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Original Articles

Exposure to decabromodiphenyl ether (BDE-209) produces mitochondrial dysfunction in rat liver and cell death

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References

  • Abella, V., A. Santoro, M. Scotece, J. Conde, V. López-López, V. Lazzaro, J. J. Gómez-Reino, R. Meli, and O. Gualillo. 2015. Non-dioxin-like polychlorinated biphenyls (PCB 101, PCB 153 and PCB 180) induce chondrocyte cell death through multiple pathways. Toxicol. Lett. 234:13–19. doi:10.1016/j.toxlet.2015.02.001.
  • Alves, C., F. L. Chagas, C. T. Souza, and M. B. P. Toralles. 2007. Environmental exposure to endocrine disruptors with estrogenic activity and the association with pubertal disorders in children. Cad. Saude Publica 23:1005–1014. doi:10.1590/S0102-311X2007000500003.
  • Bellinger, D. C. 2013. Prenatal exposures to environmental chemicals and children’s neurodevelopment: An update. Saf. Health Work 4:1–11. doi:10.5491/SHAW.2013.4.1.1.
  • Bernardi, P., L. Scorrano, R. Colonna, V. Petronilli, and F. Di Lisa. 1999. Mitochondria and cell death. Mechanistic aspects and methodological issues. Eur. J. Biochem. 264:687–701. doi:10.1046/j.1432-1327.1999.00725.x.
  • Brentnall, M., L. Rodriguez-Menocal, R. L. De Guevara, E. Cepero, and L. H. Boise. 2013. Caspase-9, caspase-3 and caspase-7 have distinct roles during intrinsic apoptosis. BMC Cell Biol. 14:32. doi:10.1186/1471-2121-14-32.
  • Chen, J., C. Liufu, W. Sun, X. Sun, and D. Chen. 2010a. Assessment of the neurotoxic mechanisms of decabrominated diphenyl ether (PBDE-209) in primary cultured neonatal rat hippocampal neurons includes alterations in second messenger signaling and oxidative stress. Toxicol. Lett. 192:431–439. doi:10.1016/j.toxlet.2009.11.020.
  • Chernyak, B. V., D. S. Izyumov, K. G. Lyamzaev, A. A. Pashkovskaya, O. Y. Pletjushkina, Y. N. Antonenko, D. V. Sakharov, K. W. A. Wirtz, and V. P. Skulachev. 2006. Production of reactive oxygen species in mitochondria of HeLa cells under oxidative stress. Biochim. Biophys. Acta 1757:525–534. doi:10.1016/j.bbabio.2006.02.019.
  • Costa, L. G., and G. Giordano. 2007. Developmental neurotoxicity of polybrominated diphenyl ether (PBDE) flame retardants. Neurotoxicology 28:1047–1067. doi:10.1016/j.neuro.2007.08.007.
  • Costa, L. G., and G. Giordano. 2011. Is decabromodiphenyl ether (BDE-209) a developmental neurotoxicant? Neurotoxicology 32:9–24. doi:10.1016/j.neuro.2010.12.010.
  • Cowens, K. R., S. Simpson, W. K. Thomas, and G. B. Carey. 2015. Polybrominated diphenyl ether (PBDE)-induced suppression of phosphoenolpyruvate carboxykinase (PEPCK) decreases hepatic glyceroneogenesis and disrupts hepatic lipid homeostasis. J. Toxicol. Environ. Health Part A 78:1437–1449. doi:10.1080/15287394.2015.1098580.
  • Darnerud, P. O. 2003. Toxic effects of brominated flame retardants in man and in wildlife. Environ. Int. 29:841–853. doi:10.1016/S0160-4120(03)00107-7.
  • Denizot, F., and R. Lang. 1986. Rapid colorimetric assay for cell growth and survival: Modifications to the tetrazolium dye procedure giving improved sensitivity and reliability. J. Immunol. Meth. 89:271–277. doi:10.1016/0022-1759(86)90368-6.
  • Dietz, R., F. F. Rigt, C. Sonne, R. J. Letcher, S. Backus, E. W. Born, M. Kirkegaard, and D. C. G. Muir. 2007. Age and seasonal variability of polybrominated diphenyl ethers in free-ranging East Greenland polar bears (Ursus maritimus). Environ. Pollut. 146:166–173. doi:10.1016/j.envpol.2006.05.040.
