Hostname: page-component-586b7cd67f-l7hp2 Total loading time: 0 Render date: 2024-11-30T15:08:56.897Z Has data issue: false hasContentIssue false
  • English
  • Français

Mechanisms Underlying Taurine Protection Against Glutamate-Induced Neurotoxicity

Published online by Cambridge University Press:  23 September 2014

Hai-Bo Ye ,
Hai-Bo Shi  and
Shan-Kai Yin
Hai-Bo Ye
Affiliation:
Department of Otorhinolaryngology, Affiliated Sixth People's Hospital of Shanghai Jiaotong University, Shanghai, China
Hai-Bo Shi*
Affiliation:
Department of Otorhinolaryngology, Affiliated Sixth People's Hospital of Shanghai Jiaotong University, Shanghai, China
Shan-Kai Yin
Affiliation:
Department of Otorhinolaryngology, Affiliated Sixth People's Hospital of Shanghai Jiaotong University, Shanghai, China
*
Department of Otorhinolaryngology, Affiliated Sixth People's Hospital of Shanghai Jiaotong University, 600 yishan Road, Shanghai 200233, China. email: [email protected]
Rights & Permissions [Opens in a new window]

Abstract:

Core share and HTML view are not available for this content. However, as you have access to this content, a full PDF is available via the ‘Save PDF’ action button.

Taurine appears to exert potent protections against glutamate (Glu)-induced injury to neurons, but the underlying molecular mechanisms are not fully understood. The possibly protected targets consist of the plasma membrane and the mitochondrial as well as endoplasmic reticulum (ER) membranes. Protection may be provided through a variety of effects, including the prevention of membrane depolarization, neuronal excitotoxicity and mitochondrial energy failure, increases in intracellular free calcium ([Ca2+]i), activation of calpain, and reduction of Bcl-2 levels. These activities are likely to be linked spatially and temporally in the neuroprotective functions of taurine. In addition, events that occur downstream of Glu stimulation, including altered enzymatic activities, apoptotic pathways, and necrosis triggered by the increased [Ca2+]i, can be inhibited by taurine. This review discusses the possible molecular mechanisms of taurine against Glu-induced neuronal injury, providing a better understanding of the protective processes, which might be helpful in the development of novel interventional strategies.

Type
Review Article
Information
Canadian Journal of Neurological Sciences , Volume 40 , Issue 5 , September 2013 , pp. 628 - 634
Copyright
Copyright © The Canadian Journal of Neurological 2013

References

1.Oja, SS, Saransaari, P.Pharmacology of taurine. Proc West Pharmacol Soc. 2007;50:8–15.Google ScholarPubMed
2.Sturman, JA.Taurine in development. Physiol Rev. 1993;73(1):119–47.CrossRefGoogle ScholarPubMed
3.Young, TL, Cepko, CL.A role for ligand-gated ion channels in rod photoreceptor development. Neuron. 2004;41(6):867–79.CrossRefGoogle ScholarPubMed
4.Hayes, KC, Carey, RE, Schmidt, SY.Retinal degeneration associated with taurine deficiency in the cat. Science. 1975;188(4191):949–51.CrossRefGoogle ScholarPubMed
5.Conte Camerino, D, Tricarico, D, Pierno, S, et al.Taurine and skeletal muscle disorders. Neurochem Res. 2004;29(1):135–42.Google Scholar
