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Organophosphorus poisoning in animals and enzymatic antidotes

  • Laetitia Poirier
  • Pauline Jacquet
  • Laure Plener
  • Patrick Masson
  • David DaudéEmail author
  • Eric ChabrièreEmail author
Innovations in environmental sciences related to chemical, biological, radiological and nuclear risks
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  • 165 Downloads

Abstract

Organophosphorus compounds (OPs) are neurotoxic molecules developed as pesticides and chemical warfare nerve agents (CWNAs). Most of them are covalent inhibitors of acetylcholinesterase (AChE), a key enzyme in nervous systems, and are therefore responsible for numerous poisonings around the world. Many animal models have been studied over the years in order to decipher the toxicity of OPs and to provide insights for therapeutic and decontamination purposes. Environmental impact on wild animal species has been analyzed to understand the consequences of OP uses in agriculture. In complement, various laboratory models, from invertebrates to aquatic organisms, rodents and primates, have been chosen to study chronic and acute toxicity as well as neurobehavioral impact, immune response, developmental disruption, and other pathological signs. Several decontamination approaches were developed to counteract the poisoning effects of OPs. Among these, enzyme-based strategies are particularly attractive as they allow efficient external decontamination without toxicity or environmental impact and may be of interest for treatment. Approaches using bioscavengers for prophylaxis, treatment, and external decontamination are emphasized and their potential is discussed in the light of toxicological observations from various animal models. The relevance of animal models, regarding their cholinergic system and the abundance of naturally protecting enzymes, is also discussed for better extrapolation of results to human.

Keywords

Organophosphorus Pesticides Chemical warfare nerve agents Animal models Decontamination Enzymatic bio-scavengers 
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Notes

Funding information

L.Po. is a PhD student funded by the Direction Générale de l’Armement (DGA). This work was supported by “Investissements d’avenir” program (Méditerranée Infection 10-IAHU-03) of the French Agence Nationale de la Recherche (ANR).

References

  1. Aboobaker AA (2011) Planarian stem cells: a simple paradigm for regeneration. Trends Cell Biol 21:304–311.  https://doi.org/10.1016/j.tcb.2011.01.005 CrossRefGoogle Scholar
  2. Aharoni A, Gaidukov L, Yagur S, Toker L, Silman I, Tawfik DS (2004) Directed evolution of mammalian paraoxonases PON1 and PON3 for bacterial expression and catalytic specialization. Proc Natl Acad Sci U S A 101:482–487.  https://doi.org/10.1073/pnas.2536901100 CrossRefGoogle Scholar
  3. Albadrany Y, Mohammad F (2007) Effects of acute and repeated oral exposure to the organophosphate insecticide chlorpyrifos on open-field activity in chicks. Toxicol Lett 174:110–116.  https://doi.org/10.1016/j.toxlet.2007.09.001 CrossRefGoogle Scholar
  4. Allon N, Raveh L, Gilat E, Cohen E, Grunwald J, Ashani Y (1998) Prophylaxis against soman inhalation toxicity in Guinea pigs by pretreatment alone with human serum butyrylcholinesterase. Toxicol Sci 43:121–128Google Scholar
  5. Ambrose Z, KewalRamani VN, Bieniasz PD, Hatziioannou T (2007) HIV/AIDS: in search of an animal model. Trends Biotechnol 25:333–337.  https://doi.org/10.1016/j.tibtech.2007.05.004 CrossRefGoogle Scholar
  6. Amine A, Arduini F, Moscone D, Palleschi G (2016) Recent advances in biosensors based on enzyme inhibition. Biosens Bioelectron 76:180–194.  https://doi.org/10.1016/j.bios.2015.07.010 CrossRefGoogle Scholar
  7. Andreescu S, Marty J-L (2006) Twenty years research in cholinesterase biosensors: from basic research to practical applications. Biomol Eng 23:1–15.  https://doi.org/10.1016/j.bioeng.2006.01.001 CrossRefGoogle Scholar
  8. Antonijevic B, Stojiljkovic MP (2007) Unequal efficacy of pyridinium oximes in acute organophosphate poisoning. Clin Med Res 5:71–82.  https://doi.org/10.3121/cmr.2007.701 CrossRefGoogle Scholar
  9. Ashani Y, Rothschild N, Segall Y, Levanon D, Raveh L (1991) Prophylaxis against organophsphate poisoning by an enzyme hydrolysing organophosphorus compounds in mice. Life Sci 49:367–374CrossRefGoogle Scholar
  10. Banerjee I, Tripathi SK, Roy AS (2014) Efficacy of pralidoxime in organophosphorus poisoning: revisiting the controversy in Indian setting. J Postgrad Med 60:27–30.  https://doi.org/10.4103/0022-3859.128803 CrossRefGoogle Scholar
  11. Barata C, Solayan A, Porte C (2004) Role of B-esterases in assessing toxicity of organophosphorus (chlorpyrifos, malathion) and carbamate (carbofuran) pesticides to Daphnia magna. Aquat Toxicol 66:125–139.  https://doi.org/10.1016/j.aquatox.2003.07.004 CrossRefGoogle Scholar
  12. Baze WB (1993) Soman-induced morphological changes: an overview in the non-human primate. J Appl Toxicol 13:173–177CrossRefGoogle Scholar
  13. Bier E (2005) Drosophila, the golden bug, emerges as a tool for human genetics. Nat Rev Genet 6:9–23.  https://doi.org/10.1038/nrg1503 CrossRefGoogle Scholar
  14. Bigley AN, Xu C, Henderson TJ, Harvey SP, Raushel FM (2013) Enzymatic neutralization of the chemical warfare agent VX: evolution of phosphotriesterase for phosphorothiolate hydrolysis. J Am Chem Soc 135:10426–10432.  https://doi.org/10.1021/ja402832z CrossRefGoogle Scholar
  15. Bigley AN, Mabanglo MF, Harvey SP, Raushel FM (2015) Variants of phosphotriesterase for the enhanced detoxification of the chemical warfare agent VR. Biochemistry (Mosc) 54:5502–5512.  https://doi.org/10.1021/acs.biochem.5b00629 CrossRefGoogle Scholar
  16. Bird SB, Sutherland TD, Gresham C, Oakeshott J, Scott C, Eddleston M (2008) OpdA, a bacterial organophosphorus hydrolase, prevents lethality in rats after poisoning with highly toxic organophosphorus pesticides. Toxicology 247:88–92.  https://doi.org/10.1016/j.tox.2008.02.005 CrossRefGoogle Scholar
  17. Bloch-Shilderman E, Rabinovitz I, Egoz I, Yacov G, Allon N, Nili U (2018) Determining a threshold sub-acute dose leading to minimal physiological alterations following prolonged exposure to the nerve agent VX in rats. Arch Toxicol 92:873–892.  https://doi.org/10.1007/s00204-017-2108-5 CrossRefGoogle Scholar
