PKM2-dependent metabolic skewing of hepatic Th17 cells regulates pathogenesis of non-alcoholic fatty liver disease
Emerging evidence suggests a key contribution to non-alcoholic fatty liver disease (NAFLD) pathogenesis by Th17 cells. The pathogenic characteristics and mechanisms of hepatic Th17 cells, however, remain unknown. Here, we uncover and characterize a distinct population of inflammatory hepatic CXCR3+T...
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| Published in | Cell metabolism Vol. 33; no. 6; pp. 1187 - 1204.e9 |
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| Main Authors | , , , , , , , , , , , , , , , , , , , , |
| Format | Journal Article |
| Language | English |
| Published |
United States
Elsevier Inc
01.06.2021
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| Subjects | |
| Online Access | Get full text |
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| Abstract | Emerging evidence suggests a key contribution to non-alcoholic fatty liver disease (NAFLD) pathogenesis by Th17 cells. The pathogenic characteristics and mechanisms of hepatic Th17 cells, however, remain unknown. Here, we uncover and characterize a distinct population of inflammatory hepatic CXCR3+Th17 (ihTh17) cells sufficient to exacerbate NAFLD pathogenesis. Hepatic ihTh17 cell accrual was dependent on the liver microenvironment and CXCR3 axis activation. Mechanistically, the pathogenic potential of ihTh17 cells correlated with increased chromatin accessibility, glycolytic output, and concomitant production of IL-17A, IFNγ, and TNFα. Modulation of glycolysis using 2-DG or cell-specific PKM2 deletion was sufficient to reverse ihTh17-centric inflammatory vigor and NAFLD severity. Importantly, ihTh17 cell characteristics, CXCR3 axis activation, and hepatic expression of glycolytic genes were conserved in human NAFLD. Together, our data show that the steatotic liver microenvironment regulates Th17 cell accrual, metabolism, and competence toward an ihTh17 fate. Modulation of these pathways holds potential for development of novel therapeutic strategies for NAFLD.
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•Obesity promotes accrual of a unique inflammatory hepatic Th17 (ihTh17) cell subset•ihTh17 cells are sufficient to exacerbate NAFLD progression•The activation of CXCR3 axis in steatotic liver promotes ihTh17 cell accrual•Glycolysis-associated PKM2 activity shapes the ihTh17 inflammatory potential
Non-alcoholic fatty liver disease (NAFLD) is associated with increased inflammation. Moreno-Fernandez et al. now show that the steatotic liver microenvironment gives rise to a distinct inflammatory hepatic Th17 (ihTh17) cell subset, which preferentially utilizes the glycolytic pathway to fuel tissue inflammation and promote NAFLD progression. |
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| AbstractList | Emerging evidence suggests a key contribution to non-alcoholic fatty liver disease (NAFLD) pathogenesis by Th17 cells. The pathogenic characteristics and mechanisms of hepatic Th17 cells, however, remain unknown. Here, we uncover and characterize a distinct population of inflammatory hepatic CXCR3+Th17 (ihTh17) cells sufficient to exacerbate NAFLD pathogenesis. Hepatic ihTh17 cell accrual was dependent on the liver microenvironment and CXCR3 axis activation. Mechanistically, the pathogenic potential of ihTh17 cells correlated with increased chromatin accessibility, glycolytic output, and concomitant production of IL-17A, IFNγ, and TNFα. Modulation of glycolysis using 2-DG or cell-specific PKM2 deletion was sufficient to reverse ihTh17-centric inflammatory vigor and NAFLD severity. Importantly, ihTh17 cell characteristics, CXCR3 axis activation, and hepatic expression of glycolytic genes were conserved in human NAFLD. Together, our data show that the steatotic liver microenvironment regulates Th17 cell accrual, metabolism, and competence toward an ihTh17 fate. Modulation of these pathways holds potential for development of novel therapeutic strategies for NAFLD.
