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. 1995 Dec;69(6):2378–2391. doi: 10.1016/S0006-3495(95)80107-4

Highly cooperative Ca2+ elevations in response to Ins(1,4,5)P3 microperfusion through a patch-clamp pipette.

J Schrenzel 1, N Demaurex 1, M Foti 1, C Van Delden 1, J Jacquet 1, G Mayr 1, D P Lew 1, K H Krause 1
PMCID: PMC1236475  PMID: 8599644

Abstract

To study the initial kinetics of Ins(1,4,5)P3-induced [Ca2+]i elevations with a high time resolution and to avoid the problem of cell-to-cell heterogeneity, we have used the combined patch-clamp/microfluorimetry technique. The mathematical description of the microperfusion of Ins(1,4,5)P3 and the subsequent Ca2+ release consists of a monoexponential decay (cytosolic Ins(1,4,5)P3 concentration) and a Hill equation (Ins(1,4,5)P3 dose-response curve). Two additional Hill equations and an integration were necessary to include a putative dependence of Ins(1,4,5)P3-induced Ca2+ release on [Ca2+]i. Best-fitting analysis assuming [Ca2+]i-independent Ca2+ release yielded Hill coefficients between 4 and 12. The high cooperativity was also observed with the poorly metabolizable analog Ins(2,4,5)P3 and was independent of extracellular [Ca2+]. Best-fitting analysis including a positive [Ca2+]i feedback suggested a cooperativity on the level of Ins(1,4,5)P3-induced channel opening (n = 2) and an enhancement of Ins(1,4,5)P3-induced Ca2+ release by [Ca2+]i. In summary, the onset kinetics of Ins(1,4,5)P3-induced [Ca2+]i elevations in single HL-60 granulocytes showed a very high cooperativity, presumably because of a cooperativity on the level of channel opening and a positive Ca2+ feedback, but not because of Ca2+ influx or Ins(1,4,5)P3 metabolism. This high cooperativity, acting in concert with negative feedback mechanisms, might play an important role in the fine-tuning of the cellular Ca2+ signal.

