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Research Article

Neurotoxicity and physiological stress in brain of zebrafish chronically exposed to tributyltin

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  • Anselmo, C. D., V. F. Sardela, V. P. de Sousa, and H. M. G. Pereira. 2018. Zebrafish (Danio rerio): A valuable tool for predicting the metabolism of xenobiotics in humans? Comp. Biochem. Physiol. C-Toxicol. Pharmacol. 212:34–46. doi:10.1016/j.cbpc.2018.06.005.
  • Bailey, J., A. Oliveri, and E. D. Levin. 2013. Zebrafish model systems for developmental neurobehavioral toxicology. Birth Defects Res. C Embryo Today 99:14–23. doi:10.1002/bdrc.21027.
  • Barros, S., A. M. Coimbra, N. Alves, M. Pinheiro, J. B. Quintana, M. M. Santos, and T. Neuparth. 2020. Chronic exposure to environmentally relevant levels of simvastin disripts zebrafish brain gene signaling involved in energy metabolism. J. Toxicol. Environ. Health Part A 83:113–25. doi:10.1080/15287394.2020.1733722.
  • Bland, L. M., T. J. Regan, M. N. Dinh, R. Ferrari, D. A. Keith, R. Lester, D. Mouillot, N. J. Murray, H. A. Nguyen, and E. Nicholson. 2017. Using multiple lines of evidence to assess the risk of ecosystem collapse. Proc Biol Sci. 284: 20170660. doi: 10.1098/rspb.2017.0660.
  • Bradford, M. M. 1976. Rapid and sensitive method for quantitation of microgram quantities of protein utilizing principle of protein dye binding. Anal. Biochem. 72:248–54. doi:10.1016/0003-2697(76)90527-3.
  • Broeg, K., and K. K. Lehtonen. 2006. Indices for the assessment of environmental pollution of the Baltic Sea coasts: Integrated assessment of a multi-biomarker approach. Mar. Pollut. Bull. 53:508–22. doi:10.1016/j.marpolbul.2006.02.004.
  • Bromek, E., A. Haduch, and W. A. Daniel. 2010. The ability of cytochrome P450 2D isoforms to synthesize dopamine in the brain: An in vitro study. Eur. J. Pharmacol. 626:171–78. doi:10.1016/j.ejphar.2009.09.062.
  • Carto, S. L., A. J. Weaver, R. Hetherington, Y. Lam, and E. C. Wiebe. 2009. Out of Africa and into an ice age: On the role of global climate change in the late Pleistocene migration of early modern humans out of Africa. J. Human Evol. 56:139–51. doi:10.1016/j.jhevol.2008.09.004.
  • Chen, J. F., C. J. Huang, L. D. Zheng, M. Simonich, C. L. Bai, R. Tanguay, and Q. X. Dong. 2011. Trimethyltin chloride (TMT) neurobehavioral toxicity in embryonic zebrafish. Neurotoxicol. Teratol. 33:721–26. doi:10.1016/j.ntt.2011.09.003.
  • Cheng, Y. C., C. A. Chen, and H. C. Chen. 2017. Endoplasmic reticulum stress-induced cell death in podocytes. Nephrology 22:43–49. doi:10.1111/nep.13145.
  • Chetwynd, A. J., and A. David. 2018. A review of nanoscale LC-ESI for metabolomics and its potential to enhance the metabolome coverage. Talanta 182:380–90. doi:10.1016/j.talanta.2018.01.084.
  • Dam, H. G. 2013. Evolutionary adaptation of marine zooplankton to global change. Ann. Rev. Mar. Sci. 5:349–70. doi:10.1146/annurev-marine-121211-172229.
  • de Esch, C., R. Slieker, A. Wolterbeek, R. Woutersen, and D. de Groot. 2012. Zebrafish as potential model for developmental neurotoxicity testing: A mini review. Neurotoxicol. Teratol. 34:545–53. doi:10.1016/j.ntt.2012.08.006.
