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K+ Transport in Toad Perfused Collecting Tubules and Ducts 899

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K+ Transport in Toad Perfused Collecting Tubules and Ducts 899 The Journal of Experimental Biology 205, 897–904 (2002) 897 Printed in Great Britain © The Company of Biologists Limited JEB3774 K+ transport in the mesonephric collecting duct system of the toad Bufo bufo: microelectrode recordings from isolated and perfused tubules Nadja Møbjerg*, Erik Hviid Larsen and Ivana Novak August Krogh Institute, Department of Zoophysiology, University of Copenhagen, Universitetsparken 13, DK-2100 Copenhagen Ø, Denmark *Author for correspondence (e-mail: [email protected]) Accepted 7 January 2001 Summary + We studied the mechanisms of K transport in cells membrane. In collecting tubules and collecting ducts a Vbl from isolated and perfused collecting tubules and ducts of –70±3 mV and –73±3 mV depolarized by 11±3 mV and from the mesonephric kidney of the toad Bufo bufo. Cells 16±3 mV, respectively (N=11; 11). This conductance could 2+ were impaled with microelectrodes across the basal cell also be inhibited by Ba , which depolarized a Vbl of –71±5 membrane. The basolateral membrane potential (Vbl) mV by 9±3 mV (N=5). The pump inhibitor ouabain + –1 depolarized upon change of bath [K ] from 3 to (1 mmol l ) depolarized Vbl, but addition of furosemide to –1 + + 20 mmol l demonstrating a large K conductance in this bath solution did not affect Vbl. The [K ] in urine varied –1 membrane. In collecting tubules and collecting ducts a Vbl from 1.3 to 22.8 mmol l . In conclusion, we propose that of –66±2 mV and –74±4 mV depolarized by 30±2 mV and the collecting duct system of B. bufo secretes K+ into the 36±3 mV, respectively (N=23; 15). The K+ channel urine via luminal K+ channels. inhibitor Ba2+ (1 mmol l–1) inhibited the basolateral K+ conductance and depolarized a Vbl of –64±4 mV by Key words: amphibian, Ba2+, Bufo bufo, collecting duct, collecting 30±6 mV (N=8). Luminal K+ steps (3 to 20 mmol l–1) tubule, K+ conductance, K+ secretion, kidney, mesonephros, ouabain, demonstrated a K+ conductance in the apical cell toad. Introduction The modern forms of amphibians, the Lissamphibia, and collecting ducts – here referred to as the collecting duct include three groups: frogs (Anura), salamanders (Urodela) system – takes part in the final adjustment of the urine. and caecilians (Gymnophiona). In many respects amphibians Most studies on amphibian renal tubules have been carried span the evolutionary gap between aquatic vertebrates and out on aquatic urodeles, because they have a large tubule fully terrestrial tetrapods. Within Amphibia today we find diameter and large cell size (Richards and Walker, 1937; forms that are fully aquatic throughout their life cycle, as well Stoner, 1977). In particular, the kidney of Amphiuma has been as forms that have adapted to the terrestrial environment. Most used as a model for vertebrate distal tubule transport studies amphibians are, however, still dependent on freshwater for (for a review, see Dietl and Stanton, 1993). Based on data reproduction and the development of larvae. The different life obtained mainly from urodeles, the collecting tubules have modes pose a challenge to the osmoregulatory epithelia of been shown to display a lumen-negative voltage, to reabsorb these animals. The mesonephros, the functional kidney of Na+ and to secrete K+ (Horisberger et al., 1987; Hunter et al., adult amphibians, is one of the organs that participates in 1987; Stoner, 1977; Wiederholt et al., 1971). However, little regulation of the salt and water balance, as well as the is known about the function of the collecting tubule and acid–base balance. especially the collecting ducts of anuran amphibians. The aim The structural and functional unit of the kidney, the nephron, of our study was to characterize K+ transport by the cells within can in the amphibian mesonephros be divided into seven these tubule segments of a terrestrial anuran, the common morphological and functional distinct sections: Malpighian European toad Bufo bufo. For this purpose we isolated and corpuscle, neck segment, proximal tubule, intermediate perfused tubules in vitro and impaled cells with conventional segment, early distal tubule, late distal tubule and, finally, the microelectrodes. collecting tubule, which opens into collecting ducts that lead Since the early work by Richards and Walker (1937), who the urine to the ureter (Dantzler, 1992; Dietl and Stanton, 1993; introduced the micropuncture technique in renal tubules Hentschel and Elger, 1989; Møbjerg et al., 1998). The from kidneys of amphibians, several investigators have heterocellular epithelium constituting the collecting tubules demonstrated the ability of the distal nephron from urodele 898 N. Møbjerg, E. H. Larsen and I. Novak amphibians to secrete K+ (Bott, 1962; Garland et al., 1975; USA). The K+ levels in the urine samples were measured on a Wiederholt et al., 1971). These data were