Lack of weight gain after angiotensin AT1 receptor blockade in diet-induced obesity is partly mediated by an angiotensin-(1-7)/Mas-dependent pathway

British Journal of Pharmacology

Volumn 172, Issue 15, 2015, Pages 3764-3778

  Schuchard, Johanna ^a,b   Winkler, Martina ^a   Stölting, Ines ^a   Schuster, Franziska ^a   Vogt, Florian M ^a   Barkhausen, Jörg ^a   Thorns, Christoph ^c   Santos, Robson A ^d   Bader, Michael ^a,b,d,e,f   Raasch, Walter ^a,b  

^a UNIVERSITY OF LÜBECK   (Germany)

^b DZHK GERMAN CENTRE FOR CARDIOVASCULAR RESEARCH   (Germany)

^c UNIVERSITY HOSPITAL SCHLESWIG HOLSTEIN   (Germany)

^d FEDERAL UNIVERSITY OF MINAS GERAIS   (Brazil)

^e MAX DELBRÜCK CENTER FOR MOLECULAR MEDICINE   (Germany)

^f CHARITÉ UNIVERSITÄTSMEDIZIN BERLIN   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

ANGIOTENSIN 1 RECEPTOR; ANGIOTENSIN RECEPTOR; ANGIOTENSIN[1-7]; ANGIOTENSIN[1-7][7 DEXTRO ALANINE]; CAPTOPRIL; GLUCOSE; INSULIN; LEPTIN; MAS RECEPTOR; TELMISARTAN; UNCLASSIFIED DRUG; 7-ALA-ANGIOTENSIN (1-7); ANGIOTENSIN 1 RECEPTOR ANTAGONIST; ANGIOTENSIN I; ANGIOTENSIN I (1-7); ANGIOTENSIN II; BENZIMIDAZOLE DERIVATIVE; BENZOIC ACID DERIVATIVE; G PROTEIN COUPLED RECEPTOR; ONCOPROTEIN; PEPTIDE FRAGMENT; PROTO-ONCOGENE PROTEINS C-MAS-1;

ANG(1-7) GENE; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CALORIC INTAKE; CONTROLLED STUDY; ENERGY EXPENDITURE; FEEDING BEHAVIOR; FOOD INTAKE; GENE OVEREXPRESSION; GLUCOSE BLOOD LEVEL; GLUCOSE UTILIZATION; GLYCEMIC CONTROL; HORMONE BLOOD LEVEL; HORMONE SENSITIVITY; INSULIN RESISTANCE; MALE; NONHUMAN; OBESITY; PRIORITY JOURNAL; RAT; RECEPTOR BLOCKING; TRANSGENICS; WEIGHT GAIN; WEIGHT REDUCTION; ADVERSE EFFECTS; AGONISTS; ANALOGS AND DERIVATIVES; ANIMAL; ANTAGONISTS AND INHIBITORS; DIET; DRUG EFFECTS; ENERGY METABOLISM; GENETICS; METABOLISM; SIGNAL TRANSDUCTION; TRANSGENIC ANIMAL;

ANGIOTENSIN I; ANGIOTENSIN II; ANGIOTENSIN II TYPE 1 RECEPTOR BLOCKERS; ANIMALS; ANIMALS, GENETICALLY MODIFIED; BENZIMIDAZOLES; BENZOATES; DIET; ENERGY INTAKE; ENERGY METABOLISM; INSULIN RESISTANCE; LEPTIN; MALE; OBESITY; PEPTIDE FRAGMENTS; PROTO-ONCOGENE PROTEINS; RATS; RECEPTORS, G-PROTEIN-COUPLED; SIGNAL TRANSDUCTION; WEIGHT GAIN; WEIGHT LOSS;

EID: 84937013108     PISSN: 00071188     EISSN: 14765381     Source Type: Journal    
DOI: 10.1111/bph.13172     Document Type: Article

References (74)

