The Cytokine GM-CSF Drives the Inflammatory Signature of CCR2+ Monocytes and Licenses Autoimmunity

Granulocyte-macrophage colony-stimulating factor (GM-CSF) has emerged as a crucial cytokine produced by auto-reactive T helper (Th) cells that initiate tissue inflammation. Multiple cell types can sense GM-CSF, but the identity of the pathogenic GM-CSF-responsive cells is unclear. By using condition...

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Published in:	Immunity (Cambridge, Mass.) Vol. 43; no. 3; p. 502
Main Authors:	Croxford, Andrew L, Lanzinger, Margit, Hartmann, Felix J, Schreiner, Bettina, Mair, Florian, Pelczar, Pawel, Clausen, Björn E, Jung, Steffen, Greter, Melanie, Becher, Burkhard
Format:	Journal Article
Language:	English
Published:	United States 15.09.2015
Subjects:	Animals Antigens, Ly - genetics Antigens, Ly - immunology Antigens, Ly - metabolism Autoimmunity - genetics Autoimmunity - immunology Cytokine Receptor Common beta Subunit - genetics Cytokine Receptor Common beta Subunit - immunology Cytokine Receptor Common beta Subunit - metabolism Dendritic Cells - drug effects Dendritic Cells - immunology Dendritic Cells - metabolism Encephalomyelitis, Autoimmune, Experimental Flow Cytometry Granulocyte-Macrophage Colony-Stimulating Factor - immunology Granulocyte-Macrophage Colony-Stimulating Factor - metabolism Granulocyte-Macrophage Colony-Stimulating Factor - pharmacology Humans Inflammation - genetics Inflammation - immunology Inflammation - metabolism Interleukin-1beta - genetics Interleukin-1beta - immunology Interleukin-1beta - metabolism Mice, Knockout Mice, Transgenic Monocytes - drug effects Monocytes - immunology Monocytes - metabolism Myeloid Cells - drug effects Myeloid Cells - immunology Myeloid Cells - metabolism Phosphorylation - drug effects Phosphorylation - immunology Receptors, CCR2 - genetics Receptors, CCR2 - immunology Receptors, CCR2 - metabolism Reverse Transcriptase Polymerase Chain Reaction Signal Transduction - drug effects Signal Transduction - genetics Signal Transduction - immunology STAT5 Transcription Factor - immunology STAT5 Transcription Factor - metabolism Transcriptome - drug effects Transcriptome - genetics Transcriptome - immunology
ISSN:	1097-4180, 1097-4180
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Abstract	Granulocyte-macrophage colony-stimulating factor (GM-CSF) has emerged as a crucial cytokine produced by auto-reactive T helper (Th) cells that initiate tissue inflammation. Multiple cell types can sense GM-CSF, but the identity of the pathogenic GM-CSF-responsive cells is unclear. By using conditional gene targeting, we systematically deleted the GM-CSF receptor (Csf2rb) in specific subpopulations throughout the myeloid lineages. Experimental autoimmune encephalomyelitis (EAE) progressed normally when either classical dendritic cells (cDCs) or neutrophils lacked GM-CSF responsiveness. The development of tissue-invading monocyte-derived dendritic cells (moDCs) was also unperturbed upon Csf2rb deletion. Instead, deletion of Csf2rb in CCR2(+)Ly6C(hi) monocytes phenocopied the EAE resistance seen in complete Csf2rb-deficient mice. High-dimensional analysis of tissue-infiltrating moDCs revealed that GM-CSF initiates a combination of inflammatory mechanisms. These results indicate that GM-CSF signaling controls a pathogenic expression signature in CCR2(+)Ly6C(hi) monocytes and their progeny, which was essential for tissue damage.
AbstractList	Granulocyte-macrophage colony-stimulating factor (GM-CSF) has emerged as a crucial cytokine produced by auto-reactive T helper (Th) cells that initiate tissue inflammation. Multiple cell types can sense GM-CSF, but the identity of the pathogenic GM-CSF-responsive cells is unclear. By using conditional gene targeting, we systematically deleted the GM-CSF receptor (Csf2rb) in specific subpopulations throughout the myeloid lineages. Experimental autoimmune encephalomyelitis (EAE) progressed normally when either classical dendritic cells (cDCs) or neutrophils lacked GM-CSF responsiveness. The development of tissue-invading monocyte-derived dendritic cells (moDCs) was also unperturbed upon Csf2rb deletion. Instead, deletion of Csf2rb in CCR2(+)Ly6C(hi) monocytes phenocopied the EAE resistance seen in complete Csf2rb-deficient mice. High-dimensional analysis of tissue-infiltrating moDCs revealed that GM-CSF initiates a combination of inflammatory mechanisms. These results indicate that GM-CSF signaling controls a pathogenic expression signature in CCR2(+)Ly6C(hi) monocytes and their progeny, which was essential for tissue damage. Granulocyte-macrophage colony-stimulating factor (GM-CSF) has emerged as a crucial cytokine produced by auto-reactive T helper (Th) cells that initiate tissue inflammation. Multiple cell types can sense GM-CSF, but the identity of the pathogenic GM-CSF-responsive cells is unclear. By using conditional gene targeting, we systematically deleted the GM-CSF receptor (Csf2rb) in specific subpopulations throughout the myeloid lineages. Experimental autoimmune encephalomyelitis (EAE) progressed normally when either classical dendritic cells (cDCs) or neutrophils lacked GM-CSF responsiveness. The development of tissue-invading monocyte-derived dendritic cells (moDCs) was also unperturbed upon Csf2rb deletion. Instead, deletion of Csf2rb in CCR2(+)Ly6C(hi) monocytes phenocopied the EAE resistance seen in complete Csf2rb-deficient mice. High-dimensional analysis of tissue-infiltrating moDCs revealed that GM-CSF initiates a combination of inflammatory mechanisms. These results indicate that GM-CSF signaling controls a pathogenic expression signature in CCR2(+)Ly6C(hi) monocytes and their progeny, which was essential for tissue damage.Granulocyte-macrophage colony-stimulating factor (GM-CSF) has emerged as a crucial cytokine produced by auto-reactive T helper (Th) cells that initiate tissue inflammation. Multiple cell types can sense GM-CSF, but the identity of the pathogenic GM-CSF-responsive cells is unclear. By using conditional gene targeting, we systematically deleted the GM-CSF receptor (Csf2rb) in specific subpopulations throughout the myeloid lineages. Experimental autoimmune encephalomyelitis (EAE) progressed normally when either classical dendritic cells (cDCs) or neutrophils lacked GM-CSF responsiveness. The development of tissue-invading monocyte-derived dendritic cells (moDCs) was also unperturbed upon Csf2rb deletion. Instead, deletion of Csf2rb in CCR2(+)Ly6C(hi) monocytes phenocopied the EAE resistance seen in complete Csf2rb-deficient mice. High-dimensional analysis of tissue-infiltrating moDCs revealed that GM-CSF initiates a combination of inflammatory mechanisms. These results indicate that GM-CSF signaling controls a pathogenic expression signature in CCR2(+)Ly6C(hi) monocytes and their progeny, which was essential for tissue damage.
