Ursodeoxycholic acid: Effects on hepatic unfolded protein response, apoptosis and oxidative stress in morbidly obese patients

Liver International

Volumn 38, Issue 3, 2018, Pages 523-531

  Mueller, Michaela ^a   Castro, Rui E ^b,c   Thorell, Anders ^d,e   Marschall, Hanns Ulrich ^f   Auer, Nicole ^a   Herac, Merima ^g   Rodrigues, Cecilia M P ^b,c   Trauner, Michael ^a  

^a MEDICAL UNIVERSITY OF VIENNA   (Austria)

^b RESEARCH INSTITUTE FOR MEDICINES IMED ULISBOA   (Portugal)

^c UNIVERSITY OF LISBON   (Portugal)

^d DANDERYD HOSPITAL   (Sweden)

^e ERSTA HOSPITAL   (Sweden)

^f UNIVERSITY OF GOTHENBURG   (Sweden)

^g UNIVERSITY OF VIENNA   (Austria)

Author keywords

CHOP; ER stress; microRNA signalling; miR 34a; NASH

Indexed keywords

4 HYDROXYNONENAL; ERDJ4 PROTEIN; GLUCOSE REGULATED PROTEIN 78; GROWTH ARREST AND DNA DAMAGE INDUCIBLE PROTEIN 153; MESSENGER RNA; MICRORNA 34A; PROTEIN; PROTEIN BAK; PROTEIN BAX; THIOBARBITURIC ACID REACTIVE SUBSTANCE; UNCLASSIFIED DRUG; URSODEOXYCHOLIC ACID; X BOX BINDING PROTEIN 1; DDIT3 PROTEIN, HUMAN; MICRORNA; MIRN34 MICRORNA, HUMAN;

APOPTOSIS; ARTICLE; BARIATRIC SURGERY; CLINICAL ARTICLE; CONTROLLED STUDY; DRUG MECHANISM; ENDOPLASMIC RETICULUM STRESS; HOMEOSTASIS; HUMAN; LIVER FIBROSIS; MORBID OBESITY; NONALCOHOLIC FATTY LIVER; OXIDATIVE STRESS; PHARMACODYNAMICS; PROTEIN EXPRESSION; RANDOMIZED CONTROLLED TRIAL; REGULATORY MECHANISM; SIGNAL TRANSDUCTION; UNFOLDED PROTEIN RESPONSE; BLOOD; COMPLICATION; DRUG EFFECT; ENDOPLASMIC RETICULUM; GENETICS; LIVER; METABOLISM; SWEDEN;

APOPTOSIS; ENDOPLASMIC RETICULUM; ENDOPLASMIC RETICULUM STRESS; HUMANS; LIVER; MICRORNAS; NON-ALCOHOLIC FATTY LIVER DISEASE; OBESITY, MORBID; OXIDATIVE STRESS; SWEDEN; TRANSCRIPTION FACTOR CHOP; UNFOLDED PROTEIN RESPONSE; URSODEOXYCHOLIC ACID;

EID: 85030123543     PISSN: 14783223     EISSN: 14783231     Source Type: Journal    
DOI: 10.1111/liv.13562     Document Type: Article

References (46)