  • Deboeck, G., G. E. Nilsson, U. Elofsson, A. Vlaeminck, and R. Blust. 1995. Brain monoamine levels and energy status in common carp (Cyprinus-Carpio) after exposure to sublethal levels of copper. Aquat. Toxicol. 33:265–77. doi:10.1016/0166-445X(95)00022-V.
  • Espitia-Perez, P., S. M. Albino, L. Espitia-Perez, H. Brango, H. da Rosa, A. Kleber Silveira, D. P. Moraes, C. Cerveira, M. Mingori, C. Tiefensee Ribeiro, et al. 2018. Neurobehavioral and oxidative stress alterations following methylmercury and retinyl palmitate co-administration in pregnant and lactating rats and their offspring. Neurotoxicology 69:164–80. doi:10.1016/j.neuro.2018.10.004.
  • Figueroa, D., A. Signore, O. Araneda, H. R. Contreras, M. Concha, and C. Garcia. 2020. Toxicity and differential oxidative stress effects on zebrafish larvae following exposure to toxins from the okadaic acid group. J. Toxicol. Environ. Health Part A 83:573–88. doi:10.1080/15287394.2020.1793046.
  • Frohlich, E. 2017. Role of omics techniques in the toxicity testing of nanoparticles. J. Nanobiotechnol. 15:84. doi:10.1186/s12951-017-0320-3.
  • Goodson, J. L., and R. R. Thompson. 2010. Nonapeptide mechanisms of social cognition, behavior and species-specific social systems. Curr. Opin. Neurobiol. 20:784–94. doi:10.1016/j.conb.2010.08.020.
  • Haduch, A., E. Bromek, J. Wojcikowski, K. Golembiowska, and W. A. Daniel. 2016. Involvement of cytochrome P450 2D in the formation of serotonin in the brain: In vivo and in vitro study. Eur. Neuropsychopharmacol. 26:S262–S262. doi:10.1016/S0924-977X(16)31140-3.
  • Heinrich, L., and T. Krause. 2017. Fishing in acid waters: A vulnerability assessment of the Norwegian fishing industry in the face of increasing ocean acidification. Integr. Environ. Assess. Manag. 13:778–89. doi:10.1002/ieam.1843.
  • Horie, Y., H. Watanabe, H. Takanobu, Y. Shigemoto, T. Yamagishi, T. Iguchi, and N. Tatarazako. 2017. Effects of triphenyltin on reproduction in Japanese medaka (Oryzias latipes) across two generations. Aquat. Toxicol. 192:16–23. doi:10.1016/j.aquatox.2017.08.016.
  • Horinouchi, T., T. Maeda, and C. Furusawa. 2018. Understanding and engineering alcohol-tolerant bacteria using OMICS technology. World J. Microbiol. Biotechnol. 34:157.
  • Illing, B., and J. L. Rummer. 2017. Physiology can contribute to better understanding, management, and conservation of coral reef fishes. Conserv. Physiol. 5:cox005. doi:10.1093/conphys/cox005.
  • Jennings, W. C., E. C. Chern, D. O’Donohue, M. G. Kellogg, and A. B. Boehm. 2018. Frequent detection of a human fecal indicator in the urban ocean: Environmental drivers and covariation with enterococci. Environ Sci Process Impacts 20:480–92. doi:10.1039/C7EM00594F.
  • Jia, Z. L., J. Cen, J. B. Wang, F. Zhang, Q. Xia, X. Wang, X. Q. Chen, R. C. Wang, C. D. Hsiao, K. C. Liu, et al. 2019. Mechanism of isoniazid-induced hepatotoxicity in zebrafish larvae: Activation of ROS-mediated ERS, apoptosis and the Nrf2 pathway. Chemosphere 227:541–50. doi:10.1016/j.chemosphere.2019.04.026.
