Structures of the dI2dIII1 complex of proton-translocating transhydrogenase with bound, inactive analogues of NADH and NADPH reveal active site geometries

Biochemistry

Volumn 46, Issue 11, 2007, Pages 3304-3318

  Bhakta, Tina ^a   Whitehead, Simon J ^a   Snaith, John S ^a   Dafforn, Tim R ^a   Wilkie, John ^a   Rajesh, Sundaresan ^a   White, Scott A ^a   Jackson, J Baz ^a  

^a UNIVERSITY OF BIRMINGHAM   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

BINDING ENERGY; BIOLOGICAL MEMBRANES; CONFORMATIONS; NUCLEOTIDES; PHOSPHATES; PROTONS; RATE CONSTANTS; REDOX REACTIONS;

INACTIVE ANALOGUES; PHYSIOLOGICAL NUCLEOTIDES; PROTON-TRANSLOCATING TRANSHYDROGENASE;

ENZYMES;

NICOTINAMIDE ADENINE DINUCLEOTIDE (PHOSPHATE) TRANSHYDROGENASE; NICOTINAMIDE ADENINE DINUCLEOTIDE PHOSPHATE; NUCLEOTIDE; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE PHOSPHATE; 1,4,5,6 TETRAHYDRONICOTINAMIDE ADENINE DINUCLEOTIDE; 1,4,5,6 TETRAHYDRONICOTINAMIDE ADENINE DINUCLEOTIDE PHOSPHATE; 1,4,5,6-TETRAHYDRONICOTINAMIDE ADENINE DINUCLEOTIDE; 1,4,5,6-TETRAHYDRONICOTINAMIDE ADENINE DINUCLEOTIDE PHOSPHATE; DRUG DERIVATIVE; NICOTINAMIDE ADENINE DINUCLEOTIDE; PROTEIN SUBUNIT; PROTON; UNCLASSIFIED DRUG;

AB INITIO CALCULATION; ARTICLE; BINDING AFFINITY; COMPLEX FORMATION; CONFORMATIONAL TRANSITION; CONTROLLED STUDY; CRYSTAL STRUCTURE; DISSOCIATION CONSTANT; ENZYME ACTIVE SITE; ENZYME BINDING; ENZYME STRUCTURE; ENZYME SUBUNIT; HYDROGENATION; MOLECULAR DYNAMICS; NONHUMAN; OXIDATION REDUCTION REACTION; PRIORITY JOURNAL; PROTON TRANSPORT; QUANTUM MECHANICS; RHODOSPIRILLUM RUBRUM; BINDING SITE; CHEMICAL STRUCTURE; CHEMISTRY; COMPUTER SIMULATION; ENZYMOLOGY; NUCLEAR MAGNETIC RESONANCE; X RAY CRYSTALLOGRAPHY;

RHODOSPIRILLUM RUBRUM;

BINDING SITES; COMPUTER SIMULATION; CRYSTALLOGRAPHY, X-RAY; MODELS, MOLECULAR; NAD; NADP; NADP TRANSHYDROGENASE; NUCLEAR MAGNETIC RESONANCE, BIOMOLECULAR; PROTEIN SUBUNITS; PROTONS; RHODOSPIRILLUM RUBRUM;

EID: 33947390415     PISSN: 00062960     EISSN: None     Source Type: Journal    
DOI: 10.1021/bi061843r     Document Type: Article

References (96)

