Magnesium-dependent RNA binding to the PA endonuclease domain of the avian influenza polymerase

Journal of Physical Chemistry B

Volumn 118, Issue 4, 2014, Pages 873-889

  Xiao, Shiyan ^a   Klein, Michael L ^b   Lebard, David N ^c   Levine, Benjamin G ^d   Liang, Haojun ^a   Macdermaid, Christopher M ^b   Alfonso Prieto, Mercedes ^b  

^a UNIVERSITY OF SCIENCE AND TECHNOLOGY OF CHINA   (China)

^b Temple University   (United States)

^c YESHIVA UNIVERSITY   (United States)

^d MICHIGAN STATE UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

AMINO ACIDS; ENZYMES; METAL IONS; MOLECULAR DYNAMICS; VIRUSES;

CATALYTIC LYSINE; DIVALENT METAL ION; ENDONUCLEASE ACTIVITIES; ENDONUCLEASE INHIBITORS; INFLUENZA A VIRUS; MG CONCENTRATIONS; N-TERMINAL DOMAINS; VIRAL REPLICATION;

RNA;

MAGNESIUM; PA PROTEIN, INFLUENZA VIRUSES; RNA; RNA DIRECTED RNA POLYMERASE; VIRUS PROTEIN;

ANIMAL; ARTICLE; BINDING SITE; BIRD; CHEMICAL STRUCTURE; CHEMISTRY; ENZYMOLOGY; INFLUENZA VIRUS A; METABOLISM; MOLECULAR DYNAMICS;

ANIMALS; BINDING SITES; BIRDS; INFLUENZA A VIRUS; MAGNESIUM; MODELS, MOLECULAR; MOLECULAR DYNAMICS SIMULATION; RNA; RNA REPLICASE; VIRAL PROTEINS;

EID: 84893473257     PISSN: 15206106     EISSN: 15205207     Source Type: Journal    
DOI: 10.1021/jp408383g     Document Type: Article

References (105)

