TGF-β signaling in Th17 cells promotes IL-22 production and colitis-associated colon cancer

IL-22 has dual functions during tumorigenesis. Short term IL-22 production protects against genotoxic stress, whereas uncontrolled IL-22 activity promotes tumor growth; therefore, tight regulation of IL-22 is essential. TGF-β1 promotes the differentiation of Th17 cells, which are known to be a major...

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Published inNature communications Vol. 11; no. 1; pp. 2608 - 14
Main Authors Perez, Laura Garcia, Kempski, Jan, McGee, Heather M., Pelzcar, Penelope, Agalioti, Theodora, Giannou, Anastasios, Konczalla, Leonie, Brockmann, Leonie, Wahib, Ramez, Xu, Hao, Vesely, Maria Carolina Amezcua, Soukou, Shiwa, Steglich, Babett, Bedke, Tanja, Manthey, Carolin, Seiz, Oliver, Diercks, Björn-Philipp, Gnafakis, Stylianos, Guse, Andreas H., Perez, Daniel, Izbicki, Jakob R., Gagliani, Nicola, Flavell, Richard A., Huber, Samuel
Format Journal Article
LanguageEnglish
Published London Nature Publishing Group UK 25.05.2020
Nature Publishing Group
Nature Portfolio
Subjects
1-Phosphatidylinositol 3-kinase
13
13/21
13/31
38
38/88
59
631/250/1619/554/1898
631/250/2152/1566/2493
64
64/60
692/4028/67/580
Animals
Basic Helix-Loop-Helix Transcription Factors - genetics
Basic Helix-Loop-Helix Transcription Factors - metabolism
Carcinogenesis - immunology
CD4 antigen
Cell Differentiation
Colitis
Colitis - complications
Colitis - immunology
Colon
Colon cancer
Colonic Neoplasms - etiology
Colonic Neoplasms - immunology
Colonic Neoplasms - pathology
Colorectal cancer
Colorectal carcinoma
Colorectal Neoplasms - etiology
Colorectal Neoplasms - immunology
Colorectal Neoplasms - pathology
Disease Models, Animal
Female
Genotoxicity
Helper cells
Humanities and Social Sciences
Humans
Interleukin 17
Interleukin 22
Interleukin-17 - genetics
Interleukin-17 - metabolism
Interleukins - biosynthesis
Lymphocytes
Lymphocytes T
Lymphocytes, Tumor-Infiltrating - immunology
Lymphocytes, Tumor-Infiltrating - pathology
Male
Medicin och hälsovetenskap
Mice
Mice, Inbred C57BL
Mice, Transgenic
multidisciplinary
Phosphatidylinositol 3-Kinases - metabolism
Receptors, Aryl Hydrocarbon - genetics
Receptors, Aryl Hydrocarbon - metabolism
Science
Science (multidisciplinary)
Signal Transduction - immunology
Signaling
Th17 Cells - immunology
Th17 Cells - pathology
Transforming Growth Factor beta - metabolism
Transforming Growth Factor beta1 - metabolism
Transforming growth factor-b1
Tumorigenesis
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Abstract IL-22 has dual functions during tumorigenesis. Short term IL-22 production protects against genotoxic stress, whereas uncontrolled IL-22 activity promotes tumor growth; therefore, tight regulation of IL-22 is essential. TGF-β1 promotes the differentiation of Th17 cells, which are known to be a major source of IL-22, but the effect of TGF-β signaling on the production of IL-22 in CD4+ T cells is controversial. Here we show an increased presence of IL-17+IL-22+ cells and TGF-β1 in colorectal cancer compared to normal adjacent tissue, whereas the frequency of IL-22 single producing cells is not changed. Accordingly, TGF-β signaling in CD4+ T cells (specifically Th17 cells) promotes the emergence of IL-22-producing Th17 cells and thereby tumorigenesis in mice. IL-22 single producing T cells, however, are not dependent on TGF-β signaling. We show that TGF-β, via AhR induction, and PI3K signaling promotes IL-22 production in Th17 cells. Poly-functional helper T cells can have a stronger effect than mono-functional T cells, but whether the response is qualitatively different is not clear. Here the authors show that a population of IL-17 + IL-22 + , but not single IL-22 + , CD4 + T cells are induced by TGF-β, enriched in patients with colorectal cancer (CRC) and drive CRC progression in mice.
