FoxO1 inhibits sterol regulatory element-binding protein-1c (SREBP-1c) gene expression via transcription factors Sp1 and SREBP-1c

Journal of Biological Chemistry

Volumn 287, Issue 24, 2012, Pages 20132-20143

  Deng, Xiong ^a,b   Zhang, Wenwei ^c,d   O Sullivan, InSug ^c,d   Williams, J Bradley ^c,d   Dong, Qingming ^a,b   Park, Edwards A ^b   Raghow, Rajendra ^a,b,e   Unterman, Terry G ^c,d   Elam, Marshall B ^a,b  

^a VETERANS AFFAIRS MEDICAL CENTER   (United States)

^b UNIVERSITY OF TENNESSEE HEALTH SCIENCE CENTER   (United States)

^c JESSE BROWN VA MEDICAL CENTER   (United States)

^d UNIVERSITY OF ILLINOIS   (United States)

^e DEPARTMENT OF VETERANS AFFAIRS   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BASAL EXPRESSION; CHROMATIN IMMUNOPRECIPITATION ASSAY; COMBINED ACTIONS; CONSTITUTIVELY ACTIVES; FEED FORWARD; IN-VITRO; IN-VIVO; INSULIN ACTION; KNOCK OUTS; LIPID METABOLISMS; LIPOGENESIS; PRIMARY HEPATOCYTES; PROMOTER ACTIVITIES; PROMOTER REGION; TRANSCRIPTIONAL ACTIVITY; TRANSCRIPTIONAL COMPLEXES; TRANSCRIPTIONAL INITIATION;

ALCOHOLS; GENES; INSULIN; TRANSCRIPTION FACTORS;

TRANSCRIPTION;

INSULIN; LIVER X RECEPTOR; LIVER X RECEPTOR AGONIST; STEROL REGULATORY ELEMENT BINDING PROTEIN 1C; TRANSCRIPTION FACTOR; TRANSCRIPTION FACTOR FOX01; TRANSCRIPTION FACTOR SP1; UNCLASSIFIED DRUG;

ANIMAL CELL; ARTICLE; CHROMATIN IMMUNOPRECIPITATION; CONTROLLED STUDY; GENE; GENE DISRUPTION; GENE EXPRESSION REGULATION; GENETIC TRANSCRIPTION; IN VITRO STUDY; IN VIVO STUDY; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROMOTER REGION; PROTEIN ASSEMBLY; PROTEIN DEPLETION; PROTEIN EXPRESSION; PROTEIN FOLDING; PROTEIN INDUCTION; PROTEIN PHOSPHORYLATION; PROTEINASE INHIBITION; SREBP1 GENE; TRANSCRIPTION INITIATION;

ANIMALS; CELLS, CULTURED; FORKHEAD TRANSCRIPTION FACTORS; GENE EXPRESSION REGULATION; HEPATOCYTES; INSULIN; LIVER; MICE; MICE, KNOCKOUT; NERVE TISSUE PROTEINS; ORPHAN NUCLEAR RECEPTORS; RATS; RESPONSE ELEMENTS; SP1 TRANSCRIPTION FACTOR; STEROL REGULATORY ELEMENT BINDING PROTEIN 1; TRANSCRIPTION, GENETIC;

MUS;

EID: 84862004148     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M112.347211     Document Type: Article

References (48)

