Crystal structure of Arabidopsis thaliana NADPH dependent thioredoxin reductase at 2.5 Å resolution

Journal of Molecular Biology

Volumn 264, Issue 5, 1996, Pages 1044-1057

  Shaodong, Dai ^a   Saarinen, Markku ^a   Ramaswamy, S ^a   Meyer, Yves ^b   Jacquot, Jean Pierre ^c   Eklund, Hans ^a  

^a SWEDISH UNIVERSITY OF AGRICULTURAL SCIENCES   (Sweden)

^b UNIVERSITÉ DE PERPIGNAN   (France)

^c INSTITUTE OF PLANT SCIENCES PARIS SACLAY IPS2   (France)

Author keywords

Crystallography; Disulphide oxidoreductase; Flavin adenine dinucleotide; Protein structure; Thioredoxin reductase

Indexed keywords

FLAVINE ADENINE NUCLEOTIDE; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE PHOSPHATE; THIOREDOXIN REDUCTASE;

ARABIDOPSIS; ARTICLE; CRYSTAL STRUCTURE; DISULFIDE BOND; ENZYME STRUCTURE; ENZYME SUBUNIT; ESCHERICHIA COLI; EUKARYOTE; NONHUMAN; PRIORITY JOURNAL; SEQUENCE HOMOLOGY; STEREOCHEMISTRY;

ARABIDOPSIS THALIANA;

EID: 0030596062     PISSN: 00222836     EISSN: None     Source Type: Journal    
DOI: 10.1006/jmbi.1996.0695     Document Type: Article

References (61)

