BRD7 regulates XBP1s' activity and glucose homeostasis through its interaction with the regulatory subunits of PI3K

Cell Metabolism

Volumn 20, Issue 1, 2014, Pages 73-84

  Park, Sang Won ^a   Herrema, Hilde ^a   Salazar, Mario ^a   Cakir, Isin ^a   Cabi, Serkan ^a   Basibuyuk Sahin, Fatma ^a   Chiu, Yu Hsin ^b,c   Cantley, Lewis C ^b,c,d   Ozcan, Umut ^a  

^a BOSTON CHILDREN S HOSPITAL   (United States)

^b HARVARD MEDICAL SCHOOL   (United States)

^c BETH ISRAEL DEACONESS MEDICAL CENTER   (United States)

^d WEILL CORNELL MEDICAL COLLEGE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ACETYL COENZYME A; BROMODOMAIN CONTAINING PROTEIN 7; DIACYLGLYCEROL ACYLTRANSFERASE 2; FATTY ACID SYNTHASE; FRUCTOSE BISPHOSPHATASE; GLUCOSE 6 PHOSPHATASE; INSULIN RECEPTOR; INSULIN RECEPTOR SUBSTRATE 1; MESSENGER RNA; PHOSPHATIDYLINOSITOL 3 KINASE; PHOSPHOENOLPYRUVATE CARBOXYKINASE (GTP); PROTEIN; PROTEIN DNAJ; PROTEIN KINASE B; PROTEIN P85; PROTEIN P85 ALPHA; PROTEIN P85 BETA; RECOMBINANT HUMAN INSULIN; SHORT HAIRPIN RNA; UNCLASSIFIED DRUG; X BOX BINDING PROTEIN 1; BRD7 PROTEIN, MOUSE; DNA BINDING PROTEIN; GLUCOSE; NONHISTONE PROTEIN; PROTEIN SUBUNIT; REGULATORY FACTOR X TRANSCRIPTION FACTORS; SMALL INTERFERING RNA; TRANSCRIPTION FACTOR; PEPTIDES AND PROTEINS; PROTEIN P85ALPHA; PROTEIN P85BETA;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; CYTOPLASM; ENDOPLASMIC RETICULUM; ENDOPLASMIC RETICULUM STRESS; GENE EXPRESSION; GLUCOSE BLOOD LEVEL; GLUCOSE HOMEOSTASIS; GLUCOSE METABOLISM; GLUCOSE TOLERANCE; HEK293 CELL LINE; IMMUNOPRECIPITATION; IN VIVO STUDY; INSULIN SENSITIVITY; INSULIN TOLERANCE TEST; INSULIN TREATMENT; LIVER; MALE; MOUSE; NONHUMAN; OBESITY; PRIORITY JOURNAL; PROTEIN PHOSPHORYLATION; PROTEIN PROTEIN INTERACTION; UNFOLDED PROTEIN RESPONSE; UPREGULATION; WESTERN BLOTTING; ANIMAL; ANTAGONISTS AND INHIBITORS; CELL LINE; CELL NUCLEUS; CHEMISTRY; DEFICIENCY; GENETICS; HUMAN; METABOLISM; MOUSE MUTANT; PROTEIN SUBUNIT; RNA INTERFERENCE; SIGNAL TRANSDUCTION;

MUS;

ANIMALS; CELL LINE; CELL NUCLEUS; CHROMOSOMAL PROTEINS, NON-HISTONE; DNA-BINDING PROTEINS; ENDOPLASMIC RETICULUM STRESS; GLUCOSE; HEK293 CELLS; HUMANS; LIVER; MALE; MICE; MICE, OBESE; PHOSPHATIDYLINOSITOL 3-KINASE; PROTEIN SUBUNITS; RNA INTERFERENCE; RNA, MESSENGER; RNA, SMALL INTERFERING; TRANSCRIPTION FACTORS;

EID: 84904050616     PISSN: 15504131     EISSN: 19327420     Source Type: Journal    
DOI: 10.1016/j.cmet.2014.04.006     Document Type: Article

References (55)