  • Dikalov, S. I., W. Li, A. K. Doughan, R. R. Blanco, and A. M. Zafari. 2012. Mitochondrial reactive oxygen species and calcium uptake regulate activation of phagocytic NADPH oxidase. Am J Physiol Regul Integr Comp Physiol 302:1134–1142. doi:10.1152/ajpregu.00842.2010.
  • Eskenazi, B., J. Chevrier, S. A. Rauch, K. Kogut, K. G. Harley, C. Johnson, C. Trujillo, A. Sjödin, and A. Bradman. 2013. In utero and childhood polybrominated diphenyl ether (PBDE) exposures and neurodevelopment in the CHAMACOS study. Environ. Health Persp. 121:257–262.
  • Frouin, H., M. Lebeuf, M. Hammill, S. Masson, and M. Fournier. 2010. Effects of individual polybrominated diphenyl ether (PBDE) congeners on harbour seal immune cells in vitro. Mar. Pollut. Bull. 60:291–298. doi:10.1016/j.marpolbul.2009.09.006.
  • Ghio, A. J., M. S. Carraway, and M. C. Madden. 2012. Composition of air pollution particles and oxidative stress in cells, tissues, and living systems. J. Toxicol. Environ. Health B 15:1–21. doi:10.1080/10937404.2012.632359.
  • Gill, S., Y. Hou, N. Li, O. Pulido, and W. Bowers. 2016. Developmental neurotoxicity of polybrominated diphenyl ethers mixture de71 in Sprague-Dawley rats. J. Toxicol. Environ. Health Part A 79:482–493. doi:10.1080/15287394.2016.1182001.
  • Goodman, J. E. 2009. Neurodevelopmental effects of decabromodiphenyl ether (BDE-209) and implications for the reference dose. Reg. Toxicol. Pharmacol. 54:91–104. doi:10.1016/j.yrtph.2009.02.006.
  • Green, D. R., and J. C. Reed. 1998. Mitochondria and apoptosis. Science 281:1309–1312. doi:10.1126/science.281.5381.1309.
  • Hale, R. C., M. J. La Guardia, E. Harvey, M. O. Gaylor, and T. M. Mainor. 2006. Brominated flame retardant concentrations and trends in abiotic media. Chemosphere 64:181–186. doi:10.1016/j.chemosphere.2005.12.006.
  • Halestrap, A. P. 2004. Mitochondrial permeability: Dual role for the ADP/ATP translocator? Nature 430:1. doi:10.1038/nature02816.
  • Hites, R. A. 2004. Polybrominated diphenyl ethers in the environment and in people: A meta-analysis of concentrations. Environ. Sci. Technol. 38:945–956. doi:10.1021/es035082g.
  • Hu, X., D. Hu, and Y. Xu. 2009. Effects of tetrabrominated diphenyl ether and hexabromocyclododecanes in single and complex exposure to hepatoma HepG2 cells. Environ. Toxicol. Pharmacol. 27:327–337. doi:10.1016/j.etap.2008.11.014.
  • Hu, X. Z., Y. Xu, D. C. Hu, Y. Hui, and F. X. Yang. 2007. Apoptosis induction on human hepatoma cells Hep G2 of decabrominated diphenyl ether (PBDE-209). Toxicol. Lett. 171:19–28. doi:10.1016/j.toxlet.2007.04.002.
  • Imberti, R., A. L. Nieminen, B. Herman, and J. J. Lemasters. 1993. Mitochondrial and glycolytic dysfunction in lethal injury to hepatocytes by t-butylhydroperoxide: Protection by fructose, cyclosporin A and trifluoperazine. J. Pharmacol. Exp. Ther. 265:392–400.
  • Jaeschke, H., G. J. Gores, A. I. Cederbaum, J. A. Hinson, D. Pessayre, and J. J. Lemasters. 2002. Mechanisms of hepatotoxicity. Toxicol. Sci. Orlando 65:166–176. doi:10.1093/toxsci/65.2.166.
