Renin-Angiotensin System Blockers Protect Pancreatic Islets against Diet-Induced Obesity and Insulin Resistance in Mice

PLoS ONE

Volumn 8, Issue 7, 2013, Pages

  Frantz, Eliete Dalla Corte ^a   Crespo Mascarenhas, Camila ^a   Barreto Vianna, Andre Rodrigues C ^a   Aguila, Marcia Barbosa ^a   Mandarim de Lacerda, Carlos Alberto ^a  

^a STATE UNIVERSITY OF RIO DE JANEIRO   (Brazil)

Author keywords

[No Author keywords available]

Indexed keywords

ADIPONECTIN; ALISKIREN; ANGIOTENSIN CONVERTING ENZYME 2; ENALAPRIL; GLUCAGON; GLUCOSE; GLUCOSE TRANSPORTER 2; INSULIN; LOSARTAN; MAS RECEPTOR PROTEIN; RECEPTOR PROTEIN; TRANSCRIPTION FACTOR PDX 1; UNCLASSIFIED DRUG;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BODY MASS; CALORIC INTAKE; CARBOHYDRATE METABOLISM; CELL SIZE; CELL STRUCTURE; CELL VOLUME; CONTROLLED STUDY; DIET RESTRICTION; FOOD INTAKE; FOOD PROCESSING; GLUCOSE INTOLERANCE; GLUCOSE METABOLISM; HOMEOSTASIS; HORMONE DETERMINATION; HORMONE METABOLISM; HORMONE RELEASE; HYPERTENSION; IMMUNOHISTOCHEMISTRY; INSULIN RESISTANCE; LIPID DIET; MALE; MORPHOMETRICS; MOUSE; NONHUMAN; OBESITY; PANCREAS INJURY; PANCREAS ISLET; PANCREAS ISLET ALPHA CELL; PANCREAS ISLET BETA CELL; PROTEIN EXPRESSION; RENIN ANGIOTENSIN ALDOSTERONE SYSTEM; STEREOLOGY; SYSTOLIC BLOOD PRESSURE; TREATMENT DURATION; WEIGHT GAIN; WESTERN BLOTTING;

ANGIOTENSIN II TYPE 1 RECEPTOR BLOCKERS; ANIMALS; BODY SIZE; DIET, HIGH-FAT; EATING; GLUCOSE TOLERANCE TEST; INSULIN RESISTANCE; ISLETS OF LANGERHANS; MALE; MICE; MICE, INBRED C57BL; OBESITY; PROTEASE INHIBITORS; RECEPTOR, ANGIOTENSIN, TYPE 1; RECEPTOR, ANGIOTENSIN, TYPE 2; RENIN; RENIN-ANGIOTENSIN SYSTEM;

EID: 84880647738     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0067192     Document Type: Article

References (57)

