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Cell Volume and Signaling pp 11–28Cite as

Twenty-Five Years of K-Cl Cotransport: From Stimulation by a Thiol Reaction to Cloning of the Full-Length KCCs

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8. References

  1. N.C. Adragna, M. Di Fulvio and P.K. Lauf, Regulation of K-Cl cotransport: From function to genes, J. Memb. Bio. (2004), in press.

    Google Scholar 

  2. E. Delpire, Cation-chloride cotransporters in neuronal communication, News Physiol. Sc. 15, 309–312 (2000).

    CAS  Google Scholar 

  3. P.K. Lauf, N.C. Adragna, K-Cl Cotransport: Properties and Molecular Mechanism, Cell Physiol. Biochem. 10, 341–354 (2000).

    Article  PubMed  CAS  Google Scholar 

  4. D.B. Mount, E. Delpire, G. Gamba, A.E. Hall, E. Poch, R.S. Hoover, and S.C. Hebert, The electroneutral cation-chloride cotransporters, J. Exp. Biol. 201, 2091–2102 (1998).

    PubMed  CAS  Google Scholar 

  5. P.B. Dunham and R. Blostein, L antigens of sheep red cell membranes and modulation of ion transport. Am. J. Physiol. 272, C357–C368 (1997).

    PubMed  CAS  Google Scholar 

  6. P.K. Lauf and B.E. Theg, A chloride-dependent K+ flux induced by N-ethylmaleimide in genetically low K+ sheep and goat erythrocytes, Biochem. Biophys. Res. Commun. 92, 1422 (1980).

    Article  PubMed  CAS  Google Scholar 

  7. A. Rothstein, Sulfhydryl groups in membrane structure and function, in Current Topics in Membrane Transport, edited by F. Bronner and A. Kleinzeller, Vol. 1, Acad. Press, New York, 135–176 (1970).

    Google Scholar 

  8. P.K. Lauf, Evidence for chloride-dependent potassium and water transport induced by hyposmotic stress in erythrocytes of the marine teleost Opsanus Tau, J. Comp. Physiol. 146, 9 (1982).

    CAS  Google Scholar 

  9. P.M. Cala, Volume Regulation by Amphiuma Red Blood Cells, J. Gen. Physiol. 76. 683 (1980).

    Article  PubMed  CAS  Google Scholar 

  10. P. Geck, C. Pietrzyk, B.C. Burckhardt, B. Pfeiffer and E. Heinz, Electrically silent cotransport of Na+,K+ and Cl− in Ehrlich cells, Biochim. Biophys. Acta 600, 432 (1980).

    Article  PubMed  CAS  Google Scholar 

  11. E. Schlatter, R. Greger and C. Weidtke, Effect of « high ceiling » diuretics on active salt transport in the cortical thick ascending limb of Henle’s loop of rabbit kidney, Pflüger’s Arc. 396, 210 (1983).

    Article  CAS  Google Scholar 

  12. P.B. Dunham and J.C. Ellory, Passive potassium transport in low potassium sheep red cells: dependence upon cell volume and chloride, J Physiol. (London) 318, 511–530 (1981).

    CAS  Google Scholar 

  13. L.A. Beauge and N.C. Adragna, The kinetics of ouabain inhibition and partition of rubidium influx in human red blood cells, J. Gen. Physiol. 57, 576–592 (1971).

    Article  PubMed  CAS  Google Scholar 

  14. P. K. Lauf, Kinetic Comparison of ouabain-resistant K:Cl fluxes (K:Cl [CO]-transport) stimulated in sheep erythrocytes by membrane thiol oxidation and alkylation, Mol Cell Biochem 82, 97–106 (1988).

    PubMed  CAS  Google Scholar 

  15. P.K. Lauf, Thiol-dependent K:Cl transport in sheep red cells: VIII. Activation through metabolically and chemically reversible oxidation by diamide, J. Memb. Bio., 101, 179–188 (1988).

    Article  CAS  Google Scholar 

  16. N.C. Adragna and P.K. Lauf, Oxidative stimulation of K-Cl cotransport in red cells of different species including human with abnormal hemoglobins, J. Memb. Biol. 155, 207–217 (1997).

    Article  CAS  Google Scholar 

  17. H. Fujise, K. Higa, T. Kanemaru, M. Fukuda, N.C. Adragna, and P.K. Lauf, Effect of GSH depletion of K-Cl cotransport and regulatory volume decrease in high K/high GSH dog red blood cells, Am. J. Physiol. 281, C2003–C2009 (2001).

