The renin-angiotensin system: A link between obesity, inflammation and insulin resistance

Obesity Reviews

Volumn 13, Issue 2, 2012, Pages 136-149

  Kalupahana, N S ^a,b   Moustaid Moussa, N ^a  

^a UNIVERSITY OF TENNESSEE   (United States)

^b UNIVERSITY OF PERADENIYA   (Sri Lanka)

Author keywords

Adipose tissue; Insulin resistance; Renin angiotensin system

Indexed keywords

ACETYL COENZYME A; AMINOPEPTIDASE; ANGIOTENSIN; ANGIOTENSIN 1 RECEPTOR; ANGIOTENSIN 2 RECEPTOR; ANGIOTENSIN CONVERTING ENZYME 2; ANGIOTENSIN I; ANGIOTENSIN II [3-8]; ANGIOTENSIN III; ANGIOTENSINOGEN; CATHEPSIN; CHYMASE; DIPEPTIDYL CARBOXYPEPTIDASE; GLUCOSE 6 PHOSPHATE; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; INSULIN; INSULIN RECEPTOR SUBSTRATE 1; INTERLEUKIN 6; JANUS KINASE; MONOCYTE CHEMOTACTIC PROTEIN 1; PHOSPHATIDYLINOSITOL 3 KINASE; PRORENIN RECEPTOR; PYRUVIC ACID; REACTIVE OXYGEN METABOLITE; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE PHOSPHATE OXIDASE; RENIN; RESISTIN; STAT PROTEIN; SUPPRESSOR OF CYTOKINE SIGNALING 3; TUMOR NECROSIS FACTOR ALPHA;

ADIPOCYTE; ADIPOGENESIS; ADIPOSE TISSUE; BODY WEIGHT; DISEASE ASSOCIATION; GENE INACTIVATION; GENE TARGETING; HUMAN; INFLAMMATION; INSULIN RESISTANCE; INSULIN SENSITIVITY; LIPID DIET; LIPID STORAGE; NON INSULIN DEPENDENT DIABETES MELLITUS; NONHUMAN; OBESITY; PLASMA RENIN ACTIVITY; PROADIPOCYTE; RENIN ANGIOTENSIN ALDOSTERONE SYSTEM; REVIEW; VASOCONSTRICTION;

ANIMALS; BLOOD PRESSURE; BODY WEIGHT; DISEASE MODELS, ANIMAL; HUMANS; INFLAMMATION; INSULIN; INSULIN RESISTANCE; MICE; OBESITY; PANCREAS; RATS; RENIN-ANGIOTENSIN SYSTEM;

EID: 84855457188     PISSN: 14677881     EISSN: 1467789X     Source Type: Journal    
DOI: 10.1111/j.1467-789X.2011.00942.x     Document Type: Review

References (139)

1. Schmieder RE, Hilgers KF, Schlaich MP, Schmidt BM. Renin-angiotensin system and cardiovascular risk. Lancet 2007; 369: 1208-1219.
2. Castrop H, Hocherl K, Kurtz A, Schweda F, Todorov V, Wagner C. Physiology of kidney renin. Physiol Rev 2010; 90: 607-673.
3. Jones BH, Standridge MK, Taylor JW, Moustaid N. Angiotensinogen gene expression in adipose tissue: analysis of obese models and hormonal and nutritional control. Am J Physiol 1997; 273: R236-R242.
4. Paul M, Poyan Mehr A, Kreutz R. Physiology of local renin-angiotensin systems. Physiol Rev 2006; 86: 747-803.
5. Steckelings UM, Rompe F, Kaschina E, Unger T. The evolving story of the RAAS in hypertension, diabetes and CV disease: moving from macrovascular to microvascular targets. Fundam Clin Pharmacol 2009; 23: 693-703.
6. Thatcher S, Yiannikouris F, Gupte M, Cassis L. The adipose renin-angiotensin system: role in cardiovascular disease. Mol Cell Endocrinol 2009; 302: 111-117.
7. Sakai K, Sigmund CD. Molecular evidence of tissue renin-angiotensin systems: a focus on the brain. Curr Hypertens Rep 2005; 7: 135-140.