1. D. Accili, and K.C. Arden FoxOs at the crossroads of cellular metabolism, differentiation, and transformation Cell 117 2004 421 426
2. S. Bernales, F.R. Papa, and P. Walter Intracellular signaling by the unfolded protein response Annu. Rev. Cell Dev. Biol. 22 2006 487 508
3. M. Blüher, B.B. Kahn, and C.R. Kahn Extended longevity in mice lacking the insulin receptor in adipose tissue Science 299 2003 572 574
4. S.M. Brachmann, K. Ueki, J.A. Engelman, R.C. Kahn, and L.C. Cantley Phosphoinositide 3-kinase catalytic subunit deletion and regulatory subunit deletion have opposite effects on insulin sensitivity in mice Mol. Cell. Biol. 25 2005 1596 1607
5. A.E. Burrows, A. Smogorzewska, and S.J. Elledge Polybromo-associated BRG1-associated factor components BRD7 and BAF180 are critical regulators of p53 required for induction of replicative senescence Proc. Natl. Acad. Sci. USA 107 2010 14280 14285
6. M. Calfon, H. Zeng, F. Urano, J.H. Till, S.R. Hubbard, H.P. Harding, S.G. Clark, and D. Ron IRE1 couples endoplasmic reticulum load to secretory capacity by processing the XBP-1 mRNA Nature 415 2002 92 96
7. Y.H. Chiu, J.Y. Lee, and L.C. Cantley BRD7, a Tumor Suppressor, Interacts with p85α and Regulates PI3K Activity Mol. Cell 54 2014 193 202
8. C. de Luca, and J.M. Olefsky Stressed out about obesity and insulin resistance Nat. Med. 12 2006 41 42 discussion 42
9. J. Drost, F. Mantovani, F. Tocco, R. Elkon, A. Comel, H. Holstege, R. Kerkhoven, J. Jonkers, P.M. Voorhoeve, R. Agami, and G. Del Sal BRD7 is a candidate tumour suppressor gene required for p53 function Nat. Cell Biol. 12 2010 380 389
10. S.G. Fonseca, J. Gromada, and F. Urano Endoplasmic reticulum stress and pancreatic β-cell death Trends Endocrinol. Metab. 22 2011 266 274
11. A. Guilherme, J.V. Virbasius, V. Puri, and M.P. Czech Adipocyte dysfunctions linking obesity to insulin resistance and type 2 diabetes Nat. Rev. Mol. Cell Biol. 9 2008 367 377
12. M.T. Harte, G.J. O'Brien, N.M. Ryan, J.J. Gorski, K.I. Savage, N.T. Crawford, P.B. Mullan, and D.P. Harkin BRD7, a subunit of SWI/SNF complexes, binds directly to BRCA1 and regulates BRCA1-dependent transcription Cancer Res. 70 2010 2538 2547
13. A.L. Hevener, M.A. Febbraio Stock Conference Working Group The 2009 stock conference report: inflammation, obesity and metabolic disease Obes. Rev. 11 2010 635 644
14. T. Kadowaki, K. Hara, T. Yamauchi, Y. Terauchi, K. Tobe, and R. Nagai Molecular mechanism of insulin resistance and obesity Exp. Biol. Med. (Maywood) 228 2003 1111 1117
15. M.D. Kaeser, A. Aslanian, M.Q. Dong, J.R. Yates 3rd, and B.M. Emerson BRD7, a novel PBAF-specific SWI/SNF subunit, is required for target gene activation and repression in embryonic stem cells J. Biol. Chem. 283 2008 32254 32263
16. B.B. Kahn, and J.S. Flier Obesity and insulin resistance J. Clin. Invest. 106 2000 473 481
17. C.J. Kenyon The genetics of ageing Nature 464 2010 504 512
18. Y. Kitamura, and D. Accili New insights into the integrated physiology of insulin action Rev. Endocr. Metab. Disord. 5 2004 143 149
19. A.C. Könner, and J.C. Brüning Selective insulin and leptin resistance in metabolic disorders Cell Metab. 16 2012 144 152
20. K. Lee, W. Tirasophon, X. Shen, M. Michalak, R. Prywes, T. Okada, H. Yoshida, K. Mori, and R.J. Kaufman IRE1-mediated unconventional mRNA splicing and S2P-mediated ATF6 cleavage merge to regulate XBP1 in signaling the unfolded protein response Genes Dev. 16 2002 452 466