1. Reid, A. H.; Taubenberger, J. K.; Fanning, T. G. The 1918 Spanish Influenza: Integrating History and Biology Microbes Infect. 2001, 2, 81-87
2. Horimoto, T.; Kawaoka, Y. Influenza: Lessons from Past Pandemics, Warnings from Current Incidents Nat. Rev. Microbiol. 2005, 3, 591-600
3. Noah, D. L.; Krug, R. M. Influenza Virus Virulence and its Molecular Determinants Adv. Virus Res. 2005, 65, 121-145
4. Hay, A. J.; Wolstenholme, A. J.; Skehel, J. J.; Smith, M. H. The Molecular Basis of the Specific Anti-Influenza Action of Amantadine EMBO J. 1985, 4, 3021-3024
5. Lamb, R. A.; Holsinger, L. J.; Pinto, L. H. The Influenza A Virus M2 Ion Channel Protein and its Role in the Influenza Virus Life Cycle. In Cellular receptors for animal viruses; Wimmer, E., Ed.; Cold Spring Harbor Laboratory Press: Woodbury, NY, 1994; pp 303-321.
6. Kim, C. U.; Lew, W.; Williams, M. A.; Liu, H.; Zhang, L.; Swaminathan, S.; Bischofberger, N.; Chen, M. S.; Mendel, D. B.; Tai, C. Y.; Laver, W. G.; Stevens, R. C. Influenza Neuraminidase Inhibitors Possessing a Novel Hydrophobic Interaction in the Enzyme Active Site: Design, Synthesis, and Structural Analysis of Carbocyclic Sialic Acid Analogues with Potent Anti-Influenza Activity J. Am. Chem. Soc. 1997, 119, 681-690
7. von Itzstein, M. Rational Design of Potent Sialidase-Based Inhibitors of Influenza Virus Replication Nature 1993, 363, 418-423
8. Drake, J. W. Rates of Spontaneous Mutation Among RNA Viruses Proc. Natl. Acad. Sci. U. S. A. 1993, 90, 4171-4175
9. Liu, Y.; Lou, Z.; Bartlam, M.; Rao, Z. Structure-Function Studies of the Influenza Virus RNA Polymerase PA Subunit Sci. China, Ser. C: Life Sci. 2009, 52, 450-458
10. Krug, R. M.; Aramini, J. M. Emerging Antiviral Targets for Influenza A Virus Trends Pharmacol. Sci. 2009, 30, 269-277
11. Das, K.; Aramini, J. M.; Ma, L.-C.; Krug, R. M.; Arnold, E. Structures of Influenza A Proteins and Insights into Antiviral Drug Targets Nat. Struct. Mol. Biol 2010, 17, 530-538
12. Boivin, S.; Cusack, S.; Ruigrok, R. W. H.; Hart, D. J. Influenza A Virus Polymerase: Structural Insights into Replication and Host Adaptation Mechanisms J. Biol. Chem. 2010, 285, 28411-28417
13. Ruigrok, R. W.; Crépin, T.; Hart, D. J.; Cusack, S. Towards an Atomic Resolution Understanding of the Influenza Virus Replication Machinery Curr. Opin. Struct. Biol. 2010, 20, 104-113
14. Rogolino, D.; Carcelli, M.; Sechi, M.; Neamati, N. Viral Enzymes Containing Magnesium: Metal Binding as a Successful Strategy in Drug Design Coord. Chem. Rev. 2012, 256, 3063-3086
15. 7GPppXM)-Dependent Influenza Virion Endonuclease Cleaves Capped RNAs to Generate the Primers that Initiate Viral RNA Transcription Cell 1981, 23, 847-858
16. Poon, L. L. M.; Pritlove, D. C.; Fodor, E.; Brownlee, G. G. Direct Evidence that the Poly(A) Tail of Influenza A Virus MRNA is Synthesized by Reiterative Copying of a U Track in the Virion RNA Template J. Virol. 1999, 73, 3473-3476
17. Zheng, H.; Lee, H. A.; Palese, P.; Garcia-Sastre, A. Influenza A Virus RNA Polymerase Has the Ability to Stutter at the Polyadenylation Site of a Viral RNA Template During RNA Replication J. Virol. 1999, 73, 5240-5243
18. Sugiyama, K.; Obayashi, E.; Kawaguchi, A.; Suzuki, Y.; Tame, J. R. H.; Nagata, K.; Park, S.-Y. Structural Insight into the Essential PB1-PB2 Subunit Contact of the Influenza Virus RNA Polymerase EMBO J. 2009, 28, 1803-1811
19. N Complex from an Avian Influenza H5N1 Virus Nature 2008, 454, 1123-1126
20. Obayashi, E.; Yoshida, H.; Kawai, F.; Shibayama, N.; Kawaguchi, A.; Nagata, K.; Tamel, J. R. H.; Park, S.-Y. The Structural Basis for an Essential Subunit Interaction in Influenza Virus RNA Polymerase Nature 2008, 454, 1127-1131