8. Lavoie JL, Sigmund CD. Minireview: overview of the renin-angiotensin system - an endocrine and paracrine system. Endocrinology 2003; 144: 2179-2183.
9. Yvan-Charvet L, Quignard-Boulange A. Role of adipose tissue renin-angiotensin system in metabolic and inflammatory diseases associated with obesity. Kidney Int 2011; 79: 162-168.
10. Vermes E, Ducharme A, Bourassa MG, Lessard M, White M, Tardif JC. Enalapril reduces the incidence of diabetes in patients with chronic heart failure: insight from the Studies of Left Ventricular Dysfunction (SOLVD). Circulation 2003; 107: 1291-1296.
11. Bosch J, Yusuf S, Gerstein HC, Pogue J, Sheridan P, Dagenais G etal. Effect of ramipril on the incidence of diabetes. N Engl J Med 2006; 355: 1551-1562.
12. Hansson L, Lindholm LH, Niskanen L, Lanke J, Hedner T, Niklason A etal. 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.
13. Yasue S, Masuzaki H, Okada S, Ishii T, Kozuka C, Tanaka T etal. Adipose tissue-specific regulation of angiotensinogen in obese humans and mice: impact of nutritional status and adipocyte hypertrophy. Am J Hypertens 2010; 23: 425-431.
14. Nguyen G, Delarue F, Burckle C, Bouzhir L, Giller T, Sraer JD. Pivotal role of the renin/prorenin receptor in angiotensin II production and cellular responses to renin. J Clin Invest 2002; 109: 1417-1427.
15. Santos RA, Simoes e Silva AC, Maric C, Silva DM, Machado RP, de Buhr I etal. Angiotensin-(1-7) is an endogenous ligand for the G protein-coupled receptor Mas. Proc Natl Acad Sci U S A 2003; 100: 8258-8263.
16. Karlsson C, Lindell K, Ottosson M, Sjostrom L, Carlsson B, Carlsson LM. Human adipose tissue expresses angiotensinogen and enzymes required for its conversion to angiotensin II. J Clin Endocrinol Metab 1998; 83: 3925-3929.
17. Engeli S, Bohnke J, Gorzelniak K, Janke J, Schling P, Bader M etal. Weight loss and the renin-angiotensin-aldosterone system. Hypertension 2005; 45: 356-362.
18. Uckaya G, Ozata M, Sonmez A, Kinalp C, Eyileten T, Bingol N etal. Plasma leptin levels strongly correlate with plasma renin activity in patients with essential hypertension. Horm Metab Res 1999; 31: 435-438.
19. Troisi RJ, Weiss ST, Parker DR, Sparrow D, Young JB, Landsberg L. Relation of obesity and diet to sympathetic nervous system activity. Hypertension 1991; 17: 669-677.
20. 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.
21. Gorzelniak K, Engeli S, Janke J, Luft FC, Sharma AM. Hormonal regulation of the human adipose-tissue renin-angiotensin system: relationship to obesity and hypertension. J Hypertens 2002; 20: 965-973.
22. Boustany CM, Bharadwaj K, Daugherty A, Brown DR, Randall DC, Cassis LA. Activation of the systemic and adipose renin-angiotensin system in rats with diet-induced obesity and hypertension. Am J Physiol Regul Integr Comp Physiol 2004; 287: R943-R949.
23. Frederich RC Jr, Kahn BB, Peach MJ, Flier JS. Tissue-specific nutritional regulation of angiotensinogen in adipose tissue. Hypertension 1992; 19: 339-344.
24. Kobori H, Katsurada A, Miyata K, Ohashi N, Satou R, Saito T etal. Determination of plasma and urinary angiotensinogen levels in rodents by newly developed ELISA. Am J Physiol Renal Physiol 2008; 294: F1257-F1263.
25. Tamura K, Umemura S, Yamakawa T, Nyui N, Hibi K, Watanabe Y etal. Modulation of tissue angiotensinogen gene expression in genetically obese hypertensive rats. Am J Physiol 1997; 272: R1704-R1711.
26. Hainault I, Nebout G, Turban S, Ardouin B, Ferre P, Quignard-Boulange A. Adipose tissue-specific increase in angiotensinogen expression and secretion in the obese (fa/fa) Zucker rat. Am J Physiol Endocrinol Metab 2002; 282: E59-E66.
