Does interference with the renin-angiotensin system protect against diabetes? Evidence and mechanisms

Diabetes, Obesity and Metabolism

Volumn 14, Issue 7, 2012, Pages 586-595

  van der Zijl, N J ^a   Moors, C C M ^b   Goossens, G H ^a   Blaak, E E ^b   Diamant, M ^a  

^a VU UNIVERSITY MEDICAL CENTER   (Netherlands)

^b MAASTRICHT UNIVERSITY   (Netherlands)

Author keywords

Antihypertensive therapy; Drug mechanism; Insulin resistance; Type 2 diabetes; cell

Indexed keywords

ADIPOCYTOKINE; ANGIOTENSIN RECEPTOR ANTAGONIST; ANTIHYPERTENSIVE AGENT; CANDESARTAN; CAPTOPRIL; CYTOKINE; DIPEPTIDYL CARBOXYPEPTIDASE INHIBITOR; GLUCOSE; INSULIN; NATEGLINIDE; OLMESARTAN; RAMIPRIL; ROSIGLITAZONE; TELMISARTAN; VALSARTAN;

ADIPOCYTE; ADIPOSE TISSUE; CELL DIFFERENTIATION; CELL FUNCTION; CELL GROWTH; DRUG MEGADOSE; ESSENTIAL HYPERTENSION; EXPERIMENTAL MODEL; FIBROSIS; GLUCOSE METABOLISM; HIGH RISK POPULATION; HUMAN; HYPERTENSION; INFLAMMATION; INSULIN RESISTANCE; INSULIN SENSITIVITY; LIPOLYSIS; MITOCHONDRION; MUSCLE BLOOD FLOW; NON INSULIN DEPENDENT DIABETES MELLITUS; NONHUMAN; OBESITY; OXIDATIVE STRESS; PANCREAS ISLET BETA CELL; RANDOMIZED CONTROLLED TRIAL (TOPIC); RENIN ANGIOTENSIN ALDOSTERONE SYSTEM; REVIEW; SKELETAL MUSCLE; TISSUE BLOOD FLOW;

EID: 84861898665     PISSN: 14628902     EISSN: 14631326     Source Type: Journal    
DOI: 10.1111/j.1463-1326.2012.01559.x     Document Type: Review

References (128)

