Exp Clin Endocrinol Diabetes 2010; 118(5): 328-332
DOI: 10.1055/s-0030-1247543
Article

© J. A. Barth Verlag in Georg Thieme Verlag KG Stuttgart · New York

Role of Electrolytes and Glucose in the Insulin-Induced Electrochemical Effect in Sheep Pleura

V. K. Kouritas1 , C. H. Hatzoglou1 , K. I. Gourgoulianis2 , P. A. Molyvdas1
  • 1Department of Physiology, Medical School of Larissa, University of Thessaly, Greece
  • 2Department of Thoracic Diseases, Larissa University Hospital, Greece
Further Information

Publication History

received 26.09.2009 first decision 09.01.2010

accepted 15.01.2010

Publication Date:
16 February 2010 (online)

Abstract

Aim: Insulin induces electrochemical alterations in sheep visceral and parietal pleura, an effect abolished by the Na+-channel blocker amiloride and the Na+-K+ pump inhibitor ouabain. The aim of this study was to further investigate the role of different electrolytes and glucose in these electrochemical changes.

Materials and methods: Sheep pleural specimens were mounted in Ussing chambers. Insulin (10−7M) was added mesothelially in Na+, K+, Ca2+-free, low H+ and glucose solutions. In other experiments, specimens were pretreated with K+ and Ca2+-free Krebs solutions. Trans-mesothelial Resistance was determined.

Results: Insulin did not increase Trans-mesothelial Resistance of visceral and parietal pleura in K+-free (p=0.008 and p=0.028 respectively), Ca2+-free (p=0.006 and p=0.012 respectively) and low glucose (p=0.009 and p=0.03 respectively) solutions. This effect was totally inhibited in Na+-free solutions or in specimens pretreated with Ca2+ -free Krebs solution and partially inhibited, when low H+ solutions were used (p=0.042 for visceral and p=0.045 for parietal).

Conclusion: Insulin-induced electrochemical changes in sheep pleura are mainly associated with alterations in Na+ and Ca2+ concentrations. Since amiloride and ouabain abolish these electrochemical changes, it may be suggested that insulin could influence the pleural fluid recycling, mainly via the Na+ transportation system, irrespective of the glucose content.

