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Possible Role of IL-25 in Eosinophilic Lung Inflammation in Patients with Chronic Eosinophilic Pneumonia

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Abstract

Purpose

Interleukin (IL)-25 and IL-33 induce IL-5 production by various types of cells, such as type 2 helper T (Th2) cells and type 2 innate lymphoid cells. The number of Th2 cells and concentration of IL-5 in the bronchoalveolar lavage fluid (BALF) are increased in patients with eosinophilic pneumonia (EP). To examine the contribution of IL-25 and IL-33 to eosinophilic inflammation of the lung in humans, we evaluated IL-5, IL-25 and IL-33 levels in the BALF of patients with EP.

Methods

IL-5, IL-25, and IL-33 concentrations in the BALF were measured by enzyme-linked immunosorbent assay in patients with acute eosinophilic pneumonia (AEP), chronic eosinophilic pneumonia (CEP), idiopathic pulmonary fibrosis (IPF), and sarcoidosis.

Results

The absolute number of eosinophils, and IL-5 levels, but not IL-33 levels, in the BALF were significantly higher in patients with EP than in patients with IPF and sarcoidosis. IL-25 levels in the BALF were significantly higher in patients with CEP, but not in patients with AEP, than in patients with IPF and sarcoidosis. The absolute number of eosinophils was significantly correlated with the IL-5 concentration in the BALF of patients with EP. IL-5 concentrations were significantly correlated with IL-25 concentrations in the BALF of patients with CEP, but not in patients with AEP. IL-5 levels were not correlated with IL-33 levels in the BALF of patients with EP.

Conclusions

Our findings suggest that IL-25 plays an important role via IL-5 in eosinophilic lung inflammation in patients with CEP.

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References

  1. Liebow AA, Carrington CB (1969) The eosinophilic pneumonia. Medicine 48:251–255

    Article  CAS  PubMed  Google Scholar 

  2. Allen JN (2006) Acute eosinophilic pneumonia. Semin Respir Crit Care Med 27:142–147

    Article  PubMed  Google Scholar 

  3. Marchand E, Cordier JF (2006) Idiopathic chronic eosinophilic pneumonia. Semin Respir Crit Care Med 27:134–141

    Article  PubMed  Google Scholar 

  4. Katoh S, Taniguchi H, Matsubara Y et al (1999) Overexpression of CD44 on alveolar eosinophils with high concentrations of soluble CD44 in bronchoalveolar lavage fluid in patients with eosinophilic pneumonia. Allergy 54:1286–1292

    Article  CAS  PubMed  Google Scholar 

  5. Katoh S, Matsumoto N, Matsumoto K et al (2004) Elevated interleukin-18 levels in bronchoalveolar lavage fluid of patients with eosinophilic pneumonia. Allergy 59:850–856

    Article  CAS  PubMed  Google Scholar 

  6. Katoh S, Fukushima K, Matsumoto N et al (2003) Accumulation of CCR4-expressing CD4 + T cells and high concentration of its ligands (TARC and MDC) in bronchoalveolar lavage fluid of patients with eosinophilic pneumonia. Allergy 58:518–523

    Article  CAS  PubMed  Google Scholar 

  7. Iwakura Y, Ishigame H, Saijo S et al (2011) Functional specialization of interleukin-17 family members. Immunity 34:149–162

    Article  CAS  PubMed  Google Scholar 

  8. Ohno T, Morita H, Arae K et al (2012) Interleukin-33 in allergy. Allergy 67:1203–1214

    Article  CAS  PubMed  Google Scholar 

  9. Ziegier SF (2012) Thymic stromal lymphopoietin and allergic disease. J Allergy Clin Immunol 130:845–852

    Article  Google Scholar 

  10. Ikutani M, Yanagibashi T, Ogasawara M et al (2012) Identification of innate IL-5-producing cells and their role in lung eosinophils regulating and antitumor immunity. J Immunol 188:703–713

    Article  CAS  PubMed  Google Scholar 

  11. Halim TYF, Krauss RH, Sun AC et al (2012) Lung natural helper cells are a critical source of Th2 cell-type cytokines in protease allergen-induced airway inflammation. Immunity 36:451–463

    Article  CAS  PubMed  Google Scholar 

  12. Yasuda K, Muto T, Kawagoe T et al (2012) Contribution of IL-33-activated type II innate lymphoid cells to pulmonary eosinophilia in intestinal nematode-infected mice. Proc Natl Acad Sci 109:3451–3456

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  13. Brusselle GG, Maes T, Bracke KR (2013) Eosinophilic airway inflammation in nonallergic asthma. Nat Med 19:977–979

    Article  CAS  PubMed  Google Scholar 

  14. Yu S, Kim HY, Chang Y-J et al (2014) Innate lymphoid cells and asthma. J Allergy Clin Immunol 133:943–950

    Article  CAS  PubMed  Google Scholar 

  15. Travis WD, Costabel U, Hansell DM et al (2013) ATS/ERS Committee on Idiopathic Interstitial Pneumonias. An official American thoracic society/European respiratory society statement: update of the international multidisciplinary classification of the idiopathic interstitial pneumonias. Am J Respir Crit Care Med 188:733–748

