Nitric Oxide Sustains IL-1β Expression in Human Dendritic Cells Enhancing Their Capacity to Induce IL-17–Producing T-Cells

The role played by lung dendritic cells (DCs) which are influenced by external antigens and by their redox state in controlling inflammation is unclear. We studied the role played by nitric oxide (NO) in DC maturation and function. Human DCs were stimulated with a long-acting NO donor, DPTA NONOate,...

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Veröffentlicht in:PloS one Jg. 10; H. 4; S. e0120134
Hauptverfasser: Obregon, Carolina, Graf, Lukas, Chung, Kian Fan, Cesson, Valerie, Nicod, Laurent P.
Format: Journal Article
Sprache:Englisch
Veröffentlicht: United States Public Library of Science 08.04.2015
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ISSN:1932-6203, 1932-6203
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Abstract The role played by lung dendritic cells (DCs) which are influenced by external antigens and by their redox state in controlling inflammation is unclear. We studied the role played by nitric oxide (NO) in DC maturation and function. Human DCs were stimulated with a long-acting NO donor, DPTA NONOate, prior to exposure to lipopolysaccharide (LPS). Dose-and time-dependent experiments were performed with DCs with the aim of measuring the release and gene expression of inflammatory cytokines capable of modifying T-cell differentiation, towardsTh1, Th2 and Th17 cells. NO changed the pattern of cytokine release by LPS-matured DCs, dependent on the concentration of NO, as well as on the timing of its addition to the cells during maturation. Addition of NO before LPS-induced maturation strongly inhibited the release of IL-12, while increasing the expression and release of IL-23, IL-1β and IL-6, which are all involved in Th17 polarization. Indeed, DCs treated with NO efficiently induced the release of IL-17 by T-cells through IL-1β. Our work highlights the important role that NO may play in sustaining inflammation during an infection through the preferential differentiation of the Th17 lineage.
AbstractList The role played by lung dendritic cells (DCs) which are influenced by external antigens and by their redox state in controlling inflammation is unclear. We studied the role played by nitric oxide (NO) in DC maturation and function. Human DCs were stimulated with a long-acting NO donor, DPTA NONOate, prior to exposure to lipopolysaccharide (LPS). Dose-and time-dependent experiments were performed with DCs with the aim of measuring the release and gene expression of inflammatory cytokines capable of modifying T-cell differentiation, towardsTh1, Th2 and Th17 cells. NO changed the pattern of cytokine release by LPS-matured DCs, dependent on the concentration of NO, as well as on the timing of its addition to the cells during maturation. Addition of NO before LPS-induced maturation strongly inhibited the release of IL-12, while increasing the expression and release of IL-23, IL-1β and IL-6, which are all involved in Th17 polarization. Indeed, DCs treated with NO efficiently induced the release of IL-17 by T-cells through IL-1β. Our work highlights the important role that NO may play in sustaining inflammation during an infection through the preferential differentiation of the Th17 lineage.
The role played by lung dendritic cells (DCs) which are influenced by external antigens and by their redox state in controlling inflammation is unclear. We studied the role played by nitric oxide (NO) in DC maturation and function. Human DCs were stimulated with a long-acting NO donor, DPTA NONOate, prior to exposure to lipopolysaccharide (LPS). Dose-and time-dependent experiments were performed with DCs with the aim of measuring the release and gene expression of inflammatory cytokines capable of modifying T-cell differentiation, towardsTh1, Th2 and Th17 cells. NO changed the pattern of cytokine release by LPS-matured DCs, dependent on the concentration of NO, as well as on the timing of its addition to the cells during maturation. Addition of NO before LPS-induced maturation strongly inhibited the release of IL-12, while increasing the expression and release of IL-23, IL-1β and IL-6, which are all involved in Th17 polarization. Indeed, DCs treated with NO efficiently induced the release of IL-17 by T-cells through IL-1β. Our work highlights the important role that NO may play in sustaining inflammation during an infection through the preferential differentiation of the Th17 lineage.The role played by lung dendritic cells (DCs) which are influenced by external antigens and by their redox state in controlling inflammation is unclear. We studied the role played by nitric oxide (NO) in DC maturation and function. Human DCs were stimulated with a long-acting NO donor, DPTA NONOate, prior to exposure to lipopolysaccharide (LPS). Dose-and time-dependent experiments were performed with DCs with the aim of measuring the release and gene expression of inflammatory cytokines capable of modifying T-cell differentiation, towardsTh1, Th2 and Th17 cells. NO changed the pattern of cytokine release by LPS-matured DCs, dependent on the concentration of NO, as well as on the timing of its addition to the cells during maturation. Addition of NO before LPS-induced maturation strongly inhibited the release of IL-12, while increasing the expression and release of IL-23, IL-1β and IL-6, which are all involved in Th17 polarization. Indeed, DCs treated with NO efficiently induced the release of IL-17 by T-cells through IL-1β. Our work highlights the important role that NO may play in sustaining inflammation during an infection through the preferential differentiation of the Th17 lineage.
