Regulation of steatohepatitis and PPARγ signaling by distinct AP-1 dimers

Cell Metabolism

Volumn 19, Issue 1, 2014, Pages 84-95

  Hasenfuss, Sebastian C ^a,b   Bakiri, Latifa ^a   Thomsen, Martin K ^a   Williams, Evan G ^c   Auwerx, Johan ^c   Wagner, Erwin F ^a  

^a BBVA University Institute for Economic and Social Analysis University of Alcalá   (Spain)

^b UNIVERSITY OF FREIBURG   (Germany)

^c EPFL   (Switzerland)

Author keywords

[No Author keywords available]

Indexed keywords

DIMER; PEROXISOME PROLIFERATOR ACTIVATED RECEPTOR GAMMA; PROTEIN C JUN; TRANSCRIPTION FACTOR AP 1; TRANSCRIPTION FACTOR FRA 1; TRANSCRIPTION FACTOR FRA 2; TRANSCRIPTION FACTOR JUND;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; GENE CONTROL; GENE EXPRESSION; GLUCOSE METABOLISM; HEMATOLOGICAL PARAMETERS; LIPID LIVER LEVEL; LIPID METABOLISM; LIVER CELL; LIVER INJURY; MOUSE; NONALCOHOLIC FATTY LIVER; NONHUMAN; OBESITY; ONCOGENE C FOS; PRIORITY JOURNAL; REGULATORY MECHANISM; STEATOSIS;

ADENOVIRIDAE; ANIMALS; CELL LINE, TUMOR; FATTY LIVER; GENE EXPRESSION REGULATION; HEPATOCYTES; HUMANS; LIPID METABOLISM; LIVER; MICE; PPAR GAMMA; PROTEIN MULTIMERIZATION; PROTO-ONCOGENE PROTEINS C-FOS; PROTO-ONCOGENE PROTEINS C-JUN; SIGNAL TRANSDUCTION; TRANSCRIPTION FACTOR AP-1;

EID: 84891877307     PISSN: 15504131     EISSN: 19327420     Source Type: Journal    
DOI: 10.1016/j.cmet.2013.11.018     Document Type: Article

References (60)

