Exp Clin Endocrinol Diabetes 2010; 118(5): 304-309
DOI: 10.1055/s-0029-1233452
Article

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

Insulin Alters the Permeability of Sheep Pleura

V. K. Kouritas1 , C. Hatzoglou1 , M. Ioannou2 , K. I. Gourgoulianis3 , P. A. Molyvdas1
  • 1Department of Physiology, Medical School, University of Thessaly, Larissa, Greece
  • 2Department of Histopathology, Larissa University Hospital, Larissa, Greece
  • 3Department of Thoracic diseases, Larissa University Hospital, Larissa, Greece
Further Information

Publication History

received 23.11.2008 first decision 06.06.2009

accepted 24.06.2009

Publication Date:
23 October 2009 (online)

Abstract

Aim: Insulin promotes ion transportation across epithelia, mainly kidneys, leading to water and electrolyte abnormalities, possibly causing ‘insulin oedema syndrome’, which rarely presents as pleural effusion. Direct stimulation of sheep pleura by insulin and the possible electrophysiology mechanisms involved were investigated.

Material and Methods: Sheep visceral and parietal pleural specimens were mounted between Ussing chambers. Insulin solutions (10−9 to 10−5 M), L-NAME, Nitroprussid sodium, amiloride and ouabain were used. Trans-mesothelial Resistance was determined. Immunohistochemistry for presence of Insulin Receptors was performed.

Results: Insulin increased Trans-mesothelial Resistance within 1st minute when added mesothelially of visceral (p=0.008) and parietal pleura (p=0.046) for concentrations higher than 10−7 M. L-NAME or Nitroprussid sodium didn’t but amiloride and ouabain inhibited insulin's effect. Immunohistochemistry revealed the presence of Insulin Receptors.

Conclusion: Insulin changes the permeability of sheep pleura by altering its electrophysiology and may interfere in pleural effusion formation. Involvement of Insulin Receptors may be suggested.

