Foxp3 Reprograms T Cell Metabolism to Function in Low-Glucose, High-Lactate Environments

Immune cells function in diverse metabolic environments. Tissues with low glucose and high lactate concentrations, such as the intestinal tract or ischemic tissues, frequently require immune responses to be more pro-tolerant, avoiding unwanted reactions against self-antigens or commensal bacteria. T...

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Published in:	Cell metabolism Vol. 25; no. 6; p. 1282
Main Authors:	Angelin, Alessia, Gil-de-Gómez, Luis, Dahiya, Satinder, Jiao, Jing, Guo, Lili, Levine, Matthew H, Wang, Zhonglin, Quinn, 3rd, William J, Kopinski, Piotr K, Wang, Liqing, Akimova, Tatiana, Liu, Yujie, Bhatti, Tricia R, Han, Rongxiang, Laskin, Benjamin L, Baur, Joseph A, Blair, Ian A, Wallace, Douglas C, Hancock, Wayne W, Beier, Ulf H
Format:	Journal Article
Language:	English
Published:	United States 06.06.2017
Subjects:	Animals Cell Line Cellular Microenvironment - genetics Cellular Microenvironment - immunology Cellular Reprogramming - genetics Cellular Reprogramming - immunology Forkhead Transcription Factors - genetics Forkhead Transcription Factors - immunology Glucose - genetics Glucose - immunology Glycolysis - genetics Glycolysis - immunology Humans Lactic Acid - immunology Mice Mice, Inbred BALB C Mice, Knockout Oxidative Phosphorylation Proto-Oncogene Proteins c-myc - genetics Proto-Oncogene Proteins c-myc - immunology T-Lymphocytes, Regulatory - immunology immunometabolism T cell metabolism immune regulation
ISSN:	1932-7420, 1932-7420
Online Access:	Get more information
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Abstract	Immune cells function in diverse metabolic environments. Tissues with low glucose and high lactate concentrations, such as the intestinal tract or ischemic tissues, frequently require immune responses to be more pro-tolerant, avoiding unwanted reactions against self-antigens or commensal bacteria. T-regulatory cells (Tregs) maintain peripheral tolerance, but how Tregs function in low-glucose, lactate-rich environments is unknown. We report that the Treg transcription factor Foxp3 reprograms T cell metabolism by suppressing Myc and glycolysis, enhancing oxidative phosphorylation, and increasing nicotinamide adenine dinucleotide oxidation. These adaptations allow Tregs a metabolic advantage in low-glucose, lactate-rich environments; they resist lactate-mediated suppression of T cell function and proliferation. This metabolic phenotype may explain how Tregs promote peripheral immune tolerance during tissue injury but also how cancer cells evade immune destruction in the tumor microenvironment. Understanding Treg metabolism may therefore lead to novel approaches for selective immune modulation in cancer and autoimmune diseases.
AbstractList	Immune cells function in diverse metabolic environments. Tissues with low glucose and high lactate concentrations, such as the intestinal tract or ischemic tissues, frequently require immune responses to be more pro-tolerant, avoiding unwanted reactions against self-antigens or commensal bacteria. T-regulatory cells (Tregs) maintain peripheral tolerance, but how Tregs function in low-glucose, lactate-rich environments is unknown. We report that the Treg transcription factor Foxp3 reprograms T cell metabolism by suppressing Myc and glycolysis, enhancing oxidative phosphorylation, and increasing nicotinamide adenine dinucleotide oxidation. These adaptations allow Tregs a metabolic advantage in low-glucose, lactate-rich environments; they resist lactate-mediated suppression of T cell function and proliferation. This metabolic phenotype may explain how Tregs promote peripheral immune tolerance during tissue injury but also how cancer cells evade immune destruction in the tumor microenvironment. Understanding Treg metabolism may therefore lead to novel approaches for selective immune modulation in cancer and autoimmune diseases.Immune cells function in diverse metabolic environments. Tissues with low glucose and high lactate concentrations, such as the intestinal tract or ischemic tissues, frequently require immune responses to be more pro-tolerant, avoiding unwanted reactions against self-antigens or commensal bacteria. T-regulatory cells (Tregs) maintain peripheral tolerance, but how Tregs function in low-glucose, lactate-rich environments is unknown. We