Organophosphate hydrolases as catalytic bioscavengers of organophosphorus nerve agents

Toxicology Letters

Volumn 206, Issue 1, 2011, Pages 14-23

  Trovaslet Leroy, Marie ^a   Musilova, Lucie ^b   Renault, Frédérique ^a   Brazzolotto, Xavier ^a   Misik, Jan ^c   Novotny, Ladislav ^d   Froment, Marie Thérèse ^a   Gillon, Emilie ^a   Loiodice, Mélanie ^a   Verdier, Laurent ^e   Masson, Patrick ^e   Rochu, Daniel ^e   Jun, Daniel ^b,f,g   Nachon, Florian ^a  

^a Institut de Recherches Biomédicales des Armées   (France)

^b UNIVERSITY HOSPITAL HRADEC KRALOVE   (Czech Republic)

^c UNIVERSITY OF DEFENCE   (Czech Republic)

^d UNIVERSITY OF VETERINARY AND PHARMACEUTICAL SCIENCES   (Czech Republic)

^e Delegation Generale pour l'Armement   (France)

^f UNIVERSITY OF DEFENCE   (Czech Republic)

^g CZECH UNIVERSITY OF LIFE SCIENCES PRAGUE   (Czech Republic)

Author keywords

Acetylcholinesterase; Bioscavenger; Organophosphate poisoning; Paraoxonase; Phosphotriesterase; Prophylaxis

Indexed keywords

ACETYLTHIOCHOLINE; ARYLDIALKYLPHOSPHATASE 1; ASPARAGINE; CHOLINESTERASE; GLYCINE; HISTIDINE; HYDROLASE; ORGANOPHOSPHATE; ORGANOPHOSPHORUS COMPOUND; PHOSPHOTRIESTERASE; SCAVENGER;

AMINO ACID SUBSTITUTION; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; BIOAVAILABILITY; CATALYSIS; CONTROLLED STUDY; ENANTIOSELECTIVITY; ENZYME ACTIVITY; ENZYME INHIBITION; ENZYME KINETICS; ENZYME STABILITY; ENZYME STRUCTURE; FEMALE; HUMAN; HYDROLYSIS; IMMUNOGENICITY; IN VIVO STUDY; MOUSE; NONHUMAN; NUCLEOPHILICITY; PHOSPHORYLATION; PRIORITY JOURNAL; PROTEIN EXPRESSION; RAT; SULFOLOBUS SOLFATARICUS; THERMOSTABILITY;

ACETYLCHOLINESTERASE; ANIMALS; ARYLDIALKYLPHOSPHATASE; BIOCATALYSIS; CHEMICAL WARFARE AGENTS; CHO CELLS; CHOLINESTERASE REACTIVATORS; CLONING, MOLECULAR; CRICETINAE; CRICETULUS; DRUG STABILITY; FEMALE; HYDROLYSIS; MUTATION; ORGANOPHOSPHORUS COMPOUNDS; PHOSPHORIC TRIESTER HYDROLASES; RATS; RATS, WISTAR; SUBSTRATE SPECIFICITY; TRANSFECTION;

BACTERIA (MICROORGANISMS); MAMMALIA; RATTUS;

EID: 80051826630     PISSN: 03784274     EISSN: 18793169     Source Type: Journal    
DOI: 10.1016/j.toxlet.2011.05.1041     Document Type: Article

References (65)