[Display omitted]
•Obesity promotes accrual of a unique inflammatory hepatic Th17 (ihTh17) cell subset•ihTh17 cells are sufficient to exacerbate NAFLD progression•The activation of CXCR3 axis in steatotic liver promotes ihTh17 cell accrual•Glycolysis-associated PKM2 activity shapes the ihTh17 inflammatory potential
Non-alcoholic fatty liver disease (NAFLD) is associated with increased inflammation. Moreno-Fernandez et al. now show that the steatotic liver microenvironment gives rise to a distinct inflammatory hepatic Th17 (ihTh17) cell subset, which preferentially utilizes the glycolytic pathway to fuel tissue inflammation and promote NAFLD progression. Emerging evidence suggests a key contribution to non-alcoholic fatty liver disease (NAFLD) pathogenesis by Th17 cells. The pathogenic characteristics and mechanisms of hepatic Th17 cells, however, remain unknown. Here, we uncover and characterize a distinct population of inflammatory hepatic CXCR3+Th17 (ihTh17) cells sufficient to exacerbate NAFLD pathogenesis. Hepatic ihTh17 cell accrual was dependent on the liver microenvironment and CXCR3 axis activation. Mechanistically, the pathogenic potential of ihTh17 cells correlated with increased chromatin accessibility, glycolytic output, and concomitant production of IL-17A, IFNγ, and TNFα. Modulation of glycolysis using 2-DG or cell-specific PKM2 deletion was sufficient to reverse ihTh17-centric inflammatory vigor and NAFLD severity. Importantly, ihTh17 cell characteristics, CXCR3 axis activation, and hepatic expression of glycolytic genes were conserved in human NAFLD. Together, our data show that the steatotic liver microenvironment regulates Th17 cell accrual, metabolism, and competence toward an ihTh17 fate. Modulation of these pathways holds potential for development of novel therapeutic strategies for NAFLD.Emerging evidence suggests a key contribution to non-alcoholic fatty liver disease (NAFLD) pathogenesis by Th17 cells. The pathogenic characteristics and mechanisms of hepatic Th17 cells, however, remain unknown. Here, we uncover and characterize a distinct population of inflammatory hepatic CXCR3+Th17 (ihTh17) cells sufficient to exacerbate NAFLD pathogenesis. Hepatic ihTh17 cell accrual was dependent on the liver microenvironment and CXCR3 axis activation. Mechanistically, the pathogenic potential of ihTh17 cells correlated with increased chromatin accessibility, glycolytic output, and concomitant production of IL-17A, IFNγ, and TNFα. Modulation of glycolysis using 2-DG or cell-specific PKM2 deletion was sufficient to reverse ihTh17-centric inflammatory vigor and NAFLD severity. Importantly, ihTh17 cell characteristics, CXCR3 axis activation, and hepatic expression of glycolytic genes were conserved in human NAFLD. Together, our data show that the steatotic liver microenvironment regulates Th17 cell accrual, metabolism, and competence toward an ihTh17 fate. Modulation of these pathways holds potential for development of novel therapeutic strategies for NAFLD. Emerging evidence suggests a key contribution to non-alcoholic fatty liver disease (NAFLD) pathogenesis by Th17 cells. The pathogenic characteristics and mechanisms of hepatic Th17 cells, however remain unknown. Here, we uncover and characterize a distinct population of inflammatory hepatic CXCR3 + Th17 cells (ihTh17) sufficient to exacerbate NAFLD pathogenesis. Hepatic ihTh17 cell accrual was dependent on the liver microenvironment and CXCR3 axis activation. Mechanistically, the pathogenic potential of ihTh17 cells correlated with increased chromatin accessibility, glycolytic output and concomitant production of IFNγ and TNFα Modulation of glycolysis using 2-DG or cell-specific PKM2 deletion was sufficient to reverse ihTh17-centric inflammatory vigor and NAFLD severity. Importantly, ihTh17 cell characteristics, CXCR3 axis activation and hepatic expression of glycolytic genes were conserved in human NAFLD. Together, our data show that the steatotic