Abstract
NO donor nitroprusside (NP) is a biologically active drug with hypotensive and neurotropic properties. Its effects are due to NO as well as to other derivates, specifically ferricyanide (FC) and ferrocyanide (F(2+)C) ions. In the present work we studied effects of NP, FC, and F(2+)C on delayed rectifier K+ current. The experiments were conducted on isolated neurons of land snail Helix using two-microelectrode voltageclamp technique. Delayed rectifier K+ current often displayed abnormal rectification. NP (1 mM) caused voltage-dependent reduction of K+ current, which looked like enhancement of the abnormal rectification. FC (1 mM)—but not F(2+)C—acted likewise; the effects of NP and FC were not additive. Dibutiryl cGMP (dbcGMP) had an opposite effect, weakening abnormal rectification of the K+ current. Protein kinase inhibitor H-8 (10 μM) caused voltage-dependent reduction of the K+ current, as NP and FC did. The effects of H-8 and NP and effects of H-8 and FC were not additive. The results suggest that: (i) NP effects on delayed rectifier K+ current are mediated by FC and (ii) the effects of these drugs involve phosphorylation processes.
Similar content being viewed by others
References
Onoue, H. and Katusic, Z.S., Role of Potassium Channels in Relaxations of Canine Middle Cerebral Arteries Induced by Nitric Oxide Donors, Stroke, 1997, vol. 28, no. 6, pp. 1264–1270.
Carrier, G.O., Fuchs, L.C., Winecoff, A.P., Giulumian, A.D., and White, R.E., Nitrovasodilators Relax Mesenteric Microvessels by cGMP-Induced Stimulation of Ca2+-Activated K+ Channels, Am. J. Physiol., 1997, vol. 273, pp. H76–H84.
Chen, M.J. and Russo-Neustadt, A.A., Nitric Oxide Signaling Participates in Norepinephrine-Induced Activity of Neuronal Intracellular Survival Pathways, Life Sci., 2007, vol. 81, no. 16, pp. 1280–1290.
Amoroso, S., Tortiglione, A., Secondo, A., Catalano, A., Montagnani, S., Di Renzo, G., and Annunziato, L., Sodium Nitroprusside Prevents Chemical Hypoxia-Induced Cell Death through Iron Ions Stimulating the Activity of the Na+-Ca2+ Exchanger in C6 Glioma Cells, J. Neurochem., 2000, vol. 74, no. 4, pp. 1505–1513.
Huang, C.Y., Yang, H.I., Chen, S.D., Shaw, F.Z, and Yang, D.I., Protective Effects of Lipopolysaccharide Preconditioning Against Nitric Oxide Neurotoxicity, J. Neurosci. Res., 2008, vol. 86, no. 6, pp. 1277–1289.
Brynczka, C. and Merrick, B.A., Nerve Growth Factor Potentiates p53 DNA Binding but Inhibits Nitric Oxide-Induced Apoptosis in Neuronal PC12 Cells, Neurochem. Res., 2007, vol. 32, no. 9, pp. 1573–1585.
Li, W., Lee, N.T., Fu, H., Kan, K.K., Pang, Y., Li, M., Tsim, K.W., Li, X., and Han, Y., Neuroprotection via Inhibition of Nitric Oxide Synthase by Bis(7)-Tacrine, NeuroRept., 2006, vol. 17, no. 5, pp. 471–474.
Serpa, V., Vernal, J., Lamattina, L., Grotewold, E., Cassia, R., and Terenzi, H., Inhibition of AtMYB2 DNABinding by Nitric Oxide Involves Cysteine S-Nitrosylation, Biochem. Biophys. Res. Commun., 2007, vol. 361, no. 4, pp. 1048–1053.
Li, G. and Wieraszko, A., Dual Effect of Sodium Nitroprusside on Potentials Recorded from Mouse Hippocampal Slices, Brain Res., 1994, vol. 667, pp. 33–38.
