Skip to main content
Cell Regulation logoLink to Cell Regulation
. 1990 Jul;1(8):585–596. doi: 10.1091/mbc.1.8.585

Mechanical stimulation and intercellular communication increases intracellular Ca2+ in epithelial cells.

M J Sanderson 1, A C Charles 1, E R Dirksen 1
PMCID: PMC361598  PMID: 2078569

Abstract

Intercellular communication of epithelial cells was examined by measuring changes in intracellular calcium concentration ([Ca2+]i). Mechanical stimulation of respiratory tract ciliated cells in culture induced a wave of increasing Ca2+ that spread, cell by cell, from the stimulated cell to neighboring cells. The communication of these Ca2+ waves between cells was restricted or blocked by halothane, an anesthetic known to uncouple cells. In the absence of extracellular Ca2+, the mechanically stimulated cell showed no change or a decrease in [Ca2+]i, whereas [Ca2+]i increased in neighboring cells. Iontophoretic injection of inositol 1,4,5-trisphosphate (IP3) evoked a communicated Ca2+ response that was similar to that produced by mechanical stimulation. These results support the hypothesis that IP3 acts as a cellular messenger that mediates communication through gap junctions between ciliated epithelial cells.

Full text

PDF
585

Images in this article

Selected References

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

  1. Bazil C. W., Minneman K. P. Effects of clinically effective concentrations of halothane on adrenergic and cholinergic synapses in rat brain in vitro. J Pharmacol Exp Ther. 1989 Jan;248(1):143–148. [PubMed] [Google Scholar]
  2. Berridge M. J., Irvine R. F. Inositol phosphates and cell signalling. Nature. 1989 Sep 21;341(6239):197–205. doi: 10.1038/341197a0. [DOI] [PubMed] [Google Scholar]
  3. Burt J. M., Spray D. C. Volatile anesthetics block intercellular communication between neonatal rat myocardial cells. Circ Res. 1989 Sep;65(3):829–837. doi: 10.1161/01.res.65.3.829. [DOI] [PubMed] [Google Scholar]
  4. Christensen O. Mediation of cell volume regulation by Ca2+ influx through stretch-activated channels. Nature. 1987 Nov 5;330(6143):66–68. doi: 10.1038/330066a0. [DOI] [PubMed] [Google Scholar]
  5. Cornell-Bell A. H., Finkbeiner S. M., Cooper M. S., Smith S. J. Glutamate induces calcium waves in cultured astrocytes: long-range glial signaling. Science. 1990 Jan 26;247(4941):470–473. doi: 10.1126/science.1967852. [DOI] [PubMed] [Google Scholar]
  6. Eberhard D. A., Holz R. W. Intracellular Ca2+ activates phospholipase C. Trends Neurosci. 1988 Dec;11(12):517–520. doi: 10.1016/0166-2236(88)90174-9. [DOI] [PubMed] [Google Scholar]
  7. Fabiato A., Fabiato F. Calcium release from the sarcoplasmic reticulum. Circ Res. 1977 Feb;40(2):119–129. doi: 10.1161/01.res.40.2.119. [DOI] [PubMed] [Google Scholar]
  8. Foster P. S., Gesini E., Claudianos C., Hopkinson K. C., Denborough M. A. Inositol 1,4,5-trisphosphate phosphatase deficiency and malignant hyperpyrexia in swine. Lancet. 1989 Jul 15;2(8655):124–127. doi: 10.1016/s0140-6736(89)90182-7. [DOI] [PubMed] [Google Scholar]
  9. Fraser S. E., Green C. R., Bode H. R., Gilula N. B. Selective disruption of gap junctional communication interferes with a patterning process in hydra. Science. 1987 Jul 3;237(4810):49–55. doi: 10.1126/science.3037697. [DOI] [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. Guharay F., Sachs F. Stretch-activated single ion channel currents in tissue-cultured embryonic chick skeletal muscle. J Physiol. 1984 Jul;352:685–701. doi: 10.1113/jphysiol.1984.sp015317. [DOI] [PMC free article] [PubMed] [Google Scholar]
  12. Gustin M. C., Zhou X. L., Martinac B., Kung C. A mechanosensitive ion channel in the yeast plasma membrane. Science. 1988 Nov 4;242(4879):762–765. doi: 10.1126/science.2460920. [DOI] [PubMed] [Google Scholar]
