RBPJ Controls Development of Pathogenic Th17 Cells by Regulating IL-23 Receptor Expression

Interleukin-17 (IL-17)-producing helper T cells (Th17 cells) play an important role in autoimmune diseases. However, not all Th17 cells induce tissue inflammation or autoimmunity. Th17 cells require IL-23 receptor (IL-23R) signaling to become pathogenic. The transcriptional mechanisms controlling th...

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Published inCell reports (Cambridge) Vol. 16; no. 2; pp. 392 - 404
Main Authors Meyer zu Horste, Gerd, Wu, Chuan, Wang, Chao, Cong, Le, Pawlak, Mathias, Lee, Youjin, Elyaman, Wassim, Xiao, Sheng, Regev, Aviv, Kuchroo, Vijay K.
Format Journal Article
LanguageEnglish
Published United States Elsevier Inc 12.07.2016
Elsevier
Subjects
Animals
Binding Sites
Encephalomyelitis, Autoimmune, Experimental - immunology
Encephalomyelitis, Autoimmune, Experimental - metabolism
Gene Expression
Gene Expression Regulation - immunology
IL-23R
Immunoglobulin J Recombination Signal Sequence-Binding Protein - physiology
Interleukin-10 - biosynthesis
Mice, 129 Strain
Mice, Inbred C57BL
Notch
Nuclear Receptor Subfamily 1, Group F, Member 3 - metabolism
pathogenicity
Promoter Regions, Genetic
Protein Binding
Proto-Oncogene Proteins c-maf - physiology
RBPJ
Receptors, Interleukin - genetics
Receptors, Interleukin - metabolism
Th17 cells
Th17 Cells - metabolism
Transcriptional Activation
pathogenicity
IL-23R
RBPJ
Notch
Th17 cells
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Abstract Interleukin-17 (IL-17)-producing helper T cells (Th17 cells) play an important role in autoimmune diseases. However, not all Th17 cells induce tissue inflammation or autoimmunity. Th17 cells require IL-23 receptor (IL-23R) signaling to become pathogenic. The transcriptional mechanisms controlling the pathogenicity of Th17 cells and IL-23R expression are unknown. Here, we demonstrate that the canonical Notch signaling mediator RBPJ is a key driver of IL-23R expression. In the absence of RBPJ, Th17 cells fail to upregulate IL-23R, lack stability, and do not induce autoimmune tissue inflammation in vivo, whereas overexpression of IL-23R rescues this defect and promotes pathogenicity of RBPJ-deficient Th17 cells. RBPJ binds and trans-activates the Il23r promoter and induces IL-23R expression and represses anti-inflammatory IL-10 production in Th17 cells. We thus find that Notch signaling influences the development of pathogenic and non-pathogenic Th17 cells by reciprocally regulating IL-23R and IL-10 expression. [Display omitted] •RBPJ promotes experimental CNS autoimmunity via the IL-23R•RBPJ-deficient Th17 cells fail to express IL-23R and related transcripts•RBPJ binds and trans-activates the Il23r promoter together with RORγt•RBPJ represses expression of IL-10 in Th17 cells Meyer zu Horste et al. find that RBPJ promotes the pathogenicity of Th17 cells by directly enhancing expression of the interleukin-23 receptor and repressing interleukin-10 production.
AbstractList Interleukin-17 (IL-17)-producing helper T cells (Th17 cells) play an important role in autoimmune diseases. However, not all Th17 cells induce tissue inflammation or autoimmunity. Th17 cells require IL-23 receptor (IL-23R) signaling to become pathogenic. The transcriptional mechanisms controlling the pathogenicity of Th17 cells and IL-23R expression are unknown. Here, we demonstrate that the canonical Notch signaling mediator RBPJ is a key driver of IL-23R expression. In the absence of RBPJ, Th17 cells fail to upregulate IL-23R, lack stability, and do not induce autoimmune tissue inflammation in vivo, whereas overexpression of IL-23R rescues this defect and promotes pathogenicity of RBPJ-deficient Th17 cells. RBPJ binds and trans-activates the Il23r promoter and induces IL-23R expression and represses anti-inflammatory IL-10 production in Th17 cells. We thus find that Notch signaling influences the development of pathogenic and non-pathogenic Th17 cells by reciprocally regulating IL-23R and IL-10 expression.
Interleukin-17 (IL-17)-producing helper T cells (Th17 cells) play an important role in autoimmune diseases. However, not all Th17 cells induce tissue inflammation or autoimmunity. Th17 cells require IL-23 receptor (IL-23R) signaling to become pathogenic. The transcriptional mechanisms controlling the pathogenicity of Th17 cells and IL-23R expression are unknown. Here, we demonstrate that the canonical Notch signaling mediator RBPJ is a key driver of IL-23R expression. In the absence of RBPJ, Th17 cells fail to upregulate IL-23R, lack stability, and do not induce autoimmune tissue inflammation in vivo, whereas overexpression of IL-23R rescues this defect and promotes pathogenicity of RBPJ-deficient Th17 cells. RBPJ binds and trans-activates the Il23r promoter and induces IL-23R expression and represses anti-inflammatory IL-10 production in Th17 cells. We thus find that Notch signaling influences the development of pathogenic and non-pathogenic Th17 cells by reciprocally regulating IL-23R and IL-10 expression.