1. Venning, J. D., Grimley, R. L., Bizouarn, T., Cotton, N. P. J., and Jackson, J. B. (1997) Evidence that the transfer of hydride equivalents between nucleotides by proton-translocating transhydrogenase is direct, J. Biol. Chem. 272, 27535-27538.
2. Lee, C. P., Simard-Duquesne, N., Ernster, L., and Hoberman, H. D. (1965) Stereochemistry of hydrogen transfer in the energy-linked pyridine nucleotide transhydrogenase and related reactions, Biochim. Biophys. Acta 105, 397-409.
3. Griffiths, D. E., and Roberton, A. M. (1966) Energy-linked reactions in mitochondria: studies on the mechanism of the energy-linked transhydrogenation reaction, Biochim. Biophys. Acta 118, 453-464.
4. - ratio of the reaction catalysed by the nicotinamide nucleotide transhydrogenase in chromatophores from over-expressing strains of Rhodospirillum rubrum and in liposomes inlaid with the purified bovine enzyme, Biochim. Biophys. Acta 1273, 4-12.
5. Jackson, J. B., White, S. A., and Brondijk, T. H. C. (2005) Hydride transfer and proton translocation by nicotinamide nucleotide transhydrogenase, in Biophysical and Structural Aspects of Bioenergetics (Wikstrom, M., Ed.) pp 376-393, Royal Society of Chemistry, Cambridge.
6. Bizouarn, T., Fjellstrom, O., Meuller, J., Axelsson, M., Bergkvist, A., Johansson, C., Karlsson, G., and Rydstrom, J. (2000) Proton translocating nicotinamide nucleotide transhydrogenase from E. coli. Mechanism of action deduced from its structural and catalytic properties, Biochim. Biophys. Acta 1457, 211-218.
7. Hatefi, Y., and Yamaguchi, M. (1996) Nicotinamide nucleotide transhydrogenase: a model for utilization of substrate binding energy for proton translocation, FASEB J. 10, 444-452.
8. Hutton, M. N., Day, J. M., Bizouarn, T., and Jackson, J. B. (1994) Kinetic resolution of the reaction catalysed by proton-translocating transhydrogenase from Escherichia coli as revealed by experiments with nucleotide substrate analogues, Eur. J. Biochem. 219, 1041-1051.
9. Bragg, P. D., and Hou, C. (2001) Characterisation of mutants of beta-histidine91, beta-aspartate213 and beta-asparagine222, possible components of the energy-transduction pathway of the proton-translocating pyridine nucleotide transhydrogenase of Escherichia coli, Arch. Biochem. Biophys. 388, 299-307.
10. Yamaguchi, M., and Stout, C. D. (2003) Essential glycine residues in the proton channel of Escherichia coli transhydrogenase, J. Biol. Chem. 278, 45333-45339.
11. Karlsson, J., Althage, M., and Rydstrom, J. (2003) Roles of individual amino acid in helix 14 of the membrane domain of proton-translocating transhydrogensae from Escherichia coli as deduced from cysteine mutagenesis, Biochemistry 42, 6575-6581.
12. Oshino, N., and Chance, B. (1977) Properties of glutathione release observed during reduction of organic hydroperoxide, demethylation of aminopyridine and oxidation of some substances in perfused rat liver, and their implications for the physiological function of catalase, Biochem. J. 162, 509-525.
13. Rydstrom, J., and Hoek, J. B. (1988) Physiological roles of nicotinamide nucleotide transhydrogenase, Biochem. J. 254, 1-10.
14. Sazanov, L. A., and Jackson, J. B. (1994) Proton translocating transhydrogenase and NAD- and NADP-linked isocitrate dehydrogenases operate in a substrate cycle which contributes to the fine regulation of the tricarboxylic acid cycle activity in mitochondria, FEBS Lett. 344, 109-116.
15. Ambartsoumian, G., Dari, R., Lin, R. T., and Newman, E. B. (1994) Altered amino-acid metabolism in LRP mutants of Escherichia coli K12 and their derivatives, Microbiology 140, 1737-1744.
