Development of an adverse outcome pathway for acetylcholinesterase inhibition leading to acute mortality

Environmental Toxicology and Chemistry

Volumn 33, Issue 10, 2014, Pages 2157-2169

  Russom, Christine L ^a   Lalone, Carlie A ^b   Villeneuve, Daniel L ^a   Ankley, Gerald T ^a  

^a U S ENVIRONMENTAL PROTECTION AGENCY   (United States)

^b UNIVERSITY OF MINNESOTA   (United States)

Author keywords

Acetylcholinesterase inhibition; Adverse outcome pathway; Ecotoxicology; Species sensitivity

Indexed keywords

BIOHAZARDS; CHEMICALS;

ACETYLCHOLINESTERASE INHIBITION; ADVERSE OUTCOMES; BIOLOGICAL PATHWAYS; CARBAMATE INSECTICIDES; CHEMICAL PERTURBATIONS; ECO-TOXICOLOGY; ORGANISATION FOR ECONOMIC CO-OPERATION AND DEVELOPMENT; SPECIES SENSITIVITY;

CHEMICAL HAZARDS;

ACETYLCHOLINESTERASE; CHOLINESTERASE INHIBITOR; POLLUTANT;

ANIMAL; CHEMISTRY; DRUG EFFECTS; HUMAN; METABOLISM; POLLUTANT; RISK ASSESSMENT; SIGNAL TRANSDUCTION; TOXICITY;

ACETYLCHOLINESTERASE; ANIMALS; CHOLINESTERASE INHIBITORS; ENVIRONMENTAL POLLUTANTS; HUMANS; RISK ASSESSMENT; SIGNAL TRANSDUCTION;

EID: 84908413350     PISSN: 07307268     EISSN: 15528618     Source Type: Journal    
DOI: 10.1002/etc.2662     Document Type: Review

References (91)

