Flavin fluorescence dynamics and photoinduced electron transfer in Escherichia coli glutathione reductase

Biophysical Journal

Volumn 74, Issue 4, 1998, Pages 2046-2058

  Van Den Berg, Petra A W ^a,b   Van Hoek, Arie ^a,b   Walentas, Christopher D ^a,b   Perham, Richard N ^a,b   Visser, Antonie J W G ^a,b  

^a WAGENINGEN UNIVERSITY   (Netherlands)

^b UNIVERSITY OF CAMBRIDGE   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

BACTERIAL ENZYME; DIHYDROLIPOAMIDE DEHYDROGENASE; FLAVINE ADENINE NUCLEOTIDE; GLUTATHIONE REDUCTASE; MUTANT PROTEIN; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE PHOSPHATE; TYROSINE;

ANISOTROPY; ARTICLE; CONTROLLED STUDY; DEPOLARIZATION; DYNAMICS; ELECTRON TRANSPORT; ENZYME STRUCTURE; ESCHERICHIA COLI; FLUORESCENCE; LIGHT; NONHUMAN; TEMPERATURE DEPENDENCE;

BACTERIA (MICROORGANISMS); ESCHERICHIA; ESCHERICHIA COLI;

EID: 0031953365     PISSN: 00063495     EISSN: None     Source Type: Journal    
DOI: 10.1016/S0006-3495(98)77911-1     Document Type: Article

References (79)

