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Lung-resident eosinophils represent a distinct regulatory eosinophil subset
Claire Mesnil, … , Thomas Marichal, Fabrice Bureau
Claire Mesnil, … , Thomas Marichal, Fabrice Bureau
Published August 22, 2016
Citation Information: J Clin Invest. 2016;126(9):3279-3295. https://doi.org/10.1172/JCI85664.
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Research Article Immunology Pulmonology

Lung-resident eosinophils represent a distinct regulatory eosinophil subset

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Abstract

Increases in eosinophil numbers are associated with infection and allergic diseases, including asthma, but there is also evidence that eosinophils contribute to homeostatic immune processes. In mice, the normal lung contains resident eosinophils (rEos), but their function has not been characterized. Here, we have reported that steady-state pulmonary rEos are IL-5–independent parenchymal Siglec-FintCD62L+CD101lo cells with a ring-shaped nucleus. During house dust mite–induced airway allergy, rEos features remained unchanged, and rEos were accompanied by recruited inflammatory eosinophils (iEos), which were defined as IL-5–dependent peribronchial Siglec-FhiCD62L–CD101hi cells with a segmented nucleus. Gene expression analyses revealed a more regulatory profile for rEos than for iEos, and correspondingly, mice lacking lung rEos showed an increase in Th2 cell responses to inhaled allergens. Such elevation of Th2 responses was linked to the ability of rEos, but not iEos, to inhibit the maturation, and therefore the pro-Th2 function, of allergen-loaded DCs. Finally, we determined that the parenchymal rEos found in nonasthmatic human lungs (Siglec-8+CD62L+IL-3Rlo cells) were phenotypically distinct from the iEos isolated from the sputa of eosinophilic asthmatic patients (Siglec-8+CD62LloIL-3Rhi cells), suggesting that our findings in mice are relevant to humans. In conclusion, our data define lung rEos as a distinct eosinophil subset with key homeostatic functions.

Authors

Claire Mesnil, Stéfanie Raulier, Geneviève Paulissen, Xue Xiao, Mark A. Birrell, Dimitri Pirottin, Thibaut Janss, Philipp Starkl, Eve Ramery, Monique Henket, Florence N. Schleich, Marc Radermecker, Kris Thielemans, Laurent Gillet, Marc Thiry, Maria G. Belvisi, Renaud Louis, Christophe Desmet, Thomas Marichal, Fabrice Bureau

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Figure 2

Characterization of lung rEos and iEos in HDM-challenged C57BL/6 mice.

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Characterization of lung rEos and iEos in HDM-challenged C57BL/6 mice.
(...
(A) Experimental outline. i.n., intranasal. (B) Absolute numbers of lung eosinophil subsets. (C) Dot plot of lung leukocytes according to Siglec-F and CD125 expression. Numbers indicate the percentage of gated cells. (D) Photographs of the 2 lung eosinophil subsets. (E) Histograms of F4/80 and CCR3 expression in the cell populations shown in D. (F) Representative electron microscopy photograph of iEos (>100 individual cells analyzed). Arrows indicate secondary granules. (G) Congo red– and (H) MBP-stained lung sections. Arrows indicate Congo red– and MBP-positive eosinophils, respectively. (I) Quantification of parenchymal and peribronchial eosinophils in Congo red–stained lung sections. Eos, eosinophils. (J) Dot plot of BALF leukocytes according to Siglec-F and CD125 expression. Numbers indicate the percentage of gated cells. (K) Photographs of the gated cell populations in J. (B and I) Results represent the mean ± SEM as well as individual values (n = 5–6/group) and are representative of 1 of more than 4 independent experiments. **P < 0.01 and ***P < 0.001, by (B) a mixed-effects model, followed by Tukey’s test for multiple comparisons on log-transformed values, and (I) a Mann-Whitney U test. (C–H) Data are representative of 1 of more than 8 mice, each of them giving similar results. Scale bars: 10 μm (D, G, and H) and 1 μm (F). Neutros, neutrophils.

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