Author	Pelczar, Pawel Lanzinger, Margit Jung, Steffen Hartmann, Felix J Schreiner, Bettina Mair, Florian Clausen, Björn E Becher, Burkhard Croxford, Andrew L Greter, Melanie
Author_xml	– sequence: 1 givenname: Andrew L surname: Croxford fullname: Croxford, Andrew L organization: Institute of Experimental Immunology, University of Zürich, Zürich 8057, Switzerland – sequence: 2 givenname: Margit surname: Lanzinger fullname: Lanzinger, Margit organization: Institute of Experimental Immunology, University of Zürich, Zürich 8057, Switzerland – sequence: 3 givenname: Felix J surname: Hartmann fullname: Hartmann, Felix J organization: Institute of Experimental Immunology, University of Zürich, Zürich 8057, Switzerland – sequence: 4 givenname: Bettina surname: Schreiner fullname: Schreiner, Bettina organization: Institute of Experimental Immunology, University of Zürich, Zürich 8057, Switzerland – sequence: 5 givenname: Florian surname: Mair fullname: Mair, Florian organization: Institute of Experimental Immunology, University of Zürich, Zürich 8057, Switzerland – sequence: 6 givenname: Pawel surname: Pelczar fullname: Pelczar, Pawel organization: Institute of Experimental Immunology, University of Zürich, Zürich 8057, Switzerland – sequence: 7 givenname: Björn E surname: Clausen fullname: Clausen, Björn E organization: Institute for Molecular Medicine, Johannes Gutenberg-University Mainz, 55131 Mainz, Germany – sequence: 8 givenname: Steffen surname: Jung fullname: Jung, Steffen organization: Department of Immunology, Weizmann Institute of Science, 76100 Rehovot, Israel – sequence: 9 givenname: Melanie surname: Greter fullname: Greter, Melanie organization: Institute of Experimental Immunology, University of Zürich, Zürich 8057, Switzerland – sequence: 10 givenname: Burkhard surname: Becher fullname: Becher, Burkhard email: becher@immunology.uzh.ch organization: Institute of Experimental Immunology, University of Zürich, Zürich 8057, Switzerland. Electronic address: becher@immunology.uzh.ch
BackLink	https://www.ncbi.nlm.nih.gov/pubmed/26341401$$D View this record in MEDLINE/PubMed
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Snippet	Granulocyte-macrophage colony-stimulating factor (GM-CSF) has emerged as a crucial cytokine produced by auto-reactive T helper (Th) cells that initiate tissue...
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SubjectTerms	Animals Antigens, Ly - genetics Antigens, Ly - immunology Antigens, Ly - metabolism Autoimmunity - genetics Autoimmunity - immunology Cytokine Receptor Common beta Subunit - genetics Cytokine Receptor Common beta Subunit - immunology Cytokine Receptor Common beta Subunit - metabolism Dendritic Cells - drug effects Dendritic Cells - immunology Dendritic Cells - metabolism Encephalomyelitis, Autoimmune, Experimental Flow Cytometry Granulocyte-Macrophage Colony-Stimulating Factor - immunology Granulocyte-Macrophage Colony-Stimulating Factor - metabolism Granulocyte-Macrophage Colony-Stimulating Factor - pharmacology Humans Inflammation - genetics Inflammation - immunology Inflammation - metabolism Interleukin-1beta - genetics Interleukin-1beta - immunology Interleukin-1beta - metabolism Mice, Knockout Mice, Transgenic Monocytes - drug effects Monocytes - immunology Monocytes - metabolism Myeloid Cells - drug effects Myeloid Cells - immunology Myeloid Cells - metabolism Phosphorylation - drug effects Phosphorylation - immunology Receptors, CCR2 - genetics Receptors, CCR2 - immunology Receptors, CCR2 - metabolism Reverse Transcriptase Polymerase Chain Reaction Signal Transduction - drug effects Signal Transduction - genetics Signal Transduction - immunology STAT5 Transcription Factor - immunology STAT5 Transcription Factor - metabolism Transcriptome - drug effects Transcriptome - genetics Transcriptome - immunology
Title	The Cytokine GM-CSF Drives the Inflammatory Signature of CCR2+ Monocytes and Licenses Autoimmunity
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