IRE1α-XBP1s induces PDI expression to increase MTP activity for hepatic VLDL assembly and lipid homeostasis

Cell Metabolism

Volumn 16, Issue 4, 2012, Pages 473-486

  Wang, Shiyu ^a,b   Chen, Zhouji ^d   Lam, Vivian ^c   Han, Jaeseok ^a,b   Hassler, Justin ^a,b   Finck, Brian N ^d   Davidson, Nicholas O ^d   Kaufman, Randal J ^a,b,c  

^a BURNHAM INSTITUTE   (United States)

^b UNIVERSITY OF MICHIGAN HEALTH SYSTEM   (United States)

^c UNIVERSITY OF MICHIGAN MEDICAL SCHOOL   (United States)

^d WASHINGTON UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

APOLIPOPROTEIN B; INOSITOL REQUIRING TRANSMEMBRANE KINASE; MEMBRANE PROTEIN; MICROSOMAL TRIGLYCERIDE TRANSFER PROTEIN; PROTEIN DISULFIDE ISOMERASE; TRIACYLGLYCEROL; UNCLASSIFIED DRUG; VERY LOW DENSITY LIPOPROTEIN; X BOX BINDING PROTEIN 1;

ANIMAL EXPERIMENT; ARTICLE; DISORDERS OF LIPID METABOLISM; ENDOPLASMIC RETICULUM; ENZYME ACTIVITY; ENZYME SYNTHESIS; FATTY LIVER; GENE DELETION; GENE OVEREXPRESSION; HYPOLIPEMIA; LIPOGENESIS; LIVER CELL; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN HOMEOSTASIS; UNFOLDED PROTEIN RESPONSE;

ANIMALS; CARRIER PROTEINS; DNA-BINDING PROTEINS; ENDORIBONUCLEASES; HEPATOCYTES; LIPID METABOLISM; LIPOPROTEINS, VLDL; MICE; MICE, KNOCKOUT; PROTEIN DISULFIDE-ISOMERASES; PROTEIN-SERINE-THREONINE KINASES; TRANSCRIPTION FACTORS; TRIGLYCERIDES; UNFOLDED PROTEIN RESPONSE;

EID: 84867063735     PISSN: 15504131     EISSN: 19327420     Source Type: Journal    
DOI: 10.1016/j.cmet.2012.09.003     Document Type: Article

References (40)