Interleukin-17 (IL-17)-producing helper T cells (Th17 cells) play an important role in autoimmune diseases. However, not all Th17 cells induce tissue inflammation or autoimmunity. Th17 cells require IL-23 receptor (IL-23R) signaling to become pathogenic. The transcriptional mechanisms controlling the pathogenicity of Th17 cells and IL-23R expression are unknown. Here, we demonstrate that the canonical Notch signaling mediator RBPJ is a key driver of IL-23R expression. In the absence of RBPJ, Th17 cells fail to upregulate IL-23R, lack stability, and do not induce autoimmune tissue inflammation in vivo, whereas overexpression of IL-23R rescues this defect and promotes pathogenicity of RBPJ-deficient Th17 cells. RBPJ binds and trans-activates the Il23r promoter and induces IL-23R expression and represses anti-inflammatory IL-10 production in Th17 cells. We thus find that Notch signaling influences the development of pathogenic and non-pathogenic Th17 cells by reciprocally regulating IL-23R and IL-10 expression. [Display omitted] •RBPJ promotes experimental CNS autoimmunity via the IL-23R•RBPJ-deficient Th17 cells fail to express IL-23R and related transcripts•RBPJ binds and trans-activates the Il23r promoter together with RORγt•RBPJ represses expression of IL-10 in Th17 cells Meyer zu Horste et al. find that RBPJ promotes the pathogenicity of Th17 cells by directly enhancing expression of the interleukin-23 receptor and repressing interleukin-10 production.
Interleukin-17 (IL-17)-producing helper T cells (Th17 cells) play an important role in autoimmune diseases. However, not all Th17 cells induce tissue inflammation or autoimmunity. Th17 cells require IL-23 receptor (IL-23R) signaling to become pathogenic. The transcriptional mechanisms controlling the pathogenicity of Th17 cells and IL-23R expression are unknown. Here, we demonstrate that the canonical Notch signaling mediator RBPJ is a key driver of IL-23R expression. In the absence of RBPJ, Th17 cells fail to upregulate IL-23R, lack stability, and do not induce autoimmune tissue inflammation in vivo, whereas overexpression of IL-23R rescues this defect and promotes pathogenicity of RBPJ-deficient Th17 cells. RBPJ binds and trans-activates the Il23r promoter and induces IL-23R expression and represses anti-inflammatory IL-10 production in Th17 cells. We thus find that Notch signaling influences the development of pathogenic and non-pathogenic Th17 cells by reciprocally regulating IL-23R and IL-10 expression.Interleukin-17 (IL-17)-producing helper T cells (Th17 cells) play an important role in autoimmune diseases. However, not all Th17 cells induce tissue inflammation or autoimmunity. Th17 cells require IL-23 receptor (IL-23R) signaling to become pathogenic. The transcriptional mechanisms controlling the pathogenicity of Th17 cells and IL-23R expression are unknown. Here, we demonstrate that the canonical Notch signaling mediator RBPJ is a key driver of IL-23R expression. In the absence of RBPJ, Th17 cells fail to upregulate IL-23R, lack stability, and do not induce autoimmune tissue inflammation in vivo, whereas overexpression of IL-23R rescues this defect and promotes pathogenicity of RBPJ-deficient Th17 cells. RBPJ binds and trans-activates the Il23r promoter and induces IL-23R expression and represses anti-inflammatory IL-10 production in Th17 cells. We thus find that Notch signaling influences the development of pathogenic and non-pathogenic Th17 cells by reciprocally regulating IL-23R and IL-10 expression.
Author Wu, Chuan
Wang, Chao
Cong, Le
Elyaman, Wassim
Kuchroo, Vijay K.
Meyer zu Horste, Gerd
Regev, Aviv
Lee, Youjin
Xiao, Sheng
Pawlak, Mathias
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BackLink https://www.ncbi.nlm.nih.gov/pubmed/27346359$$D View this record in MEDLINE/PubMed
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Keywords pathogenicity
IL-23R
RBPJ
Notch
Th17 cells
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Snippet Interleukin-17 (IL-17)-producing helper T cells (Th17 cells) play an important role in autoimmune diseases. However, not all Th17 cells induce tissue...
Interleukin-17 (IL-17)-producing helper T cells (Th17 cells) play an important role in autoimmune diseases. However, not all Th17 cells induce tissue...
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SubjectTerms Animals
Binding Sites
Encephalomyelitis, Autoimmune, Experimental - immunology
Encephalomyelitis, Autoimmune, Experimental - metabolism
Gene Expression
Gene Expression Regulation - immunology
IL-23R
Immunoglobulin J Recombination Signal Sequence-Binding Protein - physiology
Interleukin-10 - biosynthesis
Mice, 129 Strain
Mice, Inbred C57BL
Notch
Nuclear Receptor Subfamily 1, Group F, Member 3 - metabolism
pathogenicity
Promoter Regions, Genetic
Protein Binding
Proto-Oncogene Proteins c-maf - physiology
RBPJ
Receptors, Interleukin - genetics
Receptors, Interleukin - metabolism
Th17 cells
Th17 Cells - metabolism
Transcriptional Activation
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Title RBPJ Controls Development of Pathogenic Th17 Cells by Regulating IL-23 Receptor Expression
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