[en] Dysregulated lipid metabolism is a key pathology in metabolic diseases and the liver is a critical organ for lipid metabolism. The gut microbiota has been shown to regulate hepatic lipid metabolism in the host. However, the underlying mechanism by which the gut microbiota influences hepatic lipid metabolism has not been elucidated. Here, a gut microbiota depletion mouse model was constructed with an antibiotics cocktail (Abx) to study the mechanism through which intestinal microbiota regulates hepatic lipid metabolism in high-fat diet (HFD)-fed mice. Our results showed that the Abx treatment effectively eradicated the gut microbiota in these mice. Microbiota depletion reduced the body weight and fat deposition both in white adipose tissue and liver. In addition, microbiota depletion reduced serum levels of glucose, total cholesterol (TC), low-density lipoproteins (LDL), insulin, and leptin in HFD-fed mice. Importantly, the depletion of gut microbiota in HFD-fed mice inhibited excessive hepatic lipid accumulation. Mechanistically, RNA-seq results revealed that gut microbiota depletion changed the expression of hepatic genes involved in cholesterol and fatty acid metabolism, such as Cd36, Mogat1, Cyp39a1, Abcc3, and Gpat3. Moreover, gut microbiota depletion reduced the abundance of bacteria associated with abnormal metabolism and inflammation, including Lachnospiraceae, Coriobacteriaceae_UCG-002, Enterorhabdus, Faecalibaculum, and Desulfovibrio. Correlation analysis showed that there was strong association between the altered gut microbiota abundance and the serum cholesterol level. This study indicates that gut microbiota ameliorates HFD-induced hepatic lipid metabolic dysfunction, which might be associated with genes participating in cholesterol and fatty acid metabolism in the liver.
Disciplines :
Microbiology
Author, co-author :
Han, Hui ; Université de Liège - ULiège > TERRA Research Centre ; State Key Laboratory of Animal Nutrition, Institute of Animal Science, Chinese Academy of Agricultural Sciences, Beijing 100193, China
Wang, Mengyu; State Key Laboratory of Animal Nutrition, Institute of Animal Science, Chinese Academy of Agricultural Sciences, Beijing 100193, China
Zhong, Ruqing ; State Key Laboratory of Animal Nutrition, Institute of Animal Science, Chinese Academy of Agricultural Sciences, Beijing 100193, China
Yi, Bao ; State Key Laboratory of Animal Nutrition, Institute of Animal Science, Chinese Academy of Agricultural Sciences, Beijing 100193, China
This study was funded by the Central Public-interest Scientific Institution Basal Research Fund (No. Y2022GH02 and PJ01618301), the Major Scientific Research Tasks for Scientific and Technological Innovation Projects of the Chinese Academy of Agricultural Sciences (CAAS-ZDRW202006-02), State Key Laboratory of Animal Nutrition (2004DA125184G2102), and the China Agriculture Research System (CARS-41).
Loos R.J.F. Yeo G.S.H. The genetics of obesity: From discovery to biology Nat. Rev. Genet. 2022 23 120 133 10.1038/s41576-021-00414-z 34556834
Jardon K.M. Canfora E.E. Goossens G.H. Blaak E.E. Dietary macronutrients and the gut microbiome: A precision nutrition approach to improve cardiometabolic health Gut 2022 71 1214 1226 10.1136/gutjnl-2020-323715 35135841
