Enhanced pan-peroxisome proliferator-activated receptor gene and protein expression in adipose tissue of diet-induced obese mice treated with telmisartan

Experimental Physiology

Volumn 99, Issue 12, 2014, Pages 1663-1678

  Penna de Carvalho, Aline ^a   Graus Nunes, Francielle ^a   Rabelo Andrade, Júlia ^a   Mandarim de Lacerda, Carlos Alberto ^a   Souza Mello, Vanessa ^a  

^a STATE UNIVERSITY OF RIO DE JANEIRO   (Brazil)

Author keywords

[No Author keywords available]

Indexed keywords

ADIPOCYTOKINE; BETA 3 ADRENERGIC RECEPTOR; GLUCOSE; INSULIN; PEROXISOME PROLIFERATOR ACTIVATED RECEPTOR; TELMISARTAN; BENZIMIDAZOLE DERIVATIVE; BENZOIC ACID DERIVATIVE;

ADIPOSE TISSUE; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BROWN ADIPOSE TISSUE; CONTROLLED STUDY; ENERGY EXPENDITURE; GENE EXPRESSION; GLUCOSE TRANSPORT; HYPERTENSION; INFLAMMATION; INSULIN RESISTANCE; INSULIN SENSITIVITY; MALE; MOUSE; NONHUMAN; NONSHIVERING THERMOGENESIS; OBESITY; PROTEIN EXPRESSION; THERMOGENESIS; ANIMAL; DRUG EFFECTS; GENETICS; LIPID DIET; METABOLISM; MOUSE MUTANT; PHYSIOLOGY;

ADIPOSE TISSUE; ANIMALS; BENZIMIDAZOLES; BENZOATES; DIET, HIGH-FAT; GENE EXPRESSION; INSULIN RESISTANCE; MALE; MICE; MICE, OBESE; OBESITY; PEROXISOME PROLIFERATOR-ACTIVATED RECEPTORS;

EID: 84925114908     PISSN: 09580670     EISSN: 1469445X     Source Type: Journal    
DOI: 10.1113/expphysiol.2014.081596     Document Type: Article

References (61)