1. + reductase: Structure function relationship as studied by site-directed mutagenesis and X-ray crystallography. Biochemistry, 34, 8371-8379.
2. Ashai, T., Bandurski, R. S. & Wilson, L. G. (1961). Yeast sulfate-reducing system. Reduction of sulfate to sulfite. J. Biol. Chem. 236, 1822-1829.
3. Black, S., Harte, E. M., Hudson, B. & Wartofsky, L. (1960). A specific enzymatic reduction of L(-)methionine sulfoxide and a related nonspecific reduction of disulfides. J. Biol. Chem. 235, 2916-2920.
4. Brünger, T. A., Kuriyan, J. & Karplus, M. (1987). Crystallographic R-factor refinement by molecular dynamics. Science, 235, 458-460.
5. Buchanan, B., Wolosiuk, R. A. & Schürmann, P. (1979). Thioredoxin and enzyme regulation. Trends Biochem. Sci. 4, 93-96.
6. 2 assimilation in oxygenic photosynthesis: the ferredoxin/thioredoxin system. Arch. Biochem. Biophys. 288, 1-9.
7. Cohen, G., Yanko, M., Mislovati, M., Argaman, A., Schreiber, R., Av-Gay, Y. & Aharonowitz, Y. (1993). Thioredoxin-thioredoxin reductase system of Streptomyces davuligerus: sequences, expression, and organization of the genes. J. Bacteriol. 175, 5159-5167.
8. Cohen, G., Argaman, A., Schreiber, R., Mislovati, M. & Aharonowitz, Y. (1994). The thioredoxin system of Penicillum chysogenum and its possible role in penicillin biosynthesis. J. Bacteriol. 176, 973-984.
9. Cowtan, K. (1994). DM. Joint CCP4 and ESF-EACBM Newsletter on Protein Crystallography, 31, 34-38.
10. Decottignies, P., Schmitter, J. M., Dutka, S., Jacquot, J.-P. & Miginiac-Maslow, M. (1991). Characterization and primary structure of a second thioredoxin from the green alga, Chlamydomonas reinhardtii. Eur. J. Biochem. 198, 505-512.
11. Derman, A. I., Prinz, W. A., Belin, D. & Beckwith, J. (1993). Mutations that allow disulfide bond formation in the cytoplasm of Escherichia coli. Science, 262, 1744-1747.
12. Eklund H., Gleason, F. K. & Holmgren, A. (1991). Structural and functional relations among thioredoxins of different species. Proteins: Struct. Funct. Genet. 11, 13-28.
13. Eklund, H., Ingelman, M., Söderberg, B.-O., Uhlin, T., Nordlund, P., Nikkola, M., Joelson, T. & Petratos, K. (1992). The structure of oxidized bacteriophage T4 glutaredoxin (thioredoxin). Refinement of native and mutant proteins. J. Mol. Biol. 228, 596-618.
14. Fleischmann, R. D., Adams, M. D., White, O., Clayton, R. A., Kirkness, E. F., Kerlavage, A. R., Bult, C. J., Tomb, J.-F., Dougherty, B. A., Merrick, J. M., Mckenney, K., Sutton, G., Fitzhugh, W., Fields, C. A., Gocayne, J. D., Scott, J. D., Shirley, R., Liu, L.-I., Glodek, A., Kelley, J. M., Weidman, J. F., Phillips, C. A., Spriggs, T., Hedblom, E., Cotton, M. D., Utterback, T. R., Hanna, M. C., Nguyen, D. T., Saudek, D. M., Brandon, R. C., Fine, L. D., Fritchman, J. L., Fuhrmann, J. L., Geoghagen, N. S. M., Gnehm, C. L., Mcdonald, L. A., Small, K. V., Fraser, C. M., Smith, H. O. & Venter, J. C. (1995). Whole genome random sequencing and assembly of Heamophilus influenzae Rd. Science, 269, 496-512.
15. Fraser, C. M., Gocayne, J. D., White, O., Adams, M. D., Clayton, R. A., Fleischmann, R. D., Bult, C. J., Kerlavage, A. R., Sutton, G., Kelley, J. M., Fritchman, J. L., Weidman, J. F., Small, K. V., Sandusky, M., Fuhrmann, J. L., Nguyen, D. T., Utterback, T. R., Saudek, D. M., Phillips, C. A., Merrick, J. M., Tomb, J.-F., Dougherty, B. A., Bott, K. F., Hu, P.-C., Lucier, T. S., Peterson, S. N., Smith, H. O., Hutchison, C. A. & Venter, J. C. (1995). The minimal gene complement of Mycoplasma genitalium. Science, 270, 397-403.
16. Gasdaska P. Y., Gasdaska, J. R., Coharan S. & Powis, G. (1995). Cloning and sequencing of a human thioredoxin reductase. FEBS Letters, 373, 5-9.
17. Higgins, D. G & Sharp, P. M. (1989). Fast and sensitive multiple sequence alignments on a microcomputer. CABIOS, 5, 151-153.
18. Holmgren, A. (1985). Thioredoxin. Annu. Rev. Biochem. 54, 237-271.
