Metabolism - Clinical and Experimental
Volume 52, Issue 3 , Pages 273-278 , March 2003

Evidence for a direct effect of captopril on early steps of insulin action in BC3H-1 myocytes

Received 19 February 2001 ,Accepted 19 September 2002.

References 

  1. Uehara M, Kishikawa H, Isami S, et al.  Effect on insulin sensitivity of angiotensin converting enzyme inhibitors with or without sulphydryl group: Bradykinin may improve insulin resistance in dogs and humans. Diabetologia. 1994;37:300–307
  2. Henriksen EJ, Jacob S. Effects of captopril on glucose transport activity in skeletal muscle of obese Zucker rats. Metabolism. 1995;44:267–272
  3. Jacob S, Henriksen EJ, Fogt DL, et al.  Effects of trandolapril and verapamil on glucose transport in insulin-resistant rat skeletal muscle. Metabolism. 1996;45:535–541
  4. Pollare L, Lithell H, Berne C. A comparison of the effects of hydrochlorothiazide and captopril on glucose and lipid metabolism in patients with hypertension. N Engl J Med. 1989;321:868–873
  5. Ferriere M, Lachhkar H, Richard JL, et al.  Captopril and insulin sensitivity. Ann Intern Med. 1985;102:134–135
  6. Gans ROB, Biol HJG, Nauta JJP, et al.  The effect of angiotensin-I converting enzyme inhibition on insulin action in health volunteers. Eur J Clin Invest. 1991;21:527–533
  7. Dietze GJ. Modulation of the action of insulin in relation to the energy state in skeletal muscle tissue: Possible involvement of kinins and prostaglandins. Mol Cell Endocrinol. 1982;25:127–169
  8. Henriksen EJ, Jacob S, Fogt DL, et al.  Effect of chronic bradykinin administration on insulin action in an animal model of insulin resistance. Am J Physiol. 1998;275:R40–R45
  9. Leighton B, Sanderson AL, Young ME, et al.  Effects of treatment of spontaneously hypertensive rats with the angiotensin-converting enzyme inhibitor trandolapril and the calcium antagonist verapamil on the sensitivity of glucose metabolism to insulin in rat soleus muscle in vitro. Diabetes. 1996;45(suppl 1):S120–S124
  10. Miyata T, Taguchi T, Uehara M, et al.  Bradykinin potentiates insulin-stimulated glucose uptake and enhances insulin signal through the bradykinin B2 receptor in dog skeletal muscle and rat L6 myoblasts. Eur J Endocrinol. 1998;138:344–352
  11. Carvalho CRO, Thirone ACP, Gontijo JAR, et al.  Effect of captopril, losartan and bradykinin on early steps of insulin action. Diabetes. 1997;46:1950–1957
  12. Hartl WH, Jauch KW, Wolfe RR, et al.  Effects of kinins on glucose metabolism in vivo. Horm Metab Res Suppl. 1990;22:79–84
  13. Hartl WH, Jauch KW, Herndon DN, et al.  Effect of low-dose bradykinin on glucose metabolism and nitrogen balance in surgical patients. Lancet. 1990;335:69–71
  14. Kodama J, Katayama S, Tanaka K, et al.  Effect of captopril on glucose concentration: Possible role of augmented postprandial forearm blood flow. Diabetes Care. 1990;13:1109–1111
  15. Hirooka Y, Imaizuma T, Masaki H, et al.  Captopril improved impaired endothelium-dependent vasodilatation in hypertensive patients. Hypertension. 1992;20:175–180
  16. Jauch KW, Hartl W, Gunther B, et al.  Captopril enhances insulin responsiveness of forearm muscle tissue in non-insulin-dependent diabetes mellitus. Eur J Clin Invest. 1987;17:448–454
  17. Schubert D, Harris AJ, Devine CE, et al.  Characterization of a unique muscle cell line. J Cell Biol. 1974;61:398–413
  18. Mayor P, Maianu L, Garvey WT. Glucose and insulin chronically regulate insulin action via different mechanisms in BC3H1 myocytes. Effects on glucose transporter gene expression. Diabetes. 1992;41:274–284
  19. Marschall S. Kinetics of insulin receptor internalization and recycling in adipocytes. J Biol Chem. 1985;260:4136–4144
  20. Towbin H, Staehlin J, Gordon J. Electrophoretic transfer of proteins from polyacrylamide gels to nitrocellulose sheets: Procedure and some applications. Proc Natl Acad Sci USA. 1979;76:4350–4354
  21. Heidenreich KA, Gilmore P. Structural and functional characteristics of insulin receptors in rat neuroblastoma cells. J Neurochem. 1985;45:1642–1648
  22. White MF. The IRS-signaling system: A network of docking proteins that mediate insulin action. Mol Cell Biochem. 1998;182:3–11
  23. Araki E, Lipes MA, Patti ME, et al.  Alternative pathway of insulin signaling in mice with target disruption of IRS-1 gene. Nature. 1994;372:186–190