16. Hickman, J. W., Barber, R. D., Skaar, E. P., and Donohue, T. J. (2002) A link between the membrane-bound pyridine nucleotide transhydrogenase and glutathione-dependent processes in Rhodobacter sphaeroides, J. Bacteriol. 184, 400-409.
17. Arkblad, E. L., Tuck, S., Pestov, N. B., Dmitriev, R. I., Kostina, M. B., Stenvall, J., Tranberg, M., and Rydstrom, J. (2005) A Caenorhabditis elegans mutant lacking functional nicotinamide nucleotide transhydrogenase displays increased sensitivity ot oxidative stress, Free Radical Biol. Med. 38, 1518-1525.
18. Freeman, H., Shimomura, K., Horner, E., Cox, R. D., and Ashcroft, F. M. (2006) Nicotinamide nucleotide transhydrogenase: a key role in insulin secretion, Cell. Metab. 3, 35-45.
19. Meuller, J., and Rydstrom, J. (1999) The membrane topology of proton-pumping Escherichia coli transhydrogenase determined by cysteine labelling, J. Biol. Chem. 274, 19072-19080.
20. Wilson, R., Obiozo, U. M., Quirk, P. G., Besra, G. D., and Jackson, J. B. (2006) A hybrid of the transhydrogenases from Rhodospirillum rubrum and Mycobacterium tuberculosis catalyses rapid hydride transfer but not the complete, proton-translocating reaction., Biochim. Biophy. Acta 1537, 215-223.
21. Jackson, J. B., White, S. A., Quirk, P. G., and Venning, J. D. (2002) The alternating site, binding change mechanism for proton translocation by transhydrogenase, Biochemistry 41, 4173-4185.
22. Buckley, P. A., Jackson, J. B., Schneider, T., White, S. A., Rice, D. W., and Baker, P. J. (2000) Protein-protein recognition, hydride transfer and proton pumping in the transhydrogenase complex, Structure 8, 809-815.
23. Prasad, G. S., Wahlberg, M., Sridhar, V., Sundaresan, V., Yamaguchi, M., Hatefi, Y., and Stout, C. D. (2002) Crystal structures of transhydrogenase domain I with and without bound NADH, Biochemistry 41, 12745-12754.
24. Johansson, T., Oswald, C., Pedersen, A., Tornroth, S., Okvist, M., Karlsson, B. G., and Rydstrom, J. (2005) X-ray structure of domain I of the proton-pumping membrane protein transhydrogenase from Escherichia coli, J. Mol. Biol. 352, 299-312.
25. Prasad, G. S., Sridhar, V., Yamaguchi, M., Hatefi, Y., and Stout, C. D. (1999) Crystal structure of transhydrogenase domain III at 1.2 Å resolution, Nat.e Struct. Biol. 6, 1126-1131.
26. White, S. A., Peake, S. J., McSweeney, S., Leonard, G., Cotton, N. N. J., and Jackson, J. B. (2000) The high resolution structure of the NADP(H)-binding component of proton-translocating transhydrogenase from human-heart mitochondria, Structure 8, 1-12.
27. Jeeves, M., Smith, K. J., Quirk, P. G., Cotton, N. P. J., and Jackson, J. B. (2000) Solution structure of the NADP(H)-binding component (dIII) of proton-translocating transhydrogenase from Rhodospirillum rubrum, Biochim. Biophys. Acta 1459, 248-257.
28. Diggle, C., Bizouarn, T., Cotton, N. P. J., and Jackson, J. B. (1996) Properties of the purified, recombinant, NADP(H)-binding domain III of the proton-translocating nicotinamide nucleotide transhydrogenase from Rhodospirillum rubrum, Eur. J. Biochem. 241, 162-170.
29. Yamaguchi, M., and Hatefi, Y. (1997) High cyclic transhydrogenase activity catalysed by expressed an reconstituted nucleotide-binding domains of Rhodospirillum rubrum transhydrogenase, Biochim. Biophys. Acta 1318, 225-234.
30. Venning, J. D., Bizouarn, T., Cotton, N. P. J., Quirk, P. G., and Jackson, J. B. (1998) Stopped-flow kinetics of hydride transfer between nucleotides by recombinant domains of proton-translocating transhydrogenase, Eur. J. Biochem. 257, 202-209.
31. Venning, J. D., Peake, S. J., Quirk, P. G., and Jackson, J. B. (2000) Stopped-flow reaction kinetics of recombinant components of proton-translocating transhydrogenase with physiological nucleotides, J. Biol. Chem. 275, 19490-19497.
