Acid-base catalysis in the mechanism of thioredoxin reductase from Drosophila melanogaster

Biochemistry

Volumn 47, Issue 6, 2008, Pages 1721-1731

  Huang, Hsin Hung ^a   Arscott, L David ^a   Ballou, David P ^a   Williams Jr , Charles H ^a  

^a UNIVERSITY OF MICHIGAN MEDICAL SCHOOL   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CATALYSIS; DIMERS; MONOMERS; NUCLEOTIDES;

DROSOPHILA MELANOGASTER; GLUTATHIONE REDUCTASE; MALARIA VECTOR;

ENZYME ACTIVITY;

GLUTATHIONE REDUCTASE; HISTIDINE; HOMODIMER; MONOMER; NUCLEOTIDASE; OXIDOREDUCTASE; PYRIDINE; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE PHOSPHATE; THIOREDOXIN; THIOREDOXIN REDUCTASE;

ACID BASE BALANCE; AMINO TERMINAL SEQUENCE; ANOPHELES GAMBIAE; ANTIOXIDANT ACTIVITY; ARTICLE; CATALYSIS; COMPLEX FORMATION; DROSOPHILA MELANOGASTER; ELECTRON TRANSPORT; ENZYME ACTIVE SITE; MOLECULAR INTERACTION; NONHUMAN; OXIDATION REDUCTION REACTION; PH; PKA; PRIORITY JOURNAL; REACTION ANALYSIS; WILD TYPE;

ANIMALS; CATALYSIS; DROSOPHILA MELANOGASTER; HYDROGEN-ION CONCENTRATION; KINETICS; THIOREDOXIN-DISULFIDE REDUCTASE;

ANOPHELES GAMBIAE; DIPTERA; DROSOPHILA MELANOGASTER; HEXAPODA;

EID: 38949097496     PISSN: 00062960     EISSN: None     Source Type: Journal    
DOI: 10.1021/bi702040u     Document Type: Article

References (53)

