Cell-autonomous Hedgehog signaling controls Th17 polarization and pathogenicity

Th17 cells are key drivers of autoimmune disease. However, the signaling pathways regulating Th17 polarization are poorly understood. Hedgehog signaling regulates cell fate decisions during embryogenesis and adult tissue patterning. Here we find that cell-autonomous Hedgehog signaling, independent o...

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Published inNature communications Vol. 13; no. 1; p. 4075
Main Authors Hanna, Joachim, Beke, Flavio, O’Brien, Louise M., Kapeni, Chrysa, Chen, Hung-Chang, Carbonaro, Valentina, Kim, Alexander B., Kishore, Kamal, Adolph, Timon E., Skjoedt, Mikkel-Ole, Skjoedt, Karsten, de la Roche, Marc, de la Roche, Maike
Format Journal Article
LanguageEnglish
Published London Nature Publishing Group UK 14.07.2022
Nature Publishing Group
Nature Portfolio
Subjects
13
13/1
13/106
13/31
13/51
14/19
38
38/35
38/39
38/91
45/88
45/90
631/250/1619/554/1898
631/250/1619/554/1898/1273
631/250/2152/1566/2493
631/80/86/2370
64
64/60
96
96/21
Ablation
Adult
Animal models
Animals
Autoimmune diseases
CD4 antigen
Cell fate
Colitis, Ulcerative - drug therapy
Colitis, Ulcerative - genetics
Embryogenesis
Embryonic growth stage
Hedgehog protein
Hedgehog Proteins - genetics
Hedgehog Proteins - metabolism
Helper cells
Humanities and Social Sciences
Humans
Inflammatory bowel disease
Inflammatory bowel diseases
Intestine
Ligands
Lymphocytes
Lymphocytes T
Mice
multidisciplinary
Pathogenicity
Pathogens
Pattern formation
Polarization
Science
Science (multidisciplinary)
Signal Transduction
Signaling
Th17 Cells
Therapeutic targets
Ulcerative colitis
Virulence
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Abstract Th17 cells are key drivers of autoimmune disease. However, the signaling pathways regulating Th17 polarization are poorly understood. Hedgehog signaling regulates cell fate decisions during embryogenesis and adult tissue patterning. Here we find that cell-autonomous Hedgehog signaling, independent of exogenous ligands, selectively drives the polarization of Th17 cells but not other T helper cell subsets. We show that endogenous Hedgehog ligand, Ihh, signals to activate both canonical and non-canonical Hedgehog pathways through Gli3 and AMPK. We demonstrate that Hedgehog pathway inhibition with either the clinically-approved small molecule inhibitor vismodegib or genetic ablation of Ihh in CD4 +  T cells greatly diminishes disease severity in two mouse models of intestinal inflammation. We confirm that Hedgehog pathway expression is upregulated in tissue from human ulcerative colitis patients and correlates with Th17 marker expression. This work implicates Hedgehog signaling in Th17 polarization and intestinal immunopathology and indicates the potential therapeutic use of Hedgehog inhibitors in the treatment of inflammatory bowel disease. Th17 cells are critical players in the immunopathology of a range of autoimmune diseases. Here the authors implicate Hedgehog signaling in Th17 polarization and in the immunopathology of intestinal inflammation in murine models and suggest therapeutic targeting of Hedgehog signaling in the context of inflammatory bowel disease.
AbstractList Th17 cells are key drivers of autoimmune disease. However, the signaling pathways regulating Th17 polarization are poorly understood. Hedgehog signaling regulates cell fate decisions during embryogenesis and adult tissue patterning. Here we find that cell-autonomous Hedgehog signaling, independent of exogenous ligands, selectively drives the polarization of Th17 cells but not other T helper cell subsets. We show that endogenous Hedgehog ligand, Ihh, signals to activate both canonical and non-canonical Hedgehog pathways through Gli3 and AMPK. We demonstrate that Hedgehog pathway inhibition with either the clinically-approved small molecule inhibitor vismodegib or genetic ablation of Ihh in CD4 +  T cells greatly diminishes disease severity in two mouse models of intestinal inflammation. We confirm that Hedgehog pathway expression is upregulated in tissue from human ulcerative colitis patients and correlates with Th17 marker expression. This work implicates Hedgehog signaling in Th17 polarization and intestinal immunopathology and indicates the potential therapeutic use of Hedgehog inhibitors in the treatment of inflammatory bowel disease. Th17 cells are critical players in the immunopathology of a range of autoimmune diseases. Here the authors implicate Hedgehog signaling in Th17 polarization and in the immunopathology of intestinal inflammation in murine models and suggest therapeutic targeting of Hedgehog signaling in the context of inflammatory bowel disease.
