Low production of 12α-hydroxylated bile acids prevents hepatic steatosis in Cyp2c70−/− mice by reducing fat absorption

Journal of Lipid Research - Tập 62 - Trang 100134 - 2021
Rumei Li1, Anna Palmiotti1, Hilde D. de Vries2, Milaine V. Hovingh1, Martijn Koehorst2, Niels L. Mulder1, Yue Zhang1,3, Kim Kats4, Vincent W. Bloks1, Jingyuan Fu1,3, Henkjan J. Verkade1, Jan Freark de Boer1,2, Folkert Kuipers1,2
1Department of Pediatrics, University of Groningen, University Medical Center Groningen, Groningen, the Netherlands
2Department of Laboratory Medicine, University of Groningen, University Medical Center Groningen, Groningen, The Netherlands
3Department of Genetics, University of Groningen, University Medical Center Groningen, Groningen, The Netherlands
4Department of Biomedical Science of Cells and Systems, University of Groningen, University Medical Center Groningen, Groningen, The Netherlands

Tài liệu tham khảo

Tilg, 2020, From NAFLD to MAFLD: when pathophysiology succeeds, Nat. Rev. Gastroenterol. Hepatol., 17, 387, 10.1038/s41575-020-0316-6 Brunt, 2021, NAFLD: reporting histologic findings in clinical practice, Hepatology, 73, 2028, 10.1002/hep.31599 Chavez-Talavera, 2019, Bile acid alterations in nonalcoholic fatty liver disease, obesity, insulin resistance and type 2 diabetes: what do the human studies tell?, Curr. Opin. Lipidol., 30, 244, 10.1097/MOL.0000000000000597 Kuipers, 2014, Beyond intestinal soap--bile acids in metabolic control, Nat. Rev. Endocrinol., 10, 488, 10.1038/nrendo.2014.60 Rau, 2021, An update on drug development for the treatment of nonalcoholic fatty liver disease - from ongoing clinical trials to future therapy, Expert Rev. Clin. Pharmacol., 14, 333, 10.1080/17512433.2021.1884068 Lefebvre, 2009, Role of bile acids and bile acid receptors in metabolic regulation, Physiol. Rev., 89, 147, 10.1152/physrev.00010.2008 Ridlon, 2014, Bile acids and the gut microbiome, Curr. Opin. Gastroenterol., 30, 332, 10.1097/MOG.0000000000000057 Chen, 2020, Genetic and microbial associations to plasma and fecal bile acids in obesity relate to plasma lipids and liver fat content, Cell Rep., 33, 108212, 10.1016/j.celrep.2020.108212 Bisschop, 2004, Low-fat, high-carbohydrate and high-fat, low-carbohydrate diets decrease primary bile acid synthesis in humans, Am. J. Clin. Nutr., 79, 570, 10.1093/ajcn/79.4.570 Sayin, 2013, Gut microbiota regulates bile acid metabolism by reducing the levels of tauro-beta-muricholic acid, a naturally occurring FXR antagonist, Cell Metab., 17, 225, 10.1016/j.cmet.2013.01.003 Takahashi, 2016, Cyp2c70 is responsible for the species difference in bile acid metabolism between mice and humans, J. Lipid Res., 57, 2130, 10.1194/jlr.M071183 de Boer, 2021, Cholangiopathy and biliary fibrosis in Cyp2c70-deficient mice are fully reversed by ursodeoxycholic acid, Cell Mol. Gastroenterol. Hepatol., 11, 1045, 10.1016/j.jcmgh.2020.12.004 Honda, 2020, Regulation of bile acid metabolism in mouse models with hydrophobic bile acid composition, J. Lipid Res., 61, 54, 10.1194/jlr.RA119000395 Straniero, 2020, Of mice and men: murine bile acids explain species differences in the regulation of bile acid and cholesterol metabolism, J. Lipid Res., 61, 480, 10.1194/jlr.RA119000307 de Boer, 2018, New insights in the multiple roles of bile acids and their signaling pathways in metabolic control, Curr. Opin. Lipidol., 29, 194, 10.1097/MOL.0000000000000508 2011 Dommerholt, 2021, Short-term protein restriction at advanced age stimulates FGF21 signalling, energy expenditure and browning of white adipose tissue, FEBS J., 288, 2257, 10.1111/febs.15604 Wang, 2016, Intestinal phospholipid remodeling is required for dietary-lipid uptake and survival on a high-fat diet, Cell Metab., 23, 492, 10.1016/j.cmet.2016.01.001 de Boer, 2020, Large-scale electron microscopy database for human type 1 diabetes, Nat. Commun., 11, 2475, 10.1038/s41467-020-16287-5 Ravelli, 2013, Destruction of tissue, cells and organelles