1. M. Adiels, S.O. Olofsson, M.R. Taskinen, and J. Borén Overproduction of very low-density lipoproteins is the hallmark of the dyslipidemia in the metabolic syndrome Arterioscler. Thromb. Vasc. Biol. 28 2008 1225 1236
2. V. Bamba, and D.J. Rader Obesity and atherogenic dyslipidemia Gastroenterology 132 2007 2181 2190
3. P. Bradbury, C.J. Mann, S. Köchl, T.A. Anderson, S.A. Chester, J.M. Hancock, P.J. Ritchie, J. Amey, G.B. Harrison, and D.G. Levitt A common binding site on the microsomal triglyceride transfer protein for apolipoprotein B and protein disulfide isomerase J. Biol. Chem. 274 1999 3159 3164
4. S. Calandra, P. Tarugi, H.E. Speedy, A.F. Dean, S. Bertolini, and C.C. Shoulders Mechanisms and genetic determinants regulating sterol absorption, circulating LDL levels, and sterol elimination: implications for classification and disease risk J. Lipid Res. 52 2011 1885 1926
5. Z. Chen, E.P. Newberry, J.Y. Norris, Y. Xie, J. Luo, S.M. Kennedy, and N.O. Davidson ApoB100 is required for increased VLDL-triglyceride secretion by microsomal triglyceride transfer protein in ob/ob mice J. Lipid Res. 49 2008 2013 2022
6. Z. Chen, J.Y. Norris, and B.N. Finck Peroxisome proliferator-activated receptor-gamma coactivator-1alpha (PGC-1alpha) stimulates VLDL assembly through activation of cell death-inducing DFFA-like effector B (CideB) J. Biol. Chem. 285 2010 25996 26004
7. M. Flamment, H.L. Kammoun, I. Hainault, P. Ferré, and F. Foufelle Endoplasmic reticulum stress: a new actor in the development of hepatic steatosis Curr. Opin. Lipidol. 21 2010 239 246
8. H. Fukuda, N. Iritani, and T. Tanaka Effects of high-fructose diet on lipogenic enzymes and their substrate and effector levels in diabetic rats J. Nutr. Sci. Vitaminol. (Tokyo) 29 1983 691 699
9. M.M. Galteau, B. Antoine, and H. Reggio Epoxide hydrolase is a marker for the smooth endoplasmic reticulum in rat liver EMBO J. 4 1985 2793 2800
10. A. Gilchrist, C.E. Au, J. Hiding, A.W. Bell, J. Fernandez-Rodriguez, S. Lesimple, H. Nagaya, L. Roy, S.J. Gosline, and M. Hallett Quantitative proteomics analysis of the secretory pathway Cell 127 2006 1265 1281
11. S. Grubb, L. Guo, E.A. Fisher, and J.L. Brodsky Protein disulfide isomerases contribute differentially to the endoplasmic reticulum-associated degradation of apolipoprotein B and other substrates Mol. Biol. Cell 23 2012 520 532
12. C. Hetz The unfolded protein response: controlling cell fate decisions under ER stress and beyond Nat. Rev. Mol. Cell Biol. 13 2012 89 102
13. K. Hirano, S.G. Young, R.V. Farese Jr., J. Ng, E. Sande, C. Warburton, L.M. Powell-Braxton, and N.O. Davidson Targeted disruption of the mouse apobec-1 gene abolishes apolipoprotein B mRNA editing and eliminates apolipoprotein B48 J. Biol. Chem. 271 1996 9887 9890
14. W. Huang, A. Metlakunta, N. Dedousis, P. Zhang, I. Sipula, J.J. Dube, D.K. Scott, and R.M. O'Doherty Depletion of liver Kupffer cells prevents the development of diet-induced hepatic steatosis and insulin resistance Diabetes 59 2010 347 357
15. M.M. Hussain, J. Shi, and P. Dreizen Microsomal triglyceride transfer protein and its role in apoB-lipoprotein assembly J. Lipid Res. 44 2003 22 32
16. J. Iqbal, K. Dai, T. Seimon, R. Jungreis, M. Oyadomari, G. Kuriakose, D. Ron, I. Tabas, and M.M. Hussain IRE1beta inhibits chylomicron production by selectively degrading MTP mRNA Cell Metab. 7 2008 445 455
17. H.L. Kammoun, H. Chabanon, I. Hainault, S. Luquet, C. Magnan, T. Koike, P. Ferré, and F. Foufelle GRP78 expression inhibits insulin and ER stress-induced SREBP-1c activation and reduces hepatic steatosis in mice J. Clin. Invest. 119 2009 1201 1215
18. R. Kühn, F. Schwenk, M. Aguet, and K. Rajewsky Inducible gene targeting in mice Science 269 1995 1427 1429
19. A. Kulinski, S. Rustaeus, and J.E. Vance Microsomal triacylglycerol transfer protein is required for lumenal accretion of triacylglycerol not associated with ApoB, as well as for ApoB lipidation J. Biol. Chem. 277 2002 31516 31525