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Selected References

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

  1. Allbritton N. L., Meyer T., Stryer L. Range of messenger action of calcium ion and inositol 1,4,5-trisphosphate. Science. 1992 Dec 11;258(5089):1812–1815. doi: 10.1126/science.1465619. [DOI] [PubMed] [Google Scholar]
  2. Almers W., Neher E. The Ca signal from fura-2 loaded mast cells depends strongly on the method of dye-loading. FEBS Lett. 1985 Nov 11;192(1):13–18. doi: 10.1016/0014-5793(85)80033-8. [DOI] [PubMed] [Google Scholar]
  3. Barlow R., Blake J. F. Hill coefficients and the logistic equation. Trends Pharmacol Sci. 1989 Nov;10(11):440–441. doi: 10.1016/S0165-6147(89)80006-9. [DOI] [PubMed] [Google Scholar]
  4. Berridge M. J. Inositol trisphosphate and calcium signalling. Nature. 1993 Jan 28;361(6410):315–325. doi: 10.1038/361315a0. [DOI] [PubMed] [Google Scholar]
  5. Bezprozvanny I., Watras J., Ehrlich B. E. Bell-shaped calcium-response curves of Ins(1,4,5)P3- and calcium-gated channels from endoplasmic reticulum of cerebellum. Nature. 1991 Jun 27;351(6329):751–754. doi: 10.1038/351751a0. [DOI] [PubMed] [Google Scholar]
  6. Biden T. J., Wollheim C. B. Ca2+ regulates the inositol tris/tetrakisphosphate pathway in intact and broken preparations of insulin-secreting RINm5F cells. J Biol Chem. 1986 Sep 15;261(26):11931–11934. [PubMed] [Google Scholar]
  7. Bootman M. D., Berridge M. J., Taylor C. W. All-or-nothing Ca2+ mobilization from the intracellular stores of single histamine-stimulated HeLa cells. J Physiol. 1992 May;450:163–178. doi: 10.1113/jphysiol.1992.sp019121. [DOI] [PMC free article] [PubMed] [Google Scholar]
  8. Chadwick C. C., Saito A., Fleischer S. Isolation and characterization of the inositol trisphosphate receptor from smooth muscle. Proc Natl Acad Sci U S A. 1990 Mar;87(6):2132–2136. doi: 10.1073/pnas.87.6.2132. [DOI] [PMC free article] [PubMed] [Google Scholar]
  9. Champeil P., Combettes L., Berthon B., Doucet E., Orlowski S., Claret M. Fast kinetics of calcium release induced by myo-inositol trisphosphate in permeabilized rat hepatocytes. J Biol Chem. 1989 Oct 25;264(30):17665–17673. [PubMed] [Google Scholar]
  10. Combettes L., Hannaert-Merah Z., Coquil J. F., Rousseau C., Claret M., Swillens S., Champeil P. Rapid filtration studies of the effect of cytosolic Ca2+ on inositol 1,4,5-trisphosphate-induced 45Ca2+ release from cerebellar microsomes. J Biol Chem. 1994 Jul 1;269(26):17561–17571. [PubMed] [Google Scholar]
  11. Connolly T. M., Bross T. E., Majerus P. W. Isolation of a phosphomonoesterase from human platelets that specifically hydrolyzes the 5-phosphate of inositol 1,4,5-trisphosphate. J Biol Chem. 1985 Jul 5;260(13):7868–7874. [PubMed] [Google Scholar]
  12. Demaurex N., Schlegel W., Varnai P., Mayr G., Lew D. P., Krause K. H. Regulation of Ca2+ influx in myeloid cells. Role of plasma membrane potential, inositol phosphates, cytosolic free [Ca2+], and filling state of intracellular Ca2+ stores. J Clin Invest. 1992 Sep;90(3):830–839. doi: 10.1172/JCI115958. [DOI] [PMC free article] [PubMed] [Google Scholar]
  13. Favre C. J., Lew D. P., Krause K. H. Rapid heparin-sensitive Ca2+ release following Ca(2+)-ATPase inhibition in intact HL-60 granulocytes. Evidence for Ins(1,4,5)P3-dependent Ca2+ cycling across the membrane of Ca2+ stores. Biochem J. 1994 Aug 15;302(Pt 1):155–162. doi: 10.1042/bj3020155. [DOI] [PMC free article] [PubMed] [Google Scholar]
  14. 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]
  15. 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]
