Syk signaling in dendritic cells orchestrates innate resistance to systemic fungal infection

Host protection from fungal infection is thought to ensue in part from the activity of Syk-coupled C-type lectin receptors and MyD88-coupled toll-like receptors in myeloid cells, including neutrophils, macrophages and dendritic cells (DCs). Given the multitude of cell types and receptors involved, e...

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Published inPLoS pathogens Vol. 10; no. 7; p. e1004276
Main Authors Whitney, Paul G, Bär, Eva, Osorio, Fabiola, Rogers, Neil C, Schraml, Barbara U, Deddouche, Safia, LeibundGut-Landmann, Salomé, Reis e Sousa, Caetano
Format Journal Article
LanguageEnglish
Published United States Public Library of Science 01.07.2014
Public Library of Science (PLoS)
Subjects
Animals
Biology and life sciences
Cancer
Candida albicans - immunology
Candidiasis - genetics
Candidiasis - immunology
Chemokines
Dendritic cells
Dendritic Cells - immunology
Dendritic Cells - pathology
Experiments
Fungal infections
Health aspects
Immunity, Innate
Interleukin-23 Subunit p19 - genetics
Interleukin-23 Subunit p19 - immunology
Intracellular Signaling Peptides and Proteins - genetics
Intracellular Signaling Peptides and Proteins - immunology
Kidneys
Kinases
Medical research
Mice
Mice, Knockout
Mortality
Mycoses
Myeloid Differentiation Factor 88 - genetics
Myeloid Differentiation Factor 88 - immunology
Physiological aspects
Protein-Tyrosine Kinases - genetics
Protein-Tyrosine Kinases - immunology
Rodents
Studies
Syk Kinase
T cells
United Kingdom
Switzerland
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Abstract Host protection from fungal infection is thought to ensue in part from the activity of Syk-coupled C-type lectin receptors and MyD88-coupled toll-like receptors in myeloid cells, including neutrophils, macrophages and dendritic cells (DCs). Given the multitude of cell types and receptors involved, elimination of a single pathway for fungal recognition in a cell type such as DCs, primarily known for their ability to prime T cell responses, would be expected to have little effect on innate resistance to fungal infection. Here we report that this is surprisingly not the case and that selective loss of Syk but not MyD88 in DCs abrogates innate resistance to acute systemic Candida albicans infection in mice. We show that Syk expression by DCs is necessary for IL-23p19 production in response to C. albicans, which is essential to transiently induce GM-CSF secretion by NK cells that are recruited to the site of fungal replication. NK cell-derived-GM-CSF in turn sustains the anti-microbial activity of neutrophils, the main fungicidal effectors. Thus, the activity of a single kinase in a single myeloid cell type orchestrates a complex series of molecular and cellular events that underlies innate resistance to fungal sepsis.
AbstractList Host protection from fungal infection is thought to ensue in part from the activity of Syk-coupled C-type lectin receptors and MyD88-coupled toll-like receptors in myeloid cells, including neutrophils, macrophages and dendritic cells (DCs). Given the multitude of cell types and receptors involved, elimination of a single pathway for fungal recognition in a cell type such as DCs, primarily known for their ability to prime T cell responses, would be expected to have little effect on innate resistance to fungal infection. Here we report that this is surprisingly not the case and that selective loss of Syk but not MyD88 in DCs abrogates innate resistance to acute systemic Candida albicans infection in mice. We show that Syk expression by DCs is necessary for IL-23p19 production in response to C. albicans, which is essential to transiently induce GM-CSF secretion by NK cells that are recruited to the site of fungal replication. NK cell-derived-GM-CSF in turn sustains the anti-microbial activity of neutrophils, the main fungicidal effectors. Thus, the activity of a single kinase in a single myeloid cell type orchestrates a complex series of molecular and cellular events that underlies innate resistance to fungal sepsis.
  Host protection from fungal infection is thought to ensue in part from the activity of Syk-coupled C-type lectin receptors and MyD88-coupled toll-like receptors in myeloid cells, including neutrophils, macrophages and dendritic cells (DCs). Given the multitude of cell types and receptors involved, elimination of a single pathway for fungal recognition in a cell type such as DCs, primarily known for their ability to prime T cell responses, would be expected to have little effect on innate resistance to fungal infection. Here we report that this is surprisingly not the case and that selective loss of Syk but not MyD88 in DCs abrogates innate resistance to acute systemic Candida albicans infection in mice. We show that Syk expression by DCs is necessary for IL-23p19 production in response to C. albicans, which is essential to transiently induce GM-CSF secretion by NK cells that are recruited to the site of fungal replication. NK cell-derived-GM-CSF in turn sustains the anti-microbial activity of neutrophils, the main fungicidal effectors. Thus, the activity of a single kinase in a single myeloid cell type orchestrates a complex series of molecular and cellular events that underlies innate resistance to fungal sepsis.