1. National Research Council. 2007. Toxicity Testing in the 21st Century: A Vision and a Strategy. National Academies Press, Washington, DC.
2. Fleischer M. 2007. Testing costs and testing capacity according to the REACH requirements-Results of a survey of independent and corporate GLP laboratories in the EU and Switzerland. J Bus Chem 4:96-114.
3. Ankley GA, Bennett RE, Erickson RJ, Hoff DJ, Hornung MW, Johnson RD, Mount DR, Nichols JW, Russom CL, Schmieder PK, Serrano JA, Tietge JE, Villeneuve DL. 2010. Adverse outcome pathways: A conceptual framework to support ecotoxicology research and risk assessment. Environ Toxicol Chem 29:730-741.
4. Organisation for Economic Co-operation and Development. 2012. Proposal for a template, and guidance on developing and assessing the completeness of adverse outcome pathways. Paris, France.
5. Boobis AR, Cohen SM, Dellarco V, McGregor D, Meek ME, Vickers C, Willcocks D, Farland W. 2006. IPCS framework for analyzing the relevance of a cancer mode of action for humans. Crit Rev Toxicol 36:781-792.
6. Boobis AR, Doe JE, Heinrich-Hirsch B, Meek ME, Munn S, Ruchirawat M, Schlatter J, Seed J, Vickers C. 2008. IPCS framework for analyzing the relevance of a noncancer mode of action for humans. Crit Rev Toxicol 38:87-96.
7. Hill AB. 1965. The environment and disease: Association or causation? Proc R Soc Med 58:295-300.
8. LaLone CA, Villeneuve DL, Cavallin JE, Kahl MD, Durhan EJ, Makynen EA, Jensen KM, Stevens KE, Severson MN, Blanksma CA, Flynn KM, Hartig PC, Woodard JS, Berninger JP, Norberg-King TJ, Johnson RD, Ankley GT. 2013. Cross-species sensitivity to a novel androgen receptor agonist of potential environmental concern, spironolactone. Environ Toxicol Chem 32:2528-2541.
9. Celander MC, Goldstone JV, Denslow ND, Iguchi T, Kille P, Meyerhoff RD, Smith BA, Hutchinson TH, Wheeler JR. 2011. Species extrapolation for the 21st century. Environ Toxicol Chem 30:52-63.
10. Vinken M. 2013. The adverse outcome pathway concept: A pragmatic tool in toxicology. Toxicology 312:158-165.
11. Hooper MJ, Ankley GT, Cristol DA, Maryoung LA, Noyes PD, Pinkerton KE. 2013. Interactions between chemical and climate stressors: A role for mechanistic toxicology in assessing climate change risks. Environ Toxicol Chem 32:32-48.
12. Bencic DC, Villeneuve DL, Biales AD, Blake L, Durhan EJ, Jensen KM, Kahl MD, Makynen EA, Martinovic-Weigelt D, Ankley GT. 2013. Effects of the insecticide fipronil on reproductive endocrinology in the fathead minnow. Environ Toxicol Chem 32:1828-1834.
13. Watanabe KH, Andersen ME, Basu N, Carvan MJ, Crofton KM, King KA, Sunol C, Tiffany-Castiglioni E, Schultz IR. 2011. Defining and modeling known adverse outcome pathways: Domoic acid and neuronal signaling as a case study. Environ Toxicol Chem 30:9-21.
14. Perkins EJ, Chipman JK, Edwards S, Habib T, Falciani F, Taylor R, Van Aggelen G, Vulpe C, Antczak P, Loguinov A. 2011. Reverse engineering adverse outcome pathways. Environ Toxicol Chem 30:22-38.
15. Nichols JW, Breen M, Denver RJ, DiStefano JJ, Edwards JS, Hoke RA, Volz DC, Zhang X. 2011. Predicting chemical impacts on vertebrate endocrine systems. Environ Toxicol Chem 30:39-51.
16. Campos B, Garcia-Reyero N, Rivetti C, Escalon L, Habib T, Tauler R, Tsakovski S, Pina B, Barata C. 2013. Identification of metabolic pathways in Daphnia magna explaining hormetic effects of selective serotonin reuptake inhibitors and 4-nonylphenol using transcriptomic and phenotypic responses. Environ Sci Technol 47:9434-9443.
17. Villeneuve DL, Volz DC, Embry MR, Ankley GT, Belanger SE, Leonard M, Schirmer K, Tanguay R, Truong L, Wehmas L. 2014. Investigating alternatives to the fish early life-stage test: A strategy for discovering and annotating adverse outcome pathways for early fish development. Environ Toxicol Chem 33:158-169.
