Density functional theory calculations of redox properties of iron-sulphur protein analogues

Molecular Simulation

Volumn 37, Issue 7, 2011, Pages 572-590

  Niu, Shuqiang ^a   Ichiye, Toshiko ^a,b  

^a GEORGETOWN UNIVERSITY   (United States)

^b NATIONAL HEART LUNG AND BLOOD INSTITUTE   (United States)

Author keywords

density functional theory; inner sphere free energy; iron sulphur protein; reduction potential; reorganisation energy

Indexed keywords

BASIS SETS; DENSITY FUNCTIONAL THEORY CALCULATIONS; DETACHMENT ENERGY; DIFFUSE FUNCTIONS; ELECTRON DETACHMENT ENERGIES; GASPHASE; INDIVIDUAL FACTORS; INNER-SPHERE FREE ENERGY; IRON-SULPHUR PROTEIN; REDOX PROPERTY; REDOX SITES; REDUCTION POTENTIAL; REORGANISATION;

ELECTROSPRAY IONIZATION; EXPERIMENTS; IRON; PHOTOELECTRON SPECTROSCOPY; PHOTOIONIZATION; PROTEINS; SPHERES; SULFUR;

DENSITY FUNCTIONAL THEORY;

EID: 79959280662     PISSN: 08927022     EISSN: 10290435     Source Type: Journal    
DOI: 10.1080/08927022.2011.582111     Document Type: Article

References (116)