19. Jacquot, J.-P., Rivera-Madrid, R., Marinho, P., Kollarova, M., Le Marechal, P., Miginiac-Maslow, M. & Meyer, Y. (1994). Arabidopsis thaliana NADPH thioredoxin reductase cDNA characterization and expression of the recombinant protein in Escherichia coli. J. Mol. Biol. 235, 1357-1363.
20. Jeng, M.-F., Campbell, A. P., Begley, T., Holmgren, A., Case, D. A., Wright, P. E. & Dyson, H. J. (1994). High-resolution structures of oxidized and reduced Escherichia coli thioredoxin. Structure, 2, 853-868.
21. Jiao, J., Yee, B. C., Wong, J. H., Kobrehel, K. & Buchanan B. B. (1993). Thioredoxin-linked changes in regulatory properties of barley α-amylase/subtilisin inhibitors protein. Plant Physiol. Biochem. 31, 799-804.
22. Jones, T. A., Zou, J. Y., Cowan, S. W. & Kjeldgaard, M. (1991). Improved methods for building protein models in electron density maps and the location of errors in these models. Acta Crystallog. sect A, 47, 110-119.
23. Karplus, P. A. & Schulz, G. E. (1987). Refined structure of glutathione reductase at 1.54 Å resolution. J. Mol. Biol. 195, 701-729.
24. Katti, S. K., LeMaster, D. M. & Eklund, H. (1990). Crystal structure of thioredoxin from E. coli at 1.68 Å resolution. J. Mol. Biol. 212, 167-184.
25. Kraulis, P. (1991). MOLSCRIPT: a program to produce both detailed and schematic plots of protein structures. J. Appl. Crystallog. 24, 946-950.
26. Krause, G., Lundström, J., Barea, J. L., Pueyo, C. & Holmgren, A. (1991). Mimicking the active site of protein disulfide-isomerase by substitution of proline 34 in Escherichia coli thioredoxin. J. Biol. Chem. 266, 9494-9500.
27. Kumar, S., Björnstedt, M. & Holmgren, A. (1992). Selenite is a substrate for calf thymus thioredoxin reductase and thioredoxin and elicits a large non-stoichiometric oxidation of NADPH in the presence of oxygen. Eur. J. Biochem. 207, 435-439.
28. Kuriyan, J., Krishna, T. S. R., Wong, L., Guenther, B., Pahler, A., Williams, C. H. & Model, P. (1991). Convergent evolution of similar function in 2 structurally divergent enzymes. Nature, 352, 172-174.
29. Laurent, T. C, Moore, E. C. & Reichard, P. (1964). Enzymatic synthesis of deoxy-ribonucleotides IV. Isolation and characterization of thioredoxin, the hydrogen donor from Escherichia coli B. J. Biol. Chem. 239, 3436-3444.
30. Luebbers, M. & Andreesen, J. R. (1993). Components of glycine reductase from Eubacterium acidaminophilum. Cloning, sequencing and identification of the genes for thioredoxin reductase, thioredoxin and selenoprotein. Eur. J. Biochem. 217, 791-798.
31. Lundström. J. & Holmgren, A. (1990). Protein disulfideisomerase is a substrate for thioredoxin reductase and has thioredoxin-like activity. J. Biol. Chem. 265, 9114-9120.
32. Luthman. M. & Holmgren, A. (1982). Rat liver thioredoxin and thioredoxin reductase: purification and characterization. Biochemistry, 21, 6628-6633.
33. Martin, J. L., Bardwell, J. C. A. & Kuriyan, J. (1993). Crystal structure of the DsbA protein required for disulfide bond formation in vivo. Nature, 365, 464-468.
34. Mathieu, I., Meyer, J. & Moulis, J. M. (1992). Cloning, sequencing and expression in Escherichia coli of the rubredoxin gene from Clostridium pasteurianum. Biochem. J. 285, 255-262.
35. Matthews, B. W. (1968). Solvent content of protein crystals. J. Mol. Biol. 33, 491-497.
36. Minakuchi, K., Yabushita, T., Masumura, T., Ichihara, K. & Tanaka, K. (1994). Cloning and sequence analysis of a cDNA encoding rice glutaredoxin. FEBS Letters, 337, 157-160.
37. Moore, E. C., Reichard P. & Thelander, L. (1964). Enzymatic synthesis of deoxyribonucleotides. Purification and properties of thioredoxin reductase from Escherichia coli B. J. Biol. Chem. 239, 3445-3453.
38. Morell, S., Follmann, H. & Häberlein, I. (1995). Identification and localization of the first glutaredoxin in leaves of a higher plant. FEBS Letters, 369, 149-152.
39. Navaza, J. (1994). AMoRe: an automated package for molecular replacement. Acta Crystallog. sect. A, 50, 157-163.
40. + reductase family? Evidence for the catalytic role of serine 49 residue. J. Biol. Chem. 271, 16656-16661.
