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Role of Potassium Channels in the Effects of Hydrogen Sulfide on Contractility of Gastric Smooth Muscle Cells in Rats

  • Comparative and Ontogenic Physiology
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Journal of Evolutionary Biochemistry and Physiology Aims and scope Submit manuscript

An Erratum to this article was published on 01 January 2019

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Abstract

The effect of sodium hydrosulfide (NaHS), a hydrogen sulfide (H2S) donor, on spontaneous contractile activity of rat gastric smooth muscle cells was analyzed. Experiments were conducted on gastric stripes under conditions of isometric contraction. It was shown that NaHS has a biphasic effect on spontaneous contractile activity, increasing tonic tension and the amplitude of phasic contractions within the first minutes since application. This initial phase is followed by a decrease in amplitude, basal tone, and frequency of spontaneous contractions. The inhibitory effect of NaHS was dose-dependent at concentrations from 10 to 600 μM. Preliminary application of tetraethylammonium and 4-aminopirydine, inhibitors of voltage-gated and calciumactivated potassium channels, prevented a NaHS-induced initial increase in basal tone and phasic contraction amplitude. Activation of ATP-dependent potassium channels (KATP-channels) by diazoxide prevented in part a NaHS-induced decrease in basal tone and amplitude of spontaneous contractions. Glibenclamide, an inhibitor of KATP-channels, decreased the inhibitory effect of NaHS on amplitude, basal tone and frequency of spontaneous contractions. It was concluded that in rat gastric smooth muscles the excitatory effect of H2S is mediated by the inhibition of voltagegated and calcium-activated potassium channels, while its inhibitory effect involves the activation of KATP-channels.

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Change history

  • 24 April 2019

    1. On page 400. The name of the third author <Emphasis Type="Italic">L. M. Gabitova</Emphasis> should read <Emphasis Type="Italic">D. M. Gabitova</Emphasis>.

    2. On page 400, in running head. The name of the third author <Emphasis Type="Italic">L.M. Gabitova</Emphasis> should read <Emphasis Type="Italic">D.M. Gabitova</Emphasis>.

References

  1. Sitdikova, G.F. and Zefirov, A.L., Gaseous mediators in the nervous system, Ross. Fiziol. Zh., 2006, vol. 92, no. 7, pp. 872–882.

    CAS  Google Scholar 

  2. Sitdikova, G.F., Yakovlev, A.V., and Zefirov, A.L., Gaseous mediators: from toxic effects to regulation of cell functions and clinical use, Byull. Sib. Med., 2014, vol. 13, no. 6, pp. 185–200.

    Google Scholar 

  3. Linden, D.R., Hydrogen sulfide signaling in the gastrointestinal tract, Antioxid. Redox Signal., 2014, vol. 20, no. 5, pp. 818–830.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  4. Farrugia, G. and Szurszewski, J.H., Carbon monoxide, hydrogen sulfide, and nitric oxide as signaling molecules in the gastrointestinal tract, Gastroenterol., 2014, vol. 147, no. 2, pp. 303–313.

    Article  CAS  Google Scholar 

  5. Gerasimova, E., Lebedeva, J., Yakovlev, A., Zefirov, A., Giniatullin, R., and Sitdikova, G., Mechanisms of hydrogen sulfide (H2S) action on synaptic transmission at the mouse neuromuscular junction, Neurosci., 2015, vol. 303, pp. 577–585.

    Article  CAS  Google Scholar 

  6. Yakovlev, A.V., Kurmasheva, E.D., Giniatullin, R., Khalilov, I., and Sitdikova, G.F., Hydrogen sulfide inhibits giant depolarizing potentials and abolishes epileptiform activity of neonatal rat hippocampal slices, Neurosci., 2017, vol. 340, pp. 153–165.

    Article  CAS  Google Scholar 

  7. Martin, G.R., McKnight, G.W., Dicay, M.S., Coffin, C.S., Ferraz, J.G., and Wallace, J.L., Hydrogen sulphide synthesis in the rat and mouse gastrointestinal tract, Digest. Liver Dis., 2010, vol. 42, no. 2, pp. 103–109.

    Article  CAS  Google Scholar 

  8. Huang, X., Meng, X.M., Liu, D.H., Wu, Y.S., Guo, X., Lu, H.L., Kim, Y.C., and Xu, W.X., Different regulatory effects of hydrogen sulfide and nitric oxide on gastric motility in mice, Eur. J. Pharmacol., 2013, vol. 720, no. 1, pp. 276–285.