AbstractList IL-22 has dual functions during tumorigenesis. Short term IL-22 production protects against genotoxic stress, whereas uncontrolled IL-22 activity promotes tumor growth; therefore, tight regulation of IL-22 is essential. TGF-β1 promotes the differentiation of Th17 cells, which are known to be a major source of IL-22, but the effect of TGF-β signaling on the production of IL-22 in CD4+ T cells is controversial. Here we show an increased presence of IL-17+IL-22+ cells and TGF-β1 in colorectal cancer compared to normal adjacent tissue, whereas the frequency of IL-22 single producing cells is not changed. Accordingly, TGF-β signaling in CD4+ T cells (specifically Th17 cells) promotes the emergence of IL-22-producing Th17 cells and thereby tumorigenesis in mice. IL-22 single producing T cells, however, are not dependent on TGF-β signaling. We show that TGF-β, via AhR induction, and PI3K signaling promotes IL-22 production in Th17 cells. Poly-functional helper T cells can have a stronger effect than mono-functional T cells, but whether the response is qualitatively different is not clear. Here the authors show that a population of IL-17 + IL-22 + , but not single IL-22 + , CD4 + T cells are induced by TGF-β, enriched in patients with colorectal cancer (CRC) and drive CRC progression in mice.
Poly-functional helper T cells can have a stronger effect than mono-functional T cells, but whether the response is qualitatively different is not clear. Here the authors show that a population of IL-17+IL-22+, but not single IL-22+, CD4+ T cells are induced by TGF-β, enriched in patients with colorectal cancer (CRC) and drive CRC progression in mice.
Abstract IL-22 has dual functions during tumorigenesis. Short term IL-22 production protects against genotoxic stress, whereas uncontrolled IL-22 activity promotes tumor growth; therefore, tight regulation of IL-22 is essential. TGF-β1 promotes the differentiation of Th17 cells, which are known to be a major source of IL-22, but the effect of TGF-β signaling on the production of IL-22 in CD4+ T cells is controversial. Here we show an increased presence of IL-17+IL-22+ cells and TGF-β1 in colorectal cancer compared to normal adjacent tissue, whereas the frequency of IL-22 single producing cells is not changed. Accordingly, TGF-β signaling in CD4+ T cells (specifically Th17 cells) promotes the emergence of IL-22-producing Th17 cells and thereby tumorigenesis in mice. IL-22 single producing T cells, however, are not dependent on TGF-β signaling. We show that TGF-β, via AhR induction, and PI3K signaling promotes IL-22 production in Th17 cells.
IL-22 has dual functions during tumorigenesis. Short term IL-22 production protects against genotoxic stress, whereas uncontrolled IL-22 activity promotes tumor growth; therefore, tight regulation of IL-22 is essential. TGF-β1 promotes the differentiation of Th17 cells, which are known to be a major source of IL-22, but the effect of TGF-β signaling on the production of IL-22 in CD4+ T cells is controversial. Here we show an increased presence of IL-17+IL-22+ cells and TGF-β1 in colorectal cancer compared to normal adjacent tissue, whereas the frequency of IL-22 single producing cells is not changed. Accordingly, TGF-β signaling in CD4+ T cells (specifically Th17 cells) promotes the emergence of IL-22-producing Th17 cells and thereby tumorigenesis in mice. IL-22 single producing T cells, however, are not dependent on TGF-β signaling. We show that TGF-β, via AhR induction, and PI3K signaling promotes IL-22 production in Th17 cells.Poly-functional helper T cells can have a stronger effect than mono-functional T cells, but whether the response is qualitatively different is not clear. Here the authors show that a population of IL-17+IL-22+, but not single IL-22+, CD4+ T cells are induced by TGF-β, enriched in patients with colorectal cancer (CRC) and drive CRC progression in mice.
