Innate-like function of memory Th17 cells for enhancing endotoxin-induced acute lung inflammation through IL-22

Ryota Sakaguchi, Shunsuke Chikuma, Takashi Shichita, Rimpei Morita, Takashi Sekiya, Wenjun Ouyang, Tomomi Ueda, Hiroyuki Seki, Hiroshi Morisaki, Akihiko Yoshimura

Research output: Contribution to journalArticle

9 Citations (Scopus)

Abstract

Lipopolysaccharide (LPS)-induced acute lung injury (ALI) is known as a mouse model of acute respiratory distress syndrome; however, the function of T-cell-derived cytokines in ALI has not yet been established. We found that LPS challenge in one lung resulted in a rapid induction of innatetype pro-inflammatory cytokines such as IL-6 and TNF-α, followed by the expression of T-cell-type cytokines, including IL-17, IL-22 and IFN-γ. We discovered that IL-23 is important for ALI, since blockage of IL-23 by gene disruption or anti-IL-12/23p40 antibody treatment reduced neutrophil infiltration and inflammatory cytokine secretion into the bronchoalveolar lavage fluid (BALF). IL-23 was mostly produced from F4/80+CD11c+ alveolar macrophages, and IL-23 expression was markedly reduced by the pre-treatment of mice with antibiotics, suggesting that the development of IL-23-producing macrophages required commensal bacteria. Unexpectedly, among T-cell-derived cytokines, IL-22 rather than IL-17 or IFN-γ played a major role in LPS-induced ALI. IL-22 protein levels were higher than IL-17 in the BALF after LPS instillation, and the major source of IL-22 was memory Th17 cells. Lung memory CD4+ T cells had a potential to produce IL-22 at higher levels than IL-17 in response to IL-1ß plus IL-23 without TCR stimulation. Our study revealed an innate-like function of the lung memory Th17 cells that produce IL-22 in response to IL-23 and are involved in exaggeration of ALI.

Original languageEnglish
Pages (from-to)233-243
Number of pages11
JournalInternational Immunology
Volume28
Issue number5
DOIs
Publication statusPublished - 2016 May 1

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Interleukin-23
Th17 Cells
Endotoxins
Pneumonia
Acute Lung Injury
Interleukin-17
Lipopolysaccharides
Cytokines
T-Lymphocytes
Bronchoalveolar Lavage Fluid
Lung
Neutrophil Infiltration
Adult Respiratory Distress Syndrome
Alveolar Macrophages
Interleukin-12
interleukin-22
Interleukin-1
Interleukin-6
Macrophages
Anti-Bacterial Agents

Keywords

  • Acute lung injury
  • Antibiotics
  • Commensal bacteria
  • Memory T17

ASJC Scopus subject areas

  • Immunology

Cite this

Innate-like function of memory Th17 cells for enhancing endotoxin-induced acute lung inflammation through IL-22. / Sakaguchi, Ryota; Chikuma, Shunsuke; Shichita, Takashi; Morita, Rimpei; Sekiya, Takashi; Ouyang, Wenjun; Ueda, Tomomi; Seki, Hiroyuki; Morisaki, Hiroshi; Yoshimura, Akihiko.

In: International Immunology, Vol. 28, No. 5, 01.05.2016, p. 233-243.

Research output: Contribution to journalArticle

Sakaguchi, Ryota ; Chikuma, Shunsuke ; Shichita, Takashi ; Morita, Rimpei ; Sekiya, Takashi ; Ouyang, Wenjun ; Ueda, Tomomi ; Seki, Hiroyuki ; Morisaki, Hiroshi ; Yoshimura, Akihiko. / Innate-like function of memory Th17 cells for enhancing endotoxin-induced acute lung inflammation through IL-22. In: International Immunology. 2016 ; Vol. 28, No. 5. pp. 233-243.
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AU - Sekiya, Takashi

AU - Ouyang, Wenjun

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AB - Lipopolysaccharide (LPS)-induced acute lung injury (ALI) is known as a mouse model of acute respiratory distress syndrome; however, the function of T-cell-derived cytokines in ALI has not yet been established. We found that LPS challenge in one lung resulted in a rapid induction of innatetype pro-inflammatory cytokines such as IL-6 and TNF-α, followed by the expression of T-cell-type cytokines, including IL-17, IL-22 and IFN-γ. We discovered that IL-23 is important for ALI, since blockage of IL-23 by gene disruption or anti-IL-12/23p40 antibody treatment reduced neutrophil infiltration and inflammatory cytokine secretion into the bronchoalveolar lavage fluid (BALF). IL-23 was mostly produced from F4/80+CD11c+ alveolar macrophages, and IL-23 expression was markedly reduced by the pre-treatment of mice with antibiotics, suggesting that the development of IL-23-producing macrophages required commensal bacteria. Unexpectedly, among T-cell-derived cytokines, IL-22 rather than IL-17 or IFN-γ played a major role in LPS-induced ALI. IL-22 protein levels were higher than IL-17 in the BALF after LPS instillation, and the major source of IL-22 was memory Th17 cells. Lung memory CD4+ T cells had a potential to produce IL-22 at higher levels than IL-17 in response to IL-1ß plus IL-23 without TCR stimulation. Our study revealed an innate-like function of the lung memory Th17 cells that produce IL-22 in response to IL-23 and are involved in exaggeration of ALI.

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