Abstract
The volumes of acinar cells isolated from rat lacrimal gland were measured on computer by video-imaging. Cells were found to swell on exposure to hypotonic solutions; they subsequently exhibited a regulatory volume decrease (RVD). RVD was inhibited in the absence of extracellular Ca2+, and by the K+ channel blocker tetraethylammonium chloride (2 mm TEA+). The possible involvement of K+ channels in RVD was further investigated in cell-attached patches. Exposing the cells to a hypotonic solution activated channels with a conductance of 141±6 pS (n=11). These channels were partially blocked by 0.5 mm TEA+, and channel activation was not observed in the absence of extracellular Ca2+. Experiments in the inside-out patch configuration demonstrated that the channels activated by hypotonie stress were “maxi” Ca2+-activated K+ channels. It is concluded that the opening of these channels plays an important role in RVD, by facilitating K+ loss from the cell.
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Blatz, A.L., Magleby, K.L. 1984. Ion conductance and selectivity of single calcium-activated potassium channels in cultured rat muscle. J. Gen. Physiol. 84:1–23
Brown, P.D., Loo, D.D.F., Wright, E.M. 1988. Ca2+-activated K+ channels in the apical membrane of Necturus choroid plexus. J. Membrane Biol. 105:207–219
Christensen, O. 1987. Mediation of cell volume regulation by Ca2+ influx through stretch-activated channels. Nature 330:66–68
Davidson, R.M. 1993. Membrane stretch activates a high-conductance K+ channel in G292 osteoblastic-like cells. J. Membrane Biol. 131:81–92
Dubé, L., Parent, L., Sauvé, R. 1990. Hypotonic shock activates a maxi K+ channel in primary cultured proximal tubule cells. Am. J. Physiol. 259:F348-F356
Elliott, A.C., Lau, K.R., Brown, P.D. 1991. The effects of Na+ replacement on intracellular pH and [Ca2+] in rabbit salivary gland acinar cells. J. Physiol. 444:419–439
Findlay, I. 1984. A patch-clamp study of potassium channels and whole-cell currents in acinar cells of the mouse lacrimal gland. J. Physiol. 350:179–195
Foskett, J.K., Melvin, J.E. 1989. Activation of salivary secretion: coupling of cell volume and [Ca2+]i in single cells. Science 244: 1582–1585
Foskett, J.K., Wong, M.M.M., Sue-A-Quan, G., Robertson, M.A. 1994. Isosmotic modulation of cell volume and intracellular ion activities during stimulation of single exocrine cells. J. Exp. Zoology 268:104–110
Hazama, A., Okada, Y. 1988. Ca2+-sensitivity of volume-regulatory K+ and Cl− channels in cultured human epithelial cells. J. Physiol. 402:687–702
Hoffman, E.K., Simonsen, L.O. 1989. Membrane mechanisms in volume and pH regulation in vertebrate cells. Physiol. Rev. 69:315–382
Kotera, T., Brown, P.D. 1993. Calcium-dependent chloride currents activated by hyposmotic stress in rat lacrimal gland acinar cells. J. Membrane Biol. 134:67–74
Larcombe-McDouall, J.B., Seo, Y., Wood, B., Steward, M.C. 1991. Cell volume changes during fluid secretion in the isolated, perfused rat mandibular salivary gland studied by 1H NMR spectroscopy. J. Physiol. 438:358P
Lechleiter, J.D., Dartt, D.A., Brehm, P. 1988. Vasoactive intestinal peptide activates Ca2+-dependent K+ channels through a cAMP pathway in mouse lacrimal cells. Neuron 1:227–235
Moran, A., Turner, R.J. 1993. Secretagogue-induced RVD in HSY cells is due to K+ channels activated by Ca2+ and protein kinase-C. Am. J. Physiol. 265:C1405-C1411
Nakahari, T., Murakami, M., Yoshida, H., Miyamoto, M., Sohma, Y., Imai, Y. 1990. Decrease in rat submandibular acinar cell volume during ACh stimulation. Am. J. Physiol. 258:G878-G886
Nakahari, T., Yoshida, H., Imai, Y., Murakami, M., Seo, Y. 1992. Osmotically inactive space during hyperosmotic stress in the perfused submandibular gland of the rat. Jap. J. Physiol. 42:977–985
Park, K.P., Brown, P.D. 1994. Hyposmotic stress activates K+ channels in acinar cells isolated from rat lacrimal gland. J. Physiol. 475:98P
Saito, Y., Ozawa, T., Hayashi, H., Nishiyama, A. 1985. Acetylcholine-induced change in intracellular Cl− activity of mouse lacrimal acinar cells. Pfluegers Arch. 405:108–111
Sarkardi, B., Parker, J.C. 1991. Activation of ion transport pathways by changes in volume. Biochim. Biophys. Acta. 1071:407–427
Steward, M.C., Larcombe-McDouall, J.B. 1989. Absence of volume regulation in acinar cells of isolated perfused rat mandibular gland. J. Physiol. 446:102P
Steward, M.C., Seo, Y., Case, R.M. 1989. Intracellular pH during secretion in the perfused rabbit mandibular salivary gland measured by 31PNMR spectroscopy. Pfluegers Arch. 414:200–207
Taniguchi, J., Guggino, W.B. 1989. Membrane stretch: a physiological stimulator of Ca2+-activated K+ channels in thick ascending limb. Am. J. Physiol. 257:F347-F352
Trautmann, A., Marty, A. 1984. Activation of Ca-dependent K channels by carbamoylcholine in rat lacrimal glands. Proc. Natl. Acad. Sci. USA 81:611–615
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We thank Dr. T. Kotera for helpful advice. We are also grateful to Dr. A. C. Elliott for his comments on the manuscript. K.-P.P. was a Visiting Academic Fellow supported by the University of Manchester, Faculty of Medicine Bequest Fund. J.S.B. was a Wellcome Research Fellow, and I.J.D. is an MRC Postgraduate Scholar. This work was supported by the Wellcome Trust (Grants: 037321/Z/92 and 035713/Z/92).
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Park, K.P., Beck, J.S., Douglas, I.J. et al. Ca2+-activated K+ channels are involved in regulatory volume decrease in acinar cells isolated from the rat lacrimal gland. J. Membarin Biol. 141, 193–201 (1994). https://doi.org/10.1007/BF00238253
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DOI: https://doi.org/10.1007/BF00238253