Subacute developmental exposure of zebrafish to the organophosphate pesticide metabolite, chlorpyrifos-oxon, results in defects in Rohon-Beard sensory neuron development

Aquatic Toxicology

Volumn 100, Issue 1, 2010, Pages 101-111

  Jacobson, Saskia M ^a   Birkholz, Denise A ^a   McNamara, Marcy L ^a   Bharate, Sandip B ^a   George, Kathleen M ^a  

^a UNIVERSITY OF MONTANA   (United States)

Author keywords

Biomarkers; Chlorpyrifos; Developmental neurotoxicity; Organophosphate; Rohon Beard sensory neurons

Indexed keywords

ACETYLCHOLINESTERASE; ALPHA BUNGAROTOXIN; BIOLOGICAL MARKER; CHLORPYRIFOS; NICOTINIC RECEPTOR; ORGANOPHOSPHATE PESTICIDE; DRUG DERIVATIVE; INSECTICIDE; O,O DIETHYL O 3,5,6 TRICHLORO 2 PYRIDYL PHOSPHATE; O,O-DIETHYL O-3,5,6-TRICHLORO-2-PYRIDYL PHOSPHATE; ORGANOPHOSPHATE;

BIOMARKER; FISH; INHIBITION; NEUROLOGY; ORGANOPHOSPHATE; PESTICIDE; POLLUTION EXPOSURE; TOXICITY;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; BIREFRINGENCE; CONTROLLED STUDY; DEVELOPMENTAL STAGE; DOWN REGULATION; EMBRYO; EMBRYO DEVELOPMENT; ENVIRONMENTAL EXPOSURE; ENVIRONMENTAL MONITORING; ENZYME ACTIVITY; ENZYME INHIBITION; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION; HYDROLYSIS; MUSCLE CELL; NERVE CELL DIFFERENTIATION; NERVE FIBER; NERVOUS SYSTEM DEVELOPMENT; NEUROTOXICITY; NONHUMAN; PHENOTYPE; PRIORITY JOURNAL; QUANTITATIVE ANALYSIS; SENSORY NERVE CELL; ZEBRA FISH; ANIMAL; ANIMAL EMBRYO; CONGENITAL MALFORMATION; DOSE RESPONSE; DRUG EFFECT; GENE EXPRESSION; GENETICS; GROWTH, DEVELOPMENT AND AGING; NEUROMUSCULAR SYNAPSE; PRENATAL DEVELOPMENT; SENSORY RECEPTOR; TOXICITY TESTING; ULTRASTRUCTURE; WATER POLLUTANT;

DANIO RERIO;

ANIMALS; CHLORPYRIFOS; DOSE-RESPONSE RELATIONSHIP, DRUG; EMBRYO, NONMAMMALIAN; EMBRYONIC DEVELOPMENT; GENE EXPRESSION; INSECTICIDES; NEUROGENESIS; NEUROMUSCULAR JUNCTION; PHOSPHORIC ACID ESTERS; SENSORY RECEPTOR CELLS; TOXICITY TESTS; WATER POLLUTANTS, CHEMICAL; ZEBRAFISH;

EID: 77957574088     PISSN: 0166445X     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.aquatox.2010.07.015     Document Type: Article

References (42)

