1e1a › Citations

Crystal structure of diisopropylfluorophosphatase from Loligo vulgaris.

Scharff EI, Koepke J, Fritzsch G, Lücke C, Rüterjans H
Structure 9 493-502 (2001)
Related entries: 2iao, 2iap, 2iaq, 2iar, 2ias, 2iat, 2iau

Cited: 66 times
EuropePMC logo PMID: 11435114

Abstract

Background

Phosphotriesterases (PTE) are enzymes capable of detoxifying organophosphate-based chemical warfare agents by hydrolysis. One subclass of these enzymes comprises the family of diisopropylfluorophosphatases (DFPases). The DFPase reported here was originally isolated from squid head ganglion of Loligo vulgaris and can be characterized as squid-type DFPase. It is capable of hydrolyzing the organophosphates diisopropylfluorophosphate, soman, sarin, tabun, and cyclosarin.

Results

Crystals were grown of both the native and the selenomethionine-labeled enzyme. The X-ray crystal structure of the DFPase from Loligo vulgaris has been solved by MAD phasing and refined to a crystallographic R value of 17.6% at a final resolution of 1.8 A. Using site-directed mutagenesis, we have structurally and functionally characterized essential residues in the active site of the enzyme.

Conclusion

The crystal structure of the DFPase from Loligo vulgaris is the first example of a structural characterization of a squid-type DFPase and the second crystal structure of a PTE determined to date. Therefore, it may serve as a structural model for squid-type DFPases in general. The overall structure of this protein represents a six-fold beta propeller with two calcium ions bound in a central water-filled tunnel. The consensus motif found in the blades of this beta propeller has not yet been observed in other beta propeller structures. Based on the results obtained from mutants of active-site residues, a mechanistic model for the DFP hydrolysis has been developed.

Reviews - 1e1a mentioned but not cited (2)

  1. A mechanistic view of enzyme evolution. Yang G, Miton CM, Tokuriki N. Protein Sci 29 1724-1747 (2020)
  2. Enzymatic Bioremediation of Organophosphate Compounds-Progress and Remaining Challenges. Thakur M, Medintz IL, Walper SA. Front Bioeng Biotechnol 7 289 (2019)

Articles - 1e1a mentioned but not cited (11)

  1. Computational design of an enzyme catalyst for a stereoselective bimolecular Diels-Alder reaction. Siegel JB, Zanghellini A, Lovick HM, Kiss G, Lambert AR, St Clair JL, Gallaher JL, Hilvert D, Gelb MH, Stoddard BL, Houk KN, Michael FE, Baker D. Science 329 309-313 (2010)
  2. Assessing the fractions of tautomeric forms of the imidazole ring of histidine in proteins as a function of pH. Vila JA, Arnautova YA, Vorobjev Y, Scheraga HA. Proc. Natl. Acad. Sci. U.S.A. 108 5602-5607 (2011)
  3. In silico protein design by combinatorial assembly of protein building blocks. Tsai HH, Tsai CJ, Ma B, Nussinov R. Protein Sci. 13 2753-2765 (2004)
  4. The evolution of function in strictosidine synthase-like proteins. Hicks MA, Barber AE, Giddings LA, Caldwell J, O'Connor SE, Babbitt PC. Proteins 79 3082-3098 (2011)
  5. Relating destabilizing regions to known functional sites in proteins. Dessailly BH, Lensink MF, Wodak SJ. BMC Bioinformatics 8 141 (2007)
  6. Neutron structure and mechanistic studies of diisopropyl fluorophosphatase (DFPase). Chen JC, Mustyakimov M, Schoenborn BP, Langan P, Blum MM. Acta Crystallogr. D Biol. Crystallogr. 66 1131-1138 (2010)
  7. Active Site Hydrophobicity and the Convergent Evolution of Paraoxonase Activity in Structurally Divergent Enzymes: The Case of Serum Paraoxonase 1. Blaha-Nelson D, Krüger DM, Szeler K, Ben-David M, Kamerlin SC. J. Am. Chem. Soc. 139 1155-1167 (2017)
  8. New horizons for lipoprotein receptors: communication by β-propellers. Andersen OM, Dagil R, Kragelund BB. J. Lipid Res. 54 2763-2774 (2013)
  9. A comprehensive analysis of the computed tautomer fractions of the imidazole ring of histidines in Loligo vulgaris. Vorobjev YN, Scheraga HA, Vila JA. J. Biomol. Struct. Dyn. 36 3094-3105 (2018)
  10. Outline of an experimental design aimed to detect a protein A mirror image in solution. Martin OA, Vorobjev Y, Scheraga HA, Vila JA. PeerJ Phys Chem 1 e2 (2019)
  11. The Difference in Structural States between Canonical Proteins and Their Isoforms Established by Proteome-Wide Bioinformatics Analysis. Osmanli Z, Falgarone T, Samadova T, Aldrian G, Leclercq J, Shahmuradov I, Kajava AV. Biomolecules 12 1610 (2022)


