Mechanism of pyrethroid pesticide-induced apoptosis: Role of calpain and the ER stress pathway

Toxicological Sciences

Volumn 122, Issue 2, 2011, Pages 512-525

  Hossain, Muhammad M ^a   Richardson, Jason R ^a  

^a RUTGERS UNIVERSITY   (United States)

Author keywords

Apoptosis; Calpain; Caspases; Cytosolic calcium; eIF2 ; ER stress; Neurodegeneration; Pesticide; Pyrethroid; siRNA; Sodium channel; Sodium influx

Indexed keywords

CALPAIN; CASPASE 12; CASPASE 3; CASPASE 3 INHIBITOR; CASPASE 9; CASPASE 9 INHIBITOR; CHELATING AGENT; CYTOCHROME C; DELTAMETHRIN; SMALL INTERFERING RNA; SODIUM CHANNEL; TETRODOTOXIN;

APOPTOSIS; ARTICLE; CALCIUM CELL LEVEL; CALCIUM TRANSPORT; CONTROLLED STUDY; CYTOSOL; CYTOTOXICITY; DNA FRAGMENTATION; DOSE RESPONSE; ENDOPLASMIC RETICULUM STRESS; ENZYME ACTIVITY; HUMAN; HUMAN CELL; MITOCHONDRIAL MEMBRANE POTENTIAL; MOLECULAR MECHANICS; NERVE DEGENERATION; NEUROBLASTOMA CELL; SIGNAL TRANSDUCTION;

APOPTOSIS; CALCIUM; CALPAIN; CASPASE 12; CASPASE 3; CASPASE 9; CELL LINE; CYTOCHROMES C; DNA FRAGMENTATION; EGTAZIC ACID; ENDOPLASMIC RETICULUM; HUMANS; MITOCHONDRIA; NITRILES; PESTICIDES; PYRETHRINS; RNA, SMALL INTERFERING; SIGNAL TRANSDUCTION; UNFOLDED PROTEIN RESPONSE;

EID: 80051680668     PISSN: 10966080     EISSN: 10960929     Source Type: Journal    
DOI: 10.1093/toxsci/kfr111     Document Type: Article

References (59)