  • Jiao, Y. Q., Y. Tao, Y. Yang, T. Diogene, H. Yu, Z. Q. He, W. Han, Z. B. Chen, P. Wu, and Y. Zhang. 2020. Monobutyl phthalate (MBP) can dysregulate the antioxidant system and induce apoptosis of zebrafish liver. Environmental Pollution  257: 113517. dio:10.1016/j.envpol.2019.113517.
  • Jiaxin, S., W. Shengchen, C. Yirong, W. Shuting, and L. Shu. 2020. Cadmium exposure induces apoptosis, inflammation and immunosuppression through CYPs activation and antioxidant dysfunction in common carp neutrophils. Fish Shellfish Immunol. 99:284–90. doi:10.1016/j.fsi.2020.02.015.
  • Jin, S. W., Y. P. Hwang, C. Y. Choi, H. G. Kim, S. J. Kim, Y. Kim, Y. C. Chung, K. J. Lee, T. C. Jeong, and H. G. Jeong. 2017. Protective effect of rutaecarpine against t-BHP-induced hepatotoxicity by upregulating antioxidant enzymes via the CaMKII-Akt and Nrf2/ARE pathways. Food Chem. Toxicol. 100:138–48. doi:10.1016/j.fct.2016.12.031.
  • Jones, D. C., and G. W. Miller. 2008. The effects of environmental neurotoxicants on the dopaminergic system: A possible role in drug addiction. Biochem. Pharmacol. 76:569–81. doi:10.1016/j.bcp.2008.05.010.
  • Kavitha, P., and J. V. Rao. 2009. Sub-lethal effects of profenofos on tissue-specific antioxidative responses in a Euryhyaline fish, Oreochromis mossambicus. Ecotoxicol. Environ. Saf. 72:1727–33. doi:10.1016/j.ecoenv.2009.05.010.
  • Komoike, Y., and M. Matsuoka. 2013. Exposure to tributyltin induces endoplasmic reticulum stress and the unfolded protein response in zebrafish. Aquat. Toxicol. 142:221–29. doi:10.1016/j.aquatox.2013.08.017.
  • Lara-Jacobo, L. R., B. Willard, S. J. Wallace, and V. S. Langlois. 2019. Cytochrome P450 1A transcript is a suitable biomarker of both exposure and response to diluted bitumen in developing frog embryos. Environ. Pollut. 246:501–08. doi:10.1016/j.envpol.2018.12.039.
  • Le, L. T. H., S. Takahashi, K. Saeki, N. Nakatani, S. Tanabe, N. Miyazaki, and Y. Fujise. 1999. High percentage of butyltin residues in total tin in the livers of cetaceans from Japanese coastal waters. Environ. Sci. Technol. 33:1781–86. doi:10.1021/es980624t.
  • Li, P., Z. H. Li, and L. Q. Zhong. 2019a.  Effects of low concentrations of triphenyltin on neurobehavior and the thyroid endocrine system in zebrafish. Ecotoxicology and Environmental Safety 186: 109776. doi:10.1016/j.ecoenv.2019.109776
  • Li, Z., D. Yu, G. Wangbao, W. Guangjun, Y. Ermeng, and X. Jun. 2019b. Aquatic ecotoxicology and water quality criteria of three organotin compounds: A review. Nat. Environ. Pollut. Technol. 18:217–24.
  • Li, Z. H., and P. Li. 2015. Evaluation of tributyltin toxicity in Chinese rare minnow larvae by abnormal behavior, energy metabolism and endoplasmic reticulum stress. Chem-Biol. Interact. 227:32–36.
  • Li, Z. H., P. Li, and T. Randak. 2010. Effect of a human pharmaceutical carbamazepine on antioxidant responses in brain of a model teleost in vitro: An efficient approach to biomonitoring. J. Appl. Toxicol. 30:644–48. doi:10.1002/jat.1534.
  • Li, Z. H., P. Li, and Z. C. Shi. 2015. Chronic exposure to tributyltin induces brain functional damage in juvenile common carp (Cyprinus carpio). PLoS ONE 10:e0123091. doi:10.1371/journal.pone.0123091.