    CAS  Google Scholar 

  18. C.W.M. Haest, D. Kamp, G. Plasa and B. Deuticke, Intra-and intermolecular cross-linking of membrane proteins in intact erythrocytes and ghosts by SH-oxidizing agents, Biochim. Biophys. Acta 469, 226–230 (1977).

    Article  PubMed  CAS  Google Scholar 

  19. P.K. Lauf, N.C. Adragna, and R.P. Garay, Activation by N-ethylmaleimide of a latent K+Cl− flux in human erythrocytes, Am. J. Physiol. 246, C385–390, 1984.

    PubMed  CAS  Google Scholar 

  20. M.L. Jennings and N. Al-Rohil, Kinetics of activation and inactivation of swelling-stimulated K+Cl− cotransport. The volume-sensitive parameter is the rate constant for inactivation, J. Gen. Physiol. 95, 1021–1040 (1990).

    Article  PubMed  CAS  Google Scholar 

  21. W. Su, B.F. Shmukler, M.N. Chernova, A.K. Stuart-Tilley, L. De Franceschi, C. Brugnara and S.L. Alper, Mouse K-Cl cotransporter KCC1: cloning, mapping, pathological expression and functional regulation, Am. J. Physiol. 277, C860–867 (1999).

    Google Scholar 

  22. K. Kirk, The effect of N-ethylmaleimide on K+ and Cl− transport pathways in the lamprey erythrocyte membrane: activation of K+/Cl− cotransport, J. Exp. Biol. 159, 325–334 (1991).

    PubMed  CAS  Google Scholar 

  23. W.C. O’Neill, Cl-dependent K transport in a pure population of volume-regulating human erythrocytes, Am. J. Physiol. 256, C858–C864 (1989).

    PubMed  CAS  Google Scholar 

  24. P.K. Lauf, Thiol dependent, passive K/Cl transport in sheep erythrocytes. IV. Furosemide inhibition and the role of external Rb+, Na+ and Cl−, J. Memb. Biol. 77, 57–62 (1984).

    Article  CAS  Google Scholar 

  25. E. Delpire and P.K. Lauf, Kinetics of DIDS inhibition of swelling-activated K-Cl cotransport in low K sheep erythrocytes, J. Memb. Biol. 126, 89–96 (1992).

    Article  CAS  Google Scholar 

  26. P.K. Lauf, Thiol stimulated passive K/Cl transport in sheep red cells. I. Dependence on chloride and external K+ (Rb+) ions, J. Memb. Biol. 73, 237–246 (1983).

    Article  CAS  Google Scholar 

  27. P.K. Lauf, Thiol dependent passive K/Cl transport in sheep red cells. II. Loss of Cl− and N-ethylmaleimide sensitivity in maturing high K+ cells, J. Memb. Biol. 73, 247–256, (1983).

    Article  CAS  Google Scholar 

  28. A. Mercado, L. Song, N. Vasquez, D.B. Mount and G. Gamba, Functional comparison of the K+-Cl− cotransporters KCC1 and KCC4, J. Biol. Chem. 275, 30326–30334 (2000).

    Article  PubMed  CAS  Google Scholar 

  29. P.K. Lauf, Active and passive monovalent ion transport association with membrane antigens in sheep red blood cells: a molecular riddle, In: Red Cell Membrane Transport in Health and Disease, J. C. Ellory and I. Bernhardt (Eds.), Springer-Verlag, 691–720 (2003).

    Google Scholar 

  30. J. Bauer and P.K. Lauf, Thiol dependent passive K/Cl transport in sheep erythrocytes. III. Differential reactivity of membrane SH groups with N-ethylmaleimide and iodoacetamide, J. Memb. Biol. 73, 257–261, (1983).

    Article  CAS  Google Scholar 

  31. K.H. Ryu and P.K. Lauf, Evidence for inhibitory SH groups in the thiol-activated K:Cl cotransporter of low K sheep red blood cells, Molec. Cell. Biochem. 97, 145–150 (1990).

    Google Scholar 

  32. P.K. Lauf, C.M. Perkins, and N.C. Adragna, Metabolic and volume effects of N-ethylmaleimide-activated K+Cl− flux in human red cells, Am. J. Physiol. 249, C126–C128 (1985).

