Deciphering the role of protein kinase A in the control of FoxP3 expression in regulatory T cells in health and autoimmunity

The molecular mechanisms that govern differential T cell development from CD4 + CD25 - conventional T (Tconv) into CD4 + CD25 + forkhead-box-P3 + (FoxP3 + ) inducible regulatory T (iTreg) cells remain unclear. Herein, we investigated the relative contribution of protein kinase A (PKA) in this proces...

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Published inScientific reports Vol. 14; no. 1; pp. 17571 - 11
Main Authors Lepore, Maria Teresa, Bruzzaniti, Sara, La Rocca, Claudia, Fusco, Clorinda, Carbone, Fortunata, Mottola, Maria, Zuccarelli, Bruno, Lanzillo, Roberta, Brescia Morra, Vincenzo, Maniscalco, Giorgia Teresa, De Simone, Salvatore, Procaccini, Claudio, Porcellini, Antonio, De Rosa, Veronica, Galgani, Mario, Cassano, Silvana, Matarese, Giuseppe
Format Journal Article
LanguageEnglish
Published London Nature Publishing Group UK 30.07.2024
Nature Publishing Group
Nature Portfolio
Subjects
631/250/38
692/699/375
Autoimmunity
CD25 antigen
CD4 antigen
Cyclic AMP response element-binding protein
Cyclic AMP Response Element-Binding Protein - metabolism
Cyclic AMP-Dependent Protein Kinases - metabolism
Female
Forkhead protein
Forkhead Transcription Factors - genetics
Forkhead Transcription Factors - metabolism
Foxp3 protein
Gene Expression Regulation
Humanities and Social Sciences
Humans
Immunoregulation
Kinases
Lymphocytes T
Male
Molecular modelling
multidisciplinary
Multiple sclerosis
Multiple Sclerosis - immunology
Multiple Sclerosis - metabolism
Phosphorylation
Protein kinase A
Proteins
Science
Science (multidisciplinary)
T-Lymphocytes, Regulatory - immunology
T-Lymphocytes, Regulatory - metabolism
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Abstract The molecular mechanisms that govern differential T cell development from CD4 + CD25 - conventional T (Tconv) into CD4 + CD25 + forkhead-box-P3 + (FoxP3 + ) inducible regulatory T (iTreg) cells remain unclear. Herein, we investigated the relative contribution of protein kinase A (PKA) in this process. Mechanistically, we found that PKA controlled the efficiency of human iTreg cell generation through the expression of different FoxP3 splicing variants containing or not the exon 2. We found that transient PKA inhibition reduced the recruitment of cAMP-responsive element-binding protein (CREB) on regulatory regions of the FoxP3 gene, a condition that is associated with an impaired acquisition of their suppressive capacity in vitro. To corroborate our findings in a human model of autoimmunity, we measured CREB phosphorylation and FoxP3 levels in iTreg cells from treatment-naïve relapsing–remitting (RR)-multiple sclerosis (MS) subjects. Interestingly, both phospho-CREB and FoxP3 induction directly correlated and were significantly reduced in RR-MS patients, suggesting a previously unknown mechanism involved in the induction and function of human iTreg cells.
