Paradox findings may challenge orthodox reasoning in acute organophosphate poisoning

Chemico-Biological Interactions

Volumn 187, Issue 1-3, 2010, Pages 270-278

  Eyer, Peter ^a   Worek, Franz ^b   Thiermann, Horst ^b   Eddleston, Michael ^c  

^a UNIVERSITY OF MUNICH   (Germany)

^b BUNDESWEHR INSTITUTE OF PHARMACOLOGY AND TOXICOLOGY   (Germany)

^c UNIVERSITY OF EDINBURGH   (United Kingdom)

Author keywords

Isomerides; Kinetics; Organophosphorus insecticides; Oximes; Paraoxonase 1; Pathophysiology

Indexed keywords

ACETYLCHOLINE; ACETYLCHOLINESTERASE; CHLORPYRIFOS; DIMETHOATE; DOPAMINE; MALATHION; OBIDOXIME; ORGANOPHOSPHATE INSECTICIDE; OXIME; PARATHION; PROFENOFOS;

ARTICLE; CHOLINERGIC SYNAPSE; CHOLINERGIC SYSTEM; COMPUTER SIMULATION; CONTINUOUS INFUSION; ENZYME INHIBITION; ENZYME PHOSPHORYLATION; ENZYME REACTIVATION; ERYTHROCYTE; FLUID RESUSCITATION; HUMAN; HYDROLYSIS; HYPOTENSION; INHIBITION KINETICS; INTOXICATION; MICHAELIS MENTEN KINETICS; NERVE CELL PLASTICITY; NONHUMAN; OXIDATION; SELF POISONING; STEREOISOMERISM;

EID: 77955513272     PISSN: 00092797     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.cbi.2009.10.014     Document Type: Article

References (71)