1. Aharoni A., Gaidukov L., Yagur S., Toker L., Silman I., Tawfik D.S. Directed evolution of mammalian paraoxonases PON1 and PON3 for bacterial expression and catalytic specialization. Proc. Natl Acad. Sci. U.S.A. 2004, 101:482-487.
2. Ashani Y., Pistinner S. Estimation of the upper limit of human butyrylcholinesterase dose required for protection against organophosphates toxicity: a mathematically based toxicokinetic model. Toxicol. Sci. 2004, 77:358-367.
3. Aurbek N., Thiermann H., Eyer F., Eyer P., Worek F. Suitability of human butyrylcholinesterase as therapeutic marker and pseudo catalytic scavenger in organophosphate poisoning: a kinetic analysis. Toxicology 2009, 259:133-139.
4. Bourne Y., Radic Z., Sulzenbacher G., Kim E., Taylor P., Marchot P. Substrate and product trafficking through the active center gorge of acetylcholinesterase analyzed by crystallography and equilibrium binding. J. Biol. Chem. 2006, 281:29256-29267.
5. Cannard K. The acute treatment of nerve agent exposure. J. Neurol. Sci. 2006, 249:86-94.
6. Carletti E., Jacquamet L., Loiodice M., Rochu D., Masson P., Nachon F. Update on biochemical properties of recombinant Pseudomonas diminuta phosphotriesterase. J. Enzyme Inhib. Med. Chem. 2009, 24:1045-1055.
7. Carletti E., Li H., Li B., Ekstrom F., Nicolet Y., Loiodice M., Gillon E., Froment M.T., Lockridge O., Schopfer L.M., Masson P., Nachon F. Aging of cholinesterases phosphylated by tabun proceeds through O-dealkylation. J. Am. Chem. Soc. 2008, 130:16011-16020.
8. Chen-Goodspeed M., Sogorb M.A., Wu F., Hong S.B., Raushel F.M. Structural determinants of the substrate and stereochemical specificity of phosphotriesterase. Biochemistry 2001, 40:1325-1331.
9. Clery-Barraud C., Renault F., Leva J., El Bakdouri N., Masson P., Rochu D. Exploring the structural and functional stabilities of different paraoxonase-1 formulations through electrophoretic mobilities and enzyme activity parameters under hydrostatic pressure. Biochim. Biophys. Acta 2009, 1794:680-688.
10. Colletier J.P., Fournier D., Greenblatt H.M., Stojan J., Sussman J.L., Zaccai G., Silman I., Weik M. Structural insights into substrate traffic and inhibition in acetylcholinesterase. EMBO J. 2006, 25:2746-2756.
11. de Koning, M.C., van Grol, M., Noort, D., Peripheral site ligand conjugation to a non-quaternary oxime enhances reactivation of nerve agent-inhibited human acetylcholinesterase. Toxicol. Lett. doi:10.1016/j.toxlet.2011.04.004.
12. Elias M., Dupuy J., Merone L., Mandrich L., Porzio E., Moniot S., Rochu D., Lecomte C., Rossi M., Masson P., Manco G., Chabriere E. Structural basis for natural lactonase and promiscuous phosphotriesterase activities. J. Mol. Biol. 2008, 379:1017-1028.
13. Ellman G.L., Courtney K.D., Andres V., Feather-Stone R.M. A new and rapid colorimetric determination of acetylcholinesterase activity. Biochem. Pharmacol. 1961, 7:88-95.
14. Genovese R.F., Sun W., Johnson C.C., Ditargiani R.C., Doctor B.P., Saxena A. Safety of administration of human butyrylcholinesterase and its conjugates with soman or VX in rats. Basic Clin. Pharmacol. Toxicol. 2010, 106:428-434.
15. Geyer B.C., Kannan L., Cherni I., Woods R.R., Soreq H., Mor T.S. Transgenic plants as a source for the bioscavenging enzyme, human butyrylcholinesterase. Plant Biotechnol. J. 2010, 8:873-886.
16. Geyer B.C., Kannan L., Garnaud P.E., Broomfield C.A., Cadieux C.L., Cherni I., Hodgins S.M., Kasten S.A., Kelley K., Kilbourne J., Oliver Z.P., Otto T.C., Puffenberger I., Reeves T.E., Robbins N., 2nd, Woods R.R., Soreq H., Lenz D.E., Cerasoli D.M., Mor T.S. Plant-derived human butyrylcholinesterase, but not an organophosphorous-compound hydrolyzing variant thereof, protects rodents against nerve agents. Proc. Natl. Acad. Sci. U.S.A. 2010, 107:20251-20256.