18. Russom CL, Bradbury SP, Holecek WA, Grunwald DG. 1997. ECOTOX: An ecological effects database. Proceedings, Air & Waste Management Association Conference on Computing in Environmental Resource Management, Research Triangle Park, NC, USA, December 2-4, 1996, pp 387-397.
19. Lalone CA, Villeneuve DL, Burgoon LD, Russom CL, Helgen HW, Berninger JP, Tietge JE, Severson MN, Cavallin JE, Ankley GT. 2013. Molecular target sequence similarity as a basis for species extrapolation to assess the ecological risk of chemicals with known modes of action. Aquat Toxicol 144-146:141-154.
20. Wilson BW. 2010. Cholinesterases. Hayes' Handbook of Pesticide Toxicology, 3rd ed, Vol 2. Elsevier, Amsterdam, The Netherlands, pp 1457-1478.
21. Soreq H, Seidman S. 2001. Acetylcholinesterase-New roles for an old actor. Nat Rev Neurosci 2:294-302.
22. Fukuto TR. 1990. Mechanism of action of organophosphorus and carbamate insecticides. Environ Health Perspect 87:245-254.
23. Mileson BE, Chambers JE, Chen WL, Dettbarn W, Ehrich M, Eldefrawi AT, Gaylor DW, Hamernik K, Hodgson E, Karczmar AG, Padilla S, Pope CN, Richardson RJ, Saunders DR, Sheets LP, Sultatos LG, Wallace KB. 1998. Common mechanism of toxicity: A case study of organophosphorus pesticides. Toxicol Sci 41:8-20.
24. Sogob MA, Vilanova E. 2002. Enzymes involved in the detoxification of organophosphorus, carbamate and pyrethroid insecticides through hydrolysis. Toxicol Lett 128:215-228.
25. Schüürmann G. 1992. Ecotoxicology and structure-activity studies of organophosphorus compounds. In Draber W, Fujita T, eds, Rational Approaches to Structure, Activity, and Ecotoxicology of Agrochemicals. CRC, Boca Raton, FL, USA, pp 485-541.
26. Stenersen J. 2004. Specific enzyme inhibitors. In Chemical Pesticides: Mode of Action and Toxicology. CRC, Boca Raton, FL, USA, pp 73-114.
27. Lu Y, Park Y, Gao X, Zhang X, Yoo J, Pang X-P, Jiang H, Zhu KY. 2012. Cholinergic and non-cholinergic functions of two acetylcholinesterase genes revealed by gene-silencing in Tribolium castaneum. Sci Rep 2:1-7.
28. Taylor P. 2011. Anticholinesterase agents. In Brunton L, Chabner B, Knollman B, eds, Goodman and Gilman's The Pharmacological Basis of Therapeutics, 12th ed. McGraw Hill, New York, NY, USA, pp 255-276.
29. Tretyn A, Kendrick RE. 1991. Acetylcholine in plants: Metabolism and mechanism of action. Bot Rev 57:33-73.
30. Wallace KB. 1992. Species-selective toxicity of organophosphorus insecticides: A pharmacodynamics phenomenon. In Chambers JE, Levi PI, eds, Organophosphates-Chemistry, Fate, and Effects. Academic, San Diego, CA, USA, pp 79-105.
31. Wallace KB, Kemp JR. 1991. Species specificity in the chemical mechanisms of organophosphorus anticholinesterase activity. Chem Res Toxicol 4:41-49.
32. Cowman DF, Mazanti LE. 2000. Ecotoxicology of "new generation" pesticides to amphibians. In Sparling DW, Linder G, Bishop CA, Krest S, eds, Ecotoxicology of Amphibians and Reptiles. SETAC, Pensacola, FL, USA, pp 233-268.
33. Hill EF. 1988. Brain cholinesterase activity of apparently normal wild birds. J Wild Dis 24:51-61.
34. Rattner BA, Fairbrother A. 1991. Biological variability and the influence of stress on cholinesterase activity. In Hoffman DJ, Rattner BA, Burton GA Jr, Cairns J Jr, eds, Cholinesterase-Inhibiting Insecticides: Their Impact on Wildlife and the Environment. Elsevier, Amsterdam, The Netherlands, pp 89-107.
35. Ankley GT, Collyard SA. 1995. Influence of piperonyl butoxide on the toxicity of organophosphate insecticides to three species of freshwater benthic invertebrates. Comp Biochem Physiol 110C:149-155.
36. Grue CE, Powell GVN, Gladson NL. 1981. Brain cholinesterase (ChE) activity in nestling starlings: Implications for monitoring exposure of nestling songbirds to ChE inhibitors. Bull Environ Contam Toxicol 26:544-547.