    Google Scholar 

  33. P.K. Lauf, Thiol dependent, passive K/Cl transport in sheep erythrocytes. V. Stimulation by N-ethylmaleimide requires cellular ATP, Am. J. Physiol. 245, C14. 44–48 (1983).

    Google Scholar 

  34. P.K. Lauf, K+ Cl Cotransport: Sulfhydryls, divalent cations and the mechanism of volume activation in a red cell, J. Memb. Biol. 88, 1–13 (1985).

    Article  CAS  Google Scholar 

  35. O.E. Ortiz-Carranza, N.C. Adragna and P.K. Lauf, Modulation of K-Cl cotransport in volume clamped LK sheep erythrocytes by pH, magnesium and ATP, Am. J. Physiol. 271, C1049–C1058 (1996).

    PubMed  CAS  Google Scholar 

  36. P.B. Dunham, J. Klimczak and P.J. Logue. Swelling-activation of K-Cl cotransport in LK sheep erythrocytes: a three state process, J. Gen Physiol., 101, 733–765 (1993).

    Article  PubMed  CAS  Google Scholar 

  37. E. Delpire and P.K. Lauf, Magnesium and ATP dependence of K:Cl Cotransport in low K sheep red blood cells. J. Physiol. (LondoN) 441, 219–231 (1991).

    CAS  Google Scholar 

  38. W.M. Hart, Jr., and E.O. Titus, Isolation of a protein component of sodium-potassium transport adenosine triphosphatase containing ligand-protected sulfhydryl groups, J. Biol. Chem. 248, 1365–1371 (1973).

    PubMed  CAS  Google Scholar 

  39. P. K. Lauf, Thiol-dependent passive K:Cl transport in sheep red blood cells: X. A hydroxylamine-oxidation induced K:Cl flux blocked by diethylpyrocarbonate. J. Memb. Biol. 118, 153–160 (1990).

    Article  CAS  Google Scholar 

  40. P.K. Lauf, K:Cl Cotransport: Emerging molecular aspects of a ouabain-resistant, volume-responsive transport system in red blood cells, Renal Physiol. 3–5, 248–259 (1988).

    Article  Google Scholar 

  41. I. Bize, B. Güvenec, G. Buchbinder and C. Brugnara, Stimulation of human erythrocyte K-Cl cotransport and protein phosphatase type 2A by N-ethylmaleimide: role of intracellular Mg++, J. Memb. Biol. 177, 159–168 (2000).

    Article  CAS  Google Scholar 

  42. M.L. Jennings, Volume-sensitive K+Cl− cotransport in rabbit erythrocytes. Analysis of the rate-limiting activation and inactivation events, J. Gen. Physiol. 114, 743–758 (1999).

    Article  PubMed  CAS  Google Scholar 

  43. P. Flatman, N.C. Adragna and P.K. Lauf, The role of protein kinases in regulating sheep erythrocyte K-Cl cotransport, Am. J. Physiol. 271, C255–C263 (1996).

    PubMed  CAS  Google Scholar 

  44. P.K. Lauf, N.C. Adragna, and N. Agar, Glutathione removal reveals kinases as common targets for K-Cl cotransport stimulation in sheep erythrocytes, Am. J. Physiol. 269, C234–241 (1995).

    PubMed  CAS  Google Scholar 

  45. P.K. Lauf, A. Erdmann and N.C. Adragna, Response of K-Cl cotransport pH, and role of Mg in volume-clamped low K sheep erythrocytes: Three equilibrium states, Am. J. Physiol. 266, C95–C103 (1994).

    PubMed  CAS  Google Scholar 

  46. I. Bize and P.B. Dunham, Staurosporine, a protein kinase inhibitor activates K-Cl cotransport in LK sheep erythrocytes, Am. J. Physiol. 266, C759–C770 (1994).

    PubMed  CAS  Google Scholar 

  47. I. Bize, B. Güvenc, A. Robb, G. Buchbinder, C. Brugnara, Serine/threonine protein phosphatases and regulation of K-Cl cotransport in human erythrocytes, Am. J. Physiol. 277, C926–C936 (1999).

    PubMed  CAS  Google Scholar 

  48. C. Brugnara, Membrane transport of Na and K and cell dehydration in sickle erythrocytes, Experientia 49, 100–109 (1993).