1. H. B. Gray and J. R. Winkler, Electron transfer in proteins, Annu. Rev. Biochem. 65(1996), pp. 537-561. (Pubitemid 26250619)
2. T. Ichiye, Computational studies of redox potentials of electron transfer proteins, in Simulation and Theory of Electrostatic Interactions in Solution, L. R. Pratt, and G. Hummer, eds., AIP, Santa Fe, NM, 1999, pp. 431-450.
3. T. Ichiye, Simulations of electron transfer proteins, in Computational Biochemistry and Biophysics, O. M. Becker, A. D., MacKerell, Jr, B. Roux, and M. Watanabe, eds., Marcel Dekker, Inc, New York, NY, 2001, pp. 393-415.
4. H. Beinert, R. H. Holm, and E. Münck, Iron-sulfur clusters: Nature's modular, multipurpose structures, Science 277(1997), pp. 263-659.
5. H. Beinert, Iron-sulfur proteins: Ancient structure, still full of surprises, J. Biol. Inorg. Chem. 5(2000), pp. 2-15. (Pubitemid 30120582)
6. P. V. Rao and R. H. Holm, Synthetic analogues of the active sites of iron-sulfur proteins, Chem. Rev. 104(2004), pp. 527-559.
7. R. A. Marcus and N. Sutin, Electron transfer in chemistry and biology, Biochim. Biophys. Acta. 811(1985), pp. 265-322.
8. H. Reiss and A. Heller, The absolute potential of the standard hydrogen electrode: A new estimate, J. Phys. Chem. 89(1985), pp. 4207-4213.
9. R. A. Bair and W. A. Goddard, Theoretical studies of oxidized and reduced states of a model for active-site of rubredoxin, J. Am. Chem. Soc. 99(1977), pp. 3505-3507.
10. R. A. Bair and W. A. Goddard, theoretical studies of ground and excited-states of a model of active-site in oxidized and reduced rubredoxin, J. Am. Chem. Soc. 100(1978), pp. 5669-5676.
11. J. M. Mouesca, J. L. Chen, L. Noodleman, D. Bashford, and D. A. Case, Density-functional Poisson-Boltzmann calculations of redox potentials for iron-sulfur clusters, J. Am. Chem. Soc. 116(1994), pp. 11898-11914.
12. 1-, 2-, J. Phys. Chem. B 101(1997), pp. 3633-3643. (Pubitemid 127611920)
13. 2- with water: An ab initio quantum chemistry study, J. Phys. Chem. B 104(2000), pp. 2424-2431.
14. E. Sigfridsson, M. H. M. Olsson, and U. Ryde, Inner-sphere reorganization energy of iron-sulfur clusters studied with theoretical methods, Inorg. Chem. 40(2001), pp. 2509-2519. (Pubitemid 32880557)
15. P. J. Stephens, D. R. Jollie, and A. Warshel, Protein control of redox potentials of iron-sulfur proteins, Chem. Rev. 96(1996), pp. 2491-2513. (Pubitemid 126641110)
16. M. R. Gunner, A. Nicholls, and B. Honig, Electrostatic potentials in Rhodopseudomonas viridis reaction centers: Implications for the driving force and directionality of electron transfer, J. Phys. Chem. 100(1996), pp. 4277-4291. (Pubitemid 126793370)
17. P. D. Swartz, B. W. Beck, and T. Ichiye, Structural origins of redox potentials in iron-sulfur proteins: Electrostatic potentials of crystal structures, Biophys. J. 71(1996), pp. 2958-2969. (Pubitemid 26422340)
18. B. W. Beck, Q. Xie, and T. Ichiye, Sequence determination of reduction potentials by cysteinyl hydrogen bonds and peptide dipoles in [4Fe-4S] ferredoxins, Biophys. J. 81(2001), pp. 601-603.
19. A. Warshel and M. Levitt, Theoretical studies of enzymic reactions - dielectric, electrostatic and steric stabilization of carbonium-ion in reaction of lysozyme, J. Mol. Biol. 103(1976), pp. 227-249.
20. J. L. Gao, and M. A. Thompson (eds.), Combined Quantum Mechanical and Molecular Mechanical Methods, Vol. 712, American Chemical Society, Washington, DC, 1998.
21. J. L. Gao and D. G. Truhlar, Quantum mechanical methods for enzyme kinetics, Annu. Rev. Phys. Chem. 53(2002), pp. 467-505.
22. 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), pp. 6654-6659. (Pubitemid 40675372)
23. M. Sundararajan, I. H. Hillier, and N. A. Burton, Structure and redox properties of the protein, rubredoxin, and its ligand and metal mutants studied by electronic structure calculation, J. Phys. Chem. A 110(2006), pp. 785-790. (Pubitemid 43168254)
24. M. Sulpizi, S. Raugei, J. Van de Vondele, P. Carloni, and M. Sprik, Calculation of redox properties: Understanding short-and longrange effects in rubredoxin, J. Phys. Chem. B 111(2007), pp. 3969-3976. (Pubitemid 46693358)
