Kinetic mechanism of the dimeric ATP sulfurylase from plants

Bioscience Reports

Volumn 33, Issue 4, 2013, Pages 585-591

  Ravilious, Geoffrey E ^a   Herrmann, Jonathan ^a   Lee, Soon Goo ^a   Westfall, Corey S ^a   Jez, Joseph M ^a  

^a WASHINGTON UNIVERSITY   (United States)

Author keywords

Dead end inhibition; Enzyme; Isothermal titration calorimetry (ITC); Kinetic mechanism; Plant sulfur metabolism; Sulfur assimilation

Indexed keywords

ADENOSINE 5' PHOSPHOSULFATE; ISOPROTEIN; MAGNESIUM; PYROPHOSPHATE; SULFATE ADENYLYLTRANSFERASE; SULFATE ADENYLYLTRANSFERASE 1; UNCLASSIFIED DRUG; ADENOSINE TRIPHOSPHATE; CHLORATE; SULFATE; VEGETABLE PROTEIN;

ARTICLE; CONTROLLED STUDY; ENZYME ACTIVITY; ENZYME INHIBITION; ENZYME KINETICS; ENZYME REGULATION; ENZYME SUBSTRATE; ISOTHERMAL TITRATION CALORIMETRY; NONHUMAN; PROTEIN BINDING; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN STRUCTURE; PROTEIN SYNTHESIS; SOYBEAN; STRUCTURE ANALYSIS; TITRIMETRY; ANTAGONISTS AND INHIBITORS; BIOCATALYSIS; CHEMISTRY; ENZYMOLOGY; KINETICS;

ADENOSINE PHOSPHOSULFATE; ADENOSINE TRIPHOSPHATE; BIOCATALYSIS; CHLORATES; KINETICS; PLANT PROTEINS; SOYBEANS; SULFATE ADENYLYLTRANSFERASE; SULFATES;

EID: 84881484096     PISSN: 01448463     EISSN: 15734935     Source Type: Journal    
DOI: 10.1042/BSR20130073     Document Type: Article

References (44)