1. Richard D, Boisvert P, (2009) 11th Annual International Symposium in Obesity: 'Obesity in a modern world: when pleasure meets homeostasis'. Int J Obes 33 (Suppl 2):: S1-S2. doi:10.1038/ijo.2008.259.
2. Passos-Silva DG, Verano-Braga T, Santos RA, (2013) Angiotensin-(1-7): beyond the cardio-renal actions. Clin Sci (Lond) 124: 443-456. doi:10.1042/CS20120461.
3. Luther JM, Brown NJ, (2011) The renin-angiotensin-aldosterone system and glucose homeostasis. Trends Pharmacol Sci 32: 734-739. doi:10.1016/j.tips.2011.07.006. PubMed: 21880378.
4. Peach MJ, (1977) Renin-angiotensin system: biochemistry and mechanisms of action. Physiol Rev 57: 313-370. PubMed: 191856.
5. Henriksen EJ, Jacob S, Kinnick TR, Youngblood EB, Schmit MB, et al. (1999) ACE inhibition and glucose transport in insulinresistant muscle: roles of bradykinin and nitric oxide. Am J Physiol Endocrinol Metab 277: R332-R336.
6. Donoghue M, Hsieh F, Baronas E, Godbout K, Gosselin M, et al. (2000) A novel angiotensin-converting enzyme-related carboxypeptidase (ACE2) converts angiotensin I to angiotensin 1-9. Circ Res 87: E1-E9. doi:10.1161/01.RES.87.1.1. PubMed: 10969042.
7. Giani JF, Mayer MA, Munoz MC, Silberman EA, Hocht C, et al. (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. PubMed: 19001546.
8. Santos RA, Simoes e Silva AC, Maric C, Silva DM, Machado RP, et al. (2003) Angiotensin-(1-7) is an endogenous ligand for the G protein-coupled receptor Mas. PNAS 100: 8258-8263. doi:10.1073/pnas.1432869100. PubMed: 12829792.
9. Leung PS, (2003) Pancreatic renin-angiotensin system: a novel target for the potential treatment of pancreatic diseases? JOP4: 89-91. PubMed: 12629265.
10. Velloso LA, Folli F, Perego L, Saad MJ, (2006) The multi-faceted cross-talk between the insulin and angiotensin II signaling systems. Diabetes/Metab Res Rev 22: 98-107. doi:10.1002/dmrr.611.
11. van der Zijl NJ, Moors CC, Goossens GH, Blaak EE, Diamant M, (2012) Does interference with the renin-angiotensin system protect against diabetes? Evidence and mechanisms. Diabetes Obes Metab 14: 586-595. doi:10.1111/j.1463-1326.2012.01559.x. PubMed: 22226145.
12. de Kloet AD, Krause EG, Woods SC, (2010) The renin angiotensin system and the metabolic syndrome. Physiol Behav 100: 525-534. doi:10.1016/j.physbeh.2010.03.018. PubMed: 20381510.
13. Munoz MC, Giani JF, Burghi V, Mayer MA, Carranza A, et al. (2012) The Mas receptor mediates modulation of insulin signaling by angiotensin-(1-7). Regulat Peptides 177: 1-11.
14. Barros CC, Haro A, Russo FJ, Schadock I, Almeida SS, et al. (2012) Altered glucose homeostasis and hepatic function in obese mice deficient for both kinin receptor genes. PLOS ONE 7: e40573. doi:10.1371/journal.pone.0040573. PubMed: 22829877.
15. Babu DA, Deering TG, Mirmira RG, (2007) A feat of metabolic proportions: Pdx1 orchestrates islet development and function in the maintenance of glucose homeostasis. Mol Genet Metab 92: 43-55. doi:10.1016/j.ymgme.2007.06.008. PubMed: 17659992.
16. Bernardo AS, Hay CW, Docherty K, (2008) Pancreatic transcription factors and their role in the birth, life and survival of the pancreatic beta cell. Mol Cell Endocrinol 294: 1-9. doi:10.1016/j.mce.2008.07.006. PubMed: 18687378.
17. Navarro-Tableros V, Fiordelisio T, Hernandez-Cruz A, Hiriart M, (2007) Physiological development of insulin secretion, calcium channels, and GLUT2 expression of pancreatic rat beta-cells. Am J Physiol Endocrinol Metab 292: E1018-E1029. PubMed: 17148757.
18. Reeves PG, Nielsen FH, Fahey GC Jr., (1993) AIN-93 purified diets for laboratory rodents: final report of the American Institute of Nutrition ad hoc writing committee on the reformulation of the AIN-76A rodent diet. J Nutr 123: 1939-1951. PubMed: 8229312.
19. Matthews DR, Hosker JP, Rudenski AS, Naylor BA, Treacher DF, et al. (1985) Homeostasis model assessment: insulin resistance and beta-cell function from fasting plasma glucose and insulin concentrations in man. Diabetologia 28: 412-419. doi:10.1007/BF00280883. PubMed: 3899825.
20. Mandarim-de-Lacerda CA, Fernandes-Santos C, Aguila MB, (2010) Image analysis and quantitative morphology. Methods Mol Biol 611: 211-225. doi:10.1007/978-1-60327-345-9_17. PubMed: 19960334.
21. Tschanz SA, Burri PH, Weibel ER, (2011) A simple tool for stereological assessment of digital images: the STEPanizer. J Microsc 243: 47-59. doi:10.1111/j.1365-2818.2010.03481.x. PubMed: 21375529.