AbstractList The molecular mechanisms that govern differential T cell development from CD4+CD25-conventional T (Tconv) into CD4+CD25+ forkhead-box-P3+ (FoxP3+) inducible regulatory T (iTreg) cells remain unclear. Herein, we investigated the relative contribution of protein kinase A (PKA) in this process. Mechanistically, we found that PKA controlled the efficiency of human iTreg cell generation through the expression of different FoxP3 splicing variants containing or not the exon 2. We found that transient PKA inhibition reduced the recruitment of cAMP-responsive element-binding protein (CREB) on regulatory regions of the FoxP3 gene, a condition that is associated with an impaired acquisition of their suppressive capacity in vitro. To corroborate our findings in a human model of autoimmunity, we measured CREB phosphorylation and FoxP3 levels in iTreg cells from treatment-naïve relapsing-remitting (RR)-multiple sclerosis (MS) subjects. Interestingly, both phospho-CREB and FoxP3 induction directly correlated and were significantly reduced in RR-MS patients, suggesting a previously unknown mechanism involved in the induction and function of human iTreg cells.The molecular mechanisms that govern differential T cell development from CD4+CD25-conventional T (Tconv) into CD4+CD25+ forkhead-box-P3+ (FoxP3+) inducible regulatory T (iTreg) cells remain unclear. Herein, we investigated the relative contribution of protein kinase A (PKA) in this process. Mechanistically, we found that PKA controlled the efficiency of human iTreg cell generation through the expression of different FoxP3 splicing variants containing or not the exon 2. We found that transient PKA inhibition reduced the recruitment of cAMP-responsive element-binding protein (CREB) on regulatory regions of the FoxP3 gene, a condition that is associated with an impaired acquisition of their suppressive capacity in vitro. To corroborate our findings in a human model of autoimmunity, we measured CREB phosphorylation and FoxP3 levels in iTreg cells from treatment-naïve relapsing-remitting (RR)-multiple sclerosis (MS) subjects. Interestingly, both phospho-CREB and FoxP3 induction directly correlated and were significantly reduced in RR-MS patients, suggesting a previously unknown mechanism involved in the induction and function of human iTreg cells.
The molecular mechanisms that govern differential T cell development from CD4 + CD25 - conventional T (Tconv) into CD4 + CD25 + forkhead-box-P3 + (FoxP3 + ) inducible regulatory T (iTreg) cells remain unclear. Herein, we investigated the relative contribution of protein kinase A (PKA) in this process. Mechanistically, we found that PKA controlled the efficiency of human iTreg cell generation through the expression of different FoxP3 splicing variants containing or not the exon 2. We found that transient PKA inhibition reduced the recruitment of cAMP-responsive element-binding protein (CREB) on regulatory regions of the FoxP3 gene, a condition that is associated with an impaired acquisition of their suppressive capacity in vitro. To corroborate our findings in a human model of autoimmunity, we measured CREB phosphorylation and FoxP3 levels in iTreg cells from treatment-naïve relapsing–remitting (RR)-multiple sclerosis (MS) subjects. Interestingly, both phospho-CREB and FoxP3 induction directly correlated and were significantly reduced in RR-MS patients, suggesting a previously unknown mechanism involved in the induction and function of human iTreg cells.
The molecular mechanisms that govern differential T cell development from CD4+CD25-conventional T (Tconv) into CD4+CD25+ forkhead-box-P3+ (FoxP3+) inducible regulatory T (iTreg) cells remain unclear. Herein, we investigated the relative contribution of protein kinase A (PKA) in this process. Mechanistically, we found that PKA controlled the efficiency of human iTreg cell generation through the expression of different FoxP3 splicing variants containing or not the exon 2. We found that transient PKA inhibition reduced the recruitment of cAMP-responsive element-binding protein (CREB) on regulatory regions of the FoxP3 gene, a condition that is associated with an impaired acquisition of their suppressive capacity in vitro. To corroborate our findings in a human model of autoimmunity, we measured CREB phosphorylation and FoxP3 levels in iTreg cells from treatment-naïve relapsing–remitting (RR)-multiple sclerosis (MS) subjects. Interestingly, both phospho-CREB and FoxP3 induction directly correlated and were significantly reduced in RR-MS patients, suggesting a previously unknown mechanism involved in the induction and function of human iTreg cells.
The molecular mechanisms that govern differential T cell development from CD4 CD25 conventional T (Tconv) into CD4 CD25 forkhead-box-P3 (FoxP3 ) inducible regulatory T (iTreg) cells remain unclear. Herein, we investigated the relative contribution of protein kinase A (PKA) in this process. Mechanistically, we found that PKA controlled the efficiency of human iTreg cell generation through the expression of different FoxP3 splicing variants containing or not the exon 2. We found that transient PKA inhibition reduced the recruitment of cAMP-responsive element-binding protein (CREB) on regulatory regions of the FoxP3 gene, a condition that is associated with an impaired acquisition of their suppressive capacity in vitro. To corroborate our findings in a human model of autoimmunity, we measured CREB phosphorylation and FoxP3 levels in iTreg cells from treatment-naïve relapsing-remitting (RR)-multiple sclerosis (MS) subjects. Interestingly, both phospho-CREB and FoxP3 induction directly correlated and were significantly reduced in RR-MS patients, suggesting a previously unknown mechanism involved in the induction and function of human iTreg cells.
