SiglecF+Gr1hi eosinophils are a distinct subpopulation within the lungs of allergen-challenged mice

Caroline M. Percopo, Todd A. Brenner, Michelle Ma, Laura S. Kraemer, Reem M A Hakeem, James J. Lee, Helene F. Rosenberg

Research output: Contribution to journalArticle

22 Citations (Scopus)

Abstract

Although eosinophils as a group are readily identified by their unique morphology and staining properties, flow cytometry provides an important means for identification of subgroups based on differential expression of distinct surface Ags. Here, we characterize an eosinophil subpopulation defined by high levels of expression of the neutrophil Ag Gr1 (CD45+CD11c-SiglecF+Gr1hi). SiglecF+Gr1hi eosinophils, distinct from the canonical SiglecF+Gr1- eosinophil population, were detected in allergen-challenged wild-type and granule protein-deficient (EPX-/- and MBP-1-/-) mice, but not in the eosinophil-deficient ΔdblGATA strain. In contrast to Gr1+ neutrophils, which express both cross-reacting Ags Ly6C and Ly6G, SiglecF+Gr1hi eosinophils from allergen-challenged lung tissue are uniquely Ly6G+. Although indistinguishable from the more-numerous SiglecF+Gr1- eosinophils under light microscopy, FACS-isolated populations revealed prominent differences in cytokine contents. The lymphocyte-targeting cytokines CXCL13 and IL-27 were identified only in the SiglecF+Gr1hi eosinophil population (at 3.9 and 4.8 pg/106 cells, respectively), as was the prominent proinflammatory mediator IL-13 (72 pg/106 cells). Interestingly, bone marrow-derived (SiglecF+), cultured eosinophils include a more substantial Gr1+ subpopulation (~50%); Gr1+ bmEos includes primarily a single Ly6C+ and a smaller, doublepositive (Ly6C+Ly6G+) population. Taken together, our findings characterize a distinct SiglecF+Gr1hi eosinophil subset in lungs of allergen-challenged, wild-type and granule protein-deficient mice. SiglecF+Gr1hi eosinophils from wild-type mice maintain a distinct subset of cytokines, including those active on B and T lymphocytes. These cytokines may facilitate eosinophil-mediated immunomodulatory responses in the allergen-challenged lung as well as in other distinct microenvironments.

Original languageEnglish (US)
Pages (from-to)321-328
Number of pages8
JournalJournal of Leukocyte Biology
Volume101
Issue number1
DOIs
StatePublished - Jan 1 2017

Fingerprint

Eosinophils
Allergens
Lung
Cytokines
Population
Neutrophils
Interleukin-27
Interleukin-13
Microscopy
Flow Cytometry
Proteins
B-Lymphocytes
Bone Marrow
Lymphocytes
Staining and Labeling
T-Lymphocytes
Light

Keywords

  • Allergy
  • Cytokines
  • Flow cytometry
  • Inflammation

ASJC Scopus subject areas

  • Immunology
  • Cell Biology

Cite this

Percopo, C. M., Brenner, T. A., Ma, M., Kraemer, L. S., Hakeem, R. M. A., Lee, J. J., & Rosenberg, H. F. (2017). SiglecF+Gr1hi eosinophils are a distinct subpopulation within the lungs of allergen-challenged mice. Journal of Leukocyte Biology, 101(1), 321-328. https://doi.org/10.1189/jlb.3A0416-166R

SiglecF+Gr1hi eosinophils are a distinct subpopulation within the lungs of allergen-challenged mice. / Percopo, Caroline M.; Brenner, Todd A.; Ma, Michelle; Kraemer, Laura S.; Hakeem, Reem M A; Lee, James J.; Rosenberg, Helene F.

In: Journal of Leukocyte Biology, Vol. 101, No. 1, 01.01.2017, p. 321-328.

