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Sodium-Calcium Exchanger Modulates the L-Glutamate Cai 2+ Signalling in Type-1 Cerebellar Astrocytes

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Sodium Calcium Exchange: A Growing Spectrum of Pathophysiological Implications

Abstract

We have previously demonstrated that rat type-1 cerebellar astrocytes express a very active Na+/Ca2+ exchanger which accounts for most of the total plasma membrane Ca2+ fluxes and for the clearance of Ca 2+i induced by physiological agonist. In this chapter, we have explored the mechanism by which the reverse Na+/Ca2+ exchange is involved in agonist-induced Ca2+ signalling in rat cerebellar astrocytes. Laser-scanning confocal microscopy experiments using immunofluorescence labelling of Na+/Ca2+ exchanger and RyRs demonstrated that they are highly co-localized. The most important finding presented in this chapter is that L-glutamate activates the reverse mode of the Na+/Ca2+ exchange by inducing a Na+ entry through the electrogenic Na+-glutamate co-transporter and not through the ionophoric L-glutamate receptors as confirmed by pharmacological experiments with specific blockers of ionophoric L-glutamate receptors, electrogenic glutamate transporters and the Na/Ca exchange.

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References

  • P.K. Aley, H.J. Murray, J.P. Boyle, H.A. Pearson, C. Peers, Hypoxia stimulates Ca2+ release from intracellular stores in astrocytes via cyclic ADP ribose-mediated activation of ryanodine receptors. Cell Calcium 39, 95–100 (2006)

    Article  PubMed  CAS  Google Scholar 

  • A. Araque, N. Li, R.T. Doyle, P.G. Haydon, SNARE ­protein-dependent glutamate release from astrocytes. J. Neurosci. 20, 666–673 (2000)

    PubMed  CAS  Google Scholar 

  • A. Beck, R.Z. Nieden, H.P. Scheideer, J.W. Ditmer, Calcium release from intracellular stores in rodent astrocytes and neurons in situ. Cell Calcium 35, 47–58 (2004)

    Article  PubMed  CAS  Google Scholar 

  • B. Benz, G. Grima, K.Q. Do, Glutamate-induced homocysteic acid release from astrocytes: possible implication in glia-neuron signalling. Neuroscience 124, 377–386 (2004)

    Article  PubMed  CAS  Google Scholar 

  • M.P. Blaustein, J. Lederer, Sodium/calcium exchange: its physiological implication. Physiol. Rev. 79, 763–854 (1999)

    PubMed  CAS  Google Scholar 

  • F. Calegari, S. Coco, E. Taverna, M. Bassetti, C. Verderio, N. Corradi, M. Matteoti, P. Rosa, A regulated secretory pathway in cultured hippocampal astrocytes. J. Biol. Chem. 274, 22539–22547 (1999)

    Article  PubMed  CAS  Google Scholar 

  • T. Fellin, G. Carmignoto, Neurone-to-astrocyte signalling in the brain represents a distinct multifunctional unit. J. Physiol. 559, 3–15 (2004)

    Article  PubMed  CAS  Google Scholar 

  • W.F. Goldman, P.J. Yarowsky, M. Juhaszova, B.K. Krueger, M.P. Blaustein, Sodium/calcium exchange in rat cortical astrocytes. J. Neurosci. 14, 5834–5843 (1994)

    PubMed  CAS  Google Scholar 

  • V.A. Golovina, M.P. Blaustein, Unloading and refilling of two classes of spatially resolved endoplasmic reticulum Ca2+ stores in astrocytes. Glia 31, 15–28 (2000)

    Article  PubMed  CAS  Google Scholar 

  • C. Greever, T. Rauen, Electrogenic glutamate transporters in the CNS: molecular mechanism, pre-steady state kinetics, and their impact on synaptic signaling. J. Memb. Biol. 203, 1–20 (2005)

    Article  PubMed  CAS  Google Scholar 

  • X. Hua, E.B. Melarkey, V. Sunjara, S.E. Rosenwald, W.H. Li, V. Parpura, Ca2+-dependent glutamate release involves two classes of endoplasmic reticulum Ca2+ stores in astrocytes. J. Neurosci. Res. 76, 86–97 (2004)

