Transient protein interactions studied by NMR spectroscopy: The case of cytochrome c and adrenodoxin

Biochemistry

Volumn 42, Issue 23, 2003, Pages 7068-7076

  Worrall, Jonathan A R ^a   Reinle, Wolfgang ^b   Bernhardt, Rita ^b   Ubbink, Marcellus ^a  

^a LEIDEN UNIVERSITY   (Netherlands)

^b SAARLAND UNIVERSITY   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

COMPLEXATION; NUCLEAR MAGNETIC RESONANCE SPECTROSCOPY; PERTURBATION TECHNIQUES;

BOVINE ADRENODOXIN;

PROTEINS;

ADRENODOXIN; AMIDE; AMINO ACID; CYTOCHROME B5; CYTOCHROME C; CYTOCHROME C PEROXIDASE; HEME; MYOGLOBIN;

AMINO ACID SEQUENCE; ARTICLE; COMPLEX FORMATION; LIFESPAN; MOLECULAR RECOGNITION; NONHUMAN; NUCLEAR MAGNETIC RESONANCE SPECTROSCOPY; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN DOMAIN; PROTEIN PROTEIN INTERACTION;

ADRENODOXIN; AMIDES; ANIMALS; BINDING SITES; CATTLE; CYTOCHROME C GROUP; HEME; HYDROPHOBICITY; ISOENZYMES; MODELS, MOLECULAR; NITROGEN ISOTOPES; NUCLEAR MAGNETIC RESONANCE, BIOMOLECULAR; SACCHAROMYCES CEREVISIAE; TITRIMETRY;

BOVINAE;

EID: 0038470801     PISSN: 00062960     EISSN: None     Source Type: Journal    
DOI: 10.1021/bi0342968     Document Type: Article

References (58)