Th17 cells are key drivers of autoimmune disease. However, the signaling pathways regulating Th17 polarization are poorly understood. Hedgehog signaling regulates cell fate decisions during embryogenesis and adult tissue patterning. Here we find that cell-autonomous Hedgehog signaling, independent of exogenous ligands, selectively drives the polarization of Th17 cells but not other T helper cell subsets. We show that endogenous Hedgehog ligand, Ihh, signals to activate both canonical and non-canonical Hedgehog pathways through Gli3 and AMPK. We demonstrate that Hedgehog pathway inhibition with either the clinically-approved small molecule inhibitor vismodegib or genetic ablation of Ihh in CD4+ T cells greatly diminishes disease severity in two mouse models of intestinal inflammation. We confirm that Hedgehog pathway expression is upregulated in tissue from human ulcerative colitis patients and correlates with Th17 marker expression. This work implicates Hedgehog signaling in Th17 polarization and intestinal immunopathology and indicates the potential therapeutic use of Hedgehog inhibitors in the treatment of inflammatory bowel disease.
Th17 cells are key drivers of autoimmune disease. However, the signaling pathways regulating Th17 polarization are poorly understood. Hedgehog signaling regulates cell fate decisions during embryogenesis and adult tissue patterning. Here we find that cell-autonomous Hedgehog signaling, independent of exogenous ligands, selectively drives the polarization of Th17 cells but not other T helper cell subsets. We show that endogenous Hedgehog ligand, Ihh, signals to activate both canonical and non-canonical Hedgehog pathways through Gli3 and AMPK. We demonstrate that Hedgehog pathway inhibition with either the clinically-approved small molecule inhibitor vismodegib or genetic ablation of Ihh in CD4 +  T cells greatly diminishes disease severity in two mouse models of intestinal inflammation. We confirm that Hedgehog pathway expression is upregulated in tissue from human ulcerative colitis patients and correlates with Th17 marker expression. This work implicates Hedgehog signaling in Th17 polarization and intestinal immunopathology and indicates the potential therapeutic use of Hedgehog inhibitors in the treatment of inflammatory bowel disease.
Th17 cells are key drivers of autoimmune disease. However, the signaling pathways regulating Th17 polarization are poorly understood. Hedgehog signaling regulates cell fate decisions during embryogenesis and adult tissue patterning. Here we find that cell-autonomous Hedgehog signaling, independent of exogenous ligands, selectively drives the polarization of Th17 cells but not other T helper cell subsets. We show that endogenous Hedgehog ligand, Ihh, signals to activate both canonical and non-canonical Hedgehog pathways through Gli3 and AMPK. We demonstrate that Hedgehog pathway inhibition with either the clinically-approved small molecule inhibitor vismodegib or genetic ablation of Ihh in CD4 T cells greatly diminishes disease severity in two mouse models of intestinal inflammation. We confirm that Hedgehog pathway expression is upregulated in tissue from human ulcerative colitis patients and correlates with Th17 marker expression. This work implicates Hedgehog signaling in Th17 polarization and intestinal immunopathology and indicates the potential therapeutic use of Hedgehog inhibitors in the treatment of inflammatory bowel disease.
