The MoD-QM/MM methodology for structural refinement of photosystem II and other biological macromolecules

Photosynthesis Research

Volumn 102, Issue 2, 2009, Pages 455-470

  Sproviero, Eduardo M ^a   Newcomer, Michael B ^a   Gascón, José A ^a,b   Batista, Enrique R ^c   Brudvig, Gary W ^a   Batista, Victor S ^a  

^a YALE UNIVERSITY   (United States)

^b UNIVERSITY OF CONNECTICUT   (United States)

^c LOS ALAMOS NATIONAL LABORATORY   (United States)

Author keywords

EXAFS; MoD QM MM; Molecular mechanics; Photosystem II; Quantum mechanics

Indexed keywords

WATER;

CHEMISTRY; MACROMOLECULE; MOLECULAR DYNAMICS; PHOTOSYSTEM II; QUANTUM THEORY; REVIEW; SPECTROSCOPY;

MACROMOLECULAR SUBSTANCES; MOLECULAR DYNAMICS SIMULATION; PHOTOSYSTEM II PROTEIN COMPLEX; QUANTUM THEORY; SPECTRUM ANALYSIS; WATER;

EID: 76149092480     PISSN: 01668595     EISSN: None     Source Type: Journal    
DOI: 10.1007/s11120-009-9467-6     Document Type: Review

References (83)

