The Journal of Allergy and Clinical Immunology
Volume 124, Issue 5 , Pages 913-920.e7 , November 2009

Tissue remodeling induced by hypersecreted epidermal growth factor and amphiregulin in the airway after an acute asthma attack

  • Yukinori Enomoto, BSc

      Affiliations

    • Division of Molecular Cell Immunology and Allergology, Advanced Medical Research Center, Nihon University Graduate School of Medical Science, Tokyo, Japan
    • Department of Environmental Immuno-Dermatology, Yokohama City University School of Medicine, Kanagawa, Japan
    • ,
  • Kanami Orihara, PhD

      Affiliations

    • Department of Allergy and Immunology, National Research Institute for Child Health and Development, Tokyo, Japan
    • ,
  • Tetsuya Takamasu, MD

      Affiliations

    • Department of Allergy, Kanagawa Children's Medical Center, Kanagawa, Japan
    • Corresponding Author InformationTetsuya Takamasu, MD, Department of Allergy, Kanagawa Children's Medical Center, Kanagawa, Japan.
    • ,
  • Akio Matsuda, PhD

      Affiliations

    • Department of Allergy and Immunology, National Research Institute for Child Health and Development, Tokyo, Japan
    • ,
  • Yasuhiro Gon, MD, PhD

      Affiliations

    • Division of Molecular Cell Immunology and Allergology, Advanced Medical Research Center, Nihon University Graduate School of Medical Science, Tokyo, Japan
    • ,
  • Hirohisa Saito, MD, PhD

      Affiliations

    • Department of Allergy and Immunology, National Research Institute for Child Health and Development, Tokyo, Japan
    • ,
  • Chisei Ra, MD, PhD

      Affiliations

    • Division of Molecular Cell Immunology and Allergology, Advanced Medical Research Center, Nihon University Graduate School of Medical Science, Tokyo, Japan
    • ,
  • Yoshimichi Okayama, MD, PhD

      Affiliations

    • Division of Molecular Cell Immunology and Allergology, Advanced Medical Research Center, Nihon University Graduate School of Medical Science, Tokyo, Japan
    • Corresponding Author InformationReprint requests: Yoshimichi Okayama, MD, PhD, Division of Molecular Cell Immunology and Allergology, Advanced Medical Research Center, Nihon University Graduate School of Medical Science, 30-1 Oyaguchikami-machi, Itabashi-ku, Tokyo 173-8610, Japan.

Received 8 April 2009 ,Revised 23 July 2009 ,Accepted 20 August 2009.

