A serine residue in ClC-3 links phosphorylation-dephosphorylation to chloride channel regulation by cell volume

Journal of General Physiology

Volumn 113, Issue 1, 1999, Pages 57-70

  Duan, Dayue ^a   Cowley, Suzanne ^a   Horowitz, Burton ^a   Hume, Joseph R ^a  

^a UNIVERSITY OF NEVADA SCHOOL OF MEDICINE   (United States)

Author keywords

Ion channels; Osmotic stress; Protein kinase; Protein phosphatase; Signal transduction

Indexed keywords

CALCIUM ION; CHLORIDE CHANNEL; CHLORIDE ION; PHOSPHOPROTEIN PHOSPHATASE; PHOSPHOPROTEIN PHOSPHATASE INHIBITOR; PROTEIN KINASE C; SERINE;

ANIMAL CELL; ARTICLE; CELL SWELLING; CELL VOLUME; CHANNEL GATING; CONTROLLED STUDY; DEPHOSPHORYLATION; GUINEA PIG; ION TRANSPORT; NONHUMAN; OSMOTIC STRESS; PATCH CLAMP; PROTEIN PHOSPHORYLATION; SIGNAL TRANSDUCTION; SITE DIRECTED MUTAGENESIS;

ANIMALS; CELL LINE; CELL SIZE; CHLORIDE CHANNELS; ELECTRIC STIMULATION; ELECTROPHYSIOLOGY; ENZYME INHIBITORS; GUINEA PIGS; MEMBRANE POTENTIALS; MYOCARDIUM; OSMOLAR CONCENTRATION; PATCH-CLAMP TECHNIQUES; PHOSPHOPROTEIN PHOSPHATASE; PHOSPHORYLATION; PROTEIN KINASE C; SERINE;

EID: 0032891293     PISSN: 00221295     EISSN: None     Source Type: Journal    
DOI: 10.1085/jgp.113.1.57     Document Type: Article

References (77)