1. Ankudinov AL, Ravel B, Rehr JJ, Conradson SD (1998) Real-space multiple-scattering calculation and interpretation of X-ray-absorption near-edge structure. Phys Rev B 58: 7565-7576.
2. Ankudinov AL, Bouldin CE, Rehr JJ, Sims J, Hung H (2002) Parallel calculation of electron multiple scattering using Lanczos algorithms. Phys Rev B 65: 104-107.
3. Ashley CA, Doniach S (1975) Theory of extended X-ray absorption-edge fine-structure (EXAFS) in crystalline solids. Phys Rev B 11: 1279-1288.
4. Bouldin C, Sims J, Hung H, Rehr JJ, Ankudinov AL (2001) Rapid calculation of X-ray absorption near edge structure using parallel computation. X-Ray Spectrom 30: 431-434.
5. Britt RD, Peloquin JM, Campbell KA (2000) Pulsed and parallel-polarization EPR characterization of the photosystem II oxygen-evolving complex. Annu Rev Biophys Biomol Struct 29: 463-495.
6. Britt RD, Campbell KA, Peloquin JM, Gilchrist ML, Aznar CP, Dicus MM, Robblee J, Messinger J (2004) Recent pulsed EPR studies of the photosystem II oxygen-evolving complex: implications as to water oxidation mechanisms. Biochim Biophys Acta 1655: 158-171.
7. Broyden CG (1970) Convergence of single-rank quasi-Newton methods. Math Comput 24: 365-382.
8. 2 evolution. Proc Natl Acad Sci USA 83: 4586-4588.
9. Cooper SR, Calvin M (1977) Mixed-valence interactions in di-μ-oxo bridged manganese complexes. J Am Chem Soc 99: 6623-6630.
10. Cooper SR, Dismukes GC, Klein MP, Calvin M (1978) Mixed-valence interactions in di-μ-oxo bridged manganese complexes: electron-paramagnetic resonance and magnetic-susceptibility studies. J Am Chem Soc 100: 7248-7252.
11. Cornell WD, Cieplak P, Bayly CI, Gould IR, Merz KM, Ferguson DM, Spellmeyer DC, Fox T, Caldwell JW, Kollman PA (1995) A second generation force-field for the simulation of proteins, nucleic-acids, and organic-molecules. J Am Chem Soc 117: 5179-5197.
12. Dapprich S, Komaromi I, Byun KS, Morokuma K, Frisch MJ (1999) A new ONIOM implementation in Gaussian98. Part I. The calculation of energies, gradients, vibrational frequencies and electric field derivatives. THEOCHEM J Mol Struct 461: 1-21.
13. Dau H, Iuzzolino L, Dittmer J (2001) The tetra-manganese complex of photosystem II during its redox cycle: X-ray absorption results and mechanistic implications. Biochim Biophys Acta 1503: 24-39.
14. 1-state-EXAFS results in relation to recent crystallographic data. Phys Chem Chem Phys 6: 4781-4792.
15. DeRose VJ, Mukerji I, Latimer MJ, Yachandra VK, Sauer K, Klein MP (1994) Comparison of the manganese oxygen-evolving complex in photosystem II of Spinach and Synechococcus Sp with multinuclear manganese model compounds by X-ray-absorption spectroscopy. J Am Chem Soc 116: 5239-5249.
16. Dykstra CE (1993) Electrostatic interaction potentials in molecular-force fields. Chem Rev 93: 2339-2353.
17. Fan LY, Ziegler T (1991) The influence of self-consistency on nonlocal density functional calculations. J Chem Phys 94: 6057-6063.
18. Ferreira KN, Iverson TM, Maghlaoui K, Barber J, Iwata S (2004) Architecture of the photosynthetic oxygen-evolving center. Science 303: 1831-1838.
19. Flank AM, Weininger M, Mortenson LE, Cramer SP (1986) Single-crystal EXAFS of nitrogenase. J Am Chem Soc 108: 1049-1055.
20. Fletcher R (1970) A new approach to variable metric algorithms. Comput J 13: 317-322.
21. Frisch MJ, Trucks GW, Schlegel HB, Scuseria GE, Robb MA, Cheeseman JR, Montgomery Jr JA, Vreven T, Kudin KN, Burant JC, Millam JM, Iyengar SS, Tomasi J, Barone V, Mennucci B, Cossi M, Scalmani G, Rega N, Petersson GA, Nakatsuji H, Hada M, Ehara M, Toyota K, Fukuda R, Hasegawa J, Ishida M, Nakajima T, Honda Y, Kitao O, Nakai H, Klene M, Li X, Knox JE, Hratchian HP, Cross JB, Bakken V, Adamo C, Jaramillo J, Gomperts R, Stratmann RE, Yazyev O, Austin AJ, Cammi R, Pomelli C, Ochterski JW, Ayala PY, Morokuma K, Voth GA, Salvador P, Dannenberg JJ, Zakrzewski VG, Dapprich S, Daniels AD, Strain MC, Farkas O, Malick DK, Rabuck AD, Raghavachari K, Foresman JB, Ortiz JV, Cui Q, Baboul AG, Clifford S, Cioslowski J, Stefanov BB, Liu G, Liashenko A, Piskorz P, Komaromi I, Martin RL, Fox DJ, Keith T, Al-Laham MA, Peng CY, Nanayakkara A, Challacombe M, Gill PMW, Johnson B, Chen W, Wong MW, Gonzalez C, Pople JA (2004) Gaussian 03, Revision B. 04. Gaussian, Inc., Wallingford, CT.
22. Gascon JA, Leung SSF, Batista ER, Batista VS (2006a) A self-consistent space-domain decomposition method for QM/MM computations of protein electrostatic potentials. J Chem Theory Comput 2: 175-186.
