FXR activation protects against NAFLD via bile-acid-dependent reductions in lipid absorption
FXR agonists are used to treat non-alcoholic fatty liver disease (NAFLD), in part because they reduce hepatic lipids. Here, we show that FXR activation with the FXR agonist GSK2324 controls hepatic lipids via reduced absorption and selective decreases in fatty acid synthesis. Using comprehensive lip...
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| Published in | Cell metabolism Vol. 33; no. 8; pp. 1671 - 1684.e4 |
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| Main Authors | , , , , , , , , , , , , , , , , , , , , , |
| Format | Journal Article |
| Language | English |
| Published |
United States
Elsevier Inc
03.08.2021
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| Subjects | |
| Online Access | Get full text |
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| Abstract | FXR agonists are used to treat non-alcoholic fatty liver disease (NAFLD), in part because they reduce hepatic lipids. Here, we show that FXR activation with the FXR agonist GSK2324 controls hepatic lipids via reduced absorption and selective decreases in fatty acid synthesis. Using comprehensive lipidomic analyses, we show that FXR activation in mice or humans specifically reduces hepatic levels of mono- and polyunsaturated fatty acids (MUFA and PUFA). Decreases in MUFA are due to FXR-dependent repression of Scd1, Dgat2, and Lpin1 expression, which is independent of SHP and SREBP1c. FXR-dependent decreases in PUFAs are mediated by decreases in lipid absorption. Replenishing bile acids in the diet prevented decreased lipid absorption in GSK2324-treated mice, suggesting that FXR reduces absorption via decreased bile acids. We used tissue-specific FXR KO mice to show that hepatic FXR controls lipogenic genes, whereas intestinal FXR controls lipid absorption. Together, our studies establish two distinct pathways by which FXR regulates hepatic lipids.
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•Non-steroidal agonists of FXR significantly decrease intestinal lipid absorption•FXR decreases hepatic triglycerides independently of SHP and SREBP1C•FXR activation reduces expression of three key lipogenic genes, Scd1, Lpin1, and Dgat2•Intestinal and hepatic FXR are both required to decrease hepatic triglycerides
The nuclear receptor FXR lowers hepatic triglycerides to protect against the onset of NAFLD. Clifford et al. demonstrate that activation of FXR decreases hepatic triglycerides through two distinct mechanisms. First, via bile-acid-dependent decreases in intestinal lipid absorption and second, through selective changes in lipogenesis. |
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| AbstractList | FXR agonists are used to treat non-alcoholic fatty liver disease (NAFLD), in part because they reduce hepatic lipids. Here, we show that FXR activation with the FXR agonist GSK2324 controls hepatic lipids via reduced absorption and selective decreases in fatty acid synthesis. Using comprehensive lipidomic analyses, we show that FXR activation in mice or humans specifically reduces hepatic levels of mono- and polyunsaturated fatty acids (MUFA and PUFA). Decreases in MUFA are due to FXR-dependent repression of Scd1, Dgat2, and Lpin1 expression, which is independent of SHP and SREBP1c. FXR-dependent decreases in PUFAs are mediated by decreases in lipid absorption. Replenishing bile acids in the diet prevented decreased lipid absorption in GSK2324-treated mice, suggesting that FXR reduces absorption via decreased bile acids. We used tissue-specific FXR KO mice to show that hepatic FXR controls lipogenic genes, whereas intestinal FXR controls lipid absorption. Together, our studies establish two distinct pathways by which FXR regulates hepatic lipids.FXR agonists are used to treat non-alcoholic fatty liver disease (NAFLD), in part because they reduce hepatic lipids. Here, we show that FXR activation with the FXR agonist GSK2324 controls hepatic lipids via reduced absorption and selective decreases in fatty acid synthesis. Using comprehensive lipidomic analyses, we show that FXR activation in mice or humans specifically reduces hepatic levels of mono- and polyunsaturated fatty acids (MUFA and PUFA). Decreases in MUFA are due to FXR-dependent repression of Scd1, Dgat2, and Lpin1 expression, which is independent of SHP and SREBP1c. FXR-dependent decreases in PUFAs are mediated by decreases in lipid absorption. Replenishing bile acids in the diet prevented decreased lipid absorption in GSK2324-treated mice, suggesting that FXR reduces absorption via decreased bile acids. We used tissue-specific FXR KO mice to show that hepatic FXR controls lipogenic genes, whereas intestinal FXR controls lipid absorption. Together, our studies establish two distinct pathways by which FXR regulates hepatic lipids. FXR agonists are used to treat non-alcoholic fatty liver disease (NAFLD), in part because they reduce hepatic lipids. Here, we show that FXR activation with the FXR agonist GSK2324 controls hepatic lipids via reduced absorption and selective decreases in fatty acid synthesis. Using comprehensive lipidomic analyses, we show that FXR activation in mice or humans specifically reduces hepatic levels of mono- and polyunsaturated fatty acids (MUFA and PUFA). Decreases in MUFA are due to FXR-dependent repression of Scd1, Dgat2, and Lpin1 expression, which is independent of SHP and SREBP1c. FXR-dependent decreases in PUFAs are mediated by decreases in lipid absorption. Replenishing bile acids in the diet prevented decreased lipid absorption in GSK2324-treated mice, suggesting that FXR reduces absorption via decreased bile acids. We used tissue-specific FXR KO mice to show that hepatic FXR controls lipogenic genes, whereas intestinal FXR controls lipid absorption. Together, our studies establish two distinct pathways by which FXR regulates hepatic lipids. FXR agonists are used to treat non-alcoholic fatty liver disease (NAFLD), in part because they reduce hepatic lipids. Here, we show that FXR activation with the FXR agonist GSK2324 controls hepatic lipids via reduced absorption and selective decreases in fatty acid synthesis. Using comprehensive lipidomic analyses, we show that FXR activation in mice or humans specifically reduces hepatic levels of mono- and polyunsaturated fatty acids (MUFA and PUFA). Decreases in MUFA are due to FXR-dependent repression of Scd1, Dgat2, and Lpin1 expression, which is independent of SHP and SREBP1c. FXR-dependent decreases in PUFAs are mediated by decreases in lipid absorption. Replenishing bile acids in the diet prevented decreased lipid absorption in GSK2324-treated mice, suggesting that FXR reduces absorption via decreased bile acids. We used tissue-specific FXR KO mice to show that hepatic FXR controls lipogenic genes, whereas intestinal FXR controls lipid absorption. Together, our studies establish two distinct pathways by which FXR regulates hepatic lipids. [Display omitted] •Non-steroidal agonists of FXR significantly decrease intestinal lipid absorption•FXR decreases hepatic triglycerides independently of SHP and SREBP1C•FXR activation reduces expression of three key lipogenic genes, Scd1, Lpin1, and Dgat2•Intestinal and hepatic FXR are both required to decrease hepatic triglycerides The nuclear receptor FXR lowers hepatic triglycerides to protect against the onset of NAFLD. Clifford et al. demonstrate that activation of FXR decreases hepatic triglycerides through two distinct mechanisms. First, via bile-acid-dependent decreases in intestinal lipid absorption and second, through selective changes in lipogenesis. FXR agonists are used to treat non-alcoholic fatty liver disease (NAFLD), in