Skip to main content
NCBI home page
British Journal of Pharmacology logoLink to British Journal of Pharmacology
. 1993 Mar;108(3):638–645. doi: 10.1111/j.1476-5381.1993.tb12854.x

Effects of ATP on cultured smooth muscle cells from rat aorta.

P Y von der Weid 1, V N Serebryakov 1, F Orallo 1, C Bergmann 1, V A Snetkov 1, K Takeda 1
PMCID: PMC1908034  PMID: 8385531

Abstract

1. Membrane ionic currents provoked by externally applied ATP were studied by patch-clamp techniques in cultured aortic smooth muscle cells of the rat. 2. Using standard bath and pipette solutions and whole-cell voltage-clamp, ATP evoked an inward current when the cell membrane potential was held at -50 mV and an outward current when the potential was held at 30 mV, with a reversal potential near -10 mV. 3. Application of ATP gamma S gave results similar to those obtained with ATP, while adenosine, AMP and alpha,beta-methylene ATP were ineffective. The ATP-activated current was inhibited by suramin, 100 microM. 4. ATP also induced a biphasic rise in internal free Ca levels as shown directly by Fura-2 measurements and by the increase in Ca-dependent K single-channel activity in cell-attached patches. 5. With outward current through K channels blocked by internal Cs and TEA, modification of the ionic composition of bath and pipette solutions revealed that the reversal potential for the ATP-induced whole-cell current closely followed ECl, the chloride equilibrium potential, and was insensitive to manipulations of the monovalent cation gradient. 6. These results indicate that in rat cultured aortic smooth muscle cells, ATP binding to P2-purinoceptors produces increases of internal free Ca levels and subsequent activation of both Ca-dependent K and Cl currents.

Full text

PDF
638

Selected References

These references are in PubMed. This may not be the complete list of references from this article.