1. 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.
2. Arch JR, Hislop D, Wang SJ & Speakman JR (2006). Some mathematical and technical issues in the measurement and interpretation of open-circuit indirect calorimetry in small animals. Int J Obes (Lond) 30, 1322-1331.
3. Arch JR & Trayhurn P (2013). Detection of thermogenesis in rodents in response to anti-obesity drugs and genetic modification. Front Physiol 4, 64.
4. Aubert G, Burnier M, Dulloo A, Perregaux C, Mazzolai L, Pralong F & Zanchi A (2010). Neuroendocrine characterization and anorexigenic effects of telmisartan in diet- and glitazone-induced weight gain. Metabolism 59, 25-32.
5. Barbera MJ, Schluter A, Pedraza N, Iglesias R, Villarroya F & Giralt M (2001). Peroxisome proliferator-activated receptor alpha activates transcription of the brown fat uncoupling protein-1 gene. A link between regulation of the thermogenic and lipid oxidation pathways in the brown fat cell. J Biol Chem 276, 1486-1493.
6. Benson SC, Pershadsingh HA, Ho CI, Chittiboyina A, Desai P, Pravenec M, Qi N, Wang J, Avery MA & Kurtz TW (2004). Identification of telmisartan as a unique angiotensin II receptor antagonist with selective PPARγ-modulating activity. Hypertension 43, 993-1002.
7. Berndt J, Kovacs P, Ruschke K, Klöting N, Fasshauer M, Schön MR, Körner A, Stumvoll M & Blüher M (2007). Fatty acid synthase gene expression in human adipose tissue: association with obesity and type 2 diabetes. Diabetologia 50, 1472-1480.
8. Briffa JF, McAinch AJ, Poronnik P & Hryciw DH (2013). Adipokines as a link between obesity and chronic kidney disease. Am J Physiol Renal Physiol 305, F1629-F1636.
9. Burnier M & Brunner HR (2000). Angiotensin II receptor antagonists. Lancet 355, 637-645.
10. Chang L, Chiang SH & Saltiel AR (2004). Insulin signaling and the regulation of glucose transport. Mol Med 10, 65-71.
11. Chiang SH, Baumann CA, Kanzaki M, Thurmond DC, Watson RT, Neudauer CL, Macara IG, Pessin JE & Saltiel AR (2001). Insulin-stimulated GLUT4 translocation requires the CAP-dependent activation of TC10. Nature 410, 944-948.
12. Christodoulides C & Vidal-Puig A (2010). PPARs and adipocyte function. Mol Cell Endocrinol 318, 61-68.
13. Claycombe KJ, Jones BH, Standridge MK, Guo Y, Chun JT, Taylor JW & Moustaid-Moussa N (1998). Insulin increases fatty acid synthase gene transcription in human adipocytes. Am J Physiol Regul Integr Comp Physiol 274, R1253-R1259.
14. Clemenz M, Frost N, Schupp M, Caron S, Foryst-Ludwig A, Böhm C, Hartge M, Gust R, Staels B, Unger T & Kintscher U (2008). Liver-specific peroxisome proliferator-activated receptor α target gene regulation by the angiotensin type 1 receptor blocker telmisartan. Diabetes 57, 1405-1413.
15. Crowley V & Vidal-Puig AJ (2001). Mitochondrial uncoupling proteins (UCPs) and obesity. Nutr Metab Cardiovasc Dis 11, 70-75.
16. Dunham-Snary KJ & Ballinger SW (2013). Mitochondrial genetics and obesity: evolutionary adaptation and contemporary disease susceptibility. Free Radic Biol Med 65, 1229-1237.
17. Furuhashi M & Hotamisligil GS (2008). Fatty acid-binding proteins: role in metabolic diseases and potential as drug targets. Nat Rev Drug Discov 7, 489-503.
18. Garin-Shkolnik T, Rudich A, Hotamisligil GS & Rubinstein M (2014). FABP4 attenuates PPARγ and adipogenesis and is inversely correlated with PPARγ in adipose tissues. Diabetes 63, 900-911.
19. Goto T, Lee JY, Teraminami A, Kim YI, Hirai S, Uemura T, Inoue H, Takahashi N & Kawada T (2011). Activation of peroxisome proliferator-activated receptor-alpha stimulates both differentiation and fatty acid oxidation in adipocytes. J Lipid Res 52, 873-884.
20. Gupte A & Mora S (2006). Activation of the Cbl insulin signaling pathway in cardiac muscle; dysregulation in obesity and diabetes. Biochem Biophys Res Commun 342, 751-757.
21. Hanada M, Feng J & Hemmings BA (2004). Structure, regulation and function of PKB/AKT-a major therapeutic target. Biochim Biophys Acta 1697, 3-16.
22. He H, Yang D, Ma L, Luo Z, Ma S, Feng X, Cao T, Yan Z, Liu D, Tepel M & Zhu Z (2010). Telmisartan prevents weight gain and obesity through activation of peroxisome proliferator-activated receptor-δ-dependent pathways. Hypertension 55, 869-879.
