The Molecular Basis of Chloride Transport in Shark Rectal Gland
Tóm tắt
Transepithelial Cl− secretion in vertebrates is accomplished by a secondary active transport process brought about by the coordinated activity of apical and basolateral transport proteins. The principal basolateral components are the Na+/K+-ATPase pump, the Na+/K+/2Cl− cotransporter (symporter) and a K+ channel. The rate-limiting apical component is a cyclic-AMP-stimulated Cl− channel. As postulated nearly two decades ago, the net Cl− movement from the blood to the lumen involves entry into the epithelial cells with Na+ and K+, followed by active Na+ extrusion via the pump and passive K+ exit via a channel. Intracellular [Cl−] is raised above electrochemical equilibrium and exits into the lumen when the apical Cl− channel opens. Cl− secretion is accompanied by a passive paracellular flow of Na+. The tubules of the rectal glands of elasmobranchs are highly specialized for secreting concentrated NaCl by this mechanism and hence have served as an excellent experimental model in which to characterize the individual steps by electrophysiological and ion flux measurements. The recent molecular cloning and heterologous expression of the apical Cl− channel and basolateral cotransporter have enabled more detailed analyses of the mechanisms and their regulation. Not surprisingly, since hormones acting through kinases control secretion, both the Cl− channel, which is the shark counterpart of the CFTR (Cystic Fibrosis Transmembrane Conductance Regulator), and the cotransporter are regulated by phosphorylation and dephosphorylation. The primary stimulation of secretion by hormones employing cyclic AMP as second messenger activates CFTR via the direct action of protein kinase A (PKA), which phosphorylates multiple sites on the R domain. In contrast, phosphorylation of the cotransporter by as yet unidentified kinases is apparently secondary to the decrease in intracellular chloride concentration caused by anion exit through CFTR.
Từ khóa
Tài liệu tham khảo
Anderson, 1991, Demonstration that CFTR is an ion channel by alteration of its anion selectivity, Science, 253, 202, 10.1126/science.1712984
Baukrowitz, 1994, Coupling of CFTR Cl− channel gating to an ATP hydrolysis cycle, Neuron, 12, 473, 10.1016/0896-6273(94)90206-2
Bear, 1992, Purification and functional reconstitution of the cystic fibrosis transmembrane conductance regulator (CFTR), Cell, 68, 809, 10.1016/0092-8674(92)90155-6
Bertorello, 1991, Phosphorylation of the catalytic subunit of Na+, K(+)-ATPase inhibits the activity of the enzyme, Proc. natn. Acad. Sci. U.S.A., 88, 11359, 10.1073/pnas.88.24.11359
Boucher, 1993, The CF mouse: a tool for facilitating the development of gene therapy for CF lung disease, Ped. Pulmonol. Suppl., 9, 64
Burger, 1960, Function of the rectal gland in the spiny dogfish, Science, 131, 670, 10.1126/science.131.3401.670
Chang, 1994, Mapping of CFTR membrane topology by glycosylation site insertion, J. biol. Chem. (in press)
Chang, 1993, Protein kinase A (PKA) still activates CFTR chloride channel after mutagenesis of all ten PKA consensus phosphorylation sites, J. biol. Chem., 268, 11304, 10.1016/S0021-9258(18)82125-1
Cheng, 1991, Phosphorylation of the R domain by cyclic AMP-dependent protein kinase regulates the CFTR chloride channel, Cell, 66, 1027, 10.1016/0092-8674(91)90446-6