Research output: Contribution to journalArticle

Percopo, CM, Brenner, TA, Ma, M, Kraemer, LS, Hakeem, RMA, Lee, JJ & Rosenberg, HF 2017, 'SiglecF+Gr1hi eosinophils are a distinct subpopulation within the lungs of allergen-challenged mice', Journal of Leukocyte Biology, vol. 101, no. 1, pp. 321-328. https://doi.org/10.1189/jlb.3A0416-166R
Percopo, Caroline M. ; Brenner, Todd A. ; Ma, Michelle ; Kraemer, Laura S. ; Hakeem, Reem M A ; Lee, James J. ; Rosenberg, Helene F. / SiglecF+Gr1hi eosinophils are a distinct subpopulation within the lungs of allergen-challenged mice. In: Journal of Leukocyte Biology. 2017 ; Vol. 101, No. 1. pp. 321-328.
@article{89a3efa1d22c4deebb536d8d427c0982,
title = "SiglecF+Gr1hi eosinophils are a distinct subpopulation within the lungs of allergen-challenged mice",
abstract = "Although eosinophils as a group are readily identified by their unique morphology and staining properties, flow cytometry provides an important means for identification of subgroups based on differential expression of distinct surface Ags. Here, we characterize an eosinophil subpopulation defined by high levels of expression of the neutrophil Ag Gr1 (CD45+CD11c-SiglecF+Gr1hi). SiglecF+Gr1hi eosinophils, distinct from the canonical SiglecF+Gr1- eosinophil population, were detected in allergen-challenged wild-type and granule protein-deficient (EPX-/- and MBP-1-/-) mice, but not in the eosinophil-deficient ΔdblGATA strain. In contrast to Gr1+ neutrophils, which express both cross-reacting Ags Ly6C and Ly6G, SiglecF+Gr1hi eosinophils from allergen-challenged lung tissue are uniquely Ly6G+. Although indistinguishable from the more-numerous SiglecF+Gr1- eosinophils under light microscopy, FACS-isolated populations revealed prominent differences in cytokine contents. The lymphocyte-targeting cytokines CXCL13 and IL-27 were identified only in the SiglecF+Gr1hi eosinophil population (at 3.9 and 4.8 pg/106 cells, respectively), as was the prominent proinflammatory mediator IL-13 (72 pg/106 cells). Interestingly, bone marrow-derived (SiglecF+), cultured eosinophils include a more substantial Gr1+ subpopulation (~50{\%}); Gr1+ bmEos includes primarily a single Ly6C+ and a smaller, doublepositive (Ly6C+Ly6G+) population. Taken together, our findings characterize a distinct SiglecF+Gr1hi eosinophil subset in lungs of allergen-challenged, wild-type and granule protein-deficient mice. SiglecF+Gr1hi eosinophils from wild-type mice maintain a distinct subset of cytokines, including those active on B and T lymphocytes. These cytokines may facilitate eosinophil-mediated immunomodulatory responses in the allergen-challenged lung as well as in other distinct microenvironments.",
keywords = "Allergy, Cytokines, Flow cytometry, Inflammation",
author = "Percopo, {Caroline M.} and Brenner, {Todd A.} and Michelle Ma and Kraemer, {Laura S.} and Hakeem, {Reem M A} and Lee, {James J.} and Rosenberg, {Helene F.}",
year = "2017",
month = "1",
day = "1",
doi = "10.1189/jlb.3A0416-166R",
language = "English (US)",
volume = "101",
pages = "321--328",
journal = "Journal of Leukocyte Biology",
issn = "0741-5400",
publisher = "FASEB",
number = "1",

}

TY - JOUR

T1 - SiglecF+Gr1hi eosinophils are a distinct subpopulation within the lungs of allergen-challenged mice

AU - Percopo, Caroline M.

AU - Brenner, Todd A.

AU - Ma, Michelle

AU - Kraemer, Laura S.

AU - Hakeem, Reem M A

AU - Lee, James J.

AU - Rosenberg, Helene F.