  • Jin, S., F. Yang, Y. Hui, Y. Xu, Y. Lu, and J. Liu. 2010. Cytotoxicity and apoptosis induction on RTG-2 cells of 2,2ʹ,4,4ʹ-tetrabromodiphenyl ether (BDE-47) and decabrominated diphenyl ether (BDE-209). Toxicol. in Vitro 24:1190–1196. doi:10.1016/j.tiv.2010.02.012.
  • Kim, J. Y., and J. H. Park. 2003. ROS-dependent caspase-9 activation in hypoxic cell death. FEBS Lett. 549:94–98. 95-96. doi:10.1016/S0014-5793(03)00795-6.
  • Kowaltowski, A. J., and A. E. Vercesi. 1999. Mitochondrial damage induced by conditions of oxidative stress. Free Radic. Biol. 26:463–471. doi:10.1016/S0891-5849(98)00216-0.
  • Laemmli, U. K. 1970. Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature 227:680–685. doi:10.1038/227680a0.
  • Lee, J., B. P. Yu, and J. P. Herlihy. 1999. Modulation of cardiac mitochondrial membrane fluidity by age and calorie intake. Free Radic. Biol. Med. 26:260–265. doi:10.1016/S0891-5849(98)00195-6.
  • Lee, S., K. Kannan, and H. B. Moon. 2013. Assessment of exposure to polybrominated diphenyl ethers (PBDEs) via seafood consumption and dust ingestion in Korea. Sci. Total Environ. 443:24–30. doi:10.1016/j.scitotenv.2012.10.099.
  • Leist, M., B. Single, A. F. Castoldi, S. Kühnle, and P. Nicotera. 1997. Intracellular adenosine triphosphate (ATP) concentration: A switch in the decision between apoptosis and necrosis. J. Exp. Med. 185:1481–1486. doi:10.1084/jem.185.8.1481.
  • Madia, F., G. Giordano, V. Fattori, A. Vitalone, I. Branchi, F. Capone, and L. G. Costa. 2004. Differential in vitro neurotoxicity of the flame retardant PBDE-99 and of the PCB Aroclor 1254 in human astrocytoma cells. Toxicol. Lett. 154:11–21. doi:10.1016/j.toxlet.2004.06.013.
  • Malik, A. N., and A. Czajka. 2012. Is mitochondrial DNA content a potential biomarker of mitochondrial dysfunction? Mitochondrion 13:481–492. doi:10.1016/j.mito.2012.10.011.
  • McDonald, T. 2002. A perspective on the potential health risks of PBDEs. Chemosphere 46:745–755. doi:10.1016/S0045-6535(01)00239-9.
  • Meironyte, D., K. Norén, and A. Bergman. 1999. Analysis of polybrominated diphenyl ethers in Swedish human milk. A time-related trend study, 1972-1997. J. Toxicol. Environ. Health Part A 58:329–341. doi:10.1080/009841099157197.
  • Mingatto, F. E., A. C. Dos Santos, T. Rodrigues, A. A. Pigoso, S. A. Uyemura, and C. Curti. 2000. Effects of nimesulide and its reduced metabolite on mitochondria. Br. J. Pharmacol. 131:1154–1160. doi:10.1038/sj.bjp.0703667.
  • Moon, H.-B., M. Choi, J. Yu, R.-H. Jung, and H.-G. Choi. 2012. Contamination and potential sources of polybrominated diphenyl ethers (PBDEs) in water and sediment from the artificial Lake Shihwa, Korea. Chemosphere 88:837–843. doi:10.1016/j.chemosphere.2012.03.091.
  • Nagata, S. 1997. Apoptosis by death factor. Cell 88:355–365. doi:10.1016/S0092-8674(00)81874-7.
  • Nash, J. T., D. T. Szabo, and G. B. Carey. 2013. Polybrominated diphenyl ethers alter hepatic phosphoenolpyruvate carboxykinase enzyme kinetics in male Wistar rats: Implications for lipid and glucose metabolism. J. Toxicol. Environ. Health Part A 76:142–156. doi:10.1080/15287394.2012.738457.
  • Ouyang, L., Z. Shi, S. Zhao, F.-T. Wang, -T.-T. Zhou, B. Liu, and J.-K. Bao. 2012. Programmed cell death pathways in cancer: A review of apoptosis, autophagy and programmed necrosis. Cell Prolif. 45:487–498. doi:10.1111/cpr.2012.45.issue-6.