6.Schaffer, SW, Czarnecki, CM, Cawthray, M, Chovan, JP.Cardiac taurine levels and sarcolemmal calcium binding activity in furazolidone-induced cardiomyopathy. Comp Biochem Physiol C. 1981;69C(1):149–51.Google Scholar
7.Pion, PD, Kittleson, MD, Rogers, QR, Morris, JG.Myocardial failure in cats associated with low plasma taurine: a reversible cardiomyopathy. Science. 1987;237(4816):764–8.CrossRefGoogle ScholarPubMed
8.Ito, T, Kimura, Y, Uozumi, Y, et al.Taurine depletion caused by knocking out the taurine transporter gene leads to cardiomyopathy with cardiac atrophy. J Mol Cell Cardiol. 2008;44(5):927–37.Google Scholar
9.Wu, JY.Purification and characterization of cysteic acid and cysteine sulfinic acid decarboxylase and L-glutamate decarboxylase from bovine brain. Proc Natl Acad Sci USA. 1982;79(14):4270–4.Google Scholar
10.Lin, CT, Song, GX, Wu, JY.Is taurine a neurotransmitter in rabbit retina? Brain Res. 1985;337(2):293–8.Google Scholar
11.Taber, KH, Lin, CT, Liu, JW, Thalmann, RH, Wu, JY.Taurine in hippocampus: localization and postsynaptic action. Brain Res. 1986;386(1-2):113–21.Google Scholar
12.Okamoto, K, Kimura, H, Sakai, Y.Taurine-induced increase of the Cl-conductance of cerebellar Purkinje cell dendrites in vitro. Brain Res. 1983;259(2):319–23.Google Scholar
13.Song, NY, Shi, HB, Li, CY, Yin, SK.Interaction between taurine and GABA(A)/glycine receptors in neurons of the rat anteroventral cochlear nucleus. Brain Res. 2012;1472:1–10.CrossRefGoogle ScholarPubMed
14.Wu, JY, Tang, XW, Tsai, WH.Taurine receptor: kinetic analysis and pharmacological studies. Adv Exp Med Biol. 1992;315:263–8.Google Scholar
15.Chesney, RW, Zelikovic, I, Jones, DP, Budreau, A, Jolly, K.The renal transport of taurine and the regulation of renal sodium-chloridedependent transporter activity. Pediatr Nephrol. 1990;4(4):399–407.Google Scholar
16.Li, JH, Ling, YQ, Fan, JJ, Zhang, XP, Cui, S.Expression of cysteine sulfinate decarboxylase (CSD) in male reproductive organs of mice. Histochem Cell Biol. 2006;125(6):607–13.CrossRefGoogle ScholarPubMed
17.Huxtable, RJ.Physiological actions of taurine. Physiol Rev. 1992;72(1):101–63.CrossRefGoogle ScholarPubMed
18.Bouckenooghe, T, Remacle, C, Reusens, B.Is taurine a functional nutrient? Curr Opin Clin Nutr Metab Care. 2006;9(6):728–33.Google Scholar
19.Moran, J, Salazar, P, Pasantes-Morales, H.Effect of tocopherol and taurine on membrane fluidity of retinal rod outer segments. Exp Eye Res. 1987;45(6):769–76.Google Scholar
20.El Idrissi, A.Taurine increases mitochondrial buffering of calcium: role in neuroprotection. Amino Acids. 2008;34(2):321–8.Google Scholar
21.Wu, JY, Prentice, H.Role of taurine in the central nervous system. J Biomed Sci. 2010;17 Suppl 1:S1.Google Scholar
22.Saransaari, P, Oja, SS.Release of GABA and taurine from brain slices. Prog Neurobiol. 1992;38(5):455–82.Google Scholar
23.Mutani, R, Monaco, F, Durelli, L, Delsedime, M.Levels of free amino acids in serum and cerebrospinal fluid after administration of taurine to epileptic and normal subjects. Epilepsia. 1975;16(5):765–9.Google Scholar
