Hepatocyte-Macrophage Acetoacetate Shuttle Protects against Tissue Fibrosis
Metabolic plasticity has been linked to polarized macrophage function, but mechanisms connecting specific fuels to tissue macrophage function remain unresolved. Here we apply a stable isotope tracing, mass spectrometry-based untargeted metabolomics approach to reveal the metabolome penetrated by hep...
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| Published in | Cell metabolism Vol. 29; no. 2; pp. 383 - 398.e7 |
|---|---|
| Main Authors | , , , , , , , , , |
| Format | Journal Article |
| Language | English |
| Published |
United States
Elsevier Inc
05.02.2019
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| Subjects | |
| Online Access | Get full text |
| ISSN | 1550-4131 1932-7420 1932-7420 |
| DOI | 10.1016/j.cmet.2018.10.015 |
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| Abstract | Metabolic plasticity has been linked to polarized macrophage function, but mechanisms connecting specific fuels to tissue macrophage function remain unresolved. Here we apply a stable isotope tracing, mass spectrometry-based untargeted metabolomics approach to reveal the metabolome penetrated by hepatocyte-derived glucose and ketone bodies. In both classically and alternatively polarized macrophages, [13C]acetoacetate (AcAc) labeled ∼200 chemical features, but its reduced form D-[13C]β-hydroxybutyrate (D-βOHB) labeled almost none. [13C]glucose labeled ∼500 features, and while unlabeled AcAc competed with only ∼15% of them, the vast majority required the mitochondrial enzyme succinyl-coenzyme A-oxoacid transferase (SCOT). AcAc carbon labeled metabolites within the cytoplasmic glycosaminoglycan pathway, which regulates tissue fibrogenesis. Accordingly, livers of mice lacking SCOT in macrophages were predisposed to accelerated fibrogenesis. Exogenous AcAc, but not D-βOHB, ameliorated diet-induced hepatic fibrosis. These data support a hepatocyte-macrophage ketone shuttle that segregates AcAc from D-βOHB, coordinating the fibrogenic response to hepatic injury via mitochondrial metabolism in tissue macrophages.
[Display omitted]
•Macrophages oxidize acetoacetate (AcAc), but not β-hydroxybutyrate•Metabolism of AcAc in macrophages extends into pathways beyond the TCA cycle•Effective AcAc competition with glucose requires its mitochondrial metabolism•Mitochondrial AcAc metabolism in macrophages protects against liver fibrosis
Puchalska et al. combine stable isotope tracing with untargeted metabolomics to identify the specific roles of the ketone bodies, acetoacetate (AcAc) and D-β-hydroxybutyrate (D-βOHB), in mediating metabolic plasticity in macrophages. They unveil a hepatocyte-macrophage ketone shuttle and show that AcAc protects the liver from high-fat-diet-induced fibrosis. |
|---|---|
| AbstractList | Metabolic plasticity has been linked to polarized macrophage function, but mechanisms connecting specific fuels to tissue
macrophage function remain unresolved. Here we apply a stable isotope tracing, mass spectrometry-based untargeted metabolomics
approach to reveal the metabolome penetrated by hepatocyte-derived glucose and ketone bodies. In both classically and
alternatively polarized macrophages, [
13
C]acetoacetate (AcAc) labeled ~200 chemical features, but its reduced
form D-[
13
C]β-hydroxybutyrate (D-βOHB) labeled almost none. [
13
C]glucose labeled ~500
features, and while unlabeled AcAc competed with only ~15% of them, the vast majority required the mitochondrial enzyme
succinyl-CoA-oxoacid transferase (SCOT). AcAc carbon labeled metabolites within the cytoplasmic glycosaminoglycan pathway, which
regulates tissue fibrogenesis. Accordingly, livers of mice lacking SCOT in macrophages were predisposed to accelerated
fibrogenesis. Exogenous AcAc, but not D-βOHB, ameliorated diet-induced hepatic fibrosis. These data support a
hepatocyte-macrophage ketone shuttle that segregates AcAc from D-βOHB, coordinating the fibrogenic response to hepatic
injury via mitochondrial metabolism in tissue macrophages.