23. Hondares E, Rosell M, Díaz-Delfín J, Olmos Y, Monsalve M, Iglesias R, Villarroya F & Giralt M (2011). Peroxisome proliferator-activated receptor α (PPARα) induces PPARγ coactivator 1α (PGC-1α) gene expression and contributes to thermogenic activation of brown fat: involvement of PRDM16. J Biol Chem 286, 43112-43122.
24. Jun HS, Hwang K, Kim Y & Park T (2008). High-fat diet alters PP2A, TC10, and CIP4 expression in visceral adipose tissue of rats. Obesity (Silver Spring) 16, 1226-1231.
25. Kelton D, Lysecki C, Aukema H, Anderson B, Kang JX & Ma DW (2013). Endogenous synthesis of n-3 PUFA modifies fatty acid composition of kidney phospholipids and eicosanoid levels in the fat-1 mouse. Prostaglandins Leukot Essent Fatty Acids 89, 169-177.
26. Komatsu M, Tong Y, Li Y, Nakajima T, Li G, Hu R, Sugiyama E, Kamijo Y, Tanaka N, Hara A & Aoyama T (2010). Multiple roles of PPARα in brown adipose tissue under constitutive and cold conditions. Genes Cells 15, 91-100.
27. Le Dréan G, Haure-Mirande V, Ferrier L, Bonnet C, Hulin P, de Coppet P & Segain JP (2013). Visceral adipose tissue and leptin increase colonic epithelial tight junction permeability via a RhoA-ROCK-dependent pathway. FASEB J 28, 1059-1070.
28. Li L, Luo Z, Yu H, Feng X, Wang P, Chen J, Pu Y, Zhao Y, He H, Zhong J, Liu D & Zhu Z (2013). Telmisartan improves insulin resistance of skeletal muscle through peroxisome proliferator-activated receptor-δ activation. Diabetes 62, 762-774.
29. Lowell BB & Spiegelman BM (2000). Towards a molecular understanding of adaptive thermogenesis. Nature 404, 652-660.
30. Matthews DR, Hosker JP, Rudenski AS, Naylor BA, Treacher DF & Turner RC (1985). Homeostasis model assessment: insulin resistance and beta-cell function from fasting plasma glucose and insulin concentrations in man. Diabetologia 28, 412-419.
31. Maury E & Brichard SM (2010). Adipokine dysregulation, adipose tissue inflammation and metabolic syndrome. Mol Cell Endocrinol 314, 1-16.
32. Menendez JA, Vazquez-Martin A, Ortega FJ & Fernandez-Real JM (2009). Fatty acid synthase: association with insulin resistance, type 2 diabetes, and cancer. Clin Chem 55, 425-438.
33. Miura T, Suzuki W, Ishihara E, Arai I, Ishida H, Seino Y & Tanigawa K (2001). Impairment of insulin-stimulated GLUT4 translocation in skeletal muscle and adipose tissue in the Tsumura Suzuki obese diabetic mouse: a new genetic animal model of type 2 diabetes. Eur J Endocrinol 145, 785-790.
34. Moustaid N, Jones BH & Taylor JW (1996). Insulin increases lipogenic enzyme activity in human adipocytes in primary culture. J Nutr 126, 865-870.
35. Neyrinck AM, Bindels LB, De Backer F, Pachikian BD, Cani PD & Delzenne NM (2009). Dietary supplementation with chitosan derived from mushrooms changes adipocytokine profile in diet-induced obese mice, a phenomenon linked to its lipid-lowering action. Int Immunopharmacol 9, 767-773.
36. Olarescu NC, Ueland T, Godang K, Lindberg-Larsen R, Jørgensen JO & Bollerslev J (2013). Inflammatory adipokines contribute to insulin resistance in active acromegaly and respond differently to different treatment modalities. Eur J Endocrinol 170, 39-48.
37. Olefsky JM (2000). Treatment of insulin resistance with peroxisome proliferator-activated receptor γ agonists. J Clin Invest 106, 467-472.
38. 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.
39. Renne U, Langhammer M, Brenmoehl J, Walz C, Zeissler A, Tuchscherer A, Piechotta M, Wiesner RJ, Bielohuby M & Hoeflich A (2013). Lifelong obesity in a polygenic mouse model prevents age- and diet-induced glucose intolerance- obesity is no road to late-onset diabetes in mice. PLoS One 8, e79788.
40. Ricquier D, Miroux B, Larose M, Cassard-Doulcier AM & Bouillaud F (2000). Endocrine regulation of uncoupling proteins and energy expenditure. Int J Obes Relat Metab Disord 24 Suppl 2, S86-S88.
41. Rodríguez-Calvo R, Serrano L, Coll T, Moullan N, Sánchez RM, Merlos M, Palomer X, Laguna JC, Michalik L, Wahli W & Vázquez-Carrera M (2008). Activation of peroxisome proliferator-activated receptor β/δ inhibits lipopolysaccharide-induced cytokine production in adipocytes by lowering nuclear factor-κB activity via extracellular signal-related kinase 1/2. Diabetes 57, 2149-2157.
