Pesticides induce spatial memory deficits with synaptic impairments and an imbalanced tau phosphorylation in rats

Journal of Alzheimer's Disease

Volumn 30, Issue 3, 2012, Pages 585-594

  Chen, Ning Ning ^a   Luo, Dan Ju ^a   Yao, Xiu Qing ^a   Yu, Cong ^a   Wang, Yi ^a   Wang, Qun ^a   Wang, Jian Zhi ^a   Liu, Gong Ping ^a  

^a HUAZHONG UNIVERSITY OF SCIENCE AND TECHNOLOGY   (China)

Author keywords

Alzheimer's disease; glycogen synthase kinase 3 ; pesticides; protein phosphatase 2A; tau

Indexed keywords

CARBOFURAN; DELTAMETHRIN; GLYCOGEN SYNTHASE KINASE 3BETA; N METHYL DEXTRO ASPARTIC ACID RECEPTOR 1; PESTICIDE; PHOSPHOPROTEIN PHOSPHATASE 2A; SYNAPSIN I; SYNAPTOPHYSIN; TAU PROTEIN;

AMNESIA; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BRAIN CORTEX; HIPPOCAMPUS; MALE; NONHUMAN; PRIORITY JOURNAL; PROTEIN PHOSPHORYLATION; RAT; RISK FACTOR; SPATIAL MEMORY DEFICIT;

EID: 84862849047     PISSN: 13872877     EISSN: 18758908     Source Type: Journal    
DOI: 10.3233/JAD-2012-111946     Document Type: Article

References (55)

