Hippocampal ER stress and learning deficits following repeated pyrethroid exposure

Toxicological Sciences

Volumn 143, Issue 1, 2015, Pages 220-228

  Hossain, Muhammad M ^a,b   DiCicco Bloom, Emanuel ^a   Richardson, Jason R ^a,b  

^a RUTGERS ROBERT WOOD JOHNSON MEDICAL SCHOOL   (United States)

^b RUTGERS UNIVERSITY   (United States)

Author keywords

Adult neurogenesis; Deltamethrin; ER stress; Hippocampus; Water maze

Indexed keywords

BROXURIDINE; CASPASE 12; CASPASE 3; CCAAT ENHANCER BINDING PROTEIN; DELTAMETHRIN; GLUCOSE REGULATED PROTEIN 78; CASP12 PROTEIN, MOUSE; CASP3 PROTEIN, MOUSE; DDIT3 PROTEIN, MOUSE; GROWTH ARREST AND DNA DAMAGE INDUCIBLE PROTEIN 153; HEAT SHOCK PROTEIN; INSECTICIDE; MOLECULAR CHAPERONE GRP78; NITRILE; PYRETHROID;

ADULT; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; APOPTOSIS; ARTICLE; BRDU ASSAY; CELL PROLIFERATION; CONTROLLED STUDY; DENTATE GYRUS; ENDOPLASMIC RETICULUM STRESS; HIPPOCAMPUS; IMMUNOHISTOCHEMISTRY; LEARNING DISORDER; MALE; MORRIS WATER MAZE TEST; MOUSE; NEUROBLASTOMA CELL; NONHUMAN; WESTERN BLOTTING; ANIMAL; ANIMAL BEHAVIOR; C57BL MOUSE; CHEMICALLY INDUCED; DRUG EFFECTS; ENDOPLASMIC RETICULUM; MAZE TEST; METABOLISM; NERVOUS SYSTEM DEVELOPMENT; PATHOLOGY; PATHOPHYSIOLOGY; PSYCHOLOGY; SIGNAL TRANSDUCTION; TIME FACTOR; UPREGULATION;

ANIMALIA; MUS;

ANIMALS; APOPTOSIS; BEHAVIOR, ANIMAL; CASPASE 12; CASPASE 3; CELL PROLIFERATION; DENTATE GYRUS; ENDOPLASMIC RETICULUM; ENDOPLASMIC RETICULUM STRESS; HEAT-SHOCK PROTEINS; HIPPOCAMPUS; INSECTICIDES; LEARNING DISORDERS; MALE; MAZE LEARNING; MICE, INBRED C57BL; NEUROGENESIS; NITRILES; PYRETHRINS; SIGNAL TRANSDUCTION; TIME FACTORS; TRANSCRIPTION FACTOR CHOP; UP-REGULATION;

EID: 84928656632     PISSN: 10966080     EISSN: 10960929     Source Type: Journal    
DOI: 10.1093/toxsci/kfu226     Document Type: Article

References (51)

