Stress and Combined Exposure to Low Doses of Pyridostigmine Bromide, DEET, and Permethrin Produce Neurochemical and Neuropathological Alterations in Cerebral Cortex, Hippocampus, and Cerebellum

REFERENCES

• Abdel-Rahman , A. A. , Shetty , A. K. and Abou-Donia , M. B. 2001 . Subchronic dermal application of N,N-diethyl m-toluamide (DEET) and permethrin to adult rats, alone or in combination, causes diffuse neuronal cell death and cytoskeletal abnormalities in the cerebral cortex and the hippocampus, and Purkinje neuron loss in the cerebellum . Exp. Neurol. , 172 : 153 – 171 .
   PubMed Web of Science ®Google Scholar
• Abdel-Rahman , A. A. , Shetty , A. K. and Abou-Donia , M. B. 2002 . Disruption of blood brain barrier and neuronal cell death in cingulate cortex, dentate gyrus, thalamus, and hypothalamus in a rat model Gulf War syndrome . Neurobiol. Dis. , 10 : 306 – 326 .
   PubMed Web of Science ®Google Scholar
• Abou-Donia , M. B. , Wilmarth , K. R. , Jensen , K. F. , Oehme , F. W. and Kurt , T. L. 1996 . Neurotoxicity resulting from coexposure to pyridostigmine bromide, DEET, and permethrin: Implications of Gulf War chemical exposures . J. Toxicol. Environ. Health , 48 : 35 – 56 .
   PubMed Web of Science ®Google Scholar
• Abou-Donia , M. B. , Goldstein , L. B. , Bullman , S. , Jones , K. H. , Herrick , E. A. , Abdel-Rahman , A. A. and Khan , W. A. 2001a . Effect of daily dermal application of DEET and permethrin, alone or in combination, on sensorimotor performance, blood–brain barrier and blood–testis barrier in rats . J. Toxicol. Environ. Health A , 62 : 101 – 119 .
   Web of Science ®Google Scholar
• Abou-Donia , M. B. , Goldstein , L. B. , Jones , K. H. , Abdel-Rahman , A. A. , Damodaran , T. V. , Dechkovskaia , A. M. , Bullman , S. L. , Amir , B. E. and Khan , W. A. 2001b . Locomotor and sensorimotor performance deficit in rats following exposure to pyridostigmine bromide, DEET, and permethrin, alone and in combination . Toxicol. Sci. , 60 : 305 – 314 .
   PubMed Web of Science ®Google Scholar
• Abou-Donia. , M. B. , El-Masry , E. and Abu-Qare , A. W. 2001c . “ Metabolism and toxicokinetics of xenobiotics ” . In CRC handbook of toxicology , 2nd , Edited by: Derelanko , M. J. and Hollinger , M. A. 752 – 821 . Boca Raton, FL : CRC Press .
   Google Scholar
• Abou-Donia , M. B. , Suliman , H. B. , Khan , W. A. and Abdel-Rahman , A. A. 2003 . Testicular germ-cell apoptosis in stressed rat following combined exposure to pyridostigmine bromide, N,N-diethyl m-toluamide (DEET), and permethrin . J. Toxicol. Environ. Health A , 66 : 57 – 73 .
   PubMed Web of Science ®Google Scholar
• Abu-Qare , A. W. and Abou-Donia , M. B. 2000 . Increased 8-hydroxy-2′-deoxyguanosine, a biomarker of oxidative DNA damage in rat urine following a single dermal dose of DEET (N,N-diethyl-m-toluamide), and permethrin alone and in combination . Toxicol. Lett. , 117 : 151 – 160 .
   PubMed Web of Science ®Google Scholar
• Abu-Qare , A. W. and Abou-Donia , M. B. 2001a . Combined exposure to DEET (N,N-diethyl-m-toluamide) and permethrin induced release of rat brain mitochondrial cytochrome c . J. Toxicol. Environ. Health , 63 : 243 – 252 .
   PubMed Web of Science ®Google Scholar
• Abu-Qare , A. W. and Abou-Donia , M. B. 2001b . : Induction of urinary excretion of 3-nitrotyrosine, a marker of oxidative stress, following administration of pyridostigmine bromide, DEET (N,N-diethyl-m-toluamide), and permethrin alone, and in combination in rats . Toxicol. Lett. , 121 : 127 – 134 .