Reviews citing this publication (14)

  1. Emergence of diverse biochemical activities in evolutionarily conserved structural scaffolds of proteins. Anantharaman V, Aravind L, Koonin EV. Curr Opin Chem Biol 7 12-20 (2003)
  2. Novel sequences propel familiar folds. Jawad Z, Paoli M. Structure 10 447-454 (2002)
  3. Human paraoxonase: a promising approach for pre-treatment and therapy of organophosphorus poisoning. Rochu D, Chabrière E, Masson P. Toxicology 233 47-59 (2007)
  4. Catalytic mechanisms for phosphotriesterases. Bigley AN, Raushel FM. Biochim. Biophys. Acta 1834 443-453 (2013)
  5. 3D-Structure and function of strictosidine synthase--the key enzyme of monoterpenoid indole alkaloid biosynthesis. Stöckigt J, Barleben L, Panjikar S, Loris EA. Plant Physiol. Biochem. 46 340-355 (2008)
  6. Supramolecular chemistry and chemical warfare agents: from fundamentals of recognition to catalysis and sensing. Sambrook MR, Notman S. Chem Soc Rev 42 9251-9267 (2013)
  7. Organophosphorus Nerve Agents: Types, Toxicity, and Treatments. Mukherjee S, Gupta RD. J Toxicol 2020 3007984 (2020)
  8. Structural biology in plant natural product biosynthesis--architecture of enzymes from monoterpenoid indole and tropane alkaloid biosynthesis. Stöckigt J, Panjikar S. Nat Prod Rep 24 1382-1400 (2007)
  9. Organophosphorus hydrolase as an in vivo catalytic nerve agent bioscavenger. Wales ME, Reeves TE. Drug Test Anal 4 271-281 (2012)
  10. Current and emerging strategies for organophosphate decontamination: special focus on hyperstable enzymes. Jacquet P, Daudé D, Bzdrenga J, Masson P, Elias M, Chabrière E. Environ Sci Pollut Res Int 23 8200-8218 (2016)
  11. The impact of structural biology on alkaloid biosynthesis research. Panjikar S, Stoeckigt J, O'Connor S, Warzecha H. Nat Prod Rep 29 1176-1200 (2012)
  12. Use of NMR techniques for toxic organophosphorus compound profiling. Koskela H. J. Chromatogr. B Analyt. Technol. Biomed. Life Sci. 878 1365-1381 (2010)
  13. [Decontamination of organophosphorus compounds: Towards new alternatives]. Poirier L, Jacquet P, Elias M, Daudé D, Chabrière E. Ann Pharm Fr 75 209-226 (2017)
  14. Environmental Occurrence, Toxicity Concerns, and Degradation of Diazinon Using a Microbial System. Wu X, Li J, Zhou Z, Lin Z, Pang S, Bhatt P, Mishra S, Chen S. Front Microbiol 12 717286 (2021)