1. Kahn SE. The relative contributions of insulin resistance and beta-cell dysfunction to the pathophysiology of Type 2 diabetes. Diabetologia 2003; 46: 3-19.
2. Abdul-Ghani MA, Jenkinson CP, Richardson DK, Tripathy D, DeFronzo RA. Insulin secretion and action in subjects with impaired fasting glucose and impaired glucose tolerance: results from the Veterans Administration Genetic Epidemiology Study. Diabetes 2006; 55: 1430-1435.
3. van 't RE, Alssema M, Rijkelijkhuizen JM, Kostense PJ, Nijpels G, Dekker JM. Relationship between A1C and glucose levels in the general Dutch population: the new Hoorn study. Diabetes Care 2010; 33: 61-66.
4. The DECODE Study Group. Age- and sex-specific prevalences of diabetes and impaired glucose regulation in 13 European cohorts. Diabetes Care 2003; 26: 61-69.
5. Gerstein HC, Santaguida P, Raina P et al. Annual incidence and relative risk of diabetes in people with various categories of dysglycemia: a systematic overview and meta-analysis of prospective studies. Diabetes Res Clin Pract 2007; 78: 305-312.
6. Tuomilehto J, Lindstrom J, Eriksson JG et al. Prevention of type 2 diabetes mellitus by changes in lifestyle among subjects with impaired glucose tolerance. N Engl J Med 2001; 344: 1343-1350.
7. Knowler WC, Fowler SE, Hamman RF et al. 10-year follow-up of diabetes incidence and weight loss in the Diabetes Prevention Program Outcomes Study. Lancet 2009; 374: 1677-1686.
8. U.K. Prospective Diabetes Study 16. Overview of 6 years' therapy of type II diabetes: a progressive disease. U.K. Prospective Diabetes Study Group. Diabetes 1995; 44: 1249-1258.
9. van Genugten RE, van Raalte DH, Diamant M. Does glucagon-like peptide-1 receptor agonist therapy add value in the treatment of type 2 diabetes? Focus on exenatide. Diabetes Res Clin Pract 2009; 86(Suppl. 1): S26-S34.
10. van Raalte DH, van Genugten RE, Linssen MM, Ouwens DM, Diamant M. Glucagon-like peptide-1 receptor agonist treatment prevents glucocorticoid-induced glucose intolerance and islet-cell dysfunction in humans. Diabetes Care 2011; 34: 412-417.
11. Adams TD, Gress RE, Smith SC et al. Long-term mortality after gastric bypass surgery. N Engl J Med 2007; 357: 753-761.
12. Sjostrom L, Lindroos AK, Peltonen M et al. Lifestyle, diabetes, and cardiovascular risk factors 10 years after bariatric surgery. N Engl J Med 2004; 351: 2683-2693.
13. Jandeleit-Dahm KA, Tikellis C, Reid CM, Johnston CI, Cooper ME. Why blockade of the renin-angiotensin system reduces the incidence of new-onset diabetes. J Hypertens 2005; 23: 463-473.
14. Scheen AJ. Renin-angiotensin system inhibition prevents type 2 diabetes mellitus. Part 1. A meta-analysis of randomised clinical trials. Diabetes Metab 2004; 30: 487-496.
15. Scheen AJ. Renin-angiotensin system inhibition prevents type 2 diabetes mellitus. Part 2. Overview of physiological and biochemical mechanisms. Diabetes Metab 2004; 30: 498-505.
16. Cole BK, Keller SR, Wu R, Carter JD, Nadler JL, Nunemaker CS. Valsartan protects pancreatic islets and adipose tissue from the inflammatory and metabolic consequences of a high-fat diet in mice. Hypertension 2010; 55: 715-721.
17. Furuhashi M, Ura N, Takizawa H et al. Blockade of the renin-angiotensin system decreases adipocyte size with improvement in insulin sensitivity. J Hypertens 2004; 22: 1977-1982.
18. Henriksen EJ, Jacob S, Kinnick TR, Teachey MK, Krekler M. Selective angiotensin II receptor receptor antagonism reduces insulin resistance in obese Zucker rats. Hypertension 2001; 38: 884-890.
19. Tikellis C, Wookey PJ, Candido R, Andrikopoulos S, Thomas MC, Cooper ME. Improved islet morphology after blockade of the renin- angiotensin system in the ZDF rat. Diabetes 2004; 53: 989-997.
20. Peach MJ. Renin-angiotensin system: biochemistry and mechanisms of action. Physiol Rev 1977; 57: 313-370.
21. Paul M, Poyan MA, Kreutz R. Physiology of local renin-angiotensin systems. Physiol Rev 2006; 86: 747-803.
22. Miyazaki M, Takai S. Tissue angiotensin II generating system by angiotensin-converting enzyme and chymase. J Pharmacol Sci 2006; 100: 391-397.
