Ischemic stroke exhibits a multiplicity of pathophysiological mechanisms. To address the diverse pathophysiological mechanisms observed in ischemic stroke investigators seek to find therapeutic strategies that are multifaceted in their action by either investigating multipotential compounds or by using a combination of compounds. Taurine, an endogenous amino acid, exhibits a plethora of physiological functions. It exhibits antioxidative properties, stabilizes membrane, functions as an osmoregulator, modulates ionic movements, reduces the level of pro-inflammators, regulates intracellular calcium concentration; all of which contributes to its neuroprotective effect. Data are accumulating that show the neuroprotective mechanisms of taurine against stroke pathophysiology. In this review, we describe the neuroprotective mechanisms employed by taurine against ischemic stroke and its use in clinical trial for ischemic stroke.
References
[1]
Feigin, V.L.; Lawes, C.M.M.; Bennett, D.A.; Barker-Collo, S.L.; Parag, V. Worldwide stroke incidence and early case fatality reported in 56 population-based studies: A systematic review. Lancet Neurol. 2009, 8, 355–369, doi:10.1016/S1474-4422(09)70025-0.
[2]
Strong, K.; Mathers, C.; Bonita, R. Preventing stroke: Saving lives around the world. Lancet Neurol. 2007, 6, 182–187, doi:10.1016/S1474-4422(07)70031-5.
[3]
MacKay, J.; Mensah, G. The Atlast of Heart Disease and Stroke; World Health Organization: Geneva, Switzerland, 2004; pp. 50–53.
[4]
Tackling the global burden of stroke. Lancet Neurol. 2005, 4, 689, doi:10.1016/S1474-4422(05)70202-7.
[5]
Rosamond, W.; Flegal, K.; Friday, G.; Furie, K.; Go, A.; Greenlund, K.; Haase, N.; Ho, M.; Howard, V.; Kissela, B.; et al. Heart disease and stroke statistics—2007 update: A report from the American Heart Association Statistics Committee and Stroke Statistics Subcommittee. Circulation 2007, 115, 169–171.
[6]
Kirino, Y.; Yasukawa, T.; Ohta, S.; Akira, S.; Ishihara, K.; Watanabe, K.; Suzuki, T. Codon-specific translational defect caused by a wobble modification deficiency in mutant tRNA from a human mitochondrial disease. Proc. Natl. Acad. Sci. USA 2004, 101, 15070–15075, doi:10.1073/pnas.0405173101.
Hossmann, K.A. Pathophysiology and therapy of experimental stroke. Cell. Mol. Neurobiol. 2006, 26, 1057–1083, doi:10.1007/s10571-006-9008-1.
[9]
Hossmann, K.A. Viability thresholds and the penumbra of focal ischemia. Ann. Neurol. 1994, 36, 557–565, doi:10.1002/ana.410360404.
[10]
Heiss, W.D.; Grond, M.; Thiel, A.; Von Stockhausen, H.M.; Rudolf, J.; Ghaemi, M.; L?ttgen, J.; Stenzel, C.; Pawlik, G. Tissue at risk of infarction rescued by early reperfusion: A positron emission tomography study in systemic recombinant tissue plasminogen activator thrombolysis of acute stroke. J. Cereb. Blood Flow Metab. 1998, 18, 1298–1307.
[11]
Obrenovitch, T.P. The ischaemic penumbra: Twenty years on. Cerebrovasc. Brain Metab. Rev. 1995, 7, 297–323.
[12]
Fisher, M.; Garcia, J.H. Evolving stroke and the ischemic penumbra. Neurology 1996, 47, 884–888, doi:10.1212/WNL.47.4.884.
[13]
The National Institute of Neurological Disorders and Stroke (NINDS) rt-PA Stroke Study Group. Tissue Plasminogen Activator for Acute Ischemic Stroke. N. Engl. J. Med. 1995, 333, 1581–1588, doi:10.1056/NEJM199512143332401.
[14]
Hacke, W.; Kaste, M.; Bluhmki, E.; Brozman, M.; Dávalos, A.; Guidetti, D.; Larrue, V.; Lees, K.R.; Medeghri, Z.; Machnig, T.; et al. Thrombolysis with alteplase 3 to 4.5 hours after acute ischemic stroke. N. Engl. J. Med. 2008, 359, 1317–1329, doi:10.1056/NEJMoa0804656.
[15]
Jacobsen, J.G.; Smith, L.H. Biochemistry and physiology of taurine and taurine derivatives. Physiol. Rev. 1968, 48, 424–511.
[16]
Reichelt, K.L.; Edminson, P.D. Biogenic amine specificity of cortical peptide synthesis in monkey brain. FEBS Lett. 1974, 47, 185–189, doi:10.1016/0014-5793(74)80455-2.
[17]
Macaione, S.; Ruggeri, P.; De Luca, F.; Tucci, G. Free Amino Acids in Developing Rat Retina. J. Neurochem. 1974, 22, 887–891, doi:10.1111/j.1471-4159.1974.tb04313.x.
[18]
Huxtable, R.J. Metabolism and function of taurine in the heart. In Taurine; Raven Press: New York, NY, USA, 1976; pp. 99–119.
Saransaari, P.; Oja, S.S. Taurine and neural cell damage. Amino Acids 2000, 19, 509–526, doi:10.1007/s007260070003.
[21]
Warskulat, U.; Fl?gel, U.; Jacoby, C.; Hartwig, H.-G.; Thewissen, M.; Merx, M.W.; Molojavyi, A.; Heller-Stilb, B.; Schrader, J.; H?ussinger, D. Taurine transporter knockout depletes muscle taurine levels and results in severe skeletal muscle impairment but leaves cardiac function uncompromised. FASEB J. 2004, 18, 577–579.
[22]
Oja, S.S.; Saransaari, P. Pharmacology of Taurine. Proc. West. Pharmacol. Soc. 2007, 50, 8–15.
[23]
Wu, J.Y. 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, 4270–4274, doi:10.1073/pnas.79.14.4270.
Stapleton, P.P.; Charles, R.P.; Redmond, H.P.; Bouchier-Hayes, D.J. Taurine and human nutrition. Clin. Nutr. 1997, 16, 103–108, doi:10.1016/S0261-5614(97)80234-8.
[26]
Yamori, Y.; Taguchi, T.; Hamada, A.; Kunimasa, K.; Mori, H.; Mori, M. Taurine in health and diseases: Consistent evidence from experimental and epidemiological studies. J. Biomed. Sci. 2010, 17, S6, doi:10.1186/1423-0127-17-S1-S6.
[27]
Curtis, D.R.; Watkins, J.C. The pharmacology of amino acids related to gamma-aminobutyric acid. Pharmacol. Rev. 1965, 17, 347–391.
Hayes, K.C.; Carey, R.E.; Schmidt, S.Y. Retinal degeneration associated with taurine deficiency in the cat. Science 1975, 188, 949–951.
[30]
Imaki, H.; Jacobson, S.G.; Kemp, C.M.; Knighton, R.W.; Neuringer, M.; Sturman, J. Retinal morphology and visual pigment levels in 6- and 12-month-old rhesus monkeys fed a taurine-free human infant formula. J. Neurosci. Res. 1993, 36, 290–304, doi:10.1002/jnr.490360307.
[31]
Militante, J.D.; Lombardini, J.B. Taurine: Evidence of physiological function in the retina. Nutr. Neurosci. 2002, 5, 75–90, doi:10.1080/10284150290018991.
[32]
Bulley, S.; Liu, Y.; Ripps, H.; Shen, W. Taurine activates delayed rectifier KV channels via a metabotropic pathway in retinal neurons. J. Physiol. 2013, 591, 123–132, doi:10.1113/jphysiol.2012.243147.
[33]
Ito, T.; Kimura, Y.; Uozumi, Y.; Takai, M.; Muraoka, S.; Matsuda, T.; Ueki, K.; Yoshiyama, M.; Ikawa, M.; Okabe, M.; Schaffer, S.W.; Fujio, Y.; Azuma, J. Taurine depletion caused by knocking out the taurine transporter gene leads to cardiomyopathy with cardiac atrophy. J. Mol. Cell. Cardiol. 2008, 44, 927–937, doi:10.1016/j.yjmcc.2008.03.001.
[34]
Schaffer, S.W.; Jong, C.J.; Ramila, K.C.; Azuma, J. Physiological roles of taurine in heart and muscle. J. Biomed. Sci. 2010, 17, S2, doi:10.1186/1423-0127-17-S1-S2.
[35]
Sturman, J.A. Taurine in Development. Physiol. Rev. 1993, 73, 119–147.