Articles citing this publication (39)

  1. Structure and evolution of the serum paraoxonase family of detoxifying and anti-atherosclerotic enzymes. Harel M, Aharoni A, Gaidukov L, Brumshtein B, Khersonsky O, Meged R, Dvir H, Ravelli RB, McCarthy A, Toker L, Silman I, Sussman JL, Tawfik DS. Nat. Struct. Mol. Biol. 11 412-419 (2004)
  2. Loss of function of the IAA-glucose hydrolase gene TGW6 enhances rice grain weight and increases yield. Ishimaru K, Hirotsu N, Madoka Y, Murakami N, Hara N, Onodera H, Kashiwagi T, Ujiie K, Shimizu B, Onishi A, Miyagawa H, Katoh E. Nat. Genet. 45 707-711 (2013)
  3. The histidine 115-histidine 134 dyad mediates the lactonase activity of mammalian serum paraoxonases. Khersonsky O, Tawfik DS. J Biol Chem 281 7649-7656 (2006)
  4. Mechanism and cleavage specificity of the H-N-H endonuclease colicin E9. Pommer AJ, Cal S, Keeble AH, Walker D, Evans SJ, Kühlmann UC, Cooper A, Connolly BA, Hemmings AM, Moore GR, James R, Kleanthous C. J. Mol. Biol. 314 735-749 (2001)
  5. Enhanced stereoselective hydrolysis of toxic organophosphates by directly evolved variants of mammalian serum paraoxonase. Amitai G, Gaidukov L, Adani R, Yishay S, Yacov G, Kushnir M, Teitlboim S, Lindenbaum M, Bel P, Khersonsky O, Tawfik DS, Meshulam H. FEBS J. 273 1906-1919 (2006)
  6. The structure of Rauvolfia serpentina strictosidine synthase is a novel six-bladed beta-propeller fold in plant proteins. Ma X, Panjikar S, Koepke J, Loris E, Stöckigt J. Plant Cell 18 907-920 (2006)
  7. The calcium-signalling saga: tap water and protein crystals. Carafoli E. Nat. Rev. Mol. Cell Biol. 4 326-332 (2003)
  8. Sensor domain of the Mycobacterium tuberculosis receptor Ser/Thr protein kinase, PknD, forms a highly symmetric beta propeller. Good MC, Greenstein AE, Young TA, Ng HL, Alber T. J. Mol. Biol. 339 459-469 (2004)
  9. Rapid determination of hydrogen positions and protonation states of diisopropyl fluorophosphatase by joint neutron and X-ray diffraction refinement. Blum MM, Mustyakimov M, Rüterjans H, Kehe K, Schoenborn BP, Langan P, Chen JC. Proc. Natl. Acad. Sci. U.S.A. 106 713-718 (2009)
  10. In search of a catalytic bioscavenger for the prophylaxis of nerve agent toxicity. diTargiani RC, Chandrasekaran L, Belinskaya T, Saxena A. Chem. Biol. Interact. 187 349-354 (2010)
  11. Genetic and biochemical properties of an alkaline phosphatase PhoX family protein found in many bacteria. Zaheer R, Morton R, Proudfoot M, Yakunin A, Finan TM. Environ. Microbiol. 11 1572-1587 (2009)
  12. Cloning of the gene and characterization of the enzymatic properties of the monomeric alkaline phosphatase (PhoX) from Pasteurella multocida strain X-73. Wu JR, Shien JH, Shieh HK, Hu CC, Gong SR, Chen LY, Chang PC. FEMS Microbiol Lett 267 113-120 (2007)
  13. In silico analyses of substrate interactions with human serum paraoxonase 1. Hu X, Jiang X, Lenz DE, Cerasoli DM, Wallqvist A. Proteins 75 486-498 (2009)
  14. Crystal structure of human senescence marker protein 30: insights linking structural, enzymatic, and physiological functions . Chakraborti S, Bahnson BJ. Biochemistry 49 3436-3444 (2010)
