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Airway Eosinophils: Allergic Inflammation Recruited Professional Antigen-Presenting Cells¹

Hai-Bin Wang^*, Ionita Ghiran^*, Klaus Matthaei and Peter F. Weller^2,*

^* Divisions of Allergy and Inflammation and Infectious Diseases, Department of Medicine, Beth Israel Deaconess Medical Center, Harvard Medical School, Boston, MA 02115; and Gene Targeting Laboratory, Division of Molecular Bioscience, The John Curtin School of Medical Research, The Australian National University, Canberra, Australia

The capacity of airway eosinophils, potentially pertinent to allergic diseases of the upper and lower airways, to function as professional APCs, those specifically able to elicit responses from unprimed, Ag-naive CD4⁺ T cells has been uncertain. We investigated whether airway eosinophils are capable of initiating naive T cell responses in vivo. Eosinophils, isolated free of other APCs from the spleens of IL-5 transgenic mice, following culture with GM-CSF expressed MHC class II and the costimulatory proteins, CD40, CD80, and CD86. Eosinophils, incubated with OVA Ag in vitro, were instilled intratracheally into wild-type recipient mice that adoptively received i.v. infusions of OVA Ag-specific CD4⁺ T cells from OVA TCR transgenic mice. OVA-exposed eosinophils elicited activation (CD69 expression), proliferation (BrdU incorporation), and IL-4, but not IFN-, cytokine production by OVA-specific CD4⁺ T cells in paratracheal lymph nodes (LN). Exposure of eosinophils to lysosomotropic NH₄Cl, which inhibits Ag processing, blocked each of these eosinophil-mediated activation responses of CD4⁺ T cells. By three-color fluorescence microscopy, OVA Ag-loaded eosinophil APCs were physically interacting with naive OVA-specific CD4⁺ T cells in paratracheal LN after eosinophil airway instillation. Thus, recruited luminal airway eosinophils are distinct allergic "inflammatory" professional APCs able to activate primary CD4⁺ T cell responses in regional LNs.

The costs of publication of this article were defrayed in part by the payment of page charges. This article must therefore be hereby marked advertisement in accordance with 18 U.S.C. Section 1734 solely to indicate this fact.

¹ This work was supported by National Institutes of Health Grants AI20241, HL70270, and AI051645 (to P.F.W).

² Address correspondence and reprint requests to Dr. Peter F. Weller, Department of Medicine, Beth Israel Deaconess Medical Center, DA-617, 330 Brookline Avenue, Boston, MA 02215. E-mail address: pweller{at}bidmc.harvard.edu

³ Abbreviations used in this paper: DC, dendritic cell; pLN, paratracheal lymph node; MHC II, MHC class II; Tg, transgenic; BAL, bronchoalveolar lavage; i.t., intratracheal.

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