32. Cotton, N. P. J., White, S. A., Peake, S. J., McSweeney, S., and Jackson, J. B. (2001) The crystal structure of an asymmetric complex of the two nucleotide-binding components of proton-translocating transhydrogenase, Structure 9, 165-176.
33. Mather, O. M., van Boxel, G. I., White, S. A., and Jackson, J. B. (2004) Active-site conformational changes associated with hydride transfer in proton-translocating transhydrogenase, Biochemistry 43, 10952-10964.
34. Sundaresan, V., Chartron, J., Yamaguchi, M., and Stout, C. D. (2005) Conformational diversity in NAD(H) and interacting transhydrogenase nicotinamide nucleotide binding domains, J. Mol. Biol. 346, 617-629.
35. Biellman, J. F., and Jung, M. J. (1971) Mechanism of the alcohol dehydrogenase from yeast and horse liver, Eur. J. Biochem 19, 130-134.
36. +, Eur. J. Biochem 56, 116.
37. Thevenot, D. R., Godinot, C., Gautheron, D. C., Branlant, G., and Biellman, J. F. (1975) Binding of L-glutamate to glutamate dehydrogenase in the presence of 1,4,5,6-tetrahydronicotinamide adenine dinucleotide, FEBS Lett. 54, 206-211.
38. + analogues: tools for the investigation of the active site of oestradiol 17-beta-dehydrogenase from human placenta, Eur. J. Biochem. 56, 557-561.
39. Dunn, M. F., Biellman, J. F., and Branlant, G. (1975) Roles of zinc ion and reduced coenzyme in horse liver alcohol dehydrogenase catalysis. The mechanism of aldehyde activation, Biochemistry 14, 3176-3182.
40. Cedergren-zeppenauer, E., Samama, J.-P., and Eklund, H. (1982) Crystal structure determinations of coenzyme analogue and substrate complexes of liver alcohol dehydrogenase: binding of 1,4,5,6-tetrahydronicotinamide adenine dinucleotide and trans-4-(N,N-dimethylamino)cinnamaldehyde to the enzyme, Biochemistry 21, 4895-4908.
41. Chapman, A. D. M., Cortes, A., Dafforn, T. R., Clarke, A. R., and Brady, R. L. (1999) Structural basis of substrate specificity in malate dehydrogenses: crystal structure of a ternary complex of porcine cytoplasmic malate dehydrogenase, alpha-ketomalonate and tetrahydroNAD, J. Mol. Biol. 285, 703-712.
42. Weaver, P. F., Wall, J. D., and Gest, H. (1975) Characterisation of Rhodopseudomonas capsulata, Arch. Microbiol. 105, 207-216.
43. +-transhydrogenase of Rhodospirillum rubrum and the enzyme from mitochondria and Escherichia coli, Biochim. Biophys. Acta 1100, 332-338.
44. Clayton, R. K. (1963) Towards the isolation of a photochemical reaction centre in Rhodopseudomonas capsulata, Biochim. Biophys. Acta 73, 312-323.
45. Diggle, C., Hutton, M., Jones, G. R., Thomas, C. M., and Jackson, J. B. (1995) Properties of the soluble polypeptide of the proton-translocating transhydrogenase from Rhodospirillum rubrum obtained by expression in Escherichia coli, Eur. J. Biochem. 228, 719-726.
46. Jeeves, M., Smith, K. J., Quirk, P. G., Cotton, N. P. J., and Jackson, J. B. (1999) Sequence-specific resonance assignments for the NADP(H)-binding component (domain III) of proton-translocating transhydrogenase from Rhodospirillum rubrum, J. Biomol. NMR 13, 305-306.
47. + in the dill components of proton-translocating transhydrogenase from Homo sapiens and from Rhodospirillum rubrum by measurement of tryptophan fluorescence, Biochim. Biophys. Acta 1413, 81-91.
48. Mejbaum-Katzenellenbogen, S., and Drobryszycka, W. J. (1959) New methods for quantitative determination of serum proteins separated by paper chromatography, Clin. Chim. Acta 4, 515-522.
49. Dave, K. G., Dunlap, R. B., Jain, M. K., Cordes, E. H., and Wenkert, E. (1968) Highly reduced analogues of the pyridine nucleotides, J. Biol. Chem. 243, 1073-1074.
