Temporal and spatial atlas of eosinophil specialization across tissues

Temporal and spatial atlas of eosinophil specialization across tissues

  • Klion, A. D., Ackerman, S. J. & Bochner, B. S. Contributions of eosinophils to human health and disease. Annu. Rev. Pathol. 15, 179–209 (2020).

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Arnold, I. C. & Munitz, A. Spatial adaptation of eosinophils and their emerging roles in homeostasis, infection and disease. Nat. Rev. Immunol. 24, 858–877 (2024).

    Article 
    CAS 
    PubMed 

    Google Scholar
     

  • Jorssen, J. et al. Single-cell proteomics and transcriptomics capture eosinophil development and identify the role of IL-5 in their lineage transit amplification. Immunity 57, 1549–1566 e1548 (2024).

    Article 
    CAS 
    PubMed 

    Google Scholar
     

  • Rothenberg, M. E. & Hogan, S. P. The eosinophil. Annu. Rev. Immunol. 24, 147–174 (2006).

    Article 
    CAS 
    PubMed 

    Google Scholar
     

  • Nussbaum, J. C. et al. Type 2 innate lymphoid cells control eosinophil homeostasis. Nature 502, 245–248 (2013).

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Loffredo, L. F. et al. Eosinophil accumulation in postnatal lung is specific to the primary septation phase of development. Sci. Rep. 10, 4425 (2020).

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Heredia, J. E. et al. Type 2 innate signals stimulate fibro/adipogenic progenitors to facilitate muscle regeneration. Cell 153, 376–388 (2013).

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Goh, Y. P. et al. Eosinophils secrete IL-4 to facilitate liver regeneration. Proc. Natl Acad. Sci. USA 110, 9914–9919 (2013).

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Qiu, Y. et al. Eosinophils and type 2 cytokine signaling in macrophages orchestrate development of functional beige fat. Cell 157, 1292–1308 (2014).

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Wu, D. et al. Eosinophils sustain adipose alternatively activated macrophages associated with glucose homeostasis. Science 332, 243–247 (2011).

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Brigger, D. et al. Eosinophils regulate adipose tissue inflammation and sustain physical and immunological fitness in old age. Nat. Metab. 2, 688–702 (2020).

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Hu, Y. & Chakarov, S. Eosinophils in obesity and obesity-associated disorders. Discov. Immunol. 2, kyad022 (2023).

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Ignacio, A. et al. Small intestinal resident eosinophils maintain gut homeostasis following microbial colonization. Immunity 55, 1250–1267 e1212 (2022).

    Article 
    CAS 
    PubMed 

    Google Scholar
     

  • Chu, V. T. et al. Eosinophils promote generation and maintenance of immunoglobulin-A-expressing plasma cells and contribute to gut immune homeostasis. Immunity 40, 582–593 (2014).

    Article 
    CAS 
    PubMed 

    Google Scholar
     

  • Wang, W. L. et al. The aryl hydrocarbon receptor instructs the immunomodulatory profile of a subset of Clec4a4(+) eosinophils unique to the small intestine. Proc. Natl Acad. Sci. USA 119, e2204557119 (2022).

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Schworer, S. A. et al. Notch 2 signaling contributes to intestinal eosinophil adaptations in steady state and tissue burden following oral allergen challenge. J. Leukoc. Biol. 116, 379–391 (2024).

    Article 
    CAS 
    PubMed 

    Google Scholar
     

  • Li, Y. et al. Neuromedin U programs eosinophils to promote mucosal immunity of the small intestine. Science 381, 1189–1196 (2023).

    Article 
    CAS 
    PubMed 

    Google Scholar
     

  • Diny, N. L. et al. The aryl hydrocarbon receptor contributes to tissue adaptation of intestinal eosinophils in mice. J. Exp. Med. https://doi.org/10.1084/jem.20210970 (2022).

  • Vassily, I. K., Korn, L. L. & Medzhitov, R. Nutrient-derived signals regulate eosinophil adaptation to the small intestine. Proc. Natl Acad. Sci. USA 121, e2316446121 (2024).

    Article 

    Google Scholar
     

  • Gurtner, A. et al. Active eosinophils regulate host defence and immune responses in colitis. Nature 615, 151–157 (2023).

    Article 
    CAS 
    PubMed 

    Google Scholar
     

  • Liu, Z. et al. Fate mapping via Ms4a3-expression history traces monocyte-derived cells. Cell 178, 1509–1525 e1519 (2019).

    Article 
    CAS 
    PubMed 

    Google Scholar
     

  • Becht, E. et al. High-throughput single-cell quantification of hundreds of proteins using conventional flow cytometry and machine learning. Sci. Adv. 7, eabg0505 (2021).

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Zhang, T., Warden, A. R., Li, Y. & Ding, X. Progress and applications of mass cytometry in sketching immune landscapes. Clin. Transl. Med. 10, e206 (2020).

