Cognitive and histological disturbances after chlorpyrifos exposure and chronic Aβ(1-42) infusions in Wistar rats

NeuroToxicology

Volumn 32, Issue 6, 2011, Pages 836-844

  Ruiz Muñoz, Ana M ^a   Nieto Escamez, Francisco A ^a   Aznar, Susana ^c   Colomina, María T ^b   Sanchez Santed, Fernando ^a  

^a UNIVERSITY OF ALMERÍA   (Spain)

^b UNIVERSITAT ROVIRA I VIRGILI   (Spain)

^c Mental Health Services CPH   (Denmark)

Author keywords

Beta amyloid; Chlorpyrifos; Flexibility; Learning; MAPs; Memory

Indexed keywords

AMYLOID BETA PROTEIN[1-42]; CHLORPYRIFOS; MICROTUBULE ASSOCIATED PROTEIN 1; MICROTUBULE ASSOCIATED PROTEIN 1A; MICROTUBULE ASSOCIATED PROTEIN 2; UNCLASSIFIED DRUG;

ACUTE TOXICITY; ANIMAL BEHAVIOR; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BRAIN REGION; BRAIN TISSUE; COGNITIVE DEFECT; CONTROLLED STUDY; HIPPOCAMPUS; HISTOPATHOLOGY; IMMUNOREACTIVITY; LEARNING CURVE; LONG TERM EXPOSURE; MALE; MAZE TEST; NEUROPATHOLOGY; NONHUMAN; PREFRONTAL CORTEX; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN METABOLISM; RAT; REDUCTION KINETICS; SPATIAL MEMORY; TASK PERFORMANCE;

AMYLOID BETA-PEPTIDES; ANIMALS; BEHAVIOR, ANIMAL; CHLORPYRIFOS; COGNITION; HIPPOCAMPUS; IMMUNOHISTOCHEMISTRY; INFUSIONS, INTRAVENTRICULAR; INJECTIONS, SUBCUTANEOUS; INSECTICIDES; MALE; MAZE LEARNING; MEMORY; MICROTUBULE-ASSOCIATED PROTEINS; MOTOR ACTIVITY; PEPTIDE FRAGMENTS; PREFRONTAL CORTEX; RATS; RATS, WISTAR; SWIMMING;

ANIMALIA; RATTUS NORVEGICUS;

EID: 80055075098     PISSN: 0161813X     EISSN: 18729711     Source Type: Journal    
DOI: 10.1016/j.neuro.2011.05.014     Document Type: Article

References (47)

