Retinoid metabolism and diabetes mellitus

Diabetes and Metabolism Journal

Volumn 36, Issue 3, 2012, Pages 167-180

  Rhee, Eun Jung ^a   Plutzky, Jorge ^b  

^a School of Medicine   (South Korea)

^b HARVARD MEDICAL SCHOOL   (United States)

Author keywords

Diabetes mellitus; Retinoid; Rexinoid

Indexed keywords

EID: 84864628320     PISSN: 22336079     EISSN: 22336087     Source Type: Journal    
DOI: 10.4093/dmj.2012.36.3.167     Document Type: Review

References (91)

1. Kim DJ. The epidemiology of diabetes in Korea. Diabetes Metab J 2011;35: 303-8.
2. Bendich A, Olson JA. Biological actions of carotenoids. FASEB J 1989;3: 1927-32.
3. Napoli JL. Interactions of retinoid binding proteins and enzymes in retinoid metabolism. Biochim Biophys Acta 1999;1440: 139-62.
4. Wolbach SB, Howe PR. Tissue changes following deprivation of fat-soluble a vitamin. J Exp Med 1925;42: 753-77.
5. Prieur DJ, Fenstermacher JD, Guarino AM. A choroid plexus papilloma in an elasmobranch (Squalus acanthias). J Natl Cancer Inst 1976;56: 1207-9.
6. Ferrara F. Acute promyelocytic leukemia: what are the treatment options? Expert Opin Pharmacother 2010;11: 587-96.
7. Smith JE, Milch PO, Muto Y, Goodman DS. The plasma transport and metabolism of retinoic acid in the rat. Biochem J 1973; 132: 821-7.
8. Kurlandsky SB, Gamble MV, Ramakrishnan R, Blaner WS. Plasma delivery of retinoic acid to tissues in the rat. J Biol Chem 1995;270: 17850-7.
9. Kane MA, Chen N, Sparks S, Napoli JL. Quantification of endogenous retinoic acid in limited biological samples by LC/ MS/MS. Biochem J 2005;388(Pt 1): 363-9.
10. Tang GW, Russell RM. 13-cis-retinoic acid is an endogenous compound in human serum. J Lipid Res 1990;31: 175-82.
11. Sucov HM, Evans RM. Retinoic acid and retinoic acid receptors in development. Mol Neurobiol 1995;10: 169-84.
12. Chambon P. A decade of molecular biology of retinoic acid receptors. FASEB J 1996;10: 940-54.
13. Theodosiou M, Laudet V, Schubert M. From carrot to clinic: an overview of the retinoic acid signaling pathway. Cell Mol Life Sci 2010;67: 1423-45.
14. Altucci L, Gronemeyer H. The promise of retinoids to fight against cancer. Nat Rev Cancer 2001;1: 181-93.
15. Dolle P, Ruberte E, Leroy P, Morriss-Kay G, Chambon P. Retinoic acid receptors and cellular retinoid binding proteins. I. A systematic study of their differential pattern of transcription during mouse organogenesis. Development 1990;110: 1133-51.
16. Mangelsdorf DJ, Borgmeyer U, Heyman RA, Zhou JY, Ong ES, Oro AE, Kakizuka A, Evans RM. Characterization of three RXR genes that mediate the action of 9-cis retinoic acid. Genes Dev 1992;6: 329-44.
17. Yu VC, Delsert C, Andersen B, Holloway JM, Devary OV, Naar AM, Kim SY, Boutin JM, Glass CK, Rosenfeld MG. RXR beta: a coregulator that enhances binding of retinoic acid, thyroid hormone, and vitamin D receptors to their cognate response elements. Cell 1991;67: 1251-66.
18. Kliewer SA, Umesono K, Mangelsdorf DJ, Evans RM. Retinoid X receptor interacts with nuclear receptors in retinoic acid, thyroid hormone and vitamin D3 signalling. Nature 1992;355: 446-9.