1. Rinella ME. Nonalcoholic fatty liver disease: a systematic review. JAMA. 2015;313:2263-2273.
2. Angulo P. Nonalcoholic fatty liver disease. N Engl J Med. 2002;346:1221-1231.
3. Postic C, Girard J. Contribution of de novo fatty acid synthesis to hepatic steatosis and insulin resistance: lessons from genetically engineered mice. J Clin Invest. 2008;118:829-838.
4. Andrews TM, Tata JR. Protein synthesis by membrane-bound and free ribosomes of secretory and non-secretory tissues. Biochem J. 1971;121:683-694.
5. Ozcan U, Cao Q, Yilmaz E, et al. Endoplasmic reticulum stress links obesity, insulin action, and type 2 diabetes. Science. 2004;306:457-461.
6. Canbay A, Friedman S, Gores GJ. Apoptosis: the nexus of liver injury and fibrosis. Hepatology. 2004;39:273-278.
7. Janssens S, Pulendran B, Lambrecht BN. Emerging functions of the unfolded protein response in immunity. Nat Immunol. 2014;15:910-919.
8. Hu F, Liu F. Mitochondrial stress: a bridge between mitochondrial dysfunction and metabolic diseases? Cell Signal. 2011;23:1528-1533.
9. Satapati S, Kucejova B, Duarte JA, et al. Mitochondrial metabolism mediates oxidative stress and inflammation in fatty liver. J Clin Invest. 2015;125:4447-4462.
10. Wallace DC. A mitochondrial paradigm of metabolic and degenerative diseases, aging, and cancer: a dawn for evolutionary medicine. Annu Rev Genet. 2005;39:359-407.
11. Koliaki C, Szendroedi J, Kaul K, et al. Adaptation of hepatic mitochondrial function in humans with non-alcoholic fatty liver is lost in steatohepatitis. Cell Metab. 2015;21:739-746.
12. Begriche K, Massart J, Robin MA, Bonnet F, Fromenty B. Mitochondrial adaptations and dysfunctions in nonalcoholic fatty liver disease. Hepatology. 2013;58:1497-1507.
13. Sanyal AJ, Campbell-Sargent C, Mirshahi F, et al. Nonalcoholic steatohepatitis: association of insulin resistance and mitochondrial abnormalities. Gastroenterology. 2001;120:1183-1192.
14. Trauner M, Graziadei IW. Review article: mechanisms of action and therapeutic applications of ursodeoxycholic acid in chronic liver diseases. Aliment Pharmacol Ther. 1999;13:979-996.
15. Amaral JD, Castro RE, Sola S, Steer CJ, Rodrigues CM. p53 is a key molecular target of ursodeoxycholic acid in regulating apoptosis. J Biol Chem. 2007;282:34250-34259.
16. Ozcan U, Yilmaz E, Ozcan L, et al. Chemical chaperones reduce ER stress and restore glucose homeostasis in a mouse model of type 2 diabetes. Science. 2006;313:1137-1140.
17. Amaral JD, Viana RJ, Ramalho RM, Steer CJ, Rodrigues CM. Bile acids: regulation of apoptosis by ursodeoxycholic acid. J Lipid Res. 2009;50:1721-1734.
18. Kars M, Yang L, Gregor MF, et al. Tauroursodeoxycholic Acid may improve liver and muscle but not adipose tissue insulin sensitivity in obese men and women. Diabetes. 2010;59:1899-1905.
19. Mueller M, Thorell A, Claudel T, et al. Ursodeoxycholic acid exerts farnesoid X receptor-antagonistic effects on bile acid and lipid metabolism in morbid obesity. J Hepatol. 2015;62:1398-1404.
20. Wagner M, Fickert P, Zollner G, et al. Role of farnesoid X receptor in determining hepatic ABC transporter expression and liver injury in bile duct-ligated mice. Gastroenterology. 2003;125:825-838.
21. Castro RE, Ferreira DM, Zhang X, et al. Identification of microRNAs during rat liver regeneration after partial hepatectomy and modulation by ursodeoxycholic acid. American journal of physiology. Am J Physiol Gastrointest Liver Physiol. 2010;299:G887-G897.
22. Marschall HU, Wagner M, Zollner G, et al. Complementary stimulation of hepatobiliary transport and detoxification systems by rifampicin and ursodeoxycholic acid in humans. Gastroenterology. 2005;129:476-485.
23. Song Z, Zhou Z, Chen T, et al. S-adenosylmethionine (SAMe) protects against acute alcohol induced hepatotoxicity in mice. J Nutr Biochem. 2003;14:591-597.