37. Karanth S, Pope C. 2003. Age-related effects of chlorpyrifos and parathion on acetylcholine synthesis in rat striatum. Neurotoxicol Teratol 25:599-606.
38. Parkash R, Kaur K. 1982. Ontogeny of acetylcholinesterases in hybridizing Drosophila species. Proc Indian Nat Sci Acad B48:659-666.
39. Berman HA, Decker MM, Sangmee J. 1987. Reciprocal regulation of acetylcholinesterase and butyrylcholinesterase in mammalian skeletal muscle. Dev Biol 120:154-161.
40. Tsim KWK, Randall WR, Barnard EA. 1988. Synaptic acetylcholinesterase of chicken muscle changes during development from a hybrid to a homogenous enzyme. EMBO J 7:2451-2456.
41. Ludke JL, Hill EF, Dieter MP. 1975. Cholinesterase (ChE) response and related mortality among birds fed ChE inhibitors. Arch Environ Contam Toxicol 3:1-21.
42. Hoffman DJ, Eastin WC Jr. 1981. Effects of malathion, diazinon, and parathion on mallard embryo development and cholinesterase activity. Environ Res 26:472-485.
43. Phillips TA, Wu J, Summerfelt RC, Atchison GJ. 2002. Acute toxicity and cholinesterase inhibition in larval and early juvenile walleye exposed to chlorpyrifos. Environ Toxicol Chem 21:1469-1474.
44. Takimoto Y, Hagino S, Yamada H, Miyamoto J. 1984. The acute toxicity of fenitrothion to killifish (Oryzias latipes) at twelve different stages of its life history. J Pestic Sci 9:463-470.
45. Ellman GL, Courtney KD, Andres V Jr, Featherstone RM. 1961. A new and rapid colormetric determination of acetylcholinesterase activity. Biochem Pharmacol 7:88-95.
46. Wilson BW, Padilla S, Henderson JD, Brimijoin S, Dass PD, Elliot G, Jaeger B, Lanz D, Pearson R, Spies R. 1996. Factors in standardizing automated cholinesterase assays. J Toxicol Environ Health 48:187-195.
47. Johnson CD, Russell RL. 1975. A rapid, simple radiometric assay for cholinesterase suitable for multiple determinations. Anal Biochem 64:229-238.
48. Augustinsson KB. 1957. Assay methods for cholinesterases. In Glick D, ed, Methods of Biochemical Analysis, Vol 5. Interscience, New York, NY, USA, pp 1-63.
49. Zapata A, Chefer VI, Shippenberg TS, Denoroy L. 2009. Detection and quantification of neurotransmitters in dialysates. Curr Protoc Neurosci 7:1-30.
50. Reddy MS, Jayaprada P, Rao KVR. 1990. Impact of methyl parathion and malathion on cholinergic and non-cholinergic enzyme systems of penaeid prawn, Metapenaeus monoceros. Biochem Int 22:769-780.
51. Nayeemunnisa, Yasmeen N. 1986. On the presence of calmodulin in the brain of control and methyl parathion-exposed developing tadpoles of frog, Rana cyanophlictis. Curr Sci (Bangalore) 55:546-548.
52. Rao KSP, Rao KVR. 1984. Impact of methyl parathion toxicity and eserine inhibition on acetylcholinesterase activity in tissues of the teleost (Tilapia mossambica)-A correlative study. Toxicol Lett 22:351-356.
53. Kobayashi H, Yuyama A, Kudo M, Matsusaka N. 1983. Effects of organophosphorus compounds, O, O-dimethyl-o-(2, 2-dichlorovinyl)phosphate (DDVP) and O, O-dimethyl-o-(3-methyl 4-nitrophenyl)phosphorothioate (fenitrothion), on brain acetylcholine content and acetylcholinesterase activity in Japanese quail. Toxicology 28:219-227.
54. Kobayashi H, Yuyama A, Ohkawa T, Kajita T. 1988. Effect of single or chronic injection with a carbamate, propoxur, on the brain cholinergic system and behavior of mice. Jpn J Pharmacol 47:21-27.
55. Lushington GH, Guo J-X, Hurley MM. 2006. Acetylcholinesterase: Molecular modeling with the whole toolkit. Curr Topics Medic Chem 6:57-73.
56. Grue CE, Hart ADM, Mineau P. 1991. Biological consequences of depressed brain cholinesterase activity in wildlife. In Hoffman DJ, Rattner BA, Burton GA Jr, Cairns J Jr, eds, Cholinesterase-Inhibiting Insecticides: Their Impact on Wildlife and the Environment. Elsevier, Amsterdam, The Netherlands, pp 151-209.