Han H. Yi B. Zhong R. Wang M. Zhang S. Ma J. Yin Y. Yin J. Chen L. Zhang H. From gut microbiota to host appetite: Gut microbiota-derived metabolites as key regulators Microbiome 2021 9 162 10.1186/s40168-021-01093-y
Han H. Jiang Y. Wang M. Melaku M. Liu L. Zhao Y. Everaert N. Yi B. Zhang H. Intestinal dysbiosis in nonalcoholic fatty liver disease (NAFLD): Focusing on the gut-liver axis Crit. Rev. Food Sci. Nutr. 2021 18 1 18 10.1080/10408398.2021.1966738 34404276
Astbury S. Atallah E. Vijay A. Aithal G.P. Grove J.I. Valdes A.M. Lower gut microbiome diversity and higher abundance of proinflammatory genus Collinsella are associated with biopsy-proven nonalcoholic steatohepatitis Gut Microbes 2020 11 569 580 10.1080/19490976.2019.1681861 31696774
Schwimmer J.B. Johnson J.S. Angeles J.E. Behling C. Belt P.H. Borecki I. Bross C. Durelle J. Goyal N.P. Hamilton G. et al. Microbiome Signatures Associated With Steatohepatitis and Moderate to Severe Fibrosis in Children With Nonalcoholic Fatty Liver Disease Gastroenterology 2019 157 1109 1122 10.1053/j.gastro.2019.06.028 31255652
Asnicar F. Berry S.E. Valdes A.M. Nguyen L.H. Piccinno G. Drew D.A. Leeming E. Gibson R. Le Roy C. Khatib H.A. et al. Microbiome connections with host metabolism and habitual diet from 1,098 deeply phenotyped individuals Nat. Med. 2021 27 321 332 10.1038/s41591-020-01183-8
Depommier C. Everard A. Druart C. Plovier H. Van Hul M. Vieira-Silva S. Falony G. Raes J. Maiter D. Delzenne N.M. et al. Supplementation with Akkermansia muciniphila in overweight and obese human volunteers: A proof-of-concept exploratory study Nat. Med. 2019 25 1096 1103 10.1038/s41591-019-0495-2
Dao M.C. Everard A. Aron-Wisnewsky J. Sokolovska N. Prifti E. Verger E.O. Kayser B.D. Levenez F. Chilloux J. Hoyles L. et al. Akkermansia muciniphila and improved metabolic health during a dietary intervention in obesity: Relationship with gut microbiome richness and ecology Gut 2016 65 426 436 10.1136/gutjnl-2014-308778
Lee G. You H.J. Bajaj J.S. Joo S.K. Yu J. Park S. Kang H. Park J.H. Kim J.H. Lee D.H. et al. Distinct signatures of gut microbiome and metabolites associated with significant fibrosis in non-obese NAFLD Nat. Commun. 2020 11 4982 10.1038/s41467-020-18754-5
Yang M. Yin Y. Wang F. Zhang H. Ma X. Yin Y. Tan B. Chen J. Supplementation With Lycium barbarum Polysaccharides Reduce Obesity in High-Fat Diet-Fed Mice by Modulation of Gut Microbiota Front. Microbiol. 2021 12 719967 10.3389/fmicb.2021.719967
Porras D. Nistal E. Martínez-Flórez S. Pisonero-Vaquero S. Olcoz J.L. Jover R. González-Gallego J. García-Mediavilla M.V. Sánchez-Campos S. Protective effect of quercetin on high-fat diet-induced non-alcoholic fatty liver disease in mice is mediated by modulating intestinal microbiota imbalance and related gut-liver axis activation Free. Radic. Biol. Med. 2017 102 188 202 10.1016/j.freeradbiomed.2016.11.037
Ortega-Hernández A. Martínez-Martínez E. Gómez-Gordo R. López-Andrés N. Fernández-Celis A. Gutiérrrez-Miranda B. Nieto M.L. Alarcón T. Alba C. Gómez-Garre D. et al. The Interaction between Mitochondrial Oxidative Stress and Gut Microbiota in the Cardiometabolic Consequences in Diet-Induced Obese Rats Antioxidants 2020 9 640 10.3390/antiox9070640
Tilg H. Adolph T.E. Dudek M. Knolle P. Non-alcoholic fatty liver disease: The interplay between metabolism, microbes and immunity Nat. Metab. 2021 3 1596 1607 10.1038/s42255-021-00501-9
