Retinoic acid receptor signaling is required to maintain glucose-stimulated insulin secretion and β-cell mass

FASEB Journal

Volumn 29, Issue 2, 2015, Pages 671-683

  Brun, Pierre Jacques ^a   Grijalva, Ambar ^a   Rausch, Richard ^a   Watson, Elizabeth ^a   Yuen, Jason J ^a   Das, Bhaskar C ^b   Shudo, Koichi ^c   Kagechika, Hiroyuki ^d   Leibel, Rudolph L ^a   Blaner, William S ^a  

^a New York Presbyterian Columbia University Medical Center   (United States)

^b UNIVERSITY OF KANSAS SCHOOL OF MEDICINE   (United States)

^c Kawasaki   (Japan)

^d TOKYO MEDICAL AND DENTAL UNIVERSITY   (Japan)

Author keywords

Cre recombinase; Dominant negative RAR; Glucagon; Pancreatic islet; Retinoid

Indexed keywords

GLUCOSE; GLUCOSE TRANSPORTER 2; INSULIN; MESSENGER RNA; RETINOIC ACID; RETINOIC ACID RECEPTOR ALPHA; TAMOXIFEN; CRE RECOMBINASE; GLUCOSE BLOOD LEVEL; INTEGRASE; RETINOIC ACID RECEPTOR;

ADULT; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; DUODENUM; GENE OVEREXPRESSION; HISTOPATHOLOGY; HOMEOBOX; INSULIN BLOOD LEVEL; INSULIN RELEASE; MOUSE; MUTANT; NONHUMAN; PANCREAS; PANCREAS ISLET BETA CELL; PRIORITY JOURNAL; PROMOTER REGION; QUANTITATIVE ANALYSIS; REAL TIME POLYMERASE CHAIN REACTION; RNA ISOLATION; SIGNAL TRANSDUCTION; STAINING; STIMULATION; ANIMAL; APOPTOSIS; BLOOD; C57BL MOUSE; CELL DIFFERENTIATION; CELL PROLIFERATION; CYTOLOGY; GENOTYPE; GLUCOSE BLOOD LEVEL; HOMEOSTASIS; MALE; METABOLISM; PANCREAS ISLET; SECRETION (PROCESS); TRANSGENIC MOUSE;

MUS;

ANIMALS; APOPTOSIS; BLOOD GLUCOSE; CELL DIFFERENTIATION; CELL PROLIFERATION; GENOTYPE; HOMEOSTASIS; INSULIN; INSULIN-SECRETING CELLS; INTEGRASES; ISLETS OF LANGERHANS; MALE; MICE; MICE, INBRED C57BL; MICE, TRANSGENIC; RECEPTORS, RETINOIC ACID; RNA, MESSENGER; SIGNAL TRANSDUCTION; TRETINOIN;

EID: 84934961190     PISSN: 08926638     EISSN: 15306860     Source Type: Journal    
DOI: 10.1096/fj.14-256743     Document Type: Article

References (45)