1. Bendall, D. S. (1996) Interprotein Electron Transfer, in Protein Electron Transfer (Bendall, D. S., Ed.) pp 43-68, BIOS Scientific Publishers, Oxford, U.K.
2. Chapman, S. K., Knox, C. V., and Sykes, A. G. (1984) Kinetic studies on 1:1 electron-transfer reactions involving blue copper proteins. Part 10. The assignment of binding sites in the reactions of plastocyanin (and azurin) with non-physiological protein redox partners, J. Chem. Soc., Dalton Trans., 2775-2780.
3. Modi, S., He, S. P., Gray, J. C., and Bendall, D. S. (1992) The role of surface exposed Tyr-83 of plastocyanin in electron-transfer form cytochrome c, Biochim. Biophys. Acta 1101, 64-68.
4. Peerey, L. M., and Kostic, N. M. (1989) Oxidoreduction reactions involving the electrostatic and the covalent complex of cytochrome c and plastocyanin: importance of the protein rearrangement for the intracomplex electron-transfer reaction, Biochemistry 28, 1861-1868.
5. Zhou, J. S., and Kostic, N. M. (1992) Photoinduced electron-transfer from zinc cytochrome c to plastocyanin is gated by surface-diffusion within the metalloprotein complex, J. Am. Chem. Soc. 114, 3562-3563.
6. Pletneva, E. V., Fulton, D. B., Kohzuma, T., and Kostic, N. M. (2000) Protein docking and gated electron-transfer reactions between zinc cytochrome c and the new plastocyanin from the fern Dryopteris crassirhizoma. Direct kinetic evidence for multiple binary complexes, J. Am. Chem. Soc. 122, 1034-1046.
7. Ubbink, M., and Bendall, D. S. (1997) Complex of plastocyanin and cytochrome c characterized by NMR chemical shift analysis, Biochemistry 36, 6326-6335.
8. Crowley, P. B., Vintonenko, N., Bullerjahn, G. S., and Ubbink, M. (2002) Plastocyanin-cytochrome f interactions: The influence of hydrophobic patch mutations studied by NMR spectroscopy, Biochemistry 41, 15698-15705.
9. 5, J. Am. Chem. Soc. 124, 6849-6859.
10. 5: A nuclear magnetic resonance study of a highly dynamic protein complex, Biochemistry 41, 11721-11730.
11. Crowley, P. B., Rabe, K. S., Worrall, J. A. R., Canters, G. W., and Ubbink, M. (2002) The ternary complex of cytochrome f and cytochrome c: Identification of a second binding site and competition for plastocyanin binding, ChemBioChem 3, 526-533.
12. 5: Effect of methylating the heme propionates of Zn-myoglobin, J. Am. Chem. Soc. 122, 3552-3553.
13. 5, J. Biol. Inorg. Chem. 7, 580-588.
14. 5, J. Am. Chem. Soc. 124, 4008-4019.
15. Grinberg, A. V., Hannemann, F., Schiffler, B., Müller, J., Heinemann, U., and Bernhardt, R. (2000) Adrenodoxin: structure, stability, and electron transfer properties, Proteins 40, 590-612.
16. Bernhardt, R. (1996) Cytochrome P450: structure, function, and generation of reactive oxygen species, Rev. Physiol., Biochem. Pharmacol. 127, 137-221.
17. Miura, S., and Ichikawa, Y. (1991) Proton nuclear magnetic resonance investigation of adrenodoxin. Assignment of aromatic resonances and evidence for a conformational similarity with ferredoxin from Spirulina platensis, Eur. J. Biochem. 197, 747-775.
18. Pikuleva, I. A., Tesh, K., Waterman, M. R., and Kim, Y. (2000) The tertiary structure of full-length bovine adrenodoxin suggests functional dimers, Arch. Biochem. Biophys. 373, 44-55.
19. Müller, J. J., Lapko, A., Bourenkov, G., Ruckpaul, K., and Heinemann, U. (2001) Adrenodoxin reductase-adrenodoxin complex structure suggests electron transfer path in steroid biosynthesis, J. Biol. Chem. 276, 2786-2789.
20. Cupp, J. R., and Vickery, L. E. (1989) Adrenodoxin with a COOH-terminal deletion (des 116-128) exhibits enhanced activity, J. Biol. Chem. 264, 1602-1607.
21. Uhlmann, H., Kraft, R., and Bernhardt, R. (1994) C-terminal region of adrenodoxin affects its structural integrity and determines differences in its electron transfer function to cytochrome P-450, J. Biol. Chem. 269, 22557-22564.
22. Omura, T., Sanders, E., and Estabrook, R. W. (1966) Isolation from adrenal cortex of a nonheme iron protein and a flavoprotein functional as a reduced triphospyridine nucleotide-cytochrome P-450 reductase, Arch. Biochem. Biophys. 117, 660-673.
23. Lambeth, J. D., Seybert, D. W., and Kamin, H. (1979) Ionic effects in adrenal steroidogenic electron transport, J. Biol. Chem. 254, 7255-7264.
24. Geren, L. M., O'Brien, P., Stoneheuerner, J., and Millet, F. (1984) Identification of specific carboxylate groups on adrenodoxin that are involved in the interaction with adrenodoxin reductase, J. Biol. Chem. 259, 2155-2160.
25. Coghlan, V. M., and Vickery, L. E. (1991) Site-specific mutations in human ferredoxin that affect binding to ferredoxin reductase and cytochrome P450scc, J. Biol. Chem. 266, 18606-18612.
26. Lambeth, J. D., and Kamin, H. (1979) Adrenodoxin reductase: adrenodoxin complex Flavin to iron-sulfur transfer as the rate-limiting step in the NADPH-cytochrome c reductase reaction, J. Biol. Chem. 254, 2766-2774.
27. Zuiderweg, E. R. P. (2002) Mapping protein-protein interactions in solution by NMR spectroscopy, Biochemistry 41, 1-7.
28. Guiles, R. D., Sarma, S., DiGate, R. J., Banville, D., Basus, V. J., Kuntz, I. D., and Waskell, L. (1996) Pseudocontact shifts used in the restraint of the solution structures of electron transfer complexes, Nat. Struct. Biol. 3, 333-339.