1. Abdel-Rahman, A., Abou-Donia, S., El-Masry, E., Shetty, A., and Abou-Donia, M. (2004). Stress and combined exposure to low doses of pyridostigmine bromide, DEET, and permethrin produce neurochemical and neuropathological alterations in cerebral cortex, hippocampus, and cerebellum. J. Toxicol. Environ. Health A 67, 163-192.
2. Arduino, D. M., Esteves, A. R., Cardoso, S. M., and Oliveira, C. R. (2009). Endoplasmic reticulum and mitochondria interplay mediates apoptotic cell death: relevance to Parkinson's disease. Neurochem. Int. 55, 341-348.
3. Banasiak, K. J., Burenkova, O., and Haddad, G. G. (2004). Activation of voltage-sensitive sodium channels during oxygen deprivation leads to apoptotic neuronal death. Neuroscience. 126, 31-44.
4. Berger, A. B., Sexton, K. B., and Bogyo, M. (2006). Commonly used caspase inhibitors designed based on substrate specificity profiles lack selectivity. Cell Res. 16, 961-963.
5. + signals and death programmes in neurons. Philos. Trans. R. Soc. Lond. B. Biol. Sci. 360, 2255-2258.
6. Bianchi, L., Gerstbrein, B., Frokjaer-Jensen, C., Royal, D. C., Mukherjee, G., Royal, M. A., Xue, J., Schafer, W. R., and Driscoll, M. (2004). The neurotoxic MEC-4(d) DEG/ENaC sodium channel conducts calcium: implications for necrosis initiation. Nat. Neurosci. 7, 1337-1344.
7. Bloomquist, J. R., Barlow, R. L., Gillette, J. S., Li, W., and Kirby, M. L. (2002). Selective effects of insecticides on nigrostriatal dopaminergic nerve pathways. Neurotoxicology 23, 537-544.
8. Boyce, M., Bryant, K. F., Jousse, C., Long, K., Harding, H. P., Scheuner, D., Kaufman, R. J., Ma, D., Coen, D. M., Ron, D., et al. (2005). A selective inhibitor of eIF2alpha dephosphorylation protects cells from ER stress. Science 307, 935-939.
9. Bradberry, S. M., Thanacoody, H. K., Watt, B. E., Thomas, S. H., and Vale, J. A. (2005). Management of the cardiovascular complications of tricyclic antidepressant poisoning: role of sodium bicarbonate. Toxicol. Rev. 24, 195-204.
10. Breckenridge, C. B., Holden, L., Sturgess, N., Weiner, M., Sheets, L., Sargent, D., Soderlund, D. M., Choi, J. S., Symington, S., Clark, J. M., et al. (2009). Evidence for a separate mechanism of toxicity for the Type I and the Type II pyrethroid insecticides. Neurotoxicology 30(Suppl. 1), S17-S31.
11. 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 pesticiderelated illnesses among working youths, 1988-1999. Am. J. Public Health 93, 605-610.
12. Cao, Z., George, J., Gerwick, W. H., Baden, D. G., Rainier, J. D., and Murray, T. F. (2008). Influence of lipid-soluble gating modifier toxins on sodium influx in neocortical neurons. J. Pharmacol. Exp. Ther. 326, 604-613.
13. Cao, Z., Shafer, T. J., and Murray, T. F. (2011). Mechanisms of pyrethroid insecticide-induced stimulation of calcium influx in neocortical neurons. J. Pharmacol. Exp. Ther. 336, 197-205.
14. Casida, J. E., and Quistad, G. B. (1998). Golden age of insecticide research: past, present, or future? Annu. Rev. Entomol. 43, 1-16.
15. Chen, D., Huang, X., Liu, L., and Shi, N. (2007). Deltamethrin induces mitochondrial membrane permeability and altered expression of cytochrome C in rat brain. J. Appl. Toxicol. 27, 368-372.
16. - cotransporter. J. Neurochem. 106, 1563-1576.
17. 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.
18. Clark, J. M., and Symington, S. B. (2008). Neurotoxic implications of the agonistic action of CS-syndrome pyrethroids on the N-type Ca(v) 2.2 calcium channel. Pest. Manag. Sci. 64, 628-638.
19. Cohen, G. M. (1997). Caspases: the executioners of apoptosis. Biochem. J. 326(Pt 1), 1-16.
20. Culmsee, C., and Landshamer, S. (2006). Molecular insights into mechanisms of the cell death program: role in the progression of neurodegenerative disorders. Curr. Alzheimer Res. 3, 269-283.
21. Das, P. C., Streit, T. M., Cao, Y., Rose, R. L., Cherrington, N., Ross, M. K., Wallace, A. D., and Hodgson, E. (2008). Pyrethroids: cytotoxicity and induction of CYP isoforms in human hepatocytes. Drug Metabol. Drug Interact. 23, 211-236.
22. Day, W. T., Wu, C. H., and Safa, A. R. (2009). Etoposide induces protein kinase Cd- and caspase-3-dependent apoptosis in neuroblastoma cancer cells. Mol. Pharmacol. 76, 632-640.
23. Doi, H., Kikuchi, H., Murai, H., Kawano, Y., Shigeto, H., Ohyagi, Y., and Kira, J. (2006). Motor neuron disorder simulating ALS induced by chornic inhalation of pyrethroid insecticides. Neurology 67, 1894-1895.
24. 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.
25. 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 diffusion-limited model. Toxicol. Sci. 115, 330-343.
26. Gorman, A. M., Ceccatelli, S., and Orrenius, S. (2000). Role of mitochondria in neuronal apoptosis. Dev. Neurosci. 22, 348-358.
27. Jordan, J., Galindo, M. F., Calvo, S., Gonzalez-Garcia, C., and Cena, V. (2000). Veratridine induces apoptotic death in bovine chromaffin cells through superoxide production. Br. J. Pharmacol. 130, 1496-1504.