21. A.H. Lee, N.N. Iwakoshi, and L.H. Glimcher XBP-1 regulates a subset of endoplasmic reticulum resident chaperone genes in the unfolded protein response Mol. Cell. Biol. 23 2003 7448 7459
22. J. Lee, C. Sun, Y. Zhou, J. Lee, D. Gokalp, H. Herrema, S.W. Park, R.J. Davis, and U. Ozcan p38 MAPK-mediated regulation of Xbp1s is crucial for glucose homeostasis Nat. Med. 17 2011 1251 1260
23. J. Luo, S.J. Field, J.Y. Lee, J.A. Engelman, and L.C. Cantley The p85 regulatory subunit of phosphoinositide 3-kinase down-regulates IRS-1 signaling via the formation of a sequestration complex J. Cell Biol. 170 2005 455 464
24. F. Mantovani, J. Drost, P.M. Voorhoeve, G. Del Sal, and R. Agami Gene regulation and tumor suppression by the bromodomain-containing protein BRD7 Cell Cycle 9 2010 2777 2781
25. S.J. Marciniak, and D. Ron Endoplasmic reticulum stress signaling in disease Physiol. Rev. 86 2006 1133 1149
26. P.I. Merksamer, and F.R. Papa The UPR and cell fate at a glance J. Cell Sci. 123 2010 1003 1006
27. D.M. Muoio, and C.B. Newgard Obesity-related derangements in metabolic regulation Annu. Rev. Biochem. 75 2006 367 401
28. Y. Nakatani, H. Kaneto, D. Kawamori, K. Yoshiuchi, M. Hatazaki, T.A. Matsuoka, K. Ozawa, S. Ogawa, M. Hori, Y. Yamasaki, and M. Matsuhisa Involvement of endoplasmic reticulum stress in insulin resistance and diabetes J. Biol. Chem. 280 2005 847 851
29. K. Ozawa, M. Miyazaki, M. Matsuhisa, K. Takano, Y. Nakatani, M. Hatazaki, T. Tamatani, K. Yamagata, J. Miyagawa, and Y. Kitao et al. The endoplasmic reticulum chaperone improves insulin resistance in type 2 diabetes Diabetes 54 2005 657 663
30. U. Ozcan, Q. Cao, E. Yilmaz, A.H. Lee, N.N. Iwakoshi, E. Ozdelen, G. Tuncman, C. Görgün, L.H. Glimcher, and G.S. Hotamisligil Endoplasmic reticulum stress links obesity, insulin action, and type 2 diabetes Science 306 2004 457 461
31. U. Ozcan, E. Yilmaz, L. Ozcan, M. Furuhashi, E. Vaillancourt, R.O. Smith, C.Z. Görgün, and G.S. Hotamisligil Chemical chaperones reduce ER stress and restore glucose homeostasis in a mouse model of type 2 diabetes Science 313 2006 1137 1140
32. U. Ozcan, L. Ozcan, E. Yilmaz, K. Düvel, M. Sahin, B.D. Manning, and G.S. Hotamisligil Loss of the tuberous sclerosis complex tumor suppressors triggers the unfolded protein response to regulate insulin signaling and apoptosis Mol. Cell 29 2008 541 551
33. L. Ozcan, A.S. Ergin, A. Lu, J. Chung, S. Sarkar, D. Nie, M.G. Myers Jr., and U. Ozcan Endoplasmic reticulum stress plays a central role in development of leptin resistance Cell Metab. 9 2009 35 51
34. G.E. Palade The endoplasmic reticulum J. Biophys. Biochem. Cytol. 2 Suppl 1956 85 98
35. S.W. Park, and U. Ozcan Potential for therapeutic manipulation of the UPR in disease Semin. Immunopathol. 35 2013 351 373
36. S.W. Park, Y. Zhou, J. Lee, A. Lu, C. Sun, J. Chung, K. Ueki, and U. Ozcan The regulatory subunits of PI3K, p85alpha and p85beta, interact with XBP-1 and increase its nuclear translocation Nat. Med. 16 2010 429 437
37. S.W. Park, Y. Zhou, J. Lee, J. Lee, and U. Ozcan Sarco(endo)plasmic reticulum Ca2+-ATPase 2b is a major regulator of endoplasmic reticulum stress and glucose homeostasis in obesity Proc. Natl. Acad. Sci. USA 107 2010 19320 19325