  1. Amédée T., Benham C. D., Bolton T. B., Byrne N. G., Large W. A. Potassium, chloride and non-selective cation conductances opened by noradrenaline in rabbit ear artery cells. J Physiol. 1990 Apr;423:551–568. doi: 10.1113/jphysiol.1990.sp018039. [DOI] [PMC free article] [PubMed] [Google Scholar]
  2. Andre P., Schott C., Nehlig H., Stoclet J. C. Aortic smooth muscle cells are able to convert angiotensin I to angiotensin II. Biochem Biophys Res Commun. 1990 Dec 31;173(3):1137–1142. doi: 10.1016/s0006-291x(05)80904-0. [DOI] [PubMed] [Google Scholar]
  3. Bean B. P., Friel D. D. ATP-activated channels in excitable cells. Ion Channels. 1990;2:169–203. doi: 10.1007/978-1-4615-7305-0_5. [DOI] [PubMed] [Google Scholar]
  4. Benham C. D. ATP-activated channels gate calcium entry in single smooth muscle cells dissociated from rabbit ear artery. J Physiol. 1989 Dec;419:689–701. doi: 10.1113/jphysiol.1989.sp017893. [DOI] [PMC free article] [PubMed] [Google Scholar]
  5. Benham C. D., Bolton T. B., Byrne N. G., Large W. A. Action of externally applied adenosine triphosphate on single smooth muscle cells dispersed from rabbit ear artery. J Physiol. 1987 Jun;387:473–488. doi: 10.1113/jphysiol.1987.sp016585. [DOI] [PMC free article] [PubMed] [Google Scholar]
  6. Benham C. D., Tsien R. W. A novel receptor-operated Ca2+-permeable channel activated by ATP in smooth muscle. Nature. 1987 Jul 16;328(6127):275–278. doi: 10.1038/328275a0. [DOI] [PubMed] [Google Scholar]
  7. Bodin P., Richard S., Travo C., Berta P., Stoclet J. C., Papin S., Travo P. Responses of subcultured rat aortic smooth muscle myocytes to vasoactive agents and KCl-induced depolarization. Am J Physiol. 1991 Jan;260(1 Pt 1):C151–C158. doi: 10.1152/ajpcell.1991.260.1.C151. [DOI] [PubMed] [Google Scholar]
  8. Bodin P., Stoclet J. C., Travo P. Differences in myocyte subpopulations from segments of the thoracic aorta and their modifications with age and hypertension in the rat. Cell Tissue Res. 1987 Jan;247(1):227–231. doi: 10.1007/BF00216565. [DOI] [PubMed] [Google Scholar]
  9. Bregestovski P. D., Bolotina V. M., Serebryakov V. N. Fatty acid modifies Ca2+-dependent potassium channel activity in smooth muscle cells from the human aorta. Proc R Soc Lond B Biol Sci. 1989 Aug 22;237(1288):259–266. doi: 10.1098/rspb.1989.0048. [DOI] [PubMed] [Google Scholar]
  10. Bregestovski P. D., Printseva OYu, Serebryakov V., Stinnakre J., Turmin A., Zamoyski V. Comparison of Ca2+-dependent K+ channels in the membrane of smooth muscle cells isolated from adult and foetal human aorta. Pflugers Arch. 1988 Nov;413(1):8–13. doi: 10.1007/BF00581222. [DOI] [PubMed] [Google Scholar]
  11. Burnstock G., Kennedy C. A dual function for adenosine 5'-triphosphate in the regulation of vascular tone. Excitatory cotransmitter with noradrenaline from perivascular nerves and locally released inhibitory intravascular agent. Circ Res. 1986 Mar;58(3):319–330. doi: 10.1161/01.res.58.3.319. [DOI] [PubMed] [Google Scholar]
  12. Burnstock G., Kennedy C. Is there a basis for distinguishing two types of P2-purinoceptor? Gen Pharmacol. 1985;16(5):433–440. doi: 10.1016/0306-3623(85)90001-1. [DOI] [PubMed] [Google Scholar]
  13. Byrne N. G., Large W. A. Action of noradrenaline on single smooth muscle cells freshly dispersed from the rat anococcygeus muscle. J Physiol. 1987 Aug;389:513–525. doi: 10.1113/jphysiol.1987.sp016669. [DOI] [PMC free article] [PubMed] [Google Scholar]
  14. Byrne N. G., Large W. A. Membrane ionic mechanisms activated by noradrenaline in cells isolated from the rabbit portal vein. J Physiol. 1988 Oct;404:557–573. doi: 10.1113/jphysiol.1988.sp017306. [DOI] [PMC free article] [PubMed] [Google Scholar]
