Skip to main content
PMC home page
Biophysical Journal logoLink to Biophysical Journal
. 2001 Sep;81(3):1398–1405. doi: 10.1016/S0006-3495(01)75795-5

Stimulus-dependent control of inositol 1,4,5-trisphosphate-induced Ca(2+) oscillation frequency by the endoplasmic reticulum Ca(2+)-ATPase.

A Visegrády 1, Z Lakos 1, L Czimbalek 1, B Somogyi 1
PMCID: PMC1301619  PMID: 11509354

Abstract

In many cell types, receptor stimulation evokes cytosolic calcium oscillations with a frequency that depends on agonist dose. Previous studies demonstrated controversial effects of changing the activity of the endoplasmic reticulum Ca(2+)-ATPase upon the frequency of oscillations. By numerical simulations, we found that the model of De Young and Keizer (J. Keizer and G.W. De Young, 1994, J. Theor. Biol. 166: 431-442), unlike other models, can explain the observed discrepancies, assuming that the different experiments were performed at different stimulus levels. According to model predictions, partial inhibition of internal calcium pumps is expected to increase frequency at low stimulus strength and should have an opposite effect at strong stimuli. Similar results were obtained using an analytical estimation of oscillation period, based on calcium-dependent channel activation and inactivation. In experiments on HeLa cells, 4 nM thapsigargin increased the frequency of calcium oscillations induced by 1 and 2.5 microM histamine but had no effect on supramaximally stimulated cells. In HEp-2 cells, 2 nM thapsigargin slowed down the rapid, ATP-induced oscillations. Our results suggest that in the investigated cell types, the De Young-Keizer model based on inositol 1,4,5-trisphosphate-dependent calcium-induced calcium release can properly describe intracellular calcium oscillations.

Full Text

The Full Text of this article is available as a PDF (256.2 KB).

