Skip to main content
The Journal of Physiology logoLink to The Journal of Physiology
. 1995 Apr 15;484(Pt 2):287–306. doi: 10.1113/jphysiol.1995.sp020665

Efficacy of peak Ca2+ currents (ICa) as trigger of sarcoplasmic reticulum Ca2+ release in myocytes from the guinea-pig coronary artery.

Ganitkevich VYa 1, G Isenberg 1
PMCID: PMC1157894  PMID: 7541467

Abstract

1. Increments in cytosolic Ca2+ concentration (delta[Ca2+]c) were measured in single smooth muscle cells from guinea-pig coronary artery together with the density of peak Ca2+ currents (ICa) in response to clamp steps from -50 to 0 mV. The comparison of depolarization- with caffeine-induced delta[Ca2+]c was used to define the efficacy by which ICa can trigger Ca2+ release from the sarcoplasmic reticulum (SR). 2. At 2.5 mM extracellular calcium concentration ([Ca2+]o), depolarization induced a rapid rise of delta[Ca2+]c followed by a slow creep. Peak [Ca2+]c occurred within ca 30 s and could be followed by an undershoot and a second rise in [Ca2+]c. The creep was blocked by ryanodine but was insensitive to block of InsP3 receptors with heparin. The creep was not observed in Cs(+)-filled cells. After disappearance of the creep, a tonic delta[Ca2+]c became unmasked. 3. At 2.5 mM [Ca2+]o, peak ICa was -0.80 +/- 0.17 microA cm-2. delta[Ca2+] peaked at the end of the 6 s pulse at 202 +/- 98 nM while caffeine-induced delta[Ca2+]c peaked at 1330 +/- 410 nM. The ratio of depolarization- to caffeine-induced delta[Ca2+]c was 10 +/- 6%. 4. In media containing 10 mM [Ca2+]o plus 1 microM Bay K 8644, peak ICa was -2.6 +/- 1.1 microA cm-2 and delta[Ca2+]c peaked within 2.5 s at 451 +/- 194 nM. Paired measurements yielded the ratio of depolarization- to caffeine induced delta[Ca2+]c as 30 +/- 10%. Depolarization-induced delta[Ca2+]c was nearly blocked by caffeine and reduced by ryanodine to 30%, suggesting the contribution of Ca2+ release from caffeine- and ryanodine-sensitive Ca2+ stores. 5. Trypsin (1 mg ml-1) in the electrode solution (10 mM [Ca2+]o plus 1 microM Bay K 8644) increased peak ICa up to 12.5 microA cm-2. ICa induced a delta[Ca2+]c of 990 +/- 210 nM and was accompanied by a 'hump' of IK,Ca. When applied briefly after peak delta[Ca2+]c, caffeine increased [Ca2+]c only moderately. The results suggest that a peak ICa can trigger a synchronized whole-cell Ca2+ release only if ICa is strongly augmented. 6. Amplitude and rate of rise of delta[Ca2+]c were graded by test step potentials along a bell-shaped voltage-dependent curve, similar to that of L-type ICa. Steps to +80 mV induced no delta[Ca2+]c when the electrode solution contained 10 mM Na+. However, with 150 mM intrapipette Na+, pulses to +80 mV induced delta[Ca2+]c.(ABSTRACT TRUNCATED AT 400 WORDS)