1. Leustek, T., Martin, M. N., Bick, J. A. and Davies, J. P. (2000) Pathways and regulation of sulfur metabolism revealed through molecular and genetic studies. Annu. Rev. Plant Physiol. Plant Mol. Biol. 51, 141-165
2. Takahashi, H., Kopriva, S., Giordano, M., Saito, K. and Hell, R. (2011) Sulfur assimilation in photosynthetic organisms: molecular functions and regulations of transporters and assimilatory enzymes. Annu. Rev. Plant Biol. 62, 157-184
3. Yi, H., Galant, A., Ravilious, G. E., Preuss, M. L. and Jez, J. M. (2010) Sensing sulfur conditions: simple to complex protein regulatory mechanisms in plant thiol metabolism. Mol. Plant 3, 269-279
4. Yi, H., Ravilious, G. E., Galant, A., Krishnan, H. B. and Jez, J. M. (2010) From sulfur to homoglutathione: thiol metabolism in soybean. Amino Acids 39, 963-978
5. Krishnan, H. B. (2005) Engineering soybean for enhanced sulfur amino acid content. Crop Sci. 45, 454-461 (Pubitemid 40350961)
6. Kopriva, S., Mugford, S. G., Baraniecka, P., Lee, B. R., Matthewman, C. A. and Koprivova, A. (2012) Control of sulfur partitioning between primary and secondary metabolism in Arabidopsis. Front. Plant Sci. 3, 163
7. Osslund, T., Chandler, C. and Segel, I. H. (1982) ATP sulfurylase from higher plants: purification and preliminary kinetic studies on the cabbage leaf enzyme. Plant Physiol. 70, 39-45
8. Renosto, F., Patel, H. C., Martin, R. L., Thomassian, C., Zimmerman, G. and Segel, I. H. (1993) ATP sulfurylase from higher plants: kinetic and structural characterization of the chloroplast and cytosol enzymes from spinach leaf. Arch. Biochem. Biophys. 307, 272-285 (Pubitemid 24001563)
9. Murillo, M. and Leustek, T. (1995) Adenosine-5′-triphosphate- sulfurylase from Arabidopsis thaliana and Escherichia coli are functionally equivalent but structurally and kinetically divergent: nucleotide sequence of two adenosine-5′-triphosphate-sulfurylase cDNAs from Arabidopsis thaliana and analysis of a recombinant enzyme. Arch. Biochem. Biophys. 323, 195-204
10. Phartiyal, P., Kim, W. S., Cahoon, R. E., Jez, J. M. and Krishnan, H. B. (2006) Soybean ATP sulfurylase, a homodimeric enzyme involved in sulfur assimilation, is abundantly expressed in roots and induced by cold treatment. Arch. Biochem. Biophys. 450, 20-29 (Pubitemid 43782736)
11. Phartiyal, P., Kim, W. S., Cahoon, R. E., Jez, J. M. and Krishnan, H. B. (2008) The role of 5′-adenylylsulfate reductase in the sulfur assimilation pathway of soybean: molecular cloning, kinetic characterization, and gene expression. Phytochemistry 69, 356-364
12. Ravilious, G. E. and Jez, J. M. (2012) Structural biology of plant sulfur metabolism: from assimilation to biosynthesis. Nat. Prod. Rep. 29, 1138-1152
13. Klein, M. and Papenbrock, J. (2004) The multi-protein family of Arabidopsis sulphotransferases and their relatives in other plant species. J. Exp. Bot. 55, 1809-1820 (Pubitemid 39123314)
14. Mugford, S. G., Yoshimoto, N., Reichelt, M., Wirtz, M., Hill, L., Mugford, S. T., Nakazato, Y., Noji, M., Takahashi, H., Kramell, R. et al. (2009) Disruption of adenosine-5′-phosphosulfate kinase in Arabidopsis reduces levels of sulfated secondary metabolites. Plant Cell 21, 910-927
15. Yatusevich, R., Mugford, S. G., Matthewman, C., Gigolashvili, T., Frerigmann, H., Delaney, S., Koprivova, A., Flügge, U. I. and Kopriva, S. (2010) Genes of primary sulfate assimilation are part of the glucosinolate biosynthetic network in Arabidopsis thaliana. Plant J. 62, 1-11
16. Bradley, M. E., Rest, J. S., Li, W. H. and Schwartz, N. B. (2009) Sulfate activation enzymes: phylogeny and association with pyrophosphate. J. Mol. Evol. 68, 1-13
17. Leustek, T., Murillo, M. and Cervantes, M. (1994) Cloning of a cDNA encoding ATP sulfurylase from Arabidopsis thaliana by functional expression in Sacchromyces cerevisiae. Plant Physiol. 105, 897-902
18. Klonus, D., Höfgen, R., WIllmitzer, L. and Riesmeier, J. W. (1994) Isolation and characterization of two cDNA clones encoding ATP sulfurylases from potato by complementation of a yeast mutant. Plant J. 6, 105-112
19. Klonus, D., Riesmeier, J. W. and WIllmitzer, L. (1995) A cDNA clone for an ATP sulfurylase from Arabidopsis thaliana. Plant Physiol. 107, 653-654
20. Logan, H. M., Cathala, N., Grignon, C. and Davidian, J. C. (1996) Cloning of a cDNA encoded by a member of the Arabidopsis thaliana ATP sulfurylase multigene family. J. BIol. Chem. 271, 12227-12233