[36]
L’Amoreaux, W.J.; Cuttitta, C.; Santora, A.; Blaize, J.F.; Tachjadi, J.; El Idrissi, A. Taurine regulates insulin release from pancreatic beta cell lines. J. Biomed. Sci. 2010, 17, S11, doi:10.1186/1423-0127-17-S1-S11.
[37]
Sturman, J.A.; Moretz, R.C.; French, J.H.; Wisniewski, H.M. Taurine deficiency in the developing cat: Persistence of the cerebellar external granule cell layer. J. Neurosci. Res. 1985, 13, 405–416, doi:10.1002/jnr.490130307.
[38]
Sturman, J.A.; Moretz, R.C.; French, J.H.; Wisniewski, H.M. Postnatal taurine deficiency in the kitten results in a persistence of the cerebellar external granule cell layer: Correction by taurine feeding. J. Neurosci. Res. 1985, 13, 521–528, doi:10.1002/jnr.490130407.
[39]
Neuringer, M.; Palackal, T.; Kujawa, M.; Moretz, R.C.; Sturman, J.A. Visual cortex development in rhesus monkeys deprived of dietary taurine. Prog. Clin. Biol. Res. 1990, 351, 415–422.
[40]
Hernández-Benítez, R.; Pasantes-Morales, H.; Salda?a, I.T.; Ramos-Mandujano, G. Taurine stimulates proliferation of mice embryonic cultured neural progenitor cells. J. Neurosci. Res. 2010, 88, 1673–1681.
[41]
Hernández-Benítez, R.; Ramos-Mandujano, G.; Pasantes-Morales, H. Taurine stimulates proliferation and promotes neurogenesis of mouse adult cultured neural stem/progenitor cells. Stem Cell Res. 2012, 9, 24–34, doi:10.1016/j.scr.2012.02.004.
[42]
Bianchi, L.; Colivicchi, M.A.; Ballini, C.; Fattori, M.; Venturi, C.; Giovannini, M.G.; Healy, J.; Tipton, K.F.; Della Corte, L. Taurine, taurine analogues, and taurine functions: Overview. Adv. Exp. Med. Biol. 2006, 583, 443–448, doi:10.1007/978-0-387-33504-9_51.
[43]
Ripps, H.; Shen, W. Review: Taurine: A “very essential” amino acid. Mol. Vis. 2012, 18, 2673–2686.
[44]
Anuradha, C.V.; Balakrishnan, S.D. Taurine attenuates hypertension and improves insulin sensitivity in the fructose-fed rat, an animal model of insulin resistance. Can. J. Physiol. Pharmacol. 1999, 77, 749–754, doi:10.1139/y99-060.
[45]
Nakaya, Y.; Minami, A.; Harada, N.; Sakamoto, S.; Niwa, Y.; Ohnaka, M. Taurine improves insulin sensitivity in the Otsuka Long-Evans Tokushima Fatty rat, a model of spontaneous type 2 diabetes. Am. J. Clin. Nutr. 2000, 71, 54–58.
[46]
Ito, T.; Schaffer, S.W.; Azuma, J. The potential usefulness of taurine on diabetes mellitus and its complications. Amino Acids 2012, 42, 1529–1539, doi:10.1007/s00726-011-0883-5.
[47]
Murakami, S. Taurine and atherosclerosis. Amino Acids 2012, doi:10.1007/s00726-012-1432-6.
[48]
Menzie, J.; Pan, C.; Prentice, H.; Wu, J.-Y. Taurine and central nervous system disorders. Amino Acids 2012, doi:10.1007/s00726-012-1382-z.
[49]
Pion, P.D.; Kittleson, M.D.; Rogers, Q.R.; Morris, J.G. Myocardial failure in cats associated with low plasma taurine: A reversible cardiomyopathy. Science 1987, 237, 764–768.
[50]
Zulli, A. Taurine in cardiovascular disease. Curr. Opin. Clin. Nutr. Metab. Care 2011, 14, 57–60, doi:10.1097/MCO.0b013e328340d863.
[51]
Tsuji, A.; Tamai, I. Sodium- and chloride-dependent transport of taurine at the blood-brain barrier. Adv. Exp. Med. Biol. 1996, 403, 385–391.
[52]
Salim?ki, J.; Scriba, G.; Piepponen, T.P.; Rautolahti, N.; Ahtee, L. The effects of systemically administered taurine and N-pivaloyltaurine on striatal extracellular dopamine and taurine in freely moving rats. Naunyn Schmiedebergs Arch. Pharmacol. 2003, 368, 134–141, doi:10.1007/s00210-003-0776-6.
[53]
Huxtable, R.J. Taurine in the central nervous system and the mammalian actions of taurine. Prog. Neurobiol. 1989, 32, 471–533, doi:10.1016/0301-0082(89)90019-1.
[54]
Wu, J.-Y.; Prentice, H. Role of taurine in the central nervous system. J. Biomed. Sci. 2010, 17, S1, doi:10.1186/1423-0127-17-S1-S1.
[55]
Kuriyama, K. Taurine as a neuromodulator. Fed. Proc. 1980, 39, 2680–2684.
[56]
El Idrissi, A.; Trenkner, E. Taurine as a modulator of excitatory and inhibitory neurotransmission. Neurochem. Res. 2004, 29, 189–197, doi:10.1023/B:NERE.0000010448.17740.6e.
[57]
Banerjee, R.; Vitvitsky, V.; Garg, S.K. The undertow of sulfur metabolism on glutamatergic neurotransmission. Trends Biochem. Sci. 2008, 33, 413–419, doi:10.1016/j.tibs.2008.06.006.
[58]
Saransaari, P.; Oja, S.S. Taurine release in mouse brain stem slices under cell-damaging conditions. Amino Acids 2007, 32, 439–446, doi:10.1007/s00726-006-0375-1.
[59]
Chen, W.Q.; Jin, H.; Nguyen, M.; Carr, J.; Lee, Y.J.; Hsu, C.C.; Faiman, M.D.; Schloss, J.V.; Wu, J.Y. Role of taurine in regulation of intracellular calcium level and neuroprotective function in cultured neurons. J. Neurosci. Res. 2001, 66, 612–619, doi:10.1002/jnr.10027.
[60]
Foos, T.M.; Wu, J.-Y. The role of taurine in the central nervous system and the modulation of intracellular calcium homeostasis. Neurochem. Res. 2002, 27, 21–26, doi:10.1023/A:1014890219513.
[61]
El Idrissi, A.; Trenkner, E. Growth factors and taurine protect against excitotoxicity by stabilizing calcium homeostasis and energy metabolism. J. Neurosci. 1999, 19, 9459–9468.
[62]
El Idrissi, A.; Trenkner, E. Taurine regulates mitochondrial calcium homeostasis. Adv. Exp. Med. Biol. 2003, 526, 527–536.
[63]
El Idrissi, A. Taurine increases mitochondrial buffering of calcium: Role in neuroprotection. Amino Acids 2008, 34, 321–328, doi:10.1007/s00726-006-0396-9.
[64]
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, 769–776, doi:10.1016/S0014-4835(87)80094-5.
[65]
Hagar, H.H. The protective effect of taurine against cyclosporine A-induced oxidative stress and hepatotoxicity in rats. Toxicol. Lett. 2004, 151, 335–343, doi:10.1016/j.toxlet.2004.03.002.
[66]
Schaffer, S.W.; Azuma, J.; Mozaffari, M. Role of antioxidant activity of taurine in diabetes. Can. J. Physiol. Pharmacol. 2009, 87, 91–99, doi:10.1139/Y08-110.
[67]
Miao, J.; Zhang, J.; Zheng, L.; Yu, X.; Zhu, W.; Zou, S. Taurine attenuates Streptococcus uberis-induced mastitis in rats by increasing T regulatory cells. Amino Acids 2012, 42, 2417–2428, doi:10.1007/s00726-011-1047-3.
[68]
Sun, M.; Zhao, Y.; Gu, Y.; Xu, C. Anti-inflammatory mechanism of taurine against ischemic stroke is related to down-regulation of PARP and NF-κB. Amino Acids 2012, 42, 1735–1747, doi:10.1007/s00726-011-0885-3.
[69]
Wu, H.; Jin, Y.; Wei, J.; Jin, H.; Sha, D.; Wu, J.-Y. Mode of action of taurine as a neuroprotector. Brain Res. 2005, 1038, 123–131, doi:10.1016/j.brainres.2005.01.058.