50. Branlant, G., Eiler, B., and Biellman, J. F. (1982) A word of caution: 1,4,5,6-tetrahydronicotinamideandenine dinucleotide (phosphate) should be used with care in acidic and neutral media, Anal. Biochem. 125, 264-268.
51. - ratio and the activation state of the enzyme during reduction of acetyl pyridine adenine dinucleotide, Biochim. Biophys. Acta 1099, 157-162.
52. Venning, J. D., Rodrigues, D. J., Weston, C. J., Cotton, N. P. J., Quirk, P. G., Errington, N., Finet, S., White, S. A., and Jackson, J. B. (2001) The heterotrimer of the membrane-peripheral components of transhydrogenase and the alternating-site mechanism of proton translocation, J. Biol. Chem. 276, 30678-30685.
53. Diggle, C., Cotton, N. P. J., Grimley, R. L., Quirk, P. G., Thomas, C. M., and Jackson, J. B. (1995) Conformational dynamics of a mobile loop in the NAD(H)-binding subunit of proton-translocating transhydrogenases from Rhodospirillum rubrum and Escherichia coli, Eur. J. Biochem. 232, 315-326.
54. Quirk, P. G., Jeeves, M., Cotton, N. P. J., Smith, K. J., and Jackson, J. B. (1999) Structural changes in the recombinant, NADP(H)-binding component (dIII) of proton-translocating transhydrogenase revealed by NMR spectroscopy, FEBS Lett. 446, 127-132.
55. 1H 2D NMR spectra by interactive graphics, J. Magn. Reson. 24, 627-633.
56. Rajesh, S., Sakamoto, T., Iwamoto-Sugai, M., Shibata, T., Hohno, T., and Ito, Y. (1999) Ubiquitin binding interface mapping on yeast ubiquitin hydrolase by NMR chemical shift perturbation, Biochemistry 38, 9242-9253.
57. Leslie, A. G. W. (1992) Recent changes to the MOSFLM package for processing film and image data, Jt. CCCP4 ESF-EADBM Newsl. Protein Crystallogr. 226.
58. Evans, P. R. (1997) SCALA, Jt. CCP4 ESF-EACMB Newsl. 33, 22-24.
59. Kissinger, C. R., Gelhaar, D. K., and Fogel, D. B. (1999) Rapid automated molecular replacement by evolutionary search, Acta Crystallogr. D55, 484-491.
60. Murshudov, G. N., Vagin, A. A., and Dodson, E. J. (1997) REFMAC5, Acta Crystallogr. D 53, 240-255.
61. Brunger, A. T., Adams, P. D., Clore, G. M., Delano, W. L., Gros, P., Grossekunstleve, R. W., Et, A. L., and Warren, G. L. (1998) Crystallography and NMR system: A new software suite for macromolecular structure determination, Acta Crystallogr. D 54, 905-921.
62. Hooft, R. W. W., Vriend, G., Sander, C., and Abola, E. E. (1996) Errors in protein structures, Nature 381, 272.
63. Laskowski, R. A., Macarthur, M. W., Moss, D. S., and Thornton, J. M. (1993) PROCHECK: a programme to check the stereochemical quality of protein structures, J. Appl. Crystallogr. 26, 283-291.
64. Krebs, W. G., and Gerstein, M. (2000) The MORPH server: a standardized system for analyzing and visualizing macromolecular motions in a database framework, Nucleic Acids Res. 28, 1665-1675.
65. Case, D. A., Darden, T. A., Cheatham, I. T. E., Simmerling, C. L., Wang, J., Duke, R. E., Luo, R., Merz, K. M., Wang, B., Pearlman D. A., Crowley, M., Brozell, S., Tsui, V., Gohlke, H., Mongan, J., Hornak, V., Cui, G., Beroza, P., Schafmeister, C., Caldwell, J. W., Ross, W. S., and Kollman P. A. (2004) Amber8, University of California, San Francisco.
66. Holmberg, N., and Ryde, U. (2006) Redesign of the coenzyme specificity in L-lactate dehydrogenase from Bacillus stearothermophilus using site-directed mutagenesis and media engineering, Protein Eng. 12, 851-856.