1. Abdollahi M., Rainba A., Shadnia S., Nikfar S., Rezaie A. Pesticide and oxidative stress: a review. Med Sci Monitor 2004, 10:141-147.
2. Alonso A.D., Grundke-Iqbal I., Barra H.S., Iqbal K. Abnormal phosphorylation of tau and the mechanism of Alzheimer neurofibrillary degeneration: sequestration of microtubule-associated proteins 1 and 2 and the disassembly of microtubules by the abnormal tau. Proc Natl Acad Sci USA 1997, 94:298-303.
3. Avila J., Lim F., Moreno F., Belmonte C., Cuello A.C. Tau function and dysfunction in neurons: its role in neurodegenerative disorders. Mol Neurobiol 2002, 25:213-231.
4. Baldi I., Lebailly P., Mohammed-Brahim B., Letenneur L., Dartigues J.F., Brochard P. Neurodegenerative diseases and exposure to pesticides in the elderly. Am J Epidemiol 2003, 157:409-414.
5. Borchelt D.R., Ratovitski T., van Lare J., Lee M.K., Gonzales V., Jenkins N.A., et al. Accelerated amyloid deposition in the brains of transgenic mice coexpressing mutant presenilin 1 and amyloid precursor proteins. Neuron 1997, 19:939-945.
6. Butler D., Bendiske J., Michaelis M.L., Karanian D.A., Bahr B.A. Microtubule-stabilizing agent prevents protein accumulation-induced loss of synaptic markers. Eur J Pharmacol 2007, 562:20-27.
7. Cañadas F., Cardona D., Dávila E., Sánchez-Santed F. Long-term neurotoxicity of chlorpyrifos: spatial learning impairment on repeated acquisition in a water maze. Toxicol Sci 2005, 85:944-951.
8. Cardona D., López-Grancha M., López-Crespo G., Nieto-Escamez F., Sánchez-Santed F., Flores P. Vulnerability of long-term neurotoxicity of chlorpyrifos: effect on schedule-induced polydipsia and a delay discounting task. Psychopharmacology (Berl) 2006, 189:47-57.
9. de Bruin J.P., Sánchez-Santed F., Heinsbroek R.P., Donker A., Postmes P. A behavioural analysis of rats with damage to the medial prefrontal cortex using the Morris water maze: evidence for behavioural flexibility, but not for impaired spatial navigation. Brain Res 1994, 652:323-333.
10. Dehmelt L., Halpain S. The MAP2/Tau family of microtubule-associated proteins. Genome Biol 2005, 6:204.
11. Fifre A., Sponne I., Koziel V., Kriem B., Yen Potin F.T., Bihain B.E., et al. Microtubule-associated protein MAP1A, MAP1B, and MAP2 proteolysis during soluble amyloid beta-peptide-induced neuronal apoptosis. Synergistic involvement of calpain and caspase-3. J Biol Chem 2006, 281:229-240.
12. Fink J.K., Jones S.M., Esposito C., Wilkowski J. Human microtubule-associated protein 1a (MAP1A) gene: genomic organization, cDNA sequence, and developmental- and tissue-specific expression. Genomics 1996, 35:577-585.
13. Gearhart D.A., Sickles D.W., Buccafusco J.J., Prendergast M.A., Terry A.V. Chlorpyrifos, chlorpyrifos-oxon, and diisopropylfluorophosphate inhibit kinesin-dependent microtubule motility. Toxicol Appl Pharmacol 2007, 218:20-29.
14. Gevorkian G., Gonzalez-Noriega A., Acero G., Ordoñez J., Michalak C., Munguia M.E., et al. Amyloid-beta peptide binds to microtubule-associated protein 1B (MAP1B). Neurochem Int 2008, 52:1030-1036.
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. Grigoryan H., Schopfer L.M., Peeples E.S., Duysen E.G., Grigoryan M., Thompson C.M., et al. Mass spectrometry identifies multiple organophosphorylated sites on tubulin. Toxicol Appl Pharmacol 2009, 240:149-158.
17. Hayden K.M., Norton M.C., Darcey D., Ostbye T., Zandi P.P., Breitner J.C., et al. Occupational exposure to pesticides increases the risk of incident AD: the Cache County study. Neurology 2010, 74:1524-1530.
18. Iqbal K., Liu F., Gong C.-X., Alonso A., Grundke-Iqbal I. Mechanisms of tau-induced neurodegeneration. Acta Neuropathol 2009, 118:53-69.
19. Jankowsky J.L., Fadale D.J., Anderson J., Xu G.M., Gonzales V., Jenkins N.A., et al. Mutant presenilins specifically elevate the levels of the 42 residue beta-amyloid peptide in vivo: evidence for augmentation of a 42-specific gamma secretase. Hum Mol Genet 2004, 13:159-170.
20. Jaworski J., Kapitein L.C., Gouveia S.M., Dortland B.R., Wulf P.S., Grigoriev I., et al. Dynamic microtubules regulate dendritic spine morphology and synaptic plasticity. Neuron 2009, 61:85-100.
21. Jiang W., Duysen E.G., Hansen H., Shlyakhtenko L., Schopfer L.M., Lockridge O. Mice treated with chlorpyrifos or chlorpyrifos oxon have organophosphorylated tubulin in the brain and disrupted microtubule structures, suggesting a role for tubulin in neurotoxicity associated with exposure to organophosphorus agents. Toxicol Sci 2010, 115:183-193.
22. Kins S., Beyreuther K. Teasing out of the tangles. Nat Med 2006, 12:764-765.
23. López-Crespo G.A., Carvajal F., Flores P., Sánchez-Santed F., Sánchez-Amate M.C. Time course of biochemical and behavioural effects of a single high dose of chlorpyrifos. Neurotoxicology 2007, 28:541-547.
24. Mudher A., Lovestone S. Alzheimer's disease-do tauists and baptists finally shake hands?. Trends Neurosci 2002, 25:22-26.