1. L. Bakiri, and E.F. Wagner Mouse models for liver cancer Mol. Oncol. 7 2013 206 223
2. L. Bakiri, K. Matsuo, M. Wisniewska, E.F. Wagner, and M. Yaniv Promoter specificity and biological activity of tethered AP-1 dimers Mol. Cell. Biol. 22 2002 4952 4964 (Pubitemid 34620427)
3. A. Behrens, M. Sibilia, J.P. David, U. Möhle-Steinlein, F. Tronche, G. Schütz, and E.F. Wagner Impaired postnatal hepatocyte proliferation and liver regeneration in mice lacking c-jun in the liver EMBO J. 21 2002 1782 1790 (Pubitemid 34614634)
4. W.J. Boyle, T. Smeal, L.H. Defize, P. Angel, J.R. Woodgett, M. Karin, and T. Hunter Activation of protein kinase C decreases phosphorylation of c-Jun at sites that negatively regulate its DNA-binding activity Cell 64 1991 573 584 (Pubitemid 121002973)
5. J.D. Browning, and J.D. Horton Molecular mediators of hepatic steatosis and liver injury J. Clin. Invest. 114 2004 147 152 (Pubitemid 39071617)
6. B.H. Chang, L. Li, A. Paul, S. Taniguchi, V. Nannegari, W.C. Heird, and L. Chan Protection against fatty liver but normal adipogenesis in mice lacking adipose differentiation-related protein Mol. Cell. Biol. 26 2006 1063 1076 (Pubitemid 43146498)
7. J.C. Cohen, J.D. Horton, and H.H. Hobbs Human fatty liver disease: old questions and new insights Science 332 2011 1519 1523
8. K.T. Dalen, K. Schoonjans, S.M. Ulven, M.S. Weedon-Fekjaer, T.G. Bentzen, H. Koutnikova, J. Auwerx, and H.I. Nebb Adipose tissue expression of the lipid droplet-associating proteins S3-12 and perilipin is controlled by peroxisome proliferator-activated receptor-gamma Diabetes 53 2004 1243 1252 (Pubitemid 38569010)
9. R. Eferl, and E.F. Wagner AP-1: a double-edged sword in tumorigenesis Nat. Rev. Cancer 3 2003 859 868 (Pubitemid 37383716)
10. R. Eferl, R. Ricci, L. Kenner, R. Zenz, J.P. David, M. Rath, and E.F. Wagner Liver tumor development. c-Jun antagonizes the proapoptotic activity of p53 Cell 112 2003 181 192 (Pubitemid 36144108)
11. R.V. Farese Jr., R. Zechner, C.B. Newgard, and T.C. Walther The problem of establishing relationships between hepatic steatosis and hepatic insulin resistance Cell Metab. 15 2012 570 573
12. D. Feng, T. Liu, Z. Sun, A. Bugge, S.E. Mullican, T. Alenghat, X.S. Liu, and M.A. Lazar A circadian rhythm orchestrated by histone deacetylase 3 controls hepatic lipid metabolism Science 331 2011 1315 1319
13. A. Fleischmann, F. Hafezi, C. Elliott, C.E. Remé, U. Rüther, and E.F. Wagner Fra-1 replaces c-Fos-dependent functions in mice Genes Dev. 14 2000 2695 2700 (Pubitemid 32531196)
14. M. Fuest, K. Willim, S. MacNelly, N. Fellner, G.P. Resch, H.E. Blum, and P. Hasselblatt The transcription factor c-Jun protects against sustained hepatic endoplasmic reticulum stress thereby promoting hepatocyte survival Hepatology 55 2012 408 418
15. T. Fujimoto, Y. Ohsaki, J. Cheng, M. Suzuki, and Y. Shinohara Lipid droplets: a classic organelle with new outfits Histochem. Cell Biol. 130 2008 263 279
16. S. Fujioka, J. Niu, C. Schmidt, G.M. Sclabas, B. Peng, T. Uwagawa, Z. Li, D.B. Evans, J.L. Abbruzzese, and P.J. Chiao NF-kappaB and AP-1 connection: mechanism of NF-kappaB-dependent regulation of AP-1 activity Mol. Cell. Biol. 24 2004 7806 7819 (Pubitemid 39121503)
17. O. Gavrilova, M. Haluzik, K. Matsusue, J.J. Cutson, L. Johnson, K.R. Dietz, C.J. Nicol, C. Vinson, F.J. Gonzalez, and M.L. Reitman Liver peroxisome proliferator-activated receptor gamma contributes to hepatic steatosis, triglyceride clearance, and regulation of body fat mass J. Biol. Chem. 278 2003 34268 34276 (Pubitemid 37553270)
18. C.K. Glass, and K. Saijo Nuclear receptor transrepression pathways that regulate inflammation in macrophages and T cells Nat. Rev. Immunol. 10 2010 365 376
19. T.D. Halazonetis, K. Georgopoulos, M.E. Greenberg, and P. Leder c-Jun dimerizes with itself and with c-Fos, forming complexes of different DNA binding affinities Cell 55 1988 917 924
20. S.C. Hasenfuss, L. Bakiri, M.K. Thomsen, R. Hamacher, and E.F. Wagner Activator protein 1 transcription factor fos-related antigen 1 (fra-1) is dispensable for murine liver fibrosis, but modulates xenobiotic metabolism Hepatology 59 2014 261 273