  • Pazin, M., L. C. Pereira, and D. J. Dorta. 2015. Toxicity of brominated flame retardants, BDE-47 and BDE-99 stems from impaired mitochondrial bioenergetics. Toxicol. Mech. Meth. 25:34–41. doi:10.3109/15376516.2014.974233.
  • Pedersen, P. L., J. W. Greenawalt, B. Reynafarje, J. Hulliher, G. L. Decker, J. W. Soper, and E. Bustamente. 1978. Preparation and characterization of mitochondria and submitochondrial particules of rats liver: Derived tissues. Meth. Cell. Biol. 20:411–481.
  • Pereira, L. C., A. O. De Souza, and D. J. Dorta. 2013. Polybrominated diphenyl ether congener (BDE-100) induces mitochondrial impairment. Basic Clin. Pharmacol. Toxicol. 112:418–424. doi:10.1111/bcpt.2013.112.issue-6.
  • Pereira, L. C., A. O. De Souza, M. F. Franco-Bernardes, M. Pazin, M. J. Tasso, P. H. Pereira, and D. J. Dorta. 2015. A perspective on the potential risks of emerging contaminants to human and environmental health. Environ. Sci. Pollut. Res. 22:13800–13823. doi:10.1007/s11356-015-4896-6
  • Pereira, L. C., L. F. C. Miranda, A. O. De Souza, and D. J. Dorta. 2014. BDE-154 induces mitochondrial permeability transition and impairs mitochondrial bioenergetics. J. Toxicol. Environ. Health. A 77:24–36. doi:10.1080/15287394.2014.861337.
  • Porter, A. G., and R. U. Jänicke. 1999. Emerging roles of caspase-3 in apoptosis. Cell Death Differ. 6:99–104. doi:10.1038/sj.cdd.4400476.
  • Rice, D. C., E. A. Reeve, A. Herlihy, R. Thomas Zoeller, W. Douglas Thompson, and V. P. Markowski. 2007. Developmental delays and locomotor activity in the C57BL6/J mouse following neonatal exposure to the fully-brominated PBDE, decabromodiphenyl ether. Neurotoxicol. Teratol. 29:511–520. doi:10.1016/j.ntt.2007.03.061.
  • Riu, A., J.-P. Cravedi, L. Debrauwer, A. Garcia, C. Canlet, I. Jouanin, and D. Zalko. 2008. Disposition and metabolic profiling of [14C]-decabromodiphenyl ether in pregnant Wistar rats. Environ. Int. 34:318–329. doi:10.1016/j.envint.2007.03.007.
  • Sacks, V. P., and R. Lohmann. 2012. Freely dissolved PBDEs in water and porewater of an urban estuary. Environ. Pollut. 162:287–293. doi:10.1016/j.envpol.2011.11.028.
  • Selvakumar, K., L. Sheerin Banu, G. Krishnamoorthy, P. Venkataraman, P. Elumalai, and J. Arunakaran. 2011. Differential expression of androgen and estrogen receptors in PCB (Aroclor 1254)-exposed rat ventral prostate: Impact of alpha-tocopherol. Exp. Toxicol. Pathol. 63:105–112. doi:10.1016/j.etp.2009.10.003.
  • Shao, J., C. C. White, M. J. Dabrowski, T. J. Kavanagh, M. L. Eckert, and E. P. Gallagher. 2008. The role of mitochondrial and oxidative injury in BDE 47 toxicity to human fetal liver hematopoietic stem cells. Toxicol. Sci. 101:81–90. doi:10.1093/toxsci/kfm256.
  • Shen, K., C. Shen, J. Yu, C. Yu, L. Chen, D. Shi, and Y. Chen. 2011. PCB congeners induced mitochondrial dysfunction in Vero cells. J. Hazard. Mater. 185:24–28. doi:10.1016/j.jhazmat.2010.08.061.
  • Skehan, P., R. Storeng, D. Scudeiro, A. Monks, J. Mcmahon, D. Vistica, J. T. Warren, H. Bokesch, S. Keney, and M. R. Boyd. 1990. New colorimetric cytotoxicity assay for anticancer-drug screening. J. Nat. Cancer Inst. 82:1107–1112. doi:10.1093/jnci/82.13.1107.