57. Fulton MH, Key PB. 2001. Acetylcholinesterase inhibition in estuarine fish and invertebrates as an indicator of organophosphorous insecticide exposure and effects. Environ Toxicol Chem 20:37-45.
58. McKim JM, Schmieder PK, Niemi GJ, Carlson RW, Henry TR. 1987. Use of respiratory-cardiovascular responses of rainbow trout (Salmo gairdneri) in indentifying acute toxicity syndromes in fish: Part 2. Malathion, carbaryl, acrolein, and benzaldehyde. Environ Toxicol Chem 6:313-328.
59. Reddy NC, Rao JV. 2008. Biological response of earthworm, Eisenia foetida (Savigny) to an organophosphorus pesticide, profenofos. Ecotoxicol Environ Saf 71:574-582.
60. Al-Zubaidy MHI, Mousa YJ, Hasan MM, Mohammad FK. 2011. Acute toxicity of veterinary and agricultural formulations of organophosphates dichlorvos and diazinon in chicks. Arh Hig Rada Toksikol 62:317-323.
61. Karanth S, Liu J, Mirajkar N, Pope C. 2006. Effects of acute chlorpyrifos exposure on in vivo acetylcholine accumulation in rat striatum. Toxicol Appl Pharmacol 216:150-156.
62. Kobayashi H, Sato I, Akatsu Y, Fujii SI, Suzuki T, Matsusaka N, Yuyama A. 1994. Effects of single or repeated administration of a carbamate, propoxur, and an organophosphate, DDVP, on jejunal cholinergic activities and contractile responses in rats. J Appl Toxicol 14:185-190.
63. Hunt KA, Bird DM, Mineau P, Shutt L. 1991. Secondary poisoning hazard of fenthion to American kestrels. Arch Environ Contam Toxicol 21:84-90.
64. Jarvinen AW, Nordling BR, Henry ME. 1983. Chronic toxicity of dursban (chlorpyrifos) to the fathead minnow (Pimephales promelas) and the resultant acetylcholinesterase inhibition. Ecotoxicol Environ Saf 7:423-434.
65. Rajini PS, Melstrom P, Williams PL. 2008. A comparative study on the relationship between various toxicological endpoints in Caenorhabditis elegans exposed to organophosphorus insecticides. J Toxicol Environ Health 71:1043-1050.
66. Meek ME, Boobis A, Cote I, Dellarco V, Fotakis G, Munn S, Seed J, Vickers C. 2013. New developments in the evolution and application of the WHO/IPCS framework on mode of action/species concordance analysis. J Appl Toxicol 34:1-18.
67. Karen DJ, Klaine SJ, Ross PE. 2001. Further considerations of the skeletal system as a biomarker of episodic chlorpyrifos exposure. Aquat Toxicol 52:285-296.
68. Grue CE, Shipley BK. 1984. Sensitivity of nestling and adult starling to dicrotophos, an organophosphate pesticide. Environ Res 35:454-465.
69. Hudson RH, Tucker RK, Haegele MA. 1984. Handbook of Toxicity of Pesticides to Wildlife, Resource Publication 153, 2nd ed. Fish and Wildlife Service, US Department of the Interior, Washington, DC.
70. 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.
71. Bianco K, Yusseppone MS, Otero S, Luquet C, Rios de Molina MC, Kristoff G. 2013. Cholinesterases and neurotoxicity as highly sensitive biomarkers for an organophosphate insecticide in freshwater gastropod (Chilina gibbosa) with low sensitivity carboxylesterases. Aquat Toxicol 26-35:144-145.
72. Roberts DK, Silvey NJ, Bailey EM. 1988. Brain acetylcholinesterase activity recovery following acute methyl parathion intoxication in two feral rodent species: Comparison to laboratory rodents. Bull Environ Contam Toxicol 41:26-35.
73. Stavinoha WB, Ryan LC, Smith PW. 1969. Biochemical effects of an organophosphorus cholinesterase inhibitor on the rat brain. Ann N Y Acad Sci 160:378-382.
74. Kobayashi H, Yuyama A, Kajita T, Shimura K, Ohkawa T, Satoh K. 1985. Effects of insecticidal carbamates on brain acetylcholine content, acetylcholinesterase activity and behavior in mice. Toxicol Lett 29:153-159.
