Neurologic dysfunction and genotoxicity induced by low levels of chlorpyrifos

NeuroToxicology

Volumn 45, Issue , 2014, Pages 22-30

  Muller, Mariel ^a   Hess, Leonardo ^a   Tardivo, Agostina ^a   Lajmanovich, Rafael ^b,c   Attademo, Andres ^b,c   Poletta, Gisela ^b,c   Simoniello, Maria Fernanda ^b   Yodice, Agustina ^a   Lavarello, Simona ^a   Chialvo, Dante ^a,c   Scremin, Oscar ^a,c,d  

^a FACULTAD DE CIENCIAS MÉDICAS   (Argentina)

^b UNIVERSIDAD NACIONAL DEL LITORAL   (Argentina)

^c Consejo Nacional de Investigaciones Cientificas y Tecnicas ^*  (Argentina)

^d UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

Acetylcholinesterase inhibitors; Auditory startle; Comet assay; EEG; Evoked potentials

Indexed keywords

ACETYLCHOLINESTERASE; CARBOXYLESTERASE; CHLORPYRIFOS; CHOLINESTERASE; URETHAN; CHOLINESTERASE INHIBITOR; ESTERASE;

ADULT; AMPLITUDE MODULATION; ANIMAL EXPERIMENT; ARTICLE; BODY MASS; BRAIN CORTEX; CELL VIABILITY; COMET ASSAY; CONTROLLED STUDY; DNA DAMAGE; ELECTROENCEPHALOGRAM; ENZYME ACTIVITY; ENZYME BLOOD LEVEL; ENZYME INHIBITION; EVOKED SOMATOSENSORY RESPONSE; EXPOSURE; GENOTOXICITY; MALE; NEUROLOGIC DISEASE; NONHUMAN; RAT; RECTUM TEMPERATURE; STARTLE REFLEX; ANIMAL; AUDITORY STIMULATION; BLOOD; BODY TEMPERATURE; BODY WEIGHT; DOSE RESPONSE; DRUG EFFECTS; ELECTROENCEPHALOGRAPHY; MUTAGEN TESTING; PATHOPHYSIOLOGY; PREPULSE INHIBITION; SPRAGUE DAWLEY RAT; WISTAR RAT;

ACETYLCHOLINESTERASE; ACOUSTIC STIMULATION; ANIMALS; BODY TEMPERATURE; BODY WEIGHT; BUTYRYLCHOLINESTERASE; CARBOXYLESTERASE; CEREBRAL CORTEX; CHLORPYRIFOS; CHOLINESTERASE INHIBITORS; DNA DAMAGE; DOSE-RESPONSE RELATIONSHIP, DRUG; ELECTROENCEPHALOGRAPHY; ESTERASES; EVOKED POTENTIALS, SOMATOSENSORY; MALE; MUTAGENICITY TESTS; PREPULSE INHIBITION; RATS; RATS, SPRAGUE-DAWLEY; RATS, WISTAR; REFLEX, STARTLE;

EID: 84907454159     PISSN: 0161813X     EISSN: 18729711     Source Type: Journal    
DOI: 10.1016/j.neuro.2014.08.012     Document Type: Article

References (83)