Full text

PDF
287

Selected References

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

  1. Aaronson P. I., Bolton T. B., Lang R. J., MacKenzie I. Calcium currents in single isolated smooth muscle cells from the rabbit ear artery in normal-calcium and high-barium solutions. J Physiol. 1988 Nov;405:57–75. doi: 10.1113/jphysiol.1988.sp017321. [DOI] [PMC free article] [PubMed] [Google Scholar]
  2. Allbritton N. L., Meyer T. Localized calcium spikes and propagating calcium waves. Cell Calcium. 1993 Nov;14(10):691–697. doi: 10.1016/0143-4160(93)90095-n. [DOI] [PubMed] [Google Scholar]
  3. Baró I., O'Neill S. C., Eisner D. A. Changes of intracellular [Ca2+] during refilling of sarcoplasmic reticulum in rat ventricular and vascular smooth muscle. J Physiol. 1993 Jun;465:21–41. doi: 10.1113/jphysiol.1993.sp019664. [DOI] [PMC free article] [PubMed] [Google Scholar]
  4. Benham C. D., Bolton T. B. Spontaneous transient outward currents in single visceral and vascular smooth muscle cells of the rabbit. J Physiol. 1986 Dec;381:385–406. doi: 10.1113/jphysiol.1986.sp016333. [DOI] [PMC free article] [PubMed] [Google Scholar]
  5. Berridge M. J. Inositol trisphosphate and calcium signalling. Nature. 1993 Jan 28;361(6410):315–325. doi: 10.1038/361315a0. [DOI] [PubMed] [Google Scholar]
  6. Bolton T. B., Lim S. P. Properties of calcium stores and transient outward currents in single smooth muscle cells of rabbit intestine. J Physiol. 1989 Feb;409:385–401. doi: 10.1113/jphysiol.1989.sp017504. [DOI] [PMC free article] [PubMed] [Google Scholar]
  7. Bond M., Kitazawa T., Somlyo A. P., Somlyo A. V. Release and recycling of calcium by the sarcoplasmic reticulum in guinea-pig portal vein smooth muscle. J Physiol. 1984 Oct;355:677–695. doi: 10.1113/jphysiol.1984.sp015445. [DOI] [PMC free article] [PubMed] [Google Scholar]
  8. Bond M., Shuman H., Somlyo A. P., Somlyo A. V. Total cytoplasmic calcium in relaxed and maximally contracted rabbit portal vein smooth muscle. J Physiol. 1984 Dec;357:185–201. doi: 10.1113/jphysiol.1984.sp015496. [DOI] [PMC free article] [PubMed] [Google Scholar]
  9. Cheng H., Lederer W. J., Cannell M. B. Calcium sparks: elementary events underlying excitation-contraction coupling in heart muscle. Science. 1993 Oct 29;262(5134):740–744. doi: 10.1126/science.8235594. [DOI] [PubMed] [Google Scholar]
  10. Devine C. E., Somlyo A. V., Somlyo A. P. Sarcoplasmic reticulum and excitation-contraction coupling in mammalian smooth muscles. J Cell Biol. 1972 Mar;52(3):690–718. doi: 10.1083/jcb.52.3.690. [DOI] [PMC free article] [PubMed] [Google Scholar]
  11. Ganitkevich VYa, Isenberg G. Ca2+ entry through Na(+)-Ca2+ exchange can trigger Ca2+ release from Ca2+ stores in Na(+)-loaded guinea-pig coronary myocytes. J Physiol. 1993 Aug;468:225–243. doi: 10.1113/jphysiol.1993.sp019768. [DOI] [PMC free article] [PubMed] [Google Scholar]
  12. Ganitkevich VYa, Isenberg G. Caffeine-induced release and reuptake of Ca2+ by Ca2+ stores in myocytes from guinea-pig urinary bladder. J Physiol. 1992 Dec;458:99–117. doi: 10.1113/jphysiol.1992.sp019408. [DOI] [PMC free article] [PubMed] [Google Scholar]
  13. Ganitkevich VYa, Isenberg G. Contribution of two types of calcium channels to membrane conductance of single myocytes from guinea-pig coronary artery. J Physiol. 1990 Jul;426:19–42. doi: 10.1113/jphysiol.1990.sp018125. [DOI] [PMC free article] [PubMed] [Google Scholar]
  14. Ganitkevich V. Y., Isenberg G. Contribution of Ca(2+)-induced Ca2+ release to the [Ca2+]i transients in myocytes from guinea-pig urinary bladder. J Physiol. 1992 Dec;458:119–137. doi: 10.1113/jphysiol.1992.sp019409. [DOI] [PMC free article] [PubMed] [Google Scholar]
  15. Grégoire G., Loirand G., Pacaud P. Ca2+ and Sr2+ entry induced Ca2+ release from the intracellular Ca2+ store in smooth muscle cells of rat portal vein. J Physiol. 1993 Dec;472:483–500. doi: 10.1113/jphysiol.1993.sp019957. [DOI] [PMC free article] [PubMed] [Google Scholar]
  16. Han S., Schiefer A., Isenberg G. Ca2+ load of guinea-pig ventricular myocytes determines efficacy of brief Ca2+ currents as trigger for Ca2+ release. J Physiol. 1994 Nov 1;480(Pt 3):411–421. doi: 10.1113/jphysiol.1994.sp020371. [DOI] [PMC free article] [PubMed] [Google Scholar]
  17. Herrmann-Frank A., Darling E., Meissner G. Functional characterization of the Ca(2+)-gated Ca2+ release channel of vascular smooth muscle sarcoplasmic reticulum. Pflugers Arch. 1991 May;418(4):353–359. doi: 10.1007/BF00550873. [DOI] [PubMed] [Google Scholar]
