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PMID: 24315998 Published · ppublish English Journal Article Research Support, N.I.H., Extramural Research Support, Non-U.S. Gov't

T cell exit from quiescence and differentiation into Th2 cells depend on Raptor-mTORC1-mediated metabolic reprogramming.

Immunity ·Vol. 39 ·No. 6 ·2013-12-12 ·Pages 1043-56

Yang K, Shrestha S, Zeng H, Karmaus PW, Neale G, Vogel P, Guertin DA, Lamb RF, Chi H

Abstract

Naive T cells respond to antigen stimulation by exiting from quiescence and initiating clonal expansion and functional differentiation, but the control mechanism is elusive. Here we describe that Raptor-mTORC1-dependent metabolic reprogramming is a central determinant of this transitional process. Loss of Raptor abrogated T cell priming and T helper 2 (Th2) cell differentiation, although Raptor function is less important for continuous proliferation of actively cycling cells. mTORC1 coordinated multiple metabolic programs in T cells including glycolysis, lipid synthesis, and oxidative phosphorylation to mediate antigen-triggered exit from quiescence. mTORC1 further linked glucose metabolism to the initiation of Th2 cell differentiation by orchestrating cytokine receptor expression and cytokine responsiveness. Activation of Raptor-mTORC1 integrated T cell receptor and CD28 costimulatory signals in antigen-stimulated T cells. Our studies identify a Raptor-mTORC1-dependent pathway linking signal-dependent metabolic reprogramming to quiescence exit, and this in turn coordinates lymphocyte activation and fate decisions in adaptive immunity.

MeSH Terms
Adaptor Proteins, Signal Transducing/genetics,metabolism Animals Cell Cycle Cell Differentiation Cell Proliferation Cells, Cultured Cytokines/metabolism Gene Deletion Glucose/metabolism Lymphocyte Activation/physiology Mice Mice, Inbred C57BL Regulatory-Associated Protein of mTOR Signal Transduction T-Lymphocytes/cytology,immunology TOR Serine-Threonine Kinases/genetics,metabolism Th2 Cells/cytology
Chemicals
Adaptor Proteins, Signal Transducing Cytokines Regulatory-Associated Protein of mTOR Rptor protein, mouse TOR Serine-Threonine Kinases Glucose
Authors & Affiliations
9 authors, click to expand affiliations / ORCID
Yang Kai
Department of Immunology, St. Jude Children's Research Hospital, Memphis, TN 38105, USA.
Shrestha Sharad
Department of Immunology, St. Jude Children's Research Hospital, Memphis, TN 38105, USA.
Zeng Hu
Department of Immunology, St. Jude Children's Research Hospital, Memphis, TN 38105, USA.
Karmaus Peer W F
Department of Immunology, St. Jude Children's Research Hospital, Memphis, TN 38105, USA.
Neale Geoffrey
Hartwell Center for Bioinformatics and Biotechnology, St. Jude Children's Research Hospital, Memphis, TN 38105, USA.
Vogel Peter
Department of Pathology, St. Jude Children's Research Hospital, Memphis, TN 38105, USA.
Guertin David A
Program in Molecular Medicine, University of Massachusetts Medical School, Worcester, MA 01605, USA.
Lamb Richard F
University of Liverpool Cancer Research UK Centre, 200 London Road, Liverpool L3 9TA, UK.
Chi Hongbo
Department of Immunology, St. Jude Children's Research Hospital, Memphis, TN 38105, USA. Electronic address: hongbo.chi@stjude.org.
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Article Info
Journal
Immunity
Abbr.
Immunity
ISSN
1097-4180
Published
2013-12-12
Epub
2013-00-05
Pages
1043-56
Language
English
Region
United States
NLM ID
9432918
PMCID
PMC3986063
Subset
IM
Grants
NCI NIH HHS · P30 CA021765 · United States
NIAID NIH HHS · R01 AI101407 · United States
NINDS NIH HHS · R01 NS064599 · United States
NIAID NIH HHS · R21 AI094089 · United States
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GEO
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