subsequently Dionex DX-120 Ion Chromatograph (Dionex Corporation, CA, confirmed in a study on isolated and perfused tubules from the USA). distal nephron of both urodele and anuran amphibians (Stoner, Collecting tubules and collecting ducts were dissected from 1977). In an electrophysiological study on in vitro perfused the mesonephros of adult toads. The morphology and collecting tubules from Amphiuma sp., it was subsequently ultrastructure of the mesonephric kidney of Bufo bufo has been shown that the heterocellular epithelium of the collecting described in a previous study (Møbjerg et al., 1998). Only tubule secretes K+ (Horisberger et al., 1987). These workers, female toads were used for the present study, as they lack the however, could not find a significant K+ conductance in the communication between the mesonephric kidney and gonadal luminal cell membrane of the collecting tubule of Amphiuma, system, which in males is used for sperm transport. and therefore argued that K+ secretion could not occur across The animals were killed by decapitation and the kidneys the luminal membrane (Horisberger et al., 1987; Hunter et al., were immediately excised and cut into transverse sections 1987). Thus, in the light of these observations it has been approximately 1 mm thick using razor blades. The dissection postulated that K+ secretion by the amphibian collecting tubule medium contained (in mmol l–1): 96.8 Na+, 3.0 K+, 1.8 Ca2+, 2+ – – 2– 2– occurs via a passive, paracellular mechanism (Dietl and 1.0 Mg , 81.6 Cl , 20.0 HCO3 , 1.0 SO4 , 0.8 HPO4 , 0.2 + – Stanton, 1993). Therefore, it was believed that K secretion in H2PO4 , 5.5 glucose, 3.3 glycine, 0.4 PVP (polyvinyl- amphibians differs from secretion by the cortical collecting pyrolidone), 5.0 Hepes, titrated to pH 7.8 with NaOH. tubule in mammals (for reviews, see Giebisch, 1998; Palmer, Tubules were identified under a stereomicroscope during 1999). free-hand dissection with sharpened forceps and needles Nevertheless, Stoner and Viggiano (1998) recently used (Terumo, Neolus 0.4×20 mm) at 6 °C. Collecting ducts were patch clamp and characterised maxi K+ channels from cell- isolated from the dorsal zone of the kidney beneath the attached patches on the apical membrane of the everted connective tissue capsule. Collecting tubules run ventrally collecting tubule of aquatic-phase tiger salamanders from the transition zone with the ducts. The collecting ducts Ambystoma tigrinum. K+ adaptation in the salamanders caused had an outer tubule diameter of approximately 60–70 µm a tenfold increase in the number of detectable maxi K+ (Fig. 1A,B). The outer diameter of the collecting tubules was channels. After K+ adaptation the maxi K+ channels approximately 50–60 µm (Fig. 1C,D). The dissected length of contributed to the ability of the collecting tubule in A. tigrinum the tubules was in the range 300–500 µm. to secrete K+ (Stoner and Viggiano, 1999). Stoner and The isolated tubules were transferred in a small volume of Viggiano (2000) have also provided evidence for an apical dissection medium to a bath chamber mounted on an inverted intermediate conductance, amiloride-insensitive, non-specific microscope equipped with Nomarski optics (Zeiss, Axiovert cation channel in the collecting tubule of the tiger salamander. 135 TV) and perfused in vitro at room temperature. The control Since the channel is observed most frequently in K+-adapted solution, which was used to perfuse the bath and the lumen of animals it may be important in K+ secretion. the tubules, consisted of (in mmol l–1): 101.8 Na+, 3.0 K+, 1.8 + 2+ 2+ – – 2– 2– These contradictory findings on the mechanism by which K Ca , 1.0 Mg , 81.6 Cl , 25.0 HCO3 , 1.0 SO4 , 0.8 HPO4 , – is secreted by the collecting tubule led us to explore the means 0.2 H2PO4 , equilibrated with 1.8 % CO2 in O2, pH 7.8. In high of K+ transport by the collecting duct system of the [K+] solutions, the K+ concentration was raised to 20 mmol l–1 mesonephric kidney of Bufo bufo, an anuran species that in its by equimolar substitution with Na+. In experiments with Ba2+, –1 adult life is fully adapted to the terrestrial environment. 1 mmol l BaCl2 was added to the control solution, or the In the present study on isolated and perfused collecting high [K+] solution. Ouabain and furosemide were used in tubules and collecting ducts, microelectrode recordings control solution at a final concentration of 1 mmol l–1 and demonstrate the presence of a large K+ conductance in the 10–5 mmol l–1, respectively. basolateral cell membrane. Furthermore an apical K+ In order to hold the concentric pipettes used for tubule conductance is present in both collecting tubules and collecting perfusion we used the system (Luigs & Neumann, Germany) ducts. Thus, this study provides evidence that is in agreement described by Greger and Hampel (1981) for in vitro perfusion with a transcellular secretion of K+ in the collecting duct of isolated renal tubules, which was modified from the original system of the toad.
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