Skip to main content
SpringerLink
Log in

Modulation of Calcium Channels by Taurine Acting Via a Metabotropic-like Glycine Receptor

  • Original Research
  • Published:
Cellular and Molecular Neurobiology Aims and scope Submit manuscript

Abstract

Taurine is one of the most abundant free amino acids in the central nervous system, where it displays several functions. However, its molecular targets remain unknown. It is well known that taurine can activate GABA-A and strychnine-sensitive glycine receptors, which increases a chloride conductance. In this study, we describe that acute application of taurine induces a dose-dependent inhibition of voltage-dependent calcium channels in chromaffin cells from bovine adrenal medullae. This taurine effect was not explained by the activation of either GABA-A, GABA-B or strychnine-sensitive glycine receptors. Interestingly, glycine mimicked the modulatory action exerted by taurine on calcium channels, although the acute application of glycine did not elicit any ionic current in these cells. Additionally, the modulation of calcium channels exerted by both taurine and glycine was prevented by the intracellular dialysis of GDP-β-S. Thus, the modulation of voltage-dependent calcium channels by taurine seems to be mediated by a metabotropic-like glycinergic receptor coupled to G-protein activation in a membrane delimited pathway.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4

Similar content being viewed by others

References

  • Castro E, Gonzalez MA, Oset-Gasque MJ (2003) Distribution of γ-aminobutyric acid receptors in cultured adrenergic and noradrenergic bovine chromaffin cells. J Neurosci Res 71:375–382

    Article  CAS  PubMed  Google Scholar 

  • Cesetti T, Hernández-Guijo JM, Baldelli P, Carabelli V, Carbone E (2003) Opposite action of β1- and β2-adrenergic receptors on Cav1 L-Channel current in rat chromaffin cells. J Neurosci 23:3–83

    Google Scholar 

  • del Olmo N, Bustamante J, Martín del Rio R, Solís JM (2000) Taurine activates GABAA but not GABAB receptors in rat hippocampal CA1 area. Brain Res 864:298–307

    Article  CAS  PubMed  Google Scholar 

  • del Olmo N, Suárez LM, Orensanz LM, Suárez F, Bustamante J, Duarte JM, Martín del Río R, Solís JM (2004) Role of taurine uptake on the induction of long-term synaptic potentiation. Eur J Neurosci 19:1875–1886

    Article  PubMed  Google Scholar 

  • El Idrissi A (2008) Taurine increases mitochondrial buffering of calcium: role in neuroprotection. Amino Acids 34:321–328

    Article  CAS  PubMed  Google Scholar 

  • Flint AC, Liu X, Kriegstein AR (1998) Nonsynaptic glycine receptor activation during early neocortical development. Neuron 20:43–53

    Article  CAS  PubMed  Google Scholar 

  • Hanretta AT, Lombardini JB (1986) Properties of spontaneous and evoked release of taurine from hypothalamic crude P2 synaptosomal preparations. Brain Res 378:205–215

    Article  CAS  PubMed  Google Scholar 

  • Hernández-Guijo JM, Gandía L, Lara B, García AG (1998) Autocrine/paracrine modulation of calcium channels in bovine chromaffin cells. Pflügers Arch Eur J Physiol 437:104–113

    Article  Google Scholar 

  • Hernández-Guijo JM, Carabelli V, Gandía L, García AG, Carbone E (1999) Voltage independent autocrine modulation of L-type channels mediated by ATP, opioids and catecholamines in rat chromaffin cells. Eur J Neurosci 11:3574–3584

    Article  PubMed  Google Scholar 

  • Horikoshi T, Asanuma A, Yanagisawa K, Anzai K, Goto S (1988) Taurine and beta-alanine act on both GABA and glycine receptors in Xenopus oocyte injected with mouse brain messenger RNA. Brain Res 464:97–105

    CAS  PubMed  Google Scholar 

  • Hou M, Duan L, Slaughter M (2008) Synaptic inhibition by glycine acting at a metabotropic receptor in tiger salamder retina. J Physiol 586:2913–2926