[70]
Leon, R.; Wu, H.; Jin, Y.; Wei, J.; Buddhala, C.; Prentice, H.; Wu, J.-Y. Protective function of taurine in glutamate-induced apoptosis in cultured neurons. J. Neurosci. Res. 2009, 87, 1185–1194, doi:10.1002/jnr.21926.
[71]
Junyent, F.; Romero, R.; de Lemos, L.; Utrera, J.; Camins, A.; Pallàs, M.; Auladell, C. Taurine treatment inhibits CaMKII activity and modulates the presence of calbindin D28k, calretinin, and parvalbumin in the brain. J. Neurosci. Res. 2010, 88, 136–142, doi:10.1002/jnr.22192.
[72]
Pan, C.; Giraldo, G.S.; Prentice, H.; Wu, J.-Y. Taurine protection of PC12 cells against endoplasmic reticulum stress induced by oxidative stress. J. Biomed. Sci. 2010, 17, S17, doi:10.1186/1423-0127-17-S1-S17.
[73]
Pan, C.; Prentice, H.; Price, A.L.; Wu, J.-Y. Beneficial effect of taurine on hypoxia- and glutamate-induced endoplasmic reticulum stress pathways in primary neuronal culture. Amino Acids 2012, 43, 845–855.
[74]
Lima, L.; Cubillos, S. Taurine might be acting as a trophic factor in the retina by modulating phosphorylation of cellular proteins. J. Neurosci. Res. 1998, 53, 377–384, doi:10.1002/(SICI)1097-4547(19980801)53:3<377::AID-JNR12>3.0.CO;2-2.
[75]
Kontro, P.; Oja, S.S. Sodium-independent taurine binding to brain synaptic membranes. Cell. Mol. Neurobiol. 1983, 3, 183–187.
[76]
Wu, J.Y.; Moss, L.G.; Chen, M.S. Tissue and regional distribution of cysteic acid decarboxylase. A new assay method. Neurochem. Res. 1979, 4, 201–212, doi:10.1007/BF00964144.
[77]
Magnusson, K.R.; Clements, J.R.; Wu, J.Y.; Beitz, A.J. Colocalization of taurine- and cysteine sulfinic acid decarboxylase-like immunoreactivity in the hippocampus of the rat. Synapse 1989, 4, 55–69, doi:10.1002/syn.890040107.
[78]
Philibert, R.A.; Rogers, K.L.; Dutton, G.R. Stimulus-coupled taurine efflux from cerebellar neuronal cultures: On the roles of Ca2+ and Na+. J. Neurosci. Res. 1989, 22, 167–171, doi:10.1002/jnr.490220209.
[79]
Martin, D.L. Synthesis and release of neuroactive substances by glial cells. Glia 1992, 5, 81–94, doi:10.1002/glia.440050202.
[80]
Kozlowski, D.J.; Chen, Z.; Zhuang, L.; Fei, Y.J.; Navarre, S.; Ganapathy, V. Molecular characterization and expression pattern of taurine transporter in zebrafish during embryogenesis. Life Sci. 2008, 82, 1004–1011, doi:10.1016/j.lfs.2008.02.015.
[81]
Kang, Y.-S. Downregulation of taurine transport by calcium blockers in osteoblast cells. Adv. Exp. Med. Biol. 2009, 643, 513–521, doi:10.1007/978-0-387-75681-3_53.
[82]
Okamoto, K.; Kimura, H.; Sakai, Y. Taurine-induced increase of the Cl-conductance of cerebellar Purkinje cell dendrites in vitro. Brain Res. 1983, 259, 319–323, doi:10.1016/0006-8993(83)91266-0.
[83]
Del Olmo, N.; Bustamante, J.; Del Río, R.M.; Solís, J.M. Taurine activates GABA(A) but not GABA(B) receptors in rat hippocampal CA1 area. Brain Res. 2000, 864, 298–307, doi:10.1016/S0006-8993(00)02211-3.
[84]
Albrecht, J.; Schousboe, A. Taurine interaction with neurotransmitter receptors in the CNS: An update. Neurochem. Res. 2005, 30, 1615–1621, doi:10.1007/s11064-005-8986-6.
[85]
Wu, J.; Kohno, T.; Georgiev, S.K.; Ikoma, M.; Ishii, H.; Petrenko, A.B.; Baba, H. Taurine activates glycine and gamma-aminobutyric acid A receptors in rat substantia gelatinosa neurons. Neuroreport 2008, 19, 333–337, doi:10.1097/WNR.0b013e3282f50c90.
Frosini, M.; Sesti, C.; Saponara, S.; Ricci, L.; Valoti, M.; Palmi, M.; Machetti, F.; Sgaragli, G. A specific taurine recognition site in the rabbit brain is responsible for taurine effects on thermoregulation. Br. J. Pharmacol. 2003, 139, 487–494, doi:10.1038/sj.bjp.0705274.
[88]
Astrup, J.; Siesj?, B.K.; Symon, L. Thresholds in cerebral ischemia—the ischemic penumbra. Stroke 1981, 12, 723–725, doi:10.1161/01.STR.12.6.723.
Martin, R.L.; Lloyd, H.G.; Cowan, A.I. The early events of oxygen and glucose deprivation: Setting the scene for neuronal death? Trends Neurosci. 1994, 17, 251–257, doi:10.1016/0166-2236(94)90008-6.
[91]
Katsura, K.; Kristian, T.; Siesjo, B.K. Energy metabolism, ion homeostasis, and cell damage in the brain. Biochem. Soc. Trans. 1994, 22, 991–996.
[92]
Seki, Y.; Feustel, P.J.; Keller, R.W.; Tranmer, B.I.; Kimelberg, H.K.; Robinson, S.E. Inhibition of Ischemia-Induced Glutamate Release in Rat Striatum by Dihydrokinate and an Anion Channel Blocker Editorial Comment. Stroke 1999, 30, 433–440, doi:10.1161/01.STR.30.2.433.
[93]
Globus, M.Y.-T.; Busto, R.; Dietrich, W.D.; Martinez, E.; Valdes, I.; Ginsberg, M.D. Effect of Ischemia on the in Vivo Release of Striatal Dopamine, Glutamate, and γ-Aminobutyric Acid Studied by Intracerebral Microdialysis. J. Neurochem. 1988, 51, 1455–1464, doi:10.1111/j.1471-4159.1988.tb01111.x.
[94]
Hillered, L.; Hallstr?m, A.; Segersv?rd, S.; Persson, L.; Ungerstedt, U. Dynamics of extracellular metabolites in the striatum after middle cerebral artery occlusion in the rat monitored by intracerebral microdialysis. J. Cereb. Blood Flow Metab. 1989, 9, 607–616, doi:10.1038/jcbfm.1989.87.
[95]
Butcher, S.P.; Bullock, R.; Graham, D.I.; McCulloch, J. Correlation between amino acid release and neuropathologic outcome in rat brain following middle cerebral artery occlusion. Stroke 1990, 21, 1727–1733, doi:10.1161/01.STR.21.12.1727.
[96]
Yang, G.Y.; Betz, A.L. Reperfusion-induced injury to the blood-brain barrier after middle cerebral artery occlusion in rats. Stroke 1994, 25, 1658–1664, doi:10.1161/01.STR.25.8.1658.
[97]
O’Regan, M.H.; Smith-Barbour, M.; Perkins, L.M.; Phillis, J.W. A possible role for phospholipases in the release of neurotransmitter amino acids from ischemic rat cerebral cortex. Neurosci. Lett. 1995, 185, 191–194, doi:10.1016/0304-3940(95)11259-Y.
[98]
O’Regan, M.H.; Perkins, L.M.; Phillis, J.W. Arachidonic acid and lysophosphatidylcholine modulate excitatory transmitter amino acid release from the rat cerebral cortex. Neurosci. Lett. 1995, 193, 85–88, doi:10.1016/0304-3940(95)11672-J.
[99]
Phillis, J.W.; Song, D.; O’Regan, M.H. Inhibition by anion channel blockers of ischemia-evoked release of excitotoxic and other amino acids from rat cerebral cortex. Brain Res. 1997, 758, 9–16, doi:10.1016/S0006-8993(97)00155-8.
[100]
Rutledge, E.M.; Aschner, M.; Kimelberg, H.K. Pharmacological characterization of swelling-induced d-[3H]aspartate release from primary astrocyte cultures. Am. J. Physiol. Cell Physiol. 1998, 274, 1511–1520.
[101]
Feustel, P.J.; Jin, Y.; Kimelberg, H.K. Volume-regulated anion channels are the predominant contributors to release of excitatory amino acids in the ischemic cortical penumbra. Stroke 2004, 35, 1164–1168, doi:10.1161/01.STR.0000124127.57946.a1.