1. Aprea, C., Stridori, A., and Sciarra, G. (1997). Analytical method for the determination of urinary 3-phenoxybenzoic acid in subjects occupationally exposed to pyrethroid insecticides. J. Chromatogr. B 695, 227-236.
2. Berkowitz, G. S., Obel, J., Deych, E., Lapinski, R., Godbold, J., Liu, Z., Landrigan, P. J., and Wolff, M. S.. (2003). Exposure to indoor pesticides during pregnancy in a multiethnic, urban cohort. Environ. Health Persp. 111, 79-84.
3. Calvert, G. M., Mehler, L. N., Rosales, R., Baum, L., Thomsen, C., Male, D., Shafey, O., Das, R., Lackovic, M., and Arvizu, E. (2003). Acute pesticide-related illnesses among working youths, 1988-1999. Am J. Public Health 93, 605-610.
4. Cameron, H. A., Woolley, C. S., McEwen, B. S., and Gould, E. (1993). Differentiation of newly born neurons and glia in the dentate gyrus of the adult rat. Neuroscience 56, 337-344.
5. Chen, N. N., Luo, D. J., Yao, X. Q., Yu, C., Wang, Y., Wang, Q., Wang, J. Z., and Liu, G. P. (2012). Pesticides induce spatial memory deficits with synaptic impairments and an imbalanced tau phosphorylation in rats. J. Alzheimers Dis. 30, 585-594.
6. Choi, W. S., Abel, G., Klintworth, H., Flavell, R. A., and Xia, Z. (2010). JNK3 mediates paraquat- and rotenone-induced dopaminergic neuron death. J. Neuropathol. Exp. Neurol. 69, 511-520.
7. Crow, J. A., Borazjani, A., Potter, P. M., and Ross, M. K. (2007). Hydrolysis of pyrethroids by human and rat tissues: examination of intestinal, liver, and serum carboxylesterases. Toxicol. Appl. Pharmacol. 221, 1-12.
8. Elwan, M. A., Richardson, J. R., Guillot, T. S., Caudle, W. M., and Miller, G. W. (2006). Pyrethroid pesticide-induced alterations in dopamine transporter function. Toxicol. Appl. Pharmacol.211, 188-197.
9. Environmental Protection Agency (2010). Deltamethrin. Human health assessment scoping document in support of registration review. Available at: www.epa.gov/espp/litstatus/effects/redleg-frog/2013/deltamethrin/appendix-j.pdf.
10. Falluel-Morel, A., Sokolowski, K., Sisti, H. M., Zhou, X., Shors, T. J., and Dicicco-Bloom, E. (2007). Developmental mercury exposure elicits acute hippocampal cell death, reductions in neurogenesis, and severe learning deficits during puberty. J. Neurochem. 103, 1968-1981.
11. Godin, S. J., Crow, J. A., Scollon, E. J., Hughes, M. F., DeVito, M. J., and Ross, M. K. (2007). Identification of rat and human cytochrome p450 isoforms and a rat serum esterase that metabolize the pyrethroid insecticides deltamethrin and esfenvalerate. Drug Metab. Dispos. 35, 1664-1671.
12. Godin, S. J., DeVito, M. J., Hughes, M. F., Ross, D. G., Scollon, E. J., Starr, J. M., Setzer, R. W., Conolly, R. B., and Tornero-Velez, R. (2010). Physiologically based pharmacokinetic modeling of deltamethrin: development of a rat and human diffusionlimited model. Toxicol. Sci. 115, 330-343.
13. Hoozemans, J. J., van Haastert, E. S., Nijholt, D. A., Rozemuller, A. J., Eikelenboom, P., and Scheper, W. (2009). The unfolded protein response is activated in pretangle neurons in Alzheimer's disease hippocampus. Am. J. Pathol. 174, 1241-1251.
14. Hossain, M. M., and Richardson, J. R. (2011). Mechanism of pyrethroid pesticide-induced apoptosis: Role of calpain and the ER stress pathway. Toxicol. Sci. 122, 512-525.
15. Hotamisligil, G. S. (2010). Endoplasmic reticulum stress and the inflammatory basis of metabolic disease. Cell 140, 900-917.
16. Husain, R., Husain, R., Adhami, V. M., and Seth, P. K. (1996). Behavioral, neurochemical, and neuromorphological effects of deltamethrin in adult rats. J. Toxicol. Environ. Health 48, 515-526.
