The two-domain structure of 5′-adenylylsulfate (APS) reductase from Enteromorpha intestinalis is a requirement for efficient APS reductase activity

Biochemistry

Volumn 46, Issue 2, 2007, Pages 591-601

  Kim, Sung Kun ^a   Gomes, Varinnia ^b   Gao, Yu ^b,d   Chandramouli, Kala ^c   Johnson, Michael K ^c   Knaff, David B ^a   Leustek, Thomas ^b  

^a TEXAS TECH UNIVERSITY   (United States)

^b RUTGERS UNIVERSITY   (United States)

^c UNIVERSITY OF GEORGIA   (United States)

^d Biotech Center ^*  (United States)

Author keywords

[No Author keywords available]

Indexed keywords

AMINO TERMINAL DOMAINS; ENTEROMORPHA INTESTINALIS (EIAPR); GLUTATHIONE; HETEROLOGOUS SYSTEMS;

CATALYSIS; ELECTRON TRANSITIONS; KETONES; NUCLEIC ACIDS; PROTEINS; REACTION KINETICS;

ENZYME KINETICS;

ADENOSINE 5' PHOSPHOSULFATE; ADENYLYLSULFATE REDUCTASE; ALGAL PROTEIN; BACTERIAL ENZYME; BUFFER; DISULFIDE; GLUTAREDOXIN; GLUTATHIONE; HYBRID PROTEIN; IRON SULFUR PROTEIN; OXIDOREDUCTASE; RIBONUCLEOTIDE REDUCTASE; SODIUM SULFATE; SULFITE; THIOREDOXIN; UNCLASSIFIED DRUG;

AMINO TERMINAL SEQUENCE; ARTICLE; CARBOXY TERMINAL SEQUENCE; CONTROLLED STUDY; ELECTRON TRANSPORT; ENTEROMORPHA INTESTINALIS; ENZYME ACTIVE SITE; ENZYME ACTIVITY; ENZYME STRUCTURE; NONHUMAN; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; PROTEIN DOMAIN; PROTEIN EXPRESSION; PROTEIN PROTEIN INTERACTION; PSEUDOMONAS AERUGINOSA; REDUCTION; STRUCTURE ACTIVITY RELATION;

ALGAL PROTEINS; AMINO ACID SEQUENCE; BACTERIAL PROTEINS; BASE SEQUENCE; DNA, ALGAL; DNA, BACTERIAL; KINETICS; MODELS, BIOLOGICAL; MOLECULAR SEQUENCE DATA; OXIDATION-REDUCTION; OXIDOREDUCTASES ACTING ON SULFUR GROUP DONORS; PROTEIN STRUCTURE, TERTIARY; PSEUDOMONAS AERUGINOSA; RECOMBINANT FUSION PROTEINS; SEQUENCE HOMOLOGY, AMINO ACID; SPECTROPHOTOMETRY; ULVA;

PSEUDOMONAS AERUGINOSA; ULVA INTESTINALIS;

EID: 33846254144     PISSN: 00062960     EISSN: None     Source Type: Journal    
DOI: 10.1021/bi0618971     Document Type: Article

References (33)

