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An International Journal of Inorganic Chemistry Volume 43 Number 3 21 January 2014 Pages 891–1472 Dalton Transactions An international journal of inorganic chemistry www.rsc.org/dalton ISSN 1477-9226 COVER ARTICLE Gahan et al. Spectroscopic and mechanistic studies of dinuclear metallohydrolases and their biomimetic complexes Dalton Transactions View Article Online PERSPECTIVE View Journal | View Issue Spectroscopic and mechanistic studies of dinuclear metallohydrolases and their biomimetic complexes Cite this: Dalton Trans., 2014, 43, 910 Lena J. Daumann,a Gerhard Schenk,a David L. Ollisb and Lawrence R. Gahan*a An enhanced understanding of the metal ion binding and active site structural features of phospho- esterases such as the glycerophosphodiesterase from Enterobacter aerogenes (GpdQ), and the organo- phosphate degrading agent from Agrobacterium radiobacter (OpdA) have important consequences for Received 21st August 2013, potential applications. Coupled with investigations of the metalloenzymes, programs of study to syn- Accepted 10th October 2013 thesise and characterise model complexes based on these metalloenzymes can add to our understanding DOI: 10.1039/c3dt52287c of structure and function of the enzymes themselves. This review summarises some of our work and illus- www.rsc.org/dalton trates the significance and contributions of model studies to knowledge in the area. 1. Introduction targets for drug design against a variety of human disorders while in other cases their catalytic activities make them ideal The current knowledge about the structure, function, and reagents for the bioremediation of organophosphate pesticides – – mechanism of dinuclear metallohydrolases has been summar- and nerve agents.1 6,8 13 In addition, the capacity for mimicry – ised by a number of authors.1 7 Metallohydrolases are of con- of their properties through model complexes makes them – siderable interest by virtue of their biological roles and their attractive to the bioinorganic chemist.14 34 In this perspective use in bioremediation. In some cases, their roles make them we firstly describe the general classes of metallohydrolases, we review the properties of two organophosphate-hydrolysing metalloenzymes of interest to our research and discuss the a School of Chemistry and Molecular Biosciences, The University of Queensland, various model complexes of divalent metal ions synthesised in Brisbane, QLD 4072, Australia. E-mail: [email protected] bResearch School of Chemistry, Australian National University, Canberra 0200, order to probe the structure, function and spectroscopic pro- Australia perties of the metalloenzymes. Published on 18 October 2013. Downloaded by University of Queensland 12/10/2015 02:10:48. Lena Daumann received her Assoc. Prof. Schenk’s research Diploma in Chemistry from the interest is focused on the eluci- Ruprecht-Karls University of dation of the reaction mecha- Heidelberg in 2009 under the nisms of metal ion-dependent supervision of Peter Comba. enzymes, in particular dinuclear After an internship at the BASF metallohydrolases, and their SE in Ludwigshafen she moved application as drug targets or to Australia where she recently agents for bioremediation. Fol- completed her PhD under the lowing doctoral studies at the supervision of Lawrence Gahan University of Queensland and and Gerhard Schenk at The Uni- postdoctoral research at Stanford versity of Queensland holding University Assoc. Prof. Schenk Lena J. Daumann IPRS and UQCent scholarships. Gerhard Schenk commenced an academic posi- Her doctoral thesis focused on tion at the University of Queens- spectroscopic and mechanistic studies of dinuclear metallohydro- land. Until recently he also held a joint professorial appointment lases and related biomimetics. In 2013 she joined Kenneth at the National University of Ireland – Maynooth and now holds a Raymond at the University of California, Berkeley as a post- Future Fellowship from the Australian Research Council. doctoral research fellow. Her current research focuses on lumines- cent lanthanides. 910 | Dalton Trans.,2014,43,910–928 This journal is © The Royal Society of Chemistry 2014 View Article Online Dalton Transactions Perspective 2. Dinuclear metallohydrolases Phosphoesterases such as the glycerophosphodiesterase from Enterobacter aerogenes (GpdQ), the organophosphate- The family of dinuclear metallohydrolases comprises a large degrading agent (OpdA) from Agrobacterium radiobacter and number of enzymes with very different functionalities the phosphotriesterase (PTE) from Pseudomonas diminuta have (Table 1). The dual action of two metals can have different attracted attention due to their ability to degrade toxic pesti- advantages over catalysis by just one metal ion.35 These advan- cides, whereas for the purple acid