27. Rahmouni K, Mark AL, Haynes WG, Sigmund CD. Adipose depot-specific modulation of angiotensinogen gene expression in diet-induced obesity. Am J Physiol Endocrinol Metab 2004; 286: E891-E895.
28. Massiera F, Bloch-Faure M, Ceiler D, Murakami K, Fukamizu A, Gasc JM etal. Adipose angiotensinogen is involved in adipose tissue growth and blood pressure regulation. FASEB J 2001; 15: 2727-2729.
29. Kim S, Soltani-Bejnood M, Quignard-Boulange A, Massiera F, Teboul M, Ailhaud G etal. The adipose renin-angiotensin system modulates systemic markers of insulin sensitivity and activates the intrarenal renin-angiotensin system. J Biomed Biotechnol 2006; 2006: 27012.
30. Voy BH, Kim S, Urs S, Joshi R, Moustaid-Moussa N. The adipose renin angiotensin system: genetics, regulation and physiological function. In: Moustaid-Moussa N, Berdanier CD (eds). Genomics and Proteomics in Nutrition. Marcel Dekker: New York, 2004, pp. 71-90.
31. Kim S, Urs S, Massiera F, Wortmann P, Joshi R, Heo YR etal. Effects of high-fat diet, angiotensinogen (agt) gene inactivation, and targeted expression to adipose tissue on lipid metabolism and renal gene expression. Horm Metab Res 2002; 34: 721-725.
32. Cassis L, Helton M, English V, Burke G. Angiotensin II regulates oxygen consumption. Am J Physiol Regul Integr Comp Physiol 2002; 282: R445-R453.
33. Brink M, Wellen J, Delafontaine P. Angiotensin II causes weight loss and decreases circulating insulin-like growth factor I in rats through a pressor-independent mechanism. J Clin Invest 1996; 97: 2509-2516.
34. Massiera F, Seydoux J, Geloen A, Quignard-Boulange A, Turban S, Saint-Marc P etal. Angiotensinogen-deficient mice exhibit impairment of diet-induced weight gain with alteration in adipose tissue development and increased locomotor activity. Endocrinology 2001; 142: 5220-5225.
35. Mathai ML, Naik S, Sinclair AJ, Weisinger HS, Weisinger RS. Selective reduction in body fat mass and plasma leptin induced by angiotensin-converting enzyme inhibition in rats. Int J Obes (Lond) 2008; 32: 1576-1584.
36. Lee MH, Song HK, Ko GJ, Kang YS, Han SY, Han KH etal. Angiotensin receptor blockers improve insulin resistance in type 2 diabetic rats by modulating adipose tissue. Kidney Int 2008; 74: 890-900.
37. Takahashi N, Li F, Hua K, Deng J, Wang CH, Bowers RR etal. Increased energy expenditure, dietary fat wasting, and resistance to diet-induced obesity in mice lacking renin. Cell Metab 2007; 6: 506-512.
38. Jayasooriya AP, Mathai ML, Walker LL, Begg DP, Denton DA, Cameron-Smith D etal. Mice lacking angiotensin-converting enzyme have increased energy expenditure, with reduced fat mass and improved glucose clearance. Proc Natl Acad Sci U S A 2008; 105: 6531-6536.
39. Kouyama R, Suganami T, Nishida J, Tanaka M, Toyoda T, Kiso M etal. Attenuation of diet-induced weight gain and adiposity through increased energy expenditure in mice lacking angiotensin II type 1a receptor. Endocrinology 2005; 146: 3481-3489.
40. Yvan-Charvet L, Even P, Bloch-Faure M, Guerre-Millo M, Moustaid-Moussa N, Ferre P etal. Deletion of the angiotensin type 2 receptor (AT2R) reduces adipose cell size and protects from diet-induced obesity and insulin resistance. Diabetes 2005; 54: 991-999.
41. Santos SH, Fernandes LR, Mario EG, Ferreira AV, Porto LC, Alvarez-Leite JI etal. Mas deficiency in FVB/N mice produces marked changes in lipid and glycemic metabolism. Diabetes 2008; 57: 340-347.
42. Schenk S, Saberi M, Olefsky JM. Insulin sensitivity: modulation by nutrients and inflammation. J Clin Invest 2008; 118: 2992-3002.