19. Mark M, Ghyselinck NB, Chambon P. Function of retinoic acid receptors during embryonic development. Nucl Recept Signal 2009;7: e002.
20. Krezel W, Ghyselinck N, Samad TA, Dupe V, Kastner P, Borrelli E, Chambon P. Impaired locomotion and dopamine signaling in retinoid receptor mutant mice. Science 1998;279: 863-7.
21. Liao WL, Tsai HC, Wang HF, Chang J, Lu KM, Wu HL, Lee YC, Tsai TF, Takahashi H, Wagner M, Ghyselinck NB, Chambon P, Liu FC. Modular patterning of structure and function of the striatum by retinoid receptor signaling. Proc Natl Acad Sci U S A 2008;105: 6765-70.
22. Krust A, Kastner P, Petkovich M, Zelent A, Chambon P. A third human retinoic acid receptor, hRAR-gamma. Proc Natl Acad Sci U S A 1989;86: 5310-4.
23. Zelent A, Krust A, Petkovich M, Kastner P, Chambon P. Cloning of murine alpha and beta retinoic acid receptors and a novel receptor gamma predominantly expressed in skin. Nature 1989;339: 714-7.
24. Kawaguchi R, Yu J, Honda J, Hu J, Whitelegge J, Ping P, Wiita P, Bok D, Sun H. A membrane receptor for retinol binding protein mediates cellular uptake of vitamin A. Science 2007;315: 820-5.
25. Gottesman ME, Quadro L, Blaner WS. Studies of vitamin A metabolism in mouse model systems. Bioessays 2001;23: 409-19.
26. Pares X, Farres J, Kedishvili N, Duester G. Medium- and shortchain dehydrogenase/reductase gene and protein families: medium-chain and short-chain dehydrogenases/reductases in retinoid metabolism. Cell Mol Life Sci 2008;65: 3936-49.
27. Duester G. Retinoic acid synthesis and signaling during early organogenesis. Cell 2008;134: 921-31.
28. Albalat R, Canestro C. Identification of Aldh1a, Cyp26 and RAR orthologs in protostomes pushes back the retinoic acid genetic machinery in evolutionary time to the bilaterian ancestor. Chem Biol Interact 2009;178: 188-96.
29. Krempf M, Ranganathan S, Ritz P, Morin M, Charbonnel B. Plasma vitamin A and E in type 1 (insulin-dependent) and type 2 (non-insulin-dependent) adult diabetic patients. Int J Vitam Nutr Res 1991;61: 38-42.
30. Basu TK, Tze WJ, Leichter J. Serum vitamin A and retinolbinding protein in patients with insulin-dependent diabetes mellitus. Am J Clin Nutr 1989;50: 329-31.
31. Tavridou A, Unwin NC, Laker MF, White M, Alberti KG. Serum concentrations of vitamins A and E in impaired glucose tolerance. Clin Chim Acta 1997;266: 129-40.
32. Erikstrup C, Mortensen OH, Nielsen AR, Fischer CP, Plomgaard P, Petersen AM, Krogh-Madsen R, Lindegaard B, Erhardt JG, Ullum H, Benn CS, Pedersen BK. RBP-to-retinol ratio, but not total RBP, is elevated in patients with type 2 diabetes. Diabetes Obes Metab 2009;11: 204-12.
33. Codner E, Loviscach M, Ciaraldi TP, Rehman N, Carter L, Mudaliar S, Henry RR. Retinoid X receptor expression in skeletal muscle of nondiabetic, obese and type 2 diabetic individuals. Metabolism 2001;50: 830-4.
34. Wang H, Chu W, Hemphill C, Hasstedt SJ, Elbein SC. Mutation screening and association of human retinoid X receptor gamma variation with lipid levels in familial type 2 diabetes. Mol Genet Metab 2002;76: 14-22.