1. Alenda A., Nunez A. Sensory-interference in rat primary somatosensory cortical neurons. Eur J Neurosci 2004, 19:766-770.
2. Alenda A., Nunez A. Cholinergic modulation of sensory interference in rat primary somatosensory cortical neurons. Brain Res 2007, 1133:158-167.
3. Allison T., Hume A.L. A comparative analysis of short-latency somatosensory evoked potentials in man, monkey, cat, and rat. Exp Neurol 1981, 72:592-611.
4. Altieri M.A. Agroecology: the scientific basis of alternative agriculture 1987, Westview Press, Boulder, CO.
5. Amer S.M., Fahmy M.A. Cytogenetic effects of pesticides. I. Induction of micronuclei in mouse bone marrow by the insecticide Dursban. Mutat Res 1982, 101:247-255.
6. Azqueta A., Shaposhnikov S., Collins A.R. Detection of oxidised DNA using DNA repair enzymes. The comet assay in toxicology 2009, 57-78. RSC Publishing, Cambridge, UK. A. Dhawan, D. Anderson (Eds.).
7. Barr D.B., Allen R., Olsson A.O., Bravo R., Caltabiano L.M., Montesano A., et al. Concentrations of selective metabolites of organophosphorus pesticides in the United States population. Environ Res 2005, 99:314-326.
8. Barron M.G., Woodburn K.B. Ecotoxicology of chlorpyrifos. Rev Environ Contam Toxicol 1995, 144:1-93.
9. Bosch D., Schmid S. Activation of muscarinic cholinergic receptors inhibits giant neurones in the caudal pontine reticular nucleus. Eur J Neurosci 2006, 24:1967-1975.
10. Bunyan P.J., Jennings D.M., Taylor A. Organophosphorus poisoning: chronic feeding of some common pesticides to pheasants and pigeons. J Agric Food Chem 1969, 17:1027-1032.
11. Buzsaki G., Eidelberg E. Phase relations of hippocampal projection cells and interneurons to theta activity in the anesthetized rat. Brain Res 1983, 266:334-339.
12. Chang H.-T. Interactions of evoked cortical potentials. J Neurophysiol 1953, 16:133-144.
13. Chang H.-t. The evoked potentials. Handbook of physiology 1959, 299-313. American Physiological Society, Washintong, DC. V.E. Hall (Ed.).
14. Checler F. Non-cholinergic actions of acetylcholinesterases: a genuine peptidase function or contaminating proteases. Trends Biochem Sci 1990, 15(9):337-338.
15. Chippendale T.J., Jawelkow G.A., Russell R.W., Overstreet O.H. Tolerance to low acetylcholinesterase levels: modification of behavior without acute behavioral change. Psychopharmacologia 1972, 26:127-139.
16. Clark M.G., Sun W., Myers T.M., Bansal R., Doctor B.P., Saxena A. Effects of physostigmine and human butyrylcholinesterase on acoustic startle reflex and prepulse inhibition in C57BL/6J mice. Pharmacol Biochem Behav 2005, 81:497-505.
17. Clegg D.J., van Gemert M. Expert panel report of human studies on chlorpyrifos and/or other organophosphate exposures. J Toxicol Environ Health B Crit Rev 1999, 2:257-279.
18. Collins A., Dusinska M., Franklin M., Somorovska M., Petrovska H., Duthie S., et al. Comet assay in human biomonitoring studies: reliability, validation, and applications. Environ Mol Mutagen 1997, 30:139-146.
19. Desi I., Nagymajtenyi L. Neurotoxicologic investigations of the pesticide dichlorvos (DDVP). Effects on the central and peripheral nervous system. Toxicology 1988, 49:141-148.
20. Dickson C.T., Trepel C., Bland B.H. Extrinsic modulation of theta field activity in the entorhinal cortex of the anesthetized rat. Hippocampus 1994, 4:37-51.
21. Domino E.F., Dren A.T., Yamamoto K.I. Pharmacologic evidence for cholinergic mechanisms in neocortical and limbic activating systems. Prog Brain Res 1967, 27:337-364.
22. Dusinska M., Collins A.R. The comet assay in human biomonitoring: gene-environment interactions. Mutagenesis 2008, 23:191-205.