  • Li, Z. H., P. Li, and Z. C. Shi. 2016a. Physiological and molecular responses in brain of juvenile common carp (Cyprinus carpio) following exposure to tributyltin. Environ. Toxicol. 31:278–84. doi:10.1002/tox.22042.
  • Li, Z. H., L. Q. Zhong, W. N. Mu, and Y. H. Wu. 2016b. Effects of chronic exposure to tributyltin on tissue-specific cytochrome P450 1 regulation in juvenile common carp. Xenobiotica 46:511–15. doi:10.3109/00498254.2015.1092618.
  • Li, Z. H., V. Zlabek, J. Turek, J. Velisek, J. Pulkrabova, J. Kolarova, E. Sudova, P. Berankova, P. Hradkova, J. Hajslova, et al. 2011. Evaluating environmental impact of STPs situated on streams in the Czech Republic: An integrated approach to biomonitoring the aquatic environment. Water Res. 45:1403–13. doi:10.1016/j.watres.2010.10.032.
  • Li, Z. H., V. Zlabek, J. Velisek, R. Grabic, J. Machova, J. Kolarova, P. Li, and T. Randak. 2013. Multiple biomarkers responses in juvenile rainbow trout, Oncorhynchus mykiss, after acute exposure to a fungicide propiconazole. Environ. Toxicol. 28:119–26. doi:10.1002/tox.20701.
  • Lima, D., L. F. Castro, I. Coehlo, R. Lacerda, M. Gesto, J. Soares, A. Andre, R. Capela, T. Torres, A. P. Carvalho, et al. 2015. Efftects of tributyltin and other retinoid receptor agonists in reproductive-related endpoints in the zebrafish (Danio rerio). J. Toxicol. Environ. Health Part A 78:747–60. doi:10.1080/15287394.2015.1028301.
  • Liu, C. M., G. H. Zheng, Q. L. Ming, J. M. Sun, and C. Cheng. 2013. Protective effect of puerarin on lead-induced mouse cognitive impairment via altering activities of acetyl cholinesterase, monoamine oxidase and nitric oxide synthase. Environ. Toxicol. Pharmacol. 35:502–10. doi:10.1016/j.etap.2013.02.009.
  • Liu, Z. H., Y. W. Li, W. Hu, Q. L. Chen, and Y. J. Shen. 2020. Mechanisms involved in tributyltin-enhanced aggressive behaviors and fear responses in male zebrafish. Aquat. Toxicol. 220:105408. doi:10.1016/j.aquatox.2020.105408.
  • Mann, A., and R. F. Tyndale. 2010. Cytochrome P450 2D6 enzyme neuroprotects against 1-methyl-4-phenylpyridinium toxicity in SH-SY5Y neuronal cells. Eur. J. Neurosci. 31:1185–93. doi:10.1111/j.1460-9568.2010.07142.x.
  • Mearns, A. J., D. J. Reish, P. S. Oshida, A. M. Morrison, M. A. Rempel-Hester, C. Arthur, N. Rutherford, and R. Pryor. 2017. Effects of pollution on marine organisms. Water Environ. Res. 89:1704–98. doi:10.2175/106143017X15023776270647.
  • Merlo, E., I. V. Silva, C. Cardoso, and J. B. Gracelli. 2018. The obesogen tributyltin induces features of polycystic ovary syndrome (PCOS): A review. J. Toxicol. Environ. Health B 21:181–206. doi:10.1080/10937404.2018.1496214.
  • Mitra, S., W. A. Siddiqui, and S. Khandelwal. 2015. C-Phycocyanin protects against acute tributyltin chloride neurotoxicity by modulating glial cell activity along with its anti-oxidant and anti-inflammatory property: A comparative efficacy evaluation with N-acetyl cysteine in adult rat brain. Chem-Biol. Interact. 238:138–50. doi:10.1016/j.cbi.2015.06.016.
  • Miyazaki, I., and M. Asanuma. 2008. Dopaminergic neuron-specific oxidative stress caused by dopamine itself. Acta Med. Okayama 62:141–50.