35. Park PJ, Kong SW, Tebaldi T, Lai WR, Kasif S, Kohane IS. Integration of heterogeneous expression data sets extends the role of the retinol pathway in diabetes and insulin resistance. Bioinformatics 2009;25: 3121-7.
36. Moise AR, Kuksa V, Imanishi Y, Palczewski K. Identification of all-trans-retinol: all-trans-13,14-dihydroretinol saturase. J Biol Chem 2004;279: 50230-42.
37. Schupp M, Lefterova MI, Janke J, Leitner K, Cristancho AG, Mullican SE, Qatanani M, Szwergold N, Steger DJ, Curtin JC, Kim RJ, Suh MJ, Albert MR, Engeli S, Gudas LJ, Lazar MA. Retinol saturase promotes adipogenesis and is downregulated in obesity. Proc Natl Acad Sci U S A 2009;106: 1105-10.
38. Moise AR, Lobo GP, Erokwu B, Wilson DL, Peck D, Alvarez S, Dominguez M, Alvarez R, Flask CA, de Lera AR, von Lintig J, Palczewski K. Increased adiposity in the retinol saturase-knockout mouse. FASEB J 2010;24: 1261-70.
39. Altucci L, Leibowitz MD, Ogilvie KM, de Lera AR, Gronemeyer H. RAR and RXR modulation in cancer and metabolic disease. Nat Rev Drug Discov 2007;6: 793-810.
40. Singh Ahuja H, Liu S, Crombie DL, Boehm M, Leibowitz MD, Heyman RA, Depre C, Nagy L, Tontonoz P, Davies PJ. Differential effects of rexinoids and thiazolidinediones on metabolic gene expression in diabetic rodents. Mol Pharmacol 2001;59: 765-73.
41. Shen Q, Cline GW, Shulman GI, Leibowitz MD, Davies PJ. Effects of rexinoids on glucose transport and insulin-mediated signaling in skeletal muscles of diabetic (db/db) mice. J Biol Chem 2004;279: 19721-31.
42. Li X, Hansen PA, Xi L, Chandraratna RA, Burant CF. Distinct mechanisms of glucose lowering by specific agonists for peroxisomal proliferator activated receptor gamma and retinoic acid X receptors. J Biol Chem 2005;280: 38317-27.
43. Yamauchi T, Waki H, Kamon J, Murakami K, Motojima K, Komeda K, Miki H, Kubota N, Terauchi Y, Tsuchida A, Tsuboyama-Kasaoka N, Yamauchi N, Ide T, Hori W, Kato S, Fukayama M, Akanuma Y, Ezaki O, Itai A, Nagai R, Kimura S, Tobe K, Kagechika H, Shudo K, Kadowaki T. Inhibition of RXR and PPARgamma ameliorates diet-induced obesity and type 2 diabetes. J Clin Invest 2001;108: 1001-13.
44. Ogilvie KM, Saladin R, Nagy TR, Urcan MS, Heyman RA, Leibowitz MD. Activation of the retinoid X receptor suppresses appetite in the rat. Endocrinology 2004;145: 565-73.
45. Leibowitz MD, Ardecky RJ, Boehm MF, Broderick CL, Carfagna MA, Crombie DL, D'Arrigo J, Etgen GJ, Faul MM, Grese TA, Havel H, Hein NI, Heyman RA, Jolley D, Klausing K, Liu S, Mais DE, Mapes CM, Marschke KB, Michellys PY, Montrose-Rafizadeh C, Ogilvie KM, Pascual B, Rungta D, Tyhonas JS, Urcan MS, Wardlow M, Yumibe N, Reifel-Miller A. Biological characterization of a heterodimer-selective retinoid X receptor modulator: potential benefits for the treatment of type 2 diabetes. Endocrinology 2006;147: 1044-53.
46. Davies PJ, Berry SA, Shipley GL, Eckel RH, Hennuyer N, Crombie DL, Ogilvie KM, Peinado-Onsurbe J, Fievet C, Leibowitz MD, Heyman RA, Auwerx J. Metabolic effects of rexinoids: tissue-specific regulation of lipoprotein lipase activity. Mol Pharmacol 2001;59: 170-6.
47. Driscoll HK, Chertow BS, Jelic TM, Baltaro RJ, Chandor SB, Walker EM, Dadgari JM, Pofahl AB. Vitamin A status affects the development of diabetes and insulitis in BB rats. Metabolism 1996;45: 248-53.