  18. Booth LH, O’Halloran K (2001) A comparison of biomarker responses in the earthworm Aporrectodea caliginosa to the organophosphorus insecticides diazinon and chlorpyrifos. Environ Toxicol Chem 20:2494–2502CrossRefGoogle Scholar
  19. Brandeis R, Raveh L, Grunwald J, Cohen E, Ashani Y (1993) Prevention of soman-induced cognitive deficits by pretreatment with human butyrylcholinesterase in rats. Pharmacol Biochem Behav 46:889–896.  https://doi.org/10.1016/0091-3057(93)90218-I CrossRefGoogle Scholar
  20. Brimfield AA, Lenz DE, Maxwell DM, Broomfield CA (1993) Catalytic antibodies hydrolysing organophosphorus esters. Chem Biol Interact 87:95–102CrossRefGoogle Scholar
  21. Broomfield CA (1992) A purified recombinant organophosphorus acid anhydrase protects mice against soman. Basic Clin Pharmacol Toxicol 70:65–66CrossRefGoogle Scholar
  22. Broomfield C, Maxwell DM, Solana RP, Castro CA, Finger AV, Lenz DE (1991) Protection by butyrylcholinesterase against organophosphorus poisoning in nonhuman primates. J Pharmacol Exp Ther 259:633–638Google Scholar
  23. Calas A-G, Richard O, Même S, Beloeil JC, Doan BT, Gefflaut T, Même W, Crusio WE, Pichon J, Montécot C (2008) Chronic exposure to glufosinate-ammonium induces spatial memory impairments, hippocampal MRI modifications and glutamine synthetase activation in mice. NeuroToxicology 29:740–747.  https://doi.org/10.1016/j.neuro.2008.04.020 CrossRefGoogle Scholar
  24. Chang C-C, Lee P-P, Liu CH, Cheng W (2006) Trichlorfon, an organophosphorus insecticide, depresses the immune responses and resistance to Lactococcus garvieae of the giant freshwater prawn Macrobrachium rosenbergii. Fish Shellfish Immunol 20:574–585.  https://doi.org/10.1016/j.fsi.2005.06.012 CrossRefGoogle Scholar
  25. Cherny I, Greisen P, Ashani Y et al (2013) Engineering V-type nerve agents detoxifying enzymes using computationally focused libraries. ACS Chem Biol 8:2394–2403.  https://doi.org/10.1021/cb4004892 CrossRefGoogle Scholar
  26. Chilcott RP, Dalton CH, Hill I, Davidson CM, Blohm KL, Hamilton MG (2003) Clinical manifestations of VX poisoning following percutaneous exposure in the domestic white pig. Hum Exp Toxicol 22:255–261.  https://doi.org/10.1191/0960327103ht359oa CrossRefGoogle Scholar
  27. Chilcott RP, Dalton CH, Hill I, Davison CM, Blohm KL, Clarkson ED, Hamilton MG (2005) In vivo skin absorption and distribution of the nerve agent VX (O–ethyl–S–[2(diisopropylamino)ethyl] methylphosphonothioate) in the domestic white pig. Hum Exp Toxicol 24:347–352.  https://doi.org/10.1191/0960327105ht537oa CrossRefGoogle Scholar
  28. Chu CR, Szczodry M, Bruno S (2010) Animal models for cartilage regeneration and repair. Tissue Eng B Rev 16:105–115CrossRefGoogle Scholar
  29. Cochran R, Kalisiak J, Küçükkılınç T, Radić Z, Garcia E, Zhang L, Ho KY, Amitai G, Kovarik Z, Fokin VV, Sharpless KB, Taylor P (2011) Oxime-assisted acetylcholinesterase catalytic scavengers of organophosphates that resist aging. J Biol Chem 286:29718–29724.  https://doi.org/10.1074/jbc.M111.264739 CrossRefGoogle Scholar
  30. Cole RD, Anderson GL, Williams PL (2004) The nematode Caenorhabditis elegans as a model of organophosphate-induced mammalian neurotoxicity. Toxicol Appl Pharmacol 194:248–256.  https://doi.org/10.1016/j.taap.2003.09.013 CrossRefGoogle Scholar
  31. Correia FV, Moreira JC (2010) Effects of glyphosate and 2,4-D on earthworms (Eisenia foetida) in laboratory tests. Bull Environ Contam Toxicol 85:264–268.  https://doi.org/10.1007/s00128-010-0089-7 CrossRefGoogle Scholar
  32. Costanzi S, Machado J-H, Mitchell M (2018) Nerve agents: what they are, how they work, how to counter them. ACS Chem Neurosci 9:873–885.  https://doi.org/10.1021/acschemneuro.8b00148 CrossRefGoogle Scholar
  33. Cowan J, Sinton CM, Varley AW, Wians FH, Haley RW, Munford RS (2001) Gene therapy to prevent organophosphate intoxication. Toxicol Appl Pharmacol 173:1–6.  https://doi.org/10.1006/taap.2001.9169 CrossRefGoogle Scholar
  34. De Angelis S, Tassinari R, Maranghi F et al (2009) Developmental exposure to chlorpyrifos induces alterations in thyroid and thyroid hormone levels without other toxicity signs in Cd1 mice. Toxicol Sci 108:311–319.  https://doi.org/10.1093/toxsci/kfp017 CrossRefGoogle Scholar
  35. Deveci HA, Karapehlivan M (2017) Chlorpyrifos-induced parkinsonian model in mice: behavior, histopathology and biochemistry. Pestic Biochem Physiol 144:36–41.  https://doi.org/10.1016/j.pestbp.2017.11.002 CrossRefGoogle Scholar
  36. Dorandeu F, Mikler JR, Thiermann H, Tenn C, Davidson C, Sawyer TW, Lallement G, Worek F (2007) Swine models in the design of more effective medical countermeasures against organophosphorus poisoning. Toxicology 233:128–144.  https://doi.org/10.1016/j.tox.2006.09.013 CrossRefGoogle Scholar
  37. Dorandeu F, Foquin A, Briot R, Delacour C, Denis J, Alonso A, Froment MT, Renault F, Lallement G, Masson P (2008) An unexpected plasma cholinesterase activity rebound after challenge with a high dose of the nerve agent VX. Toxicology 248:151–157.  https://doi.org/10.1016/j.tox.2008.03.013 CrossRefGoogle Scholar
  38. Duncan EJ, Conley JD, Grychowski KD, Conley SA, Lundy PM, Hamilton MG, Sawyer TW (2001) A comparison of the effects of sarin and succinylcholine on respiratory parameters in anesthetized domestic swine. Mil Med 166:322–327CrossRefGoogle Scholar
  39. Duysen EG, Parikh K, Aleti V, Manne V, Lockridge O, Chilukuri N (2011) Adenovirus-mediated human paraoxonase1 gene transfer to provide protection against the toxicity of the organophosphorus pesticide toxicant diazoxon. Gene Ther 18:250–257CrossRefGoogle Scholar
  40. Eddleston M (2018) Are oximes still indicated for acute organophosphorus insecticide self-poisoning? J Med Toxicol Off J Am Coll Med Toxicol 14:1–2.  https://doi.org/10.1007/s13181-018-0651-y CrossRefGoogle Scholar
  41. Eddleston M, Karalliedde L, Buckley N, Fernando R, Hutchinson G, Isbister G, Konradsen F, Murray D, Piola JC, Senanayake N, Sheriff R, Singh S, Siwach SB, Smit L (2002) Pesticide poisoning in the developing world—a minimum pesticides list. Lancet 360:1163–1167.  https://doi.org/10.1016/S0140-6736(02)11204-9 CrossRefGoogle Scholar