24.Schaffer, S, Takahashi, K, Azuma, J.Role of osmoregulation in the actions of taurine. Amino Acids. 2000;19(3-4):527–46.CrossRefGoogle ScholarPubMed
25.Wade, JV, Olson, JP, Samson, FE, Nelson, SR, Pazdernik, TL.A possible role for taurine in osmoregulation within the brain. J Neurochem. 1988;51(3):740–5.Google Scholar
26.Tang, XW, Deupree, DL, Sun, Y, Wu, JY.Biphasic effect of taurine on excitatory amino acid-induced neurotoxicity. Adv Exp Med Biol. 1996;403:499–505.Google Scholar
27.Azuma, J, Takihara, K, Awata, N, et al.Taurine and failing heart: experimental and clinical aspects. Prog Clin Biol Res. 1985;179:195–213.Google ScholarPubMed
28.Smith, LJ, Lacaille, F, Lepage, G, Ronco, N, Lamarre, A, Roy, CC.Taurine decreases fecal fatty acid and sterol excretion in cystic fibrosis. A randomized double-blind trial. Am J Dis Child. 1991;145(12):1401–4.Google Scholar
29.Matsuyama, Y, Morita, T, Higuchi, M, Tsujii, T.The effect of taurine administration on patients with acute hepatitis. Prog Clin Biol Res. 1983;125:461–8.Google Scholar
30.Airaksinen, EM, Oja, SS, Marnela, KM, Leino, E, Paakkonen, L.Effects of taurine treatment on epileptic patients. Prog Clin biol Res. 1980;39:157–66.Google Scholar
31.Csernansky, JG, Bardgett, ME, Sheline, YI, Morris, JC, Olney, JW.CSF excitatory amino acids and severity of illness in Alzheimer's disease. Neurology. 1996;46(6):1715–20.CrossRefGoogle ScholarPubMed
32.Fonnum, F.Glutamate: a neurotransmitter in mammalian brain. J Neurochem. 1984;42(1):1–11.Google Scholar
33.Hirai, K, Yoshioka, H, Kihara, M, et al.Inhibiting neuronal migration by blocking NMDA receptors in the embryonic rat cerebral cortex: a tissue culture study. Brain Res Dev Brain Res. 1999;114(1):63–7.Google Scholar
34.Ikonomidou, C, Bosch, F, Miksa, M, et al.Blockade of NMDA receptors and apoptotic neurodegeneration in the developing brain. Science. 1999;283(5398):70–4.CrossRefGoogle ScholarPubMed
35.Behar, TN, Scott, CA, Greene, CL, et al.Glutamate acting at NMDA receptors stimulates embryonic cortical neuronal migration. J Neurosci. 1999;19(11):4449–61.Google Scholar
36.Wu, G, Malinow, R, Cline, HT.Maturation of a central glutamatergic synapse. Science. 1996;274(5289):972–6.Google Scholar
37.Gurevich, VS.[Taurine and the function of excitable tissues]. Fiziol Zh SSSR Im I M Sechenova. 1984;70(7):1046–56.Google ScholarPubMed
38.Bonfoco, E, Krainc, D, Ankarcrona, M, Nicotera, P, Lipton, SA.Apoptosis and necrosis: two distinct events induced, respectively, by mild and intense insults with N-methyl-D-aspartate or nitric oxide/superoxide in cortical cell cultures. Proc Natl Acad Sci USA. 1995;92(16):7162–6.Google Scholar
39.Lau, A, Tymianski, M.Glutamate receptors, neurotoxicity and neurodegeneration. Pflugers Arch. 2010;460(2):525–42.CrossRefGoogle ScholarPubMed
40.Saransaari, P, Oja, SS.Taurine and neural cell damage. Amino Acids. 2000;19(3-4):509–26.Google Scholar
41.Wu, JY, Wu, H, Jin, Y, et al.Mechanism of neuroprotective function of taurine. Adv Exp Med Biol. 2009;643:169–79.Google Scholar
42.Mankovskaya, IN, Serebrovskaya, TV, Swanson, RJ, Vavilova, GL, Kharlamova, ON.Mechanisms of taurine antihypoxic and antioxidant action. High Alt Med Biol. 2000;1(2):105–10.Google Scholar