Author Nicod, Laurent P.
Chung, Kian Fan
Graf, Lukas
Cesson, Valerie
Obregon, Carolina
AuthorAffiliation 2 Clinic and Polyclinic of Pneumology, University Hospital of Bern, Bern, Switzerland
University Medical Center Freiburg, GERMANY
1 Pneumology Service, Centre Hospitalier Universitaire Vaudois and University of Lausanne, Lausanne, Switzerland
3 Airways Disease Section, National Heart & Lung Institute, Imperial College, London, United Kingdom
AuthorAffiliation_xml – name: University Medical Center Freiburg, GERMANY
– name: 1 Pneumology Service, Centre Hospitalier Universitaire Vaudois and University of Lausanne, Lausanne, Switzerland
– name: 2 Clinic and Polyclinic of Pneumology, University Hospital of Bern, Bern, Switzerland
– name: 3 Airways Disease Section, National Heart & Lung Institute, Imperial College, London, United Kingdom
Author_xml – sequence: 1
  givenname: Carolina
  surname: Obregon
  fullname: Obregon, Carolina
– sequence: 2
  givenname: Lukas
  surname: Graf
  fullname: Graf, Lukas
– sequence: 3
  givenname: Kian Fan
  surname: Chung
  fullname: Chung, Kian Fan
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  givenname: Valerie
  surname: Cesson
  fullname: Cesson, Valerie
– sequence: 5
  givenname: Laurent P.
  surname: Nicod
  fullname: Nicod, Laurent P.
BackLink https://www.ncbi.nlm.nih.gov/pubmed/25853810$$D View this record in MEDLINE/PubMed
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Conceived and designed the experiments: CO LN. Performed the experiments: LG VC CO. Analyzed the data: LG VC CO KFC. Contributed reagents/materials/analysis tools: CO LN. Wrote the paper: KFC CO LN VC LG.
Competing Interests: The authors have declared that no competing interests exist.
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Snippet The role played by lung dendritic cells (DCs) which are influenced by external antigens and by their redox state in controlling inflammation is unclear. We...
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StartPage e0120134
SubjectTerms Alkenes - pharmacology
Antigens
Benzoates - pharmacology
Cell differentiation
Cytokines
Dendritic cells
Dendritic Cells - drug effects
Dendritic Cells - immunology
Dendritic Cells - metabolism
Differentiation (biology)
Dose-Response Relationship, Drug
Gene expression
Gene Expression Regulation - drug effects
Helper cells
Humans
Imidazoles - pharmacology
Inflammation
Interleukin 12
Interleukin 17
Interleukin 23
Interleukin 6
Interleukin-17 - biosynthesis
Interleukin-17 - metabolism
Interleukin-1beta - genetics
Lipopolysaccharides
Lungs
Lymphocytes T
Maturation
Nitric oxide
Nitric Oxide - pharmacology
Redox properties
T-Lymphocytes - drug effects
T-Lymphocytes - immunology
T-Lymphocytes - metabolism
Time Factors
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Title Nitric Oxide Sustains IL-1β Expression in Human Dendritic Cells Enhancing Their Capacity to Induce IL-17–Producing T-Cells
URI https://www.ncbi.nlm.nih.gov/pubmed/25853810
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http://dx.doi.org/10.1371/journal.pone.0120134
Volume 10
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