Abstract
Adult frog skin transports Na+ from the apical to the basolateral side across the skin. Antidiuretic hormone (ADH) is involved in the regulation of Na+ transport in both mammals and amphibians. We investigated the effect of arginine vasotocin (AVT), the ADH of amphibians, on the short-circuit current (SCC) across intact skin and on the basolateral Na+/K+-pump current across apically nystatin-permeabilized skin of the tree frog, Hyla japonica, in which the V2-type ADH receptor is expressed in vitro. In intact skin, 1 pM AVT had no effect on the SCC, but 10 nM AVT was sufficient to stimulate the SCC since 10 nM and 1 μM of AVT increased the SCC 3.2- and 3.4-fold, respectively (P > 0.9). However, in permeabilized skin, AVT (1 μM) decreased the Na+/K+-pump current to 0.79 times vehicle control. Similarly, 500 μM of 8Br-cAMP increased the SCC 3.2-fold, yet 1 mM of 8Br-cAMP decreased the Na+/K+-pump current to 0.76 times vehicle control. Arachidonic acid (10−5 M) tended to decrease the Na+/K+-pump current. To judge from these in vitro experiments, AVT has the potential to inhibit the basolateral Na+/K+-pump current via the V2-type receptor/cAMP pathway in the skin of the tree frog.
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Abbreviations
- ADH:
-
Antidiuretic hormone
- AVT:
-
Arginine vasotocin
- 8Br-cAMP:
-
8-Bromoadenosine 3′, 5′-cyclic monophosphate
- SCC:
-
Short-circuit current
- ENaC:
-
Epithelial sodium channel
- CCD:
-
Cortical collecting duct
References
Acharjee S, Do-Rego J-L, Oh DY, Mon JS, Ahn RS, Lee K, Bai DG, Vaudry H, Kwon HB, Seong JY (2004) Molecular cloning, pharmacological characterization, and histochemical distribution of frog vasotocin and mesotocin receptors. J Mol Endocrinol 33:293–313
Blazer-Yost BL, Nofziger C (2005) Phosphoinositide lipid second messengers: new paradigms for transepithelial signal transduction. Pflügers Arch-Eur J Physiol 450:75–82
Blot-Chabaud M, Coutry NC, Laplace M, Bonvalet J-P, Farman N (1996) Role of protein phosphatase in the regulation of Na+-K+-ATPase by vasopressin in the cortical collecting duct. J Membr Biol 153:233–239
Carranza ML, Rousselot M, Chibalin AV, Bertorello AM, Favre H, Féraille E (1998) Protein kinase A induces recruitment of active Na+, K+-ATPase units to the plasma membrane of rat proximal convoluted tubule cells. J Physiol 511:235–243
Coutry N, Farman N, Bonvalet JP, Blot-Chabau M (1995) Synergistic action of vasopressin and aldosterone on basolateral Na+-K+-ATPase in the cortical collecting duct. J Membr Biol 145:99–106
Cox TC, Alvarado RH (1983) Nystatin studies of the skin of larval Rana catesbeiana. Am J Physiol 244(13):R58–R65
Deyrup IJ (1964) Water balance and kidney. In: Moore JA (ed) Physiology of the amphibia. Academic Press, New York, pp 251–328
Ecelbarger CA, Kim G-H, Terris J, Masilamani S, Mitchell C, Reyes I, Verbalis JG, Knepper MA (2000) Vasopressin-mediated regulation of epithelial sodium channel abundance in rat kidney. Am J Physiol Renal Physiol 279:F46–F53
Farquhar MG, Palade GE (1965) Cell junctions in amphibian skin. J Cell Biol 26:263–291
Féraille E, Doucet A (2001) Sodium-potassium-adenosinetriphosphatase-dependent sodium transport in the kidney: hormonal control. Physiol Rev 81:345–418
Hasumuma I, Sakai T, Nakada T, Toyoda F, Namiki H, Kikuyama S (2007) Molecular cloning of three types of arginine vasotocin receptor in the newt, Cynops pyrrhogaster. Gen Comp Endocrinol 151:252–258
Hayslett JP, Macala LJ, Smallwood JI, Kalghatgi L, Gassala-Herraiz J, Isales C (1995) Vasopressin-stimulated electrogenic sodium transport in A6 cells is linked to a Ca2+-mobilizing signal mechanism. J Biol Chem 270:16082–16088
Helman SI, Cox TC, Van Driessche W (1983) Hormonal control of apical membrane Na transport in epithelia. J Gen Physiol 82:201–220
Kleyman TR, Ernst SA, Coupaye-Gerard B (1994) Arginine vasopressin and forskolin regulate apical cell surface expression of epithelial Na channels in A6 cells. Am J Physiol 266:F506–F511
Koefoed-Johnsen V, Ussing HH (1958) The nature of the frog skin potential. Acta Physiol Scand 42:298–308
