Cholesterol 7α-hydroxylase protects the liver from inflammation and fibrosis by maintaining cholesterol homeostasis

Journal of Lipid Research

Volumn 57, Issue 10, 2016, Pages 1831-1844

  Liu, Hailiang ^a   Pathak, Preeti ^a   Boehme, Shannon ^a   Chiang, John Y L ^a  

^a Northeastern Ohio Medical University   (United States)

Author keywords

Bile acid; Farnesoid X receptor; Nuclear receptor; Takeda G protein coupled receptor 5

Indexed keywords

BILE ACID; CHOLESTEROL 7ALPHA MONOOXYGENASE; CHOLINE; FARNESOID X RECEPTOR; G PROTEIN COUPLED RECEPTOR 54; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; METHIONINE; STEROID RECEPTOR COACTIVATOR 1; TUMOR NECROSIS FACTOR; CHOLESTEROL; CYP7A1 PROTEIN, HUMAN; CYP7A1 PROTEIN, MOUSE; G PROTEIN COUPLED RECEPTOR; GPBAR1 PROTEIN, MOUSE;

ANIMAL EXPERIMENT; ANIMAL MODEL; APOPTOSIS; ARTICLE; BILE ACID SYNTHESIS; BIOACCUMULATION; CELL INFILTRATION; CHOLESTEROL HOMEOSTASIS; CHROMATIN IMMUNOPRECIPITATION; CONTROLLED STUDY; CYTOKINE PRODUCTION; ENZYME MECHANISM; FATTY LIVER; HEPATITIS; HOMEOSTASIS; HUMAN; HUMAN CELL; INFLAMMATORY CELL; LIVER FIBROSIS; LIVER PROTECTION; LUCIFERASE ASSAY; MALE; MOUSE; NONHUMAN; OXIDATIVE STRESS; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN PROTEIN INTERACTION; SIGNAL TRANSDUCTION; UPREGULATION; ANIMAL; CHEMICALLY INDUCED; ENZYMOLOGY; GENETICS; HEP-G2 CELL LINE; KNOCKOUT MOUSE; LIVER; LIVER CIRRHOSIS; METABOLISM; PATHOLOGY;

ANIMALS; CHOLESTEROL; CHOLESTEROL 7-ALPHA-HYDROXYLASE; HEP G2 CELLS; HOMEOSTASIS; HUMANS; LIVER; LIVER CIRRHOSIS; MICE; MICE, KNOCKOUT; NF-KAPPA B; OXIDATIVE STRESS; RECEPTORS, G-PROTEIN-COUPLED; TUMOR NECROSIS FACTOR-ALPHA;

EID: 84991011170     PISSN: 00222275     EISSN: 15397262     Source Type: Journal    
DOI: 10.1194/jlr.M069807     Document Type: Article

References (44)

