Abstract
The metabolism of sulfur has been widely studied with major progress in plant model systems. In plants and humans alike, activation occurs in canonical steps starting from the highly inert oxy-anion sulfate by the action of the enzymes ATP sulfurylase and APS kinase, resulting in the production of the atypical nucleotides adenosine-5′-phosphosulfate (APS) and PAPS (3′-phospho-APS). This review compares novel insights into structure, mechanism and regulation of plant ATP sulfurylases and APS kinases with findings from human sulfation pathways to highlight the benefit of “looking over the fence” and engaging in truly interdisciplinary research.
Access this chapter
Tax calculation will be finalised at checkout
Purchases are for personal use only
Similar content being viewed by others
References
Chan KX, Wirtz M, Phua SY, Estavillo GM, Pogson BJ (2013) Balancing metabolites in drought: the sulfur assimilation conundrum. Trends Plant Sci 18:18–29
Cummings JA, Vetting M, Ghodge SV, Xu C, Hillerich B, Seidel RD, Almo SC, Raushel FM (2014) Prospecting for unannotated enzymes: discovery of a 3′,5′-nucleotide bisphosphate phosphatase within the amidohydrolase superfamily. Biochemistry 53:591–600
Estavillo GM, Crisp PA, Pornsiriwong W, Wirtz M, Collinge D, Carrie C, Giraud E, Whelan J, David P, Javot H, Brearley C, Hell R, Marin E, Pogson BJ (2011) Evidence for a SAL1-PAP chloroplast retrograde pathway that functions in drought and high light signaling in Arabidopsis. Plant Cell 23:3992–4012
Faiyaz ul Haque M, King LM, Krakow D, Cantor RM, Rusiniak ME, Swank RT, Superti-Furga A, Haque S, Abbas H, Ahmad W, Ahmad M, Cohn DH (1998) Mutations in orthologous genes in human spondyloepimetaphyseal dysplasia and the brachymorphic mouse. Nat Genet 20:157–162
Flicek P, Amode MR, Barrell D, Beal K, Billis K, Brent S, Carvalho-Silva D, Clapham P, Coates G, Fitzgerald S, Gil L, Giron CG, Gordon L, Hourlier T, Hunt S, Johnson N, Juettemann T, Kahari AK, Keenan S, Kulesha E, Martin FJ, Maurel T, McLaren WM, Murphy DN, Nag R, Overduin B, Pignatelli M, Pritchard B, Pritchard E, Riat HS, Ruffier M, Sheppard D, Taylor K, Thormann A, Trevanion SJ, Vullo A, Wilder SP, Wilson M, Zadissa A, Aken BL, Birney E, Cunningham F, Harrow J, Herrero J, Hubbard TJ, Kinsella R, Muffato M, Parker A, Spudich G, Yates A, Zerbino DR, Searle SM (2014) Ensembl 2014. Nucleic Acids Res 42:D749–D755
Grum D, van den Boom J, Neumann D, Matena A, Link NM, Mueller JW (2010) A heterodimer of human 3′-phospho-adenosine-5′-phosphosulphate (PAPS) synthases is a new sulphate activating complex. Biochem Biophys Res Commun 395:420–425
Guranowski A, Wojdyla AM, Zimny J, Wypijewska A, Kowalska J, Jemielity J, Davis RE, Bieganowski P (2010) Dual activity of certain HIT-proteins: A. thaliana Hint4 and C. elegans DcpS act on adenosine 5′-phosphosulfate as hydrolases (forming AMP) and as phosphorylases (forming ADP). FEBS Lett 584:93–98
Harjes S, Bayer P, Scheidig AJ (2005) The crystal structure of human PAPS synthetase 1 reveals asymmetry in substrate binding. J Mol Biol 347:623–635
Herrmann J, Ravilious GE, McKinney SE, Westfall CS, Lee SG, Baraniecka P, Giovannetti M, Kopriva S, Krishnan HB, Jez JM (2014) Structure and mechanism of soybean ATP sulfurylase and the committed step in plant sulfur assimilation. J Biol Chem 289:10919–10929
Hirsch J, Misson J, Crisp PA, David P, Bayle V, Estavillo GM, Javot H, Chiarenza S, Mallory AC, Maizel A, Declerck M, Pogson BJ, Vaucheret H, Crespi M, Desnos T, Thibaud MC, Nussaume L, Marin E (2011) A novel fry1 allele reveals the existence of a mutant phenotype unrelated to 5′- >3′ exoribonuclease (XRN) activities in Arabidopsis thaliana roots. PLoS One 6:e16724
Hudson BH, York JD (2012) Roles for nucleotide phosphatases in sulfate assimilation and skeletal disease. Adv Biol Regul 52:229–238
Hudson BH, Frederick JP, Drake LY, Megosh LC, Irving RP, York JD (2013) Role for cytoplasmic nucleotide hydrolysis in hepatic function and protein synthesis. Proc Natl Acad Sci U S A 110:5040–5045
Klein M, Papenbrock J (2004) The multi-protein family of Arabidopsis sulphotransferases and their relatives in other plant species. J Exp Bot 55:1809–1820
Kopriva S, Mugford SG, Baraniecka P, Lee BR, Matthewman CA, Koprivova A (2012) Control of sulfur partitioning between primary and secondary metabolism in Arabidopsis. Front Plant Sci 3:163
Lansdon EB, Fisher AJ, Segel IH (2004) Human 3′-phosphoadenosine 5′-phosphosulfate synthetase (isoform 1, brain): kinetic properties of the adenosine triphosphate sulfurylase and adenosine 5′-phosphosulfate kinase domains. Biochemistry 43:4356–4365