[102]
Szatkowski, M.; Barbour, B.; Attwell, D. Non-vesicular release of glutamate from glial cells by reversed electrogenic glutamate uptake. Nature 1990, 348, 443–446, doi:10.1038/348443a0.
[103]
Rossi, D.J.; Oshima, T.; Attwell, D. Glutamate release in severe brain ischaemia is mainly by reversed uptake. Nature 2000, 403, 316–321, doi:10.1038/35002090.
[104]
Reuter, H.; Philipson, K.D. Sodium-calcium exchanger overexpression in the heart—insights from a transgenic mouse model. Basic Res. Cardiol. 2002, 97, 131–135.
[105]
Meldrum, B.S. Glutamate as a Neurotransmitter in the Brain: Review of Physiology and Pathology. J. Nutr. 2000, 130, 1007S–1015S.
[106]
Kwak, S.; Weiss, J.H. Calcium-permeable AMPA channels in neurodegenerative disease and ischemia. Curr. Opin. Neurobiol. 2006, 16, 281–287, doi:10.1016/j.conb.2006.05.004.
[107]
Berridge, M.J. Inositol Trisphosphate and Calcium Signaling. Ann. N. Y. Acad. Sci. 1995, 766, 31–43, doi:10.1111/j.1749-6632.1995.tb26646.x.
[108]
Sukhareva, M.; Smith, S.V.; Maric, D.; Barker, J.L. Functional Properties of Ryanodine Receptors in Hippocampal Neurons Change during Early Differentiation in Culture. J. Neurophysiol. 2002, 88, 1077–1087.
[109]
Paschen, W.; Mengesdorf, T. Endoplasmic reticulum stress response and neurodegeneration. Cell Calcium 2005, 38, 409–415, doi:10.1016/j.ceca.2005.06.019.
[110]
Ding, D.; Moskowitz, S.I.; Li, R.; Lee, S.B.; Esteban, M.; Tomaselli, K.; Chan, J.; Bergold, P.J. Acidosis induces necrosis and apoptosis of cultured hippocampal neurons. Exp. Neurol. 2000, 162, 1–12.
[111]
Yermolaieva, O.; Leonard, A.S.; Schnizler, M.K.; Abboud, F.M.; Welsh, M.J. Extracellular acidosis increases neuronal cell calcium by activating acid-sensing ion channel 1a. Proc. Natl. Acad. Sci. USA 2004, 101, 6752–6757.
[112]
Araújo, I.M.; Verdasca, M.J.; Leal, E.C.; Bahr, B.A.; Ambrósio, A.F.; Carvalho, A.P.; Carvalho, C.M. Early calpain-mediated proteolysis following AMPA receptor activation compromises neuronal survival in cultured hippocampal neurons. J. Neurochem. 2004, 91, 1322–1331, doi:10.1111/j.1471-4159.2004.02811.x.
[113]
Montague, J.; Gaido, M.; Frye, C.; Cidlowski, J. A calcium-dependent nuclease from apoptotic rat thymocytes is homologous with cyclophilin. Recombinant cyclophilins A, B, and C have nuclease activity. J. Biol. Chem. 1994, 269, 18877–18880.
[114]
Farooqui, A.A.; Yang, H.-C.; Rosenberger, T.A.; Horrocks, L.A. Phospholipase A2 and Its Role in Brain Tissue. J. Neurochem. 2002, 69, 889–901, doi:10.1046/j.1471-4159.1997.69030889.x.
[115]
Dykens, J.A. Isolated Cerebral and Cerebellar Mitochondria Produce Free Radicals when Exposed to Elevated Ca2+ and Na+: Implications for Neurodegeneration. J. Neurochem. 2002, 63, 584–591, doi:10.1046/j.1471-4159.1994.63020584.x.
[116]
Lièvre, V.; Becuwe, P.; Bianchi, A.; Bossenmeyer-Pourié, C.; Koziel, V.; Franck, P.; Nicolas, M.; Dau?a, M.; Vert, P.; Daval, J. Intracellular generation of free radicals and modifications of detoxifying enzymes in cultured neurons from the developing rat forebrain in response to transient hypoxia. Neuroscience 2001, 105, 287–297, doi:10.1016/S0306-4522(01)00189-0.
[117]
Duan, Y.; Gross, R.A.; Sheu, S.-S. 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, 741–758, doi:10.1113/jphysiol.2007.145409.
[118]
Lipton, P. Ischemic Cell Death in Brain Neurons. Physiol. Rev. 1999, 79, 1431–1568.
[119]
Nakka, V.P.; Gusain, A.; Mehta, S.L.; Raghubir, R. Molecular mechanisms of apoptosis in cerebral ischemia: Multiple neuroprotective opportunities. Mol. Neurobiol. 2008, 37, 7–38, doi:10.1007/s12035-007-8013-9.
[120]
Pellegrini-Giampietro, D.E. The distinct role of mGlu1 receptors in post-ischemic neuronal death. Trends Pharmacol Sci. 2003, 24, 461–470, doi:10.1016/S0165-6147(03)00231-1.
[121]
Yamori, Y.; Liu, L.; Mori, M.; Sagara, M.; Murakami, S.; Nara, Y.; Mizushima, S. Taurine as the nutritional factor for the longevity of the Japanese revealed by a world-wide epidemiological survey. Adv. Exp. Med. Biol. 2009, 643, 13–25, doi:10.1007/978-0-387-75681-3_2.
[122]
Wu, J.Y.; Lin, C.T.; Johansen, F.F.; Liu, J.W. Taurine neurons in rat hippocampal formation are relatively inert to cerebral ischemia. Adv. Exp. Med. Biol. 1994, 359, 289–298.
[123]
Schurr, A.; Rigor, B.M. The mechanism of neuronal resistance and adaptation to hypoxia. FEBS Lett. 1987, 224, 4–8, doi:10.1016/0014-5793(87)80411-8.
[124]
Matsumoto, K.; Lo, E.H.; Pierce, A.R.; Halpern, E.F.; Newcomb, R. Secondary elevation of extracellular neurotransmitter amino acids in the reperfusion phase following focal cerebral ischemia. J. Cereb. Blood Flow Metab. 1996, 16, 114–124.
[125]
Torp, R.; Andiné, P.; Hagberg, H.; Karagülle, T.; Blackstad, T.W.; Ottersen, O.P. Cellular and subcellular redistribution of glutamate-, glutamine- and taurine-like immunoreactivities during forebrain ischemia: A semiquantitative electron microscopic study in rat hippocampus. Neuroscience 1991, 41, 433–447, doi:10.1016/0306-4522(91)90339-P.
[126]
Uchiyama-Tsuyuki, Y.; Araki, H.; Yae, T.; Otomo, S. Changes in the Extracellular Concentrations of Amino Acids in the Rat Striatum During Transient Focal Cerebral Ischemia. J. Neurochem. 2008, 62, 1074–1078, doi:10.1046/j.1471-4159.1994.62031074.x.
[127]
Lo, E.; Pierce, A.; Matsumoto, K.; Kano, T.; Evans, C.; Newcomb, R. Alterations in K+ evoked profiles of neurotransmitter and neuromodulator amino acids after focal ischemia-reperfusion. Neuroscience 1997, 83, 449–458, doi:10.1016/S0306-4522(97)00434-X.
[128]
Oja, S.S.; Saransaari, P. Modulation of taurine release by glutamate receptors and nitric oxide. Prog. Neurobiol. 2000, 62, 407–425, doi:10.1016/S0301-0082(00)00005-8.
[129]
Barakat, L.; Wang, D.; Bordey, A. Carrier-mediated uptake and release of taurine from Bergmann glia in rat cerebellar slices. J. Physiol. 2002, 541, 753–767, doi:10.1113/jphysiol.2001.015834.
[130]
Büyükuysal, R.L. Ischemia and reoxygenation induced amino acid release and tissue damage in the slices of rat corpus striatum. Amino Acids 2004, 27, 57–67.
[131]
Saransaari, P.; Oja, S.S. Modulation of taurine release in ischemia by glutamate receptors in mouse brain stem slices. Amino Acids 2010, 38, 739–746, doi:10.1007/s00726-009-0278-z.
[132]
Fariello, R.G.; Golden, G.T.; Pisa, M. Homotaurine (3 aminopropanesulfonic acid; 3APS) protects from the convulsant and cytotoxic effect of systemically administered kainic acid. Neurology 1982, 32, 241–245, doi:10.1212/WNL.32.3.241.