43.Jong, CJ, Azuma, J, Schaffer, S.Mechanism underlying the antioxidant activity of taurine: prevention of mitochondrial oxidant production. Amino Acids. 2012;42(6):2223–32.Google Scholar
44.El Idrissi, A, Trenkner, E.Growth factors and taurine protect against excitotoxicity by stabilizing calcium homeostasis and energy metabolism. J Neurosci. 1999;19(21):9459–68.CrossRefGoogle ScholarPubMed
45.Kocak-Toker, N, Giris, M, Tulubas, F, Uysal, M, Aykac-Toker, G.Peroxynitrite induced decrease in Na+, K+-ATPase activity is restored by taurine. World J Gastroenterol. 2005;11(23):3554–7.Google Scholar
46.Magalov, Shl, Arzumanova, KG.[Familial Friedreich's ataxia (review of foreign literature)]. Zh Nevropatol Psikhiatr Im S S Korsakova. 1989;89(3):136–41.Google Scholar
47.Trenkner, E, Liu, D, Harris, C, Sturman, J.Regulation of protein kinase C activity by taurine and beta-alanine during excitotoxicity in cat and mouse cerebellar cultures. Adv Exp Med Biol. 1994;359:309–16.Google Scholar
48.Yu, X, Xu, Z, Mi, M, et al.Dietary taurine supplementation ameliorates diabetic retinopathy via anti-excitotoxicity of glutamate in streptozotocin-induced Sprague-Dawley rats. Neurochem Res. 2008;33(3):500–7.Google Scholar
49.Wu, H, Jin, Y, Wei, J, Jin, H, Sha, D, Wu, JY.mode of action of taurine as a neuroprotector. Brain Res. 2005;1038(2):123–31.Google Scholar
50.Bianchi, L, Colivicchi, MA, Ballini, C, et al.Taurine, taurine analogues, and taurine functions: overview. Adv Exp Med Biol. 2006;583:443–8.CrossRefGoogle ScholarPubMed
51.Foos, TM, Wu, JY.The role of taurine in the central nervous system and the modulation of intracellular calcium homeostasis. Neurochem Res. 2002;27(1-2):21–6.Google Scholar
52.Brustovetsky, N, Dubinsky, JM.Dual responses of CNS mitochondria to elevated calcium. J Neurosci. 2000;20(1):103–13.CrossRefGoogle ScholarPubMed
53.Khodorov, B.Glutamate-induced deregulation of calcium homeostasis and mitochondrial dysfunction in mammalian central neurones. Prog Biophys Mol Biol. 2004;86(2):279–351.Google Scholar
54.Takatani, T, Takahashi, K, Uozumi, Y, et al.Taurine inhibits apoptosis by preventing formation of the Apaf-1/caspase-9 apoptosome. Am J Physiol Cell Physiol. 2004;287(4):C949–53.Google Scholar
55.Sun, M, Xu, C.Neuroprotective mechanism of taurine due to up-regulating calpastatin and down-regulating calpain and caspase-3 during focal cerebral ischemia. Cell Mol Neurobiol. 2008;28(4):593–611.CrossRefGoogle ScholarPubMed
56.Tenneti, L, Lipton, SA.Involvement of activated caspase-3-like proteases in N-methyl-D-aspartate-induced apoptosis in cerebrocortical neurons. J Neurochem. 2000;74(1):134–42.Google Scholar
57.Bachis, A, Colangelo, AM, Vicini, S, et al.Interleukin-10 prevents glutamate-mediated cerebellar granule cell death by blocking caspase-3-like activity. J Neurosci. 2001;21(9):3104–12.Google Scholar
58.Schinder, AF, Olson, EC, Spitzer, NC, Montal, M.Mitochondrial dysfunction is a primary event in glutamate neurotoxicity. J Neurosci. 1996;16(19):6125–33.Google Scholar
