Proton pathways in a [NiFe]-hydrogenase: A theoretical study

Proteins: Structure, Function and Genetics

Volumn 70, Issue 3, 2008, Pages 1010-1022

  Teixeira, Vitor H ^a   Soares, Cláudio M ^a   Baptista, António M ^a  

^a INSTITUTO DE TECNOLOGIA QUÍMICA E BIOLÓGICA   (Portugal)

Author keywords

Desulfovibrio gigas; Electrostatic interactions; Monte Carlo; Poisson Boltzmann; Proton correlation; Titration curves

Indexed keywords

NICKEL IRON HYDROGENASE;

ARTICLE; CORRELATION ANALYSIS; DESULFOVIBRIO GIGAS; ENZYME ACTIVE SITE; ENZYME CONFORMATION; ENZYME MECHANISM; MONTE CARLO METHOD; NONHUMAN; PH; POISSON DISTRIBUTION; PRIORITY JOURNAL; PROTON TRANSPORT; THEORETICAL STUDY;

BINDING SITES; COMPUTER SIMULATION; DESULFOVIBRIO GIGAS; ELECTROSTATICS; GLUTAMIC ACID; HISTIDINE; HYDROGENASE; MODELS, MOLECULAR; MONTE CARLO METHOD; OXIDATION-REDUCTION; PROTONS; WATER;

DESULFOVIBRIO GIGAS;

EID: 38549139111     PISSN: 08873585     EISSN: 10970134     Source Type: Journal    
DOI: 10.1002/prot.21588     Document Type: Article

References (61)