   PubMed Web of Science ®Google Scholar
• Adachi , S. , Kawamura , K. and Takemoto , K. 1993 . Oxidative damage of nuclear DNA in liver of rats exposed to psychological stress . Cancer Res. , 53 : 4153 – 4155 .
   PubMed Web of Science ®Google Scholar
• Bakry , N. M. , El-Rashidy , A. H. , Eldefrawi , A. T. and Eldefrawi , M. E. 1988 . Direct actions of organophosphate anticholinesterases on nicotinic and muscarinic acetylcholine receptors . J. Biochem. Toxicol. , 3 : 21 – 32 .
   PubMedGoogle Scholar
• Balk , J. , Leaver , C. J. and McCabe , P. F. 1999 . Translocation of cytochrome c from the mitochondria to the cytosol occurs during heat-induced programmed cell death in cucumber plants . FEBS Lett. , 463 : 151 – 154 .
   PubMed Web of Science ®Google Scholar
• Blick , D. W. , Kerenyi , S. Z. , Miller , S. , Murphy , M. R. , Brown , G. C. and Hartgraves , S. L. 1991 . Behavioral toxicity of anticholinesterases in primates; Chronic pyridostigmine and soman interactions . Pharmacol. Biochem. Behav. , 38 : 527 – 532 .
   PubMed Web of Science ®Google Scholar
• Bryan , R. M. 1990 . Cerebral blood flow and energy metabolism during stress . Am. J. Physiol , : H269 – H280 .
   Google Scholar
• Butterworth , R. F. 1996 . The neurobiology of hepatic encephalopathy . Semin. Liver Dis. , 16 : 235 – 244 .
   PubMed Web of Science ®Google Scholar
• Casida , J. E. , Gammon , D. W. , Glickman , A. H. and Lawrence , L. J. 1983 . Mechanisms of selective action of pyrethroid insecticides . Annu. Rev. Pharmacol. Toxicol , 23 : 413 – 438 .
   PubMed Web of Science ®Google Scholar
• Chaney , L. A. , Wineman , R. W. , Rockhold , R. W. and Hume , A. S. 2000 . Acute effects of an insect repellent, N,N-diethyl-m-toluamide, on cholinesterase inhibition induced by pyridostigmme bromide in rats . Toxicol. Appl. Pharmacol. , 165 : 107 – 114 .
   PubMed Web of Science ®Google Scholar
• Chauhan , N. B. , Sabri , M. I. and Spencer , P. S. 1991 . Acrylamide alters the distribution of MAP1 and MAP2 immunoreactivity in rat brain . Soc. Neurosci. Abstr. , 17 : 1465
   Google Scholar
• Chauhan , N. B. , Sabri , M. I. and Spencer , P. S. 1992 . Maps immunoreactivity in rat striatum is decreased by acrylamide . Toxicologist , 12 : 193
   Google Scholar
• Chauhan , N. B. , Spencer , P. S. and Sabri , M. I. 1993 . Acrylamide-induced depletion of microtubule-associ-ated proteins (MAP1 and MAP2) in the rat extrapyramidal system . Brain Res. , 602 : 111 – 118 .
   PubMed Web of Science ®Google Scholar
• Corcoran , G. B. , Mitchell , J. R. , Vaishnav , Y. N. and Horning , E. C. 1980 . Evidence that acetaminophen and N-hydroxyacetaminophen form a common arylating intermediate, N-acetyl-p-benzoquinoneimine . Mol. Pharmacol. , 18 : 536 – 542 .
   PubMed Web of Science ®Google Scholar
• Edwards , D. L. and Johnson , C. E. 1987 . Insect repellent-induced toxic encephalopathy in a child . Clin. Pharmacol. , 6 : 496 – 498 .
   PubMedGoogle Scholar
• Eiermann , B. , Sommer , N. , Winne , D. , Schumm , F. , Maier , U. and Breyer-Pfaff , U. 1993 . Renal clearance of pyridostigmine in myasthenic patients and volunteers under the influence of ranitidine and pirenzepine . Xenobiotica. , 23 : 1263 – 1275 .