43. Olefsky JM, Glass CK. Macrophages, inflammation, and insulin resistance. Annu Rev Physiol 2010; 72: 219-246.
44. Stumvoll M, Goldstein BJ, van Haeften TW. Type 2 diabetes: principles of pathogenesis and therapy. Lancet 2005; 365: 1333-1346.
45. Bonnet F, Patel S, Laville M, Balkau B, Favuzzi A, Monti LD etal. Influence of the ACE gene insertion/deletion polymorphism on insulin sensitivity and impaired glucose tolerance in healthy subjects. Diabetes Care 2008; 31: 789-794.
46. Cong ND, Hamaguchi K, Saikawa T, Hara M, Sakata T. The I/D polymorphism of angiotensin-converting enzyme gene but not the angiotensinogen gene is associated with insulin response to oral glucose in Japanese. Proc Soc Exp Biol Med 1999; 220: 46-51.
47. Han T, Wang X, Cui Y, Ye H, Tong X, Piao M. Relationship between angiotensin-converting enzyme gene insertion or deletion polymorphism and insulin sensitivity in healthy newborns. Pediatrics 2007; 119: 1089-1094.
48. Pollex RL, Hanley AJ, Zinman B, Harris SB, Khan HM, Hegele RA. Metabolic syndrome in aboriginal Canadians: prevalence and genetic associations. Atherosclerosis 2006; 184: 121-129.
49. Schlemm L, Haumann HM, Ziegner M, Stirnberg B, Sohn A, Alter M etal. New evidence for the fetal insulin hypothesis: fetal angiotensinogen M235T polymorphism is associated with birth weight and elevated fetal total glycated hemoglobin at birth. J Hypertens 2010; 28: 732-739.
50. Miyanaga K, Fukuo K, Akasaka H, Katsuya T, Fukada R, Rakugi H etal. C allele of angiotensin II type 1 receptor gene A1166C polymorphism affects plasma adiponectin concentrations in healthy young Japanese women. Hypertens Res 2009; 32: 901-905.
51. Mehri S, Koubaa N, Hammami S, Mahjoub S, Chaaba R, Nakbi A etal. Genotypic interactions of renin-angiotensin system genes with diabetes type 2 in a Tunisian population. Life Sci 2010; 87: 49-54.
52. Yusuf S, Gerstein H, Hoogwerf B, Pogue J, Bosch J, Wolffenbuttel BH etal. Ramipril and the development of diabetes. JAMA 2001; 286: 1882-1885.
53. 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.
54. Iwai M, Kanno H, Tomono Y, Inaba S, Senba I, Furuno M etal. Direct renin inhibition improved insulin resistance and adipose tissue dysfunction in type 2 diabetic KK-A(y) mice. J Hypertens 2010; 28: 1471-1481.
55. Ran J, Hirano T, Adachi M. Chronic ANG II infusion increases plasma triglyceride level by stimulating hepatic triglyceride production in rats. Am J Physiol Endocrinol Metab 2004; 287: E955-E961.
56. Buchanan TA, Thawani H, Kades W, Modrall JG, Weaver FA, Laurel C etal. Angiotensin II increases glucose utilization during acute hyperinsulinemia via a hemodynamic mechanism. J Clin Invest 1993; 92: 720-726.
57. Juan CC, Chien Y, Wu LY, Yang WM, Chang CL, Lai YH etal. Angiotensin II enhances insulin sensitivity in vitro and in vivo. Endocrinology 2005; 146: 2246-2254.
58. Fliser D, Arnold U, Kohl B, Hartung R, Ritz E. Angiotensin II enhances insulin sensitivity in healthy volunteers under euglycemic conditions. J Hypertens 1993; 11: 983-988.
59. Ogihara T, Asano T, Ando K, Chiba Y, Sakoda H, Anai M etal. Angiotensin II-induced insulin resistance is associated with enhanced insulin signaling. Hypertension 2002; 40: 872-879.
60. Sloniger JA, Saengsirisuwan V, Diehl CJ, Dokken BB, Lailerd N, Lemieux AM etal. Defective insulin signaling in skeletal muscle of the hypertensive TG(mREN2)27 rat. Am J Physiol Endocrinol Metab 2005; 288: E1074-E1081.