1. Ross, A. C. (2006) Vitamin A and carotenoids. In Modern Nutrition in Health and Disease (Shils, M. E., Shike, M., Ross, A. C., Caballero, B., and Cousins, R. J., eds.), pp. 351-375, Lippincott Williams &Wilkins, Philadelphia
2. Gudas, J. M., Sporn, M. B., and Roberts, A. B. (1994) Cellular biology and biochemistry of the retinoids. In The Retinoids: Biology, Chemistry and Medicine (Sporn, M. B., Roberts, A. B., and Goodman, D. S., eds.), pp. 443-520, Raven Press, New York
3. Gudas, L. J. (2012) Emerging roles for retinoids in regeneration and differentiation in normal and disease states. Biochim. Biophys. Acta 1821, 213-221
4. Mangelsdorf, D. J., Umesono, K., and Evans, R. M. (1994) The retinoids receptors. In The Retinoids: Biology, Chemistry, and Medicine (Sporn, M. B., Roberts, A. B., and Goodman, D. S., eds.), pp. 319-349, Raven Press, New York
5. Chambon, P. (1996) A decade of molecular biology of retinoic acid receptors. FASEB J. 10, 940-954
6. Chawla, A., Repa, J. J., Evans, R. M., and Mangelsdorf, D. J. (2001) Nuclear receptors and lipid physiology: opening the X-files. Science 294, 1866-1870
7. Balmer, J. E., and Blomhoff, R. (2002) Gene expression regulation by retinoic acid. J. Lipid Res. 43, 1773-1808
8. Chertow, B. S., Baranetsky, N. G., Sivitz, W. I., Meda, P., Webb, M. D., and Shih, J. C. (1983) Cellular mechanisms of insulin release. Effects of retinoids on rat islet cell-to-cell adhesion, reaggregation, and insulin release. Diabetes 32, 568-574
9. Kato, M., Kato, K., Blaner, W. S., Chertow, B. S., and Goodman, D. S. (1985) Plasma and cellular retinoid-binding proteins and transthyretin (prealbumin) are all localized in the islets of Langerhans in the rat. Proc. Natl. Acad. Sci. USA 82, 2488-2492
10. Chertow, B. S., Blaner, W. S., Baranetsky, N. G., Sivitz, W. I., Cordle, M. B., Thompson, D., and Meda, P. (1987) Effects of vitamin A deficiency and repletion on rat insulin secretion in vivo and in vitro from isolated islets. J. Clin. Invest. 79, 163-169
11. Chertow, B. S., Moore, M. R., Blaner, W. S., Wilford, M. R., and Cordle, M. B. (1989) Cytoplasmic retinoid-binding proteins and retinoid effects on insulin release in RINm5F beta-cells. Diabetes 38, 1544-1548
12. Chertow, B. S., Webb, M. D., Leidy, J. W., Jr., and Cordle, M. B. (1989) Protective effects of retinyl palmitate on streptozotocin- and alloxan-induced beta cell toxicity and diabetes in the rat. Res. Commun. Chem. Pathol. Pharmacol. 63, 27-44
13. Fernandez-Mejia, C., and Davidson, M. B. (1992) Regulation of glucokinase and proinsulin gene expression and insulin secretion in RIN-m5F cells by dexamethasone, retinoic acid, and thyroid hormone. Endocrinology 130, 1660-1668
14. Clark, A. R., Wilson, M. E., London, N. J., James, R. F., and Docherty, K. (1995) Identification and characterization of a functional retinoic acid/thyroid hormone-response element upstream of the human insulin gene enhancer. Biochem. J. 309, 863-870
15. Cabrera-Valladares, G., German, M. S., Matschinsky, F. M., Wang, J., and Fernandez-Mejia, C. (1999) Effect of retinoic acid on glucokinase activity and gene expression and on insulin secretion in primary cultures of pancreatic islets. Endocrinology 140, 3091-3096
16. Blumentrath, J., Neye, H., and Verspohl, E. J. (2001) Effects of retinoids and thiazolidinediones on proliferation, insulin release, insulin mRNA, GLUT 2 transporter protein and mRNA of INS-1 cells. Cell Biochem. Funct. 19, 159-169