21. Dias, A.; Bouvier, D.; Crépin, T.; McCarthy, A. A.; Hart, D. J.; Baudin, F.; Cusack, S.; Ruigrok, R. W. H. The Cap-Snatching Endonuclease of Influenza Virus Polymerase Resides in the PA Subunit Nature 2009, 458, 914-918
22. N Reveals an Endonuclease Active Site Nature 2009, 458, 909-913
23. Kowalinski, E.; Zubieta, C.; Wolkerstorfer, A.; Szolar, O. H. J.; Ruigrok, R. W.; Cusack, S. Structural Studies of Specific Metal Chelating Inhibitor Binding to the Endonuclease Domain of Influenza PH1N1 (2009) Polymerase PLoS Pathog. 2012, 8, e1002831
24. DuBois, R. M.; Slavish, P. J.; Baughman, B. M.; Yun, M.-K.; Bao, J.; Webby, R. J.; Webb, T. R.; White, S. W. Structural and Biochemical Basis for Development of Influenza Virus Inhibitors Targeting the PA Endonuclease PLoS Pathog. 2012, 8, e1002830
25. Crépin, T.; Dias, A.; Andrés Palencia, C. S.; Cusack, S.; Ruigrok, R. W. H. Mutational and Metal Binding Analysis of the Endonuclease Domain of the Influenza Virus Polymerase PA Subunit J. Virol. 2010, 84, 9096-9104
26. Harding, M. M.; Nowicki, M. W.; Walkinshaw, M. D. Metals in Protein Structures: a Review of Their Principal Features Crystallogr. Rev. 2010, 16, 247-302
27. Dudev, T.; Lin, Y.; Dudev, M.; Lim, C. First-Second Shell Interactions in Metal Binding Sites in Proteins: A PDB Survey and DFT/CDM Calculations J. Am. Chem. Soc. 2003, 125, 3168-3180
28. Yang, T.-Y.; Dudev, T.; Lim, C. Mononuclear versus Binuclear Metal-Binding Sites: A Metal-Binding Affinity and Selectivity from PDB Survey and DFT/CDM Calculations J. Am. Chem. Soc. 2008, 130, 3844-3852
29. Bock, C. W.; Katz, A. K.; Markham, G. D.; Glusker, J. P. Manganese as a Replacement for Magnesium and Zinc: Functional Comparison of the Divalent Ions J. Am. Chem. Soc. 1999, 121, 7360-7372
30. Doan, L.; Handa, B.; Roberts, N. A.; Klumpp, K. Metal Ion Catalysis of RNA Cleavage by the Influenza Virus Endonuclease Biochemistry 1999, 38, 5612-5619
31. Zhao, C.; Lou, Z.; Guo, Y.; Ma, M.; Chen, Y.; Liang, S.; Zhang, L.; Chen, S.; Li, X.; Liu, Y.; Bartlam, M.; Rao, Z. Nucleoside Monophosphate Complex Structures of the Endonuclease Domain from the Influenza Polymerase PA Subunit Reveal the Substrate Binding Site inside the Catalytic Center J. Virol. 2009, 83, 9024-9030
32. Vettori, M. V.; Gatti, R.; Orlandini, G.; Belleti, S.; Alinovi, R.; Smargiassi, A.; Mutti, A. An in vitro Model for the Assessment of Manganese Neurotoxicity Toxicol. In Vitro 1999, 13, 931-938
33. Dobson, A. W.; Erikson, K. M.; Aschner, M. Manganese Neurotoxicity Ann. N. Y. Acad. Sci. 2004, 1012, 115-128
34. Maret, W. Metalloproteomics, Metalloproteomes, and the Annotation of Metalloproteins Metallomics 2010, 2, 117-125
35. Jahnen-Dechent, W.; Ketteler, M. Magnesium Basics Clin. Kidney J. 2012, 5, i3-i14
36. Dupureur, C. M. Roles of Metal Ions in Nucleases Curr. Opin. Chem. Biol. 2008, 12, 250-255
37. MacKerell, A. D.; Nilsson, L. Molecular Dynamics Simulations of Nucleic Acid-Protein Complexes Curr. Opin. Struct. Biol. 2008, 18, 194-199
38. Abyzov, A.; Uzun, A.; Strauss, P. R.; Ilyin, V. A. An AP Endonuclease 1-DNA Polymerase β Complex: Theoretical Prediction of Interacting Surfaces PLoS Comput. Biol. 2008, 4, e1000066
39. Allawi, H. T.; Kaiser, M. W.; Onufriev, A. V.; Ma, W.-P.; Brogaard, A. E.; Case, D. A.; Neri, B. P.; Lyamichev, V. I. Modeling of Flap Endonuclease Interactions with DNA Substrate J. Mol. Biol. 2003, 328, 537-554
40. Swift, R. V.; Durrant, J.; Amaro, R. E.; McCammon, J. A. Toward Understanding the Conformational Dynamics of RNA Ligation Biochemistry 2009, 48, 709-719