[133]
French, E.D.; Vezzani, A.; Whetsell, W.O.; Schwarcz, R. Anti-excitotoxic actions of taurine in the rat hippocampus studied in vivo and in vitro. Adv. Exp. Med. Biol. 1986, 203, 349–362, doi:10.1007/978-1-4684-7971-3_26.
[134]
Wu, J.Y.; Johansen, F.F.; Lin, C.T.; Liu, J.W. Taurine system in the normal and ischemic rat hippocampus. Adv. Exp. Med. Biol. 1987, 217, 265–274.
[135]
Trenkner, E. The role of taurine and glutamate during early postnatal cerebellar development of normal and Weaver mutant mice. Adv. Exp. Med. Biol. 1990, 268, 239–244.
Wu, J.; Chen, W.; Tang, X.W.; Jin, H.; Foos, T.; Schloss, J.V.; Davis, K.; Faiman, M.D.; Hsu, C. Mode of Action of Taurine and regulation Dynamics of Its Synthesis in the CNS. Adv. Exp. Med. Biol. 2000, 483, 35–44.
Chen, W. Mode of Action of Taurine. Ph.D Thesis, University of Kansas, Lawrence, KS, USA, 2000.
[140]
Schurr, A.; Tseng, M.T.; West, C.A.; Rigor, B.M. Taurine improves the recovery of neuronal function following cerebral hypoxia: An in vitro study. Life Sci. 1987, 40, 2059–2066, doi:10.1016/0024-3205(87)90098-1.
[141]
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, 26–32, doi:10.1016/j.ejphar.2009.08.017.
[142]
Zhao, P.; Huang, Y.L.; Cheng, J.S. Taurine antagonizes calcium overload induced by glutamate or chemical hypoxia in cultured rat hippocampal neurons. Neurosci. Lett. 1999, 268, 25–28, doi:10.1016/S0304-3940(99)00373-0.
[143]
Wang, G.-H.; Jiang, Z.-L.; Fan, X.-J.; Zhang, L.; Li, X.; Ke, K.-F. Neuroprotective effect of taurine against focal cerebral ischemia in rats possibly mediated by activation of both GABAA and glycine receptors. Neuropharmacology 2007, 52, 1199–1209, doi:10.1016/j.neuropharm.2006.10.022.
[144]
Molchanova, S.M.; Oja, S.S.; Saransaari, P. Taurine attenuates d-[3H]aspartate release evoked by depolarization in ischemic corticostriatal slices. Brain Res. 2006, 1099, 64–72, doi:10.1016/j.brainres.2006.04.105.
[145]
Nicholls, D.G. Mitochondrial calcium function and dysfunction in the central nervous system. Biochim. Biophys. Acta 2009, 1787, 1416–1424, doi:10.1016/j.bbabio.2009.03.010.
[146]
Brustovetsky, N.; Brustovetsky, T.; Jemmerson, R.; Dubinsky, J.M. Calcium-induced cytochrome c release from CNS mitochondria is associated with the permeability transition and rupture of the outer membrane. J. Neurochem. 2002, 80, 207–218, doi:10.1046/j.0022-3042.2001.00671.x.
[147]
Bernardi, P.; Krauskopf, A.; Basso, E.; Petronilli, V.; Blachly-Dyson, E.; Blalchy-Dyson, E.; Di Lisa, F.; Forte, M.A. The mitochondrial permeability transition from in vitro artifact to disease target. FEBS J. 2006, 273, 2077–2099, doi:10.1111/j.1742-4658.2006.05213.x.
[148]
Jemmerson, R.; Dubinsky, J.M.; Brustovetsky, N. Cytochrome C release from CNS mitochondria and potential for clinical intervention in apoptosis-mediated CNS diseases. Antioxid. Redox Signal. 2005, 7, 1158–1172, doi:10.1089/ars.2005.7.1158.
[149]
Dedkova, E.N.; Ji, X.; Lipsius, S.L.; Blatter, L.A. Mitochondrial calcium uptake stimulates nitric oxide production in mitochondria of bovine vascular endothelial cells. Am J. Physiol. Cell Physiol. 2004, 286, 406–415, doi:10.1152/ajpcell.00155.2003.
[150]
Ottersen, O.P. Quantitative assessment of taurine-like immunoreactivity in different cell types and processes in rat cerebellum: An electronmicroscopic study based on a postembedding immunogold labelling procedure. Anat. Embryol. 1988, 178, 407–421, doi:10.1007/BF00306047.
[151]
Lobo, M.V.; Alonso, F.J.; Martin del Rio, R. Immunocytochemical localization of taurine in different muscle cell types of the dog and rat. Histochem. J. 2000, 32, 53–61, doi:10.1023/A:1003910429346.
[152]
Bollard, M.E.; Murray, A.J.; Clarke, K.; Nicholson, J.K.; Griffin, J.L. A study of metabolic compartmentation in the rat heart and cardiac mitochondria using high-resolution magic angle spinning 1H NMR spectroscopy. FEBS Lett. 2003, 553, 73–78, doi:10.1016/S0014-5793(03)00969-4.
[153]
Palmi, M.; Youmbi, G.T.; Fusi, F.; Sgaragli, G.P.; Dixon, H.B.; Frosini, M.; Tipton, K.F. Potentiation of mitochondrial Ca2+ sequestration by taurine. Biochem. Pharmacol. 1999, 58, 1123–1131, doi:10.1016/S0006-2952(99)00183-5.
[154]
Hansen, S.H.; Andersen, M.L.; Birkedal, H.; Cornett, C.; Wibrand, F. The important role of taurine in oxidative metabolism. Adv. Exp. Med. Biol. 2006, 583, 129–135, doi:10.1007/978-0-387-33504-9_13.
[155]
Chen, K.; Zhang, Q.; Wang, J.; Liu, F.; Mi, M.; Xu, H.; Chen, F.; Zeng, K. Taurine protects transformed rat retinal ganglion cells from hypoxia-induced apoptosis by preventing mitochondrial dysfunction. Brain Res. 2009, 1279, 131–138, doi:10.1016/j.brainres.2009.04.054.
[156]
Hansen, S.H.; Andersen, M.L.; Cornett, C.; Gradinaru, R.; Grunnet, N. A role for taurine in mitochondrial function. J. Biomed. Sci. 2010, 17, S23, doi:10.1186/1423-0127-17-S1-S23.
[157]
Suzuki, T.; Suzuki, T.; Wada, T.; Saigo, K.; Watanabe, K. Taurine as a constituent of mitochondrial tRNAs: New insights into the functions of taurine and human mitochondrial diseases. EMBO J. 2002, 21, 6581–6589, doi:10.1093/emboj/cdf656.
[158]
Yasukawa, T.; Suzuki, T.; Ueda, T.; Ohta, S.; Watanabe, K. Modification defect at anticodon wobble nucleotide of mitochondrial tRNAs(Leu)(UUR) with pathogenic mutations of mitochondrial myopathy, encephalopathy, lactic acidosis, and stroke-like episodes. J. Biol. Chem. 2000, 275, 4251–4257.
[159]
Suzuki, T.; Nagao, A.; Suzuki, T. Human mitochondrial diseases caused by lack of taurine modification in mitochondrial tRNAs. Wiley Interdiscip. Rev. RNA 2011, 2, 376–386, doi:10.1002/wrna.65.
[160]
Rikimaru, M.; Ohsawa, Y.; Wolf, A.M.; Nishimaki, K.; Ichimiya, H.; Kamimura, N.; Nishimatsu, S. Taurine Ameliorates Impaired the Mitochondrial Function and Prevents Stroke-like Episodes in Patients with MELAS. Intern. Med. 2012, 51, 3351–3357.
Endres, M.; Namura, S.; Shimizu-Sasamata, M.; Waeber, C.; Zhang, L.; Gómez-Isla, T.; Hyman, B.T.; Moskowitz, M.A. Attenuation of delayed neuronal death after mild focal ischemia in mice by inhibition of the caspase family. J. Cereb. Blood Flow Metab. 1998, 18, 238–247.
[163]
Rami, A.; Agarwal, R.; Botez, G.; Winckler, J. μ-Calpain activation, DNA fragmentation, and synergistic effects of caspase and calpain inhibitors in protecting hippocampal neurons from ischemic damage. Brain Res. 2000, 866, 299–312, doi:10.1016/S0006-8993(00)02301-5.
[164]
Love, S. Apoptosis and brain ischaemia. Prog. Neuropsychopharmacol. Biol. Psychiatry 2003, 27, 267–282, doi:10.1016/S0278-5846(03)00022-8.