23. de Gasparo M, Catt KJ, Inagami T, Wright JW, Unger T. International union of pharmacology. XXIII. The angiotensin II receptors. Pharmacol Rev 2000; 52: 415-472.
24. Carlsson PO, Berne C, Jansson L. Angiotensin II and the endocrine pancreas: effects on islet blood flow and insulin secretion in rats. Diabetologia 1998; 41: 127-133.
25. Fliser D, Schaefer F, Schmid D, Veldhuis JD, Ritz E. Angiotensin II affects basal, pulsatile, and glucose-stimulated insulin secretion in humans. Hypertension 1997; 30: 1156-1161.
26. Richey JM, Ader M, Moore D, Bergman RN. Angiotensin II induces insulin resistance independent of changes in interstitial insulin. Am J Physiol 1999; 277: E920-E926.
27. Wei Y, Sowers JR, Nistala R et al. Angiotensin II-induced NADPH oxidase activation impairs insulin signaling in skeletal muscle cells. J Biol Chem 2006; 281: 35137-35146.
28. Chu KY, Lau T, Carlsson PO, Leung PS. Angiotensin II type 1 receptor blockade improves beta-cell function and glucose tolerance in a mouse model of type 2 diabetes. Diabetes 2006; 55: 367-374.
29. Engeli S, Gorzelniak K, Kreutz R, Runkel N, Distler A, Sharma AM. Co-expression of renin-angiotensin system genes in human adipose tissue. J Hypertens 1999; 17: 555-560.
30. Lau T, Carlsson PO, Leung PS. Evidence for a local angiotensin-generating system and dose-dependent inhibition of glucose-stimulated insulin release by angiotensin II in isolated pancreatic islets. Diabetologia 2004; 47: 240-248.
31. Lastra-Lastra G, Sowers JR, Restrepo-Erazo K, Manrique-Acevedo C, Lastra-Gonzalez G. Role of aldosterone and angiotensin II in insulin resistance: an update. Clin Endocrinol (Oxf) 2009; 71: 1-6.
32. Sloniger JA, Saengsirisuwan V, Diehl CJ et al. Defective insulin signaling in skeletal muscle of the hypertensive TG(mREN2)27 rat. Am J Physiol Endocrinol Metab 2005; 288: E1074-E1081.
33. Velloso LA, Folli F, Sun XJ, White MF, Saad MJ, Kahn CR. Cross-talk between the insulin and angiotensin signaling systems. Proc Natl Acad Sci U S A 1996; 93: 12490-12495.
34. Dahlof B, Devereux RB, Kjeldsen SE et al. Cardiovascular morbidity and mortality in the Losartan Intervention For Endpoint reduction in hypertension study (LIFE): a randomised trial against atenolol. Lancet 2002; 359: 995-1003.
35. Hansson L, Lindholm LH, Niskanen L et al. 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 1999; 353: 611-616.
36. Julius S, Kjeldsen SE, Weber M et al. Outcomes in hypertensive patients at high cardiovascular risk treated with regimens based on valsartan or amlodipine: the VALUE randomised trial. Lancet 2004; 363: 2022-2031.
37. Abuissa H, Jones PG, Marso SP, O'Keefe JH Jr. Angiotensin-converting enzyme inhibitors or angiotensin receptor blockers for prevention of type 2 diabetes: a meta-analysis of randomized clinical trials. J Am Coll Cardiol 2005; 46: 821-826.
38. Bosch J, Yusuf S, Gerstein HC et al. Effect of ramipril on the incidence of diabetes. N Engl J Med 2006; 355: 1551-1562.
39. McMurray JJ, Holman RR, Haffner SM et al. Effect of valsartan on the incidence of diabetes and cardiovascular events. N Engl J Med 2010; 362: 1477-1490.
40. Tahmasebi M, Puddefoot JR, Inwang ER, Vinson GP. The tissue renin-angiotensin system in human pancreas. J Endocrinol 1999; 161: 317-322.
41. Huang Z, Jansson L, Sjoholm A. Vasoactive drugs enhance pancreatic islet blood flow, augment insulin secretion and improve glucose tolerance in female rats. Clin Sci (Lond) 2007; 112: 69-76.
42. Leung PS, Chan WP, Nobiling R. Regulated expression of pancreatic renin-angiotensin system in experimental pancreatitis. Mol Cell Endocrinol 2000; 166: 121-128.
43. Cai H, Li Z, Dikalov S et al. NAD(P)H oxidase-derived hydrogen peroxide mediates endothelial nitric oxide production in response to angiotensin II. J Biol Chem 2002; 277: 48311-48317.
44. Grankvist K, Marklund SL, Taljedal IB. CuZn-superoxide dismutase, Mn-superoxide dismutase, catalase and glutathione peroxidase in pancreatic islets and other tissues in the mouse. Biochem J 1981; 199: 393-398.
