Simulation of multihaem cytochromes

FEBS Letters

Volumn 586, Issue 5, 2012, Pages 510-518

  Soares, Cláudio M ^a   Baptista, António M ^a  

^a INSTITUTO DE TECNOLOGIA QUÍMICA E BIOLÓGICA   (Portugal)

Author keywords

Continuum electrostatics; Electron transfer; Electron proton coupling; Molecular dynamics simulations; Monte Carlo; Proton transfer; Redox Bohr effect

Indexed keywords

CYTOCHROME; CYTOCHROME C3; PROTON;

CONFORMATIONAL TRANSITION; DESULFOVIBRIO DESULFURICANS; DESULFOVIBRIO GIGAS; DESULFOVIBRIO VULGARIS; ELECTRON; ISOMERISM; MOLECULAR DYNAMICS; NONHUMAN; OXIDATION REDUCTION POTENTIAL; PH; PRIORITY JOURNAL; PROTEIN CONFORMATION; PROTEIN STRUCTURE; PROTON TRANSPORT; REVIEW; SIMULATION; SOLVATION; THERMODYNAMICS;

BACTERIAL PROTEINS; CYTOCHROMES; HEME; MODELS, MOLECULAR; MOLECULAR DYNAMICS SIMULATION; OXIDATION-REDUCTION; PROTEIN CONFORMATION; SOLVENTS; STATIC ELECTRICITY; THERMODYNAMICS;

EID: 84857916893     PISSN: 00145793     EISSN: 18733468     Source Type: Journal    
DOI: 10.1016/j.febslet.2011.10.019     Document Type: Review

References (92)

