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      Reciprocal regulation between taurine and glutamate response via Ca 2+- dependent pathways in retinal third-order neurons

      research-article
      1 , 1 ,
      Journal of Biomedical Science
      BioMed Central
      17th International Meeting of Taurine
      14–19 December 2009

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          Abstract

          Although taurine and glutamate are the most abundant amino acids conducting neural signals in the central nervous system, the communication between these two neurotransmitters is largely unknown. This study explores the interaction of taurine and glutamate in the retinal third-order neurons. Using specific antibodies, both taurine and taurine transporters were localized in photoreceptors and Off-bipolar cells, glutamatergic neurons in retinas. It is possible that Off-bipolar cells release juxtaposed glutamate and taurine to activate the third-order neurons in retina. The interaction of taurine and glutamate was studied in acutely dissociated third-order neurons in whole-cell patch-clamp recording and Ca 2+ imaging. We find that taurine effectively reduces glutamate-induced Ca 2+ influx via ionotropic glutamate receptors and voltage-dependent Ca 2+ channels in the neurons, and the effect of taurine was selectively inhibited by strychnine and picrotoxin, but not GABA receptor antagonists, although GABA receptors are present in the neurons. A CaMKII inhibitor partially reversed the effect of taurine, suggesting that a Ca 2+/calmodulin-dependent pathway is involved in taurine regulation. On the other hand, a rapid influx of Ca 2+ through ionotropic glutamate receptors could inhibit the amplitude and kinetics of taurine-elicited currents in the third-order neurons, which could be controlled with intracellular application of BAPTA a fast Ca 2+ chelator. This study indicates that taurine is a potential neuromodulator in glutamate transmission. The reciprocal inhibition between taurine and glutamate in the postsynaptic neurons contributes to computation of visual signals in the retinal neurons.

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          Most cited references55

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          Taurine interaction with neurotransmitter receptors in the CNS: an update.

          Taurine appears to have multiple functions in the brain participating both in volume regulation and neurotransmission. In the latter context it may exert its actions by serving as an agonist at receptors of the GABAergic and glycinergic neurotransmitter systems. Its interaction with GABAA and GABAB receptors as well as with glycine receptors is reviewed and the physiological relevance of such interactions is evaluated. The question as to whether local extracellular concentrations of taurine are likely to reach the threshold level for the pertinent receptor populations cannot presently be answered satisfactorily. Hence more sophisticated analytical methods are warranted in order to obtain a definite answer to this important question.
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            Taurine is a potent activator of extrasynaptic GABA(A) receptors in the thalamus.

            Taurine is one of the most abundant free amino acids in the brain. In a number of studies, taurine has been reported to activate glycine receptors (Gly-Rs) at moderate concentrations (> or = 100 microM), and to be a weak agonist at GABA(A) receptors (GABA(A)-Rs), which are usually activated at high concentrations (> or = 1 mM). In this study, we show that taurine reduced the excitability of thalamocortical relay neurons and activated both extrasynaptic GABA(A)-Rs and Gly-Rs in neurons in the mouse ventrobasal (VB) thalamus. Low concentrations of taurine (10-100 microM) decreased neuronal input resistance and firing frequency, and elicited a steady outward current under voltage clamp, but had no effects on fast inhibitory synaptic currents. Currents elicited by 50 microM taurine were abolished by gabazine, insensitive to midazolam, and partially blocked by 20 microM Zn2+, consistent with the pharmacological properties of extrasynaptic GABA(A)-Rs (alpha4beta2delta subtype) involved in tonic inhibition in the thalamus. Tonic inhibition was enhanced by an inhibitor of taurine transport, suggesting that taurine can act as an endogenous activator of these receptors. Taurine-evoked currents were absent in relay neurons from GABA(A)-R alpha4 subunit knock-out mice. The amplitude of the taurine current was larger in neurons from adult mice than juvenile mice. Taurine was a more potent agonist at recombinant alpha4beta2delta GABA(A)-Rs than at alpha1beta2gamma2 GABA(A)-Rs. We conclude that physiological concentrations of taurine can inhibit VB neurons via activation of extrasynaptic GABA(A)-Rs and that taurine may function as an endogenous regulator of excitability and network activity in the thalamus.
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              Taurine in development.

              E Sturman (1988)
              Taurine is a ubiquitous dietary constituent of most mammals and is present in especially high concentrations in the tissues of developing mammals. Research to date indicates that taurine plays an important role in the development of the nervous system and the process of migration in particular. It is speculated that taurine uptake and release, in conjunction with glutamate uptake and release, may represent one form of communication between neurons and glial cells. The need of taurine by the body is emphasized by the ability of the kidney to curtail taurine excretion to conserve taurine in the face of a low dietary taurine intake. The evidence for a special role of taurine in development is considered and discussed.
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                Author and article information

                Conference
                J Biomed Sci
                Journal of Biomedical Science
                BioMed Central
                1021-7770
                1423-0127
                2010
                24 August 2010
                : 17
                : Suppl 1
                : S5
                Affiliations
                [1 ]College of Biomedical Science, Florida Atlantic University, Boca Raton, FL 33431, USA
                Article
                1423-0127-17-S1-S5
                10.1186/1423-0127-17-S1-S5
                2994392
                20804625
                f110a9f0-37bb-4442-9f7c-89bbbdffe4f8
                Copyright ©2010 Shen and Bulley; licensee BioMed Central Ltd.

                This is an open access article distributed under the terms of the Creative Commons Attribution License ( http://creativecommons.org/licenses/by/2.0), which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.

                17th International Meeting of Taurine
                Fort Lauderdale, FL, USA
                14–19 December 2009
                History
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                Research

                Molecular medicine
                Molecular medicine

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