Transcriptional cross talk between orphan nuclear receptor ERRγ and transmembrane transcription factor ATF6α coordinates endoplasmic reticulum stress response

Nucleic Acids Research

Volumn 41, Issue 14, 2013, Pages 6960-6974

  Misra, Jagannath ^a   Kim, Don Kyu ^a   Choi, Woogyun ^b   Koo, Seung Hoi ^c   Lee, Chul Ho ^d   Back, Sung Hoon ^b   Kaufman, Randal J ^e   Choi, Hueng Sik ^a,f  

^a Chonnam National University   (South Korea)

^b University of Ulsan   (South Korea)

^c Korea University   (South Korea)

^d Korea Research Institute of Bioscience and Biotechnology (KRIBB)   (South Korea)

^e BURNHAM INSTITUTE   (United States)

^f Chonnam National University Medical School   (South Korea)

Author keywords

[No Author keywords available]

Indexed keywords

ACTIVATING TRANSCRIPTION FACTOR 6; ACTIVATING TRANSCRIPTION FACTOR 6 ALPHA; ESTROGEN RELATED RECEPTOR GAMMA; HISTONE H3; HISTONE H4; ORPHAN NUCLEAR RECEPTOR; PEROXISOME PROLIFERATOR ACTIVATED RECEPTOR GAMMA COACTIVATOR 1ALPHA; UNCLASSIFIED DRUG;

ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; BINDING SITE; CELLULAR STRESS RESPONSE; CHROMATIN IMMUNOPRECIPITATION; CONTROLLED STUDY; DNA RESPONSIVE ELEMENT; ENDOPLASMIC RETICULUM STRESS; GENE EXPRESSION REGULATION; GENETIC TRANSCRIPTION; HISTONE ACETYLATION; HUMAN; HUMAN CELL; MALE; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROMOTER REGION; PROTEIN BINDING; TRANSCRIPTION INITIATION;

ACTIVATING TRANSCRIPTION FACTOR 6; ANIMALS; CELL LINE; ENDOPLASMIC RETICULUM STRESS; HUMANS; MALE; MICE; MICE, INBRED C57BL; RECEPTORS, ESTROGEN; RESPONSE ELEMENTS; TRANSCRIPTION FACTORS; TRANSCRIPTIONAL ACTIVATION;

EID: 84881525905     PISSN: 03051048     EISSN: 13624962     Source Type: Journal    
DOI: 10.1093/nar/gkt429     Document Type: Article

References (79)