17. Matthews, K. A., Rhoten, W. B., Driscoll, H. K., and Chertow, B. S. (2004) Vitamin A deficiency impairs fetal islet development and causes subsequent glucose intolerance in adult rats. J. Nutr. 134, 1958-1963
18. Pérez, R. J., Benoit, Y. D., and Gudas, L. J. (2013) Deletion of retinoic acid receptor b (RARb) impairs pancreatic endocrine differentiation. Exp. Cell Res. 319, 2196-2204
19. Chertow, B. S., Blaner, W. S., Rajan, N., Primerano, D. A., Meda, P., Cirulli, V., Krozowski, Z., Smith, R., and Cordle, M. B. (1993) Retinoic acid receptor, cytosolic retinol-binding and retinoic acid-binding protein mRNA transcripts and proteins in rat insulin-secreting cells. Diabetes 42, 1109-1114
20. Kutlu, B., Burdick, D., Baxter, D., Rasschaert, J., Flamez, D., Eizirik, D. L., Welsh, N., Goodman, N., and Hood, L. (2009) Detailed transcriptome atlas of the pancreatic beta cell. BMC Med. Genomics 2, 3
21. Miyazaki, S., Taniguchi, H., Moritoh, Y., Tashiro, F., Yamamoto, T., Yamato, E., Ikegami, H., Ozato, K., and Miyazaki, J. (2010) Nuclear hormone retinoid X receptor (RXR) negatively regulates the glucose-stimulated insulin secretion of pancreatic β-cells. Diabetes 59, 2854-2861
22. Kane, M. A., Folias, A. E., Pingitore, A., Perri, M., Obrochta, K. M., Krois, C. R., Cione, E., Ryu, J. Y., and Napoli, J. L. (2010) Identification of 9-cis-retinoic acid as a pancreas-specific autacoid that attenuates glucose-stimulated insulin secretion. Proc. Natl. Acad. Sci. USA 107, 21884-21889
23. Oström, M., Loffler, K. A., Edfalk, S., Selander, L., Dahl, U., Ricordi, C., Jeon, J., Correa-Medina, M., Diez, J., and Edlund, H. (2008) Retinoic acid promotes the generation of pancreatic endocrine progenitor cells and their further differentiation into beta-cells. PLoS One 3, e2841
24. Ravnskjaer, K., Boergesen, M., Rubi, B., Larsen, J. K., Nielsen, T., Fridriksson, J., Maechler, P., and Mandrup, S. (2005) Peroxisome proliferator-activated receptor alpha (PPARalpha) potentiates, whereas PPARgamma attenuates, glucose-stimulated insulin secretion in pancreatic beta-cells. Endocrinology 146, 3266-3276
25. Tsutusmi, A., Shiota, G., Yamazaki, H., Kunisada, T., Terada, T., and Kawasaki, H. (2000) Accelerated growth of hepatocytes in association with Up-regulation of cyclin E in transgenic mice expressing the dominant negative form of retinoic acid receptor. Biochem. Biophys. Res. Commun. 278, 229-235
26. Yanagitani, A., Yamada, S., Yasui, S., Shimomura, T., Murai, R., Murawaki, Y., Hashiguchi, K., Kanbe, T., Saeki, T., Ichiba, M., Tanabe, Y., Yoshida, Y., Morin, S., Kurimasa, A., Usuda, N., Yamazaki, H., Kunisada, T., Ito, H., Murawaki, Y., and Shiota, G. (2004) Retinoic acid receptor alpha dominant negative form causes steatohepatitis and liver tumors in transgenic mice. Hepatology 40, 366-375
27. Somenzi, G., Sala, G., Rossetti, S., Ren, M., Ghidoni, R., and Sacchi, N. (2007) Disruption of retinoic acid receptor alpha reveals the growth promoter face of retinoic acid. PLoS One 2, e836
28. Rajaii, F., Bitzer, Z. T., Xu, Q., and Sockanathan, S. (2008) Expression of the dominant negative retinoid receptor, RAR403, alters telencephalic progenitor proliferation, survival, and cell fate specification. Dev. Biol. 316, 371-382
29. Gu, G., Dubauskaite, J., and Melton, D. A. (2002) Direct evidence for the pancreatic lineage: NGN3+ cells are islet progenitors and are distinct from duct progenitors. Development 129, 2447-2457