Aron-Wisnewsky J. Warmbrunn M.V. Nieuwdorp M. Clément K. Nonalcoholic Fatty Liver Disease: Modulating Gut Microbiota to Improve Severity? Gastroenterology 2020 158 1881 1898 10.1053/j.gastro.2020.01.049
Michail S. Lin M. Frey M.R. Fanter R. Paliy O. Hilbush B. Reo N.V. Altered gut microbial energy and metabolism in children with non-alcoholic fatty liver disease FEMS Microbiol. Ecol. 2015 91 1 9 10.1093/femsec/fiu002
Aron-Wisnewsky J. Warmbrunn M.V. Nieuwdorp M. Clément K. Metabolism and Metabolic Disorders and the Microbiome: The Intestinal Microbiota Associated With Obesity, Lipid Metabolism, and Metabolic Health-Pathophysiology and Therapeutic Strategies Gastroenterology 2021 160 573 599 10.1053/j.gastro.2020.10.057
Nogal A. Valdes A.M. Menni C. The role of short-chain fatty acids in the interplay between gut microbiota and diet in cardio-metabolic health Gut Microbes 2021 13 1 24 10.1080/19490976.2021.1897212
Canfora E.E. Jocken J.W. Blaak E.E. Short-chain fatty acids in control of body weight and insulin sensitivity Nat. Rev. Endocrinol. 2015 11 577 591 10.1038/nrendo.2015.128
Xu J. Xu H.M. Peng Y. Zhao C. Zhao H.L. Huang W. Huang H.L. He J. Du Y.L. Zhou Y.J. et al. The effect of different combinations of antibiotic cocktails on mice and selection of animal models for further microbiota research Appl. Microbiol. Biotechnol. 2021 105 1669 1681 10.1007/s00253-021-11131-2
Zeng S.L. Li S.Z. Xiao P.T. Cai Y.Y. Chu C. Chen B.Z. Li P. Li J. Liu E.H. Citrus polymethoxyflavones attenuate metabolic syndrome by regulating gut microbiome and amino acid metabolism Sci. Adv. 2020 6 eaax6208 10.1126/sciadv.aax6208
Xu M. Shen Y. Cen M. Zhu Y. Cheng F. Tang L. Zheng X. Kim J.J. Dai N. Hu W. Modulation of the Gut Microbiota-farnesoid X Receptor Axis Improves Deoxycholic Acid-induced Intestinal Inflammation in Mice J. Crohns Colitis 2021 15 1197 1210 10.1093/ecco-jcc/jjab003
Zarrinpar A. Chaix A. Xu Z.Z. Chang M.W. Marotz C.A. Saghatelian A. Knight R. Panda S. Antibiotic-induced microbiome depletion alters metabolic homeostasis by affecting gut signaling and colonic metabolism Nat. Commun. 2018 9 2872 10.1038/s41467-018-05336-9
Sun L. Pang Y. Wang X. Wu Q. Liu H. Liu B. Liu G. Ye M. Kong W. Jiang C. Ablation of gut microbiota alleviates obesity-induced hepatic steatosis and glucose intolerance by modulating bile acid metabolism in hamsters Acta Pharm. Sin. B 2019 9 702 710 10.1016/j.apsb.2019.02.004
Almeida J.I. Tenreiro M.F. Martinez-Santamaria L. Guerrero-Aspizua S. Gisbert J.P. Alves P.M. Serra M. Baptista P.M. Hallmarks of the human intestinal microbiome on liver maturation and function J. Hepatol. 2022 76 694 725 10.1016/j.jhep.2021.10.015
De Vos W.M. Tilg H. Van Hul M. Cani P.D. Gut microbiome and health: Mechanistic insights Gut 2022 71 1020 1032 10.1136/gutjnl-2021-326789
Delzenne N.M. Knudsen C. Beaumont M. Rodriguez J. Neyrinck A.M. Bindels L.B. Contribution of the gut microbiota to the regulation of host metabolism and energy balance: A focus on the gut-liver axis Proc. Nutr. Soc. 2019 78 319 328 10.1017/S0029665118002756
DesOrmeaux G.J. Petrick H.L. Brunetta H.S. Holloway G.P. Independent of mitochondrial respiratory function, dietary nitrate attenuates HFD-induced lipid accumulation and mitochondrial ROS emission within the liver Am. J. Physiol. Endocrinol. Metab. 2021 321 e217 e228 10.1152/ajpendo.00610.2020