21. P. Hasselblatt, M. Rath, V. Komnenovic, K. Zatloukal, and E.F. Wagner Hepatocyte survival in acute hepatitis is due to c-Jun/AP-1-dependent expression of inducible nitric oxide synthase Proc. Natl. Acad. Sci. USA 104 2007 17105 17110 (Pubitemid 350210999)
22. J. Hess, P. Angel, and M. Schorpp-Kistner AP-1 subunits: quarrel and harmony among siblings J. Cell Sci. 117 2004 5965 5973 (Pubitemid 40123963)
23. M. Hibi, A. Lin, T. Smeal, A. Minden, and M. Karin Identification of an oncoprotein- and UV-responsive protein kinase that binds and potentiates the c-Jun activation domain Genes Dev. 7 1993 2135 2148 (Pubitemid 23336140)
24. W. Huang, B.T. Sherman, and R.A. Lempicki Systematic and integrative analysis of large gene lists using DAVID bioinformatics resources Nat. Protoc. 4 2009 44 57
25. R.A. Irizarry, B. Hobbs, F. Collin, Y.D. Beazer-Barclay, K.J. Antonellis, U. Scherf, and T.P. Speed Exploration, normalization, and summaries of high density oligonucleotide array probe level data Biostatistics 4 2003 249 264
26. M. Kanehisa, S. Goto, Y. Sato, M. Furumichi, and M. Tanabe KEGG for integration and interpretation of large-scale molecular data sets Nucleic Acids Res. 40 Database issue 2012 D109 D114
27. S.J. Kim, and C.R. Kahn Insulin stimulates phosphorylation of c-Jun, c-Fos, and Fos-related proteins in cultured adipocytes J. Biol. Chem. 269 1994 11887 11892 (Pubitemid 24196677)
28. H.I. Kim, Y.K. Koh, T.H. Kim, S.K. Kwon, S.S. Im, H.S. Choi, K.S. Kim, and Y.H. Ahn Transcriptional activation of SHP by PPAR-gamma in liver Biochem. Biophys. Res. Commun. 360 2007 301 306
29. S.C. Kim, C. Kim, D. Axe, A. Cook, M. Lee, T. Li, N. Smallwood, J.Y. Chiang, J.P. Hardwick, D.D. Moore, and Y.K. Lee All-trans-retinoic acid ameliorates hepatic steatosis in mice via a novel transcriptional cascade Hepatology 2013 10.1002/hep.26699 Published online August 26, 2013
30. S.K. Knutson, B.J. Chyla, J.M. Amann, S. Bhaskara, S.S. Huppert, and S.W. Hiebert Liver-specific deletion of histone deacetylase 3 disrupts metabolic transcriptional networks EMBO J. 27 2008 1017 1028 (Pubitemid 351508160)
31. C. Lara-Castro, and W.T. Garvey Intracellular lipid accumulation in liver and muscle and the insulin resistance syndrome Endocrinol. Metab. Clin. North Am. 37 2008 841 856
32. M. Lazo, and J.M. Clark The epidemiology of nonalcoholic fatty liver disease: a global perspective Semin. Liver Dis. 28 2008 339 350
33. Y.J. Lee, E.H. Ko, J.E. Kim, E. Kim, H. Lee, H. Choi, J.H. Yu, H.J. Kim, J.K. Seong, K.S. Kim, and J.W. Kim Nuclear receptor PPARγ-regulated monoacylglycerol O-acyltransferase 1 (MGAT1) expression is responsible for the lipid accumulation in diet-induced hepatic steatosis Proc. Natl. Acad. Sci. USA 109 2012 13656 13661
34. K. Machida, H. Tsukamoto, J.C. Liu, Y.P. Han, S. Govindarajan, M.M. Lai, S. Akira, and J.H. Ou c-Jun mediates hepatitis C virus hepatocarcinogenesis through signal transducer and activator of transcription 3 and nitric oxide-dependent impairment of oxidative DNA repair Hepatology 52 2010 480 492
35. K. Matsuo, J.M. Owens, M. Tonko, C. Elliott, T.J. Chambers, and E.F. Wagner Fosl1 is a transcriptional target of c-Fos during osteoclast differentiation Nat. Genet. 24 2000 184 187 (Pubitemid 30094722)
36. K. Matsusue, M. Haluzik, G. Lambert, S.H. Yim, O. Gavrilova, J.M. Ward, B. Brewer Jr., M.L. Reitman, and F.J. Gonzalez Liver-specific disruption of PPARgamma in leptin-deficient mice improves fatty liver but aggravates diabetic phenotypes J. Clin. Invest. 111 2003 737 747 (Pubitemid 36278592)
37. K. Matsusue, T. Kusakabe, T. Noguchi, S. Takiguchi, T. Suzuki, S. Yamano, and F.J. Gonzalez Hepatic steatosis in leptin-deficient mice is promoted by the PPARgamma target gene Fsp27 Cell Metab. 7 2008 302 311 (Pubitemid 351455219)
38. G. Medina-Gomez, S.L. Gray, L. Yetukuri, K. Shimomura, S. Virtue, M. Campbell, R.K. Curtis, M. Jimenez-Linan, M. Blount, and G.S. Yeo et al. PPAR gamma 2 prevents lipotoxicity by controlling adipose tissue expandability and peripheral lipid metabolism PLoS Genet. 3 2007 e64
39. A. Mehlem, C.E. Hagberg, L. Muhl, U. Eriksson, and A. Falkevall Imaging of neutral lipids by oil red O for analyzing the metabolic status in health and disease Nat. Protoc. 8 2013 1149 1154