1. Berendt, U., Haverkamp, T., Prior, A., and Schwenn, J. D. (1995) Reaction mechanism of thioredoxin: 3′-Phospho-adenylylsulfate reductase investigated by site-directed mutagenesis, Eur. J. Biochem. 233, 347-356.
2. Koprivova, A., Meyer, A. J., Schween, G., Herschbach, C., Reski, R., and Kopriva, S. (2002) Functional knockout of the adenosine 5′-phosphosulfate reductase gene in Physcomitrella patens revives an old route of sulfate assimilation, J. Biol. Chem. 277, 32195-32201.
3. Lillig, C. H., Prior, A., Schwenn, J. D., Aslund, F., Ritz, D., Vlamis-Gardikas, A., and Holmgren, A. (1999) New thioredoxins and glutaredoxins as electron donors of 3′-phosphoadenylylsulfate reductase, J. Biol. Chem. 274, 7695-7698.
4. Bick, J. A., Dennis, J. J., Zylstra, G. J., Nowack, J., and Leustek, T. (2000) Identification of a new class of 5′-adenylylsulfate (APS) reductases from sulfate-assimilating bacteria, J. Bacteriol. 182, 135-142.
5. Carroll, K. S., Gao, H., Chen, H., Stout, C. D., Leary, J. A., and Bertozzi, C. R. (2005) A conserved mechanism for sulfonucleotide reduction, PLoS Biol. 3, e250.
6. Kim, S. K., Rahman, A., Bick, J. A., Conover, R. C., Johnson, M. K., Mason, J. T., Hirasawa, M., Leustek, T., and Knaff, D. B. (2004) Properties of the cysteine residues and iron-sulfur cluster of the assimilatory 5′-adenylyl sulfate reductase from Pseudomonas aeruginosa, Biochemistry 43, 13478-13486.
7. Kopriva, S., Buchert, T., Fritz, G., Suter, M., Benda, R., Schunemann, V., Koprivova, A., Schurmann, P., Trautwein, A. X., Kroneck, P. M., and Brunold, C. (2002) The presence of an iron-sulfur cluster in adenosine 5′-phosphosulfate reductase separates organisms utilizing adenosine 5′-phosphosulfate and phosphoadenosine 5′-phosphosulfate for sulfate assimilation, J. Biol. Chem. 277, 21786-21791.
8. Berndt, C., Lillig, C. H., Wollenberg, M., Bill, E., Mansilla, M. C., de Mendoza, D., Seidler, A., and Schwenn, J. D. (2004) Characterization and reconstitution of a 4Fe-4S adenylyl sulfate/ phosphoadenylyl sulfate reductase from Bacillus subtilis, J. Biol. Chem. 279, 7850-7855.
9. Setya, A., Murillo, M., and Leustek, T. (1996) Sulfate reduction in higher plants: Molecular evidence for a novel 5′-adenylylsulfate reductase, Proc. Natl. Acad. Sci. U.S.A. 93, 13383-13388.
10. Gutierrez-Marcos, J. F., Roberts, M. A., Campbell, E. I., and Wray, J. L. (1996) Three members of a novel small gene-family from Arabidopsis thaliana able to complement functionally an Escherichia coli mutant defective in PAPS reductase activity encode proteins with a thioredoxin-like domain and "APS reductase" activity, Proc. Natl Acad. Sci. U.S.A. 93, 13377-13382.
11. Kopriva, S., Buchert, T., Fritz, G., Suter, M., Weber, M., Benda, R., Schaller, J., Feller, U., Schurmann, P., Schunemann, V., Trautwein, A. X., Kroneck, P. M., and Brunold, C. (2001) Plant adenosine 5′-phosphosulfate reductase is a novel iron-sulfur protein, J. Biol. Chem. 276, 42881-42886.
12. Gao, Y., Schofield, O. M., and Leustek, T. (2000) Characterization of sulfate assimilation in marine algae focusing on the enzyme 5′- adenylylsulfate reductase, Plant Physiol 123, 1087-1096.
13. Kim, S. K., Rahman, A., Conover, R. C., Johnson, M. K., Mason, J. T., Gomes, V., Hirasawa, M., Moore, M. L., Leustek, T., and Knaff, D. B. (2006) Properties of the cysteine residues and the iron-sulfur cluster of the assimilatory 5′-adenylyl sulfate reductase from Enteromorpha intestinalis, Biochemistry 45, 5010-5018.
14. Bick, J. A., Aslund, F., Chen, Y., and Leustek, T. (1998) Glutaredoxin function for the carboxyl-terminal domain of the plant-type 5′- adenylylsulfate reductase, Proc. Natl. Acad. Sci. U.S.A. 95, 8404-8409.