1. Barthel, A., Schmoll, D., and Unterman, T. G. (2005) FoxO proteins in insulin action and metabolism. Trends Endocrinol. Metab. 16, 183-189 (Pubitemid 40603098)
2. Haeusler, R. A., and Accili, D. (2008) The double life of IRS. Cell Metab. 8, 7-9 (Pubitemid 351859234)
3. Horton, J. D., Goldstein, J. L., and Brown, M. S. (2002) SREBPs. Activators of the complete program of cholesterol and fatty acid synthesis in the liver. J. Clin. Invest. 109, 1125-1131 (Pubitemid 34496588)
4. Puigserver, P., Rhee, J., Donovan, J., Walkey, C. J., Yoon, J. C., Oriente, F., Kitamura, Y., Altomonte, J., Dong, H., Accili, D., and Spiegelman, B. M. (2003) Insulin-regulated hepatic gluconeogenesis through FOXO1-PGC-1α interaction. Nature 423, 550-555 (Pubitemid 36648580)
5. Raghow, R., Yellaturu, C., Deng, X., Park, E. A., and Elam, M. B. (2008) SREBPs. The cross-roads of physiological and pathological lipid homeostasis. Trends Endocrinol. Metab. 19, 65-73 (Pubitemid 351317897)
6. Zhang, W., Patil, S., Chauhan, B., Guo, S., Powell, D. R., Le, J., Klotsas, A., Matika, R., Xiao, X., Franks, R., Heidenreich, K. A., Sajan, M. P., Farese, R. V., Stolz, D. B., Tso, P., Koo, S. H., Montminy, M., and Unterman, T. G. (2006) FoxO1 regulates multiple metabolic pathways in the liver. Effects on gluconeogenic, glycolytic, and lipogenic gene expression. J. Biol. Chem. 281, 10105-10117 (Pubitemid 43864546)
7. Matsumoto, M., Han, S., Kitamura, T., and Accili, D. (2006) Dual role of transcription factor FoxO1 in controlling hepatic insulin sensitivity and lipid metabolism. J. Clin. Invest. 116, 2464-2472 (Pubitemid 44330145)
8. Brunet, A., Bonni, A., Zigmond, M. J., Lin, M. Z., Juo, P., Hu, L. S., Anderson, M. J., Arden, K. C., Blenis, J., and Greenberg, M. E. (1999) Akt promotes cell survival by phosphorylating and inhibiting a Forkhead transcription factor. Cell 96, 857-868 (Pubitemid 29165088)
9. Scheimann, A. O., Durham, S. K., Suwanichkul, A., Snuggs, M. B., and Powell, D. R. (2001) Role of three FKHR phosphorylation sites in insulin inhibition of FKHR action in hepatocytes. Horm. Metab. Res. 33, 631-638 (Pubitemid 33151460)
10. Woods, Y. L., Rena, G., Morrice, N., Barthel, A., Becker, W., Guo, S., Unterman, T. G., and Cohen, P. (2001) The kinase DYRK1A phosphorylates the transcription factor FKHR at Ser-329 in vitro, a novel in vivo phosphorylation site. Biochem. J. 355, 597-607 (Pubitemid 32434075)
11. Rena, G., Guo, S., Cichy, S. C., Unterman, T. G., and Cohen, P. (1999) Phosphorylation of the transcription factor forkhead family member FKHR by protein kinase B. J. Biol. Chem. 274, 17179-17183
12. Rena, G., Prescott, A. R., Guo, S., Cohen, P., and Unterman, T. G. (2001) Roles of the forkhead in rhabdomyosarcoma (FKHR) phosphorylation sites in regulating 14-3-3 binding, transactivation, and nuclear targetting. Biochem. J. 354, 605-612 (Pubitemid 32269724)
13. Zhao, X., Gan, L., Pan, H., Kan, D., Majeski, M., Adam, S. A., and Unterman, T. G. (2004) Multiple elements regulate nuclear/cytoplasmic shuttling of FOXO1. Characterization of phosphorylation- and 14-3-3-dependent and -independent mechanisms. Biochem. J. 378, 839-849 (Pubitemid 38406861)
14. Paik, J. H., Kollipara, R., Chu, G., Ji, H., Xiao, Y., Ding, Z., Miao, L., Tothova, Z., Horner, J. W., Carrasco, D. R., Jiang, S., Gilliland, D. G., Chin, L., Wong, W. H., Castrillon, D. H., and DePinho, R. A. (2007) FoxOs are lineage-restricted redundant tumor suppressors and regulate endothelial cell homeostasis. Cell 128, 309-323 (Pubitemid 46123514)
15. Cagen, L. M., Deng, X., Wilcox, H. G., Park, E. A., Raghow, R., and Elam, M. B. (2005) Insulin activates the rat sterol regulatory element-binding protein 1c (SREBP-1c) promoter through the combinatorial actions of SREBP, LXR, Sp-1, and NF-Y cis-acting elements. Biochem. J. 385, 207-216
16. Deng, X., Yellaturu, C., Cagen, L., Wilcox, H. G., Park, E. A., Raghow, R., and Elam, M. B. (2007) Expression of the rat sterol regulatory element-binding protein-1c gene in response to insulin is mediated by increased transactivating capacity of specificity protein 1 (Sp1). J. Biol. Chem. 282, 17517-17529 (Pubitemid 47100272)