in type 1 diabetic rats presented at macromolecular resolution, Sci. Rep., 3, 1804, 10.1038/srep01804 Kuipers, 2020, Neodymium as an alternative contrast for uranium in electron microscopy, Histochem. Cell Biol., 153, 271, 10.1007/s00418-020-01846-0 Böttcher, 1961, A rapid and sensitive sub-micro phosphorus determination, Analytica Chimica Acta, 24, 203, 10.1016/0003-2670(61)80041-X Bligh, 1959, A rapid method of total lipid extraction and purification, Can. J. Biochem. Physiol., 37, 911, 10.1139/y59-099 Eggink, 2018, Chronic infusion of taurolithocholate into the brain increases fat oxidation in mice, J. Endocrinol., 236, 85, 10.1530/JOE-17-0503 Ronda, 2016, Measurement of intestinal and peripheral cholesterol fluxes by a dual-tracer balance method, Curr. Protoc. Mouse Biol., 6, 408, 10.1002/cpmo.16 Dikkers, 2013, Scavenger receptor BI and ABCG5/G8 differentially impact biliary sterol secretion and reverse cholesterol transport in mice, Hepatology, 58, 293, 10.1002/hep.26316 Stricker, 2008, BrightStat.com: free statistics online, Comput. Methods Programs Biomed., 92, 135, 10.1016/j.cmpb.2008.06.010 de Boer, 2020, A human-like bile acid pool induced by deletion of hepatic Cyp2c70 modulates effects of FXR activation in mice, J. Lipid Res., 61, 291, 10.1194/jlr.RA119000243 Heuman, 1989, Quantitative estimation of the hydrophilic-hydrophobic balance of mixed bile salt solutions, J. Lipid Res., 30, 719, 10.1016/S0022-2275(20)38331-0 Wahlstrom, 2016, Intestinal crosstalk between bile acids and microbiota and its impact on host metabolism, Cell Metab., 24, 41, 10.1016/j.cmet.2016.05.005 Zhernakova, 2016, Population-based metagenomics analysis reveals markers for gut microbiome composition and diversity, Science, 352, 565, 10.1126/science.aad3369 Aron-Wisnewsky, 2020, Gut microbiota and human NAFLD: disentangling microbial signatures from metabolic disorders, Nat. Rev. Gastroenterol. Hepatol., 17, 279, 10.1038/s41575-020-0269-9 Quraishi, 2017, The gut-adherent microbiota of PSC-IBD is distinct to that of IBD, Gut, 66, 386, 10.1136/gutjnl-2016-311915 Voshol, 2000, Postprandial chylomicron formation and fat absorption in multidrug resistance gene 2 P-glycoprotein–deficient mice, Gastroenterology, 118, 173, 10.1016/S0016-5085(00)70426-4 Kennelly, 2018, Intestinal de novo phosphatidylcholine synthesis is required for dietary lipid absorption and metabolic homeostasis, J. Lipid Res., 59, 1695, 10.1194/jlr.M087056 Haeusler, 2013, Human insulin resistance is associated with increased plasma levels of 12α-hydroxylated bile acids, Diabetes, 62, 4184, 10.2337/db13-0639 Bertaggia, 2017, Cyp8b1 ablation prevents Western diet-induced weight gain and hepatic steatosis because of impaired fat absorption, Am. J. Physiol. Endocrinol. Metab., 313, E121, 10.1152/ajpendo.00409.2016 Higuchi, 2020, Bile acid composition regulates GPR119-dependent intestinal lipid sensing and food intake regulation in mice, Gut, 69, 1620, 10.1136/gutjnl-2019-319693 Bonde, 2016, Mice abundant in muricholic bile acids show resistance to dietary induced steatosis, weight gain, and to impaired glucose metabolism, PLoS One, 11, 10.1371/journal.pone.0147772 Roda, 1983, The influence of bile salt structure on self-association in aqueous solutions, J. Biol. Chem., 258, 6362, 10.1016/S0021-9258(18)32418-9 Song, 2015, Individual bile acids have differential effects on bile acid signaling in mice, Toxicol. Appl. Pharmacol., 283, 57, 10.1016/j.taap.2014.12.005 Jahan, 2005, Cytokine regulation of human sterol 12alpha-hydroxylase (CYP8B1) gene, Am. J. Physiol. Gastrointest. Liver Physiol., 288, G685, 10.1152/ajpgi.00207.2004 Haeusler, 2012, Impaired generation of 12-hydroxylated bile acids links hepatic insulin signaling with dyslipidemia, Cell Metab., 15, 65, 10.1016/j.cmet.2011.11.010 Hori, 2020, Association between 12alpha-hydroxylated bile acids and hepatic steatosis in rats fed a high-fat diet, J. Nutr. Biochem., 83, 108412, 10.1016/j.jnutbio.2020.108412 Koopen, 