1. Ariazi E.A., Ariazi J.L., Cordera F. and Jordan V.C. (2006) Estrogen receptors as therapeutic targets in breast cancer. Curr. Top. Med. Chem., 6, 181-202
2. Lui K., Huang Y., Choi H.L., Yu S., Wong K.B., Chen S. and Chan F.L. (2006) Molecular cloning and functional study of rat estrogen receptor-related receptor gin rat prostatic cells. Prostate., 66, 1600-1619
3. Giguère V. (2008) Transcriptional control of energy homeostasis by the estrogen-related receptors. Endocr. Rev., 29, 677-696
4. Riggins R.B., Lan J.P., Zhu Y., Klimach U., Zwart A., Cavalli L.R., Haddad B.R., Chen L., Gong T., Xuan J. et al. (2008) ERRg mediates tamoxifen resistance in novel models of invasive lobular breast cancer. Cancer Res., 68, 8908-8917
5. Dufour C.R., Wilson B.J., Huss J.M., Kelly D.P., Alaynick W.A., Downes M., Evans R.M., Blanchette M. and Giguère V. (2007) Genome-wide orchestration of cardiac functions by the orphan nuclear receptors ERRalpha and g. Cell Metab., 5, 345-356
6. Kim D.K., Ryu D., Koh M., Lee M.W., Lim D., Kim M.J., Kim Y.H., Cho W.J., Lee C.H., Park S.B. et al. (2012) Orphan nuclear receptor estrogen-related receptor g (ERRg) is key regulator of hepatic gluconeogenesis. J. Biol. Chem., 287, 21628-21639
7. Kim D.K., Kim J.R., Koh M., Kim Y.D., Lee J.M., Chanda D., Park S.B., Min J.J., Lee C.H., Park T.S. et al. (2011) Estrogenrelated receptor g (ERRg) is a novel transcriptional regulator of phosphatidic acid phosphatase, LIPIN1, and inhibits hepatic insulin signaling. J. Biol. Chem., 286, 38035-38042
8. Kim D.K., Kim Y.H., Jang H.H., Park J., Kim J.R., Koh M., Jeong W.I., Koo S.H., Park T.S., Yun C.H. et al. (2012) Estrogen-related receptor g controls hepatic CB1 receptormediated CYP2E1 expression and oxidative liver injury by alcohol. Gut., 62, 1044-1054
9. Lee J.H., Kim E.J., Kim D.K., Lee J.M., Park S.B., Lee I.K., Harris R.A., Lee M.O. and Choi H.S. (2012) Hypoxia induces PDK4 gene expression through induction of the orphan nuclear receptor ERRg. PLoS One, 7, e46324
10. Kaplowitz N., Than T.A., Shinohara M. and Ji C. (2007) Endoplasmic reticulum stress and liver injury. Semin Liver Dis., 27, 367-377
11. Ji C. and Kaplowitz N. (2006) ER stress: Can the liver copé J. Hepatol., 45, 321-333
12. Malhi H. and Kaufman R.J. (2011) Endoplasmic reticulum stress in liver disease. J. Hepatol., 54, 795-809
13. Harding H.P. and Ron D. (2002) Endoplasmic reticulum stress and the development of diabetes. Diabetes, 51, S455-S461
14. Hai T.W., Liu F., Coukos W.J. and Green M.R. (1989) Transcription factor ATF cDNA clones: An extensive family of leucine zipper proteins able to selectively form DNA-binding heterodimers. Genes Dev., 3, 2083-2090
15. Haze K., Yoshida H., Yanagi H., Yura T. and Mori K. (1999) Mammalian transcription factor ATF6 is synthesized as a transmembrane protein and activated by proteolysis in response to endoplasmic reticulum stress. Mol. Biol. Cell, 10, 3787-3799
16. Ye J., Rawson R.B., Komuro R., Chen X., Davé.U.P., Prywes R., Brown M.S. and Goldstein J.L. (2000) ER stress induces cleavage of membrane-bound ATF6 by the same proteases that process SREBPs. Mol. Cell, 6, 1355-1364
17. Wang Y., Shen J., Arenzana N., Tirasophon W., Kaufman R.J. and Prywes R. (2000) Activation of ATF6 and an ATF6 DNA binding site by the endoplasmic reticulum stress response. J. Biol. Chem., 275, 27013-27020