  16. Henne V., Mayr G. W., Grabowski B., Koppitz B., Söling H. D. Semisynthetic derivatives of inositol 1,4,5-trisphosphate substituted at the 1-phosphate group. Effects on calcium release from permeabilized guinea-pig parotid acinar cells and comparison with binding to aldolase A. Eur J Biochem. 1988 May 16;174(1):95–101. doi: 10.1111/j.1432-1033.1988.tb14067.x. [DOI] [PubMed] [Google Scholar]
  17. Iino M. Biphasic Ca2+ dependence of inositol 1,4,5-trisphosphate-induced Ca release in smooth muscle cells of the guinea pig taenia caeci. J Gen Physiol. 1990 Jun;95(6):1103–1122. doi: 10.1085/jgp.95.6.1103. [DOI] [PMC free article] [PubMed] [Google Scholar]
  18. Iino M., Endo M. Calcium-dependent immediate feedback control of inositol 1,4,5-triphosphate-induced Ca2+ release. Nature. 1992 Nov 5;360(6399):76–78. doi: 10.1038/360076a0. [DOI] [PubMed] [Google Scholar]
  19. Iino M., Tsukioka M. Feedback control of inositol trisphosphate signalling bycalcium. Mol Cell Endocrinol. 1994 Jan;98(2):141–146. doi: 10.1016/0303-7207(94)90132-5. [DOI] [PubMed] [Google Scholar]
  20. Joseph S. K., Rice H. L., Williamson J. R. The effect of external calcium and pH on inositol trisphosphate-mediated calcium release from cerebellum microsomal fractions. Biochem J. 1989 Feb 15;258(1):261–265. doi: 10.1042/bj2580261. [DOI] [PMC free article] [PubMed] [Google Scholar]
  21. Levitan I., Payne R., Potter B. V., Hillman P. Facilitation of the responses to injections of inositol 1,4,5-trisphosphate analogs in Limulus ventral photoreceptors. Biophys J. 1994 Sep;67(3):1161–1172. doi: 10.1016/S0006-3495(94)80584-3. [DOI] [PMC free article] [PubMed] [Google Scholar]
  22. MONOD J., WYMAN J., CHANGEUX J. P. ON THE NATURE OF ALLOSTERIC TRANSITIONS: A PLAUSIBLE MODEL. J Mol Biol. 1965 May;12:88–118. doi: 10.1016/s0022-2836(65)80285-6. [DOI] [PubMed] [Google Scholar]
  23. Marshall I. C., Taylor C. W. Biphasic effects of cytosolic Ca2+ on Ins(1,4,5)P3-stimulated Ca2+ mobilization in hepatocytes. J Biol Chem. 1993 Jun 25;268(18):13214–13220. [PubMed] [Google Scholar]
  24. Mathias R. T., Cohen I. S., Oliva C. Limitations of the whole cell patch clamp technique in the control of intracellular concentrations. Biophys J. 1990 Sep;58(3):759–770. doi: 10.1016/S0006-3495(90)82418-8. [DOI] [PMC free article] [PubMed] [Google Scholar]
  25. Mauger J. P., Lièvremont J. P., Piétri-Rouxel F., Hilly M., Coquil J. F. The inositol 1,4,5-trisphosphate receptor: kinetic properties and regulation. Mol Cell Endocrinol. 1994 Jan;98(2):133–139. doi: 10.1016/0303-7207(94)90131-7. [DOI] [PubMed] [Google Scholar]
  26. Meyer T., Holowka D., Stryer L. Highly cooperative opening of calcium channels by inositol 1,4,5-trisphosphate. Science. 1988 Apr 29;240(4852):653–656. doi: 10.1126/science.2452482. [DOI] [PubMed] [Google Scholar]
  27. Meyer T., Stryer L. Transient calcium release induced by successive increments of inositol 1,4,5-trisphosphate. Proc Natl Acad Sci U S A. 1990 May;87(10):3841–3845. doi: 10.1073/pnas.87.10.3841. [DOI] [PMC free article] [PubMed] [Google Scholar]
  28. Meyer T., Wensel T., Stryer L. Kinetics of calcium channel opening by inositol 1,4,5-trisphosphate. Biochemistry. 1990 Jan 9;29(1):32–37. doi: 10.1021/bi00453a004. [DOI] [PubMed] [Google Scholar]
  29. Missiaen L., De Smedt H., Parys J. B., Casteels R. Co-activation of inositol trisphosphate-induced Ca2+ release by cytosolic Ca2+ is loading-dependent. J Biol Chem. 1994 Mar 11;269(10):7238–7242. [PubMed] [Google Scholar]
  30. Nunn D. L., Taylor C. W. Liver inositol, 1,4,5-trisphosphate-binding sites are the Ca2(+)-mobilizing receptors. Biochem J. 1990 Aug 15;270(1):227–232. doi: 10.1042/bj2700227. [DOI] [PMC free article] [PubMed] [Google Scholar]
  31. Nüsse O., Lindau M. The calcium signal in human neutrophils and its relation to exocytosis investigated by patch-clamp capacitance and Fura-2 measurements. Cell Calcium. 1993 Apr;14(4):255–269. doi: 10.1016/0143-4160(93)90047-a. [DOI] [PubMed] [Google Scholar]