20. D.L. Lankester, A.M. Brown, and V.A. Zammit Use of cytosolic triacylglycerol hydrolysis products and of exogenous fatty acid for the synthesis of triacylglycerol secreted by cultured rat hepatocytes J. Lipid Res. 39 1998 1889 1895
21. 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
22. A.H. Lee, E.F. Scapa, D.E. Cohen, and L.H. Glimcher Regulation of hepatic lipogenesis by the transcription factor XBP1 Science 320 2008 1492 1496
23. J.H. Lee, P. Giannikopoulos, S.A. Duncan, J. Wang, C.T. Johansen, J.D. Brown, J. Plutzky, R.A. Hegele, L.H. Glimcher, and A.H. Lee The transcription factor cyclic AMP-responsive element-binding protein H regulates triglyceride metabolism Nat. Med. 17 2011 812 815
24. K.L. Lipson, S.G. Fonseca, S. Ishigaki, L.X. Nguyen, E. Foss, R. Bortell, A.A. Rossini, and F. Urano Regulation of insulin biosynthesis in pancreatic beta cells by an endoplasmic reticulum-resident protein kinase IRE1 Cell Metab. 4 2006 245 254
25. T. Ota, C. Gayet, and H.N. Ginsberg Inhibition of apolipoprotein B100 secretion by lipid-induced hepatic endoplasmic reticulum stress in rodents J. Clin. Invest. 118 2008 316 332
26. X. Pan, Y. Zhang, L. Wang, and M.M. Hussain Diurnal regulation of MTP and plasma triglyceride by CLOCK is mediated by SHP Cell Metab. 12 2010 174 186
27. 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
28. W. Qiu, R.K. Avramoglu, A.C. Rutledge, J. Tsai, and K. Adeli Mechanisms of glucosamine-induced suppression of the hepatic assembly and secretion of apolipoprotein B-100-containing lipoproteins J. Lipid Res. 47 2006 1749 1761
29. H. Quan, G. Fan, and C.C. Wang Independence of the chaperone activity of protein disulfide isomerase from its thioredoxin-like active site J. Biol. Chem. 270 1995 17078 17080
30. M. Raabe, M.M. Véniant, M.A. Sullivan, C.H. Zlot, J. Björkegren, L.B. Nielsen, J.S. Wong, R.L. Hamilton, and S.G. Young Analysis of the role of microsomal triglyceride transfer protein in the liver of tissue-specific knockout mice J. Clin. Invest. 103 1999 1287 1298
31. A. Rusiñol, H. Verkade, and J.E. Vance Assembly of rat hepatic very low density lipoproteins in the endoplasmic reticulum J. Biol. Chem. 268 1993 3555 3562
32. S. Rustaeus, P. Stillemark, K. Lindberg, D. Gordon, and S.O. Olofsson The microsomal triglyceride transfer protein catalyzes the post-translational assembly of apolipoprotein B-100 very low density lipoprotein in McA-RH7777 cells J. Biol. Chem. 273 1998 5196 5203
33. D.T. Rutkowski, J. Wu, S.H. Back, M.U. Callaghan, S.P. Ferris, J. Iqbal, R. Clark, H. Miao, J.R. Hassler, and J. Fornek UPR pathways combine to prevent hepatic steatosis caused by ER stress-mediated suppression of transcriptional master regulators Dev. Cell 15 2008 829 840
34. M. Sundaram, and Z. Yao Recent progress in understanding protein and lipid factors affecting hepatic VLDL assembly and secretion Nutr. Metab. (Lond) 7 2010 35
35. J.R. Wetterau, K.A. Combs, L.R. McLean, S.N. Spinner, and L.P. Aggerbeck Protein disulfide isomerase appears necessary to maintain the catalytically active structure of the microsomal triglyceride transfer protein Biochemistry 30 1991 9728 9735
36. L.Y. Yang, A. Kuksis, J.J. Myher, and G. Steiner Origin of triacylglycerol moiety of plasma very low density lipoproteins in the rat: structural studies J. Lipid Res. 36 1995 125 136
37. K. Zhang, and R.J. Kaufman From endoplasmic-reticulum stress to the inflammatory response Nature 454 2008 455 462
38. K. Zhang, X. Shen, J. Wu, K. Sakaki, T. Saunders, D.T. Rutkowski, S.H. Back, and R.J. Kaufman Endoplasmic reticulum stress activates cleavage of CREBH to induce a systemic inflammatory response Cell 124 2006 587 599
39. K. Zhang, S. Wang, J. Malhotra, J.R. Hassler, S.H. Back, G. Wang, L. Chang, W. Xu, H. Miao, and R. Leonardi The unfolded protein response transducer IRE1α prevents ER stress-induced hepatic steatosis EMBO J. 30 2011 1357 1375
40. C. Zhang, G. Wang, Z. Zheng, K.R. Maddipati, X. Zhang, G. Dyson, P. Williams, S.A. Duncan, R.J. Kaufman, and K. Zhang 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 2012 1070 1082