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Crystal structure of phosphoadenylyl sulphate (PAPS) reductase: a new family of adenine nucleotide alpha hydrolases.

Structure 5 895-906 (1997)
Cited: 25 times
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Abstract

Background

Assimilatory sulphate reduction supplies prototrophic organisms with reduced sulphur for the biosynthesis of all sulphur-containing metabolites. This process is driven by a sequence of enzymatic steps involving phosphoadenylyl sulphate (PAPS) reductase. Thioredoxin is used as the electron donor for the reduction of PAPS to phospho-adenosine-phosphate (PAP) and sulphite. Unlike most electron-transfer reactions, there are no cofactors or prosthetic groups involved in this reduction and PAPS reductase is one of the rare examples of an enzyme that is able to store two electrons. Determination of the structure of PAPS reductase is the first step towards elucidating the biochemical details of the reduction of PAPS to sulphite.

Results

We have determined the crystal structure of PAPS reductase at 2.0 A resolution in the open, reduced form, in which a flexible loop covers the active site. The protein is active as a dimer, each monomer consisting of a central six-stranded beta sheet with alpha helices packing against each side. A highly modified version of the P loop, the fingerprint peptide of mononucleotide-binding proteins, is present in the active site of the protein, which appears to be a positively charged cleft containing a number of conserved arginine and lysine residues. Although PAPS reductase has no ATPase activity, it shows a striking similarity to the structure of the ATP pyrophosphatase (ATP PPase) domain of GMP synthetase, indicating that both enzyme families have evolved from a common ancestral nucleotide-binding fold.

Conclusion

The sequence conservation between ATP sulphurylases, a subfamily of ATP PPases, and PAPS reductase and the similarities in both their mechanisms and folds, suggest an evolutionary link between the ATP PPases and PAPS reductases. Together with the N type ATP PPases, PAPS reductases and ATP sulphurylases are proposed to form a new family of homologous enzymes with adenine nucleotide alpha-hydrolase activity. The open, reduced form of PAPS reductase is able to bind PAPS, whereas the closed oxidized form cannot. A movement between the two monomers of the dimer may allow this switch in conformation to occur.

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Reviews citing this publication (4)

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  1. Identification of a new class of 5'-adenylylsulfate (APS) reductases from sulfate-assimilating bacteria. Bick JA, Dennis JJ, Zylstra GJ, Nowack J, Leustek T. J. Bacteriol. 182 135-142 (2000)
  2. Dimeric dUTPases, HisE, and MazG belong to a new superfamily of all-alpha NTP pyrophosphohydrolases with potential "house-cleaning" functions. Moroz OV, Murzin AG, Makarova KS, Koonin EV, Wilson KS, Galperin MY. J. Mol. Biol. 347 243-255 (2005)
  3. Substrate recognition, protein dynamics, and iron-sulfur cluster in Pseudomonas aeruginosa adenosine 5'-phosphosulfate reductase. Chartron J, Carroll KS, Shiau C, Gao H, Leary JA, Bertozzi CR, Stout CD. J. Mol. Biol. 364 152-169 (2006)
  4. Molecular basis for G protein control of the prokaryotic ATP sulfurylase. Mougous JD, Lee DH, Hubbard SC, Schelle MW, Vocadlo DJ, Berger JM, Bertozzi CR. Mol. Cell 21 109-122 (2006)
  5. Local and global regulators linking anaerobiosis to cupA fimbrial gene expression in Pseudomonas aeruginosa. Vallet-Gely I, Sharp JS, Dove SL. J. Bacteriol. 189 8667-8676 (2007)
  6. A novel deamido-NAD+-binding site revealed by the trapped NAD-adenylate intermediate in the NAD+ synthetase structure. Rizzi M, Bolognesi M, Coda A. Structure 6 1129-1140 (1998)
  7. Oxazolomycin biosynthesis in Streptomyces albus JA3453 featuring an "acyltransferase-less" type I polyketide synthase that incorporates two distinct extender units. Zhao C, Coughlin JM, Ju J, Zhu D, Wendt-Pienkowski E, Zhou X, Wang Z, Shen B, Deng Z. J. Biol. Chem. 285 20097-20108 (2010)
  8. 3'-Phosphoadenosine-5'-phosphosulfate reductase in complex with thioredoxin: a structural snapshot in the catalytic cycle. Chartron J, Shiau C, Stout CD, Carroll KS. Biochemistry 46 3942-3951 (2007)
  9. Structure and mechanism of a eukaryotic FMN adenylyltransferase. Huerta C, Borek D, Machius M, Grishin NV, Zhang H. J. Mol. Biol. 389 388-400 (2009)
  10. Structural plasticity of the thioredoxin recognition site of yeast methionine S-sulfoxide reductase Mxr1. Ma XX, Guo PC, Shi WW, Luo M, Tan XF, Chen Y, Zhou CZ. J. Biol. Chem. 286 13430-13437 (2011)
  11. Identification of critical ligand binding determinants in Mycobacterium tuberculosis adenosine-5'-phosphosulfate reductase. Hong JA, Bhave DP, Carroll KS. J. Med. Chem. 52 5485-5495 (2009)
  12. Sulfate activation enzymes: phylogeny and association with pyrophosphatase. Bradley ME, Rest JS, Li WH, Schwartz NB. J. Mol. Evol. 68 1-13 (2009)
  13. A universal entropy-driven mechanism for thioredoxin-target recognition. Palde PB, Carroll KS. Proc. Natl. Acad. Sci. U.S.A. 112 7960-7965 (2015)
  14. Spectroscopic studies on the [4Fe-4S] cluster in adenosine 5'-phosphosulfate reductase from Mycobacterium tuberculosis. Bhave DP, Hong JA, Lee M, Jiang W, Krebs C, Carroll KS. J. Biol. Chem. 286 1216-1226 (2011)
  15. The CgrA and CgrC proteins form a complex that positively regulates cupA fimbrial gene expression in Pseudomonas aeruginosa. McManus HR, Dove SL. J. Bacteriol. 193 6152-6161 (2011)
  16. Deciphering the role of histidine 252 in mycobacterial adenosine 5'-phosphosulfate (APS) reductase catalysis. Hong JA, Carroll KS. J. Biol. Chem. 286 28567-28573 (2011)
  17. Interaction domain on thioredoxin for Pseudomonas aeruginosa 5'-adenylylsulfate reductase. Chung JS, Noguera-Mazon V, Lancelin JM, Kim SK, Hirasawa M, Hologne M, Leustek T, Knaff DB. J. Biol. Chem. 284 31181-31189 (2009)
  18. The "super mutant" of yeast FMN adenylyltransferase enhances the enzyme turnover rate by attenuating product inhibition. Huerta C, Grishin NV, Zhang H. Biochemistry 52 3615-3617 (2013)
  19. The X-ray crystal structure of APR-B, an atypical adenosine 5'-phosphosulfate reductase from Physcomitrella patens. Stevenson CE, Hughes RK, McManus MT, Lawson DM, Kopriva S. FEBS Lett. 587 3626-3632 (2013)
  20. Functional Site Discovery in a Sulfur Metabolism Enzyme by Using Directed Evolution. Paritala H, Palde PB, Carroll KS. Chembiochem 17 1873-1878 (2016)