42. Rotter V, Nagaev I & Smith U (2003). Interleukin-6 (IL-6) induces insulin resistance in 3T3-L1 adipocytes and is, like IL-8 and tumor necrosis factor-α, overexpressed in human fat cells from insulin-resistant subjects. J Biol Chem 278, 45777-45784.
43. Seok H & Cha BS (2013). Refocusing peroxisome proliferator activated receptor-α: a new insight for therapeutic roles in diabetes. Diabetes Metab J 37, 326-332.
44. Serrano-Marco L, Chacón MR, Maymó-Masip E, Barroso E, Salvadó L, Wabitsch M, Garrido-Sánchez L, Tinahones FJ, Palomer X, Vendrell J & Vázquez-Carrera M (2012). TNF-α inhibits PPARβ/δ activity and SIRT1 expression through NF-κB in human adipocytes. Biochim Biophys Acta 1821, 1177-1185.
45. Serrano-Marco L, Rodríguez-Calvo R, El Kochairi I, Palomer X, Michalik L, Wahli W & Vázquez-Carrera M (2011). Activation of peroxisome proliferator-activated receptor-β/-δ (PPAR-β/-δ) ameliorates insulin signaling and reduces SOCS3 levels by inhibiting STAT3 in interleukin-6-stimulated adipocytes. Diabetes 60, 1990-1999.
46. Souza-Mello V, Gregório BM, Cardoso-de-Lemos FS, de Carvalho L, Aguila MB & Mandarim-de-Lacerda CA (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.
47. Souza-Mello V, Gregório BM, Relvas-Lucas B, da Silva Faria T, Aguila MB & Mandarim-de-Lacerda CA (2011). Pancreatic ultrastructural enhancement due to telmisartan plus sitagliptin treatment in diet-induced obese C57BL/6 mice. Pancreas 40, 715-722.
48. Steinberg GR & Dyck DJ (2000). Development of leptin resistance in rat soleus muscle in response to high-fat diets. Am J Physiol Endocrinol Metab 279, E1374-E1382.
49. Sugimoto K, Qi NR, Kazdová 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.
50. Surwit RS, Wang S, Petro AE, Sanchis D, Raimbault S, Ricquier D & Collins S (1998). Diet-induced changes in uncoupling proteins in obesity-prone and obesity-resistant strains of mice. Proc Natl Acad Sci U S A 95, 4061-4065.
51. Tai MM (1994). A mathematical model for the determination of total area under glucose tolerance and other metabolic curves. Diabetes Care 17, 152-154.
52. Takagi H, Niwa M, Mizuno Y, Goto SN & Umemoto T; ALICE (All-Literature Investigation of Cardiovascular Evidence) Group (2013). Telmisartan as a metabolic sartan: the first meta-analysis of randomized controlled trials in metabolic syndrome. J Am Soc Hypertens 7, 229-235.
53. Thirone AC, Huang C & Klip A (2006). Tissue-specific roles of IRS proteins in insulin signaling and glucose transport. Trends Endocrinol Metab 17, 72-78.
54. Tiraby C & Langin D (2003). Conversion from white to brown adipocytes: a strategy for the control of fat mass? Trends Endocrinol Metab 14, 439-441.
55. Tontonoz P, Graves RA, Budavari AI, Erdjument-Bromage H, Lui M, Hu E, Tempst P & Spiegelman BM (1994). Adipocyte-specific transcription factor ARF6 is a heterodimeric complex of two nuclear hormone receptors, PPARγ and RXRα. Nucleic Acids Res 22, 5628-5634.
56. Ushijima K, Takuma M, Ando H, Ishikawa-Kobayashi E, Nozawa M, Maekawa T, Shiga T & Fujimura A (2013). Effects of telmisartan and valsartan on insulin sensitivity in obese diabetic mice. Eur J Pharmacol 698, 505-510.
57. Wang Y, Jones Voy B, Urs S, Kim S, Soltani-Bejnood M, Quigley N, Heo YR, Standridge M, Andersen B, Dhar M, Joshi R, Wortman P, Taylor JW, Chun J, Leuze M, Claycombe K, Saxton AM & Moustaid-Moussa N (2004). The human fatty acid synthase gene and de novo lipogenesis are coordinately regulated in human adipose tissue. J Nutr 134, 1032-1038.
58. Yadav A, Kataria MA & Saini V (2013). Role of leptin and adiponectin in insulin resistance. Clin Chim Acta 417, 80-84.
59. y mice. Nutr Metab (Lond) 10, 16.
60. Ziemke F & Mantzoros CS (2010). Adiponectin in insulin resistance: lessons from translational research. Am J Clin Nutr 91, 258S-261S.
61. Zúñiga J, Cancino M, Medina F, Varela P, Vargas R, Tapia G, Videla LA & Fernández V (2011). N-3 PUFA supplementation triggers PPAR-α activation and PPAR-α/NF-κB interaction: anti-inflammatory implications in liver ischemia-reperfusion injury. PLoS One 6, e28502.