17. Kimata, A., Kondo, T., Ueyama, J., Yamamoto, K., Yoshitake, J., Takagi, K., Suzuki, K., Inoue, T., Ito, Y., Hamajima, N., et al. (2009). Comparison of urinary concentrations of 3-phenoxybenzoic acid among general residents in rural and suburban areas and employees of pest control firms. Int. Arch. Occ.Environ. Health 82, 1173-1178.
18. Kitazawa, M., Anantharam, V., and Kanthasamy, A. G. (2003). Dieldrin induces apoptosis by promoting caspase-3-dependent proteolytic cleavage of protein kinase Cdelta in dopaminergic cells: Relevance to oxidative stress and dopaminergic degeneration. Neuroscience 119, 945-964.
19. Lemaire, V., Koehl, M., Le Moal, M., and Abrous, D. N. (2000). Prenatal stress produces learning deficits associated with an inhibition of neurogenesis in the hippocampus. Proc. Natl Acad. Sci. USA 97, 11032-11037.
20. Lindholm, D., Wootz, H., and Korhonen, L. (2006). ER stress and neurodegenerative diseases. Cell Death Differ. 13, 385-392.
21. Lu, B., and Chang, J. H. (2004). Regulation of neurogenesis by neurotrophins: Implications in hippocampus-dependent memory. Neuron Glia Biol. 1, 377-384.
22. Mishra, D., Tiwari, S. K., Agarwal, S., Sharma, V. P., and Chaturvedi, R. K. (2012). Prenatal carbofuran exposure inhibits hippocampal neurogenesis and causes learning and memory deficits in offspring. Toxicol. Sci. 127, 84-100.
23. Morgan, M. K. (2012). Children's exposures to pyrethroid insecticides at home: A review of data collected in published exposure measurement studies conducted in the United States. Int. J. Environ. Res. Pub. Health 9, 2964-2985.
24. Morishima, N., Nakanishi, K., Takenouchi, H., Shibata, T., and Yasuhiko, Y. (2002). An endoplasmic reticulum stress-specific caspase cascade in apoptosis. Cytochrome c-independent activation of caspase-9 by caspase-12. J. Biol. Chem. 277, 34287-34294.
25. Morris, R. (1984). Developments of a water-maze procedure for studying spatial learning in the rat. J. Neurosci. Methods 11, 47-60.
26. Muller-Mohnssen, H. (1999). Chronic sequelae and irreversible injuries following acute pyrethroid intoxication. Toxicol. Lett.107, 161-176.
27. Nakagawa, T., Zhu, H., Morishima, N., Li, E., Xu, J., Yankner, B. A., and Yuan, J. (2000). Caspase-12 mediates endoplasmicreticulum-specific apoptosis and cytotoxicity by amyloidbeta. Nature 403, 98-103.
28. Ojo, J. O., Abdullah, L., Evans, J., Reed, J. M., Montague, H., Mullan, M. J., et al. (2014). Exposure to an organophosphate pesticide, individually or in combination with other Gulf War agents, impairs synaptic integrity and neuronal differentiation, and is accompanied by subtle microvascular injury in a mouse model of Gulf War agent exposure. Neuropathology 34, 109-127.
29. Oyadomari, S., and Mori, M. (2004). Roles of CHOP/GADD153 in endoplasmic reticulum stress. Cell Death Differ. 11, 381-389.
30. Prell, T., Lautenschlager, J., Weidemann, L., Ruhmer, J., Witte, O.W., and Grosskreutz, J. (2014). Endoplasmic reticulum stress is accompanied by activation of NF-kappaB in amyotrophic lateral sclerosis. J. Neuroimmunol. 270, 29-36.
31. Ramachandiran, S., Hansen, J. M., Jones, D. P., Richardson, J. R., and Miller, G. W. (2007). Divergent mechanisms of paraquat, MPP{thorn}, and rotenone toxicity: Oxidation of thioredoxin and caspase-3 activation. Toxicol. Sci. 95, 163-171.
32. Rohlman, D. S., Lasarev, M., Anger, W. K., Scherer, J., Stupfel, J., and McCauley, L. (2007). Neurobehavioral performance of adult and adolescent agricultural workers. Neurotoxicology 28, 374-380.