18. Wu J., Rutkowski D.T., Dubois M., Swathirajan J., Saunders T., Wang J., Song B., Yau G.D. and Kaufman R.J. (2007) ATF6a optimizes long-Term endoplasmic reticulum function to protect cells from chronic stress. Dev. Cell, 13, 351-364
19. Terai K., Hiramoto Y., Masaki M., Sugiyama S., Kuroda T., Hori M., Kawase I. and Hirota H. (2005) AMP-Activated protein kinase protects cardiomyocytes against hypoxic injury through attenuation of endoplasmic reticulum stress. Mol. Cell. Biol., 25, 9554-9575
20. Shuda M., Kondoh N., Imazeki N., Tanaka K., Okada T., Mori K., Hada A., Arai M., Wakatsuki T., Matsubara O. et al. (2003) Activation of the ATF6, XBP1 and grp78 genes in human hepatocellular carcinoma: A possible involvement of the ER stress pathway in hepatocarcinogenesis. J. Hepatol., 38, 605-614
21. Zhu C., Johansen F.E. and Prywes R. (1997) Interaction of ATF6 and serum response factor. Mol. Cell. Biol., 17, 4957-4966
22. Wu J., Ruas J.L., Estall J.L., Rasbach K.A., Choi J.H., Ye L., Boström P., Tyra H.M., Crawford R.W., Campbell K.P. et al. (2011) The unfolded protein response mediates adaptation to exercise in skeletal muscle through a PGC-1a/ATF6a complex. Cell Metab., 13, 160-169
23. Puigserver P., Wu Z., Park C.W., Graves R., Wright M. and Spiegelman B.M. (1998) A cold-inducible coactivator of nuclear receptors linked to adaptive thermogenesis. Cell, 92, 829-839
24. Puigserver P. and Spiegelman B.M. (2003) Peroxisome proliferator- Activated receptor-g coactivator 1 alpha (PGC-1 alpha): Transcriptional coactivator and metabolic regulator. Endocr. Rev., 24, 78-90
25. Knutti D. and Kralli A. (2001) PGC-1, a versatile coactivator. Trends Endocrinol. Metab., 12, 360-365
26. Knutti D., Kaul A. and Kralli A. (2000) A tissue-specific coactivator of steroid receptors, identified in a functional genetic screen. Mol. Cell. Biol., 20, 2411-2422
27. Wu Z., Puigserver P., Andersson U., Zhang C., Adelmant G., Mootha V., Troy A., Cinti S., Lowell B., Scarpulla R.C. et al. (1999) Mechanisms controlling mitochondrial biogenesis and respiration through the thermogenic coactivator PGC-1. Cell, 98, 115-124
28. Yoon J.C., Puigserver P., Chen G., Donovan J., Wu Z., Rhee J., Adelmant G., Stafford J., Kahn C.R., Granner D.K. et al. (2001) Control of hepatic gluconeogenesis through the transcriptional coactivator PGC-1. Nature, 413, 131-138
29. Tcherepanova I., Puigserver P., Norris J.D., Spiegelman B.M. and McDonnell D.P. (2000) Modulation of estrogen receptor-Alpha transcriptional activity by the coactivator PGC-1. J. Biol. Chem., 275, 16302-16308
30. Vega R.B., Huss J.M. and Kelly D.P. (2000) The coactivator PGC-1 cooperates with peroxisome proliferator-Activated receptor alpha in transcriptional control of nuclear genes encoding mitochondrial fatty acid oxidation enzymes. Mol. Cell. Biol., 20, 1868-1876
31. Delerive P., Wu Y., Burris T.P., Chin W.W. and Suen C.S. (2002) PGC-1 functions as a transcriptional coactivator for the retinoid X receptors. J. Biol. Chem., 277, 3913-3917
32. Schreiber S.N., Knutti D., Brogli K., Uhlmann T. and Kralli A. (2003) The transcriptional coactivator PGC-1 regulates the expression and activity of the orphan nuclear receptor estrogenrelated receptor alpha (ERRalpha). J. Biol. Chem., 278, 9013-9018
33. Knutti D., Kressler D. and Kralli A. (2001) Regulation of the transcriptional coactivator PGC-1 via MAPK-sensitive interaction with a repressor. Proc. Natl. Acad. Sci. USA, 98, 9713-9718