25. R. G. Parr and W. Yang, Density-functional Theory of Atoms and Molecules, Oxford University Press, Oxford, 1989.
26. M. K. Gilson, K. A. Sharp, and B. H. Honig, Calculating the electrostatic potential of molecules in solution - method and error assessment, J. Comput. Chem. 9(1988), pp. 327-335.
27. B. Honig and A. Nicholls, Classical electrostatics in biology and chemistry, Science 268(1995), pp. 1144-1149.
28. R. A. Torres, T. Lovell, L. Noodleman, and D. A. Case, Density functional and reduction potential calculations of Fe4S4 clusters, J. Am. Chem. Soc. 125(2003), pp. 1923-1936. (Pubitemid 36236149)
29. B. S. Perrin and T. Ichiye, Fold versus sequence effects on the driving force for protein-mediated electron transfer, Proteins Struct. Funct. Bioinf. 78(2010), pp. 2798-2808.
30. E. Lewars, Computational Chemistry: Introduction to the Theory and Applications of Molecular and Quantum Mechanics, Kluwer Academic, Boston, MA, 2003.
31. S. Q. Niu and M. B. Hall, Theoretical studies on reactions of transition-metal complexes, Chem. Rev. 100(2000), pp. 353-405.
32. A. J. Cohen, P. Mori-Sanchez, and W. T. Yang, Insights into current limitations of density functional theory, Science 321(2008), pp. 792-794.
33. Y. Zhao and D. G. Truhlar, Density functionals with broad applicabilityinchemistry, Acc. Chem. Res. 41(2008), pp. 157-167.
34. S. Q. Niu, X. B. Wang, J. A. Nichols, L. S. Wang, and T. Ichiye, Combined quantum chemistry and photoelectron spectroscopy study of the electronic structure and reduction potentials of rubredoxin redox site analogues, J. Phys. Chem. A 107(2003), pp. 2898-2907.
35. S. Q. Niu, J. A. Nichols, and T. Ichiye, Optimization of spinunrestricted density functional theory for redox properties of rubredoxin redox site analogues, J. Chem. Theory Comput. 5(2009), pp. 1361-1368.
36. X. B. Wang, S. Q. Niu, X. Yang, S. K. Ibrahim, C. J. Pickett, T. Ichiye, and L. S. Wang, Probing the intrinsic electronic structure of the cubane [4Fe-4S] cluster: Nature's favorite cluster for electron transfer and storage, J. Am. Chem. Soc. 125(2003), pp. 14072-14081. (Pubitemid 37424013)
37. X. Yang, X. B. Wang, S. Q. Niu, C. J. Pickett, T. Ichiye, and L. S. Wang, Coulomb-and antiferromagnetic-induced fission in doubly charged cubelike Fe-S clusters, Phys. Rev. Lett. 89(2002), pp. 163401-163401.
38. X. Yang, S. Q. Niu, T. Ichiye, and L. S. Wang, Direct measurement of the hydrogen-bonding effect on the intrinsic redox potentials of [4Fe-4S] cubane complexes, J. Am. Chem. Soc. 126(2004), pp. 15790-15794. (Pubitemid 39610513)
39. + clusters with tri-and tetracoordinate iron sites, Inorg. Chem. 44(2005), pp. 1202-1204. (Pubitemid 40333444)
40. X. B. Wang and L. S. Wang, Probing the electronic structure of redox species and direct determination of intrinsic reorganization energies of electron transfer reactions, J. Chem. Phys. 112(2000), pp. 6959-6962.
41. X. Yang, X. B. Wang, Y. J. Fu, and L. S. Wang, On the electronic structure of [1Fe] Fe-S complexes from anionic photoelectron spectroscopy, J. Phys. Chem. A 107(2003), pp. 1703-1709.
42. 2+ cubane clusters, Inorg. Chem. 43(2004), pp. 3647-3655.
43. n- complexes, J. Am. Chem. Soc. 126(2004), pp. 8413-8420. (Pubitemid 38917963)
44. S. Q. Niu and T. Ichiye, Probing ligand effects on the redox energies of [4Fe-4S] clusters using broken-symmetry density functional theory, J. Phys. Chem. A 113(2009), pp. 5671-5676.
45. E. I. Solomon, B. Hedman, K. O. Hodgson, A. Dey, and R. K. Szilagyi, Ligand K-edge X-ray absorption spectroscopy: covalency of ligand-metal bonds, Coord. Chem. Rev. 249(2005), pp. 97-129. (Pubitemid 40023314)
46. S. Q. Niu, X. B. Wang, X. Yang, L. S. Wang, and T. Ichiye, Mechanistic insight into the symmetric fission of [4Fe-4S] analogue complexes and implications for cluster conversions in iron-sulfur proteins, J. Phys. Chem. A 108(2004), pp. 6750-6757.
47. + clusters, a broken-symmetry density functional theory study, Theor. Chem. Acc. 117(2007), pp. 275-281.
