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. 1990 Jun 1;95(6):1103–1122. doi: 10.1085/jgp.95.6.1103

Biphasic Ca2+ dependence of inositol 1,4,5-trisphosphate-induced Ca release in smooth muscle cells of the guinea pig taenia caeci

PMCID: PMC2216357  PMID: 2373998

Abstract

Ca2+ dependence of the inositol 1,4,5-trisphosphate (IP3)-induced Ca release was studied in saponin-skinned smooth muscle fiber bundles of the guinea pig taenia caeci at 20-22 degrees C. Ca release from the skinned fiber bundles was monitored by microfluorometry of fura-2. Fiber bundles were first treated with 30 microM ryanodine for 120 s in the presence of 45 mM caffeine to lock open the Ca-induced Ca release channels which are present in approximately 40% of the Ca store of the smooth muscle cells of the taenia. The Ca store with the Ca-induced Ca release mechanism was functionally removed by this treatment, but the rest of the store, which was devoid of the ryanodine-sensitive Ca release mechanism, remained intact. The Ca2+ dependence of the IP3- induced Ca release mechanism was, therefore, studied independently of the Ca-induced Ca release. The rate of IP3-induced Ca release was enhanced by Ca2+ between 0 and 300 nM, but further increase in the Ca2+ concentration also exerted an inhibitory effect. Thus, the rate of IP3- induced Ca release was about the same in the absence of Ca2+ and at 3 microM Ca2+, and was about six times faster at 300 nM Ca2+. Hydrolysis of IP3 within the skinned fiber bundles was not responsible for these effects, because essentially the same effects were observed with or without Mg2+, an absolute requirement of the IP3 phosphatase activity. Ca2+, therefore, is likely to affect the gating mechanism and/or affinity for the ligand of the IP3-induced Ca release mechanism. The biphasic effect of Ca2+ on the IP3-induced Ca release is expected to form a positive feedback loop in the IP3-induced Ca mobilization below 300 nM Ca2+, and a negative feedback loop above 300 nM Ca2+.