41. Kormos, B. L.; Baranger, A. M.; Beveridge, D. L. Do Collective Atomic Fluctuations Account for Cooperative Effects? Molecular Dynamics Studies of the U1A-RNA Complex J. Am. Chem. Soc. 2006, 128, 8992-8993
42. Ditzler, M. A.; Otyepka, M.; Sponer, J.; Walter, N. G. Molecular Dynamics and Quantum Mechanics of RNA: Conformational and Chemical Change We Can Believe In Acc. Chem. Res. 2010, 43, 40-47
43. Formoso, E.; Matxain, J. M.; López, X. Molecular Dynamics Simulation of Bovine Pancreatic Ribonuclease A-CpA and Transition State-Like Complexes J. Phys. Chem. B 2010, 114, 7371-7382
44. Feig, M.; Burton, Z. F. RNA Polymerase II with Open and Closed Trigger Loops: Active Site Dynamics and Nucleic Acid Translocation Biophys. J. 2010, 99, 2577-2586
45. Palermo, G.; Stenta, M.; Cavalli, A.; Dal-Peraro, M.; De-Vivo, M. Molecular Simulations Highlight the Role of Metals in Catalysis and Inhibition of Type II Topoisomerase J. Chem. Theory Comput. 2013, 9, 857-862
46. Guéroult, M.; Picot, D.; Abi-Ghanem, J.; Hartmann, B.; Baaden, M. How Cations Can Assist DNase I in DNA Binding and Hydrolysis PLoS Comput Biol 2010, 6, e1001000
47. Zahran, M.; Daidone, I.; Smith, J. C.; Imhof, P. Mechanism of DNA Recognition by the Restriction Enzyme EcoRV J. Mol. Biol. 2010, 401, 415-432
48. Zahran, M.; Berezniak, T.; Imhof, P.; Smith, J. C. Role of Magnesium Ions in DNA Recognition by the EcoRV Restriction Endonuclease FEBS Lett. 2011, 585, 2739-2743
49. Chen, C.; Krause, K.; Pettitt, B. M. Advantage of Being a Dimer for Serratia Marcescens Endonuclease J. Phys. Chem. B 2009, 113, 511-521
50. Davis, B. C.; Thorpe, I. F. Molecular Simulations Illuminate the Role of Regulatory Components of the RNA Polymerase from Hepatitis C Virus in Influencing Protein Structure and Dynamics Biochemistry 2013, 52, 4541-4552
51. Fuxreiter, M.; Osman, R. Probing the General Base Catalysis in the First Step of BamHI Action by Computer Simulation Biochemistry 2001, 40, 15017-15023
52. De-Vivo, M.; Dal-Peraro, M.; Klein, M. L. Phosphodiester Cleavage in Ribonuclease H Occurs Via an Associative Two-Metal-Aided Catalytic Mechanism J. Am. Chem. Soc. 2008, 130, 10955-10962
53. De-Vivo, M.; Ensing, B.; Dal-Peraro, M.; Gomez, G. A.; Christianson, D. W.; Klein, M. L. Proton Shuttles and Phosphatase Activity in Soluble Epoxide Hydrolase J. Am. Chem. Soc. 2007, 129, 387-394
54. Rosta, E.; Nowotny, M.; Yang, W.; Hummer, G. Catalytic Mechanism of RNA Backbone Cleavage by Ribonuclease H from Quantum Mechanics/Molecular Mechanics Simulations J. Am. Chem. Soc. 2011, 133, 8934-8941
55. Imhof, P.; Fischer, S.; Smith, J. C. Catalytic Mechanism of DNA Backbone Cleavage by the Restriction Enzyme EcoRV: a Quantum Mechanical/Molecular Mechanical Analysis Biochemistry 2009, 48, 9061-9075
56. 2+ Ions in a Class I RNA Polymerase Ribozyme: a Molecular Simulation Study J. Phys. Chem. B 2012, 116, 2259-2268
57. Ho, M.-H.; De-Vivo, M.; Dal-Peraro, M.; Klein, M. L. Understanding the Effect of Magnesium Ion Concentration on the Catalytic Activity of Ribonuclease H Through Computation: Does a Third Metal Binding Site Modulate Endonuclease Catalysis? J. Am. Chem. Soc. 2010, 132, 13702-13712
58. Li, P.; Roberts, B. P.; Chakravorty, D. K.; Merz, K. M., Jr. Rational Design of Particle Mesh Ewald Compatible Lennard-Jones Parameters for +2 Metal Cations in Explicit Solvent J. Chem. Theory Comput. 2013, 9, 2733-2748
59. Nowotny, M.; Yang, W. Stepwise Analyses of Metal Ions in RNAse H Catalysis from Substrate Destabilization to Product Release EMBO J. 2006, 25, 1924-1933
60. Humphrey, W.; Dalke, A.; Schulten, K. VMD-Visual Molecular Dynamics J. Mol. Graph. 1996, 14, 33-38