1. Jeyaratnam J. Acute pesticide poisoning: a major global health problem. World Health Stat. Q. 1990, 43:139-144.
2. Gunnell D., Eddleston M., Phillips M.R., Konradsen F. The global distribution of fatal pesticide self-poisoning: systematic review. BMC Public Health 2007, 7:357.
3. Mileson B.E., Chambers J.E., Chen W.L., Dettbarn W., Ehrich M., Eldefrawi A.T., Gaylor D.W., Hamernik K., Hodgson E., Karczmar A.G., Padilla S., Pope C.N., Richardson R.J., Saunders D.R., Sheets L.P., Sultatos L.G., Wallace K.B. Common mechanism of toxicity: a case study of organophosphorus pesticides. Toxicol. Sci. 1998, 41:8-20.
4. Johnson M.K. Organophosphorus esters causing delayed neurotoxic effects. Mechanism of action and structure/activity studies. Arch. Toxicol. 1975, 34:259-288.
5. Pope C.N. Organophosphorus pesticides: do they all have the same mechanism of toxicity?. J. Toxicol. Environ. Health Part B 1999, 2:161-181.
6. Pope C.N., Karanth S., Liu J. Pharmacology and toxicology of cholinesterase inhibitors: uses and misuses of a common mechanism of action. Environ. Toxicol. Pharmacol. 2005, 19:433-446.
7. Nallapaneni A., Liu J., Karanth S., Pope C. Pharmacological enhancement of endocannabinoid signaling reduces the cholinergic toxicity of diisopropylfluorophosphate. Neurotoxicology 2008, 29:1037-1043.
8. Worek F., Bäcker M., Thiermann H., Szinicz L., Mast U., Klimmek R., Eyer P. Reappraisal of indications and limitations of oxime therapy in organophosphate poisoning. Hum. Exp. Toxicol. 1997, 16:466-472.
9. Thiermann H., Mast U., Klimmek R., Eyer P., Hibler A., Pfab R., Felgenhauer N., Zilker T. Cholinesterase status, pharmacokinetics and laboratory findings during obidoxime therapy in organophosphate poisoned patients. Hum. Exp. Toxicol. 1997, 16:473-480.
10. Eyer F., Worek F., Eyer P., Felgenhauer N., Haberkorn M., Zilker T., Thiermann H. Obidoxime in acute organophosphate poisoning: 1. Clinical effectiveness. Clin. Toxicol. 2009, 47:798-806.
11. Thiermann H., Worek F., Eyer P., Eyer F., Felgenhauer N., Zilker T. Obidoxime in acute organophosphate poisoning: 2. PK/PD relationships. Clin. Toxicol. 2009, 47:807-813.
12. Eyer P. The role of oximes in the management of organophosphorus pesticide poisoning. Toxicol. Rev. 2003, 22:165-190.
13. Main A.R. Affinity and phosphorylation constants for the inhibition of esterases by organophosphates. Science 1964, 144:992-993.
14. Aldridge W.N., Reiner E. Enzyme inhibitors as substrates. Interactions of esterases with esters of organophosphorus and carbamic acids 1972, North-Holland Publ. Co., Amsterdam.
15. Carr R.L., Chambers J.E. Kinetic analysis of the in vitro inhibition, aging, and reactivation of brain acetylcholinesterase from rat and channel catfish by paraoxon and chlorpyrifos-oxon. Toxicol. Appl. Pharmacol. 1996, 139:365-373.
16. Rosenfeld C.A., Sultatos L.G. Concentration-dependent kinetics of acetylcholinesterase inhibition by the organophosphate paraoxon. Toxicol. Sci. 2006, 90:460-469.
17. Eyer F., Eyer P. Enzyme-based assay for quantification of paraoxon in blood of parathion poisoned patients. Hum. Exp. Toxicol. 1998, 17:645-651.
18. Kardos S.A., Sultatos L.G. Interactions of the organophosphates paraoxon and methyl paraoxon with mouse brain acetylcholinesterase. Toxicol. Sci. 2000, 58:118-126.
19. Kousba A.A., Sultatos L.G., Poet T.S., Timchalk C. Comparison of chlorpyrifos-oxon and paraoxon acetylcholinesterase inhibition dynamics: potential role of a peripheral binding site. Toxicol. Sci. 2004, 80:239-248.
20. Kaushik R., Rosenfeld C.A., Sultatos L.G. Concentration-dependent interactions of the organophosphates chlorpyrifos oxon and methyl paraoxon with human recombinant acetylcholinesterase. Toxicol. Appl. Pharmacol. 2007, 221:243-250.
21. Stenzel J., Worek F., Eyer P. Preparation and characterization of dialkylphosphoryl-obidoxime conjugates, potent anticholinesterase derivatives that are quickly hydrolyzed by human paraoxonase (PON1(192Q)). Biochem. Pharmacol. 2007, 74:1390-1400.
22. Eyer P., Kiderlen D., Stenzel J., Thiermann H., Worek F. Paraoxonase polymorphism. A modifying factor that influences oxime effectiveness. Clin. Toxicol. 2006, 44:440-441.
23. Worek F., Diepold C., Eyer P. Dimethylphosphoryl-inhibited human cholinesterases: inhibition, reactivation, and aging kinetics. Arch. Toxicol. 1999, 73:7-14.
24. Heilmair R., Eyer F., Eyer P. Enzyme-based assay for quantification of chlorpyrifos oxon in human plasma. Toxicol. Lett. 2008, 181:19-24.