29. Morelli, X., Dolla, A., Czjek, M., Palma, P. N., Blasco, F., Krippahl, L., Moura, J. J. G., and Guerlesquin, F. (2000) Heteronuclear NMR and soft docking: An experimental approach for a structural model of the cytochrome c(553)-ferredoxin complex, Biochemistry 39, 2530-2537.
30. 5 with cytochrome c, Biochemistry 39, 14025-14039.
31. Hall, D. A., Kooi, C. W. V., Stasik, C. N., Stevens, S. Y., Zuiderweg, E. R. P., and Matthews, R. G. (2001) Mapping the interactions between flavodoxin and its physiological partners flavodoxin reductase and cobalamin-dependent methionine synthase, Proc. Natl. Acad. Sci. U.S.A. 98, 9521-9526.
32. Arnesano, F., Banci, L., Bertini, I., Cantini, F., Ciofi-Baffoni, S., Huffman, D. L., and O'Halloran, T. V. (2001) Characterization of the binding interface between the copper chaperone Atx1 and the first cystolic domain of Ccc2 ATPase, J. Biol. Chem. 276, 41365-41376.
33. 6 and cytochrome f: Characterized by NMR, J. Biol. Chem. 277, 48685-48689.
34. 1H] heteronuclear NMR spectroscopy, Biochemistry 40, 7069-7076.
35. Pollock, W. B. R., Rosell, F. I., Twitchett, M. B., Dumont, M. E., and Mauk, A. G. (1998) Bacterial expression of mitochondrial cytochrome c. Trimethylation of Lys72 in yeast iso-1-cytochrome c and the alkaline conformational transition, Biochemistry 37, 6124-6131.
36. 15N-labeled eukaryotic cytochrome c in Escherichia coli, J. Biol. Inorg. Chem. 4, 220-222.
37. Margoliash, E., and Frohwirt, N. (1959) Spectrum of horse-heart cytochrome c, Biochem. J. 71, 570-572.
38. Kimura, T. (1968) Biochemical aspects of iron-sulfur linkage in non-heme iron proteins, with special reference to "adrenodoxin", Struct. Bonding 5, 1-40.
39. 1H 2D-NMR spectra by interactive computer-graphics, J. Magn. Reson. 84, 627-633.
40. Kraulis, P. J., Domaille, P. J., Campbell-Burk, S. L., Van Aken, T., and Laue, E. D. (1994) Solution structure and dynamics of Ras P21-center-DOT-GDP determined by heteronuclear 3-Dimensional and 4-Dimensional NMR spectroscopy, Biochemistry 33, 3515-3531.
41. 15N signals of bovine adrenodoxin, J. Biomol. NMR 17, 355-356.
42. Andersson, P., Gsell, B., Wipf, B., Senn, H., and Otting, G. (1998) HMQC and HSQC experiments with water flip-back optimized for large proteins, J. Biomol. NMR 11, 278-288.
43. Kannt, A., Young, S., and Bendall, D. S. (1996) The role of acidic residues of plastocyanin in its interaction with cytochrome f, Biochim. Biophys. Acta 1277, 115-126.
44. Garrett, D. S., Seok, Y. J., Liao, D. I., Peterkofsky, A., Gronenborn, A. M., and Clore, G. M. (1997) Solution structure of the 30 kDa N-terminal domain of enzyme I of the Escherichia coli phosphoenolpyruvate: sugar phosphotransferase system by multidimensional NMR, Biochemistry 36, 2517-2530.
45. Bertini, I., Luchinat, C., and Rosato, A. (1999) NMR spectra of iron-sulfur proteins, Adv. Inorg. Chem. 47, 251-282.
46. Louie, G. V., and Brayer, G. D. (1990) High-resolution refinement of yeast iso-1-cytochrome c and comparisons with other eukaryotic cytochromes c, J. Mol. Biol. 214, 527-555.
47. Nicholls, A., Sharp, K., and Honig, B. (1991) Protein folding and association: insights from the interfacial and thermodynamic properties of hydrocarbons, Proteins 11, 281-296.
48. Müller, A., Müller, J. J., Muller, Y. A., Uhlmann, H., Bernhardt, R., and Heinemann, U. (1998) New aspects of electron transfer revealed by the crystal structure of a truncated bovine adrenodoxin, Adx(4-108), Structure 6, 269-280.
49. Kostic, M., Pochapsky, S. S., Obenauer, J., Mo, H., Pagani, G. M., Pejchal, R., and Pochapsky, T. C. (2002) Comparison of functional domains in vertebrate-type ferredoxins, Biochemistry 41, 5978-5989.
50. Xia, B., Volkman, B. F., and Markley, J. L. (1998) Evidence for oxidation-state-dependent conformational changes in human ferredoxin from multinuclear, multidimensional NMR spectroscopy, Biochemistry 37, 3965-3973.
51. Ubbink, M., Ejdeback, M., Karlsson, B. G., and Bendall, D. S. (1998) The structure of the complex of plastocyanin and cytochrome f, determined by paramagnetic NMR and restrained rigid-body molecular dynamics, Structure 6, 323-335.
52. Crowley, P. B., Otting, G., Schlarb-Ridley, B. G., Canters, G. W., and Ubbink, M. (2001) Hydrophobic interactions in a cyanobacterial plastocyanin-cytochrome f complex, J. Am. Chem. Soc. 123, 10444-10453.
53. Pelletier, H., and Kraut, J. (1992) Crystal structure of a complex between electron transfer partners, cytochrome c peroxidase and cytochrome c, Science 258, 1748-1755.
54. 2, J. Biol. Inorg. Chem. 3, 246-252.
55. Hannemann, F., Rottmann, M., Schiffler, B., and Bernhardt, R. (2001) The loop region covering the iron-sulfur cluster in bovine adrenodoxin comprises a new interaction site for redox partners, J. Biol. Chem. 276, 1369-1375.
56. cam-putidaredoxin interactions, Biochimie 78, 723-733.
57. cam. Theory and experiments, J. Am. Chem. Soc. 120, 8927-8932.
58. Beckert, V., Schrauber, H., Bernhardt, R., Van Dijk, A. A., Kakoschke, C., and Wray, V. (1995) Mutational effects on the spectroscopic properties and biological activities of oxidized bovine adrenodoxin, and their structural implications, Eur. J. Biochem. 231, 226-235.