41. O'Donnell, M. E. & Williams, C. H., Jr (1983). Proton stoichiometry in the reduction of the FAD and disulfide of Escherichia coli thioredoxin reductase. J. Biol. Chem. 258, 13795-13805.
42. Oswald, W. (1994). Thesis, Justus Liebig Universität, Frankfurt, Germany.
43. Otwinowski, Z. (1993). Data collection & processing. In Proceedings of the CCP4 Study Weekend (Sawyer, L., Issacs, N. & Bailey, S., eds), pp. 56-62, SERC Daresbury Laboratory, UK.
44. Pai, E. F. (1991). Variations on a theme: the family of FAD-dependent NAD(P)H-(disulphide)-oxidoreductases. Curr. Opin. Struct. Biol. 1, 796-803.
45. Qin, J., Clore, M. & Gronenborn, A. M (1994). The high-resolution three-dimensional solution structures of the oxidized & reduced states of human thioredoxin. Structure, 2, 503-522.
46. Rivera-Madrid, R., Mestres, D., Marinho, P., Jacquot, J. P., Decottignies, P., Miginiac-Maslow, M., & Meyer, Y. (1995). Evidence for five divergent thioredoxin h sequences in Arabidopsis thaliana. Proc. NatlAcad. Sci. USA, 92, 5620-5624.
47. Russel, M. & Model, P. (1988). Sequence of thioredoxin reductase from Escherichia coli. Relation to other flavoprotein disulfide oxidoreductases. J. Biol. Chem. 263, 9015-9019.
48. Russel, M., Model, P. & Holmgren, A. (1990). Thioredoxin or glutaredoxin in Escherichia coli is essential for sulfate reduction but not for deoxyribonucleotide synthesis. J. Bacteriol. 172, 1923-1929.
49. Saarinen M., Gleason F. K. & Eklund H. (1995). Crystal structure of thioredoxin-2 from Anabaena. Structure, 3, 1097-1108.
50. Schulz, G. E., Schirmer, R. H., Sachsenheimer, W. & Pai, E. F. (1978). The structure of the flavoenzyme glutathione reductase. Nature, 273, 120-124.
51. Scrutton, N. S., Berry, A. & Perham, R. N. (1990). Redesign of the coenzyme specificity of a dehydrogenase by protein engineering. Nature, 343, 38-43.
52. Tamura, T. & Stadtman, T. C. (1996). A new seleno-protein from human lung adenocarcinoma cells: purification, properties and thioredoxin reductase activity. Proc. Natl Acad. Sci. USA, 93, 1006-1011.
53. Tsang, M. L.-S. (1981). Assimilatory sulfate reduction in Escherichia coli: identification of the alternate cofactor for adenosine 3′-phosphate 5′-phosphosulfate reductase as glutaredoxin. J. Bacteriol. 146, 1059-1066.
54. Waksman, G., Krishna, T. S. R., Williams, C. H. & Kuriyan, J. (1994). Crystal structure of Escherichia coli thioredoxin reductase refined at 2 Å resolution: Implications for a large conformational change during catalysis. J. Mol. Biol. 236, 800-816.
55. Wang, P. F., Veine, D. M., Ahn, S. H. & Williams, C. H. (1996). A stable mixed disulfide between thioredoxin reductase and its substrate, thioredoxin: Preparation and characterization. Biochemistry, 35, 4812-4819.
56. Weichsel, A., Gasdaska, J. R., Powis, G. & Montfort, W. R. (1996). Crystal structures of reduced, oxidized, and mutated human thioredoxins: evidence for a regulatory homodimer. Structure, 4, 735-751.
57. Wieles, B., Soolingen, D., Holmgren, A., Offringa, R., Ottenhoff, T. & Thole, J. (1995). Unique gene organization of thioredoxin and thioredoxin reductase in Mycobacterium leprae. Mol. Microbiol. 16, 921-929.
58. Wieles B., Dai S.-D., Nikkola, M. & Eklund H. (1996a). A 3-D model for the Mycobacterium leprae thioredoxin/thioredoxin reductase hybrid protein. Thesis of Brigitte Weiles, University of Leiden, 65-77.
59. Wieles, B., Phillip, W., Offringa, R. & Ottenhoff, T. H. M. (1996b). Sequence analysis, expression and functional characterization of the thioredoxin-thioredoxin reductase system of Mycobaterium tuberculosis. Thesis of Brigitte Wieles.
60. Williams, C. H., Jr (1976). Flavin containing dehydrogenases. In The Enzymes (Boyer, P. D., ed.), vol. 13, pp. 89-173, Academic Press, New York.
61. Wong, J. H., Kobrehel, K., Nimbona, C, Yee, B. C, Balogh, A., Kiss, F. & Buchanan, B. B. (1993). Thioredoxin and bread wheat. Cereal. Chem. 70, 113-114.