Distinct effects of endogenous interleukin-23 on eosinophilic airway inflammation in response to different antigens

Rika Ogawa, Yusuke Suzuki, Shizuko Kagawa, Katsunori Masaki, Koichi Fukunaga, Akihiko Yoshimura, Seitaro Fujishima, Takeshi Terashima, Tomoko Betsuyaku, Koichiro Asano

Research output: Contribution to journalArticle

2 Citations (Scopus)

Abstract

Background: The role of interleukin (IL)-23 in asthma pathophysiology is still controversial. We examined its role in allergic airway inflammation in response to two distinct antigens using IL-23-deficient mice. Methods: Allergic airway inflammation was evaluated in wild-type and IL-23p19 <sup>-/-</sup> mice. Mice were sensitized to ovalbumin (OVA) or house dust mite (HDM) by intraperitoneal injection of antigen and their airways were then exposed to the same antigen. Levels of antigen-specific immunoglobulins in serum as well as cytokines in bronchoalveolar or peritoneal lavage fluid and lung tissue were determined by enzyme-linked immunosorbent assay and/or quantitative polymerase chain reaction. Results: Deficiency of IL-23p19 decreased eosinophils and Th2 cytokines in bronchoalveolar lavage fluid (BALF) of OVA-treated mice, while it increased BALF eosinophils of HDM-treated mice. Peritoneal injection of OVA with alum, but not of HDM, induced local synthesis of IL-6, IL-10, and IL-23. Systemic production of antigen-specific IgG<inf>1</inf> was partially dependent on IL-23. In contrast, airway exposure to HDM, but not to OVA, induced IL-23p19 mRNA expression in the lungs. In IL-23p19-deficient mice, HDM-exposed lungs did not exhibit the induction of IL-17A, which negatively regulates eosinophilic inflammation. Conclusions: Different antigens induced IL-23 at different part of the body in our similar asthma models. Endogenous IL-23 production at the site of antigen sensitization facilitates type-2 immune responses, whereas IL-23 production and subsequent IL-17A synthesis in the airways suppresses allergic inflammation.

Original languageEnglish
JournalAllergology International
DOIs
Publication statusAccepted/In press - 2015 Jan 4

Fingerprint

Interleukin-23
Pyroglyphidae
Inflammation
Antigens
Interleukins
Ovalbumin
Interleukin-17
Bronchoalveolar Lavage Fluid
Eosinophils
Lung
Asthma
Cytokines
Peritoneal Lavage
Ascitic Fluid
Bronchoalveolar Lavage
Intraperitoneal Injections
Human Body
Interleukin-10
Immunoglobulins
Interleukin-6

Keywords

  • Asthma
  • Eosinophils
  • Interleukin-17A
  • Interleukin-23
  • Th17

ASJC Scopus subject areas

  • Immunology and Allergy

Cite this

Distinct effects of endogenous interleukin-23 on eosinophilic airway inflammation in response to different antigens. / Ogawa, Rika; Suzuki, Yusuke; Kagawa, Shizuko; Masaki, Katsunori; Fukunaga, Koichi; Yoshimura, Akihiko; Fujishima, Seitaro; Terashima, Takeshi; Betsuyaku, Tomoko; Asano, Koichiro.

In: Allergology International, 04.01.2015.

Research output: Contribution to journalArticle

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title = "Distinct effects of endogenous interleukin-23 on eosinophilic airway inflammation in response to different antigens",
abstract = "Background: The role of interleukin (IL)-23 in asthma pathophysiology is still controversial. We examined its role in allergic airway inflammation in response to two distinct antigens using IL-23-deficient mice. Methods: Allergic airway inflammation was evaluated in wild-type and IL-23p19 -/- mice. Mice were sensitized to ovalbumin (OVA) or house dust mite (HDM) by intraperitoneal injection of antigen and their airways were then exposed to the same antigen. Levels of antigen-specific immunoglobulins in serum as well as cytokines in bronchoalveolar or peritoneal lavage fluid and lung tissue were determined by enzyme-linked immunosorbent assay and/or quantitative polymerase chain reaction. Results: Deficiency of IL-23p19 decreased eosinophils and Th2 cytokines in bronchoalveolar lavage fluid (BALF) of OVA-treated mice, while it increased BALF eosinophils of HDM-treated mice. Peritoneal injection of OVA with alum, but not of HDM, induced local synthesis of IL-6, IL-10, and IL-23. Systemic production of antigen-specific IgG1 was partially dependent on IL-23. In contrast, airway exposure to HDM, but not to OVA, induced IL-23p19 mRNA expression in the lungs. In IL-23p19-deficient mice, HDM-exposed lungs did not exhibit the induction of IL-17A, which negatively regulates eosinophilic inflammation. Conclusions: Different antigens induced IL-23 at different part of the body in our similar asthma models. Endogenous IL-23 production at the site of antigen sensitization facilitates type-2 immune responses, whereas IL-23 production and subsequent IL-17A synthesis in the airways suppresses allergic inflammation.",
keywords = "Asthma, Eosinophils, Interleukin-17A, Interleukin-23, Th17",
author = "Rika Ogawa and Yusuke Suzuki and Shizuko Kagawa and Katsunori Masaki and Koichi Fukunaga and Akihiko Yoshimura and Seitaro Fujishima and Takeshi Terashima and Tomoko Betsuyaku and Koichiro Asano",
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AU - Ogawa, Rika