Dulhanty, 1994, Phosphorylation by cyclic AMP-dependent protein kinase causes a conformational change in the R domain of the cystic fibrosis transmembrane conductance regulator, Biochemistry, N.Y., 33, 4072, 10.1021/bi00179a036
Dulhanty, 1994, A two-domain model for the R domain of the cystic fibrosis transmembrane conductance regulator based on sequence similarities, FEBS Letts., 343, 109, 10.1016/0014-5793(94)80300-5
Epstein, 1985, Na–K–Cl cotransport in chloride transporting epithelia, Ann. N.Y. Acad. Sci., 456, 187, 10.1111/j.1749-6632.1985.tb14864.x
Epstein, 1983, Mechanism and control of hyperosmotic NaCl-rich secretion by the rectal gland of Squalus acanthias, J. exp. Biol., 106, 25, 10.1242/jeb.106.1.25
Forbush Iii, 1992, Na–K–Cl cotransport in the shark rectal gland. I. Regulation in the intact perfused gland, Am. J. Physiol., 262, C1000, 10.1152/ajpcell.1992.262.4.C1000
Gamba, 1993, Primary structure and functional expression of a cDNA encoding the thiazide-sensitive, electroneutral sodium-chloride cotransporter, Proc. natn. Acad. Sci. U.S.A., 90, 2749, 10.1073/pnas.90.7.2749
Greger, 1984, Mechanism of NaCl secretion in the rectal gland of spiny dogfish (Squalus acanthias). I. Experiments in isolated in vitro perfused rectal gland tubules, Pflügers Arch., 402, 63, 10.1007/BF00584833
Greger, 1984, Mechanism of NaCl secretion in rectal gland tubules of spiny dogfish (Squalus acanthias). II. Effects of inhibitors, Pflügers Arch., 402, 364, 10.1007/BF00583937
Greger, 1985, Cl− channels in the apical cell membrane of the rectal gland ‘induced’ by cyclic AMP, Pflügers Arch., 403, 446, 10.1007/BF00589260
Greger, 1987, Chloride channels in the luminal membrane of the rectal gland of the dogfish (Squalus acanthias). Properties of the ‘larger’ conductance channel, Pflügers Arch., 409, 114, 10.1007/BF00584757
Greger, 1984, Mechanism of NaCl secretion in rectal gland tubules of spiny dogfish (Squalus acanthias). III. Effects of stimulation of secretion by cyclic AMP, Pflügers Arch., 402, 376, 10.1007/BF00583938
Grzelczak, 1990, The molecular cloning of a CFTR homologue from shark rectal gland, Ped. Pulmonol. Suppl., 5, 95
Haas, 1989, Properties and diversity of Na–K–Cl cotransporters, A. Rev. Physiol., 51, 443, 10.1146/annurev.ph.51.030189.002303
Hanrahan, 1993, Low-conductance chloride channel activated by cyclic AMP in the rectal gland of the shark Squalus acanthias and in cells heterologously expressing the shark CFTR gene, Bull. Mt. Desert Island biol. Lab., 32, 48
Hanrahan, 1993, Patch clamp studies of apical membrane chloride channels, Cystic Fibrosis – Current Topics, 1, 93
Kelley, 1991, Endogenous adenosine is an autocoid feedback inhibitor of chloride transport in shark rectal gland, J. clin. Invest., 88, 1933, 10.1172/JCI115517
Kelley, 1990, A1 adenosine receptors inhibit chloride transport in the shark rectal gland. Dissociation of inhibition and cyclic AMP, J. clin. Invest., 85, 1629, 10.1172/JCI114614
Kinne, 1985, The use of membrane vesicles to study the NaCl/KCl cotransporter involved in active transepithelial chloride transport, Pflügers Arch., 405, 5101, 10.1007/BF00581788
La, 1991, Regulation of epithelial chloride channels by protein phosphatase, Am. J. Physiol., 260, C1217, 10.1152/ajpcell.1991.260.6.C1217
Lytle, 1992, The Na–K–Cl cotransport protein of shark rectal gland. II. Regulation by direct phosphorylation, J. biol. Chem., 267, 25438, 10.1016/S0021-9258(19)74060-5