Dyck L. Prendeville H. Raverdeau M. Wilk M.M. Loftus R.M. Douglas A. McCormack J. Moran B. Wilkinson M. Mills E.L. et al. Suppressive effects of the obese tumor microenvironment on CD8 T cell infiltration and effector function J. Exp. Med. 2022 219 e20210042 10.1084/jem.20210042
Fan Y. Pedersen O. Gut microbiota in human metabolic health and disease Nat. Rev. Microbiol. 2021 19 55 71 10.1038/s41579-020-0433-9 32887946
Rao Y. Kuang Z. Li C. Guo S. Xu Y. Zhao D. Hu Y. Song B. Jiang Z. Ge Z. et al. Gut Akkermansia muciniphila ameliorates metabolic dysfunction-associated fatty liver disease by regulating the metabolism of L-aspartate via gut-liver axis Gut Microbes 2021 13 1 19 10.1080/19490976.2021.1927633 34030573
Wilson B.C. Vatanen T. Jayasinghe T.N. Leong K.S.W. Derraik J.G.B. Albert B.B. Chiavaroli V. Svirskis D.M. Beck K.L. Conlon C.A. et al. Strain engraftment competition and functional augmentation in a multi-donor fecal microbiota transplantation trial for obesity Microbiome 2021 9 107 10.1186/s40168-021-01060-7 33985595
Yu E.W. Gao L. Stastka P. Cheney M.C. Mahabamunuge J. Torres Soto M. Ford C.B. Bryant J.A. Henn M.R. Hohmann E.L. Fecal microbiota transplantation for the improvement of metabolism in obesity: The FMT-TRIM double-blind placebo-controlled pilot trial PLoS Med. 2020 17 e1003051 10.1371/journal.pmed.1003051 32150549
Van der Vossen E.W.J. Bastos D. Stols-Gonçalves D. de Goffau M.C. Davids M. Pereira J.P.B. Li Yim A.Y.F. Henneman P. Netea M.G. de Vos W.M. et al. Effects of fecal microbiota transplant on DNA methylation in subjects with metabolic syndrome Gut Microbes 2021 13 1993513 10.1080/19490976.2021.1993513
Kim Y. Hwang S.W. Kim S. Lee Y.S. Kim T.Y. Lee S.H. Kim S.J. Yoo H.J. Kim E.N. Kweon M.N. Dietary cellulose prevents gut inflammation by modulating lipid metabolism and gut microbiota Gut Microbes 2020 11 944 961 10.1080/19490976.2020.1730149
Peng C. Xu X. He Z. Li N. Ouyang Y. Zhu Y. Lu N. He C. Helicobacter pylori infection worsens impaired glucose regulation in high-fat diet mice in association with an altered gut microbiome and metabolome Appl. Microbiol. Biotechnol. 2021 105 2081 2095 10.1007/s00253-021-11165-6
Peng C. Xu X. Li Y. Li X. Yang X. Chen H. Zhu Y. Lu N. He C. Sex-specific association between the gut microbiome and high-fat diet-induced metabolic disorders in mice Biol Sex Differ. 2020 11 5 10.1186/s13293-020-0281-3
Titchenell P.M. Lazar M.A. Birnbaum M.J. Unraveling the Regulation of Hepatic Metabolism by Insulin Trends Endocrinol. Metab. TEM 2017 28 497 505 10.1016/j.tem.2017.03.003
Harris R.B. Direct and indirect effects of leptin on adipocyte metabolism Biochim. Biophys. Acta 2014 1842 414 423 10.1016/j.bbadis.2013.05.009
Pereira S. Cline D.L. Glavas M.M. Covey S.D. Kieffer T.J. Tissue-Specific Effects of Leptin on Glucose and Lipid Metabolism Endocr. Rev. 2021 42 1 28 10.1210/endrev/bnaa027
Guerra-Cantera S. Frago L.M. Collado-Pérez R. Canelles S. Ros P. Freire-Regatillo A. Jiménez-Hernaiz M. Barrios V. Argente J. Chowen J.A. Sex Differences in Metabolic Recuperation After Weight Loss in High Fat Diet-Induced Obese Mice Front. Endocrinol. 2021 12 796661 10.3389/fendo.2021.796661