AU - Suzuki, Yusuke

AU - Kagawa, Shizuko

AU - Masaki, Katsunori

AU - Fukunaga, Koichi

AU - Yoshimura, Akihiko

AU - Fujishima, Seitaro

AU - Terashima, Takeshi

AU - Betsuyaku, Tomoko

AU - Asano, Koichiro

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N2 - Background: The role of interleukin (IL)-23 in asthma pathophysiology is still controversial. We examined its role in allergic airway inflammation in response to two distinct antigens using IL-23-deficient mice. Methods: Allergic airway inflammation was evaluated in wild-type and IL-23p19 -/- mice. Mice were sensitized to ovalbumin (OVA) or house dust mite (HDM) by intraperitoneal injection of antigen and their airways were then exposed to the same antigen. Levels of antigen-specific immunoglobulins in serum as well as cytokines in bronchoalveolar or peritoneal lavage fluid and lung tissue were determined by enzyme-linked immunosorbent assay and/or quantitative polymerase chain reaction. Results: Deficiency of IL-23p19 decreased eosinophils and Th2 cytokines in bronchoalveolar lavage fluid (BALF) of OVA-treated mice, while it increased BALF eosinophils of HDM-treated mice. Peritoneal injection of OVA with alum, but not of HDM, induced local synthesis of IL-6, IL-10, and IL-23. Systemic production of antigen-specific IgG1 was partially dependent on IL-23. In contrast, airway exposure to HDM, but not to OVA, induced IL-23p19 mRNA expression in the lungs. In IL-23p19-deficient mice, HDM-exposed lungs did not exhibit the induction of IL-17A, which negatively regulates eosinophilic inflammation. Conclusions: Different antigens induced IL-23 at different part of the body in our similar asthma models. Endogenous IL-23 production at the site of antigen sensitization facilitates type-2 immune responses, whereas IL-23 production and subsequent IL-17A synthesis in the airways suppresses allergic inflammation.

AB - Background: The role of interleukin (IL)-23 in asthma pathophysiology is still controversial. We examined its role in allergic airway inflammation in response to two distinct antigens using IL-23-deficient mice. Methods: Allergic airway inflammation was evaluated in wild-type and IL-23p19 -/- mice. Mice were sensitized to ovalbumin (OVA) or house dust mite (HDM) by intraperitoneal injection of antigen and their airways were then exposed to the same antigen. Levels of antigen-specific immunoglobulins in serum as well as cytokines in bronchoalveolar or peritoneal lavage fluid and lung tissue were determined by enzyme-linked immunosorbent assay and/or quantitative polymerase chain reaction. Results: Deficiency of IL-23p19 decreased eosinophils and Th2 cytokines in bronchoalveolar lavage fluid (BALF) of OVA-treated mice, while it increased BALF eosinophils of HDM-treated mice. Peritoneal injection of OVA with alum, but not of HDM, induced local synthesis of IL-6, IL-10, and IL-23. Systemic production of antigen-specific IgG1 was partially dependent on IL-23. In contrast, airway exposure to HDM, but not to OVA, induced IL-23p19 mRNA expression in the lungs. In IL-23p19-deficient mice, HDM-exposed lungs did not exhibit the induction of IL-17A, which negatively regulates eosinophilic inflammation. Conclusions: Different antigens induced IL-23 at different part of the body in our similar asthma models. Endogenous IL-23 production at the site of antigen sensitization facilitates type-2 immune responses, whereas IL-23 production and subsequent IL-17A synthesis in the airways suppresses allergic inflammation.

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KW - Interleukin-23

KW - Th17

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