    Article  PubMed  Google Scholar 

  16. Katoh S, Matsumoto N, Fukushima K et al (2000) Elevated chemokines levels in bronchoalveolar lavage fluid of patients with eosinophilic pneumonia. J Allergy Clin Immunol 106:730–736

    Article  CAS  PubMed  Google Scholar 

  17. Valizadeh A, Khosravi A, Zadeh LJ et al (2015) Role of IL-25 in immunity. J Clin Diag Res 9(4):OE01–OE04

    Google Scholar 

  18. Tang W, Smith SG, Beaudin S et al (2014) IL-25 and IL-25 receptor expression on eosinophils from subjects with allergic asthma. Int Arch Allergy Immunol 163:5–10

    Article  CAS  PubMed  Google Scholar 

  19. Terrier B, Bieche I, Maisonobe T et al (2010) Interleukin-25: a cytokine linking eosinophils and adaptive immunity in Churg–Strauss syndrome. Blood 116:4523–4531

    Article  CAS  PubMed  Google Scholar 

  20. Endo Y, Nakayama T (2015) Pathogenic Th2 (Tpath2) cells in airway inflammation. Oncotarget 6:32303–32304

    Article  PubMed  PubMed Central  Google Scholar 

  21. Liu B, Lee J-B, Chen C-Y et al (2015) Collaborative interactions between type 2 innate lymphoid cells and antigen-specific CD4 + Th2 cells exacerbate murine allergic airway diseases with prominent eosinophilia. J Immunol 194:3583–3593

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  22. Kamijo S, Takeda H, Tokura T et al (2013) IL-33-mediated innate response and adaptive immune cells contribute to maximum responses of protease allergen-induced allergic airway inflammation. J Immunol 190:4489–4499

    CAS  PubMed  Google Scholar 

  23. Barlow JL, Peel S, Fox J et al (2013) IL-33 is more potent than IL-25 in provoking IL-13-producing nuocytes (type 2 innate lymphoid cells) and airway contraction. J Allergy Clin Immunol 132:933–941

    Article  CAS  PubMed  Google Scholar 

  24. Kim H-R, Jun C-D, Lee Y-J et al (2010) Levels of circulating IL-33 and eosinophil cationic protein in patients with hypereosinophilia or pulmonary eosinophilia. J Allergy Clin Immunol 126:880–882

    Article  PubMed  Google Scholar 

  25. Mato N, Bando M, Kusano A et al (2013) Clinical significance of interleukin 33 (IL-33) in patients with eosinophilic pneumonia. Allergol Int 62:45–52

    Article  CAS  PubMed  Google Scholar 

  26. Jeong YJ, Kim K-I, Seo IJ et al (2007) Eosinophilic lung diseases: a clinical, radiologic, and pathologic overview. RadioGraphics 27:617–639

    Article  PubMed  Google Scholar 

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Acknowledgements

The authors thank Ms. Tae Uesaka and Ms. Mariko Takaya for their skillful assistance. This research received no specific grant from any funding agency in the public, commercial, or not-for-profit sectors.

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Authors and Affiliations

  1. Department of Respiratory Medicine, Kawasaki Medical School, 577 Matsushima, Kurashiki, Okayama, 701-0192, Japan

    Shigeki Katoh, Masaki Ikeda, Hiroki Shimizu, Masaaki Abe, Yoshihiro Ohue, Keiji Mouri, Yoshihiro Kobashi & Mikio Oka

  2. Neurology, Respirology, Endocrinology, and Metabolism, Department of Internal Medicine, Faculty of Medicine, University of Miyazaki, Miyazaki, Japan

    Nobuhiro Matsumoto & Masamitsu Nakazato

Authors
  1. Shigeki Katoh
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  2. Masaki Ikeda
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  3. Nobuhiro Matsumoto
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  4. Hiroki Shimizu
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  5. Masaaki Abe
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  6. Yoshihiro Ohue
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  7. Keiji Mouri
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  8. Yoshihiro Kobashi
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  9. Masamitsu Nakazato
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  10. Mikio Oka
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Corresponding author

Correspondence to Shigeki Katoh.

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The authors have no conflict of interest to declare.

Ethical Approval

All procedures performed in studies involving human participants were in accordance with the ethical standards of the institutional and/or national research committee and with the 1964 Helsinki declaration and its later amendments or comparable ethical standards.

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Katoh, S., Ikeda, M., Matsumoto, N. et al. Possible Role of IL-25 in Eosinophilic Lung Inflammation in Patients with Chronic Eosinophilic Pneumonia. Lung 195, 707–712 (2017). https://doi.org/10.1007/s00408-017-0048-8

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  • DOI: https://doi.org/10.1007/s00408-017-0048-8

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