLUSTERS;

MONOMERS;

EID: 61949215056     PISSN: 15206106     EISSN: None     Source Type: Journal    
DOI: 10.1021/jp8057838     Document Type: Article

References (57)

1. Rangarajan, E. S.; Shankar, V. Sugar non-specific endonucleases. FEMS Microbiol. Rev. 2001, 25, 583-613.
2. Arnone, A.; Bier, C. J.; Cotton, F. A.; Day, V. W.; Hazen, E. E.; Richardson, D. C.; Yonath, A.; Richardson, J. S. A high resolution structure of an inhibitor complex of the extracellular nuclease of Staphylococcus aureus. I. Experimental procedures and chain tracing. J. Biol. Chem. 1971, 246, 2302-2316.
3. Miller, M. D.; Tanner, J.; Alpaugh, M.; Benedik, M. J.; Krause, K. L. 2.1 Angstrom structure of Serratia endonuclease suggests a mechanism for binding to double-stranded DNA. Nat. Struct. Biol. 1994, 1, 461-468.
4. Shlyapnikov, S. V.; Lunin, V. V.; Perbandt, M.; Polyakov, K. M.; Lunin, V. Y.; Levdikov, V. M.; Betzel, C.; Mikhailov, A. M. Atomic structure of the Serratia marcescens endonuclease at 1.1 A resolution and the enzyme reaction mechanism. Acta Crystallogr. 2000, D56, 567-572.
5. Volbeda, A.; Lahm, A.; Sakiyama, F.; Suck, D. Crystal structure of Penicillium citrinum P1 nuclease at 2.8 Angstrom resolution. EMBO J. 1991, 10, 1607-1618.
6. Li, C. L.; Hor, L.-I.; Chang, Z.-F.; Tsai, L.-C.; Yang, W.-Z.; Yuan, H. S. DNA binding and cleavage by the periplasmic nuclease Vvn: a novel structure with a known active site. EMBO J. 2003, 22, 4014-4025.
7. Cheng, Y.-S.; Hsia, K.-C.; Doudeva, L. G.; Chak, K.-F.; Yuan, H. S. The crystal structure of the nuclease domain of ColE7 suggests a mechanism for binding to double-stranded DNA by the H-N-H endonucleases. J. Mol. Biol. 2002, 324, 227-236.
8. Kuhlmann, U. C.; Pommer, A. J.; Moore, G. R.; James, R.; Kleanthous, C.; Hemmings, A. M. Structure of the E9 Dnase domain in comparison with the inhibited structure of the E9 Dnase/lm9 complex. Manuscript to be published.
9. Hsia, K.-C.; Chak, K.-F.; Liang, P.-H.; Cheng, Y.-S.; Ku, W.-Y.; Yuan, H. S. DNA binding and degradation by the HNH endonuclease ColE7. Structure 2004, 12, 205-214.
10. Mate, M. J.; Kleanthous, C. Structure-based analysis of the metal-dependent mechanism of H-N-H endonucleases. J. Biol. Chem. 2004, 279, 34763-34769.
11. Meiss, G.; Friedhoff, P.; Hahn, M.; Gimadutdinow, O.; Pingoud, A. Sequence preferences in cleavage of dsDNA and ssDNA by extracellular Serratia marcescens endonuclease. Biochemistry 1995, 34, 11979-11988.
12. Meiss, G.; Gast, F.-U.; Pingoud, A. M. The DNA/RNA non-specific Serratia nuclease prefers double-stranded A-form nucleic acids as substrates. J. Mol. Biol. 1999, 288, 377-390.
13. Friedhoff, P.; Kolmes, B.; Gimadutdinow, O.; Wende, W.; Krause, K. L.; Pingoud, A. Analysis of the mechanism of the Serratia nuclease using site-directed mutagenesis. Nucleic Acids Res. 1996, 24, 2632-2639.
14. Miller, M. D.; Cai, J.; Krause, K. L. The active site of Serratia endonuclease contains a conserved magnesium-water cluster. J. Mol. Biol. 1999, 288, 975-987.
15. Kuhlmanna, U. C.; Moore, G. R.; James, R.; Kleanthous, C.; Hemmings, A. M. Structural parsimony in endonuclease active sites: should the number of homing endonuclease families be redefined? FEBS Lett. 1999, 463, 1-2.
16. Friedhoff, P.; Franke, I.; Meiss, G.; Wende, W.; Krause, K. L.; Pingoud, A. A similar active site for non-specific and specific endonucleases. Nat. Struct. Biol. 1999, 6, 112-113.
