Temporal clustering of gene expression links the metabolic transcription factor HNF4α to the ER stress-dependent gene regulatory network

Frontiers in Genetics

Volumn 4, Issue SEP, 2013, Pages

  Arensdorf, Angela M ^a   McCabe, Diane DeZwaan ^a   Kaufman, Randal J ^b   Thomas Rutkowski, D ^a  

^a UNIVERSITY OF IOWA   (United States)

^b BURNHAM INSTITUTE   (United States)

Author keywords

ER stress; Fatty liver; Functional genomics; Gene regulatory network; Lipid metabolism

Indexed keywords

EID: 84886060349     PISSN: None     EISSN: 16648021     Source Type: Journal    
DOI: 10.3389/fgene.2013.00188     Document Type: Article

References (53)

1. Arensdorf, A. M., and Rutkowski, D. T. (2013). Endoplasmic reticulum stress impairs IL-4/IL-13 signaling through C/EBPβ-mediated transcriptional suppression. J. Cell. Sci. 126, 4026-4036. doi:10.1242/jcs.130757.
2. Caviglia, J. M., Gayet, C., Ota, T., Hernandez-Ono, A., Conlon, D. M., Jiang, H., et al. (2011). Different fatty acids inhibit apoB100 secretion by different pathways:unique roles for ER stress, ceramide, and autophagy. J. Lipid Res. 52, 1636-1651. doi:10.1194/jlr. M016931.
3. Chen, W. S., Manova, K., Weinstein, D. C., Duncan, S. A., Plump, A. S., Prezioso, V. R., et al. (1994). Disruption of the HNF-4 gene, expressed in visceral endoderm, leads to cell death in embryonic ectoderm and impaired gastrulation of mouse embryos. Genes Dev. 8, 2466-2477. doi:10.1101/gad.8.20.2466.
4. Chikka, M. R., McCabe, D. D., Tyra, H. M., and Rutkowski, D. T. (2013). C/EBP homologous protein (CHOP) contributes to suppression of metabolic genes during ER stress in the liver. J. Biol. Chem. 288, 4405-4415. doi:10.1074/jbc. M112.432344.
5. Cinaroglu, A., Gao, C., Imrie, D., and Sadler, K. C. (2011). Activating transcription factor 6 plays protective and pathological roles in steatosis due to endoplasmic reticulum stress in zebrafish. Hepatology 54, 495-508. doi:10.1002/hep.24396.
6. Dalton, S., and Treisman, R. (1992). Characterization of SAP-1, a protein recruited by serum response factor to the c-fos serum response element. Cell 68, 597-612. doi:10.1016/0092-8674(92)90194-H.
7. Desvergne, B., Michalik, L., and Wahli, W. (2006). Transcriptional regulation of metabolism. Physiol. Rev. 86, 465-514. doi:10.1152/physrev.00025.2005.
8. Ellrott, K., Yang, C., Sladek, F. M., and Jiang, T. (2002). Identifying transcription factor binding sites through Markov chain optimization. Bioinformatics 18(Suppl. 2), S100-S109. doi:10.1093/bioinformatics/18.suppl_2.S100.
9. Harding, H. P., Zhang, Y., Zeng, H., Novoa, I., Lu, P. D., Calfon, M., et al. (2003). An integrated stress response regulates amino acid metabolism and resistance to oxidative stress. Mol. Cell 11, 619-633. doi:10.1016/S1097-2765(03)00105-9.
10. Hayhurst, G. P., Lee, Y. H., Lambert, G., Ward, J. M., and Gonzalez, F. J. (2001). Hepatocyte nuclear factor 4alpha (nuclear receptor 2A1) is essential for maintenance of hepatic gene expression and lipid homeostasis. Mol. Cell. Biol. 21, 1393-1403. doi:10.1128/MCB.21.4.1393-1403.2001.
11. Ho Sui, S. J., Mortimer, J. R., Arenillas, D. J., Brumm, J., Walsh, C. J., Kennedy, B. P., et al. (2005). oPOSSUM:identification of over-represented transcription factor binding sites in co-expressed genes. Nucleic Acids Res. 33, 3154-3164. doi:10.1093/nar/gki624.
12. Hollien, J., and Weissman, J. S. (2006). Decay of endoplasmic reticulum-localized mRNAs during the unfolded protein response. Science 313, 104-107. doi:10.1126/science.1129631.