45. Evans JL, Goldfine ID, Maddux BA, Grodsky GM. Are oxidative stress-activated signaling pathways mediators of insulin resistance and beta-cell dysfunction? Diabetes 2003; 52: 1-8.
46. Green K, Brand MD, Murphy MP. Prevention of mitochondrial oxidative damage as a therapeutic strategy in diabetes. Diabetes 2004; 53(Suppl. 1): S110-S118.
47. Sakuraba H, Mizukami H, Yagihashi N, Wada R, Hanyu C, Yagihashi S. Reduced beta-cell mass and expression of oxidative stress-related DNA damage in the islet of Japanese Type II diabetic patients. Diabetologia 2002; 45: 85-96.
48. Schrauwen P, Hesselink MK. Oxidative capacity, lipotoxicity, and mitochondrial damage in type 2 diabetes. Diabetes 2004; 53: 1412-1417.
49. Lameloise N, Muzzin P, Prentki M, Assimacopoulos-Jeannet F. Uncoupling protein 2: a possible link between fatty acid excess and impaired glucose-induced insulin secretion? Diabetes 2001; 50: 803-809.
50. Medvedev AV, Robidoux J, Bai X et al. Regulation of the uncoupling protein-2 gene in INS-1 beta-cells by oleic acid. J Biol Chem 2002; 277: 42639-42644.
51. Shao J, Iwashita N, Ikeda F et al. Beneficial effects of candesartan, an angiotensin II type 1 receptor blocker, on beta-cell function and morphology in db/db mice. Biochem Biophys Res Commun 2006; 344: 1224-1233.
52. Chu KY, Leung PS. Angiotensin II Type 1 receptor antagonism mediates uncoupling protein 2-driven oxidative stress and ameliorates pancreatic islet beta-cell function in young Type 2 diabetic mice. Antioxid Redox Signal 2007; 9: 869-878.
53. Yuan L, Li X, Li J, Li HL, Cheng SS. Effects of renin-angiotensin system blockade on the islet morphology and function in rats with long-term high-fat diet. Acta Diabetol 2010; in press.
54. Donath MY, Ehses JA, Maedler K et al. Mechanisms of beta-cell death in type 2 diabetes. Diabetes 2005; 54(Suppl. 2): S108-S113.
55. Mandrup-Poulsen T. Beta-cell apoptosis: stimuli and signaling. Diabetes 2001; 50(Suppl. 1): S58-S63.
56. Johnson JD, Ahmed NT, Luciani DS et al. Increased islet apoptosis in Pdx1+/- mice. J Clin Invest 2003; 111: 1147-1160.
57. Tikellis C, Cooper ME, Thomas MC. Role of the renin-angiotensin system in the endocrine pancreas: implications for the development of diabetes. Int J Biochem Cell Biol 2006; 38: 737-751.
58. Ko SH, Kwon HS, Kim SR et al. Ramipril treatment suppresses islet fibrosis in Otsuka Long-Evans Tokushima fatty rats. Biochem Biophys Res Commun 2004; 316: 114-122.
59. Lupi R, Del GS, Bugliani M et al. The direct effects of the angiotensin-converting enzyme inhibitors, zofenoprilat and enalaprilat, on isolated human pancreatic islets. Eur J Endocrinol 2006; 154: 355-361.
60. Lam KY, Leung PS. Regulation and expression of a renin-angiotensin system in human pancreas and pancreatic endocrine tumours. Eur J Endocrinol 2002; 146: 567-572.
61. Ramracheya RD, Muller DS, Wu Y et al. Direct regulation of insulin secretion by angiotensin II in human islets of Langerhans. Diabetologia 2006; 49: 321-331.
62. Bokhari S, Israelian Z, Schmidt J, Brinton E, Meyer C. Effects of angiotensin II type 1 receptor blockade on beta-cell function in humans. Diabetes Care 2007; 30: 181.
63. Suzuki K, Nakagawa O, Aizawa Y. Improved early-phase insulin response after candesartan treatment in hypertensive patients with impaired glucose tolerance. Clin Exp Hypertens 2008; 30: 309-314.
64. Pollare T, 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.
65. van der Zijl NJ, Moors CC, Goossens GH, Hermans MM, Blaak EE, Diamant M. Valsartan improves beta-cell function and insulin sensitivity in subjects with impaired glucose metabolism: a randomized controlled trial. Diabetes Care 2011; 34: 845-851.
66. Goossens GH, Jocken JW, Blaak EE, Schiffers PM, Saris WH, van Baak MA. Endocrine role of the renin-angiotensin system in human adipose tissue and muscle: effect of beta-adrenergic stimulation. Hypertension 2007; 49: 542-547.