liver microenvironment regulates Th17 cell accrual, metabolism and competence towards an ihTh17 fate. Modulation of these pathways holds potential for development of novel therapeutic strategies for NAFLD. Nonalcoholic fatty liver disease (NAFLD) is associated with increased inflammation. Maria E. Moreno-Fernandez and colleagues now show that the steatotic liver microenvironment gives rise to a distinct inflammatory hepatic Th17 (ihTh17) cell subset, which preferentially utilizes the glycolytic pathway to fuel tissue inflammation and promote NAFLD progression. Emerging evidence suggests a key contribution to non-alcoholic fatty liver disease (NAFLD) pathogenesis by Th17 cells. The pathogenic characteristics and mechanisms of hepatic Th17 cells, however, remain unknown. Here, we uncover and characterize a distinct population of inflammatory hepatic CXCR3 Th17 (ihTh17) cells sufficient to exacerbate NAFLD pathogenesis. Hepatic ihTh17 cell accrual was dependent on the liver microenvironment and CXCR3 axis activation. Mechanistically, the pathogenic potential of ihTh17 cells correlated with increased chromatin accessibility, glycolytic output, and concomitant production of IL-17A, IFNγ, and TNFα. Modulation of glycolysis using 2-DG or cell-specific PKM2 deletion was sufficient to reverse ihTh17-centric inflammatory vigor and NAFLD severity. Importantly, ihTh17 cell characteristics, CXCR3 axis activation, and hepatic expression of glycolytic genes were conserved in human NAFLD. Together, our data show that the steatotic liver microenvironment regulates Th17 cell accrual, metabolism, and competence toward an ihTh17 fate. Modulation of these pathways holds potential for development of novel therapeutic strategies for NAFLD. |
| Author | Stankiewicz, Traci E. Shah, Amy S. Chetal, Kashish Szabo, Sara Xanthakos, Stavra A. Helmrath, Michael A. Weirauch, Matthew T. Salomonis, Nathan Divanovic, Senad Chan, Calvin C. Chen, Xiaoting Oates, Jarren R. Karns, Rebekah Moreno-Fernandez, Maria E. Romick-Rosendale, Lindsey Giles, Daniel A. Sheridan, Rachel Damen, Michelle S.M.A. Doll, Jessica R. Deshmukh, Hitesh Inge, Thomas H. |
| AuthorAffiliation | 4 Division of Biomedical Informatics, Cincinnati Children’s Hospital Medical Center, Cincinnati, OH 45229 13 The Center for Stem Cell & Organoid Medicine, Cincinnati Children’s Hospital Medical Center, Cincinnati, Ohio, USA 45229 10 Medical Scientist Training Program, Cincinnati Children’s Hospital Medical Center and the University of Cincinnati College of Medicine, Cincinnati, OH 45220, USA 7 Division of Endocrinology, Cincinnati Children’s Hospital Medical Center, Cincinnati, OH 45229 5 Division of Developmental Biology, Cincinnati Children’s Hospital Medical Center, Cincinnati, OH 45229 9 Division of Neonatology and Pulmonary Biology, Cincinnati Children’s Hospital Medical Center, Cincinnati, OH 45229 16 The Center for Inflammation and Tolerance, Cincinnati Children’s Hospital Medical Center, Cincinnati, Ohio, USA 45229 2 Division of Immunobiology, Cincinnati Children’s Hospital Medical Center, Cincinnati, OH 45229 11 Immunology Graduate Program, Cincinnati Children’s Hospital Medical Cente |
| AuthorAffiliation_xml | – name: 9 Division of Neonatology and Pulmonary Biology, Cincinnati Children’s Hospital Medical Center, Cincinnati, OH 45229 – name: 12 The Center for Autoimmune Genomics and Etiology, Cincinnati Children’s Hospital Medical Center, Cincinnati, Ohio, USA 45229 – name: 6 Division of Pathology, Cincinnati Children’s Hospital Medical Center, Cincinnati, OH 45229 – name: 11 Immunology Graduate Program, Cincinnati Children’s Hospital Medical Center and the University of Cincinnati College of Medicine, Cincinnati, OH 45220, USA – name: 7 Division of Endocrinology, Cincinnati Children’s Hospital Medical Center, Cincinnati, OH 45229 – name: 16 The Center for Inflammation and Tolerance, Cincinnati Children’s Hospital Medical Center, Cincinnati, Ohio, USA 45229 – name: 15 