23. Gascon JA, Sproviero EM, Batista VS (2006b) Computational studies of the primary phototransduction event in visual rhodopsin. Acc Chem Res 39: 184-193.
24. Goldfarb D (1970) A family of variable-metric methods derived by variational means. Math Comput 24: 23-26.
25. Z in calcium-depleted photosystem II. Biochim Biophys Acta 1411: 121-133.
26. 0) characterized by X-ray absorption spectroscopy at 20 K and room temperature. Biochemistry 44: 1894-1908.
27. 2 state of photosystem II. Biochemistry 41: 13328-13334.
28. 18O isotope exchange measurements reveal that calcium is involved in the binding of one substrate-water molecule to the oxygen-evolving complex in photosystem II. Biochemistry 42: 6209-6217.
29. Hillier W, Wydrzynski T (2004) Substrate water interactions within the photosystem II oxygen evolving complex. Phys Chem Chem Phys 6: 4882-4889.
30. 18O-Water exchange in photosystem II: substrate binding and intermediates of the water splitting cycle. Coord Chem Rev 252: 306-317.
31. Hoganson CW, Babcock GT (1997) A metalloradical mechanism for the generation of oxygen from water in photosynthesis. Science 277: 1953-1956.
32. Jaguar (2003) Jaguar 5. 5. Schrodinger LLC, Portland, OR.
33. Kronig RD (1931) The quantum theory of dispersion in metallic conductors II. In: Proceedings of the Royal Society of London Series A Containing Papers of a Mathematical and Physical Character, vol 133, pp 255-265.
34. Kronig RD, Penney WG (1931) Quantum mechanics of electrons on crystal lattices. In: Proceedings of the Royal Society of London Series A Containing Papers of a Mathematical and Physical Character, vol 130, pp 499-513.
35. Lee PA, Pendry JB (1975) Theory of the extended X-ray absorption fine structure. Phys Rev B 11: 2795-2811.
36. 2-evolving complex in photosystem II. Science 283: 1524-1527.
37. Loll B, Kern J, Saenger W, Zouni A, Biesiadka J (2005) Towards complete cofactor arrangement in the 3. 0 Å resolution structure of photosystem II. Nature 438: 1040-1044.
38. Lundberg M, Siegbahn PEM (2004) Theoretical investigations of structure and mechanism of the oxygen-evolving complex in PSII. Phys Chem Chem Phys 6: 4772-4780.
39. Lundberg M, Blomberg MRA, Siegbahn PEM (2003) Modeling water exchange on monomeric and dimeric Mn centers. Theor Chem Acc 110: 130-143.
40. 2O. Inorg Chem 33: 5157-5160.
41. Maseras F, Morokuma K (1995) IMOMM: a new integrated ab initio plus molecular mechanics geometry optimization scheme of equilibrium structures and transition-states. J Comput Chem 16: 1170-1179.
42. McEvoy JP, Brudvig GW (2004) Structure-based mechanism of photosynthetic water oxidation. Phys Chem Chem Phys 6: 4754-4763.
43. Menikarachchi LC, Gascon JA (2008) Optimization of cutting schemes for the evaluation of molecular electrostatic potentials in proteins via moving-domain QM/MM. J Mol Model 14: 479-487.
44. xCa structures for the catalytic site and spectroscopic data. Phys Chem Chem Phys 6: 4764-4771.
45. 3 state of photosystem II. Proc Natl Acad Sci USA 92: 3209-3213.
46. Newcomer MB, Ragain CM, Gascón JA, Batista ER, Strobel SA, Loria JP, Batista VS (2009) A self-consistent MOD-QM/MM structural refinement method: characterization of hydrogen bonding in the oxytricha nova G-quadruplex. J Chem Theory Comput (submitted).
47. Noodleman L (1981) Valence bond description of anti-ferromagnetic coupling in transition-metal dimers. J Chem Phys 74: 5737-5743.
48. Noodleman L, Case DA (1992) Density functional theory of spin polarization and spin coupling in iron-sulfur clusters. Adv Inorg Chem 38: 423-470.
49. Noodleman L, Davidson ER (1986) Ligand spin polarization and antiferromagnetic coupling in transition-metal dimers. Chem Phys 109: 131-143.
50. Noodleman L, Peng CY, Case DA, Mouesca JM (1995) Orbital interactions, electron delocalization and spin coupling in iron-sulfur clusters. Coord Chem Rev 144: 199-244.
51. Nugent JHA, Rich AM, Evans MCW (2001) Photosynthetic water oxidation: towards a mechanism. Biochim Biophys Acta 1503: 138-146.
52. Pantazis DA, Orio M, Petrenko T, Zein S, Bill E, Lubitz W, Messinger J, Neese F (2009) A new quantum chemical approach to the magnetic properties of oligonuclear transition-metal complexes: application to a model for the tetranuclear manganese cluster of photosystem II. Chem Eur J 15: 5108-5123.
53. Pecoraro VL, Baldwin MJ, Gelasco A (1994) Interaction of manganese with dioxygen and its reduced derivatives. Chem Rev 94: 807-826.