48. Kobayashi H, Spilde TL, Bhatia AM, Buckingham RB, Hembree MJ, Prasadan K, Preuett BL, Imamura M, Gittes GK. Retinoid signaling controls mouse pancreatic exocrine lineage selection through epithelial-mesenchymal interactions. Gastroenterology 2002;123: 1331-40.
49. Kadison A, Kim J, Maldonado T, Crisera C, Prasadan K, Manna P, Preuett B, Hembree M, Longaker M, Gittes G. Retinoid signaling directs secondary lineage selection in pancreatic organogenesis. J Pediatr Surg 2001;36: 1150-6.
50. Chertow BS, Blaner WS, Baranetsky NG, Sivitz WI, Cordle MB, Thompson D, Meda P. Effects of vitamin A deficiency and repletion on rat insulin secretion in vivo and in vitro from isolated islets. J Clin Invest 1987;79: 163-9.
51. Tuch BE, Osgerby KJ. Maturation of insulinogenic response to glucose in human fetal pancreas with retinoic acid. Horm Metab Res Suppl 1990;25: 233-8.
52. Fernandez-Mejia C, Davidson MB. Regulation of glucokinase and proinsulin gene expression and insulin secretion in RINm5F cells by dexamethasone, retinoic acid, and thyroid hormone. Endocrinology 1992;130: 1660-8.
53. Blumentrath J, Neye H, Verspohl EJ. Effects of retinoids and thiazolidinediones on proliferation, insulin release, insulin mRNA, GLUT 2 transporter protein and mRNA of INS-1 cells. Cell Biochem Funct 2001;19: 159-69.
54. Kane MA, Folias AE, Pingitore A, Perri M, Obrochta KM, Krois CR, Cione E, Ryu JY, Napoli JL. Identification of 9-cisretinoic acid as a pancreas-specific autacoid that attenuates glucose-stimulated insulin secretion. Proc Natl Acad Sci U S A 2010;107: 21884-9.
55. Chertow BS, Driscoll HK, Goking NQ, Primerano D, Cordle MB, Matthews KA. Retinoid-X receptors and the effects of 9-cis-retinoic acid on insulin secretion from RINm5F cells. Metabolism 1997;46: 656-60.
56. Karasawa H, Nagata-Goto S, Takaishi K, Kumagae Y. A novel model of type 2 diabetes mellitus based on obesity induced by high-fat diet in BDF1 mice. Metabolism 2009;58: 296-303.
57. Shimamura M, Karasawa H, Sakakibara S, Shinagawa A. Raldh3 expression in diabetic islets reciprocally regulates secretion of insulin and glucagon from pancreatic islets. Biochem Biophys Res Commun 2010;401: 79-84.
58. Lenhard JM, Lancaster ME, Paulik MA, Weiel JE, Binz JG, Sundseth SS, Gaskill BA, Lightfoot RM, Brown HR. The RXR agonist LG100268 causes hepatomegaly, improves glycaemic control and decreases cardiovascular risk and cachexia in diabetic mice suffering from pancreatic beta-cell dysfunction. Diabetologia 1999;42: 545-54.
59. Atkinson MA, Eisenbarth GS. Type 1 diabetes: new perspectives on disease pathogenesis and treatment. Lancet 2001;358: 221-9.
60. Baena RM, Campoy C, Bayes R, Blanca E, Fernandez JM, Molina-Font JA. Vitamin A, retinol binding protein and lipids in type 1 diabetes mellitus. Eur J Clin Nutr 2002;56: 44-50.
61. Van YH, Lee WH, Ortiz S, Lee MH, Qin HJ, Liu CP. All-trans retinoic acid inhibits type 1 diabetes by T regulatory (Treg)-dependent suppression of interferon-gamma-producing T-cells without affecting Th17 cells. Diabetes 2009;58: 146-55.