67. Stump CS, Henriksen EJ, Wei Y, Sowers JR. The metabolic syndrome: role of skeletal muscle metabolism. Ann Med 2006; 38: 389-402.
68. Barrett EJ, Eggleston EM, Inyard AC et al. The vascular actions of insulin control its delivery to muscle and regulate the rate-limiting step in skeletal muscle insulin action. Diabetologia 2009; 52: 752-764.
69. Goossens GH, Blaak EE, Saris WH, van Baak MA. Angiotensin II-induced effects on adipose and skeletal muscle tissue blood flow and lipolysis in normal-weight and obese subjects. J Clin Endocrinol Metab 2004; 89: 2690-2696.
70. Saris JJ, van Dijk MA, Kroon I, Schalekamp MA, Danser AH. Functional importance of angiotensin-converting enzyme-dependent in situ angiotensin II generation in the human forearm. Hypertension 2000; 35: 764-768.
71. Kodama J, Katayama S, Tanaka K, Itabashi A, Kawazu S, Ishii J. Effect of captopril on glucose concentration. Possible role of augmented postprandial forearm blood flow. Diabetes Care 1990; 13: 1109-1111.
72. Rizzoni D, Pasini E, Flati V et al. Angiotensin receptor blockers improve insulin signaling and prevent microvascular rarefaction in the skeletal muscle of spontaneously hypertensive rats. J Hypertens 2008; 26: 1595-1601.
73. Chai W, Wang W, Liu J et al. Angiotensin II type 1 and type 2 receptors regulate basal skeletal muscle microvascular volume and glucose use. Hypertension 2010; 55: 523-530.
74. Sabino B, Lessa MA, Nascimento AR et al. Effects of antihypertensive drugs on capillary rarefaction in spontaneously hypertensive rats: intravital microscopy and histologic analysis. J Cardiovasc Pharmacol 2008; 51: 402-409.
75. van der Zijl NJ, Serne EH, Goossens GH et al. Valsartan induced improvement of insulin sensitivity was not associated with improved microvascular function in subjects with impaired glucose metabolism. Diabetologia 2010; 53: S241.
76. Bjornholm M, Kawano Y, Lehtihet M, Zierath JR. Insulin receptor substrate-1 phosphorylation and phosphatidylinositol 3-kinase activity in skeletal muscle from NIDDM subjects after in vivo insulin stimulation. Diabetes 1997; 46: 524-527.
77. Goodyear LJ, Giorgino F, Sherman LA, Carey J, Smith RJ, Dohm GL. Insulin receptor phosphorylation, insulin receptor substrate-1 phosphorylation, and phosphatidylinositol 3-kinase activity are decreased in intact skeletal muscle strips from obese subjects. J Clin Invest 1995; 95: 2195-2204.
78. Krook A, Bjornholm M, Galuska D et al. Characterization of signal transduction and glucose transport in skeletal muscle from type 2 diabetic patients. Diabetes 2000; 49: 284-292.
79. Zierath JR, He L, Guma A, Odegoard WE, Klip A, Wallberg-Henriksson H. Insulin action on glucose transport and plasma membrane GLUT4 content in skeletal muscle from patients with NIDDM. Diabetologia 1996; 39: 1180-1189.
80. Blendea MC, Jacobs D, Stump CS et al. Abrogation of oxidative stress improves insulin sensitivity in the Ren-2 rat model of tissue angiotensin II overexpression. Am J Physiol Endocrinol Metab 2005; 288: E353-E359.
81. Folli F, Kahn CR, Hansen H, Bouchie JL, Feener EP. 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 1997; 100: 2158-2169.
82. Ogihara T, Asano T, Ando K et al. Angiotensin II-induced insulin resistance is associated with enhanced insulin signaling. Hypertension 2002; 40: 872-879.
83. Shiuchi T, Iwai M, Li HS et al. Angiotensin II type-1 receptor blocker valsartan enhances insulin sensitivity in skeletal muscles of diabetic mice. Hypertension 2004; 43: 1003-1010.
84. Wei Y, Sowers JR, Clark SE, Li W, Ferrario CM, Stump CS. Angiotensin II-induced skeletal muscle insulin resistance mediated by NF-kappaB activation via NADPH oxidase. Am J Physiol Endocrinol Metab 2008; 294: E345-E351.
85. Mitsuishi M, Miyashita K, Muraki A, Itoh H. Angiotensin II reduces mitochondrial content in skeletal muscle and affects glycemic control. Diabetes 2009; 58: 710-717.
86. Goossens GH. The role of adipose tissue dysfunction in the pathogenesis of obesity-related insulin resistance. Physiol Behav 2008; 94: 206-218.