1. 3 Eur. J. Biochem. 141 1984 283 296
2. 3 from Desulfovibrio gigas Eur. J. Biochem. 202 1991 1101 1106
3. 3 Eur. J. Biochem. 202 1991 1107 1113
4. 3 from Desulfovibrio vulgaris BBA 1187 1994 232 235 (Pubitemid 24267061)
5. 3 by 2D-NMR FEBS Lett. 314 1992 155 158
6. 3 from Desulfovibrio vulgaris: a model for energy transduction mechanisms JBIC 1 1996 34 38 (Pubitemid 126489979)
7. 3 from Desulfovibrio vulgaris Eur. J. Biochem. 241 1996 723 731 (Pubitemid 26379372)
8. 3 from Desulfomicrobium baculatum. Identification of the low-potential heme Eur. J. Biochem. 230 1995 1007 1013
9. 3 J. Biol. Inorg. Chem. 1 1996 542 550 (Pubitemid 126490066)
10. 3 coupled to hydrogenase works as a 'proton thruster' in Desulfovibrio vulgaris JBIC 2 1997 488 491 (Pubitemid 27375239)
11. 3 JBIC 2 1997 343 349 (Pubitemid 27287444)
12. 3 of Desulfovibrio vulgaris (Hildenborough) Biochemistry 37 1998 12160 12165 (Pubitemid 28411300)
13. 3: structural basis for functional cooperativity J. Mol. Biol. 281 1998 719 739 (Pubitemid 28383142)
14. 1H-NMR FEBS Lett. 390 1996 59 62 (Pubitemid 26233267)
15. 3 from Desulfovibrio gigas: solution structures of the oxidised and reduced states J. Mol. Biol. 298 2000 61 82
16. 3 from Desulfovibrio gigas: thermodynamics of a "proton thruster" Biochemistry 37 1998 15808 15815 (Pubitemid 28524752)
17. 3 from Desulfovibrio vulgaris Hildenborough ChemBioChem 2 2001 895 905 (Pubitemid 33722703)
18. 3: the importance of mechano-chemical coupling for energy transduction ChemBioChem. 2 2001 831 837 (Pubitemid 33722675)
19. A.V. Xavier A mechano-chemical model for energy transduction in cytochrome c oxidase: the work of a Maxwell's god FEBS Lett. 532 2002 261 266 (Pubitemid 35441358)
20. 3 from Desulfovibrio vulgaris Eur. J. Biochem. 244 1997 721 734 (Pubitemid 27130507)
21. T. Yagi, M. Honya, and N. Tamiya Purification and properties of hydrogenases of different origins BBA 153 1968 699 705
22. P.M. Matias, I.A. Pereira, C.M. Soares, and M.A. Carrondo Sulphate respiration from hydrogen in Desulfovibrio bacteria: a structural biology overview Prog. Biophys. Mol. Biol. 89 2005 292 329 (Pubitemid 40801818)
23. I.A.C. Pereira, A.R. Ramos, F. Grein, M.C. Marques, S.M. Silva, and S.S. Venceslau A comparative genomic analysis of energy metabolism in sulfate reducing bacteria and archaea Front. Microbiol. 2 2011 69
24. J. Warwicker, and H.C. Watson Calculation of the electric potential in the active site cleft due to alpha-helix dipoles J. Mol. Biol. 157 1982 671 679
25. D. Bashford, and M. Karplus PKa's of ionizable groups in proteins: atomic detail from a continuum electrostatic model Biochemistry 29 1990 10219 10225 (Pubitemid 20384527)
26. A.-S. Yang, M.R. Gunner, R. Sampogna, K. Sharp, and B. Honig On the calculation of pKás in proteins Proteins 15 1993 252 265
27. T. Simonson Macromolecular electrostatics: continuum models and their growing pains Curr. Opin. Struct. Biol. 11 2001 243 252 (Pubitemid 32289429)
28. D. Bashford Macroscopic electrostatic models for protonation states in proteins Front. Biosci. 9 2004 1082 1099 (Pubitemid 39060831)
29. J. Antosiewicz, and D. Porschke The nature of protein dipole moments: experimental and calculated permanent dipole of alpha-chymotrypsin Biochemistry 28 1989 10072 10078 (Pubitemid 20033695)
30. P. Beroza, D.R. Fredkin, M.Y. Okamura, and G. Feher Protonation of interacting residues in a protein by a Monte Carlo method: application to lysozyme and the photosynthetic reaction center of Rhodobacter sphaeroides Proc. Natl. Acad. Sci. USA 88 1991 5804 5808 (Pubitemid 21914834)
31. M. Schaefer, M. Sommer, and M. Karplus PH-dependence of protein stability: absolute electrostatic free energy differences between conformations† J. Phys. Chem. B 101 1997 1663 1683 (Pubitemid 127628043)
32. 3 from Desulfovibrio vulgaris Hildenborough JBIC 2 1997 714 727 (Pubitemid 28030880)
33. S. Papa, F. Guerrieri, and G. Izzo Redox Bohr-effects in the cytochrome system of mitochondria FEBS Lett. 105 1979 213 216
34. A.V. Xavier In Frontiers in Bioinorganic Chemistry (Xavier, A.V., ed.) 1985 VCH Publishers Weinheim
35. 3 from Desulfovibrio species using continuum electrostatic methods JBIC 4 1999 73 86 (Pubitemid 29113815)
36. K. Mizuguchi, C.M. Deane, T.L. Blundell, and J.P. Overington HOMSTRAD: a database of protein structure alignments for homologous families Protein Sci. 7 1998 2469 2471 (Pubitemid 28506965)
37. G. Vriend WHAT IF - A molecular modeling and drug design program J. Mol. Graph. 8 1990 52 56 (Pubitemid 20717037)
