Oral administration of angiotensin-(1-7) ameliorates type 2 diabetes in rats

Journal of Molecular Medicine

Volumn 92, Issue 3, 2014, Pages 255-265

  Santos, Sérgio H S ^a   Giani, Jorge F ^b   Burghi, Valeria ^b   Miquet, Johanna G ^b   Qadri, Fatimunnisa ^c   Braga, Janaina F ^a   Todiras, Mihail ^c   Kotnik, Katarina ^c   Alenina, Natalia ^c   Dominici, Fernando P ^b   Santos, Robson A S ^a   Bader, Michael ^c  

^a FEDERAL UNIVERSITY OF MINAS GERAIS   (Brazil)

^b UNIVERSIDAD DE BUENOS AIRES   (Argentina)

^c MAX DELBRÜCK CENTER FOR MOLECULAR MEDICINE   (Germany)

Author keywords

Angiotensin (1 7); Antidiabetic; Diabetes; RNA interference

Indexed keywords

2 HYDROXYPROPYL BETA CYCLODEXTRIN; ANGIOTENSIN[1-7]; GLUCOSE; GLUCOSE TRANSPORTER 4; GLYCOGEN SYNTHASE KINASE 3BETA; INSULIN; INSULIN RECEPTOR; INSULIN RECEPTOR SUBSTRATE 1; PROTEIN KINASE B;

ANIMAL CELL; ANIMAL CELL CULTURE; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ANTIDIABETIC ACTIVITY; ARTICLE; BODY WEIGHT; CELL ISOLATION; CELL MEMBRANE; CONTROLLED STUDY; DIABETIC NEPHROPATHY; DIURESIS; DOWN REGULATION; DRUG FORMULATION; ENZYME PHOSPHORYLATION; GLUCOSE BLOOD LEVEL; GLUCOSE TRANSPORT; HEART MUSCLE CELL; HISTOLOGY; HYPERGLYCEMIA; IMMUNOBLOTTING; IN VITRO STUDY; INSULIN BLOOD LEVEL; INSULIN RESISTANCE; INSULIN SENSITIVITY; LONG TERM CARE; MALE; NEWBORN; NON INSULIN DEPENDENT DIABETES MELLITUS; NONHUMAN; PREVENTION STUDY; RAT; SIGNAL TRANSDUCTION; THERAPY EFFECT; URINE VOLUME;

ADMINISTRATION, ORAL; ANGIOTENSIN I; ANIMALS; ANIMALS, NEWBORN; DEOXYGLUCOSE; DIABETES MELLITUS, TYPE 2; HYPERGLYCEMIA; HYPOGLYCEMIC AGENTS; INSULIN; MALE; MYOCYTES, CARDIAC; PEPTIDE FRAGMENTS; PHOSPHORYLATION; PROTO-ONCOGENE PROTEINS C-AKT; RATS; RATS, SPRAGUE-DAWLEY; SIGNAL TRANSDUCTION;

EID: 84898472204     PISSN: 09462716     EISSN: 14321440     Source Type: Journal    
DOI: 10.1007/s00109-013-1087-0     Document Type: Article

References (51)