13. Janknecht, R., and Hunter, T. (1997). Activation of the Sap-1a transcription factor by the c-Jun N-terminal kinase (JNK) mitogen-activated protein kinase. J. Biol. Chem. 272, 4219-4224. doi:10.1074/jbc.272.7.4219.
14. Jo, H., Choe, S. S., Shin, K. C., Jang, H., Lee, J. H., Seong, J. K., et al. (2013). Endoplasmic reticulum stress induces hepatic steatosis via increased expression of the hepatic very low-density lipoprotein receptor. Hepatology 57, 1366-1377. doi:10.1002/hep.26126.
15. Kimura, A., Nishiyori, A., Murakami, T., Tsukamoto, T., Hata, S., Osumi, T., et al. (1993). Chicken ovalbumin upstream promoter-transcription factor (COUP-TF) represses transcription from the promoter of the gene for ornithine transcarbamylase in a manner antagonistic to hepatocyte nuclear factor-4 (HNF-4). J. Biol. Chem. 268, 11125-11133.
16. Kokame, K., Kato, H., and Miyata, T. (2001). Identification of ERSE-II, a new cis-acting element responsible for the ATF6-dependent mammalian unfolded protein response. J. Biol. Chem. 276, 9199-9205. doi:10.1074/jbc. M010486200.
17. Ktistaki, E., and Talianidis, I. (1997). Chicken ovalbumin upstream promoter transcription factors act as auxiliary cofactors for hepatocyte nuclear factor 4 and enhance hepatic gene expression. Mol. Cell. Biol. 17, 2790-2797.
18. Lee, A. H., Iwakoshi, N. N., and Glimcher, L. H. (2003). XBP-1 regulates a subset of endoplasmic reticulum resident chaperone genes in the unfolded protein response. Mol. Cell. Biol. 23, 7448-7459. doi:10.1128/MCB.23.21.7448-7459.2003.
19. Lee, A. H., Scapa, E. F., Cohen, D. E., and Glimcher, L. H. (2008). Regulation of hepatic lipogenesis by the transcription factor XBP1. Science 320, 1492-1496. doi:10.1126/science.1158042.
20. Li, Y., Bevilacqua, E., Chiribau, C. B., Majumder, M., Wang, C., Croniger, C. M., et al. (2008). Differential control of the CCAAT/enhancer-binding protein beta (C/EBPbeta) products liver-enriched transcriptional activating protein (LAP) and liver-enriched transcriptional inhibitory protein (LIP) and the regulation of gene expression during the response to endoplasmic reticulum stress. J. Biol. Chem. 283, 22443-22456. doi:10.1074/jbc. M801046200.
21. Lin, J., Handschin, C., and Spiegelman, B. M. (2005a). Metabolic control through the PGC-1 family of transcription coactivators. Cell Metab. 1, 361-370. doi:10.1016/j.cmet.2005.05.004.
22. Lin, J., Yang, R., Tarr, P. T., Wu, P. H., Handschin, C., Li, S., et al. (2005b). Hyperlipidemic effects of dietary saturated fats mediated through PGC-1beta coactivation of SREBP. Cell 120, 261-273. doi:10.1016/j.cell.2004.11.043.
23. Lin, J., Tarr, P. T., Yang, R., Rhee, J., Puigserver, P., Newgard, C. B., et al. (2003). PGC-1beta in the regulation of hepatic glucose and energy metabolism. J. Biol. Chem. 278, 30843-30848. doi:10.1074/jbc. M303643200.
24. Louet, J. F., Hayhurst, G., Gonzalez, F. J., Girard, J., and Decaux, J. F. (2002). The coactivator PGC-1 is involved in the regulation of the liver carnitine palmitoyltransferase I gene expression by cAMP in combination with HNF4 alpha and cAMP-response element-binding protein (CREB). J. Biol. Chem. 277, 37991-38000. doi:10.1074/jbc. M205087200.
25. Luebke-Wheeler, J., Zhang, K., Battle, M., Si-Tayeb, K., Garrison, W., Chhinder, S., et al. (2008). Hepatocyte nuclear factor 4alpha is implicated in endoplasmic reticulum stress-induced acute phase response by regulating expression of cyclic adenosine monophosphate responsive element binding protein H. Hepatology 48, 1242-1250. doi:10.1002/hep.22439.