61. Lastra G, Habibi J, Whaley-Connell AT, Manrique C, Hayden MR, Rehmer J etal. Direct renin inhibition improves systemic insulin resistance and skeletal muscle glucose transport in a transgenic rodent model of tissue renin overexpression. Endocrinology 2009; 150: 2561-2568.
62. Sloniger JA, Saengsirisuwan V, Diehl CJ, Kim JS, Henriksen EJ. Selective angiotensin II receptor antagonism enhances whole-body insulin sensitivity and muscle glucose transport in hypertensive TG(mREN2)27 rats. Metabolism 2005; 54: 1659-1668.
63. Soltani-Bejnood M, Fletcher S, Morris J, Das S, Voy BH, Moustaid-Moussa N. Overexpression of renin in the liver impairs glucose tolerance. FASEB J 2007; 21: A831.
64. Kalupahana NS, Massiera F, Quignard-Boulange A, Ailhaud G, Voy BH, Wasserman D etal. Overproduction of angiotensinogen from adipose tissue induces adipose inflammation, glucose intolerance and insulin resistance. Obesity (Silver Spring) 2011; doi:10.1038/oby.2011.299.
65. Wasserman DH. Four grams of glucose. Am J Physiol Endocrinol Metab 2009; 296: E11-E21.
66. 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.
67. Wei Y, Sowers JR, Nistala R, Gong H, Uptergrove GM, Clark SE etal. Angiotensin II-induced NADPH oxidase activation impairs insulin signaling in skeletal muscle cells. J Biol Chem 2006; 281: 35137-35146.
68. 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.
69. Marrero MB, Fulton D, Stepp D, Stern DM. Angiotensin II-induced insulin resistance and protein tyrosine phosphatases. Arterioscler Thromb Vasc Biol 2004; 24: 2009-2013.
70. Calegari VC, Alves M, Picardi PK, Inoue RY, Franchini KG, Saad MJ etal. Suppressor of cytokine signaling-3 provides a novel interface in the cross-talk between angiotensin II and insulin signaling systems. Endocrinology 2005; 146: 579-588.
71. 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.
72. Henriksen EJ, Jacob S. Angiotensin converting enzyme inhibitors and modulation of skeletal muscle insulin resistance. Diabetes Obes Metab 2003; 5: 214-222.
73. Rao RH. Pressor doses of angiotensin II increase hepatic glucose output and decrease insulin sensitivity in rats. J Endocrinol 1996; 148: 311-318.
74. Toblli JE, Munoz MC, Cao G, Mella J, Pereyra L, Mastai R. ACE inhibition and AT1 receptor blockade prevent fatty liver and fibrosis in obese Zucker rats. Obesity (Silver Spring) 2008; 16: 770-776.
75. 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.
76. Bindom SM, Lazartigues E. The sweeter side of ACE2: physiological evidence for a role in diabetes. Mol Cell Endocrinol 2009; 302: 193-202.
77. Bindom SM, Hans CP, Xia H, Boulares AH, Lazartigues E. Angiotensin I-converting enzyme type 2 (ACE2) gene therapy improves glycemic control in diabetic mice. Diabetes 2010; 59: 2540-2548.
78. Kim S, Voy BH, Huang T, Koontz J, Quignard-Boulange A, Hayser P etal. Angiotensin II regulates adipocyte metabolism via insulin signaling molecules. Adipocytes 2005; 1: 239-248.
79. Harte A, McTernan P, Chetty R, Coppack S, Katz J, Smith S etal. Insulin-mediated upregulation of the renin angiotensin system in human subcutaneous adipocytes is reduced by rosiglitazone. Circulation 2005; 111: 1954-1961.
80. Ran J, Hirano T, Fukui T, Saito K, Kageyama H, Okada K etal. Angiotensin II infusion decreases plasma adiponectin level via its type 1 receptor in rats: an implication for hypertension-related insulin resistance. Metabolism 2006; 55: 478-488.
81. Serazin-Leroy V, Morot M, de Mazancourt P, Giudicelli Y. Androgen regulation and site specificity of angiotensinogen gene expression and secretion in rat adipocytes. Am J Physiol Endocrinol Metab 2000; 279: E1398-E1405.