17. Thijssen-Timmer, D. C., Schiphorst, M. P., Kwakkel, J., Emter, R., Kralli, A., Wiersinga, W. M., and Bakker, O. (2006) PGC-1α regulates the isoform mRNA ratio of the alternatively spliced thyroid hormone receptor α transcript. J. Mol. Endocrinol. 37, 251-257 (Pubitemid 44615297)
18. Haeusler, R. A., Kaestner, K. H., and Accili, D. (2010) FoxOs function synergistically to promote glucose production. J. Biol. Chem. 285, 35245-35248
19. Tothova, Z., Kollipara, R., Huntly, B. J., Lee, B. H., Castrillon, D. H., Cullen, D. E., McDowell, E. P., Lazo-Kallanian, S., Williams, I. R., Sears, C., Armstrong, S. A., Passegué, E., DePinho, R. A., and Gilliland, D. G. (2007) FoxOs are critical mediators of hematopoietic stem cell resistance to physiologic oxidative stress. Cell 128, 325-339 (Pubitemid 46137992)
20. Guo, S., Rena, G., Cichy, S., He, X., Cohen, P., and Unterman, T. (1999) Phosphorylation of serine 256 by protein kinase B disrupts transactivation by FKHR and mediates effects of insulin on insulin-like growth factor-binding protein-1 promoter activity through a conserved insulin response sequence. J. Biol. Chem. 274, 17184-17192
21. Deng, X., Cagen, L. M., Wilcox, H. G., Park, E. A., Raghow, R., and Elam, M. B. (2002) Regulation of the rat SREBP-1c promoter in primary rat hepatocytes. Biochem. Biophys. Res. Commun. 290, 256-262 (Pubitemid 34694492)
22. Amemiya-Kudo, M., Shimano, H., Yoshikawa, T., Yahagi, N., Hasty, A. H., Okazaki, H., Tamura, Y., Shionoiri, F., Iizuka, Y., Ohashi, K., Osuga, J., Harada, K., Gotoda, T., Sato, R., Kimura, S., Ishibashi, S., and Yamada, N. (2000) Promoter analysis of the mouse sterol regulatory element-binding protein-1c gene. J. Biol. Chem. 275, 31078-31085
23. Chen, G., Liang, G., Ou, J., Goldstein, J. L., and Brown, M. S. (2004) Central role for liver X receptor in insulin-mediated activation of Srebp-1c transcription and stimulation of fatty acid synthesis in liver. Proc. Natl. Acad. Sci. U.S.A. 101, 11245-11250 (Pubitemid 39038332)
24. Howell, G., 3rd, Deng, X., Yellaturu, C., Park, E. A., Wilcox, H. G., Raghow, R., and Elam, M. B. (2009) N-3 polyunsaturated fatty acids suppress insulin-induced SREBP-1c transcription via reduced trans-activating capacity of LXRα. Biochim. Biophys. Acta 1791, 1190-1196
25. Yellaturu, C. R., Deng, X., Cagen, L. M., Wilcox, H. G., Mansbach, C. M., 2nd, Siddiqi, S. A., Park, E. A., Raghow, R., and Elam, M. B. (2009) Insulin enhances post-translational processing of nascent SREBP-1c by promoting its phosphorylation and association with COPII vesicles. J. Biol. Chem. 284, 7518-7532
26. Liu, X., Qiao, A., Ke, Y., Kong, X., Liang, J., Wang, R., Ouyang, X., Zuo, J., Chang, Y., and Fang, F. (2010) FoxO1 represses LXRα-mediated transcriptional activity of SREBP-1c promoter in HepG2 cells. FEBS Lett. 584, 4330-4334
27. Dong, X. C., Copps, K. D., Guo, S., Li, Y., Kollipara, R., DePinho, R. A., and White, M. F. (2008) Inactivation of hepatic Foxo1 by insulin signaling is required for adaptive nutrient homeostasis and endocrine growth regulation. Cell Metab. 8, 65-76 (Pubitemid 351863393)
28. Hirota, K., Daitoku, H., Matsuzaki, H., Araya, N., Yamagata, K., Asada, S., Sugaya, T., and Fukamizu, A. (2003) Hepatocyte nuclear factor-4 is a novel downstream target of insulin via FKHR as a signal-regulated transcriptional inhibitor. J. Biol. Chem. 278, 13056-13060 (Pubitemid 36800073)
29. Dowell, P., Otto, T. C., Adi, S., and Lane, M. D. (2003) Convergence of peroxisome proliferator-activated receptor γ and FoxO1 signaling pathways. J. Biol. Chem. 278, 45485-45491 (Pubitemid 37432687)
30. Liu, Z. P., Wang, Z., Yanagisawa, H., and Olson, E. N. (2005) Phenotypic modulation of smooth muscle cells through interaction of FoxO4 and myocardin. Dev Cell 9, 261-270
31. Kamei, Y., Miura, S., Suganami, T., Akaike, F., Kanai, S., Sugita, S., Katsumata, A., Aburatani, H., Unterman, T. G., Ezaki, O., and Ogawa, Y. (2008) Regulation of SREBP1c gene expression in skeletal muscle. Role of retinoid X receptor/liver X receptor and forkhead-O1 transcription factor. Endocrinology 149, 2293-2305
