Conformational diversity in NAD(H) and interacting transhydrogenase nicotinamide nucleotide binding domains

Journal of Molecular Biology

Volumn 346, Issue 2, 2005, Pages 617-629

  Sundaresan, Vidyasankar ^a   Chartron, Justin ^a   Yamaguchi, Mutsuo ^a   Stout, C David ^a  

^a SCRIPPS RESEARCH INSTITUTE   (United States)

Author keywords

cocrystal structure; interacting nicotinamides; NAD binding domain; NADP binding domain; proton translocating transhydrogenase

Indexed keywords

NICOTINAMIDE ADENINE DINUCLEOTIDE (PHOSPHATE) TRANSHYDROGENASE; NUCLEOTIDE; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE;

ARTICLE; BINDING AFFINITY; CONFORMATIONAL TRANSITION; CRYSTAL STRUCTURE; ENZYME SUBSTRATE; MOLECULAR INTERACTION; NUCLEOTIDE BINDING SITE; OXIDATION REDUCTION REACTION; PRIORITY JOURNAL; PROTEIN DOMAIN; PROTEIN FOLDING; PROTEIN METABOLISM; PROTEIN PROTEIN INTERACTION; PROTEIN STRUCTURE; PROTON TRANSPORT; STEREOCHEMISTRY; STEREOSPECIFICITY;

RHODOSPIRILLUM; RHODOSPIRILLUM RUBRUM;

EID: 12544250957     PISSN: 00222836     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.jmb.2004.11.070     Document Type: Article

References (58)