33. Salminen, A., Kauppinen, A., Suuronen, T., Kaarniranta, K., and Ojala, J. (2009). ER stress in Alzheimer's disease: A novel neuronal trigger for inflammation and Alzheimer's pathology. J. Neuroinflammation 6, 41.
34. Sama, D. M., and Norris, C. M. (2013). Calcium dysregulation and neuroinflammation: Discrete and integrated mechanisms for age-related synaptic dysfunction. Ageing Res. Rev. 12, 982-995.
35. Shors, T. J., Townsend, D. A., Zhao, M., Kozorovitskiy, Y., and Gould, E. (2002). Neurogenesis may relate to some but not all types of hippocampal-dependent learning. Hippocampus 12, 578-584.
36. 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 bicinchoninic acid. Anal Biochem. 150, 76-85.
37. Snyder, J. S., Hong, N. S., McDonald, R. J., and Wojtowicz, J. M. (2005). A role for adult neurogenesis in spatial long-term memory. Neuroscience 130, 843-852.
38. Sokolowski, K., Obiorah, M., Robinson, K., McCandlish, E., Buckley, B., and DiCicco-Bloom, E. (2013). Neural stem cell apoptosis after low-methylmercury exposures in postnatal hippocampus produce persistent cell loss and adolescent memory deficits. Dev. Neurobiol. 73, 936-949.
39. Stanfield, B. B., and Trice, J. E. (1988). Evidence that granule cells generated in the dentate gyrus of adult rats extend axonal projections. Exp. Brain Res. 72, 399-406.
40. Tait, S. W., and Green, D. R. (2010). Mitochondria and cell death: outer membrane permeabilization and beyond. Nat. Rev. Mol.Cell Biol. 11, 621-632.
41. Thuret, S., Toni, N., Aigner, S., Yeo, G. W., and Gage, F. H. (2009). Hippocampus-dependent learning is associated with adult neurogenesis in MRL/MpJ mice. Hippocampus 19, 658-669.
42. Trunnelle, K. J., Bennett, D. H., Ahn, K. C., Schenker, M. B., Tancredi, D. J., Gee, S. J., Stoecklin-Marois, M. T., and Hammock, B. D. (2014). Concentrations of the urinary pyrethroid metabolite 3-phenoxybenzoic acid in farm worker families in the MICASA study. Environ. Res. 131, 153-159.
43. Ueyama, J., Kimata, A., Kamijima, M., Hamajima, N., Ito, Y., Suzuki, K., Inoue, T., Yamamoto, K., Takagi, K., Saito, I., et al. (2009).Urinary excretion of 3-phenoxybenzoic acid in middle-aged and elderly general population of Japan. Environ.Res. 109, 175-180.
44. Winocur, G., Wojtowicz, J. M., Sekeres, M., Snyder, J. S., and Wang, S. (2006). Inhibition of neurogenesis interferes with hippocampus-dependent memory function. Hippocampus 16, 296-304.
45. Wu, A., Li, L., and Liu, Y. (2003). Deltamethrin induces apoptotic cell death in cultured cerebral cortical neurons. Toxicol. Appl. Pharmacol. 187, 50-57.
46. Wu, A, and Liu, Y. (2000). Apoptotic cell death in rat brain following deltamethrin treatment. Neurosci. Lett. 279, 85-88.
47. Xia, Y., Zhao, P., Xue, J., Gu, X. Q., Sun, X., Yao, H., et al. (2003). Na{thorn} channel expression and neuronal function in the Na{thorn}/H{thorn} exchanger 1 null mutant mouse. J. Neurophysiol. 89, 229-236.
48. Xu, C., Bailly-Maitre, B., and Reed, J. C. (2005). Endoplasmic reticulum stress: Cell life and death decisions. J. Clin. Investig. 115, 2656-2664.
49. Zhang, K., and Kaufman, R. J. (2008). From endoplasmic-reticulum stress to the inflammatory response. Nature 454, 455-462.
50. Zhang, X., Xu, L., He, D., and Ling, S. (2013). Endoplasmic reticulum stress-mediated hippocampal neuron apoptosis involved in diabetic cognitive impairment. BioMed. Res. Int.2013, 924327.
51. Zhao, C., Deng, W., and Gage, F. H. (2008). Mechanisms and functional implications of adult neurogenesis. Cell 132, 645-660.