XXX et al combine stable isotope tracing with untargeted metabolomics to identify the specific roles of the ketone bodies,
acetoacetate (AcAc) and D-hydroxybutyrate (D-βOHB), in mediating metabolic plasticity in macrophages. They unveil a
hepatocyte-macrophage ketone shuttle and show that AcAc protects the liver from high fat diet-induced fibrosis. Metabolic plasticity has been linked to polarized macrophage function, but mechanisms connecting specific fuels to tissue macrophage function remain unresolved. Here we apply a stable isotope tracing, mass spectrometry-based untargeted metabolomics approach to reveal the metabolome penetrated by hepatocyte-derived glucose and ketone bodies. In both classically and alternatively polarized macrophages, [13C]acetoacetate (AcAc) labeled ∼200 chemical features, but its reduced form D-[13C]β-hydroxybutyrate (D-βOHB) labeled almost none. [13C]glucose labeled ∼500 features, and while unlabeled AcAc competed with only ∼15% of them, the vast majority required the mitochondrial enzyme succinyl-coenzyme A-oxoacid transferase (SCOT). AcAc carbon labeled metabolites within the cytoplasmic glycosaminoglycan pathway, which regulates tissue fibrogenesis. Accordingly, livers of mice lacking SCOT in macrophages were predisposed to accelerated fibrogenesis. Exogenous AcAc, but not D-βOHB, ameliorated diet-induced hepatic fibrosis. These data support a hepatocyte-macrophage ketone shuttle that segregates AcAc from D-βOHB, coordinating the fibrogenic response to hepatic injury via mitochondrial metabolism in tissue macrophages.Metabolic plasticity has been linked to polarized macrophage function, but mechanisms connecting specific fuels to tissue macrophage function remain unresolved. Here we apply a stable isotope tracing, mass spectrometry-based untargeted metabolomics approach to reveal the metabolome penetrated by hepatocyte-derived glucose and ketone bodies. In both classically and alternatively polarized macrophages, [13C]acetoacetate (AcAc) labeled ∼200 chemical features, but its reduced form D-[13C]β-hydroxybutyrate (D-βOHB) labeled almost none. [13C]glucose labeled ∼500 features, and while unlabeled AcAc competed with only ∼15% of them, the vast majority required the mitochondrial enzyme succinyl-coenzyme A-oxoacid transferase (SCOT). AcAc carbon labeled metabolites within the cytoplasmic glycosaminoglycan pathway, which regulates tissue fibrogenesis. Accordingly, livers of mice lacking SCOT in macrophages were predisposed to accelerated fibrogenesis. Exogenous AcAc, but not D-βOHB, ameliorated diet-induced hepatic fibrosis. These data support a hepatocyte-macrophage ketone shuttle that segregates AcAc from D-βOHB, coordinating the fibrogenic response to hepatic injury via mitochondrial metabolism in tissue macrophages. Metabolic plasticity has been linked to polarized macrophage function, but mechanisms connecting specific fuels to tissue macrophage function remain unresolved. Here we apply a stable isotope tracing, mass spectrometry-based untargeted metabolomics approach to reveal the metabolome penetrated by hepatocyte-derived glucose and ketone bodies. In both classically and alternatively polarized macrophages, [13C]acetoacetate (AcAc) labeled ∼200 chemical features, but its reduced form D-[13C]β-hydroxybutyrate (D-βOHB) labeled almost none. [13C]glucose labeled ∼500 features, and while unlabeled AcAc competed with only ∼15% of them, the vast majority required the mitochondrial enzyme succinyl-coenzyme A-oxoacid transferase (SCOT). AcAc carbon labeled metabolites within the cytoplasmic glycosaminoglycan pathway, which regulates tissue fibrogenesis. Accordingly, livers of mice lacking SCOT in macrophages were predisposed to accelerated fibrogenesis. Exogenous AcAc, but not D-βOHB, ameliorated diet-induced hepatic fibrosis. These data support a hepatocyte-macrophage ketone shuttle that segregates AcAc from D-βOHB, coordinating the fibrogenic response to hepatic injury via mitochondrial metabolism in tissue macrophages. [Display omitted] •Macrophages oxidize