Abstract
The goal of the study is to investigate the preventive effect of taurine against arsenite-induced arrest of neuronal differentiation in N2a cells. Our results revealed that taurine reinstated the neurite outgrowth in arsenite-treated N2a cells. Meanwhile, arsenite-induced oxidative stress and mitochondrial dysfunction as well as degradation of mitochondria DNA (mtDNA) were also inhibited by co-treatment of taurine. Since oxidative stress and mitochondrial dysfunction is closely associated with endoplasmic reticulum (ER) stress, we further examined indicators of ER stress, 78 kDa glucose-regulated protein (GRP78), and C/EBP-homologous protein (CHOP) protein expression. The results demonstrated that taurine significantly reduced arsenite-induced ER stress in N2a cells. In the parallel experiment, arsenite-induced disruption of intracellular calcium homeostasis was also ameliorated by taurine. The proven bio-function of taurine preserved a preventive effect against deleteriously cross-talking between oxidative stress, mitochondria, and ER. Overall, the results of the study suggested that taurine reinstated neuronal differentiation by inhibiting oxidative stress, ER stress, and mitochondrial dysfunction in arsenite-treated N2a cells.
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Abramov AY, Canevari L, Duchen MR (2004) β-Amyloid peptides induce mitochondrial dysfunction and oxidative stress in astrocytes and death of neurons through activation of NADPH oxidase. J Neurosci 24:565–575
Ahmad S, Kitchin KT, Cullen WR (2000) Arsenic species that cause release of iron from ferritin and generation of activated oxygen. Arch Biochem Biophys 382:195–202
ATSDR (Agency for Toxic Substances and Disease Registry). (2011) The ATSDR 2011 Substance Priority List. Atlanta, GA: ATSDR. Available http://www.atsdr.cdc.gov/SPL/index.html. Accessed 2 Oct 2012
Brookes PS, Yoon Y, Robotham JL, Anders MW, Sheu SS (2004) Calcium, ATP, and ROS: a mitochondrial love-hate triangle. Am J Physiol Cell Physiol 287:817–833
Chou CT, Lin WF, Kong ZL, Chen SY, Hwang DF (2013) Taurine prevented cell cycle arrest and restored neurotrophic gene expression in arsenite-treated SH-SY5Y cells. Amino Acids 45:811–819
Dhar P, Mohari N, Mehra RD (2007) Preliminary morphological and morphometric study of rat cerebellum following sodium arsenite exposure during rapid brain growth (RBG) period. Toxicology 234:10–20
Dragicevic N, Mamcarz M, Zhu Y, Buzzeo R, Tan J, Arendash GW, Bradshaw PC (2010) Mitochondrial amyloid-β levels are associated with the extent of mitochondrial dysfunction in different brain regions and the degree of cognitive impairment in Alzheimer’s transgenic mice. J Alzheimers Dis 20:535–550
Dragicevic N, Bradshaw PC, Mamcarz M, Lin X, Wang L, Cao C, Arendash GW (2011) Long-term electromagnetic field treatment enhances brain mitochondrial function of both Alzheimer’s transgenic mice and normal mice: a mechanism for electromagnetic field-induced cognitive benefit? Neuroscience 185:135–149
Emsley J (2011) Nature’s building blocks: an AZ guide to the elements. Oxford University Press, pp. 47–55
Fan SF, Chao PL, Lin AMY (2010) Arsenite induces oxidative injury in rat brain. Ann NY Acad Sci 1199:27–35
Florea AM, Frank S, Dietrich B (2007) Arsenic trioxide (As2O3) induced calcium signals and cytotoxicity in two human cell lines: sY-5Y neuroblastoma and 293 embryonic kidney (HEK). Toxicol Appl Pharmacol 220:292–301
Goebel HH, Schmidt PF, Bohl J, Tettenborn B, Kramer G, Gutmann L (1990) Polyneuropathy due to acute arsenic intoxication: biopsy studies. J Neuropathol Exp Neurol 49:137–149
Grandjean P, Landrigan PJ (2014) Neurobehavioural effects of developmental toxicity. Lancet Neurol 13:330–338
Hansen SH, Andersen ML, Cornett C, Gradinaru R, Grunnet N (2010) A role for taurine in mitochondrial function. J Biomed Sci 17:S23
Heath CJ, Picciotto MR (2009) Nicotine-induced plasticity during development: modulation of the cholinergic system and long-term consequences for circuits involved in attention and sensory processing. Neuropharmacology 56:254–262
Kurosawa S, Hashimoto E, Ukai W, Toki S, Saito S, Saito T (2007) Olanzapine potentiates neuronal survival and neural stem cell differentiation: regulation of endoplasmic reticulum stress response proteins. J Neural Transm 114:1121–1128
Ladran I, Tran N, Topol A, Brennand KJ (2013) Neural stem and progenitor cells in health and disease. Wiley Interdiscip Rev Syst Biol Med 5:701–715
Liu X, Piao F, Li Y (2013) Protective effect of taurine on the decreased biogenic amine neurotransmitter levels in the brain of mice exposed to arsenic. Adv Exp Med Biol 776:277–287