Lytle, 1992, Regulation of Na–K–Cl cotransport in the Cl-secreting cells of the shark (Squalus acanthias) rectal gland, Bull. Mt Desert Island biol. Lab., 32, 48
Lytle, 1992, The Na–K–Cl cotransport protein of shark rectal gland. I. Development of monoclonal antibodies, immunoaffinity purification and partial biochemical characterization, J. biol. Chem., 267, 25428, 10.1016/S0021-9258(19)74059-9
Marshall, 1991, Identification and localization of a dogfish homolog of human cystic fibrosis transmembrane conductance regulator, J. biol. Chem., 266, 22749, 10.1016/S0021-9258(18)54631-7
Nellans, 1973, Coupled sodium–chloride influx across the brush border of rabbit ileum, Am. J. Physiol., 226, 467, 10.1152/ajplegacy.1973.225.2.467
Payne, 1994, Alternatively spliced isoforms of the putative renal Na–K–Cl cotransporter are differentially distributed within the rabbit kidney, Proc. natn. Acad. Sci. U.S.A., 91, 4544, 10.1073/pnas.91.10.4544
Quinton, 1992, Control of CFTR chloride conductance by ATP levels through non-hydrolytic binding, Nature, 360, 79, 10.1038/360079a0
Rich, 1991, Effect of deleting the R domain in CFTR-generated chloride channels, Science, 253, 205, 10.1126/science.1712985
Riordan, 1993, The cystic fibrosis transmembrane conductance regulator, A. Rev. Physiol., 55, 609, 10.1146/annurev.ph.55.030193.003141
Riordan, 1991, The CF gene product as a member of a membrane transporter (TM6-NBF) super family, Adv. exp. Biol. Med., 290, 19, 10.1007/978-1-4684-5934-0_3
Riordan, 1993, Role of phosphorylation domains in CFTR function, Ped. Pulmonol. Suppl., 9, 177
Riordan, 1989, Identification of the cystic fibrosis gene: Cloning and characterization of complementary DNA, Science, 245, 1066, 10.1126/science.2475911
Shull, 1985, Amino acid sequence of the catalytic subunit of the (Na++K+) ATPase deduced from a complementary DNA, Nature, 316, 691, 10.1038/316691a0
Siegel, 1976, Evidence for active chloride transport in dogfish rectal gland, Am. J. Physiol., 230, 1250, 10.1152/ajplegacy.1976.230.5.1250
Silva, 1981, Inhibition of chloride secretion by BaCl2 in the rectal gland of the spiny dogfish, Squalus acanthias, Bull. Mt Desert Island biol. Lab., 21, 12
Silva, 1983, Ouabain binding in rectal gland of Squalus acanthias, J. Membr. Biol., 75, 105, 10.1007/BF01995630
Silva, 1977, Mechanism of active chloride secretion by shark rectal gland: role of Na–K–ATPase in chloride transport, Am. J. Physiol., 233, F298
Silva, 1983, Evidence that sodium is secreted via the paracellular pathway in shark rectal gland, Bull. Mt Desert Island biol. Lab., 23, 46
Simon, 1982, The osmoregulatory system of birds with salt glands, Comp. Biochem. Physiol., 71, 547, 10.1016/0300-9629(82)90203-1
Stoff, 1979, Hormonal regulation of active chloride transport in dogfish rectal gland, Am. J. Physiol., 237, F138
Sullivan, 1991, cAMP-activated Cl conductance is expressed in Xenopus oocytes by injection of shark rectal gland mRNA, Am. J. Physiol., 260, C664, 10.1152/ajpcell.1991.260.3.C664
Tabcharani, 1991, Phosphorylation-regulated Cl channel in CHO cells stably expressing the cystic fibrosis gene, Nature, 352, 628, 10.1038/352628a0
Tabcharani, 1993, Multi-ion pore behaviour in the CFTR chloride channel, Nature, 366, 79, 10.1038/366079a0
Welsh, 1993, Molecular mechanisms of CFTR chloride channel dysfunction in cystic fibrosis, Cell, 73, 1251, 10.1016/0092-8674(93)90353-R