82. Kalupahana NS, Claycombe K, Moustaid-Moussa N. (n-3) fatty acids alleviate adipose tissue inflammation and insulin resistance: mechanistic insights. Adv Nutr 2011; 2: 304-316.
83. Nishimura S, Manabe I, Nagasaki M, Eto K, Yamashita H, Ohsugi M etal. CD8+ effector T cells contribute to macrophage recruitment and adipose tissue inflammation in obesity. Nat Med 2009; 15: 914-920.
84. Lumeng CN, Maillard I, Saltiel AR. T-ing up inflammation in fat. Nat Med 2009; 15: 846-847.
85. Danforth E Jr. Failure of adipocyte differentiation causes type II diabetes mellitus? Nat Genet 2000; 26: 13.
86. Fowler JD, Krueth SB, Bernlohr DA, Katz SA. Renin dynamics in adipose tissue: adipose tissue control of local renin concentrations. Am J Physiol Endocrinol Metab 2009; 296: E343-E350.
87. Safonova I, Aubert J, Negrel R, Ailhaud G. Regulation by fatty acids of angiotensinogen gene expression in preadipose cells. Biochem J 1997; 322(Pt 1): 235-239.
88. Chen X, Zhang SL, Pang L, Filep JG, Tang SS, Ingelfinger JR etal. Characterization of a putative insulin-responsive element and its binding protein(s) in rat angiotensinogen gene promoter: regulation by glucose and insulin. Endocrinology 2001; 142: 2577-2585.
89. Brasier AR, Li J. Mechanisms for inducible control of angiotensinogen gene transcription. Hypertension 1996; 27: 465-475.
90. Gabriely I, Yang XM, Cases JA, Ma XH, Rossetti L, Barzilai N. Hyperglycemia modulates angiotensinogen gene expression. Am J Physiol Regul Integr Comp Physiol 2001; 281: R795-R802.
91. Einstein FH, Fishman S, Bauman J, Thompson RF, Huffman DM, Atzmon G etal. Enhanced activation of a 'nutrient-sensing' pathway with age contributes to insulin resistance. FASEB J 2008; 22: 3450-3457.
92. 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.
93. Yvan-Charvet L, Even P, Lamande N, Ferre P, Quignard-Boulange A. Prevention of adipose tissue depletion during food deprivation in angiotensin type 2 receptor-deficient mice. Endocrinology 2006; 147: 5078-5086.
94. Jones BH, Standridge MK, Moustaid N. Angiotensin II increases lipogenesis in 3T3-L1 and human adipose cells. Endocrinology 1997; 138: 1512-1519.
95. Prat-Larquemin L, Oppert JM, Clement K, Hainault I, Basdevant A, Guy-Grand B etal. Adipose angiotensinogen secretion, blood pressure, and AGT M235T polymorphism in obese patients. Obes Res 2004; 12: 556-561.
96. Karelis AD, St-Pierre DH, Conus F, Rabasa-Lhoret R, Poehlman ET. Metabolic and body composition factors in subgroups of obesity: what do we know? J Clin Endocrinol Metab 2004; 89: 2569-2575.
97. Kalupahana NS, Moustaid-Moussa N. Overview of symposium 'systems genetics in nutrition and obesity research'. J Nutr 2011; 141: 512-514.
98. Gustafson B, Gogg S, Hedjazifar S, Jenndahl L, Hammarstedt A, Smith U. Inflammation and impaired adipogenesis in hypertrophic obesity in man. Am J Physiol Endocrinol Metab 2009; 297: E999-E1003.
99. Furuhashi M, Ura N, Takizawa H, Yoshida D, Moniwa N, Murakami H etal. Blockade of the renin-angiotensin system decreases adipocyte size with improvement in insulin sensitivity. J Hypertens 2004; 22: 1977-1982.
100. 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.
101. Zorad S, Dou JT, Benicky J, Hutanu D, Tybitanclova K, Zhou J etal. 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.
102. Schupp M, Janke J, Clasen R, Unger T, Kintscher U. Angiotensin type 1 receptor blockers induce peroxisome proliferator-activated receptor-gamma activity. Circulation 2004; 109: 2054-2057.