    Article  CAS  PubMed  Google Scholar 

  9. Meng, X.M., Huang, X., Zhang, C.M., Liu, D.H., Lu, H.L., Kim, Y.C., and Xu, W.X., Hydrogen sulfide-induced enhancement of gastric fundus smooth muscle tone is mediated by voltage-dependent potassium and calcium channels in mice, World J. Gastroenterol., 2015, vol. 21, no. 16, p. 4840.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  10. Wallace, J.L., Caliendo, G., Santagada, V., and Cirino, G., Markedly reduced toxicity of a hydrogen sulphide-releasing derivative of naproxen (ATB-346), Brit. J. Pharmacol., 2010, vol. 159, no. 6, pp. 1236–1246.

    Article  CAS  Google Scholar 

  11. Gallego, D., Clave, P., Donovan, J., Rahmati, R., Grundy, D., Jimenez, M., and Beyak, M.J., The gaseous mediator, hydrogen sulphide, inhibits in vitro motor patterns in the human, rat and mouse colon and jejunum, Neurogastroenterol. Motil., 2008, vol. 20, pp. 1306–1316.

    Article  CAS  PubMed  Google Scholar 

  12. Shafigullin, M.Y., Zefirov, R.A., Sabirullina, G.I., Zefirov, A.L., and Sitdikova, G.F., Effects of a hydrogen sulfide donor on spontaneous contractile activity of rat stomach and jejunum, Bull. Exp. Biol. Med., 2014, vol. 157, no. 3, pp. 302–306.

    Article  CAS  PubMed  Google Scholar 

  13. Gabitova, D.M., Shaidullov, I.F., Sabirullina, G.I., Shafigullin, M.U., Sitdikov, F.G., and Sitdikova, G.F., Role of cyclic nucleotides in the effect of hydrogen sulfide on contractions of rat jejunum, Bull. Exp. Biol. Med., 2017, vol. 163, no. 1, pp. 14–17.

    Article  CAS  PubMed  Google Scholar 

  14. Medeiros, J.V.R., Bezerra, V.H., Lucetti, L.T., Lima-Júnior, R.C.P., Barbosa, A.L.R., Tavares, B.M., Magalhães, P.J.C., Santos, A.A., Cunha, F.Q., Soares, P.M.G., and Souza, M.H., Role of KATP channels and TRPV1 receptors in hydrogen sulfide-enhanced gastric emptying of liquid in awake mice, Eur. J. Pharmacol., 2012, vol. 693, no. 1, pp. 57–63.

    Article  CAS  PubMed  Google Scholar 

  15. Xiao, A., Wang, H., Lu, X., Zhu, J., Huang, D., Xu, T., Guo, J., Liu, C., and Li, J., H2S, a novel gasotransmitter, involves in gastric accommodation, Sci. Rep., 2015, vol.5.

  16. DeLeon, E.R., Stoy, G.F., and Olson, K.R., Passive loss of hydrogen sulfide in biological experiments, Anal. Biochem., 2012, vol. 421, no. 1, pp. 203–207.

    Article  CAS  PubMed  Google Scholar 

  17. Sitdikova, G.F., Fuchs, R., Kainz, V., Weiger, T.M., and Hermann, A., Phosphorylation of BK channels modulates the sensitivity to hydrogen sulfide (H2S), Front. Physiol., 2014, vol. 5, p.431.

    Article  PubMed  PubMed Central  Google Scholar 

  18. Furne, J., Saeed, A., and Levitt, M.D., Whole tissue hydrogen sulfide concentrations are orders of magnitude lower than presently accepted values, Am. J. Physiol. Reg. Integr. Comp. Physiol., 2008, vol. 295, no. 5, pp. R1479–R1485.

    Article  CAS  Google Scholar 

  19. Zhao, P., Huang, X., Wang, Z.Y., Qiu, Z.X., Han, Y.F., Lu, H.L., Kim, Y.C., and Xu, W.X., Dual effect of exogenous hydrogen sulfide on the spontaneous contraction of gastric smooth muscle in guinea-pig, Eur. J. Pharmacol., 2009, vol. 616, no. 1, pp. 223–228.

    Article  CAS  PubMed  Google Scholar 

  20. Han, Y.F., Huang, X., Guo, X., Wu, Y.S., Liu, D.H., Lu, H.L., Kim, Y.C., and Xu, W.X., Evidence that endogenous hydrogen sulfide exerts an excitatory effect on gastric motility in mice, Eur. J. Pharmacol., 2011, vol. 673, no. 1, pp. 85–95.

    Article  CAS  PubMed  Google Scholar 

  21. Sitdikova, G.F., Weiger, T.M., and Hermann, A., Hydrogen sulfide increases calcium-activated potassium (BK) channel activity of rat pituitary tumor cells, Pflügers Arch. Eur. J. Physiol., 2010, vol. 459, no. 3, pp. 389–397.