  • Miyazaki, I., and M. Asanuma. 2009. Approaches to prevent dopamine quinone-induced neurotoxicity. Neurochem. Res. 34:698–706. doi:10.1007/s11064-008-9843-1.
  • MohanKumar, S. M. J., B. S. Kasturi, A. C. Shin, P. Balasubramanian, E. T. Gilbreath, M. Subramanian, and P. S. MohanKumar. 2011. Chronic estradiol exposure induces oxidative stress in the hypothalamus to decrease hypothalamic dopamine and cause hyperprolactinemia. Am. J. Physiol-Regul. Integr. Comp. Physiol. 300:R693–R699.
  • Pan, X., I. Uno, Z. Wang, S. Yamamoto, and Y. Hara. 2018. Seasonal variabilities in chemical compounds and acidity of aerosol particles at urban site in the west Pacific. Environ. Pollut. 237:868–77. doi:10.1016/j.envpol.2017.11.089.
  • Pereira, A. C., T. Gomes, M. R. F. Machado, and T. L. Rocha. 2019. The zebrafish embryotoxicity test (ZET) for nanotoxicity assessment: From morphological to molecular approach. Environ. Pollut. 252:1841–53. doi:10.1016/j.envpol.2019.06.100.
  • Ronan, P. J., M. P. Gaikowski, S. J. Hamilton, K. J. Buhl, and C. H. Summers. 2007. Ammonia causes decreased brain monoamines in fathead minnows (Pimephales promelas). Brain Res. 1147:184–91. doi:10.1016/j.brainres.2007.02.015.
  • Sachett, A., F. Bevilaqua, R. Chitolina, C. Garbinato, H. Gasparetto, J. Dal Magro, G. M. Conterato, and A. M. Siebel. 2018. Ractopamine hydrochloride induces behavioral alterations and oxidative stress in zebrafish. J. Toxicol. Environ. Health Part A 81:194–201. doi:10.1080/15287394.2018.1434848.
  • Saifi, M. A., W. Khan, and C. Godugu. 2018. Cytotoxicity of nanomaterials: Using nanotoxicology to address the safety concerns of nanoparticles. Pharm. Nanotechnol. 6:3–16. doi:10.2174/2211738505666171023152928.
  • Schulte, P. M. 2014. What is environmental stress? Insights from fish living in a variable environment. J. Exp. Biol. 217:23–34. doi:10.1242/jeb.089722.
  • Silbiger, N. J., C. E. Nelson, K. Remple, J. K. Sevilla, Z. A. Quinlan, H. M. Putnam, M. D. Fox, and M. J. Donahue. 2018. Nutrient pollution disrupts key ecosystem functions on coral reefs. Proc Biol Sci 285, 20172718. doi:10.1098/rspb.2017.2718.
  • Tabassum, H., J. Khan, M. Salman, S. Raisuddin, and S. Parvez. 2016. Propiconazole induced toxicological alterations in brain of freshwater fish Channa punctata Bloch. Ecol. Indicators 62:242–48. doi:10.1016/j.ecolind.2015.11.001.
  • Takahashi, S., H. Mukai, S. Tanabe, K. Sakayama, T. Miyazaki, and H. Masuno. 1999. Butyltin residues in livers of humans and wild terrestrial mammals and in plastic products. Environ. Pollut. 106:213–18. doi:10.1016/S0269-7491(99)00068-8.
  • Tong, K. I., A. Kobayashi, F. Katsuoka, and M. Yamamoto. 2006. Two-site substrate recognition model for the Keap1-Nrf2 system: A hinge and latch mechanism. Biol. Chem. 387:1311–20. doi:10.1515/BC.2006.164.
  • Tsunoda, M., A. Aizawa, B. Konno, K. Kimura, and T. Sugita-Konishi. 2006. Subacute administration of tributyltin chloride modulates neurotransmitters and their metabolites in discrete brain regions of maternal mice and their F1 offspring. Toxicol Ind Health 22:15–25. doi:10.1191/0748233706th240oa.
