Sustained expression of the transcription factor GLIS3 is required for normal beta cell function in adults

EMBO Molecular Medicine

Volumn 5, Issue 1, 2013, Pages 92-104

  Yang, Yisheng ^a   Chang, Benny Hung Junn ^a   Chan, Lawrence ^a,b  

^a BAYLOR COLLEGE OF MEDICINE   (United States)

^b ST LUKE S EPISCOPAL HOSPITAL   (United States)

Author keywords

Beta cells; Cyclin D2; Diabetes; Glis3; Insulin

Indexed keywords

GLUCOSE; INSULIN; TAMOXIFEN; TRANSCRIPTION FACTOR; TRANSCRIPTION FACTOR CCND2; TRANSCRIPTION FACTOR GLIS3; TRANSCRIPTION FACTOR PDX 1; UNCLASSIFIED DRUG;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; APOPTOSIS; ARTICLE; BODY WEIGHT; CELL EXPANSION; CELL FUNCTION; CELL PROLIFERATION; CONTROLLED STUDY; DIABETES MELLITUS; DOWN REGULATION; GLUCOSE BLOOD LEVEL; GLYCEMIC CONTROL; INSULIN BLOOD LEVEL; INSULIN RELEASE; LIPID DIET; MALE; MOUSE; NONHUMAN; PANCREAS ISLET BETA CELL; PRIORITY JOURNAL; PROMOTER REGION; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN PROTEIN INTERACTION; RAT;

ANIMALS; APOPTOSIS; BLOOD GLUCOSE; CELL LINE; CELL PROLIFERATION; CYCLIN D2; DIABETES MELLITUS, EXPERIMENTAL; DIET, HIGH-FAT; FEMALE; GENE EXPRESSION; HAPLOINSUFFICIENCY; INSULIN; INSULIN-SECRETING CELLS; MALE; MICE; MICE, KNOCKOUT; MICE, TRANSGENIC; RATS; REPRESSOR PROTEINS; TRANS-ACTIVATORS; TRANSCRIPTION, GENETIC;

EID: 84871949294     PISSN: 17574676     EISSN: 17574684     Source Type: Journal    
DOI: 10.1002/emmm.201201398     Document Type: Article

References (37)