1. Buncel E, Menon B. Carbanion mechanism. 6.1 metalation of arylmethanes by potassium hydride/18-Crown-6 ether in tetrahydrofuran and the acidity of hydrogen. J Am Chem Soc 1977;99:4457-4461.
2. Chinn MS, Heynekey DM, Payne NG, Sofield CD. Highly reactive dihydrogen complexes of ruthenium and rhenium: facile heterolysis of coordinated dihydrogen. Organometallics 1989;8:1824-1826.
3. Heinekey DM, Oldham WJ. Coordination of dihydrogen. Chem Rev 1993;93:913-926.
4. 2 to electron transfer. Nature Struct Biol 1996;3:213-217.
5. Frey M. Hydrogenases: hydrogen-activating enzymes. Chem Biochem 2002;3:153-160.
6. Vignais PM, Billoud B, Meyer J. Classification and phylogeny of hydrogenases. FEMS Microbiol Rev 2001;25:455-501.
7. Hatchikian EC, Bruschi M, LeGall J. Characterization of the periplasmic hydrogenase from Desulfovibrio gigas. Biochem Biophys Res Commun 1978;82:451-461.
8. Huynh BH, Patil DS, Moura I, Teixeira M, Moura JJG, Der Vartanian DV, Czechowski MH, Prickril BC, Peck HD, Jr., LeGall J. On the active site of the [NiFe] hydrogenase from Desulfovibrio gigas. J Biol Chem 1987;262:795-800.
9. Volbeda A, Charon M, Piras C, Hatchikian EC, Frey M, Fontecilla-Camps JC. Crystal structure of the nickel-iron hydrogenase from Desulfovibrio gigas. Nature 1995;373:580-587.
10. Volbeda A, Garcin E, Piras C, De Lacey AL, Fernandez VM, Hatchikian EC, Frey M, Fontecilla-Camps JC. Structure of the [NiFe] hydrogenase active site: evidence for biologically uncommon Fe ligands. J Am Chem Soc 1996;118:12989-12996.
11. Bagley KA, Duin EC, Roseboom W, Albracht SPJ, Woodruff WH. Infrared-detectable groups sence changes in charge density on the nickel center in hydrogenase from Chromatium vinosum. Biochemistry 1995;34:5527-5535.
12. 57Fe Q-band pulsed ENDOR of the hetero-dinuclear site of nickel hydrogenase: comparison of the NiA, NiB, and NiC states. J Am Chem Soc 1997;119:9291-9292.
13. Niu S, Thomson LM, Hall MB. Theoretical characterization of the reaction intermediates in a model of the nickel-iron hydrogenase of Desulfovibrio gigas. J Am Chem Soc 1999;121:4000-4007.
14. 2 towards the active site of [NiFe]-hydrogenase. Biophys J 2006;91:2035-2045.
15. Teixeira M, Moura I, Xavier AV, Huynh BH, Der Vartanian DV, Peck HD, Jr., LeGall J, Moura JJG. Electron paramagnetic resonance studies on the mechanism of activation and the catalytic cycle of the nickel-containing hydrogenase from Desulfovibrio gigas. J Biol Chem 1985;260:8942-8950.
16. Yagi T, Honya M, Tamiya N. Purification and properties of hydrogenases of different origins. Biochim Biophys Acta 1968;153:699-705.
17. 3. J Biol Inorg Chem 2001;6:63-81.
18. 3: electron transfer mechanisms. Eur J Biochem 1982;127: 151-155.
19. Fernandez VM, Hatchikian EC, Cammack R. Properties and reactivation of two different deactivated forms of Desulfovibrio gigas hydrogenase. Biochim Biophys Acta 1985;832:69-79.
20. Fernandez VM, Hatchikian EC, Patil D, Cammack R. ESR-detectable nickel and iron-sulphur centres in relation to the reversible activation of Desulfovibrio gigas hydrogenase. Biochim Biophys Acta 1986;883:145-154.
21. Cammack R, Patil ED, Hatchikian C, Fernandez VM. Nickel and iron-sulphur centres in Desulfovibrio gigas hydrogenase: ESR spectra, redox properties and interactions. Biochim Biophys Acta 1987;912:98-109.
22. Albracht SPJ. Nickel hydrogenases: in search of the active site. Biochim Biophys Acta 1994;1188:167-204.
23. de Lacey AL, Hatchikian EC, Volbeda A, Frey M, Fontecilla-Camps JC, Fernandez VM. Infrared-spectroelectrochemical characterization of the [NiFe] hydrogenase of Desulfovibrio gigas. J Am Chem Soc 1997;119:7181-7189.
24. Bagyinka C, Whitehead JP, Maroney MJ. An X-ray absorption spectroscopy of nickel redox chemistry in hydrogenase. J Am Chem Soc 1993;115:3576-3585.
25. Gu Z, Dong J, Allan CB, Choudhury SB, Franco R, Moura JJG, Moura I, LeGall J, Przybyla AE, Roseboom W, Albracht SPJ, Axley MJ, Scott RA, Maroney MJ. Structure of the Ni Sites in hydrogenase by X-ray absorption spectroscopy. Species variation and the effects of redox poise. J Am Chem Soc 1996;118:11155-11165.
26. 2] chromophores. J Am Chem Soc 1995;117:1584-1594.
27. Dole F, Fournel A, Magro V, Hatchikian EC, Bertrand P, Guigliarelli B. Nature and electronic structure of the Ni-X dinuclear center of Desulfovibrio gigas hydrogenase. Implications for the enzyme mechanism. Biochemistry 1997;36:7847-7854.
28. Pavlov M, Siegbahn PEM, Blomberg MRA, Crabtree RH. Mechanism of H-H activation by nickel-iron hydrogenase. J Am Chem Soc 1998;120:548-555.
29. Amara P, Volbeda A, Fontecilla-Camps JC, Field MJ. A hybrid density functional theory/molecular mechanics study of nickel-iron hydrogenase: investigation of the active site redox states. J Am Chem Soc 1999;121:4468-4477.
30. de Gioia L, Fantucci P, Guigliarelli B, Bertrand P. Ni-Fe hydrogenases: a density functional theory study of active site models. Inorg Chem 1999;38:2658-2662.
31. Fan H-J, Hall MB. Recent theoretical predictions of the active site for the observed forms in the catalytic cycle of Ni-Fe hydrogenase. J Biol Inorg Chem 2001;6:467-473.
32. Siegbahn PEM, Blomberg MRA, Pavlov MW, Crabtree RH. The mechanism of the Ni-Fe hydrogenase: a quantum chemical perspective. J Biol Inorg Chem 2001;6:460-466.
33. Frey M, Fontecilla-Camps JC, Volbeda A. Nickel-iron hydrogenases. In: Messerschmidt A, Huber R, Poulos T, Wieghardt K, editors. Handbook of metalloproteins, Vol. 2. New York: Wiley; 2001. pp 880-896.