67. Frisch, M. J., Trucks, G. W., Schlegel, H. B., Scuseria, G. E., Robb, M. A., Cheeseman, J. R., Zakrzewski, V. G., Montgomery, J. A., Jr., Stratmann, R. E., Burant, J. C., Dapprich, S., Millam, J. M., Daniels, A. D., Kudin, K. N., Montgomery, J. A., Jr., Stratmann, R. E., Burant, J. C., Dapprich, S., Millam, J. M., Daniels, A. D., Kudin, K. N., Strain, M. C., Farkas, O., Tomasi, J., Barone, V., Cossi, M., Cammi, R., Mennucci, B., Pomelli, C., Adamo, C., Clifford, S., Ochterski, J., Petersson, G. A., Ayala, P. Y., Cui, Q., Morokuma, K., Malick, D. K., Rabuck, A. D., Raghavachari, K., Foresman, J. B., Cioslowski, J., Ortiz, J. V., Stefanov, B. B., Liu, G., Liashenko, A., Piskorz, P., Raghavachari, K., Foresman, J. B., Cioslowski, J., Ortiz, J. V., Stefanov, B. B., Liu, G., Liashenko, A., Piskorz, P., Gonzalez, C., Challacombe, M., Gill, P. M. W., Johnson, B. G., Chen, W., Wong, M. W., Andres, J. L., Head-Gordon, M., Replogle, E. S., and Pople, J. A. (1998) Gaussian 98, revision A.7, Gaussian Inc., Pittsburgh, PA.
68. Bayly, C. I., Cieplak, P., Cornell, W. D., and Kollman, P. A. (1993) A well-behaved electrostatic potential based method using charge restraints for determining atom-centered charges: The RESP model, J. Phys. Chem. 97, 10269-10280.
69. Cornell, W. D., Cieplak, P., Bayly, C. I., Gould, I. R., Merz, K. M., Jr., Ferguson, D. M., Spellmeyer, D. C., Fox, T., Caldwell, J. W., and Kollman, P. A. (1995) A second generation force field for the simulation of proteins, nucleic acids, and organic molecules, J. Am. Chem. Soc. 117, 5179-5197.
70. Wang, J., Wolf, R. M., Caldwell, J. W., Kollman, P. A., and Case, D. A. (2004) Development and testing of a general Amber force field, J. Comput. Chem. 25, 1157-1174.
71. Duan, Y., Wu, C., Chowdhury, S., Lee, M. C., Xiong, G., Zhang, W., Yang, R., Cieplak, P., Luo, R., and Lee, T. (2003) A point-charge force field for molecular mechanics simulations of proteins, J. Comput. Chem. 24, 1999-2012.
72. Jorgensen, W., Chandrasekhar, J., Mandura, J., Impey, R., and Klein, M. (1983) Comparison of simple potential functions for simulating liquid water, J. Phys. Chem. 79, 926-935.
73. Berendsen, H. J. C., Postma, J. P. M., van Gunsteren, W. F., DiNola, A., and Haak, J. R. (1984) Molecular dynamics with coupling to an external bath, J. Chem. Phys. 81, 3684-3690.
74. Ryckaert, J.-P., Ciccotti, G., and Berendsen, H. J. C. (1977) Numerical integration of the Cartesian equations of motion of a system with constraints: molecular dynamics of n-alkanes, J. Comput. Phys. 23, 327-341.
75. Darden, T., York, D., and Pedersen, L. (1993) Particle mesh Ewald-an Nlog(N) method for Ewald sums in large systems, J. Chem. Phys. 98, 10089-10092.
76. Wu, Y.-D., Lai, D. K. W., and Houk, K. N. (1995) Transition structures of hydride transfer reactions of protonated pyridinium ion with 1,4-dihydropyridine and protonated nicotinamide with 1,4-dihydronicotinamide, J. Am. Chem. Soc. 117, 4100-4108.
77. Delano, W. L. (2002) The PyMOL molecular graphics system, DeLano Scientific, San Carlos, CA.
78. Quirk, P. G., Smith, K. J., Thomas, C. M., and Jackson, J. B. (1999) The mobile loop region of the NAD(H)-binding component (dI) of proton-translocating transhydrogenase from Rhodospirillum rubrum: complete NMR assignment and effects of bound nucleotides, Biochim. Biophys. Acta 1412, 139-148.
79. Bizouarn, T., Diggle, C., and Jackson, J. B. (1996) The binding of nucleotides to domain I proteins of the proton-translocating transhydrogenases of Rhodospirillum rubrum and Escherichia coli as measured by equilibrium dialysis, Eur. J. Biochem. 239, 737-741.
80. Grimley, R. L., Quirk, P. G., Bizouarn, T., Thomas, C. M., and Jackson, J. B. (1997) The role of methionine-239, an amino acid residue in the mobile loop region of proton-translocating transhydrogenase, Biochemistry 36, 14762-14770.
81. Fjellstrom, O., Johansson, C., and Rydstrom, J. (1997) Structural and catalytic properties of the expressed and purified NAD(H)- and NADP(H)-binding domains of proton-pumping transhydrogenase from Escherichia coli, Biochemistry 36, 11331-11341.
