Endoplasmic reticulum stress does not contribute to steatohepatitis in obese and insulin-resistant high-fat-diet-fed foz/foz mice

Clinical Science

Volumn 127, Issue 7, 2014, Pages 507-518

  Legry, Vanessa ^a   Van Rooyen, Derrick M ^b   Lambert, Barbara ^a   Sempoux, Christine ^c   Poekes, Laurence ^a   Español suñer, Regina ^a   Molendi Coste, Olivier ^a   Horsmans, Yves ^a   Farrell, Geoffrey C ^b   Leclercq, Isabelle A ^a  

^a UNIVERSITÉ CATHOLIQUE DE LOUVAIN   (Belgium)

^b The Australian National University   (Australia)

^c CLINIQUES UNIVERSITAIRES SAINT LUC   (Belgium)

Author keywords

Apoptosis; Endoplasmic reticulum stress; Inflammation; Insulin resistance; Non alcoholic fatty liver disease

Indexed keywords

ACTIVATING TRANSCRIPTION FACTOR 4; ALANINE AMINOTRANSFERASE; C PEPTIDE; GLUCOSE; GROWTH ARREST AND DNA DAMAGE INDUCIBLE PROTEIN 153; INITIATION FACTOR 2ALPHA; INOSITOL REQUIRING ENZYME 1ALPHA; INSULIN; PROTEIN IRE1; STRESS ACTIVATED PROTEIN KINASE; TAUROURSODEOXYCHOLIC ACID; TUNICAMYCIN; UNCLASSIFIED DRUG; X BOX BINDING PROTEIN 1;

ALANINE AMINOTRANSFERASE BLOOD LEVEL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; APOPTOSIS; ARTICLE; BODY WEIGHT; CALORIC INTAKE; CONTROLLED STUDY; DIET RESTRICTION; ENDOPLASMIC RETICULUM STRESS; ENZYME ACTIVATION; ENZYME ACTIVITY; EPIDIDYMIS FAT; EVALUATION STUDY; FATTY LIVER; FEMALE; GENETIC TRANSCRIPTION; GLUCOSE BLOOD LEVEL; GLUCOSE INTOLERANCE; GLUCOSE TOLERANCE; HEPATITIS; INSULIN BLOOD LEVEL; INSULIN RESISTANCE; LIPID DIET; LIPID LIVER LEVEL; LIVER CELL; LIVER INJURY; LIVER WEIGHT; MALE; MOUSE; NONALCOHOLIC FATTY LIVER; NONHUMAN; OBESITY; PHENOTYPE; PRIORITY JOURNAL; PROTEIN BLOOD LEVEL; UNFOLDED PROTEIN RESPONSE; UPREGULATION;

ANIMALS; BLOOD GLUCOSE; DIET, HIGH-FAT; DNA-BINDING PROTEINS; ENDOPLASMIC RETICULUM STRESS; FATTY LIVER; FEMALE; INSULIN RESISTANCE; MALE; MICE; MICE, INBRED NOD; MICE, OBESE; PHENOTYPE;

EID: 84904012910     PISSN: 01435221     EISSN: None     Source Type: Journal    
DOI: 10.1042/CS20140026     Document Type: Article

References (39)