34. Arany Z., He H., Lin J., Hoyer K., Handschin C., Toka O., Ahmad F., Matsui T., Chin S., Wu P.H. et al. (2005) Transcriptional coactivator PGC-1 alpha controls the energy state and contractile function of cardiac muscle. Cell Metab., 1, 259-271
35. Seo H.Y., Kim Y.D., Lee K.M., Min A.K., Kim M.K., Kim H.S., Won K.C., Park J.Y., Lee K.U., Choi H.S. et al. (2008) Endoplasmic reticulum stress-induced activation of activating transcription factor 6 decreases insulin gene expression via upregulation of orphan nuclear receptor small heterodimer partner. Endocrinology, 149, 3832-3841
36. Khozoie C., Borland M.G., Zhu B., Baek S., John S., Hager G.L., Shah Y.M., Gonzalez F.J. and Peters J.M. (2012) Analysis of the peroxisome proliferator-Activated receptor-beta/delta (PPARbeta/ delta) cistrome reveals novel co-regulatory role of ATF4. BMC Genomics, 13, 665
37. Fang Y., Yan J., Ding L., Liu Y., Zhu J., Huang C., Zhao H., Lu Q., Zhang X., Yang X. et al. (2004) XBP-1 increases ERalpha transcriptional activity through regulation of large-scale chromatin unfolding. Biochem. Biophys. Res. Commun., 323, 269-274
38. Ding L., Yan J., Zhu J., Zhong H., Lu Q., Wang Z., Huang C. and Ye Q. (2003) Ligand-independent activation of estrogen receptor alpha by XBP-1. Nucleic Acids Res., 31, 5266-5274
39. Zhang K., Shen X., Wu J., Sakaki K., Saunders T., Rutkowski D.T., Back S.H. and Kaufman R.J. (2006) Endoplasmic reticulum stress activates cleavage of CREBH to induce a systemic inflammatory response. Cell, 124, 587-599
40. Danno H., Ishii K.A., Nakagawa Y., Mikami M., Yamamoto T., Yabe S., Furusawa M., Kumadaki S., Watanabe K., Shimizu H. et al. (2010) The liver-enriched transcription factor CREBH is nutritionally regulated and activated by fatty acids and PPARalpha. Biochem. Biophys. Res. Commun., 391, 1222-1227
41. Luebke-Wheeler J., Zhang K., Battle M., Si-Tayeb K., Garrison W., Chhinder S., Li J., Kaufman R.J. and Duncan S.A. (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
42. Cao M., Tong Y., Lv Q., Chen X., Long Y., Jiang L., Wan J., Zhang Y., Zhang F. and Tong N. (2012) PPARd activation rescues pancreatic b-cell line INS-1E from palmitate-induced endoplasmic reticulum stress through enhanced fatty acid oxidation. PPAR Res., 2012, 680684
43. Park S.H., Choi H.J., Yang H., Do K.H., Kim J., Lee D.W. and Moon Y. (2010) Endoplasmic reticulum stress-Activated C/EBP homologous protein enhances nuclear factor-kappaB signals via repression of peroxisome proliferator- Activated receptor g. J. Biol. Chem., 285, 35330-35339
44. Tirasophon W., Welihinda A.A. and Kaufman R.J. (1998) A stress response pathway from the endoplasmic reticulum to the nucleus requires a novel bifunctional protein kinase/ endoribonuclease (Ire1p) in mammalian cells. Genes Dev., 12, 1812-1824
45. Ryu D., Seo W.Y., Yoon Y.S., Kim Y.N., Kim S.S., Kim H.J., Park T.S., Choi C.S. and Koo S.H. (2011) Endoplasmic reticulum stress promotes LIPIN2-dependent hepatic insulin resistance. Diabetes, 60, 1072-1081
46. Misra J., Chanda D., Kim D.K., Li T., Koo S.H., Back S.H., Chiang J.Y. and Choi H.S. (2011) Curcumin differentially regulates endoplasmic reticulum stress through transcriptional corepressor SMILE (small heterodimer partner-interacting leucine zipper protein)-mediated inhibition of CREBH (cAMP responsive element-binding protein H). J. Biol. Chem., 286, 41972-41984
