Cell-Intrinsic Glycogen Metabolism Supports Early Glycolytic Reprogramming Required for Dendritic Cell Immune Responses

Dendritic cell (DC) activation by Toll-like receptor (TLR) agonists causes rapid glycolytic reprogramming that is required to meet the metabolic demands of their immune activation. Recent efforts in the field have identified an important role for extracellular glucose sourcing to support DC activati...

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Published in:	Cell metabolism Vol. 26; no. 3; p. 558
Main Authors:	Thwe, Phyu M, Pelgrom, Leonard R, Cooper, Rachel, Beauchamp, Saritha, Reisz, Julie A, D'Alessandro, Angelo, Everts, Bart, Amiel, Eyal
Format:	Journal Article
Language:	English
Published:	United States 05.09.2017
Subjects:	Animals Cell Differentiation - drug effects Cell Respiration - drug effects Cell Survival - drug effects Cellular Reprogramming - drug effects Dendritic Cells - cytology Dendritic Cells - drug effects Dendritic Cells - immunology Dendritic Cells - ultrastructure Glycogen - metabolism Glycogen Phosphorylase - antagonists & inhibitors Glycogen Phosphorylase - metabolism Glycolysis - drug effects Hypoglycemia - pathology Lipopolysaccharides - pharmacology Mice Mitochondria - drug effects Mitochondria - metabolism dendritic cells glycogen glycogenolysis glycogen shunt glycolysis PYG
ISSN:	1932-7420, 1932-7420
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Abstract	Dendritic cell (DC) activation by Toll-like receptor (TLR) agonists causes rapid glycolytic reprogramming that is required to meet the metabolic demands of their immune activation. Recent efforts in the field have identified an important role for extracellular glucose sourcing to support DC activation. However, the contributions of intracellular glucose stores to these processes have not been well characterized. We demonstrate that DCs possess intracellular glycogen stores and that cell-intrinsic glycogen metabolism supports the early effector functions of TLR-activated DCs. Inhibition of glycogenolysis significantly attenuates TLR-mediated DC maturation and impairs their ability to initiate lymphocyte activation. We further report that DCs exhibit functional compartmentalization of glucose- and glycogen-derived carbons, where these substrates preferentially contribute to distinct metabolic pathways. This work provides novel insights into nutrient homeostasis in DCs, demonstrating that differential utilization of glycogen and glucose metabolism regulates their optimal immune function.
AbstractList	Dendritic cell (DC) activation by Toll-like receptor (TLR) agonists causes rapid glycolytic reprogramming that is required to meet the metabolic demands of their immune activation. Recent efforts in the field have identified an important role for extracellular glucose sourcing to support DC activation. However, the contributions of intracellular glucose stores to these processes have not been well characterized. We demonstrate that DCs possess intracellular glycogen stores and that cell-intrinsic glycogen metabolism supports the early effector functions of TLR-activated DCs. Inhibition of glycogenolysis significantly attenuates TLR-mediated DC maturation and impairs their ability to initiate lymphocyte activation. We further report that DCs exhibit functional compartmentalization of glucose- and glycogen-derived carbons, where these substrates preferentially contribute to distinct metabolic pathways. This work provides novel insights into nutrient homeostasis in DCs, demonstrating that differential utilization of glycogen and glucose metabolism regulates their optimal immune function.Dendritic cell (DC) activation by Toll-like receptor (TLR) agonists causes rapid glycolytic reprogramming that is required to meet the metabolic demands of their immune activation. Recent efforts in the field have identified an important role for extracellular glucose sourcing to support DC activation. However, the contributions of intracellular glucose stores to these processes have not been well characterized. We demonstrate that DCs possess intracellular glycogen stores and that cell-intrinsic glycogen metabolism supports the early effector functions of TLR-activated DCs. Inhibition of glycogenolysis significantly attenuates TLR-mediated DC maturation and impairs their ability to initiate lymphocyte activation. We further report that DCs exhibit functional compartmentalization of glucose- and glycogen-derived carbons, where these substrates preferentially contribute to distinct metabolic pathways. This work provides novel insights into nutrient homeostasis in DCs, demonstrating that differential utilization of glycogen and glucose metabolism regulates their optimal immune function. Dendritic cell (DC) activation by Toll-like receptor (TLR) agonists causes rapid glycolytic reprogramming that is required to meet the metabolic demands of their immune activation. Recent efforts in the field have identified an important role for extracellular glucose sourcing to support DC activation. However, the contributions of intracellular glucose stores to these processes have not been well characterized. We demonstrate that DCs possess intracellular glycogen stores and that cell-intrinsic glycogen metabolism supports the early effector functions of TLR-activated DCs. Inhibition of glycogenolysis significantly attenuates TLR-mediated DC maturation and impairs their ability to initiate lymphocyte activation. We further report that DCs exhibit functional compartmentalization of glucose- and glycogen-derived carbons, where these substrates preferentially contribute to distinct metabolic pathways. This work provides novel insights into nutrient homeostasis in DCs, demonstrating that differential utilization of glycogen and glucose metabolism regulates their optimal immune function.
