K+ current stimulation by Cl- in the midgut epithelium of tobacco hornworm (Manduca sexta)
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Summary
Goblet cells in the midgut epithelium of the tobacco hornworm (Manduca sexta larva, 5th instar) actively secrete K+. This can be measured as short-circuit current (Isc) when the tissue is mounted in an Ussing chamber and bathed in K+-rich standard saline containing 32 mmol K+ · l-1. Isc depends strictly on basolateral (i.e. haemolymph side) K+ and is therefore termed K+ current, IK. Basolateral, but not apical, chloride, bromide and iodide stimulate IK when compared to the baseline current recorded with gluconate-, nitrate- or thiocyanate-containing salines. So-called “Cl--specific” transport inhibitors (frusemide, 9-anthracene carboxylic acid, diphenylamine carboxylic acid and 4,4′-diisothiocyanato-stilbene-2,2′-disulphonic acid) reduce IK when added to the basolateral bath, whether Cl- or gluconate is the principal ambient anion. Cl- stimulates IK according to saturation kinetics. The Michaelis-Menten-type, K+ concentration-dependent, saturation of IK is altered in a highly specific manner when gluconate is replaced by Cl-: maximal K+ current, as well as the apparent Michaelis constant, are increased by a factor of 4. Since IK develops in these conditions exclusively via basolateral, Ba2+-blockable K+ channels, these results can be understood if it is assumed that haemolymph Cl- interferes with the K+ channel by simultaneously lowering the binding affinity for K+ ions and increasing their subsequent transfer rate across the basolateral goblet cell membrane.
Key words
K+ current Cl- stimulation Cl- blockers Midgut Manduca sexta larvaAbbreviations
- 9-AC
9-anthracene carboxylic acid
- DPC
diphenylamine carboxylic acid
- DIDS
4,4′-diisothiocyanato-stilbene-2,2′-disulphonic acid
- DMSO
dimethylsulphoxide
- G
conductance [cellular (c), shunt (sh)]
- Gt
transepithelial conductance
- GK
K+ conductance
- GCl
Cl- conductance
- GNa
Na+ conductance
- xG
conductance in absence of Cl-
- GNa, KCl
transepithelial conductance with Cl- saline
- GNa, Kglu
transepithelial conductance with gluconate saline
- IK(max)
maximal K+ current
- Isc
short-circuit current
- K
Michaelis constant for saturating Cl- stimulation (index Cl) or K+ current saturation (index m)
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References
- Alpert G (1989) Mechanismen der Stimulation des aktiven K+ Transports im Mitteldarm der Larve des Tabakschwärmers Manduca sexta durch Hämolymph-Chlorid oder Hypotonie. MSc thesis, Freie Universität BerlinGoogle Scholar
- Cabantchik ZI, Rothstein A (1972) The nature of the membrane sites controlling anion permeability of human red blood cells as determined by studies with disulfonic stibene derivatives. J Membr Biol 10:311–330Google Scholar
- Carmeliet E, Verdonck F (1977) Reduction of potassium permeability by chloride substitution in cardiac cells. J Physiol (Lond) 265:193–206Google Scholar
- Chamberlin ME (1990) Ion transport across the midgut of the tobacco hornworm (Manduca sexta). J Exp Biol 150:425–442Google Scholar
- Chao AC, Koch AR, Moffett DF (1989) Active chloride transport in isolated posterior midgut of tobacco hornworm (Manduca sexta). Am J Physiol 257:R752-R761PubMedGoogle Scholar
- Chao AC, Koch AR, Moffett DF (1990) Basal membrane uptake in potassium-secreting cells of midgut of tobacco hornworm (Manduca sexta). Am J Physiol 258:R112-R119PubMedGoogle Scholar
- Cioffi M (1979) The morphology and fine structure of the larval midgut of a moth (Manduca sexta) in relation to active ion transport. Tissue Cell 11:467–479Google Scholar
- Cioffi M, Harvey WR (1981) Comparison of potassium transport in three structurally distinct regions of the insect midgut. J Exp Biol 91:103–116Google Scholar
- De Wolf I, Van Driessche W (1986) Voltage-dependent Ba2+ block of K+ channels in apical membrane of frog skin. Am J Physiol 251:C696-C706Google Scholar