1. Williams, C. H. (1992) Lipoamide Dehydrogenase, Glutathione Reductase, Thioredoxin Reductase, and Mercuric Ion Reductase: A Family of Flavoenzyme Transhydrogenase, Vol. 3, CRC Press, Inc., Boca Raton, FL.
2. Williams, C. H., Arscott, L. D., Muller, S., Lennon, B. W., Ludwig, M. L., Wang, P. F., Veine, D. M., Becker, K., and Schirmer, R. H. (2000) Thioredoxin reductase: Two modes of catalysis have evolved, Eur. J. Biochem. 267, 6110-6117.
3. Moore, E. C., Reichard, P., and Thelander, L. (1964) Enzymatic synthesis of deoxyribonucleotides, V. Purification and properties of thioredoxin reductase from Escherichia coli B, J. Biol. Chem. 239, 3445-3452.
4. Watson, W. H., Yang, X., Choi, Y. E., Jones, D. P., and Kehrer, J. P. (2004) Thioredoxin and its role in toxicology, Toxicol. Sci. 78, 3-14.
5. Mau, B. L., and Powis, G. (1992) Inhibition of cellular thioredoxin reductase by diaziquone and doxorubicin. Relationship to the inhibition of cell proliferation and decreased ribonucleotide reductase activity, Biochem. Pharmacol. 43, 1621-1627.
6. Bertini, R., Howard, O. M., Dong, H. F., Oppenheim, J. J., Bizzarri, C., Sergi, R., Caselli, G., Pagliei, S., Romines, B., Wilshire, J. A., Mengozzi, M., Nakamura, H., Yodoi, J., Pekkari, K., Gurunath, R., Holmgren, A., Herzenberg, L. A., and Ghezzi, P. (1999) Thioredoxin, a redox enzyme released in infection and inflammation, is a unique chemoattractant for neutrophils, monocytes, and T cells, J. Exp. Med. 189, 1783-1789.
7. Gromer, S., Urig, S., and Becker, K. (2004) The thioredoxin system: From science to clinic, Med. Res. Rev. 24, 40-89.
8. Burke-Gaffney, A., Callister, M. E., and Nakamura, H. (2005) Thioredoxin: Friend or foe in human disease? Trends Pharmacol. Sci. 26, 398-404.
9. Boschi-Muller, S., Olry, A., Antoine, M., and Branlant, G. (2005) The enzymology and biochemistry of methionine sulfoxide reductases, Biochim. Biophys. Acta 1703, 231-238.
10. Gon, S., Faulkner, M. J., and Beckwith, J. (2006) In vivo requirement for glutaredoxins and thioredoxins in the reduction of the ribonucleotide reductases of Escherichia coli, Antioxid. Redox Signaling 8, 735-742.
11. Yodoi, J., Masutani, H., and Nakamura, H. (2001) Redox regulation by the human thioredoxin system, Biofactors 15, 107-111.
12. Nguyen, P., Awwad, R. T., Smart, D. D., Spitz, D. R., and Gius, D. (2006) Thioredoxin reductase as a novel molecular target for cancer therapy, Cancer Lett. 236, 164-174.
13. Berndt, C., Lillig, C. H., and Holmgren, A. (2007) Thiol-based mechanisms of the thioredoxin and glutaredoxin systems: Implications for diseases in the cardiovascular system, Am. J. Physiol. Heart Circ. Physiol. 292, 1227-1236.
14. Chae, H. Z., Chung, S. J., and Rhee, S. G. (1994) Thioredoxin-dependent peroxide reductase from yeast, J. Biol. Chem. 269, 27670-27678.
15. Kanzok, S. M., Fechner, A., Bauer, H., Ulschmid, J. K., Muller, H. M., Botella-Munoz, J., Schneuwly, S., Schirmer, R., and Becker, K. (2001) Substitution of the thioredoxin system for glutathione reductase in Drosophila melanogaster, Science (Washington, DC, U.S.) 291, 643-646.
16. Bauer, H., Gromer, S., Urbani, A., Schnolzer, M., Schirmer, R. H., and Muller, H. M. (2003) Thioredoxin reductase from the malaria mosquito Anopheles gambiae, Eur. J. Biochem. 270, 4272-4281.
17. Bauer, H., Kanzok, S. M., and Schirmer, R. H. (2002) Thioredoxin-2 but not thioredoxin-1 is a substrate of thioredoxin peroxidase-1 from Drosophila melanogaster: Isolation and characterization of a second thioredoxin in D. melanogaster and evidence for distinct biological functions of Trx-1 and Trx-2, J. Biol. Chem. 277, 17457-17463.
18. Thelander, L. (1967) Thioredoxin reductase. Characterization of a homogenous preparation from Escherichia coli B, J. Biol. Chem. 242, 852-859.
19. Luthman, M., and Holmgren, A. (1982) Rat liver thioredoxin and thioredoxin reductase: Purification and characterization, Biochemistry 21, 6628-6633.