22. Frantz ED, Aguila MB, Pinheiro-Mulder Ada R, Mandarim-de-Lacerda CA, (2011) Transgenerational endocrine pancreatic adaptation in mice from maternal protein restriction in utero. Mech Ageing Dev 132: 110-116.
23. Lacy PE, Kostianovsky M, (1967) Method for the isolation of intact islets of Langerhans from the rat pancreas. Diabetes 16: 35-39. PubMed: 5333500.
24. Yuan L, Li X, Xu GL, Qi CJ, (2010) Effects of renin-angiotensin system blockade on islet function in diabetic rats. J Endocrinol Invest 33: 13-19.
25. Takeda M, Yamamoto K, Takemura Y, Takeshita H, Hongyo K, et al. (2012) Loss of ACE 2 Exaggerates High-Calorie Diet-Induced Insulin Resistance by Reduction of GLUT4 in Mice. Diabetes 62: 223-233. PubMed: 22933108.
26. 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. doi:10.2337/db09-0782. PubMed: 20660625.
27. Santos SH, Fernandes LR, Mario EG, Ferreira AV, Porto LC, et al. (2008) Mas deficiency in FVB/N mice produces marked changes in lipid and glycemic metabolism. Diabetes 57: 340-347. PubMed: 18025412.
28. Lowell BB, Shulman GI, (2005) Mitochondrial dysfunction and type 2 diabetes. Science 307: 384-387. doi:10.1126/science.1104343. PubMed: 15662004.
29. Bonora E, (2008) Protection of pancreatic beta-cells: is it feasible? Nutr Metab Cardiovasc Dis 18: 74-83. doi:10.1016/j.numecd.2007.05.004. PubMed: 18096375.
30. Liu Z, Kim W, Chen Z, Shin YK, Carlson OD, et al. (2011) Insulin and glucagon regulate pancreatic alpha-cell proliferation. PLOS ONE 6: e16096. doi:10.1371/journal.pone.0016096. PubMed: 21283589.
31. Janssen SW, Hermus AR, Lange WP, Knijnenburg Q, van der Laak JA, et al. (2001) Progressive histopathological changes in pancreatic islets of Zucker Diabetic Fatty rats. Exp Clin Endocrinol Diabetes 109: 273-282. doi:10.1055/s-2001-16347. PubMed: 11507651.
32. Yang BT, Dayeh TA, Volkov PA, Kirkpatrick CL, Malmgren S, et al. (2012) Increased DNA methylation and decreased expression of PDX-1 in pancreatic islets from patients with type 2 diabetes. Mol Endocrinol 26: 1203-1212. doi:10.1210/me.2012-1004. PubMed: 22570331.
33. Folli F, Okada T, Perego C, Gunton J, Liew CW, et al. (2011) Altered insulin receptor signalling and beta-cell cycle dynamics in type 2 diabetes mellitus. PLOS ONE 6: e28050. doi:10.1371/journal.pone.0028050. PubMed: 22140505.
34. Dong YF, Liu L, Kataoka K, Nakamura T, Fukuda M, et al. (2010) Aliskiren prevents cardiovascular complications and pancreatic injury in a mouse model of obesity and type 2 diabetes. Diabetologia 53: 180-191. doi:10.1007/s00125-009-1575-5. PubMed: 19894030.
35. Pereira LM, Bezerra DG, Machado DL, Mandarim-de-Lacerda CA, (2004) Enalapril attenuates cardiorenal damage in nitric-oxide-deficient spontaneously hypertensive rats. Clin Sci (Lond) 106: 337-343. doi:10.1042/CS20030268.
36. Chu KY, Lau T, Carlsson PO, Leung PS, (2006) Angiotensin II type 1 receptor blockade improves beta-cell function and glucose tolerance in a mouse model of type 2 diabetes. Diabetes 55: 367-374. doi:10.2337/diabetes.55.02.06.db05-1022. PubMed: 16443769.
37. Staessen JA, Li Y, Richart T, (2006) Oral renin inhibitors. Lancet 368: 1449-1456. doi:10.1016/S0140-6736(06)69442-7. PubMed: 17055947.
38. Masuo K, Mikami H, Ogihara T, Tuck ML, (2001) Weight reduction and pharmacologic treatment in obese hypertensives. Am J Hypertens 14: 530-538. doi:10.1016/S0895-7061(00)01279-6. PubMed: 11411732.
39. Santos EL, de Picoli Souza K, da Silva ED, Batista EC, Martins PJ, et al. (2009) Long term treatment with ACE inhibitor enalapril decreases body weight gain and increases life span in rats. Biochem Pharmacol 78: 951-958. doi:10.1016/j.bcp.2009.06.018. PubMed: 19549507.
40. Barzilay JI, Davis BR, Cutler JA, Pressel SL, Whelton PK, et al. (2006) Fasting glucose levels and incident diabetes mellitus in older nondiabetic adults randomized to receive 3 different classes of antihypertensive treatment: a report from the Antihypertensive and Lipid-Lowering Treatment to Prevent Heart Attack Trial (ALLHAT). Arch Intern Med 166: 2191-2201. doi:10.1001/archinte.166.20.2191. PubMed: 17101936.
41. Yusuf S, Sleight P, Pogue J, Bosch J, Davies R, et al. (2000) Effects of an angiotensin-converting-enzyme inhibitor, ramipril, on cardiovascular events in high-risk patients. The Heart Outcomes Prevention Evaluation Study Investigators. NEJM 342: 145-153. doi:10.1056/NEJM200001203420301. PubMed: 10639539.