48. S. Q. Niu and T. Ichiye, Cleavage of [4Fe-4S]-type clusters: Breaking the symmetry, J. Phys. Chem. A 113(2009), pp. 5710-5717.
49. S. Q. Niu and T. Ichiye, Insight into environmental effects on bonding and redox properties of [4Fe-4S] clusters in proteins, J. Am. Chem. Soc. 131(2009), pp. 5724-5725.
50. C. J. Cramer, Essentials of Computational Chemistry: Theories and Models, 2nd ed., Wiley, New York, 2004.
51. E. R. Davidson and A. A. Jarzecki, Zero point corrections to vertical excitation energies, Chem. Phys. Lett. 285(1998), pp. 155-159. (Pubitemid 128180259)
52. Y. Luo, S. Q. Niu, and T. Ichiye, Density Functional Theory Study of Rubredoxin Redox Site Analogues, Unpublished work.
53. R. S. Mulliken, Electronic population analysis on LCAO MO molecular wave functions. I, J. Chem. Phys. 23(1955), pp. 1833-1840.
54. A. E. Reed, L. A. Curtiss, and F. Weinhold, Intermolecular interactions from a natural bond orbital, donor-acceptor viewpoint, Chem. Rev. 88(1988), pp. 899-926.
55. E. I. Solomon, R. K. Szilagyi, S. D. George, and L. Basumallick, Electronic structures of metal sites in proteins and models: Contributions to function in blue copper proteins, Chem. Rev. 104(2004), pp. 419-458.
56. J.-M. Mouesca, L. Noodleman, D. A. Case, and B. Lamotte, Spin densities and spin coupling in iron-sulfur clusters, Inorg. Chem. 34(1995), p. 4347.
57. L. Noodleman and D. A. Case, Density-functional theory of spin polarization and spin coupling in iron-sulfur clusters, in Advances in Inorganic Chemistry, R. Cammack, ed., Academic Press, San Diego, CA, 1992, pp. 423-470.
58. L. Noodleman, C. Y. Peng, D. A. Case, and J. M. Mouesca, Orbital interactions, electron delocalization and spin coupling in iron-sulfur clusters, Coord. Chem. Rev. 144(1995), pp. 199-244. (Pubitemid 126000788)
59. M. Shoji, K. Koizumi, Y. Kitagawa, S. Yamanaka, T. Kawakami, M. Okumura, and K. Yamaguchi, Theory of chemical bonds in metalloenzymes II: Hybrid-DFT studies in iron-sulfur clusters, Int. J. Quantum Chem. 105(2005), pp. 628-644. (Pubitemid 43082100)
60. M. Shoji, K. Koizumi, T. Taniguchi, Y. Kitagawa, S. Yamanaka, M. Okumura, and K. Yamaguchi, Theory of chemical bonds in metalloenzymes III: Full geometry optimization and vibration analysis of ferredoxin-type [2Fe-2S] cluster, Int. J. Quantum Chem. 107(2007), pp. 116-133. (Pubitemid 44831375)
61. S. E. Shadle, B. Hedman, K. O. Hodgson, and E. I. Solomon, Ligand K-edge X-ray-absorption spectroscopic studies - metalligand covalency in a series of transition-metal tetrachlorides, J. Am. Chem. Soc. 117(1995), pp. 2259-2272.
62. J. M. Mouesca and B. Lamotte, Iron-sulfur clusters and their electronic and magnetic properties, Coord. Chem. Rev. 178(1998), pp. 1573-1614. (Pubitemid 128452093)
63. A. J. Cohen and N. C. Handy, Assessment of exchange correlation functionals, Chem. Phys. Lett. 316(2000), pp. 160-166.
64. A. D. Becke, Density-functional thermochemistry. 3. The role of exact exchange, J. Chem. Phys. 98(1993), pp. 5648-5652.
65. A. D. Becke, Density-functional exchange-energy approximation with correct asymptotic behavior, Phys. Rev. A38(1988), pp. 3098-3100.
66. C. Lee, W. Yang, and R. G. Parr, Development of the Colle-Salvetti correlation-energy formula into a functional of the electron density, Phys. Rev. B37(1988), pp. 785-789.
67. A. D. Becke, A new mixing of Hartree-Fock and local densityfunctional theories, J. Chem. Phys. 98(1993), pp. 1372-1377.
68. J. P. Perdew and Y. Wang, Accurate and simple analytic representation of the electron-gas correlation-energy, Phys. Rev. B 45(1992), pp. 13244-13249.
69. A. D. Becke, Density-functional thermochemistry. 5. Systematic optimization of exchange-correlation functionals, J. Chem. Phys. 107(1997), pp. 8554-8560. (Pubitemid 127611634)
70. W. J. Stevens, H. Basch, and M. Krauss, Compact effective potentials and efficient shared-exponent basis sets for the firstand second-row atoms, J. Chem. Phys. 81(1984), pp. 6026-6033.
71. P. J. Hay and W. R. Wadt, Ab initio effective core potentials for molecular calculations. Potentials for K to Au including the outermost core orbitals, J. Chem. Phys. 82(1985), pp. 299-310.