Abstract The molecular mechanisms that govern differential T cell development from CD4+CD25-conventional T (Tconv) into CD4+CD25+ forkhead-box-P3+ (FoxP3+) inducible regulatory T (iTreg) cells remain unclear. Herein, we investigated the relative contribution of protein kinase A (PKA) in this process. Mechanistically, we found that PKA controlled the efficiency of human iTreg cell generation through the expression of different FoxP3 splicing variants containing or not the exon 2. We found that transient PKA inhibition reduced the recruitment of cAMP-responsive element-binding protein (CREB) on regulatory regions of the FoxP3 gene, a condition that is associated with an impaired acquisition of their suppressive capacity in vitro. To corroborate our findings in a human model of autoimmunity, we measured CREB phosphorylation and FoxP3 levels in iTreg cells from treatment-naïve relapsing–remitting (RR)-multiple sclerosis (MS) subjects. Interestingly, both phospho-CREB and FoxP3 induction directly correlated and were significantly reduced in RR-MS patients, suggesting a previously unknown mechanism involved in the induction and function of human iTreg cells.
ArticleNumber 17571
Author Carbone, Fortunata
Fusco, Clorinda
Cassano, Silvana
Galgani, Mario
Brescia Morra, Vincenzo
Mottola, Maria
La Rocca, Claudia
Porcellini, Antonio
De Rosa, Veronica
Matarese, Giuseppe
Lepore, Maria Teresa
De Simone, Salvatore
Lanzillo, Roberta
Bruzzaniti, Sara
Zuccarelli, Bruno
Maniscalco, Giorgia Teresa
Procaccini, Claudio
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BackLink https://www.ncbi.nlm.nih.gov/pubmed/39080325$$D View this record in MEDLINE/PubMed
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Snippet The molecular mechanisms that govern differential T cell development from CD4 + CD25 - conventional T (Tconv) into CD4 + CD25 + forkhead-box-P3 + (FoxP3 + )...
The molecular mechanisms that govern differential T cell development from CD4 CD25 conventional T (Tconv) into CD4 CD25 forkhead-box-P3 (FoxP3 ) inducible...
The molecular mechanisms that govern differential T cell development from CD4+CD25-conventional T (Tconv) into CD4+CD25+ forkhead-box-P3+ (FoxP3+) inducible...
Abstract The molecular mechanisms that govern differential T cell development from CD4+CD25-conventional T (Tconv) into CD4+CD25+ forkhead-box-P3+ (FoxP3+)...
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SubjectTerms 631/250/38
692/699/375
Autoimmunity
CD25 antigen
CD4 antigen
Cyclic AMP response element-binding protein
Cyclic AMP Response Element-Binding Protein - metabolism
Cyclic AMP-Dependent Protein Kinases - metabolism
Female
Forkhead protein
Forkhead Transcription Factors - genetics
Forkhead Transcription Factors - metabolism
Foxp3 protein
Gene Expression Regulation
Humanities and Social Sciences
Humans
Immunoregulation
Kinases
Lymphocytes T
Male
Molecular modelling
multidisciplinary
Multiple sclerosis
Multiple Sclerosis - immunology
Multiple Sclerosis - metabolism
Phosphorylation
Protein kinase A
Proteins
Science
Science (multidisciplinary)
T-Lymphocytes, Regulatory - immunology
T-Lymphocytes, Regulatory - metabolism
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Title Deciphering the role of protein kinase A in the control of FoxP3 expression in regulatory T cells in health and autoimmunity
URI https://link.springer.com/article/10.1038/s41598-024-68098-z
https://www.ncbi.nlm.nih.gov/pubmed/39080325
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https://pubmed.ncbi.nlm.nih.gov/PMC11289137
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Volume 14
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