Cross-talk between glutamate and nucleotide receptors in cerebellar granule neurons in culture

  1. Salas, Elvira 1
  2. León Navarro, David Agustín 1
  3. Sánchez Nogueiro, Jesús 1
  4. Marín García, Patricia 1
  5. Miras Portugal, María Teresa 1
  1. 1 Facultad de Veterinaria, Universidad Complutense de Madrid
Revista:
Anales de la Real Academia Nacional de Farmacia

ISSN: 1697-4298,  0034-0618

Año de publicación: 2010

Número: 1

Páginas: 3-22

Tipo: Artículo

SCOPUS: 2-s2.0-77953094568 DIALNET GOOGLE SCHOLAR lock_openAcceso abierto editor

Otras publicaciones en: Anales de la Real Academia Nacional de Farmacia

Resumen

ATP elicits Ca2+ transients in cultured cerebellar granule neurons acting through specific ionotropic (P2X) and metabotropic (P2Y) purinergic receptors. In these neurons, application of L-Glutamate (L-Glu) immediately before ATP induced a prolonged reduction of ATP-mediated responses that remains at least 5 minutes after L-Glu wash out. alpha-amino-3-hydro-5-methyl-4-isoxazolpropionic acid (AMPA), N-methyl-D-aspartate (NMDA) and 3,5-dihydroxyphenyl-glycine (DHPG), selective agonists of ionotropic non-NMDA, NMDA and Group I metabotropic glutamate receptors respectively, mimicked Glu-induced attenuating effects. The activity of calcium-calmodulin dependent protein kinase II (CaMKII) seems to be involved, at least at long term, because inhibitors of CaMKII, 1-[N,O-bis(5-isoquinolinesulfonyl)-N-methyl-L-tyrosyl]-4phenylpiperazine (KN-62) and N-[2-[[[3-(4'-chlorophenyl)-2-propenyl]methylamino]methyl]phenyl]-N-(2-hydroxyethyl)-4'-methoxybenzenesulfonamide (KN-93), abolished the inhibitory effect of L-Glu on ATP-mediated responses. However, it is likely that other protein kinases could be involved in the cross-talk process between both groups of receptors at short term. Therefore, these results demonstrate that the activation of glutamate receptors is able to modulate nucleotide responses in cerebellar granule neurons.