72. P. J. Hay and W. R. Wadt, Ab initio effective core potentials for molecular calculations. Potentials for the transition metal atoms Sc to Hg, J. Chem. Phys. 82(1985), p. 284.
73. M. Couty and M. B. Hall, Basis sets for transition metals: Optimized outer p functions, J. Comput. Chem. 17(1996), pp. 1359-1370. (Pubitemid 126576753)
74. W. J. Hehre, L. Radom, P.v. R. Schleyer, and J. A. Pople, Ab initio molecular orbital theory, Wiley, New York, 1986.
75. P. C. Hariharan and J. A. Pople, The influence of polarization functions on molecular orbital hydrogenation energies, Theor. Chim. Acta 28(1973), pp. 213-222.
76. M. M. Francl, W. J. Petro, W. J. Hehre, J. S. Binkley, M. S. Gordon, D. J. DeFrees, and J. A. Pople, Self-consistent molecular orbital methods. XXIII. A polarization-type basis set for second-row elements, J. Chem. Phys. 77(1982), pp. 3654-3665.
77. * basis set for atoms K through Zn, J. Chem. Phys. 109(1998), pp. 1223-1229. (Pubitemid 128678537)
78. N. Godbout, D. R. Salahub, J. Andzelm, and E. Wimmer, Optimization of Gaussian-type basis sets for local spin density functional calculations. Part I. Boron through neon, optimization technique and validation, Can. J. Chem. 70(1992), pp. 560-571.
79. R. W. Lane, J. A. Ibers, R. B. Frankel, G. C. Papaefthymiou, and R. H. Holm, Synthetic analogues of the active sites of iron-sulfur proteins. 14. Synthesis, properties, and structures of bis (o-xylyl-α, α′-dithiolato) ferrate (II, III) anions, analogues of oxidized and reduced rubredoxin sites, J. Am. Chem. Soc. 99(1977), pp. 84-98.
80. 4] center in oxidized rubredoxin, Inorg. Chem. 31(1992), pp. 4594-4600.
81. 2-), J. Am. Chem. Soc. 113(1991), pp. 3819-3828.
82. 2) and Mossbauer-Spectra of 2-coordinate and 3-coordinate complexes, Inorg. Chem. 34(1995), pp. 1815-1822.
83. T. Clark, GW. Spitznagel, J. Chandrasekhar, and P.v. R. Schleyer, Efficient diffuse function-augmented basis sets for anion calculations. III. The 3-21 + G basis set for first-row elements, Li-F, J. Comp. Chem. 4(1983), pp. 294-301.
84. 4-, J. Am. Chem. Soc. 97(1975), pp. 3833-3835.
85. - - an unusual electronic-structure for high-spin D5 complexes, J. Am. Chem. Soc. 112(1990), pp. 2231-2242.
86. M. Belinskii, Heisenberg-model for tetrameric iron clusters in highpotential iron-sulfur proteins. 1. Exchange states, G-factors, hyperfine interactions, Chem. Phys. 176(1993), pp. 15-36.
87. M. Belinskii, Heisenberg-model for tetrameric iron clusters in high-potential iron-sulfur proteins. 2. Double exchange in distorted cluster, Chem. Phys. 176(1993), pp. 37-45.
88. 3+ cluster, J. Am. Chem. Soc. 111(1989), pp. 2464-2469.
89. L. Lepape, B. Lamotte, J. M. Mouesca, and G. Rius, Paramagnetic states of four iron four sulfur clusters. 2. Proton ENDOR study of a 1 + state in an asymmetrical cluster, J. Am. Chem. Soc. 119(1997), pp. 9771-9781. (Pubitemid 27466844)
90. J. J. Girerd, Electron-transfer between magnetic ions in mixedvalence binuclear systems, J. Chem. Phys. 79(1983), pp. 1766-1775.
91. 0 cores in proteins and models, J. Am. Chem. Soc. 115(1993), pp. 5155-5168.
92. 2+ clusters: Effects of H-bonding and structural distortion on covalency and spin topology, Inorg. Chem. 44(2005), pp. 8349-8354. (Pubitemid 41712934)
93. R. K. Szilagyi and MA. Winslow, On the accuracy of density functional theory for iron-sulfur clusters, J. Comput. Chem. 27(2006), pp. 1385-1397. (Pubitemid 44230427)
94. 3 (M=Mn, Fe, Co, Ni, X=Cl, Br), using photoelectron spectroscopy and density functional calculations, J. Chem. Phys. 119(2003), pp. 8311-8320.
95. M. Reiher, O. Salomon, and BA. Hess, Reparameterization of hybrid functionals based on energy differences of states of different multiplicity, Theor. Chem. Acc. 107(2001), pp. 48-55. (Pubitemid 33576519)
96. J. Li, Calculation of iron-sulfur clusters in FeS protein active sites by broken symmetry density functional method, Acta Chim. Sin. 58(2000), pp. 1529-1533.