part because they reduce hepatic lipids. Here, we show that FXR activation with the FXR agonist GSK2324 controls hepatic lipids via reduced absorption and selective decreases in fatty acid synthesis. Using comprehensive lipidomic analyses, we show that FXR activation in mice or humans specifically reduces hepatic levels of mono- and polyunsaturated fatty acids (MUFA and PUFA). Decreases in MUFA are due to FXR-dependent repression of Scd1, Dgat2 , and Lpin1 expression, which is independent of SHP and SREBP1c. FXR-dependent decreases in PUFAs are mediated by decreases in lipid absorption. Replenishing bile acids in the diet prevented decreased lipid absorption in GSK2324-treated mice, suggesting that FXR reduces absorption via decreased bile acids. We used tissue-specific FXR KO mice to show that hepatic FXR controls lipogenic genes, whereas intestinal FXR controls lipid absorption. Together, our studies establish two distinct pathways by which FXR regulates hepatic lipids. The nuclear receptor FXR lowers hepatic triglycerides to protect against the onset of NAFLD. Clifford et al. demonstrate that activation of FXR decreases hepatic triglycerides through two distinct mechanisms. First, via bile-acid-dependent decreases in intestinal lipid absorption and second, through selective changes in lipogenesis. |
| Author | Cheng, Angela Jarrett, Kelsey E. Clifford, Bethan L. Barshop, William Drew, Brian G. Marschall, Hanns-Ulrich Thorell, Anders Williams, Kevin J. Wahlström, Annika Meikle, Peter J. Sedgeman, Leslie R. Calkin, Anna C. Morand, Pauline Ashby, Julianne W. Edwards, Peter A. de Aguiar Vallim, Thomas Q. Mack, Julia J. Liu, Yingying Tarling, Elizabeth J. Brearley-Sholto, Madelaine C. Wohlschlegel, James Chan, Alvin P. |
| AuthorAffiliation | 2 Department of Biological Chemistry, David Geffen School of Medicine, University of California, Los Angeles (UCLA), Los Angeles, CA, USA 11 Molecular Biology Institute, University of California, Los Angeles (UCLA), Los Angeles, CA, USA 12 These authors contributed equally 13 Lead contact 9 Metabolomics Laboratory, Baker Heart & Diabetes Institute, Melbourne, VIC, Australia 3 Lipidomics Core Facility, Department of Biological Chemistry, David Geffen School of Medicine, University of California, Los Angeles (UCLA), Los Angeles, CA, USA 1 Department of Medicine, Division of Cardiology, University of California, Los Angeles (UCLA), Los Angeles, CA, USA 8 Karolinska Institutet, Department of Clinical Science, Danderyd Hospital and Department of Surgery, Ersta Hospital, Stockholm, Sweden 5 Lipid Metabolism & Cardiometabolic Disease Laboratory, Baker Heart & Diabetes Institute, Melbourne, VIC, Australia 7 Molecular Metabolism & Ageing Laboratory, Baker Heart & Diabetes Institute, Melbourne, VIC, Aust |
| AuthorAffiliation_xml | – name: 12 These authors contributed equally – name: 1 Department of Medicine, Division of Cardiology, University of California, Los Angeles (UCLA), Los Angeles, CA, USA – name: 2 Department of Biological Chemistry, David Geffen School of Medicine, University of California, Los Angeles (UCLA), Los Angeles, CA, USA – name: 6 Central Clinical School, Monash University, Melbourne, VIC, Australia – name: 11 Molecular Biology Institute, University of California, Los Angeles (UCLA), Los Angeles, CA, USA – name: 4 Department of Molecular and Clinical Medicine/Wallenberg Laboratory, Sahlgrenska Academy, University of Gothenburg, Gothenburg, Sweden – name: 3 Lipidomics Core Facility, Department of Biological Chemistry, David Geffen School of Medicine, University of California, Los Angeles (UCLA), Los Angeles, CA, USA – name: 13 Lead contact – name: 8 Karolinska Institutet, Department of Clinical Science, Danderyd Hospital and Department of Surgery, Ersta Hospital, Stockholm, Sweden – name: 9 Metabolomics Laboratory, Baker Heart & Diabetes Institute, Melbourne, VIC, Australia – name: 5 Lipid Metabolism & Cardiometabolic Disease Laboratory, Baker Heart & Diabetes Institute, Melbourne, VIC, Australia – name: 10 Jonsson Comprehensive Cancer Center (JCCC), UCLA, Los Angeles, CA, USA – name: 7 Molecular Metabolism & Ageing Laboratory, Baker Heart & Diabetes Institute, Melbourne, VIC, Australia |