IL-22 has dual functions during tumorigenesis. Short term IL-22 production protects against genotoxic stress, whereas uncontrolled IL-22 activity promotes tumor growth; therefore, tight regulation of IL-22 is essential. TGF-β1 promotes the differentiation of Th17 cells, which are known to be a major source of IL-22, but the effect of TGF-β signaling on the production of IL-22 in CD4+ T cells is controversial. Here we show an increased presence of IL-17+IL-22+ cells and TGF-β1 in colorectal cancer compared to normal adjacent tissue, whereas the frequency of IL-22 single producing cells is not changed. Accordingly, TGF-β signaling in CD4+ T cells (specifically Th17 cells) promotes the emergence of IL-22-producing Th17 cells and thereby tumorigenesis in mice. IL-22 single producing T cells, however, are not dependent on TGF-β signaling. We show that TGF-β, via AhR induction, and PI3K signaling promotes IL-22 production in Th17 cells.
ArticleNumber 2608
Author Giannou, Anastasios
Perez, Daniel
Xu, Hao
Guse, Andreas H.
Huber, Samuel
Flavell, Richard A.
Pelzcar, Penelope
Gnafakis, Stylianos
Wahib, Ramez
Gagliani, Nicola
Kempski, Jan
Bedke, Tanja
Konczalla, Leonie
Soukou, Shiwa
Vesely, Maria Carolina Amezcua
Perez, Laura Garcia
Agalioti, Theodora
Izbicki, Jakob R.
McGee, Heather M.
Seiz, Oliver
Manthey, Carolin
Diercks, Björn-Philipp
Steglich, Babett
Brockmann, Leonie
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SSID ssj0000391844
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Snippet IL-22 has dual functions during tumorigenesis. Short term IL-22 production protects against genotoxic stress, whereas uncontrolled IL-22 activity promotes...
Abstract IL-22 has dual functions during tumorigenesis. Short term IL-22 production protects against genotoxic stress, whereas uncontrolled IL-22 activity...
Poly-functional helper T cells can have a stronger effect than mono-functional T cells, but whether the response is qualitatively different is not clear. Here...
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SubjectTerms 1-Phosphatidylinositol 3-kinase
13
13/21
13/31
38
38/88
59
631/250/1619/554/1898
631/250/2152/1566/2493
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Animals
Basic Helix-Loop-Helix Transcription Factors - genetics
Basic Helix-Loop-Helix Transcription Factors - metabolism
Carcinogenesis - immunology
CD4 antigen
Cell Differentiation
Colitis
Colitis - complications
Colitis - immunology
Colon
Colon cancer
Colonic Neoplasms - etiology
Colonic Neoplasms - immunology
Colonic Neoplasms - pathology
Colorectal cancer
Colorectal carcinoma
Colorectal Neoplasms - etiology
Colorectal Neoplasms - immunology
Colorectal Neoplasms - pathology
Disease Models, Animal
Female
Genotoxicity
Helper cells
Humanities and Social Sciences
Humans
Interleukin 17
Interleukin 22
Interleukin-17 - genetics
Interleukin-17 - metabolism
Interleukins - biosynthesis
Lymphocytes
Lymphocytes T
Lymphocytes, Tumor-Infiltrating - immunology
Lymphocytes, Tumor-Infiltrating - pathology
Male
Medicin och hälsovetenskap
Mice
Mice, Inbred C57BL
Mice, Transgenic
multidisciplinary
Phosphatidylinositol 3-Kinases - metabolism
Receptors, Aryl Hydrocarbon - genetics
Receptors, Aryl Hydrocarbon - metabolism
Science
Science (multidisciplinary)
Signal Transduction - immunology
Signaling
Th17 Cells - immunology
Th17 Cells - pathology
Transforming Growth Factor beta - metabolism
Transforming Growth Factor beta1 - metabolism
Transforming growth factor-b1
Tumorigenesis
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Title TGF-β signaling in Th17 cells promotes IL-22 production and colitis-associated colon cancer
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Volume 11
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