17. Franke, I.; Meiss, G.; Belcher, D.; Gimadutdinow, O.; Urbanke, C.; Pingoud, A. Genetic engineering, production and characterisation of monomeric variants of the dimeric. Serratia marcescens endonuclease. FEBS Lett. 1998, 425, 517-522.
18. Franke, I.; Meiss, G.; Pingoud, A. On the advantage of being a dimer, a case study using the dimeric Serratia nuclease and the monomeric nuclease from Anabaena sp. Strain PCC 7120. J. Biol. Chem. 1999, 274, 825-832.
19. Chen, C.; Beck, B. W.; Krause, K. L.; Pettitt, B. M. Solvent participation in Serratia marcescens endonuclease complexes. Proteins: Struct. Funct., Bioinf. 2006, 62, 982-995.
20. Chen, C.; Beck, B. W.; Krause, K. L.; Pettitt, B. M. The effects of dimerization of Serratia marcescens endonuclease on water dynamics. Biopolymers 2007, 85, 241-252.
21. Jen-Jacobson, L. Protein-DNA recognition complexes: conservation of structure and binding energy in the transition state. Biopolymers 1997, 44, 153-180.
22. Oda, M.; Nakamura, H. Thermodynamic and kinetic analyses for understanding sequence-specific DNA recognition. Genes Cells 2000, 5, 319-326.
23. Brooks, B. R.; Bruccoleri, R. E.; Olafson, B. D.; States, D. J.; Swanminathan, S.; Karplus, M. CHARMM: a program for macromolecular energy, minimization, and dynamics calculations. J. Comput. Chem. 1983, 4, 187-217.
24. Smith, P. E.; Holder, M. E.; Dang, L. X.; Feig, M.; Pettitt, B. M. ESP; University of Houston: Houston, TX, 1996.
25. MacKerell, A. D.; Bashford, D.; Bellott, R. L.; Dunbrack, R. L.; Evanseck, J.; Field, M. J.; Fischer, S.; Gao, J.; Guo, H.; Ha, S.; Joseph, D.; Kuchnir, L.; Kuczera, K.; Lau, F. T. K.; Mattos, C.; Michnik, S.; Ngo, T.; Nguyen, D. T.; Prodhom, B.; Reiher, W. E., III; Roux, B.; Schlenkrich, M.; Smith, J.; Stote, R.; Straub, J.; Watanabe, M.; Wiorkiewicz-Kuczera, J.; Yin, D.; Karplus, M. All-atom empirical potential for molecular modeling and dynamics studies of proteins. J. Phys. Chem. B 1998, 102, 3586-3616.
26. Foloppe, N.; Mackerell, A. D. All-atom empirical force field for nucleic acids: I. Parameter optimization based on small molecule and condensed phase macromolecular target data. J. Comput. Chem. 2002, 21, 86-104.
27. de Leeuw, S. W.; Perram, J. W.; Smith, E. R. Ewald summations and dielectric constants. Proc. R. Soc. London 1980, A373, 27-56.
28. Sharp, K. A.; Honig, B. Calculation total electrostatic energies with nonlinear Possion-Boltzmann equation. J. Phys. Chem. 1990, 94, 7684-7692.
29. Misra, V. K.; Sharp, K. A.; Friedman, R. A.; Honig, B. Salt-effects on ligand-DNA: binding minor groove binding antibiotics. J. Mol. Biol. 1994, 23, 8-263.
30. Baker, N. A.; Sept, D.; Joseph, S.; Holst, M. J.; McCammon, J. A. Electrostatics of nanosystems: application to microtubules and the ribosome. Proc. Natl. Acad. Sci. U.S.A. 2001, 98, 10037-10041.
31. Nina, M.; Im, W.; Roux, B. Optimized atomic radii for protein continuum electrostatic solvation forces. Biophys Chem. 1999, 78, 89-96.
32. Makarov, V. A.; Andrews, B. K.; Smith, P. E.; Pettitt, B. M. Residence times of water molecules in the hydration sites of myoglobin. Biophys J. 2000, 79, 2966-2974.
33. Bizzarri, A. R.; Cannistraro, S. Molecular dynamics of water at the protein-solvent interface. J. Phys. Chem. B 2002, 106, 6617-6633.
34. Shamblin, S.; Hancock, B. C.; Dupuis, Y.; Pikal, M. J. Interpretation of relaxation time constants for amorphous pharmaceutical systems. J. Pharm. Sci. 2000, 89, 417-427.