1999, Differential effects of 17alpha-ethinylestradiol on the neutral and acidic pathways of bile salt synthesis in the rat, J. Lipid Res., 40, 100, 10.1016/S0022-2275(20)33344-7 Hoogerland, 2019, Glucose-6-phosphate regulates hepatic bile acid synthesis in mice, Hepatology, 70, 2171, 10.1002/hep.30778 Wang, 2007, Differential hepatocellular zonation pattern of cholesterol 7alpha-hydroxylase (Cyp7a1) and sterol 12alpha-hydroxylase (Cyp8b1) in the mouse, Histochem. Cell Biol., 127, 253, 10.1007/s00418-006-0239-5 Ogrodnik, 2017, Cellular senescence drives age-dependent hepatic steatosis, Nat. Commun., 13, 15691, 10.1038/ncomms15691 Li, 2021, Gut microbiome and bile acids in obesity-related diseases, Best Pract. Res. Clin. Endocrinol. Metab., 101493, 10.1016/j.beem.2021.101493 Preidis, 2017, Nutrient-sensing nuclear receptors PPARalpha and FXR control liver energy balance, J. Clin. Invest, 127, 1193, 10.1172/JCI88893 Watanabe, 2006, Bile acids induce energy expenditure by promoting intracellular thyroid hormone activation, Nature, 439, 484, 10.1038/nature04330 Hijmans, 2015, A systems biology approach reveals the physiological origin of hepatic steatosis induced by liver X receptor activation, FASEB J., 29, 1153, 10.1096/fj.14-254656 Kalivianakis, 2000, Detection of impaired intestinal absorption of long-chain fatty acids: validation studies of a novel test in a rat model of fat malabsorption, Am. J. Clin. Nutr., 72, 174, 10.1093/ajcn/72.1.174 Abumrad, 2012, Role of the gut in lipid homeostasis, Physiol. Rev., 92, 1061, 10.1152/physrev.00019.2011 Drover, 2008, CD36 mediates both cellular uptake of very long chain fatty acids and their intestinal absorption in mice, J. Biol. Chem., 283, 13108, 10.1074/jbc.M708086200 Shim, 2009, Fatty acid transport protein 4 is dispensable for intestinal lipid absorption in mice, J. Lipid Res., 50, 491, 10.1194/jlr.M800400-JLR200 Wang, 2003, Feeding natural hydrophilic bile acids inhibits intestinal cholesterol absorption: studies in the gallstone-susceptible mouse, Am. J. Physiol. Gastrointest. Liver Physiol., 285, G494, 10.1152/ajpgi.00156.2003 Ferrell, 2016, Cholesterol 7alpha-hydroxylase-deficient mice are protected from high-fat/high-cholesterol diet-induced metabolic disorders, J. Lipid Res., 57, 1144, 10.1194/jlr.M064709 Murphy, 2005, Cholic acid as key regulator of cholesterol synthesis, intestinal absorption and hepatic storage in mice, Biochim. Biophys. Acta, 1735, 167, 10.1016/j.bbalip.2005.06.001 Rajagopalan, 1984, Kinetics and thermodynamics of the formation of mixed micelles of egg phosphatidylcholine and bile salts, J. Lipid Res., 25, 135, 10.1016/S0022-2275(20)37834-2 Coreta-Gomes, 2016, Quantification of cholesterol solubilized in dietary micelles: dependence on human bile salt variability and the presence of dietary food ingredients, Langmuir, 32, 4564, 10.1021/acs.langmuir.6b00723 Ponz de Leon, 1979, The effect of chenodeoxycholic acid (CDCA) on cholesterol absorption, Gastroenterology, 77, 223, 10.1016/0016-5085(79)90269-5 Voshol, 2001, Down-regulation of intestinal scavenger receptor class B, type I (SR-BI) expression in rodents under conditions of deficient bile delivery to the intestine, Biochem. J., 356, 317, 10.1042/bj3560317 Zhao, 2017, A combination of quercetin and resveratrol reduces obesity in high-fat diet-fed rats by modulation of gut microbiota, Food Funct., 8, 4644, 10.1039/C7FO01383C Bermingham, 2017, Key bacterial families (Clostridiaceae, Erysipelotrichaceae and Bacteroidaceae) are related to the digestion of protein and energy in dogs, PeerJ, 5, 10.7717/peerj.3019 Bosner, 1999, Percent cholesterol absorption in normal women and men quantified with dual stable isotopic tracers and negative ion mass spectrometry, J. Lipid Res., 40, 302, 10.1016/S0022-2275(20)33370-8 Walther, 2019, GutSelf: Interindividual variability in the processing of dietary compounds by the human gastrointestinal tract, Mol. Nutr. Food Res., 63, 10.1002/mnfr.201900677