1. Dandona P, Aljada A (2002) A rational approach to pathogenesis and treatment of type 2 diabetes mellitus, insulin resistance, inflammation, and atherosclerosis. Am J Cardiol 90:27G-33G
2. Mauvais-Jarvis F, Kahn CR (2000) Understanding the pathogenesis and treatment of insulin resistance and type 2 diabetes mellitus: what can we learn from transgenic and knockout mice? Diabetes Metab 26:433-448
3. Molitch ME, DeFronzo RA, Franz MJ, Keane WF, Mogensen CE, Parving HH, Steffes MW (2004) Nephropathy in diabetes. Diabetes Care 27(Suppl 1):S79-S83
4. KDOQI (2007) Clinical practice guidelines and clinical practice recommendations for diabetes and chronic kidney disease. Am J Kidney Dis 49:S12-154
5. Prasad A, Quyyumi AA (2004) Renin-angiotensin system and angiotensin receptor blockers in the metabolic syndrome. Circulation 110:1507-1512
6. Giacchetti G, Sechi LA, Rilli S, Carey RM (2005) The renin-angiotensin- aldosterone system, glucose metabolism and diabetes. Trends Endocrinol Metab 16:120-126
7. Strazzullo P, Galletti F (2004) Impact of the renin-angiotensin system on lipid and carbohydrate metabolism. Curr Opin Nephrol Hypertens 13:325-332
8. Gurley SB, Coffman TM (2007) The renin-angiotensin system and diabetic nephropathy. Semin Nephrol 27:144-152
9. Putnam K, Shoemaker R, Yiannikouris F, Cassis LA (2012) The renin-angiotensin system: a target of and contributor to dyslipidemias, altered glucose homeostasis, and hypertension of the metabolic syndrome. Am J Physiol Heart Circ Physiol 302:H1219-H1230
10. Bader M (2010) Tissue renin-angiotensin-aldosterone systems: targets for pharmacological therapy. Ann Rev Pharmacol Toxicol 50:439-465
11. Boustany CM, Bharadwaj K, Daugherty A, Brown DR, Randall DC, Cassis LA (2004) Activation of the systemic and adipose renin-angiotensin system in rats with diet-induced obesity and hypertension. Am J Physiol Regul Integr Comp Physiol 287:R943-R949
12. Crackower MA, Sarao R, Oudit GY, Yagil C, Kozieradzki I, Scanga SE, Oliveira-dos-Santos AJ, da Costa J, Zhang L, Pei Y et al (2002) Angiotensin-converting enzyme 2 is an essential regulator of heart function. Nature 417:822-828
13. Santos RA, Ferreira AJ, Pinheiro SV, Sampaio WO, Touyz R, Campagnole-Santos MJ (2005) Angiotensin-(1-7) and its receptor as a potential targets for new cardiovascular drugs. Expert Opin Investig Drugs 14:1019-1031
14. Tipnis SR, Hooper NM, Hyde R, Karran E, Christie G, Turner AJ (2000) A human homolog of angiotensin-converting enzyme. Cloning and functional expression as a captopril-insensitive carboxypeptidase. J Biol Chem 275:33238-33243
15. Reudelhuber TL (2005) The renin-angiotensin system: peptides and enzymes beyond angiotensin II. Curr Opin Nephrol Hypertens 14:155-159
16. Santos RA, Simoes e Silva AC, Maric C, Silva DMR, Machado RP, de Buhr I, Heringer-Walther S, Pinheiro SVB, Lopes MT, Bader M et al (2003) Angiotensin-(1-7) is an endogenous ligand for the G-protein coupled receptor Mas. Proc Natl Acad Sci U S A 100:8258-8263
17. Fraga da Silva RA, Pinheiro SVB, Goncalves ACC, Alenina N, Bader M, Santos RA (2008) The NO-mediated antithrombotic effect of angiotensin-(1-7) is abolished in mas-knockout mice. Mol Med 14:28-35
18. Santos RA, Ferreira AJ (2007) Angiotensin-(1-7) and the renin-angiotensin system. Curr Opin Nephrol Hypertens 16:122-128
19. Niu MJ, Yang JK, Lin SS, Ji XJ, Guo LM (2008) Loss of angiotensin-converting enzyme 2 leads to impaired glucose homeostasis in mice. Endocrine 34:56-61
