Abstract
Two glutamate receptor agonists, NMDA (N-methyl-d-aspartic acid) and ACPD (cis-(1S/3R)-1-aminocyclopentane-1,3-dicarboxylic acid), induce the reactive oxygen species (ROS) production in rat cerebellum granule cells, whereas the third one, 3-HPG (3-hydroxyphenylglycine), decreases this parameter. The simultaneous presence of 3-HPG, together with NMDA or ACPD, prevents the generation of ROS by neuronal cells. A similar effect of these ligands on Na+/K+-ATPase can be demonstrated: NMDA and ACPD inhibited the enzyme activity, but 3-HPG activated Na+/K+-ATPase and prevented its inhibition by NMDA or ACPD. In terms of current classification, NMDA is an agonist of ionotropic glutamate receptors of the so-called NMDA class, whereas ACPD and 3-HPG belong to metabotropic agonists, the former primarily being an activator of metabotropic glutamate receptors (mGluRs) of groups 2 and 3, and the latter, that of mGluRs of groups 1 and 5. Thus, the data presented illustrate the existence of diverse mechanisms of the cross talk between Na+/K+-ATPase and different glutamate receptors, as well as that between glutamate receptors of different classes.
This is a preview of subscription content, log in via an institution to check access.
Similar content being viewed by others
References
Abdul-Ghani M. A., Valiante T. A., Carlen P. L., and Pennefather P. S. (1996) Metabotropic glutamate receptors coupled to IP3 production mediate inhibition of IAHP in rat dentate granule neurons. J. Neurophysiol. 76, 2691–2670.
Ambrosini A., Bresciani L., Fracchia S., Brunello N., and Racagni G. (1995) Metabotropic glutamate receptors negatively coupled to adenylate cyclase inhibit N-methyl-D-aspartate receptor activity and prevent neurotoxicity in mesencephalic neurons in vitro. Mol. Pharmacol. 47, 1057–1064.
Avrova N. F., Viktorov I. V., Tyurin V. A., Zacharova I. O., Sokolova T. V., Andreeva N. A., et al. (1998) Inhibition of glutamate-induced intensification of free radical reactions by gangliosides. Neurochem. Res. 23, 945–952.
Belusa R., Aizman O., Andersson R.- H., and Aperia A. (2002) Changes in Na/K-ATPase activity influence cell attachment to fibronectin. Am. J. Physiol. 282, C302-C309.
Boldyrev A. (2001) Na/K-ATPase as an oligomeric ensemble. Biochemistry (Moscow) 66, 821–831.
Boldyrev A. A. (2002) Significance of reactive oxygen species for neuronal function, in Free Radicals, Nitric Oxide and Inflammation: Molecular, Biochemical, and Clinical Aspects, Tomasi, A., Ozben T., and Skulachev V., pp. 157–173.
Boldyrev A., Bulygina E., Yuneva M., and Schoner W. (2003) Na/K-ATPase regulates intracellular ROS level in rat cerebellum granule cells. Ann. NY Acad. Sci. 986, 519–521.
Boldyrev A., Carpenter D., and Johnson P. (2000a) Natural mechanisms of protection of neurons against oxidative stress. Recent Res. Dev. Comp. Biochem. Physiol. 1, 91–103.
Boldyrev A., Song R., Dyatlov V., Lawrence D., and Carpenter D. (2000b) Neuronal cell death and reactive oxygen species. Cell. Mol. Neurobiol. 20, 433–450.
Boldyrev A., Song R., Lawrence D., and Carpenter D. O. (1999) Carnosine protects against excitototxic cell death independently of effects on reactive oxygen species. Neuroscience 94, 571–577.
Bulygina E., Lyapina L., and Boldyrev A. (2002) Activation of glutamate receptors inhibits Na/K-ATPase of cerebellum granule cells. Biochemistry (Moscow) 67, 1209–1214.
Cambonie G., Kamenka J.-M., and Barbanel G. (2001) Glutamate inhibition of NMDA-induced hydroxyl radical release: an ontogenic study in rat. Neuropharmacol. Neurotoxicol. 12, 2035–2039.
Chibalin A., Kovalenko M., Ryder J.-M., Feraille E., Wallberg H., and Zieratt J. R. (2001) Insulin and glucose induced phosphorylation of the Na/K-ATPase alpha-subunits in rat skeletal muscle. Endocrinology 142, 3474–3482.
Conn P. J. and Pin J.-P. (1997) Pharmacology and functions of metabotropic glutamate receptors. Annu. Rev. Pharmacol. Toxicol. 17, 205–237.
