Chronic blockade of angiotensin AT1 receptors improves cardinal symptoms of metabolic syndrome in diet-induced obesity in rats

British Journal of Pharmacology

Volumn 171, Issue 3, 2014, Pages 746-760

  Müller Fielitz, Helge ^a,b   Hübel, Nils ^a   Mildner, Martin ^a   Vogt, Florian M ^a   Barkhausen, Jörg ^a   Raasch, Walter ^a,b  

^a UNIVERSITY OF LÜBECK   (Germany)

^b DZHK GERMAN CENTRE FOR CARDIOVASCULAR RESEARCH   (Germany)

Author keywords

AT1 receptor blockade; leptin resistance; metabolic syndrome; obesity; rat; telmisartan; weight loss

Indexed keywords

AMLODIPINE; AMLODIPINE PLUS TELMISARTAN; ANGIOTENSIN 1 RECEPTOR; FATTY ACID; INSULIN; LEPTIN; LOW DENSITY LIPOPROTEIN; TELMISARTAN; TRIACYLGLYCEROL;

ABDOMINAL FAT; ANIMAL EXPERIMENT; ANIMAL MODEL; ANTI OBESITY ACTIVITY; ARTICLE; BLOOD PRESSURE REGULATION; CALORIC INTAKE; CONTROLLED STUDY; DIETARY INTAKE; DOSE RESPONSE; DRUG ACTIVITY; DRUG MEGADOSE; FAT MASS; FATTY ACID BLOOD LEVEL; FEEDING BEHAVIOR; GLUCOSE UTILIZATION; HORMONE RESISTANCE; HYPERLIPIDEMIA; HYPERPHAGIA; INSULIN RESISTANCE; LEPTIN RESISTANCE; LIPOPROTEIN BLOOD LEVEL; LUNG GAS EXCHANGE; MALE; METABOLIC SYNDROME X; NONHUMAN; OBESITY; PRIORITY JOURNAL; RAT; RECEPTOR BLOCKING; RESPIRATORY RATIO; RESPIRATORY TRACT PARAMETERS; SPONTANEOUSLY HYPERTENSIVE RAT; TREATMENT DURATION; TRIACYLGLYCEROL BLOOD LEVEL; WEIGHT GAIN;

AT1-RECEPTOR BLOCKADE; LEPTIN RESISTANCE; METABOLIC SYNDROME; OBESITY; RAT; TELMISARTAN; WEIGHT LOSS;

AMLODIPINE; ANGIOTENSIN II TYPE 1 RECEPTOR BLOCKERS; ANIMALS; ANTI-OBESITY AGENTS; ANTIHYPERTENSIVE AGENTS; BEHAVIOR, ANIMAL; BENZIMIDAZOLES; BENZOATES; DIET, HIGH-FAT; DIETARY SUCROSE; DRUG THERAPY, COMBINATION; ENERGY INTAKE; HYPERLIPIDEMIAS; HYPERTENSION; HYPOLIPIDEMIC AGENTS; INSULIN RESISTANCE; LEPTIN; MALE; METABOLIC SYNDROME X; OBESITY; RANDOM ALLOCATION; RATS; RATS, INBRED SHR; WEIGHT GAIN;

EID: 84892415944     PISSN: 00071188     EISSN: 14765381     Source Type: Journal    
DOI: 10.1111/bph.12510     Document Type: Article

References (65)