1. Y. Hatefi, and M. Yamaguchi The energy-transducing nicotinamide nucleotide transhydrogenase L. Ernster Molecular Mechanisms in Bioenergetics 1992 Elsevier Science Publishers B.V. Amsterdam 265 281
2. Y. Hatefi, and M. Yamaguchi Nicotinamide nucleotide transhydrogenase: a model for utilization of substrate binding energy for proton translocation (1996) FASEB J. 10 1996 444 452
3. J.B. Jackson, S.A. White, P.G. Quirk, and J.D. Venning The alternating site, binding change mechanism for proton translocation by transhydrogenase Biochemistry 41 2002 4173 4185
4. T. Bizouarn, O. Fjellström, J. Meuller, M. Axelsson, A. Bergkvist, and C. Johansson Proton translocating nicotinamide nucleotide transhydrogenase from E. coli: mechanism of action deduced from its structural and catalytic properties Biochim. Biophys. Acta 1457 2000 211 228
5. J.B. Hoek, and J. Rydström Physiological roles of nicotinamide nucleotide transhydrogenase Biochem. J. 254 1988 1 10
6. V. Maddaiah Glutathione correlates with lipid peroxidation in live mitochondria of triiodothyronine-injected hypophysectomized rats FASEB J. 4 1990 1513 1518
7. A. Meister Mitochondrial changes associated with glutathione deficiency Biochim. Biophys. Acta 1271 1995 35 42
8. J.W. Hickman, R.D. Barber, E.P. Skaar, and T.J. Donohue Link between the membrane-bound pyridine nucleotide transhydrogenase and glutathione-dependent processes in Rhodobacter sphaeroides J. Bacteriol. 184 2002 400 409
9. M. Yamaguchi, and Y. Hatefi Energy-transducing nicotinamide nucleotide transhydrogenase: nucleotide binding properties of the purified enzyme and proteolytic fragments J. Biol. Chem. 268 1993 17871 17877
10. J.M. Clarke, T.W. Loo, S. Gillam, and P.D. Bragg Nucleotide sequence of the pntA and pntB genes encoding the pyridine nucleotide transhydrogenase of Escherichia coli Eur. J. Biochem. 158 1986 647 653
11. M. Yamaguchi, and Y. Hatefi Energy-transducing nicotinamide nucleotide transhydrogenase: nucleotide sequences of the genes and predicted amino acid sequences of the subunits of the enzyme from Rhodospirillum rubrum J. Bioenerg. Biomembr. 26 1994 435 445
12. D.M. Clarke, and P.D. Bragg Purification and properties of reconstitutively active nicotinamide nucleotide transhydrogenase of Escherichia coli Eur. J. Biochem. 149 1985 517 523
13. +-nicotinamide nucleotide transhydrogenase from Rhodobacter capsulatus Eur. J. Biochem. 197 1991 247 255
14. J. Meuller, and J. Rydström The membrane topology of proton-pumping Escherichia coli transhydrogenase determined by cysteine labeling J. Biol. Chem. 274 1999 19072 19080
15. P.D. Bragg, and C. Hou Mutation of conserved polar residues in the transmembrane domain of the proton-pumping pyridine nucleotide transhydrogenase of Escherichia coli Arch. Biochem. Biophys. 363 1999 182 190
16. M. Yamaguchi, C.D. Stout, and Y. Hatefi The proton channel of the energy-transducing nicotinamide nucleotide transhydrogenase of Escherichia coli J. Biol. Chem. 277 2002 33670 33675
17. M. Yamaguchi, and C.D. Stout Essential glycine in the proton channel of Escherichia coli transhydrogenase J. Biol. Chem. 278 2003 45333 45339
18. C. Hou, and P.D. Bragg Intersubunit crosslinking of the heterotetrameric proton-translocating pyridine nucleotide transhydrogenase of Escherichia coli defines intersubunit contacts between transmembrane helices of the β subunits Biochem. Biophys. Res. Commun. 280 2001 466 470
19. T. Bizouarn, M. Althage, A. Pedersen, A. Tigerström, J. Karlsson, C. Johansson, and J. Rydström The organization of the membrane domain and its interaction with the NADP(H)-binding site in proton-translocating transhydrogenase from E. coli Biochim. Biophys. Acta 1555 2002 122 127
20. M. Althage, T. Bizouarn, B. Kindlund, J. Mullins, J. Ålander, and J. Rydström Crosslinking of transmembrane helices in proton-translocating nicotinamide nucleotide transhydrogenase from Escherichia coli. Implications for the structure and function of the membrane domain Biochim. Biophys. Acta 1659 2004 73 82
21. O. Fjellström, C. Johansson, and J. Rydström Structural and catalytic properties of the expressed and purified NAD(H)- and NADP(H)-binding domains of the proton-pumping transhydrogenase from Escherichia coli Biochemistry 36 1997 11331 11341
22. G.S. Prasad, V. Sridhar, M. Yamaguchi, Y. Hatefi, and C.D. Stout Crystal structure of transhydrogenase domain III at 1.2 Å Resolution Nature Struct. Biol. 6 1999 1126 1131
23. P.G. Quirk, M. Jeeves, N.P.J. Cotton, J.K. Smith, and J.B. Jackson Structural changes in the recombinant, NADP(H)-binding component of proton translocating transhydrogenase revealed by NMR spectroscopy FEBS Lett. 446 1999 127 132
24. C. Johansson, A. Bergkvist, O. Fjellström, J. Rydström, and B.G. Karlsson NMR characterization of the NADP(H)-binding domain of Escherichia coli transhydrogenase: sequential assignment and global fold FEBS Lett. 458 1999 180 184
25. S.A. White, S.J. Peake, S. McSweeney, G. Leonard, N.P.J. Cotton, and J.B. Jackson The high-resolution structure of the NADP(H)-binding component (dIII) of proton-translocating transhydrogenase from human heart mitochondria Structure 8 2000 1 12
26. M. Jeeves, K.J. Smith, P.G. Quirk, N.P.J. Cotton, and J.B. Jackson Solution structure of the NADP(H)-binding component (dIII) of proton-translocating transhydrogenase from Rhodospirillum rubrum Biochim. Biophys. Acta 1459 2000 248 257
27. V. Sundaresan, M. Yamaguchi, J. Chartron, and C.D. Stout Conformational change in the NADP(H) binding domain of transhydrogenase defines four states Biochemistry 42 2003 12143 12153
28. A. Bergkvist, C. Johansson, T. Johansson, J. Rydström, and B.G. Karlsson 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 2000 12595 12605
