Retinoic acid receptor β2 agonists restore glycaemic control in diabetes and reduce steatosis

Diabetes, Obesity and Metabolism

Volumn 18, Issue 2, 2016, Pages 142-151

  Trasino, S E ^a   Tang, X H ^a   Jessurun, J ^a   Gudas, L J ^a  

^a WEILL CORNELL MEDICAL COLLEGE   (United States)

Author keywords

Antidiabetic drug; Fatty liver; Insulin resistance; Renal steatosis; Retinoids; Type 2 diabetes

Indexed keywords

AC 261066; ANTIDIABETIC AGENT; CARNITINE PALMITOYLTRANSFERASE I; CARNITINE PALMITOYLTRANSFERASE I ALPHA; FATTY ACID SYNTHASE; INSULIN; MESSENGER RNA; STEROL REGULATORY ELEMENT BINDING PROTEIN 1; TRANSLOCASE OF OUTER MITOCHONDRIAL MEMBRANE 20; TRIACYLGLYCEROL; UNCLASSIFIED DRUG; 4'-OCTYL-4-BIPHENYLCARBOXYLIC ACID; 4-(4-(2-(N-BUTOXY)ETHOXY)-5-METHYLTHIAZOL-2-YL)-2-FLUOROBENZOIC ACID; BENZOIC ACID DERIVATIVE; BIPHENYL DERIVATIVE; NEW DRUG; RETINOIC ACID RECEPTOR; RETINOIC ACID RECEPTOR BETA; RETINOIC ACID RECEPTOR BETA2, MOUSE; THIAZOLE DERIVATIVE;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; BODY WEIGHT; CONTROLLED STUDY; DIABETES MELLITUS; DRUG EFFICACY; FATTY ACID OXIDATION; FATTY LIVER; GENETIC MODEL; GLYCEMIC CONTROL; INSULIN RELEASE; INSULIN RESISTANCE; LIPID PEROXIDATION; LIPOGENESIS; MALE; MOUSE; NONHUMAN; OBESITY; OXIDATIVE STRESS; PANCREAS ISLET; WILD TYPE; ADVERSE EFFECTS; AGONISTS; ANIMAL; C57BL MOUSE; COMPLICATION; DIABETES MELLITUS, TYPE 2; DRUG EFFECTS; HYPERGLYCEMIA; KIDNEY; LIPID DIET; LIVER; METABOLISM; MUTANT MOUSE STRAIN; NON-ALCOHOLIC FATTY LIVER DISEASE; PANCREAS; PATHOLOGY; SKELETAL MUSCLE;

ANIMALS; BENZOATES; BIPHENYL COMPOUNDS; DIABETES MELLITUS, TYPE 2; DIET, HIGH-FAT; DRUGS, INVESTIGATIONAL; HYPERGLYCEMIA; HYPOGLYCEMIC AGENTS; INSULIN RESISTANCE; KIDNEY; LIPID PEROXIDATION; LIVER; MALE; MICE, INBRED C57BL; MICE, MUTANT STRAINS; MUSCLE, SKELETAL; NON-ALCOHOLIC FATTY LIVER DISEASE; OBESITY; OXIDATIVE STRESS; PANCREAS; RECEPTORS, RETINOIC ACID; THIAZOLES;

EID: 84956887616     PISSN: 14628902     EISSN: 14631326     Source Type: Journal    
DOI: 10.1111/dom.12590     Document Type: Article

References (46)

