FOXO1 competes with carbohydrate response element-binding protein (ChREBP) and inhibits thioredoxin-interacting protein (TXNIP) transcription in pancreatic beta cells

Journal of Biological Chemistry

Volumn 288, Issue 32, 2013, Pages 23194-23202

  Kibbe, Carly ^a,b   Chen, Junqin ^a   Xu, Guanlan ^a   Jing, Gu ^a   Shalev, Anath ^a  

^a UNIVERSITY OF ALABAMA AT BIRMINGHAM   (United States)

^b UNIVERSITY OF WISCONSIN MADISON   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BETA CELL; ELEMENT-BINDING PROTEINS; NOVEL GENES; PANCREATIC BETA CELLS; REGULATORY MECHANISM;

GLUCOSE; PROTEINS;

TRANSCRIPTION;

BINDING PROTEIN; CARBOHYDRATE RESPONSE ELEMENT BINDING PROTEIN; PYRUVATE KINASE; THIOREDOXIN INTERACTING PROTEIN; TRANSCRIPTION FACTOR FKHR; UNCLASSIFIED DRUG;

ANIMAL CELL; ARTICLE; BINDING SITE; CELL LINE; CELL STRAIN INS 1; CHROMATIN IMMUNOPRECIPITATION; CONTROLLED STUDY; GEL MOBILITY SHIFT ASSAY; GENETIC TRANSFECTION; MOLECULAR MECHANICS; MUTANT; NONHUMAN; PANCREAS ISLET BETA CELL; PRIORITY JOURNAL; PROMOTER REGION; PROTEIN BINDING; PROTEIN DNA BINDING; PROTEIN EXPRESSION; PROTEIN MOTIF; RAT; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; SIGNAL TRANSDUCTION; WESTERN BLOTTING;

BETA CELL; CHREBP; DIABETES; FOXO; THIOREDOXIN; TRANSCRIPTION REGULATION; TXNIP;

AMINO ACID SUBSTITUTION; ANIMALS; BASIC HELIX-LOOP-HELIX LEUCINE ZIPPER TRANSCRIPTION FACTORS; CARRIER PROTEINS; CELL LINE, TUMOR; FORKHEAD TRANSCRIPTION FACTORS; GENE EXPRESSION REGULATION; GLUCOSE; HUMANS; INSULIN-SECRETING CELLS; MUTATION, MISSENSE; NERVE TISSUE PROTEINS; PROMOTER REGIONS, GENETIC; RATS; TRANSCRIPTION, GENETIC;

EID: 84881461824     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M113.473082     Document Type: Article

References (33)