1. Abdel-Rahman A.A., Blumenthal G.M., Abou-Donia S.A., Ali F.A., Abdel-Monem A.E., Abou-Donia M.B. Pharmacokinetic profile and placental transfer of a single intravenous injection of [(14)C]chlorpyrifos in pregnant rats. Arch. Toxicol. 2002, 76:452-459.
2. Behra M., Cousin X., Bertrand C., Vonesch J.L., Biellmann D., Chatonnet A., Strahle U. Acetylcholinesterase is required for neuronal and muscular development in the zebrafish embryo. Nat. Neurosci. 2002, 5:111-118.
3. Behra M., Etard C., Cousin X., Strahle U. The use of zebrafish mutants to identify secondary target effects of acetylcholine esterase inhibitors. Toxicol. Sci. 2004, 77:325-333.
4. Benjaminov O., Hoffer E., Taitelman U., Urbach J., Brandes J.M. Parathion transfer and acetylcholinesterase activity in an in-vitro perfused term human placenta. Vet. Hum. Toxicol. 1992, 34:10-12.
5. Bertrand C., Chatonnet A., Takke C., Yan Y.L., Postlethwait J., Toutant J.P., Cousin X. Zebrafish acetylcholinesterase is encoded by a single gene localized on linkage group 7. Gene structure and polymorphism; molecular forms and expression pattern during development. J. Biol. Chem. 2001, 276:464-474.
6. Clarke J.D., Hayes B.P., Hunt S.P., Roberts A. Sensory physiology, anatomy and immunohistochemistry of Rohon-Beard neurones in embryos of Xenopus laevis. J. Physiol. 1984, 348:511-525.
7. Costa L.G. Current issues in organophosphate toxicology. Clin. Chim. Acta 2006, 366:1-13.
8. Downes G.B., Granato M. Acetylcholinesterase function is dispensable for sensory neurite growth but is critical for neuromuscular synapse stability. Dev. Biol. 2004, 270:232-245.
9. Egan R.J., Bergner C.L., Hart P.C., Cachat J.M., Canavello P.R., Elegante M.F., Elkhayat S.I., Bartels B.K., Tien A.K., Tien D.H., Mohnot S., Beeson E., Glasgow E., Amri H., Zukowska Z., Kalueff A.V. Understanding behavioral and physiological phenotypes of stress and anxiety in zebrafish. Behav. Brain Res. 2009, 205:38-44.
10. 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.
11. EPA, U. S., 2006. Organophosphorus Cumulative Risk Assessment. O. P. Programs.
12. Eskenazi B., Marks A.R., Bradman A., Harley K., Barr D.B., Johnson C., Morga N., Jewell N.P. Organophosphate pesticide exposure and neurodevelopment in young Mexican-American children. Environ. Health Perspect. 2007, 115:792-798.
13. Finn R.N. The physiology and toxicology of salmonid eggs and larvae in relation to water quality criteria. Aquat. Toxicol. 2007, 81:337-354.
14. Fukuto T.R. Mechanism of action of organophosphorus and carbamate insecticides. Environ. Health Perspect. 1990, 87:245-254.
15. Grigoryan H., Lockridge O. Nanoimages show disruption of tubulin polymerization by chlorpyrifos oxon: implications for neurotoxicity. Toxicol. Appl. Pharmacol. 2009, 240:143-148.
16. Hen Chow E.S., Cheng S.H. Cadmium affects muscle type development and axon growth in zebrafish embryonic somitogenesis. Toxicol. Sci. 2003, 73:149-159.
17. Jacobson S.W., Jacobson J.L. New evidence of effects of organophosphate pesticides on neurodevelopment in children: commentary on the article by Kofman et al. on page 88. Pediatr. Res. 2006, 60:22-23.
18. Karnovsky M.J., Roots L. A direct-coloring thiocholine method for cholinesterases. J. Histochem. Cytochem. 1964, 12:219-221.
19. Kim M.J., Liu I.H., Song Y., Lee J.A., Halfter W., Balice-Gordon R.J., Linney E., Cole G.J. Agrin is required for posterior development and motor axon outgrowth and branching in embryonic zebrafish. Glycobiology 2007, 17:231-247.
20. Kruse J., Mailhammer R., Wernecke H., Faissner A., Sommer I., Goridis C., Schachner M. Neural cell adhesion molecules and myelin-associated glycoprotein share a common carbohydrate moiety recognized by monoclonal antibodies L2 and HNK-1. Nature 1984, 311:153-155.
21. Kuster E., Altenburger R. Comparison of cholin- and carboxylesterase enzyme inhibition and visible effects in the zebra fish embryo bioassay under short-term paraoxon-methyl exposure. Biomarkers 2006, 11:341-354.