1. Alcala, J. R., E. Gratton, and F. G. Prendergast. 1987. Interpretation of fluorescence decays in proteins using continuous lifetime distributions. Biophys. J. 51:925-936.
2. Bailey, S., A. H. Fairlamb, and W. N. Hunter. 1994. Structure of trypanothione reductase from Crithidia fasciculata at 2.6 Å resolution: enzymeNADP interactions at 2.8 Å resolution. Acta Crystallogr. D. 50: 139-154.
3. Bajzer, Z. and F. G. Prendergast. 1993. A model for multiexponential tryptophan fluorescence intensity decay in proteins. Biophys. J. 65: 2313-2323.
4. Barbara, P. F., T. J. Meyer, and M. A. Ratner. 1996. Contemporary issues in electron transfer research. J. Phys. Chem. 100:13148-13168.
5. Barry, B. A., and G. T. Babcock. 1987. Tyrosine radicals are involved in the photosynthetic oxygen-evolving system. Proc. Natl. Acad. Sci. USA. 84:7099-7103.
6. Bashir, A., R. N. Perham, N. S. Scrutton, and A. Berry. 1995. Altering kinetic mechanism and enzyme stability by mutagenesis of the dimer interface of glutathione reductase. Biochem. J. 312:527-533.
7. Bastiaens, P. I. H., A. van Hoek, J. A. E. Benen, J. C. Brochon, and A. J. W. G. Visser. 1992a. Conformational dynamics and intersubunit energy transfer in wild-type and mutant lipoamide dehydrogenase from Azotobacter vinelandii. Biophys. J. 63:839-853.
8. Bastiaens, P. I. H., A. van Hoek, W. F. Wolkers, J. C. Brochon, and A. J. W. G. Visser. 1992b. Comparison of the dynamical structures of lipoamide dehydrogenase and glutathione reductase by time-resolved polarized flavin fluorescence. Biochemistry. 31:7050-7060.
9. Beechem, J. M., and L. Brand. 1985. Time-resolved fluorescence of proteins. Annu. Rev. Biochem. 54:43-71.
10. Benen, J., W. van Berkel. Z. Zak. T. Visser, C. Veeger, and A. de Kok. 1991. Lipoamide dehydrogenase from Azotobacter vinelandii: sitedirected mutagenesis of the His450-Glu455 diad. Spectral properties of wild type and mutated enzymes. Eur. J. Biochem. 202:863-872.
11. Berry, A., N. S. Scrutton, and R. N. Perham. 1989. Switching kinetic mechanism and putative proton donor by directed mutagenesis of glutathione reductase. Biochemistry. 28:1264-1269.
12. Bismuto, E., G. Irace. I. Sirangelo, and H. Gratton. 1996. Pressure-induced perturbation of ANS-apomyoglobin complex: frequency domain fluorescence studies on native and acidic compact states. Protein Sci. 5:121-126.
13. Boussac, A., and A. L. Etienne. 1984. Midpoint potential of signal II (slow) in tris-washed photosystem-II particles. Biochim. Biophys. Acta. 766: 576-581.
14. Bradbury, S. L., and W. B. Jakoby. 1972. Glycerol as an enzymestabilizing agent: effects on aldchyde dehydrogenase. Proc. Natl. Acad. Sci. USA. 69:2373-2376.
15. Brochon, J. C. 1994. Maximum entropy method of data analysis in timeresolved spectroscopy. Methods Enzymol. 240:262-311.
16. Calcaterra, N. B., G. A. Picó. E. G. Orcllano, J. Ottado, N. Carrillo, and E. A. Ceccarelli. 1995. Contribution of the FAD binding site residue tyrosine 308 to the stability of pea ferredoxin-NADP' oxidoreductase. Biochemistry. 34:12842-12848.
17. Careri, G., P. Fasella, and E. Gratton. 1979. Enzyme dynamics: the statistical physics approach. Annu. Rev. Biophys. Bioeng. 8:69-97.
18. Deonarain, M. P., A. Berry, N. S. Scrutton, and R. N. Perham. 1989. Directed mutagenesis of the redox-active disulphide bridge in glutathione reductase from Esrherichia coli. Biochemistry. 28:9602-9607.
19. Deonarain, M. P., N. S. Scrutton, A. Berry, and R. N. Perham. 1990. Alternative proton donors/acceptors in the catalytic mechanism of the glutathione reductase of Escherichia coli: the role of histidine-439 and tyrosine-99. Proc. R. Soc. Lond. B. 241:179-186.
20. Draper, R. D., and L. L. Ingraham. 1968. A potentiometric study of the flavin semiquinone equilibrium. Arch. Biochem. Biophys. 125:802-808.
21. Ekberg, M., M. Sahlin, M. Eriksson, and B.-M. Sjöberg. 1996. Two conserved tyrosine residues in protein R1 participate in an intermolecular electron transfer in ribonucleotide reductase. J. Biol. Chem. 271: 20655-20659.
22. Ermler, U., and G. E. Schulz. 1991. The three-dimensional structure of glutathione reductase from Escherichia coli at 3.0 Å resolution. Proteins Struct, Funct. Genet. 9:174-179.
23. farreira, S. T., L. Stella, and E. Gratton. 1994. Conformational dynamics of bovine Cu. Zn Superoxide dismutase revealed by time-resolved fluorescence spectroscopy of the single tyrosine residue, Biophys. J. 66: 1185-1196
24. Rauenfelder, H., and E. Gratton. 1986. Protein dynamics and hydration. Methods Enzymol. 127:207-216.
25. Frauenleideer H., F. Parak, and R. D. Young. 1988. Conformational substates in proteins. Annu. Rev. Biophys. Biophys. Chem. 17:451-479.