1. Shalev, A., Pise-Masison, C. A., Radonovich, M., Hoffmann, S. C., Hirshberg, B., Brady, J. N., and Harlan, D. M. (2002) Oligonucleotide microarray analysis of intact human pancreatic islets: identification of glucose-responsive genes and a highly regulated TGFsignaling pathway. Endocrinology 143, 3695-3698
2. Chen, K. S., and DeLuca, H. F. (1994) Isolation and characterization of a novel cDNA from HL-60 cells treated with 1,25-dihydroxyvitamin D3. Biochim. Biophys. Acta 1219, 26-32
3. Junn, E., Han, S. H., Im, J. Y., Yang, Y., Cho, E. W., Um, H. D., Kim, D. K., Lee, K. W., Han, P. L., Rhee, S. G., and Choi, I. (2000) Vitamin D3 upregulated protein 1 mediates oxidative stress via suppressing the thioredoxin function. J. Immunol. 164, 6287-6295
4. Nishiyama, A., Masutani, H., Nakamura, H., Nishinaka, Y., and Yodoi, J. (2001) Redox regulation by thioredoxin and thioredoxin-binding proteins. IUBMB Life 52, 29-33
5. Nishiyama, A., Matsui, M., Iwata, S., Hirota, K., Masutani, H., Nakamura, H., Takagi, Y., Sono, H., Gon, Y., and Yodoi, J. (1999) Identification of thioredoxin-binding protein-2/vitamin D3 up-regulated protein 1 as a negative regulator of thioredoxin function and expression. J. Biol. Chem. 274, 21645-21650
6. Yamanaka, H., Maehira, F., Oshiro, M., Asato, T., Yanagawa, Y., Takei, H., and Nakashima, Y. (2000) A possible interaction of thioredoxin with VDUP1 in HeLa cells detected in a yeast two-hybrid system. Biochem. Biophys. Res. Commun. 271, 796-800
7. Chen, J., Saxena, G., Mungrue, I. N., Lusis, A. J., and Shalev, A. (2008) Thioredoxin-interacting protein: a critical link between glucose toxicity and beta cell apoptosis. Diabetes 57, 938-944
8. Minn, A. H., Hafele, C., and Shalev, A. (2005) Thioredoxin-interacting protein is stimulated by glucose through a carbohydrate response element and induces beta cell apoptosis. Endocrinology 146, 2397-2405
9. Minn, A. H., Pise-Masison, C. A., Radonovich, M., Brady, J. N., Wang, P., Kendziorski, C., and Shalev, A. (2005) Gene expression profiling in INS-1 cells overexpressing thioredoxin-interacting protein. Biochem. Biophys. Res. Commun. 336, 770-778
10. Chen, J., Hui, S. T., Couto, F. M., Mungrue, I. N., Davis, D. B., Attie, A. D., Lusis, A. J., Davis, R. A., and Shalev, A. (2008) Thioredoxin-interacting protein deficiency induces Akt/Bcl-xL signaling and pancreatic beta cell mass and protects against diabetes. FASEB J. 22, 3581-3594
11. Masson, E., Koren, S., Razik, F., Goldberg, H., Kwan, E. P., Sheu, L., Gaisano, H. Y., and Fantus, I. G. (2009) High beta cell mass prevents streptozotocin-induced diabetes in thioredoxin-interacting protein-deficient mice. Am. J. Physiol. Endocrinol. Metab. 296, E1251-1261
12. Cha-Molstad, H., Saxena, G., Chen, J., and Shalev, A. (2009) Glucosestimulated expression of TXNIP is mediated by carbohydrate response element-binding protein, p300, and histone H4 acetylation in pancreatic beta cells. J. Biol. Chem. 284, 16898-16905
13. Boergesen, M., Poulsen, L. L., Schmidt, S. F., Frigerio, F., Maechler, P., and Mandrup, S. (2011) ChREBP mediates glucose repression of peroxisome proliferator-activated receptor expression in pancreatic beta cells. J. Biol. Chem. 286, 13214-13225
14. Poungvarin, N., Lee, J. K., Yechoor, V. K., Li, M. V., Assavapokee, T., Suksaranjit, P., Thepsongwajja, J. J., Saha, P. K., Oka, K., and Chan, L. (2012) Carbohydrate response element-binding protein (ChREBP) plays a pivotal role in beta cell glucotoxicity. Diabetologia 55, 1783-1796
15. Kawaguchi, T., Takenoshita, M., Kabashima, T., and Uyeda, K. (2001) Glucose andcAMPregulate the L-type pyruvate kinase gene by phosphorylation/ dephosphorylation of the carbohydrate response element binding protein. Proc. Natl. Acad. Sci. U.S.A. 98, 13710-13715
