The Transcription Factor Myc Controls Metabolic Reprogramming upon T Lymphocyte Activation
To fulfill the bioenergetic and biosynthetic demand of proliferation, T cells reprogram their metabolic pathways from fatty acid β-oxidation and pyruvate oxidation via the TCA cycle to the glycolytic, pentose-phosphate, and glutaminolytic pathways. Two of the top-ranked candidate transcription facto...
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Veröffentlicht in: | Immunity (Cambridge, Mass.) Mass.), 2011-12, Vol.35 (6), p.871-882 |
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creator | Wang, Ruoning Dillon, Christopher P. Shi, Lewis Zhichang Milasta, Sandra Carter, Robert Finkelstein, David McCormick, Laura L. Fitzgerald, Patrick Chi, Hongbo Munger, Joshua Green, Douglas R. |
description | To fulfill the bioenergetic and biosynthetic demand of proliferation, T cells reprogram their metabolic pathways from fatty acid β-oxidation and pyruvate oxidation via the TCA cycle to the glycolytic, pentose-phosphate, and glutaminolytic pathways. Two of the top-ranked candidate transcription factors potentially responsible for the activation-induced T cell metabolic transcriptome, HIF1α and Myc, were induced upon T cell activation, but only the acute deletion of Myc markedly inhibited activation-induced glycolysis and glutaminolysis in T cells. Glutamine deprivation compromised activation-induced T cell growth and proliferation, and this was partially replaced by nucleotides and polyamines, implicating glutamine as an important source for biosynthetic precursors in active T cells. Metabolic tracer analysis revealed a Myc-dependent metabolic pathway linking glutaminolysis to the biosynthesis of polyamines. Therefore, a Myc-dependent global metabolic transcriptome drives metabolic reprogramming in activated, primary T lymphocytes. This may represent a general mechanism for metabolic reprogramming under patho-physiological conditions.
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► T cell activation drives the transcription of a distinct set of metabolic genes ► Myc is required for activation-induced metabolic reprogramming ► HIF1 is not required for activation-induced metabolic reprogramming ► Myc-driven glutaminolysis fuels polyamine biosynthesis upon T cell activation |
doi_str_mv | 10.1016/j.immuni.2011.09.021 |
format | Article |
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► T cell activation drives the transcription of a distinct set of metabolic genes ► Myc is required for activation-induced metabolic reprogramming ► HIF1 is not required for activation-induced metabolic reprogramming ► Myc-driven glutaminolysis fuels polyamine biosynthesis upon T cell activation</description><identifier>ISSN: 1074-7613</identifier><identifier>EISSN: 1097-4180</identifier><identifier>DOI: 10.1016/j.immuni.2011.09.021</identifier><identifier>PMID: 22195744</identifier><language>eng</language><publisher>United States: Elsevier Inc</publisher><subject>Animals ; Bioenergetics ; Cell activation ; Cell cycle ; Cell growth ; Cell proliferation ; Fatty acids ; Gene expression ; Gene Expression Regulation ; Glucose - metabolism ; Glutamine ; Glutamine - metabolism ; Glycolysis ; Hypoxia-Inducible Factor 1, alpha Subunit - metabolism ; Kinases ; Lymphocyte Activation - genetics ; Lymphocytes T ; Metabolic Networks and Pathways - genetics ; Metabolic pathways ; Metabolites ; Mice ; Mice, Inbred C57BL ; Mice, Knockout ; Myc protein ; Nucleotides ; Ornithine - metabolism ; Oxidation ; polyamines ; Polyamines - metabolism ; Proto-Oncogene Proteins c-myc - genetics ; Proto-Oncogene Proteins c-myc - metabolism ; Pyruvic acid ; T-Lymphocytes - immunology ; T-Lymphocytes - metabolism ; TOR Serine-Threonine Kinases - metabolism ; Tracers ; Transcription factors ; Transcriptome ; Tricarboxylic acid cycle</subject><ispartof>Immunity (Cambridge, Mass.), 2011-12, Vol.35 (6), p.871-882</ispartof><rights>2011 Elsevier Inc.</rights><rights>Copyright © 2011 Elsevier Inc. All rights reserved.</rights><rights>Copyright Elsevier Limited Dec 23, 2011</rights><rights>2011 Elsevier Inc. All rights reserved. 2011</rights><lds50>peer_reviewed</lds50><oa>free_for_read</oa><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-c523t-52e1ec90cd561cb52be2857cd2a9bc0f002abeb27062c2e806a4bf875f8cfb063</citedby><cites>FETCH-LOGICAL-c523t-52e1ec90cd561cb52be2857cd2a9bc0f002abeb27062c2e806a4bf875f8cfb063</cites></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Tsyndetics_thumb_exl</thumbnail><linktohtml>$$Uhttps://www.sciencedirect.com/science/article/pii/S1074761311005152$$EHTML$$P50$$Gelsevier$$Hfree_for_read</linktohtml><link.rule.ids>230,314,776,780,881,3537,27901,27902,65306</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/22195744$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink></links><search><creatorcontrib>Wang, Ruoning</creatorcontrib><creatorcontrib>Dillon, Christopher P.</creatorcontrib><creatorcontrib>Shi, Lewis Zhichang</creatorcontrib><creatorcontrib>Milasta, Sandra</creatorcontrib><creatorcontrib>Carter, Robert</creatorcontrib><creatorcontrib>Finkelstein, David</creatorcontrib><creatorcontrib>McCormick, Laura L.</creatorcontrib><creatorcontrib>Fitzgerald, Patrick</creatorcontrib><creatorcontrib>Chi, Hongbo</creatorcontrib><creatorcontrib>Munger, Joshua</creatorcontrib><creatorcontrib>Green, Douglas R.</creatorcontrib><title>The Transcription Factor Myc Controls Metabolic Reprogramming upon T Lymphocyte Activation</title><title>Immunity (Cambridge, Mass.)</title><addtitle>Immunity</addtitle><description>To fulfill the bioenergetic and biosynthetic demand of proliferation, T cells reprogram their metabolic pathways from fatty acid β-oxidation and pyruvate oxidation via the TCA cycle to the glycolytic, pentose-phosphate, and glutaminolytic pathways. Two of the top-ranked candidate transcription factors potentially responsible for the activation-induced T cell metabolic transcriptome, HIF1α and Myc, were induced upon T cell activation, but only the acute deletion of Myc markedly inhibited activation-induced glycolysis and glutaminolysis in T cells. Glutamine deprivation compromised activation-induced T cell growth and proliferation, and this was partially replaced by nucleotides and polyamines, implicating glutamine as an important source for biosynthetic precursors in active T cells. Metabolic tracer analysis revealed a Myc-dependent metabolic pathway linking glutaminolysis to the biosynthesis of polyamines. Therefore, a Myc-dependent global metabolic transcriptome drives metabolic reprogramming in activated, primary T lymphocytes. This may represent a general mechanism for metabolic reprogramming under patho-physiological conditions.