26. Frauenfelder, H., S. G. Sligar, and P. G. Wolynes. 1991. The energy landscapes and motions of proteins. Science. 254:1598-1603.
27. Gekko, K., and S. N. Timasheff. 1981a. Mechanism of protein stabilization by glycerol: preferential hydration in glycerol-water mixtures. Biochemistry. 20:4667-4676.
28. Gekko, K., and S. N. Timasheff. 1981b. Thermodynamic and kinetic examination of protein stabilization by glycerol. Biochemistry. 20: 4677-4686.
29. Greer, S., and R. N. Perham. 1986. Glutathione reductase from Escherichia coli: cloning and sequence analysis of the gene and relationship to other flavoprotein disulfide oxidoreductases. Biochemistry. 25:2736-2742.
30. Harriman, A. 1987. Further comments on the redox potentials of tryptoPhan and tyrosine. J. Phys. Chem. 91:6102-6104.
31. Holmgren, A. 1985. Thioredoxin. Annu. Rev. Biochem. 54:237-271.
32. Larabak, J., A. E. Seeds, Jr., and P. Talalay. 1966. Reversible cold inactivation of 17β-hydroxysteroid dehydrogenase of human placenta: pro- rective effect of glycerol. Biochemistry. 5:1269-1279.
33. Karen, T. Sawada, F. Tanaka, and N. Mataga. 1987. Dynamics of Photobiol flavo proteins-picosecond laser photolysis studies. Photochem. photobiol 45:49-53.
34. +-reductase: prototype for a structurally novel flavoenzyme family. Science. 251:60-66.
35. Karplus M., and J. A. McCammon. 1983. Dynamics of proteins: elements and function. Annu. Rev. Biochem. 53:263-300.
36. Karplus. P. A., and G. E. Schulz. 1987. Refined structure of glutathione reductase at 1.54 Å resolution. J. Mol. Biol. 195:701-729.
37. Karplus, P. A., and G. E. Schulz. 1989. Suhstrate binding and catalysis by glutathione reductase as derived from refined enzyme:substrate crystal structures at 2 Å resolution. J. Mol. Biol. 210:163-180.
38. Li. R., M. A. Bianchet, P. Talalay, and L. M. Amzel. 1995. The three-dimensional structure of NAD(P)H:quinone reductase. a flavoprotein involved in cancer chemoprotection and chemotherapy: mechanism of the two-electron reduction. Proc. Natl. Acad. Sci. USA. 92:8846-8850.
39. Livesey, A. K., and J. C. Brochon. 1987. Analyzing the distribution of decay constants in pulse-fluorimetry using the maximum entropy method. Biophys. J. 52:693-706.
40. Maeda-Yorita, K., G. C. Russell, J. R. Guest, V. Massey, and C. H. Williams, Jr. 1991. Properties of lipoamide dehydrogenase altered by site-directed mutagenesis at a key residue (1184Y) in the pyridine nucleotide binding domain. Biochemistry. 30:11788-11795.
41. Marcus, R. A. 1956. On the theory of oxidation-reduction reactions involving electron transfer. J. Chem. Phys. 24:966-978.
42. Marcus, R. A., and N. Sutin. 1985. Electron transfers in chemistry and biology. Biochim. Biophys. Acta. 811:265-322.
43. Mattevi, A., A. J. Schierheek, and W. G. Hol. 1991. Refined crystal structure of lipoamide dehydrogenase from Azotobacter vinelandii at 2.2 Å resolution. A comparison with the structure of glutathione reductase. J. Mol. Biol. 220:975-994.
44. Mérola, F., R. Rigler, A. Holmgren, and J. C. Brochon. 1989. Picosecond tryptophan fluorescence of thioredoxin: evidence for discrete species in slow exchange. Biochemistry. 28:3383-3398.
45. Millar, D. P. 1996. Time-resolved fluorescence spectroscopy. Curr. Opin. Struct. Biol. 6:637-642.
46. Mittl, P. R. F., and G. E. Schulz. 1994. Structure of glutathione reductase from Escherichia coli at 1.86 Å resolution: comparison with the enzyme from human erythrocytes. Protein Sci. 3:799-809.
47. Moser, C. C., J. M. Keske, K. Warncke, R. S. Hand, and P. L. Dutton. 1992. Nature of biological electron transfer. Nature. 355:796-802.
48. O'Connor, D. V., and D. Phillips. 1984. Time-Correlated Single Photon Counting. Academic Press. London.
49. O'Donnell, M. E., and C. H. Williams, Jr. 1983. Proton stoichiometry in the reduction of the FAD and disulfide of Escherichia coli thioredoxin reductase. J. Biol. Chem. 258:13795-13805.
50. Ogle, T. F. 1983. Action of glycerol and sodium molyhdate in stabilization of the progesterone receptor from rat trophoblast. J. Biol. Chem. 258: 4982-4988.
51. Pai, E. F., P. A. Karplus, and G. E. Schulz. 1988. Crystallographic analysis of the binding of NADPH. NADPH fragments, and NADPH analogues to glutathione reductase. Biochemistry. 27:4465-4474.
52. Pai, E. F., and G. E. Schulz. 1983. The catalytic mechanism of glutathione reductase as derived from x-ray diffraction analyses of reaction intermediates. J. Biol. Chem. 258:1752-1757.
53. Parsonage, D., and A. Claiborne. 1995. Analysis of the kinetic and redox properties of NADH peroxidase C42S and C42A mutants lacking the cysteine- sulfenic acid redox center. Biochemistry. 34:435-441.
