Hybrid dynamics simulation engine for metalloproteins

Biophysical Journal

Volumn 103, Issue 4, 2012, Pages 767-776

  Sparta, Manuel ^a   Shirvanyants, David ^b   Ding, Feng ^b   Dokholyan, Nikolay V ^b   Alexandrova, Anastassia N ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b UNIVERSITY OF NORTH CAROLINA SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CALCIUM; CATECHOL METHYLTRANSFERASE; MAGNESIUM; RUBREDOXIN; S ADENOSYLMETHIONINE;

ARTICLE; CHEMISTRY; ELECTRON TRANSPORT; GENETICS; ION EXCHANGE; METABOLISM; MOLECULAR DYNAMICS; MUTATION; PROTEIN CONFORMATION; QUANTUM THEORY;

CALCIUM; CATECHOL O-METHYLTRANSFERASE; ELECTRON TRANSPORT; ION EXCHANGE; MAGNESIUM; MOLECULAR DYNAMICS SIMULATION; MUTATION; PROTEIN CONFORMATION; QUANTUM THEORY; RUBREDOXINS; S-ADENOSYLMETHIONINE;

EID: 84865400296     PISSN: 00063495     EISSN: 15420086     Source Type: Journal    
DOI: 10.1016/j.bpj.2012.06.024     Document Type: Article

References (90)

1. L.W. Chung, X. Li, and K. Morokuma Modeling enzymatic reactions in metalloenzymes and photobiology by quantum mechanics (QM) and quantum mechanics/molecular mechanics (QM/MM) calculations C.F. Matta, Quantum Biochemistry 2010 Wiley-VCH Weinheim, Germany 85 128
2. A. Warshel Computer Modeling of Chemical Reactions in Enzymes and Solutions 1997 John Wiley & Sons New York
3. K.M. Keating, and L.R. Ghosaini J.M. Sturtevant Thermal denaturation of T4 gene 32 protein: effects of zinc removal and substitution Biochemistry 27 1988 5240 5245
4. T. Matt, and M.A. Martinez-Yamout P.E. Wright The CBP/p300 TAZ1 domain in its native state is not a binding partner of MDM2 Biochem. J. 381 2004 685 691 (Pubitemid 39120477)
5. F. Ding, and N.V. Dokholyan Dynamical roles of metal ions and the disulfide bond in Cu, Zn superoxide dismutase folding and aggregation Proc. Natl. Acad. Sci. USA 105 2008 19696 19701
6. L. Banci, and I. Bertini M.S. Viezzoli Solution structure of Apo Cu,Zn superoxide dismutase: role of metal ions in protein folding Biochemistry 42 2003 9543 9553 (Pubitemid 37006303)
7. Y. Cao, T. Yoo, and H. Li Single molecule force spectroscopy reveals engineered metal chelation is a general approach to enhance mechanical stability of proteins Proc. Natl. Acad. Sci. USA 105 2008 11152 11157
8. O. Blum, and A. Haiek H.B. Gray Isolation of a myoglobin molten globule by selective cobalt(III)-induced unfolding Proc. Natl. Acad. Sci. USA 95 1998 6659 6662
9. R.J. Radford, and P.C. Nguyen F.A. Tezcan Controlled protein dimerization through hybrid coordination motifs Inorg. Chem. 49 2010 4362 4369
10. A. Warshel, and M. Levitt Theoretical studies of enzymic reactions: dielectric, electrostatic and steric stabilization of the carbonium ion in the reaction of lysozyme J. Mol. Biol. 103 1976 227 249
11. D. Bakowies, and W. Thiel Semiempirical treatment of electrostatic potentials and partial charges in combined quantum mechanical and molecular mechanical approaches J. Comput. Chem. 17 1996 87 108 (Pubitemid 126581862)
12. M. Svensson, and S. Humbel K. Morokuma ONIOM: A multilayered integrated MO + MM method for geometry optimizations and single point energy predictions. A test for Diels-Alder reactions and Pt(P(t-Bu)3)2 + H2 oxidative addition J. Phys. Chem. 100 1996 19357 19363 (Pubitemid 126786970)
13. M.J. Field, P.A. Bash, and M. Karplus A combined quantum mechanical and molecular mechanical potential for molecular dynamics simulations J. Comput. Chem. 11 1990 700 733