17. Gupta R.D., Goldsmith M., Ashani Y., Simo Y., Mullokandov G., Bar H., Ben-David M., Leader H., Margalit R., Silman I., Sussman J.L., Tawfik D.S. Directed evolution of hydrolases for prevention of G-type nerve agent intoxication. Nat. Chem. Biol. 2011, 7:120-125.
18. Harel M., Aharoni A., Gaidukov L., Brumshtein B., Khersonsky O., Meged R., Dvir H., Ravelli R.B., McCarthy A., Toker L., Silman I., Sussman J.L., Tawfik D.S. Structure and evolution of the serum paraoxonase family of detoxifying and anti-atherosclerotic enzymes. Nat. Struct. Mol. Biol. 2004, 11:412-419.
19. Harris J.M., Chess R.B. Effect of pegylation on pharmaceuticals. Nat. Rev. Drug Discov. 2003, 2:214-221.
20. Heffron P.F., Hobbiger F. Relationship between inhibition of acetylcholinesterase and response of the rat phrenic nerve-diaphragm preparation to indirect stimulation at higher frequencies. Br. J. Pharmacol. 1979, 66:323-329.
21. Huang Y.J., Huang Y., Baldassarre H., Wang B., Lazaris A., Leduc M., Bilodeau A.S., Bellemare A., Cote M., Herskovits P., Touati M., Turcotte C., Valeanu L., Lemee N., Wilgus H., Begin I., Bhatia B., Rao K., Neveu N., Brochu E., Pierson J., Hockley D.K., Cerasoli D.M., Lenz D.E., Karatzas C.N., Langermann S. Recombinant human butyrylcholinesterase from milk of transgenic animals to protect against organophosphate poisoning. Proc. Natl. Acad. Sci. U. S. A. 2007, 104:13603-13608.
22. Huang Y.J., Lundy P.M., Lazaris A., Huang Y., Baldassarre H., Wang B., Turcotte C., Cote M., Bellemare A., Bilodeau A.S., Brouillard S., Touati M., Herskovits P., Begin I., Neveu N., Brochu E., Pierson J., Hockley D.K., Cerasoli D.M., Lenz D.E., Wilgus H., Karatzas C.N., Langermann S. Substantially improved pharmacokinetics of recombinant human butyrylcholinesterase by fusion to human serum albumin. BMC Biotechnol. 2008, 8:50.
23. Järv J. Stereochemical aspects of cholinesterase catalysis. Bioorganic Chemistry 1984, 12:259-278.
24. Jun D., Kuca K., Balgar J., Hruby M., Kucka J., Renault F., Masson P. Phosphotriesterase modified by poly[N-(2-hydroxypropyl)methacrylamide]. Toxicology 2007, 233:235.
25. Jun D., Musilova L., Link M., Loiodice M., Nachon F., Rochu D., Renault F., Masson P. Preparation and characterization of methoxy polyethylene glycol-conjugated phosphotriesterase as a potential catalytic bioscavenger against organophosphate poisoning. Chem. Biol. Interact. 2010, 187:380-383.
26. Kalisiak J., Ralph E.C., Zhang J., Cashman J.R. Amidine-oximes: reactivators for organophosphate exposure. J. Med. Chem. 2011, 54:3319-3330.
27. Kovarik Z., Katalinic M., Sinko G., Binder J., Holas O., Jung Y.S., Musilova L., Jun D., Kuca K. Pseudo-catalytic scavenging: searching for a suitable reactivator of phosphorylated butyrylcholinesterase. Chem. Biol. Interact. 2010, 187:167-171.
28. Kovarik Z., Radic Z., Berman H.A., Taylor P. Mutation of acetylcholinesterase to enhance oxime-assisted catalytic turnover of methylphosphonates. Toxicology 2007, 233:79-84.
29. Kronman C., Cohen O., Mazor O., Ordentlich A., Raveh L., Velan B., Shafferman A. Next generation OP-bioscavengers: a circulatory long-lived 4-PEG hypolysine mutant of F338A-HuAChE with optimal pharmacokinetics and pseudo-catalytic characteristics. Chem. Biol. Interact. 2010, 187:253-258.
30. Lenz D.E., Broomfield C.A., Yeung D.T., Masson P., Maxwell D.M., Cerasoli D.M. Nerve agent bioscavengers: progress in development of a new mode of protection against organophosphorus exposure. Chemical Warfare Agents: Chemistry, Pharmacology, Toxicology and Therapeutics 2007, 145-173. CRC Press, Boca Raton, FL. J.A. Romano, B.J. Luckey, H. Salem (Eds.).
31. Li W.S., Lum K.T., Chen-Goodspeed M., Sogorb M.A., Raushel F.M. Stereoselective detoxification of chiral sarin and soman analogues by phosphotriesterase. Bioorg. Med. Chem. 2001, 9:2083-2091.
