Characterization of the Anti-Inflammatory Capacity of IL-10-Producing Neutrophils in Response to Streptococcus pneumoniae Infection
Neutrophils are immune cells classically defined as pro-inflammatory effector cells. However, current accumulated evidence indicates that neutrophils have more versatile immune-modulating properties. During acute lung infection with Streptococcus pneumoniae in mice, interleukin-10 (IL-10) production...
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Format: | Article |
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Frontiers Media S.A.
2021-04-01
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Series: | Frontiers in Immunology |
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Online Access: | https://www.frontiersin.org/articles/10.3389/fimmu.2021.638917/full |
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DOAJ |
language |
English |
format |
Article |
sources |
DOAJ |
author |
Liliana A. González Felipe Melo-González Valentina P. Sebastián Omar P. Vallejos Loreani P. Noguera Isidora D. Suazo Bárbara M. Schultz Andrés H. Manosalva Hernán F. Peñaloza Jorge A. Soto Dane Parker Claudia A. Riedel Pablo A. González Alexis M. Kalergis Alexis M. Kalergis Susan M. Bueno |
spellingShingle |
Liliana A. González Felipe Melo-González Valentina P. Sebastián Omar P. Vallejos Loreani P. Noguera Isidora D. Suazo Bárbara M. Schultz Andrés H. Manosalva Hernán F. Peñaloza Jorge A. Soto Dane Parker Claudia A. Riedel Pablo A. González Alexis M. Kalergis Alexis M. Kalergis Susan M. Bueno Characterization of the Anti-Inflammatory Capacity of IL-10-Producing Neutrophils in Response to Streptococcus pneumoniae Infection Frontiers in Immunology pneumonia Streptococcus pneumoniae interleukin-10 IL-10-producing neutrophils adoptive neutrophil transfer |
author_facet |
Liliana A. González Felipe Melo-González Valentina P. Sebastián Omar P. Vallejos Loreani P. Noguera Isidora D. Suazo Bárbara M. Schultz Andrés H. Manosalva Hernán F. Peñaloza Jorge A. Soto Dane Parker Claudia A. Riedel Pablo A. González Alexis M. Kalergis Alexis M. Kalergis Susan M. Bueno |
author_sort |
Liliana A. González |
title |
Characterization of the Anti-Inflammatory Capacity of IL-10-Producing Neutrophils in Response to Streptococcus pneumoniae Infection |
title_short |
Characterization of the Anti-Inflammatory Capacity of IL-10-Producing Neutrophils in Response to Streptococcus pneumoniae Infection |
title_full |
Characterization of the Anti-Inflammatory Capacity of IL-10-Producing Neutrophils in Response to Streptococcus pneumoniae Infection |
title_fullStr |
Characterization of the Anti-Inflammatory Capacity of IL-10-Producing Neutrophils in Response to Streptococcus pneumoniae Infection |
title_full_unstemmed |
Characterization of the Anti-Inflammatory Capacity of IL-10-Producing Neutrophils in Response to Streptococcus pneumoniae Infection |
title_sort |
characterization of the anti-inflammatory capacity of il-10-producing neutrophils in response to streptococcus pneumoniae infection |
publisher |
Frontiers Media S.A. |
series |
Frontiers in Immunology |
issn |
1664-3224 |
publishDate |
2021-04-01 |
description |
Neutrophils are immune cells classically defined as pro-inflammatory effector cells. However, current accumulated evidence indicates that neutrophils have more versatile immune-modulating properties. During acute lung infection with Streptococcus pneumoniae in mice, interleukin-10 (IL-10) production is required to temper an excessive lung injury and to improve survival, yet the cellular source of IL-10 and the immunomodulatory role of neutrophils during S. pneumoniae infection remain unknown. Here we show that neutrophils are the main myeloid cells that produce IL-10 in the lungs during the first 48 h of infection. Importantly, in vitro assays with bone-marrow derived neutrophils confirmed that IL-10 can be induced by these cells by the direct recognition of pneumococcal antigens. In vivo, we identified the recruitment of two neutrophil subpopulations in the lungs following infection, which exhibited clear morphological differences and a distinctive profile of IL-10 production at 48 h post-infection. Furthermore, adoptive transfer of neutrophils from WT mice into IL-10 knockout mice (Il10-/-) fully restored IL-10 production in the lungs and reduced lung histopathology. These results suggest that IL-10 production by neutrophils induced by S. pneumoniae limits lung injury and is important to mediate an effective immune response required for host survival. |
topic |
pneumonia Streptococcus pneumoniae interleukin-10 IL-10-producing neutrophils adoptive neutrophil transfer |
url |
https://www.frontiersin.org/articles/10.3389/fimmu.2021.638917/full |
work_keys_str_mv |