Lee BR, Huseby S, Koprivova A, Chetelat A, Wirtz M, Mugford ST, Navid E, Brearley C, Saha S, Mithen R, Hell R, Farmer EE, Kopriva S (2012) Effects of fou8/fry1 mutation on sulfur metabolism: is decreased internal sulfate the trigger of sulfate starvation response? PLoS One 7:e39425
Mougous JD, Lee DH, Hubbard SC, Schelle MW, Vocadlo DJ, Berger JM, Bertozzi CR (2006) Molecular basis for G protein control of the prokaryotic ATP sulfurylase. Mol Cell 21:109–122
Mueller JW, Shafqat N (2013) Adenosine-5′-phosphosulfate–a multifaceted modulator of bifunctional 3′-phospho-adenosine-5′-phosphosulfate synthases and related enzymes. FEBS J 280:3050–3057
Mugford SG, Matthewman CA, Hill L, Kopriva S (2010) Adenosine-5′-phosphosulfate kinase is essential for Arabidopsis viability. FEBS Lett 584:119–123
Noordam C, Dhir V, McNelis JC, Schlereth F, Hanley NA, Krone N, Smeitink JA, Smeets R, Sweep FC, Claahsen-van der Grinten HL, Arlt W (2009) Inactivating PAPSS2 mutations in a patient with premature pubarche. N Engl J Med 360:2310–2318
Parey K, Demmer U, Warkentin E, Wynen A, Ermler U, Dahl C (2013) Structural, biochemical and genetic characterization of dissimilatory ATP sulfurylase from Allochromatium vinosum. PLoS One 8:e74707
Patron NJ, Durnford DG, Kopriva S (2008) Sulfate assimilation in eukaryotes:fusions, relocations and lateral transfers. BMC Evol Biol 8:39
Purohit A, Foster PA (2012) Steroid sulfatase inhibitors for estrogen- and androgen-dependent cancers. J Endocrinol 212:99–110
Ravilious GE, Jez JM (2012) Nucleotide binding site communication in Arabidopsis thaliana adenosine 5′-phosphosulfate kinase. J Biol Chem 287:30385–30394
Ravilious GE, Nguyen A, Francois JA, Jez JM (2012) Structural basis and evolution of redox regulation in plant adenosine-5′-phosphosulfate kinase. Proc Natl Acad Sci U S A 109:309–314
Robles P, Fleury D, Candela H, Cnops G, Alonso-Peral MM, Anami S, Falcone A, Caldana C, Willmitzer L, Ponce MR, Van Lijsebettens M, Micol JL (2010) The RON1/FRY1/SAL1 gene is required for leaf morphogenesis and venation patterning in Arabidopsis. Plant Physiol 152:1357–1372
Schroder E, Gebel L, Eremeev AA, Morgner J, Grum D, Knauer SK, Bayer P, Mueller JW (2012) Human PAPS synthase isoforms are dynamically regulated enzymes with access to nucleus and cytoplasm. PLoS One 7:e29559
Sekulic N, Dietrich K, Paarmann I, Ort S, Konrad M, Lavie A (2007) Elucidation of the active conformation of the APS-kinase domain of human PAPS synthetase 1. J Mol Biol 367:488–500
Sun M, Leyh TS (2006) Channeling in sulfate activating complexes. Biochemistry 45:11304–11311
Takahashi H, Kopriva S, Giordano M, Saito K, Hell R (2011) Sulfur assimilation in photosynthetic organisms: molecular functions and regulations of transporters and assimilatory enzymes. Annu Rev Plant Biol 62:157–184
Ullrich TC, Blaesse M, Huber R (2001) Crystal structure of ATP sulfurylase from Saccharomyces cerevisiae, a key enzyme in sulfate activation. EMBO J 20:316–329
van den Boom J, Heider D, Martin SR, Pastore A, Mueller JW (2012) 3′-Phosphoadenosine 5′-phosphosulfate (PAPS) synthases, naturally fragile enzymes specifically stabilized by nucleotide binding. J Biol Chem 287:17645–17655
Wu H, Wu W, Chen Z, Wang W, Zhou G, Kajiyama T, Kambara H (2011) Highly sensitive pyrosequencing based on the capture of free adenosine 5′ phosphosulfate with adenosine triphosphate sulfurylase. Anal Chem 83:3600–3605
Acknowledgement
W. Arlt is cordially acknowledged for her generous support and critical review of the manuscript. JWM also wants to acknowledge David Lodge from the University of Birmingham for various insights. JWM is a recipient of the Marie Curie IEF award 625451 SUPA-HD: Sulfation pathways in Health and Disease. Finally, we thank the Biochemical Society, UK, for a travel award (to JWM) to attend the 9th International Workshop on Sulfur Metabolism in Plants, Freiburg, Germany.
Author information
Authors and Affiliations
Corresponding author
Editor information
Editors and Affiliations
Rights and permissions
Copyright information
© 2015 Springer International Publishing Switzerland
About this chapter
Cite this chapter
Mueller, J.W., O’Neill, N., Shafqat, N. (2015). Small World: A Plant Perspective on Human Sulfate Activation. In: De Kok, L., Hawkesford, M., Rennenberg, H., Saito, K., Schnug, E. (eds) Molecular Physiology and Ecophysiology of Sulfur. Proceedings of the International Plant Sulfur Workshop. Springer, Cham. https://doi.org/10.1007/978-3-319-20137-5_6
Download citation
DOI: https://doi.org/10.1007/978-3-319-20137-5_6
Publisher Name: Springer, Cham
Print ISBN: 978-3-319-20136-8
Online ISBN: 978-3-319-20137-5
eBook Packages: Biomedical and Life SciencesBiomedical and Life Sciences (R0)