87. Boden G, Chen X, Ruiz J, White JV, Rossetti L. Mechanisms of fatty acid-induced inhibition of glucose uptake. J Clin Invest 1994; 93: 2438-2446.
88. Roden M, Price TB, Perseghin G et al. Mechanism of free fatty acid-induced insulin resistance in humans. J Clin Invest 1996; 97: 2859-2865.
89. Erbe DV, Gartrell K, Zhang YL et al. Molecular activation of PPARgamma by angiotensin II type 1-receptor antagonists. Vascul Pharmacol 2006; 45: 154-162.
90. Engeli S, Negrel R, Sharma AM. Physiology and pathophysiology of the adipose tissue renin-angiotensin system. Hypertension 2000; 35: 1270-1277.
91. Giacchetti G, Faloia E, Mariniello B et al. Overexpression of the renin-angiotensin system in human visceral adipose tissue in normal and overweight subjects. Am J Hypertens 2002; 15: 381-388.
92. Levy BI, Schiffrin EL, Mourad JJ et al. Impaired tissue perfusion: a pathology common to hypertension, obesity, and diabetes mellitus. Circulation 2008; 118: 968-976.
93. Paolisso G, Tataranni PA, Foley JE, Bogardus C, Howard BV, Ravussin E. A high concentration of fasting plasma non-esterified fatty acids is a risk factor for the development of NIDDM. Diabetologia 1995; 38: 1213-1217.
94. Weyer C, Foley JE, Bogardus C, Tataranni PA, Pratley RE. Enlarged subcutaneous abdominal adipocyte size, but not obesity itself, predicts type II diabetes independent of insulin resistance. Diabetologia 2000; 43: 1498-1506.
95. Lundgren M, Svensson M, Lindmark S, Renstrom F, Ruge T, Eriksson JW. Fat cell enlargement is an independent marker of insulin resistance and 'hyperleptinaemia'. Diabetologia 2007; 50: 625-633.
96. Saiki A, Koide N, Watanabe F, Murano T, Miyashita Y, Shirai K. Suppression of lipoprotein lipase expression in 3T3-L1 cells by inhibition of adipogenic differentiation through activation of the renin-angiotensin system. Metabolism 2008; 57: 1093-1100.
97. Lee MH, Song HK, Ko GJ et al. Angiotensin receptor blockers improve insulin resistance in type 2 diabetic rats by modulating adipose tissue. Kidney Int 2008; 74: 890-900.
98. Tomono Y, Iwai M, Inaba S, Mogi M, Horiuchi M. Blockade of AT1 receptor improves adipocyte differentiation in atherosclerotic and diabetic models. Am J Hypertens 2008; 21: 206-212.
99. Janke J, Engeli S, Gorzelniak K, Luft FC, Sharma AM. Mature adipocytes inhibit in vitro differentiation of human preadipocytes via angiotensin type 1 receptors. Diabetes 2002; 51: 1699-1707.
100. Matsushita K, Wu Y, Okamoto Y, Pratt RE, Dzau VJ. Local renin angiotensin expression regulates human mesenchymal stem cell differentiation to adipocytes. Hypertension 2006; 48: 1095-1102.
101. Sarzani R, Marcucci P, Salvi F et al. Angiotensin II stimulates and atrial natriuretic peptide inhibits human visceral adipocyte growth. Int J Obes (Lond) 2008; 32: 259-267.
102. Crandall DL, Herzlinger HE, Saunders BD, Armellino DC, Kral JG. Distribution of angiotensin II receptors in rat and human adipocytes. J Lipid Res 1994; 35: 1378-1385.
103. Jones BH, Standridge MK, Moustaid N. Angiotensin II increases lipogenesis in 3T3-L1 and human adipose cells. Endocrinology 1997; 138: 1512-1519.
104. Goossens GH, Moors CCM, van der Zijl NJ, Cleutjens JP, Diamant M, Blaak EE. Long-term treatment with the angiotensin-receptor blocker valsartan improves adipose tissue function in normotensive subjects with impaired glucose metabolism. Diabetologia 2010; 53: 242.
105. Benson SC, Pershadsingh HA, Ho CI et al. Identification of telmisartan as a unique angiotensin II receptor antagonist with selective PPARgamma-modulating activity. Hypertension 2004; 43: 993-1002.
106. Picard F, Auwerx J. PPAR(gamma) and glucose homeostasis. Annu Rev Nutr 2002; 22: 167-197.
107. Fogari R, Zoppi A, Corradi L, Lazzari P, Mugellini A, Lusardi P. Comparative effects of lisinopril and losartan on insulin sensitivity in the treatment of non diabetic hypertensive patients. Br J Clin Pharmacol 1998; 46: 467-471.
108. Storka A, Vojtassakova E, Mueller M et al. Angiotensin inhibition stimulates PPARgamma and the release of visfatin. Eur J Clin Invest 2008; 38: 820-826.