Riediger, T., Giannini, P., Erguven, E., and Lutz, T., Nitric Oxide Directly Inhibits Ghrelin-Activated Neurons of the Arcuate Nucleus, Brain Res., 2006, vol. 1125, no. 1, pp. 37–45.
Yang, C.Y., Tan, P.C., Wu, W.C., Hsu, J.C., See, L.C., and Chai, C.Y., Inhibitory Effects of Propofol on Neuron Firing Activities in the Rostral Ventrolateral Medulla, Chin. J. Physiol., 2007, vol. 50, no. 5, pp. 251–257.
Sitmo, M., Rehn, M., and Diener, M., Stimulation of Voltage-Dependent Ca2+ Channels by NO at Rat Myenteric Neurons, Am. J. Physiol. Gastrointest. Liver Physiol., 2007, vol. 293, no. 4, pp. G886–G893.
Manzoni, O., Prezeau, L., Desagher, S., Sahuquet, A., Sladeczek, F., Bockaert, J., and Fagni, L., Sodium Nitroprusside Blocks NMDA Receptors via Formation of Ferrocyanide Ions, NeuroRept., 1992, vol. 3, no. 1, pp. 77–80.
Kiedrowski, L., Costa, E., and Wroblewski, J.T., Sodium Nitroprusside Inhibits N-Methyl-D-Aspartate-Evoked Calcium Influx via a Nitric Oxide- and cGMP-Independent Mechanism, Mol. Pharmacol., 1992, vol. 41, no. 4, pp. 779–784.
Kadekaro, M., Su, G., Chu, R., Lei, Y., Li, J., and Fang, L., Nitric Oxide Up-Regulates the Expression of Calcium-Dependent Potassium Channels in the Supraoptic Nuclei and Neural Lobe of Rats Following Dehydration, Neurosci. Lett., 2006, vol. 404, nos. 1–2, pp. 50–55.
Schrofner, S., Zsomboka, A., Hermann, A., and Kerschbaum, H.H., Nitric Oxide Decreases a Calcium-Activated Potassium Current via Activation of Phosphodiesterase 2 in Helix U-Cells, Brain Res., 2004, vol. 999, pp. 98–105.
Ahern, G.P., Klyachko, V.A., and Jackson, M.B., cGMP and S-Nitrosylation: Two Routes for Modulation of Neuronal Excitability by NO, Trends Neurosci., 2002, vol. 25, no. 10, pp. 510–517.
Almanza, A., Navarrete, F., Vega, R., and Soto, E., Modulation of Voltage-Gated Ca2+ Current in Vestibular Hair Cells by Nitric Oxide, J. Neurophysiol., 2007, vol. 97, no. 2, pp. 1188–1195.
Biasetti, M. and Dawson, R. Jr., Effects of Sulfur Containing Amino Acids on Iron and Nitric Oxide Stimulated Catecholamine Oxidation, Amino Acids, 2002, vol. 22, no. 4, pp. 351–368.
Solntseva, E.I., Bukanova, J.V., and Skrebitsky, V.G., NO-Free Ferricyanide Simulates the Effects of Sodium Nitroprusside on High Threshold Potassium Currents in Molluscan Neurons, Biol. Membrany (Rus.), 2001, vol. 18, pp. 271–276.
Gutman, G.A., Chandy, K.G., Grissmer, S., Lazdunski, M., McKinnon, D., Pardo, L.A., Robertson, G.A., Rudy, B., Sangunetti, M.C., Stuhmer, W., and Wang, X., International Union of Pharmacology. LIII. Nomenclature and Molecular Relationships of Voltage-Gated Potassium Channels, Pharmacol. Rev., 2005, vol. 57, pp. 473–508.