  • Souza, A. O., L. C. Pereira, D. P. Oliveira, and D. J. Dorta. 2013. BDE-99 congener induces cell death by apoptosis of human hepatoblastoma cell line: HepG2. Toxicol. In Vitro 27:580–587. doi:10.1016/j.tiv.2012.09.022.
  • Stapleton, H. M., and N. G. Dodder. 2008. Photodegradation of decabromodiphenyl ether in house dust by natural sunlight. Environ. Toxicol. Chem. 27:306–312. doi:10.1897/07-301R.1.
  • Stapleton, H. M., S. M. Kelly, R. Pei, R. J. Letcher, and C. Gunsch. 2009. Metabolism of polybrominated diphenyl ethers (PBDEs) by human hepatocytes. Environ. Health Persp. 117:197–202. doi:10.1289/ehp.11807.
  • Stasinska, A., A. Reid, A. Hinwood, G. Stevenson, A. Callan, J. Odland, and J. Heyworth. 2013. Chemosphere Concentrations of polybrominated diphenyl ethers (PBDEs) in residential dust samples from Western Australia. Chemosphere 91:187–193. doi:10.1016/j.chemosphere.2012.12.044.
  • Viberg, H. 2009. Neonatal ontogeny and neurotoxic effect of decabrominated diphenyl ether (PBDE 209) on levels of synaptophysin and tau. Int. J. Dev. Neurosci. 27:423–429. doi:10.1016/j.ijdevneu.2009.05.007.
  • Wallace, D. C. 2000. Mitochondrial defects in cardiomyopathy and neuromuscular disease. Am. Heart J. 139:S70–S85. doi:10.1067/mhj.2000.103934.
  • Yan, C., D. Huang, and Y. Zhang. 2011. The involvement of ROS overproduction and mitochondrial dysfunction in PBDE-47-induced apoptosis on Jurkat cells. Exp. Toxicol. Pathol. 63:413–417. doi:10.1016/j.etp.2010.02.018.
  • Yan, S., S. B. Subramanian, R. D. Tyagi, R. Y. Surampalli, and T. C. Zhang. 2010. Emerging contaminants of environmental concern: Source, transport, fate, and treatment. Pract. Period. Hazardous Toxic Radioact. Waste Manage. 14:2–20. doi:10.1061/(ASCE)HZ.1944-8376.0000015.
  • Yarana, C., J. Sripetchwandee, J. Sanit, S. Chattipakorn, and N. Chattipakorn. 2012. Calcium-induced cardiac mitochondrial dysfunction is predominantly mediated by cyclosporine A-dependent mitochondrial permeability transition pore. Arch. Med. Res. 43:333–338. doi:10.1016/j.arcmed.2012.06.010.
  • Zhang, X., F. Yang, C. Xu, W. Liu, S. Wen, and Y. Xu. 2008a. Cytotoxicity evaluation of three pairs of hexabromocyclododecane (HBCD) enantiomers on Hep G2 cell. Toxicol. Vitro. 22:1520–1527. doi:10.1016/j.tiv.2008.05.006.
  • Zhang, Y., G. L. Guo, X. Han, C. Zhu, B. A. Kilfoy, Y. Zhu, P. Boyle, and T. Zheng. 2008b. Do polybrominated diphenyl ethers (PBDEs) increase the risk of thyroid cancer? Biosci. Hypotheses 1:195–199. doi:10.1016/j.bihy.2008.06.003.
  • Zhivotovsky, B., A. Samali, A. Gahm, and S. Orrenius. 1999. Caspases: Their intracellular localization and translocation during apoptosis. Cell Death Differ. 6:644–651. doi:10.1038/sj.cdd.4400536.
  • Zhong, Y., P. Guo, X. Wang, and J. An. 2015. Aroclor 1254 inhibits cell viability and induces apoptosis of human A549 lung cancer cells by modulating the intracellular Ca 2+ level and ROS production through the mitochondrial pathway. J. Environ. Sci. Health Part A 50:806–813. doi:10.1080/10934529.2015.1019797.
  • Zuo, Y., B. Xiang, J. Yang, X. Sun, Y. Wang, H. Cang, and J. Yi. 2009. Oxidative modification of caspase-9 facilitates its activation via disulfide-mediated interaction with Apaf-1. Cell Res. 19:449–457. doi:10.1038/cr.2009.19.

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