Lu TH, Tseng TJ, Su CC, Tang FC, Yen CC, Liu YY, Yang CY, Wu CC, Chen KL, Hung DZ, Chen YW (2014) Arsenic induces reactive oxygen species-caused neuronal cell apoptosis through JNK/ERK-mediated mitochondria-dependent and GRP 78/CHOP-regulated pathways. Toxicol Lett 224:130–140
Mandal BK, Suzuki KT (2002) Arsenic round the world: a review. Talanta 58:201–235
Mandic A, Viktorsson K, Strandberg L, Heiden T, Hansson J, Linder S, Shoshan MC (2002) Calpain-mediated Bid cleavage and calpain-independent Bak modulation: two separate pathways in cisplatin-induced apoptosis. Mol Cell Biol 22:3003–3013
Pan C, Giraldo GS, Prentice H, Wu JY (2010) Taurine protection of PC12 cells against endoplasmic reticulum stress induced by oxidative stress. Journal of Biomedical Science S17
R´ros R, Zarazúa S, Santoyo ME, Sepúlveda SJ, Romero DV, imúnez JV, Pérez-Severiano F, Delgado JM, Jiménez-Capdeville ME (2009) Decreased nitric oxide makers and morphological changes in the brain of arsenic-exposed rats. Toxicology 261:68–75
Rosado JL, Ronquillo D, Kordas K, Rojas O, Alatorre J, Lopez P, Gonzalo Garcia-Vargas G, Caamaño MC, Cebrián ME, Stoltzfus RJ (2007) Arsenic exposure and cognitive performance in Mexican schoolchildren. Environmental Health Perspectives: 371-1375
Samikkannu T, Chen CH, Yih LH, Wang ASS, Lin SY, Chen TC, Jan KY (2003) Reactive oxygen species are involved in arsenic trioxide inhibition of pyruvate dehydrogenase activity. Chem Res Toxicol 16:409–414
Sandro LP, Grãos M, Rodrigues AS, Anjo SI, Carvalho RA, Oliveira PJ, Arenas E, Ramalho-Santos J (2013) Inhibition of mitochondrial Ccomplex III blocks neuronal differentiation and maintains embryonic stem cell pluripotency. PLoS One 8:e82095
Sarkar A, Kazy SK, Sar P (2013) Characterization of arsenic resistant bacteria from arsenic rich groundwater of West Bengal, India. Ecotoxicology 22:363–376
Song B, Scheuner D, Ron D, Pennathur S, Kaufman RJ (2008) Chop deletion reduces oxidative stress, improves β cell function, and promotes cell survival in multiple mouse models of diabetes. J Clin Investig 118:3378–3389
Suzuki T, Suzuki T, Wada T, Saigo K, Watanabe K (2002) Taurine as a constituent of mitochondrial tRNAs: new insights into the functions of taurine and human mitochondrial diseases. EMBO J 21:6581–6589
Vahidnia A, Romijn F, Tiller M, Van Der Voet GB, De Wolff FA (2006) Arsenic-induced toxicity: effect on protein composition in sciatic nerve. Hum Exp Toxicol 25:667–674
Wang M, Wey S, Zhang Y, Ye R, Lee AS (2009) Role of the unfolded protein response regulator GRP78/BiP in development, cancer, and neurological disorders. Antioxid Redox Signal 11:2307–2316
Wang X, Meng D, Chang Q, Pan J, Zhang Z, Chen G, Ke Z, Luo J, Shi X (2010a) Arsenic inhibits neurite outgrowth by inhibiting the LKB1-AMPK signaling pathway. Environ Health Perspect 118:627
Wang W, Osenbroch P, Skinnes R, Esbensen Y, Bjørås M, Eide L (2010b) Mitochondrial DNA integrity is essential for mitochondrial maturation during differentiation of neural stem cells. Stem Cell 28:2195–2204
Wang W, Esbensen Y, Kunke D, Suganthan R, Rachek L, Bjørås M, Eide L (2011) Mitochondrial DNA damage level determines neural stem cell differentiation fate. J Neurosci 31:9746–9751
Wright RO, Amarasiriwardena C, Woolf AD, Jim R, Bellinger DC (2006) Neuropsychological correlates of hair arsenic, manganese, and cadmium levels in school-age children residing near a hazardous waste site. Neurotoxicology 27:210–216
Yen YP, Tsai KS, Chen YW, Huang CF, Yang RS, Liu SH (2012) Arsenic induces apoptosis in myoblasts through a reactive oxygen species-induced endoplasmic reticulum stress and mitochondrial dysfunction pathway. Arch Toxicol 86:923–933
Zhang S, Ong CN, Shen HM (2004) Critical roles of intracellular thiols and calcium in parthenolide-induced apoptosis in human colorectal cancer cells. Cancer Lett 208:143–153
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This study was supported by the National Science Council, Taiwan, and the Center of Excellence for Marine Bioenvironment and Biotechnology.
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The authors declare that they have no conflict of interest.
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Chou, CT., Lin, HT., Hwang, PA. et al. Taurine resumed neuronal differentiation in arsenite-treated N2a cells through reducing oxidative stress, endoplasmic reticulum stress, and mitochondrial dysfunction. Amino Acids 47, 735–744 (2015). https://doi.org/10.1007/s00726-014-1901-1
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DOI: https://doi.org/10.1007/s00726-014-1901-1