Host protection from fungal infection is thought to ensue in part from the activity of Syk-coupled C-type lectin receptors and MyD88-coupled toll-like receptors in myeloid cells, including neutrophils, macrophages and dendritic cells (DCs). Given the multitude of cell types and receptors involved, elimination of a single pathway for fungal recognition in a cell type such as DCs, primarily known for their ability to prime T cell responses, would be expected to have little effect on innate resistance to fungal infection. Here we report that this is surprisingly not the case and that selective loss of Syk but not MyD88 in DCs abrogates innate resistance to acute systemic Candida albicans infection in mice. We show that Syk expression by DCs is necessary for IL-23p19 production in response to C. albicans , which is essential to transiently induce GM-CSF secretion by NK cells that are recruited to the site of fungal replication. NK cell-derived-GM-CSF in turn sustains the anti-microbial activity of neutrophils, the main fungicidal effectors. Thus, the activity of a single kinase in a single myeloid cell type orchestrates a complex series of molecular and cellular events that underlies innate resistance to fungal sepsis. Multiple cell types bearing a vast array of immune receptors with different modes of signaling ensure that the host response to infection is both robust and reliable. For this reason, loss of a single signaling pathway in a given cell type is often not enough to impact host resistance. Here, we find, surprisingly, that this is not the case in a mouse model of systemic fungal infection with Candida albicans . We show that a single kinase (Syk) in a single cell type (dendritic cells, DCs) coordinates the entire host resistance network. We highlight Syk-dependent production of IL-23p19 by DCs as the key to protection and show that IL-23p19 acts on another white blood cell type, NK cells, to specifically induce production of another mediator, GM-CSF. The latter is key for yet another cell, the neutrophil, to be mobilized into action and kill Candida organisms. This study places DCs, best known for their role in priming T cells, at the center of a cellular relay of innate immunity to fungal infection. It highlights key nodes of antifungal immunity that could be targeted in combination with antifungal drugs to provide new ways to treat patients with fungal sepsis, who generally have poor outcomes.
Audience Academic
Author Osorio, Fabiola
Whitney, Paul G
Bär, Eva
LeibundGut-Landmann, Salomé
Schraml, Barbara U
Deddouche, Safia
Rogers, Neil C
Reis e Sousa, Caetano
AuthorAffiliation 1 Immunobiology Laboratory, Cancer Research UK, London Research Institute, Lincoln's Inn Fields Laboratories, London, United Kingdom
University of Pittsburgh, United States of America
2 Institute of Microbiology, ETH Zurich, Zürich, Switzerland
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2014 Whitney et al 2014 Whitney et al
2014 Public Library of Science. This is an open-access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited: Whitney PG, Bär E, Osorio F, Rogers NC, Schraml BU, Deddouche S, et al. (2014) Syk Signaling in Dendritic Cells Orchestrates Innate Resistance to Systemic Fungal Infection. PLoS Pathog 10(7): e1004276. doi:10.1371/journal.ppat.1004276
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– notice: 2014 Public Library of Science. This is an open-access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited: Whitney PG, Bär E, Osorio F, Rogers NC, Schraml BU, Deddouche S, et al. (2014) Syk Signaling in Dendritic Cells Orchestrates Innate Resistance to Systemic Fungal Infection. PLoS Pathog 10(7): e1004276. doi:10.1371/journal.ppat.1004276
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Conceived and designed the experiments: PGW CReS EB FO SLL. Performed the experiments: PGW EB FO SD. Analyzed the data: PGW EB FO CReS SLL. Contributed reagents/materials/analysis tools: NCR BUS. Wrote the paper: PGW CReS FO SLL.
SLL and CReS also contributed equally to this work.
The authors have declared that no competing interests exist.
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Snippet Host protection from fungal infection is thought to ensue in part from the activity of Syk-coupled C-type lectin receptors and MyD88-coupled toll-like...
  Host protection from fungal infection is thought to ensue in part from the activity of Syk-coupled C-type lectin receptors and MyD88-coupled toll-like...
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StartPage e1004276
SubjectTerms Animals
Biology and life sciences
Cancer
Candida albicans - immunology
Candidiasis - genetics
Candidiasis - immunology
Chemokines
Dendritic cells
Dendritic Cells - immunology
Dendritic Cells - pathology
Experiments
Fungal infections
Health aspects
Immunity, Innate
Interleukin-23 Subunit p19 - genetics
Interleukin-23 Subunit p19 - immunology
Intracellular Signaling Peptides and Proteins - genetics
Intracellular Signaling Peptides and Proteins - immunology
Kidneys
Kinases
Medical research
Mice
Mice, Knockout
Mortality
Mycoses
Myeloid Differentiation Factor 88 - genetics
Myeloid Differentiation Factor 88 - immunology
Physiological aspects
Protein-Tyrosine Kinases - genetics
Protein-Tyrosine Kinases - immunology
Rodents
Studies
Syk Kinase
T cells
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Title Syk signaling in dendritic cells orchestrates innate resistance to systemic fungal infection
URI https://www.ncbi.nlm.nih.gov/pubmed/25033445
https://search.proquest.com/docview/1546215453
https://pubmed.ncbi.nlm.nih.gov/PMC4102599
https://doaj.org/article/2c4e2c44d7d24d1e905c74d078f927fb
http://dx.doi.org/10.1371/journal.ppat.1004276
Volume 10
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