    Article  CAS  PubMed  Google Scholar 

  • Hussy N, Deleuze C, Pantaloni A, Desarmenien MG, Moos F (1997) Agonist action of taurine on glycine receptors in rat supraoptic magnocellular neurones: possible role in osmoregulation. J Physiol 502:609–621

    Article  CAS  PubMed  Google Scholar 

  • Huxtable R (1992) Physiological actions of taurine. Physiol Rev 7:101–163

    Google Scholar 

  • Jia F, Yue M, Chandra D, Keramidas A, Goldstein PA, Homanics GE, Harrison NL (2008) Taurine is a potent activator of extrasynaptic GABA(A) receptors in the thalamus. J Neurosci 28:106–115

    Article  CAS  PubMed  Google Scholar 

  • Kimelberg HK, Goderie SK, Higman S, Pang S, Waniewski RA (1990) Swelling-induced release of glutamate, aspartate, and taurine from astrocyte cultures. J Neurosci 10:1583–1591

    CAS  PubMed  Google Scholar 

  • Lerma J, Herranz AS, Herreras O, Abraira V, Martin del Rio R (1986) In vivo determination of extracellular concentration of amino acids in the rat hippocampus. A method based on brain dialysis and computerized analysis. Brain Res 384:145–155

    Article  CAS  PubMed  Google Scholar 

  • Livett BG (1984) Adrenal medullary chromaffin cells in vitro. Physiol Rev 64:1103–1161

    CAS  PubMed  Google Scholar 

  • Lobo MV, Alonso FJ, Martín del Rio R (2000) Immunocytochemical localization of taurine in different muscle cell types of the dog and rat. Histochem J 32:53–61

    Article  CAS  PubMed  Google Scholar 

  • Mongin AA, Cai Z, Kimelberg HK (1999) Volume-dependent taurine release from cultured astrocytes requires permissive [Ca2+]I and calmodulin. Am J Physiol 277:823–832

    Google Scholar 

  • Mori M, Gahwiler BH, Gerber U (2002) Beta-alanine and taurine as endogenous agonists at glycine receptors in rat hippocampus in vitro. J Physiol 539:191–200

    Article  CAS  PubMed  Google Scholar 

  • Nicoll RA (2004) My close encounter with GABA-B receptors. Biochem Pharmacol 68:1667–1674

    Article  CAS  PubMed  Google Scholar 

  • Ottersen OP (1988) 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 178:407–421

    Article  CAS  PubMed  Google Scholar 

  • Palkovits M, Elekes I, Lang T, Patthy A (1986) Taurine levels in discrete brain nuclei of rats. J Neurochem 47:1333–1335

    Article  CAS  PubMed  Google Scholar 

  • Palmi M, Youmbi GT, Fusi F, Sgaragli GP, Dixon HB, Frosini M, Tipton KF (1999) Potentiation of mitochondrial Ca2+ sequestration by taurine. Biochem Pharmacol 58:1123–1131

    Article  CAS  PubMed  Google Scholar 

  • Pasantes-Morales H, Schousboe A (1988) Volume regulation in astrocytes: a role for taurine as an osmoeffector. J Neurosci Res 20:503–509

    CAS  PubMed  Google Scholar 

  • Satoh H, Sperelakis N (1993) Effects of taurine on Ca2+ currents in young embryonic chick cardiomyocytes. Eur J Pharmacol 231:443–449

    Article  CAS  PubMed  Google Scholar 

  • Satoh H, Sperelakis N (1998) Review of some actions of taurine on ion channels of cardiac muscle cells and others. Gen Pharmacol 30:451–463

    Article  CAS  PubMed  Google Scholar 

  • Sergeeva OA, Chepkova AN, Doreulee N, Eriksson KS, Poelchen W, Monnighoff I, Heller-Stilb B, Warskulat U, Haussinger D, Haas HL (2003) Taurine-induced long-lasting enhancement of synaptic transmission in mice: role of transporters. J Physiol 550:911–919