    Article  CAS  Google Scholar 

  22. Mustafina, A.N., Yakovlev, A.V., Gaifullina, A.S., Weiger, T.M., Hermann, A., and Sitdikova, G.F., Hydrogen sulfide induces hyperpolarization and decreases the exocytosis of secretory granules of rat GH3 pituitary tumor cells, Biochem. Biophys. Res. Commun., 2015, vol. 465, no. 4, pp. 825–831.

    Article  CAS  PubMed  Google Scholar 

  23. Dhaese, I. and Lefebvre, R.A., Myosin light chain phosphatase activation is involved in the hydrogen sulfide-induced relaxation in mouse gastric fundus, Eur. J. Pharmacol., 2009, vol. 606, no. 1, pp. 180–186.

    Article  CAS  PubMed  Google Scholar 

  24. Nalli, A.D., Rajagopal, S., Mahavadi, S., Grider, J.R., and Murthy, K.S., Inhibition of RhoA-dependent pathway and contraction by endogenous hydrogen sulfide in rabbit gastric smooth muscle cells, Am. J. Physiol. Cell Physiol., 2015, vol. 308, no. 6, pp. 485–495.

    Article  CAS  Google Scholar 

  25. Vogalis, F., Potassium channels in gastrointestinal smooth muscle, J. Auton. Pharmacol., 2000, vol. 20, no. 4, pp. 207–219.

    Article  CAS  PubMed  Google Scholar 

  26. Lee, J.Y., Ko, E.J., Ahn, K.D., Kim, S., and Rhee, P.L., The role of K+ conductances in regulating membrane excitability in human gastric corpus smooth muscle, Am. J. Physiol. Gastrointest. Liver Physiol., 2015, vol. 308, no. 7, pp. G625–G633.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  27. Zhao, W., Zhang, J., Lu, Y., and Wang, R., The vasorelaxant effect of H2S as a novel endogenous gaseous KATP channel opener, EMBO J., 2001, vol. 20, no. 21, pp. 6008–6016.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  28. Blair, P.J., Rhee, P.L., Sanders, K.M., and Ward, S.M., The significance of interstitial cells in neurogastroenterology, J. Neurogastroenterol. Motil., 2014, vol. 20, no. 3, pp. 294–317.

    Article  PubMed  PubMed Central  Google Scholar 

  29. Parajuli, S.P., Choi, S., Lee, J., Kim, Y.D., Park, C.G., Kim, M.Y., Kim, H.I., Yeum, C.H., and Jun, J.Y., The inhibitory effects of hydrogen sulfide on pacemaker activity of interstitial cells of ?ajal from mouse small intestine, Korean J. Physiol. Pharmacol., 2010, vol. 14, no. 2, pp. 83–89.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  30. Mustafa, A.K., Sikka, G., Gazi, S.K., Steppan, J., Jung, S.M., Bhunia, A.K., and Amzel, L.M., Hydrogen sulfide as endothelium-derived hyperpolarizing factor sulfhydrates potassium channels novelty and significance, Circ. Res., 2011, vol. 109, no. 11, pp. 1259–1268.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  31. Dorman, D.C., Moulin, F.J.M., McManus, B.E., Mahle, K.C., James, R.A., and Struve, M.F., Cytochrome oxidase inhibition induced by acute hydrogen sulfide inhalation: correlation with tissue sulfide concentrations in the rat brain, liver, lung, and nasal epithelium, Toxicol. Sci., 2002, vol. 65, no. 1, pp. 18–25.

    Article  CAS  PubMed  Google Scholar 

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Authors and Affiliations

  1. Kazan Federal University, Kazan, Russia

    I. F. Shaidullov, M. U. Shafigullin, L. M. Gabitova, F. G. Sitdikov & G. F. Sitdikova

  2. Kazan State Medical University, Kazan, Russia

    A. L. Zefirov

Authors
  1. I. F. Shaidullov
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  2. M. U. Shafigullin
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  3. L. M. Gabitova
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  4. F. G. Sitdikov
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  5. A. L. Zefirov
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  6. G. F. Sitdikova
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Corresponding author

Correspondence to G. F. Sitdikova.

Additional information

Original Russian Text © I.F. Shaidullov, M.U. Shafigullin, L.M. Gabitova, F.G. Sitdikov, A.L. Zefirov, G.F. Sitdikova, 2018, published in Zhurnal Evolyutsionnoi Biokhimii i Fiziologii, 2018, Vol. 54, No. 5, pp. 355–361.

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Shaidullov, I.F., Shafigullin, M.U., Gabitova, L.M. et al. Role of Potassium Channels in the Effects of Hydrogen Sulfide on Contractility of Gastric Smooth Muscle Cells in Rats. J Evol Biochem Phys 54, 400–407 (2018). https://doi.org/10.1134/S0022093018050083

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  • DOI: https://doi.org/10.1134/S0022093018050083

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