20. Zanetti, G., and Williams, C. H., Jr. (1967) Characterization of the active center of thioredoxin reductase, J. Biol. Chem. 242, 5232-5236.
21. Thelander, L. (1968) Studies on thioredoxin reductase from Escherichia coli B. The relation of structure and function, Eur. J. Biochem. 4, 407-419.
22. Arscott, L. D., Gromer, S., Schirmer, R. H., Becker, K., and Williams, C. H., Jr. (1997) The mechanism of thioredoxin reductase from human placenta is similar to the mechanisms of lipoamide dehydrogenase and glutathione reductase and is distinct from the mechanism of thioredoxin reductase from Escherichia coli, Proc. Natl. Acad. Sci. U.S.A. 94, 3621-3626.
23. Zhong, L., Arner, E. S., and Holmgren, A. (2000) Structure and mechanism of mammalian thioredoxin reductase: The active site is a redox-active selenolthiol/selenenylsulfide formed from the conserved cysteine-selenocysteine sequence, Proc. Natl. Acad. Sci. U.S.A. 97, 5854-5859.
24. Zhong, L., and Holmgren, A. (2000) Essential role of selenium in the catalytic activities of mammalian thioredoxin reductase revealed by characterization of recombinant enzymes with selenocysteine mutations, J. Biol. Chem. 275, 18121-18128.
25. Lennon, B. W., Williams, C. H., Jr., and Ludwig, M. L. (2000) Twists in catalysis: Alternating conformations of Escherichia coli thioredoxin reductase, Science (Washington, DC, U.S.) 289, 1190-1194.
26. Sandalova, T., Zhong, L., Lindqvist, Y., Holmgren, A., and Schneider, G. (2001) Three-dimensional structure of a mammalian thioredoxin reductase: Implications for mechanism and evolution of a selenocysteine-dependent enzyme, Proc. Natl. Acad. Sci. U.S.A. 98, 9533-9538.
27. Gromer, S., Johansson, L., Bauer, H., Arscott, L. D., Rauch, S., Ballou, D. P., Williams, C. H., Jr., Schirmer, R. H., and Arner, E. S. (2003) Active sites of thioredoxin reductases: Why selenoproteins? Proc. Natl. Acad. Sci. U.S.A. 100, 12618-12623.
28. Biterova, E. I., Turanov, A. A., Gladyshev, V. N., and Barycki, J. J. (2005) Crystal structures of oxidized and reduced mitochondrial thioredoxin reductase provide molecular details of the reaction mechanism, Proc. Natl. Acad. Sci. U.S.A. 102, 15018-15023.
29. Eckenroth, B. E., Rould, M. A., Hondal, R. J., and Everse, S. J. (2007) Structural and biochemical studies reveal differences in the catalytic mechanisms of mammalian and Drosophila melanogaster thioredoxin reductases, Biochemistry 46, 4694-4705.
30. Bauer, H., Massey, V., Arscott, L. D., Schirmer, R. H., Ballou, D. P., and Williams, C. H., Jr. (2003) The mechanism of high Mr thioredoxin reductase from Drosophila melanogaster, J. Biol. Chem. 278, 33020-33028.
31. McMillan, P. J., Arscott, L. D., Ballou, D. P., Becker, K., Williams, C. H., Jr., and Muller, S. (2006) Identification of acid-base catalytic residues of high-Mr thioredoxin reductase from Plasmodium falciparum, J. Biol. Chem. 281, 32967-32977.
32. Sahlman, L., and Williams, C. H., Jr. (1989) Titration studies on the active sites of pig heart lipoamide dehydrogenase and yeast glutathione reductase as monitored by the charge transfer absorbance, J. Biol. Chem. 264, 8033-8038.
33. Matthews, R. G., Ballou, D. P., Thorpe, C., and Williams, C. H., Jr. (1977) Ion pair formation in pig heart lipoamide dehydrogenase: Rationalization of pH profiles for reactivity of oxidized enzyme with dihydrolipoamide and 2-electron-reduced enzyme with lipoamide and iodoacetamide, J. Biol. Chem. 252, 3199-3207.
34. Pai, E. F., and Schulz, G. E. (1983) The catalytic mechanism of glutathione reductase as derived from X-ray diffraction analyses of reaction intermediates, J. Biol. Chem. 258, 1752-1757.
35. Karplus, P. A., and Schulz, G. E. (1987) Refined structure of glutathione reductase at 1.54 Å resolution, J. Mol. Biol. 195, 701-729.