42. Hansson L, Lindholm LH, Niskanen L, Lanke J, Hedner T, et al. (1999) Effect of angiotensin-converting-enzyme inhibition compared with conventional therapy on cardiovascular morbidity and mortality in hypertension: the Captopril Prevention Project (CAPPP) randomised trial. Lancet 353: 611-616. doi:10.1016/S0140-6736(98)05012-0. PubMed: 10030325.
43. Shindler DM, Kostis JB, Yusuf S, Quinones MA, Pitt B, et al. (1996) Diabetes mellitus, a predictor of morbidity and mortality in the Studies of Left Ventricular Dysfunction (SOLVD) Trials and Registry. Am J Cardiol 77: 1017-1020. doi:10.1016/S0002-9149(97)89163-1. PubMed: 8644628.
44. Santos EL, de Picoli Souza K, da Silva ED, Batista EC, Martins PJ, et al. (2009) Long term treatment with ACE inhibitor enalapril decreases body weight gain and increases life span in rats. Biochem Pharmacol 78: 951-958. doi:10.1016/j.bcp.2009.06.018. PubMed: 19549507.
45. Weisinger RS, Stanley TK, Begg DP, Weisinger HS, Spark KJ, et al. (2009) Angiotensin converting enzyme inhibition lowers body weight and improves glucose tolerance in C57BL/6J mice maintained on a high fat diet. Physiol Behav 98: 192-197. doi:10.1016/j.physbeh.2009.05.009. PubMed: 19465040.
46. Carvalho CR, Thirone AC, Gontijo JA, Velloso LA, Saad MJ, (1997) Effect of captopril, losartan, and bradykinin on early steps of insulin action. Diabetes 46: 1950-1957. doi:10.2337/diabetes.46.12.1950. PubMed: 9392479.
47. Oh YB, Kim JH, Park BM, Park BH, Kim SH, (2012) Captopril intake decreases body weight gain via angiotensin-(1-7). Peptides 37: 79-85. doi:10.1016/j.peptides.2012.06.005. PubMed: 22743141.
48. Santos RA, Ferreira AJ, Esac, Simoes (2008) Recent advances in the angiotensin-converting enzyme 2-angiotensin(1-7)-Mas axis. Exp Physiol 93: 519-527. doi:10.1113/expphysiol.2008.042002. PubMed: 18310257.
49. Jayasooriya AP, Mathai ML, Walker LL, Begg DP, Denton DA, et al. (2008) Mice lacking angiotensin-converting enzyme have increased energy expenditure, with reduced fat mass and improved glucose clearance. PNAS 105: 6531-6536. doi:10.1073/pnas.0802690105. PubMed: 18443281.
50. Santos SH, Braga JF, Mario EG, Porto LC, Rodrigues-Machado MG, et al. (2010) Improved lipid and glucose metabolism in transgenic rats with increased circulating angiotensin-(1-7). Arterioscler Thromb Vasc Biol 30: 953-961. doi:10.1161/ATVBAHA.109.200493. PubMed: 20203301.
51. Souza-Mello V, Gregorio BM, Cardoso-de-Lemos FS, de Carvalho L, Aguila MB, et al. (2010) Comparative effects of telmisartan, sitagliptin and metformin alone or in combination on obesity, insulin resistance, and liver and pancreas remodelling in C57BL/6 mice fed on a very high-fat diet. Clin Sci (Lond) 119: 239-250. doi:10.1042/CS20100061.
52. Kintscher U, (2012) And in the end-- Telmisartan directly binds to PPARgamma. Hypert Res 35: 704-705.
53. Perlstein TS, Henry RR, Mather KJ, Rickels MR, Abate NI, et al. (2012) Effect of angiotensin receptor blockade on insulin sensitivity and endothelial function in abdominally obese hypertensive patients with impaired fasting glucose. Clin Sci (Lond) 122: 193-202.
54. Ohshima K, Mogi M, Jing F, Iwanami J, Tsukuda K, et al. (2012) Direct Angiotensin II Type 2 Receptor Stimulation Ameliorates Insulin Resistance in Type 2 Diabetes Mice with PPARgamma Activation. PLOS ONE 7: e48387. doi:10.1371/journal.pone.0048387. PubMed: 23155382.
55. Yvan-Charvet L, Even P, Bloch-Faure M, Guerre-Millo M, Moustaid-Moussa N, et al. (2005) Deletion of the angiotensin type 2 receptor (AT2R) reduces adipose cell size and protects from diet-induced obesity and insulin resistance. Diabetes 54: 991-999. doi:10.2337/diabetes.54.4.991. PubMed: 15793237.
56. Yvan-Charvet L, Quignard-Boulange A, (2011) Role of adipose tissue renin-angiotensin system in metabolic and inflammatory diseases associated with obesity. Kidney Int 79: 162-168. doi:10.1038/ki.2010.391. PubMed: 20944545.
57. Mario EG, Santos SH, Ferreira AV, Bader M, Santos RA, et al. (2012) Angiotensin-(1-7) Mas-receptor deficiency decreases peroxisome proliferator-activated receptor gamma expression in adipocytes. Peptides 33: 174-177. doi:10.1016/j.peptides.2011.11.014. PubMed: 22119778.