1. Alexander SPH, Benson HE, Faccenda E, Pawson AJ, Sharman JL, Spedding M, et al. (2013a). The Concise Guide to PHARMACOLOGY 2013/14: G Protein-Coupled Receptors. Br J Pharmacol 170: 1459-1581.
2. Alexander SPH, Benson HE, Faccenda E, Pawson AJ, Sharman JL, Spedding M, et al. (2013b). The Concise Guide to PHARMACOLOGY 2013/14: Enzymes. Br J Pharmacol 170: 1797-1867.
3. Bader M, (2013). ACE2, angiotensin-(1-7), and Mas: the other side of the coin. Pflugers Arch 465: 79-85.
4. 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.
5. Banks WA, DiPalma CR, Farrell CL, (1999). Impaired transport of leptin across the blood-brain barrier in obesity. Peptides 20: 1341-1345.
6. 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.
7. Benter IF, Yousif MH, Al Saleh FM, Raghupathy R, Chappell MC, Diz DI, (2011). Angiotensin-(1-7) blockade attenuates captopril- or hydralazine-induced cardiovascular protection in spontaneously hypertensive rats treated with NG-nitro-L-arginine methyl ester. J Cardiovasc Pharmacol 57: 559-567.
8. 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.
9. Birkenfeld AL, Shulman GI, (2014). Nonalcoholic fatty liver disease, hepatic insulin resistance, and type 2 diabetes. Hepatology 59: 713-723.
10. Bosnyak S, Widdop RE, Denton KM, Jones ES, (2012). Differential mechanisms of ang (1-7)-mediated vasodepressor effect in adult and aged candesartan-treated rats. Int J Hypertens 2012: 192567.
11. 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.
12. 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.
13. Corwin RL, Avena NM, Boggiano MM, (2011). Feeding and reward: perspectives from three rat models of binge eating. Physiol Behav 104: 87-97.
14. Dallman MF, la Fleur SE, Pecoraro NC, Gomez F, Houshyar H, Akana SF, (2004). Minireview: glucocorticoids-food intake, abdominal obesity, and wealthy nations in 2004. Endocrinology 145: 2633-2638.
15. Duvivier BM, Schaper NC, Bremers MA, van Crombrugge G, Menheere PP, Kars M, et al. (2013). Minimal intensity physical activity (standing and walking) of longer duration improves insulin action and plasma lipids more than shorter periods of moderate to vigorous exercise (cycling) in sedentary subjects when energy expenditure is comparable. PLoS ONE 8: e55542.
16. Engeli S, Negrel R, Sharma AM, (2000). Physiology and pathophysiology of the adipose tissue renin-angiotensin system. Hypertension 35: 1270-1277.
17. Feltenberger JD, Andrade JM, Paraiso A, Barros LO, Filho AB, Sinisterra RD, et al. (2013). Oral formulation of angiotensin-(1-7) improves lipid metabolism and prevents high-fat diet-induced hepatic steatosis and inflammation in mice. Hypertension 62: 324-330.
18. Ferrario CM, Jessup J, Gallagher PE, Averill DB, Brosnihan KB, Ann TE, et al. (2005). Effects of renin-angiotensin system blockade on renal angiotensin-(1-7) forming enzymes and receptors. Kidney Int 68: 2189-2196.
19. Fu Z, Zhao L, Aylor KW, Carey RM, Barrett EJ, Liu Z, (2014). Angiotensin-(1-7) recruits muscle microvasculature and enhances insulin's metabolic action via mas receptor. Hypertension 63: 1219-1227.
20. 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.
21. Giani JF, Mayer MA, Munoz MC, Silberman EA, Hocht C, Taira CA, 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.
22. Giani JF, Burghi V, Veiras LC, Tomat A, Munoz MC, Cao G, et al. (2012). Angiotensin-(1-7) attenuates diabetic nephropathy in Zucker diabetic fatty rats. Am J Physiol Renal Physiol 302: F1606-F1615.
23. Gironacci MM, Longo Carbajosa NA, Goldstein J, Cerrato BD, (2013). Neuromodulatory role of angiotensin-(1-7) in the central nervous system. Clin Sci (Lond) 125: 57-65.
24. Handa RK, Ferrario CM, Strandhoy JW, (1996). Renal actions of angiotensin-(1-7): in vivo and in vitro studies. Am J Physiol 270: F141-F147.
25. 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.
26. Igase M, Strawn WB, Gallagher PE, Geary RL, Ferrario CM, (2005). Angiotensin II AT1 receptors regulate ACE2 and angiotensin-(1-7) expression in the aorta of spontaneously hypertensive rats. Am J Physiol Heart Circ Physiol 289: H1013-H1019.