Bai, C.X., Takahashi, K., Masumiya, H., Sawanobori, T., and Furukawa, T., Nitric Oxide-Dependent Modulation of the Delayed Rectifier K+ Current and the L-Type Ca2+ Current by Ginsenoside Re, an Ingredient of Panax Ginseng, in Guinea-Pig Cardiomyocytes, Br. J. Pharmacol., 2004, vol. 142, no. 3, pp. 567–575
Nunez, L., Vaquero, M., Gomez, R., Caballero, R., Mateos-Caceres, P., Macaya, C., Iriepa, I., Galvez, E., Lopez-Farre, A., Tamargo, J., and Delpon, E., Nitric Oxide Blocks hKv1.5 Channels by S-Nitrosylation and by a Cyclic GMP-Dependent Mechanism, Cardiovasc. Res., 2006, vol. 72, no. 1, pp. 80–89.
Bukanova, J.V., Solntseva, E.I., and Skrebitsky, V.G., The Effects of Ferric Iron on Voltage-Gated Potassium Currents in Molluscan Neurons, NeuroRept., 2007, vol. 18, pp. 1395–1398.
Aldrich, R.W., Getting, P.A., and Thompson, S.H., Inactivation of Delayed Outward Current in Molluscan Neurone Somata, J. Physiol., 1979, vol. 291, pp. 507–530.
Lopatin, A.N., Makhina, E.N., and Nichols, C.G., Potassium Channel Block by Cytoplasmic Polyamines as the Mechanism of Intrinsic Rectification, Nature, 1994, vol. 372, no. 6504, pp. 366–369.
Lopatin, A.N. and Nichols, C.G., Internal Na+ and Mg2+ Blockade of DRK1 (Kv2.1) Potassium Channels Expressed in Xenopus Oocytes. Inward Rectification of a Delayed Rectifier, J. Gen. Physiol., 1994, vol. 103, pp. 203–216.
Gomez-Hernandez, J.M., Lorra, C., Pardo, L.A., Stuhmer, W., Pongs, O., Heinemann, S.H., and Elliott, A.A., Molecular Basis for Different Pore Properties of Potassium Channels from the Rat Brain Kv1 Gene Family, Pflügers Arch., 1997, vol. 434, no. 6, pp. 661–668.
Hidaka, H. and Kobayashi, R., Pharmacology of Protein Kinase Inhibitors, Annu. Rev. Pharmacol. Toxicol., 1992, vol. 32, pp. 377–397.
Giovannini, M.G., The Role of the Extracellular Signal-Regulated Kinase Pathway in Memory Encoding, Rev. Neurosci., 2006, vol. 17, no. 6, pp. 619–634.
Reuhl, T.O., Amador, M., Moorman, J.R., Pinkham, J., and Dani, J.A. Nicotinic Acetylcholine Receptors are Directly Affected by Agents Used to Study Protein Phosphorylation, J. Neurophysiol., 1992, vol. 68, no. 2, pp. 407–416.
Wei, J.Y., Cohen, E.D., and Barnstable, C.J., Direct Blockade of Both Cloned Rat Rod Photoreceptor Cyclic Nucleotide-Gated Non-Selective Cation (CNG) Channel Alpha-Subunit and Native CNG Channels from Xenopus Rod Outer Segments by H-8, a Non-Specific Cyclic Nucleotide-Dependent Protein Kinase Inhibitor, Neurosci. Lett., 1997, vol. 233, no. 1, pp. 37–40.
Author information
Authors and Affiliations
Corresponding author
Additional information
Original Russian Text © E.I. Solntseva, J.V. Bukanova, V.G. Skrebitsky, 2009, published in Biologicheskie Membrany, 2009, Vol. 26, No. 6, pp. 486492–123123123.
The article was translated by the authors.
Rights and permissions
About this article
Cite this article
Solntseva, E.I., Bukanova, J.V. & Skrebitsky, V.G. Voltage-dependent blockade of delayed rectifier K+ current by nitroprusside and ferricyanide. Biochem. Moscow Suppl. Ser. A 3, 431–437 (2009). https://doi.org/10.1134/S1990747809040102
Received:
Published:
Issue Date:
DOI: https://doi.org/10.1134/S1990747809040102