23. Eccles J.C. Interpretation of action potentials evoked in the cerebral cortex. Electroencephalogr Clin Neurophysiol 1951, 3:449-464.
24. Ellison C.A., Smith J.N., Lein P.J., Olson J.R. Pharmacokinetics and pharmacodynamics of chlorpyrifos in adult male Long-Evans rats following repeated subcutaneous exposure to chlorpyrifos. Toxicology 2011, 287:137-144.
25. Ellman G.L., Courtney K.D., Andres V., Featherstone R.M. A new and rapid colorimetric determination of acetylcholinesterase activity. Biochem Pharmacol 1961, 7:88-95.
26. Farahat F.M., Ellison C.A., Bonner M.R., McGarrigle B.P., Crane A.L., Fenske R.A., et al. Biomarkers of chlorpyrifos exposure and effect in Egyptian cotton field workers. Environ Health Perspect 2011, 119:801-806.
27. Gomori G. Human esterases. J Lab Clin Med 1953, 42:445-453.
28. Hill R.H., Head S.L., Baker S., Gregg M., Shealy D.B., Bailey S.L., et al. Pesticide residues in urine of adults living in the United States: reference range concentrations. Environ Res 1995, 71:99-108.
29. Holschneider D.P., Leuchter A., Walton N.Y., Scremin O., Treiman D. Changes in cortical EEG and cholinergic function in response to NGF in rats with nucleus basalis lesions. Brain Res 1997, 765:228-237.
30. Holschneider D.P., Waite J.J., Leuchter A.F., Walton N.Y., Scremin O.U. Changes in electrocortical power and coherence in response to the selective cholinergic immunotoxin 192 IgG-saporin. Exp Brain Res 1999, 126:270-280.
31. Jellema T., Brunia C.H., Wadman W.J. Sequential activation of microcircuits underlying somatosensory-evoked potentials in rat neocortex. Neuroscience 2004, 129:283-295.
32. Jergentz S., Pessacq P., Mugni H., Bonetto C., Schulz R. Linking in situ bioassays and population dynamics of macroinvertebrates to assess agricultural contamination in streams of the Argentine pampa. Ecotoxicol Environ Saf 2004, 59:133-141.
33. Jett D.A. Chemical toxins that cause seizures. Neurotoxicology 2012, 33:1473-1475.
34. Johnson M.K. Organophosphorus esters causing delayed neurotoxic effects. Arch Toxicol 1975, 34:259-288.
35. Jones C.K., Shannon H.E. Muscarinic cholinergic modulation of prepulse inhibition of the acoustic startle reflex. J Pharmacol Exp Ther 2000, 294:1017-1023.
36. Khokhar J.Y., Tyndale R.F. Rat brain CYP2B-enzymatic activation of chlorpyrifos to the oxon mediates cholinergic neurotoxicity. Toxicol Sci 2012, 126:325-335.
37. Kinney G.G., Vogel G.W., Feng P. Brainstem carbachol injections in the urethane anesthetized rat produce hippocampal theta rhythm and cortical desynchronization: a comparison of pedunculopontine tegmental versus nucleus pontis oralis injections. Brain Res 1998, 809:307-313.
38. Kobayashi H., Sugiyama C., Morikawa Y., Hayashi M., Sofuni T. A comparison between manual microscopic analysis and computerized image analysis in the single cell gel electrophoresis assay. MMS Commun 1995, 3:103-115.
39. Koch M. The neurobiology of startle. Prog Neurobiol 1999, 59:107-128.
40. Leung L.S., Martin L.A., Stewart D.J. Hippocampal theta rhythm in behaving rats following ibotenic acid lesion of the septum. Hippocampus 1994, 4:136-147.
41. Li B., Stribley J.A., Ticu A., Xie W., Schopfer L.M., Hammond P., et al. Abundant tissue butyrylcholinesterase and its possible function in the acetylcholinesterase knockout mouse. J Neurochem 2000, 75:1320-1331.
42. Loewy R.M., Monza L.B., Kirs V.E., Savini M.C. Pesticide distribution in an agricultural environment in Argentina. J Environ Sci Health B 2011, 46:662-670.
43. Lopez-Crespo G.A., Carvajal F., Flores P., Sanchez-Santed F., Sanchez-Amate M.C. Time course of biochemical and behavioural effects of a single high dose of chlorpyrifos. Neurotoxicology 2007, 28:541-547.