- Dow JAT (1984) Extremely high pH in biological systems: a model for carbonate transport. Am J Physiol 246:R633-R655Google Scholar
- Dow JAT, Harvey WR (1988) Role of midgut electrogenic K+ pump potential difference in regulating lumen K+ and pH in larval lepidoptera. J Exp Biol 140:455–463Google Scholar
- Dow JAT, Gupta BL, Hall TA Harvey WR (1984) X-ray micro-analysis of elements in frozen-hydrated sections of an electrogenic K+ transport system: the posterior midgut of tobacco hornworm (Manduca sexta) in vivo and in vitro. J Membr Biol 77:223–241Google Scholar
- Fuchs W, Hviid Larsen E, Lindemann B (1977) Current-voltage curve of Na+ channels and concentration dependence of Na+ permeability in frog skin. J Physiol (Lond) 267:137–166Google Scholar
- Geck P, Heinz E (1986) The Na−K−2Cl cotransport system. J Membr Biol 91:97–105Google Scholar
- Griego VM, Moffett D, Spence KD (1979) Inhibtion of active K+ transport in the tobacco hornworm (Manduca sexta) midgut after ingestion of Bacillus thuringensis endotoxin. J Insect Physiol 25:283–288Google Scholar
- Gullans SR, Avison MJ, Ogino T, Shulman RG, Giebisch G (1986) Furosemide-sensitive K+ efflux induced by glucose in the rabbit proximal tubule. Kidney Int 29:396Google Scholar
- Gögelein H (1988) Chloride channels in epithelia. Biochim Biophys Acta 947:521–547Google Scholar
- Harvey WR (1980) Water and ions in the gut. In: Podesta R, Dean LL, McDiarmid SS, Timmer SF, Young BW (eds) Insec biology in the future. ‘VBW 80’. Marcell Dekker, New York, pp 496–566Google Scholar
- Harvey WR, Cioffi M, Dow JAT, Wolfersberger MG (1983) Potassium ion transport ATPase in insect epithelia. J Exp Biol 106:91–117Google Scholar
- Hille B (1984) Ionic channels of excitable membranes. Sinauer, Sunderland, MassGoogle Scholar
- Inoue I (1986) Modification of K+ conductance of the squid axon membrane by SITS. J Gen Physiol 88:507–520Google Scholar
- Jungreis A, Vaughan GL (1977) Insensitivity of lepidopteran tissues to ouabain: absence of ouabain binding and Na+−K+-ATPase in larval and adult midgut. J Insect Physiol 23:505–509Google Scholar
- Koch A, Moffett DF (1987) Kinetics of extracellular solute movement in the isolated midgut of tobacco hornworm (Manduca sexta). J Exp Biol 133:199–214Google Scholar
- Moffett DF (1979) Bathing solution tonicity and potassium transport by the midgut of the tobacco hornworm (Manduca sexta). J Exp Biol 78:213–223Google Scholar
- Moffett DF (1980) Voltage-current relation and K+ transport in tobacco hornworm (Manduca sexta) midgut. J Membr Biol 54:213–219Google Scholar
- Moffett DF, Koch AR (1983) The kinetics of active K+ transport by the midgut of lepidopteran larvae: effect of divalent ions. J Exp Biol 105:403–405Google Scholar
- Moffett DF, Koch AR (1985) Barium modifies the concentration dependence of active potassium transport by insect midgut. J Membr Biol 86:89–97Google Scholar
- Moffett DF, Koch AR (1988) Electrophysiology of K+ transport by midgut epithelium of lepidopteran insect larvae (Manduca sexta): I. The transbasal electrochemical gradient. J Exp Biol 135:25–38Google Scholar
- Moffett DF, Koch AR (1991) Lidocaine and barium distinguish separate routes for transbasal K+ uptake in the posterior midgut of the tobacco hornworm (Manduca sexta). J Exp Biol 157:243–256Google Scholar
- Moffett DF, Hudson RL, Moffett SB, Ridgway RL (1982) Intracellular K+ activities and cell membrane potentials in a K+ transporting epithelium, the midgut of tobacco hornworm (Manduca sexta). J Membr Biol 70:59–68Google Scholar
- Nielsen R (1984) Active transepithelial potassium transport in frog skin via specific potassium channels in the apical membrane. Acta Physiol Scand 120:287–296Google Scholar
- O'Donnell MJ, Maddrell SHP (1984) Secretion by the Malpighian tubules of Rhodnius prolixus Stal: electrical events. J Exp Biol 110:275–290Google Scholar
- Onken H, Graszynski K (1989) Active Cl- absorption by the Chinese crab (Eriocheir sinensis) gill epithelium measured by transepithelial potential difference. J Comp Physiol B 159:21–28Google Scholar