acetoacetate (AcAc), but not β-hydroxybutyrate•Metabolism of AcAc in macrophages extends into pathways beyond the TCA cycle•Effective AcAc competition with glucose requires its mitochondrial metabolism•Mitochondrial AcAc metabolism in macrophages protects against liver fibrosis Puchalska et al. combine stable isotope tracing with untargeted metabolomics to identify the specific roles of the ketone bodies, acetoacetate (AcAc) and D-β-hydroxybutyrate (D-βOHB), in mediating metabolic plasticity in macrophages. They unveil a hepatocyte-macrophage ketone shuttle and show that AcAc protects the liver from high-fat-diet-induced fibrosis. Metabolic plasticity has been linked to polarized macrophage function, but mechanisms connecting specific fuels to tissue macrophage function remain unresolved. Here we apply a stable isotope tracing, mass spectrometry-based untargeted metabolomics approach to reveal the metabolome penetrated by hepatocyte-derived glucose and ketone bodies. In both classically and alternatively polarized macrophages, [ C]acetoacetate (AcAc) labeled ∼200 chemical features, but its reduced form D-[ C]β-hydroxybutyrate (D-βOHB) labeled almost none. [ C]glucose labeled ∼500 features, and while unlabeled AcAc competed with only ∼15% of them, the vast majority required the mitochondrial enzyme succinyl-coenzyme A-oxoacid transferase (SCOT). AcAc carbon labeled metabolites within the cytoplasmic glycosaminoglycan pathway, which regulates tissue fibrogenesis. Accordingly, livers of mice lacking SCOT in macrophages were predisposed to accelerated fibrogenesis. Exogenous AcAc, but not D-βOHB, ameliorated diet-induced hepatic fibrosis. These data support a hepatocyte-macrophage ketone shuttle that segregates AcAc from D-βOHB, coordinating the fibrogenic response to hepatic injury via mitochondrial metabolism in tissue macrophages. |
| Author | Huang, Xiaojing Graham, Mark J. Daniel, Bence Puchalska, Patrycja Crawford, Peter A. Lengfeld, Justin E. Han, Xianlin Nagy, Laszlo Patti, Gary J. Martin, Shannon E. |
| AuthorAffiliation | 8 Barshop Institute for Longevity and Aging Studies, Department of Medicine, Division of Diabetes, University of Texas Health Science Center at San Antonio, San Antonio, TX 78229 USA 4 Department of Chemistry, Washington University, St. Louis, MO 63110 USA 5 Department of Radiation Oncology, Memorial Sloan Kettering Cancer Center, New York, NY 10065 USA 9 Department of Biological Chemistry, Johns Hopkins University School of Medicine, Johns Hopkins All Children’s Hospital, Saint Petersburg, FL 33701 USA 1 Division of Molecular Medicine, Department of Medicine, University of Minnesota, Minneapolis, MN 55455 USA 10 Department of Biochemistry, Molecular Biology, and Biophysics, University of Minnesota, Minneapolis, MN 55455 USA 3 Pathobiology Graduate Program, Brown University, Providence, RI 02912 USA 6 Department of Medicine, Johns Hopkins University School of Medicine, Johns Hopkins All Children’s Hospital, Saint Petersburg, FL 33701 USA 2 Center for Metabolic Origins of Disease, Sanford Burnh |
| AuthorAffiliation_xml | – name: 6 Department of Medicine, Johns Hopkins University School of Medicine, Johns Hopkins All Children’s Hospital, Saint Petersburg, FL 33701 USA – name: 4 Department of Chemistry, Washington University, St. Louis, MO 63110 USA – name: 2 Center for Metabolic Origins of Disease, Sanford Burnham Prebys Medical Discovery Institute, Orlando, FL 32827 USA – name: 5 Department of Radiation Oncology, Memorial Sloan Kettering Cancer Center, New York, NY 10065 USA – name: 7 Ionis Pharmaceuticals, Carlsbad, CA 92010 USA – name: 11 Lead contact: Peter A. Crawford MD, PhD, University of Minnesota, 401 East River Parkway, MMC 194, Minneapolis, MN 55455, USA, Tel: +1 612-301-2202, crawforp@umn.edu – name: 1 Division of Molecular Medicine, Department of Medicine, University of Minnesota, Minneapolis, MN 55455 USA – name: 3 Pathobiology Graduate Program, Brown University, Providence, RI 02912 USA – name: 10 Department of Biochemistry, Molecular Biology, and Biophysics, University of Minnesota, Minneapolis, MN 55455 USA – name: 8 Barshop Institute for Longevity and Aging Studies, Department of Medicine, Division of Diabetes, University of Texas Health Science Center at San Antonio, San Antonio, TX 78229 USA – name: 9 Department of Biological Chemistry, Johns Hopkins University School of Medicine, Johns Hopkins All Children’s Hospital, Saint Petersburg, FL 33701 USA |