59.White, RJ, Reynolds, IJ.mitochondrial depolarization in glutamate-stimulated neurons: an early signal specific to excitotoxin exposure. J Neurosci. 1996;16(18):5688–97.CrossRefGoogle ScholarPubMed
60.Green, D, Kroemer, G.The central executioners of apoptosis: caspases or mitochondria? Trends Cell Biol. 1998;8(7):267–71.Google Scholar
61.Gil-Parrado, S, Fernandez-Montalvan, A, Assfalg-Machleidt, I, et al.Ionomycin-activated calpain triggers apoptosis. A probable role for Bcl-2 family members. J Biol Chem. 2002;277(30):27217–26.Google Scholar
62.Gross, A, McDonnell, JM, Korsmeyer, SJ.BCL-2 family members and the mitochondria in apoptosis. Genes Dev. 1999;13(15):1899–911.Google Scholar
63.Choi, DW, Rothman, SM.The role of glutamate neurotoxicity in hypoxic-ischemic neuronal death. Annu Rev Neurosci. 1990;13:171–82.Google Scholar
64.El Idrissi, A, Trenkner, E.Taurine as a modulator of excitatory and inhibitory neurotransmission. Neurochem Res. 2004;29(1):189–97.Google Scholar
65.Takatani, T, Takahashi, K, Uozumi, Y, et al.Taurine prevents the ischemia-induced apoptosis in cultured neonatal rat cardiomyocytes through Akt/caspase-9 pathway. Biochem Biophys Res Commun. 2004;316(2):484–9.CrossRefGoogle ScholarPubMed
66.Wang, GH, Jiang, ZL, Fan, XJ, Zhang, L, Li, X, Ke, KF.Neuroprotective effect of taurine against focal cerebral ischemia in rats possibly mediated by activation of both GABAA and glycine receptors. Neuropharmacology. 2007;52(5):1199–209.Google Scholar
67.Taranukhin, AG, Taranukhina, EY, Saransaari, P, Djatchkova, IM, Pelto-Huikko, M, Oja, SS.Taurine reduces caspase-8 and caspase-9 expression induced by ischemia in the mouse hypothalamic nuclei. Amino Acids. 2008;34(1):169–74.Google Scholar
68.Sun, M, Gu, Y, Zhao, Y, Xu, C.Protective functions of taurine against experimental stroke through depressing mitochondria-mediated cell death in rats. Amino Acids. 2011;40(5):1419–29.Google Scholar
69.Anelli, T, Sitia, R.Protein quality control in the early secretory pathway. EMBO J. 2008;27(2):315–27.Google Scholar
70.Ma, Y, Hendershot, LM.ER chaperone functions during normal and stress conditions. J Chem Neuroanat. 2004;28(1-2):51–65.Google Scholar
71.Pizzo, P, Pozzan, T.Mitochondria-endoplasmic reticulum choreography: structure and signaling dynamics. Trends Cell Biol. 2007;17(10):511–7.CrossRefGoogle ScholarPubMed
72.Azfer, A, Niu, J, Rogers, LM, Adamski, FM, Kolattukudy, PE.Activation of endoplasmic reticulum stress response during the development of ischemic heart disease. Am J Physiol Heart Circ Physiol. 2006;291(3):H1411–20.CrossRefGoogle ScholarPubMed
73.DeGracia, DJ, Montie, HL.Cerebral ischemia and the unfolded protein response. J Neurochem. 2004;91(1):1–8.Google Scholar
74.Nicholls, D, Attwell, D.The release and uptake of excitatory amino acids. Trends Pharmacol Sci. 1990;11(11):462–8.Google Scholar
75.Pan, C, Prentice, H, Price, AL, Wu, JY.Beneficial effect of taurine on hypoxia- and glutamate-induced endoplasmic reticulum stress pathways in primary neuronal culture. Amino Acids. 2012;43(2):845–55.Google Scholar
76.Pan, C, Gupta, A, Prentice, H, Wu, JY.Protection of taurine and granulocyte colony-stimulating factor against excitotoxicity induced by glutamate in primary cortical neurons. J Biomed Sci. 2010;17 Suppl 1:S18.CrossRefGoogle ScholarPubMed