27. Ishiyama Y, Gallagher PE, Averill DB, Tallant EA, Brosnihan KB, Ferrario CM, (2004). Upregulation of angiotensin-converting enzyme 2 after myocardial infarction by blockade of angiotensin II receptors. Hypertension 43: 970-976.
28. Kadoguchi T, Kinugawa S, Takada S, Fukushima A, Furihata T, Homma T, et al. (2015). Angiotensin II can directly induce mitochondrial dysfunction, decrease oxidative fibre number and induce atrophy in mouse hindlimb skeletal muscle. Exp Physiol 100: 312-322.
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. King VL, English VL, Bharadwaj K, Cassis LA, (2013). Angiotensin II stimulates sympathetic neurotransmission to adipose tissue. Physiol Rep 1: e00014.
31. Kintscher U, Bramlage P, Paar WD, Thoenes M, Unger T, (2007). Irbesartan for the treatment of hypertension in patients with the metabolic syndrome: a sub analysis of the Treat to Target post authorization survey. Prospective observational, two armed study in 14,200 patients. Cardiovasc Diabetol 6: 12.
32. Larsen PJ, Jensen PB, Sorensen RV, Larsen LK, Vrang N, Wulff EM, et al. (2003). Differential influences of peroxisome proliferator-activated receptors gamma and -alpha on food intake and energy homeostasis. Diabetes 52: 2249-2259.
33. Liu C, Lv XH, Li HX, Cao X, Zhang F, Wang L, et al. (2012). Angiotensin-(1-7) suppresses oxidative stress and improves glucose uptake via Mas receptor in adipocytes. Acta Diabetol 49: 291-299.
34. 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.
35. 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.
36. 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.
37. 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.
38. 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.
39. 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.
40. Müller-Fielitz H, Hübel N, Mildner M, Vogt FM, Barkhausen J, Raasch W, (2014). Chronic blockade of angiotensin AT(1) receptors improves cardinal symptoms of metabolic syndrome in diet-induced obesity in rats. Br J Pharmacol 171: 746-760.
41. 1 receptors in diet-induced obese rats. Br J Pharmacol 172: 857-868.
42. 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.
43. Pawson AJ, Sharman JL, Benson HE, Faccenda E, Alexander SP, Buneman OP, et al.; NC-IUPHAR. (2014). The IUPHAR/BPS Guide to PHARMACOLOGY: an expert-driven knowledge base of drug targets and their ligands. Nucl Acids Res 42 (Database Issue): D1098-D1106.
44. Pecoraro N, Reyes F, Gomez F, Bhargava A, Dallman MF, (2004). Chronic stress promotes palatable feeding, which reduces signs of stress: feedforward and feedback effects of chronic stress. Endocrinology 145: 3754-3762.
45. Pimentel GD, Ganeshan K, Carvalheira JB, (2014). Hypothalamic inflammation and the central nervous system control of energy homeostasis. Mol Cell Endocrinol 397: 15-22.
46. Pinheiro SV, Ferreira AJ, Kitten GT, da Silveira KD, da Silva DA, Santos SH, et al. (2009). Genetic deletion of the angiotensin-(1-7) receptor Mas leads to glomerular hyperfiltration and microalbuminuria. Kidney Int 75: 1184-1193.
47. Prasannarong M, Santos FR, Henriksen EJ, (2012). ANG-(1-7) reduces ANG II-induced insulin resistance by enhancing Akt phosphorylation via a Mas receptor-dependent mechanism in rat skeletal muscle. Biochem Biophys Res Commun 426: 369-373.
48. Raasch W, Bartels T, Schwartz C, Hauser W, Rutten 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, Jöhren O, Schwartz S, Gieselberg A, Dominiak P, (2004). Combined blockade of AT1-receptors and ACE synergistically potentiates antihypertensive effects in SHR. J Hypertens 22: 611-618.
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. Rubio-Ruiz ME, Valle-Mondragon L, Castrejon-Tellez V, Carreon-Torres E, Diaz-Diaz E, Guarner-Lans V, (2014). Angiotensin II and 1-7 during aging in metabolic syndrome rats. Expression of AT1, AT2 and Mas receptors in abdominal white adipose tissue. Peptides 57: 101-108.
52. Santos RA, (2014). Angiotensin-(1-7). Hypertension 63: 1138-1147.
53. Santos RA, Ferreira AJ, Nadu AP, Braga AN, de Almeida AP, Campagnole-Santos MJ, et al. (2004). Expression of an angiotensin-(1-7)-producing fusion protein produces cardioprotective effects in rats. Physiol Genomics 17: 292-299.