References

  • 1 Aldoretta PW, Carver TD, Hay Jr WW. Maturation of glucose-stimulated insulin secretion in fetal sheep.  Biol Neonate. 1998;  73 375-386
  • 2 Blazer-Yost BL, Cox M, Furlanetto R. Insulin and IGF-I receptor mediated Na+ transport in toad urinary bladders  Am J Physiol. 1989;  257 612-620
  • 3 Blazer-Yost BL, Xuehong L, Helman SI. Hormonal regulation of ENaCs: insulin and aldosterone.  Am J Physiol Cell Physio. 1998;  274 1373-1379
  • 4 Carstens S, Danielsen G, Guldhammer B. et al . Transport of insulin across rabbit nasal mucosa in vitro induced by didecanoyl-L-a-P-tidylcholine.  Diabetes. 1993;  42 1032-1040
  • 5 Carver TD, Anderson SM, Aldoretta PA. et al . Glucose suppression of insulin secretion in chronically hyperglycemic fetal sheep.  Pediatr Res. 1995;  38 754-762
  • 6 Chelliah A, Burge MR. Insulin edema in the twenty-first century: review of the existing literature.  J Invest Med. 2004;  52 104-108
  • 7 Cox M, Guzzo J, Shook A. et al . Effects of tetracyclines on aldosterone- and insulin- mediated Na+ transport in the toad urinary bladder  Biochim Biophys Acta. 1979;  552 162-168
  • 8 Cox M, Singer I. Insulin mediated Na+ transport in the toad urinary bladder  Am J Physiol. 1977;  232 270-277
  • 9 Crabbe J, Fanestil DD, Peletier M. et al . Effect of ouabain on sodium transport across hormone-stimulated toad bladder skin.  Pflugers Arch. 1969;  347 275-292
  • 10 del Valle HL, Lascano LC, Negroni JA. et al . Absence of ischemic preconditioning in diabetic sheep hearts: Role of sarcolemmal KATP channels dysfunction.  Mol Cell Biochem. 2003;  249 21-30
  • 11 Dellow WJ, Chambers ST, Barrell GK. et al . Glycine betaine excretion is not directly linked to plasma glucose concentrations in hyperglycaemia.  Diabetes Res Clin Pract. 2001;  52 165-169
  • 12 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
  • 13 Harding JE, Bloomfield FH. Prenatal treatment of intrauterine growth restriction: lessons from the sheep model.  Pediatr Endocrinol Rev. 2004;  2 182-192
  • 14 Hatzoglou CH, Gourgoulianis KI, Hatzoglou A. et al . Rapid effects of 17β-estradiol and progesterone on sheep visceral and parietal pleurae via a nitric oxide pathway.  J Appl Physiol. 2002;  93 752-758
  • 15 Hatzoglou CH, Gourgoulianis KI, Molyvdas PA. Effects of nitroprussid sodium, ouabain and amiloride on electrical potential profile of isctrical potential profile.  uabain and amiloride on electrical potential profile of isolated sheep pleura. J Appl Physiol. 2001;  90 1565-1569
  • 16 Herrera FC. Effect of insulin on short-circuit current and sodium transport across toad urinary bladder.  Am J Physiol. 1965;  209 819-824
  • 17 Kahn A, Seidel C, Allen JC. et al . Insulin reduces contraction and intracellular calcium concentration in vascular smooth muscle.  Hypertension. 1993;  22 735-742
  • 18 Kalambokis GN, Tsatsoulis AA, Tsianos EV. The edematogenic properties of insulin.  Am J Kid Dis. 2004;  44 575-590
  • 19 Kosior-Korzecka U, Bobwiec R, Lipecka C. Fasting induced changes in ovulation rate, plasma leptin, gonadotrophins, GH, IGF-I and insulin concentrations during oestrus in ewes.  J Vet Med Physiol Pathol Clin Med. 2006;  53 5-11
  • 20 Kouritas VK, Hatzoglou CH, Foroulis CN. et al . Human parietal pleura present electrophysiology variations according to location in pleural cavity.  ICVTS. 2008;  7 544-547
  • 21 Lai-Fook SJ. Pleural mechanics and fluid exchange.  Physiol Rev. 2004;  84 385-410
  • 22 Lee P, Kinsella J, Borkman M. et al . Bilateral pleural effusions, ascites, and facial and peripheral oedema in a 19-year-old woman 2 weeks following commencement of insulin lispro and detemir – an unusual presentation of insulin oedema.  Diabet Med. 2007;  24 1282-1285
  • 23 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
  • 24 Molina RD, Carver TD, Hay Jr WW. Ontogeny of insulin effect in fetal sheep.  Pediatr Res. 1993;  34 654-660
  • 25 Nofziger C, Chen L, Shane MA. et al . PPARgamma agonists do not directly enhance basal or insulin-stimulated Na+ transport via the epithelial Na+channel  Pflugers Arch. 2005;  451 445-453
  • 26 Papayianni M, Gourgoulianis KI, Molyvdas PA. Insulin NO-dependent action on airway smooth muscles.  Nitric oxide. 2001;  5 72-76
  • 27 Ribiere C, Jaubert AM, Sabourault D. et al . Insulin stimulates nitric oxide production in rat adipocytes.  Biochem Biophys Res Commun. 2002;  291 394-399
  • 28 Siegel B, Civan MM. Aldosterone and insulin effects on driving force of Na+ pump on toad bladder  Am J Physiol. 1976;  230 1603-1608
  • 29 Smet PD, Erlij D, Van Driessche W. Insulin effects on ouabain binding in A6 renal cells.  Pflugers Arch. 1997;  434 11-18
  • 30 Sugahara K, Freidenberg GR, Mason RJ. Insulin binding and effects on glucose and transepithelial transport by alveolar type II cells.  Am J Physiol. 1984;  247 472-477
  • 31 Tack CJ, Lutterman JA, Vervoort G. et al . Activation of the sodium-potassium pump contributes to insulin-induced vasodilation in humans.  Hypertension. 1996;  28 426-432
  • 32 Wilkinson JS. Spontaneous diabetes in domestic animals.  Vet Rev Annot. 1957;  3 69-96
  • 33 Yamamoto A, Tanaka H, Okumura S. et al . Evaluation of insulin permeability and effects of absorption enhancers on its permeability by an in vitro pulmonary epithelial system using Xenopus pulmonary membrane.  Biol Pharm Bull. 2001;  24 385-389
  • 34 Zenda T, Murase Y, Yoshida I. et al . Does the use of insulin in a patient with liver dysfunction increase water retention in the body, i.  e. cause insulin oedema? Eur J Gastroenterol Hepatol. 2003;  15 545-549

1 Ohm's law correlates the potential difference (U) at the edges of a conductor with the current (I) that flows the conductor and with conductor's resistance (R). I=U/R. For pleural membrane U=PD TM which is being measured, I=current of viable intensity applied on tissue (i. e. 300 μ Ampere) and R=R after correction for S.I. units and the surface of the tissue exposed to solutions (in Ohm or Ωcm2).

Correspondence

V. K. KouritasMD, PhD 

Department of Physiology

Medical School University of Thessaly

New Buildings

41 100 Mezourlo PO Box 1400

Larissa, Greece

Phone: +30 2410 68 55 56

Fax: +30 2410 67 02 40

Email: kouritas@otenet.gr

    >