Summary
The short-circuit current (SCC) across isolated skin from bullfrog larvae in developmental stage XXI was small and insensitive to amiloride. Overnight incubation of this tissue with 10-6 M aldosterone stimulated the SCC from 1.35±0.55 to 14.55±4.12 μA·cm-2 with 11.18±4.46 μA·cm-2 being blocked by 100 μM amiloride. Histologic examination of aldosterone-treated skins revealed a separation of the apical cell layer from the underlying epidermis that was not seen in untreated preparations. The onset of amiloride-sensitive Na+ transport thus coincided with the exposure of the apical surface of newly differentiated epithelial cells. Similar results were obtained with skin from stage XXI larvae whose rate of metamorphosis had been stimulated by 10 μg·l-1 thyroxine (T4) but not with skin from T4-treated larvae in stages XIX and XX. Fluctuation analysis of the amiloride-sensitive SCC of the above preparations failed to show a consistent Lorentzian component in the power-density spectrum. Fluctuation analysis was possible on skins from larvae whose development had been accelerated by 7–9 days treatment with 10 μg·l-1 triiodothyronine (T3). Aldosterone treatment of these tissues resulted in a significant increase in Na+ channel density.
Similar content being viewed by others
Abbreviations
- ASCC :
-
component of the short-circuit current (μA·cm-2) that is blocked by amiloride
- fc :
-
frequency (Hz) at which the magnitude of the Lorenzian component of the power spectra is reduced by half
- i :
-
current (pA) through individual amiloride-sensitive Na+ channels
- I Na+ :
-
amiloride-sensitive short-circuit current (μA·cm-2) that remains after treatment with a given amiloride concentration
- k 01 :
-
the rate constant (s-1·μM-1) for the association of amiloride with Na+ channels
- k 10 :
-
rate constant (s-1) for the dissociation of amiloride from Na+ channels
- K b :
-
magnitude of the power spectrum (A2·s·cm-2) at a frequency of 1 Hz
- KSCC :
-
short-circuit (μA·cm-2) current with K+ as the primary mucosal cation
- M :
-
density of amiloride-sensitive Na+ channels in the apical cell membrane
- SCC :
-
short-circuit current (μA·cm-2)
- S (f) :
-
magnitude of the power spectra (A2·s·cm-2) at a given frequency
- S 0 :
-
the magnitude of the plateau region of the Lorentzian component of the power spectra (A2·s·cm-2)
- T 3 :
-
Triiodothyronine
- T 4 :
-
Thyroxine
References
Abramcheck FJ, Van Driessche W, Helman SI (1985) Autoregulation of apical membrane Na+ permeability of tight epithelia: noise analysis with amiloride and CGS 4270. J Gen Physiol 85:555–582
Benos DJ, Mandel LJ, Balaban RS (1979) On the mechanism of the amiloride-sodium entry site interaction in anuran skin epithelia. J Gen Physiol 73:307–320
Brown SC, Savage LM, Brown PS (1988) Electrophysiology of newt skin: responses to salt-depletion, aldosterone, arginine vasotocin, and epinephrine. Comp Biochem Physiol 91A:715–719
Buron MI, Navas P (1988) Thyroxine specifically stimulates anuran larvae epidermal sodium pump during metamorphosis. Comp Biochem Physiol 91A:693–695
Cox TC, Alvarado RH (1979) Electrical and transport characteristics of skin of larval Rana catesbeiana. Am J Physiol 237:R74-R79
De Wolf I, Van Driessche W (1986) Voltage-dependent Ba2+ block of K+ channels in apical membrane of frog skin. Am J Physiol 251:C696–706
Galigher AE, Kozloff EN (1971) Essentials of practical microtechnique, 2nd ed. Lea and Febiger, Philadelphia, p 531
Garty H (1986) Mechanisms of aldosterone action in tight epithelia. J Membr Biol 90:193–205
Hillyard SD, Van Driessche W (1989) Effect of amiloride on the poorly-selective cation channel of larval bullfrog skin. Am J Physiol 256:C168-C174
Hillyard SD, Zeiske W, Van Driessche W (1982a) A fluctuation analysis study of the development of amiloride sensitive Na+ transport in the skin of larval bullfrogs (Rana catesbeiana). Biochim Biophys Acta 692:455–461
Hillyard SD, Zeiske W, Van Driessche W (1982b) Poorly selective cation channels in the skin of the larval frog (<stage XIX). Pflügers Arch 394:287–293
Hviid-Larsen E (1971) The relative contributions of sodium and chloride ions to the conductance of toad skin in relation to shedding of the stratum corneum. Acta Physiol Scand 81:254–263
Kikuyama SM, Suzuki R, Iwamuro S (1986) Elevation of plasma aldosterone levels of tadpoles at metamorphic climax. Gen Comp Endocrinol 63:186–190
Krug EC, Honn KV, Battista J, Nicoll CS (1983) Corticosteroids in serum of Rana catesbeiana during development and metamorphosis. Gen Comp Endocrinol 55:232–241
Lindemann B, Van Driessche W (1977) Sodum-specific membrane channels of frog skins are pores: current fluctuations reveal high turnover. Science 195:292–294
Palmer LG, Li J-Y, Lindemann B, Edelman I (1982) Aldosterone control of the density of sodium channels in the toad urinary bladder. J Membr Biol 64:91–102
Porter GA (1971) The actions of aldosterone on transepithelial sodium transport in siolated ventral toad skin. Gen Comp Endocrinol 16:443–451
Robinson DA, Heintzelman MB (1987) Morphology of ventral epidermis of Rana catesbeiana during metamorphosis. Anat Rec 217:305–317
Robinson DA, Mills JW (1987a) Ouabain binding in tadpole ventral skin. I. Kinetics and effect on intracellular ions. Am J Physiol 253:R402-R409
Robinson DA, Mills JW (1987b) Ouabain binding in tadpole ventral skin. II. Localization of Na pump sites. Am J Physiol 253:R410-R417
Takada M (1990) Differentiation of frog skin active transport during metamorphosis is induced by thyroid hormone. Gen Comp Endocrinol 77:442–447
Taylor RE, Barker SB (1965) Transepidermal potential difference: development in anuran larvae. Science 148:1612–1613
Taylor AC, Kollros JJ (1946) Stages in the normal development of Rana pipiens larvae. Anat Rec 94:7–23
Van Driessche W, Gullentops K (1982) Conductance fluctuation analysis in epithelia. In: Techniques in cellular physiology. Elsevier/North Holland, Amsterdam, pp 1–13
Van Driessche W, Lindemann B (1978) Low-noise amplification of voltage and current fluctuations arising in epithelia. Rev Sci Instr 49:52–57
Van Driessche W, Zeiske W (1985) Ca2+-sensitive, spontaneously fluctuating, cation channels in the apical membrane of the adult frog skin epithelium. Pflügers Arch 405:250–259
Weed IG (1934) Cytological studies of the epidermis of Rana pipiens and Rana climitans tadpoles with special references to the figures of Eberth. J Morphol 56:213–229
White BA, Nicoll CS (1981) Hormonal control of amphibian metamorphosis. In: Gilbert LI, Frieden E (eds) Metamorphosis is a problem in development. Plenum, New York London, pp 363–396
Author information
Authors and Affiliations
Rights and permissions
About this article
Cite this article
Hillyard, S.D., Van Driessche, W. Development of aldosterone-stimulation of short-circuit current across larval frog skin. J Comp Physiol B 161, 257–263 (1991). https://doi.org/10.1007/BF00262306
Accepted:
Issue Date:
DOI: https://doi.org/10.1007/BF00262306