61. Noble, E.; Cox, A.; Deval, J.; Kim, B. Endonuclease Substrate Selectivity Characterized with Full-Length PA of Influenza A Virus Polymerase Virology 2012, 433, 27-34
62. Horton, N. C.; Perona, J. J. Recognition of Flanking DNA Sequences by EcoRV Endonuclease Involves Alternative Patterns of Water-Mediated Contacts J. Biol. Chem. 1998, 273, 21721-21729
63. Deka, P.; Rajan, P. K.; Perez-Canadillas, J. M.; Varani, G. Protein and RNA Dynamics Play Key Roles in Determining the Specific Recognition of GU-Rich Polyadenylation Regulatory Elements by Human Cstf-64 Protein J. Mol. Biol. 2005, 347, 719-733
64. Cornell, W. D.; Cieplak, P.; Bayly, C. I.; Gould, I. R.; Merz, K. M.; Ferguson, D. M.; Spellmeyer, D. C.; Fox, T.; Caldwell, J. W.; Kollman, P. A. A Second Generation Force Field for the Simulation of Proteins, Nucleic Acids and Organic Molecules J. Am. Chem. Soc. 1995, 117, 5179-5197
65. Pérez, A.; Marchán, I.; Svozil, D.; Sponer, J.; Cheatham, T. E.; Laughton, C. A.; Orozco, M. Refinement of the AMBER Force Field for Nucleic Acids: Improving the Description of α/γ Conformers Biophys. J. 2007, 92, 3817-3829
66. Jorgensen, W. L.; Chandrasekhar, J.; Madura, J. D.; Impey, R. W.; Klein, M. L. Comparison of Simple Potential Functions for Simulating Liquid Water J. Chem. Phys. 1983, 79, 926-935
67. Bader, R. F. Atoms In Molecules-A Quantum Theory; Oxford University Press: Oxford, U.K., 1990.
68. Dal-Peraro, M.; Spiegel, K.; Lamoureux, G.; De-Vivo, M.; DeGrado, W. F.; Klein, M. L. Modeling the Charge Distribution at Metal Sites in Proteins for Molecular Dynamics Simulations J. Struct. Biol. 2007, 157, 444-453
69. Aaqvist, J. Ion-Water Interaction Potentials Derived from Free Energy Perturbation Simulations J. Phys. Chem. 1990, 94, 8021-8024
70. Phillips, J. C.; Braun, R.; Wang, W.; Gumbart, J.; Tajkhorshid, E.; Villa, E.; Chipot, C.; Skeel, R. D.; Kalé, L.; Schulten, K. Scalable Molecular Dynamics with NAMD J. Comput. Chem. 2005, 26, 1781-1802
71. Ryckaert, J.-P.; Ciccotti, G.; Berendsen, H. J. C. Numerical Integration of the Cartesian Equations of Motion of a System with Constraints: Molecular Dynamics of N-Alkanes J. Comput. Phys. 1977, 23, 327-341
72. Jesus A. Izaguirre, S. R.; Skeel, R. D. Longer Time Steps for Molecular Dynamics J. Chem. Phys. 1999, 110, 9853-9864
73. Darden, T.; York, D.; Pedersen, L. Particle Mesh Ewald: an N Log(N) Method for Ewald Sums in Large Systems J. Chem. Phys. 1993, 98, 10089
74. Hoover, W. G. Canonical Dynamics: Equilibrium Phase-Space Distributions Phys. Rev. A 1985, 31, 1695-1697
75. Parkes, K. E. B.; Ermert, P.; Fässler, J.; Ives, J.; Martin, J. A.; Merrett, J. H.; Obrecht, D.; Williams, G.; Klumpp, K. Use of a Pharmacophore Model to Discover a New Class of Influenza Endonuclease Inhibitors J. Med. Chem. 2003, 46, 1153-1164
76. Harding, M. M. Small Revisions to Predicted Distances Around Metal Sites in Proteins Acta Crystallogr. D 2006, 62, 678-682
77. Spiegel, K.; DeGrado, W. F.; Klein, M. L. Structural and Dynamical Properties of Manganese Catalase and the Synthetic Protein DF1 and Their Implication for Reactivity from Classical Molecular Dynamics Calculations Proteins 2006, 65, 317-330
78. 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
79. Yang, W. Nucleases: Diversity of Structure, Function and Mechanism Q. Rev. Biophys. 2011, 44, 1-93
80. Pingoud, A.; Fuxreiter, M.; Pingoud, V.; Wende, W. Type II Restriction Endonucleases: Structure and Mechanism Cell. Mol. Life Sci. 2005, 62, 685-707
81. Dupureur, C. M. One is Enough: Insights into the Two-Metal Ion Nuclease Mechanism from Global Analysis and Computational Studies Metallomics 2010, 2, 609-620
82. Horton, N. C.; Perona, J. J. Crystallographic Snapshots along a Protein-Induced DNA-Bending Pathway Proc. Natl. Acad. Sci. U. S. A. 2000, 97, 5729-5734