    Article  CAS  PubMed  Google Scholar 

  • Solís JM, Herranz AS, Herreras O, Lerma J, Martín del Rio R (1988) Does taurine act as an osmoregulatory substance in the rat brain? Neurosci Lett 91:53–58

    Article  PubMed  Google Scholar 

  • Stipanuk MH, Londono M, Lee JI, Hu M, Yu AF (2002) Enzymes and metabolites of cysteine metabolism in nonhepatic tissues of rats show little response to changes in dietary protein or sulfur amino acid levels. J Nutr 132:3369–3378

    CAS  PubMed  Google Scholar 

  • Terauchi A, Nakazaw A, Johkura K, Yan L, Usuda N (1998) Immunohistochemical localization of taurine in various tissues of the mouse. Amino Acids 15:151–160

    Article  CAS  PubMed  Google Scholar 

  • Ye G, Tse AC, Yung W (1997) Taurine inhibits rat substantia nigra pars reticulata neurons by activation of GABA- and glycine-linked chloride conductance. Brain Res 749:175–179

    Article  CAS  PubMed  Google Scholar 

  • Zhao P, Huang YL, Chen JS (1999) Taurine antagonizes calcium overload induced by glutamate or chemical hypoxia in cultured hippocampal neurons. Neurosci Lett 268:25–28

    Article  CAS  PubMed  Google Scholar 

Download references

Acknowledgments

This study was supported by Instituto de Salud Carlos III (grant PI080227 to J.M.H-G; and grant PI081067 to J.M.S.). E.A. is a fellow of Fundación Teófilo Hernando. We also acknowledge financial support from the CEAL-UAM-Banco de Santander.

Author information

Authors and Affiliations

  1. Instituto Teófilo Hernando, Univ. Autónoma de Madrid, Av. Arzobispo Morcillo 4, 28029, Madrid, Spain

    E. Albiñana & J. M. Hernández-Guijo

  2. Departamento de Farmacología y Terapéutica, Facultad de Medicina, Univ. Autónoma de Madrid, Av. Arzobispo Morcillo 4, 28029, Madrid, Spain

    E. Albiñana & J. M. Hernández-Guijo

  3. Servicio de Neurobiología-Investigación, Hospital Ramón y Cajal, IRYCIS, Ctra. de Colmenar Km 9.1, 28034, Madrid, Spain

    S. Sacristán, R. Martín del Río & J. M. Solís

Authors
  1. E. Albiñana
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. S. Sacristán
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. R. Martín del Río
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. J. M. Solís
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. J. M. Hernández-Guijo
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to J. M. Hernández-Guijo.

Additional information

A commentary to this article can be found at doi: 10.1007/s10571-010-9611-z.

Electronic supplementary material

Below is the link to the electronic supplementary material.

10571_2010_9574_MOESM1_ESM.tif

Supplementary Fig. 1. Inmunofluorescence images showing the localisation of taurine in chromaffin cells. A 1 Inmunostaining with antibodies against taurine in an adrenal gland slice. Note the strong signal detected in the cortical tissue. A 2 Magnification of medullae region. Note the labelling of the nucleus in approximately half of adrenal chromaffin cells. B 1 Immunostaining with antibodies anti-taurine transporter in an adrenal gland slice. Note the strong signal detected in the cortical tissue. B 2 Magnification of medullae region. Note the lack of signal in the totality of adrenal chromaffin cells. Controls without primary antibodies for TAU (C 1 ) and TAUT (C 2 ) show a very faint immunostaining, these photographs were obtained with the same exposure times used in A and B. Scale bars: A 1 , B 1 , C 1 , C 2 : 50 μm; A 2 , B 2 : 25 μm. l (TIFF 1,613 kb)

Rights and permissions

Reprints and permissions

About this article

Cite this article

Albiñana, E., Sacristán, S., Martín del Río, R. et al. Modulation of Calcium Channels by Taurine Acting Via a Metabotropic-like Glycine Receptor. Cell Mol Neurobiol 30, 1225–1233 (2010). https://doi.org/10.1007/s10571-010-9574-0

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10571-010-9574-0

Keywords

Search

Navigation