1. Alexander SPH, et al. (2013). The Concise Guide to PHARMACOLOGY 2013/14: Overview. Br J Pharmacol 170: 1449-1867.
2. Araki K, Masaki T, Katsuragi I, Tanaka K, Kakuma T, Yoshimatsu H, (2006). Telmisartan prevents obesity and increases the expression of uncoupling protein 1 in diet-induced obese mice. Hypertension 48: 51-57.
3. Banks WA, Farrell CL, (2003). Impaired transport of leptin across the blood-brain barrier in obesity is acquired and reversible. Am J Physiol Endocrinol Metab 285: E10-E15.
4. Banks WA, DiPalma CR, Farrell CL, (1999). Impaired transport of leptin across the blood-brain barrier in obesity. Peptides 20: 1341-1345.
5. Banks WA, Coon AB, Robinson SM, Moinuddin A, Shultz JM, Nakaoke R, et al. (2004). Triglycerides induce leptin resistance at the blood-brain barrier. Diabetes 53: 1253-1260.
6. Barseghian G, Levine R, (1980). Effect of corticosterone on insulin and glucagon secretion by the isolated perfused rat pancreas. Endocrinology 106: 547-552.
7. Benson SC, Pershadsingh HA, Ho CI, Chittiboyina A, Desai P, Pravenec M, et al. (2004). Identification of telmisartan as a unique angiotensin II receptor antagonist with selective PPARgamma-modulating activity. Hypertension 43: 993-1002.
8. 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.
9. Brink M, Wellen J, Delafontaine P, (1996). Angiotensin II causes weight loss and decreases circulating insulin-like growth factor I in rats through a pressor-independent mechanism. J Clin Invest 97: 2509-2516.
10. Cabassi A, Coghi P, Govoni P, Barouhiel E, Speroni E, Cavazzini S, et al. (2005). Sympathetic modulation by carvedilol and losartan reduces angiotensin II-mediated lipolysis in subcutaneous and visceral fat. J Clin Endocrinol Metab 90: 2888-2897.
11. Cassis LA, English VL, Bharadwaj K, Boustany CM, (2004). Differential effects of local versus systemic angiotensin II in the regulation of leptin release from adipocytes. Endocrinology 145: 169-174.
12. Chodobski A, Szmydynger-Chodobska J, (2001). Choroid plexus: target for polypeptides and site of their synthesis. Microsc Res Tech 52: 65-82.
13. Clasen R, Schupp M, Foryst-Ludwig A, Sprang C, Clemenz M, Krikov M, et al. (2005). PPARgamma-activating angiotensin type-1 receptor blockers induce adiponectin. Hypertension 46: 137-143.
14. Cole BK, Keller SR, Wu R, Carter JD, Nadler JL, Nunemaker CS, (2010). Valsartan protects pancreatic islets and adipose tissue from the inflammatory and metabolic consequences of a high-fat diet in mice. Hypertension 55: 715-721.
15. Davani B, Portwood N, Bryzgalova G, Reimer MK, Heiden T, Ostenson CG, et al. (2004). Aged transgenic mice with increased glucocorticoid sensitivity in pancreatic beta-cells develop diabetes. Diabetes 53 (Suppl. 1): S51-S59.
16. Delaunay F, Khan A, Cintra A, Davani B, Ling ZC, Andersson A, et al. (1997). Pancreatic beta cells are important targets for the diabetogenic effects of glucocorticoids. J Clin Invest 100: 2094-2098.
17. Engeli S, Gorzelniak K, Kreutz R, Runkel N, Distler A, Sharma AM, (1999). Co-expression of renin-angiotensin system genes in human adipose tissue. J Hypertens 17: 555-560.
18. Engeli S, Bohnke J, Gorzelniak K, Janke J, Schling P, Bader M, et al. (2005). Weight loss and the renin-angiotensin-aldosterone system. Hypertension 45: 356-362.
19. Frederich RC, Hamann A, Anderson S, Lollmann B, Lowell BB, Flier JS, (1995). Leptin levels reflect body lipid content in mice: evidence for diet-induced resistance to leptin action. Nat Med 1: 1311-1314.
20. Friedman JM, (2009). Leptin at 14 y of age: an ongoing story. Am J Clin Nutr 89: 973S-979S.
21. Gembardt F, Heringer-Walther S, van Esch JH, Sterner-Kock A, van Veghel R, Le TH, et al. (2008). Cardiovascular phenotype of mice lacking all three subtypes of angiotensin II receptors. FASEB J 22: 3068-3077.
22. Giacchetti G, Faloia E, Mariniello B, Sardu C, Gatti C, Camilloni MA, et al. (2002). Overexpression of the renin-angiotensin system in human visceral adipose tissue in normal and overweight subjects. Am J Hypertens 15: 381-388.
23. Harte A, McTernan P, Chetty R, Coppack S, Katz J, Smith S, et al. (2005). Insulin-mediated upregulation of the renin angiotensin system in human subcutaneous adipocytes is reduced by rosiglitazone. Circulation 111: 1954-1961.
24. He H, Yang D, Ma L, Luo Z, Ma S, Feng X, et al. (2010). Telmisartan prevents weight gain and obesity through activation of peroxisome proliferator-activated receptor-delta-dependent pathways. Hypertension 55: 869-879.