40. L. Min, Y. Ji, L. Bakiri, Z. Qiu, J. Cen, X. Chen, L. Chen, H. Scheuch, H. Zheng, and L. Qin et al. Liver cancer initiation is controlled by AP-1 through SIRT6-dependent inhibition of survivin Nat. Cell Biol. 14 2012 1203 1211
41. E. Morán-Salvador, M. López-Parra, V. García-Alonso, E. Titos, M. Martínez-Clemente, A. González-Périz, C. López-Vicario, Y. Barak, V. Arroyo, and J. Clària Role for PPARγ in obesity-induced hepatic steatosis as determined by hepatocyte- and macrophage-specific conditional knockouts FASEB J. 25 2011 2538 2550
42. E.P. Newberry, Y. Xie, S. Kennedy, X. Han, K.K. Buhman, J. Luo, R.W. Gross, and N.O. Davidson Decreased hepatic triglyceride accumulation and altered fatty acid uptake in mice with deletion of the liver fatty acid-binding protein gene J. Biol. Chem. 278 2003 51664 51672 (Pubitemid 38020412)
43. E.P. Newberry, Y. Xie, S.M. Kennedy, J. Luo, and N.O. Davidson Protection against Western diet-induced obesity and hepatic steatosis in liver fatty acid-binding protein knockout mice Hepatology 44 2006 1191 1205 (Pubitemid 44748370)
44. J.L. Peirce, L. Lu, J. Gu, L.M. Silver, and R.W. Williams A new set of BXD recombinant inbred lines from advanced intercross populations in mice BMC Genet. 5 2004 7
45. V. Puri, S. Ranjit, S. Konda, S.M. Nicoloro, J. Straubhaar, A. Chawla, M. Chouinard, C. Lin, A. Burkart, and S. Corvera et al. Cidea is associated with lipid droplets and insulin sensitivity in humans Proc. Natl. Acad. Sci. USA 105 2008 7833 7838 (Pubitemid 351872724)
46. A. Purushotham, T.T. Schug, Q. Xu, S. Surapureddi, X. Guo, and X. Li Hepatocyte-specific deletion of SIRT1 alters fatty acid metabolism and results in hepatic steatosis and inflammation Cell Metab. 9 2009 327 338
47. M. Ricote, and C.K. Glass PPARs and molecular mechanisms of transrepression Biochim. Biophys. Acta 1771 2007 926 935 (Pubitemid 47198544)
48. R. Saladin, L. Fajas, S. Dana, Y.D. Halvorsen, J. Auwerx, and M. Briggs Differential regulation of peroxisome proliferator activated receptor gamma1 (PPARgamma1) and PPARgamma2 messenger RNA expression in the early stages of adipogenesis Cell Growth Differ. 10 1999 43 48 (Pubitemid 29086918)
49. J.K. Sethi, and A.J. Vidal-Puig Thematic review series: adipocyte biology. Adipose tissue function and plasticity orchestrate nutritional adaptation J. Lipid Res. 48 2007 1253 1262 (Pubitemid 47312027)
50. E. Shaulian, and M. Karin AP-1 as a regulator of cell life and death Nat. Cell Biol. 4 2002 E131 E136
51. A. Smedile, and E. Bugianesi Steatosis and hepatocellular carcinoma risk Eur. Rev. Med. Pharmacol. Sci. 9 2005 291 293 (Pubitemid 41387394)
52. Z. Sun, R.A. Miller, R.T. Patel, J. Chen, R. Dhir, H. Wang, D. Zhang, M.J. Graham, T.G. Unterman, and G.I. Shulman et al. Hepatic Hdac3 promotes gluconeogenesis by repressing lipid synthesis and sequestration Nat. Med. 18 2012 934 942
53. D. Thépot, J.B. Weitzman, J. Barra, D. Segretain, M.G. Stinnakre, C. Babinet, and M. Yaniv Targeted disruption of the murine junD gene results in multiple defects in male reproductive function Development 127 2000 143 153 (Pubitemid 30064396)
54. P. Tontonoz, and B.M. Spiegelman Fat and beyond: the diverse biology of PPARgamma Annu. Rev. Biochem. 77 2008 289 312
55. G.M. Varela, D.A. Antwi, R. Dhir, X. Yin, N.S. Singhal, M.J. Graham, R.M. Crooke, and R.S. Ahima Inhibition of ADRP prevents diet-induced insulin resistance Am. J. Physiol. Gastrointest. Liver Physiol. 295 2008 G621 G628
56. P. Verde, L. Casalino, F. Talotta, M. Yaniv, and J.B. Weitzman Deciphering AP-1 function in tumorigenesis: fra-ternizing on target promoters Cell Cycle 6 2007 2633 2639 (Pubitemid 350224046)
57. E.F. Wagner, and A.R. Nebreda Signal integration by JNK and p38 MAPK pathways in cancer development Nat. Rev. Cancer 9 2009 537 549
58. E.F. Wagner, H.B. Schonthaler, J. Guinea-Viniegra, and E. Tschachler Psoriasis: what we have learned from mouse models Nat. Rev. Rheumatol. 6 2010 704 714
59. Y. Wan, L.W. Chong, and R.M. Evans PPAR-gamma regulates osteoclastogenesis in mice Nat. Med. 13 2007 1496 1503
60. L. Zhou, L. Xu, J. Ye, D. Li, W. Wang, X. Li, L. Wu, H. Wang, F. Guan, and P. Li Cidea promotes hepatic steatosis by sensing dietary fatty acids Hepatology 56 2012 95 107