1. Bize, I., and P.B. Dunham. 1994. Staurosporine, a protein kinase inhibitor, activates K-Cl cotransport in LK sheep erythrocytes. Am. J. Physiol. 266:C759-C770.
2. Bond, T.D., M.A. Valverde, and C.F. Higgins. 1998. Protein kinase C phosphorylation disengages human and mouse-1a P-glycoproteins from influencing the rate of activation of swelling-activated chloride currents. J. Physiol. (Lond.). 508:333-340.
3. Brinkmeier, H., and H. Jockusch. 1987. Activators of protein kinase C induce myotonia by lowering chloride conductance in muscle. Biochem. Biophys. Res. Commun. 148:1383-1389.
4. Chartier, L., L.L. Rankin, R.E. Allen, Y. Kato, N. Fusetani, H. Karaki, S. Watabe, and D.J. Hartshorne. 1991. Calyculin-A increases the level of protein phosphorylation and changes the shape of 3T3 fibroblasts. Cell Motil. Cytoskelet. 18:26-40.
5. Clapham, D.E. 1998. The list of potential volume-sensitive chloride currents continues to swell (and shrink). J. Gen. Physiol. 111: 623-624.
6. - channels associated with ciliary epithelial homologue of pICln. Am. J. Physiol. 268:C572-C579.
7. - transport by human nonpigmented ciliary epithelial cells. J. Membr. Biol. 150:197-208.
8. Cohen, P., C.F. Holmes, and Y. Tsukitani. 1990. Okadaic acid: a new probe for the study of cellular regulation. Trends Biochem. Sci. 15:98-102.
9. Cohen, P. 1992. Signal integration at the level of protein kinases, protein phosphatases and their substrates. Trends Biochem. Sci. 17: 408-413.
10. Deng, W.P., and J.A. Nickoloff. 1992. Site-directed mutagenesis of virtually any plasmid by eliminating a unique site. Anal. Biochem. 200:81-88.
11. Dick, G.M., K.A. Kuenzli, B. Horowitz, J.R. Hume, and K.M. Sanders. 1998, Functional and molecular identification of a novel chloride conductance in canine colonic smooth muscle. Am. J. Physiol. 275:C940-C950.
12. Doroshenko, P. 1998. Pervanadate inhibits volume-sensitive chloride current in bovine chromaffin cells. Pflügers Arch. 435:303-309.
13. Dove, S.K., C.W. Lloyd, and B.K. Drobak. 1994. Identification of a phosphatidylinositol 3-hydroxy kinase in plant cells: association with the cytoskeleton. Biochem. J. 303:347-350.
14. Dove, S.K., F.T. Cooke, M.R. Douglas, L.G. Sayers, P.J. Parker, and R.H. Michell. 1997. Osmotic stress activates phosphatidylinositol-3,5-bisphosphate synthesis. Nature. 390:187-192.
15. - current. Am. J. Physiol. 263:H1967-H1971.
16. - currents in rabbit atrial myocytes. Characterization of a novel ionic regulatory mechanism. Circ. Res. 77: 379-393.
17. 2 currents in heart. Circ. Res. 80:103-113.
18. Duan, D., C. Winter, S. Cowley, J.R. Hume, and B. Horowitz. 1997b. Molecular identification of a volume-regulated chloride channel. Nature. 390:417-421.
19. - current in human intestinal T84 epithelial cells by phosphorylation. J. Physiol. (Lond.). 490:115-128.
20. Fritsch, J., and A. Edelman. 1997. Osmosensitivity of the hyperpolarization-activated chloride current in human intestinal T84 cells. Am. J. Physiol. 272:C778-C786.
21. Fulton, A.B. 1982. How crowded is the cytoplasm? Cell. 30:345-347.
22. Garner, M.M., and M.B. Burg. 1994. Macromolecular crowding and confinement in cells exposed to hypertonicity. Am. J. Physiol. 266: C877-C892.
23. Gekeler, V., R. Boer, F. Uberall, W. Ise, C. Schubert, I. Utz, J. Hofmann, K.H. Sanders, C. Schachtele, K. Klemm, and H. Grunicke. 1996. Effects of the selective bisindolylmaleimide protein kinase C inhibitor GF 109203X on P-glycoprotein-mediated multidrug resistance. Br. J. Cancer. 74:897-905.
24. Gibson, J.S., and A.C. Hall. 1995. Stimulation of KCl co-transport in equine erythrocytes by hydrostatic pressure: effects of kinase/ phosphatase inhibition. Pflügers Arch. 429:446-448.
25. Grinstein, S., W. Furuya, and L. Bianchini. 1992. Protein kinases, phosphatases, and the control of cell volume. NIPS (News Physiol. Sci.). 7:232-237.
26. Haas, M., D. McBrayer, and C. Lytle. 1995. [Cl-]i-dependent phosphorylation of the Na-K-Cl cotransport protein of dog tracheal epithelial cells. J. Biol. Chem. 270:28955-28961.
27. Hall, S.K., J. Zhang, and M. Lieberman. 1995. Cyclic AMP prevents activation of a swelling-induced chloride-sensitive conductance in chick heart cells. J. Physiol. (Lond.). 488:359-369.
28. Hamill, O.P., A. Marty, E. Neher, B. Sakmann, and F.J. Sigworth. 1981. Improved patch-clamp techniques for high-resolution current recording from cells and cell-free membrane patches. Pflügers Arch. 391:85-100.