34. Dementin S, Burlat B, de Lacey AL, Pardo A, Adryanczyk-Perrier G, Guigliarelli B, Fernandez VM, Rousset M. A Glutamate is the essential proton transfer gate during the catalytic cycle of the [NiFe] hydrogenase. J Biol Chem 2004;279:10508-10513.
35. 3 haem-copper oxygen reductase. J Biol Inorg Chem 2004;9:124-134.
36. Kato M, Pisliakov AV, Warshel A. The barrier for proton transport in aquaporins as a challenge for electrostatic models: the role of protein relaxation in mutational calculations. Proteins: Struct Funct Bioinf 2006;64:829-844.
37. Li S, Hall MB. Modeling the active sites of metalloenzymes. 4. Predictions of the unready states of [NiFe] Desulfovibrio gigas hydrogenase from density functional theory. Inorg Chem 2001;40:18-24.
38. Frisch MJ, Trucks GW, Schlegel HB, Scuseria GE, Robb MA, Cheeseman JR, Zakrzewski VG, Montgomery JA, Stratmann RE, Burant JC, Dapprich S, Millan JM, Daniels AD, Kudin KN, Strain MC, Farkas O, Tomasi J, Barone V, Cossi M, Cammi R, Mennucci B, Pomelli C, Adamo C, Clifford S, Ochterski J, Petersson GA, Ayala PY, Cui Q, Morokuma K, Malick DK, Rabuck AD, Raghavachari K, Foresman JB, Cioslowski J, Ortiz JV, Baboul AG, Stefanov BB, Liu G, Liashenko A, Piskorz P, Komaromi I, Gomperts R, Martin RL, Fox DJ, Keith T, Al-Laham MA, Peng CY, Nanayakkara A, Gonzalez C, Challacombe M, Gill PMW, Johnson B, Chen W, Wong MW, Andres JL, Gonzalez C, Head-Gordon M, Replogle ES, Pople JA. Gaussian 98, Revision A.7. Pittsburgh PA; 1998.
39. Bayly CI, Cieplak P, Cornell WD, Kollman PA. A well behaved electrostatic based method using charge restraints for deriving atomic charges: the RESP model. J Phys Chem 1993;97:10269-10280.
40. Teixeira M, Moura I, Xavier AV, Moura JJG, LeGall J, Der Vartanian DV, Peck HD, Jr., Huynh BH. Redox intermediates of Desulfovibrio gigas [NiFe] hydrogenase generated under hydrogen. J Biol Chem 1989;264:16435-16450.
41. Baptista AM, Soares CM. Some theoretical and computational aspects of the inclusion of proton isomerism in the protonation equilibrium of proteins. J Phys Chem B 2001;105:293-309.
42. Teixeira VH, Cunha CC, Machuqueiro M, Oliveira ASF, Victor BL, Soares CM, Baptista AM. On the use of different dielectric constants for computing individual and pairwise terms in Poisson-Boltzmann studies of protein ionization equilibrium. J Phys Chem B 2005;109:14691-14706.
43. Eisenhaber F, Argos P. Improved strategy in analytic surface calculation for molecular systems: handling of singularities and computational efficiency. J Comp Chem 1993;14:1272-1280.
44. Eisenhaber F, Lijnzaad P, Argos P, Sander C, Scharf M. The double cubic lattice method - efficient approaches to numerical-integration of surface-area and volume and to dot surface contouring of molecular assemblies. J Comp Chem 1995;16:273-284.
45. Teixeira VH, Soares CM, Baptista AM. Studies of the reduction and protonation behavior of the tetraheme cytochromes using atomic detail. J Biol Inorg Chem 2002;7:200-216.
46. Bashford D. An object-oriented programming suite for electrostatic effects in biological molecules. In: Ishikawa Y, Oldehoeft RR, Reynders JVW, Tholburn M, editors. Scientific computing in object-oriented parallel environments, Vol. 1343,Lecture notes in computer science. Berlin: Springer; 1997. pp 233-240 (ISCOPE97).
47. a values of ionizable groups in bacteriorhodopsin. J Mol Biol 1992;224:473-486.
48. Scott WRP, Hünenberger PH, Tironi IG, Mark AE, Billeter SR, Fennen J, Torda AE, Huber T, Krüger P, van Gunsteren WF. The GROMOS biomolecular simulation program package. J Phys Chem A 1999;103:3596-3607.
49. Simonson T, Archontis G, Karplus M. A Poisson-Boltzmann study of charge insertion in an enzyme active site: the effect of dielectric relaxation. J Phys Chem B 1999;103:6142-6156.
50. Warshel A, Sharma PK, Kato M, Parson WW. Modeling electrostatic effects in proteins. Biochim Biophys Acta 2006;1764:1647-1676.
51. 3 using continuum electrostatics. Biophys J 1999;76:2978-2998.
52. DeLano WL. The PyMOL User's Manual. San Carlos, CA: DeLano Scientific; 2002.
53. 3 with [NiFe] hydrogenase from Desulfovibrio vulgaris Miyazaki F. Biochemistry 2006;45:1653-1662.
54. Katz AK, Glusker JP, Markham GD, Bock CW. Deprotonation of water in the presence of carboxylate and magnesium ions. J Phys Chem B 1998;102:6342-6350.
55. Volbeda A, Fontecilla-Camps JC. Structure-function relationships of nickel-iron sites in hydrogenase and a comparison with the active sites of other nickel-iron enzymes. Coord Chem Rev 2005;249:1609-1619.
56. Nagle JF, Mille M. Molecular models of proton pumps. J Chem Phys 1981;74:1367-1372.
57. Siegbahn PEM, Blomberg MRA. Transition-metal systems in biochemistry studied by high-accuracy quantum chemical methods. Chem Rev 2000;100:421-438.
58. Ferreira AM, Bashford D. Model for proton transport coupled to protein conformational change: application to proton pumping in the bacteriorhodopsin photocycle. J Am Chem Soc 2006;128:16778-16790.
59. Kim YC, Wikström M, Hummer G. Kinetic models of redox-coupled proton pumping. Proc Natl Acad Sci USA 2007;104:2169-2174.
60. Olsson MHM, Warshel A. Monte Carlo simulations of proton pumps: on the working principles of the biological valve that controls proton pumping in cytochrome c oxidase. Proc Natl Acad Sci USA 2006;103:6500-6505.
61. Olsson MHM, Siegbahn PEM, Blomberg MRA, Warshel A. Exploring pathways and barriers for coupled ET/PT in cytochrome c oxidase: a general framework for examining energetics and mechanistic alternatives. Biochim Biophys Acta 2007;1767:244-260.