Pistell P.J. Utsuki T. Francis J. Ebenezer P.J. Terrebonne J. Roth G.S. Ingram D.K. An Avocado Extract Enriched in Mannoheptulose Prevents the Negative Effects of a High-Fat Diet in Mice Nutrients 2021 14 155 10.3390/nu14010155
Gart E. van Duyvenvoorde W. Toet K. Caspers M.P.M. Verschuren L. Nielsen M.J. Leeming D.J. Souto Lima E. Menke A. Hanemaaijer R. et al. Butyrate Protects against Diet-Induced NASH and Liver Fibrosis and Suppresses Specific Non-Canonical TGF-β Signaling Pathways in Human Hepatic Stellate Cells Biomedicines 2021 9 1954 10.3390/biomedicines9121954
Zhao S. Zhu Y. Schultz R.D. Li N. He Z. Zhang Z. Caron A. Zhu Q. Sun K. Xiong W. et al. Partial Leptin Reduction as an Insulin Sensitization and Weight Loss Strategy Cell Metab. 2019 30 706 719.e6 10.1016/j.cmet.2019.08.005
Bechmann L.P. Hannivoort R.A. Gerken G. Hotamisligil G.S. Trauner M. Canbay A. The interaction of hepatic lipid and glucose metabolism in liver diseases J. Hepatol. 2012 56 952 964 10.1016/j.jhep.2011.08.025
Yki-Järvinen H. Luukkonen P.K. Hodson L. Moore J.B. Dietary carbohydrates and fats in nonalcoholic fatty liver disease Nat. Rev. Gastroenterol. Hepatol. 2021 18 770 786 10.1038/s41575-021-00472-y
Groen A.K. Bloks V.W. Verkade H. Kuipers F. Cross-talk between liver and intestine in control of cholesterol and energy homeostasis Mol. Asp. Med. 2014 37 77 88 10.1016/j.mam.2014.02.001
Wang N. Westerterp M. ABC Transporters, Cholesterol Efflux, and Implications for Cardiovascular Diseases Adv. Exp. Med. Biol. 2020 1276 67 83
Tsao C.C. Foley J. Coulter S.J. Maronpot R. Zeldin D.C. Goldstein J.A. CYP2C40, a unique arachidonic acid 16-hydroxylase, is the major CYP2C in murine intestinal tract Mol. Pharmacol. 2000 58 279 287 10.1124/mol.58.2.279
Sonnweber T. Pizzini A. Nairz M. Weiss G. Tancevski I. Arachidonic Acid Metabolites in Cardiovascular and Metabolic Diseases Int. J. Mol. Sci. 2018 19 3285 10.3390/ijms19113285
Gai Z. Visentin M. Gui T. Zhao L. Thasler W.E. Häusler S. Hartling I. Cremonesi A. Hiller C. Kullak-Ublick G.A. Effects of Farnesoid X Receptor Activation on Arachidonic Acid Metabolism, NF-kB Signaling, and Hepatic Inflammation Mol. Pharmacol. 2018 94 802 811 10.1124/mol.117.111047
Guan X.X. Rao D.N. Liu Y.Z. Zhou Y. Yang H.H. Epoxyeicosatrienoic Acids and Fibrosis: Recent Insights for the Novel Therapeutic Strategies Int. J. Mol. Sci. 2021 22 10714 10.3390/ijms221910714
Liu W.M. Shi F.X. Lu L.Z. Zhang C. Liu Y.L. Zhang J. Tao Z.R. Shen J.D. Li G.Q. Wang D.Q. et al. Effects of linoleic acid and eicosapentaenoic acid on cell proliferation and lipid-metabolism gene expression in primary duck hepatocytes Mol. Cell. Biochem. 2011 352 19 24 10.1007/s11010-011-0735-3
Honda A. Miyazaki T. Iwamoto J. Hirayama T. Morishita Y. Monma T. Ueda H. Mizuno S. Sugiyama F. Takahashi S. et al. Regulation of bile acid metabolism in mouse models with hydrophobic bile acid composition J. Lipid Res. 2020 61 54 69 10.1194/jlr.RA119000395
Wang D.Q. Tazuma S. Cohen D.E. Carey M.C. Feeding natural hydrophilic bile acids inhibits intestinal cholesterol absorption: Studies in the gallstone-susceptible mouse Am. J. Physiol. Gastrointest. Liver Physiol. 2003 285 G494 G502 10.1152/ajpgi.00156.2003
Ikeda H. Ueda M. Ikeda M. Kobayashi H. Honda Y. Oxysterol 7alpha-hydroxylase (CYP39A1) in the ciliary nonpigmented epithelium of bovine eye Lab. Investig. 2003 83 349 355 10.1097/01.LAB.0000059933.35157.40