Referencias bibliográficas

  • Bastian, A. J.; Mugnaini, E. & Thach, W. T. (1999) Cerebellum. In Fundamental Neuroscience, Ed. Zigmond, M. J.; Bloom, F. E.; Landis, S. C.; Roberts, J. L. & Squire, L. R. Academic Press, San Diego, California, USA. pp. 973-992.
  • Cavaliere, F.; Amadio, S.; Angelini, D. F.; Sancesario, G.; Bernardi, G. & Volonté, C. (2004) Role of the metabotropic P2Y(4) receptor during hypoglycemia: cross talk with the ionotropic NMDAR1 receptor. Exp. Cell Res. 300: 149-158.
  • Colbran, R. J. (2004) Targeting of calcium/calmodulin-dependent protein kinase II. Biochem. J. 378: 1-16.
  • D'Angelo, E.; Rossi, P.; Armano, S. & Taglietti, V. (1999) Evidence for NMDA and mGlu receptor-dependent long-term potentiation of mossy fiber-granule cell transmission in rat cerebellum. J. Neurophysiol. 81: 277-287.
  • Díaz-Hernández, M.; Sánchez-Nogueiro, J. & Miras-Portugal, M. T. (2006) Role of CaCMKII in the cross talk between ionotropic nucleotides and nicotinic receptors in individual cholinergic terminals. J. Mol. Neurosci. 30: 177-180.
  • Fountain, S. J. & North, R. A. (2006) A C-terminal lysine that controls human P2X4 receptor desensitization. J. Biol. Chem. 281: 15044-15049.
  • Gargett, C. E. & Wiley, J. S. (1997) The isoquinoline derivative KN-62 a potent antagonist of the P2Z-receptor of human lymphocytes. Brit. J. Pharmacol. 120: 1483-1490.
  • Garthwaite, J. & Brodbelt, A. R. (1990) Glutamate as the principal mossy fibre transmitter in rat cerebellum: pharmacological evidence. Eur. J. Neurosci. 2: 177-180.
  • Gasteiger, E.; Gattiker, A.; Hoogland, C.; Ivanyi, I.; Appel, R. D. & Bairoch, A. (2003) ExPASy: The proteomics server for in-depth protein knowledge and analysis. Nucleic Acids Res. 31: 3784-3788.
  • Gómez-Villafuertes, R.; Gualix, J. & Miras-Portugal, M. T. (2001) Single GABAergic synaptic terminals from rat midbrain exhibit functional P2X and dinucleotide receptors, able to induce GABA secretion. J. Neurochem. 77: 84-93. (Pubitemid 32245082)
  • Grynkiewicz, G.; Poeni, M. & Tsien, R. Y. (1985) A new generation of fluorescent calcium indicators with greatly improved fluorescence properties. J. Biol. Chem. 260: 3440-3450.
  • Gualix, J.; Gómez-Villafuertes, R.; Díaz-Hernández, M. & Miras-Portugal, M. T. (2003) Presence of functional ATP and dinucleotide receptors in glutamatergic synaptic terminal from rat midbrain. J. Neurochem. 87: 160-171. (Pubitemid 37210650)
  • Hervás, C.; Pérez-Sen, R. & Miras-Portugal, M. T. (2003) Coexpression of functional P2X and P2Y nucleotide receptors in single cerebellar granule cells. J. Neurosci. Res. 73: 384-399.
  • Humphreys, B. D.; Virginio, C.; Surprenant, A.; Rice, J. & Dubyak, G. R. (1998) Isoquinolines as antagonists of the P2X7 nucleotide receptor: high selectivity for the human versus rat receptor homologues. Mol. Pharmacol. 54: 22-32.
  • Ito, I.; Kohda, A.; Tanabe, S.; Hirose, E.; Hayashi, M.; Mitsunaga, S. & Sugiyama, H. (1992) 3,5-Dihydroxyphenyl-glycine: a potent agonist of metabotropic glutamate receptors. Neuroreport. 3: 1013-1016.
  • Jo, Y. H. & Schlichter, R. (1999) Synaptic corelease of ATP and GABA in cultured spinal neurons. Nature Neurosci. 2: 241-245.
  • Kim, M.; Jiang, L. H.; Wilson, H. L.; North, R. A. & Surprenant, A. (2001) Proteomic and functional evidence for a P2X7 receptor signalling complex. EMBO J. 20: 6347-6358.
  • León, D.; Hervás, C. & Miras-Portugal, M. T. (2006) P2Y 1 and P2X 7 receptors induce calcium/calmodulin- dependent protein kinase II phosphorylation in cerebellar granule neurons. Eur. J. Neurosci. 23: 2999-3013.
  • León, D.; Sánchez-Nogueiro, J.; Marín-García, P. & Miras-Portugal, M. T. (2008) Glutamate release and synapsin-I phosphorylation induced by P2X 7 receptors activation in cerebellar granule neurons. Neurochem. Int. 52: 1148-1159.