Kohno S, Kamishima Y, Iguchi T (2003) Molecular cloning of an anuran V2 type [Arg8] vasotocin receptor and mesotocin receptor: functional characterization and tissue expression in the Japanese tree frog (Hyla japonica). Gen Comp Endocrinol 132:485–498
Konno N, Hyodo S, Takei Y, Matsuda K, Uchiyama M (2005) Plasma aldosterone, angiotensin II, and arginin vasotocin concentrations in the toad, Bufo marinus, following osmotic treatment. Gen Comp Endocrinol 140:86–93
Li D, Belusa R, Nowicki S, Aperia A (2000) Arachidonic acid metabolic pathways regulating activity of renal Na+-K+-ATPase are age dependent. Am J Physiol Renal Physiol 278:F823–F829
Lichtenstein NS, Leaf A (1965) Effect of amphotericin B on the permeability of the toad bladder. J Clin Invest 44:1328–1343
Maejima S, Yamada T, Hamada T, Matsuda K, Uchiyama M (2008) Effects of hypertonic stimuli and arginine vasotocin (AVT) on water absorption response in Japanese treefrog, Hyla japonica. Gen Comp Endocrinol (in press). doi:10.1016/j.ygcen.2008.04.014
Martinez-Palomo A, Erlij D, Bracho H (1971) Localization of permeability barriers in the frog skin epithelium. J Cell Biol 50:277–287
Marunaka Y (1997) Hormonal and osmotic regulation of NaCl transport in renal distal nephron epithelium. Jpn J Physiol 47:499–511
Marunaka Y, Eaton DC (1991) Effects of vasopressin and cAMP on single amiloride-blockable Na channels. Am J Physiol Cell Physiol 260:C1071–C1084
Mordasini D, Bustamante M, Rousselot M, Martin P-Y, Hasler U, Féraille E (2005) Stimulation of Na+ transport by AVP is independent of PKA phosphorylation of the Na–K-ATPase in collecting duct principal cells. Am J Physiol Renal Physiol 289:F1031–F1039
Nielsen R (1997) Correlation between transepithelial Na+ transport and transepithelial water movement across isolated frog skin (Rana esculenta). J Membr Biol 159:61–69
Rossier BC (2002) Hormonal regulation of the epithelial sodium channel ENaC: N or Po? J Gen Physiol 120:67–70
Satoh T, Cohen HT, Katz AI (1992) Intracellular signaling in the regulation of renal Na–K-ATPase. I. Role of cyclic AMP and phospholipase A2. J Clin Invest 89:1496–1500
Shane MA, Nofziger C, Blazer-Yost BL (2006) Hormonal regulation of the epithelial Na+ channel: from amphibians to mammals. Gen Comp Endocrinol 147:85–92
Silver RB, Palmer LG (1989) 8BrcAMP-induced capacitance and transport of H2O and Na in skin and urinary bladder of urodele amphibians. Am J Physiol 256(25):C1145–C1152
Summa S, Camargo SMR, Bauch C, Zecevice M, Verry F (2004) Isoform specificity of human Na+, K+-ATPase localization and aldosterone regulation in mouse kidney cells. J Physiol 555:355–364
Takada M, Hokari S (2007) Prolactin increases Na+ transport across adult bullfrog skin via stimulation of both ENaC and Na+/K+-pump. Gen Comp Endocrinol 151:325–331
Tomita K, Owada A, Iino Y, Yoshiyama N, Shiigai T (1987) Effect of vasopressin on Na–K-ATPase activity in rat cortical collecting duct. Am J Physiol 253(Renal Fluid Electrolyte Physiol 22):F874–F879
Uchiyama M, Konno N (2006) Hormonal regulation of ion and water transport in anuran amphibians. Gen Comp Endocrinol 147:54–61
Urbach V, Van Kerkhove E, Maguire D, Harvey BJ (1996) Rapid activation of KATP channels by aldosterone in principal cells of frog skin. J Physiol 491:111–120
Acknowledgments
All procedures complied with the relevant Japanese law governing animal experimentation (Law no. 105, notification no. 000398). We greatly thank Dr. Suge (Saitama Medical University) for her valuable advice on the statistical analysis.
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Communicated by G. Heldmaier.
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Takada, M., Fujimaki, K. & Hokari, S. Vasotocin has the potential to inhibit basolateral Na+/K+-pump current across isolated skin of tree frog in vitro, via its V2-type receptor/cAMP pathway. J Comp Physiol B 178, 957–962 (2008). https://doi.org/10.1007/s00360-008-0278-4
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DOI: https://doi.org/10.1007/s00360-008-0278-4