  15. Droogmans G., Callewaert G., Declerck I., Casteels R. ATP-induced Ca2+ release and Cl- current in cultured smooth muscle cells from pig aorta. J Physiol. 1991;440:623–634. doi: 10.1113/jphysiol.1991.sp018728. [DOI] [PMC free article] [PubMed] [Google Scholar]
  16. Droogmans G., Declerck I., Casteels R. Effect of adrenergic agonists on Ca2+-channel currents in single vascular smooth muscle cells. Pflugers Arch. 1987 Jun;409(1-2):7–12. doi: 10.1007/BF00584744. [DOI] [PubMed] [Google Scholar]
  17. Dunn P. M., Blakeley A. G. Suramin: a reversible P2-purinoceptor antagonist in the mouse vas deferens. Br J Pharmacol. 1988 Feb;93(2):243–245. doi: 10.1111/j.1476-5381.1988.tb11427.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  18. Friel D. D. An ATP-sensitive conductance in single smooth muscle cells from the rat vas deferens. J Physiol. 1988 Jul;401:361–380. doi: 10.1113/jphysiol.1988.sp017167. [DOI] [PMC free article] [PubMed] [Google Scholar]
  19. Fujii K. Evidence for adenosine triphosphate as an excitatory transmitter in guinea-pig, rabbit and pig urinary bladder. J Physiol. 1988 Oct;404:39–52. doi: 10.1113/jphysiol.1988.sp017277. [DOI] [PMC free article] [PubMed] [Google Scholar]
  20. Grynkiewicz G., Poenie M., Tsien R. Y. A new generation of Ca2+ indicators with greatly improved fluorescence properties. J Biol Chem. 1985 Mar 25;260(6):3440–3450. [PubMed] [Google Scholar]
  21. Hallam T. J., Jacob R., Merritt J. E. Evidence that agonists stimulate bivalent-cation influx into human endothelial cells. Biochem J. 1988 Oct 1;255(1):179–184. doi: 10.1042/bj2550179. [DOI] [PMC free article] [PubMed] [Google Scholar]
  22. Hamill O. P., Marty A., Neher E., Sakmann B., Sigworth F. J. Improved patch-clamp techniques for high-resolution current recording from cells and cell-free membrane patches. Pflugers Arch. 1981 Aug;391(2):85–100. doi: 10.1007/BF00656997. [DOI] [PubMed] [Google Scholar]
  23. Hume R. I., Honig M. G. Excitatory action of ATP on embryonic chick muscle. J Neurosci. 1986 Mar;6(3):681–690. doi: 10.1523/JNEUROSCI.06-03-00681.1986. [DOI] [PMC free article] [PubMed] [Google Scholar]
  24. Karashima T., Takata Y. The effects of ATP related compounds on the electrical activity of the rat portal vein. Gen Pharmacol. 1979;10(6):477–487. doi: 10.1016/0306-3623(79)90013-2. [DOI] [PubMed] [Google Scholar]
  25. Klöckner U., Isenberg G. Endothelin depolarizes myocytes from porcine coronary and human mesenteric arteries through a Ca-activated chloride current. Pflugers Arch. 1991 Mar;418(1-2):168–175. doi: 10.1007/BF00370467. [DOI] [PubMed] [Google Scholar]
  26. Krishtal O. A., Marchenko S. M., Pidoplichko V. I. Receptor for ATP in the membrane of mammalian sensory neurones. Neurosci Lett. 1983 Jan 31;35(1):41–45. doi: 10.1016/0304-3940(83)90524-4. [DOI] [PubMed] [Google Scholar]
  27. Kubo Y. Properties of ionic currents induced by external ATP in a mouse mesodermal stem cell line. J Physiol. 1991 Oct;442:691–710. doi: 10.1113/jphysiol.1991.sp018815. [DOI] [PMC free article] [PubMed] [Google Scholar]
  28. Martin S. C. ATP activates a Ca(2+)-dependent Cl- current in the rat thyroid cell line, FRTL-5. J Membr Biol. 1992 Feb;125(3):243–253. doi: 10.1007/BF00236437. [DOI] [PubMed] [Google Scholar]
  29. Matsuura H., Ehara T. Activation of chloride current by purinergic stimulation in guinea pig heart cells. Circ Res. 1992 Apr;70(4):851–855. doi: 10.1161/01.res.70.4.851. [DOI] [PubMed] [Google Scholar]
  30. Nakazawa K., Fujimori K., Takanaka A., Inoue K. An ATP-activated conductance in pheochromocytoma cells and its suppression by extracellular calcium. J Physiol. 1990 Sep;428:257–272. doi: 10.1113/jphysiol.1990.sp018211. [DOI] [PMC free article] [PubMed] [Google Scholar]