28. Kaul, S., Kanthasamy, A., Kitazawa, M., Anantharam, V., and Kanthasamy, A. G. (2003). Caspase-3 dependent proteolytic activation of protein kinase C delta mediates and regulates 1-methyl-4-phenylpyridinium (MPP+)-induced apoptotic cell death in dopaminergic cells: relevance to oxidative stress in dopaminergic degeneration. Eur. J. Neurosci. 18, 1387-1401.
29. Kim, K. B., Anand, S. S., Kim, H. J., White, C. A., Fisher, J. W., Tornero-Velez, R., and Bruckner, J. V. (2010). Age, dose, and timedependency of plasma and tissue distribution of deltamethrin in immature rats. Toxicol. Sci. 115, 354-368.
30. 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. Occup. Environ. Health 82, 1173-1178.
31. 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.
32. Knoblach, S. M., Alroy, D. A., Nikolaeva, M., Cernak, I., Stoica, B. A., and Faden, A. I. (2004). Caspase inhibitor z-DEVD-fmk attenuates calpain and necrotic cell death in vitro and after traumatic brain injury. J. Cereb. Blood Flow Metab. 24, 1119-1132.
33. Lee, H. C., and Wei, Y. H. (2000). Mitochondrial role in life and death of the cell. J. Biomed. Sci. 7, 2-15.
34. 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.
35. Muller-Mohnssen, H. (1999). Chronic sequelae and irreversible injuries following acute pyrethroid intoxication. Toxicol. Lett. 107, 161-176.
36. Nakagawa, T., and Yuan, J. (2000). Cross-talk between two cysteine protease families. Activation of caspase-12 by calpain in apoptosis. J. Cell. Biol. 150, 887-894.
37. Narahashi, T. (1996). Neuronal ion channels as the target sites of insecticides. Pharmacol. Toxicol. 79, 1-14.
38. + release in rat optic nerve during in vitro chemical ischemia. J. Neurosci. 25, 9960-9967.
39. Oyadomari, S., and Mori, M. (2004). Roles of CHOP/GADD153 in endoplasmic reticulum stress. Cell Death Differ. 11, 381-389.
40. Power, L. E., and Sudakin, D. L. (2007). Pyrethrin and pyrethroid exposures in the United States: a longitudinal analysis of incidents reported to poison centers. J. Med. Toxicol. 3, 94-99.
41. +, and rotenone toxicity: oxidation of thioredoxin and caspase-3 activation. Toxicol. Sci. 95, 163-171.
42. Rami, A., Agarwal, R., Botez, G., and Winckler, J. (2000). l-Calpain activation, DNA fragmentation, and synergistic effects of caspase and calpain inhibitors in protecting hippocampal neurons from ischemic damage. Brain Res. 866, 299-312.
43. Rao, R. V., Hermel, E., Castro-Obregon, S., del Rio, G., Ellerby, L. M., Ellerby, H. M., and Bredesen, D. E. (2001). Coupling endoplasmic reticulum stress to the cell death program. Mechanism of caspase activation. J. Biol. Chem. 276, 33869-33874.
44. Saido, T. C., Sorimachi, H., and Suzuki, K. (1994). Calpain: new perspectives in molecular diversity and physiological-pathological involvement. FASEB J. 8, 814-822.
45. Saito, K., Elce, J. S., Hamos, J. E., and Nixon, R. A. (1993). 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. U.S.A. 90, 2628-2632.
46. Sherer, T. B., Betarbet, R., Testa, C. M., Seo, B. B., Richardson, J. R., Kim, J. H., Miller, G. W., Yagi, T., Matsuno-Yagi, A., and Greenamyre, J. T. (2003). Mechanism of toxicity in rotenone models of Parkinson's disease. J. Neurosci. 23, 10756-10764.
47. 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.
48. Soderlund, D. M., Clark, J. M., Sheets, L. P., Mullin, L. S., Piccirillo, V. J., Sargent, D., Stevens, J. T., and Weiner, M. L. (2002). Mechanisms of pyrethroid neurotoxicity: implications for cumulative risk assessment. Toxicology 171, 3-59.
49. Tayebati, S. K., Di Tullio, M. A., Ricci, A., and Amenta, F. (2009). Influence of dermal exposure to the pyrethroid insecticide deltamethrin on rat brain microanatomy and cholinergic/dopaminergic neurochemistry. Brain Res. 1301, 180-188.
50. Tsuji, T., Shimohama, S., Kimura, J., and Shimizu, K. (1998). m-Calpain (calcium-activated neutral proteinase) in Alzheimer's disease brains. Neurosci. Lett. 248, 109-112.
51. + influx and not via calpain inhibition. Neuropharmacology 42, 706-713.
52. Verkhratsky, A. (2005). Physiology and pathophysiology of the calcium store in the endoplasmic reticulum of neurons. Physiol. Rev. 85, 201-279.
53. Vosler, P. S., Brennan, C. S., and Chen, J. (2008). Calpain-mediated signaling mechanisms in neuronal injury and neurodegeneration. Mol. Neurobiol. 38, 78-100.
54. Wang, J., and Bannon, M. J. (2005). Sp1 and Sp3 activate transcription of the human dopamine transporter gene. J. Neurochem. 93, 474-482.
55. Wu, A., Li, L., and Liu, Y. (2003). Deltamethrin induces apoptotic cell death in cultured cerebral cortical neurons. Toxicol. Appl. Pharmacol. 187, 50-57.
56. Wu, A., and Liu, Y. (2000a). Apoptotic cell death in rat brain following deltamethrin treatment. Neurosci. Lett. 279, 85-88.
57. Wu, A., and Liu, Y. (2000b). Deltamethrin induces delayed apoptosis and altered expression of p53 and bax in rat brain. Environ. Toxicol. Pharmacol. 8, 183-189.
58. Wu, A., Ren, T., Hu, Q., and Liu, Y. (2000). Deltamethrin induces altered expression of P53, Bax and Bcl-2 in rat brain. Neurosci. Lett. 284, 29-32.
59. Xu, C., Bailly-Maitre, B., and Reed, J. C. (2005). Endoplasmic reticulum stress: cell life and death decisions. J. Clin. Invest. 115, 2656-2664.