De Boer J.F. Kuipers F. Groen A.K. Cholesterol Transport Revisited: A New Turbo Mechanism to Drive Cholesterol Excretion Trends Endocrinol. Metab. TEM 2018 29 123 133 10.1016/j.tem.2017.11.006
Ji F. Zhang J. Liu N. Gu Y. Zhang Y. Huang P. Zhang N. Lin S. Pan R. Meng Z. et al. Blocking hepatocarcinogenesis by a cytochrome P450 family member with female-preferential expression Gut 2022 10.1136/gutjnl-2021-326050
Lu M. Hu X.H. Li Q. Xiong Y. Hu G.J. Xu J.J. Zhao X.N. Wei X.X. Chang C.C. Liu Y.K. et al. A specific cholesterol metabolic pathway is established in a subset of HCCs for tumor growth J. Mol. Cell Biol. 2013 5 404 415 10.1093/jmcb/mjt039
Wang R. Salem M. Yousef I.M. Tuchweber B. Lam P. Childs S.J. Helgason C.D. Ackerley C. Phillips M.J. Ling V. Targeted inactivation of sister of P-glycoprotein gene (spgp) in mice results in nonprogressive but persistent intrahepatic cholestasis Proc. Natl. Acad. Sci. USA 2001 98 2011 2016 10.1073/pnas.98.4.2011
Henkel A.S. LeCuyer B. Olivares S. Green R.M. Endoplasmic Reticulum Stress Regulates Hepatic Bile Acid Metabolism in Mice Cell Mol. Gastroenterol. Hepatol. 2017 3 261 271 10.1016/j.jcmgh.2016.11.006 28275692
Garzel B. Zhang L. Huang S.M. Wang H. A Change in Bile Flow: Looking Beyond Transporter Inhibition in the Development of Drug-induced Cholestasis Curr. Drug Metab. 2019 20 621 632 10.2174/1389200220666190709170256 31288715
Hall A.M. Kou K. Chen Z. Pietka T.A. Kumar M. Korenblat K.M. Lee K. Ahn K. Fabbrini E. Klein S. et al. Evidence for regulated monoacylglycerol acyltransferase expression and activity in human liver J. Lipid Res. 2012 53 990 999 10.1194/jlr.P025536 22394502
Soufi N. Hall A.M. Chen Z. Yoshino J. Collier S.L. Mathews J.C. Brunt E.M. Albert C.J. Graham M.J. Ford D.A. et al. Inhibiting monoacylglycerol acyltransferase 1 ameliorates hepatic metabolic abnormalities but not inflammation and injury in mice J. Biol. Chem. 2014 289 30177 30188 10.1074/jbc.M114.595850
Cao J. Li J.L. Li D. Tobin J.F. Gimeno R.E. Molecular identification of microsomal acyl-CoA:glycerol-3-phosphate acyltransferase, a key enzyme in de novo triacylglycerol synthesis Proc. Natl. Acad. Sci. USA 2006 103 19695 19700 10.1073/pnas.0609140103
Hall A.M. Soufi N. Chambers K.T. Chen Z. Schweitzer G.G. McCommis K.S. Erion D.M. Graham M.J. Su X. Finck B.N. Abrogating monoacylglycerol acyltransferase activity in liver improves glucose tolerance and hepatic insulin signaling in obese mice Diabetes 2014 63 2284 2296 10.2337/db13-1502
Lee Y.J. Ko E.H. Kim J.E. Kim E. Lee H. Choi H. Yu J.H. Kim H.J. Seong J.K. Kim K.S. et al. Nuclear receptor PPARγ-regulated monoacylglycerol O-acyltransferase 1 (MGAT1) expression is responsible for the lipid accumulation in diet-induced hepatic steatosis Proc. Natl. Acad. Sci. USA 2012 109 13656 13661 10.1073/pnas.1203218109
Demers A. Samami S. Lauzier B. Des Rosiers C. Ngo Sock E.T. Ong H. Mayer G. PCSK9 Induces CD36 Degradation and Affects Long-Chain Fatty Acid Uptake and Triglyceride Metabolism in Adipocytes and in Mouse Liver Arterioscler. Thromb. Vasc. Biol. 2015 35 2517 2525 10.1161/ATVBAHA.115.306032
Rada P. González-Rodríguez Á. García-Monzón C. Valverde Á.M. Understanding lipotoxicity in NAFLD pathogenesis: Is CD36 a key driver? Cell Death Dis. 2020 11 802 10.1038/s41419-020-03003-w
