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Epigenetic and transcriptional programming of murine eosinophils in the esophagus

Author

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  • Jennifer M. Felton

    (Cincinnati Children’s Hospital Medical Center, Division of Allergy and Immunology)

  • Lee E. Edsall

    (Cincinnati Children’s Hospital Medical Center, Division of Allergy and Immunology
    Cincinnati Children’s Hospital Medical Center, Center for Autoimmune Genomics and Etiology, Division of Human Genetics)

  • Ty D. Troutman

    (Cincinnati Children’s Hospital Medical Center, Division of Allergy and Immunology
    University of Cincinnati College of Medicine, Department of Pediatrics)

  • Lydia Mack

    (Cincinnati Children’s Hospital Medical Center, Division of Allergy and Immunology)

  • Michael Kotliar

    (Cincinnati Children’s Hospital Medical Center, Division of Allergy and Immunology)

  • Netali Ben-Baruch Morgenstern

    (Cincinnati Children’s Hospital Medical Center, Division of Allergy and Immunology)

  • Annalise M. Psaila

    (UNSW Sydney, School of Biotechnology and Biomolecular Sciences)

  • Mark Rochman

    (Cincinnati Children’s Hospital Medical Center, Division of Allergy and Immunology)

  • Andrea M. Klingler

    (Cincinnati Children’s Hospital Medical Center, Division of Allergy and Immunology)

  • Garrett A. Osswald

    (Cincinnati Children’s Hospital Medical Center, Division of Allergy and Immunology)

  • Simin Zhang

    (Cincinnati Children’s Hospital Medical Center, Division of Allergy and Immunology
    University of Cincinnati College of Medicine, Division of Rheumatology, Allergy and Immunology, Department of Medicine)

  • Julia L. M. Dunn

    (Cincinnati Children’s Hospital Medical Center, Division of Allergy and Immunology)

  • Ben Wronowski

    (Cincinnati Children’s Hospital Medical Center, Division of Allergy and Immunology)

  • Tetsuo Shoda

    (Cincinnati Children’s Hospital Medical Center, Division of Allergy and Immunology
    University of Cincinnati College of Medicine, Department of Pediatrics)

  • Julie M. Caldwell

    (Cincinnati Children’s Hospital Medical Center, Division of Allergy and Immunology)

  • Rana Herro

    (University of Cincinnati College of Medicine, Department of Pediatrics
    Cincinnati Children’s Hospital Medical Center, Division of Immunobiology)

  • Artem Barski

    (Cincinnati Children’s Hospital Medical Center, Division of Allergy and Immunology
    Cincinnati Children’s Hospital Medical Center, Division of Human Genetics)

  • Kate G. R. Quinlan

    (UNSW Sydney, School of Biotechnology and Biomolecular Sciences)

  • Matthew T. Weirauch

    (Cincinnati Children’s Hospital Medical Center, Division of Allergy and Immunology
    Cincinnati Children’s Hospital Medical Center, Center for Autoimmune Genomics and Etiology, Division of Human Genetics
    Cincinnati Children’s Hospital Medical Center, Division of Human Genetics
    Cincinnati Children’s Hospital Medical Center, Division of Biomedical Informatics)

  • Marc E. Rothenberg

    (Cincinnati Children’s Hospital Medical Center, Division of Allergy and Immunology
    University of Cincinnati College of Medicine, Department of Pediatrics)

Abstract

Eosinophils accumulate in different tissues in allergies, cancer, and infectious diseases, adopting distinct properties. Herein, we profiled murine esophageal eosinophils during allergic inflammation using single-cell sequencing, epigenomic mapping, and flow cytometry. Esophageal eosinophils displayed an altered chromatin accessibility profile compared to bone marrow eosinophils, with 761 epi-transcriptionally regulated genes enriched in inflammation, immunoregulation, bacterial sensing, angiogenesis, migration, and apoptosis. The local environment entrains the unique esophageal eosinophil immunophenotype, as suggested by eosinophil-esophageal epithelial co-cultures, esophageal eosinophil transcriptional similarities regardless of the upstream cytokines driving their esophageal localization, and transcription factor gene editing altering esophageal eosinophilia and the associated eosinophil and global esophageal transcriptomes. Finally, the epigenomic and transcriptomic properties of murine esophageal eosinophils are largely conserved in humans. Thus, our data indicate that tissue specialization of esophageal eosinophils is entrained by local environmental cues that induce genome-wide epigenetic reprogramming and regulated by discrete transcription factors and provide a public, epigenetic database of murine tissue eosinophils.

Suggested Citation

  • Jennifer M. Felton & Lee E. Edsall & Ty D. Troutman & Lydia Mack & Michael Kotliar & Netali Ben-Baruch Morgenstern & Annalise M. Psaila & Mark Rochman & Andrea M. Klingler & Garrett A. Osswald & Simin, 2025. "Epigenetic and transcriptional programming of murine eosinophils in the esophagus," Nature Communications, Nature, vol. 16(1), pages 1-20, December.
    • Handle: RePEc:nat:natcom:v:16:y:2025:i:1:d:10.1038_s41467-025-65440-5
    DOI: 10.1038/s41467-025-65440-5
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