25. Eyer F., Roberts D.M., Buckley N.A., Eddleston M., Thiermann H., Worek F., Eyer P. Extreme variability in the formation of chlorpyrifos oxon (CPO) in patients poisoned by chlorpyrifos (CPF). Biochem. Pharmacol. 2009, 78:531-537.
26. Erdmann W.D., Zech R., Franke P., Bosse J. On the problem of the therapeutic effectiveness of esterase reactivators in dimethoate poisoning. Arzneim. Forsch. 1966, 4:492-494.
27. Eddleston M., Eyer P., Worek F., Mohamed F., Senarathna L., von Meyer L., Juszczak E., Hittarage A., Azhar S., Dissanayake W., Sheriff M.H., Szinicz L., Dawson A.H., Buckley N.A. Differences between organophosphorus insecticides in human self-poisoning: a prospective cohort study. Lancet 2005, 366:1452-1459.
28. Meleney W.P., Peterson H.O. The relationship of shelf age to toxicity of dimethoate to sheep. J. Am. Vet. Med. Assoc. 1964, 144:756-758.
29. Andreozzi R., Ialongo G., Marotta R., Sanchirico R. The thermal decomposition of dimethoate. J. Hazard. Mater. 1999, 64:283-294.
30. Eyer P., Radtke M., Worek F. Reactions of isodimethoate with human red cell acetylcholinesterase. Biochem. Pharmacol. 2008, 75:2045-2053.
31. FAO, FAO specifications and evaluations for agricultural pesticides: dimethoate, http://www.who.int/whopes/quality/en/Dimethoate_eval_april_2006.pdf.
32. M. Eddleston, J.B. Harris, R.E. Clutton, A Göttingen minipig model of dimethoate organophosphorus pesticide poisoning, 10th International Meeting on Cholinesterases, 20-25 September, 2009, Sibenik, Croatia, Abstract L5-1.
33. Thompson C.M., Frick J.A., Natke B.C., Hansen L.K. Preparation, analysis, and anticholinesterase properties of O,O-dimethyl phosphorothioate isomerides. Chem. Res. Toxicol. 1989, 2:386-391.
34. Ryu S.M., Lin J., Thompson C.M. Comparative anticholinesterase potency of chiral isoparathion methyl. Chem. Res. Toxicol. 1991, 4:517-520.
35. Aldridge W.N., Miles J.W., Mount D.L., Verschoyle R.D. The toxicological properties of impurities in malathion. Arch. Toxicol. 1979, 42:95-106.
36. Berkman C.E., Ryu S., Quinn D.A., Thompson C.M. Kinetics of the postinhibitory reactions of acetylcholinesterase poisoned by chiral isomalathion: a surprising nonreactivation induced by the RP stereoisomers. Chem. Res. Toxicol. 1993, 6:28-32.
37. Jianmongkol S., Marable B.R., Berkman C.E., Talley T.T., Thompson C.M., Richardson R.J. Kinetic evidence for different mechanisms of acetylcholinesterase inhibition by (1R)- and (1S)-stereoisomers of isomalathion. Toxicol. Appl. Pharmacol. 1999, 155:43-53.
38. Doorn J.A., Gage D.A., Schall M., Talley T.T., Thompson C.M., Richardson R.J. Inhibition of acetylcholinesterase by (1S, 3S)-isomalathion proceeds with loss of thiomethyl: kinetic and mass spectral evidence for an unexpected primary leaving group. Chem. Res. Toxicol. 2000, 13:1313-1320.
39. Doorn J.A., Thompson C.M., Christner R.B., Richardson R.J. Stereoselective inactivation of torpedo californica acetylcholinesterase by isomalathion: Inhibitory reactions with (1-R)- and (1-S)-isomers proceed by different mechanisms. Chem. Res. Toxicol. 2003, 16:958-965.
40. Thompson C.M., Ryu S., Berkman C.E. Consequence of phosphorus stereochemistry upon the postinhibitory reaction kinetics of acetylcholinesterse poisoned by phosphorothiolates. J. Am. Chem. Soc. 1992, 114:10710-10715.
41. Clothier B., Johnson M.K., Reiner E. Interaction of some trialkyl phosphorothiolates with acetylcholinesterase. Characterization of inhibition, aging and reactivation. Biochim. Biophys. Acta 1981, 660:306-316.
42. Eddleston M., Worek F., Eyer P., Thiermann H., von Meyer L., Jeganathan K., Sheriff M.H., Dawson A.H., Buckley N.A. Poisoning with the S-alkyl organophosphorus insecticides profenofos and prothiofos. Q. J. Med. 2009, 102:785-792.
43. Nillos M.G., Rodriguez-Fuentes G., Gan J., Schlenk D. Enantioselective acetylcholinesterase inhibition of the organophosphorous insecticides profenofos, fonofos, and crotoxyphos. Environ. Toxicol. Chem. 2007, 26:1949-1954.
44. Wing K.D., Glickman A.H., Casida J.E. Oxidative bioactivation of S-alkyl phosphorothiolate pesticides: stereospecificity of profenofos insecticide activation. Science 1983, 219:63-65.
45. Segall Y., Casida J.E. Oxidative conversion of phosphorothiolates to phosphinyloxysulfonates probably via phosphorothiolate S-oxides. Tetrahedron Lett. 1982, 23:139-142.
46. Wing K.D., Glickman A.H., Casida J.E. Phosphorothiolate pesticides and related compounds: oxidative bioactivation and aging of the inhibited acetylcholinesterase. Pesticide Biochem. Physiol. 1984, 21:22-30.