References 

  1. Cohn L, Elias JA, Chupp GL. Asthma: mechanisms of disease persistence and progression. Annu Rev Immunol. 2004;22:789–815
  2. Busse W, Elias J, Sheppard D, Banks-Schlegel S. Airway remodeling and repair. Am J Respir Crit Care Med. 1999;160:1035–1042
  3. Phipps S, Benyahia F, Ou TT, Barkans J, Robinson DS, Kay AB. Acute allergen-induced airway remodeling in atopic asthma. Am J Respir Cell Mol Biol. 2004;31:626–632
  4. Cohen L, E X, Tarsi J, Ramkumar T, Horiuchi TK, Cochran R, et al. Epithelial cell proliferation contributes to airway remodeling in severe asthma. Am J Respir Crit Care Med. 2007;176:138–145
  5. Hamilton LM, Puddicombe SM, Dearman RJ, Kimber I, Sandstrom T, Wallin A, et al. Altered protein tyrosine phosphorylation in asthmatic bronchial epithelium. Eur Respir J. 2005;25:978–985
  6. Polosa R, Prosperini G, Leir SH, Holgate ST, Lackie PM, Davies DE. Expression of c-erbB receptors and ligands in human bronchial mucosa. Am J Respir Cell Mol Biol. 1999;20:914–923
  7. Barrow RE, Wang CZ, Evans MJ, Herndon DN. Growth factors accelerate epithelial repair in sheep trachea. Lung. 1993;171:335–344
  8. Dorscheid DR, Wojcik KR, Yule K, White SR. Role of cell surface glycosylation in mediating repair of human airway epithelial cell monolayers. Am J Physiol Lung Cell Mol Physiol. 2001;281:L982–L992
  9. Okumura S, Sagara H, Fukuda T, Saito H, Okayama Y. FcepsilonRI-mediated amphiregulin production by human mast cells increases mucin gene expression in epithelial cells. J Allergy Clin Immunol. 2005;115:272–279
  10. Fahy JV. Goblet cell and mucin gene abnormalities in asthma. Chest. 2002;122:320S–326S
  11. Willey JC, Laveck MA, McClendon IA, Lechner JF. Relationship of ornithine decarboxylase activity and cAMP metabolism to proliferation of normal human bronchial epithelial cells. J Cell Physiol. 1985;124:207–212
  12. Yoshisue H, Kirkham-Brown J, Healy E, Holgate ST, Sampson AP, Davies DE. Cysteinyl leukotrienes synergize with growth factors to induce proliferation of human bronchial fibroblasts. J Allergy Clin Immunol. 2007;119:132–140
  13. Ediger TL, Toews ML. Synergistic stimulation of airway smooth muscle cell mitogenesis. J Pharmacol Exp Ther. 2000;294:1076–1082
  14. Perrais M, Pigny P, Copin MC, Aubert JP, Van Seuningen I. Induction of MUC2 and MUC5AC mucins by factors of the epidermal growth factor (EGF) family is mediated by EGF receptor/Ras/Raf/extracellular signal-regulated kinase cascade and Sp1. J Biol Chem. 2002;277:32258–32267
  15. Schuger L, Johnson GR, Gilbride K, Plowman GD, Mandel R. Amphiregulin in lung branching morphogenesis: interaction with heparan sulfate proteoglycan modulates cell proliferation. Development. 1996;122:1759–1767
  16. Ogawa Y, Calhoun WJ. The role of leukotrienes in airway inflammation. J Allergy Clin Immunol. 2006;118:789–798
  17. Allahverdian S, Harada N, Singhera GK, Knight DA, Dorscheid DR. Secretion of IL-13 by airway epithelial cells enhances epithelial repair via HB-EGF. Am J Respir Cell Mol Biol. 2008;38:153–160
  18. Holgate ST. The airway epithelium is central to the pathogenesis of asthma. Allergol Int. 2008;57:1–10
  19. Willmarth NE, Ethier SP. Autocrine and juxtacrine effects of amphiregulin on the proliferative, invasive, and migratory properties of normal and neoplastic human mammary epithelial cells. J Biol Chem. 2006;281:37728–37737
  20. Streicher KL, Willmarth NE, Garcia J, Boerner JL, Dewey TG, Ethier SP. Activation of a nuclear factor kappaB/interleukin-1 positive feedback loop by amphiregulin in human breast cancer cells. Mol Cancer Res. 2007;5:847–861
  21. Wolff GS, Chiang PJ, Smith SM, Romero R, Armant DR. Epidermal growth factor-like growth factors prevent apoptosis of alcohol-exposed human placental cytotrophoblast cells. Biol Reprod. 2007;77:53–60
  22. Adam R, Drummond DR, Solic N, Holt SJ, Sharma RP, Chamberlin SG, et al. Modulation of the receptor binding affinity of amphiregulin by modification of its carboxyl terminal tail. Biochim Biophys Acta. 1995;1266:83–90
  23. Gilmore JL, Scott JA, Bouizar Z, Robling A, Pitfield SE, Riese DJ, et al. Amphiregulin-EGFR signaling regulates PTHrP gene expression in breast cancer cells. Breast Cancer Res Treat. 2008;110:493–505
  24. Levkowitz G, Waterman H, Zamir E, Kam Z, Oved S, Langdon WY, et al. c-Cbl/Sli-1 regulates endocytic sorting and ubiquitination of the epidermal growth factor receptor. Genes Dev. 1998;12:3663–3674
  25. Levkowitz G, Waterman H, Ettenberg SA, Katz M, Tsygankov AY, Alroy I, et al. Ubiquitin ligase activity and tyrosine phosphorylation underlie suppression of growth factor signaling by c-Cbl/Sli-1. Mol Cell. 1999;4:1029–1040
  26. Olayioye MA, Neve RM, Lane HA, Hynes NE. The ErbB signaling network: receptor heterodimerization in development and cancer. EMBO J. 2000;19:3159–3167
  27. Tao RH, Maruyama IN. All EGF(ErbB) receptors have preformed homo- and heterodimeric structures in living cells. J Cell Sci. 2008;121:3207–3217
  28. Wilson KJ, Gilmore JL, Foley J, Lemmon MA, Riese DJ. Functional selectivity of EGF family peptide growth factors: Implications for cancer. Pharmacol Ther. 2009;122:1–8
  29. Casalino-Matsuda SM, Monzon ME, Forteza RM. Epidermal growth factor receptor activation by epidermal growth factor mediates oxidant-induced goblet cell metaplasia in human airway epithelium. Am J Respir Cell Mol Biol. 2006;34:581–591
  30. Zhen G, Park SW, Nguyenvu LT, Rodriguez MW, Barbeau R, Paquet AC, et al. IL-13 and epidermal growth factor receptor have critical but distinct roles in epithelial cell mucin production. Am J Respir Cell Mol Biol. 2007;36:244–253
  31. Shao MX, Nadel JA. Neutrophil elastase induces MUC5AC mucin production in human airway epithelial cells via a cascade involving protein kinase C, reactive oxygen species, and TNF-alpha-converting enzyme. J Immunol. 2005;175:4009–4016
  32. McDowell EM, Keenan KP, Huang M. Effects of vitamin A-deprivation on hamster tracheal epithelium: a quantitative morphologic study. Virchows Arch B Cell Pathol Incl Mol Pathol. 1984;45:197–219
  33. Hartl D, He CH, Koller B, Da Silva CA, Homer R, Lee CG, et al. Acidic mammalian chitinase is secreted via an ADAM17/epidermal growth factor receptor-dependent pathway and stimulates chemokine production by pulmonary epithelial cells. J Biol Chem. 2008;283:33472–33482

 Supported in part by Grants-in-Aid for Scientific Research (C) programs of the Ministry of Education, Culture, Sports, Science and Technology of the Japanese Government (project nos. 18604009 and 20591195, awarded to Y.O.), the Nihon University Joint Research Grant for 2008 (awarded to Y.O), a grant from the National Institute of Biomedical Innovation (project no. ID05-24, awarded to H.S. and Y.O.), and the Matching Fund Subsidy for Private Universities from the Ministry of Education, Culture, Sports, Science and Technology of the Japanese Government (to C.R).

 Disclosure of potential conflict of interest: H. Saito has received research support from the National Institute of Biomedical Innovation. The rest of the authors have declared that they have no conflict of interest.

PII: S0091-6749(09)01328-1

doi: 10.1016/j.jaci.2009.08.044

The Journal of Allergy and Clinical Immunology
Volume 124, Issue 5 , Pages 913-920.e7 , November 2009

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