25. Jöhren O, Saavedra JM, (1996). Expression of AT1A and AT1B angiotensin II receptor messenger RNA in forebrain of 2-wk-old rats. Am J Physiol 271: E104-E112.
26. Kadowaki T, Yamauchi T, Kubota N, (2008). The physiological and pathophysiological role of adiponectin and adiponectin receptors in the peripheral tissues and CNS. FEBS Lett 582: 74-80.
27. Karlsson C, Lindell K, Ottosson M, Sjostrom L, Carlsson B, Carlsson LM, (1998). Human adipose tissue expresses angiotensinogen and enzymes required for its conversion to angiotensin II. J Clin Endocrinol Metab 83: 3925-3929.
28. Kieffer TJ, Habener JF, (2000). The adipoinsular axis: effects of leptin on pancreatic beta-cells. Am J Physiol Endocrinol Metab 278: E1-E14.
29. Kilkenny C, Browne W, Cuthill IC, Emerson M, Altman DG, (2010). Animal research: reporting in vivo experiments: the ARRIVE guidelines. Br J Pharmacol 160: 1577-1579.
30. Kim S, Whelan J, Claycombe K, Reath DB, Moustaid-Moussa N, (2002). Angiotensin II increases leptin secretion by 3T3-L1 and human adipocytes via a prostaglandin-independent mechanism. J Nutr 132: 1135-1140.
31. Kintscher U, Unger T, (2005). Vascular protection in diabetes: a pharmacological view of angiotensin II type 1 receptor blockers. Acta Diabetol 42 (Suppl. 1): S26-S32.
32. Kintscher U, Foryst-Ludwig A, Unger T, (2008). Inhibiting angiotensin type 1 receptors as a target for diabetes. Expert Opin Ther Targets 12: 1257-1263.
33. Kohya T, Yokoshiki H, Tohse N, Kanno M, Nakaya H, Saito H, et al. (1995). Regression of left ventricular hypertrophy prevents ischemia-induced lethal arrhythmias. Beneficial effect of angiotensin II blockade. Circ Res 76: 892-899.
34. Konner AC, Brüning JC, (2012). Selective insulin and leptin resistance in metabolic disorders. Cell Metab 16: 144-152.
35. Kouyama R, Suganami T, Nishida J, Tanaka M, Toyoda T, Kiso M, et al. (2005). Attenuation of diet-induced weight gain and adiposity through increased energy expenditure in mice lacking angiotensin II type 1a receptor. Endocrinology 146: 3481-3489.
36. Lambillotte C, Gilon P, Henquin JC, (1997). Direct glucocorticoid inhibition of insulin secretion. An in vitro study of dexamethasone effects in mouse islets. J Clin Invest 99: 414-423.
37. Leite LH, Lacerda AC, Marubayashi U, Coimbra CC, (2006). Central angiotensin AT1-receptor blockade affects thermoregulation and running performance in rats. Am J Physiol Regul Integr Comp Physiol 291: R603-R607.
38. McGrath JC, Drummond GB, McLachlan EM, Kilkenny C, Wainwright CL, (2010). Guidelines for reporting experiments involving animals: the ARRIVE guidelines. Br J Pharmacol 160: 1573-1576.
39. Miesel A, Müller H, Thermann M, Heidbreder M, Dominiak P, Raasch W, (2010). Overfeeding-induced obesity in spontaneously hypertensive rats: an animal model of the human metabolic syndrome. Ann Nutr Metab 56: 127-142.
40. Miesel A, Müller-Fielitz H, Jöhren O, Vogt FM, Raasch W, (2012). Double blockade of angiotensin II (AT(1))-receptors and ACE does not improve weight gain and glucose homeostasis better than single-drug treatments in obese rats. Br J Pharmacol 165: 2721-2735.
41. Mukawa H, Toki Y, Miyazaki Y, Matsui H, Okumura K, Ito T, (2003). Angiotensin II type 2 receptor blockade partially negates antihypertrophic effects of type 1 receptor blockade on pressure-overload rat cardiac hypertrophy. Hypertens Res 26: 89-95.
42. Müller H, Schweitzer N, Jöhren O, Dominiak P, Raasch W, (2007). Angiotensin II stimulates the reactivity of the pituitary-adrenal axis in leptin-resistant Zucker rats, thereby influencing the glucose utilization. Am J Physiol Endocrinol Metab 293: E802-E810.
43. Müller-Fielitz H, Raasch W, (2013). Angiotensin II impairs glucose utilization in obese Zucker rats by increasing HPA activity via an adrenal-dependent mechanism. Horm Metab Res 45: 173-180.
44. Müller-Fielitz H, Markert A, Wittmershaus C, Pahlke F, Jöhren O, Raasch W, (2011). Weight loss and hypophagia after high-dose AT1-blockade is only observed after high dosing and depends on regular leptin signalling but not blood pressure. Naunyn Schmiedebergs Arch Pharmacol 383: 373-384.
45. Müller-Fielitz H, Landolt J, Heidbreder M, Werth S, Vogt FM, Jöhren O, et al. (2012a). Improved insulin sensitivity after long-term treatment with AT1 blockers is not associated with PPARgamma target gene regulation. Endocrinology 153: 1103-1115.