| Author_xml | – sequence: 1 givenname: Bethan L. surname: Clifford fullname: Clifford, Bethan L. organization: Department of Medicine, Division of Cardiology, University of California, Los Angeles (UCLA), Los Angeles, CA, USA – sequence: 2 givenname: Leslie R. surname: Sedgeman fullname: Sedgeman, Leslie R. organization: Department of Medicine, Division of Cardiology, University of California, Los Angeles (UCLA), Los Angeles, CA, USA – sequence: 3 givenname: Kevin J. surname: Williams fullname: Williams, Kevin J. organization: Department of Biological Chemistry, David Geffen School of Medicine, University of California, Los Angeles (UCLA), Los Angeles, CA, USA – sequence: 4 givenname: Pauline surname: Morand fullname: Morand, Pauline organization: Department of Biological Chemistry, David Geffen School of Medicine, University of California, Los Angeles (UCLA), Los Angeles, CA, USA – sequence: 5 givenname: Angela surname: Cheng fullname: Cheng, Angela organization: Department of Biological Chemistry, David Geffen School of Medicine, University of California, Los Angeles (UCLA), Los Angeles, CA, USA – sequence: 6 givenname: Kelsey E. surname: Jarrett fullname: Jarrett, Kelsey E. organization: Department of Medicine, Division of Cardiology, University of California, Los Angeles (UCLA), Los Angeles, CA, USA – sequence: 7 givenname: Alvin P. surname: Chan fullname: Chan, Alvin P. organization: Department of Medicine, Division of Cardiology, University of California, Los Angeles (UCLA), Los Angeles, CA, USA – sequence: 8 givenname: Madelaine C. surname: Brearley-Sholto fullname: Brearley-Sholto, Madelaine C. organization: Department of Medicine, Division of Cardiology, University of California, Los Angeles (UCLA), Los Angeles, CA, USA – sequence: 9 givenname: Annika surname: Wahlström fullname: Wahlström, Annika organization: Department of Molecular and Clinical Medicine/Wallenberg Laboratory, Sahlgrenska Academy, University of Gothenburg, Gothenburg, Sweden – sequence: 10 givenname: Julianne W. surname: Ashby fullname: Ashby, Julianne W. organization: Department of Medicine, Division of Cardiology, University of California, Los Angeles (UCLA), Los Angeles, CA, USA – sequence: 11 givenname: William surname: Barshop fullname: Barshop, William organization: Department of Biological Chemistry, David Geffen School of Medicine, University of California, Los Angeles (UCLA), Los Angeles, CA, USA – sequence: 12 givenname: James surname: Wohlschlegel fullname: Wohlschlegel, James organization: Department of Biological Chemistry, David Geffen School of Medicine, University of California, Los Angeles (UCLA), Los Angeles, CA, USA – sequence: 13 givenname: Anna C. surname: Calkin fullname: Calkin, Anna C. organization: Lipid Metabolism & Cardiometabolic Disease Laboratory, Baker Heart & Diabetes Institute, Melbourne, VIC, Australia – sequence: 14 givenname: Yingying surname: Liu fullname: Liu, Yingying organization: Lipid Metabolism & Cardiometabolic Disease Laboratory, Baker Heart & Diabetes Institute, Melbourne, VIC, Australia – sequence: 15 givenname: Anders surname: Thorell fullname: Thorell, Anders organization: Karolinska Institutet, Department of Clinical Science, Danderyd Hospital and Department of Surgery, Ersta Hospital, Stockholm, Sweden – sequence: 16 givenname: Peter J. surname: Meikle fullname: Meikle, Peter J. organization: Metabolomics Laboratory, Baker Heart & Diabetes Institute, Melbourne, VIC, Australia – sequence: 17 givenname: Brian G. surname: Drew