35. Yoshioka, S.; Tajimar, S.; Aso, Y.; Kojima, S. Inactivation and aggregation of β-galactosidase in lyophilized formulation described by Kohlrausch-Williams-Watts stretched exponential function. Pharm. Res. 2003, 20, 1655-1660.
36. Paul, S.; Chandra, A. Hydrogen dynamics at vapor-water and metal-water interface. Chem. Phys. Lett. 2004, 386, 218-224.
37. Bandyopadhyay, S.; Chakraborty, S.; Bagchi, B. Secondary structure sensitivity of hydrogen bond lifetime dynamics in the protein hydration layer. J. Am. Chem. Soc. 2005, 127, 16660-16667.
38. Cowan, J. A. Metal activiation of enzymes in nucleic acid biochemistry. Chem. Rev. 1998, 98, 1067-1087.
39. Adrian-Scotto, M.; Vasileva, D.; Mallet, G.; Vasilescu, D. About hydration of Mg 2+: a quantum DFT study. Internet electron. J. Mol. Des. 2004, 4, 400-411.
40. Markham, G. D.; Glusker, J. P.; Bock, C. L.; Trachtman, M.; Bock, C. W. Hydration energies of divalent beryllium and magnesium Ions: An ab initio molecular orbital study. J. Phys. Chem. 1996, 100, 3488-3497.
41. Black, C. B.; Cowan, J. A. Inert chromium and cobalt complexes as probes of magesium-dependent enzymes: Evaluation of the mechanistic role of the essential metal cofactor in Escherichia coli exonuclease III. Eur. J. Biochem. 1997, 243, 684-689.
42. Petrov, A. S.; Lamm, G.; Pack, G. R. Water-mediated magnesium-guanine interactions. J. Phys. Chem. B 2002, 106, 3294-3300.
43. Misra, V. K.; Hecht, J. L.; Yang, A. S.; Honig, B. Electrostatic contributions to the binding free energy of the ëcI repressor to DNA. Biophys. J. 1998, 75, 2262-2273.
44. Antosiewicz, J.; McCammon, J. A.; Glison, M. K. Prediction of pH-dependent properties of proteins. J. Mol. Biol. 1994, 238, 415-436.
45. Antosiewicz, J.; Miller, M. D.; Krause, K. L.; McCammon, J. A. Simulation of electrostatic and hydrodynamic properties of Serratia endo-nuclease. Biopolymers 1997, 44, 443-450.
46. Record, M. T.; Lohman, T. M.; deHaseth, P. Ion effects on ligand-nucleic acid interactions. J. Mol. Biol. 1976, 107, 145-158.
47. 8+) to the center of DNA oligomers. Biophys. J. 1995, 68, 634-647.
48. Jayaram, B.; Janin, T. The role of water in protein-DNA recognition. Annu. Rev. Biophys. Biomol. Struct. 2004, 33, 343-361.
49. Joachimiak, A.; Haran, T. E.; Sigler, P. B. Mutagensis supports water mediated recognition in the trp repressor-operator system. EMBO J. 1994, 13, 367-372.
50. Newman, M.; Strzelecka, T.; dorner, L.; Schildkraut, I.; Aggarwal, A. K. Structure of BamH1 endonuclease bound to DNA: partial folding and unfolding on DNA binding. Science 1995, 269, 656-663.
51. Dong, F.; Vijayakumar, M.; Zhou, H. X. Comparison of calculation and experiment implications significant electrostatic contributions to the binding stability of barnase and barstar. Biophys. J. 2003, 85, 49-60.
52. Smith, P. E.; Brunne, R. M.; Mark, A. E.; van Gunsteren, W. F. Dielectric properties of trypsin inhibitor and lysozyme calculated from Molecular Dynamics simulations. J. Phys. Chem. 1993, 97, 2009-2014.
53. Pitera, J. W.; Falta, M.; van Gunsteren, W. F. Dielectric properties of proteins from simulation: the effects of solvent, ligands, pH, and temperature. Biophys. J. 2001, 80, 2546-2555.
54. Yang, L.; Weerasinghe, S.; Smith, P. E.; Pettitt, B. M. Dielectric response of triplex NA in ionic solution from simulations. Biophys. J. 1995, 69, 1519-1527.
55. Reddy, M. R.; Berkowitz, M. Dielectric constant of SPC/E water. Chem. Phys. Lett. 1989, 155, 173-176.
56. Frank, F., Ed. Water - A comprehensive treatise; Plenum: New York, 1973; Vols. 1 and 3.
57. Humphrey, W.; Dalke, A.; Schulten, K. VMD: visual molecular dynamics. J. Mol. Graphics 1996, 14, 33-38.