77.Jatzke, C, Watanabe, J, Wollmuth, LP.Voltage and concentration dependence of Ca(2+) permeability in recombinant glutamate receptor subtypes. J Physiol. 2002 Jan 1;538(Pt 1):25–39.Google Scholar
78.Lazarewicz, JW, Noremberg, K, Lehmann, A, Hamberger, A.Effects of taurine on calcium binding and accumulation in rabbit hippocampal and cortical synaptosomes. Neurochem Int. 1985;7(3):421–7.Google Scholar
79.Lombardini, JB.Effects of taurine on calcium ion uptake and protein phosphorylation in rat retinal membrane preparations. J Neurochem. 1985;45(1):268–75.Google Scholar
80.Takahashi, K, Azuma, J, Awata, N, et al.Protective effect of taurine on the irregular beating pattern of cultured myocardial cells induced by high and low extracellular calcium ion. J Mol Cell Cardiol. 1988;20(5):397–403.Google Scholar
81.Liu, HY, Chi, FL, Gao, WY.Taurine modulates calcium influx under normal and ototoxic conditions in isolated cochlear spiral ganglion neurons. Pharmacol Rep. 2008;60(4):508–13.Google Scholar
82.Liu, HY, Gao, WY, Wen, W, Zhang, YM.Taurine modulates calcium influx through L-type voltage-gated calcium channels in isolated cochlear outer hair cells in guinea pigs. Neurosci Lett. 2006;399 (1-2):23–6.Google Scholar
83.Chen, WQ, Jin, H, Nguyen, M, et al.Role of taurine in regulation of intracellular calcium level and neuroprotective function in cultured neurons. J Neurosci Res. 2001;66(4):612–9.Google Scholar
84.Takuma, K, Matsuda, T, Hashimoto, H, Asano, S, Baba, A.Cultured rat astrocytes possess Na(+)-Ca2+ exchanger. Glia. 1994;12(4):336–42.Google Scholar
85.Schaffer, S, Azuma, J, Takahashi, K, Mozaffari, M.Why is taurine cytoprotective? Adv Exp Med Biol. 2003;526:307–21.Google Scholar
86.Leon, R, Wu, H, Jin, Y, et al.Protective function of taurine in glutamate-induced apoptosis in cultured neurons. J Neurosci Res. 2009;87(5):1185–94.Google Scholar
87.Oja, SS, Saransaari, P.Modulation of taurine release by glutamate receptors and nitric oxide. Prog Neurobiol. 2000;62(4):407–25.CrossRefGoogle ScholarPubMed
88.Saransaari, P, Oja, SS.Mechanisms of inhibitory amino acid release in the brain stem under normal and ischemic conditions. Neurochem Res. 2010;35(12):1948–56.Google Scholar
89.Duan, Y, Gross, RA, Sheu, SS.Ca2+-dependent generation of mitochondrial reactive oxygen species serves as a signal for poly(ADP-ribose) polymerase-1 activation during glutamate excitotoxicity. J Physiol. 2007;585(Pt 3):741–58.Google Scholar
90.Araujo, IM, Verdasca, MJ, Leal, EC, et al.Early calpain-mediated proteolysis following AMPA receptor activation compromises neuronal survival in cultured hippocampal neurons. J Neurochem. 2004;91(6):1322–31.Google Scholar
91.Del Olmo, N, Bustamante, J, del Rio, RM, Solis, JM.Taurine activates GABA(A) but not GABA(B) receptors in rat hippocampal CA1 area. Brain Res. 2000;864(2):298–307.Google Scholar
92.Ricci, L, Valoti, M, Sgaragli, G, Frosini, M.Protection by taurine of rat brain cortical slices against oxygen glucose deprivation- and reoxygenation-induced damage. Eur J Pharmacol. 2009;621(1-3):26–32.Google Scholar