  24. Burgering BM, Coffer PJ. Protein kinase B (AKT) in phosphatidylinositol-3-OH-kinase signal transduction. Nature. 1995;376:599–602
  25. Franke TF, Yang SI, Chan TO, et al.  The protein kinase encoded by the AKT proto-oncogene is a target of PDGF-activated phosphatidylinositol 3-kinase. Cell. 1995;81:727–736
  26. Coffer PJ, Jin J, Woodgett JR. Protein kinase (c-AKT): A multifunctional mediator of phosphatidylinositol 3-kinase activation. Biochem J. 1998;335:1–13
  27. Patrick J, McMilan J, Wolfson H, et al.  Acethylcholine receptor metabolism in a nonfusing muscle cell line. J Biol Chem. 1977;252:2143–2153
  28. Standaert ML, Schimmel SD, Pollet RJ. The development of insulin-receptors and responses in the differentiating nonfusing muscle cell line BC3H-1. J Biol Chem. 1984;259:2337–2345
  29. Olson EN, Caldwell KL, Gordon GI, et al.  Regulation of creatine phosphokinase expression during differentiation of BC3H-1 cells. J Biol Chem. 1983;258:2644–2652
  30. Sechi LA, Griffin CA, Zingaro L, et al.  Effects of angiotensin II on insulin receptor binding and mRNA levels in normal and diabetic rats. Diabetologia. 1997;40:770–777
  31. Dominguez LJ, Barbagallo M, Jacober SJ, et al.  Bisoprolol and captopril effects on insulin receptor tyrosine kinase activity in essential hypertension. Am J Hypertens. 1997;10:1349–1355
  32. Sun XJ, Rothenberg PL, Kahn CR, et al.  Structure of the insulin receptor substrate IRS-1 defines a unique signal transduction protein. Nature. 1991;352:73–77
  33. White MF, Maron R, Kahn CR. Insulin rapidly stimulates tyrosine phosphorylation of a Mr 185,000 protein in intact cells. Nature. 1985;318:183–186
  34. Ebina Y, Araki E, Taira M, et al.  Replacement of lysine residue 1030 in the putative ATP-binding region of the insulin receptor abolishes insulin-and antibody-stimulated glucose uptake and receptor kinase activity. Proc Natl Acad Sci USA. 1987;84:704–708
  35. White MF, Kahn CR. The insulin signaling system. J Biol Chem. 1994;269:1–5
  36. Chou CK, Dull TJ, Russel DS, et al.  Human insulin receptors mutated at the ATP-binding site lack protein tyrosine kinase activity and fail to mediate postreceptor effects of insulin. J Biol Chem. 1987;262:1842–1847
  37. Kerouz NJ, Horsch D, Pons S, et al.  Differential regulation of insulin receptor substrates-1 and -2 (IRS-1 and IRS-2) and phosphatidylinositol 3-kinase isoforms in liver and muscle of obese diabetic (ob/ob) mouse. J Clin Invest. 1997;100:3164–3172
  38. Kido Y, Burks DJ, Withers D, et al.  Tissue-specific insulin resistance in mice with mutations in the insulin receptor, IRS-1, and IRS-2. J Clin Invest. 2000;105:199–205
  39. Previs SF, Whiters DJ, Ren JM, et al.  Contrasting effects of IRS-1 versus IRS-2 gene disruption on carbohydrate and lipid metabolism in vivo. J Biol Chem. 2000;275:38990–38994
  40. Cheatham B, Vlahos CJ, Cheatham L, et al.  Phosphatidylinositol 3-kinase activation is required for insulin stimulation of pp70 S6 kinase, DNA synthesis and glut4 transporter translocation. Mol Cell Biol. 1994;14:4902–4911
  41. Barthel A, Okino ST, Liao J, et al.  Regulation of GLUT1 gene transcription by the serine/threonine kinase AKT. J Biol Chem. 1999;274:20281–20286
  42. Taha C, Liu Z, Jin J, et al.  Opposite translational control of GLUT1 and GLUT4 glucose transporter mRNAs in response to insulin. J Biol Chem. 1999;274:33085–33091
  43. Cross DA, Alessi DR, Cohen O, et al.  Inhibition of glycogen synthase kinase-3 mediated by protein kinase B. Nature. 1995;378:785–789
  44. Kodama J, Katayama S, Tanaka K, et al.  Effect of captopril on glucose concentration: Possible role of augmented postprandial forearm blood flow. Diabetes Care. 1990;13:1109–1111
  45. Hirooka Y, Imaizumi T, Masaki H, et al.  Captopril improved impaired endothelium-dependent vasodilatation in hypertensive patients. Hypertension. 1992;20:175–180

 Supported by FAPESP and CNPq grants. R.S.M. and C.R.O C. contributed equally to this study.

☆☆ Address reprint requests to Regina S. Moisés, MD, PhD; Universidade Federal de São Paulo, Escola Paulista de Medicina, Disciplina de Endocrinologia, Rua Botucatu, 740–2° andar, 04034-970 São Paulo, SP, Brazil.

PII: S0026-0495(02)05260-5

doi: 10.1053/meta.2003.50044

Metabolism - Clinical and Experimental
Volume 52, Issue 3 , Pages 273-278 , March 2003