54. Santos RA, Ferreira AJ, Verano-Braga T, Bader M, (2012a). Angiotensin-converting enzyme 2, Angiotensin-(1-7) and Mas: new players of the renin angiotensin system. J Endocrinol 216: R1-R17.
55. Santos SH, Fernandes LR, Mario EG, Ferreira AV, Porto LC, Alvarez-Leite JI, et al. (2008). Mas deficiency in FVB/N mice produces marked changes in lipid and glycemic metabolism. Diabetes 57: 340-347.
56. Santos SH, Braga JF, Mario EG, Porto LC, Rodrigues-Machado MG, Murari A, et al. (2010). Improved lipid and glucose metabolism in transgenic rats with increased circulating angiotensin-(1-7). Arterioscler Thromb Vasc Biol 30: 953-961.
57. Santos SH, Fernandes LR, Pereira CS, Guimaraes AL, de Paula AM, Campagnole-Santos MJ, et al. (2012b). Increased circulating angiotensin-(1-7) protects white adipose tissue against development of a proinflammatory state stimulated by a high-fat diet. Regul Pept 178: 64-70.
58. Santos SH, Andrade JM, Fernandes LR, Sinisterra RD, Sousa FB, Feltenberger JD, et al. (2013). Oral Angiotensin-(1-7) prevented obesity and hepatic inflammation by inhibition of resistin/TLR4/MAPK/NF-kappaB in rats fed with high-fat diet. Peptides 46: 47-52.
59. Santos SH, Giani JF, Burghi V, Miquet JG, Qadri F, Braga JF, et al. (2014). Oral administration of angiotensin-(1-7) ameliorates type 2 diabetes in rats. J Mol Med (Berl) 92: 255-265.
60. 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.
61. Silva AR, Aguilar EC, Alvarez-Leite JI, da Silva RF, Arantes RM, Bader M, et al. (2013). Mas receptor deficiency is associated with worsening of lipid profile and severe hepatic steatosis in ApoE-knockout mice. Am J Physiol Regul Integr Comp Physiol 305: R1323-R1330.
62. Skurk T, van Harmelen 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.
63. Song YH, Li Y, Du J, Mitch WE, Rosenthal N, Delafontaine P, (2005). Muscle-specific expression of IGF-1 blocks angiotensin II-induced skeletal muscle wasting. J Clin Invest 115: 451-458.
64. de Souza CJ, Eckhardt M, Gagen K, Dong M, Chen W, Laurent D, et al. (2001). Effects of pioglitazone on adipose tissue remodeling within the setting of obesity and insulin resistance. Diabetes 50: 1863-1871.
65. Stragier B, Hristova I, Sarre S, Ebinger G, Michotte Y, (2005). In vivo characterization of the angiotensin-(1-7)-induced dopamine and gamma-aminobutyric acid release in the striatum of the rat. Eur J Neurosci 22: 658-664.
66. Tabony AM, Yoshida T, Sukhanov S, Delafontaine P, (2014). Protein phosphatase 2C-alpha knockdown reduces angiotensin II-mediated skeletal muscle wasting via restoration of mitochondrial recycling and function. Skelet Muscle 4: 20.
67. Turner N, Cooney GJ, Kraegen EW, Bruce CR, (2014). Fatty acid metabolism, energy expenditure and insulin resistance in muscle. J Endocrinol 220: T61-T79.
68. Vazquez-Medina JP, Popovich I, Thorwald MA, Viscarra JA, Rodriguez R, Sonanez-Organis JG, et al. (2013). Angiotensin receptor-mediated oxidative stress is associated with impaired cardiac redox signaling and mitochondrial function in insulin-resistant rats. Am J Physiol Heart Circ Physiol 305: H599-H607.
69. Yamada K, Iyer SN, Chappell MC, Ganten D, Ferrario CM, (1998). Converting enzyme determines plasma clearance of angiotensin-(1-7). Hypertension 32: 496-502.
70. Yoshida T, Semprun-Prieto L, Wainford RD, Sukhanov S, Kapusta DR, Delafontaine P, (2012). Angiotensin II reduces food intake by altering orexigenic neuropeptide expression in the mouse hypothalamus. Endocrinology 153: 1411-1420.
71. Yuan L, Li Y, Li G, Song Y, Gong X, (2013). Ang(1-7) treatment attenuates beta-cell dysfunction by improving pancreatic microcirculation in a rat model of type 2 diabetes. J Endocrinol Invest 36: 931-937.
72. Zhang L, Du J, Hu Z, Han G, Delafontaine P, Garcia G, et al. (2009). IL-6 and serum amyloid A synergy mediates angiotensin II-induced muscle wasting. J Am Soc Nephrol 20: 604-612.
73. Zhu D, Tong Q, Liu W, Tian M, Xie W, Ji L, et al. (2014). Angiotensin (1-7) protects against stress-induced gastric lesions in rats. Biochem Pharmacol 87: 467-476.
74. 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.