Skip to main content
SpringerLink
Log in

CGRP-induced activation of KATP channels in follicular Xenopus oocytes

  • Published:
Pflügers Archiv Aims and scope Submit manuscript

Abstract

The two-microelectrode voltage-clamp technique was used to monitor K+ channel activity in Xenopus oocyte follicular cells, which are electrically coupled to the oocyte itself by gap junctions. Endogenous vasodilators such as calcitonin gene-related peptide (CGRP), vasoactive intestinal peptide (VIP), prostaglandin E2 (PGE2) and adenosine activate glibenclamide-ATP-sensitive K+ (KATP) channels in Xenopus oocyte follicular cells. The mechanism of action of CGRP was studied in detail. CGRP effects undergo a rapid desensitization. CGRP acts via CGRPI receptors. Its effects are antagonized by the amino-truncated CGRP analog hCGRP(8–37). The second messenger for CGRP activation of KATP channels is cAMP. Phosphodiesterase inhibition by 3-isobutyl-1-methylxanthine enhances the CGRP response while adenyl cyclase inhibition by either 2′,5′-dideoxyadenosine or progesterone nearly completely depresses the CGRP response. Vasoconstrictors such as ACh and angiotensin II also have receptors in follicular cells. ACh strongly inhibits the CGRP activation of K+ channels as it inhibits the activation of KATP channels by P1060, but angiotensin II does not. It is concluded that as in vascular smooth muscle cells, CGRP and probably other hyperpolarizing vasodilators open KATP channels in follicular cells by protein kinase A activation.

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

Access this article

Log in via an institution

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

Instant access to the full article PDF.

Institutional subscriptions

Similar content being viewed by others

References

  1. Amara SG, Jonas V, Rosenfeld MG, Ong ES, Evans R (1982) Alternative RNA processing in calcitonin gene expression generates mRNAs encoding different polypeptide products. Nature 298:240–244

    Google Scholar 

  2. Beech DJ, Zhang H, Nakao K, Bolton TB (1993) Single channel and whole-cell K-currents evoked by levcromakalim in smooth muscle cells from the rabbit portal vein. Br J Pharmacol 110:583–590

    Google Scholar 

  3. Bhogal R, Smith DM, Purkiss P, Bloom SR (1993) Molecular identification of binding sites for calcitonin gene-related peptide (CGRP) and islet amyloid polypeptide (IAP) in mammalian lung: species variation and binding of truncated CGRP and IAPP. J Endocrinol 133:2351–2361

    Google Scholar 

  4. Bonev AD, Nelson MT (1993) Muscarinic inhibition of ATP-sensitive K+ channels by protein kinase C in urinary bladder smooth muscle. Am J Physiol C1723–C1728

  5. Brain SD, Williams TJ, Tippins JR, Morris HR, MacIntyre I (1985) Calcitonin gene-related peptide is a potent vasodilator. Nature 313:54–56

    Google Scholar 

  6. Brayden JE, Nelson MT (1992) Regulation of arterial tone by activation of calcium-dependent potassium channels. Science 256:532–535

    Google Scholar 

  7. Cavero I, Mondot S, Mestre M (1989) Vasorelaxant effects of cromakalim in rats are mediated by glibenclamide-sensitive potassium channels. J Pharmacol Exp Ther 248:1261–1268

    Google Scholar 

  8. Cook DL, Hales CN (1984) Intracellular ATP directly blocks K+ channels in pancreatic β cells. Nature 311:271–273

    Google Scholar 

  9. Dascal N (1987) The use of Xenopus oocytes for the study of ion channels. CRC Crit Rev Biochem 22:318–387

    Google Scholar 

  10. Donoso MV, Fournier A, Saint-Pierre S, Huidobro-Toro JP (1990) Pharmacological characterization of CGRP1 receptor subtype in the vascular system of the rat: studies with hCGRP fragments and analogs. Peptides 11:885–889

    Google Scholar 

  11. Dunne MJ, Petersen OH (1991) Potassium selective ion channels in insulin-secreting cells: physiology, pharmacology and their role in stimulus-secretion coupling. Biochim Biophys Acta 1071:67–82

    Google Scholar 

  12. Edvinsson L, Ekman R, Jansen I, McCulloch J, Uddman R (1987) Calcitonin gene-related peptide and cerebral blood vessels: distribution and vasomotor effects. J Cereb Blood Flow Metab 7:720–728

    Google Scholar 

  13. Guillemare E, Honoré E, De Weille JR, Fosset M, Lazdunski M, Meisheri K (1994) Evidence for a functional receptor in Xenopus oocyte for U-37883A, a novel KATP channel blocker: comparison with rat insulinoma cells. Mol Pharmacol (in press)

  14. Honoré E, Lazdunski M (1991) Hormone-regulated K+ channels in follicle-enclosed oocytes are activated by vasorelaxing K+ channel openers and blocked by antidiabetic sulfonylureas. Proc Natl Acad Sci USA 88:5438–5442

    Google Scholar 

  15. Honoré E, Lazdunski M (1991) Two different types of channels are targets for potassium channel openers in Xenopus oocyte. FEBS Lett 287:75–79

    Google Scholar 

  16. Honoré E, Lazdunski M (1993) Single channel properties and regulation of pinacidil/glibenclamide-sensitive K+ channels in follicular cells from Xenopus oocyte. Pflügers Arch 424:113–121

    Google Scholar 

  17. Johnson RA, Yeung SMH, Stübner D, Bushfield M, Shoshani I (1989) Cation and structural requirements for P site-mediated inhibition of adenylate cyclase. Mol Pharmacol 35:681–688