47. Koo S.H., Satoh H., Herzig S., Lee C.H., Hedrick S., Kulkarni R., Evans R.M., Olefsky J. and Montminy M. (2004) PGC-1 promotes insulin resistance in liver through PPAR-Alphadependent induction of TRB-3. Nat. Med., 10, 530-534
48. Xie Y.B., Nedumaran B. and Choi H.S. (2009) Molecular characterization of SMILE as a novel corepressor of nuclear receptors. Nucleic Acids Res., 37, 4100-4115
49. Sakaki K., Wu J. and Kaufman R.J. (2008) Protein kinase C is required for autophagy in response to stress in the endoplasmic reticulum. J. Biol. Chem., 283, 15370-15380
50. Chanda D., Li T., Song K.H., Kim Y.H., Sim J., Lee C.H., Chiang J.Y. and Choi H.S. (2009) Hepatocyte growth factor family negatively regulates hepatic gluconeogenesis via induction of orphan nuclear receptor small heterodimer partner in primary hepatocytes. J. Biol. Chem., 284, 28510-25821
51. Xie Y.B., Park J.H., Kim D.K., Hwang J.H., Oh S., Park S.B., Shong M., Lee I.K. and Choi H.S. (2009) Transcriptional corepressor SMILE recruits SIRT1 to inhibit nuclear receptor estrogen receptor-related receptor g transactivation. J. Biol. Chem., 284, 28762-28774
52. Gu Y., Sun X.X., Ye J.M., He L., Yan S.S., Zhang H.H., Hu L.H., Yuan J.Y. and Yu Q. (2012) Arctigenin alleviates ER stress via activating AMPK. Acta Pharmacol. Sin., 33, 941-952
53. Wang S. and Kaufman R.J. (2012) The impact of the unfolded protein response on human disease. J. Cell Biol., 197, 857-867
54. Kanemoto S., Kondo S., Ogata M., Murakami T., Urano F. and Imaizumi K. (2005) XBP1 activates the transcription of its target genes via an ACGT core sequence under ER stress. Biochem. Biophys. Res. Commun., 331, 1146-1153
55. Marciniak S.J., Yun C.Y., Oyadomari S., Novoa I., Zhang Y., Jungreis R., Nagata K., Harding H.P. and Ron D. (2004) CHOP induces death by promoting protein synthesis and oxidation in the stressed endoplasmic reticulum. Genes Dev., 18, 3066-3077
56. Yemelyanov A., Bhalla P., Yang X., Ugolkov A., Iwadate K., Karseladze A. and Budunova I. (2012) Differential targeting of androgen and glucocorticoid receptors induces ER stress and apoptosis in prostate cancer cells: A novel therapeutic modality. Cell Cycle, 11, 395-406
57. Verdin E., Dequiedt F. and Kasler H.G. (2003) Class II histone deacetylases: Versatile regulators. Trends Genet., 19, 286-293
58. Benjamin I.J. (2006) Viewing a stressful episode of ER: Is ATF6 the triage nursé Circ. Res., 98, 1120-1122
59. Nagamori I., Yomogida K., Ikawa M., Okabe M., Yabuta N. and Nojima H. (2006) The testes-specific bZip type transcription factor Tisp40 plays a role in ER stress responses and chromatin packaging during spermiogenesis. Genes Cells, 11, 1161-1171
60. Wallberg A.E., Yamamura S., Malik S., Spiegelman B.M. and Roeder R.G. (2003) Coordination of p300-mediated chromatin remodeling and TRAP/mediator function through coactivator PGC-1alpha. Mol. Cell, 12, 1137-1149
61. Zhang Y., Ma K., Sadana P., Chowdhury F., Gaillard S., Wang F., McDonnell D.P., Unterman T.G., Elam M.B. and Park E.A. (2006) Estrogen-related receptors stimulate pyruvate dehydrogenase kinase isoform 4 gene expression. J. Biol. Chem., 281, 39897-39906
62. Longato L., Ripp K., Setshedi M., Dostalek M., Akhlaghi F., Branda M., Wands J.R. and de la Monte S.M. (2012) Insulin resistance, ceramide accumulation, and endoplasmic reticulum stress in human chronic alcohol-related liver disease. Oxid. Med. Cell Longev., 2012, 479348