16. Wang, H., and Wollheim, C. B. (2002) ChREBP rather than USF2 regulates glucose stimulation of endogenous L-pyruvate kinase expression in insulin-secreting cells. J. Biol. Chem. 277, 32746-32752
17. O'Callaghan, B. L., Koo, S. H., Wu, Y., Freake, H. C., and Towle, H. C. (2001) Glucose regulation of the acetyl-CoA carboxylase promoter PI in rat hepatocytes. J. Biol. Chem. 276, 16033-16039
18. Rufo, C., Teran-Garcia, M., Nakamura, M. T., Koo, S. H., Towle, H. C., and Clarke, S. D. (2001) Involvement of a unique carbohydrate-responsive factor in the glucose regulation of rat liver fatty-acid synthase gene transcription. J. Biol. Chem. 276, 21969-21975
19. Glauser, D. A., and Schlegel, W. (2007) The emerging role of FOXO transcription factors in pancreatic beta cells. J. Endocrinol. 193, 195-207
20. Kitamura, T., and Ido Kitamura, Y. (2007) Role of FOXO proteins in pancreatic beta cells. Endocr. J. 54, 507-515
21. Maiese, K., Chong, Z. Z., Hou, J., and Shang, Y. C. (2009) The "O" class: crafting clinical care with FOXO transcription factors. Adv. Exp. Med. Biol. 665, 242-260
22. Buteau, J., and Accili, D. (2007) Regulation of pancreatic beta cell function by the forkhead protein FOXO1. Diabetes Obes. Metab. 9, 140-146
23. Kitamura, Y. I., Kitamura, T., Kruse, J. P., Raum, J. C., Stein, R., Gu, W., and Accili, D. (2005) FOXO1 protects against pancreatic beta cell failure through NeuroD and MafA induction. Cell Metab. 2, 153-163
24. Buteau, J., Spatz, M. L., and Accili, D. (2006) Transcription factor FOXO1 mediates glucagon-like peptide-1 effects on pancreatic beta cell mass. Diabetes 55, 1190-1196
25. Kawamori, D., Kaneto, H., Nakatani, Y., Matsuoka, T. A., Matsuhisa, M., Hori, M., and Yamasaki, Y. (2006) The forkhead transcription factor FOXO1 bridges the JNK pathway and the transcription factor PDX-1 through its intracellular translocation. J. Biol. Chem. 281, 1091-1098
26. Okamoto, H., Hribal, M. L., Lin, H. V., Bennett, W. R., Ward, A., and Accili, D. (2006) Role of the forkhead protein FOXO1 in beta cell compensation to insulin resistance. J. Clin. Invest. 116, 775-782
27. Kitamura, T., Nakae, J., Kitamura, Y., Kido, Y., Biggs, W. H., 3rd, Wright, C. V., White, M. F., Arden, K. C., and Accili, D. (2002) The forkhead transcription factor FOXO1 links insulin signaling to Pdx1 regulation of pancreatic beta cell growth. J. Clin. Invest. 110, 1839-1847
28. de Candia, P., Blekhman, R., Chabot, A. E., Oshlack, A., and Gilad, Y. (2008) A combination of genomic approaches reveals the role of FOXO1a in regulating an oxidative stress response pathway. PLoS One 3, e1670
29. Al-Mubarak, B., Soriano, F. X., and Hardingham, G. E. (2009) Synaptic NMDAR activity suppresses FOXO1 expression via a cis-acting FOXO binding site: FOXO1 is a FOXO target gene. Channels 3, 233-238
30. Li, X., Rong, Y., Zhang, M., Wang, X. L., LeMaire, S. A., Coselli, J. S., Zhang, Y., and Shen, Y. H. (2009) Up-regulation of thioredoxin-interacting protein (TXNIP) by p38 MAPK and FOXO1 contributes to the impaired thioredoxin activity and increased ROS in glucose-treated endothelial cells. Biochem. Biophys. Res. Commun. 381, 660-665
31. Tang, E. D., Nuñez, G., Barr, F. G., and Guan, K. L. (1999) Negative regulation of the forkhead transcription factor FKHR by Akt. J. Biol. Chem. 274, 16741-16746
32. Talchai, C., Xuan, S., Lin, H. V., Sussel, L., and Accili, D. (2012) Pancreatic beta cell dedifferentiation as a mechanism of diabetic beta cell failure. Cell 150, 1223-1234
33. Ma, L., Robinson, L. N., and Towle, H. C. (2006) ChREBP*Mlx is the principal mediator of glucose-induced gene expression in the liver. J. Biol. Chem. 281, 28721-28730