44. Lorente de No R. Cerebral cortex: architecture, intracortical connections, motor projections. Physiology of the nervous system 1949, 288-330. Oxford University Press, New York. 3rd ed. J.F. Fulton (Ed.).
45. Ma T., Chambers J.E. Kinetic parameters of desulfuration and dearylation of parathion and chlorpyrifos by rat liver microsomes. Food Chem Toxicol 1994, 32:763-767.
46. Malcolm J.L., Saraiva P., Spear P.J. Cholinergic and adrenergic inhibition in the rat cerebral cortex. Int J Neuropharmacol 1967, 6:509-527.
47. Manzo L., Castoldi A.F., Coccini T., Prockop L.D. Assessing effects of neurotoxic pollutants by biochemical markers. Environ Res 2001, 85:31-36.
48. Marino D., Ronco A. Cypermethrin and chlorpyrifos concentration levels in surface water bodies of the Pampa Ondulada, Argentina. Bull Environ Contam Toxicol 2005, 75:820-826.
49. Mercille S., Massie B. Induction of apoptosis in nutrient-deprived cultures of hybridoma and myeloma cells. Biotechnol Bioeng 1994, 44:1140-1154.
50. Mesulam M.M., Guillozet A., Shaw P., Levey A., Duysen E.G., Lockridge O. Acetylcholinesterase knockouts establish central cholinergic pathways and can use butyrylcholinesterase to hydrolyze acetylcholine. Neuroscience 2002, 110:627-639.
51. Morgan M.K., Sheldon L.S., Jones P.A., Croghan C.W., Chuang J.C., Wilson N.K. The reliability of using urinary biomarkers to estimate children's exposures to chlorpyrifos and diazinon. J Expo Sci Environ Epidemiol 2011, 21:280-290.
52. Mugni H., Demetrio P., Paracampo A., Pardi M., Bulus G., Bonetto C. Toxicity persistence in runoff water and soil in experimental soybean plots following chlorpyrifos application. Bull Environ Contam Toxicol 2012, 89:208-212.
53. Muniz J.F., McCauley L., Scherer J., Lasarev M., Koshy M., Kow Y.W., et al. Biomarkers of oxidative stress and DNA damage in agricultural workers: a pilot study. Toxicol Appl Pharmacol 2008, 227:97-107.
54. Mwanza J.C., Lyke D.F., Hertzberg R.C., Haber L., Kohrman-Vincent M., Li R., et al. Cholinesterase inhibition and depression of the photic after discharge of flash evoked potentials following acute or repeated exposures to a mixture of carbaryl and propoxur. Neurotoxicology 2012, 33:332-346.
55. Nagymajtenyi L., Schulz H., Papp A., Desi I. Developmental neurotoxicological effects of lead and dimethoate in animal experiments. Neurotoxicology 1998, 19:617-622.
56. Papp A., Gyorgyi K., Nagymajtenyi L., Desi I. Opposite short-term changes induced by an organophosphate in cortical and hippocampal evoked activity. Neurobiology (Bp) 1996, 4:431-440.
57. Patnaik K.K., Tripathy N.K. Farm-grade chlorpyrifos (Durmet) is genotoxic in somatic and germ-line cells of Drosophila. Mutat Res 1992, 279:15-20.
58. Paxinos G., Watson C. The rat brain in stereotaxic coordinates 1998, Academic Press, San Diego. 4th ed.
59. Rao M.R., Kanji V.K., Sekhar V. Pesticide induced changes of nitric oxide synthase in rat brain in vitro. Drug Chem Toxicol 1999, 22:411-420.
60. Reigart J.R., Roberts J.R. Recognition and management of pesticide poisonings 1999, U.S. Environmental Protection Agency, Washington, DC.
61. Riekkinen P., Sirvio J., Jakala P., Lammintausta R., Riekkinen P. Effect of alpha2 antagonists and an agonist on EEG slowing induced by scopolamine and lesion of the nucleus basalis. Neuropharmacology 1990, 29:993-999.
62. Rosenstock L., Keifer M., Daniell W.E., McConnell R., Claypoole K. Chronic central nervous system effects of acute organophosphate pesticide intoxication. The Pesticide Health Effects Study Group. Lancet 1991, 338:223-227.