54. Robblee JH, Cinco RM, Yachandra VK (2001) X-ray spectroscopy-based structure of the Mn cluster and mechanism of photosynthetic oxygen evolution. Biochim Biophys Acta 1503: 7-23.
55. +: a model for the photosynthetic water oxidizing complex. Inorg Chem 38: 1036-1037.
56. 3+ complexes. J Am Chem Soc 112: 7255-7260.
57. Sayers DE, Stern EA, Lytle FW (1971) New technique for investigating noncrystalline structures: Fourier analysis of extended X-ray absorption fine structure. Phys Rev Lett 27: 1204-1207.
58. Schlegel HB (1987) Optimization of equilibrium geometries and transition structures. Adv Chem Phys 67: 249-285.
59. Schlodder E, Witt HT (1999) Stoichiometry of proton release from the catalytic center in photosynthetic water oxidation: reexamination by a glass electrode study at pH 5. 5-7. 2. J Biol Chem 274: 30387-30392.
60. Scott RA, Hahn JE, Doniach S, Freeman HC, Hodgson KO (1982) Polarized X-ray absorption-spectra of oriented plastocyanin single-crystals: investigation of methionine copper coordination. J Am Chem Soc 104: 5364-5369.
61. Shanno DF (1970) Conditioning of quasi-Newton methods for function minimization. Math Comput 24: 647-656.
62. Soderhjelm P, Ryde U (2006) Combined computational and crystallographic study of the oxidised states of NiFe hydrogenase. THEOCHEM J Mol Struct 770: 199-219.
63. 2-evolving complex in photosystem II: evaluation of the DFT/B3LYP level of theory. J Inorg Biochem 100: 786-800.
64. 2-evolving complex of photosystem II. J Chem Theory Comput 2: 1119-1134.
65. Sproviero EM, Gascon JA, McEvoy JP, Brudvig GW, Batista VS (2007) Structural models of the oxygen-evolving complex of photosystem II. Curr Opin Struct Biol 17: 173-180.
66. Sproviero EM, Brudvig GW, Batista VS (2008a) A P-EXAFS molecular refinement protocol. J Phys Chem (in preparation).
67. 2-evolving complex of photosystem II and biomimetic oxomanganese complexes. Coord Chem Rev 252: 395-415.
68. Sproviero EM, Gascon JA, McEvoy JP, Brudvig GW, Batista VS (2008c) A model of the oxygen evolving center of photosystem II predicted by structural refinement based on EXAFS simulations. J Am Chem Soc 130: 6728-6730.
69. Sproviero EM, Gascon JA, McEvoy JP, Brudvig GW, Batista VS (2008d) QM/MM study of the catalytic cycle of water splitting in photosystem II. J Am Chem Soc 130: 3428-3442.
70. Sproviero EM, Shinopoulos K, Gascon JA, McEvoy JP, Brudvig GW, Batista VS (2008e) QM/MM computational studies of substrate water binding to the oxygen evolving complex of Photosystem II. Phil Trans R Soc Lond B 363: 1149-1156.
71. 3CN (Phen = 1, 10-Phenanthroline): crystal-structure analyses at 100-K, interpretation of disorder, and optical, magnetic, and electrochemical results. Inorg Chem 25: 4743-4750.
72. Stern EA (1974) Theory of extended X-ray-absorption fine-structure. Phys Rev B 10: 3027-3037.
73. Thorp HH, Brudvig GW (1991) The physical inorganic-chemistry of manganese relevant to photosynthetic oxygen evolution. New J Chem 15: 479-490.
74. Tsutsui Y, Wasada H, Funahashi S (1999) Reaction mechanism of water exchange on di- and trivalent cations of the first transition series and structural stability of seven-coordinate species. J Mol Struct THEOCHEM 462: 379-390.
75. Versluis L, Ziegler T (1988) The determination of molecular-structures by density functional theory: the evaluation of analytical energy gradients by numerical-integration. J Chem Phys 88: 322-328.
76. Vreven T, Morokuma K (2000a) On the application of the IMOMO (integrated molecular orbital plus molecular orbital) method. J Comput Chem 21: 1419-1432.
77. Vreven T, Morokuma K (2000b) The ONIOM (our own N-layered integrated molecular orbital plus molecular mechanics) method for the first singlet excited (S-1) state photoisomerization path of a retinal protonated Schiff base. J Chem Phys 113: 2969-2975.
78. Warshel A, Levitt M (1976) Theoretical studies of enzymic reactions: dielectric, electrostatic and steric stabilization of carbonium-ion in reaction of lysozyme. J Mol Biol 103: 227-249.
79. Yachandra VK (2002) Structure of the manganese complex in photosystem II: insights from X-ray spectroscopy. Phil Trans R Soc Lond Ser B 357: 1347-1357.
80. Yachandra VK, Sauer K, Klein MP (1996) Manganese cluster in photosynthesis: where plants oxidize water to dioxygen. Chem Rev 96: 2927-2950.
81. 4Ca cluster. J Am Chem Soc 127: 14974-14975.
82. 4Ca cluster. Science 314: 821-825.
83. 4Ca catalyst from X-ray spectroscopy. Phil Trans R Soc Lond B 363: 1139-1147.