- Scholtz E, Zeiske W (1988) A novel synergistic stimulation of Na+ transport across frog skin (Xenopus laevis) by external Cd2+ and Ca2+ ions. Pflügers Arch 413:174–180Google Scholar
- Schröder H (1987) Anionen-Stimulation der K+-Permeabilität der serosalen Membran im K+-sezernierenden Mitteldarmepithel der Larven des Tabak-Schwärmers Manduca sexta. MSc thesis, Freie Universität BerlinGoogle Scholar
- Schultz SG (1981) Potassium transport by rabbit descending colon, in vitro. Fed Proc 40:2408–2411Google Scholar
- Schweikl H, Klein U, Schindlbeck M, Wieczorek H (1989) Electrogenic potassium transport in the tobacco hornworm midgut. I. A vacuolar-type ATPase, partially purified from potassium-transporting plasma membranes. J Biol Chem 264:11136–11142Google Scholar
- Thomas MV, May TE (1984a) Active potassium ion transport across the caterpillar midgut: I. Tissue electrical properties and potassium ion transport inhibition. J Exp Biol 108:273–291Google Scholar
- Thomas MV, May TE (1984b) Active potassium ion transport across the caterpillar midgut: II. Intracellular microelectrode studies. J Exp Biol 108:293–304Google Scholar
- Van Driessche W (1984) Physiological role of apical potassium ion channels in frog skin. J Physiol (Lond) 356:79–95Google Scholar
- Van Driessche W, Zeiske W (1985) Ionic channels in epithelial cell membranes. Physiol Rev 65:833–903PubMedGoogle Scholar
- wangemann P, Wittner P, Di Stefano A, Englert HC, Schlatter E, Greger R (1986) Cl- channel blockers in the thick ascending limb of the loop of Henle. Structure-activity relationship. Pflügers Arch 407 [Suppl]:S128-S141Google Scholar
- Wieczorek H, Weerth S, Schindlbeck M, Klein U (1989) Electrogenic potassium transport in the tobacco hornworm midgut: II. A vacuolar-type proton pump in a vesicle fraction enriched with potassium-transporting plasma membranes from tobacco hornworm midgut. J Biol Chem 264:11143–11148Google Scholar
- Wolosin JM, Forte JG (1985) K+ and Cl- conductances in the apical membrane from secreting oxyntic cells are concurrently inhibited by divalent cations. J Membr Biol 83:261–272Google Scholar
- Wood JL, Moreton RB (1978) Refinements in the short-circuit technique and its application to active potassium transport across the Cecropia midgut. J Exp Biol 77:123–140Google Scholar
- Zeiske W (1978) The stimulation of Na+ uptake in frog skin by uranyl ions. Biochim Biophys Acta 509:218–229Google Scholar
- Zeiske W (1979) Die Na+-Aufnahme durch die apikale Membran des froschhautepithels: Ihr Mechanismus und ihre Steuerung durch Ionen und lipophile Substanzen. PhD thesis, Universität des Saarlandes, SaarbrückenGoogle Scholar
- Zeiske W, Lindemann B (1974) Chemical stimulation of Na+ current through the outer surface of frog skin epithelium. Biochim Biophys Acta 352:323–326Google Scholar
- Zeiske W, Schröder H (1988) Apical and serosal K+ channels in larval insect midgut (abstract). Comp Biochem Physiol 90A:836Google Scholar
- Zeiske W, Van Driessche W (1983) The interaction of “K+-like” cations with the apical K+ channel in frog skin. J Membr Biol 76:57–72Google Scholar
- Zeiske W, Van Driessche W, Ziegler R (1986) Current-noise analysis of the basolateral route for K+ ions across a K+-secreting insect midgut epithelium (Manduca sexta). Pflügers Arch 407:657–663Google Scholar
- Zeiske W, Alpert G, Marin H (1990) The chloride-stimulated K+ secretion by insect midgut and its modification in the presence of osmotic gradients (congress communication). J Bask Clin Physiol Pharmacol 1:399–404Google Scholar
- Zerahn K (1982) Inhibition of active K+ transport in the isolated midgut of Hyalophora cecropia by Tl+. J Exp Biol 96:307–313Google Scholar
- Zerahn K, Koefoed B (1979) Transport of thallium ions across the isolated midgut of Hyalophora cecropia. J Exp Biol 78:105–120Google Scholar
- Zeuthen T, Christensen O, Cherksey B (1987) Electrodiffusion of Cl- and K+ in epithelial membranes reconstituted into planar lipid bilayers. Pflügers Arch 408:275–281Google Scholar