Author	Thwe, Phyu M Pelgrom, Leonard R D'Alessandro, Angelo Beauchamp, Saritha Cooper, Rachel Reisz, Julie A Everts, Bart Amiel, Eyal
Author_xml	– sequence: 1 givenname: Phyu M surname: Thwe fullname: Thwe, Phyu M organization: Cell, Molecular, and Biomedical Sciences Program, University of Vermont, Burlington, VT 05405, USA; Department of Medical Laboratory and Radiation Sciences, College of Nursing and Health Sciences, University of Vermont, Burlington, VT 05405, USA – sequence: 2 givenname: Leonard R surname: Pelgrom fullname: Pelgrom, Leonard R organization: Department of Parasitology, Leiden University Medical Center, 2333 ZA Leiden, the Netherlands – sequence: 3 givenname: Rachel surname: Cooper fullname: Cooper, Rachel organization: Department of Medical Laboratory and Radiation Sciences, College of Nursing and Health Sciences, University of Vermont, Burlington, VT 05405, USA – sequence: 4 givenname: Saritha surname: Beauchamp fullname: Beauchamp, Saritha organization: Department of Medical Laboratory and Radiation Sciences, College of Nursing and Health Sciences, University of Vermont, Burlington, VT 05405, USA – sequence: 5 givenname: Julie A surname: Reisz fullname: Reisz, Julie A organization: Department of Biochemistry and Molecular Genetics, University of Colorado Denver - Anschutz Medical Campus, Aurora, CO 80045, USA – sequence: 6 givenname: Angelo surname: D'Alessandro fullname: D'Alessandro, Angelo organization: Department of Biochemistry and Molecular Genetics, University of Colorado Denver - Anschutz Medical Campus, Aurora, CO 80045, USA – sequence: 7 givenname: Bart surname: Everts fullname: Everts, Bart organization: Department of Parasitology, Leiden University Medical Center, 2333 ZA Leiden, the Netherlands – sequence: 8 givenname: Eyal surname: Amiel fullname: Amiel, Eyal email: eyal.amiel@med.uvm.edu organization: Cell, Molecular, and Biomedical Sciences Program, University of Vermont, Burlington, VT 05405, USA; Department of Medical Laboratory and Radiation Sciences, College of Nursing and Health Sciences, University of Vermont, Burlington, VT 05405, USA. Electronic address: eyal.amiel@med.uvm.edu
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SubjectTerms	Animals Cell Differentiation - drug effects Cell Respiration - drug effects Cell Survival - drug effects Cellular Reprogramming - drug effects Dendritic Cells - cytology Dendritic Cells - drug effects Dendritic Cells - immunology Dendritic Cells - ultrastructure Glycogen - metabolism Glycogen Phosphorylase - antagonists & inhibitors Glycogen Phosphorylase - metabolism Glycolysis - drug effects Hypoglycemia - pathology Lipopolysaccharides - pharmacology Mice Mitochondria - drug effects Mitochondria - metabolism
Title	Cell-Intrinsic Glycogen Metabolism Supports Early Glycolytic Reprogramming Required for Dendritic Cell Immune Responses
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