103. Schupp M, Lee LD, Frost N, Umbreen S, Schmidt B, Unger T etal. Regulation of peroxisome proliferator-activated receptor gamma activity by losartan metabolites. Hypertension 2006; 47: 586-589.
104. Yvan-Charvet L, Massiera F, Lamande N, Ailhaud G, Teboul M, Moustaid-Moussa N etal. Deficiency of angiotensin type 2 receptor rescues obesity but not hypertension induced by overexpression of angiotensinogen in adipose tissue. Endocrinology 2009; 150: 1421-1428.
105. Darimont C, Vassaux G, Ailhaud G, Negrel R. Differentiation of preadipose cells: paracrine role of prostacyclin upon stimulation of adipose cells by angiotensin-II. Endocrinology 1994; 135: 2030-2036.
106. 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.
107. 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.
108. Brucher R, Cifuentes M, Acuna MJ, Albala C, Rojas CV. Larger anti-adipogenic effect of angiotensin II on omental preadipose cells of obese humans. Obesity (Silver Spring) 2007; 15: 1643-1646.
109. Fuentes P, Acuna MJ, Cifuentes M, Rojas CV. The anti-adipogenic effect of angiotensin II on human preadipose cells involves ERK1, 2 activation and PPARG phosphorylation. J Endocrinol 2010; 206: 75-83.
110. 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.
111. Hollenberg NK, Stevanovic R, Agarwal A, Lansang MC, Price DA, Laffel LM etal. Plasma aldosterone concentration in the patient with diabetes mellitus. Kidney Int 2004; 65: 1435-1439.
112. Kalupahana NS, Claycombe K, Newman SJ, Stewart T, Siriwardhana N, Matthan N etal. Eicosapentaenoic acid prevents and reverses insulin resistance in high-fat diet-induced obese mice via modulation of adipose tissue inflammation. J Nutr 2010; 140: 1915-1922.
113. Kalupahana NS, Voy BH, Saxton AM, Moustaid-Moussa N. Energy-restricted high-fat diets only partially improve markers of systemic and adipose tissue inflammation. Obesity (Silver Spring) 2011; 19: 245-254.
114. Skurk T, van Harmelen V, Hauner H. Angiotensin II stimulates the release of interleukin-6 and interleukin-8 from cultured human adipocytes by activation of NF-kappaB. Arterioscler Thromb Vasc Biol 2004; 24: 1199-1203.
115. Asamizu S, Urakaze M, Kobashi C, Ishiki M, Norel Din AK, Fujisaka S etal. Angiotensin II enhances the increase in monocyte chemoattractant protein-1 production induced by tumor necrosis factor-{alpha} from 3T3-L1 preadipocytes. J Endocrinol 2009; 202: 199-205.
116. Cooper R, Forrester T, Ogunbiyi O, Muffinda J. Angiotensinogen levels and obesity in four black populations. ICSHIB Investigators. J Hypertens 1998; 16: 571-575.
117. Schorr U, Blaschke K, Turan S, Distler A, Sharma AM. Relationship between angiotensinogen, leptin and blood pressure levels in young normotensive men. J Hypertens 1998; 16: 1475-1480.
118. Bloem LJ, Manatunga AK, Tewksbury DA, Pratt JH. The serum angiotensinogen concentration and variants of the angiotensinogen gene in white and black children. J Clin Invest 1995; 95: 948-953.
119. Umemura S, Nyui N, Tamura K, Hibi K, Yamaguchi S, Nakamaru M etal. Plasma angiotensinogen concentrations in obese patients. Am J Hypertens 1997; 10: 629-633.
120. Cooper R, McFarlane-Anderson N, Bennett FI, Wilks R, Puras A, Tewksbury D etal. ACE, angiotensinogen and obesity: a potential pathway leading to hypertension. J Hum Hypertens 1997; 11: 107-111.
121. Faloia E, Gatti C, Camilloni MA, Mariniello B, Sardu C, Garrapa GG etal. Comparison of circulating and local adipose tissue renin-angiotensin system in normotensive and hypertensive obese subjects. J Endocrinol Invest 2002; 25: 309-314.
122. Licata G, Scaglione R, Ganguzza A, Corrao S, Donatelli M, Parrinello G etal. Central obesity and hypertension. Relationship between fasting serum insulin, plasma renin activity, and diastolic blood pressure in young obese subjects. Am J Hypertens 1994; 7: 314-320.