   PubMed Web of Science ®Google Scholar
• Ellman , G. L. , Courtney , K. D. , Andres , V. and Featherstone , R. M. 1961 . A new and rapid colorimetric determination of acetylcholinesterase activity . Biochem. pharmacol. , 7 : 88 – 95 .
   PubMed Web of Science ®Google Scholar
• Friedman , A. , Kaufer , D. , Shemer , J. , Hendler , I. , Soreq , H. and Tur-Kaspa , I. 1996 . Pyridostigmine brain penetration under stress enhances neuronal excitability and induces early immediate transcriptional response . Nat. Med. , 2 : 1382 – 1385 .
   PubMed Web of Science ®Google Scholar
• Gaughan , L. C. , Ackerman , M. E. , Unai , T. and Casida , J. E. 1978 . Distribution and metabolism of trans-and cis-permethrin in lactating Jersey cows . J. Agric. Food Chem. , 26 : 613 – 618 .
   PubMed Web of Science ®Google Scholar
• Grauer , E. , Alkalai , D. , Kapon , J. , Cohen , G. and Raveh , L. 2000 . Stress does not enable pyridostigmine to inhibit brain cholinesterase after parenteral administration . Toxicol. Appl. Pharmacol. , 164 : 301 – 304 .
   PubMed Web of Science ®Google Scholar
• Grauer , E. , Ben Nathan , D. , Lustig , S. , Kobiler , D. , Kapon , J. and Daneberg , H. D. 2001 . Viral neuroinvasion as a marker for BBB integrity following exposure to cholinesterase inhibitors . Life Sci. , 68 : 985 – 990 .
   PubMed Web of Science ®Google Scholar
• Gryboski , J. , Weinstein , D. and Ordway , N. K. 1961 . Toxic encephalopathy apparently related to the use of an insect repellent . N. Engl. J. Med. , 264 : 289 – 291 .
   PubMed Web of Science ®Google Scholar
• Halliwell , B. 1992 . Reactive oxygen species and the central nervous system . J. Neurochem. , 59 : 1609 – 1623 .
   PubMed Web of Science ®Google Scholar
• Hsu , S. M. , Raine , L. and Fanger , H. 1981 . The use of avidin-biotin-peroxidase complex (ABC) in immunoperoxidase techniques: A comparison between ABC and unlabelled antibody (PAP) procedures . J. Histochem. Cytochem. , 29 : 577 – 580 .
   PubMed Web of Science ®Google Scholar
• Huff , R. A. , Corcoran , J. J. , Anderson , J. K. and Abou-Donia , M. B. 1994 . Chlorpyrifos oxon binds directly to muscarinic receptors and inhibitors cAMP accumulation in rat striatum . J. Pharmacol. Exp. Ther. , 269 : 329 – 335 .
   PubMed Web of Science ®Google Scholar
• Institute of Medicine . l995 . Health consequences of service during the Persian Gulf War: Initial findings and recommendation for immediate action , Washington, DC : National Academy Press .
   Google Scholar
• Johnson , G. V. and Jope , R. S. 1992 . The role of microtubule-associated protein2 (MAP-2) in neuronal growth, plasticity, and degeneration . J. Neurosci. Res. , 23 : 505 – 512 .
   Google Scholar
• Kaufmann , W. E. and Moser , H. W. 2000 . Dendritic anomalies in disorders associated with mental retardation . Cerebral Cortex , 10 : 981 – 991 .
   PubMed Web of Science ®Google Scholar
• Kaufmann , W. E. , Theda , C. , Naidu , S. , Watkins , P. A. , Moser , A. B. and Moser , H. W. 1996 . Neuronal migration abnormality in peroxisomal bifunctional enzyme defect . Ann. Neurol. , 39 : 268 – 271 .
   PubMed Web of Science ®Google Scholar
• Keeler , J. R. and Hurst , C. G. 1991 . Pyridostigmine used as nerve agent pretreatment under wartime conditions . J. Am. Med. Assoc. , 266 : 693 – 695 .
   PubMed Web of Science ®Google Scholar
• Kitagawa , K. , Matsumoto , M. , Niinobe , M. , Mikoshiba , K. , Hata , R. , Ueda , H. , Handa , N. , Fukunaga , R. , Isaka , Y. and Kimura , K. 1989 . Microtuble-associated protein 2 as a sensitive marker for cerebral ischemic damage—Immunohistochemical investigation of dendritic damage . Neuroscience. , 31 : 401 – 411 .