1. D'Ambrosio DN, Clugston RD, Blaner WS. Vitamin A metabolism: an update. Nutrients 2011; 3: 63-103.
2. Gudas LJ. Emerging roles for retinoids in regeneration and differentiation in normal and disease states. Biochim Biophys Acta 2012; 1821: 213-221.
3. Martín M, Gallego-Llamas J, Ribes V etal. Dorsal pancreas agenesis in retinoic acid-deficient Raldh2 mutant mice. Dev Biol 2005; 284: 399-411.
4. Oström M, Loffler KA, Edfalk S etal. Retinoic acid promotes the generation of pancreatic endocrine progenitor cells and their further differentiation into beta-cells. PLoS One 2008; 3: e2841.
5. Brun PJ, Yang KJ, Lee SA, Yuen JJ, Blaner WS. Retinoids: potent regulators of metabolism. Biofactors 2013; 39: 151-163.
6. Schwarz EJ, Reginato MJ, Shao D, Krakow SL, Lazar MA. Retinoic acid blocks adipogenesis by inhibiting C/EBPbeta-mediated transcription. Mol Cell Biol 1997; 17: 1552-1561.
7. Pérez RJ, Benoit YD, Gudas LJ. Deletion of retinoic acid receptor β (RARβ) impairs pancreatic endocrine differentiation. Exp Cell Res 2013; 319: 2196-2204.
8. Trasino SE, Benoit YD, Gudas LJ. Vitamin A deficiency causes hyperglycemia and loss of pancreatic β-cell mass. J Biol Chem 2015; 290: 1456-1473.
9. Lund BW, Piu F, Gauthier NK etal. Discovery of a potent, orally available, and isoform-selective retinoic acid beta2 receptor agonist. J Med Chem 2005; 48: 7517-7519.
10. Chua SC, Chung WK, Wu-Peng XS et al. Phenotypes of mouse diabetes and rat fatty due to mutations in the OB (leptin) receptor. Science 1996; 271: 994-996.
11. Pelleymounter MA, Cullen MJ, Baker MB et al. Effects of the obese gene product on body weight regulation in ob/ob mice. Science 1995; 269: 540-543.
12. Brunt EM, Janney CG, Di Bisceglie AM, Neuschwander-Tetri BA, Bacon BR. Nonalcoholic steatohepatitis: a proposal for grading and staging the histological lesions. Am J Gastroenterol 1999; 94: 2467-2474.
13. Folch J, Lees M, Sloane Stanley GH. A simple method for the isolation and purification of total lipides from animal tissues. J Biol Chem 1957; 226: 497-509.
14. Tang XH, Osei-Sarfo K, Urvalek AM, Zhang T, Scognamiglio T, Gudas LJ. Combination of bexarotene and the retinoid CD1530 reduces murine oral-cavity carcinogenesis induced by the carcinogen 4-nitroquinoline 1-oxide. Proc Natl Acad Sci U S A 2014; 111: 8907-8912.
15. Steil GM, Trivedi N, Jonas JC etal. Adaptation of beta-cell mass to substrate oversupply: enhanced function with normal gene expression. Am J Physiol Endocrinol Metab 2001; 280: E788-E796.
16. Savage DB, Petersen KF, Shulman GI. Disordered lipid metabolism and the pathogenesis of insulin resistance. Physiol Rev 2007; 87: 507-520.
17. Murea M, Freedman BI, Parks JS, Antinozzi PA, Elbein SC, Ma L. Lipotoxicity in diabetic nephropathy: the potential role of fatty acid oxidation. Clin J Am Soc Nephrol 2010; 5: 2373-2379.
18. Unger RH. Lipid overload and overflow: metabolic trauma and the metabolic syndrome. Trends Endocrinol Metab 2003; 14: 398-403.
19. Patti ME, Butte AJ, Crunkhorn S etal. Coordinated reduction of genes of oxidative metabolism in humans with insulin resistance and diabetes: potential role of PGC1 and NRF1. Proc Natl Acad Sci U S A 2003; 100: 8466-8471.
20. Patti ME. Gene expression in humans with diabetes and prediabetes: what have we learned about diabetes pathophysiology? Curr Opin Clin Nutr Metab Care 2004; 7: 383-390.
21. Wurm CA, Neumann D, Lauterbach MA etal. Nanoscale distribution of mitochondrial import receptor Tom20 is adjusted to cellular conditions and exhibits an inner-cellular gradient. Proc Natl Acad Sci U S A 2011; 108: 13546-13551.
22. Furukawa S, Fujita T, Shimabukuro M etal. Increased oxidative stress in obesity and its impact on metabolic syndrome. J Clin Invest 2004; 114: 1752-1761.
23. Raptis SA, Dimitriadis GD. Oral hypoglycemic agents: insulin secretagogues, alpha-glucosidase inhibitors and insulin sensitizers. Exp Clin Endocrinol Diabetes 2001; 109(Suppl. 2): S265-S287.
24. Liu YQ, Jetton TL, Leahy JL. Beta-cell adaptation to insulin resistance. Increased pyruvate carboxylase and malate-pyruvate shuttle activity in islets of nondiabetic Zucker fatty rats. J Biol Chem 2002; 277: 39163-39168.