  • Marín-García, P.; Sánchez-Nogueiro, J. & León, D. (2007) Glutamate determinations using Amplex Red Glutamic Acid Assay are afected by P2X agonist BzATP. An. R. Acad. Nac. Farm. 73: 441-452.
  • Masgrau, R.; Servitja, J. M.; Young, K. W.; Pardo, R.; Sarri, E.; Nahorski, S. R. & Picatoste, F. (2001) Characterization of the metabotropic glutamate receptors mediating phospholipase C activation and calcium release in cerebellar granule cells: calcium-dependence of the phospholipase C response. Eur. J. Neurosci. 13: 248-256.
  • Miras-Portugal, M. T.; Marín-García, P.; Carrasquero, L. M. G.; Delicado, E. G.; Díaz-Hernández, M.; Díaz- Hernández, J. I.; Díez-Zaera, M.; Fideu, M. D.; Gómez-Villafuertes, R.; Gualix, J.; León, D.; León-Otegui, M.; Ortega, F.; Pérez-Sen, R.; Salas, E. & Sánchez-Nogueiro, J. (2007) Physiological role of extra-cellular nucleotides at the central nervous system: signalling through P2X and P2Y receptors. An. R. Acad. Nac. Farm. 73: 1127-1157.
  • North, R. A. & Verkhratsky, A. (2006) Purinergic transmission in the central nervous system. Pflugers Arch. 452: 479-485.
  • Obenauer, J. C.; Cantley, L. C. & Yaffe, M. B. (2003) Scansite 2.0: Proteome-wide prediction of cell signaling interactions using short sequence motifs. Nucleic Acids Res. 31: 3635-3641.
  • Pankratov, Y.; Lalo, U.; Verkhratsky, A. & North, R. A. (2006) Vesicular release of ATP at central synapses. Pflugers Arch. 452: 589-597.
  • Portzehl, H.; Caldwell, P. C. & Rueegg, J. C. (1964) The dependence of contraction and relaxation of muscle fibres from the crab Maia squinado on the internal concentration of free calcium ions. Biochim. Biophys. Acta. 79: 581-591.
  • Rodrigues, R. J.; Almeida, T.; de Mendonca, A. & Cunha, R. A. (2006) Interaction between P2X and nicotinic acetylcholine receptors in glutamate nerve terminals of the rat hippocampus. J. Mol. Neurosci. 30: 173-176.
  • Sánchez-Nogueiro, J.; Marín-García, P. & Miras-Portugal, M. T. (2005) Characterization of a functional P2X 7-like receptor in cerebellar granule neurons from P2X 7 knockout mice. FEBS Lett. 579: 3783-3788. (Pubitemid 40897725)
  • Sánchez-Nogueiro, J.; Marín-García, P.; León, D.; León-Otegui, M.; Salas, E.; Gómez-Villafuertes, R.; Gualix, J. & Miras-Portugal, M. T. (2009) Axodendritic fibres of mouse cerebellar granule neurons exhibit a diversity of functional P2X receptors. Neurochem. Int. 55: 671-682.
  • Silinsky, E. M. & Redman, R. S. (1996) Synchronous release of ATP and neurotransmitter within milliseconds of a motor nerve impulse in the frog. J. Physiol. 492 (Pt 3): 815-822.
  • Sumi, M.; Kiuchi, K.; Ishikawa, T.; Ishii, A.; Hagiwara, M.; Nagatsu, T. & Hidaka, H. (1991) The newly synthesized selective Ca2+/calmodulin dependent protein kinase II inhibitor KN-93 reduces dopamine contents in PC12h cells. Biochem. Biophys. Res. Commun. 181: 968-975.
  • Tokumitsu, H.; Chijiwa, T.; Hagiwara, M.; Mizutani, A.; Terasawa, M. & Hidaka, H. (1990) KN-62, 1-[N,O-bis(5-isoquinolinesulfonyl)-N-methyl-L- tyrosyl]-4-phenylpiperazi ne, a specific inhibitor of Ca2+/calmodulin-dependent protein kinase II. J. Biol. Chem. 265: 4315-4320.
  • Tulapurkar, M. E.; Zundorf, G. & Reiser, G. (2006) Internalization and desensitization of a green fluorescent protein-tagged P2Y nucleotide receptor are differently controlled by inhibition of calmodulin-dependent protein kinase II. J. Neurochem. 96: 624-634.
  • Volonté, C.; Amadio, S.; D'Ambrosi, N.; Colpi, M. & Burnstock, G. (2006) P2 receptor web: complexity and fine-tuning. Pharmacol. Therap. 112: 264-280.
  • Xue, Y.; Zhou, F.; Zhu, M.; Ahmed, K.; Chen, G. & Yao, X. (2005) GPS: a comprehensive www server for phosphorylation sites prediction. Nucleic Acids Res. 33: W184-187. (Pubitemid 44529905)
Fuente de los datos: Dialnet