  42. Eddleston M, Singh S, Buckley N (2005) Organophosphorus poisoning (acute). Clin Evid 1744–1755Google Scholar
  43. Eddleston M, Buckley NA, Eyer P, Dawson AH (2008) Management of acute organophosphorus pesticide poisoning. Lancet 371:597–607.  https://doi.org/10.1016/S0140-6736(07)61202-1 CrossRefGoogle Scholar
  44. Efremenko EN, Lyagin IV, Klyachko NL, Bronich T, Zavyalova NV, Jiang Y, Kabanov AV (2017) A simple and highly effective catalytic nanozyme scavenger for organophosphorus neurotoxins. J Control Release 247:175–181.  https://doi.org/10.1016/j.jconrel.2016.12.037 CrossRefGoogle Scholar
  45. El-Bouhy ZM, El-Nobi G, Reda RM, Ibrahim RE (2017) Effect of insecticide “chlorpyrifos” on immune response of Oreochromis niloticus. Zagazig Vet J Zag Vet J 44Google Scholar
  46. Elliott JE, Langelier KM, Mineau P, Wilson LK (1996) Poisoning of bald eagles and red-tailed hawks by carbofuran and fensulfothion in the fraser delta of British Columbia, Canada. J Wildl Dis 32:486–491.  https://doi.org/10.7589/0090-3558-32.3.486 CrossRefGoogle Scholar
  47. Elliott JE, Wilson LK, Langelier KM et al (1997) Secondary poisoning of birds of prey by the organophosphorus insecticide, phorate. Ecotoxicology 6:219–231CrossRefGoogle Scholar
  48. Escartín E, Porte C (1997) The use of cholinesterase and carboxylesterase activities from Mytilus galloprovincialis in pollution monitoring. Environ Toxicol Chem 16:2090–2095CrossRefGoogle Scholar
  49. Faria M, Garcia-Reyero N, Padrós F, Babin PJ, Sebastián D, Cachot J, Prats E, Arick M, Rial E, Knoll-Gellida A, Mathieu G, le Bihanic F, Escalon BL, Zorzano A, Soares AMVM, Raldúa D (2015) Zebrafish models for human acute organophosphorus poisoning. Sci Rep 5.  https://doi.org/10.1038/srep15591
  50. Gaidukov L, Bar D, Yacobson S, et al (2009) In vivo administration of BL-3050: highly stable engineered PON1-HDL complexes. BMC Clin Pharmacol 9.  https://doi.org/10.1186/1472-6904-9-18
  51. Galgani F, Bocquené G, Cadiou Y (1992) Evidence of variation in cholinesterase activity in fish along a pollution gradient in the North Sea. Mar Ecol Prog Ser 91:77–82CrossRefGoogle Scholar
  52. Gao Y, Truong YB, Cacioli P, Butler P, Kyratzis IL (2014) Bioremediation of pesticide contaminated water using an organophosphate degrading enzyme immobilized on nonwoven polyester textiles. Enzym Microb Technol 54:38–44.  https://doi.org/10.1016/j.enzmictec.2013.10.001 CrossRefGoogle Scholar
  53. Gause EM, Hartmann RJ, Leal BZ, Geller I (1985) Neurobehavioral effects of repeated sublethal soman in primates. Pharmacol Biochem Behav 23:1003–1012.  https://doi.org/10.1016/0091-3057(85)90107-8 CrossRefGoogle Scholar
  54. Geyer BC, Kannan L, Garnaud P-E, Broomfield CA, Cadieux CL, Cherni I, Hodgins SM, Kasten SA, Kelley K, Kilbourne J, Oliver ZP, Otto TC, Puffenberger I, Reeves TE, Robbins N, Woods RR, Soreq H, Lenz DE, Cerasoli DM, Mor TS (2010) Plant-derived human butyrylcholinesterase, but not an organophosphorous-compound hydrolyzing variant thereof, protects rodents against nerve agents. Proc Natl Acad Sci 107:20251–20256CrossRefGoogle Scholar
  55. Goldsmith M, Ashani Y, Simo Y, Ben-David M, Leader H, Silman I, Sussman JL, Tawfik DS (2012) Evolved stereoselective hydrolases for broad-spectrum G-type nerve agent detoxification. Chem Biol 19:456–466.  https://doi.org/10.1016/j.chembiol.2012.01.017 CrossRefGoogle Scholar
  56. Gomes J, Dawodu AH, Lloyd O, Revitt DM, Anilal SV (1999) Hepatic injury and disturbed amino acid metabolism in mice following prolonged exposure to organophosphorus pesticides. Hum Exp Toxicol 18:33–37.  https://doi.org/10.1177/096032719901800105 CrossRefGoogle Scholar
  57. Gordon RK, Gunduz AT, Askins LY, et al (2003) Decontamination and detoxification of toxic chemical warfare agents using polyurethane sponges. WALTER REED ARMY INST OF RESEARCH SILVER SPRING MDGoogle Scholar
  58. Gresham C, Rosenbaum C, Gaspari RJ, Jackson CJ, Bird SB (2010) Kinetics and efficacy of an organophosphorus hydrolase in a rodent model of methyl-parathion poisoning: KINETICS AND EFFICACY OF AN ORGANOPHOSPHORUS HYDROLASE. Acad Emerg Med 17:736–740.  https://doi.org/10.1111/j.1553-2712.2010.00798.x CrossRefGoogle Scholar
  59. Gunnell D, Eddleston M, Phillips MR, Konradsen F (2007) The global distribution of fatal pesticide self-poisoning: systematic review. BMC Public Health 7:357.  https://doi.org/10.1186/1471-2458-7-357 CrossRefGoogle Scholar
  60. Guyton KZ, Loomis D, Grosse Y, el Ghissassi F, Benbrahim-Tallaa L, Guha N, Scoccianti C, Mattock H, Straif K, International Agency for Research on Cancer Monograph Working Group, IARC, Lyon, France (2015) Carcinogenicity of tetrachlorvinphos, parathion, malathion, diazinon, and glyphosate. Lancet Oncol 16:490–491.  https://doi.org/10.1016/S1470-2045(15)70134-8 CrossRefGoogle Scholar
  61. Hagstrom D, Cochet-Escartin O, Zhang S, Khuu C, Collins EMS (2015) Freshwater planarians as an alternative animal model for neurotoxicology. Toxicol Sci 147:270–285.  https://doi.org/10.1093/toxsci/kfv129 CrossRefGoogle Scholar
  62. Hagstrom D, Cochet-Escartin O, Collins E-MS (2016) Planarian brain regeneration as a model system for developmental neurotoxicology: planarian regeneration as a neurotoxicology model. Regeneration 3:65–77.  https://doi.org/10.1002/reg2.52 CrossRefGoogle Scholar
  63. Hagstrom D, Hirokawa H, Zhang L, Radic Z, Taylor P, Collins EMS (2017) Planarian cholinesterase: in vitro characterization of an evolutionarily ancient enzyme to study organophosphorus pesticide toxicity and reactivation. Arch Toxicol 91:2837–2847.  https://doi.org/10.1007/s00204-016-1908-3 CrossRefGoogle Scholar
  64. Hallberg GR (1989) Pesticides pollution of groundwater in the humid United States. Agric Ecosyst Environ 26:299–367CrossRefGoogle Scholar
  65. Hamilton MG, Hill I, Conley J, Sawyer TW (2004) Clinical aspects of percutaneous poisoning by the chemical warfare agent VX: effects of application site and decontamination. Mil Med 169:856–862CrossRefGoogle Scholar
  66. Havens PL, Rase HF (1993) Reusable immobilized enzyme/polyurethane sponge for removal and detoxification of localized organophosphate pesticide spills. Ind Eng Chem Res 32:2254–2258.  https://doi.org/10.1021/ie00022a009 CrossRefGoogle Scholar