22. Levin E.D., Chrysanthis E., Yacisin K., Linney E. Chlorpyrifos exposure of developing zebrafish: effects on survival and long-term effects on response latency and spatial discrimination. Neurotoxicol. Teratol. 2003, 25:51-57.
23. Levin E.D., Swain H.A., Donerly S., Linney E. Developmental chlorpyrifos effects on hatchling zebrafish swimming behavior. Neurotoxicol. Teratol. 2004, 26:719-723.
24. Linney E., Upchurch L., Donerly S. Zebrafish as a neurotoxicological model. Neurotoxicol. Teratol. 2004, 26:709-718.
25. Liu Y., Halloran M.C. Central and peripheral axon branches from one neuron are guided differentially by Semaphorin3D and transient axonal glycoprotein-1. J. Neurosci. 2005, 25:10556-10563.
26. Meier E.P., Dennis W.H., Rosencrance A.B., Randall W.F., Cooper W.J., Warner M.C. Sulfotepp, a toxic impurity in formulations of diazinon. Bull. Environ. Contam. Toxicol. 1979, 23:158-164.
27. Meikle R.W., Youngson C.R. The hydrolysis rate of chlorpyrifos, O-O-diethyl O-(3,5,6-trichloro-2-pyridyl) phosphorothioate, and its dimethyl analog, chlorpyrifos-methyl, in dilute aqueous solution. Arch. Environ. Contam. Toxicol. 1978, 7:13-22.
28. Nitkin R.M., Smith M.A., Magill C., Fallon J.R., Yao Y.M., Wallace B.G., McMahan U.J. Identification of agrin, a synaptic organizing protein from Torpedo electric organ. J. Cell Biol. 1987, 105:2471-2478.
29. Paraoanu L.E., Layer P.G. Acetylcholinesterase in cell adhesion, neurite growth and network formation. FEBS J. 2008, 275:618-624.
30. Racke K.D. Environmental fate of chlorpyrifos. Rev. Environ. Contam. Toxicol. 1993, 131:1-150.
31. Slotkin T.A. Cholinergic systems in brain development and disruption by neurotoxicants: nicotine, environmental tobacco smoke, organophosphates. Toxicol. Appl. Pharmacol. 2004, 198:132-151.
32. Smit J.W., Huisman M.T., van Tellingen O., Wiltshire H.R., Schinkel A.H. Absence or pharmacological blocking of placental P-glycoprotein profoundly increases fetal drug exposure. J. Clin. Invest. 1999, 104:1441-1447.
33. Smith J.N., Campbell J.A., Busby-Hjerpe A.L., Lee S., Poet T.S., Barr D.B., Timchalk C. Comparative chlorpyrifos pharmacokinetics via multiple routes of exposure and vehicles of administration in the adult rat. Toxicology 2009, 261:47-58.
34. Sultatos L.G. Mammalian toxicology of organophosphorus pesticides. J. Toxicol. Environ. Health 1994, 43:271-289.
35. Thullbery M.D., Cox H.D., Schule T., Thompson C.M., George K.M. Differential localization of acetylcholinesterase in neuronal and non-neuronal cells. J. Cell. Biochem. 2005, 96:599-610.
36. Trevarrow B., Marks D.L., Kimmel C.B. Organization of hindbrain segments in the zebrafish embryo. Neuron 1990, 4:669-679.
37. van Eeden F.J., Granato M., Schach U., Brand M., Furutani-Seiki M., Haffter P., Hammerschmidt M., Heisenberg C.P., Jiang Y.J., Kane D.A., Kelsh R.N., Mullins M.C., Odenthal J., Warga R.M., Allende M.L., Weinberg E.S., Nusslein-Volhard C. Mutations affecting somite formation and patterning in the zebrafish, Danio rerio. Development 1996, 123:153-164.
38. Wan M.T., Moul D.J., Watts R.G. Acute toxicity to juvenile Pacific salmonids of Garlon 3A, Garlon 4, triclopyr, triclopyr ester, and their transformation products: 3,5,6-trichloro-2-pyridinol and 2-methoxy-3,5,6-trichloropyridine. Bull. Environ. Contam. Toxicol. 1987, 39:721-728.
39. Westerfield M. The Zebrafish Book. A Guide for the Laboratory use of Zebrafish (Danio rerio) 2000, University of Oregon Press, Eugene.
40. Williams J.A., Barrios A., Gatchalian C., Rubin L., Wilson S.W., Holder N. Programmed cell death in zebrafish rohon beard neurons is influenced by TrkC1/NT-3 signaling. Dev. Biol. 2000, 226:220-230.
41. Yang D., Howard A., Bruun D., Ajua-Alemanj M., Pickart C., Lein P.J. Chlorpyrifos and chlorpyrifos-oxon inhibit axonal growth by interfering with the morphogenic activity of acetylcholinesterase. Toxicol. Appl. Pharmacol. 2008, 228:32-41.
42. Young J.G., Eskenazi B., Gladstone E.A., Bradman A., Pedersen L., Johnson C., Barr D.B., Furlong C.E., Holland N.T. Association between in utero organophosphate pesticide exposure and abnormal reflexes in neonates. Neurotoxicology 2005, 26:199-209.