Abstract
K homeostasis is maintained in higher animals by epithelia of the kidney and intestine. Little is known regarding the molecular regulation of K secretion. We injected Xenopus oocytes with mRNA from teleost intestine, a K-secreting epithelium with apical membrane K channels. Oocytes expressed a conductance that displayed whole-cell current properties with the following characteristics: marked selectivity for K over Na and Cl, voltage-independent kinetics, Ca insensitivity, tonic activation, and inward rectification in symmetrical K. Barium, quinine, and tetraethylammonium blocked the conductance, whereas apamin, charybdotoxin, and 4-aminopyridine did not. The K conductance was rapidly (t1/2 = 10 min) and completely inactivated by 4 beta-phorbol 12-myristate 13-acetate but not by 4 alpha-phorbol 12,13-didecanoate. Sucrose density gradient fractionation revealed that mRNA required for expression is in the 1- to 2-kilobase size range, suggesting the possibility that a single subunit encodes the channel. The K conductance expressed from injection of size-fractionated mRNA was identical in all respects to that seen using unfractionated mRNA, including response to 4 beta-phorbol 12-myristate 13-acetate. The results suggest that protein kinase C regulates K secretion in epithelia by modulation of apical K channels.
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- Alkon D. L., Naito S., Kubota M., Chen C., Bank B., Smallwood J., Gallant P., Rasmussen H. Regulation of Hermissenda K+ channels by cytoplasmic and membrane-associated C-kinase. J Neurochem. 1988 Sep;51(3):903–917. doi: 10.1111/j.1471-4159.1988.tb01827.x. [DOI] [PubMed] [Google Scholar]
- Apkon M., Nerbonne J. M. Alpha 1-adrenergic agonists selectively suppress voltage-dependent K+ current in rat ventricular myocytes. Proc Natl Acad Sci U S A. 1988 Nov;85(22):8756–8760. doi: 10.1073/pnas.85.22.8756. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Baraban J. M., Snyder S. H., Alger B. E. Protein kinase C regulates ionic conductance in hippocampal pyramidal neurons: electrophysiological effects of phorbol esters. Proc Natl Acad Sci U S A. 1985 Apr;82(8):2538–2542. doi: 10.1073/pnas.82.8.2538. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Barish M. E. A transient calcium-dependent chloride current in the immature Xenopus oocyte. J Physiol. 1983 Sep;342:309–325. doi: 10.1113/jphysiol.1983.sp014852. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Christie M. J., Adelman J. P., Douglass J., North R. A. Expression of a cloned rat brain potassium channel in Xenopus oocytes. Science. 1989 Apr 14;244(4901):221–224. doi: 10.1126/science.2539643. [DOI] [PubMed] [Google Scholar]
- Colby K. A., Blaustein M. P. Inhibition of voltage-gated K channels in synaptosomes by sn-1,2-dioctanoylglycerol, an activator of protein kinase C. J Neurosci. 1988 Dec;8(12):4685–4692. doi: 10.1523/JNEUROSCI.08-12-04685.1988. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Doerner D., Pitler T. A., Alger B. E. Protein kinase C activators block specific calcium and potassium current components in isolated hippocampal neurons. J Neurosci. 1988 Nov;8(11):4069–4078. doi: 10.1523/JNEUROSCI.08-11-04069.1988. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Dumont J. N. Oogenesis in Xenopus laevis (Daudin). I. Stages of oocyte development in laboratory maintained animals. J Morphol. 1972 Feb;136(2):153–179. doi: 10.1002/jmor.1051360203. [DOI] [PubMed] [Google Scholar]
- Farley J., Auerbach S. Protein kinase C activation induces conductance changes in Hermissenda photoreceptors like those seen in associative learning. Nature. 1986 Jan 16;319(6050):220–223. doi: 10.1038/319220a0. [DOI] [PubMed] [Google Scholar]
- Frech G. C., VanDongen A. M., Schuster G., Brown A. M., Joho R. H. A novel potassium channel with delayed rectifier properties isolated from rat brain by expression cloning. Nature. 1989 Aug 24;340(6235):642–645. doi: 10.1038/340642a0. [DOI] [PubMed] [Google Scholar]
- Frindt G., Palmer L. G. Ca-activated K channels in apical membrane of mammalian CCT, and their role in K secretion. Am J Physiol. 1987 Mar;252(3 Pt 2):F458–F467. doi: 10.1152/ajprenal.1987.252.3.F458. [DOI] [PubMed] [Google Scholar]
- Frindt G., Palmer L. G. Low-conductance K channels in apical membrane of rat cortical collecting tubule. Am J Physiol. 1989 Jan;256(1 Pt 2):F143–F151. doi: 10.1152/ajprenal.1989.256.1.F143. [DOI] [PubMed] [Google Scholar]
- Frizzell R. A., Halm D. R., Musch M. W., Stewart C. P., Field M. Potassium transport by flounder intestinal mucosa. Am J Physiol. 1984 Jun;246(6 Pt 2):F946–F951. doi: 10.1152/ajprenal.1984.246.6.F946. [DOI] [PubMed] [Google Scholar]