    Google Scholar 

  18. Kajioka S, Kitamura K, Kuriyama H (1991) Guanosine-diphosphate activates an adenosine 5′-triphosphate-sensitive K+ channel in the rabbit portal vein. J Physiol (Lond) 444:397–418

    Google Scholar 

  19. Kitazono T, Heistad DD, Faraci FM (1993) Role of ATP-sensitive K+ channels in CGRP-induced dilatation of basilar artery in vivo. Am J Physiol 265:H581-H585

    Google Scholar 

  20. Miledi R, Woodward RM (1989) Effects of defolliculation on membrane current responses of Xenopus oocytes. J Physiol (Lond) 416:601–621

    Google Scholar 

  21. Miledi R, Woodward RM (1989) Membrane currents elicited by prostaglandins, atrial natriuretic factor and oxytocin in follicle-enclosed Xenopus oocytes. J Physiol (Lond) 416:623–643

    Google Scholar 

  22. Miller CE, Moczydlowski E, Latorre M, Phillips M (1985) Charybdotoxin, a protein inhibitor of a single Ca2+-activated K+ channel from mammalian skeletal muscle. Nature 313:316–318

    Google Scholar 

  23. Morrill GA, Schatz F, Kostellow AB, Poupko JM (1977) Changes in cyclic AMP levels in the amphibian ovarian follicle following progesterone induction of meiotic maturation. Differentiation 8:97–104

    Google Scholar 

  24. Nelson MT, Huang Y, Brayden JE, Hescheler J, Standen NB (1990) Arterial dilations in response to calcitonin gene-related peptide involve activation of K+ channels. Nature 344:770–773

    Google Scholar 

  25. Nelson MT, Patlak JB, Worley JF, Standen NB (1990) Calcium channels, potassium channels, and voltage dependence of arterial smooth muscle tone. Am J Physiol 259:C3-C18

    Google Scholar 

  26. Okabe K, Kajioka S, Nakao K, Kitamura K, Kuriyama H, Weston AH (1990) Actions of cromakalim on ionic currents recorded from single smooth muscle cells of the rat portal vein. J Pharmacol Exp Ther 252:832–839

    Google Scholar 

  27. Okimura Y, Chihara K, Abe H, Kita T, Kashio Y Sato M, Fujita T (1987) Calcitonin gene-relation peptide-like immunoreactivity in the central nervous system and peripheral organs of rats. Regul Pept 17:327–337

    Google Scholar 

  28. Parent L, Coronado R (1989) Reconstitution of the ATP-sensitive potassium channel of skeletal muscle. J Gen Physiol 94:445–463

    Google Scholar 

  29. Quast U (1993) Do the K+ channel openers relax smooth muscle by opening K+ channels ? Trends Pharmacol Sci 14:332–337

    Google Scholar 

  30. Quast U, Cook NS (1989) Moving together, K+ channels openers and ATP-sensitive K+ channels. Trends Pharmacol Sci 10:431–435

    Google Scholar 

  31. Quayle, JM, Bonev, AD, Brayden, JE, Nelson, MT (1994) Calcitonin gene-related peptide activated ATP-sensitive K+ currents in rabbit arterial smooth muscle via protein kinase A. J Physiol (Lond) 475:9–13

    Google Scholar 

  32. Schmid-Antomarchi H, De Weille JR, Fosset M, Lazdunski M (1987) The receptor for antidiabetic sulfonylureas controls the activity of the ATP-modulated K+ channel in insulin-secreting cells. J Biol Chem 262:15840–15844

    Google Scholar 

  33. Standen NB, Quayle JM, Davies NW, Brayden JE, Huang Y, Nelson MT (1989) Hyperpolarizing vasodilatators activate ATP-sensitive K+ channels in arterial smooth muscle. Science 245:177–180

    Google Scholar 

  34. Stevenson JC, MacDonald DWR, Warren RC, Booker MW, Whitehead MI (1986) Increased concentration of circulating calcitonin gene related peptide during normal human pregnancy. Br Med J 293:1329–1333

    Google Scholar 

  35. Terzic, A., Tung, RT, Inanobe, A, Katada, T, Kurachi, Y (1994) G proteins activate ATP-sensitive K+ channels by antagonizing ATP-dependent gating. Neuron 12:885–893

    Google Scholar 

  36. Wibrand F, Honoré E, Lazdunski M (1992) Opening of glibenclamide-sensitive K+ channel in follicular cells promotes Xenopus oocyte maturation. Proc Natl Acad Sci USA 89:5133–5137

    Google Scholar 

Download references

Author information

Authors and Affiliations

  1. Institut de Pharmacologie Moléculaire et Cellulaire, 660 route des Lucioles, Sophia Antipolis, F-06560, Valbonne, France

    Eric Guillemare, Michel Lazdunski & Eric Honoré

Authors
  1. Eric Guillemare
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Michel Lazdunski
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Eric Honoré
    View author publications

    You can also search for this author in PubMed Google Scholar

Additional information

Thanks are due to C. Roulinat and F. Aguila for expert technical assistance. This work was supported by the Centre National de la Recherche Scientifique (CNRS).

Rights and permissions

Reprints and permissions

About this article

Cite this article

Guillemare, E., Lazdunski, M. & Honoré, E. CGRP-induced activation of KATP channels in follicular Xenopus oocytes. Pflugers Arch. 428, 604–609 (1994). https://doi.org/10.1007/BF00374584

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Issue Date:

  • DOI: https://doi.org/10.1007/BF00374584

Key words

Search

Navigation