Department of Surgery, Children’s Hospital Colorado, Aurora CO 80045, USA – name: 3 Division of Gastroenterology, Hepatology and Nutrition, Cincinnati Children’s Hospital Medical Center, Cincinnati, OH 45229 – name: 8 Division of Pediatric General and Thoracic Surgery, Cincinnati Children’s Hospital Medical Center, Cincinnati, OH 45229 – name: 14 NMR Metabolomics Core, Cincinnati Children’s Hospital Medical Center, Cincinnati, Ohio, USA 45229 – name: 17 Lead contact – name: 5 Division of Developmental Biology, Cincinnati Children’s Hospital Medical Center, Cincinnati, OH 45229 – name: 10 Medical Scientist Training Program, Cincinnati Children’s Hospital Medical Center and the University of Cincinnati College of Medicine, Cincinnati, OH 45220, USA – name: 1 Department of Pediatrics, University of Cincinnati College of Medicine, Cincinnati, OH 45220 – name: 13 The Center for Stem Cell & Organoid Medicine, Cincinnati Children’s Hospital Medical Center, Cincinnati, Ohio, USA 45229 – name: 4 Division of Biomedical Informatics, Cincinnati Children’s Hospital Medical Center, Cincinnati, OH 45229 – name: 2 Division of Immunobiology, Cincinnati Children’s Hospital Medical Center, Cincinnati, OH 45229 |
| Author_xml | – sequence: 1 givenname: Maria E. surname: Moreno-Fernandez fullname: Moreno-Fernandez, Maria E. organization: Department of Pediatrics, University of Cincinnati College of Medicine, Cincinnati, OH 45220, USA – sequence: 2 givenname: Daniel A. surname: Giles fullname: Giles, Daniel A. organization: Department of Pediatrics, University of Cincinnati College of Medicine, Cincinnati, OH 45220, USA – sequence: 3 givenname: Jarren R. orcidid: 0000-0002-4734-5597 surname: Oates fullname: Oates, Jarren R. organization: Department of Pediatrics, University of Cincinnati College of Medicine, Cincinnati, OH 45220, USA – sequence: 4 givenname: Calvin C. orcidid: 0000-0002-9933-3061 surname: Chan fullname: Chan, Calvin C. organization: Department of Pediatrics, University of Cincinnati College of Medicine, Cincinnati, OH 45220, USA – sequence: 5 givenname: Michelle S.M.A. orcidid: 0000-0003-4617-2564 surname: Damen fullname: Damen, Michelle S.M.A. organization: Department of Pediatrics, University of Cincinnati College of Medicine, Cincinnati, OH 45220, USA – sequence: 6 givenname: Jessica R. orcidid: 0000-0001-5225-801X surname: Doll fullname: Doll, Jessica R. organization: Department of Pediatrics, University of Cincinnati College of Medicine, Cincinnati, OH 45220, USA – sequence: 7 givenname: Traci E. surname: Stankiewicz fullname: Stankiewicz, Traci E. organization: Department of Pediatrics, University of Cincinnati College of Medicine, Cincinnati, OH 45220, USA – sequence: 8 givenname: Xiaoting surname: Chen fullname: Chen, Xiaoting organization: Department of Pediatrics, University of Cincinnati College of Medicine, Cincinnati, OH 45220, USA – sequence: 9 givenname: Kashish surname: Chetal fullname: Chetal, Kashish organization: Department of Pediatrics, University of Cincinnati College of Medicine, Cincinnati, OH 45220, USA – sequence: 10 givenname: Rebekah surname: Karns fullname: Karns, Rebekah organization: Division of Gastroenterology, Hepatology and Nutrition, Cincinnati Children’s Hospital Medical Center, Cincinnati, OH 45229, USA – sequence: 11 givenname: Matthew T. surname: Weirauch fullname: Weirauch, Matthew T. organization: Department of Pediatrics, University of Cincinnati College of Medicine, Cincinnati, OH 45220, USA – sequence: 12 givenname: Lindsey surname: Romick-Rosendale fullname: Romick-Rosendale, Lindsey organization: Department of Pediatrics, University of Cincinnati College of Medicine, Cincinnati, OH 45220, USA – sequence: 13 givenname: Stavra A. surname: Xanthakos fullname: Xanthakos, Stavra A. organization: Department of Pediatrics, University of Cincinnati College of Medicine, Cincinnati, OH 45220, USA – sequence: 14 givenname: Rachel orcidid: 0000-0002-8318-8920 surname: Sheridan fullname: Sheridan, Rachel organization: Department of Pediatrics, University of Cincinnati College of Medicine, Cincinnati, OH 45220, USA – sequence: 15 givenname: Sara surname: Szabo fullname: Szabo, Sara organization: Department of Pediatrics, University of Cincinnati College of Medicine, Cincinnati, OH 45220, USA – sequence: 16 givenname: Amy S. orcidid: 0000-0001-7297-139X surname: Shah fullname: Shah, Amy S. organization: Department of Pediatrics, University of Cincinnati College of Medicine, Cincinnati, OH 45220, USA – sequence: 17 givenname: Michael A. surname: Helmrath fullname: Helmrath, Michael A. organization: Division of Pediatric General and Thoracic Surgery, Cincinnati Children’s Hospital Medical Center, Cincinnati, OH 45229, USA – sequence: 18 givenname: Thomas H. surname: Inge fullname: Inge, Thomas H. organization: Department of Surgery, Children’s Hospital Colorado, Aurora, CO 80045, USA – sequence: 19 givenname: Hitesh surname: Deshmukh fullname: Deshmukh, Hitesh organization: Department of Pediatrics, University of Cincinnati College of Medicine, Cincinnati, OH 45220, USA – sequence: 20 givenname: Nathan orcidid: 0000-0001-9689-2469 surname: Salomonis fullname: Salomonis, Nathan organization: Department of Pediatrics, University of Cincinnati College of Medicine, Cincinnati, OH 45220, USA – sequence: 21 givenname: Senad surname: Divanovic fullname: Divanovic, Senad email: senad.divanovic@cchmc.org organization: Department of Pediatrics, University of Cincinnati College of Medicine, Cincinnati, OH 45220, USA |
| BackLink | https://www.ncbi.nlm.nih.gov/pubmed/34004162$$D View this record in MEDLINE/PubMed |
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| IEDL.DBID | IXB |
| ISSN | 1550-4131 1932-7420 |
| IngestDate | Thu Aug 21 18:31:20 EDT 2025 Sun Aug 24 04:09:17 EDT 2025 Mon Jul 21 06:02:22 EDT 2025 Tue Jul 01 03:58:19 EDT 2025 Thu Apr 24 22:54:55 EDT 2025 Fri Feb 23 02:46:35 EST 2024 |
| IsDoiOpenAccess | false |
| IsOpenAccess | true |
| IsPeerReviewed | true |
| IsScholarly | true |
| Issue | 6 |
| Keywords | IFNγ NAFLD PKM liver CXCR3 T cell cellular metabolism glycolysis TNF obesity |
| Language | English |
| License | Copyright © 2021 Elsevier Inc. All rights reserved. |
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| Notes | ObjectType-Article-1 SourceType-Scholarly Journals-1 ObjectType-Feature-2 content type line 23 AUTHOR CONTRIBUTION MEMF, DAG, JRO, CCC, MSMAD, JRD, TES, RK, MW, LRR, RS, SS, HD, NS, and SD participated in data generation. MEMF, RK, LRR, SAX, RS, SS, ASS, HD, NS, XC, KC, MTW, and SD participated in analysis and interpretation of data. MAH and THI provided materials, technical support, interpretation of data and participated in review of the manuscript. MEMF and SD participated in the conception and design of the study, obtained the funding and wrote the manuscript. All authors have reviewed the manuscript and approve the final version. |
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| OpenAccessLink | http://www.cell.com/article/S1550413121002163/pdf |
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| PublicationTitle | Cell metabolism |
| PublicationTitleAlternate | Cell Metab |
| PublicationYear | 2021 |
| Publisher | Elsevier Inc |
| Publisher_xml | – name: Elsevier Inc |
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| SubjectTerms | Animals Carrier Proteins - immunology Cell Line cellular metabolism CXCR3 Female glycolysis Humans IFNγ liver Male Membrane Proteins - immunology Mice Mice, Inbred C57BL Mice, Knockout NAFLD Non-alcoholic Fatty Liver Disease - immunology obesity PKM Pyruvate Kinase - immunology Receptors, CXCR3 - immunology T cell Th17 Cells - cytology Th17 Cells - immunology Thyroid Hormone-Binding Proteins Thyroid Hormones - immunology TNF |
| Title | PKM2-dependent metabolic skewing of hepatic Th17 cells regulates pathogenesis of non-alcoholic fatty liver disease |
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