38. D. Bashford, M. Karplus, and G.W. Canters Electrostatic effects of charge perturbations introduced by metal oxidation in proteins J. Mol. Biol. 203 1988 507 510
39. M.R. Gunner, and B. Honig Electrostatic control of midpoint potentials in the cytochrome subunit of the Rhodopseudomonas viridis reaction center Proc. Natl. Acad. Sci. USA 88 1991 9151 9155 (Pubitemid 21915587)
40. C.N. Schutz, and A. Warshel What are the dielectric "constants" of proteins and how to validate electrostatic models? Proteins 44 2001 400 417 (Pubitemid 32768578)
41. J. Antosiewicz, J.A. McCammon, and M.K. Gilson Prediction of pH-dependent properties of proteins J. Mol. Biol. 238 1994 415 436 (Pubitemid 24154721)
42. T. Simonson, and C.L. Brooks III Charge screening and the dielectric constant of proteins: insights from molecular dynamics J. Am. Chem. Soc. 118 1996 8452 8458 (Pubitemid 26305268)
43. 3 using continuum electrostatics Biophys. J. 76 1999 2978 2998 (Pubitemid 29269447)
44. 3 J. Phys. Chem. B 104 2000 6293 6301
45. E.G. Alexov, and M.R. Gunner Incorporating protein conformational flexibility into the calculation of pH-dependent protein properties Biophys. J. 72 1997 2075 2093 (Pubitemid 27184435)
46. A.M. Baptista, and C.M. Soares Some theoretical and computational aspects of the inclusion of proton isomerism in the protonation equilibrium of proteins J. Phys. Chem. B 105 2001 293 309
47. V.H. Teixeira, C.M. Soares, and A.M. Baptista Studies of the reduction and protonation behaviour of tetrahaem cytochromes using atomic detail JBIC 7 2002 200 216 (Pubitemid 41490233)
48. Z. Zheng, and A.R. Gunner Analysis of the electrochemistry of hemes with E(m)s spanning 800 mV Proteins-Struct. Funct. Bioinformat. 75 2008 719 734
49. 3 from Desulfovibrio desulfuricans ATCC 27774: crystallographic and modelling studies of oxidised and reduced high resolution structures at pH 7.6 Proteins 54 2004 135 152 (Pubitemid 38036921)
50. I. Bento, V.H. Teixeira, A.M. Baptista, C.M. Soares, P.M. Matias, and M.A. Carrondo Redox-Bohr and other cooperativity effects in the nine heme cytochrome c from Desulfovibrio desulfuricans ATCC 27774: crystallographic and modeling studies J. Biol. Chem. 278 2003 36455 36469 (Pubitemid 37139975)
51. B.M. Fonseca, I.H. Saraiva, C.M. Paquete, C.M. Soares, I. Pacheco, C.A. Salgueiro, and R.O. Louro The tetraheme cytochrome from Shewanella oneidensis MR-1 shows thermodynamic bias for functional specificity of the hemes J. Biol. Inorg. Chem. 14 2009 375 385
52. D.M. Popovic, S.D. Zaric, B. Rabenstein, and E.-W. Knapp Artificial cytochrome b: computer modeling and evaluation of redox potentials J. Am. Chem. Soc. 123 2001 6040 6053 (Pubitemid 32888472)
53. R.O. Louro Conformational component in the coupled transfer of multiple electrons and protons in a monomeric tetraheme cytochrome J. Biol. Chem. 276 2001 44044 44051 (Pubitemid 37383975)
54. C.I. Bayly, P. Cieplak, W.D. Cornell, and P.A. Kollman A well-behaved electrostatic potential based method using charge restraints for deriving atomic charges: the RESP model J. Phys. Chem. 97 1993 10269 10280
55. 3. Studying the reduction processes using free energy calculations Biophys. J. 74 1998 1708 1721 (Pubitemid 28157910)
56. W.F. van Gunsteren, and H.J.C. Berendsen Groningen molecular simulation (GROMOS) library manual, Biomos B.V, Nijenborgh 16, 9747 1987 AG Groningen The Netherlands
57. L.J. Smith, A.E. Mark, C.M. Dobson, and W.F. van Gunsteren Comparison of MD simulations and NMR experiments for hen lysozyme: analysis of local fluctuations, cooperative motions and global changes Biochemistry 34 1995 10918 10931
58. P. Kollman Free energy calculations: applications to chemical and biochemical phenomena Chem. Rev. 93 1993 2395 2417
59. 3 in oxidized and reduced forms Biophys. J. 83 2002 3049 3065 (Pubitemid 36041928)
60. W.R.P. Scott The GROMOS biomolecular simulation program package J. Phys. Chem. 103 1999 3596 3607 (Pubitemid 129570863)
61. W.F. van Gunsteren, S.R. Billeter, A.A. Eising, P.H. Hunenberger, P. Kruger, A.E. Mark, W.R.P. Scott, and I.G. Tironi Biomolecular simulation: The GROMOS96 manual and user guide 1996 BIOMOS b.v Zurich, Groninger
62. E. Lindahl, B. Hess, and D. van der Spoel GROMACS 3.0: a package for molecular simulation and trajectory analysis J. Mol. Model. 7 2001 306 317 (Pubitemid 36153547)
63. A.S. Oliveira, V.H. Teixeira, A.M. Baptista, and C.M. Soares Reorganization and conformational changes in the reduction of tetraheme cytochromes Biophys. J. 89 2005 3919 3930 (Pubitemid 41725614)
64. 3 from Desulfovibrio vulgaris Hildenborough at 1.9 resolution J. Mol. Biol. 234 1993 680 699 (Pubitemid 24007795)