  • Ulla, H. R. A., S. K. Vijayasarathi, and R. N. S. Gowda. 2001. Neurotoxicity of trimethyltin - An organotin compound in adult hens. Indian Vet. J. 78:394–96.
  • Wang, A. M., Y. Miyata, S. Klinedinst, H. M. Peng, J. P. Chua, T. Komiyama, X. K. Li, Y. Morishima, D. E. Merry, W. B. Pratt, et al. 2013. Activation of Hsp70 reduces neurotoxicity by promoting polyglutamine protein degradation. Nat. Chem. Biol. 9:112–18. doi:10.1038/nchembio.1140.
  • Wang, L., X. Sun, J. Weiszmann, and W. Weckwerth. 2017. System-level and Granger network analysis of integrated proteomic and metabolomic dynamics identifies key points of Grape Berry development at the interface of primary and secondary metabolism. Front Plant Sci 8:1066.
  • Xiao, W. Y., Y. W. Li, Q. L. Chen, and Z. H. Liu. 2018. Tributyltin impaired reproductive success in female zebrafish through disrupting oogenesis, reproductive behaviors and serotonin synthesis. Aquat. Toxicol. 200:206–16. doi:10.1016/j.aquatox.2018.05.009.
  • Ximenes, C. F., S. M. L. Rodrigues, P. L. Podratz, E. Merlo, J. F. P. de Araujo, L. C. M. Rodrigues, J. B. Coitinho, D. V. Vassallo, J. B. Graceli, and I. Stefanon. 2017. Tributyltin chloride disrupts aortic vascular reactivity and increases reactive oxygen species production in female rats. Environ. Sci. Pollut. Res. 24:24509–20.
  • Xing, H., S. Li, X. Wang, X. Gao, and S. Xu. 2013. Effects of atrazine and chlorpyrifos on the mRNA levels of HSP70 and HSC70 in the liver, brain, kidney and gill of common carp (Cyprinus carpio L.). Chemosphere 90:910–16. doi:10.1016/j.chemosphere.2012.06.028.
  • Yu, A., X. L. Wang, Z. H. Zuo, J. L. Cai, and C. G. Wang. 2013. Tributyltin exposure influences predatory behavior, neurotransmitter content and receptor expression in Sebastiscus marmoratus. Aquat. Toxicol. 128:158–62. doi:10.1016/j.aquatox.2012.12.008.
  • Zajac, R. N., J. M. Vozarik, and B. R. Gibbons. 2013. Spatial and temporal patterns in macrofaunal diversity components relative to sea floor landscape structure. PLoS ONE 8:e65823.
  • Zhang, J. L., P. Sun, T. Kong, F. Yang, and W. C. Guan. 2016b. Tributyltin promoted hepatic steatosis in zebrafish (Danio rerio) and the molecular pathogenesis involved. Aquat. Toxicol. 170:208–15. doi:10.1016/j.aquatox.2015.11.028.
  • Zhang, J. L., C. N. Zhang, P. Sun, and X. Shao. 2016a. Tributyltin affects shoaling and anxiety behavior in female rare minnow (Gobiocypris rarus). Aquat. Toxicol. 178:80–87. doi:10.1016/j.aquatox.2016.07.007.
  • Zhao, J., M. Temimi, H. Ghedira, and C. Hu. 2014. Exploring the potential of optical remote sensing for oil spill detection in shallow coastal waters–a case study in the Arabian Gulf. Opt Express 22:13755–72. doi:10.1364/OE.22.013755.
  • Zhao, L., F. Yang, S. Milano, T. Han, E. O. Walliser, and B. R. Schone. 2018. Transgenerational acclimation to seawater acidification in the Manila clam Ruditapes philippinarum: Preferential uptake of metabolic carbon. Sci. Total Environ. 627:95–103. doi:10.1016/j.scitotenv.2018.01.225.

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