  15. Reconstruction of gene association network reveals a transmembrane protein required for adipogenesis and targeted by PPARγ. Bogner-Strauss JG, Prokesch A, Sanchez-Cabo F, Rieder D, Hackl H, Duszka K, Krogsdam A, Di Camillo B, Walenta E, Klatzer A, Lass A, Pinent M, Wong WC, Eisenhaber F, Trajanoski Z. Cell. Mol. Life Sci. 67 4049-4064 (2010)
  16. Structural characterization of the catalytic calcium-binding site in diisopropyl fluorophosphatase (DFPase)--comparison with related beta-propeller enzymes. Blum MM, Chen JC. Chem. Biol. Interact. 187 373-379 (2010)
  17. Simultaneous measurement of protein one-bond and two-bond nitrogen-carbon coupling constants using an internally referenced quantitative J-correlated [(15)N,(1)H]-TROSY-HNC experiment. Wienk HL, Martínez MM, Yalloway GN, Schmidt JM, Pérez C, Rüterjans H, Löhr F. J. Biomol. NMR 25 133-145 (2003)
  18. The first crystal structure of gluconolactonase important in the glucose secondary metabolic pathways. Chen CN, Chin KH, Wang AH, Chou SH. J. Mol. Biol. 384 604-614 (2008)
  19. A strategy to obtain backbone resonance assignments of deuterated proteins in the presence of incomplete amide 2H/1H back-exchange. Löhr F, Katsemi V, Hartleib J, Günther U, Rüterjans H. J. Biomol. NMR 25 291-311 (2003)
  20. Hydrolysis of DFP and the nerve agent (S)-sarin by DFPase proceeds along two different reaction pathways: implications for engineering bioscavengers. Wymore T, Field MJ, Langan P, Smith JC, Parks JM. J Phys Chem B 118 4479-4489 (2014)
  21. The geometry of interactions between catalytic residues and their substrates. Torrance JW, Holliday GL, Mitchell JB, Thornton JM. J. Mol. Biol. 369 1140-1152 (2007)
  22. Variation in protein C(alpha)-related one-bond J couplings. Schmidt JM, Howard MJ, Maestre-Martínez M, Pérez CS, Löhr F. Magn Reson Chem 47 16-30 (2009)
  23. Hyperthermophilic phosphotriesterases/lactonases for the environment and human health. Mandrich L, Merone L, Manco G. Environ Technol 31 1115-1127 (2010)
  24. Monitoring the hydrolysis of toxic organophosphonate nerve agents in aqueous buffer and in bicontinuous microemulsions by use of diisopropyl fluorophosphatase (DFPase) with (1)H- (31)P HSQC NMR spectroscopy. Gäb J, Melzer M, Kehe K, Wellert S, Hellweg T, Blum MM. Anal Bioanal Chem 396 1213-1221 (2010)
  25. Quantification of hydrolysis of toxic organophosphates and organophosphonates by diisopropyl fluorophosphatase from Loligo vulgaris by in situ Fourier transform infrared spectroscopy. Gäb J, Melzer M, Kehe K, Richardt A, Blum MM. Anal. Biochem. 385 187-193 (2009)
  26. Hydrogen atoms in protein structures: high-resolution X-ray diffraction structure of the DFPase. Elias M, Liebschner D, Koepke J, Lecomte C, Guillot B, Jelsch C, Chabriere E. BMC Res Notes 6 308 (2013)
  27. Biochemical and biophysical characterization of the selenium-binding and reducing site in Arabidopsis thaliana homologue to mammals selenium-binding protein 1. Schild F, Kieffer-Jaquinod S, Palencia A, Cobessi D, Sarret G, Zubieta C, Jourdain A, Dumas R, Forge V, Testemale D, Bourguignon J, Hugouvieux V. J. Biol. Chem. 289 31765-31776 (2014)