  67. Hela DG, Lambropoulou DA, Konstantinou IK, Albanis TA (2005) Environmental monitoring and ecological risk assessment for pesticide contamination and effects in Lake Pamvotis, northwestern Greece. Environ Toxicol Chem 24:1548–1556CrossRefGoogle Scholar
  68. Hiblot J, Gotthard G, Chabriere E, Elias M (2012) Characterisation of the organophosphate hydrolase catalytic activity of SsoPox. Sci Rep 2.  https://doi.org/10.1038/srep00779
  69. Hosseini SE, Saeidian H, Amozadeh A, Naseri MT, Babri M (2016) Fragmentation pathways and structural characterization of organophosphorus compounds related to the chemical weapons convention by electron ionization and electrospray ionization tandem mass spectrometry. Rapid Commun Mass Spectrom 30:2585–2593.  https://doi.org/10.1002/rcm.7757 CrossRefGoogle Scholar
  70. Husain K, Vijayaraghavan R, Pant SC, Raza SK, Pandey KS (1993) Delayed neurotoxic effect of sarin in mice after repeated inhalation exposure. J Appl Toxicol 13:143–145CrossRefGoogle Scholar
  71. Iyer R, Iken B (2015) Protein engineering of representative hydrolytic enzymes for remediation of organophosphates. Biochem Eng J 94:134–144.  https://doi.org/10.1016/j.bej.2014.11.010 CrossRefGoogle Scholar
  72. Jackson CJ, Carville A, Ward J, Mansfield K, Ollis DL, Khurana T, Bird SB (2014) Use of OpdA, an organophosphorus (OP) hydrolase, prevents lethality in an African green monkey model of acute OP poisoning. Toxicology 317:1–5.  https://doi.org/10.1016/j.tox.2014.01.003 CrossRefGoogle Scholar
  73. Jacquet P, Daudé D, Bzdrenga J, Masson P, Elias M, Chabrière E (2016) Current and emerging strategies for organophosphate decontamination: special focus on hyperstable enzymes. Environ Sci Pollut Res 23:8200–8218.  https://doi.org/10.1007/s11356-016-6143-1 CrossRefGoogle Scholar
  74. Jacquet P, Hiblot J, Daudé D, Bergonzi C, Gotthard G, Armstrong N, Chabrière E, Elias M (2017) Rational engineering of a native hyperthermostable lactonase into a broad spectrum phosphotriesterase. Sci Rep 7:16745.  https://doi.org/10.1038/s41598-017-16841-0 CrossRefGoogle Scholar
  75. Jeibmann A, Paulus W (2009) Drosophila melanogaster as a model organism of brain diseases. Int J Mol Sci 10:407–440.  https://doi.org/10.3390/ijms10020407 CrossRefGoogle Scholar
  76. Jun D, Musilová L, Link M, Loiodice M, Nachon F, Rochu D, Renault F, Masson P (2010) Preparation and characterization of methoxy polyethylene glycol-conjugated phosphotriesterase as a potential catalytic bioscavenger against organophosphate poisoning. Chem Biol Interact 187:380–383.  https://doi.org/10.1016/j.cbi.2010.03.017 CrossRefGoogle Scholar
  77. Kernchen RJ (2011) Enzyme stabilization in nanostructured materials, for use in organophosphorus nerve agent detoxification and prophylaxis. In: Biodefence. Springer, Dordrecht, pp 135–145Google Scholar
  78. King AM, Aaron CK (2015) Organophosphate and carbamate poisoning. Emerg Med Clin North Am 33:133–151.  https://doi.org/10.1016/j.emc.2014.09.010 CrossRefGoogle Scholar
  79. Kolarević S, Kračun-Kolarević M, Kostić J, Slobodnik J, Liška I, Gačić Z, Paunović M, Knežević-Vukčević J, Vuković-Gačić B (2016) Assessment of the genotoxic potential along the Danube River by application of the comet assay on haemocytes of freshwater mussels: The Joint Danube Survey 3. Sci Total Environ 540:377–385.  https://doi.org/10.1016/j.scitotenv.2015.06.061 CrossRefGoogle Scholar
  80. Kondakala S, Lee JH, Ross MK, Howell GE (2017) Effects of acute exposure to chlorpyrifos on cholinergic and non-cholinergic targets in normal and high-fat fed male C57BL/6J mice. Toxicol Appl Pharmacol 337:67–75.  https://doi.org/10.1016/j.taap.2017.10.019 CrossRefGoogle Scholar
  81. Lainee P, Robineau P, Guittin P, Coq H, Benchetrit G (1991) Mechanisms of pulmonary edema induced by an organophosphorus compound in anesthetized dogs. Fundam Appl Toxicol 17:177–185CrossRefGoogle Scholar
  82. LeJeune KE, Russell AJ (1996) Covalent binding of a nerve agent hydrolyzing enzyme within polyurethane foams. Biotechnol Bioeng 51:450–457.  https://doi.org/10.1002/(SICI)1097-0290(19960820)51:4<450::AID-BIT8>3.0.CO;2-H CrossRefGoogle Scholar
  83. LeJeune KE, Russell AJ (1999) Biocatalytic nerve agent detoxification in fire fighting foams. Biotechnol Bioeng 62:659–665.  https://doi.org/10.1002/(SICI)1097-0290(19990320)62:6<659::AID-BIT5>3.0.CO;2-N CrossRefGoogle Scholar
  84. LeJeune KE, Mesiano AJ, Bower SB et al (1997) Dramatically stabilized phosphotriesterase—polymers for nerve agent degradation. Biotechnol Bioeng 54:105–114.  https://doi.org/10.1002/(SICI)1097-0290(19970420)54:2<105::AID-BIT2>3.0.CO;2-P CrossRefGoogle Scholar
  85. LeJeune KE, Wild JR, Russell AJ (1998) Nerve agents degraded by enzymatic foams. Nature 395:27–28.  https://doi.org/10.1038/25634 CrossRefGoogle Scholar
  86. Lenz DE, Brimfield AA, Hunter KW et al (1984) Studies using a monoclonal antibody against soman. Toxicol Sci 4:156–164.  https://doi.org/10.1093/toxsci/4.2part2.156 CrossRefGoogle Scholar
  87. Lenz DE, Maxwell DM, Koplovitz I, Clark CR, Capacio BR, Cerasoli DM, Federko JM, Luo C, Saxena A, Doctor BP, Olson C (2005) Protection against soman or VX poisoning by human butyrylcholinesterase in Guinea pigs and cynomolgus monkeys. Chem Biol Interact 157–158:205–210.  https://doi.org/10.1016/j.cbi.2005.10.025 CrossRefGoogle Scholar
  88. Lenz DE, Yeung D, Smith JR, Sweeney RE, Lumley LA, Cerasoli DM (2007) Stoichiometric and catalytic scavengers as protection against nerve agent toxicity: a mini review. Toxicology 233:31–39CrossRefGoogle Scholar
  89. Lenz DE, Clarkson ED, Schulz SM, Cerasoli DM (2010) Butyrylcholinesterase as a therapeutic drug for protection against percutaneous VX. Chem Biol Interact 187:249–252.  https://doi.org/10.1016/j.cbi.2010.05.014 CrossRefGoogle Scholar
  90. Letort S, Balieu S, Erb W, Gouhier G, Estour F (2016) Interactions of cyclodextrins and their derivatives with toxic organophosphorus compounds. Beilstein J Org Chem 12:204–228.  https://doi.org/10.3762/bjoc.12.23 CrossRefGoogle Scholar
  91. Li WF, Furlong CE, Costa LG (1995) Paraoxonase protects against chlorpyrifos toxicity in mice. Toxicol Lett 76:219–226CrossRefGoogle Scholar