phosphatases (PAPs), tages include that the thermodynamic driving force for redox metallo-β-lactamases (MβLs) and ureases the interest is mainly reactions is lowered due to charge-delocalization; as well, the due to their role in human disorders and therapy.7,36,37 The activation barrier is also lowered for solvent and enzyme re- active site structures of dinuclear metallohydrolases typically organization.35 In addition, substrates can be more effectively have the metal ions coordinated to histidine, glutamic acid, oriented and the electrostatic activation of substrates is more aspartate, asparagine and (carboxylated) lysine amino acid easily achieved.35 Furthermore, two metal ions facilitate the residues, in addition to terminal or bridging water/hydroxide formation of hydrolysis-initiating nucleophiles more readily, ligands. The two metal binding sites are often defined as and lower lying energy transition states for hydrolysis reactions the α- and β-site, differentiated by their coordination can be achieved.35 The metal ion content and oxidation states environments.38 of the dinuclear metallohydrolases are as diverse as their pro- In this review we focus on the dinuclear metalloenzymes posed mechanisms, nucleophiles and substrates utilized. OpdA and, in particular, GpdQ. OpdA is an extremely efficient Table 1 Overview of hydrolytic metalloenzymes Enzyme Metal ion composition Biological function Research incentive Glycerophospho-diesterase Fe(II)–Zn(II), Co(II)–Co(II), Hydrolysis of 3′-5′ phosphodiester Potential bioremediator 8,11,38,41,42,77–80 (GpdQ) Mn(II)–Mn(II), Cd(II)–Cd(II) bond of glycerophosphodiesters Purple acid phosphatases Fe(III)–Fe(II), Fe(III)–Mn(II), Bone metabolism (animals) and Target for anti-osteoporotic drugs 191–199 (PAP) Fe(III)–Zn(II) phosphate uptake (plants) 117 Metallo-β-lactamases Zn(II)–Zn(II) Hydrolysis of β-lactam substrates Study potential inhibitors to fight (antibiotics) antibiotic resistance 39,40 a Rv0805 Fe(III)–Mn(II) Cleavage of cAMP/cGMP Potential bioremediator phosphodiester bonds Phosphotriesterases Co(II)–Co(II), Mn(II)–Mn(II), Organophosphate hydrolysis Potential bioremediator 49,64,68,71 (OpdA, OPH) Cd(II)–Cd(II), Fe(II)–Zn(II) 200 Ureases Ni(II)–Ni(II) Hydrolysis of urea Treatment of bacterial infections, regulation of nitrogen uptake in plants 2,191 Ser/Thr phosphatase Fe(II)–Fe(II), Fe(II)–Zn(II), Gene expression Target in chemotherapy Mn(II)–Mn(II) 201 Leucine aminopeptidases Zn(II)–Zn(II) Amino acid synthesis Target for drugs against leukemia 35,202 Arginase Mn(II)Mn(II) Hydrolysis of Arginine Involved in vascular diseases Published on 18 October 2013. Downloaded by University of Queensland 12/10/2015 02:10:48. a Proposed in vivo. David Ollis graduated from the Lawrence Gahan obtained a BSc University of NSW before under- in chemistry and a PhD from La taking doctoral studies at Sydney Trobe University, Melbourne, University under the direction of Australia. After postdoctoral Professor Hans Freeman and Dr positions in the United States Cyril Appleby of the CSIRO. He and England he was a research worked on the first DNA poly- fellow in the Research School of merase structure during his post- Chemistry at the Australian doctoral studies at Yale under National University, Canberra, Professor Tom Steitz. He then Australia, with Professor Allan established a laboratory in the Sargeson. Following a position Biochemistry and Molecular at Monash University, Mel- David L. Ollis Biology Department at North- Lawrence R. Gahan bourne, he moved to the Univer- western University in Chicago sity of Queensland in Brisbane, before taking his present position in the Research School of Australia, in 1984 where he is currently a Professor of Chemistry. Chemistry at the ANU. During the course of his career the empha- His current research focuses on bioinorganic and transition metal sis of his research has shifted from structural biology to evolving chemistry. proteins using directed evolution. This journal is © The Royal Society of Chemistry 2014 Dalton Trans.,2014,43,910–928 | 911 View Article Online Perspective Dalton Transactions phosphotriesterase with low levels of activity towards phospho- molecule undergoing nucleophilic attack by a serine-OH diesters. GpdQ rapidly degrades a variety of phosphodiesters moiety in the active site of the enzyme acetylcholine esterase and has weak activity towards mono- and triphosphate ester (AChE), subsequently blocking the site for the neurotransmit- substrates. Attempts to duplicate the catalytic, spectroscopic ter acetylcholine.54,55 With the enzyme inhibited, acetylcholine and mechanistic properties of phosphoesterases have been builds up in the synapses and nerve impulses are continually one of our goals, and the goals of many other workers in the transmitted. The
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