  28. In vitro and in vivo efficacy of PEGylated diisopropyl fluorophosphatase (DFPase). Melzer M, Heidenreich A, Dorandeu F, Gäb J, Kehe K, Thiermann H, Letzel T, Blum MM. Drug Test Anal 4 262-270 (2012)
  29. The DFPase from Loligo vulgaris in sugar surfactant-based bicontinuous microemulsions: structure, dynamics, and enzyme activity. Wellert S, Tiersch B, Koetz J, Richardt A, Lapp A, Holderer O, Gäb J, Blum MM, Schulreich C, Stehle R, Hellweg T. Eur. Biophys. J. 40 761-774 (2011)
  30. The Dca gene involved in cold adaptation in Drosophila melanogaster arose by duplication of the ancestral regucalcin gene. Arboleda-Bustos CE, Segarra C. Mol. Biol. Evol. 28 2185-2195 (2011)
  31. Cell surface proteins in archaeal and bacterial genomes comprising "LVIVD", "RIVW" and "LGxL" tandem sequence repeats are predicted to fold as beta-propeller. Adindla S, Inampudi KK, Guruprasad L. Int. J. Biol. Macromol. 41 454-468 (2007)
  32. Engineering strictosidine synthase: rational design of a small, focused circular permutation library of the β-propeller fold enzyme. Fischereder E, Pressnitz D, Kroutil W, Lutz S. Bioorg. Med. Chem. 22 5633-5637 (2014)
  33. In vitro toxicokinetic studies of cyclosarin: molecular mechanisms of elimination. Reiter G, Müller S, Koller M, Thiermann H, Worek F. Toxicol. Lett. 227 1-11 (2014)
  34. Similar Active Sites and Mechanisms Do Not Lead to Cross-Promiscuity in Organophosphate Hydrolysis: Implications for Biotherapeutic Engineering. Purg M, Elias M, Kamerlin SCL. J. Am. Chem. Soc. 139 17533-17546 (2017)
  35. Ultrahigh-Throughput Directed Evolution of a Metal-Free α/β-Hydrolase with a Cys-His-Asp Triad into an Efficient Phosphotriesterase. Schnettler JD, Klein OJ, Kaminski TS, Colin PY, Hollfelder F. J Am Chem Soc 145 1083-1096 (2023)
  36. Computational enzymology for degradation of chemical warfare agents: promising technologies for remediation processes. de Castro AA, Assis LC, Silva DR, Corrêa S, Assis TM, Gajo GC, Soares FV, Ramalho TC. AIMS Microbiol 3 108-135 (2017)
  37. Probing the Suitability of Different Ca2+ Parameters for Long Simulations of Diisopropyl Fluorophosphatase. Zlobin A, Diankin I, Pushkarev S, Golovin A. Molecules 26 5839 (2021)
  38. Theoretical Studies on Catalysis Mechanisms of Serum Paraoxonase 1 and Phosphotriesterase Diisopropyl Fluorophosphatase Suggest the Alteration of Substrate Preference from Paraoxonase to DFP. Zhang H, Yang L, Ma YY, Zhu C, Lin S, Liao RZ. Molecules 23 (2018)
  39. Three-dimensional structure and ligand-binding site of carp fishelectin (FEL). Capaldi S, Faggion B, Carrizo ME, Destefanis L, Gonzalez MC, Perduca M, Bovi M, Galliano M, Monaco HL. Acta Crystallogr. D Biol. Crystallogr. 71 1123-1135 (2015)


Related citations provided by authors (1)

  1. Crystallization and preliminary X-ray crystallographic analysis of DFPase from Loligo vulgaris.. Scharff EI, Lücke C, Fritzsch G, Koepke J, Hartleib J, Dierl S, Rüterjans H Acta Crystallogr D Biol Crystallogr 57 148-9 (2001)

Quick links