32. Liu, P., Li, S., Gan, L., Kao, T. P., and Huang, H. (2008) A transcription-independent function of FOXO1 in inhibition of androgen-independent activation of the androgen receptor in prostate cancer cells. Cancer Res. 68, 10290-10299
33. Nasrin, N., Ogg, S., Cahill, C. M., Biggs, W., Nui, S., Dore, J., Calvo, D., Shi, Y., Ruvkun, G., and Alexander-Bridges, M. C. (2000) DAF-16 recruits the CREB-binding protein coactivator complex to the insulin-like growth factor-binding protein 1 promoter in HepG2 cells. Proc. Natl. Acad. Sci. U.S.A. 97, 10412-10417
34. Wasner, C., Grempler, R., Walther, R., and Schmoll, D. (2001) Basal level of glucose-6-phosphatase gene transcription requires binding site for Sp family proteins within the gene promoter. Biochim. Biophys. 1521, 126-129 (Pubitemid 33020774)
35. Nakae, J., Kitamura, T., Ogawa, W., Kasuga, M., and Accili, D. (2001) Insulin regulation of gene expression through the forkhead transcription factor Foxo1 (Fkhr) requires kinases distinct from Akt. Biochemistry 40, 11768-11776 (Pubitemid 32906038)
36. Unterman, T. G., Lacson, R. G., McGary, E., Whalen, C., Purple, C., and Goswami, R. G. (1992) Cloning of the rat insulin-like growth factor binding protein-1 gene and analysis of its 5′ promoter region. Biochem. Biophys. Res. Commun. 185, 993-999
37. Pugh, B. F., and Tjian, R. (1991) Transcription from a TATA-less promoter requires a multisubunit TFIID complex. Genes Dev. 5, 1935-1945 (Pubitemid 21905887)
38. Solomon, S. S., Majumdar, G., Martinez-Hernandez, A., and Raghow, R. (2008) A critical role of Sp1 transcription factor in regulating gene expression in response to insulin and other hormones. Life Sci. 83, 305-312
39. Tzivion, G., Dobson, M., and Ramakrishnan, G. (2011) FoxO transcription factors: Regulation by AKT and 14-3-3 proteins. Biochim. Biophys. Acta, 1813, 1938-1945
40. Qu, S., Altomonte, J., Perdomo, G., He, J., Fan, Y., Kamagate, A., Meseck, M., and Dong, H. H. (2006) Aberrant Forkhead box O1 function is associated with impaired hepatic metabolism. Endocrinology 147, 5641-5652 (Pubitemid 44833481)
41. Nakae, J., Barr, V., and Accili, D. (2000) Differential regulation of gene expression by insulin and IGF-1 receptors correlates with phosphorylation of a single amino acid residue in the forkhead transcription factor FKHR. EMBO J. 19, 989-996 (Pubitemid 30119824)
42. Naïmi, M., Gautier, N., Chaussade, C., Valverde, A. M., Accili, D., and Van Obberghen, E. (2007) Nuclear forkhead box O1 controls and integrates key signaling pathways in hepatocytes. Endocrinology 148, 2424-2434 (Pubitemid 46997056)
43. Rena, G., Woods, Y. L., Prescott, A. R., Peggie, M., Unterman, T. G., Williams, M. R., and Cohen, P. (2002) Two novel phosphorylation sites on FKHR that are critical for its nuclear exclusion. EMBO J. 21, 2263-2271 (Pubitemid 34516785)
44. Zhang, X., Gan, L., Pan, H., Guo, S., He, X., Olson, S. T., Mesecar, A., Adam, S., and Unterman, T. G. (2002) Phosphorylation of serine 256 suppresses transactivation by FKHR (FOXO1) by multiple mechanisms. Direct and indirect effects on nuclear/cytoplasmic shuttling and DNA binding. J. Biol. Chem. 277, 45276-45284 (Pubitemid 36159133)
45. Fleischmann, M., and Iynedjian, P. B. (2000) Regulation of sterol regulatory element-binding protein 1 gene expression in liver. Role of insulin and protein kinase B/cAkt. Biochem. J. 349, 13-17 (Pubitemid 30440159)
46. Yecies, J. L., Zhang, H. H., Menon, S., Liu, S., Yecies, D., Lipovsky, A. I., Gorgun, C., Kwiatkowski, D. J., Hotamisligil, G. S., Lee, C. H., and Manning, B. D. (2011) Akt stimulates hepatic SREBP1c and lipogenesis through parallel mTORC1-dependent and -independent pathways. Cell Metab. 14, 21-32
47. Chen, C. C., Jeon, S. M., Bhaskar, P. T., Nogueira, V., Sundararajan, D., Tonic, I., Park, Y., and Hay, N. (2010) FoxOs inhibitmTORC1and activate Akt by inducing the expression of Sestrin3 and Rictor. Dev. Cell 18, 592-604
48. Haeusler, R. A., Han, S., and Accili, D. (2010) Hepatic FoxO1 ablation exacerbates lipid abnormalities during hyperglycemia. J. Biol. Chem. 285, 26861-26868