  18. Iino M. Calcium release mechanisms in smooth muscle. Jpn J Pharmacol. 1990 Dec;54(4):345–354. doi: 10.1254/jjp.54.345. [DOI] [PubMed] [Google Scholar]
  19. Isenberg G., Han S. Gradation of Ca(2+)-induced Ca2+ release by voltage-clamp pulse duration in potentiated guinea-pig ventricular myocytes. J Physiol. 1994 Nov 1;480(Pt 3):423–438. doi: 10.1113/jphysiol.1994.sp020372. [DOI] [PMC free article] [PubMed] [Google Scholar]
  20. Kargacin G., Fay F. S. Ca2+ movement in smooth muscle cells studied with one- and two-dimensional diffusion models. Biophys J. 1991 Nov;60(5):1088–1100. doi: 10.1016/S0006-3495(91)82145-2. [DOI] [PMC free article] [PubMed] [Google Scholar]
  21. Kobayashi S., Somlyo A. V., Somlyo A. P. Heparin inhibits the inositol 1,4,5-trisphosphate-dependent, but not the independent, calcium release induced by guanine nucleotide in vascular smooth muscle. Biochem Biophys Res Commun. 1988 Jun 16;153(2):625–631. doi: 10.1016/s0006-291x(88)81141-0. [DOI] [PubMed] [Google Scholar]
  22. Komori S., Bolton T. B. Inositol trisphosphate releases stored calcium to block voltage-dependent calcium channels in single smooth muscle cells. Pflugers Arch. 1991 Jun;418(5):437–441. doi: 10.1007/BF00497770. [DOI] [PubMed] [Google Scholar]
  23. Langton P. D., Standen N. B. Calcium currents elicited by voltage steps and steady voltages in myocytes isolated from the rat basilar artery. J Physiol. 1993 Sep;469:535–548. doi: 10.1113/jphysiol.1993.sp019828. [DOI] [PMC free article] [PubMed] [Google Scholar]
  24. McCarron J. G., Walsh J. V., Jr, Fay F. S. Sodium/calcium exchange regulates cytoplasmic calcium in smooth muscle. Pflugers Arch. 1994 Feb;426(3-4):199–205. doi: 10.1007/BF00374772. [DOI] [PubMed] [Google Scholar]
  25. Neher E., Augustine G. J. Calcium gradients and buffers in bovine chromaffin cells. J Physiol. 1992 May;450:273–301. doi: 10.1113/jphysiol.1992.sp019127. [DOI] [PMC free article] [PubMed] [Google Scholar]
  26. Nowycky M. C., Pinter M. J. Time courses of calcium and calcium-bound buffers following calcium influx in a model cell. Biophys J. 1993 Jan;64(1):77–91. doi: 10.1016/S0006-3495(93)81342-0. [DOI] [PMC free article] [PubMed] [Google Scholar]
  27. Obejero-Paz C. A., Jones S. W., Scarpa A. Calcium currents in the A7r5 smooth muscle-derived cell line. Increase in current and selective removal of voltage-dependent inactivation by intracellular trypsin. J Gen Physiol. 1991 Dec;98(6):1127–1140. doi: 10.1085/jgp.98.6.1127. [DOI] [PMC free article] [PubMed] [Google Scholar]
  28. Rooney T. A., Thomas A. P. Intracellular calcium waves generated by Ins(1,4,5)P3-dependent mechanisms. Cell Calcium. 1993 Nov;14(10):674–690. doi: 10.1016/0143-4160(93)90094-m. [DOI] [PubMed] [Google Scholar]
  29. Smirnov S. V., Aaronson P. I. Ca2+ currents in single myocytes from human mesenteric arteries: evidence for a physiological role of L-type channels. J Physiol. 1992 Nov;457:455–475. doi: 10.1113/jphysiol.1992.sp019387. [DOI] [PMC free article] [PubMed] [Google Scholar]
  30. Trafford A. W., O'Neill S. C., Eisner D. A. Factors affecting the propagation of locally activated systolic Ca transients in rat ventricular myocytes. Pflugers Arch. 1993 Oct;425(1-2):181–183. doi: 10.1007/BF00374521. [DOI] [PubMed] [Google Scholar]
  31. Zholos A. V., Baidan L. V., Shuba M. F. Properties of the late transient outward current in isolated intestinal smooth muscle cells of the guinea-pig. J Physiol. 1991 Nov;443:555–574. doi: 10.1113/jphysiol.1991.sp018851. [DOI] [PMC free article] [PubMed] [Google Scholar]
  32. Zholos A. V., Baidan L. V., Shuba M. F. Some properties of Ca(2+)-induced Ca2+ release mechanism in single visceral smooth muscle cell of the guinea-pig. J Physiol. 1992 Nov;457:1–25. doi: 10.1113/jphysiol.1992.sp019362. [DOI] [PMC free article] [PubMed] [Google Scholar]
  33. Zholos A. V., Baidan L. V., Shuba M. F. The inhibitory action of caffeine on calcium currents in isolated intestinal smooth muscle cells. Pflugers Arch. 1991 Oct;419(3-4):267–273. doi: 10.1007/BF00371106. [DOI] [PubMed] [Google Scholar]
  34. Zhou Z., Neher E. Mobile and immobile calcium buffers in bovine adrenal chromaffin cells. J Physiol. 1993 Sep;469:245–273. doi: 10.1113/jphysiol.1993.sp019813. [DOI] [PMC free article] [PubMed] [Google Scholar]
  35. van Breemen C., Saida K. Cellular mechanisms regulating [Ca2+]i smooth muscle. Annu Rev Physiol. 1989;51:315–329. doi: 10.1146/annurev.ph.51.030189.001531. [DOI] [PubMed] [Google Scholar]

Articles from The Journal of Physiology are provided here courtesy of The Physiological Society

RESOURCES