fullname: Drew, Brian G. organization: Central Clinical School, Monash University, Melbourne, VIC, Australia – sequence: 18 givenname: Julia J. surname: Mack fullname: Mack, Julia J. organization: Department of Medicine, Division of Cardiology, University of California, Los Angeles (UCLA), Los Angeles, CA, USA – sequence: 19 givenname: Hanns-Ulrich surname: Marschall fullname: Marschall, Hanns-Ulrich organization: Department of Molecular and Clinical Medicine/Wallenberg Laboratory, Sahlgrenska Academy, University of Gothenburg, Gothenburg, Sweden – sequence: 20 givenname: Elizabeth J. surname: Tarling fullname: Tarling, Elizabeth J. organization: Department of Medicine, Division of Cardiology, University of California, Los Angeles (UCLA), Los Angeles, CA, USA – sequence: 21 givenname: Peter A. surname: Edwards fullname: Edwards, Peter A. organization: Department of Medicine, Division of Cardiology, University of California, Los Angeles (UCLA), Los Angeles, CA, USA – sequence: 22 givenname: Thomas Q. surname: de Aguiar Vallim fullname: de Aguiar Vallim, Thomas Q. email: tvallim@mednet.ucla.edu organization: Department of Medicine, Division of Cardiology, University of California, Los Angeles (UCLA), Los Angeles, CA, USA |
| BackLink | https://www.ncbi.nlm.nih.gov/pubmed/34270928$$D View this record in MEDLINE/PubMed https://gup.ub.gu.se/publication/308972$$DView record from Swedish Publication Index http://kipublications.ki.se/Default.aspx?queryparsed=id:147355319$$DView record from Swedish Publication Index |
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| Keywords | intestinal lipid absorption FXR NAFLD bile acids |
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| Notes | ObjectType-Article-1 SourceType-Scholarly Journals-1 ObjectType-Feature-2 content type line 23 AUTHOR CONTRIBUTIONS T.Q.d.A.V., E.J.T., and P.A.E. oversaw and supervised the projects. Mouse experiments were performed by B.L.C., L.R.S., K.E.J., and A.C. Lipidomic analyses were performed by K.J.W. at the UCLA lipidomics core except for one study, which was performed by Y.L., A.C.C., B.G.D., and P.J.M. Radiolabeled absorption studies were performed by L.R.S. Bodipy-labeling study tissue processing, imaging, and quantification were performed by L.R.S., J.W.A., and J.J.M. Bile analysis by LC-MS was performed by L.R.S., M.C.B.-S., and W.B. under the supervision of J.W. GC-MS analyses were performed by P.M. and B.L.C. Sample collection and preparation for GC-MS were performed by B.L.C., A.P.C., and K.E.J. Human samples were collected by A.T., A.W., and H.U.M. Data analysis and statistical analyses were performed by B.L.C., L.R.S., and T.Q.d.A.V. Figures were generated by B.L.C., L.R.S., and T.Q.d.A.V. The manuscript was written by B.L.C., P.A.E., and T.Q.d.A.V. All authors revised and approved the final manuscript. |
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| Snippet | FXR agonists are used to treat non-alcoholic fatty liver disease (NAFLD), in part because they reduce hepatic lipids. Here, we show that FXR activation with... |
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| SubjectTerms | Animals beta-muricholic acid Bile bile acids Bile Acids and Salts - metabolism binding Cell Biology cholesterol Endocrinology & Metabolism Endocrinology and Diabetes Endokrinologi och diabetes farnesoid-x-receptor fatty liver-disease FXR Humans intestinal lipid absorption Lipids Liver - metabolism metabolism Mice Mice, Inbred C57BL NAFLD Non-alcoholic Fatty Liver Disease - metabolism Non-alcoholic Fatty Liver Disease - prevention & control nuclear receptor Phosphatidate Phosphatase - metabolism Receptors, Cytoplasmic and Nuclear - metabolism small heterodimer partner |
| Title | FXR activation protects against NAFLD via bile-acid-dependent reductions in lipid absorption |
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