    Article  PubMed  CAS  Google Scholar 

  49. N.C. Adragna L. Lu and P.K. Lauf, Functional expression of K-Cl cotransport in Xenopus Oocytes. In: Fifth Biennial Conference of the Membrane Biophysics Subgroup, October 14–17 (1995).

    Google Scholar 

  50. C.M. Gillen, S. Brill, J.A. Payne and B. Forbush III, Molecular cloning and functional expression of the K-Cl cotransporter from rabbit, rat and human, J. Biol. Chem. 271, 16237–16244 (1996).

    Article  PubMed  CAS  Google Scholar 

  51. J.A. Payne, T.J. Stevenson and L.F. Donaldson, Molecular characterization of a putative K-Cl cotransporter in rat brain, J. Biol. Chem. 271, 16245–16252 (1996).

    Article  PubMed  CAS  Google Scholar 

  52. K. Hiki, R.J. D’Andrea, J. Furze, J. Crawford, E. Woollatt, G.R. Sutherland, M.A. Vadas, and J.R. Gamble, Cloning, characterization, and chromosomal location of a novel human K+-Cl− cotransporter, J. Biol. Chem. 274:10661-10667 (1999).

    Google Scholar 

  53. J.E. Race, F.N. Makhlouf, P.J. Logue, F.H. Wilson, P.B. Dunham, and E.J. Holtzman. Molecular cloning and functional characterization of KCCC3, a new K-Cl cotransporter, Am. J. Physiol. 277, C1210–C1219 (1999).

    PubMed  CAS  Google Scholar 

  54. D.B. Mount, A. Mercado, L. Song, J. Xu, A.L. George, Jr., E. Delpire, and G. Gamba, Cloning and expression of KCC3 and KCC4, new members of the cation-chloride cotransporter gene family, J. Biol. Chem. 274, 16355–16362 (1999).

    Article  PubMed  CAS  Google Scholar 

  55. M. Di Fulvio, T.M. Lincoln, P.K. Lauf, and N.C. Adragna, Protein kinase G regulates the potassium-chloride cotransporter-3 (KCC3) expression in primary cultures of rat vascular smooth muscle cells, J. Biol. Chem. 276, 21046–21052 (2001).

    Article  PubMed  Google Scholar 

  56. M. Di Fulvio, P.K. Lauf, and N.C. Adragna, Nitric oxide signaling pathway regulates the potassium-chloride cotransporter-1 mRNA expression in vascular smooth muscle cells, J. Biol. Chem. 276, 44534–44540 (2001).

    Article  PubMed  CAS  Google Scholar 

  57. P.K. Lauf, J.J. Zhang, E. Delpire, R.E.W. Fyffe, and N.C. Adragna, K-Cl Cotransport: Immunohistochemical and ion flux studies in human embryonic kidney (HEK293) cells transfected with full-length and C-terminal-domain-truncated KCC1 cDNAs, Cell Physiol Biochem. 11, 143–160 (2001).

    Article  PubMed  CAS  Google Scholar 

  58. M.R. Shen, C.H. Chou, and J.C. Ellory, Volume-sensitive KCl cotransport associated with human cervical carcinogenesis. Pflüger’s Arch. 440, 751–760 (2000).

    Article  CAS  Google Scholar 

  59. J. Zhang, P.K. Lauf and N.C. Adragna, Platelet-derived growth factor regulates K-Cl cotransport in vascular smooth muscle cells, Am. J. Physiol., 284, C674–C680 (2003).

    CAS  Google Scholar 

  60. K. Gagnon, N.C. Adragna, R.E.W. Fyffe and P.K. Lauf, Functional and immunochemical evidence for K-Cl cotransport KCC1 in C6 Glia cells, Glia, submitted for publication (2004).

    Google Scholar 

  61. P.K. Lauf, S. Misri, R. Warwar, T.L. Brown and N.C. Adragna, Functional and molecular evidence for K-Cl cotransport and KCC1,3a,b and 4 isoforms in human lens epithelial cells and in human lens tissue, Exp. Eye Research (2004) submitted.

    Google Scholar 

  62. T. Boettger, C.A. Huebner, H. Maler, M.B. Rust, F.X. Beck and T.J. Jentsch, Deafness and renal tubular acidosis in mice lacking the K-Cl cotransporter KCC4, Nature 416, 874–878 (2002).