References

  • 1 Blazer-Yost BL, Cox M, Furlanetto R. Insulin and IGF-I receptor mediated Na+ transport in toad urinary bladders.  Am J Physiol Cell Physiol. 1989;  257 C612-C620
  • 2 Blazer-Yost BL, Shah N, Jarett L. et al . Insulin and IGF-I receptors in a model renal epithelium: receptor localization and characterization.  Biochem Int. 1992;  28 143-153
  • 3 Blazer-Yost BL, Liu X, Helman SI. Insulin stimulated Na+ transport is mediated by increase of apical Na+ channels and not open probability in control and aldosterone prestimulated A6 epithelia (Abstract).  FASEB J. 1996;  10 A78
  • 4 Blazer-Yost BL, Xuehong L, Helman SI. Hormonal regulation of ENaCs: insulin and aldosterone.  Am J Physiol Cell Physio. 1998;  274 1373-1379
  • 5 Clausen T, Flatman JA. Effects of insulin and epinephrine on Na+-K+ and glucose transport in soleus muscle.  Am J Physiol. 1987;  252 E492-E499
  • 6 Cox M, Singer I. Insulin mediated Na+ transport in the toad urinary bladder.  Am J Physiol. 1977;  232 F270-F277
  • 7 De Smet P, Erlij D, Van Driessche W. Insulin effects on ouabain binding in A6 renal cells.  Pflugers Arch. 1997;  434 11-18
  • 8 De Smet P, Simaels J, Van Driessche W. Regulatory volume decrease in a renal distal tubular cell line (A6). II. Effect of Na+ transport rate.  Pflugers Arch. 1995;  430 945-953
  • 9 Deachapunya C, Palmer-Densmore M, O’Grady SM. Insulin Stimulates Transepithelial Sodium Transport by Activation of a Protein Phosphatase that Increases Na-K ATPase Activity in Endometrial Epithelial Cells.  JGP. 1999;  114 561-574
  • 10 Erlij D, De Smet P, Van Driessche W. Effect of insulin on area and Na+ channel density of apical membrane of cultured toad kidney cells.  Am J Physiol. 1994;  481 533-542
  • 11 Féraille E, Carranza ML, Rousselot M. et al . Insulin enhances sodium sensitivity of Na-K-ATPase in isolated rat proximal convoluted tubule.  Am J Physiol. 1994;  267 F55-62
  • 12 Féraille E, Carranza ML, Rousselot M. et al . Modulation of Na+, K(+)-ATPase activity by a tyrosine phosphorylation process in rat proximal convoluted tubule.  J Physiol. 1997;  498 99-108
  • 13 Féraille E, Rousselot M, Rajerison R. et al . Effect of insulin on Na+, K(+)-ATPase in rat collecting duct.  J Physiol. 1995;  488 171-180
  • 14 Gesek FA, Schoolwerth AC. Insulin increases Na(+)-H+ exchange activity in proximal tubules from normotensive and hypertensive rats.  Am J Physiol. 1991;  260 F695-F703
  • 15 Gosmanov AR, Fan Z, Mi X. et al . ATP-sensitive potassium channels mediate hyperosmotic stimulation of NKCC in slow-twitch muscle.  Am J Physiol Cell Physiol. 2004;  286 C586-C595
  • 16 Hatzoglou CH, Gourgoulianis KI, Molyvdas PA. Effects of SNP, ouabain and amiloride on electrical potential profile of isolated sheep pleura.  J Appl Physiol. 2001;  90 1565-1569
  • 17 Hundal HS, Marette A, Mitsumoto Y. et al . Insulin induces translocation of the α-2 and β-1 subunits of the Na+, K+-ATPase from intracellular compartments to the plasma membrane in mammalian skeletal muscle.  J Biol Chem. 1992;  267 5040-5043
  • 18 Ito O, Kondo Y, Takahashi N. et al . Insulin stimulates NaCl transport in isolated perfused MTAL of Henle's loop of rabbit kidney.  Am J Physiol. 1994;  267 F265-70
  • 19 Kahn AM, Allen JC, Seidel CL. et al . Insulin inhibits serotonin-induced Ca2+ influx in vascular smooth muscle.  Circulation. 1994;  90 384-390
  • 20 Kaloyianni M, Bourikas D, Koliakos G. The effect of insulin on Na+-H+ antiport activity of obese and normal subjects’ erythrocytes.  Cell Physiol Biochem. 2001;  11 253-258
  • 21 Kouritas VK, Hatzoglou C, Foroulis CN. et al . Low glucose level and low pH alter the electrochemical function of human parietal pleura.  Eur Respir J. 2007;  30 354-357
  • 22 Kouritas VK, Hatzoglou CH, Ioannou M. et al . Insulin alters the permeability of sheep pleura.  Exp Clin Endocrinol Diabetes. 2009;  73E Article in Press
  • 23 Lai-Fook SJ. Pleural mechanics and fluid exchange.  Physiol Rev. 2004;  84 385-410
  • 24 Lyoussi B, Crabbé J. Effects of dexamethasone on (Na+/K+)-ATPase and other parameters related to transepithelial Na+ transport by amphibian renal distal cells (A6) in culture.  J Steroid Biochem Mol Biol. 1996;  59 333-338
  • 25 Marunaka Y, Hagiwara N, Tohda H. Insulin activates single amiloride blockable Na channels in a distal nephron cell line (A6).  Am J Physiol Renal Fluid Electrolyte Physiol. 1991;  263 F392-F400
  • 26 Marunaka Y, Niisato N, O’Brodovich H. et al . Role of Ca2+ and protein tyrosine kinase on insulin action on cell volume via Na+ and K+ channels and Na+/K+/2Cl- cotransporter in fetal rat alveolar type II pneumocyte.  J Memb Biol. 1999;  168 91-101
  • 27 Marunaka Y. Amiloride-blockable Ca2+-activated Na+-permeant channels in the fetal distal lung epithelium.  Pflugers Arch. 1996;  431 748-756
  • 28 Marunaka Y. The sensitivity of insulin-stimulated and basal Na efflux to ouabain in frog skeletal muscle cells.  Gen Pharmacol. 1991;  22 949-954
  • 29 McKenna MJ, Gissel H, Clausen T. Effects of electrical stimulation and insulin on Na+-K+-ATPase ([3H]ouabain binding) in rat skeletal muscle.  J Physiol. 2003;  547 567-580
  • 30 Quintanilla RA, Porras OH, Castro J. et al . Cytosolic [Ca(2+)] modulates basal GLUT1 activity and plays a permissive role in its activation by metabolic stress and insulin in rat epithelial cells.  Cell Calcium. 2000;  28 97-106
  • 31 Record RD, Johnson M, Lee SY. et al . Aldosterone and insulin stimulate amiloride-sensitive sodium transport in A6 cells by additive mechanisms.  Am J Physiol Cell Physiol. 1996;  271 C1079-C1084
  • 32 Sage SO, van Breemen C, Cannell MB. Sodium-calcium exchange in cultured bovine pulmonary artery endothelial cells.  J Physiol. 1991;  440 569-580
  • 33 Sargeant RB, Liu Z, Klip A. Action of insulin on Na+-K+ ATPase and the Na+-K+-2Cl- cotransporter in 3T3-L1 adipocytes.  Am J Physiol. 1995;  269 C217-C225
  • 34 Schoen HF, Erlij D. Basolateral membrane responses to transport modifiers in the frog skin epithelium.  Pflugers Arch. 1985;  405 S33-8
  • 35 Siegel B, Civan MM. Aldosterone and insulin effects on driving force of Na+ pump on toad bladder.  Am J Physiol. 1976;  230 1603-1608
  • 36 Walker TC, Fidelman ML, Watlington CO, Biber TU. Insulin decreases apical membrane resistance in cultured kidney cells (A6).  Biochem Biophys Res Commun. 1984;  124 614-618
  • 37 Witowski J, Breborowicz A, Topley N. et al . Insulin stimulates the activity of Na+/K(+)-ATPase in human peritoneal mesothelial cells.  Perit Dial Int. 1997;  17 186-193

Correspondence

V. K. KouritasMD, PhD 

Department of Physiology

Medical School of Larissa

University of Thessaly

Mezourlo 41 100

PO Box 1400

Larissa

Greece

Phone: +30 2410 655 655

Fax: +30 2410 670 240

Email: kouritas@otenet.gr

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