Th17 cells are key drivers of autoimmune disease. However, the signaling pathways regulating Th17 polarization are poorly understood. Hedgehog signaling regulates cell fate decisions during embryogenesis and adult tissue patterning. Here we find that cell-autonomous Hedgehog signaling, independent of exogenous ligands, selectively drives the polarization of Th17 cells but not other T helper cell subsets. We show that endogenous Hedgehog ligand, Ihh, signals to activate both canonical and non-canonical Hedgehog pathways through Gli3 and AMPK. We demonstrate that Hedgehog pathway inhibition with either the clinically-approved small molecule inhibitor vismodegib or genetic ablation of Ihh in CD4+ T cells greatly diminishes disease severity in two mouse models of intestinal inflammation. We confirm that Hedgehog pathway expression is upregulated in tissue from human ulcerative colitis patients and correlates with Th17 marker expression. This work implicates Hedgehog signaling in Th17 polarization and intestinal immunopathology and indicates the potential therapeutic use of Hedgehog inhibitors in the treatment of inflammatory bowel disease.Th17 cells are critical players in the immunopathology of a range of autoimmune diseases. Here the authors implicate Hedgehog signaling in Th17 polarization and in the immunopathology of intestinal inflammation in murine models and suggest therapeutic targeting of Hedgehog signaling in the context of inflammatory bowel disease.
Th17 cells are critical players in the immunopathology of a range of autoimmune diseases. Here the authors implicate Hedgehog signaling in Th17 polarization and in the immunopathology of intestinal inflammation in murine models and suggest therapeutic targeting of Hedgehog signaling in the context of inflammatory bowel disease.
ArticleNumber 4075
Author Adolph, Timon E.
Kapeni, Chrysa
Kim, Alexander B.
Chen, Hung-Chang
de la Roche, Marc
Skjoedt, Karsten
Kishore, Kamal
de la Roche, Maike
O’Brien, Louise M.
Carbonaro, Valentina
Hanna, Joachim
Beke, Flavio
Skjoedt, Mikkel-Ole
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BackLink https://www.ncbi.nlm.nih.gov/pubmed/35835905$$D View this record in MEDLINE/PubMed
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crossref_primary_10_1038_s41467_022_31722_5
pubmed_primary_35835905
springer_journals_10_1038_s41467_022_31722_5
PublicationCentury 2000
PublicationDate 2022-07-14
PublicationDateYYYYMMDD 2022-07-14
PublicationDate_xml – month: 07
  year: 2022
  text: 2022-07-14
  day: 14
PublicationDecade 2020
PublicationPlace London
PublicationPlace_xml – name: London
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PublicationTitle Nature communications
PublicationTitleAbbrev Nat Commun
PublicationTitleAlternate Nat Commun
PublicationYear 2022
Publisher Nature Publishing Group UK
Nature Publishing Group
Nature Portfolio
Publisher_xml – name: Nature Publishing Group UK
– name: Nature Publishing Group
– name: Nature Portfolio
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Snippet Th17 cells are key drivers of autoimmune disease. However, the signaling pathways regulating Th17 polarization are poorly understood. Hedgehog signaling...
Th17 cells are critical players in the immunopathology of a range of autoimmune diseases. Here the authors implicate Hedgehog signaling in Th17 polarization...
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SubjectTerms 13
13/1
13/106
13/31
13/51
14/19
38
38/35
38/39
38/91
45/88
45/90
631/250/1619/554/1898
631/250/1619/554/1898/1273
631/250/2152/1566/2493
631/80/86/2370
64
64/60
96
96/21
Ablation
Adult
Animal models
Animals
Autoimmune diseases
CD4 antigen
Cell fate
Colitis, Ulcerative - drug therapy
Colitis, Ulcerative - genetics
Embryogenesis
Embryonic growth stage
Hedgehog protein
Hedgehog Proteins - genetics
Hedgehog Proteins - metabolism
Helper cells
Humanities and Social Sciences
Humans
Inflammatory bowel disease
Inflammatory bowel diseases
Intestine
Ligands
Lymphocytes
Lymphocytes T
Mice
multidisciplinary
Pathogenicity
Pathogens
Pattern formation
Polarization
Science
Science (multidisciplinary)
Signal Transduction
Signaling
Th17 Cells
Therapeutic targets
Ulcerative colitis
Virulence
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Title Cell-autonomous Hedgehog signaling controls Th17 polarization and pathogenicity
URI https://link.springer.com/article/10.1038/s41467-022-31722-5
https://www.ncbi.nlm.nih.gov/pubmed/35835905
https://www.proquest.com/docview/2689409732
https://search.proquest.com/docview/2691052626
https://pubmed.ncbi.nlm.nih.gov/PMC9281293
https://doaj.org/article/37d7f063bb4e46ea82ad72c1a4b36302
Volume 13
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