   PubMed Web of Science ®Google Scholar
• Konstandi , M. , Marselos , M. , Radon-Camus , A. M. , Johnson , E. and Lang , M. A. 1998 . The role of stress in the regulation of drug metabolizing enzymes in mice . Eur. J. Drug Metab. Pharmacokinet. , 23 : 483 – 490 .
   PubMed Web of Science ®Google Scholar
• Lallement , G. , Foquin , A. , Baubichon , D. , Burckhart , M. F. , Carpentier , D. and Canini , F. 1998 . Heat stress, even extreme, does not induce penetration of pyridostigmine into the brain of guinea pigs . Neurotoxicology , 19 : 759 – 766 .
   PubMed Web of Science ®Google Scholar
• Lima , E. Jr. , Knopfholz , J. and Menini , C. M. 2002 . Stress during ACLS courses: Is it important for learning skills? . Arq. Bras. Cardiol. , 79 : 589 – 592 .
   PubMedGoogle Scholar
• Li , L. , Guanasekar , P. G. , Borowitz , J. L. and Isom , G. E. 2000 . Muscarinic receptor-mediated pyridostigmineinduced neuronal apoptosis . Neurotoxicology , 21 : 541 – 552 .
   PubMed Web of Science ®Google Scholar
• Li , L. , Shou , Y. , Borowitz , J. L. and Isom , G. E. 2001 . Reactive oxygen species mediate pyridostigmineinduced neuronal apoptosis: Involvement of muscarinic and NMDA receptor . Toxicol. Appl. Pharmacol. , 177 : 17 – 25 .
   PubMed Web of Science ®Google Scholar
• Madrigal , J. L. , Moro , M. A. , Lizasoain , I. , Lorenzo , P. , Castrillo , A. , Bosca , L. and Leza , J. C. 2001 . Inducible nitric oxide synthase expression in brain cortex after acute restraint stress is regulated by nuclear factor kappaB-mediated mechanisms . J. Neurochem. , 76 : 532 – 538 .
   PubMed Web of Science ®Google Scholar
• Martinou , J. C. , Desagher , S. and Antonsson , B. 2000 . Cytochrome c release from mitochondria: All or nothing . Nature Cell Biol. , 3 : E41 – E43 .
   Google Scholar
• Moghaddam , B. , Boliano , M. L. , Stein- Behrens , B. and Sapolsky , R. 1994 . Glucocorticords mediate the stress-induced extracellular accumulation of glutamate . Brain Res. , 655 : 730 – 735 .
   Web of Science ®Google Scholar
• Narahashi , T. 1985 . Nerve membrane ionic channels as the primary target of pyrethroid . Neurotoxicology , 6 : 3 – 22 .
   PubMed Web of Science ®Google Scholar
• Norenberg , M. D. 1987 . The role of astrocytes in hepatic encephalopathy . Neurochem. Pathol. , 6 : 13 – 33 .
   PubMedGoogle Scholar
• Pollack , G. M. , Browne , J. L. , Marton , J. and Haberer , L. J. 1991 . Chronic stress impairs oxidative metabolism and hepatic excretion of model xenobiotic substrates in rat . Drug Metab Dispos. , 19 : 130 – 134 .
   PubMed Web of Science ®Google Scholar
• Rao , G. V. and Rao , K. S. 1995 . Modulation in acetylcholinesterase of rat brain by pyrethroids in vivo and in vitro study . J. Neurochem , 6S : 2259 – 2275 .
   Google Scholar
• Robbins , P. J. and Cherniack , M. G. 1986 . Review of the biodistribution and toxicity of the insect repellant N,N-diethyl-m-toluamide (DEET) . J. Toxicol. Environ. Health , 18 : 503 – 525 .
   PubMed Web of Science ®Google Scholar
• Roland , E. H. , Jan , J. E. and Rigg , J. M. 1985 . Toxic encephalopathy in a child after brief exposure to insect repellents . Can. Med. Assoc. J. , 132 : 155 – 156 .