Crow J. P. (1997) Dichlorodihydrofluorescein and dihydrorhodamine 123 are sensitive indicators of peroxinitrite in vitro: implications for intracellular measurement of reactive nitrogen and oxygen species. Nitric Oxide 1, 145–157.
Curtin J., Donovan M., and Cotter T. (2002) Regulation and measurement of oxidative stress in apoptosis. J. Immunol. Methods 265, 49–72.
Debanne D. and Thompson S. M. (1996) Associative long-term depression in the hippocampus in vitro. Hippocampus 6, 9–16.
Halliwell B. (1992) Reactive oxygen species and the central nervous system. J. Neurochem. 59, 1609–1632.
Hartley D. M., Kurth M. C., Bjerkness L., Weiss J. H., and Choi D. W. (1993) Glutamate receptor-induced 45Ca2+ accumulation in cortical cell culture correlates with subsequent neuronal degeneration. J. Neurosci. 13, 1993–2000.
Haug L. S., Jensen V., Hvalby O., Walaas S. I., and Ostvold A. C. (1999) Phosphorylation of the inositol 1,4,5-triphosphate receptor by cyclic nucleotide-dependent kinase in vitro and in rat cerebellar slices in situ. J. Biol. Chem. 274, 7467–7473.
Inoue N. and Matsui H. (1990) Activation of a brain type Na-pump after glutamate excitation of cerebral neurons. Brain Res. 534, 309–312.
Jones O. and Hancock J. (2002) The NADPH oxidase of neutrophils and other cells, in Free Radicals and Inflammation, Winyard, P. G., Blake, D. R., and Evans, C. H., eds., Birkhauser, Boston, MA, pp. 21–46.
Knoflach F., Woltering T., Adam G., Mutel V., and Kemp J.-A. (2001) Pharmacological properties of native metabotropic glutamate receptors in freshly dissociated Golgi cells of the rat cerebellum. Neuropharmacology 40, 163–169.
Marcaida G., Kosenko E., Minana M., Grisolia S., and Felipo V. (1996) Glutamate induces a calcineurin-mediated dephosphorylation of Na/K-ATPase that results in its activation in cerebellar neurons in culture. J. Neurochem. 66, 99–104.
Mochammadi K., Kometiani P., Xie Z., and Askari A. (2001) Role of protein kinase C in the signal pathways that link Na/K-ATPase to ERK1/2. J. Biol. Chem. 276, 42050–42056.
Oyama Y., Carpenter D., Chikahisa L., and Okazaki E. (1996) Flow cytometric estimation on glutamate and kainite induced increases in intracellular calcium of brain neurons: a technical aspect. Brain Res. 728, 121–124.
Prisco S., Natoli S., Bernardi G., and Mercuri N.-B. (2002) Group 1 metabotropic glutamate receptors activate burst firing in rat midbrain dopaminergic neurons. Neuropharmacology 42, 289–296.
Scheiner-Bobis G. and Schoner W. (2001) A fresh facet for ouabain action. Nat. Med. 7, 1288–1289.
Schoner W. (2002) Endogenous cardiac glycosides, a new class of steroid hormones. Eur. J. Biochem. 269, 2440–2448.
Sureda F., Camins A., Trullas R., Camarasa J., and Eskubedo E. (1996) A flow cytometric study of N-methyl-D-aspartate effects on dissociated cerebellar cells. Brain Res. 723, 110–114.
Watkins J. C. and Collingridge G. L. (1994) Phenylglycine derivatives as antagonists of metabrotropic glutamate receptors. Trends Pharmacol. Sci. 15, 333–342.
Xie Z. and Askari A. (2002) Na+/K+-ATPase as a signal inducer, Eur. J. Biochem. 269, 2434–2439.
Xie Z., Kometiani P., Liu J., Li, J., Shapiro J., and Askari A. (1999) Intracellular reactive oxygen species mediate the linkage of Na/K-ATPase to hypertrophy and its marker genes in cardiac myocytes. J. Biol. Chem. 274, 19323–19328.
Author information
Authors and Affiliations
Corresponding author
Rights and permissions
About this article
Cite this article
Boldyrev, A., Bulygina, E., Carpenter, D. et al. Glutamate receptors communicate with Na+/K+-ATPase in rat cerebellum granule cells. J Mol Neurosci 21, 213–222 (2003). https://doi.org/10.1385/JMN:21:3:213
Received:
Accepted:
Issue Date:
DOI: https://doi.org/10.1385/JMN:21:3:213