25. Nakagawa Y., Kawashima T., Yamada T., Harano M., Monji A., Yuzuriha T., et al. Aluminium chloride does not facilitate deposition of human synthetic amyloid beta 1-42 peptide in the rat ventricular system of a short-term infusion model. Neuropathology 2005, 25:195-200.
26. Nakagawa Y., Yuzuriha T., Iwaki T. Active clearance of human amyloid beta 1-42 peptide aggregates from the rat ventricular system. Neuropathology 2004, 4:194-200.
27. Nakamura S., Murayama N., Noshita T., Annoura H., Ohno T. Progressive brain dysfunction following intracerebroventricular infusion of beta (1-42)-amyloid peptide. Brain Res 2001, 912:128-136.
28. Nyakas C., Granic I., Halmy L.G., Banerjee P., Luiten P.G. The basal forebrain cholinergic system in aging and dementia. Rescuing cholinergic neurons from neurotoxic amyloid-β42 with memantine. Behav Brain Res 2010, May 27, 2010 [Epub ahead of print].
29. Paxinos G., Watson C. The Rat Brain in Stereotaxic Coordinates 1998, Academic Press, San Diego, CA.
30. Peng Y., Xing C., Xu S., Lemere C.A., Chen G., Liu B., et al. L-3-n-butylphthalide improves cognitive impairment induced by intracerebroventricular infusion of amyloid-beta peptide in rats. Eur J Pharmacol 2009, 621:38-45.
31. Penzes P., Srivastava D.P., Woolfrey K.M. Not just actin? A role for dynamic microtubules in dendritic spines. Neuron 2009, 61:3-5.
32. Pepeu G., Casamenti F., Pedata F., Bartolini L. Usefulness, constraints and limits of animal investigations in the study of aging brain and senile dementia. Modem Trends in Aging Research Y 1986, 331-334. John Libbey, London. B. Courtois, B. Faucheux, D.L. Forette, J.A. Knook, Treton (Eds.).
33. Perez J.L., Carrero I., Gonzalo P., Arevalo-Serrano J., Sanz-Anquela J.M., Ortega J., et al. Soluble oligomeric forms of beta-amyloid (Abeta) peptide stimulate Abeta production via astrogliosis in the rat brain. Exp Neurol 2010, 223:410-421.
34. Pope C.N., Chakraborti T.K., Chapman M.L., Farrar J.D., Arthun D. Comparison of in vivo cholinesterase inhibition in neonatal and adult rats by three organophosphorothioate insecticides. Toxicology 1991, 168:51-61.
35. Praprotnik D., Smith M.A., Richey P.L., Vinters H.V., Perry G. Filament heterogeneity within the dystrophic neurites of senile plaques suggest blockade of fast axonal transport in Alzheimer's disease. Acta Neuropathol 1996, 91:226-235.
36. Prendergast M.A., Self R.L., Smith K.J., Ghayoumi L., Mullins M.M., Butler T.R., et al. Microtubule-associated targets in chlorpyrifos oxon hippocampal neurotoxicity. Neuroscience 2007, 146:330-339.
37. Roldán-Tapia L., Nieto-Escamez F.A., del Aguila E.M., Laynez F., Parron T., Sanchez-Santed F. Neuropsychological sequelae from acute poisoning and long-term exposure to carbamate and organophosphate pesticides. Neurotoxicol Teratol 2006, 28:694-703.
38. Roldán-Tapia L., Parrón T., Sánchez-Santed F. Neuropsychological effects of long-term exposure to organophosphate pesticides. Neurotoxicol Teratol 2005, 27:259-266.
39. Salazar JG, Ribes D, Cabré M, Domingo JL, Sanchez-Santed F, Colomina MT. Amyloid Beta peptide levels increase in brain of AβPP swedish mice after exposure to chlorpyrifos. Current Alzheimer Research 2011, in press.
40. Saito K., Elce J.S., Hamos J.E., Nixon R.A. Widespread activation of calcium-activated neutral proteinase (calpain) in the brain in Alzheimer disease: a potential molecular basis for neuronal degeneration. Proc Natl Acad Sci USA 1993, 90:2628-2632.
41. Sánchez-Santed F., Cañadas F., Flores P., López-Grancha M., Cardona D. Long-term functional neurotoxicity of paraoxon and chlorpyrifos: behavioural and pharmacological evidence. Neurotoxicol Teratol 2004, 26:305-317.
42. Santibáñez M., Bolumar F., García A. Occupational risk factors in Alzheimer's disease: a review assessing the quality of published epidemiological studies. Occup Environ Med 2007, 64:723-732.
43. Sponne I., Fifre A., Drouet B., Klein C., Koziel V., Pinçon-Raymond M., et al. Apoptotic neuronal cell death induced by the non-fibrillar amyloid-beta peptide proceeds through an early reactive oxygen species-dependent cytoskeleton perturbation. J Biol Chem 2003, 278:3437-3445.
44. Stephan A., Laroche S., Davis S. Generation of aggregated beta-amyloid in the rat hippocampus impairs synaptic transmission and plasticity and causes memory deficits. J Neurosci 2001, 21:5703-5714.
45. Takata K., Kitamura Y., Umeki M., Tsuchiya D., Kakimura J., Taniguchi T., et al. Possible involvement of small oligomers of amyloid-beta peptides in 15-deoxy-delta 12,14 prostaglandin J2-sensitive microglial activation. J Pharmacol Sci 2003, 91330-91333.
46. Terry A.V., 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.
47. Zaja-Milatovic S., Gupta R.C., Aschner M., Milatovic D. Protection of DFP-induced oxidative damage and neurodegeneration by antioxidants and NMDA receptor antagonist. Toxicol Appl Pharmacol 2009, 240:124-131.