  92. Liu H-X, Liu C-F, Yang W-H (2015) Clinical study of continuous micropump infusion of atropine and pralidoxime chloride for treatment of severe acute organophosphorus insecticide poisoning. J Chin Med Assoc 78:709–713.  https://doi.org/10.1016/j.jcma.2015.08.006 CrossRefGoogle Scholar
  93. Lotti M (2010) Chapter 72—clinical toxicology of anticholinesterase agents in humans. In: Krieger R (ed) Hayes’ handbook of pesticide toxicology, 3rd edn. Academic Press, New York, pp 1543–1589CrossRefGoogle Scholar
  94. Luo X-J, Zhao J, Li C-X, Bai YP, Reetz MT, Yu HL, Xu JH (2016) Combinatorial evolution of phosphotriesterase toward a robust malathion degrader by hierarchical iteration mutagenesis. Biotechnol Bioeng 113:2350–2357.  https://doi.org/10.1002/bit.26012 CrossRefGoogle Scholar
  95. Lushchekina SV, Schopfer LM, Grigorenko BL, Nemukhin AV, Varfolomeev SD, Lockridge O, Masson P (2018) Optimization of cholinesterase-based catalytic bioscavengers against organophosphorus agents. Front Pharmacol 9.  https://doi.org/10.3389/fphar.2018.00211
  96. Masson P, Lushchekina SV (2016) Emergence of catalytic bioscavengers against organophosphorus agents. Chem Biol Interact 259:319–326.  https://doi.org/10.1016/j.cbi.2016.02.010 CrossRefGoogle Scholar
  97. Masson P, Nachon F (2017) Cholinesterase reactivators and bioscavengers for pre- and post-exposure treatments of organophosphorus poisoning. J Neurochem 142:26–40.  https://doi.org/10.1111/jnc.14026 CrossRefGoogle Scholar
  98. Masson P, Rochu D (2009) Catalytic bioscavengers against toxic esters, an alternative approach for prophylaxis and treatments of poisonings. Acta Nat 1:68–79Google Scholar
  99. Masson P, Josse D, Lockridge O, Viguié N, Taupin C, Buhler C (1998) Enzymes hydrolyzing organophosphates as potential catalytic scavengers against organophosphate poisoning. J Physiol-Paris 92:357–362.  https://doi.org/10.1016/S0928-4257(99)80005-9 CrossRefGoogle Scholar
  100. Masuda N, Takatsu M, Morinari H, Ozawa T, Nozaki H, Aikawa N (1995) Sarin poisoning in Tokyo subway. Lancet 345:1446–1447.  https://doi.org/10.1016/S0140-6736(95)92637-2 CrossRefGoogle Scholar
  101. Maxwell DM, Castro CA, Denise M et al (1992) Protection of rhesus monkeys against soman and prevention of performance decrement by pretreatment with acetylcholinesterase. Toxicol Appl Pharmacol 115:44–49CrossRefGoogle Scholar
  102. Maxwell DM, Brecht K, Saxena A, et al (1998) Comparison of cholinesterases and carboxylesterase as bioscavengers for organophosphorus compounds. In: Structure and function of cholinesterases and related proteins. Springer, Boston, MA, pp 387–392Google Scholar
  103. McKelvey W, Jacobson JB, Kass D, Barr DB, Davis M, Calafat AM, Aldous KM (2013) Population-based biomonitoring of exposure to organophosphate and pyrethroid pesticides in New York City. Environ Health Perspect 121:1349–1356.  https://doi.org/10.1289/ehp.1206015 CrossRefGoogle Scholar
  104. Mehrani H (2004) Protective effect of polyurethane immobilized human butyrylcholinesterase against parathion inhalation in rat. Environ Toxicol Pharmacol 16:179–185.  https://doi.org/10.1016/j.etap.2004.01.001 CrossRefGoogle Scholar
  105. Mew EJ, Padmanathan P, Konradsen F, Eddleston M, Chang SS, Phillips MR, Gunnell D (2017) The global burden of fatal self-poisoning with pesticides 2006-15: systematic review. J Affect Disord 219:93–104.  https://doi.org/10.1016/j.jad.2017.05.002 CrossRefGoogle Scholar
  106. Mişe Yonar S, Ural MŞ, Silici S, Yonar ME (2014) Malathion-induced changes in the haematological profile, the immune response, and the oxidative/antioxidant status of Cyprinus carpio carpio: protective role of propolis. Ecotoxicol Environ Saf 102:202–209.  https://doi.org/10.1016/j.ecoenv.2014.01.007 CrossRefGoogle Scholar
  107. Moorthy KS, Reddy BK, Swami KS, Chetty CS (1984) Changes in respiration and ionic content in tissues of freshwater mussel exposed to methyl parathion toxicity. Toxicol Lett 21:287–291CrossRefGoogle Scholar
  108. Mostafalou S, Abdollahi M (2017) Pesticides: an update of human exposure and toxicity. Arch Toxicol 91:549–599.  https://doi.org/10.1007/s00204-016-1849-x CrossRefGoogle Scholar
  109. Mullin CA, Frazier M, Frazier JL, Ashcraft S, Simonds R, vanEngelsdorp D, Pettis JS (2010) High levels of miticides and agrochemicals in north American apiaries: implications for honey bee health. PLoS One 5:e9754.  https://doi.org/10.1371/journal.pone.0009754 CrossRefGoogle Scholar
  110. Mumford H, Troyer JK (2011) Post-exposure therapy with recombinant human BuChE following percutaneous VX challenge in Guinea-pigs. Toxicol Lett 206:29–34.  https://doi.org/10.1016/j.toxlet.2011.05.1016 CrossRefGoogle Scholar
  111. Mumford H, Price EM, Lenz DE, Cerasoli DM (2011) Post-exposure therapy with human butyrylcholinesterase following percutaneous VX challenge in Guinea pigs. Clin Toxicol 49:287–297.  https://doi.org/10.3109/15563650.2011.568944 CrossRefGoogle Scholar
  112. Mumford H, Docx CJ, Price ME, Green AC, Tattersall JEH, Armstrong SJ (2013) Human plasma-derived BuChE as a stoichiometric bioscavenger for treatment of nerve agent poisoning. Chem Biol Interact 203:160–166.  https://doi.org/10.1016/j.cbi.2012.08.018 CrossRefGoogle Scholar
  113. Muñoz-Quezada MT, Lucero BA, Iglesias VP, Muñoz MP, Cornejo CA, Achu E, Baumert B, Hanchey A, Concha C, Brito AM, Villalobos M (2016) Chronic exposure to organophosphate (OP) pesticides and neuropsychological functioning in farm workers: a review. Int J Occup Environ Health 22:68–79.  https://doi.org/10.1080/10773525.2015.1123848 CrossRefGoogle Scholar
  114. Newcomb RD, Campbell PM, Ollis DL, Cheah E, Russell RJ, Oakeshott JG (1997) A single amino acid substitution converts a carboxylesterase to an organophosphorus hydrolase and confers insecticide resistance on a blowfly. Proc Natl Acad Sci 94:7464–7468CrossRefGoogle Scholar
  115. Newmark PA, Alvarado AS (2002) Not your father’s planarian: a classic model enters the era of functional genomics. Nat Rev Genet 3:210–219.  https://doi.org/10.1038/nrg759 CrossRefGoogle Scholar
  116. Omburo GA, Kuo JM, Mullins LS, Raushel FM (1992) Characterization of the zinc binding site of bacterial phosphotriesterase. J Biol Chem 267:13278–13283Google Scholar