82. Bergkvist, A., Johansson, C., Johansson, T., Rydstrom, J., and Karlsson, B. G. (2000) Interactions of the NADP(H)-binding domain III of proton-translocating transhydrogenase from Escherichia coli with NADP(H) and the NAD(H)-binding domain I studied by NMR and site-directed mutagenesis, Biochemistry 39, 12595-12605.
83. Sundaresan, V., Yamaguchi, M., Chartron, J., and Stout, C. D. (2003) Conformational change in the NADP(H)-binding domain of transhydrogenase defines four states, Biochemistry 42, 12143-12153.
84. Bizouarn, T., Stilwell, S. N., Venning, J. M., Cotton, N. P. J., and Jackson, J. B. (1997) The pH dependences of reactions catalysed by the complete proton-translocating transhydrogenase from Rhodospirillum rubrum, and by the complex formed from its recombinant peripheral, nucleotide-binding domains, Biochim. Biophys. Acta 1322, 19-32.
85. Bizouarn, T., van Boxel, G. I., Bhakta, T., and Jackson, J. B. (2005) Nucleotide binding affinities of the intact proton-translocating transhydrogenase from Escherichia coli, Biochim. Biophys. Acta 1708, 404-410.
86. Brondijk, T. H. C., van Boxel, G. I., Singh, A., Mather, O. M., White, H. A., Quirk, P. G., White, S. A., and Jackson, J. B. (2006) The role of invariant amino acid residues at the hydride-transfer site of proton-translocating transhydrogenase, J. Biol. Chem. 281, 13345-13354.
87. van Boxel, G. I., Quirk, P., Cotton, N. J. P., White, S. A., and Jackson, J. B. (2003) Glutamine-132 in the NAD(H)-binding component of proton-translocating transhydrogenase tethers the nucleotides before hydride transfer, Biochemistry 42, 1217-1226.
88. Pinheiro, T. J. T., Venning, J. D., and Jackson, J. B. (2001) Fast hydride transfer in proton-translocating transhydrogenase revealed in a rapid-mixing, continuous-flow device, J. Biol. Chem. 276, 44757-44761.
89. Singh, A., Venning, J. D., Quirk, P., van Boxel, G. I., Rodrigues, D. J., White, S. A., and Jackson, J. B. (2003) Interactions between transhydrogenase and thio-nicotinamide analogues of NAD(H) and NADP(H) underline the importance of nucleotide conformational changes in coupling to proton translocation, J. Biol. Chem. 278, 33208-33216.
90. Johansson, C., Pedersen, A., Karlsson, B. G., and Rydstrom, J. (2002) Redox-sensitive loops D and E regulate NADP(H) binding in domain III and domain I-domain III interactions in proton-translocating Escherichia coli transhydrogenase, Eur. J. Biochem. 269, 4505-4515.
91. Yu, Y., and Samuelson, J. (1994) Primary structure of an Entamoeba histolytica nicotinamide nucleotide transhydrogenase, Mol. Biochem. Parasitol. 68, 323-328.
92. Clark, C. G., and Roger, A. J. (1995) Direct evidence for secondary loss of mitochondria in Entamoeba histolytica, Proc. Natl. Acad. Sci. U.S.A. 92, 6518-6521.
93. Kramer, R. A., Tomchak, L. A., McAndrew, S. J., Becker, K., Hug, D., Pasamontes, L., and Humbelin, M. (1993) An Eimeria tenella gene encoding a protein with homology to the nucleotide transhydrogenase of Escherichia coli and bovine mitochondria, Mol. Biochem. Parasitol. 60, 327-332.
94. Vermeulen, A. N., Kok, J. J., Van Den Boogart, P., Dijkema, R., and Claessens, J. A. J. (1993) Eimeria refractile body proteins contain two potential functional charcteristics: Transhydrogenase and carbohydrate transport, FEMS Micobiol. Lett. 110, 223-230.
95. Weston, C. J., Venning, J. D., and Jackson, J. B. (2002) The membrane-peripheral subunits of transhydrogenase from Entamoeba histolytica are functional only when dimerized, J. Biol. Chem. 277, 26163-26170.
96. Weston, C. J., White, S. A., and Jackson, J. B. (2001) The unusual transhydrogenase of Entamoeba histolytica, FEBS Lett. 488, 51-54.