Selected References

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

  1. Atri A., Amundson J., Clapham D., Sneyd J. A single-pool model for intracellular calcium oscillations and waves in the Xenopus laevis oocyte. Biophys J. 1993 Oct;65(4):1727–1739. doi: 10.1016/S0006-3495(93)81191-3. [DOI] [PMC free article] [PubMed] [Google Scholar]
  2. Barrero M. J., Montero M., Alvarez J. Dynamics of [Ca2+] in the endoplasmic reticulum and cytoplasm of intact HeLa cells. A comparative study. J Biol Chem. 1997 Oct 31;272(44):27694–27699. doi: 10.1074/jbc.272.44.27694. [DOI] [PubMed] [Google Scholar]
  3. Berridge M. J. Inositol trisphosphate and calcium signalling. Nature. 1993 Jan 28;361(6410):315–325. doi: 10.1038/361315a0. [DOI] [PubMed] [Google Scholar]
  4. Bootman M. D., Cheek T. R., Moreton R. B., Bennett D. L., Berridge M. J. Smoothly graded Ca2+ release from inositol 1,4,5-trisphosphate-sensitive Ca2+ stores. J Biol Chem. 1994 Oct 7;269(40):24783–24791. [PubMed] [Google Scholar]
  5. Bootman M. D., Young K. W., Young J. M., Moreton R. B., Berridge M. J. Extracellular calcium concentration controls the frequency of intracellular calcium spiking independently of inositol 1,4,5-trisphosphate production in HeLa cells. Biochem J. 1996 Feb 15;314(Pt 1):347–354. doi: 10.1042/bj3140347. [DOI] [PMC free article] [PubMed] [Google Scholar]
  6. Camacho P., Lechleiter J. D. Calreticulin inhibits repetitive intracellular Ca2+ waves. Cell. 1995 Sep 8;82(5):765–771. doi: 10.1016/0092-8674(95)90473-5. [DOI] [PubMed] [Google Scholar]
  7. Camacho P., Lechleiter J. D. Increased frequency of calcium waves in Xenopus laevis oocytes that express a calcium-ATPase. Science. 1993 Apr 9;260(5105):226–229. doi: 10.1126/science.8385800. [DOI] [PubMed] [Google Scholar]
  8. Clapham D. E. Calcium signaling. Cell. 1995 Jan 27;80(2):259–268. doi: 10.1016/0092-8674(95)90408-5. [DOI] [PubMed] [Google Scholar]
  9. De Koninck P., Schulman H. Sensitivity of CaM kinase II to the frequency of Ca2+ oscillations. Science. 1998 Jan 9;279(5348):227–230. doi: 10.1126/science.279.5348.227. [DOI] [PubMed] [Google Scholar]
  10. De Young G. W., Keizer J. A single-pool inositol 1,4,5-trisphosphate-receptor-based model for agonist-stimulated oscillations in Ca2+ concentration. Proc Natl Acad Sci U S A. 1992 Oct 15;89(20):9895–9899. doi: 10.1073/pnas.89.20.9895. [DOI] [PMC free article] [PubMed] [Google Scholar]
  11. Finch E. A., Turner T. J., Goldin S. M. Calcium as a coagonist of inositol 1,4,5-trisphosphate-induced calcium release. Science. 1991 Apr 19;252(5004):443–446. doi: 10.1126/science.2017683. [DOI] [PubMed] [Google Scholar]
  12. Girard S., Clapham D. Acceleration of intracellular calcium waves in Xenopus oocytes by calcium influx. Science. 1993 Apr 9;260(5105):229–232. doi: 10.1126/science.8385801. [DOI] [PubMed] [Google Scholar]
  13. Goldbeter A., Dupont G., Berridge M. J. Minimal model for signal-induced Ca2+ oscillations and for their frequency encoding through protein phosphorylation. Proc Natl Acad Sci U S A. 1990 Feb;87(4):1461–1465. doi: 10.1073/pnas.87.4.1461. [DOI] [PMC free article] [PubMed] [Google Scholar]
  14. Hajnóczky G., Robb-Gaspers L. D., Seitz M. B., Thomas A. P. Decoding of cytosolic calcium oscillations in the mitochondria. Cell. 1995 Aug 11;82(3):415–424. doi: 10.1016/0092-8674(95)90430-1. [DOI] [PubMed] [Google Scholar]
  15. Hajnóczky G., Thomas A. P. Minimal requirements for calcium oscillations driven by the IP3 receptor. EMBO J. 1997 Jun 16;16(12):3533–3543. doi: 10.1093/emboj/16.12.3533. [DOI] [PMC free article] [PubMed] [Google Scholar]
  16. Harkins A. B., Kurebayashi N., Baylor S. M. Resting myoplasmic free calcium in frog skeletal muscle fibers estimated with fluo-3. Biophys J. 1993 Aug;65(2):865–881. doi: 10.1016/S0006-3495(93)81112-3. [DOI] [PMC free article] [PubMed] [Google Scholar]
  17. Harootunian A. T., Kao J. P., Paranjape S., Tsien R. Y. Generation of calcium oscillations in fibroblasts by positive feedback between calcium and IP3. Science. 1991 Jan 4;251(4989):75–78. doi: 10.1126/science.1986413. [DOI] [PubMed] [Google Scholar]
  18. Ilyin V., Parker I. Role of cytosolic Ca2+ in inhibition of InsP3-evoked Ca2+ release in Xenopus oocytes. J Physiol. 1994 Jun 15;477(Pt 3):503–509. doi: 10.1113/jphysiol.1994.sp020211. [DOI] [PMC free article] [PubMed] [Google Scholar]
  19. Jafri M. S., Keizer J. On the roles of Ca2+ diffusion, Ca2+ buffers, and the endoplasmic reticulum in IP3-induced Ca2+ waves. Biophys J. 1995 Nov;69(5):2139–2153. doi: 10.1016/S0006-3495(95)80088-3. [DOI] [PMC free article] [PubMed] [Google Scholar]
  20. Lechleiter J. D., Clapham D. E. Molecular mechanisms of intracellular calcium excitability in X. laevis oocytes. Cell. 1992 Apr 17;69(2):283–294. doi: 10.1016/0092-8674(92)90409-6. [DOI] [PubMed] [Google Scholar]