  31. Nakazawa K., Fujimori K., Takanaka A., Inoue K. Reversible and selective antagonism by suramin of ATP-activated inward current in PC12 phaeochromocytoma cells. Br J Pharmacol. 1990 Sep;101(1):224–226. doi: 10.1111/j.1476-5381.1990.tb12117.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  32. Nakazawa K., Matsuki N. Adenosine triphosphate-activated inward current in isolated smooth muscle cells from rat vas deferens. Pflugers Arch. 1987 Aug;409(6):644–646. doi: 10.1007/BF00584668. [DOI] [PubMed] [Google Scholar]
  33. Pacaud P., Loirand G., Baron A., Mironneau C., Mironneau J. Ca2+ channel activation and membrane depolarization mediated by Cl- channels in response to noradrenaline in vascular myocytes. Br J Pharmacol. 1991 Dec;104(4):1000–1006. doi: 10.1111/j.1476-5381.1991.tb12540.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  34. Pacaud P., Loirand G., Mironneau C., Mironneau J. Noradrenaline activates a calcium-activated chloride conductance and increases the voltage-dependent calcium current in cultured single cells of rat portal vein. Br J Pharmacol. 1989 May;97(1):139–146. doi: 10.1111/j.1476-5381.1989.tb11934.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  35. Phaneuf S., Berta P., Casanova J., Cavadore J. C. ATP stimulates inositol phosphates accumulation and calcium mobilization in a primary culture of rat aortic myocytes. Biochem Biophys Res Commun. 1987 Mar 13;143(2):454–460. doi: 10.1016/0006-291x(87)91375-1. [DOI] [PubMed] [Google Scholar]
  36. Sasaki T., Gallacher D. V. Extracellular ATP activates receptor-operated cation channels in mouse lacrimal acinar cells to promote calcium influx in the absence of phosphoinositide metabolism. FEBS Lett. 1990 May 7;264(1):130–134. doi: 10.1016/0014-5793(90)80782-e. [DOI] [PubMed] [Google Scholar]
  37. Schneider P., Hopp H. H., Isenberg G. Ca2+ influx through ATP-gated channels increments [Ca2+]i and inactivates ICa in myocytes from guinea-pig urinary bladder. J Physiol. 1991;440:479–496. doi: 10.1113/jphysiol.1991.sp018720. [DOI] [PMC free article] [PubMed] [Google Scholar]
  38. Serebryakov V., Takeda K. Voltage-dependent calcium current and the effects of adrenergic modulation in rat aortic smooth muscle cells. Philos Trans R Soc Lond B Biol Sci. 1992 Jul 29;337(1279):37–47. doi: 10.1098/rstb.1992.0081. [DOI] [PubMed] [Google Scholar]
  39. Suzuki H. Electrical responses of smooth muscle cells of the rabbit ear artery to adenosine triphosphate. J Physiol. 1985 Feb;359:401–415. doi: 10.1113/jphysiol.1985.sp015592. [DOI] [PMC free article] [PubMed] [Google Scholar]
  40. Tawada Y., Furukawa K., Shigekawa M. ATP-induced calcium transient in cultured rat aortic smooth muscle cells. J Biochem. 1987 Dec;102(6):1499–1509. doi: 10.1093/oxfordjournals.jbchem.a122197. [DOI] [PubMed] [Google Scholar]
  41. Van Helden D. F. An alpha-adrenoceptor-mediated chloride conductance in mesenteric veins of the guinea-pig. J Physiol. 1988 Jul;401:489–501. doi: 10.1113/jphysiol.1988.sp017174. [DOI] [PMC free article] [PubMed] [Google Scholar]
  42. Vincent P. Cationic channels sensitive to extracellular ATP in rat lacrimal cells. J Physiol. 1992 Apr;449:313–331. doi: 10.1113/jphysiol.1992.sp019088. [DOI] [PMC free article] [PubMed] [Google Scholar]
  43. Xiong Z. L., Kitamura K., Kuriyama H. ATP activates cationic currents and modulates the calcium current through GTP-binding protein in rabbit portal vein. J Physiol. 1991;440:143–165. doi: 10.1113/jphysiol.1991.sp018701. [DOI] [PMC free article] [PubMed] [Google Scholar]

Articles from British Journal of Pharmacology are provided here courtesy of The British Pharmacological Society

RESOURCES