Skip to main content
Log in

Effects of polyamines on voltage-activated calcium channels in guinea-pig intestinal smooth muscle

  • Original Article
  • Neurophysiology, Muscle and Sensory Organs
  • Published:
Pflügers Archiv Aims and scope Submit manuscript

Abstract

Effects of polyamines on the spontaneous mechanical and electrical activity of guinea-pig intestinal smooth muscle were studied. Spermine and spermidine inhibited action potential generation and contractions, while putrescine had no effect. Single smooth muscle cells were isolated from the longitudinal muscle layer of the guinea-pig ileum. Whole-cell voltage-clamp experiments were carried out to investigate the effects of polyamines on current through voltage-activated Ca2+ channels. Spermine and spermidine (0.1–1 mM) reduced the inward current in a concentration-dependent manner. Spermine blocked current activated by the dihydropyridine agonist BAY K 8644 (1 μM), whereas no additional inhibition by spermine was seen after blockage of dihydropyridine-sensitive channels by nifedipine (0.1 μM). Inhibition by spermine or spermidine did not shift the peak of the current voltage relation of the inward current. Steady-state activation and inactivation relationships were not affected and thus the amplitude, but not the voltage dependence, of the window current responsible for Ca2+ inflow during sustained depolarization was affected. Putrescine (1 mM) had no significant effect on the inward current. These results suggest that spermine and spermidine inhibit contraction in spontaneously active intestinal smooth muscle by inhibiting Ca2+ current responsible for generation of action potentials.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Similar content being viewed by others

References

  1. De Meis L (1967) Relaxing effect of spermine and spermidine on intact and glycerol treated muscle. Am J Physiol 212:92–96

    PubMed  Google Scholar 

  2. Droogmans G, Callewaert G (1986) Ca2+-channel current and its modification by the dihydropyridine agonist BAY K 8644 in isolated smooth muscle cells. Pflügers Arch 406:259–265

    Google Scholar 

  3. Drouin H, Hermann A (1994) Intracellular action of spermine on neuronal Ca2+ and K+ currents. Eur J Neurosci 6:412–419

    PubMed  Google Scholar 

  4. Picker E, Taglialatela M, Wible BA, Henley CM, Brown AM (1994) Spermine and spermidine as gating molecules for inward rectifier K+ channels. Science 266:1068–1072

    PubMed  Google Scholar 

  5. Hamill OP, Marty A, Neher E, Sakmann B, Sigworth FJ (1981) Improved patch-clamp techniques for high-resolution current recording from cells and cell-free membrane patches. Pflügers Arch 391:85–100

    Google Scholar 

  6. Hashimoto H, Unemoto T, Hayashi M (1973) Inhibitory action of spermine on the contractions of the rat uterus. Am J Physiol 225:743–746

    PubMed  Google Scholar 

  7. Hellstrand P, Lydrup M-L (1988) Spontaneous electrical and contractile activity correlated to 86Rb+ efflux in smooth muscle of the guinea-pig mesotubarium. J Physiol (Lond) 407:587–597

    Google Scholar 

  8. Herman MD, Reuveny E, Narahashi T (1993) The effect of polyamines on voltage-activated Ca2+ channels in mouse neuroblastoma cells. J Physiol (Lond) 462:645–660

    Google Scholar 

  9. Hille B (1992) Ionic channels of excitable membranes, 2nd edn. Sinauer, Sunderland. Mass., pp 457–462

    Google Scholar 

  10. Imaizumi Y, Muraki K, Takeda M, Watanabe M (1989) Measurement and stimulation of noninactivating Ca current in smooth muscle cells. Am J Physiol 256:C880-C885

    PubMed  Google Scholar 

  11. Inoue Y, Xiong Z, Kitamura K, Kuriyama H (1989) Modulation produced by nifedipine of the unitary Ba current of dispersed smooth muscle cells of the rabbit ileum. Pflügers Arch 414:534–542

    Google Scholar 

  12. Langton PD, Burke EP, Sanders KM (1989) Participation of Ca currents in colonic electrical activity. Am J Physiol 257:C451-C460