62. Stosic-Grujicic S, Cvjeticanin T, Stojanovic I. Retinoids differentially regulate the progression of autoimmune diabetes in three preclinical models in mice. Mol Immunol 2009;47: 79-86.
63. Mukherjee R, Davies PJ, Crombie DL, Bischoff ED, Cesario RM, Jow L, Hamann LG, Boehm MF, Mondon CE, Nadzan AM, Paterniti JR Jr, Heyman RA. Sensitization of diabetic and obese mice to insulin by retinoid X receptor agonists. Nature 1997; 386: 407-10.
64. Sugita S, Kamei Y, Akaike F, Suganami T, Kanai S, Hattori M, Manabe Y, Fujii N, Takai-Igarashi T, Tadaishi M, Oka J, Aburatani H, Yamada T, Katagiri H, Kakehi S, Tamura Y, Kubo H, Nishida K, Miura S, Ezaki O, Ogawa Y. Increased systemic glucose tolerance with increased muscle glucose uptake in transgenic mice overexpressing RXRgamma in skeletal muscle. PLoS One 2011;6: e20467.
65. Jeyakumar SM, Vajreswari A, Giridharan NV. Chronic dietary vitamin A supplementation regulates obesity in an obese mutant WNIN/Ob rat model. Obesity (Silver Spring) 2006;14: 52-9.
66. Jeyakumar SM, Vijaya Kumar P, Giridharan NV, Vajreswari A. Vitamin A improves insulin sensitivity by increasing insulin receptor phosphorylation through protein tyrosine phosphatase 1B regulation at early age in obese rats of WNIN/Ob strain. Diabetes Obes Metab 2011;13: 955-8.
67. Berry DC, Noy N. Signaling by vitamin A and retinol-binding protein in regulation of insulin responses and lipid homeostasis. Biochim Biophys Acta 2012;1821: 168-76.
68. Matschinsky FM, Magnuson MA, Zelent D, Jetton TL, Doliba N, Han Y, Taub R, Grimsby J. The network of glucokinase-expressing cells in glucose homeostasis and the potential of glucokinase activators for diabetes therapy. Diabetes 2006;55: 1-12.
69. Chen G, Zhang Y, Lu D, Li NQ, Ross AC. Retinoids synergize with insulin to induce hepatic Gck expression. Biochem J 2009; 419: 645-53.
70. Li R, Chen W, Li Y, Zhang Y, Chen G. Retinoids synergized with insulin to induce Srebp-1c expression and activated its promoter via the two liver X receptor binding sites that mediate insulin action. Biochem Biophys Res Commun 2011;406: 268-72.
71. Flower DR. The lipocalin protein family: structure and function. Biochem J 1996;318 (Pt 1): 1-14.
72. Manolescu DC, Sima A, Bhat PV. All-trans retinoic acid lowers serum retinol-binding protein 4 concentrations and increases insulin sensitivity in diabetic mice. J Nutr 2010;140: 311-6.
73. Yang Q, Graham TE, Mody N, Preitner F, Peroni OD, Zabolotny JM, Kotani K, Quadro L, Kahn BB. Serum retinol binding protein 4 contributes to insulin resistance in obesity and type 2 diabetes. Nature 2005;436: 356-62.
74. Graham TE, Yang Q, Bluher M, Hammarstedt A, Ciaraldi TP, Henry RR, Wason CJ, Oberbach A, Jansson PA, Smith U, Kahn BB. Retinol-binding protein 4 and insulin resistance in lean, obese, and diabetic subjects. N Engl J Med 2006;354: 2552-63.
75. Janke J, Engeli S, Boschmann M, Adams F, Bohnke J, Luft FC, Sharma AM, Jordan J. Retinol-binding protein 4 in human obesity. Diabetes 2006;55: 2805-10.