  117. Organisation for the Prohibition of Chemical Weapons (2005) Convention on the Prohibition of the Development, Production, Stockpiling and Use of Chemical Weapons and on Their Destruction, 3rd ed., the Technical Secretariat of the Organisation for the Prohibition of Chemical Weapons, Hague. Conv Prohib Dev Prod Stock Use Chem Weapons Their Destr 3rd ed:Google Scholar
  118. Padilla-Carlin DJ, McMurray DN, Hickey AJ (2008) The Guinea pig as a model of infectious diseases. Comp Med 58:324–340Google Scholar
  119. Patel V, Ramasundarahettige C, Vijayakumar L, Thakur JS, Gajalakshmi V, Gururaj G, Suraweera W, Jha P, Million Death Study Collaborators (2012) Suicide mortality in India: a nationally representative survey. Lancet 379:2343–2351.  https://doi.org/10.1016/S0140-6736(12)60606-0 CrossRefGoogle Scholar
  120. Patocka J (2016) Syria conflict and chemical weapons: what is the reality? Mil Med Sci Lett 85:39–43CrossRefGoogle Scholar
  121. Patočka J (2017) What killed Kim Jong-Nam? Was it the agent VX? Vojen Zdr Listy Mil Med Sci Lett Věd Orgán Českoslov Vojen Lékařů Zvěrolékařů Lékárníků Vydávaný Vojen Zdr Porad Sborem Za Podpory Minist Národní Obrany 86:86–89Google Scholar
  122. Pereira EFR, Aracava Y, DeTolla LJ et al (2014) Animal models that best reproduce the clinical manifestations of human intoxication with organophosphorus compounds. J Pharmacol Exp Ther 350:313–321.  https://doi.org/10.1124/jpet.114.214932 CrossRefGoogle Scholar
  123. Petrikovics I, Cheng T-C, Papahadjopoulos D, Hong K, Yin R, DeFrank J, Jaing J, Song ZH, McGuinn W, Sylvester D, Pei L, Madec J, Tamulinas C, Jaszberenyi JC, Barcza T, Way JL (2000a) Long circulating liposomes encapsulating organophosphorus acid anhydrolase in diisopropylfluorophosphate antagonism. Toxicol Sci 57:16–21.  https://doi.org/10.1093/toxsci/57.1.16 CrossRefGoogle Scholar
  124. Petrikovics I, McGuinn JJDWD, Sylvester D, Yuzapavik P, Jiang J, Way JL, Papahadjopoulos D, Hong K, Yin R, Cheng TC (2000b) In vitro studies on sterically stabilized liposomes (SL) as enzyme carriers in organophosphorus (OP) antagonism. Drug Deliv 7:83–89.  https://doi.org/10.1080/107175400266641 CrossRefGoogle Scholar
  125. Petrikovics I, Wales ME, Jaszberenyi JC, Budai M, Baskin SI, Szilasi M, Logue BA, Chapela P, Wild JR (2007) Enzyme-based intravascular defense against organophosphorus neurotoxins: synergism of dendritic-enzyme complexes with 2-PAM and atropine. Nanotoxicology 1:85–92.  https://doi.org/10.1080/17435390500128271 CrossRefGoogle Scholar
  126. Phillips KF, Deshpande LS (2016) Repeated low-dose organophosphate DFP exposure leads to the development of depression and cognitive impairment in a rat model of Gulf War Illness. NeuroToxicology 52:127–133.  https://doi.org/10.1016/j.neuro.2015.11.014 CrossRefGoogle Scholar
  127. Phillips JP, Xin JH, Kirby K, Milne CP, Krell P, Wild JR (1990) Transfer and expression of an organophosphate insecticide-degrading gene from Pseudomonas in Drosophila melanogaster. Proc Natl Acad Sci 87:8155–8159CrossRefGoogle Scholar
  128. Poirier L, Brun L, Jacquet P, Lepolard C, Armstrong N, Torre C, Daudé D, Ghigo E, Chabrière E (2017) Enzymatic degradation of organophosphorus insecticides decreases toxicity in planarians and enhances survival. Sci Rep 7:15194.  https://doi.org/10.1038/s41598-017-15209-8 CrossRefGoogle Scholar
  129. Pope CN, Brimijoin S (2018) Cholinesterases and the fine line between poison and remedy. Biochem Pharmacol 153:205–216.  https://doi.org/10.1016/j.bcp.2018.01.044 CrossRefGoogle Scholar
  130. Prendergast MA, Terry AV, Buccafusco JJ (1998) Effects of chronic, low-level organophosphate exposure on delayed recall, discrimination, and spatial learning in monkeys and rats. Neurotoxicol Teratol 20:115–122CrossRefGoogle Scholar
  131. Pundir CS, Chauhan N (2012) Acetylcholinesterase inhibition-based biosensors for pesticide determination: a review. Anal Biochem 429:19–31.  https://doi.org/10.1016/j.ab.2012.06.025 CrossRefGoogle Scholar
  132. Rao JV, Kavitha P (2004) Toxicity of azodrin on the morphology and acetylcholinesterase activity of the earthworm Eisenia foetida. Environ Res 96:323–327.  https://doi.org/10.1016/j.envres.2004.02.014 CrossRefGoogle Scholar
  133. Raveh L, Ashani Y, Levy D, de la Hoz D, Wolfe AD, Doctor BP (1989) Acetylcholinesterase prophylaxis against organophosphate poisoning: quantitative correlation between protection and blood-enzyme level in mice. Biochem Pharmacol 38:529–534CrossRefGoogle Scholar
  134. Raveh L, Grunwald J, Marcus D, Papier Y, Cohen E, Ashani Y (1993) Human butyrylcholinesterase as a general prophylactic antidote for nerve agent toxicity: in vitro and in vivo quantitative characterization. Biochem Pharmacol 45:2465–2474CrossRefGoogle Scholar
  135. Raveh L, Grauer E, Grunwald J, Cohen E, Ashani Y (1997) The stoichiometry of protection against soman and VX toxicity in monkeys pretreated with human butyrylcholinesterase. Toxicol Appl Pharmacol 145:43–53.  https://doi.org/10.1006/taap.1997.8160 CrossRefGoogle Scholar
  136. Reed BA, Sabourin CL, Lenz DE (2017) Human butyrylcholinesterase efficacy against nerve agent exposure: Reed, Sabourin and Lenz. J Biochem Mol Toxicol 31:e21886.  https://doi.org/10.1002/jbt.21886 CrossRefGoogle Scholar
  137. Renick VC, Weinersmith K, Vidal-Dorsch DE, Anderson TW (2016) Effects of a pesticide and a parasite on neurological, endocrine, and behavioral responses of an estuarine fish. Aquat Toxicol 170:335–343.  https://doi.org/10.1016/j.aquatox.2015.09.010 CrossRefGoogle Scholar
  138. Ricceri L, Venerosi A, Capone F, Cometa MF, Lorenzini P, Fortuna S, Calamandrei G (2006) Developmental neurotoxicity of organophosphorous pesticides: fetal and neonatal exposure to chlorpyrifos alters sex-specific behaviors at adulthood in mice. Toxicol Sci 93:105–113.  https://doi.org/10.1093/toxsci/kfl032 CrossRefGoogle Scholar
  139. Roberts DM, Aaron CK (2007) Management of acute organophosphorus pesticide poisoning. BMJ 334:629–634.  https://doi.org/10.1136/bmj.39134.566979.BE CrossRefGoogle Scholar
  140. Robineau P, Guittin P (1987) Effects of an organophosphorous compound on cardiac rhythm and haemodynamics in anaesthetized and conscious beagle dogs. Toxicol Lett 37:95–102CrossRefGoogle Scholar