36. Karplus, P. A., and Schulz, G. E. (1989) Substrate binding and catalysis by glutathione reductase as derived from refined enzyme: Substrate crystal structures at 2 Å resolution, J. Mol. Biol. 210, 163-180.
37. Gromer, S., Wessjohann, L. A., Eubel, J., and Brandt, W. (2006) Mutational studies confirm the catalytic triad in the human selenoenzyme thioredoxin reductase predicted by molecular modeling, ChemBiochem 7, 1649-1652.
38. Fritz-Wolf, K., Urig, S., and Becker, K. (2007) The structure of human thioredoxin reductase 1 provides insights into C-terminal rearrangements during catalysis, J. Mol. Biol. 370, 116-127.
39. Cheng, Z., Arscott, L. D., Ballou, D. P., and Williams, C. H., Jr. (2007) The relationship of the redox potentials of thioredoxin and thioredoxin reductase from Drosophila melanogaster to the enzymatic mechanism: Reduced thioredoxin is the reductant of glutathione in Drosophila, Biochemistry 46, 7875-7885.
40. Kooter, I. M., Steiner, R. A., Dijkstra, B. W., van Noort, P. I., Egmond, M. R., and Huber, M. (2002) EPR characterization of the mononuclear Cu-containing Aspergillus japonicus quercetin 2,3-dioxygenase reveals dramatic changes upon anaerobic binding of substrates, Eur. J. Biochem. 269, 2971-2979.
41. Benen, J., van Berkel, W., Dieteren, N., Arscott, D., Williams, C., Jr., Veeger, C., and de Kok, A. (1992) Lipoamide dehydrogenase from Azotobacter vinelandii: Site-directed mutagenesis of the His450-Glu455 diad. Kinetics of wild-type and mutated enzymes, Eur. J. Biochem. 207, 487-497.
42. Rietveld, P., Arscott, L. D., Berry, A., Scrutton, N. S., Deonarain, M. P., Perham, R. N., and Williams, C. H., Jr. (1994) Reductive and oxidative half-reactions of glutathione reductase from Escherichia coli, Biochemistry 33, 13888-13895.
43. Johnson, F. A., Lewis, S. D., and Shafer, J. A. (1981) Determination of a low pK for histidine-159 in the S-methylthio derivative of papain by proton nuclear magnetic resonance spectroscopy, Biochemistry 20, 44-48.
44. Lewis, S. D., Johnson, F. A., and Shafer, J. A. (1981) Effect of cysteine-25 on the ionization of histidine-159 in papain as determined by proton nuclear magnetic resonance spectroscopy. Evidence for a His-159-Cys-25 ion pair and its possible role in catalysis, Biochemistry 20, 48-51.
45. Chivers, P. T., and Raines, R. T. (1997) General acid/base catalysis in the active site of Escherichia coli thioredoxin, Biochemistry 36, 15810-15816.
46. Tsukada, H., and Blow, D. M. (1985) Structure of α-chymotrypsin refined at 1.68 Å resolution, J. Mol. Biol. 184, 703-711.
47. Craik, C. S., Roczniak, S., Largman, C., and Rutter, W. J. (1987) The catalytic role of the active site aspartic acid in serine proteases, Science (Washington, DC, U.S.) 237, 909-913.
48. Krauth-Siegel, R. L., Arscott, L. D., Schonleben-Janas, A., Schirmer, R. H., and Williams, C. H., Jr. (1998) Role of active site tyrosine residues in catalysis by human glutathione reductase, Biochemistry 37, 13968-13977.
49. Wong, K. K., Vanoni, M. A., and Blanchard, J. S. (1988) Glutathione reductase: Solvent equilibrium and kinetic isotope effects, Biochemistry 27, 7091-7096.
50. Linares, G. E., and Rodriguez, J. B. (2007) Current status and progresses made in malaria chemotherapy, Curr. Med. Chem. 14, 289-314.
51. Huber, R. E., and Criddle, R. S. (1967) Comparison of the chemical properties of selenocysteine and selenocystine with their sulfur analogues, Arch. Biochem. Biophys. 122, 164-173.
52. Boggaram, V., and Mannervik, B. (1978) An essential histidine residue in the catalytic mechanism of mammalian glutathione reductase, Biochem. Biophys. Res. Commun. 83, 558-564.
53. Brandt, W., and Wessjohann, L. A. (2005) The functional role of selenocysteine (Sec) in the catalysis mechanism of large thioredoxin reductases: Proposition of a swapping catalytic triad including a Sec-His-Glu state, ChemBiochem 6, 386-394.