[165]
Kambe, A.; Yokota, M.; Saido, T.C.; Satokata, I.; Fujikawa, H.; Tabuchi, S.; Kamitani, H.; Watanabe, T. Spatial resolution of calpain-catalyzed proteolysis in focal cerebral ischemia. Brain Res. 2005, 1040, 36–43, doi:10.1016/j.brainres.2005.01.080.
[166]
Han, F.; Shirasaki, Y.; Fukunaga, K. 3-[2-[4-(3-Chloro-2-methylphenylmethyl)-1-piperazinyl]ethyl]-5,6-dimethoxy-1-(4-imidazolylmethyl)-1H-indazole dihydro-chloride 3.5 hydrate (DY-9760e) is neuroprotective in rat microsphere embolism: Role of the cross-talk between calpain and caspase-3 through calpastatin. J. Pharmacol. Exp. Ther. 2006, 317, 529–536, doi:10.1124/jpet.105.095018.
[167]
Goll, D.E.; Thompson, V.F.; Li, H.; Wei, W.; Cong, J. The Calpain System. Physiol. Rev. 1990, 731–801.
[168]
Wang, K.K. Calpain and caspase: Can you tell the difference? Trends Neurosci. 2000, 23, 20–26, doi:10.1016/S0166-2236(99)01479-4.
[169]
Ling, Y.-H.; Liebes, L.; Ng, B.; Buckley, M.; Elliott, P.J.; Adams, J.; Jiang, J.-D.; Muggia, F.M.; Perez-Soler, R. PS-341, a Novel Proteasome Inhibitor, Induces Bcl-2 Phosphorylation and Cleavage in Association with G2-M Phase Arrest and Apoptosis. Mol. Cancer Ther. 2002, 1, 841–849.
[170]
Nakagawa, T.; Yuan, J. Cross-Talk between Two Cysteine Protease Families: Activation of Caspase-12 by Calpain in Apoptosis. J. Cell Biol. 2000, 150, 887–894, doi:10.1083/jcb.150.4.887.
[171]
Gao, G.; Dou, Q.P. N-terminal cleavage of bax by calpain generates a potent proapoptotic 18-kDa fragment that promotes bcl-2-independent cytochrome c release and apoptotic cell death. J. Cell Biochem. 2000, 80, 53–72, doi:10.1002/1097-4644(20010101)80:1<53::AID-JCB60>3.0.CO;2-E.
[172]
Castro, R.E.; Solá, S.; Ramalho, R.M.; Steer, C.J.; Rodrigues, C.M.P. The bile acid tauroursodeoxycholic acid modulates phosphorylation and translocation of bad via phosphatidylinositol 3-kinase in glutamate-induced apoptosis of rat cortical neurons. J. Pharmacol. Exp. Ther. 2004, 311, 845–852, doi:10.1124/jpet.104.070532.
[173]
Gil-Parrado, S.; Fernández-Montalván, A.; Assfalg-Machleidt, I.; Popp, O.; Bestvater, F.; Holloschi, A.; Knoch, T.A.; Auerswald, E.A.; Welsh, K.; Reed, J.C.; et al. Ionomycin-activated calpain triggers apoptosis. A probable role for Bcl-2 family members. J. Biol. Chem. 2002, 277, 27217–27226, doi:10.1074/jbc.M202945200.
Li, P.; Nijhawan, D.; Budihardjo, I.; Srinivasula, S.M.; Ahmad, M.; Alnemri, E.S.; Wang, X. Cytochrome c and dATP-dependent formation of Apaf-1/caspase-9 complex initiates an apoptotic protease cascade. Cell 1997, 91, 479–489, doi:10.1016/S0092-8674(00)80434-1.
[176]
Takatani, T.; Takahashi, K.; Uozumi, Y.; Shikata, E.; Yamamoto, Y.; Ito, T.; Matsuda, T.; Schaffer, S.W.; Fujio, Y.; Azuma, J. Taurine inhibits apoptosis by preventing formation of the Apaf-1/caspase-9 apoptosome. Am. J. Physiol. Cell Physiol. 2004, 287, 949–953, doi:10.1152/ajpcell.00042.2004.
[177]
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, 593–611, doi:10.1007/s10571-007-9183-8.
[178]
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, 1419–1429, doi:10.1007/s00726-010-0751-8.
[179]
Taranukhin, A.G.; Taranukhina, E.Y.; Saransaari, P.; Djatchkova, I.M.; Pelto-Huikko, M.; Oja, S.S. Taurine reduces caspase-8 and caspase-9 expression induced by ischemia in the mouse hypothalamic nuclei. Amino Acids 2008, 34, 169–174, doi:10.1007/s00726-006-0405-z.
[180]
Kumar, R.; Azam, S.; Sullivan, J.M.; Owen, C.; Cavener, D.R.; Zhang, P.; Ron, D.; Harding, H.P.; Chen, J.-J.; Han, A.; et al. Brain ischemia and reperfusion activates the eukaryotic initiation factor 2α kinase, PERK. J. Neurochem. 2001, 77, 1418–1421, doi:10.1046/j.1471-4159.2001.00387.x.
[181]
Azfer, A.; Niu, J.; Rogers, L.M.; Adamski, F.M.; Kolattukudy, P.E. Activation of endoplasmic reticulum stress response during the development of ischemic heart disease. Am. J. Physiol. Heart Circ. Physiol. 2006, 291, 1411–1420, doi:10.1152/ajpheart.01378.2005.
[182]
Kuznetsov, G.; Brostrom, M.; Brostrom, C. Demonstration of a calcium requirement for secretory protein processing and export. Differential effects of calcium and dithiothreitol. J. Biol. Chem. 1992, 267, 3932–3939.
[183]
Verkhratsky, A.; Toescu, E.C. Endoplasmic reticulum Ca(2+) homeostasis and neuronal death. J. Cell. Mol. Med. 2003, 7, 351–361, doi:10.1111/j.1582-4934.2003.tb00238.x.
[184]
Pizzo, P.; Pozzan, T. Mitochondria-endoplasmic reticulum choreography: Structure and signaling dynamics. Trends Cell Biol. 2007, 17, 511–517, doi:10.1016/j.tcb.2007.07.011.
[185]
Morimoto, N.; Oida, Y.; Shimazawa, M.; Miura, M.; Kudo, T.; Imaizumi, K.; Hara, H. Involvement of endoplasmic reticulum stress after middle cerebral artery occlusion in mice. Neuroscience 2007, 14, 957–967.
[186]
Malhotra, J.D.; Kaufman, R.J. The endoplasmic reticulum and the unfolded proteinresponse. Semin. Cell Dev. Biol. 2007, 18, 716–731, doi:10.1016/j.semcdb.2007.09.003.
Ron, D.; Walter, P. Signal integration in the endoplasmic reticulum unfolded protein response. Nat. Rev. Mol. Cell Biol. 2007, 8, 519–529, doi:10.1038/nrm2199.
[189]
Chakrabarti, A.; Chen, A.W.; Varner, J.D. A review of the mammalian unfolded protein response. Biotechnol. Bioeng. 2011, 108, 2777–2793, doi:10.1002/bit.23282.
[190]
Gharibani, P.M.; Modi, J.; Pan, C.; Menzie, J.; Ma, Z.; Chen, P.C.; Tao, R.; Prentice, H.; Wu, J.Y. The Mechanism of Taurine Protection Against Endoplasmic recticulum Stress in an Animal Stroke Model of Cerebral Artery Occlusion and Stroke-Related Conditions in Primary Neuronal Cell Culture. Adv. Exp. Med. Biol. 2013, 776, 241–258, doi:10.1007/978-1-4614-6093-0_23.
[191]
Ghosh, A.P.; Klocke, B.J.; Ballestas, M.E.; Roth, K.A. CHOP potentially co-operates with FOXO3a in neuronal cells to regulate PUMA and BIM expression in response to ER stress. PLoS One 2012, 7, e39586.
[192]
McCullough, K.D.; Martindale, J.L.; Klotz, L.O.; Aw, T.Y.; Holbrook, N.J. Gadd153 sensitizes cells to endoplasmic reticulum stress by down-regulating Bcl2 and perturbing the cellular redox state. Mol. Cell. Biol. 2001, 21, 1249–1259, doi:10.1128/MCB.21.4.1249-1259.2001.
[193]
Schuller-Levis, G.B.; Park, E. Taurine and Its Chloramine: Modulators of Immunity. Neurochem Res. 2004, 29, 117–126, doi:10.1023/B:NERE.0000010440.37629.17.