    Article  PubMed  CAS  Google Scholar 

  • J. Hurtado, S. Borges, M. Wilson, Na+-Ca2+ exchanger controls the gain of the Ca2+ amplifier in the dendrites of amacrine cells. J. Neurophysiol. 88, 2765–2777 (2002)

    Article  PubMed  CAS  Google Scholar 

  • S.D. Jeftinija, K.V. Jeftinija, G. Stefanovic, Cultured astrocytes express proteins involved in vesicular glutamate release. Brain Res. 750, 41–47 (1997)

    Article  PubMed  CAS  Google Scholar 

  • M. Juhaszova, H. Shimizu, M.L. Borin, R.K. Yip, E.M. Santiago, G.E. Lindenmayer, M.P. Blaustein, Localization of the Na+-Ca2+ exchanger in vascular smooth muscle, and in neurons and astrocytes. Ann. N. Y. Acad. Sci. 779, 318–335 (1996)

    Article  PubMed  CAS  Google Scholar 

  • M. Kano, O. Garaschuk, A. Verkhratsky, A. Konnerth, Ryanodine receptor-mediated intracellular calcium release in rat cerebellar Purkinje neurones. J. Physiol. 487, 1–16 (1995)

    PubMed  CAS  Google Scholar 

  • M.H. Kin-Lee, B.T. Stoke, A.J. Yates, Reperfusion paradox: a novel mode of glial cell injury. Glia 5, 56–64 (1992)

    Article  Google Scholar 

  • D. Langley, B. Pearce, Ryanodine-induce intracellular calcium mobilization in culture astrocytes. Glia 12, 128–134 (1994)

    Article  PubMed  CAS  Google Scholar 

  • I. Llano, J. Gonzalez, C. Caputo, F.A. Lai, L.M. Blaynet, Y.P. Tan, A. Marty, Presynaptic calcium stores underlie large-amplitude miniature IPSCs and spontaneous calcium transients. Nat. Neurosci. 3, 1256–1265 (2000)

    Article  PubMed  CAS  Google Scholar 

  • K. Lo, H.N. Luk, T.Y. Chin, S.H. Chueh, Store depletion-induced calcium influx in rat cerebellar astrocytes. Br. J. Pharmacol. 135, 1383–1392 (2002)

    Article  PubMed  CAS  Google Scholar 

  • T. Iwamoto, T. Watano, M. shigegawa, A novel isothiourea frrivative selectivele inhibits de reverse mode of Na/Ca exchange in cells expresing NCX1. J Biol Biochem. 271, 22391–23397 (1998)

    PubMed  CAS  Google Scholar 

  • T. Matsuda, K. Takuma, E. Nishiguchi, H. Hashimoto, J. Azuma, A. Baba, Involvement of Na+-Ca2+ exchanger in reperfusion-induced delayed cell death of cultured rat astrocytes. Eur. J. Neurosci. 8, 951–958 (1996)

    Article  PubMed  CAS  Google Scholar 

  • M. Matyash, V. Matyash, C. Nolte, V. Sorrentino, H. Kettenmann, Requirement of functional ryanodine receptor type 3 for astrocyte migration. FASEB. J. 16, 84–86 (2002)

    PubMed  CAS  Google Scholar 

  • M.A. Micci, B.N. Cristensen, Na+/Ca2+ exchange in catfish retina horizontal cells: regulation of intracellular Ca2+ store function. Am. J. Physiol. 274, C1625–C1633 (1998)

    PubMed  CAS  Google Scholar 

  • M.A. Nazer, C. van Breemen, Functional linkage of Na+-Ca2+ exchange and sarcoplasmic reticulum Ca2+ release mediates Ca2+ cycling in vascular smooth muscle. Cell Calcium 24, 275–283 (1998)

    Article  PubMed  CAS  Google Scholar 

  • V. Parpura, T.A. Basarsky, F. Liu, S. Jeftinija, P.G. Haydon, Glutamate-mediated astrocyte-neuron signalling. Nature 369, 744–747 (1994)

    Article  PubMed  CAS  Google Scholar 

  • L. Pasti, T. Pozzan, G. Carmignoto, Long-lasting changes of calcium oscillations in astrocytes. A new form of glutamate-mediated plasticity. J. Biol. Chem. 270, 15203–15210 (1995)