29. P.A. Buckley, J.B. Jackson, T. Schneider, S.A. White, D.W. Rice, and P.J. Baker Protein-protein recognition, hydride transfer and proton pumping in the transhydrogenase complex Structure 8 2000 809 815
30. G.S. Prasad, M. Wahlberg, V. Sridhar, V. Sundaresan, M. Yamaguchi, Y. Hatefi, and C.D. Stout Crystal structures of transhydrogenase domain I with and without bound NADH Biochemistry 41 2002 12745 12754
31. M. Yamaguchi, and Y. Hatefi Proton-translocating nicotinamide nucleotide transhydrogenase: reconstitution of the extramembranous nucleotide binding domains J. Biol. Chem. 270 1995 28165 28168
32. M. Yamaguchi, and Y. Hatefi High cyclic transhydrogenase activity catalyzed by expressed and reconstituted nucleotide-binding domains of Rhodospirillum rubrum transhydrogenase Biochim. Biophys. Acta 1318 1997 225 234
33. O. Fjellström, T. Bizouarn, J.-W. Zhang, J. Rydström, J.D. Venning, and J.B. Jackson Catalytic properties of hybrid complexes of the NAD(H)-binding and NADP(H)-binding domains of the proton-translocating transhydrogenases from Escherichia coli and Rhodospirillum rubrum Biochemistry 38 1999 415 422
34. J.D. Venning, S.J. Peake, P.G. Quirk, and J.B. Jackson Stopped-flow reaction kinetics of recombinant components of proton-translocating transhydrogenase with physiological nucleotides J. Biol. Chem. 275 2000 19490 19497
35. T.J.T. Pinheiro, J.D. Venning, and J.B. Jackson Fast hydride transfer in proton-translocating transhydrogenase revealed in a rapid mixing continuous flow device J. Biol. Chem. 276 2001 44757 44761
36. N.P.J. Cotton, S.A. White, S.J. Peake, S. McSweeney, and J.B. Jackson The crystal structure of an asymmetric complex of the two nucleotide binding components of proton-translocating transhydrogenase Structure 9 2001 165 176
37. J.D. Venning, D.J. Rodrigues, C.J. Weston, N.P.J. Cotton, P.G. Quirk, and N. Errington The heterotrimer of the membrane-peripheral components of transhydrogenase and the alternating-site mechanism of proton translocation J. Biol. Chem. 276 2001 30678 30685
38. O.C. Mather, A. Singh, G.I. van Boxel, S.A. White, and J.B. Jackson Active-site conformational changes associated with hydride transfer in proton-translocating transhydrogenase Biochemistry 43 2004 10952 10964
39. E.E. Scott, Y.A. He, M.R. Wester, M.A. White, C.C. Chin, and J.R. Halpert An open conformation of mammalian cytochrome P450 2B4 at 1.6 Å resolution Proc. Natl Acad. Sci. USA 100 2003 13196 13201
40. E.E. Scott, M.A. White, Y.A. He, E.F. Johnson, C.D. Stout, and J.R. Halpert Structure of mammalian cytochrome P450 2B4 complexed with 4-(4-chlorophenyl)imidazole at 1.9 Å resolution: insight into the range of P450 conformations and coordination of redox partner binding J. Biol. Chem. 279 2004 27294 27301
41. 1 Nature 392 1998 677 684
42. J.B. Jackson, P.G. Quirk, N.P.J. Cotton, J.D. Venning, S. Gupta, and T. Bizouarn Interdomain hydride transfer in proton-translocating transhydrogenase Biochim. Biophys. Acta 1365 1998 79 86
43. I.F. Sevrioukova, H. Li, and T.L. Poulos Crystal structure of putidaredoxin reductase from Pseudomonas putida, the final structural component of the cytochrome P450cam monooxygenase J. Mol. Biol. 336 2004 889 902
44. Y.-D. Wu, D.K.W. Lai, and K.N. Houk 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 1995 4100 4108
45. L. Young, and C.B. Post Catalysis by entropic guidance from enzymes Biochemistry 35 1996 15129 15133
46. K. Deng, A. Aliverti, G. Zanetti, A.K. Arakak, J. Ottado, and E.G. Orellano A productive NADP binding mode of ferredoxin-NADP reductase revealed by protein engineering and crystallographic studies Nature Struct. Biol. 6 1999 847 853
47. J.J. Barycki, L.K. O'Brien, A.W. Strauss, and L.J. Banaszak Sequestration of the active site by interdomain shifting: crystallographic and spectroscopic evidence for distinct conformations of L-3-hydroxyacyl-CoA dehydrogenase J. Biol. Chem. 275 2000 27186 27196
48. G.I. van Boxel, P.G. Quirk, N.P.J. Cotton, S.A. White, and J.B. Jackson Glutamine 132 in the NAD(H)-binding component of proton-translocating transhydrogenase tethers the nucleotides before hydride transfer Biochemistry 42 2003 1217 1226
49. A. Singh, J.D. Venning, P.G. Quirk, G.I. van Boxel, D.J. Rodrigues, S.A. White, and J.B. Jackson 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 2003 33208 33216
50. D.J. Rodrigues, J.D. Venning, P.G. Quirk, and J.B. Jackson A change in ionization of the NADP(H)-binding component (dIII) of proton-translocating transhydrogenase regulates both hydride transfer and nucleotide release Eur. J. Biochem. 268 2001 1430 1438
51. D.J. Rodrigues, and J.B. Jackson A conformational change in the isolated NADP(H)-binding component (dIII) of transhydrogenase induced by low pH: a reflection of events during proton translocation by the complete enzyme? Biochim. Biophys. Acta 1555 2002 8 13
52. A. Pedersen, J. Karlsson, M. Althage, and J. Rydström Properties of the apo-form of the NADP(H)-binding domain III of proton-pumping Escherichia coli transhydrogenase: implications for the reaction mechanism of the intact enzyme Biochim. Biophys. Acta 1604 2003 55 59
53. A.G.W. Leslie The CCP4 suite: programs for protein crystallography Acta Crystallog. D50 1994 760 763
54. R.J. Read Pushing the boundaries of molecular replacement with maximum likelihood Acta Crystallog. D57 2001 1373 1382
55. A.T. Brünger, P.D. Adams, G.M. Clore, W.L. DeLano, P. Gros, and R.W. Grosse-Kunstleve System: a new software suite for macromolecular structure determination Acta Crystallog. D54 1998 905 921
56. D.E. McRee XtalView/Xfit - a versatile program for manipulating atomic coordinates and electron density J. Struct. Biol. 125 1999 156 165
57. J.R. Somoa, A. Szöke, and H. Szöke A simple method for calculating electron-density maps Acta Crystallog. A57 2001 678 680
58. W.L. DeLano The PyMOL Molecular Graphics System 2002 DeLano Scientific San Carlos, CA, USA