54. Pourplanche, C., C. Lambert, M. Berjot, J. Marx, C. Chopard, A. J. P. Alix, and V. Larreta-Garde. 1994. Conformational changes of lipoxygenase (LOX) in modified environments. J. Biol. Chem. 269:31585-31591.
55. Priev, A., A. Almagor, S. Yedgar, and B. Gavish. 1996. Glycerol decreases the volume and compressibility of protein interior. Biochemistry. 35: 2061-2066.
56. Prince, R. C. 1988. Tyrosine radicals. Trends Biochem. Sci. 13:286-288.
57. Raibekas, A. A., and V. Massey. 1996. Glycerol-induced development of catalytically active conformation of Crotalus adamanteus L-amino acid oxidase m vitro. Proc. Natl. Acad. Sci. USA. 93:7546-7551.
58. Rehm, D., and A. Weller. 1970. Kinetics of fluorescence quenching by electron and H-atom transfer. Israel J. Chem. 8:259-271.
59. Reichard, P., and A. Ehrenberg. 1983. Ribonucleotide reductase - a radical enzyme. Science. 221:514-519.
60. Rice, D. W., G. E. Schulz, and J. R. Guest. 1984. Structural relationship between glutathione reductase and lipoamide dehydrogenase. J. Mol. Biol. 174:483-496.
61. Scrutton, N. S., A. Berry, and R. N. Perham. 1987. Purification and characterization of glutathionc rcductase encoded by a cloned and overexpressed gene in Escherichia coli. Biochem. J. 245:875-880.
62. Scrutton, N. S., A. Berry, and R. N. Perham. 1990. Redesign of the coenzyme specificity of a dehydrogenase by protein engineering. Nature. 343:38-43.
63. + binding at 2.25 Å resolution. J. Mol. Biol. 263:20-39.
64. Sicmiaraczuk, A., B. D. Wagner, and W. R. Ware. 1990. Comparison of the maximum entropy and exponential series methods for the recovery of distributions of lifetimes from fluorescence lifetime data. J. Phys. Chem. 94:1661-1666.
65. Thieme, R., E. F. Pai, R. H. Schirmer, and G. E. Schulz. 1981. Threedimensional structure of glutathione reductase at 2 Å resolution. J. Mol. Biol. 152:763-782.
66. Timasheff. S. N. 1993. The control of protein stability and association by weak interactions with water: how do solvents affect these processes? Annu. Rev. Biophys. Bimnol. Struct. 22:67-97.
67. Timasheff, S. N., J. C. Lee, E. P. Pittz., and N. Tweedy. 1976. The interaction of tubulin and other proteins with structure-stabilizing solvents. J. Colloid Interface Sci. 55:658-663.
68. van Hoek, A., and A. J. W. G. Visser. 1985. Artefact and distortion sources in time correlated single photon counting. Anal. Instrum. 14:359-378.
69. van Hoek, A., and A. J. W. G. Visser. 1992. Cw dye laser synchronously pumped by the third harmonic of a mode-locked cw Nd:YLF laser for tunable blue and green excitation and picosecond time-correlated photon counting detection. Proc. SPIE. 1640:325-329.
70. van Hoek, A., K. Vos, and A. J. W. G. Visser. 1987. Ultrasensitive time-resolved polarized fluorescence spectroscopy as a tool in biology and medicine. IEEF. J. Quantum Electron. QE-2.3:1812-1820.
71. Visser, A. J. W. G., and J. Lee. 1980. Lumazine protein from the biola- minescent bacterium Phoiobacterium phosphoreum. A fluorescence study of the protein-ligand equilibrium. Biochemistry. 19:4366-4372
72. Visser, A. J. W. G., A. van Hoek, T. Kulinski, and J. Le Gall. 1987 Time-resolved fluorescence studies of flavodoxin. Demonstration of a picosecond fluorescence lifetimes of FMN in Desulfovibrio flavodoxins FEBS Lett. 224:406-410.
73. Vos, K., A. van Hoek, and A. J. W. G. Visser. 1987. Application of a reference convolution method to tryptophan fluorescence in proteins. A refined description of rotational dynamics. Eur. J. Biochem. 165:55-63.
74. Welch, G. R., B. Somogyi, and S. Damjanovich. 1982. The role of protein fluctuations in enzyme action: a review. Prog. Biophys. Mol. Biol. 39:109-146.
75. Wilkinson, K. D., and C. H. Williams, Jr. 1979. Evidence for multiple electronic forms of two-electron-reduced lipoamide dchydrogenase from Kscherichia coli. J. Biol. Chem. 254:852-862.
76. Williams, C. H., Jr. 1976. Flavin-containing dehydrogenases. In The Enzymes, 3rd Ed., Vol. 13. P. D. Boyer, editor. Academic Press, New York. 89-173.
77. Williams, C. H., Jr. 1992. Lipoamide dehydrogenase. glutathione reductase. thioredoxin reductase, and mercuric ion reductase - a family of flavoenzyme transhydrogenases. In Chemistry and Biochemistry of Flavoenzymes. Vol 3. F. Müller, editor. CRC Press, Boca Raton, FL. 121-213.
78. 2 escape from respiratory proteins as a function of cosolvent molecular weight. Biophys. J. 68:665-670.
79. Zhang, Y., C. S. Bond, S. Bailey, M. L. Cunningham, A. H. Fairlamb, and W. N. Hunter. 1996. The crystal structure of trypanothione reductase from the human pathogen Trypanosoma cruzi at 2.3 Ä resolution. Protein Sci. 5:52-61.