  21. Lechleiter J. D., John L. M., Camacho P. Ca2+ wave dispersion and spiral wave entrainment in Xenopus laevis oocytes overexpressing Ca2+ ATPases. Biophys Chem. 1998 May 5;72(1-2):123–129. doi: 10.1016/s0301-4622(98)00128-8. [DOI] [PubMed] [Google Scholar]
  22. Lytton J., Westlin M., Burk S. E., Shull G. E., MacLennan D. H. Functional comparisons between isoforms of the sarcoplasmic or endoplasmic reticulum family of calcium pumps. J Biol Chem. 1992 Jul 15;267(20):14483–14489. [PubMed] [Google Scholar]
  23. Lytton J., Westlin M., Hanley M. R. Thapsigargin inhibits the sarcoplasmic or endoplasmic reticulum Ca-ATPase family of calcium pumps. J Biol Chem. 1991 Sep 15;266(26):17067–17071. [PubMed] [Google Scholar]
  24. Marchant J. S., Parker I. Role of elementary Ca(2+) puffs in generating repetitive Ca(2+) oscillations. EMBO J. 2001 Jan 15;20(1-2):65–76. doi: 10.1093/emboj/20.1.65. [DOI] [PMC free article] [PubMed] [Google Scholar]
  25. Marchant J. S., Taylor C. W. Cooperative activation of IP3 receptors by sequential binding of IP3 and Ca2+ safeguards against spontaneous activity. Curr Biol. 1997 Jul 1;7(7):510–518. doi: 10.1016/s0960-9822(06)00222-3. [DOI] [PubMed] [Google Scholar]
  26. Martin S. C., Shuttleworth T. J. Ca2+ influx drives agonist-activated [Ca2+]i oscillations in an exocrine cell. FEBS Lett. 1994 Sep 19;352(1):32–36. doi: 10.1016/0014-5793(94)00913-9. [DOI] [PubMed] [Google Scholar]
  27. Meyer T., Stryer L. Calcium spiking. Annu Rev Biophys Biophys Chem. 1991;20:153–174. doi: 10.1146/annurev.bb.20.060191.001101. [DOI] [PubMed] [Google Scholar]
  28. Missiaen L., De Smedt H., Pary J. B., Oike M., Casteels R. Kinetics of empty store-activated Ca2+ influx in HeLa cells. J Biol Chem. 1994 Feb 25;269(8):5817–5823. [PubMed] [Google Scholar]
  29. Miyakawa T., Mizushima A., Hirose K., Yamazawa T., Bezprozvanny I., Kurosaki T., Iino M. Ca(2+)-sensor region of IP(3) receptor controls intracellular Ca(2+) signaling. EMBO J. 2001 Apr 2;20(7):1674–1680. doi: 10.1093/emboj/20.7.1674. [DOI] [PMC free article] [PubMed] [Google Scholar]
  30. Morgan A. J., Jacob R. Differential modulation of the phases of a Ca2+ spike by the store Ca2+-ATPase in human umbilical vein endothelial cells. J Physiol. 1998 Nov 15;513(Pt 1):83–101. doi: 10.1111/j.1469-7793.1998.083by.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  31. Petersen C. C., Dupont G. The initiation of a calcium signal in Xenopus oocytes. Cell Calcium. 1994 Nov;16(5):391–403. doi: 10.1016/0143-4160(94)90032-9. [DOI] [PubMed] [Google Scholar]
  32. Petersen C. C., Petersen O. H., Berridge M. J. The role of endoplasmic reticulum calcium pumps during cytosolic calcium spiking in pancreatic acinar cells. J Biol Chem. 1993 Oct 25;268(30):22262–22264. [PubMed] [Google Scholar]
  33. Rossi F. M., Kao J. P. Nmoc-DBHQ, a new caged molecule for modulating sarcoplasmic/endoplasmic reticulum Ca2+ ATPase activity with light flashes. J Biol Chem. 1997 Feb 7;272(6):3266–3271. doi: 10.1074/jbc.272.6.3266. [DOI] [PubMed] [Google Scholar]
  34. Sauvé R., Diarra A., Chahine M., Simoneau C., Morier N., Roy G. Ca2+ oscillations induced by histamine H1 receptor stimulation in HeLa cells: Fura-2 and patch clamp analysis. Cell Calcium. 1991 Feb-Mar;12(2-3):165–176. doi: 10.1016/0143-4160(91)90018-a. [DOI] [PubMed] [Google Scholar]
  35. Thomas A. P., Bird G. S., Hajnóczky G., Robb-Gaspers L. D., Putney J. W., Jr Spatial and temporal aspects of cellular calcium signaling. FASEB J. 1996 Nov;10(13):1505–1517. [PubMed] [Google Scholar]
  36. Uneyama C., Uneyama H., Akaike N., Takahashi M. Cyclic GMP inhibits cytoplasmic Ca2+ oscillation by increasing Ca2+-ATPase activity in rat megakaryocytes. Eur J Pharmacol. 1998 Apr 24;347(2-3):355–361. doi: 10.1016/s0014-2999(98)00123-x. [DOI] [PubMed] [Google Scholar]
  37. Visegrády A., Grama L., Somogyi B., Lustyik G. Characterization of intracellular calcium oscillations induced by extracellular nucleotides in HEp-2 cells. J Photochem Photobiol B. 2000 Nov;58(2-3):80–86. doi: 10.1016/s1011-1344(00)00107-x. [DOI] [PubMed] [Google Scholar]
  38. Wakui M., Osipchuk Y. V., Petersen O. H. Receptor-activated cytoplasmic Ca2+ spiking mediated by inositol trisphosphate is due to Ca2(+)-induced Ca2+ release. Cell. 1990 Nov 30;63(5):1025–1032. doi: 10.1016/0092-8674(90)90505-9. [DOI] [PubMed] [Google Scholar]
  39. Wakui M., Potter B. V., Petersen O. H. Pulsatile intracellular calcium release does not depend on fluctuations in inositol trisphosphate concentration. Nature. 1989 May 25;339(6222):317–320. doi: 10.1038/339317a0. [DOI] [PubMed] [Google Scholar]
  40. Zhu D. M., Tekle E., Huang C. Y., Chock P. B. Inositol tetrakisphosphate as a frequency regulator in calcium oscillations in HeLa cells. J Biol Chem. 2000 Mar 3;275(9):6063–6066. doi: 10.1074/jbc.275.9.6063. [DOI] [PubMed] [Google Scholar]

Articles from Biophysical Journal are provided here courtesy of The Biophysical Society

RESOURCES