  32. Oldershaw K. A., Nunn D. L., Taylor C. W. Quantal Ca2+ mobilization stimulated by inositol 1,4,5-trisphosphate in permeabilized hepatocytes. Biochem J. 1991 Sep 15;278(Pt 3):705–708. doi: 10.1042/bj2780705. [DOI] [PMC free article] [PubMed] [Google Scholar]
  33. Oliva C., Cohen I. S., Mathias R. T. Calculation of time constants for intracellular diffusion in whole cell patch clamp configuration. Biophys J. 1988 Nov;54(5):791–799. doi: 10.1016/S0006-3495(88)83017-0. [DOI] [PMC free article] [PubMed] [Google Scholar]
  34. Parker I., Ivorra I. Inhibition by Ca2+ of inositol trisphosphate-mediated Ca2+ liberation: a possible mechanism for oscillatory release of Ca2+. Proc Natl Acad Sci U S A. 1990 Jan;87(1):260–264. doi: 10.1073/pnas.87.1.260. [DOI] [PMC free article] [PubMed] [Google Scholar]
  35. Parker I., Miledi R. Nonlinearity and facilitation in phosphoinositide signaling studied by the use of caged inositol trisphosphate in Xenopus oocytes. J Neurosci. 1989 Nov;9(11):4068–4077. doi: 10.1523/JNEUROSCI.09-11-04068.1989. [DOI] [PMC free article] [PubMed] [Google Scholar]
  36. Pietri F., Hilly M., Mauger J. P. Calcium mediates the interconversion between two states of the liver inositol 1,4,5-trisphosphate receptor. J Biol Chem. 1990 Oct 15;265(29):17478–17485. [PubMed] [Google Scholar]
  37. Pittet D., Schlegel W., Lew D. P., Monod A., Mayr G. W. Mass changes in inositol tetrakis- and pentakisphosphate isomers induced by chemotactic peptide stimulation in HL-60 cells. J Biol Chem. 1989 Nov 5;264(31):18489–18493. [PubMed] [Google Scholar]
  38. Pusch M., Neher E. Rates of diffusional exchange between small cells and a measuring patch pipette. Pflugers Arch. 1988 Feb;411(2):204–211. doi: 10.1007/BF00582316. [DOI] [PubMed] [Google Scholar]
  39. Spät A., Bradford P. G., McKinney J. S., Rubin R. P., Putney J. W., Jr A saturable receptor for 32P-inositol-1,4,5-triphosphate in hepatocytes and neutrophils. Nature. 1986 Feb 6;319(6053):514–516. doi: 10.1038/319514a0. [DOI] [PubMed] [Google Scholar]
  40. Taylor C. W. Kinetics of inositol 1,4,5-trisphosphate-stimulated Ca2+ mobilization. Adv Second Messenger Phosphoprotein Res. 1992;26:109–142. [PubMed] [Google Scholar]
  41. Van Delden C., Favre C., Spät A., Cerny E., Krause K. H., Lew D. P. Purification of an inositol 1,4,5-trisphosphate-binding calreticulin-containing intracellular compartment of HL-60 cells. Biochem J. 1992 Feb 1;281(Pt 3):651–656. doi: 10.1042/bj2810651. [DOI] [PMC free article] [PubMed] [Google Scholar]
  42. Van Delden C., Foti M., Lew D. P., Krause K. H. Ca2+ and Mg2+ regulation of inositol 1,4,5-triphosphate binding in myeloid cells. J Biol Chem. 1993 Jun 15;268(17):12443–12448. [PubMed] [Google Scholar]
  43. Varnai P., Demaurex N., Jaconi M., Schlegel W., Lew D. P., Krause K. H. Highly co-operative Ca2+ activation of intermediate-conductance K+ channels in granulocytes from a human cell line. J Physiol. 1993 Dec;472:373–390. doi: 10.1113/jphysiol.1993.sp019952. [DOI] [PMC free article] [PubMed] [Google Scholar]
  44. Worley P. F., Baraban J. M., Snyder S. H. Inositol 1,4,5-trisphosphate receptor binding: autoradiographic localization in rat brain. J Neurosci. 1989 Jan;9(1):339–346. doi: 10.1523/JNEUROSCI.09-01-00339.1989. [DOI] [PMC free article] [PubMed] [Google Scholar]
  45. 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]
  46. von Tscharner V., Deranleau D. A., Baggiolini M. Calcium fluxes and calcium buffering in human neutrophils. J Biol Chem. 1986 Aug 5;261(22):10163–10168. [PubMed] [Google Scholar]

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