75. Oyama Y, Hori N, Evans ML, Allen CN, Carpenter DO. 1989. Electrophysiological estimation of the actions of acetylcholinesterase inhibitors on acetylcholine receptor and cholinesterase in physically isolated Aplysia neurons. Br J Pharmacol 96:573-582.
76. Futagawa H, Kakinuma Y, Takahashi H. 1997. Cardiovascular collapse through non-cholinergic mechanism after intravenous injection of n-methylcarbamate insecticide in rabbits. Toxicology 117:163-170.
77. Dasgupta R, Chakravorty PP, Kaviraj A. 2012. Effects of carbaryl, chlorpyrifos and endosulfan on growth, reproduction and respiration of tropical epigeic earthworm, Perionyx excavatus (Perrier). J Environ Sci Health B 47:99-103.
78. US Environmental Protection Agency. 2006. Organophosphorus cumulative risk assessment-2006. Update. Office of Pesticide Programs, Washington, DC.
79. Venturino A, Gauna L, Bergoc RM, Peschen de D'Angelo AM. 2001. Toxicokinetics of malathion in larval stages of the toad Bufo arenarum (Hensel): Effect of exogenous spermidine. Pest Biochem Phys 70:142-150.
80. Ferrari A, Venturino A, Pechen de D'angelo AM. 2004. Time course of brain cholinesterase inhibition and recovery following acute and subsacute azinphosmethyl, parathion and carbaryl exposure in the goldfish (Carassius auratus). Ecotoxicol Environ Saf 57:420-425.
81. Rao JV. 2008. Brain acetylcholinesterase activity as a potential biomarker for the rapid assessment of chlorpyrifos toxicity in euryhaline fish, Oreochromis mossambicus. Environ Bioindic 3:11-22.
82. Rose RL, Sparks TC. 1984. Acephate toxicity, metabolism, and anticholinesterase activity in Heliothis virescens (F.) and Anthonomus grandis grandis (Boheman). Pest Biochem Physiol 22:69-77.
83. Duangsawasdi M. 1977. Organophosphate insecticide toxicity in rainbow trout (Salmo gairdneri). Effects of temperature and investigations on the sites of action. PhD thesis. University of Manitoba, Manitoba, Canada.
84. Duangsawasdi M, Klaverkamp JF. 1979. Acephate and fenitrothion toxicity in rainbow trout: Effects of temperature stress and investigations on the sites of action. In Aquatic Toxicology, Vol 2, STP 667. ASTM International, Philadelphia, PA, USA, pp 35-51.
85. Grue CE, Gibert PL, Seeley ME. 1997. Neurophysiological and behavioral changes in non-target wildlife exposed to organophosphate and carbamate pesticides: Thermoregulation, food consumption, and reproduction. Amer Zool 37:369-388.
86. Perkins EJ, Ankley GT, Crofton KM, Garcia-Reyero N, LaLone CA, Johnson MS, Tietge JE, Villeneuve DL. 2013. Current perspectives on the use of alternative species in human health and ecological hazard assessments. Environ Health Perspect 121:1002-1010.
87. Kramer VJ, Etterson MA, Hecker M, Murphy CA, Roesijadi G, Spade DJ, Spromberg JA, Wang M, Ankley GT. 2011. Adverse outcome pathways and ecological risk assessment: Bridging to population-level effects. Environ Toxicol Chem 30:64-76.
88. Sipes N, Martin M, Kothiya P, Reif T, Judson T, Richard A, Houck K, Dix D, Kavlock R, Knudsen T. 2013. Profiling 976 ToxCast chemicals across 331 enzymatic and receptor signaling assays. Chem Res Toxicol 26:878-895.
89. Monserrat JM, Bianchini A. 2001. Anticholinesterase effect of eserine (physostigmine) in fish and crustacean species. Braz Arch Biol Technol 44:63-68.
90. Call DJ, Poirier SH, Lindberg CA, Harting SL, Markee TP, Brooke LT, Zarvan N, Northcott CE. 1989. Toxicity of selected uncoupling and acetylcholinesterase-inhibiting pesticides to the fathead minnow (Pimephales promelas). In Weigmann DL, ed, Pesticides in Terrestrial and Aquatic Environments. Virginia Polytechnic Institute and State University, Blacksburg, VA, USA, pp 317-336.
91. de Bruijn J, Hermens JLM. 1993. Inhibition of acetylcholinesterase and acute toxicity of organophosphorous compounds to fish: A preliminary structure-activity analysis. Aquat Toxicol 24:257-274.