  141. Rochu D, Chabrière E, Masson P (2007) Human paraoxonase: a promising approach for pre-treatment and therapy of organophosphorus poisoning. Toxicology 233:47–59.  https://doi.org/10.1016/j.tox.2006.08.037 CrossRefGoogle Scholar
  142. Rodríguez HH, Espinoza-Navarro O, Silva I, Needham D, Castro ME, Sarabia L, Inostroza J, Jimenez L (2011) The effect of paraoxon on spermatogenesis in Dugesia gonocephala from the Chilean Altiplano: proliferation and apoptosis. Environ Sci Pollut Res 18:497–502.  https://doi.org/10.1007/s11356-010-0385-0 CrossRefGoogle Scholar
  143. Roex EWM, Keijzers R, van Gestel CAM (2003) Acetylcholinesterase inhibition and increased food consumption rate in the zebrafish, Danio rerio, after chronic exposure to parathion. Aquat Toxicol 64:451–460.  https://doi.org/10.1016/S0166-445X(03)00100-0 CrossRefGoogle Scholar
  144. Rosenberg YJ, Wang J, Ooms T, Rajendran N, Mao L, Jiang X, Lees J, Urban L, Momper JD, Sepulveda Y, Shyong YJ, Taylor P (2017) Post-exposure treatment with the oxime RS194B rapidly reactivates and reverses advanced symptoms of lethal inhaled paraoxon in macaques. Toxicol Lett 293:229–234.  https://doi.org/10.1016/j.toxlet.2017.10.025 CrossRefGoogle Scholar
  145. Rosenstock L, Keifer M, Daniell WE et al (1991) Chronic central nervous system effects of acute organophosphate pesticide intoxication. Lancet 338:223–227.  https://doi.org/10.1016/0140-6736(91)90356-T CrossRefGoogle Scholar
  146. Roth GS, Mattison JA, Ottinger MA, Chachich ME, Lane MA, Ingram DK (2004) Aging in rhesus monkeys: relevance to human health interventions. Science 305:1423–1426.  https://doi.org/10.1126/science.1102541 CrossRefGoogle Scholar
  147. Rowland SS, Speedie MK, Pogell BM (1991) Purification and characterization of a secreted recombinant phosphotriesterase (parathion hydrolase) from Streptomyces lividans. Appl Environ Microbiol 57:440–444Google Scholar
  148. Saffih-Hdadi K, Bruckler L, Amichot M, Belzunces L (2005) Modeling impact of parathion and its metabolite paraoxon on the nematode Caenorhabditis etegans in soil. Environ Toxicol Chem 24:1387–1394CrossRefGoogle Scholar
  149. Sakamoto T, Sawada Y, Nishide K, Sadamitsu D, Yoshioka T, Sugimoto T, Nishii S, Kishi H (1984) Delayed neurotoxicity produced by an organophosphorous compound (Sumithion). Arch Toxicol 56:136–138.  https://doi.org/10.1007/BF00349087 CrossRefGoogle Scholar
  150. Salem MH, Abo-Elezz Z, Abd-Allah GA, Hassan GA, Shaker N (1988) Effect of organophosphorus (dimethoate) and pyrethroid (deltamethrin) pesticides on semen characteristics in rabbits. J Environ Sci Health Part B 23:279–290.  https://doi.org/10.1080/03601238809372604 CrossRefGoogle Scholar
  151. Sánchez Alvarado A (2006) Planarian regeneration: its end is its beginning. Cell 124:241–245.  https://doi.org/10.1016/j.cell.2006.01.012 CrossRefGoogle Scholar
  152. Saxena A, Sun W, Dabisch PA, Hulet SW, Hastings NB, Jakubowski EM, Mioduszewski RJ, Doctor BP (2008) Efficacy of human serum butyrylcholinesterase against sarin vapor. Chem Biol Interact 175:267–272.  https://doi.org/10.1016/j.cbi.2008.05.022 CrossRefGoogle Scholar
  153. Saxena A, Sun W, Fedorko JM, Koplovitz I, Doctor BP (2011) Prophylaxis with human serum butyrylcholinesterase protects Guinea pigs exposed to multiple lethal doses of soman or VX. Biochem Pharmacol 81:164–169.  https://doi.org/10.1016/j.bcp.2010.09.007 CrossRefGoogle Scholar
  154. Scheffel C, Niessen KV, Rappenglück S, Wanner KT, Thiermann H, Worek F, Seeger T (2017) Counteracting desensitization of human α7-nicotinic acetylcholine receptors with bispyridinium compounds as an approach against organophosphorus poisoning. Toxicol Lett 293:149–156.  https://doi.org/10.1016/j.toxlet.2017.12.005 CrossRefGoogle Scholar
  155. Soares F, de Castro A, Pereira A, Leal D, Mancini D, Krejcar O, Ramalho T, da Cunha E, Kuca K (2018) Theoretical studies applied to the evaluation of the DFPase bioremediation potential against chemical warfare agents intoxication. Int J Mol Sci 19:1257.  https://doi.org/10.3390/ijms19041257 CrossRefGoogle Scholar
  156. Sogorb MA, Vilanova E, Carrera V (2004) Future applications of phosphotriesterases in the prophylaxis and treatment of organophosporus insecticide and nerve agent poisonings. Toxicol Lett 151:219–233.  https://doi.org/10.1016/j.toxlet.2004.01.022 CrossRefGoogle Scholar
  157. Stevens RC, Suzuki SM, Cole TB, Park SS, Richter RJ, Furlong CE (2008) Engineered recombinant human paraoxonase 1 (rHuPON1) purified from Escherichia coli protects against organophosphate poisoning. Proc Natl Acad Sci 105:12780–12784CrossRefGoogle Scholar
  158. Szinicz L (2005) History of chemical and biological warfare agents. Toxicology 214:167–181.  https://doi.org/10.1016/j.tox.2005.06.011 CrossRefGoogle Scholar
  159. Theriot CM, Du X, Tove SR, Grunden AM (2010) Improving the catalytic activity of hyperthermophilic Pyrococcus prolidases for detoxification of organophosphorus nerve agents over a broad range of temperatures. Appl Microbiol Biotechnol 87:1715–1726.  https://doi.org/10.1007/s00253-010-2614-3 CrossRefGoogle Scholar
  160. Toualy SO, Jean-Michel P, Marina K, Tia JG (2017) Effect of pesticides and micro-organisms on earthworm Eisenia fetida (Savigny, 1826). Afr J Agric Res 12:706–715.  https://doi.org/10.5897/AJAR2016.11844 CrossRefGoogle Scholar
  161. Tsai P-C, Fox N, Bigley AN, Harvey SP, Barondeau DP, Raushel FM (2012) Enzymes for the homeland defense: optimizing phosphotriesterase for the hydrolysis of organophosphate nerve agents. Biochemistry (Mosc) 51:6463–6475.  https://doi.org/10.1021/bi300811t CrossRefGoogle Scholar
  162. Tuovinen K, Kaliste-Korhonen E, Raushel FM, Hänninen O (1994) Phosphotriesterase—a promising candidate for use in detoxification of organophosphates. Fundam Appl Toxicol 23:578–584.  https://doi.org/10.1006/faat.1994.1143 CrossRefGoogle Scholar
  163. Valiyaveettil M, Alamneh Y, Rezk P, Perkins MW, Sciuto AM, Doctor BP, Nambiar MP (2011) Recombinant paraoxonase 1 protects against sarin and soman toxicity following microinstillation inhalation exposure in Guinea pigs. Toxicol Lett 202:203–208.  https://doi.org/10.1016/j.toxlet.2011.02.007 CrossRefGoogle Scholar