32. Lockridge O., Blong R.M., Masson P., Froment M.T., Millard C.B., Broomfield C.A. A single amino acid substitution, Gly117His, confers phosphotriesterase (organophosphorus acid anhydride hydrolase) activity on human butyrylcholinesterase. Biochemistry 1997, 36:786-795.
33. Lorke D.E., Kalasz H., Petroianu G.A., Tekes K. Entry of oximes into the brain: a review. Curr. Med. Chem. 2008, 15:743-753.
34. Lushchekina, S., Masson, P., Nachon, F., Nemukhin, A.V., Varfolomeev, S.D., 2011. QM/MM modeling of the G117H butyrylcholinesterase catalyzed echothiophate hydrolysis reaction mechanism. Poster at the 13th Medical Chemical Defence Conference, Munich, 13-14th April 2011.
35. Masson P., Nachon F., Broomfield C.A., Lenz D.E., Verdier L., Schopfer L.M., Lockridge O. A collaborative endeavor to design cholinesterase-based catalytic scavengers against toxic organophosphorus esters. Chem. Biol. Interact. 2008, 175:273-280.
36. Masson P., Nachon F., Lockridge O. Structural approach to the aging of phosphylated cholinesterases. Chem. Biol. Interact. 2010, 187:157-162.
37. Maxwell D.M., Brecht K.M., Koplovitz I., Sweeney R.E. Acetylcholinesterase inhibition: does it explain the toxicity of organophosphorus compounds?. Arch. Toxicol. 2006, 80:756-760.
38. Maynard R.L., Beswick F.W. Organophosphorus compounds as chemical warfare agents. Clinical and Experimental Toxicology of Organophosphates and Carbamates. 1992, 373-385. Butterworth, Oxford. B. Ballantyne, T.C. Marrs (Eds.).
39. Mercey G., Verdelet T., Saint-Andre G., Gillon E., Wagner A., Baati R., Jean L., Nachon F., Renard P.Y. First efficient uncharged reactivators for the dephosphylation of poisoned human acetylcholinesterase. Chem. Commun. (Camb.) 2011, 47:5295-5297.
40. Merone L., Mandrich L., Porzio E., Rossi M., Muller S., Reiter G., Worek F., Manco G. Improving the promiscuous nerve agent hydrolase activity of a thermostable archaeal lactonase. Bioresour. Technol. 2010, 101:9204-9212.
41. Merone L., Mandrich L., Rossi M., Manco G. A thermostable phosphotriesterase from the archaeon Sulfolobus solfataricus: cloning, overexpression and properties. Extremophiles 2005, 9:297-305.
42. Millard C.B., Lockridge O., Broomfield C.A. Design and expression of organophosphorus acid anhydride hydrolase activity in human butyrylcholinesterase. Biochemistry 1995, 34:15925-15933.
43. Millard C.B., Lockridge O., Broomfield C.A. Organophosphorus acid anhydride hydrolase activity in human butyrylcholinesterase: synergy results in a somanase. Biochemistry 1998, 37:237-247.
44. Nachon F., Carletti E., Wandhammer M., Nicolet Y., Schopfer L.M., Masson P., Lockridge O. X-ray crystallographic snapshots of reaction intermediates in the G117H mutant of human butyrylcholinesterase, a nerve agent target engineered into a catalytic bioscavenger. Biochem. J. 2011, 434:73-82.
45. Offord R.E. Electrophoretic mobilities of peptides on paper and their use in the determination of amide groups. Nature 1966, 211:591-593.
46. Omburo G.A., Kuo J.M., Mullins L.S., Raushel F.M. Characterization of the zinc binding site of bacterial phosphotriesterase. J. Biol. Chem. 1992, 267:13278-13283.
47. Otto T.C., Harsch C.K., Yeung D.T., Magliery T.J., Cerasoli D.M., Lenz D.E. Dramatic differences in organophosphorus hydrolase activity between human and chimeric recombinant mammalian paraoxonase-1 enzymes. Biochemistry 2009, 48:10416-10422.
48. Poyot T., Nachon F., Froment M.T., Loiodice M., Wieseler S., Schopfer L.M., Lockridge O., Masson P. Mutant of Bungarus fasciatus acetylcholinesterase with low affinity and low hydrolase activity toward organophosphorus esters. Biochim. Biophys. Acta 2006, 1764:1470-1478.
49. Radic Z., Pickering N.A., Vellom D.C., Camp S., Taylor P. Three distinct domains in the cholinesterase molecule confer selectivity for acetyl- and butyrylcholinesterase inhibitors. Biochemistry 1993, 32:12074-12084.