29. Hardy, S.P., H.R. Goodfellow, M.A. Valverde, D.R. Gill, V. Sepulveda, and C.F. Higgins. 1995. Protein kinase C-mediated phosphorylation of the human multidrug resistance P-glycoprotein regulates cell volume-activated chloride channels [published erratum appears in EMBO J. 1995. 14:1844]. EMBO (Eur. Mol. Biol. Organ.) J. 14:68-75.
30. Hille, B. 1992. Ionic Channels of Excitable Membranes. Sinauer Associates, Inc., Sunderland, MA.
31. Hug, H., and T.F. Sarre. 1993. Protein kinase C isoenzymes: divergence in signal transduction? Biochem. J. 291:329-343.
32. Hunter, T. 1995. Protein kinases and phosphatases: the yin and yang of protein phosphorylation and signaling. Cell. 80:225-236.
33. Ishihara, H., B.L. Martin, D.L. Brautigan, H. Karaki, H. Ozaki, Y. Kato, N. Fusetani, S. Watabe, K. Hashimoto, and D. Uemura. 1989. Calyculin A and okadaic acid: inhibitors of protein phosphatase activity. Biochem. Biophys. Res. Commun. 159:871-877.
34. Jackson, P.S., and K. Strange. 1993. Volume-sensitive anion channels mediate swelling-activated inositol and taurine efflux. Am. J. Physiol. 265:C1489-C1500.
35. - transport. The volume-sensitive parameter is the rate constant for inactivation. J. Gen. Physiol. 95:1021-1040.
36. Jennings, M.L., and R.K. Schulz. 1991. Okadaic acid inhibition of KCl cotransport. Evidence that protein dephosphorylation is necessary for activation of transport by either cell swelling or N-ethylmaleimide. J. Gen. Physiol. 97:799-817.
37. Jentsch, T.J. 1996. Chloride channels: a molecular perspective. Curr. Opin. Neurobiol. 6:303-310.
38. Kawasaki, M., S. Uchida, T. Monkawa, A. Miyawaki, K. Mikoshiba, F. Marumo, and S. Sasaki. 1994. Cloning and expression of a protein kinase C-regulated chloride channel abundantly expressed in rat brain neuronal cells. Neuron. 12:597-604.
39. Kawasaki, M., M. Suzuki, S. Uchida, S. Sasaki, and F. Marumo. 1995. Stable and functional expression of the CIC-3 chloride channel in somatic cell lines. Neuron. 14:1285-1291.
40. Klein, J.D., P.B. Perry, and W.C. O'Neill. 1993. Regulation by cell volume of Na(+)-K(+)-2Cl-cotransport in vascular endothelial cells: role of protein phosphorylation. J. Membr. Biol. 132:243-252.
41. - cotransport in Ehrlich cells: regulation by protein phosphatases and kinases. Am. J. Physiol. 275:C239-C250.
42. Krick, W., J. Disser, A. Hazama, G. Burckhardt, and E. Fromter. 1991. Evidence for a cytosolic inhibitor of epithelial chloride channels. Pflügers Arch. 418:491-499.
43. Lang, F., G.L. Busch, M. Ritter, H. Volkl, S. Waldegger, E. Gulbins, and D. Haussinger. 1998. Functional significance of cell volume regulatory mechanisms. Physiol. Rev. 78:247-306.
44. Larsen, A.K., B.S. Jensen, and E.K. Hoffmann. 1994. Activation of protein kinase C during cell volume regulation in Ehrlich mouse ascites tumor cells. Biochim. Biophys. Acta. 1222:477-482.
45. Li, M., J.D. McCann, M.P. Anderson, J.P. Clancy, C.M. Liedtke, A.C. Nairn, P. Greengard, and M.J. Welsch. 1989. Regulation of chloride channels by protein kinase C in normal and cystic fibrosis airway epithelia. Science. 244:1353-1356.
46. 2+ and cAMP. J. Membr. Biol. 141:59-68.
47. Lorenz, C., M. Pusch, and T.J. Jentsch. 1996. Heteromultimeric CLC chloride channels with novel properties. Proc. Natl. Acad. Sci. USA. 93:13362-13366.
48. Lytle, C. 1998. A volume-sensitive protein kinase regulates the Na-K-2Cl cotransport in duck red blood cells. Am. J. Physiol. 274: C1002-C1010.
49. Madison, D.V., R.C. Malenka, and R.A. Nicoll. 1986. Phorbol esters block a voltage-sensitive chloride current in hippocampal pyramidal cells. Nature. 321:695-697.
50. Minton, A.P., G.C. Colclasure, and J.C. Parker. 1992. Model for the role of macromolecular crowding in regulation of cellular volume. Proc. Natl. Acad. Sci. USA. 89:10504-10506.
51. - channel. J. Membr. Biol. 157:63-69.
52. Nelson, D.J., X.Y. Tien, W. Xie, T.A. Brasitus, M.A. Kaetzel, and J.R. Dedman. 1996. Shrinkage activates a nonselective conductance: involvement of a Walker-motif protein and PKC. Am. J. Physiol. 270:C179-C191.
53. - channels. Gen. Pharmacol. 27:1131-1140.
54. Nishizuka, Y. 1988. The molecular heterogeneity of protein kinase C and its implications for cellular regulation. Nature. 334:661-665.