14. M. Eichinger, and P. Tavan M. Parrinello A hybrid method for solutes in complex solvents: density functional theory with empirical force fields J. Chem. Phys. 110 1999 10452 10467
15. D. Das, and K.P. Eurenius B.R. Brooks Optimization of quantum mechanical molecular mechanical partitioning schemes: Gaussian delocalization of molecular mechanical charges and the double link atom method J. Chem. Phys. 117 2002 10534 10547
16. R.V. Stanton, D.S. Hartsough, and K.M. Merz Calculation of solvation free energies using a density functional/molecular dynamics coupled potential J. Phys. Chem. 97 1993 11868 11870
17. T. Vreven, and K.S. Byun M.J. Frisch Combining quantum mechanics methods with molecular mechanics methods in ONIOM J. Chem. Theory Comput. 2 2006 815 826
18. - exchange reaction and gas phase protonation of polyethers J. Comput. Chem. 7 1986 718 730
19. V. Thery, and D. Rinaldi G.G. Ferenczy Quantum mechanical computations on very large molecular systems: the local self-consistent field method J. Comput. Chem. 15 1994 269 282
20. F. Maseras, and K. Morokuma IMOMM - a new integrated ab initio plus molecular mechanics geometry optimization scheme of equilibrium structures and transition states J. Comput. Chem. 16 1995 1170 1179
21. Y.K. Zhang, T.S. Lee, and W.T. Yang A pseudobond approach to combining quantum mechanical and molecular mechanical methods J. Chem. Phys. 110 1999 46 54
22. D.M. Philipp, and R.A. Friesner Mixed ab initio QM/MM modeling using frozen orbitals and tests with alanine dipeptide and tetrapeptide J. Comput. Chem. 20 1999 1468 1494 (Pubitemid 129651764)
23. H. Hu, and W.T. Yang Free energies of chemical reactions in solution and in enzymes with ab initio quantum mechanics/molecular mechanics methods Annu. Rev. Phys. Chem. 59 2008 573 601 (Pubitemid 351703398)
24. S.C.L. Kamerlin, and S. Vicatos A. Warshel Coarse-grained (multiscale) simulations in studies of biophysical and chemical systems Annu. Rev. Phys. Chem. 62 2011 41 64
25. C.R.W. Guimarães, M. Udier-Blagović, and W.L. Jorgensen Macrophomate synthase: QM/MM simulations address the Diels-Alder versus Michael-Aldol reaction mechanism J. Am. Chem. Soc. 127 2005 3577 3588 (Pubitemid 40365296)
26. I. Tubert-Brohman, O. Acevedo, and W.L. Jorgensen Elucidation of hydrolysis mechanisms for fatty acid amide hydrolase and its Lys142Ala variant via QM/MM simulations J. Am. Chem. Soc. 128 2006 16904 16913 (Pubitemid 46032766)
27. A.N. Alexandrova, and D. Röthlisberger W.L. Jorgensen Catalytic mechanism and performance of computationally designed enzymes for Kemp elimination J. Am. Chem. Soc. 130 2008 15907 15915
28. G.A. Kaminski, and W.L. Jorgensen A QM/MM method based on CM1A charges: applications to solvent effects on organic equilibria and reactions J. Phys. Chem. B 102 1998 1787 1796 (Pubitemid 128605019)
29. J. Chandrasekhar, S. Shariffskul, and W.L. Jorgensen QM/MM simulations of cycloaddition reactions in water: contribution of enhanced hydrogen nonding at the transition state to the solvent effects J. Phys. Chem. B 106 2002 8078 8085 (Pubitemid 35382912)
30. O. Acevedo, and W.L. Jorgensen Solvent effects and mechanism for a nucleophilic aromatic substitution from QM/MM simulations Org. Lett. 6 2004 2881 2884 (Pubitemid 39178031)
31. J.L. Gao Absolute free energy of solvation from Monte Carlo simulations using combined quantum and molecular mechanical potentials J. Phys. Chem. 96 1992 537 540