24. Bedossa P, Poitou C, Veyrie N, et al. Histopathological algorithm and scoring system for evaluation of liver lesions in morbidly obese patients. Hepatology. 2012;56:1751-1759.
25. Han J, Kaufman RJ. The role of ER stress in lipid metabolism and lipotoxicity. J Lipid Res. 2016;57:1329-1338.
26. Urano F, Wang X, Bertolotti A, et al. Coupling of stress in the ER to activation of JNK protein kinases by transmembrane protein kinase IRE1. Science. 2000;287:664-666.
27. Nakamura T, Furuhashi M, Li P, et al. Double-stranded RNA-dependent protein kinase links pathogen sensing with stress and metabolic homeostasis. Cell. 2010;140:338-348.
28. Ohoka N, Yoshii S, Hattori T, Onozaki K, Hayashi H. TRB3, a novel ER stress-inducible gene, is induced via ATF4-CHOP pathway and is involved in cell death. EMBO J. 2005;24:1243-1255.
29. Yamaguchi H, Wang HG. CHOP is involved in endoplasmic reticulum stress-induced apoptosis by enhancing DR5 expression in human carcinoma cells. J Biol Chem. 2004;279:45495-45502.
30. Castro RE, Ferreira DM, Afonso MB, et al. miR-34a/SIRT1/p53 is suppressed by ursodeoxycholic acid in the rat liver and activated by disease severity in human non-alcoholic fatty liver disease. J Hepatol. 2013;58:119-125.
31. Chang TC, Wentzel EA, Kent OA, et al. Transactivation of miR-34a by p53 broadly influences gene expression and promotes apoptosis. Mol Cell. 2007;26:745-752.
32. Tang Y, Zhao W, Chen Y, Zhao Y, Gu W. Acetylation is indispensable for p53 activation. Cell. 2008;133:612-626.
33. Malaguarnera L, Madeddu R, Palio E, Arena N, Malaguarnera M. Heme oxygenase-1 levels and oxidative stress-related parameters in non-alcoholic fatty liver disease patients. J Hepatol. 2005;42:585-591.
34. Gutteridge JM, Halliwell B. The measurement and mechanism of lipid peroxidation in biological systems. Trends Biochem Sci. 1990;15:129-135.
35. Doorn JA, Petersen DR. Covalent modification of amino acid nucleophiles by the lipid peroxidation products 4-hydroxy-2-nonenal and 4-oxo-2-nonenal. Chem Res Toxicol. 2002;15:1445-1450.
36. Tan KP, Yang M, Ito S. Activation of nuclear factor (erythroid-2 like) factor 2 by toxic bile acids provokes adaptive defense responses to enhance cell survival at the emergence of oxidative stress. Mol Pharmacol. 2007;72:1380-1390.
37. Puri P, Mirshahi F, Cheung O, et al. Activation and dysregulation of the unfolded protein response in nonalcoholic fatty liver disease. Gastroenterology. 2008;134:568-576.
38. Lee AH, Scapa EF, Cohen DE, Glimcher LH. Regulation of hepatic lipogenesis by the transcription factor XBP1. Science. 2008;320:1492-1496.
39. Lee JS, Mendez R, Heng HH, Yang ZQ, Zhang K. Pharmacological ER stress promotes hepatic lipogenesis and lipid droplet formation. Am J Transl Res. 2012;4:102-113.
40. Lew JL, Zhao A, Yu J, et al. The farnesoid X receptor controls gene expression in a ligand- and promoter-selective fashion. J Biol Chem. 2004;279:8856-8861.
41. Boden G, Duan X, Homko C, et al. Increase in endoplasmic reticulum stress-related proteins and genes in adipose tissue of obese, insulin-resistant individuals. Diabetes. 2008;57:2438-2444.
42. Oyadomari S, Mori M. Roles of CHOP/GADD153 in endoplasmic reticulum stress. Cell Death Differ. 2004;11:381-389.
43. Thind A, Wilson C. Exosomal miRNAs as cancer biomarkers and therapeutic targets. J Extracell Vesicles. 2016;5:31292.
44. Chalasani N, Deeg MA, Crabb DW. Systemic levels of lipid peroxidation and its metabolic and dietary correlates in patients with nonalcoholic steatohepatitis. Am J Gastoenterol. 2004;99:1497-1502.
45. Yesilova Z, Yaman H, Oktenli C, et al. Systemic markers of lipid peroxidation and antioxidants in patients with nonalcoholic Fatty liver disease. Am J Gastroeneterol. 2005;100:850-855.
46. Dufour JF, Oneta CM, Gonvers JJ, et al. Randomized placebo-controlled trial of ursodeoxycholic acid with vitamin e in nonalcoholic steatohepatitis. Clin Gastroeneterol Hepatol. 2006;4:1537-1543.