1. Ackermann AM, Gannon M (2007) Molecular regulation of pancreatic beta-cell mass development, maintenance, and expansion. J Mol Endocrinol 38: 193- 206
2. Barker A, Sharp SJ, Timpson NJ, Bouatia-Naji N, Warrington NM, Kanoni S, Beilin LJ, Brage S, Deloukas P, Evans DM, et al (2011) Association of genetic Loci with glucose levels in childhood and adolescence: a meta-analysis of over 6, 000 children. Diabetes 60: 1805- 1812
3. Barrett JC, Clayton DG, Concannon P, Akolkar B, Cooper JD, Erlich HA, Julier C, Morahan G, Nerup J, Nierras C, et al (2009) Genome-wide association study and meta-analysis find that over 40 loci affect risk of type 1 diabetes. Nat Genet 41: 703- 707
4. Boesgaard TW, Grarup N, Jorgensen T, Borch-Johnsen K, Hansen T, Pedersen O (2010) Variants at DGKB/TMEM195, ADRA2A, GLIS3 and C2CD4B loci are associated with reduced glucose-stimulated beta cell function in middle-aged Danish people. Diabetologia 53: 1647- 1655
5. Cho YS, Chen CH, Hu C, Long J, Ong RT, Sim X, Takeuchi F, Wu Y, Go MJ, Yamauchi T, et al (2012) Meta-analysis of genome-wide association studies identifies eight new loci for type 2 diabetes in east Asians. Nat Genet 44: 67- 72
6. Cozar-Castellano I, Fiaschi-Taesch N, Bigatel TA, Takane KK, Garcia-Ocana A, Vasavada R, Stewart AF (2006) Molecular control of cell cycle progression in the pancreatic beta-cell. Endocr Rev 27: 356- 370
7. Dupuis J, Langenberg C, Prokopenko I, Saxena R, Soranzo N, Jackson AU, Wheeler E, Glazer NL, Bouatia-Naji N, Gloyn AL, et al (2010) New genetic loci implicated in fasting glucose homeostasis and their impact on type 2 diabetes risk. Nat Genet 42: 105- 116
8. Gannon M, Herrera PL, Wright CV (2000) Mosaic Cre-mediated recombination in pancreas using the pdx-1 enhancer/promoter. Genesis 26: 143- 144
9. Georgia S, Bhushan A (2004) Beta cell replication is the primary mechanism for maintaining postnatal beta cell mass. J Clin Invest 114: 963- 968
10. Georgia S, Hinault C, Kawamori D, Hu J, Meyer J, Kanji M, Bhushan A, Kulkarni RN (2010) Cyclin D2 is essential for the compensatory beta-cell hyperplastic response to insulin resistance in rodents. Diabetes 59: 987- 996
11. Gu C, Stein GH, Pan N, Goebbels S, Hornberg H, Nave KA, Herrera P, White P, Kaestner KH, Sussel L, et al (2010) Pancreatic beta cells require NeuroD to achieve and maintain functional maturity. Cell Metab 11: 298- 310
12. Hohmeier HE, Mulder H, Chen GX, Henkel-Rieger R, Prentki M, Newgard CB (2000) Isolation of INS-1-derived cell lines with robust ATP-sensitive K+ channel-dependent and -independent glucose-stimulated insulin secretion. Diabetes 49: 424- 430
13. Jensen J, Serup P, Karlsen C, Nielsen TF, Madsen OD (1996) mRNA profiling of rat islet tumors reveals nkx 6.1 as a beta-cell-specific homeodomain transcription factor. J Biol Chem 271: 18749- 18758
14. Jonsson J, Carlsson L, Edlund T, Edlund H (1994) Insulin-promoter-factor 1 is required for pancreas development in mice. Nature 371: 606- 609
15. Kang HS, Kim YS, ZeRuth G, Beak JY, Gerrish K, Kilic G, Sosa-Pineda B, Jensen J, Pierreux CE, Lemaigre FP, et al (2009) Transcription factor Glis3, a novel critical player in the regulation of pancreatic beta-cell development and insulin gene expression. Mol Cell Biol 29: 6366- 6379
16. Kim YS, Nakanishi G, Lewandoski M, Jetten AM (2003) GLIS3, a novel member of the GLIS subfamily of Kruppel-like zinc finger proteins with repressor and activation functions. Nucleic Acids Res 31: 5513- 5525
17. Kushner JA, Ciemerych MA, Sicinska E, Wartschow LM, Teta M, Long SY, Sicinski P, White MF (2005) Cyclins D2 and D1 are essential for postnatal pancreatic beta-cell growth. Mol Cell Biol 25: 3752- 3762
18. Liu C, Li H, Qi L, Loos RJ, Qi Q, Lu L, Gan W, Lin X (2011) Variants in GLIS3 and CRY2 are associated with type 2 diabetes and impaired fasting glucose in Chinese Hans. PLoS One 6: e21464