[Display omitted]
► T cell activation drives the transcription of a distinct set of metabolic genes ► Myc is required for activation-induced metabolic reprogramming ► HIF1 is not required for activation-induced metabolic reprogramming ► Myc-driven glutaminolysis fuels polyamine biosynthesis upon T cell activation</description><subject>Animals</subject><subject>Bioenergetics</subject><subject>Cell activation</subject><subject>Cell cycle</subject><subject>Cell growth</subject><subject>Cell proliferation</subject><subject>Fatty acids</subject><subject>Gene expression</subject><subject>Gene Expression Regulation</subject><subject>Glucose - metabolism</subject><subject>Glutamine</subject><subject>Glutamine - metabolism</subject><subject>Glycolysis</subject><subject>Hypoxia-Inducible Factor 1, alpha Subunit - metabolism</subject><subject>Kinases</subject><subject>Lymphocyte Activation - genetics</subject><subject>Lymphocytes T</subject><subject>Metabolic Networks and Pathways - genetics</subject><subject>Metabolic pathways</subject><subject>Metabolites</subject><subject>Mice</subject><subject>Mice, Inbred C57BL</subject><subject>Mice, Knockout</subject><subject>Myc protein</subject><subject>Nucleotides</subject><subject>Ornithine - metabolism</subject><subject>Oxidation</subject><subject>polyamines</subject><subject>Polyamines - metabolism</subject><subject>Proto-Oncogene Proteins c-myc - genetics</subject><subject>Proto-Oncogene Proteins c-myc - metabolism</subject><subject>Pyruvic acid</subject><subject>T-Lymphocytes - immunology</subject><subject>T-Lymphocytes - metabolism</subject><subject>TOR Serine-Threonine Kinases - metabolism</subject><subject>Tracers</subject><subject>Transcription factors</subject><subject>Transcriptome</subject><subject>Tricarboxylic acid cycle</subject><issn>1074-7613</issn><issn>1097-4180</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2011</creationdate><recordtype>article</recordtype><sourceid>EIF</sourceid><recordid>eNp9kV-L1DAUxYMo7jr6DUQKPqwvrTdp0jQvwjK47sIsgowvvoQ0vZ3J0DY1aQfm29sy6_rnYZ8SyD0n554fIW8pZBRo8fGQua6bepcxoDQDlQGjz8glBSVTTkt4vtwlT2VB8wvyKsYDAOVCwUtywRhVQnJ-SX5s95hsg-mjDW4Yne-TG2NHH5L7k03Wvh-Db2Nyj6OpfOts8g2H4HfBdJ3rd8k0zIJtsjl1w97b04jJtR3d0SxGr8mLxrQR3zycK_L95vN2fZtuvn65W19vUitYPqaCIUWrwNaioLYSrEJWCmlrZlRloQFgpsKKSSiYZVhCYXjVlFI0pW0qKPIV-XT2Haaqw9rinNm0egiuM-GkvXH635fe7fXOH3XOeClVORtcPRgE_3PCOOrORYtta3r0U9SKMqkkn9OuyIcnJykwJgoh6JLq_X-jBz-Ffi5CUwGcFSqfwawIP0_Z4GMM2DzGpqAXzPqgz5j1glmD0jPmWfbu75UfRb-5_ukE5-KPDoOO1mFvsXYB7ahr757-4RcjTbyD</recordid><startdate>20111223</startdate><enddate>20111223</enddate><creator>Wang, Ruoning</creator><creator>Dillon, Christopher P.</creator><creator>Shi, Lewis Zhichang</creator><creator>Milasta, Sandra</creator><creator>Carter, Robert</creator><creator>Finkelstein, David</creator><creator>McCormick, Laura L.</creator><creator>Fitzgerald, Patrick</creator><creator>Chi, Hongbo</creator><creator>Munger, Joshua</creator><creator>Green, Douglas R.</creator><general>Elsevier Inc</general><general>Elsevier Limited</general><scope>6I.</scope><scope>AAFTH</scope><scope>CGR</scope><scope>CUY</scope><scope>CVF</scope><scope>ECM</scope><scope>EIF</scope><scope>NPM</scope><scope>AAYXX</scope><scope>CITATION</scope><scope>7QL</scope><scope>7QP</scope><scope>7QR</scope><scope>7T5</scope><scope>7T7</scope><scope>7TK</scope><scope>7TM</scope><scope>7U9</scope><scope>8FD</scope><scope>C1K</scope><scope>FR3</scope><scope>H94</scope><scope>K9.