- Hays S. R., Baum M., Kokko J. P. Effects of protein kinase C activation on sodium, potassium, chloride, and total CO2 transport in the rabbit cortical collecting tubule. J Clin Invest. 1987 Dec;80(6):1561–1570. doi: 10.1172/JCI113242. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Hockberger P., Toselli M., Swandulla D., Lux H. D. A diacylglycerol analogue reduces neuronal calcium currents independently of protein kinase C activation. Nature. 1989 Mar 23;338(6213):340–342. doi: 10.1038/338340a0. [DOI] [PubMed] [Google Scholar]
- Hunter M., Lopes A. G., Boulpaep E., Giebisch G. Regulation of single potassium ion channels from apical membrane of rabbit collecting tubule. Am J Physiol. 1986 Oct;251(4 Pt 2):F725–F733. doi: 10.1152/ajprenal.1986.251.4.F725. [DOI] [PubMed] [Google Scholar]
- Iverson L. E., Tanouye M. A., Lester H. A., Davidson N., Rudy B. A-type potassium channels expressed from Shaker locus cDNA. Proc Natl Acad Sci U S A. 1988 Aug;85(15):5723–5727. doi: 10.1073/pnas.85.15.5723. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Julius D., MacDermott A. B., Axel R., Jessell T. M. Molecular characterization of a functional cDNA encoding the serotonin 1c receptor. Science. 1988 Jul 29;241(4865):558–564. doi: 10.1126/science.3399891. [DOI] [PubMed] [Google Scholar]
- Musch M. W., Orellana S. A., Kimberg L. S., Field M., Halm D. R., Krasny E. J., Jr, Frizzell R. A. Na+-K+-Cl- co-transport in the intestine of a marine teleost. Nature. 1982 Nov 25;300(5890):351–353. doi: 10.1038/300351a0. [DOI] [PubMed] [Google Scholar]
- O'Grady S. M., Palfrey H. C., Field M. Characteristics and functions of Na-K-Cl cotransport in epithelial tissues. Am J Physiol. 1987 Aug;253(2 Pt 1):C177–C192. doi: 10.1152/ajpcell.1987.253.2.C177. [DOI] [PubMed] [Google Scholar]
- Ribalet B., Eddlestone G. T., Ciani S. Metabolic regulation of the K(ATP) and a maxi-K(V) channel in the insulin-secreting RINm5F cell. J Gen Physiol. 1988 Aug;92(2):219–237. doi: 10.1085/jgp.92.2.219. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Sansom S. C., O'Neil R. G. Mineralocorticoid regulation of apical cell membrane Na+ and K+ transport of the cortical collecting duct. Am J Physiol. 1985 Jun;248(6 Pt 2):F858–F868. doi: 10.1152/ajprenal.1985.248.6.F858. [DOI] [PubMed] [Google Scholar]
- Smith P. L., McCabe R. D. Mechanism and regulation of transcellular potassium transport by the colon. Am J Physiol. 1984 Nov;247(5 Pt 1):G445–G456. doi: 10.1152/ajpgi.1984.247.5.G445. [DOI] [PubMed] [Google Scholar]
- Soliven B., Szuchet S., Arnason B. G., Nelson D. J. Forskolin and phorbol esters decrease the same K+ conductance in cultured oligodendrocytes. J Membr Biol. 1988 Oct;105(2):177–186. doi: 10.1007/BF02009170. [DOI] [PubMed] [Google Scholar]
- Syková E. Extracellular K+ accumulation in the central nervous system. Prog Biophys Mol Biol. 1983;42(2-3):135–189. doi: 10.1016/0079-6107(83)90006-8. [DOI] [PubMed] [Google Scholar]
- Takumi T., Ohkubo H., Nakanishi S. Cloning of a membrane protein that induces a slow voltage-gated potassium current. Science. 1988 Nov 18;242(4881):1042–1045. doi: 10.1126/science.3194754. [DOI] [PubMed] [Google Scholar]
- Timpe L. C., Schwarz T. L., Tempel B. L., Papazian D. M., Jan Y. N., Jan L. Y. Expression of functional potassium channels from Shaker cDNA in Xenopus oocytes. Nature. 1988 Jan 14;331(6152):143–145. doi: 10.1038/331143a0. [DOI] [PubMed] [Google Scholar]
- Walsh K. B., Kass R. S. Regulation of a heart potassium channel by protein kinase A and C. Science. 1988 Oct 7;242(4875):67–69. doi: 10.1126/science.2845575. [DOI] [PubMed] [Google Scholar]
- Walz W., Hertz L. Functional interactions between neurons and astrocytes. II. Potassium homeostasis at the cellular level. Prog Neurobiol. 1983;20(1-2):133–183. doi: 10.1016/0301-0082(83)90013-8. [DOI] [PubMed] [Google Scholar]
- Wang W. H., White S., Geibel J., Giebisch G. A potassium channel in the apical membrane of rabbit thick ascending limb of Henle's loop. Am J Physiol. 1990 Feb;258(2 Pt 2):F244–F253. doi: 10.1152/ajprenal.1990.258.2.F244. [DOI] [PubMed] [Google Scholar]
- Wollheim C. B., Dunne M. J., Peter-Riesch B., Bruzzone R., Pozzan T., Petersen O. H. Activators of protein kinase C depolarize insulin-secreting cells by closing K+ channels. EMBO J. 1988 Aug;7(8):2443–2449. doi: 10.1002/j.1460-2075.1988.tb03090.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
- de Weille J. R., Schmid-Antomarchi H., Fosset M., Lazdunski M. Regulation of ATP-sensitive K+ channels in insulinoma cells: activation by somatostatin and protein kinase C and the role of cAMP. Proc Natl Acad Sci U S A. 1989 Apr;86(8):2971–2975. doi: 10.1073/pnas.86.8.2971. [DOI] [PMC free article] [PubMed] [Google Scholar]