15. Carroll, K. S., Gao, H., Chen, H., Leary, J. A., and Bertozzi, C. R. (2005) Investigation of the iron-sulfur cluster in Mycobacterium tuberculosis APS reductase: Implications for substrate binding and catalysis, Biochemistry 44, 14647-14657.
16. Kim, S. K., Rahman, A., Mason, J. T., Hirasawa, M., Conover, R. C., Johnson, M. K., Miginiac-Maslow, M., Keryer, E., Knaff, D. B., and Leustek, T. (2005) The interaction of 5′-adenylylsulfate reductase from Pseudomonas aeruginosa with its substrates, Biochim. Biophys. Acta 1710, 103-112.
17. Weber, M., Suter, M., Brunold, C., and Kopriva, S. (2000) Sulfate assimilation in higher plants characterization of a stable intermediate in the adenosine 5′-phosphosulfate reductase reaction, Eur. J. Biochem. 267, 3647-3653.
18. Sun, Q. A., Su, D., Novoselov, S. V., Carlson, B. A., Hatfield, D. L., and Gladyshev, V. N. (2005) Reaction mechanism and regulation of mammalian thioredoxin/glutathione reductase, Biochemistry 44, 14528-14537.
19. Rouhier, N., Gama, F., Wingsle, G., Gelhaye, E., Gans, P., and Jacquot, J.-P. (2006) Engineering functional artificial hybrid proteins between poplar peroxiredoxin II and glutaredoxin or thioredoxin, Biochem. Biophys. Res. Commun. 341, 1300.
20. Li, X., Nield, J., Hayman, D., and Langridge, P. (1995) Thioredoxin activity in the C terminus of Phalaris S protein, Plant J. 8, 133-138.
21. Prior, A., Uhrig, J. F., Heins, L., Wiesmann, A., Lillig, C. H., Stoltze, C., Soll, J., and Schwenn, J. D. (1999) Structural and kinetic properties of adenylyl sulfate reductase from Catharanthus roseus cell cultures, Biochim. Biophys. Acta 1430, 25-38.
22. Kanno, N., Nagahisa, E., Sato, M., and Sato, Y. (1996) Adenosine 5′-phosphosulfate sulfotransferase from the marine macroalga Porphyra yezoensis Ueda (Rhodophyta) - Stabilization, purification, and properties, Planta 198, 440-446.
23. Schmidt, A. (1975) A sulfotransferase from spinach leaves using adenosine-5′-phosphosulfate, Planta 124, 267-275.
24. Bradford, M. M. (1976) A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding, Anal. Biochem. 72, 248-254.
25. 13C NMR, Eur. J. Biochem. 255, 185-195.
26. Hirasawa, M., Schurmann, P., Jacquot, J. P., Manieri, W., Jacquot, P., Keryer, E., Hartman, F. C., and Knaff, D. B. (1999) Oxidation-reduction properties of chloroplast thioredoxins, ferredoxin: thioredoxin reductase, and thioredoxin f-regulated enzymes, Biochemistry 38, 5200-5205.
27. Setterdahl, A. T., Goldman, B. S., Hirasawa, M., Jacquot, P., Smith, A. J., Kranz, R. G., and Knaff, D. B. (2000) Oxidation-reduction properties of disulfide-containing proteins of the Rhodobacter capsulatus cytochrome c biogenesis system, Biochemistry 39, 10172-10176.
28. Massey, V. (1957) Studies on succinic dehydrogenase. VII. Valency state of the iron in beef heart succinic dehydrogenase, J. Biol. Chem. 229, 763-770.
29. King, T. E., and Morris, R. O. (1967) Determination of acid-labile sulfide and sulfhydryl groups, Methods Enzymol. 10, 634-641.
30. 4 clusters: Resonance Raman evidence for different degrees of distortion in HiPIP and ferredoxin, J. Am. Chem. Soc. 109, 7178-7187.
31. Bick, J. A., Setterdahl, A. T., Knaff, D. B., Chen, Y., Pitcher, L. H., Zilinskas, B. A., and Leustek, T. (2001) Regulation of theplant-type 5′-adenylyl sulfate reductase by oxidative stress, Biochemistry 40, 9040-9048.
32. Melander, W. R., Corradini, D., and Horvath, C. (1984) Salt-mediated retention of proteins in hydrophobia-interaction chromatography. Application of solvophobic theory, J. Chromatogr. 317, 67-85.
33. Holmgren, A. (1979) Glutathione-dependent synthesis of deoxyribonucleotides. Characterization of the enzymatic mechanism of Escherichia coli glutaredoxin, J. Biol Chem. 254, 3672-3678.