1. SmallGW, Rabins PV, Barry PP, Buckholtz NS, DeKosky ST, Ferris SH, Finkel SI, Gwyther LP, Khachaturian ZS, Lebowitz BD, McRae TD, Morris JC, Oakley F, Schneider LS, Streim JE, Sunderland T, Teri LA, Tune LE (1997) Diagnosis and treatment of Alzheimer disease and related disorders. Consensus statement of the American Association for Geriatric Psychiatry, the Alzheimer's Association, and the American Geriatrics Society. JAMA 278, 1363-1371.
2. Fratiglioni L, De Ronchi D, Ag̈uero-Torres H (1999) Worldwide prevalence and incidence of dementia. Drugs Aging 15, 365-375.
3. Lee VM (2001) Tauists and beta-aptists united -well almost! Science 293, 1446-1447.
4. Dosunmu R, Wu J, Basha MR, Zawia NH (2007) Environmental and dietary risk factors in Alzheimer's disease. Expert Rev Neurother 7, 887-900.
5. Migliore L, Copped̀e F (2009) Environmental-induced oxidative stress in neurodegenerative disorders and aging. Mutat Res 674, 73-84.
6. Migliore L, Copped̀e F (2009) Genetics, environmental factors and the emerging role of epigenetics in neurodegenerative diseases. Mutat Res 667, 82-97.
7. Wolansky MJ, Harrill JA (2008) Neurobehavioral toxicology of pyrethroid insecticides in adult animals: A critical review. Neurotoxicol Teratol 30, 55-78.
8. Henderson AS (1988) The risk factors for Alzheimer's disease: A review and a hypothesis. Acta Psychiatr Scand 78, 257-275.
9. Parŕon T, Requena M, Herńandez AF, Alarćon R (2011) Association between environmental exposure to pesticides and neurodegenerative diseases. Toxicol Appl Pharmacol 256, 379-385.
10. Baldi I, Lebailly P, Mohammed-Brahim B, Letenneur L, Dartigues JF, Brochard P (2003) Neurodegenerative diseases and exposure to pesticides in the elderly. Am J Epidemiol 157, 409-414.
11. Casida JE, Gammon DW, Glickman AH, Lawrence LJ (1983) Mechanisms of selective action of pyrethroid insecticides. Annu Rev Pharmacol Toxicol 23, 413-438.
12. Soderlund DM, Clark JM, Sheets LP, Mullin LS, Piccirillo VJ, Sargent D, Stevens JT, Weiner ML (2002) Mechanisms of pyrethroid neurotoxicity: Implications for cumulative risk assessment. Toxicology 171, 3-59.
13. Soderlund DM, Bloomquist JR (1989) Neurotoxic actions of pyrethroid insecticides. Annu Rev Entomol 34, 77-96.
14. Soderlund DM (1997) Molecular mechanism of insecticide resistance. In: Molecular Mechanisms of Resistance to Agrochemicals, Sjut V, Ed. Springer, Berlin, pp. 21-56.
15. Liu GP, Ma Q, Shi N (2006) Tyrosine hydroxylase as a target for deltamethrin in the nigrostriatal dopaminergic pathway. Biomed Environ Sci 19, 27-34.
16. Liu GP, Shi N (2006) The inhibitory effects of deltamethrin on dopamine biosynthesis in rat PC12 cells. Toxicol Lett 161, 195-199.
17. Senger MR, Rico EP, de Bem Arizi M, Rosemberg DB, Dias RD, Bogo MR, Bonan CD (2005) Carbofuran and malathion inhibit nucleotide hydrolysis in zebrafish (Danio rerio) brain membranes. Toxicology 212, 107-115.
18. Kamboj SS, Kumar V, Kamboj A, Sandhir R (2008) Mitochondrial oxidative stress and dysfunction in rat brain induced by carbofuran exposure. Cell Mol Neurobiol 28, 961-969.
19. Gupta RC (1994) Carbofuran toxicity. J Toxicol Environ Health 43, 383-418.
20. Kamboj A, Kiran R, Sandhir R (2006) Carbofuran-induced neurochemical and neurobehavioral alterations in rats: Attenuation by N-acetylcysteine. Exp Brain Res 170, 567-575.
21. Morris R (1984) Developments of a water-maze procedure for studying spatial learning in the rat. J Neurosci Methods 11, 47-60.
22. Palop JJ, Jones B, Kekonius L, Chin J, Yu GQ, Raber J, Masliah E, Mucke L (2003) Neuronal depletion of calciumdependent proteins in the dentate gyrus is tightly linked to Alzheimer's disease-related cognitive deficits. Proc Natl Acad Sci U S A 100, 9572-9577.
23. Zeng YC, Bongrani S, Bronzetti E, Cadel S, Ricci A, Valsecchi B, Amenta F (1994) Influence of long-term treatment with L-deprenyl on the age-dependent changes in rat brain microanatomy. Mech Ageing Dev 73, 113-126.
24. Gong CX, Lidsky T, Wegiel J, Zuck L, Grundke-Iqbal I, Iqbal K (2005) Phosphorylation of microtubule-associated protein tau is regulated by protein phosphatase 2A in mammalian brain. Implications for neurofibrillary degeneration in Alzheimer's disease. J Biol Chem 275, 5535-5544.
25. Gong CX, Shaikh S,Wang JZ, Zaidi T, Grundke-Iqbal I, Iqbal K(1995) Phosphatase activity toward abnormally phosphorylated tau: Decrease in Alzheimer disease brain. J Neurochem 65, 732-738.
26. Trojanowski JQ, Lee VM (1995) Phosphorylation of paired helical filament tau in Alzheimer's disease neurofibrillary lesions: Focusing on phosphatases. FASEB J 9, 1570-1576.
27. Tian Q,Wang J (2002) Role of serine/threonine protein phosphatase in Alzheimer's disease. Neurosignals 11, 262-269.
28. Bhat RV, Budd Haeberlein SL, Avila J (2004) Glycogen synthase kinase 3: A drug target for CNS therapies. J Neurochem 89, 1313-1317.
29. Cui Z, Wang H, Tan Y, Zaia KA, Zhang S, Tsien JZ (2004) Inducible and reversible NR1 knockout reveals crucial role of the NMDA receptor in preserving remote memories in the brain. Neuron 41, 781-793.
30. Goeldner C, Reiss D, Wichmann J, Meziane H, Kieffer BL, Ouagazzal AM (2008) Nociceptin receptor impairs recognition memory via interaction with NMDA receptordependent mitogen-activated protein kinase/extracellular signal-regulated kinase signaling in the hippocampus. J Neurosci 28, 2190-2198.