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Larsen, L. D., Dockstader, K., Olbrich, C. L., Cartwright, I. M. & Spencer, L. A. Modulation of surface CD11c expression tracks plasticity in murine intestinal tissue eosinophils. J. Leukoc. Biol. 111, 943–952 (2022).

    Article 
    CAS 
    PubMed 

    Google Scholar
     

  • Reis e Sousa, C., Yamasaki, S. & Brown, G. D. Myeloid C-type lectin receptors in innate immune recognition. Immunity 57, 700–717 (2024).

    Article 
    CAS 
    PubMed 

    Google Scholar
     

  • Trapnell, C. et al. The dynamics and regulators of cell fate decisions are revealed by pseudotemporal ordering of single cells. Nat. Biotechnol. 32, 381–386 (2014).

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Adams, J. M. & Cory, S. The Bcl-2 protein family: arbiters of cell survival. Science 281, 1322–1326 (1998).

    Article 
    CAS 
    PubMed 

    Google Scholar
     

  • Carneiro, B. A. & El-Deiry, W. S. Targeting apoptosis in cancer therapy. Nat. Rev. Clin. Oncol. 17, 395–417 (2020).

    Article 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Ng, M. S. F. et al. Deterministic reprogramming of neutrophils within tumors. Science 383, eadf6493 (2024).

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Mesnil, C. et al. Lung-resident eosinophils represent a distinct regulatory eosinophil subset. J. Clin. Invest. 126, 3279–3295 (2016).

    Article 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Dolitzky, A. et al. Mouse resident lung eosinophils are dependent on IL-5. Allergy 77, 2822–2825 (2022).

    Article 
    CAS 
    PubMed 

    Google Scholar
     

  • Evrard, M. et al. Developmental analysis of bone marrow neutrophils reveals populations specialized in expansion, trafficking, and effector functions. Immunity 48, 364–379.e368 (2018).

    Article 
    CAS 
    PubMed 

    Google Scholar
     

  • Kimura, I., Ichimura, A., Ohue-Kitano, R. & Igarashi, M. Free fatty acid receptors in health and disease. Physiol. Rev. 100, 171–210 (2020).

    Article 
    CAS 
    PubMed 

    Google Scholar
     

  • Wen, T. et al. The pan-B cell marker CD22 is expressed on gastrointestinal eosinophils and negatively regulates tissue eosinophilia. J. Immunol. 188, 1075–1082 (2012).

    Article 
    CAS 
    PubMed 

    Google Scholar
     

  • Ma, A. & Malynn, B. A. A20: linking a complex regulator of ubiquitylation to immunity and human disease. Nat. Rev. Immunol. 12, 774–785 (2012).

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Coelho, A. L. et al. The chemokine CCL6 promotes innate immunity via immune cell activation and recruitment. J. Immunol. 179, 5474–5482 (2007).

    Article 
    CAS 
    PubMed 

    Google Scholar
     

  • Yuan, K. et al. Novel diagnostic biomarkers of oxidative stress, immune- infiltration characteristics and experimental validation of SERPINE1 in colon cancer. Discov. Oncol. 14, 206 (2023).

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Lee, N. A. et al. Expression of IL-5 in thymocytes/T cells leads to the development of a massive eosinophilia, extramedullary eosinophilopoiesis, and unique histopathologies. J. Immunol. 158, 1332–1344 (1997).

    Article 
    CAS 
    PubMed 

    Google Scholar
     

  • Jiménez-Saiz, R. et al. Microbial regulation of enteric eosinophils and its impact on tissue remodeling and Th2 immunity. Front. Immunol. 11, 155 (2020).

    Article 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Li, J. et al. Sexual dimorphism in obesity is governed by RELMα regulation of adipose macrophages and eosinophils. eLife https://doi.org/10.7554/elife.86001 (2023).

  • Karkout, R. et al. Female-specific enhancement of eosinophil recruitment and activation in a type 2 innate inflammation model in the lung. Clin. Exp. Immunol. 216, 13–24 (2024).

    Article 
    CAS 
    PubMed 

    Google Scholar
     

  • Artham, S., Chang, C. Y. & McDonnell, D. P. Eosinophilia in cancer and its regulation by sex hormones. Trends Endocrinol. Metab. 34, 5–20 (2023).

    Article 
    CAS 
    PubMed 

    Google Scholar
     

  • Finck, R. et al. Normalization of mass cytometry data with bead standards. Cytometry A 83, 483–494 (2013).

    Article 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Newell, E. W., Sigal, N., Bendall, S. C., Nolan, G. P. & Davis, M. M. Cytometry by time-of-flight shows combinatorial cytokine expression and virus-specific cell niches within a continuum of CD8+ T cell phenotypes. Immunity 36, 142–152 (2012).

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Z. Li. Temporal and spatial determinants of eosinophil specialization across tissues. Figshare https://doi.org/10.6084/m9.figshare.29816303 (2025).