32. V. Luzhkov, and A. Warshel Microscopic calculations of solvent effects on absorption spectra of conjugated molecules J. Am. Chem. Soc. 113 1991 4491 4499
33. + crown-ether interactions - a hybrid quantum mechanical-molecular mechanical study J. Phys. Chem. 98 1994 10465 10476
34. I. Tunon, and M.T.C. Martins-Costa J.L. Rivail A coupled density functional-molecular mechanics Monte Carlo simulation method. The water molecule in liquid water J. Comput. Chem. 17 1996 19 29 (Pubitemid 126581856)
35. I. Tunon, and M.T.C. Martins-Costa M.F. Ruiz-Lopez Molecular dynamics simulations of elementary chemical processes in liquid water using density functional and molecular mechanics potentials. I. Proton transfer in strongly H-bonded complexes J. Chem. Phys. 106 1997 3633 3642 (Pubitemid 127584987)
36. M. Strand, and M.T.C. Martins-Costa J.L. Rivail Molecular dynamics simulations of elementary chemical processes in liquid water using density functional and molecular mechanics potentials. II. Charge separation processes J. Chem. Phys. 106 1997 3643 3657
37. R. Car, and M. Parrinello Unified approach for molecular dynamics and density-functional theory Phys. Rev. Lett. 55 1985 2471 2474
38. P.K. Biswas, and V. Gogonea A regularized and renormalized electrostatic coupling Hamiltonian for hybrid quantum-mechanical-molecular-mechanical calculations J. Chem. Phys. 123 2005 164114 164119
39. P. Carloni, U. Rothlisberger, and M. Parrinello The role and perspective of ab initio molecular dynamics in the study of biological systems Acc. Chem. Res. 35 2002 455 464
40. A. Laio, J. VandeVondele, and U. Rothlisberger A Hamiltonian electrostatic coupling scheme for hybrid Car-Parrinello simulations J. Chem. Phys. 116 2002 6941 6947 (Pubitemid 34537077)
41. R. Iftimie, P. Minary, and M.E. Tuckerman Ab initio molecular dynamics: concepts, recent developments, and future trends Proc. Natl. Acad. Sci. USA 102 2005 6654 6659 (Pubitemid 40675372)
42. E.J. Bylaska, and K. Tsemekhman H. Jonsson Parallel implementation of Γ-point pseudopotential plane-wave DFT with exact exchange J. Comput. Chem. 32 2011 54 69
43. J. Hutter, and A. Curioni Car-Parrinello molecular dynamics on massively parallel computers ChemPhysChem 6 2005 1788 1793 (Pubitemid 41329999)
44. I.S. Ufimtsev, and T.J. Martínez Quantum chemistry on graphical processing units. 1. Strategies for two-electron integral evaluation J. Chem. Theory Comput. 4 2008 222 231
45. I.S. Ufimtsev, and T.J. Martínez Quantum chemistry on graphical processing units. 2. Direct self-consistent field implementation J. Chem. Theory Comput. 5 2009 1004 1015
46. I.S. Ufimtsev, and T.J. Martínez Quantum chemistry on graphical processing units. 3. Analytical energy gradients and first principle molecular dynamics J. Chem. Theory Comput. 5 2009 2619 2628
47. H.M. Senn, and W. Thiel Atomistic approaches in modern biology M. Reiher, L. Bertini, Quantum Chemistry to Molecular Simulations 2007 Springer Berlin 173 290
48. M.R. Reddy, and M.D. Erion Calculation of relative binding free energy differences for fructose 1,6-bisphosphatase inhibitors using the thermodynamic cycle perturbation approach J. Am. Chem. Soc. 123 2001 6246 6252 (Pubitemid 32904651)
49. M.A. Thompson, and G.K. Schenter Excited states of the bacteriochlorophyll-b dimer of Rhodopseudomonas viridis - a QM/MM study of the photosynthetic reaction center that includes MM polarization J. Phys. Chem. 99 1995 6374 6386