97. C. M. Breneman and K. B. Wiberg, Determining atom-centered monopoles from molecular electrostatic potentials. The need for high sampling density in formamide conformational analysis, J. Comput. Chem. 11(1990), pp. 361-373.
98. A. D. MacKerell, Jr, D. Bashford, M. Bellot, R. L. Dunbrack, Jr, M. J. Field, S. Fischer, J. Gao, H. Guo, S. Ha, D. Joseph, K. Kuchnir, K. Kuczera, F. T. K. Lau, M. Mattos, S. Michnick, D. T. Nguyen, T. Ngo, B. Prodhom, B. Roux, M. Schlenkrich, J. Smith, R. Stote, J. Straub, J. Wiorkiewicz-Kuczera, and M. Karplus, All-atom empirical potential for molecular modeling and dynamics studies of proteins, J. Phys. Chem. B 102(1998), pp. 3586-3616. (Pubitemid 128576688)
99. A. Warshel and W. W. Parson, Computer simulations of electrontransfer reactions in solution and in photosynthetic reaction centers, Annu. Rev. Phys. Chem. 42(1991), pp. 279-309.
100. B. T. Miller, R. P. Singh, J. B. Klauda, M. Hodoscek, B. R. Brooks, and H. L. Woodcock, CHARMMing: A new, flexible web portal for CHARMM, J. Chem. Inf. Model. 48(2008), pp. 1920-1929.
101. B. R. Brooks, R. E. Bruccoleri, B. D. Olafson, D. J. States, S. Swaminathan, and M. Karplus, CHARMM: A program for macromolecular energy, minimization, and dynamics calculations, J. Comput. Chem. 4(1983), pp. 187-217.
102. Y. Luo, C. E. Ergenekan, J. T. Fischer, M. L. Tan, and T. Ichiye, The molecular determinants of the increased reduction potential of the rubredoxin domain of rubrerythrin relative to rubredoxin, Biophys. J. 98(2010), pp. 560-568.
103. R. B. Yelle, N. S. Park, and T. Ichiye, Molecular-dynamics simulations of rubredoxin from Clostridium pasteurianum - changes in structure and electrostatic potential during redox reactions, Proteins Struct. Funct. Genet. 22(1995), pp. 154-167.
104. P. D. Swartz and T. Ichiye, Temperature dependence of the redox potential of rubredoxin from Pyrococcus furiosus: A molecular dynamics study, Biochem. 35(1996), pp. 13772-13779. (Pubitemid 26363920)
105. T. Min, C. E. Ergenekan, M. K. Eidsness, T. Ichiye, and C. Kang, Leucine 41 is a gate for water entry in the reduction of Clostridium pasteurianum rubredoxin, Protein Sci. 1(2001), pp. 463-676.
106. S. Q. Niu, T. Ichiye, Y. J. Fu, X. Yang, and L. S. Wang, Electronic and electrostatic effects on the electronic structure and intrinsic reduction potential of the [4Fe-4S] cluster in ferredoxin and HiPIP, Abstr. Pap. Am. Chem. Soc. 230(2005), pp. U2156-U2157.
107. T. A. Link, The structures of Rieske and Rieske-type proteins, in Iron-sulfur proteins, A. G. Sykes, and R. Cammack, eds., Academic Press, Inc., San Diego, CA, 1999, pp. 83-157.
108. 2+ cluster in ferredoxin and HiPIP, J. Am. Chem. Soc. 123(2001), pp. 4859-4860. (Pubitemid 32895793)
109. A. Dey, E. J. Francis, M. W. W. Adams, E. Babini, Y. Takahashi, K. Fukuyama, K. O. Hodgson, B. Hedman, and E. I. Solomon, Solvent tuning of electrochemical potentials in the active sites of HiPIP versus ferredoxin, Science 318(2007), pp. 1464-1468. (Pubitemid 350208960)
110. H. B. Gray, B. G. Malmstrom, and R. J. P. Williams, Copper coordination in blue proteins, J. Biol. Inorg. Chem. 5(2000), pp. 551-559.
111. M. C. Machczynski, H. B. Gray, and J. H. Richards, An outer-sphere hydrogen-bond network constrains copper coordination in blue proteins, J. Inorg. Biochem. 88(2002), pp. 375-380. (Pubitemid 34207850)
112. R. Cammack, Iron-sulfur cluster in enzymes: Themes and variations, Adv. Inorg. Chem. 38(1992), pp. 281-322.
113. - S hydrogen bonds in Peptococcus aerogenes ferredoxin, Clostridium pasteurianum rubredoxin and Chromatium high potential iron protein, Proc. Natl Acad. Sci. USA 72(1975), pp. 4854-4858.
114. 4 clusters in ferredoxins and high-potential iron proteins. New information from X-ray crystallography and resonance Raman spectroscopy, J. Am. Chem. Soc. 113(1991), pp. 2055-2064.
115. D. C. Johnson, D. R. Dean, A. D. Smith, and M. K. Johnson, Structure, function, and formation of biological iron-sulfur clusters, Annu. Rev. Biochem. 74(2005), pp. 247-281. (Pubitemid 40995508)
116. 2-/1- (x=0-4), Int. J. Mass. Spectrom. 255(2006), pp. 102-110.