21. Heiss, S., Schäfer, H. J., Haag-Kerwer, A. and Rausch, T. (1999) Cloning sulfur assimilation genes of Brassica juncea L.: cadmium differentially affects the expression of a putative low-affinity sulfate transporter and isoforms of ATP sulfurylase and APS reductase. Plant Mol. Biol. 39, 847-857
22. Hatzfeld, Y., Lee, S., Lee, M., Leustek, T. and Saito, K. (2000) Functional characterization of a gene encoding a fourth ATP sulfurylase isoform from Arabidopsis thaliana. Gene 248, 51-58 (Pubitemid 30259201)
23. Rotte, C. and Leustek, T. (2000) Differential subcellular localization and expression of ATP sulfurylase and 5'-adenylylsulfate reductase during ontogenesis of Arabidopsis leaves indicates that cytosolic and plastid forms of ATP sulfurylase may have specialized functions. Plant Physiol. 124, 715-724
24. Mougous, J. D., Lee, D. H., Hubbard, S. C., Schelle, M. W., Vocadio, D. J., Berger, J. M. and Bertozzi, C. R. (2006) Molecular basis for G protein control of the prokaryotic ATP sulfurylase. Mol. Cell 21, 109-122 (Pubitemid 43017853)
25. Ullrich, T. C., Blaesse, M. and Huber, R. (2001) Crystal structure of ATP sulfurylase from Saccharomyces cerevisiae, a key enzyme in sulfate activation. EMBO J. 20, 316-329 (Pubitemid 32126968)
26. MacRae, I. J., Segel, I. H. and Fisher, A. J. (2001) Crystal structure of ATP sulfurylase from Penicillium chrysogenum: insights into the allosteric regulation of sulfate assimilation. Biochemistry 40, 6795-6804 (Pubitemid 32538225)
27. Harjes, S., Bayer, P. and Scheidig, A. J. (2005) The crystal structure of human PAPS synthetase 1 reveals asymmetry in substrate binding. J. Mol. Biol. 347, 623-635 (Pubitemid 40332369)
28. Marzluf, G. A. (1997) Molecular genetics of sulfur assimilation in filamentous fungi and yeast. Annu. Rev. Microbiol. 51, 73-96 (Pubitemid 27433043)
29. Cumming, M., Leung, S., McCallum, J. and McManus, M. T. (2007) Complex formation between recombinant ATP sulfurylase and APS reductase of Allium cepa (L.). FEBS Lett. 581, 4139-4147 (Pubitemid 47301847)
30. Ravilious, G. E., Nguyen, A., Francois, J. A. and Jez, J. M. (2012) Structural basis and evolution of redox regulation in plant adenosine-5′- phosphosulfate kinase. Proc. Natl. Acad. Sci. U.S.A. 109, 309-14
31. Ravilious, G. E. and Jez, J. M. (2012) Nucleotide binding site communication in Arabidopsis thaliana adenosine 5′-phosphosulfate kinase. J. Biol. Chem. 287, 30385-30394
32. Ravilious, G. E., Westfall, C. S. and Jez, J. M. (2013) Redox-linked gating of nucleotide binding by the N-terminal domain of adenosine 5′-phosphosulfate kinase. J. Biol. Chem. 288, 6107-6115
33. Segal, I. H. (1975) Enzyme kinetics: behavior and analysis of rapid equilibrium and steady-state enzyme systems, John Wiley & Sons, New York
34. Cleland, W. W. (1979) Statistical analysis of enzyme kinetic data. Methods Enzymol. 63, 103-138
35. Baeuerle, P. A. and Huttner, W. B. (1986) Chlorate-a potent inhibitor of protein sulfation in intact cells. Biochem. Biophys. Res. Comm. 141, 870-877 (Pubitemid 17001937)
36. Farley, J. R., Cryns, D. F., Yang, Y. H. and Segel, I. H. (1976) Adenosine triphosphate sulfurylase from Penicillium chrysogenum: steady-state kinetics of the forward and reverse reactions. J. Biol. Chem. 251, 4389-4397
37. Ludwig, R. A. (1995) Arabidopsis chloroplasts dissimilate L-arginine and L-citrulline for use as N source. Plant Physiol. 101, 429-434
38. Copeland, R. A. (2000) Enzymes: a practical introduction to structure, mechanism, and data analysis, John Wiley & Sons, New York
39. Höfgen, R., Kreft, O., Willmitzer, L. and Hesse, H. (2001) Manipulation of thiol contents in plants. Amino Acids 20, 291-299 (Pubitemid 32260961)
40. 2- transport activities. Plant Physiol. 116, 1307-1313 (Pubitemid 128500519)
41. 2- uptake, and oxidative stress response in intact canola roots. Plant Physiol. 114, 177-183 (Pubitemid 28110907)
42. Vauclare, P., Kopriva, S., Fell, D., Suter, M., Sticher, L., von Ballmoos, P., Krähenbühl, U., den Camp, R. O. and Brunold, C. (2002) Flux control of sulphate assimilation in Arabidopsis thaliana: adenosine 5′-phosphosulphate reductase is more susceptible than ATP sulphurylase to negative control by thiols. Plant J. 31, 729-740
43. Lyle, S., Geller, D. H., Ng, K., Westley, J. and Schwartz, N. B. (1994) Kinetic mechanism of ATP sulfurylase from rat chondrosarcoma. Biochem. J. 301, 349-354 (Pubitemid 24231933)
44. Renosto, F., Seubert, P. A., Knudson, P. and Segel, I. H. (1985) Adenosine 5′-phosphosulfate kinase from Penicillium chrysogenum: determining ligand dissociation constants of binary and ternary complexes from the kinetics of enzyme inactivation. J. Biol. Chem. 260, 11903-11913 (Pubitemid 16228345)