  13. Jacob R. Imaging cytoplasmic free calcium in histamine stimulated endothelial cells and in fMet-Leu-Phe stimulated neutrophils. Cell Calcium. 1990 Feb-Mar;11(2-3):241–249. doi: 10.1016/0143-4160(90)90075-6. [DOI] [PubMed] [Google Scholar]
  14. Johnston M. F., Simon S. A., Ramón F. Interaction of anaesthetics with electrical synapses. Nature. 1980 Jul 31;286(5772):498–500. doi: 10.1038/286498a0. [DOI] [PubMed] [Google Scholar]
  15. Lansman J. B., Hallam T. J., Rink T. J. Single stretch-activated ion channels in vascular endothelial cells as mechanotransducers? 1987 Feb 26-Mar 4Nature. 325(6107):811–813. doi: 10.1038/325811a0. [DOI] [PubMed] [Google Scholar]
  16. Loewenstein W. R. Junctional intercellular communication: the cell-to-cell membrane channel. Physiol Rev. 1981 Oct;61(4):829–913. doi: 10.1152/physrev.1981.61.4.829. [DOI] [PubMed] [Google Scholar]
  17. O'Sullivan A. J., Cheek T. R., Moreton R. B., Berridge M. J., Burgoyne R. D. Localization and heterogeneity of agonist-induced changes in cytosolic calcium concentration in single bovine adrenal chromaffin cells from video imaging of fura-2. EMBO J. 1989 Feb;8(2):401–411. doi: 10.1002/j.1460-2075.1989.tb03391.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  18. Reed W., Satir P. Spreading ciliary arrest in a mussel gill epithelium: characterization by quick fixation. J Cell Physiol. 1986 Feb;126(2):191–205. doi: 10.1002/jcp.1041260207. [DOI] [PubMed] [Google Scholar]
  19. Sachs F. Mechanical transduction in biological systems. Crit Rev Biomed Eng. 1988;16(2):141–169. [PubMed] [Google Scholar]
  20. Sanderson M. J., Chow I., Dirksen E. R. Intercellular communication between ciliated cells in culture. Am J Physiol. 1988 Jan;254(1 Pt 1):C63–C74. doi: 10.1152/ajpcell.1988.254.1.C63. [DOI] [PubMed] [Google Scholar]
  21. Sanderson M. J., Dirksen E. R. A versatile and quantitative computer-assisted photoelectronic technique used for the analysis of ciliary beat cycles. Cell Motil. 1985;5(4):267–292. doi: 10.1002/cm.970050402. [DOI] [PubMed] [Google Scholar]
  22. Sanderson M. J., Dirksen E. R. Mechanosensitivity of cultured ciliated cells from the mammalian respiratory tract: implications for the regulation of mucociliary transport. Proc Natl Acad Sci U S A. 1986 Oct;83(19):7302–7306. doi: 10.1073/pnas.83.19.7302. [DOI] [PMC free article] [PubMed] [Google Scholar]
  23. Sanderson M. J., Sleigh M. A. Ciliary activity of cultured rabbit tracheal epithelium: beat pattern and metachrony. J Cell Sci. 1981 Feb;47:331–347. doi: 10.1242/jcs.47.1.331. [DOI] [PubMed] [Google Scholar]
  24. Scanlon M., Williams D. A., Fay F. S. A Ca2+-insensitive form of fura-2 associated with polymorphonuclear leukocytes. Assessment and accurate Ca2+ measurement. J Biol Chem. 1987 May 5;262(13):6308–6312. [PubMed] [Google Scholar]
  25. Spray D. C., Bennett M. V. Physiology and pharmacology of gap junctions. Annu Rev Physiol. 1985;47:281–303. doi: 10.1146/annurev.ph.47.030185.001433. [DOI] [PubMed] [Google Scholar]
  26. Vergara J., Tsien R. Y., Delay M. Inositol 1,4,5-trisphosphate: a possible chemical link in excitation-contraction coupling in muscle. Proc Natl Acad Sci U S A. 1985 Sep;82(18):6352–6356. doi: 10.1073/pnas.82.18.6352. [DOI] [PMC free article] [PubMed] [Google Scholar]
  27. Wier W. G., Cannell M. B., Berlin J. R., Marban E., Lederer W. J. Cellular and subcellular heterogeneity of [Ca2+]i in single heart cells revealed by fura-2. Science. 1987 Jan 16;235(4786):325–328. doi: 10.1126/science.3798114. [DOI] [PubMed] [Google Scholar]
  28. 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]
  29. Williams D. A., Fogarty K. E., Tsien R. Y., Fay F. S. Calcium gradients in single smooth muscle cells revealed by the digital imaging microscope using Fura-2. Nature. 1985 Dec 12;318(6046):558–561. doi: 10.1038/318558a0. [DOI] [PubMed] [Google Scholar]

Articles from Cell Regulation are provided here courtesy of American Society for Cell Biology

RESOURCES