47. Xie W., Stribley J.A., Chatonnet A., Wilder P., Rizzino A., McComb R., Taylor P., Hinrichs S., Lockridge O. Postnatal developmental delay and supersensitivity to organophosphate in gene-targeted mice lacking acetylcholinesterase. J. Pharmacol. Exp. Ther. 2000, 293:896-902.
48. Lockridge O., Duysen E.G., Voelker T., Thompson C.B., Schopfer L.M. Life without acetylcholinesterase: the implications of cholinesterase inhibitor toxicity in AChE-knockout mice. Environ. Toxicol. Pharmacol. 2005, 19:463-469.
49. Duysen E.G., Li B., Darvesh S., Lockridge O. Sensitivity of butyrylcholinesterase knockout mice to (-)-huperzine A and donepezil suggest humans with butyrylcholinesterase deficiency may not tolerate the Alzheimer's disease drugs and indicates butyrylcholinesterase function in neurotransmission. Toxicology 2007, 233:60-69.
50. Meeter E., Wolthuis O.L. The spontaneous recovery of respiration and neuromuscular transmission in the rat after anticholinesterase poisoning. Eur. J. Pharmacol. 1968, 2:377-386.
51. Cisson C.M., Wilson B.W. Paraoxon increases the rate of synthesis of acetylcholinesterase in cultured muscle. Toxicol. Lett. 1981, 9:131-135.
52. Gisiger V., Vigny M. A specific form of acetylcholinesterase is secreted by rat sympathetic ganglia. FEBS Lett. 1977, 84:253-256.
53. Grubic Z., Sketelj J., Klinar B., Brzin M. Recovery of acetylcholinesterase in the diaphragm, brain, and plasma of the rat after irreversible inhibition by soman: a study of cytochemical localization and molecular forms of the enzyme in the motor end plate. J. Neurochem. 1981, 37:909-916.
54. Van Dongen C.J., Valkenburg P.W., Van Helden H.P. Contribution of de novo synthesis of acetylcholinesterase to spontaneous recovery of neuromuscular transmission following soman intoxication. Eur. J. Pharmacol. 1988, 149:381-384.
55. Soreq H., Seidman S. Acetylcholinesterase-new roles for an old actor. Nat. Rev. Neurosci. 2001, 2:294-302.
56. Meshorer E., Soreq H. Virtues and woes of AChE alternative splicing in stress-related neuropathologies. Trends Neurosci. 2006, 29:216-224.
57. Shaked I., Zimmerman G., Soreq H. Stress-induced alternative splicing modulations in brain and periphery: acetylcholinesterase as a case study. Ann. N. Y. Acad. Sci. 2008, 1148:269-281.
58. Pick M., Perry C., Lapidot T., Guimaraes-Sternberg C., Naparstek E., Deutsch V., Soreq H. Stress-induced cholinergic signaling promotes inflammation-associated thrombopoiesis. Blood 2006, 107:3397-3406.
59. Tracey K.J. The inflammatory reflex. Nature 2002, 420:853-859.
60. Namba T., Nolte C.T., Jackrel J., Grob D. Poisoning due to organophosphate insecticides. Acute and chronic manifestations. Am. J. Med. 1971, 50:475-492.
61. Davies J.O., Roberts D., Eyer P., Buckley N., Eddleston M. Hypotension in severe dimethoate self-poisoning. Clin. Toxicol. 2008, 46:880-884.
62. Caulfield M.P. Muscarinic receptors-characterization, coupling and function. Pharmacol. Ther. 1993, 58:319-379.
63. Lamping K.G., Wess J., Cui Y., Nuno D.W., Faraci F.M. Muscarinic (M) receptors in coronary circulation: gene-targeted mice define the role of M2 and M3 receptors in response to acetylcholine. Arterioscler. Thromb. Vasc. Biol. 2004, 24:1253-1258.
64. Tran Q.-K., Watanabe H. Calcium signalling in the endothelium. The Vascular Endothelium I 2006, 145-187. Springer-Verlag, Berlin, Heidelberg. S. Moncada, A. Higgs (Eds.).
65. Wang S.Z., Zhu S.Z., El-Fakahany E.E. Efficient coupling of m5 muscarinic acetylcholine receptors to activation of nitric oxide synthase. J. Pharm. Exp. Ther. 1994, 268:552-557.
66. vanTeeffelen J.W., Segal S.S. Rapid dilation of arterioles with single contraction of hamster skeletal muscle. Am. J. Physiol. Heart Circ. Physiol. 2006, 290:H119-127.
67. Welsh D.G., Segal S.S. Coactivation of resistance vessels and muscle fibers with acetylcholine release from motor nerves. Am. J. Physiol. 1997, 273:H156-H163.
68. Maltz J.S., Eberling J.L., Jagust W.J., Budinger T.F. Enhanced cutaneous vascular response in AD subjects under donepezil therapy. Neurobiol. Aging 2004, 25:475-481.
69. Thompson-Torgerson C.S., Champion H.C., Santhanam L., Harris Z.L., Shoukas A.A. Cyclohexanone contamination from extracorporeal circuits impairs cardiovascular function. Am. J. Physiol. Heart Circ. Physiol. 2009, 296:H1926-H1932.
70. Li B., Schopfer L.M., Grigoryan H., Thompson C.M., Hinrichs S.H., Masson P., Lockridge O. Tyrosines of human and mouse transferrin covalently labeled by organophosphorus agents: a new motif for binding to proteins that have no active site serine. Toxicol. Sci. 2009, 107:144-155.
71. Eddleston M. The pathophysiology of organophosphorus pesticide self-poisoning is not so simple. Neth. J. Med. 2008, 66:146-148.