63. Sanchez-Hernandez J.C., Carbonell R., Henriquez Perez A., Montealegre M., Gomez L. Inhibition of plasma butyrylcholinesterase activity in the lizard Gallotia galloti palmae by pesticides: a field study. Environ Pollut 2004, 132:479-488.
64. Savage E.P., Keefe T.J., Mounce L.M., Heaton R.K., Lewis J.A., Burcar P.J. Chronic neurological sequelae of acute organophosphate pesticide poisoning. Arch Environ Health 1988, 43:38-45.
65. Schlatter J., Lutz W.K. The carcinogenic potential of ethyl carbamate (urethane): risk assessment at human dietary exposure levels. Food Chem Toxicol 1990, 28:205-211.
66. Scremin O.U., Chialvo D.R., Lavarello S., Berra H.H., Lucero M.A. The environmental pollutant endosulfan disrupts cerebral cortical function at low doses. Neurotoxicology 2011, 32:31-37.
67. Scremin O.U., Rovere A.A., Raynald A.C., Giardini A. Cholinergic control of blood flow in the cerebral cortex of the rat. Stroke 1973, 4:232-239.
68. SENASA Importacion Agroquimicos 2011, http://www.senasa.gov.ar/contenido.php%3Fto=n%26in=524%26ino=524%26io=7331.
69. Seppalainen A.M. Applications of neurophysiological methods in occupational medicine. A review. Scand J Work Environ Health 1975, 1:1-14.
70. Singh N.P. Microgels for estimation of DNA strand breaks, DNA protein crosslinks and apoptosis. Mutat Res 2000, 455:111-127.
71. Singh N.P., McCoy M.T., Tice R.R., Schneider E.L. A simple technique for quantitation of low levels of DNA damage in individual cells. Exp Cell Res 1988, 175:184-191.
72. Steenland K., Jenkins B., Ames R.G., O'Malley M., Chrislip D., Russo J. Chronic neurological sequelae to organophosphate pesticide poisoning. Am J Public Health 1994, 84:731-736.
73. Sumerford W.T., Hayes W.J., Johnston J.M., Walker K., Spillane J. Cholinesterase response and symptomatology from exposure to organic phosphorus insecticides. AMA Arch Ind Hyg Occup Med 1953, 7:383-398.
74. Taylor P. Anticholinesterase Agents. Goodman and Gilman's the pharmacological basis of therapeutics 1990, 131-149. Pergamon Press, New York. A. Goodman Gilman, T.W. Rall, A.S. Nies, P. Taylor (Eds.).
75. Terry A.V.J., Stone J.D., Buccafusco J.J., Sickles D.W., Sood A., Prendergast M.A. Repeated exposures to subthreshold doses of chlorpyrifos in rats: hippocampal damage, impaired axonal transport, and deficits in spatial learning. J Pharmacol Exp Ther 2003, 305:375-384.
76. Timofeeva O.A., Gordon C.J. Changes in EEG power spectra and behavioral states in rats exposed to the acetylcholinesterase inhibitor chlorpyrifos and muscarinic agonist oxotremorine. Brain Res 2001, 893:165-177.
77. Timofeeva O.A., Gordon C.J. EEG spectra, behavioral states and motor activity in rats exposed to acetylcholinesterase inhibitor chlorpyrifos. Pharmacol Biochem Behav 2002, 72:669-679.
78. Valverde M., Rojas E. Environmental and occupational biomonitoring using the Comet assay. Mutat Res 2009, 681:93-109.
79. Vanderwolf C.H. The electrocorticogram in relation to physiology and behavior: a new analysis. Electroencephalogr Clin Neurophysiol 1992, 82:165-175.
80. Wheelock C.E., Phillips B.M., Anderson B.S., Miller J.L., Miller M.J., Hammock B.D. Applications of carboxylesterase activity in environmental monitoring and toxicity identification evaluations (TIEs). Rev Environ Contam Toxicol 2008, 195:117-178.
81. WHO Data Sheets on Pesticides No. 18 1975, IPCS INCHEM.
82. Wurpel J.N., Hirt P.C., Bidanset J.H. Amygdala kindling in immature rats: proconvulsant effect of the organophosphate insecticide-chlorpyrifos. Neurotoxicology 1993, 14:429-436.
83. Yamamoto K.I., Domino E.F. Cholinergic agonist-antagonist interactions on neocortical and limbic EEG activation. Int J Neuropharmacol 1967, 6:357-373.