55. - channel: fresh start to the molecular identity and volume sensor. Am. J. Physiol. 273:C755-C789.
56. Palfrey, H.C. 1994. Protein phosphorylation control in the activity of volume-sensitive transport systems. In Cellular and Molecular Physiology of Cell Volume Regulation. K. Strange, editor. CRC Press Inc., Boca Raton, FL. 201-214.
57. Pears, C.J., and N.T. Goode. 1997. PKC downregulation: signal or adaptation? In Protein Kinase C. P.J. Parker and L.V. Dekker, editors. R.G. Landes Company, Austin, TX. 45-56.
58. Rosenbohm, A., A.L. George, R. Rudel, and C. Fahlke. 1995. Effect of activators of protein kinase C (PKC) on the muscle chloride channel, CLC-1, studied in native and heterologous expression systems. Pflügers Arch. 429:R25.
59. Saigusa, A., and S. Kokubun. 1988. Protein kinase C may regulate resting anion conductance in vascular smooth muscle cells. Biochem. Biophys. Res. Commun. 155:882-889.
60. Santell, L., R.L. Rubin, and E.G. Levin. 1993. Enhanced phosphorylation and dephosphorylation of a histone-like protein in response to hyperosmotic and hypoosmotic conditions. J. Biol. Chem. 268:21443-21447.
61. Schmidt-Rose, T., and T.J. Jentsch. 1997. Transmembrane topology of a CLC chloride channel. Proc. Natl. Acad. Sci. USA. 94:7633-7638.
62. Staley, K.J. 1994. The role of an inwardly rectifying chloride conductance in postsynaptic inhibition. J. Neurophysiol. 72:273-284.
63. Staley, K.J., R. Smith, J. Schaack, C. Wilcox, and T.J. Jentsch. 1996. Alteration of GABAA receptor function following gene transfer of the CLC-2 chloride channel. Neuron. 17:543-551.
64. Starke, L.C., and M.L. Jennings. 1993. K-Cl cotransport in rabbit red cells: further evidence for regulation by protein phosphatase type 1. Am. J. Physiol. 264:C118-C124.
65. Strange, K., F. Emma, and P.S. Jackson. 1996. Cellular and molecular physiology of volume-sensitive anion channels. Am. J. Physiol. 270:C711-C730.
66. Strange, K. 1998. Molecular identity of the outwardly rectifying, swelling-activated anion channel: time to reevaluate pICln. J. Gen. Physiol. 111:617-622.
67. Szallasi, Z., C.B. Smith, G.R. Pettit, and P.M. Blumberg. 1994. Differential regulation of protein kinase C isozymes by bryostatin 1 and phorbol 12-myristate 13-acetate in NIH 3T3 fibroblasts. J. Biol. Chem. 269:2118-2124.
68. Szücs, G., S. Heinke, C. De Greef, L. Raeymaekers, J. Eggermont, G. Droogmans, and B. Nilius. 1996. The volume-activated chloride current in endothelial cells from bovine pulmonary artery is not modulated by phosphorylation. Pflügers Arch. 431:540-548.
69. Toullec, D., P. Pianetti, H. Coste, P. Bellevergue, T. Grand-Perret, M. Ajakane, V. Baudet, P. Boissin, E. Boursier, and F. Loriolle. 1991. The bisindolylmaleimide GF 109203X is a potent and selective inhibitor of protein kinase C. J. Biol. Chem. 266:15771-15781.
70. Vandenberg, J.I., A. Yoshida, K. Kirk, and T. Powell. 1994. Swelling-activated and isoprenaline-activated chloride currents in guinea pig cardiac myocytes have distinct electrophysiology and pharmacology. J. Gen. Physiol. 104:997-1017.
71. Villaz, M., J.C. Cinniger, and W.J. Moody. 1995. A voltage-gated chloride channel in ascidian embryos modulated by both the cell cycle clock and cell volume. J. Physiol. (Lond.). 488:689-699.
72. Voets, T., G. Droogmans, and B. Nilius. 1996. Membrane currents and the resting membrane potential in cultured bovine pulmonary artery endothelial cells. J. Physiol. (Lond.). 497:95-107.
73. Waldegger, S., P. Barth, G. Raber, and F. Lang. 1997a. Cloning and characterization of a putative human serine/threonine protein kinase transcriptionally modified during anisotonic and isotonic alterations of cell volume. Proc. Natl. Acad. Sci. USA. 94:4440-4445.
74. Waldegger, S., G.L. Busch, N.K. Kaba, G. Zempel, H. Ling, A. Heidland, D. Haussinger, and F. Lang. 1997b. Effect of cellular hydration on protein metabolism. Miner. Electrolyte Metab. 23: 201-205.
75. Waldegger, S., and F. Lang. 1998. Cell volume and gene expression. J. Membr. Biol. 162:95-100.
76. Witters, L.A. 1990. Protein phosphorylation and dephosphorylation. Curr. Opin. Cell Biol. 2:212-220.
77. Yamazaki, J., D. Duan, R. Janiak, K. Kuenzli, B. Horowitz, and J.R. Hume. 1998. Functional and molecular expression of volume-regulated chloride channels in canine vascular smooth muscle cells. J. Physiol. (Lond.). 507:729-736.