26. Maere, S., Heymans, K., and Kuiper, M. (2005). BiNGO:a Cytoscape plugin to assess overrepresentation of gene ontology categories in biological networks. Bioinformatics 21, 3448-3449. doi:10.1093/bioinformatics/bti551.
27. Marciniak, S. J., Yun, C. Y., Oyadomari, S., Novoa, I., Zhang, Y., Jungreis, R., et al. (2004). CHOP induces death by promoting protein synthesis and oxidation in the stressed endoplasmic reticulum. Genes Dev. 18, 3066-3077. doi:10.1101/gad.1250704.
28. Ota, T., Gayet, C., and Ginsberg, H. N. (2008). Inhibition of apolipoprotein B100 secretion by lipid-induced hepatic endoplasmic reticulum stress in rodents. J. Clin. Invest. 118, 316-332. doi:10.1172/JCI32752.
29. Prifti, E., Zucker, J. D., Clement, K., and Henegar, C. (2008). FunNet:an integrative tool for exploring transcriptional interactions. Bioinformatics 24, 2636-2638. doi:10.1093/bioinformatics/btn492.
30. Qiu, Y., Pereira, F. A., DeMayo, F. J., Lydon, J. P., Tsai, S. Y., and Tsai, M. J. (1997). Null mutation of mCOUP-TFI results in defects in morphogenesis of the glossopharyngeal ganglion, axonal projection, and arborization. Genes Dev. 11, 1925-1937. doi:10.1101/gad.11.15.1925.
31. Rhee, J., Ge, H., Yang, W., Fan, M., Handschin, C., Cooper, M., et al. (2006). Partnership of PGC-1alpha and HNF4alpha in the regulation of lipoprotein metabolism. J. Biol. Chem. 281, 14683-14690. doi:10.1074/jbc. M512636200.
32. Ron, D., and Habener, J. F. (1992). CHOP, a novel developmentally regulated nuclear protein that dimerizes with transcription factors C/EBP and LAP and functions as a dominant-negative inhibitor of gene transcription. Genes Dev. 6, 439-453. doi:10.1101/gad.6.3.439.
33. Ron, D., and Walter, P. (2007). Signal integration in the endoplasmic reticulum unfolded protein response. Nat. Rev. Mol. Cell Biol. 8, 519-529. doi:10.1038/nrm2199.
34. Rutkowski, D. T., Arnold, S. M., Miller, C. N., Wu, J., Li, J., Gunnison, K. M., et al. (2006). Adaptation to ER stress is mediated by differential stabilities of pro-survival and pro-apoptotic mRNAs and proteins. PLoS Biol. 4:e374. doi:10.1371/journal.pbio.0040374.
35. Rutkowski, D. T., Wu, J., Back, S. H., Callaghan, M. U., Ferris, S. P., Iqbal, J., et al. (2008). UPR pathways combine to prevent hepatic steatosis caused by ER stress-mediated suppression of transcriptional master regulators. Dev. Cell 15, 829-840. doi:10.1016/j.devcel.2008.10.015.
36. Schmidt, D., Wilson, M. D., Ballester, B., Schwalie, P. C., Brown, G. D., Marshall, A., et al. (2010). Five-vertebrate ChIP-seq reveals the evolutionary dynamics of transcription factor binding. Science 328, 1036-1040. doi:10.1126/science.1186176.
37. Schuldiner, M., and Weissman, J. S. (2013). The contribution of systematic approaches to characterizing the proteins and functions of the endoplasmic reticulum. Cold Spring Harb. Perspect. Biol. 5:a013284. doi:10.1101/cshperspect.a013284.
38. So, J. S., Hur, K. Y., Tarrio, M., Ruda, V., Frank-Kamenetsky, M., Fitzgerald, K., et al. (2012). Silencing of lipid metabolism genes through IRE1alpha-mediated mRNA decay lowers plasma lipids in mice. Cell Metab. 16, 487-499. doi:10.1016/j.cmet.2012.09.004.
39. Tyra, H. M., Spitz, D. R., and Rutkowski, D. T. (2012). Inhibition of fatty acid oxidation enhances oxidative protein folding and protects hepatocytes from endoplasmic reticulum stress. Mol. Biol. Cell 23, 811-819. doi:10.1091/mbc. E11-12-1011.
40. Urano, F., Wang, X., Bertolotti, A., Zhang, Y., Chung, P., Harding, H. P., et al. (2000). Coupling of stress in the ER to activation of JNK protein kinases by transmembrane protein kinase IRE1. Science 287, 664-666. doi:10.1126/science.287.5453.664.