1. Li, T., and J. Y. Chiang. 2014. Bile acid signaling in metabolic disease and drug therapy. Pharmacol. Rev. 66: 948-983.
2. Chiang, J. Y. 2009. Bile acids: regulation of synthesis. J. Lipid Res. 50: 1955-1966.
3. Trauner, M., P. Fickert, and R. E. Stauber. 1999. Inflammation-induced cholestasis. J. Gastroenterol. Hepatol. 14: 946-959.
4. Luedde, T., and R. F. Schwabe. 2011. NF-kappaB in the liver-linking injury, fibrosis and hepatocellular carcinoma. Nat. Rev. Gastroenterol Hepatol. 8: 108-118.
5. Greve, J. W., D.J. Gouma, and W. A. Buurman. 1989. Bile acids inhibit endotoxin-induced release of tumor necrosis factor by monocytes: an in vitro study. Hepatology. 10: 454-458.
6. Zhang, S., J. Wang, Q. Liu, and D. C. Harnish. 2009. Farnesoid X receptor agonist WAY-362450 attenuates liver inflammation and fibrosis in murine model of non-alcoholic steatohepatitis. J. Hepatol 51: 380-388.
7. Vavassori, P., A. Mencarelli, B. Renga, E. Distrutti, and S. Fiorucci. 2009. The bile acid receptor FXR is a modulator of intestinal innate immunity. J. Immunol. 183: 6251-6261.
8. Gadaleta, R. M., K.J. van Erpecum, B. Oldenburg, E. C. Willemsen, W. Renooij, S. Murzilli, L. W. Klomp, P. D. Siersema, M. E. Schipper, S. Danese, et al. 2011. Farnesoid X receptor activation inhibits inflammation and preserves the intestinal barrier in inflammatory bowel disease. Gut. 60: 463-472.
9. McMahan, R. H., X. X. Wang, L. L. Cheng, T. Krisko, M. Smith, K El Kasmi, M. Pruzanski, L. Adorini, L. Golden-Mason, M. Levi, et al. 2013. Bile acid receptor activation modulates hepatic monocyte activity and improves nonalcoholic fatty liver disease. J. Biol. Chem. 288: 11761-11770.
10. Pols, T. W., M. Nomura, T. Harach, G. Lo Sasso, M. H. Oosterveer, C. Thomas, G. Rizzo, A. Gioiello, L. Adorini, R. Pellicciari, et al. 2011. TGR5 activation inhibits atherosclerosis by reducing macrophage inflammation and lipid loading. Cell Metab. 14: 747-757.
11. Cipriani, S., A Mencarelli, M. G. Chini, E. Distrutti, B. Renga, G Bifulco, F. Baldelli, A. Donini, and S. Fiorucci. 2011. The bile acid receptor GPBAR-1 (TGR5) modulates integrity of intestinal barrier and immune response to experimental colitis. PLoS One. 6: e25637.
12. Keitel, V., R. Reinehr, P. Gatsios, C. Rupprecht, B. Gorg, O. Selbach, D. Haussinger, and R Kubitz. 2007. The G-protein coupled bile salt receptor TGR5 is expressed in liver sinusoidal endothelial cells. Hepatology. 45: 695-704.
13. Katsuma, S., A. Hirasawa, and G. Tsujimoto. 2005. Bile acids promote glucagon-like peptide-1 secretion through TGR5 in a murine enteroendocrine cell line STC-1. Biochem. Biophys. Res. Commun. 329: 386-390.
14. Keitel, V., M. Donner, S. Winandy, R. Kubitz, and D. Haussinger. 2008. Expression and function of the bile acid receptor TGR5 in Kupffer cells. Biochem. Biophys. Res. Commun. 372: 78-84.
15. Wang, Y. D., W. D. Chen, D. Yu, B. M. Forman, and W. Huang. 2011. The G-protein-coupled bile acid receptor, Gpbar1 (TGR5), negatively regulates hepatic inflammatory response through antagonizing nuclear factor kappa light-chain enhancer of activated B cells (NF-kappaB) in mice. Hepatology. 54: 1421-1432.
16. Lou, G., X. Ma, X. Fu, Z. Meng, W. Zhang, Y D. Wang, C. Van Ness, D. Yu, R. Xu, and W. Huang. 2014. GPBAR1/TGR5 mediates bile acid-induced cytokine expression in murine Kupffer cells. PLoS One. 9: e93567.
17. Mobraten, K, T. Haugbro, E. Karlstrom, C. R Kleiveland, and T. Lea. 2015. Activation of the bile acid receptor TGR5 enhances LPS-induced inflammatory responses in a human monocytic cell line. J. Recept. Signal Transduct Res. 35: 402-409.
18. Tilg, H., and A. R. Moschen. 2010. Evolution of inflammation in nonalcoholic fatty liver disease: the multiple parallel hits hypothesis. Hepatology. 52: 1836-1846.
19. Farrell, G. C, and C. Z. Larter. 2006. Nonalcoholic fatty liver disease: from steatosis to cirrhosis. Hepatology. 43: S99-S112.
20. Buzzetti, E., M. Pinzani, and E. A. Tsochatzis. 2016. The multiplehit pathogenesis of non-alcoholic fatty liver disease (NAFLD). Metabolism. 65: 1038-1048.
21. Woo Baidal, J. A., and J. E. Lavine. 2016. The intersection of nonalcoholic fatty liver disease and obesity. Sci. Transl. Med. 8: 323rv1.
22. Wouters, K, P.J. van Gorp, V. Bieghs, M.J. Gijbels, H. Duimel, D. Lutjohann, A. Kerksiek, R. van Kruchten, N. Maeda, B. Staels, et al. 2008. Dietary cholesterol, rather than liver steatosis, leads to hepatic inflammation in hyperlipidemic mouse models of nonalcoholic steatohepatitis. Hepatology. 48: 474-486.
23. Tomita, K, T. Teratani, T. Suzuki, M. Shimizu, H. Sato, K Narimatsu, Y. Okada, C. Kurihara, R Irie, H. Yokoyama, et al. 2014. Free cholesterol accumulation in hepatic stellate cells: mechanism of liver fibrosis aggravation in nonalcoholic steatohepatitis in mice. Hepatology. 59: 154-169.