31. Sultana R, BanksWA, ButterfieldDA(2010) Decreased levels of PSD95 and two associated proteins and increased levels of BCl2 and caspase 3 in hippocampus from subjects with amnestic mild cognitive impairment: Insights into their potential roles for loss of synapses and memory, accumulation of Abeta, and neurodegeneration in a prodromal stage of Alzheimer's disease. J Neurosci Res 88, 469-477.
32. M̈ussig L, Richlitzki A, R̈ossler R, Eisenhardt D, Menzel R, Leboulle G (2010) Acute disruption of the NMDA receptor subunit NR1 in the honeybee brain selectively impairs memory formation. J Neurosci 30, 7817-7825.
33. Wiedenmann B, FrankeWW(1985) Identification and localization of synaptophysin, an integral membrane glycoprotein of Mr 38,000 characteristic of presynaptic vesicles. Cell 41, 1017-1028.
34. Lambert TJ, Fernandez SM, Frick KM (2005) Different types of environmental enrichment have discrepant effects on spatial memory and synaptophysin levels in female mice. Neurobiol Learn Mem 83, 206-216.
35. Kopec CD, Real E, Kessels HW, Malinow R (2007) GluR1 links structural and functional plasticity at excitatory synapses. J Neurosci 27, 13706-13718.
36. Yang Y, Wang XB, Frerking M, Zhou Q (2008) Delivery of AMPAreceptors to perisynaptic sites precedes the full expression of long-term potentiation. Proc Natl Acad Sci U S A 105, 11388-11393.
37. Slipczuk L, Bekinschtein P, Katche C, Cammarota M, Izquierdo I, Medina JH (2009) BDNF activates mTOR to regulate GluR1 expression required for memory formation. PLoS One 4, e6007.
38. Parker MJ, Zhao S, Bredt DS, Sanes JR, FengG(2004) PSD93 regulates synaptic stability at neuronal cholinergic synapses. J Neurosci 24, 378-388.
39. Kushner SA, Elgersma Y, Murphy GG, Jaarsma D, vanWoerden GM, Hojjati MR, Cui Y, LeBoutillier JC, Marrone DF, Choi ES, De Zeeuw CI, Petit TL, Pozzo-Miller L, Silva AJ (2005) Modulation of presynaptic plasticity and learning by the H-ras/extracellular signal-regulated kinase/synapsin I signaling pathway. J Neurosci 25, 9721-9734.
40. Corradi A, Zanardi A, Giacomini C, Onofri F, Valtorta F, Zoli M, Benfenati F (2008) Synapsin-I-and synapsin-II-null mice display an increased age-dependent cognitive impairment. J Cell Sci 121, 3042-3051.
41. Lin Y, Jover-Mengual T, Wong J, Bennett MV, Zukin RS (2006) PSD-95 and PKC converge in regulating NMDA receptor trafficking and gating. Proc Natl Acad Sci U S A 103, 19902-19907.
42. Shiraishi Y, Mizutani A, Mikoshiba K, Furuichi T (2003) Coincidence in dendritic clustering and synaptic targeting of homer proteins and NMDA receptor complex proteins NR2B and PSD95 during development of cultured hippocampal neurons. Mol Cell Neurosci 22, 188-201.
43. Wu A, Ren T, Hu Q, Liu Y (2000) Deltamethrin induces altered expression of P53, Bax and Bcl-2 in rat brain. Neurosci Lett 284, 29-32.
44. Avila J, Lim F, Moreno F, Belmonte C, Cuello AC (2002) Tau function and dysfunction in neurons: Its role in neurodegenerative disorders. Mol Neurobiol 25, 213-231.
45. Grundke-Iqbal I, Iqbal K, Quinlan M, Tung YC, Zaidi MS, Wisniewski HM (1986) Microtubule-associated protein tau. A component of Alzheimer paired helical filaments. J Biol Chem 261, 6084-6089.
46. Grundke-Iqbal I, Iqbal K, Tung YC, Quinlan M, Wisniewski HM, Binder LI (1986) Abnormal phosphorylation of the microtubule-associated protein tau (tau) in Alzheimer cytoskeletal pathology. Proc Natl Acad Sci U S A 83, 4913-4917.
47. Terwel D, Lasrado R, Snauwaert J, Vandeweert E, Van Haesendonck C, Borghgraef P, Van Leuven F (2005) Changed conformation of mutant Tau-P301L underlies the moribund tauopathy, absent in progressive, nonlethal axonopathy of Tau-4R/2N transgenic mice. J Biol Chem 280, 3963-3973.
48. Cross DA, Alessi DR, Cohen P, Andjelkovich M, Hemmings BA(1995) Inhibition of glycogen synthase kinase-3 by insulin mediated by protein kinase B. Nature 378, 785-789.
49. Shaw M, Cohen P, Alessi DR (1997) Further evidence that the inhibition of glycogen synthase kinase-3beta by IGF-1 is mediated by PDK1/PKB-induced phosphorylation of Ser-9 and not by dephosphorylation of Tyr-216. FEBS Lett 416, 307-311.
50. Fang X, Yu SX, Lu Y, Bast RC Jr, Woodgett JR, Mills GB (2000) Phosphorylation and inactivation of glycogen synthase kinase 3 by protein kinase A. Proc Natl Acad Sci U S A 97, 11960-11965.
51. Shimizu S, Ugi S, Maegawa H, Egawa K, Nishio Y, Yoshizaki T, Shi K, Nagai Y, Morino K, Nemoto K (2003) Protein-tyrosine phosphatase 1B as new activator for hepatic lipogenesis via sterol regulatory element-binding protein-1 gene expression. J Biol Chem 278, 43095-43101.
52. Yokoyama N, Miller WT (2001) Inhibition of Src by direct interaction with protein phosphatase 2A. FEBS Lett 505, 460-464.
53. Hooper C, Markevich V, Plattner F, Killick R, Schofield E, Engel T, Hernandez F, Anderton B, Rosenblum K, Bliss T, Cooke SF, Avila J, Lucas JJ, Giese KP, Stephenson J, Lovestone S (2007) Glycogen synthase kinase-3 inhibition is integral to long-term potentiation. Eur J Neurosci 25, 81-86.
54. Peineau S, Taghibiglou C, Bradley C, Wong TP, Liu L, Lu J, Lo E,Wu D, Saule E, Bouschet T, Matthews P, Isaac JT, Bortolotto ZA, Wang YT, Collingridge GL (2007) LTP inhibits LTD in the hippocampus via regulation of GSK3beta. Neuron 53, 703-717.
55. Kimura T, Yamashita S, Nakao S, Park JM, Murayama M, Mizoroki T, Yoshiike Y, Sahara N, Takashima A (2008) GSK-3beta is required for memory reconsolidation in adult brain. PLoS One 3, e3540.