| Author_xml | – sequence: 1 givenname: Patrycja surname: Puchalska fullname: Puchalska, Patrycja organization: Division of Molecular Medicine, Department of Medicine, University of Minnesota, 401 East River Parkway, MMC 194, Minneapolis, MN 55455, USA – sequence: 2 givenname: Shannon E. surname: Martin fullname: Martin, Shannon E. organization: Center for Metabolic Origins of Disease, Sanford Burnham Prebys Medical Discovery Institute, Orlando, FL 32827, USA – sequence: 3 givenname: Xiaojing surname: Huang fullname: Huang, Xiaojing organization: Center for Metabolic Origins of Disease, Sanford Burnham Prebys Medical Discovery Institute, Orlando, FL 32827, USA – sequence: 4 givenname: Justin E. surname: Lengfeld fullname: Lengfeld, Justin E. organization: Division of Molecular Medicine, Department of Medicine, University of Minnesota, 401 East River Parkway, MMC 194, Minneapolis, MN 55455, USA – sequence: 5 givenname: Bence surname: Daniel fullname: Daniel, Bence organization: Center for Metabolic Origins of Disease, Sanford Burnham Prebys Medical Discovery Institute, Orlando, FL 32827, USA – sequence: 6 givenname: Mark J. surname: Graham fullname: Graham, Mark J. organization: Ionis Pharmaceuticals, Carlsbad, CA 92010, USA – sequence: 7 givenname: Xianlin surname: Han fullname: Han, Xianlin organization: Center for Metabolic Origins of Disease, Sanford Burnham Prebys Medical Discovery Institute, Orlando, FL 32827, USA – sequence: 8 givenname: Laszlo surname: Nagy fullname: Nagy, Laszlo organization: Center for Metabolic Origins of Disease, Sanford Burnham Prebys Medical Discovery Institute, Orlando, FL 32827, USA – sequence: 9 givenname: Gary J. surname: Patti fullname: Patti, Gary J. organization: Department of Chemistry, Washington University, St. Louis, MO 63110, USA – sequence: 10 givenname: Peter A. surname: Crawford fullname: Crawford, Peter A. email: crawforp@umn.edu organization: Division of Molecular Medicine, Department of Medicine, University of Minnesota, 401 East River Parkway, MMC 194, Minneapolis, MN 55455, USA |
| BackLink | https://www.ncbi.nlm.nih.gov/pubmed/30449686$$D View this record in MEDLINE/PubMed |
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| Keywords | macrophages stable isotope tracing untargeted metabolomics nonalcoholic fatty liver disease acetoacetate immunometabolism beta-hydroxybutyrate ketone bodies fibrosis |
| Language | English |
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| Notes | ObjectType-Article-1 SourceType-Scholarly Journals-1 ObjectType-Feature-2 content type line 23 Conceptualization, P.P., X.H., and P.A.C.; Methodology, P.P., S.E.M., X.H., J.E.L., B.D., L.N., M.J.G., X.Ha., G.J.P., and P.A.C.; Investigation, P.P., S.E.M., X.H., J.E.L., and B.D.; Resources, P.A.C., M.J.G.; Writing – Original Draft, P.P. and P.A.C.; Writing – Review & Editing, all authors; Visualization, P.P., X.H., J.E.L., B.D., and P.A.C.; Supervision, X.Ha., L.N., G.J.P. and P.A.C.; Funding Acquisition, P.A.C. Author Contributions |
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| SubjectTerms | 3-Hydroxybutyric Acid - metabolism acetoacetate Acetoacetates - metabolism Animals beta-hydroxybutyrate fibrosis Hepatocytes - metabolism Hepatocytes - pathology immunometabolism ketone bodies Liver Cirrhosis, Experimental - metabolism macrophages Macrophages - cytology Macrophages - metabolism Mice Mice, Inbred C57BL Mitochondria - metabolism nonalcoholic fatty liver disease stable isotope tracing untargeted metabolomics |
| Title | Hepatocyte-Macrophage Acetoacetate Shuttle Protects against Tissue Fibrosis |
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