20. Bindom SM, Hans CP, Xia H, Boulares AH, Lazartigues E (2010) Angiotensin I-converting enzyme type 2 (ACE2) gene therapy improves glycemic control in diabetic mice. Diabetes 59:2540-2548
21. Santos SHS, Braga JF, Mario EG, Porto LCJ, Botion LM, Alenina N, Bader M, Santos RA (2010) Improved lipid and glucose metabolism in transgenic rats with increased circulating angiotensin-(1-7). Arterioscler Thromb Vasc Biol 30:953-961
22. Giani JF, Mayer MA, Munoz MC, Silberman EA, Hocht C, Taira CA, Gironacci MM, Turyn D, Dominici FP (2009) Chronic infusion of angiotensin-(1-7) improves insulin resistance and hypertension induced by a high-fructose diet in rats. Am J Physiol Endocrinol Metab 296:E262-E271
23. Marcus Y, Shefer G, Sasson K, Kohen F, Limor R, Pappo O, Nevo N, Biton I, Bach M, Berkutzki T et al (2013) Angiotensin 1-7 as means to prevent the metabolic syndrome: Lessons from the fructose-fed rat model. Diabetes 62:1121-1130
24. Benter IF, Yousif MH, Dhaunsi GS, Kaur J, Chappell MC, Diz DI (2008) Angiotensin-(1-7) prevents activation of NADPH oxidase and renal vascular dysfunction in diabetic hypertensive rats. Am J Nephrol 28:25-33
25. Dhaunsi GS, Yousif MH, Akhtar S, Chappell MC, Diz DI, Benter IF (2010) Angiotensin-(1-7) prevents diabetes-induced attenuation in PPAR-gamma and catalase activities. Eur J Pharmacol 638:108-114
26. Santos SHS, Fernandes LR, Mario EG, Ferreira AVM, Porto LCJ, Alvarez-Leite JI, Botion LM, Bader M, Alenina N, Santos RA (2008) Mas deficiency in FVB/N in mice produces marked changes in lipid and glycemic metabolism. Diabetes 57:340-347
27. Lula I, Denadai AL, Resende JM, de Sousa FB, de Lima GF, Pilo-Veloso D, Heine T, Duarte HA, Santos RA, Sinisterra RD (2007) Study of angiotensin-(1-7) vasoactive peptide and its beta-cyclodextrin inclusion complexes: complete sequence-specific NMR assignments and structural studies. Peptides 28:2199-2210
28. Marques FD, Ferreira AJ, Sinisterra RD, Jacoby BA, Sousa FB, Caliari MV, Silva GA, Melo MB, Nadu AP, Souza LE et al (2011) An oral formulation of angiotensin-(1-7) produces cardioprotective effects in infarcted and isoproterenol-treated rats. Hypertension 57:477-483
29. Fraga-Silva RA, Costa-Fraga FP, Sousa FB, Alenina N, Bader M, Sinisterra RD, Santos RA (2011) An orally-active formulation of angiotensin-(1-7) produces antithrombotic effect. Clinics 66:837-841
30. Kotnik K, Popova E, Todiras M, Mori MA, Alenina N, Seibler J, Bader M (2009) Inducible transgenic rat model for diabetes mellitus based on shRNA-mediated gene knockdown. PLoS ONE 4:e5124
31. Nigro J, Osman N, Dart AM, Little PJ (2006) Insulin resistance and atherosclerosis. Endocr Rev 27:242-259
32. DeFronzo RA (1997) Insulin resistance: a multifaceted syndrome responsible for NIDDM, obesity, hypertension, dyslipidaemia and atherosclerosis. Neth J Med 50:191-197
33. Grundy SM (2012) Pre-diabetes, metabolic syndrome, and cardiovascular risk. J Am Coll Cardiol 59:635-643
34. Miranda PJ, DeFronzo RA, Califf RM, Guyton JR (2005) Metabolic syndrome: definition, pathophysiology, and mechanisms. Am Heart J 149:33-45
35. Hainault I, Nebout G, Turban S, Ardouin B, Ferre P, Quignard-Boulange A (2002) Adipose tissue-specific increase in angiotensinogen expression and secretion in the obese (fa/fa) Zucker rat. Am J Physiol Endocrinol Metab 282:E59-E66
36. Batlle D, Wysocki J, Soler MJ, Ranganath K (2012) Angiotensin-converting enzyme 2: enhancing the degradation of angiotensin II as a potential therapy for diabetic nephropathy. Kidney Int 81:520-528