109. Yao Y, Zou R, Liu X et al. Telmisartan but not valsartan inhibits TGF-beta-mediated accumulation of extracellular matrix via activation of PPARgamma. J Huazhong Univ Sci Technolog Med Sci 2008; 28: 543-548.
110. Jansson PA, Larsson A, Lonnroth PN. Relationship between blood pressure, metabolic variables and blood flow in obese subjects with or without non-insulin-dependent diabetes mellitus. Eur J Clin Invest 1998; 28: 813-818.
111. Summers LK, Samra JS, Humphreys SM, Morris RJ, Frayn KN. Subcutaneous abdominal adipose tissue blood flow: variation within and between subjects and relationship to obesity. Clin Sci (Lond) 1996; 91: 679-683.
112. Karpe F, Fielding BA, Ilic V, Macdonald IA, Summers LK, Frayn KN. Impaired postprandial adipose tissue blood flow response is related to aspects of insulin sensitivity. Diabetes 2002; 51: 2467-2473.
113. Edens NK, Leibel RL, Hirsch J. Mechanism of free fatty acid re-esterification in human adipocytes in vitro. J Lipid Res 1990; 31: 1423-1431.
114. Goossens GH, McQuaid SE, Dennis AL et al. Angiotensin II: a major regulator of subcutaneous adipose tissue blood flow in humans. J Physiol 2006; 571: 451-460.
115. Boschmann M, Adams F, Schaller K et al. Hemodynamic and metabolic responses to interstitial angiotensin II in normal weight and obese men. J Hypertens 2006; 24: 1165-1171.
116. Shoelson SE, Lee J, Goldfine AB. Inflammation and insulin resistance. J Clin Invest 2006; 116: 1793-1801.
117. Kim S, Whelan J, Claycombe K, Reath DB, Moustaid-Moussa N. Angiotensin II increases leptin secretion by 3T3-L1 and human adipocytes via a prostaglandin-independent mechanism. J Nutr 2002; 132: 1135-1140.
118. Skurk T, Lee YM, Hauner H. Angiotensin II and its metabolites stimulate PAI-1 protein release from human adipocytes in primary culture. Hypertension 2001; 37: 1336-1340.
119. Kurata A, Nishizawa H, Kihara S et al. Blockade of angiotensin II type-1 receptor reduces oxidative stress in adipose tissue and ameliorates adipocytokine dysregulation. Kidney Int 2006; 70: 1717-1724.
120. Zorad S, Dou JT, Benicky J et al. Long-term angiotensin II AT1 receptor inhibition produces adipose tissue hypotrophy accompanied by increased expression of adiponectin and PPARgamma. Eur J Pharmacol 2006; 552: 112-122.
121. Munoz MC, Giani JF, Dominici FP, Turyn D, Toblli JE. Long-term treatment with an angiotensin II receptor blocker decreases adipocyte size and improves insulin signaling in obese Zucker rats. J Hypertens 2009; 27: 2409-2420.
122. Miyazaki Y, Mahankali A, Wajcberg E, Bajaj M, Mandarino LJ, DeFronzo RA. Effect of pioglitazone on circulating adipocytokine levels and insulin sensitivity in type 2 diabetic patients. J Clin Endocrinol Metab 2004; 89: 4312-4319.
123. Yilmaz MI, Sonmez A, Caglar K et al. Effect of antihypertensive agents on plasma adiponectin levels in hypertensive patients with metabolic syndrome. Nephrology (Carlton) 2007; 12: 147-153.
124. Tian F, Luo R, Zhao Z, Wu Y, Ban D. Blockade of the RAS increases plasma adiponectin in subjects with metabolic syndrome and enhances differentiation and adiponectin expression of human preadipocytes. Exp Clin Endocrinol Diabetes 2010; 118: 258-265.
125. Nagel JM, Tietz AB, Goke B, Parhofer KG. The effect of telmisartan on glucose and lipid metabolism in nondiabetic, insulin-resistant subjects. Metabolism 2006; 55: 1149-1154.
126. Pscherer S, Heemann U, Frank H. Effect of renin-angiotensin system blockade on insulin resistance and inflammatory parameters in patients with impaired glucose tolerance. Diabetes Care 2010; 33: 914-919.
127. Furuhashi M, Ura N, Higashiura K et al. Blockade of the renin-angiotensin system increases adiponectin concentrations in patients with essential hypertension. Hypertension 2003; 42: 76-81.
128. Manabe S, Okura T, Watanabe S, Fukuoka T, Higaki J. Effects of angiotensin II receptor blockade with valsartan on pro-inflammatory cytokines in patients with essential hypertension. J Cardiovasc Pharmacol 2005; 46: 735-739.