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doaj-3b6b24aea2d74f65890f1cab496d0f5a2021-04-28T07:25:13ZengFrontiers Media S.A.Frontiers in Immunology1664-32242021-04-011210.3389/fimmu.2021.638917638917Characterization of the Anti-Inflammatory Capacity of IL-10-Producing Neutrophils in Response to Streptococcus pneumoniae InfectionLiliana A. González0Felipe Melo-González1Valentina P. Sebastián2Omar P. Vallejos3Loreani P. Noguera4Isidora D. Suazo5Bárbara M. Schultz6Andrés H. Manosalva7Hernán F. Peñaloza8Jorge A. Soto9Dane Parker10Claudia A. Riedel11Pablo A. González12Alexis M. Kalergis13Alexis M. Kalergis14Susan M. Bueno15Millennium Institute on Immunology and Immunotherapy, Departamento de Genética Molecular y Microbiología, Facultad de Ciencias Biológicas, Pontificia Universidad Católica de Chile, Santiago, ChileMillennium Institute on Immunology and Immunotherapy, Departamento de Genética Molecular y Microbiología, Facultad de Ciencias Biológicas, Pontificia Universidad Católica de Chile, Santiago, ChileMillennium Institute on Immunology and Immunotherapy, Departamento de Genética Molecular y Microbiología, Facultad de Ciencias Biológicas, Pontificia Universidad Católica de Chile, Santiago, ChileMillennium Institute on Immunology and Immunotherapy, Departamento de Genética Molecular y Microbiología, Facultad de Ciencias Biológicas, Pontificia Universidad Católica de Chile, Santiago, ChileMillennium Institute on Immunology and Immunotherapy, Departamento de Genética Molecular y Microbiología, Facultad de Ciencias Biológicas, Pontificia Universidad Católica de Chile, Santiago, ChileMillennium Institute on Immunology and Immunotherapy, Departamento de Genética Molecular y Microbiología, Facultad de Ciencias Biológicas, Pontificia Universidad Católica de Chile, Santiago, ChileMillennium Institute on Immunology and Immunotherapy, Departamento de Genética Molecular y Microbiología, Facultad de Ciencias Biológicas, Pontificia Universidad Católica de Chile, Santiago, ChileServicio de Anatomía Patológica, Hospital Barros Luco Trudeau, Santiago, ChileAcute Lung Injury Center of Excellence, Division of Pulmonary, Allergy, and Critical Care Medicine, Department of Medicine, University of Pittsburgh, Pittsburgh, PA, United StatesMillennium Institute on Immunology and Immunotherapy, Departamento de Genética Molecular y Microbiología, Facultad de Ciencias Biológicas, Pontificia Universidad Católica de Chile, Santiago, ChileDepartment of Pathology, Immunology and Laboratory Medicine, Center for Immunity and Inflammation, Rutgers New Jersey Medical School, Newark, NJ, United StatesMillennium Institute on Immunology and Immunotherapy, Departamento de Biología Celular, Facultad de Ciencias Biológicas y Facultad de Medicina, Universidad Andrés Bello, Santiago, ChileMillennium Institute on Immunology and Immunotherapy, Departamento de Genética Molecular y Microbiología, Facultad de Ciencias Biológicas, Pontificia Universidad Católica de Chile, Santiago, ChileMillennium Institute on Immunology and Immunotherapy, Departamento de Genética Molecular y Microbiología, Facultad de Ciencias Biológicas, Pontificia Universidad Católica de Chile, Santiago, ChileDepartamento de Endocrinología, Facultad de Medicina, Pontificia Universidad Católica de Chile, Santiago, ChileMillennium Institute on Immunology and Immunotherapy, Departamento de Genética Molecular y Microbiología, Facultad de Ciencias Biológicas, Pontificia Universidad Católica de Chile, Santiago, ChileNeutrophils are immune cells classically defined as pro-inflammatory effector cells. However, current accumulated evidence indicates that neutrophils have more versatile immune-modulating properties. During acute lung infection with Streptococcus pneumoniae in mice, interleukin-10 (IL-10) production is required to temper an excessive lung injury and to improve survival, yet the cellular source of IL-10 and the immunomodulatory role of neutrophils during S. pneumoniae infection remain unknown. Here we show that neutrophils are the main myeloid cells that produce IL-10 in the lungs during the first 48 h of infection. Importantly, in vitro assays with bone-marrow derived neutrophils confirmed that IL-10 can be induced by these cells by the direct recognition of pneumococcal antigens. In vivo, we identified the recruitment of two neutrophil subpopulations in the lungs following infection, which exhibited clear morphological differences and a distinctive profile of IL-10 production at 48 h post-infection. Furthermore, adoptive transfer of neutrophils from WT mice into IL-10 knockout mice (Il10-/-) fully restored IL-10 production in the lungs and reduced lung histopathology. These results suggest that IL-10 production by neutrophils induced by S. pneumoniae limits lung injury and is important to mediate an effective immune response required for host survival.https://www.frontiersin.org/articles/10.3389/fimmu.2021.638917/fullpneumoniaStreptococcus pneumoniaeinterleukin-10IL-10-producing neutrophilsadoptive neutrophil transfer |