37. Singh T, Singh K, Sharma PL (2010) Ameliorative potential of angiotensin1-7/Mas receptor axis in streptozotocin-induced diabetic nephropathy in rats. Methods Find Exp Clin Pharmacol 32:19-25, 1434160
38. Giani JF, Munoz MC, Pons RA, Cao G, Toblli JE, Turyn D, Dominici FP (2011) Angiotensin-(1-7) reduces proteinuria and diminishes structural damage in renal tissue of stroke-prone spontaneously hypertensive rats. Am J Physiol Ren Physiol 300:F272-F282
39. Giani JF, Burghi V, Veiras LC, Tomat A, Munoz MC, Cao G, Turyn D, Toblli JE, Dominici FP (2012) Angiotensin-(1-7) attenuates diabetic nephropathy in Zucker diabetic fatty rats. Am J Physiol Ren Physiol 302:F1606-F1615
40. Pinheiro SVB, Ferreira AJ, Kitten GT, da Silveira KD, da Silva DA, Santos SHS, Gava E, Castro CH, Magalhaes JA, da Mota RK et al (2009) Genetic deletion of the angiotensin(1-7) receptor Mas leads to glomerular hyperfiltration and microalbuminuria. Kidney Int 75:1184-1193
41. Taniguchi CM, Emanuelli B, Kahn CR (2006) Critical nodes in signalling pathways: insights into insulin action. Nat Rev Mol Cell Biol 7:85-96
42. Folli F, Kahn CR, Hansen H, Bouchie JL, Feener EP (1997) Angiotensin II inhibits insulin signaling in aortic smooth muscle cells at multiple levels. A potential role for serine phosphorylation in insulin/angiotensin II crosstalk. J Clin Invest 100:2158-2169
43. Folli F, Saad MJ, Velloso L, Hansen H, Carandente O, Feener EP, Kahn CR (1999) Crosstalk between insulin and angiotensin II signalling systems. Exp Clin Endocrinol Diabetes 107:133-139
44. Giani JF, Gironacci MM, Munoz MC, Pena C, Turyn D, Dominici FP (2007) Angiotensin-(1 7) stimulates the phosphorylation of JAK2, IRS-1 and Akt in rat heart in vivo: role of the AT1 and Mas receptors. Am J Physiol Heart Circ Physiol 293:H1154-H1163
45. Sampaio WO, Souza dos Santos RA, Faria-Silva R, Mata Machado LT, Schiffrin EL, Touyz RM (2007) Angiotensin-(1-7) through receptor Mas mediates endothelial nitric oxide synthase activation via Akt-dependent pathways. Hypertension 49:185-192
46. Munoz MC, Giani JF, Burghi V, Mayer MA, Carranza A, Taira CA, Dominici FP (2012) The Mas receptor mediates modulation of insulin signaling by angiotensin-(1-7). Regul Pept 177:1-11
47. Hotamisligil GS, Peraldi P, Budavari A, Ellis R, White MF, Spiegelman BM (1996) IRS-1-mediated inhibition of insulin receptor tyrosine kinase activity in TNF-alpha- and obesity-induced insulin resistance. Science 271:665-668
48. Aguirre V, Werner ED, Giraud J, Lee YH, Shoelson SE, White MF (2002) Phosphorylation of Ser307 in insulin receptor substrate-1 blocks interactions with the insulin receptor and inhibits insulin action. J Biol Chem 277:1531-1537
49. Andreozzi F, Laratta E, Sciacqua A, Perticone F, Sesti G (2004) Angiotensin II impairs the insulin signaling pathway promoting production of nitric oxide by inducing phosphorylation of insulin receptor substrate-1 on Ser312 and Ser616 in human umbilical vein endothelial cells. Circ Res 94:1211-1218
50. Liu C, Lv XH, Li HX, Cao X, Zhang F, Wang L, Yu M, Yang JK (2012) Angiotensin-(1-7) suppresses oxidative stress and improves glucose uptake via Mas receptor in adipocytes. Acta Diabetol 49:291-299
51. Mario EG, Santos SH, Ferreira AV, Bader M, Santos RA, Botion LM (2012) Angiotensin-(1-7) Mas-receptor deficiency decreases peroxisome proliferator-activated receptor gamma expression in adipocytes. Peptides 33:174-177