50. G. Alagona, and P. Desmeules P.A. Kollman Quantum mechanical and molecular mechanical studies on a model for the dihydroxyacetone phosphate-glyceraldehyde phosphate isomerization catalyzed by triose phosphate isomerase (TIM) J. Am. Chem. Soc. 106 1984 3623 3632
51. T. Matsubara, and F. Maseras K. Morokuma Application of the New "Integrated MO + MM" (IMOMM) Method to the Organometallic Reaction Pt(PR3)2 + H2 (R = H, Me, t-Bu, and Ph) J. Phys. Chem. 100 1996 2573 2580 (Pubitemid 126793209)
52. P.L. Cummins, and J.E. Gready Coupled semiempirical molecular orbital and molecular mechanics model (QM/MM) for organic molecules in aqueous solution J. Comput. Chem. 18 1997 1496 1512 (Pubitemid 127637347)
53. G.L. Cui, and W.T. Yang Conical intersections in solution: formulation, algorithm, and implementation with combined quantum mechanics/molecular mechanics method J. Chem. Phys. 134 2011 204115
54. N.V. Dokholyan, and S.V. Buldyrev E.I. Shakhnovich Discrete molecular dynamics studies of the folding of a protein-like model Fold. Des. 3 1998 577 587 (Pubitemid 29023621)
55. F. Ding, and W. Guo J.E. Shea Reconstruction of the src-SH3 protein domain transition state ensemble using multiscale molecular dynamics simulations J. Mol. Biol. 350 2005 1035 1050 (Pubitemid 40943460)
56. N.V. Dokholyan Studies of folding and misfolding using simplified models Curr. Opin. Struct. Biol. 16 2006 79 85 (Pubitemid 43221875)
57. F. Ding, and D. Tsao N.V. Dokholyan Ab initio folding of proteins with all-atom discrete molecular dynamics Structure 16 2008 1010 1018 (Pubitemid 351899281)
58. R. Cammack Iron-sulfur clusters in enzymes: themes and variations Adv. Inorg. Chem. 38 1992 281 322
59. A.P. Gamiz-Hernandez, A.S. Galstyan, and E.W. Knapp Understanding rubredoxin redox potentials: role of H-bonds on model complexes J. Chem. Theory Comput. 5 2009 2898 2908
60. A.P. Gamiz-Hernandez, and G. Kieseritzky E.W. Knapp Rubredoxin function: redox behavior from electrostatics J. Chem. Theory Comput. 7 2011 742 752
61. K. Rutherford, and I. Le Trong W.W. Parson Crystal structures of human 108V and 108M catechol O-methyltransferase J. Mol. Biol. 380 2008 120 130
62. L. Hu, P. Söderhjelm, and U. Ryde On the convergence of QM/MM energies J. Chem. Theory Comput. 7 2011 761 777
63. P.E. Siegbahn, and M.R. Blomberg Density functional theory of biologically relevant metal centers Annu. Rev. Phys. Chem. 50 1999 221 249 (Pubitemid 129565549)
64. P.A.M. Dirac Quantum mechanics of many electron systems Proc. R. Soc. Lond. A Math. Phys. Sci. 123 1929 714 733
65. J.C. Slater A simplification of the Hartree-Fock method Phys. Rev. 81 1951 385 390
66. S.H. Vosko, L. Wilk, and M. Nusair Accurate spin-dependent electron liquid correlation energies for local spin density calculations: a critical analysis Can. J. Phys. 80 1980 1200 1211
67. A.D. Becke Density-functional exchange-energy approximation with correct asymptotic behavior Phys. Rev. A 38 1988 3098 3100
68. J.P. Perdew Density-functional approximation for the correlation energy of the inhomogeneous electron gas Phys. Rev. B Condens. Matter 33 1986 8822 8824
69. M.V. Arnim, and R. Ahlrichs Performance of Parallel TURBOMOLE for density functional calculations J. Comput. Chem. 19 1998 1746 1757 (Pubitemid 128597452)