63. Connaughton S., Chowdhury F., Attia R.R., Song S., Zhang Y., Elam M.B., Cook G.A. and Park E.A. (2010) Regulation of pyruvate dehydrogenase kinase isoform 4 (PDK4) gene expression by glucocorticoids and insulin. Mol. Cell Endocrinol., 315, 159-167
64. Lee M.W., Chanda D., Yang J., Oh H., Kim S.S., Yoon Y.S., Hong S., Park K.G., Lee I.K., Choi C.S. et al. (2010) Regulation of Hepatic Gluconeogenesis by an ER-Bound Transcription Factor, CREBH. Cell Metab., 11, 331-339
65. Zhang L.H. and Zhang X. (2010) Roles of GRP78 in physiology and cancer. J. Cell Biochem., 110, 1299-1305
66. Rutkowski D.T., Wu J., Back S.H., Callaghan M.U., Ferris S.P., Iqbal J., Clark R., Miao H., Hassler J.R., Fornek 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
67. Yamamoto K., Takahara K., Oyadomari S., Okada T., Sato T., Harada A. and Mori K. (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
68. Lowe C.E., Dennis R.J., Obi U., O'Rahilly S. and Rochford J.J. (2012) Investigating the involvement of the ATF6a pathway of the unfolded protein response in adipogenesis. Int. J. Obes. (Lond), 36, 1248-1251
69. Usui M., Yamaguchi S., Tanji Y., Tominaga R., Ishigaki Y., Fukumoto M., Katagiri H., Mori K., Oka Y. and Ishihara H. (2012) Atf6a-null mice are glucose intolerant due to pancreatic b-cell failure on a high-fat diet but partially resistant to diet-induced insulin resistance. Metabolism, 61, 1118-1128
70. Poidatz D., Dos Santos E., Brulé,A., De, Mazancourt P. and Dieudonné,M.N. (2012) Estrogen-related receptor g modulates energy metabolism target genes in human trophoblast. Placenta, 33, 688-695
71. Raciti G.A., Iadicicco C., Ulianich L., Vind B.F., Gaster M., Andreozzi F., Longo M., Teperino R., Ungaro P., Di Jeso B. et al. (2010) Glucosamine-induced endoplasmic reticulum stress affects GLUT4 expression via activating transcription factor 6in rat and human skeletal muscle cells. Diabetologia, 53, 955-965
72. He B. (2006) Viruses, endoplasmic reticulum stress, and interferon responses. Cell Death Differ., 13, 393-403
73. Avidal L.M., Ló pez S. and Arias C.F. (2008) Endoplasmic reticulum chaperones are involved in the morphogenesis of rotavirus infectious particles. J. Virol., 82, 5368-5380
74. Alhusaini S., McGee K., Schisano B., Harte A., McTernan P., Kumar S. and Tripathi G. (2010) Lipopolysaccharide, high glucose and saturated fatty acids induce endoplasmic reticulum stress in cultured primary human adipocytes: Salicylate alleviates this stress. Biochem. Biophys. Res. Commun., 397, 472-478
75. Belmont P.J., Chen W.J., Thuerauf D.J. and Glembotski C.C. (2012) Regulation of microRNA expression in the heart by the ATF6 branch of the ER stress response. J. Mol. Cell Cardiol., 52, 1176-1182
76. Voleti B., Hammond D.J. Jr, Thirumalai A. and Agrawal A. (2012) Oct-1 acts as a transcriptional repressor on the C-reactive protein promoter. Mol. Immunol., 52, 242-248
77. 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
78. Luo S., Baumeister P., Yang S., Abcouwer S.F. and Lee A.S. (2003) Induction of Grp78/BiP by translational block: Activation of the Grp78 promoter by ATF4 through and upstream ATF/ CRE site independent of the endoplasmic reticulum stress elements. J. Biol. Chem., 278, 37375-37385
79. Shen J. and Prywes R. (2005) ER stress signaling by regulated proteolysis of ATF6. Methods, 35, 382-389