76. Broch M, Vendrell J, Ricart W, Richart C, Fernandez-Real JM. Circulating retinol-binding protein-4, insulin sensitivity, insulin secretion, and insulin disposition index in obese and nonobese subjects. Diabetes Care 2007;30: 1802-6.
77. Kotnik P, Fischer-Posovszky P, Wabitsch M. RBP4: a controversial adipokine. Eur J Endocrinol 2011;165: 703-11.
78. Preitner F, Mody N, Graham TE, Peroni OD, Kahn BB. Longterm Fenretinide treatment prevents high-fat diet-induced obesity, insulin resistance, and hepatic steatosis. Am J Physiol Endocrinol Metab 2009;297: E1420-9.
79. Ellis CN, Kang S, Vinik AI, Grekin RC, Cunningham WJ, Voorhees JJ. Glucose and insulin responses are improved in patients with psoriasis during therapy with etretinate. Arch Dermatol 1987;123: 471-5.
80. Corbetta S, Angioni R, Cattaneo A, Beck-Peccoz P, Spada A. Effects of retinoid therapy on insulin sensitivity, lipid profile and circulating adipocytokines. Eur J Endocrinol 2006;154: 83-6.
81. Rodondi N, Darioli R, Ramelet AA, Hohl D, Lenain V, Perdrix J, Wietlisbach V, Riesen WF, Walther T, Medinger L, Nicod P, Desvergne B, Mooser V. High risk for hyperlipidemia and the metabolic syndrome after an episode of hypertriglyceridemia during 13-cis retinoic acid therapy for acne: a pharmacogenetic study. Ann Intern Med 2002;136: 582-9.
82. Stoll D, Binnert C, Mooser V, Tappy L. Short-term administration of isotretinoin elevates plasma triglyceride concentrations without affecting insulin sensitivity in healthy humans. Metabolism 2004;53: 4-10.
83. Ertugrul DT, Karadag AS, Tutal E, Akin KO. Isotretinoin does not induce insulin resistance in patients with acne. Clin Exp Dermatol 2011;36: 124-8.
84. Heliovaara MK, Remitz A, Reitamo S, Teppo AM, Karonen SL, Ebeling P. 13-cis-Retinoic acid therapy induces insulin resistance, regulates inflammatory parameters, and paradoxically increases serum adiponectin concentration. Metabolism 2007;56: 786-91.
85. Fu M, Sun T, Bookout AL, Downes M, Yu RT, Evans RM, Mangelsdorf DJ. A nuclear receptor atlas: 3T3-L1 adipogenesis. Mol Endocrinol 2005;19: 2437-50.
86. Xue JC, Schwarz EJ, Chawla A, Lazar MA. Distinct stages in adipogenesis revealed by retinoid inhibition of differentiation after induction of PPARgamma. Mol Cell Biol 1996;16: 1567-75.
87. Napoli JL. Retinoic acid: its biosynthesis and metabolism. Prog Nucleic Acid Res Mol Biol 1999;63: 139-88.
88. Ziouzenkova O, Orasanu G, Sharlach M, Akiyama TE, Berger JP, Viereck J, Hamilton JA, Tang G, Dolnikowski GG, Vogel S, Duester G, Plutzky J. Retinaldehyde represses adipogenesis and diet-induced obesity. Nat Med 2007;13: 695-702.
89. Ress NB, Hailey JR, Maronpot RR, Bucher JR, Travlos GS, Haseman JK, Orzech DP, Johnson JD, Hejtmancik MR. Toxicology and carcinogenesis studies of microencapsulated citral in rats and mice. Toxicol Sci 2003;71: 198-206.
90. Berry DC, Noy N. All-trans-retinoic acid represses obesity and insulin resistance by activating both peroxisome proliferationactivated receptor beta/delta and retinoic acid receptor. Mol Cell Biol 2009;29: 3286-96.
91. Barish GD, Narkar VA, Evans RM. PPAR delta: a dagger in the heart of the metabolic syndrome. J Clin Invest 2006;116: 590-7.