[194]
Halliwell, B. Reactive oxygen species and the central nervous system. J. Neurochem. 1992, 59, 1609–1623, doi:10.1111/j.1471-4159.1992.tb10990.x.
[195]
Zini, I.; Tomasi, A.; Grimaldi, R.; Vannini, V.; Agnati, L.F. Detection of free radicals during brain ischemia and reperfusion by spin trapping and microdialysis. Neurosci. Lett. 1992, 138, 279–282, doi:10.1016/0304-3940(92)90933-X.
[196]
Sohal, R.S.; Orr, W.C. Relationship between antioxidants, prooxidants, and the aging proces. Ann. N. Y. Acad. Sci. 1992, 663, 74–84, doi:10.1111/j.1749-6632.1992.tb38651.x.
[197]
Turrens, J.F. Mitochondrial formation of reactive oxygen species. J. Physiol. 2003, 552, 335–344, doi:10.1113/jphysiol.2003.049478.
[198]
Brookes, P.S.; Darley-Usmar, V.M. Role of calcium and superoxide dismutase in sensitizing mitochondria to peroxynitrite-induced permeability transition. Am. J. Physiol. Heart Circ. Physiol. 2004, 286, 39–46, doi:10.1152/ajpheart.00742.2003.
[199]
Wikstr?m, M.; Saari, H. A spectral shift in cytochrome a induced by calcium ions. Biochim. Biophys. Acta 1975, 408, 170–179, doi:10.1016/0005-2728(75)90009-2.
[200]
Jekabsone, A.; Ivanoviene, L.; Brown, G.C.; Borutaite, V. Nitric oxide and calcium together inactivate mitochondrial complex I and induce cytochrome c release. J. Mol. Cell. Cardiol. 2003, 35, 803–809, doi:10.1016/S0022-2828(03)00137-8.
[201]
Grijalba, M.T.; Vercesi, A.E.; Schreier, S. Ca2+-induced increased lipid packing and domain formation in submitochondrial particles. A possible early step in the mechanism of Ca2+-stimulated generation of reactive oxygen species by the respiratory chain. Biochemistry 1999, 38, 13279–13287, doi:10.1021/bi9828674.
[202]
Cleeter, M.W.; Cooper, J.M.; Darley-Usmar, V.M.; Moncada, S.; Schapira, A.H. Reversible inhibition of cytochrome c oxidase, the terminal enzyme of the mitochondrial respiratory chain, by nitric oxide. Implications for neurodegenerative diseases. FEBS Lett. 1994, 345, 50–54, doi:10.1016/0014-5793(94)00424-2.
[203]
Zoccarato, F.; Cavallini, L.; Alexandre, A. Respiration-dependent removal of exogenous H2O2 in brain mitochondria: Inhibition by Ca2+. J. Biol. Chem. 2004, 279, 4166–4174, doi:10.1074/jbc.M308143200.
[204]
Patterson, S.D.; Spahr, C.S.; Daugas, E.; Susin, S.A.; Irinopoulou, T.; Koehler, C.; Kroemer, G. Mass spectrometric identification of proteins released from mitochondria undergoing permeability transition. Cell Death Differ. 2000, 7, 137–144, doi:10.1038/sj.cdd.4400640.
[205]
Ricci, C.; Pastukh, V.; Leonard, J.; Turrens, J.; Wilson, G.; Schaffer, D.; Schaffer, S.W. Mitochondrial DNA damage triggers mitochondrial-superoxide generation and apoptosis. Am. J. Physiol. 2008, 294, 413–422.
[206]
Mochizuki, H.; Oda, H.; Yokogoshi, H. Dietary taurine alters ascorbic acid metabolism in rats fed diets containing polychlorinated biphenyls. J. Nutr. 2000, 130, 873–876.
[207]
Vohra, B.P.; Hui, X. Taurine protects against carbon tetrachloride toxicity in the cultured neurons and in vivo. Arch. Physiol. Biochem. 2001, 109, 90–94, doi:10.1076/apab.109.1.90.4287.
[208]
Balkan, J.; Kanba?li, O.; Ayka?-Toker, G.; Uysal, M. Taurine treatment reduces hepatic lipids and oxidative stress in chronically ethanol-treated rats. Biol. Pharm. Bull. 2002, 25, 1231–1233, doi:10.1248/bpb.25.1231.
[209]
Mahalakshmi, K.; Pushpakiran, G.; Anuradha, C.V. Taurine prevents acrylonitrile-induced oxidative stress in rat brain. Pol. J. Pharmacol. 2003, 55, 1037–1043.
[210]
Pushpakiran, G.; Mahalakshmi, K.; Anuradha, C.V. Taurine restores ethanol-induced depletion of antioxidants and attenuates oxidative stress in rat tissues. Amino Acids 2004, 27, 91–96.
[211]
Aruoma, O.I.; Halliwell, B.; Hoey, B.M.; Butler, J. The antioxidant action of taurine, hypotaurine and their metabolic precursors. Biochem. J. 1988, 256, 251–255.
[212]
Jong, C.J.; Azuma, J.; Schaffer, S. Mechanism underlying the antioxidant activity of taurine: Prevention of mitochondrial oxidant production. Amino Acids 2012, 42, 2223–2232, doi:10.1007/s00726-011-0962-7.
[213]
Jong, C.J.; Ito, T.; Mozaffari, M.; Azuma, J.; Schaffer, S. Effect of beta-alanine treatment on mitochondrial taurine level and 5-taurinomethyluridine content. J. Biomed. Sci. 2010, 17, S25, doi:10.1186/1423-0127-17-S1-S25.
[214]
Amantea, D.; Nappi, G.; Bernardi, G.; Bagetta, G.; Corasaniti, M.T. Post-ischemic brain damage: Pathophysiology and role of inflammatory mediators. FEBS J. 2009, 276, 13–26, doi:10.1111/j.1742-4658.2008.06766.x.
[215]
Koh, S.-H.; Chang, D.-I.; Kim, H.-T.; Kim, J.; Kim, M.-H.; Kim, K. S.; Bae, I.; Kim, H.; Kim, D.W.; Kim, S.H. Effect of 3-aminobenzamide, PARP inhibitor, on matrix metalloproteinase-9 level in plasma and brain of ischemic stroke model. Toxicology 2005, 214, 131–139, doi:10.1016/j.tox.2005.06.023.
[216]
Haddad, M.; Rhinn, H.; Bloquel, C.; Coqueran, B.; Szabó, C.; Plotkine, M.; Scherman, D.; Margaill, I. Anti-inflammatory effects of PJ34, a poly(ADP-ribose) polymerase inhibitor, in transient focal cerebral ischemia in mice. Br. J. Pharmacol. 2006, 149, 23–30, doi:10.1038/sj.bjp.0706837.
[217]
Sun, M.; Zhao, Y.-M.; Gu, Y.; Xu, C. Therapeutic window of taurine against experimental stroke in rats. Transl. Res. 2012, 160, 223–229, doi:10.1016/j.trsl.2012.02.007.
[218]
Walz, W.; Klimaszewski, A.; Paterson, I.A. Glial swelling in ischemia: A hypothesis. Dev. Neurosci. 1993, 15, 216–225, doi:10.1159/000111337.
[219]
Haugstad, T.S.; Langmoen, I.A. Release of brain amino acids during hyposmolar stress and energy deprivation. J. Neurosurg. Anesthesiol. 1996, 8, 159–168, doi:10.1097/00008506-199604000-00011.
[220]
Saransaari, P.; Oja, S.S. Taurine release is enhanced in cell-damaging conditions in cultured cerebral cortical astrocytes. Neurochem. Res. 1999, 24, 1523–1529, doi:10.1023/A:1021195830773.
[221]
Estevez, A.Y.; O’Regan, M.H.; Song, D.; Phillis, J.W. Hyposmotically induced amino acid release from the rat cerebral cortex: Role of phospholipases and protein kinases. Brain Res. 1999, 844, 1–9, doi:10.1016/S0006-8993(99)01801-6.
[222]
Inoue, H.; Mori, S.-I.; Morishima, S.; Okada, Y. Volume-sensitive chloride channels in mouse cortical neurons: Characterization and role in volume regulation. Eur. J. Neurosci. 2005, 21, 1648–1658, doi:10.1111/j.1460-9568.2005.04006.x.
[223]
Molchanova, S.M.; Oja, S.S.; Saransaari, P. Properties of basal taurine release in the rat striatum in vivo. Adv. Exp. Med. Biol. 2006, 583, 365–375, doi:10.1007/978-0-387-33504-9_41.