report that the Treg transcription factor Foxp3 reprograms T cell metabolism by suppressing Myc and glycolysis, enhancing oxidative phosphorylation, and increasing nicotinamide adenine dinucleotide oxidation. These adaptations allow Tregs a metabolic advantage in low-glucose, lactate-rich environments; they resist lactate-mediated suppression of T cell function and proliferation. This metabolic phenotype may explain how Tregs promote peripheral immune tolerance during tissue injury but also how cancer cells evade immune destruction in the tumor microenvironment. Understanding Treg metabolism may therefore lead to novel approaches for selective immune modulation in cancer and autoimmune diseases. Immune cells function in diverse metabolic environments. Tissues with low glucose and high lactate concentrations, such as the intestinal tract or ischemic tissues, frequently require immune responses to be more pro-tolerant, avoiding unwanted reactions against self-antigens or commensal bacteria. T-regulatory cells (Tregs) maintain peripheral tolerance, but how Tregs function in low-glucose, lactate-rich environments is unknown. We report that the Treg transcription factor Foxp3 reprograms T cell metabolism by suppressing Myc and glycolysis, enhancing oxidative phosphorylation, and increasing nicotinamide adenine dinucleotide oxidation. These adaptations allow Tregs a metabolic advantage in low-glucose, lactate-rich environments; they resist lactate-mediated suppression of T cell function and proliferation. This metabolic phenotype may explain how Tregs promote peripheral immune tolerance during tissue injury but also how cancer cells evade immune destruction in the tumor microenvironment. Understanding Treg metabolism may therefore lead to novel approaches for selective immune modulation in cancer and autoimmune diseases.
Author	Akimova, Tatiana Angelin, Alessia Wang, Liqing Laskin, Benjamin L Han, Rongxiang Wallace, Douglas C Gil-de-Gómez, Luis Beier, Ulf H Wang, Zhonglin Liu, Yujie Kopinski, Piotr K Blair, Ian A Dahiya, Satinder Jiao, Jing Baur, Joseph A Hancock, Wayne W Guo, Lili Levine, Matthew H Quinn, 3rd, William J Bhatti, Tricia R
Author_xml	– sequence: 1 givenname: Alessia surname: Angelin fullname: Angelin, Alessia organization: Center for Mitochondrial and Epigenomic Medicine, Children's Hospital of Philadelphia, Philadelphia, PA 19104, USA – sequence: 2 givenname: Luis surname: Gil-de-Gómez fullname: Gil-de-Gómez, Luis organization: Penn SRP Center, Center of Excellence in Environmental Toxicology and Department of Systems Pharmacology and Translational Therapeutics, Perelman School of Medicine, University of Pennsylvania, Philadelphia, PA 19104, USA – sequence: 3 givenname: Satinder surname: Dahiya fullname: Dahiya, Satinder organization: Division of Transplant Immunology, Department of Pathology and Laboratory Medicine, and Biesecker Center for Pediatric Liver Disease, Children's Hospital of Philadelphia and University of Pennsylvania, Philadelphia, PA 19104, USA – sequence: 4 givenname: Jing surname: Jiao fullname: Jiao, Jing organization: Division of Nephrology and Department of Pediatrics, Children's Hospital of Philadelphia and University of Pennsylvania, Philadelphia, PA 19104, USA – sequence: 5 givenname: Lili surname: Guo fullname: Guo, Lili organization: Penn SRP Center, Center of Excellence in Environmental Toxicology and Department of Systems Pharmacology and Translational Therapeutics, Perelman School of Medicine, University of Pennsylvania, Philadelphia, PA 19104, USA – sequence: 6 givenname: Matthew H surname: Levine fullname: Levine, Matthew H organization: Department of Surgery, Penn Transplant Institute, Perelman School of Medicine, Children's Hospital of Philadelphia and University of Pennsylvania, Philadelphia, PA 19104, USA – sequence: 7 givenname: Zhonglin surname: Wang fullname: Wang, Zhonglin organization: Department of Surgery, Penn Transplant Institute, Perelman School of Medicine, Children's Hospital of Philadelphia and University of Pennsylvania, Philadelphia, PA 19104, USA – sequence: 8 givenname: William J surname: Quinn, 3rd fullname: Quinn, 3rd, William J organization: Department of Physiology and Institute of Diabetes, Obesity, and Metabolism, University of Pennsylvania, Philadelphia, PA 19104, USA – sequence: 9 givenname: Piotr K surname: Kopinski fullname: Kopinski, Piotr K organization: Center for Mitochondrial and Epigenomic Medicine, Children's Hospital of Philadelphia, Philadelphia, PA 19104, USA; Howard Hughes Medical Institute, Perelman School of Medicine, University of Pennsylvania, Philadelphia, PA 19104, USA – sequence: 10 givenname: Liqing surname: Wang fullname: Wang, Liqing organization: Division of Transplant Immunology, Department of Pathology and Laboratory Medicine, and Biesecker Center for Pediatric Liver Disease, Children's Hospital of Philadelphia and University of Pennsylvania, Philadelphia, PA 19104, USA – sequence: 11 givenname: Tatiana surname: Akimova fullname: Akimova, Tatiana organization: Division of Transplant Immunology, Department of Pathology and Laboratory Medicine, and Biesecker Center for Pediatric Liver Disease, Children's Hospital of Philadelphia and University of Pennsylvania, Philadelphia, PA 19104, USA – sequence: 12 givenname: Yujie surname: Liu fullname: Liu, Yujie organization: Division of Transplant Immunology, Department of Pathology and Laboratory Medicine, and Biesecker Center for Pediatric Liver Disease, Children's Hospital of Philadelphia and University of Pennsylvania, Philadelphia, PA 19104, USA – sequence: 13 givenname: Tricia R surname: Bhatti fullname: Bhatti, Tricia R organization: Division of Transplant Immunology, Department of Pathology and Laboratory Medicine, and Biesecker Center for Pediatric Liver Disease, Children's Hospital of Philadelphia and University of Pennsylvania, Philadelphia, PA 19104, USA – sequence: 14 givenname: Rongxiang surname: Han fullname: Han, Rongxiang organization: Division of Transplant Immunology, Department of Pathology and Laboratory Medicine, and Biesecker Center for Pediatric Liver Disease, Children's Hospital of Philadelphia and University of Pennsylvania, Philadelphia, PA 19104, USA – sequence: 15 givenname: Benjamin L surname: Laskin fullname: Laskin, Benjamin L organization: Division of Nephrology and Department of Pediatrics, Children's Hospital of Philadelphia and University of Pennsylvania, Philadelphia, PA 19104, USA – sequence: 16 givenname: Joseph A surname: Baur fullname: Baur, Joseph A organization: Department of Physiology and Institute of Diabetes, Obesity, and Metabolism, University of Pennsylvania, Philadelphia, PA 19104, USA – sequence: 17 givenname: Ian A surname: Blair fullname: Blair, Ian A organization: Penn SRP Center, Center of Excellence in Environmental Toxicology and Department of Systems Pharmacology and Translational Therapeutics, Perelman School of Medicine, University of Pennsylvania, Philadelphia, PA 19104, USA – sequence: 18 givenname: Douglas C surname: Wallace fullname: Wallace, Douglas C organization: Center for Mitochondrial and Epigenomic Medicine, Children's Hospital of Philadelphia, Philadelphia, PA 19104, USA; Department of Pathology and Laboratory Medicine, University of Pennsylvania, Philadelphia, PA 19104, USA – sequence: 19 givenname: Wayne W surname: Hancock fullname: Hancock, Wayne W organization: Division of Transplant Immunology, Department of Pathology and Laboratory Medicine, and Biesecker Center for Pediatric Liver Disease, Children's Hospital of Philadelphia and University of Pennsylvania, Philadelphia, PA 19104, USA – sequence: 20 givenname: Ulf H surname: Beier fullname: Beier, Ulf H email: beieru@email.chop.edu organization: Division of Nephrology and Department of Pediatrics, Children's Hospital of Philadelphia and University of Pennsylvania, Philadelphia, PA 19104, USA. Electronic address: beieru@email.chop.edu
BackLink	https://www.ncbi.nlm.nih.gov/pubmed/28416194$$D View this record in MEDLINE/PubMed
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SubjectTerms	Animals Cell Line Cellular Microenvironment - genetics Cellular Microenvironment - immunology Cellular Reprogramming - genetics Cellular Reprogramming - immunology Forkhead Transcription Factors - genetics Forkhead Transcription Factors - immunology Glucose - genetics Glucose - immunology Glycolysis - genetics Glycolysis - immunology Humans Lactic Acid - immunology Mice Mice, Inbred BALB C Mice, Knockout Oxidative Phosphorylation Proto-Oncogene Proteins c-myc - genetics Proto-Oncogene Proteins c-myc - immunology T-Lymphocytes, Regulatory - immunology
Title	Foxp3 Reprograms T Cell Metabolism to Function in Low-Glucose, High-Lactate Environments
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