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

Orginal Paper

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 (> 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.

Keywords

Vasotocin Antidiuretic hormone (ADH) Na+/K+-pump V2 receptor/cAMP pathway Frog skin 

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

  1. 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 33:293–313PubMedCrossRefGoogle Scholar
  2. Blazer-Yost BL, Nofziger C (2005) Phosphoinositide lipid second messengers: new paradigms for transepithelial signal transduction. Pflügers Arch-Eur J Physiol 450:75–82CrossRefGoogle Scholar
  3. 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 153:233–239PubMedCrossRefGoogle Scholar
  4. 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 511:235–243PubMedCrossRefGoogle Scholar
  5. 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 145:99–106PubMedGoogle Scholar
  6. Cox TC, Alvarado RH (1983) Nystatin studies of the skin of larval Rana catesbeiana. Am J Physiol 244(13):R58–R65Google Scholar
  7. Deyrup IJ (1964) Water balance and kidney. In: Moore JA (ed) Physiology of the amphibia. Academic Press, New York, pp 251–328Google Scholar
  8. 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–F53PubMedGoogle Scholar
  9. Farquhar MG, Palade GE (1965) Cell junctions in amphibian skin. J Cell Biol 26:263–291PubMedCrossRefGoogle Scholar
  10. Féraille E, Doucet A (2001) Sodium-potassium-adenosinetriphosphatase-dependent sodium transport in the kidney: hormonal control. Physiol Rev 81:345–418PubMedGoogle Scholar
  11. 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 151:252–258CrossRefGoogle Scholar
  12. 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 270:16082–16088PubMedCrossRefGoogle Scholar
  13. Helman SI, Cox TC, Van Driessche W (1983) Hormonal control of apical membrane Na transport in epithelia. J Gen Physiol 82:201–220PubMedCrossRefGoogle Scholar
  14. 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–F511PubMedGoogle Scholar
  15. Koefoed-Johnsen V, Ussing HH (1958) The nature of the frog skin potential. Acta Physiol Scand 42:298–308PubMedCrossRefGoogle Scholar
  16. 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 132:485–498PubMedCrossRefGoogle Scholar
  17. 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 140:86–93PubMedCrossRefGoogle Scholar
  18. 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–F829PubMedGoogle Scholar
  19. Lichtenstein NS, Leaf A (1965) Effect of amphotericin B on the permeability of the toad bladder. J Clin Invest 44:1328–1343PubMedCrossRefGoogle Scholar
  20. 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
  21. Martinez-Palomo A, Erlij D, Bracho H (1971) Localization of permeability barriers in the frog skin epithelium. J Cell Biol 50:277–287PubMedCrossRefGoogle Scholar
  22. Marunaka Y (1997) Hormonal and osmotic regulation of NaCl transport in renal distal nephron epithelium. Jpn J Physiol 47:499–511PubMedCrossRefGoogle Scholar
  23. Marunaka Y, Eaton DC (1991) Effects of vasopressin and cAMP on single amiloride-blockable Na channels. Am J Physiol Cell Physiol 260:C1071–C1084Google Scholar
  24. 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–F1039PubMedCrossRefGoogle Scholar
  25. Nielsen R (1997) Correlation between transepithelial Na+ transport and transepithelial water movement across isolated frog skin (Rana esculenta). J Membr Biol 159:61–69PubMedCrossRefGoogle Scholar
  26. Rossier BC (2002) Hormonal regulation of the epithelial sodium channel ENaC: N or Po? J Gen Physiol 120:67–70PubMedCrossRefGoogle Scholar
  27. 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 89:1496–1500PubMedCrossRefGoogle Scholar
  28. Shane MA, Nofziger C, Blazer-Yost BL (2006) Hormonal regulation of the epithelial Na+ channel: from amphibians to mammals. Gen Comp Endocrinol 147:85–92PubMedCrossRefGoogle Scholar
  29. 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–C1152Google Scholar
  30. 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 555:355–364PubMedCrossRefGoogle Scholar
  31. 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 151:325–331PubMedCrossRefGoogle Scholar
  32. 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–F879Google Scholar
  33. Uchiyama M, Konno N (2006) Hormonal regulation of ion and water transport in anuran amphibians. Gen Comp Endocrinol 147:54–61PubMedCrossRefGoogle Scholar
  34. 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 491:111–120PubMedGoogle Scholar

Copyright information

© Springer-Verlag 2008

Authors and Affiliations

  1. 1.Department of Physiology, School of MedicineSaitama Medical UniversityIruma-gunJapan
  2. 2.Department of Biochemistry, School of MedicineSaitama Medical UniversityIruma-gunJapan

Personalised recommendations