</scope><scope>M7N</scope><scope>NAPCQ</scope><scope>P64</scope><scope>RC3</scope><scope>7X8</scope><scope>5PM</scope></search><sort><creationdate>20111223</creationdate><title>The Transcription Factor Myc Controls Metabolic Reprogramming upon T Lymphocyte Activation</title><author>Wang, Ruoning ; Dillon, Christopher P. ; Shi, Lewis Zhichang ; Milasta, Sandra ; Carter, Robert ; Finkelstein, David ; McCormick, Laura L. ; Fitzgerald, Patrick ; Chi, Hongbo ; Munger, Joshua ; Green, Douglas R.</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c523t-52e1ec90cd561cb52be2857cd2a9bc0f002abeb27062c2e806a4bf875f8cfb063</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2011</creationdate><topic>Animals</topic><topic>Bioenergetics</topic><topic>Cell activation</topic><topic>Cell cycle</topic><topic>Cell growth</topic><topic>Cell proliferation</topic><topic>Fatty acids</topic><topic>Gene expression</topic><topic>Gene Expression Regulation</topic><topic>Glucose - metabolism</topic><topic>Glutamine</topic><topic>Glutamine - metabolism</topic><topic>Glycolysis</topic><topic>Hypoxia-Inducible Factor 1, alpha Subunit - metabolism</topic><topic>Kinases</topic><topic>Lymphocyte Activation - genetics</topic><topic>Lymphocytes T</topic><topic>Metabolic Networks and Pathways - genetics</topic><topic>Metabolic pathways</topic><topic>Metabolites</topic><topic>Mice</topic><topic>Mice, Inbred C57BL</topic><topic>Mice, Knockout</topic><topic>Myc protein</topic><topic>Nucleotides</topic><topic>Ornithine - metabolism</topic><topic>Oxidation</topic><topic>polyamines</topic><topic>Polyamines - metabolism</topic><topic>Proto-Oncogene Proteins c-myc - genetics</topic><topic>Proto-Oncogene Proteins c-myc - metabolism</topic><topic>Pyruvic acid</topic><topic>T-Lymphocytes - immunology</topic><topic>T-Lymphocytes - metabolism</topic><topic>TOR Serine-Threonine Kinases - metabolism</topic><topic>Tracers</topic><topic>Transcription factors</topic><topic>Transcriptome</topic><topic>Tricarboxylic acid cycle</topic><toplevel>peer_reviewed</toplevel><toplevel>online_resources</toplevel><creatorcontrib>Wang, Ruoning</creatorcontrib><creatorcontrib>Dillon, Christopher P.</creatorcontrib><creatorcontrib>Shi, Lewis Zhichang</creatorcontrib><creatorcontrib>Milasta, Sandra</creatorcontrib><creatorcontrib>Carter, Robert</creatorcontrib><creatorcontrib>Finkelstein, David</creatorcontrib><creatorcontrib>McCormick, Laura L.</creatorcontrib><creatorcontrib>Fitzgerald, Patrick</creatorcontrib><creatorcontrib>Chi, Hongbo</creatorcontrib><creatorcontrib>Munger, Joshua</creatorcontrib><creatorcontrib>Green, Douglas R.</creatorcontrib><collection>ScienceDirect Open Access Titles</collection><collection>Elsevier:ScienceDirect:Open Access</collection><collection>Medline</collection><collection>MEDLINE</collection><collection>MEDLINE (Ovid)</collection><collection>MEDLINE</collection><collection>MEDLINE</collection><collection>PubMed</collection><collection>CrossRef</collection><collection>Bacteriology Abstracts (Microbiology B)</collection><collection>Calcium & Calcified Tissue Abstracts</collection><collection>Chemoreception Abstracts</collection><collection>Immunology Abstracts</collection><collection>Industrial and Applied Microbiology Abstracts (Microbiology A)</collection><collection>Neurosciences Abstracts</collection><collection>Nucleic Acids Abstracts</collection><collection>Virology and AIDS Abstracts</collection><collection>Technology Research Database</collection><collection>Environmental Sciences and Pollution Management</collection><collection>Engineering Research Database</collection><collection>AIDS and Cancer Research Abstracts</collection><collection>ProQuest Health & Medical Complete (Alumni)</collection><collection>Algology Mycology and Protozoology Abstracts (Microbiology C)</collection><collection>Nursing & Allied Health Premium</collection><collection>Biotechnology and BioEngineering Abstracts</collection><collection>Genetics Abstracts</collection><collection>MEDLINE - Academic</collection><collection>PubMed Central (Full Participant titles)</collection><jtitle>Immunity (Cambridge, Mass.)