30. Rosselot, C., Spraggon, L., Chia, I., Batourina, E., Riccio, P., Lu, B., Niederreither, K., Dolle, P., Duester, G., Chambon, P., Costantini, F., Gilbert, T., Molotkov, A., and Mendelsohn, C. (2010) Non-cell-autonomous retinoid signaling is crucial for renal development. Development 137, 283-292
31. Reeves, P. G., Nielsen, F. H., and Fahey, G. C., 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
32. National Research Council. (2011) Guide for the Care and Use of Laboratory Animals, 8th ed., National Academies Press, Washington, DC
33. Eizirik, D. L., Sandler, S., Hallberg, A., Bendtzen, K., Sener, A., and Malaisse, W. J. (1989) Differential sensitivity to beta-cell secretagogues in cultured rat pancreatic islets exposed to human interleukin-1 beta. Endocrinology 125, 752-759
34. Dokmanovic-Chouinard, M., Chung, W. K., Chevre, J. C., Watson, E., Yonan, J., Wiegand, B., Bromberg, Y., Wakae, N., Wright, C. V., Overton, J., Ghosh, S., Sathe, G. M., Ammala, C. E., Brown, K. K., Ito, R., LeDuc, C., Solomon, K., Fischer, S. G., and Leibel, R. L. (2008) Positional cloning of "Lisch-Like", a candidate modifier of susceptibility to type 2 diabetes in mice. PLoS Genet. 4, e1000137
35. Pfaffl, M. W. (2001) A new mathematical model for relative quantification in real-time RT-PCR. Nucleic Acids Res. 29, e45
36. Umemiya, H., Fukasawa, H., Ebisawa, M., Eyrolles, L., Kawachi, E., Eisenmann, G., Gronemeyer, H., Hashimoto, Y., Shudo, K., and Kagechika, H. (1997) Regulation of retinoidal actions by diazepinylbenzoic acids. Retinoid synergists which activate the RXR-RAR heterodimers. J. Med. Chem. 40, 4222-4234
37. Das, B. C., McCartin, K., Liu, T. C., Peterson, R. T., and Evans, T. (2010) A forward chemical screen in zebrafish identifies a retinoic acid derivative with receptor specificity. PLoS One 5, e10004
38. Unger, R. H., and Cherrington, A. D. (2012) Glucagonocentric restructuring of diabetes: a pathophysiologic and therapeutic makeover. J. Clin. Invest. 122, 4-12
39. Ramnanan, C. J., Edgerton, D. S., Kraft, G., and Cherrington, A. D. (2011) Physiologic action of glucagon on liver glucose metabolism. Diabetes Obes. Metab. 13(Suppl 1), 118-125
40. Lee, Y., Wang, M.-Y., Du, X. Q., Charron, M. J., and Unger, R. H. (2011) Glucagon receptor knockout prevents insulin-deficient type 1 diabetes in mice. Diabetes 60, 391-397
41. Meier, J. J., Ueberberg, S., Korbas, S., and Schneider, S. (2011) Diminished glucagon suppression after β-cell reduction is due to impaired α-cell mass function rather than an expansion of α-cell mass. Am. J. Physiol. Endocrinol. Metab. 300, E717-E223
42. Talchai, C., Xuan, S., Lin, H. V., Sussel, L., and Accili, D. (2012) Pancreatic β cell dedifferentiation as a mechanism of diabetic β cell failure. Cell 150, 1223-1234
43. Du, A., Hunter, C. S., Murray, J., Noble, D., Cai, C. L., Evans, S. M., Stein, R., and May, C. L. (2009) Islet-1 is required for the maturation, proliferation, and survival of the endocrine pancreas. Diabetes 58, 2059-2069
44. Hunter, C. S., Dixit, S., Cohen, T., Ediger, B., Wilcox, C., Ferreira, M., Westphal, H., Stein, R., and May, C. L. (2013) Islet α-, β-, and δ-cell development is controlled by the Ldb1 coregulator, acting primarily with the islet-1 transcription factor. Diabetes 62, 875-886
45. Kappen, C., and Salbaum, J. M. (2009) Identification of regulatory elements in the Isl1 gene locus. Int. J. Dev. Biol. 53, 935-946