    Article  PubMed  CAS  Google Scholar 

  • H. Rojas, M. Ramos, R. DiPolo, A genistein-sensitive Na+/Ca2+ exchange is responsible for the resting [Ca2+]i and most of the Ca2+ plasma membrane fluxes in stimulated rat cerebellar type 1 astrocytes. Jpn. J. Physiol. 54, 249–262 (2004)

    Article  PubMed  CAS  Google Scholar 

  • H. Rojas, C. Colina, M. Ramos, G. Benaim, H. Jaffe, C. Caputo, R. Dipolo, Na+ entry via glutamate transporter activates the reverse Na+/Ca2+ exchange and triggers Ca 2+i -induced Ca2+ release in rat cerebellar Type-1 astrocytes. J. Neurochem. 100, 1188–1202 (2007)

    Article  PubMed  CAS  Google Scholar 

  • P.B. Simpson, S. Mehotra, D. Langley, C.A. Sheppard, J.T. Russell, Specialized distribution of mitochondria and endoplasmic reticulum proteins define Ca2+ wave amplification sites in cultured astrocytes. J. Neurosci. Res. 52, 672–683 (1998a)

    Article  PubMed  CAS  Google Scholar 

  • P.B. Simpson, L.A. Holtzclaw, D.B. Langley, J.T. Russel, Characterization of ryanodine receptors in oligodendrocytes, type 2 astrocytes, and O-2A progenitors. J. Neurosci. Res. 52, 468–482 (1998b)

    Article  PubMed  CAS  Google Scholar 

  • K. Takuma, T. Matsuda, H. Hashimoto, S. Asano, A. BaBa, Culture rat astrocytes posses Na+-Ca2+ exchanger. Glia 12, 336–342 (1994)

    Article  PubMed  CAS  Google Scholar 

  • K. Takuma, T. Matsuda, U. Hashimoto, J. Kitanaka, S. Asano, A. Baba, Role of Na+-Ca2+ exchanger in agonist-induce Ca2+ signalling in cultured rat astrocytes. J. Neurochem. 67, 1840–1845 (1996)

    Article  PubMed  CAS  Google Scholar 

  • H. Uneyama, M. Munakata, N. Akaike, Caffeine response in pyramidal neurones freshly dissociated from rat hippocampus. Brain Res. 604, 24–31 (1993)

    Article  PubMed  CAS  Google Scholar 

  • Y. Usachev, A. Shmigol, P. Pronchuk, A. Kostyuk, A. Verkhratsky, Caffeine-induce calcium release from internal stores in cultured rat sensory neurones. Neuroscience 57, 845–859 (1993)

    Article  PubMed  CAS  Google Scholar 

  • A. Verkhratsky, H. Kettenmann, Calcium signalling in glial cells. TINS 19, 346–352 (1994)

    Google Scholar 

  • A. Verkhratsky, A. Shmilgol, Calcium-induce calcium release in neurons. Cell Calcium 19, 1–14 (1996)

    Article  PubMed  CAS  Google Scholar 

  • C. Vermeiren, M. Najimi, M. Vanhoutte, S. Tilleux, L. de Hemptinne, J.M. Maloteaux, E. hermans, Acute up-regulation of glutamate uptake mediated by mGluR5a in reactive astrocytes. J. Neurochem. 94, 405–416 (2005)

    Google Scholar 

  • D.J.A. Wyllie, A. Mathie, C.D. Symonds, S.G. Cull-Candy, Activation of glutamate receptors and mGluR5a Glutamate uptake in identified macroglial cells in rat cerebellar culture. J. Physiol. 432, 235–258 (1991)

    Google Scholar 

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Acknowledgements

This work was supported by FONACIT-Venezuela (G-0010000637).

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Correspondence to Reinaldo Di Polo .

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Rojas, H. et al. (2013). Sodium-Calcium Exchanger Modulates the L-Glutamate Cai 2+ Signalling in Type-1 Cerebellar Astrocytes. In: Annunziato, L. (eds) Sodium Calcium Exchange: A Growing Spectrum of Pathophysiological Implications. Advances in Experimental Medicine and Biology, vol 961. Springer, Boston, MA. https://doi.org/10.1007/978-1-4614-4756-6_22

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