1. Leclercq, I. A. (2013) Emerging concepts on the pathogenesis on non-alcoholic steatohepatitis (NASH). In Non-Alcoholic Fatty Liver Disease: a Practical Guide (Farrell, G. C., McCullough, A. J. and Day, C. P., eds), Wiley-Blackwell, Oxford, U.K.
2. Tilg, H. and Moschen, A. R. (2010) Evolution of inflammation in nonalcoholic fatty liver disease: the multiple parallel hits hypothesis. Hepatology 52, 1836-1846
3. Ron, D. and Walter, P. (2007) Signal integration in the endoplasmic reticulum unfolded protein response. Nat. Rev. Mol. Cell Biol. 8, 519-529
4. Hendershot, L. M. (2004) The ER function BiP is a master regulator of ER function. Mt. Sinai J. Med. 71, 289-297
5. Dara, L., Ji, C. and Kaplowitz, N. (2011) The contribution of endoplasmic reticulum stress to liver diseases. Hepatology 53, 1752-1763
6. Scheuner, D., Song, B., McEwen, E., Liu, C., Laybutt, R., Gillespie, P., Saunders, T., Bonner-Weir, S. and Kaufman, R. J. (2001) Translational control is required for the unfolded protein response and in vivo glucose homeostasis. Mol. Cell 7, 1165-1176
7. Kammoun, H. L., Chabanon, H., Hainault, I., Luquet, S., Magnan, C., Koike, T., Ferre, P. and Foufelle, F. (2009) GRP78 expression inhibits insulin and ER stress-induced SREBP-1c activation and reduces hepatic steatosis in mice. J. Clin. Invest. 119, 1201-1215
8. Ozcan, U., Cao, Q., Yilmaz, E., Lee, A. H., Iwakoshi, N. N., Ozdelen, E., Tuncman, G., Gorgun, C., Glimcher, L. H. and Hotamisligil, G. S. (2004) Endoplasmic reticulum stress links obesity, insulin action, and type 2 diabetes. Science 306, 457-461
9. Yang, J. S., Kim, J. T., Jeon, J., Park, H. S., Kang, G. H., Park, K. S., Lee, H. K., Kim, S. and Cho, Y. M. (2010) Changes in hepatic gene expression upon oral administration of taurine-conjugated ursodeoxycholic acid in ob/ob mice. PLoS ONE 5, e13858
10. Puri, P., Mirshahi, F., Cheung, O., Natarajan, R., Maher, J. W., Kellum, J. M. and Sanyal, A. J. (2008) Activation and dysregulation of the unfolded protein response in nonalcoholic fatty liver disease. Gastroenterology 134, 568-576
11. Gregor, M. F., Yang, L., Fabbrini, E., Mohammed, B. S., Eagon, J. C., Hotamisligil, G. S. and Klein, S. (2009) Endoplasmic reticulum stress is reduced in tissues of obese subjects after weight loss. Diabetes 58, 693-700
12. Kumashiro, N., Erion, D. M., Zhang, D., Kahn, M., Beddow, S. A., Chu, X., Still, C. D., Gerhard, G. S., Han, X., Dziura, J. et al. (2011) Cellular mechanism of insulin resistance in nonalcoholic fatty liver disease. Proc. Natl. Acad. Sci. U.S.A. 108, 16381-16385
13. Heydet, D., Chen, L. X., Larter, C. Z., Inglis, C., Silverman, M. A., Farrell, G. C. and Leroux, M. R. (2013) A truncating mutation of Alms1 reduces the number of hypothalamic neuronal cilia in obese mice. Dev. Neurobiol. 73, 1-13
14. Arsov, T., Silva, D. G., O'Bryan, M. K., Sainsbury, A., Lee, N. J., Kennedy, C., Manji, S. S., Nelms, K., Liu, C., Vinuesa, C. G. et al. (2006) Fat aussie - a new Alstrom syndrome mouse showing a critical role for ALMS1 in obesity, diabetes, and spermatogenesis. Mol. Endocrinol. 20, 1610-1622
15. Arsov, T., Larter, C. Z., Nolan, C. J., Petrovsky, N., Goodnow, C. C., Teoh, N. C., Yeh, M. M. and Farrell, G. C. (2006) Adaptive failure to high-fat diet characterizes steatohepatitis in Alms1 mutant mice. Biochem. Biophys. Res. Commun. 342, 1152-1159
16. Schaap, F. G., Kremer, A. E., Lamers, W. H., Jansen, P. L. and Gaemers, I. C. (2013) Fibroblast growth factor 21 is induced by endoplasmic reticulum stress. Biochimie 95, 692-699
17. Liang, B., Wang, S., Wang, Q., Zhang, W., Viollet, B., Zhu, Y. and Zou, M. H. (2013) Aberrant endoplasmic reticulum stress in vascular smooth muscle increases vascular contractility and blood pressure in mice deficient of AMP-activated protein kinase-alpha2 in vivo. Arterioscler. Thromb. Vasc. Biol. 33, 595-604
18. Lanthier, N., Molendi-Coste, O., Cani, P. D., van, R. N., Horsmans, Y. and Leclercq, I. A. (2011) Kupffer cell depletion prevents but has no therapeutic effect on metabolic and inflammatory changes induced by a high-fat diet. FASEB J. 25, 4301-4311
19. Larter, C. Z., Yeh, M. M., Van Rooyen, D. M., Teoh, N. C., Brooling, J., Hou, J. Y., Williams, J., Clyne, M., Nolan, C. J. and Farrell, G. C. (2009) Roles of adipose restriction and metabolic factors in progression of steatosis to steatohepatitis in obese, diabetic mice. J. Gastroenterol. Hepatol. 24, 1658-1668