46. Müller-Fielitz H, Lau M, Jöhren O, Stellmacher F, Schwaninger M, Raasch W, (2012b). Blood pressure response to angiotensin ii is enhanced in obese zucker rats and is attributed to an aldosterone-dependent mechanism. Br J Pharmacol 166: 2417-2429.
47. Nolan CJ, Madiraju MS, Delghingaro-Augusto V, Peyot ML, Prentki M, (2006). Fatty acid signaling in the beta-cell and insulin secretion. Diabetes 55 (Suppl. 2): S16-S23.
48. Raasch W, Bartels T, Schwartz C, Häuser W, Rütten H, Dominiak P, (2002). Regression of ventricular and vascular hypertrophy: are there differences between structurally different angiotensin-converting enzyme inhibitors? J Hypertens 20: 2495-2504.
49. Raasch W, Wittmershaus C, Dendorfer A, Voges I, Pahlke F, Dodt C, et al. (2006). Angiotensin II inhibition reduces stress sensitivity of hypothalamo-pituitary-adrenal axis in spontaneously hypertensive rats. Endocrinology 147: 3539-3546.
50. Rong X, Li Y, Ebihara K, Zhao M, Naowaboot J, Kusakabe T, et al. (2010). Angiotensin II type 1 receptor-independent beneficial effects of telmisartan on dietary-induced obesity, insulin resistance and fatty liver in mice. Diabetologia 53: 1727-1731.
51. Sahu A, Metlakunta AS, (2005). Hypothalamic phosphatidylinositol 3-kinase-phosphodiesterase 3B-cyclic AMP pathway of leptin signalling is impaired following chronic central leptin infusion. J Neuroendocrinol 17: 720-726.
52. Scarpace PJ, Matheny M, Tumer N, (2001). Hypothalamic leptin resistance is associated with impaired leptin signal transduction in aged obese rats. Neuroscience 104: 1111-1117.
53. Scheen AJ, (2004a). Renin-angiotensin system inhibition prevents type 2 diabetes mellitus. Part 1. A meta-analysis of randomised clinical trials. Diabetes Metab 30: 487-496.
54. Scheen AJ, (2004b). Renin-angiotensin system inhibition prevents type 2 diabetes mellitus. Part 2. Overview of physiological and biochemical mechanisms. Diabetes Metab 30: 498-505.
55. Schupp M, Janke J, Clasen R, Unger T, Kintscher U, (2004). Angiotensin type 1 receptor blockers induce peroxisome proliferator-activated receptor-gamma activity. Circulation 109: 2054-2057.
56. Schupp M, Clemenz M, Gineste R, Witt H, Janke J, Helleboid S, et al. (2005). Molecular characterization of new selective peroxisome proliferator-activated receptor gamma modulators with angiotensin receptor blocking activity. Diabetes 54: 3442-3452.
57. Schupp M, Lee LD, Frost N, Umbreen S, Schmidt B, Unger T, et al. (2006). Regulation of peroxisome proliferator-activated receptor gamma activity by losartan metabolites. Hypertension 47: 586-589.
58. Schutz Y, (1995). Abnormalities of fuel utilization as predisposing to the development of obesity in humans. Obes Res 3 (Suppl. 2): 173S-178S.
59. Skurk T, van Hamelen V, Blum WF, Hauner H, (2005). Angiotensin II promotes leptin production in cultured human fat cells by an ERK1/2-dependent pathway. Obes Res 13: 969-973.
60. Skurk T, Alberti-Huber C, Herder C, Hauner H, (2007). Relationship between adipocyte size and adipokine expression and secretion. J Clin Endocrinol Metab 92: 1023-1033.
61. Sueta D, Nakamura T, Dong YF, Kataoka K, Koibuchi N, Yamamoto E, et al. (2012). Amlodipine enhances amelioration of vascular insulin resistance, oxidative stress, and metabolic disorders by candesartan in metabolic syndrome rats. Am J Hypertens 25: 704-710.
62. Sugimoto K, Qi NR, Kazdova L, Pravenec M, Ogihara T, Kurtz TW, (2006). Telmisartan but not valsartan increases caloric expenditure and protects against weight gain and hepatic steatosis. Hypertension 47: 1003-1009.
63. Wosik K, Cayrol R, Dodelet-Devillers A, Berthelet F, Bernard M, Moumdjian R, et al. (2007). Angiotensin II controls occludin function and is required for blood brain barrier maintenance: relevance to multiple sclerosis. J Neurosci 27: 9032-9042.
64. Zanchi A, Dulloo AG, Perregaux C, Montani JP, Burnier M, (2007). Telmisartan prevents the glitazone-induced weight gain without interfering with its insulin-sensitizing properties. Am J Physiol Endocrinol Metab 293: E91-E95.
65. Zorad S, Dou JT, Benicky J, Hutanu D, Tybitanclova K, Zhou J, et al. (2006). Long-term angiotensin II AT1 receptor inhibition produces adipose tissue hypotrophy accompanied by increased expression of adiponectin and PPARgamma. Eur J Pharmacol 552: 112-122.