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Selected References

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  1. Abdel-Latif A. A. Calcium-mobilizing receptors, polyphosphoinositides, and the generation of second messengers. Pharmacol Rev. 1986 Sep;38(3):227–272. [PubMed] [Google Scholar]
  2. Berridge M. J., Irvine R. F. Inositol trisphosphate, a novel second messenger in cellular signal transduction. Nature. 1984 Nov 22;312(5992):315–321. doi: 10.1038/312315a0. [DOI] [PubMed] [Google Scholar]
  3. 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]
  4. 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]
  5. Connolly T. M., Lawing W. J., Jr, Majerus P. W. Protein kinase C phosphorylates human platelet inositol trisphosphate 5'-phosphomonoesterase, increasing the phosphatase activity. Cell. 1986 Sep 12;46(6):951–958. doi: 10.1016/0092-8674(86)90077-2. [DOI] [PubMed] [Google Scholar]
  6. Danoff S. K., Supattapone S., Snyder S. H. Characterization of a membrane protein from brain mediating the inhibition of inositol 1,4,5-trisphosphate receptor binding by calcium. Biochem J. 1988 Sep 15;254(3):701–705. doi: 10.1042/bj2540701. [DOI] [PMC free article] [PubMed] [Google Scholar]
  7. Downes C. P., Mussat M. C., Michell R. H. The inositol trisphosphate phosphomonoesterase of the human erythrocyte membrane. Biochem J. 1982 Apr 1;203(1):169–177. doi: 10.1042/bj2030169. [DOI] [PMC free article] [PubMed] [Google Scholar]
  8. Fabiato A. Time and calcium dependence of activation and inactivation of calcium-induced release of calcium from the sarcoplasmic reticulum of a skinned canine cardiac Purkinje cell. J Gen Physiol. 1985 Feb;85(2):247–289. doi: 10.1085/jgp.85.2.247. [DOI] [PMC free article] [PubMed] [Google Scholar]
  9. Fleischer S., Ogunbunmi E. M., Dixon M. C., Fleer E. A. Localization of Ca2+ release channels with ryanodine in junctional terminal cisternae of sarcoplasmic reticulum of fast skeletal muscle. Proc Natl Acad Sci U S A. 1985 Nov;82(21):7256–7259. doi: 10.1073/pnas.82.21.7256. [DOI] [PMC free article] [PubMed] [Google Scholar]
  10. 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]
  11. Hansen C. A., Johanson R. A., Williamson M. T., Williamson J. R. Purification and characterization of two types of soluble inositol phosphate 5-phosphomonoesterases from rat brain. J Biol Chem. 1987 Dec 25;262(36):17319–17326. [PubMed] [Google Scholar]
  12. Hirata M., Suematsu E., Hashimoto T., Hamachi T., Koga T. Release of Ca2+ from a non-mitochondrial store site in peritoneal macrophages treated with saponin by inositol 1,4,5-trisphosphate. Biochem J. 1984 Oct 1;223(1):229–236. doi: 10.1042/bj2230229. [DOI] [PMC free article] [PubMed] [Google Scholar]
  13. Iino M. Calcium dependent inositol trisphosphate-induced calcium release in the guinea-pig taenia caeci. Biochem Biophys Res Commun. 1987 Jan 15;142(1):47–52. doi: 10.1016/0006-291x(87)90449-9. [DOI] [PubMed] [Google Scholar]
  14. Iino M. Calcium-induced calcium release mechanism in guinea pig taenia caeci. J Gen Physiol. 1989 Aug;94(2):363–383. doi: 10.1085/jgp.94.2.363. [DOI] [PMC free article] [PubMed] [Google Scholar]
  15. Iino M., Kobayashi T., Endo M. Use of ryanodine for functional removal of the calcium store in smooth muscle cells of the guinea-pig. Biochem Biophys Res Commun. 1988 Apr 15;152(1):417–422. doi: 10.1016/s0006-291x(88)80730-7. [DOI] [PubMed] [Google Scholar]
  16. Kukita M., Hirata M., Koga T. Requirement of Ca2+ for the production and degradation of inositol 1,4,5-trisphosphate in macrophages. Biochim Biophys Acta. 1986 Jan 23;885(1):121–128. doi: 10.1016/0167-4889(86)90046-7. [DOI] [PubMed] [Google Scholar]
  17. Meissner G. Ryanodine activation and inhibition of the Ca2+ release channel of sarcoplasmic reticulum. J Biol Chem. 1986 May 15;261(14):6300–6306. [PubMed] [Google Scholar]
  18. 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]
  19. Rousseau E., Smith J. S., Meissner G. Ryanodine modifies conductance and gating behavior of single Ca2+ release channel. Am J Physiol. 1987 Sep;253(3 Pt 1):C364–C368. doi: 10.1152/ajpcell.1987.253.3.C364. [DOI] [PubMed] [Google Scholar]
  20. Sasaguri T., Hirata M., Kuriyama H. Dependence on Ca2+ of the activities of phosphatidylinositol 4,5-bisphosphate phosphodiesterase and inositol 1,4,5-trisphosphate phosphatase in smooth muscles of the porcine coronary artery. Biochem J. 1985 Nov 1;231(3):497–503. doi: 10.1042/bj2310497. [DOI] [PMC free article] [PubMed] [Google Scholar]
  21. Scarpa A., Brinley F. J., Jr, Dubyak G. Antipyrylazo III, a "middle range" Ca2+ metallochromic indicator. Biochemistry. 1978 Apr 18;17(8):1378–1386. doi: 10.1021/bi00601a004. [DOI] [PubMed] [Google Scholar]
  22. Somlyo A. V., Bond M., Somlyo A. P., Scarpa A. Inositol trisphosphate-induced calcium release and contraction in vascular smooth muscle. Proc Natl Acad Sci U S A. 1985 Aug;82(15):5231–5235. doi: 10.1073/pnas.82.15.5231. [DOI] [PMC free article] [PubMed] [Google Scholar]
  23. Suematsu E., Hirata M., Hashimoto T., Kuriyama H. Inositol 1,4,5-trisphosphate releases Ca2+ from intracellular store sites in skinned single cells of porcine coronary artery. Biochem Biophys Res Commun. 1984 Apr 30;120(2):481–485. doi: 10.1016/0006-291x(84)91279-8. [DOI] [PubMed] [Google Scholar]
  24. Supattapone S., Worley P. F., Baraban J. M., Snyder S. H. Solubilization, purification, and characterization of an inositol trisphosphate receptor. J Biol Chem. 1988 Jan 25;263(3):1530–1534. [PubMed] [Google Scholar]
  25. Walker J. W., Somlyo A. V., Goldman Y. E., Somlyo A. P., Trentham D. R. Kinetics of smooth and skeletal muscle activation by laser pulse photolysis of caged inositol 1,4,5-trisphosphate. Nature. 1987 May 21;327(6119):249–252. doi: 10.1038/327249a0. [DOI] [PubMed] [Google Scholar]
  26. Williams D. A., Becker P. L., Fay F. S. Regional changes in calcium underlying contraction of single smooth muscle cells. Science. 1987 Mar 27;235(4796):1644–1648. doi: 10.1126/science.3103219. [DOI] [PubMed] [Google Scholar]
  27. Worley P. F., Baraban J. M., Supattapone S., Wilson V. S., Snyder S. H. Characterization of inositol trisphosphate receptor binding in brain. Regulation by pH and calcium. J Biol Chem. 1987 Sep 5;262(25):12132–12136. [PubMed] [Google Scholar]
  28. Yagi S., Becker P. L., Fay F. S. Relationship between force and Ca2+ concentration in smooth muscle as revealed by measurements on single cells. Proc Natl Acad Sci U S A. 1988 Jun;85(11):4109–4113. doi: 10.1073/pnas.85.11.4109. [DOI] [PMC free article] [PubMed] [Google Scholar]

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