</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>Wang, Ruoning</au><au>Dillon, Christopher P.</au><au>Shi, Lewis Zhichang</au><au>Milasta, Sandra</au><au>Carter, Robert</au><au>Finkelstein, David</au><au>McCormick, Laura L.</au><au>Fitzgerald, Patrick</au><au>Chi, Hongbo</au><au>Munger, Joshua</au><au>Green, Douglas R.</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>The Transcription Factor Myc Controls Metabolic Reprogramming upon T Lymphocyte Activation</atitle><jtitle>Immunity (Cambridge, Mass.)</jtitle><addtitle>Immunity</addtitle><date>2011-12-23</date><risdate>2011</risdate><volume>35</volume><issue>6</issue><spage>871</spage><epage>882</epage><pages>871-882</pages><issn>1074-7613</issn><eissn>1097-4180</eissn><abstract>To fulfill the bioenergetic and biosynthetic demand of proliferation, T cells reprogram their metabolic pathways from fatty acid β-oxidation and pyruvate oxidation via the TCA cycle to the glycolytic, pentose-phosphate, and glutaminolytic pathways. Two of the top-ranked candidate transcription factors potentially responsible for the activation-induced T cell metabolic transcriptome, HIF1α and Myc, were induced upon T cell activation, but only the acute deletion of Myc markedly inhibited activation-induced glycolysis and glutaminolysis in T cells. Glutamine deprivation compromised activation-induced T cell growth and proliferation, and this was partially replaced by nucleotides and polyamines, implicating glutamine as an important source for biosynthetic precursors in active T cells. Metabolic tracer analysis revealed a Myc-dependent metabolic pathway linking glutaminolysis to the biosynthesis of polyamines. Therefore, a Myc-dependent global metabolic transcriptome drives metabolic reprogramming in activated, primary T lymphocytes. This may represent a general mechanism for metabolic reprogramming under patho-physiological conditions.
[Display omitted]
► T cell activation drives the transcription of a distinct set of metabolic genes ► Myc is required for activation-induced metabolic reprogramming ► HIF1 is not required for activation-induced metabolic reprogramming ► Myc-driven glutaminolysis fuels polyamine biosynthesis upon T cell activation</abstract><cop>United States</cop><pub>Elsevier Inc</pub><pmid>22195744</pmid><doi>10.1016/j.immuni.2011.09.021</doi><tpages>12</tpages><oa>free_for_read</oa></addata></record> |
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subjects | Animals Bioenergetics Cell activation Cell cycle Cell growth Cell proliferation Fatty acids Gene expression Gene Expression Regulation Glucose - metabolism Glutamine Glutamine - metabolism Glycolysis Hypoxia-Inducible Factor 1, alpha Subunit - metabolism Kinases Lymphocyte Activation - genetics Lymphocytes T Metabolic Networks and Pathways - genetics Metabolic pathways Metabolites Mice Mice, Inbred C57BL Mice, Knockout Myc protein Nucleotides Ornithine - metabolism Oxidation polyamines Polyamines - metabolism Proto-Oncogene Proteins c-myc - genetics Proto-Oncogene Proteins c-myc - metabolism Pyruvic acid T-Lymphocytes - immunology T-Lymphocytes - metabolism TOR Serine-Threonine Kinases - metabolism Tracers Transcription factors Transcriptome Tricarboxylic acid cycle |
title | The Transcription Factor Myc Controls Metabolic Reprogramming upon T Lymphocyte Activation |
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