19. Offield MF, Jetton TL, Labosky PA, Ray M, Stein RW, Magnuson MA, Hogan BL, Wright CV (1996) PDX-1 is required for pancreatic outgrowth and differentiation of the rostral duodenum. Development 122: 983- 995
20. Ohlsson H, Karlsson K, Edlund T (1993) IPF1, a homeodomain-containing transactivator of the insulin gene. EMBO J 12: 4251- 4259
21. Olson LK, Redmon JB, Towle HC, Robertson RP (1993) Chronic exposure of HIT cells to high glucose concentrations paradoxically decreases insulin gene transcription and alters binding of insulin gene regulatory protein. J Clin Invest 92: 514- 519
22. Oster A, Jensen J, Serup P, Galante P, Madsen OD, Larsson LI (1998) Rat endocrine pancreatic development in relation to two homeobox gene products (Pdx-1 and Nkx 6.1). J Histochem Cytochem 46: 707- 715
23. Pang K, Mukonoweshuro C, Wong GG (1994) Beta cells arise from glucose transporter type 2 (Glut2)-expressing epithelial cells of the developing rat pancreas. Proc Natl Acad Sci USA 91: 9559- 9563
24. Poitout V, Robertson RP (2002) Minireview: secondary beta-cell failure in type 2 diabetes - a convergence of glucotoxicity and lipotoxicity. Endocrinology 143: 339- 342
25. Poitout V, Robertson RP (2008) Glucolipotoxicity: fuel excess and beta-cell dysfunction. Endocr Rev 29: 351- 366
26. Preitner F, Ibberson M, Franklin I, Binnert C, Pende M, Gjinovci A, Hansotia T, Drucker DJ, Wollheim C, Burcelin R, et al (2004) Gluco-incretins control insulin secretion at multiple levels as revealed in mice lacking GLP-1 and GIP receptors. J Clin Invest 113: 635- 645
27. Rees SD, Hydrie MZ, O'Hare JP, Kumar S, Shera AS, Basit A, Barnett AH, Kelly MA (2011) Effects of 16 genetic variants on fasting glucose and type 2 diabetes in South Asians: ADCY5 and GLIS3 variants may predispose to type 2 diabetes. PLoS One 6: e24710
28. Robertson RP, Harmon J, Tran PO, Poitout V (2004) Beta-cell glucose toxicity, lipotoxicity, and chronic oxidative stress in type 2 diabetes. Diabetes 53 (Suppl 1): S119- S124
29. Rudnick A, Ling TY, Odagiri H, Rutter WJ, German MS (1994) Pancreatic beta cells express a diverse set of homeobox genes. Proc Natl Acad Sci USA 91: 12203- 12207
30. Sachdeva MM, Stoffers DA (2009) Minireview: meeting the demand for insulin: molecular mechanisms of adaptive postnatal beta-cell mass expansion. Mol Endocrinol 23: 747- 758
31. Senee V, Chelala C, Duchatelet S, Feng D, Blanc H, Cossec JC, Charon C, Nicolino M, Boileau P, Cavener DR, et al (2006) Mutations in GLIS3 are responsible for a rare syndrome with neonatal diabetes mellitus and congenital hypothyroidism. Nat Genet 38: 682- 687
32. Thorens B, Weir GC, Leahy JL, Lodish HF, Bonner-Weir S (1990) Reduced expression of the liver/beta-cell glucose transporter isoform in glucose-insensitive pancreatic beta cells of diabetic rats. Proc Natl Acad Sci USA 87: 6492- 6496
33. Wang S, Jensen JN, Seymour PA, Hsu W, Dor Y, Sander M, Magnuson MA, Serup P, Gu G (2009) Sustained Neurog3 expression in hormone-expressing islet cells is required for endocrine maturation and function. Proc Natl Acad Sci USA 106: 9715- 9720
34. Watanabe N, Hiramatsu K, Miyamoto R, Yasuda K, Suzuki N, Oshima N, Kiyonari H, Shiba D, Nishio S, Mochizuki T, et al (2009) A murine model of neonatal diabetes mellitus in Glis3-deficient mice. FEBS Lett 583: 2108- 2113
35. Weir GC, Bonner-Weir S (2004) Five stages of evolving beta-cell dysfunction during progression to diabetes. Diabetes 53 (Suppl 3): S16- S21
36. Yang Y, Chang BH, Samson SL, Li MV, Chan L (2009) The Kruppel-like zinc finger protein Glis3 directly and indirectly activates insulin gene transcription. Nucleic Acids Res 37: 2529- 2538
37. Yang Y, Chang BH, Yechoor V, Chen W, Li L, Tsai MJ, Chan L (2011) The Kruppel-like zinc finger protein GLIS3 transactivates neurogenin 3 for proper fetal pancreatic islet differentiation in mice. Diabetologia 54: 2595- 2605