20. Larter, C. Z., Yeh, M. M., Haigh, W. G., Van Rooyen, D. M., Brooling, J., Heydet, D., Nolan, C. J., Teoh, N. C. and Farrell, G. C. (2013) Dietary modification dampens liver inflammation and fibrosis in obesity-related fatty liver disease. Obesity (Silver Spring) 21, 1189-1199
21. Van Rooyen, D. M., Gan, L. T., Yeh, M. M., Haigh, W. G., Larter, C. Z., Ioannou, G., Teoh, N. C. and Farrell, G. C. (2013) Pharmacological cholesterol lowering reverses fibrotic NASH in obese, diabetic mice with metabolic syndrome. J. Hepatol. 59, 144-152
22. Ozcan, U., Yilmaz, E., Ozcan, L., Furuhashi, M., Vaillancourt, E., Smith, R. O., Gorgun, C. Z. and Hotamisligil, G. S. (2006) Chemical chaperones reduce ER stress and restore glucose homeostasis in a mouse model of type 2 diabetes. Science 313, 1137-1140
23. Lloyd, D. J., Wheeler, M. C. and Gekakis, N. (2010) A point mutation in Sec61alpha1 leads to diabetes and hepatosteatosis in mice. Diabetes 59, 460-470
24. Donnelly, K. L., Smith, C. I., Schwarzenberg, S. J., Jessurun, J., Boldt, M. D. and Parks, E. J. (2005) Sources of fatty acids stored in liver and secreted via lipoproteins in patients with nonalcoholic fatty liver disease. J. Clin. Invest. 115, 1343-1351
25. Nakayama, Y., Endo, M., Tsukano, H., Mori, M., Oike, Y. and Gotoh, T. (2010) Molecular mechanisms of the LPS-induced non-apoptotic ER stress-CHOP pathway. J. Biochem. 147, 471-483
26. Oyadomari, S. and Mori, M. (2004) Roles of CHOP/GADD153 in endoplasmic reticulum stress. Cell Death Differ. 11, 381-389
27. Fornace, Jr, A. J., Nebert, D. W., Hollander, M. C., Luethy, J. D., Papathanasiou, M., Fargnoli, J. and Holbrook, N. J. (1989) Mammalian genes coordinately regulated by growth arrest signals and DNA-damaging agents. Mol. Cell Biol. 9, 4196-4203
28. Schmitt-Ney, M. and Habener, J. F. (2000) CHOP/GADD153 gene expression response to cellular stresses inhibited by prior exposure to ultraviolet light wavelength band C (UVC). Inhibitory sequence mediating the UVC response localized to exon 1. J. Biol. Chem. 275, 40839-40845
29. Urano, F., Wang, X., Bertolotti, A., Zhang, Y., Chung, P., Harding, H. P. and Ron, D. (2000) Coupling of stress in the ER to activation of JNK protein kinases by transmembrane protein kinase IRE1. Science 287, 664-666
30. Sharma, M., Urano, F. and Jaeschke, A. (2012) Cdc42 and Rac1 are major contributors to the saturated fatty acid-stimulated JNK pathway in hepatocytes. J. Hepatol. 56, 192-198
31. Malhi, H., Bronk, S. F., Werneburg, N. W. and Gores, G. J. (2006) Free fatty acids induce JNK-dependent hepatocyte lipoapoptosis. J. Biol. Chem. 281, 12093-12101
32. Loria, P., Bozzoli, M., Concari, M., Guicciardi, M. E., Carubbi, F., Bertolotti, M., Piani, D., Nistri, A., Angelico, M., Romani, M. and Carulli, N. (1997) Effect of taurohyodeoxycholic acid on biliary lipid secretion in humans. Hepatology 25, 1306-1314
33. Rinella, M. E., Siddiqui, M. S., Gardikiotes, K., Gottstein, J., Elias, M. and Green, R. M. (2011) Dysregulation of the unfolded protein response in db/db mice with diet-induced steatohepatitis. Hepatology 54, 1600-1609
34. Xu, T. Y., Chen, R. H., Wang, P., Zhang, R. Y., Ke, S. F. and Miao, C. Y. (2010) 4-Phenyl butyric acid does not generally reduce glucose levels in rodent models of diabetes. Clin. Exp. Pharmacol. Physiol. 37, 441-446
35. Fu, S., Yang, L., Li, P., Hofmann, O., Dicker, L., Hide, W., Lin, X., Watkins, S. M., Ivanov, A. R. and Hotamisligil, G. S. (2011) Aberrant lipid metabolism disrupts calcium homeostasis causing liver endoplasmic reticulum stress in obesity. Nature 473, 528-531
36. Dentin, R., Benhamed, F., Hainault, I., Fauveau, V., Foufelle, F., Dyck, J. R., Girard, J. and Postic, C. (2006) Liver-specific inhibition of ChREBP improves hepatic steatosis and insulin resistance in ob/ob mice. Diabetes 55, 2159-2170
37. Shimomura, I., Bashmakov, Y. and Horton, J. D. (1999) Increased levels of nuclear SREBP-1c associated with fatty livers in two mouse models of diabetes mellitus. J. Biol. Chem. 274, 30028-30032
38. Henkel, A. S., Dewey, A. M., Anderson, K. A., Olivares, S. and Green, R. M. (2012) Reducing endoplasmic reticulum stress does not improve steatohepatitis in mice fed a methionine- and choline-deficient diet. Am. J. Physiol. Gastrointest. Liver Physiol. 303, G54-G59
39. Wu, S. D., Li, L. and Wang, J. Y. (2012) Ursodeoxycholic acid for nonalcoholic steatohepatitis. Eur. J. Gastroenterol. Hepatol. 24, 1247-1253