24. Teratani, T., K Tomita, T. Suzuki, T. Oshikawa, H. Yokoyama, K Shimamura, S. Tominaga, S. Hiroi, R. Irie, Y Okada, et al. 2012. A high-cholesterol diet exacerbates liver fibrosis in mice via accumulation of free cholesterol in hepatic stellate cells. Gastroenterology. 142: 152-164.e10.
25. Ioannou, G. N., W. G. Haigh, D. Thorning, and C. Savard. 2013. Hepatic cholesterol crystals and crown-like structures distinguish NASH from simple steatosis. J. Lipid Res. 54: 1326-1334.
26. Li, T., E. Owsley, M. Matozel, P. Hsu, C. M. Novak, and J. Y. Chiang. 2010. Transgenic expression of cholesterol 7alpha-hydroxylase in the liver prevents high-fat diet-induced obesity and insulin resistance in mice. Hepatology. 52: 678-690.
27. FerrellJ. M., S. Boehme, F. Li, and J. Y. Chiang. 2016. Cholesterol 7{alpha}-hydroxylase-deficient mice are protected from high fat/high cholesterol diet-induced metabolic disorders. J. Lipid Res. 57: 1144-1154.
28. Pathak, P., T. Li, and J. Y. Chiang. 2013. Retinoic acid-related orphan receptor alpha regulates diurnal rhythm and fasting induction of sterol 12alpha-hydroxylase in bile acid synthesis. J. Biol. Chem. 288: 37154-37165.
29. Li, T.J. M. Francl, S. Boehme, and J. Y. Chiang. 2013. Regulation of cholesterol and bile acid homeostasis by the cholesterol 7alpha-hydroxylase/steroid response element-binding protein 2/microRNA-33a axis in mice. Hepatology. 58: 1111-1121.
30. Pandak, W. M., C. Schwarz, P. B. Hylemon, D. Mallonee, K Valerie, D. M. Heuman, R. A. Fisher, K Redford, and Z. R. Vlahcevic. 2001. Effects of CYP7A1 overexpression on cholesterol and bile acid homeostasis. Am. J. Physiol. Gastrointest Liver Physiol. 281: G878-G889.
31. Guo, L., Z. Zheng, J. Ai, B. Huang, and X. A. Li. 2014. Hepatic scavenger receptor BI protects against polymicrobial-induced sepsis through promoting LPS clearance in mice. J. Biol. Chem. 289: 14666-14673.
32. Topchiy, E., M. Cirstea, H.J. Kong, J. H. Boyd, Y. Wang, J. A. Russell, and K R. Walley. 2016. Lipopolysaccharide is cleared from the circulation by hepatocytes via the low density lipoprotein receptor. PLoS One. 11: e0155030.
33. Bramlett, K. S., S. Yao, and T. P. Burris. 2000. Correlation of farnesoid X receptor coactivator recruitment and cholesterol 7alpha-hydroxylase gene repression by bile acids. Mol. Genet. Metab. 71: 609-615.
34. Gao, Z., P. Chiao, X. Zhang, X. Zhang, M. A. Lazar, E. Seto, H. A Young, and J. Ye. 2005. Coactivators and corepressors of NF-kappaB in IkappaB alpha gene promoter. J. Biol. Chem. 280: 21091-21098.
35. Repa, J. J., K E. Berge, C. Pomajzl, J. A. Richardson, H. Hobbs, and D.J. Mangelsdorf. 2002. Regulation of ATP-binding cassette sterol transporters ABCG5 and ABCG8 by the liver X receptors alpha and beta. J. Biol. Chem. 277: 18793-18800.
36. Li, T., M. Matozel, S. Boehme, B. Kong, L. M. Nilsson, G. Guo, E. Ellis, and J. Y. Chiang. 2011. Overexpression of cholesterol 7alpha-hydroxylase promotes hepatic bile acid synthesis and secretion and maintains cholesterol homeostasis. Hepatology. 53: 996-1006.
37. Khovidhunkit, W., A H. Moser, J. K Shigenaga, C. Grunfeld, and K R Feingold. 2003. Endotoxin down-regulates ABCG5 and ABCG8 in mouse liver and ABCA1 and ABCG1 in J774 murine macrophages: differential role of LXR. J. Lipid Res. 44: 1728-1736.
38. Matsuzawa, N., T. Takamura, S. Kurita, H. Misu, T. Ota, H. Ando, M. Yokoyama, M. Honda, Y. Zen, Y Nakanuma, et al. 2007. Lipid-induced oxidative stress causes steatohepatitis in mice fed an atherogenic diet. Hepatology. 46: 1392-1403.
39. Marí, M., F. Caballero, A. Colell, A. Morales, J. Caballeria, A. Fernandez, C. Enrich, J. C. Fernandez-Checa, and C. Garcia-Ruiz. 2006. Mitochondrial free cholesterol loading sensitizes to TNF- and Fas-mediated steatohepatitis. Cell Metab. 4: 185-198.
40. Kim, D. H., Z. Xiao, S. Kwon, X. Sun, D. Ryerson, D. Tkac, P. Ma, S. Y Wu, C. M. Chiang, E. Zhou, et al. 2015. A dysregulated acetyl/SUMO switch of FXR promotes hepatic inflammation in obesity. EMBO J. 34: 184-199.
41. Dietschy, J. M., and S. D. Turley. 2002. Control of cholesterol turnover in the mouse. J. Biol. Chem. 277: 3801-3804.
42. Thomas, C, A Gioiello, L. Noriega, A. Strehle, J. Oury, G. Rizzo, A Macchiarulo, H. Yamamoto, C. Mataki, M. Pruzanski, et al. 2009. TGR5-mediated bile acid sensing controls glucose homeostasis. Cell Metab. 10: 167-177.
43. Lefebvre, P., B. Cariou, F. Lien, F. Kuipers, and B. Staels. 2009. Role of bile acids and bile acid receptors in metabolic regulation. Physiol. Rev. 89: 147-191.
44. Haeusler, R. A., B. Astiarraga, S. Camastra, D. Accili, and E. Ferrannini. 2013. Human insulin resistance is associated with increased plasma levels of 12alpha-hydroxylated bile acids. Diabetes. 62: 4184-4191.