123. Egan BM, Stepniakowski K, Goodfriend TL. Renin and aldosterone are higher and the hyperinsulinemic effect of salt restriction greater in subjects with risk factors clustering. Am J Hypertens 1994; 7: 886-893.
124. Van Harmelen V, Ariapart P, Hoffstedt J, Lundkvist I, Bringman S, Arner P. Increased adipose angiotensinogen gene expression in human obesity. Obes Res 2000; 8: 337-341.
125. Giacchetti G, Faloia E, Sardu C, Camilloni MA, Mariniello B, Gatti C etal. Gene expression of angiotensinogen in adipose tissue of obese patients. Int J Obes Relat Metab Disord 2000; 24(Suppl. 2): S142-S143.
126. van Harmelen V, Elizalde M, Ariapart P, Bergstedt-Lindqvist S, Reynisdottir S, Hoffstedt J etal. The association of human adipose angiotensinogen gene expression with abdominal fat distribution in obesity. Int J Obes Relat Metab Disord 2000; 24: 673-678.
127. Coelho MS, Lopes KL, Freitas Rde A, de Oliveira-Sales EB, Bergasmaschi CT, Campos RR etal. High sucrose intake in rats is associated with increased ACE2 and angiotensin-(1-7) levels in the adipose tissue. Regul Pept 2010; 162: 61-67.
128. Dobrian AD, Davies MJ, Prewitt RL, Lauterio TJ. Development of hypertension in a rat model of diet-induced obesity. Hypertension 2000; 35: 1009-1015.
129. Harker CT, O'Donnell MP, Kasiske BL, Keane WF, Katz SA. The renin-angiotensin system in the type II diabetic obese Zucker rat. J Am Soc Nephrol 1993; 4: 1354-1361.
130. Alonso-Galicia M, Brands MW, Zappe DH, Hall JE. Hypertension in obese Zucker rats. Role of angiotensin II and adrenergic activity. Hypertension 1996; 28: 1047-1054.
131. Juan CC, Au LC, Fang VS, Kang SF, Ko YH, Kuo SF etal. Suppressed gene expression of adipocyte resistin in an insulin-resistant rat model probably by elevated free fatty acids. Biochem Biophys Res Commun 2001; 289: 1328-1333.
132. Giacchetti G, Sechi LA, Griffin CA, Don BR, Mantero F, Schambelan M. The tissue renin-angiotensin system in rats with fructose-induced hypertension: overexpression of type 1 angiotensin II receptor in adipose tissue. J Hypertens 2000; 18: 695-702.
133. Cassis LA, Fettinger MJ, Roe AL, Shenoy UR, Howard G. Characterization and regulation of angiotensin II receptors in rat adipose tissue. Angiotensin receptors in adipose tissue. Adv Exp Med Biol 1996; 396: 39-47.
134. Granger JP, West D, Scott J. Abnormal pressure natriuresis in the dog model of obesity-induced hypertension. Hypertension 1994; 23: I8-11.
135. Morris AD, Petrie JR, Ueda S, Connell JM, Elliott HL, Small M etal. Pressor and subpressor doses of angiotensin II increase insulin sensitivity in NIDDM. Dissociation of metabolic and blood pressure effects. Diabetes 1994; 43: 1445-1449.
136. Jonk AM, Houben AJ, Schaper NC, de Leeuw PW, Serne EH, Smulders YM etal. Angiotensin II enhances insulin-stimulated whole-body glucose disposal but impairs insulin-induced capillary recruitment in healthy volunteers. J Clin Endocrinol Metab 2010; 95: 3901-3908.
137. Cassis LA, Marshall DE, Fettinger MJ, Rosenbluth B, Lodder RA. Mechanisms contributing to angiotensin II regulation of body weight. Am J Physiol 1998; 274: E867-E876.
138. Giani JF, Mayer MA, Munoz MC, Silberman EA, Hocht C, Taira CA etal. Chronic infusion of angiotensin-(1-7) improves insulin resistance and hypertension induced by a high-fructose diet in rats. Am J Physiol Endocrinol Metab 2009; 296: E262-E271.
139. 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.