38. C. Peng, J. Zhou, H.Y. Liu, M. Zhou, L.L. Wang, Q.H. Zhang, Y.X. Yang, W. Xiong, S.R. Shen, X.L. Li, and G.Y. Li The transcriptional regulation role of BRD7 by binding to acetylated histone through bromodomain J. Cell. Biochem. 97 2006 882 892
39. C. Peng, H.Y. Liu, M. Zhou, L.M. Zhang, X.L. Li, S.R. Shen, and G.Y. Li BRD7 suppresses the growth of Nasopharyngeal Carcinoma cells (HNE1) through negatively regulating beta-catenin and ERK pathways Mol. Cell. Biochem. 303 2007 141 149
40. M. Qatanani, and M.A. Lazar Mechanisms of obesity-associated insulin resistance: many choices on the menu Genes Dev. 21 2007 1443 1455
41. D. Ron, and P. Walter Signal integration in the endoplasmic reticulum unfolded protein response Nat. Rev. Mol. Cell Biol. 8 2007 519 529
42. S.J. Russell, and C.R. Kahn Endocrine regulation of ageing Nat. Rev. Mol. Cell Biol. 8 2007 681 691
43. M. Schröder, and R.J. Kaufman The mammalian unfolded protein response Annu. Rev. Biochem. 74 2005 739 789
44. B. Sun, and M. Karin Obesity, inflammation, and liver cancer J. Hepatol. 56 2012 704 713
45. A. Taguchi, L.M. Wartschow, and M.F. White Brain IRS2 signaling coordinates life span and nutrient homeostasis Science 317 2007 369 372
46. K. Ueki, D.A. Fruman, S.M. Brachmann, Y.H. Tseng, L.C. Cantley, and C.R. Kahn Molecular balance between the regulatory and catalytic subunits of phosphoinositide 3-kinase regulates cell signaling and survival Mol. Cell. Biol. 22 2002 965 977
47. K. Ueki, D.A. Fruman, C.M. Yballe, M. Fasshauer, J. Klein, T. Asano, L.C. Cantley, and C.R. Kahn Positive and negative roles of p85 alpha and p85 beta regulatory subunits of phosphoinositide 3-kinase in insulin signaling J. Biol. Chem. 278 2003 48453 48466
48. P. Walter, and D. Ron The unfolded protein response: from stress pathway to homeostatic regulation Science 334 2011 1081 1086
49. S. Wang, and R.J. Kaufman The impact of the unfolded protein response on human disease J. Cell Biol. 197 2012 857 867
50. J.N. Winnay, J. Boucher, M.A. Mori, K. Ueki, and C.R. Kahn A regulatory subunit of phosphoinositide 3-kinase increases the nuclear accumulation of X-box-binding protein-1 to modulate the unfolded protein response Nat. Med. 16 2010 438 445
51. J.N. Winnay, E. Dirice, C.W. Liew, R.N. Kulkarni, and C.R. Kahn p85α deficiency protects β-cells from endoplasmic reticulum stress-induced apoptosis Proc. Natl. Acad. Sci. USA 111 2014 1192 1197
52. H. Yoshida, T. Matsui, A. Yamamoto, T. Okada, and K. Mori XBP1 mRNA is induced by ATF6 and spliced by IRE1 in response to ER stress to produce a highly active transcription factor Cell 107 2001 881 891
53. K. Zhang, and R.J. Kaufman From endoplasmic-reticulum stress to the inflammatory response Nature 454 2008 455 462
54. J. Zhou, J. Ma, B.C. Zhang, X.L. Li, S.R. Shen, S.G. Zhu, W. Xiong, H.Y. Liu, H. Huang, M. Zhou, and G.Y. Li BRD7, a novel bromodomain gene, inhibits G1-S progression by transcriptionally regulating some important molecules involved in ras/MEK/ERK and Rb/E2F pathways J. Cell. Physiol. 200 2004 89 98
55. Y. Zhou, J. Lee, C.M. Reno, C. Sun, S.W. Park, J. Chung, J. Lee, S.J. Fisher, M.F. White, S.B. Biddinger, and U. Ozcan Regulation of glucose homeostasis through a XBP-1-FoxO1 interaction Nat. Med. 17 2011 356 365 10.1038/nm.2293