FoxO-Dependent Regulation of Diacylglycerol Kinase α Gene Expression

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Published inMolecular and Cellular Biology Vol. 32; no. 20; pp. 4168 - 4180
Main Authors Martínez-Moreno, Mónica, García-Liévana, Job, Soutar, Denise, Torres-Ayuso, Pedro, Andrada, Elena, Zhong, Xiao-Ping, Koretzky, Gary A., Mérida, Isabel, Ávila-Flores, Antonia
Format Journal Article
LanguageEnglish
Published United States American Society for Microbiology 01.10.2012
Taylor & Francis
Subjects
Animals
Binding Sites
Cell Line
Diacylglycerol Kinase - genetics
Forkhead Box Protein O1
Forkhead Box Protein O3
Forkhead Transcription Factors - metabolism
Gene Expression Regulation, Enzymologic
Humans
Interleukin-2 - pharmacology
Lymphocyte Activation - physiology
Mice
Mice, Inbred BALB C
Mice, Inbred C57BL
Mice, Transgenic
Phosphorylation
Receptors, Interleukin-2
T-Lymphocytes - enzymology
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Diacylglycerol kinase α (DGKα) regulates diacylglycerol levels, catalyzing its conversion into phosphatidic acid. The α isoform is central to immune response regulation; it downmodulates Ras-dependent pathways and is necessary for establishment of the unresponsive state termed anergy. DGKα functions are regulated in part at the transcriptional level although the mechanisms involved remain poorly understood. Here, we analyzed the 5′ end structure of the mouse DGK α gene and detected three binding sites for forkhead box O (FoxO) transcription factors, whose function was confirmed using luciferase reporter constructs. FoxO1 and FoxO3 bound to the 5′ regulatory region of DGKα in quiescent T cells, as well as after interleukin-2 (IL-2) withdrawal in activated T cells. FoxO binding to this region was lost after complete T cell activation or IL-2 addition, events that correlated with FoxO phosphorylation and a sustained decrease in DGKα gene expression. These data strongly support a role for FoxO proteins in promoting high DGKα levels and indicate a mechanism by which DGKα function is downregulated during productive T cell responses. Our study establishes a basis for a causal relationship between DGKα downregulation, IL-2, and anergy avoidance.
Diacylglycerol kinase α (DGKα) regulates diacylglycerol levels, catalyzing its conversion into phosphatidic acid. The α isoform is central to immune response regulation; it downmodulates Ras-dependent pathways and is necessary for establishment of the unresponsive state termed anergy. DGKα functions are regulated in part at the transcriptional level although the mechanisms involved remain poorly understood. Here, we analyzed the 5′ end structure of the mouse DGK α gene and detected three binding sites for forkhead box O (FoxO) transcription factors, whose function was confirmed using luciferase reporter constructs. FoxO1 and FoxO3 bound to the 5′ regulatory region of DGKα in quiescent T cells, as well as after interleukin-2 (IL-2) withdrawal in activated T cells. FoxO binding to this region was lost after complete T cell activation or IL-2 addition, events that correlated with FoxO phosphorylation and a sustained decrease in DGKα gene expression. These data strongly support a role for FoxO proteins in promoting high DGKα levels and indicate a mechanism by which DGKα function is downregulated during productive T cell responses. Our study establishes a basis for a causal relationship between DGKα downregulation, IL-2, and anergy avoidance.
Diacylglycerol kinase α (DGKα) regulates diacylglycerol levels, catalyzing its conversion into phosphatidic acid. The α isoform is central to immune response regulation; it downmodulates Ras-dependent pathways and is necessary for establishment of the unresponsive state termed anergy. DGKα functions are regulated in part at the transcriptional level although the mechanisms involved remain poorly understood. Here, we analyzed the 5' end structure of the mouse DGKα gene and detected three binding sites for forkhead box O (FoxO) transcription factors, whose function was confirmed using luciferase reporter constructs. FoxO1 and FoxO3 bound to the 5' regulatory region of DGKα in quiescent T cells, as well as after interleukin-2 (IL-2) withdrawal in activated T cells. FoxO binding to this region was lost after complete T cell activation or IL-2 addition, events that correlated with FoxO phosphorylation and a sustained decrease in DGKα gene expression. These data strongly support a role for FoxO proteins in promoting high DGKα levels and indicate a mechanism by which DGKα function is downregulated during productive T cell responses. Our study establishes a basis for a causal relationship between DGKα downregulation, IL-2, and anergy avoidance.
Author Job García-Liévana
Antonia Ávila-Flores
Gary A. Koretzky
Xiao-Ping Zhong
Mónica Martínez-Moreno
Denise Soutar
Pedro Torres-Ayuso
Elena Andrada
Isabel Mérida
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Snippet Article Usage Stats Services MCB Citing Articles Google Scholar PubMed Related Content Social Bookmarking CiteULike Delicious Digg Facebook Google+ Mendeley...
Diacylglycerol kinase α (DGKα) regulates diacylglycerol levels, catalyzing its conversion into phosphatidic acid. The α isoform is central to immune response...
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StartPage 4168
SubjectTerms Animals
Binding Sites
Cell Line
Diacylglycerol Kinase - genetics
Forkhead Box Protein O1
Forkhead Box Protein O3
Forkhead Transcription Factors - metabolism
Gene Expression Regulation, Enzymologic
Humans
Interleukin-2 - pharmacology
Lymphocyte Activation - physiology
Mice
Mice, Inbred BALB C
Mice, Inbred C57BL
Mice, Transgenic
Phosphorylation
Receptors, Interleukin-2
T-Lymphocytes - enzymology
Title FoxO-Dependent Regulation of Diacylglycerol Kinase α Gene Expression
URI http://mcb.asm.org/content/32/20/4168.abstract
https://www.tandfonline.com/doi/abs/10.1128/MCB.00654-12
https://www.ncbi.nlm.nih.gov/pubmed/22890845
https://search.proquest.com/docview/1080883169
https://pubmed.ncbi.nlm.nih.gov/PMC3457341
Volume 32
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