Zhou J. Febbraio M. Wada T. Zhai Y. Kuruba R. He J. Lee J.H. Khadem S. Ren S. Li S. et al. Hepatic fatty acid transporter Cd36 is a common target of LXR, PXR, and PPARgamma in promoting steatosis Gastroenterology 2008 134 556 567 10.1053/j.gastro.2007.11.037
Wang K. Liao M. Zhou N. Bao L. Ma K. Zheng Z. Wang Y. Liu C. Wang W. Wang J. et al. Parabacteroides distasonis Alleviates Obesity and Metabolic Dysfunctions via Production of Succinate and Secondary Bile Acids Cell Rep. 2019 26 222 235.e5 10.1016/j.celrep.2018.12.028
David L.A. Maurice C.F. Carmody R.N. Gootenberg D.B. Button J.E. Wolfe B.E. Ling A.V. Devlin A.S. Varma Y. Fischbach M.A. et al. Diet rapidly and reproducibly alters the human gut microbiome Nature 2014 505 559 563 10.1038/nature12820
Smith B.J. Miller R.A. Ericsson A.C. Harrison D.C. Strong R. Schmidt T.M. Changes in the gut microbiome and fermentation products concurrent with enhanced longevity in acarbose-treated mice BMC Microbiol. 2019 19 130 10.1186/s12866-019-1494-7
Hu W. Lu W. Li L. Zhang H. Lee Y.K. Chen W. Zhao J. Both living and dead Faecalibacterium prausnitzii alleviate house dust mite-induced allergic asthma through the modulation of gut microbiota and short-chain fatty acid production J. Sci. Food Agric. 2021 101 5563 5573 10.1002/jsfa.11207
Ormerod K.L. Wood D.L. Lachner N. Gellatly S.L. Daly J.N. Parsons J.D. Dal’Molin C.G. Palfreyman R.W. Nielsen L.K. Cooper M.A. et al. Genomic characterization of the uncultured Bacteroidales family S24-7 inhabiting the guts of homeothermic animals Microbiome 2016 4 36 10.1186/s40168-016-0181-2
Ye J. Zhao Y. Chen X. Zhou H. Yang Y. Zhang X. Huang Y. Zhang N. Lui E.M.K. Xiao M. Pu-erh tea ameliorates obesity and modulates gut microbiota in high fat diet fed mice Food Res. Int. 2021 144 110360 10.1016/j.foodres.2021.110360
Zhao Q. Hou D. Fu Y. Xue Y. Guan X. Shen Q. Adzuki Bean Alleviates Obesity and Insulin Resistance Induced by a High-Fat Diet and Modulates Gut Microbiota in Mice Nutrients 2021 13 3240 10.3390/nu13093240
Jiao N. Baker S.S. Nugent C.A. Tsompana M. Cai L. Wang Y. Buck M.J. Genco R.J. Baker R.D. Zhu R. et al. Gut microbiome may contribute to insulin resistance and systemic inflammation in obese rodents: A meta-analysis Physiol. Genom. 2018 50 244 254 10.1152/physiolgenomics.00114.2017
Everard A. Belzer C. Geurts L. Ouwerkerk J.P. Druart C. Bindels L.B. Guiot Y. Derrien M. Muccioli G.G. Delzenne N.M. et al. Cross-talk between Akkermansia muciniphila and intestinal epithelium controls diet-induced obesity Proc. Natl. Acad. Sci. USA 2013 110 9066 9071 10.1073/pnas.1219451110
Lee N.Y. Shin M.J. Youn G.S. Yoon S.J. Choi Y.R. Kim H.S. Gupta H. Han S.H. Kim B.K. Lee D.Y. et al. Lactobacillus attenuates progression of nonalcoholic fatty liver disease by lowering cholesterol and steatosis Clin. Mol. Hepatol. 2021 27 110 124 10.3350/cmh.2020.0125
Cani P.D. Human gut microbiome: Hopes, threats and promises Gut 2018 67 1716 1725 10.1136/gutjnl-2018-316723
Liu J. Hao W. He Z. Kwek E. Zhao Y. Zhu H. Liang N. Ma K.Y. Lei L. He W.S. et al. Beneficial effects of tea water extracts on the body weight and gut microbiota in C57BL/6J mice fed with a high-fat diet Food Funct. 2019 10 2847 2860 10.1039/C8FO02051E
