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](https://cdn.ncbi.nlm.nih.gov/pmc/blobs/75cc/361598/9a11c3934039/cellregul00045-0037.png)
![586](https://cdn.ncbi.nlm.nih.gov/pmc/blobs/75cc/361598/5c0d9fdc0c6e/cellregul00045-0038.png)
![587](https://cdn.ncbi.nlm.nih.gov/pmc/blobs/75cc/361598/575ed8215061/cellregul00045-0039.png)
![588](https://cdn.ncbi.nlm.nih.gov/pmc/blobs/75cc/361598/14a03bc19780/cellregul00045-0040.png)
![589](https://cdn.ncbi.nlm.nih.gov/pmc/blobs/75cc/361598/f77bf6b4cb73/cellregul00045-0041.png)
![590](https://cdn.ncbi.nlm.nih.gov/pmc/blobs/75cc/361598/c9b31ff4c63d/cellregul00045-0042.png)
![591](https://cdn.ncbi.nlm.nih.gov/pmc/blobs/75cc/361598/311f52b7f140/cellregul00045-0043.png)
![592](https://cdn.ncbi.nlm.nih.gov/pmc/blobs/75cc/361598/e0fce5a255f2/cellregul00045-0044.png)
![593](https://cdn.ncbi.nlm.nih.gov/pmc/blobs/75cc/361598/70f4e0edcf5d/cellregul00045-0045.png)
![594](https://cdn.ncbi.nlm.nih.gov/pmc/blobs/75cc/361598/5e44b876e25a/cellregul00045-0046.png)
![595](https://cdn.ncbi.nlm.nih.gov/pmc/blobs/75cc/361598/1b08da468b64/cellregul00045-0047.png)
![596](https://cdn.ncbi.nlm.nih.gov/pmc/blobs/75cc/361598/4e7df3b5aabc/cellregul00045-0048.png)
Images in this article
Selected References
These references are in PubMed. This may not be the complete list of references from this article.
- 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]
- 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]
- 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]
- 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]
- 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]
- 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]
- 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]
- 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]
- 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]
- 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]
- 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]
- 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]
- 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]
- 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]
- 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]
- 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]
- 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]
- 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]
- Sachs F. Mechanical transduction in biological systems. Crit Rev Biomed Eng. 1988;16(2):141–169. [PubMed] [Google Scholar]
- 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]
- 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]
- 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]
- 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]
- 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]
- 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]
- 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]
- 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]
- 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]
- 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]