   PubMed Web of Science ®Google Scholar
• Saatman , K. E. , Bareyre , F. M. , Grady , M. S. and McIntosh , T. K. 200l . Acute cytoskeletal alterations and cell death induced by experimental brain injury are attenuated by magnesium treatment and exacerbated by magnesium deficiency . J. Neuropathol. Exp. Neurol , 60 : 183 – 194 .
   PubMed Web of Science ®Google Scholar
• Selim , S. , Hartnagel , R. E. Jr. , Osimitz , T. G. , Gabriel , K. L. and Schoenig , G. P. 1995 . Absorption, metabolism and excretion of N, N-diethyl-m-toluamide following dermal application to human volunteers . Fundam. Appl. Toxicol. , 25 : 95 – 100 .
   PubMedGoogle Scholar
• Sharma , H. S. , Cervos-Navarro , J. and Dey , P. K. 1991 . Increased blood–brain barrier permeability following acute short-term swimming exercise in conscious normotensive young rats . Neurosci. Res. , 10 : 211 – 221 .
   PubMed Web of Science ®Google Scholar
• Slotkin , T. A. , Epps , I. A. , Stenger , M. L. , Sawyer , K. J. and Seidler , F. J. 1999 . Cholinergic receptors in heart and brainstem of rats exposed to nicotine during development: Implications for hypoxia tolerance and prenatal mortality . Brain Res. Dev. Brain Res. , 113 : 1 – 12 .
   PubMedGoogle Scholar
• Smith , P. K. , Krohn , R. I. , Hermanson , G. T. , Mallia , A. K. , Gartner , F. H. , Provenzano , M. D. , Fujimoto , E. K. , Goeke , N. M. , Olson , B. J. and Klenk , D. C. 1985 . Measurement of protein using bicinchonic acid . Anal. Biochem. , 150 : 76 – 85 .
   PubMed Web of Science ®Google Scholar
• Telang , F. W. , Ding , Y. S. , Volkow , N. D. , Molina , P. E. and Gatley , S. J. 1999 . Failure of [14C]-pyridostig-mine to cross the blood–brain barrier in stressed mice . Nucl. Med. Biol. , 26 : 249 – 250 .
   PubMedGoogle Scholar
• Vasterling , J. J. , Brailey , K. , Constans , J. I. , Borges , A. and Sutker , P. B. 1997 . Assessment of intellectual resources in Gulf War veterans: Relationship to PTSD . Assessment , 4 : 51 – 59 .
   Web of Science ®Google Scholar
• Verschoyle , R. D. , Brown , A. W. , Nolan , C. , Ray , D. E. and Lister , T. 1992 . A comparison of the acute toxicity, neuropathology, and electrophysiology of N,N-dimethyl-m-toluamide and N,N-diethyl 2,2-diphenylacetamide in rats . Fundam. Appl. Toxicol. , 18 : 79 – 88 .
   PubMedGoogle Scholar
• Ward , T. R. , Ferris , D. J. , Tilson , H. A. and Mundy , W. R. 1993 . Correlation of the anticholinesterase activity of a series of organophosphates with their ability to compete with agonist binding to muscarinic receptors . Toxicol. Appl. Pharmacol. , 122 : 300 – 307 .
   PubMed Web of Science ®Google Scholar
• Watanabe , Y. , Gould , E. , Cameron , H. A. , Daniels , D. C. and McEwen , B. S. 1992 . Phenytoin prevents stress- and corticosterone-induced atrophy of CA3 pyramidal neurons . Hippocampus , 2 : 431 – 436 .
   PubMed Web of Science ®Google Scholar
• Weiner , L. , Kreimer , D. , Roth , E. and Silman , I. 1994 . Oxidative stress transforms acetylcholinesterase to a molten-globule-like state . Biochem. Biophys. Res. Commun. , 189 : 915 – 922 .
   Google Scholar
• White , R. F. , Proctor , S. P. , Heeren , T. , Wolfe , J. , Krengel , M. , Vasterling , J. , Lindem , K. , Heaton , K. , Sutker , P. B. and Ozonoff , D. M. 2001 . Neuropsychological function in Gulf War veterans: Relationships to self-reported toxicant exposures . Am. J. Ind. Med. , 40 : 42 – 54 .
   PubMed Web of Science ®Google Scholar