  164. Vecchio PD, Elias M, Merone L et al (2009) Structural determinants of the high thermal stability of SsoPox from the hyperthermophilic archaeon Sulfolobus solfataricus. Extremophiles 13:461–470.  https://doi.org/10.1007/s00792-009-0231-9 CrossRefGoogle Scholar
  165. Verma SR, Rani S, Bansal SK, Dalela RC (1981) Evaluation of the comparative toxicity of Thiotox, Dichlorvos and Carbofuran to two fresh water teleosts Ophiocephalus punctatus and Mystus vittatus. CLEAN–Soil Air Water 9:119–129Google Scholar
  166. Vidal M, Cagan RL (2006) Drosophila models for cancer research. Curr Opin Genet Dev 16:10–16.  https://doi.org/10.1016/j.gde.2005.12.004 CrossRefGoogle Scholar
  167. Villar D, Gonzalez M, Gualda MJ, Schaeffer DJ (1994) Effects of organophosphorus insecticides on Dugesia tigrina: cholinesterase activity and head regeneration. Bull Environ Contam Toxicol 52:319–324CrossRefGoogle Scholar
  168. VodičKa P, Smetana K, DvořáNková B et al (2005) The miniature pig as an animal model in biomedical research. Ann N Y Acad Sci 1049:161–171.  https://doi.org/10.1196/annals.1334.015 CrossRefGoogle Scholar
  169. Wallace TJ, Ghosh S, McLean Grogan W (1999) Molecular cloning and expression of rat lung carboxylesterase and its potential role in the detoxification of organophosphorus compounds. Am J Respir Cell Mol Biol 20:1201–1208CrossRefGoogle Scholar
  170. Wang Y (2004) Resistance to organophosphorus agent toxicity in transgenic mice expressing the G117H mutant of human butyrylcholinesterase. Toxicol Appl Pharmacol 196:356–366.  https://doi.org/10.1016/j.taap.2003.12.018 CrossRefGoogle Scholar
  171. Wang S, Liu Y, Fang D, Shi S (2007) The miniature pig: a useful large animal model for dental and orofacial research. Oral Dis 13:530–537.  https://doi.org/10.1111/j.1601-0825.2006.01337.x CrossRefGoogle Scholar
  172. Watkins LM, Mahoney HJ, McCulloch JK, Raushel FM (1997) Augmented hydrolysis of diisopropyl fluorophosphate in engineered mutants of phosphotriesterase. J Biol Chem 272:25596–25601.  https://doi.org/10.1074/jbc.272.41.25596 CrossRefGoogle Scholar
  173. White DH, Hayes LE, Bush PB (1989) Case histories of wild birds killed intentionally with famphur in Georgia and West Virginia. J Wildl Dis 25:184–188.  https://doi.org/10.7589/0090-3558-25.2.184 CrossRefGoogle Scholar
  174. Wilson L, Harris M, Elliott J (1998) Impact of agricultural pesticides on birds of prey in the lower Fraser valley. Health Fraser River Aquat Ecosyst 1Google Scholar
  175. Winrow CJ, Hemming ML, Allen DM, Quistad GB, Casida JE, Barlow C (2003) Loss of neuropathy target esterase in mice links organophosphate exposure to hyperactivity. Nat Genet 33:477–485.  https://doi.org/10.1038/ng1131 CrossRefGoogle Scholar
  176. Wolfe AD, Blick DW, Murphy MR, Miller SA, Gentry MK, Hartgraves SL, Doctor BP (1992) Use of cholinesterases as pretreatment drugs for the protection of rhesus monkeys against soman toxicity. Toxicol Appl Pharmacol 117:189–193.  https://doi.org/10.1016/0041-008X(92)90236-L CrossRefGoogle Scholar
  177. Worek F, Seeger T, Goldsmith M, Ashani Y, Leader H, Sussman JS, Tawfik D, Thiermann H, Wille T (2014a) Efficacy of the rePON1 mutant IIG1 to prevent cyclosarin toxicity in vivo and to detoxify structurally different nerve agents in vitro. Arch Toxicol 88:1257–1266.  https://doi.org/10.1007/s00204-014-1204-z CrossRefGoogle Scholar
  178. Worek F, Seeger T, Reiter G, Goldsmith M, Ashani Y, Leader H, Sussman JL, Aggarwal N, Thiermann H, Tawfik DS (2014b) Post-exposure treatment of VX poisoned Guinea pigs with the engineered phosphotriesterase mutant C23: a proof-of-concept study. Toxicol Lett 231:45–54.  https://doi.org/10.1016/j.toxlet.2014.09.003 CrossRefGoogle Scholar
  179. Worek F, Seeger T, Zengerle M, Kubik S, Thiermann H, Wille T (2014c) Effectiveness of a substituted β-cyclodextrin to prevent cyclosarin toxicity in vivo. Toxicol Lett 226:222–227.  https://doi.org/10.1016/j.toxlet.2014.02.010 CrossRefGoogle Scholar
  180. Yair S, Ofer B, Arik E, Shai S, Yossi R, Tzvika D, Amir K (2008) Organophosphate degrading microorganisms and enzymes as biocatalysts in environmental and personal decontamination applications. Crit Rev Biotechnol 28:265–275.  https://doi.org/10.1080/07388550802455742 CrossRefGoogle Scholar
  181. Yanagisawa N, Morita H, Nakajima T (2006) Sarin experiences in Japan: acute toxicity and long-term effects. J Neurol Sci 249:76–85.  https://doi.org/10.1016/j.jns.2006.06.007 CrossRefGoogle Scholar
  182. Yang C-Y, Renfrew PD, Olsen AJ, Zhang M, Yuvienco C, Bonneau R, Montclare JK (2014) Improved stability and half-life of fluorinated phosphotriesterase using Rosetta. ChemBioChem 15:1761–1764.  https://doi.org/10.1002/cbic.201402062 CrossRefGoogle Scholar
  183. Yousef MI, Salem MH, Ibrahim HZ, Helmi S, Seehy MA, Bertheussen K (1995) Toxic effects of carbofuran and glyphosate on semen characteristics in rabbits. J Environ Sci Health Part B 30:513–534.  https://doi.org/10.1080/03601239509372951 CrossRefGoogle Scholar
  184. Zhang Z-Y, Yu X-Y, Wang D-L, Yan HJ, Liu XJ (2010) Acute toxicity to zebrafish of two organophosphates and four pyrethroids and their binary mixtures. Pest Manag Sci 66:84–89.  https://doi.org/10.1002/ps.1834 CrossRefGoogle Scholar
  185. Zhang Z, Troldborg M, Yates K, Osprey M, Kerr C, Hallett PD, Baggaley N, Rhind SM, Dawson JJC, Hough RL (2016) Evaluation of spot and passive sampling for monitoring, flux estimation and risk assessment of pesticides within the constraints of a typical regulatory monitoring scheme. Sci Total Environ 569–570:1369–1379.  https://doi.org/10.1016/j.scitotenv.2016.06.219 CrossRefGoogle Scholar
  186. Zhang H-C, Liu T-Y, Shi C-Y, Chen GW, Liu DZ (2017) Genotoxicity evaluation of an Urban River on freshwater planarian by RAPD assay. Bull Environ Contam Toxicol 98:484–488.  https://doi.org/10.1007/s00128-016-2027-9 CrossRefGoogle Scholar

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Authors and Affiliations

  1. 1.IRD, APHM, MEPHI, IHU-Méditerranée InfectionAix Marseille UniversityMarseilleFrance
  2. 2.Gene&GreenTKMarseilleFrance
  3. 3.Neuropharmacology LaboratoryKazan Federal UniversityKazanRussia

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