70. M. Sierka, A. Hogekamp, and R. Ahlrichs Fast evaluation of the coulomb potential for electron densities using multipole accelerated resolution of identity approximation J. Chem. Phys. 118 2003 9136 9148
71. S. Grimme Accurate description of van der Waals complexes by density functional theory including empirical corrections J. Comput. Chem. 25 2004 1463 1473
72. A. Schafer, H. Horn, and R. Ahlrichs Fully optimized contracted Gaussian basis sets for atoms Li to Kr J. Chem. Phys. 97 1992 2571 2577
73. J.P. Perdew, and Y. Wang Accurate and simple analytic representation of the electron-gas correlation energy Phys. Rev. B Condens. Matter 45 1992 13244 13249
74. J. Tao, and J.P. Perdew G.E. Scuseria Climbing the density functional ladder: nonempirical meta-generalized gradient approximation designed for molecules and solids Phys. Rev. Lett. 91 2003 146401 146404
75. F. Weigend, and R. Ahlrichs Balanced basis sets of split valence, triple zeta valence and quadruple zeta valence quality for H to Rn: Design and assessment of accuracy Phys. Chem. Chem. Phys. 7 2005 3297 3305 (Pubitemid 41412231)
76. A. Klamt, and G. Schüürmann COSMO: a new approach to dielectric screening in solvents with explicit expressions for the screening energy and its gradient J. Chem. Soc., Perkin Trans. 2 1993 799 805
77. R. Ahlrichs, and M. Bär C. Kölmel Electronic structure calculations on workstation computers: The program system Turbomole Chem. Phys. Lett. 162 1989 165 169
78. B.R. Brooks, and R.E. Bruccoleri M. Karplus CHARMM: A program for macromolecular energy, minimization, and dynamics calculations J. Comput. Chem. 4 1983 187 217
79. T. Min, and C.E. Ergenekan C. Kang Leucine 41 is a gate for water entry in the reduction of Clostridium pasteurianum rubredoxin Protein Sci. 10 2001 613 621 (Pubitemid 32221149)
80. I.-J. Lin, and E.B. Gebel J.L. Markley Correlation between hydrogen bond lengths and reduction potentials in Clostridium pasteurianum rubredoxin J. Am. Chem. Soc. 125 2003 1464 1465 (Pubitemid 36206212)
81. 13C resonance assignment in an iron-sulfur protein with quantum chemical verification: aliphatic C-H⋯S 3-center-4-electron interactions J. Am. Chem. Soc. 133 2011 1210 1216
82. M.K. Eidsness, and A.E. Burden C. Kang Modulation of the redox potential of the [Fe(SCys)(4)] site in rubredoxin by the orientation of a peptide dipole Biochemistry 38 1999 14803 14809
83. R.A. Marcus On the theory of oxidation-reduction reactions involving electron transfer. I J. Chem. Phys. 24 1956 966 978
84. A.N. Alexandrova, and A.I. Boldyrev L.-S. Wang All-boron aromatic clusters as potential new inorganic ligands and building blocks in chemistry Coord. Chem. Rev. 250 2006 2811 2866 (and references therein)
85. A.I. Boldyrev, and L.-S. Wang All-metal aromaticity and antiaromaticity Chem. Rev. 105 2005 3716 3757 (and references therein) (Pubitemid 41622396)
86. 4 coordination unit in a protein Proc. Natl. Acad. Sci. USA 93 1996 8836 8840 (Pubitemid 26281977)
87. H.C. Andersen Molecular dynamics at constant pressure and/or temperature J. Chem. Phys. 72 1980 2384 2393
88. S. Ramachandran, and P. Kota N.V. Dokholyan Automated minimization of steric clashes in protein structures Proteins 79 2011 261 270
89. W. Kabsch A solution of the best rotation to relate two sets of vectors Acta Crystallogr. A 32 1976 922 923
90. Barton, G. J. 1993, 2002 "OC - A cluster analysis program", University of Dundee, Scotland, UK. http://www.compbio.dundee.ac.uk/downloads/ oc.