65. 3 from Desulfovibrio vulgaris Hildenborough at 1.67 resolution and from Desulfovibrio desulfuricans ATCC 27774 at 1.6 resolution Inorg. Chim. Acta 273 1998 213 224 (Pubitemid 128355103)
66. G. Ciccotti, G. Jacucci, and I.R. McDonald Thought experiments by molecular dynamics J. Stat. Phys. 21 1979 1 21
67. A.M. Baptista, P.J. Martel, and S.B. Petersen Simulation of protein conformational freedom as a function of pH: constant-pH molecular dynamics using implicit titration Proteins 27 1997 523 544 (Pubitemid 27212352)
68. A.M. Baptista, V.H. Teixeira, and C.M. Soares Constant-pH molecular dynamics using stochastic titration J. Chem. Phys. 17 2002 4184 4200 (Pubitemid 35037650)
69. M. Machuqueiro, and A.M. Baptista Constant-pH molecular dynamics with ionic strength effects: protonation-conformation coupling in decalysine J. Phys. Chem. B 110 2006 2927 2933 (Pubitemid 43342889)
70. M. Machuqueiro, and A.M. Baptista The pH-dependent conformational states of kyotorphin: a constant-pH molecular dynamics study Biophys. J. 92 2007 1836 1845 (Pubitemid 46495250)
71. M. Machuqueiro, and A.M. Baptista Acidic range titration of HEWL using a constant-pH molecular dynamics method Proteins 72 2008 289 298 (Pubitemid 351809167)
72. S.R.R. Campos, and A.M. Baptista Conformational Analysis in a Multidimensional Energy Landscape: Study of an Arginylglutamate Repeat J. Phys. Chem. B 113 2009 15989 16001
73. S.R.R. Campos, M. Machuqueiro, and A.M. Baptista Constant-pH Molecular Dynamics Simulations Reveal a beta-Rich Form of the Human Prion Protein J. Phys. Chem. B 114 2010 12692 12700
74. 3 J. Am. Chem. Soc. 131 2009 12586 12594
75. G.R. Moore Haemoproteins. In Protein Electron Transfer (Bendall, D.S., ed. eds), pp. 189-216 1996 BIOS Scientific Publishers Ltd. Oxford, UK
76. R.A. Marcus, and N. Sutin Electron transfers in chemistry and biology BBA 811 1985 265 322 (Pubitemid 15246565)
77. A. Warshel Dynamics of reactions in polar solvents. Semiclassical trajectory studies of electron-transfer and proton-transfer reactions J. Phys. Chem. 86 1982 2218 2224
78. F. Drepper, M. Hippler, W. Nitschke, and W. Haehnel Binding dynamics and electron transfer between plastocyanin and photosystem I Biochemistry 35 1996 1282 1295 (Pubitemid 26050792)
79. H. Zhang, C.J. Carrell, D. Huang, V. Sled, T. Ohnishi, J.L. Smith, and W.A. Cramer Characterization and crystallization of the Lumen side domain of the chloroplast Rieske iron-sulfur protein J. Biol. Chem. 271 1996 31360 31366 (Pubitemid 26408586)
80. H.-X. Zhou Effects of mutations and complex formation on the reduction potentials of cytochrome c and cytochrome c peroxidase JACS 116 1994 10362 10375 (Pubitemid 24981848)
81. G.M. Soriano, W.A. Cramer, and L.I. Krishtalik Electrostatic effects on electron-transfer kinetics in the cytochrome f-plastocyanin complex Biophys. J. 73 1997 3265 3276 (Pubitemid 27525789)
82. 3 Biophys. J. 86 2004 2773 2785 (Pubitemid 38552684)
83. 3 from Desulfovibrio africanus: nucleotide sequences, EPR spectroscopy and biological activity BBA 1342 1997 149 163 (Pubitemid 27490362)
84. 3 with different specificity BBA 1273 1996 51 61 (Pubitemid 26035803)
85. D.S. Goodsell, H. Lauble, C.D. Stout, and A.J. Olson Automated docking in crystallography: analysis of the substrates of aconitase Proteins 17 1993 1 10 (Pubitemid 23261053)
86. D.S. Goodsell, and A.J. Olson Automated docking of substrates to proteins by simulated annealing Proteins 8 1990 195 202 (Pubitemid 20363304)
87. N. Froloff, A. Windemuth, and B. Honig On the calculation of binding free energies using continuum methods: application to MHC class I protein-peptide interactions Protein Sci. 6 1997
88. B. Kuhn, and P.A. Kollman A ligand that is predicted to bind better to avidin than biotin: insights from computational fluorine scanning J. Am. Chem. Soc. 122 2000 3909 3916 (Pubitemid 30241593)
89. L. Rivas, C.M. Soares, A.M. Baptista, J. Simaan, R.E. Di Paolo, D.H. Murgida, and P. Hildebrandt Electric-field-induced redox potential shifts of tetraheme cytochromes c3 immobilized on self-assembled monolayers: Surface-enhanced resonance Raman spectroscopy and simulation studies Biophys. J. 88 2005 4188 4199 (Pubitemid 40991130)
90. W. Delano The PyMol molecular graphics system (Eds.). Delano Scientific LLC 2003 San Carlos CA, USA
91. 3 JBIC 4 1999 478 494 (Pubitemid 29426305)
92. D. Leys, T.E. Meyer, A.S. Tsapin, K.H. Nealson, M.A. Cusanovich, and J.J. Van Beeumen Crystal structures at atomic resolution reveal the novel concept of "electron-harvesting" as a role for the small tetraheme cytochrome c J. Biol. Chem. 277 2002 35703 35711