    Article  PubMed  CAS  Google Scholar 

  63. Y. Chen, M. Morris, E. Delpire, P.K. Lauf and N.C. Adragna, Hypertension in K-Cl cotransporter-3 knockout mice, FASEB J 17, A 858 (2003).

    Article  CAS  Google Scholar 

  64. P.K. Lauf and N.C. Adragna, Temperature-induced functional deocclusion of thiols inhibitory for sheep erythrocyte K-Cl cotransport, Am. J. Physiol. 269, C1167–C1175 (1995).

    PubMed  CAS  Google Scholar 

  65. P.K. Lauf, Jin Zhang, Jing Zhang, and N.C. Adragna, Transient nature of the stimulatory “NEM Effect” on K-Cl cotransport in KCCl-transfected HEK 293 and primary rat aortic smooth muscle cells, J. Gen. Physiol. 116:20a (2000).

    Google Scholar 

  66. N.C. Adragna, J. Zhang, M. Di Fulvio, T.M. Lincoln, and P.K. Lauf, K-Cl cotransport regulation and protein kinase G in cultured vascular smooth muscle cells, J. Memb. Biol. 187, 157–165 (2002).

    Article  CAS  Google Scholar 

  67. S. Casula, B.E. Shmukler, S. Wilhelm, A.K. Stuart-Tilley, W. Su, M.N. Chernova, C. Brugnara and S. Alpers, A dominant negative mutant of the KCC1 K-Cl cotransporter, J. Biol. Chem. 276, 41870–41878 (2001).

    Article  PubMed  CAS  Google Scholar 

  68. M.J. Davies and C.L Hawkins, EPR spin trapping of protein radicals. Free Radical Biol. Med. 36, 1072–1086 (2004).

    Article  CAS  Google Scholar 

  69. J.J. Zhang, S. Misri, N.C. Adragna, K.E.B. Gagnon, R.E.W. Fyffe and P.K. Lauf, Cloning and expression of sheep K-Cl cotransporter KCC1, Cell Physiol Biochem., submitted (2004).

    Google Scholar 

  70. C.J. Oliver and S. Shenolikar, Physiologic importance of protein phosphatase inhibitors, in Frontiers in Biosciences 3, 961–972 (1998).

    Google Scholar 

  71. K. Piechotta, J. Lu, and E. Delpire, Cation chloride cotransporters interact with the stress-related kinases Ste20-related proline-alanine-rich kinase (SPAK) and oxidative stress response I (OSR1), J. Biol. Chem. 277, 50812–50819 (2002).

    Article  PubMed  CAS  Google Scholar 

  72. R.E. Weber, W. Voelter, A. Fago, H. Echner, E. Campanella, and P.S. Low, Modulation of red cell glycolysis: Interaction between vertebrate hemoglobins and cytoplasmic domains of band 3 red cell membrane proteins, Am. J. Physiol. (2004) in press.

    Google Scholar 

  73. S.A. Jewell, G. Bellomo, H. Thor, S. Orrenius and M.T. Smith, Bleb formation in hepatocytes during drug metabolism is caused by disturbances in thiol and calcium ion homeostasis Science, 217, 1257–1258 (1982).

    Article  PubMed  CAS  Google Scholar 

  74. H.E. Sheerin, L.M Snyder and G. Fairbanks, Cation transport in oxidant-stressed erythrocytes: heightened N-ethylmaleimide activation of passive K+ influx after mild peroxidation, Biochim. Biophys. Acta 983, 65–76 (1989).

    Article  PubMed  CAS  Google Scholar 

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  1. Cell Biophysics Laboratory, Dept of Pathology, Wright State University School of Medicine, Dayton, OH

    Peter K. Lauf

  2. Cell Biophysics Laboratory, Dept. of Pharmacology and Toxicology, Wright State University School of Medicine, Dayton, OH

    Norma C. Adragna

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  1. Wright State University, Dayton, Ohio

    Peter K. Lauf  & Norma C. Adragna  & 

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Lauf, P.K., Adragna, N.C. (2004). Twenty-Five Years of K-Cl Cotransport: From Stimulation by a Thiol Reaction to Cloning of the Full-Length KCCs. In: Lauf, P.K., Adragna, N.C. (eds) Cell Volume and Signaling. Advances in Experimental Medicine and Biology, vol 559. Springer, Boston, MA . https://doi.org/10.1007/0-387-23752-6_2

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