PY - 2017/1/1

Y1 - 2017/1/1

N2 - Although eosinophils as a group are readily identified by their unique morphology and staining properties, flow cytometry provides an important means for identification of subgroups based on differential expression of distinct surface Ags. Here, we characterize an eosinophil subpopulation defined by high levels of expression of the neutrophil Ag Gr1 (CD45+CD11c-SiglecF+Gr1hi). SiglecF+Gr1hi eosinophils, distinct from the canonical SiglecF+Gr1- eosinophil population, were detected in allergen-challenged wild-type and granule protein-deficient (EPX-/- and MBP-1-/-) mice, but not in the eosinophil-deficient ΔdblGATA strain. In contrast to Gr1+ neutrophils, which express both cross-reacting Ags Ly6C and Ly6G, SiglecF+Gr1hi eosinophils from allergen-challenged lung tissue are uniquely Ly6G+. Although indistinguishable from the more-numerous SiglecF+Gr1- eosinophils under light microscopy, FACS-isolated populations revealed prominent differences in cytokine contents. The lymphocyte-targeting cytokines CXCL13 and IL-27 were identified only in the SiglecF+Gr1hi eosinophil population (at 3.9 and 4.8 pg/106 cells, respectively), as was the prominent proinflammatory mediator IL-13 (72 pg/106 cells). Interestingly, bone marrow-derived (SiglecF+), cultured eosinophils include a more substantial Gr1+ subpopulation (~50%); Gr1+ bmEos includes primarily a single Ly6C+ and a smaller, doublepositive (Ly6C+Ly6G+) population. Taken together, our findings characterize a distinct SiglecF+Gr1hi eosinophil subset in lungs of allergen-challenged, wild-type and granule protein-deficient mice. SiglecF+Gr1hi eosinophils from wild-type mice maintain a distinct subset of cytokines, including those active on B and T lymphocytes. These cytokines may facilitate eosinophil-mediated immunomodulatory responses in the allergen-challenged lung as well as in other distinct microenvironments.

AB - Although eosinophils as a group are readily identified by their unique morphology and staining properties, flow cytometry provides an important means for identification of subgroups based on differential expression of distinct surface Ags. Here, we characterize an eosinophil subpopulation defined by high levels of expression of the neutrophil Ag Gr1 (CD45+CD11c-SiglecF+Gr1hi). SiglecF+Gr1hi eosinophils, distinct from the canonical SiglecF+Gr1- eosinophil population, were detected in allergen-challenged wild-type and granule protein-deficient (EPX-/- and MBP-1-/-) mice, but not in the eosinophil-deficient ΔdblGATA strain. In contrast to Gr1+ neutrophils, which express both cross-reacting Ags Ly6C and Ly6G, SiglecF+Gr1hi eosinophils from allergen-challenged lung tissue are uniquely Ly6G+. Although indistinguishable from the more-numerous SiglecF+Gr1- eosinophils under light microscopy, FACS-isolated populations revealed prominent differences in cytokine contents. The lymphocyte-targeting cytokines CXCL13 and IL-27 were identified only in the SiglecF+Gr1hi eosinophil population (at 3.9 and 4.8 pg/106 cells, respectively), as was the prominent proinflammatory mediator IL-13 (72 pg/106 cells). Interestingly, bone marrow-derived (SiglecF+), cultured eosinophils include a more substantial Gr1+ subpopulation (~50%); Gr1+ bmEos includes primarily a single Ly6C+ and a smaller, doublepositive (Ly6C+Ly6G+) population. Taken together, our findings characterize a distinct SiglecF+Gr1hi eosinophil subset in lungs of allergen-challenged, wild-type and granule protein-deficient mice. SiglecF+Gr1hi eosinophils from wild-type mice maintain a distinct subset of cytokines, including those active on B and T lymphocytes. These cytokines may facilitate eosinophil-mediated immunomodulatory responses in the allergen-challenged lung as well as in other distinct microenvironments.

KW - Allergy

KW - Cytokines

KW - Flow cytometry

KW - Inflammation

UR - http://www.scopus.com/inward/record.url?scp=85008515660&partnerID=8YFLogxK

UR - http://www.scopus.com/inward/citedby.url?scp=85008515660&partnerID=8YFLogxK

U2 - 10.1189/jlb.3A0416-166R

DO - 10.1189/jlb.3A0416-166R

M3 - Article

C2 - 27531929

AN - SCOPUS:85008515660

VL - 101

SP - 321

EP - 328

JO - Journal of Leukocyte Biology

JF - Journal of Leukocyte Biology

SN - 0741-5400

IS - 1

ER -