50. Renault F., Carus T., Clery-Barraud C., Elias M., Chabriere E., Masson P., Rochu D. Integrative analytical approach by capillary electrophoresis and kinetics under high pressure optimized for deciphering intrinsic and extrinsic cofactors that modulate activity and stability of human paraoxonase (PON1). J. Chromatogr. B: Analyt. Technol. Biomed. Life. Sci. 2010, 878:1346-1355.
51. Renault F., Chabriere E., Andrieu J.P., Dublet B., Masson P., Rochu D. Tandem purification of two HDL-associated partner proteins in human plasma, paraoxonase (PON1) and phosphate binding protein (HPBP) using hydroxyapatite chromatography. J. Chromatogr. B Analyt. Technol. Biomed. Life. Sci. 2006, 836:15-21.
52. Rochu D., Beaufet N., Renault F., Viguie N., Masson P. The wild type bacterial Co(2+)/Co(2+)-phosphotriesterase shows a middle-range thermostability. Biochim. Biophys. Acta 2002, 1594:207-218.
53. Rochu D., Chabriere E., Masson P. Human paraoxonase: a promising approach for pre-treatment and therapy of organophosphorus poisoning. Toxicology 2007, 233:47-59.
54. Rochu D., Chabriere E., Renault F., Elias M., Clery-Barraud C., Masson P. Stabilization of the active form(s) of human paraoxonase by human phosphate-binding protein. Biochem. Soc. Trans. 2007, 35:1616-1620.
55. Rochu D., Ducret G., Masson P. Measuring conformational stability of proteins using an optimized temperature-controlled capillary electrophoresis approach. J. Chromatogr. A 1999, 838:157-165.
56. Rochu D., Renault F., Clery-Barraud C., Chabriere E., Masson P. Stability of highly purified human paraoxonase (PON1): association with human phosphate binding protein (HPBP) is essential for preserving its active conformation(s). Biochim. Biophys. Acta 2007, 1774:874-883.
57. Rochu D., Viguie N., Renault F., Crouzier D., Froment M.T., Masson P. Contribution of the active-site metal cation to the catalytic activity and to the conformational stability of phosphotriesterase: temperature- and pH-dependence. Biochem. J. 2004, 380:627-633.
58. Roodveldt C., Tawfik D.S. Directed evolution of phosphotriesterase from Pseudomonas diminuta for heterologous expression in Escherichia coli results in stabilization of the metal-free state. Protein Eng. Des. Sel. 2005, 18:51-58.
59. Saxena A., Sun W., Fedorko J.M., Koplovitz I., Doctor B.P. Prophylaxis with human serum butyrylcholinesterase protects guinea pigs exposed to multiple lethal doses of soman or VX. Biochem. Pharmacol. 2011, 81:164-169.
60. Saxena A., Tipparaju P., Luo C., Doctor B.P. Pilot-scale production of human serum butyrylcholinesterase suitable for use as a bioscavenger against nerve agent toxicity. Process Biochemistry 2010, 45:1313-1318.
61. Sweeney R.E., Maxwell D.M. A theoretical expression for the protection associated with stoichiometric and catalytic scavengers in a single compartment model of organophosphorus poisoning. Math. Biosci. 2003, 181:133-143.
62. Tsai P.C., Bigley A., Li Y., Ghanem E., Cadieux C.L., Kasten S.A., Reeves T.E., Cerasoli D.M., Raushel F.M. Stereoselective hydrolysis of organophosphate nerve agents by the bacterial phosphotriesterase. Biochemistry 2010, 49:7978-7987.
63. Wang Y., Boeck A.T., Duysen E.G., Van Keuren M., Saunders T.L., Lockridge O. Resistance to organophosphorus agent toxicity in transgenic mice expressing the G117H mutant of human butyrylcholinesterase. Toxicol. Appl. Pharmacol. 2004, 196:356-366.
64. Wolfe A.D., Rush R.S., Doctor B.P., Koplovitz I., Jones D. Acetylcholinesterase prophylaxis against organophosphate toxicity. Fundam. Appl. Toxicol. 1987, 9:266-270.
65. Worek F., Thiermann H., Szinicz L., Eyer P. Kinetic analysis of interactions between human acetylcholinesterase, structurally different organophosphorus compounds and oximes. Biochem. Pharmacol. 2004, 68:2237-2248.