25. Ferrannini E, Camastra S, Gastaldelli A etal. Beta-cell function in obesity: effects of weight loss. Diabetes 2004; 53(Suppl. 3): S26-S33.
26. Gastaldelli A, Ferrannini E, Miyazaki Y, Matsuda M, Mari A, DeFronzo RA. Thiazolidinediones improve beta-cell function in type 2 diabetic patients. Am J Physiol Endocrinol Metab 2007; 292: E871-E883.
27. Shimomura I, Bashmakov Y, Horton JD. Increased levels of nuclear SREBP-1c associated with fatty livers in two mouse models of diabetes mellitus. J Biol Chem 1999; 274: 30028-30032.
28. Jiang T, Wang Z, Proctor G etal. Diet-induced obesity in C57BL/6J mice causes increased renal lipid accumulation and glomerulosclerosis via a sterol regulatory element-binding protein-1c-dependent pathway. J Biol Chem 2005; 280: 32317-32325.
29. Lenhard JM. Lipogenic enzymes as therapeutic targets for obesity and diabetes. Curr Pharm Des 2011; 17: 325-331.
30. Amengual J, Ribot J, Bonet ML, Palou A. Retinoic acid treatment enhances lipid oxidation and inhibits lipid biosynthesis capacities in the liver of mice. Cell Physiol Biochem 2010; 25: 657-666.
31. Kang HW, Bhimidi GR, Odom DP, Brun PJ, Fernandez ML, McGrane MM. Altered lipid catabolism in the vitamin A deficient liver. Mol Cell Endocrinol 2007; 271: 18-27.
32. Kim SC, Kim CK, Axe D etal. All-trans-retinoic acid ameliorates hepatic steatosis in mice by a novel transcriptional cascade. Hepatology 2014; 59: 1750-1760.
33. Amengual J, Ribot J, Bonet ML, Palou A. Retinoic acid treatment increases lipid oxidation capacity in skeletal muscle of mice. Obesity (Silver Spring) 2008; 16: 585-591.
34. Bonet ML, Ribot J, Palou A. Lipid metabolism in mammalian tissues and its control by retinoic acid. Biochim Biophys Acta 2012; 1821: 177-189.
35. Johnson EM. A risk assessment of topical tretinoin as a potential human developmental toxin based on animal and comparative human data. J Am Acad Dermatol 1997; 36: S86-S90.
36. Tallman MS, Andersen JW, Schiffer CA etal. All-trans retinoic acid in acute promyelocytic leukemia: long-term outcome and prognostic factor analysis from the North American Intergroup protocol. Blood 2002; 100: 4298-4302.
37. Tsuchiya H, Ikeda Y, Ebata Y etal. Retinoids ameliorate insulin resistance in a leptin-dependent manner in mice. Hepatology 2012; 56: 1319-1330.
38. Rogue A, Spire C, Brun M, Claude N, Guillouzo A. Gene expression changes induced by PPAR gamma agonists in animal and human liver. PPAR Res 2010; 2010: 325183.
39. Shin J, Li B, Davis ME, Suh Y, Lee K. Comparative analysis of fatty acid-binding protein 4 promoters: conservation of peroxisome proliferator-activated receptor binding sites. J Anim Sci 2009; 87: 3923-3934.
40. Graham DJ, Ouellet-Hellstrom R, MaCurdy TE etal. Risk of acute myocardial infarction, stroke, heart failure, and death in elderly Medicare patients treated with rosiglitazone or pioglitazone. JAMA 2010; 304: 411-418.
41. Kostapanos MS, Kei A, Elisaf MS. Current role of fenofibrate in the prevention and management of non-alcoholic fatty liver disease. World J Hepatol 2013; 5: 470-478.
42. Hong YA, Lim JH, Kim MY et al. Fenofibrate improves renal lipotoxicity through activation of AMPK-PGC-1α in db/db mice. PLoS One 2014; 9: e96147.
43. Liu M, Montgomery MK, Fiveash CE etal. PPARα-independent actions of omega-3 PUFAs contribute to their beneficial effects on adiposity and glucose homeostasis. Sci Rep 2014; 4: 5538.
44. Bajaj M, Suraamornkul S, Hardies LJ, Glass L, Musi N, DeFronzo RA. Effects of peroxisome proliferator-activated receptor (PPAR)-alpha and PPAR-gamma agonists on glucose and lipid metabolism in patients with type 2 diabetes mellitus. Diabetologia 2007; 50: 1723-1731.
45. Robertson RP, Harmon J, Tran PO, Poitout V. Beta-cell glucose toxicity, lipotoxicity, and chronic oxidative stress in type 2 diabetes. Diabetes 2004; 53(Suppl. 1): S119-S124.
46. Li Y, Wong K, Walsh K, Gao B, Zang M. Retinoic acid receptor β stimulates hepatic induction of fibroblast growth factor 21 to promote fatty acid oxidation and control whole-body energy homeostasis in mice. J Biol Chem 2013; 288: 10490-10504.