[224]
Inoue, H.; Okada, Y. Roles of volume-sensitive chloride channel in excitotoxic neuronal injury. J. Neurosci. 2007, 27, 1445–1455, doi:10.1523/JNEUROSCI.4694-06.2007.
[225]
Shuaib, A. The role of taurine in cerebral ischemia: Studies in transient forebrain ischemia and embolic focal ischemia in rodents. Adv. Exp. Med. Biol. 2003, 526, 421–431, doi:10.1007/978-1-4615-0077-3_51.
[226]
Kudo, Y.; Akiyoshi, E.; Akagi, H. Identification of two taurine receptor subtypes on the primary afferent terminal of frog spinal cord. Br. J. Pharmacol. 1988, 94, 1051–1056, doi:10.1111/j.1476-5381.1988.tb11621.x.
[227]
Sanberg, P.R.; Willow, M. Dose-dependent effects of taurine on convulsions induced by hypoxia in the rat. Neurosci Lett. 1980, 16, 297–300, doi:10.1016/0304-3940(80)90014-2.
[228]
Stummer, W.; Betz, A.L.; Shakui, P.; Keep, R.F. Blood-brain barrier taurine transport during osmotic stress and in focal cerebral ischemia. J. Cereb. Blood Flow. Metab. 1995, 15, 852–859, doi:10.1038/jcbfm.1995.106.
[229]
Azuma, J.; Sawamura, A.; Awata, N.; Ohta, H.; Hamaguchi, T.; Haradam, H.; Takiharma, K.; Hasegawa, H.; Yamagami, T.; Ishiyama, T.; et al. Therapeutic Effect of Taurine in Congestive Heart Failure: A Double-Blind Crossover Trial. Clin. Cardiol. 1985, 8, 276–282, doi:10.1002/clc.4960080507.
[230]
Azuma, J.; Sawamura, A.; Awata, N. Usefulness of taurine in chronic congestive heart failure and its prospective application. Jpn. Circ. J. 1992, 56, 95–99, doi:10.1253/jcj.56.95.
[231]
Yamori, Y.; Nara, Y.; Mizushima, S.; Sawamura, M.; Horie, R. Nutritional factors for stroke and major cardiovascular diseases: International epidemiological comparison of dietary prevention. Health Rep. 1994, 6, 22–27.
[232]
Jeejeebhoy, F.; Keith, M.; Freeman, M.; Barr, A.; McCall, M.; Kudan, R.; Mazer, D.; Errett, L. Nutritional supplementation with MyoVive repletes essential cardiac myocyte nutrients and reduces left ventricular dysfunction. Am. Heart J. 2002, 143, 10092–10100.
[233]
Kingston, R.; Kelly, C.J.; Murray, P. The therapeutic role of taurine in ischaemia-reperfusion injury. Curr. Pharm. Des. 2004, 10, 2401–2410, doi:10.2174/1381612043384015.
[234]
Fisher, M.; Feuerstein, G.; Howells, D.W.; Hurn, P.D.; Kent, T.A.; Savitz, S.I.; Lo, E.H.; STAIR Group. Update of the stroke therapy academic industry roundtable preclinical recommendations. Stroke 2009, 40, 2244–2250, doi:10.1161/STROKEAHA.108.541128.
[235]
Kanthan, R.; Shuaib, A.; Griebel, R.; Miyashita, H. Intracerebral human microdialysis. In vivo study of an acute focal ischemic model of the human brain. Stroke 1995, 26, 870–873, doi:10.1161/01.STR.26.5.870.
[236]
Zhang, M.; Bi, L.F.; Fang, J.H.; Su, X.L.; Da, G.L.; Kuwamori, T.; Kagamimori, S. Beneficial effects of taurine on serum lipids in overweight or obese non-diabetic subjects. Amino Acids 2004, 26, 267–271.
[237]
Takahashi, H.; Mori, T.; Fujihira, E.; Nakazawa, M. Long-term feeding of taurine in rats. Pharmacometrics 1972, 6, 529–534.
[238]
Takahashi, H.; Kaneda, S.; Fukuda, K.; Fujihira, E.; Nakazawa, M. Studies on the teratology and three generation reproduction of taurine in mice. Pharmacometrics 1972, 6, 535–540.
[239]
Sturman, J.A.; Messing, J.M. High dietary taurine effects on feline tissue taurine concentrations and reproductive performance. J. Nutr. 1992, 122, 82–88.
[240]
Furukawa, S.; Katto, M.; Kouyama, H.; Nishida, I.; Kikumori, M.; Taniguchi, Y.; Toda, T.; Araki, H. Repeated dose toxicity study of intravenous treatment with taurine for 13 weeks and recovery test for 5 weeks in rat. Jpn. Pharmacol. Ther. 1991, 19, 275–306.
[241]
Cantafora, A.; Mantovani, A.; Masella, R.; Mechelli, L.; Alvaro, D. Effect of taurine administration on liver lipids in guinea pig. Experientia 1986, 42, 407–408, doi:10.1007/BF02118631.
[242]
European Food Safety Authority (EFSA). EFSA adopts opinion on two ingredients commonly used in some energy drinks. 2009. Available online: http://www.efsa.europa.eu/en/press/news/ans090212.htm (accessed on 15 February 2013).
[243]
Schaffer, S.; Takahashi, K.; Azuma, J. Role of osmoregulation in the actions of taurine. Amino Acids 2000, 19, 527–546, doi:10.1007/s007260070004.
[244]
Morales, I.; Dopico, J.G.; Sabate, M.; Gonzalez-Hernandez, T.; Rodriguez, M. Substantia nigra osmoregulation: Taurine and ATP involvement. Am. J. Physiol. Cell Physiol. 2007, 292, 1934–1941.
[245]
O’Byrne, M.B.; Tipton, K.F. Taurine-induced attenuation of MPP+ neurotoxicity in vitro: A possible role for the GABA(A) subclass of GABA receptors. J. Neurochem. 2000, 74, 2087–2093.
[246]
Paula-Lima, A.C.; de Felice, F.G.; Brito-Moreira, J.; Ferreira, S.T. Activation of GABA(A) receptors by taurine and muscimol blocks the neurotoxicity of beta-amyloid in rat hippocampal and cortical neurons. Neuropharmacology 2005, 49, 1140–1148, doi:10.1016/j.neuropharm.2005.06.015.
[247]
Chen, P.C.; Pan, C.; Gharibani, P.M.; Prentice, H.; Wu, J.Y. Taurine exerts robust protection against hypoxia and oxygen/glucose deprivation in human neuroblastoma cell culture. Adv. Exp. Med. Biol. 2013, 775, 167–175, doi:10.1007/978-1-4614-6130-2_14.
[248]
Das, J.; Ghosh, J.; Manna, P.; Sil, P.C. Taurine suppresses doxorubicin-triggered oxidative stress and cardiac apoptosis in rat via up-regulation of PI3-K/Akt and inhibition of p53, p38-JNK. Biochem. Pharmacol. 2011, 81, 891–909, doi:10.1016/j.bcp.2011.01.008.
[249]
Smith, K.E.; Borden, L.A.; Wang, C.H.; Hartig, P.R.; Branchek, T.A.; Weinshank, R.L. Cloning and expression of a high affinity taurine transporter from rat brain. Mol. Pharmacol. 1992, 42, 563–569.
[250]
Pow, D.V.; Sullivan, R.; Reye, P.; Hermanussen, S. Localization of taurine transporters, taurine, and (3)H taurine accumulation in the rat retina, pituitary, and brain. Glia 2002, 37, 153–168, doi:10.1002/glia.10026.
López-Colomé, A.M.; Fragoso, G.; Salceda, R. Taurine receptors in membranes from retinal pigment epithelium cells in culture. Neuroscience 1991, 41, 791–796, doi:10.1016/0306-4522(91)90369-Y.
[253]
Sung, D.-Y.; Walthall, W.W.; Derby, C.D. Identification and partial characterization of putative taurine receptor proteins from the olfactory organ of the spiny lobster. Comp. Biochem. Physiol. B Biochem. Mol. Biol. 1996, 115, 19–26, doi:10.1016/0305-0491(96)00083-1.
[254]
Anderson, P.A.; Trapido-Rosenthal, H.G. Physiological and chemical analysis of neurotransmitter candidates at a fast excitatory synapse in the jellyfish Cyanea capillata (Cnidaria, Scyphozoa). Invert. Neurosci. 2009, 9, 167–173, doi:10.1007/s10158-009-0095-9.