    PubMed  Google Scholar 

  13. Lopatin AN, Makhina EN, Nichols CG (1994) Potassium channel block by cytoplasmic polyamines as the mechanism of intrinsic rectification. Nature 372:366–369

    Article  PubMed  Google Scholar 

  14. Maruta K, Mizoguchi Y, Osa T (1985) Effects of polyamines on the mechanical and electrical activities of the isolated circular muscle of rat uterus. Jpn J Physiol 36:903–915

    Google Scholar 

  15. Nilsson B-O, Hellstrand P (1993) Effects of polyamines on intracellular calcium and mechanical activity in smooth muscle of guinea-pig taenia coli. Acta Physiol Scand 148:37–43

    PubMed  Google Scholar 

  16. Pegg AE (1986) Recent advances in the biochemistry of the polyamines in eukaryotes. Biochem J 234:249–262

    PubMed  Google Scholar 

  17. Pullan LM, Keith RA, LaMonte D, Stumpo RJ Salama AI (1990) The polyamine spermine affects ω-conotoxin binding and function at N-type voltage-sensitive calcium channels. J Auton Pharmacol 10:213–219

    PubMed  Google Scholar 

  18. Schoemaker H (1992) Polyamines allosterically modulate [3H]nitrendipine binding to the voltage-sensitive calcium in rat brain. Eur J Pharmacol 225:167–169

    Article  PubMed  Google Scholar 

  19. Schuber F (1989) Influence of polyamines on membrane functions. Biochem J 260:1–10

    PubMed  Google Scholar 

  20. Scott RH, Sutton KG, Dolphin AC (1993) Interactions of polyamines with neuronal ion channels. Trends Neuroci 16:153–160

    Article  Google Scholar 

  21. Seiler N, Dezeure F (1990) Polyamine transport in mammalian cells. Int J Biochem 22:211–218

    Article  PubMed  Google Scholar 

  22. Sjöholm Å, Arkhammar P, Welsh N, Bokvist K, Rorsman P, Hallberg A, Nilsson T, Welsh M, Berggren P-O (1993) Enhanced stimulus-secretion coupling in polyamine-depleted rat insulinoma cells. J Clin Invest 92:1910–1917

    PubMed  Google Scholar 

  23. Sutton KG, Dolphin AC, Scott RH (1993) Inhibition of the voltage-activated Ca2+ currents from cultured neurons by spermine, argiotoxin-636 and a synthetic arginine polyamine. Mol Neuropharmacol 3:37–43

    Google Scholar 

  24. Swärd K, Nillsson B-O, Hellstrand P (1994) Polyamines increase Ca2+ sensitivity in permeabilized smooth muscle of guinea pig ileum. Am J Physiol 266:C1754-C1763

    PubMed  Google Scholar 

  25. Swärd K, Pato MD, Nilsson B-O, Nordström I, Hellstrand P (1995) Polyamines selectively inhibit a myosin phosphatase and increase myosin LC20 phosphorylation and contraction in smooth muscle. Am J Physiol (in press)

  26. Tabor CW, Tabor H (1984) Polyamines. Annu Rev Biochem 53:749–790

    Article  PubMed  Google Scholar 

  27. Vivaudou MB, Singer JJ, Walsh JV Jr (1991) Multiple types of Ca2+ channels in visceral smooth muscle cells. Pflügers Arch 418:144–152

    Google Scholar 

  28. Yamamoto Y, Hu SL, Kao CY (1989) Inward current in single smooth muscle cells of the guinea-pig taenia coli. J Gen Physiol 93:521–550

    Article  PubMed  Google Scholar 

  29. Yoshino M, Someya T, Nishio A, Yazawa K, Usuki T, Yabu H (1989) Multiple types of voltage-dependent Ca channels in mammalian intestinal smooth muscle cells. Pflügers Arch 414:401–409

    Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Rights and permissions

Reprints and permissions

About this article

Cite this article

Gomez, M., Hellstrand, P. Effects of polyamines on voltage-activated calcium channels in guinea-pig intestinal smooth muscle. Pflugers Arch. 430, 501–507 (1995). https://doi.org/10.1007/BF00373886

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Issue Date:

  • DOI: https://doi.org/10.1007/BF00373886

Key words

Navigation