83. Datta, K.; Wolkerstorfer, A.; Szolar, O. H.; Cusack, S.; Klumpp, K. Characterization of PA-N Domain of Influenza A Polymerase Reveals Sequence Specific RNA Cleavage Nucleic Acids Res. 2013, 41, 8289-8299
84. Allers, J.; Shamoo, Y. Structure-Based Analysis of Protein-RNA Interactions Using the Program ENTANGLE J. Mol. Biol. 2001, 311, 75-86
85. Messias, A. C.; Sattler, M. Structural Basis of Single-Stranded RNA Recognition Acc. Chem. Res. 2004, 37, 279-287
86. Morozova, N.; Allers, J.; Myers, J.; Shamoo, Y. Protein-RNA Interactions: Exploring Binding Patterns with a Three-Dimensional Superposition Analysis of High Resolution Structures Bioinformatics 2006, 22, 2746-2752
87. 2+ Confers DNA Binding Specificity to the EcoRV Restriction Endonuclease Biochemistry 1992, 31, 3727-3732
88. Amadei, A.; Linssen, A. B. M.; Berendsen, H. J. C. Essential Dynamics of Proteins Proteins 1993, 17, 412-425
89. Pérez, A.; Blas, J. R.; Rueda, M.; López-Bes, J. M.; de la Cruz, X.; Orozco, M. Exploring the Essential Dynamics of B-DNA J. Chem. Theory Comput. 2005, 1, 790-800
90. 2+ Ions Reveals Two Divalent Metals Bound in the Active Site J. Biol. Chem. 2001, 276, 7266-7271
91. Nowotny, M.; Gaidamakov, S. A.; Crouch, R. J.; Yang, W. Crystal Structures of RNAse H Bound to an RNA/DNA Hybrid: Substrate Specificity and Metal-Dependent Catalysis Cell 2005, 121, 1005-1016
92. Vipond, I. B.; Halford, S. E. Specific DNA Recognition by EcoRV Restriction Endonuclease Induced by Calcium Ions Biochemistry 1995, 34, 1113-1119
93. Viadiu, H.; Aggarwal, A. K. Structure of BamHI Bound to Nonspecific DNA: a Model for DNA Sliding Mol. Cell 2000, 5, 889-895
94. Lee, J. Y.; Chang, J.; Joseph, N.; Ghirlando, R.; Rao, D. N.; Yang, W. MutH Complexed with Hemi- and Unmethylated DNAs: Coupling Base Recognition and DNA Cleavage Mol. Cell 2005, 20, 155-166
95. 2+ J. Phys. Chem. B 2007, 111, 6272-6279
96. Bowen, L. M.; Dupureur, C. M. Investigation of Restriction Enzyme Cofactor Requirements: a Relationship between Metal Ion Properties and Sequence Specificity Biochemistry 2003, 42, 12643-12653
97. 2+-Ion Catalysis and Substrate Specificity Mol. Cell 2006, 22, 5-13
98. Pingoud, V.; Wende, W.; Friedhoff, P.; Reuter, M.; Alves, J.; Jeltsch, A.; Mones, L.; Fuxreiter, M.; Pingoud, A. On the Divalent Metal Ion Dependence of DNA Cleavage by Restriction Endonucleases of the EcoRI Family J. Mol. Biol. 2009, 393, 140-160
99. Keck, J. L.; Goedken, E. R.; Marqusee, S. Activation/Attenuation Model for RNAse H: a One-Metal Mechanism with a Second Metal Inhibition J. Biol. Chem. 1998, 273, 34128-34133
100. Cowan, J. A. Metal Activation of Enzymes in Nucleic Acid Biochemistry Chem. Rev. 1998, 98, 1067-1087
101. Cisneros, G. A.; Perera, L.; Schaaper, R. M.; Pedersen, L. C.; London, R. E.; Pedersen, L. G.; Darden, T. A. Reaction Mechanism of the Ïμ Subunit of E. coli DNA Polymerase III: Insights into Active Site Metal Coordination and Catalytically Significant Residues J. Am. Chem. Soc. 2009, 131, 1550-1556
102. Pearson, R. G. Hard and Soft Acids and Bases J. Am. Chem. Soc. 1963, 85, 3533-3539
103. Horton, N. C.; Perona, J. J. DNA Cleavage by EcoRV Endonuclease: Two Metal Ions in Three Metal Ion Binding Sites Biochemistry 2004, 43, 6841-6857
104. Horton, N. C.; Newberry, K. J.; Perona, J. J. Metal Ion-Mediated Substrate-Assisted Catalysis in Type II Restriction Endonucleases Proc. Natl. Acad. Sci. 1998, 95, 13489-13404
105. Xie, F.; Briggs, J. M.; Dupureur, C. M. Nucleophile Activation in PD...(D/E)XK Metallonucleases: an Experimental and Computational Study J. Inorg. Biochem. 2010, 104, 665-672