He W.S. Li L. Rui J. Li J. Sun Y. Cui D. Xu B. Tomato seed oil attenuates hyperlipidemia and modulates gut microbiota in C57BL/6J mice Food Funct. 2020 11 4275 4290 10.1039/D0FO00133C
Wu T. Sun M. Liu R. Sui W. Zhang J. Yin J. Fang S. Zhu J. Zhang M. Bifidobacterium longum subsp. longum Remodeled Roseburia and Phosphatidylserine Levels and Ameliorated Intestinal Disorders and liver Metabolic Abnormalities Induced by High-Fat Diet J. Agric. Food Chem. 2020 68 4632 4640 10.1021/acs.jafc.0c00717
Zhao L. Zhang Q. Ma W. Tian F. Shen H. Zhou M. A combination of quercetin and resveratrol reduces obesity in high-fat diet-fed rats by modulation of gut microbiota Food Funct. 2017 8 4644 4656 10.1039/C7FO01383C
Martínez I. Wallace G. Zhang C. Legge R. Benson A.K. Carr T.P. Moriyama E.N. Walter J. Diet-induced metabolic improvements in a hamster model of hypercholesterolemia are strongly linked to alterations of the gut microbiota Appl. Environ. Microbiol. 2009 75 4175 4184 10.1128/AEM.00380-09
Clavel T. Desmarchelier C. Haller D. Gérard P. Rohn S. Lepage P. Daniel H. Intestinal microbiota in metabolic diseases: From bacterial community structure and functions to species of pathophysiological relevance Gut Microbes 2014 5 544 551 10.4161/gmic.29331
Claus S.P. Ellero S.L. Berger B. Krause L. Bruttin A. Molina J. Paris A. Want E.J. de Waziers I. Cloarec O. et al. Colonization-induced host-gut microbial metabolic interaction mBio 2011 2 e00271-10 10.1128/mBio.00271-10
Cai W. Xu J. Li G. Liu T. Guo X. Wang H. Luo L. Ethanol extract of propolis prevents high-fat diet-induced insulin resistance and obesity in association with modulation of gut microbiota in mice Food Res. Int. 2020 130 108939 10.1016/j.foodres.2019.108939
Yang X. He Z. Hu R. Yan J. Zhang Q. Li B. Yuan X. Zhang H. He J. Wu S. Dietary β-Carotene on Postpartum Uterine Recovery in Mice: Crosstalk Between Gut Microbiota and Inflammation Front. Immunol. 2021 12 744425 10.3389/fimmu.2021.744425
Xu P. Hong F. Wang J. Cong Y. Dai S. Wang S. Wang J. Jin X. Wang F. Liu J. et al. Microbiome Remodeling via the Montmorillonite Adsorption-Excretion Axis Prevents Obesity-related Metabolic Disorders EBioMedicine 2017 16 251 261 10.1016/j.ebiom.2017.01.019 28126594
Panasevich M.R. Meers G.M. Linden M.A. Booth F.W. Perfield J.W. 2nd Fritsche K.L. Wankhade U.D. Chintapalli S.V. Shankar K. Ibdah J.A. et al. High-fat, high-fructose, high-cholesterol feeding causes severe NASH and cecal microbiota dysbiosis in juvenile Ossabaw swine Am. J. Physiol. Endocrinol. Metab. 2018 314 e78 e92 10.1152/ajpendo.00015.2017 28899857
Tian B. Zhao J. Zhang M. Chen Z. Ma Q. Liu H. Nie C. Zhang Z. An W. Li J. Lycium ruthenicum Anthocyanins Attenuate High-Fat Diet-Induced Colonic Barrier Dysfunction and Inflammation in Mice by Modulating the Gut Microbiota Mol. Nutr. Food Res. 2021 65 e2000745 10.1002/mnfr.202000745 33629483
Saad M.J. Santos A. Prada P.O. Linking Gut Microbiota and Inflammation to Obesity and Insulin Resistance Physiology (Bethesda) 2016 31 283 293 10.1152/physiol.00041.2015
Davin-Regli A. Lavigne J.P. Pagès J.M. Enterobacter spp.: Update on Taxonomy, Clinical Aspects, and Emerging Antimicrobial Resistance Clin. Microbiol. Rev. 2019 32 e00002-19 10.1128/CMR.00002-19
Zong Z. Feng Y. McNally A. Carbapenem and Colistin Resistance in Enterobacter: Determinants and Clones Trends Microbiol. 2021 29 473 476 10.1016/j.tim.2020.12.009