41. Wang, S., Chen, Z., Lam, V., Han, J., Hassler, J., Finck, B. N., et al. (2012). IRE1alpha-XBP1s induces PDI expression to increase MTP activity for hepatic VLDL assembly and lipid homeostasis. Cell Metab. 16, 473-486. doi:10.1016/j.cmet.2012.09.003.
42. Wang, Y., Vera, L., Fischer, W. H., and Montminy, M. (2009). The CREB coactivator CRTC2 links hepatic ER stress and fasting gluconeogenesis. Nature 460, 534-537.
43. Wolfrum, C., and Stoffel, M. (2006). Coactivation of Foxa2 through Pgc-1beta promotes liver fatty acid oxidation and triglyceride/VLDL secretion. Cell Metab. 3, 99-110. doi:10.1016/j.cmet.2006.01.001.
44. Wu, J., Rutkowski, D. T., Dubois, M., Swathirajan, J., Saunders, T., Wang, J., et al. (2007). ATF6alpha optimizes long-term endoplasmic reticulum function to protect cells from chronic stress. Dev. Cell 13, 351-364. doi:10.1016/j.devcel.2007.07.005.
45. Yamamoto, K., Sato, T., Matsui, T., Sato, M., Okada, T., Yoshida, H., et al. (2007). Transcriptional induction of mammalian ER quality control proteins is mediated by single or combined action of ATF6alpha and XBP1. Dev. Cell 13, 365-376. doi:10.1016/j.devcel.2007.07.018.
46. Yamamoto, K., Takahara, K., Oyadomari, S., Okada, T., Sato, T., Harada, A., et al. (2010). Induction of liver steatosis and lipid droplet formation in ATF6alpha-knockout mice burdened with pharmacological endoplasmic reticulum stress. Mol. Biol. Cell 21, 2975-2986. doi:10.1091/mbc. E09-02-0133.
47. Yanai, K., Hirota, K., Taniguchi-Yanai, K., Shigematsu, Y., Shimamoto, Y., Saito, T., et al. (1999). Regulated expression of human angiotensinogen gene by hepatocyte nuclear factor 4 and chicken ovalbumin upstream promoter-transcription factor. J. Biol. Chem. 274, 34605-34612. doi:10.1074/jbc.274.49.34605.
48. Yin, L., Ma, H., Ge, X., Edwards, P. A., and Zhang, Y. (2011). Hepatic hepatocyte nuclear factor 4alpha is essential for maintaining triglyceride and cholesterol homeostasis. Arterioscler. Thromb. Vasc. Biol. 31, 328-336. doi:10.1161/ATVBAHA.110.217828.
49. Yoshida, H., Okada, T., Haze, K., Yanagi, H., Yura, T., Negishi, M., et al. (2001). Endoplasmic reticulum stress-induced formation of transcription factor complex ERSF including NF-Y (CBF) and activating transcription factors 6alpha and 6beta that activates the mammalian unfolded protein response. Mol. Cell. Biol. 21, 1239-1248. doi:10.1128/MCB.21.4.1239-1248.2001.
50. Yoshida, H., Okada, T., Haze, K., Yanagi, H., Yura, T., Negishi, M., et al. (2000). ATF6 activated by proteolysis binds in the presence of NF-Y (CBF) directly to the cis-acting element responsible for the mammalian unfolded protein response. Mol. Cell. Biol. 20, 6755-6767. doi:10.1128/MCB.20.18.6755-6767.2000.
51. Zhang, C., Wang, G., Zheng, Z., Maddipati, K. R., Zhang, X., Dyson, G., et al. (2012). Endoplasmic reticulum-tethered transcription factor cAMP responsive element-binding protein, hepatocyte specific, regulates hepatic lipogenesis, fatty acid oxidation, and lipolysis upon metabolic stress in mice. Hepatology 55, 1070-1082. doi:10.1002/hep.24783.
52. Zhang, K., Shen, X., Wu, J., Sakaki, K., Saunders, T., Rutkowski, D. T., et al. (2006). Endoplasmic reticulum stress activates cleavage of CREBH to induce a systemic inflammatory response. Cell 124, 587-599. doi:10.1016/j.cell.2005.11.040.
53. Zhang, K., Wang, S., Malhotra, J., Hassler, J. R., Back, S. H., Wang, G., et al. (2011). The unfolded protein response transducer IRE1alpha prevents ER stress-induced hepatic steatosis. EMBO J. 30, 1357-1375. doi:10.1038/emboj.2011.52.