Functions of tissue-resident eosinophils (original) (raw)
Drissen, R. et al. Distinct myeloid progenitor-differentiation pathways identified through single-cell RNA sequencing. Nat. Immunol.17, 666–676 (2016). CASPubMedPubMed Central Google Scholar
Acharya, K. R. & Ackerman, S. J. Eosinophil granule proteins: form and function. J. Biol. Chem.289, 17406–17415 (2014). CASPubMedPubMed Central Google Scholar
Lee, J. J. et al. Human versus mouse eosinophils: “that which we call an eosinophil, by any other name would stain as red”. J. Allergy Clin. Immunol.130, 572–584 (2012). CASPubMedPubMed Central Google Scholar
Huang, L. & Appleton, J. A. Eosinophils in helminth infection: defenders and dupes. Trends Parasitol.32, 798–807 (2016). CASPubMedPubMed Central Google Scholar
Makepeace, B. L., Martin, C., Turner, J. D. & Specht, S. Granulocytes in helminth infection — who is calling the shots? Curr. Med. Chem.19, 1567–1586 (2012). CASPubMedPubMed Central Google Scholar
Huang, L. et al. Eosinophils and IL-4 support nematode growth coincident with an innate response to tissue injury. PLoS Pathog.11, e1005347 (2015). PubMedPubMed Central Google Scholar
Neves, J. S., Perez, S. A., Spencer, L. A., Melo, R. C. & Weller, P. F. Subcellular fractionation of human eosinophils: isolation of functional specific granules on isoosmotic density gradients. J. Immunol. Methods344, 64–72 (2009). CASPubMedPubMed Central Google Scholar
Kato, M. et al. Eosinophil infiltration and degranulation in normal human tissue. Anat. Rec.252, 418–425 (1998). CASPubMed Google Scholar
Yu, Y. R. et al. A protocol for the comprehensive flow cytometric analysis of immune cells in normal and inflamed murine non-lymphoid tissues. PLoS ONE11, e0150606 (2016). PubMedPubMed Central Google Scholar
Diener, K. R., Robertson, S. A., Hayball, J. D. & Lousberg, E. L. Multi-parameter flow cytometric analysis of uterine immune cell fluctuations over the murine estrous cycle. J. Reproductive Immunol.113, 61–67 (2016). CAS Google Scholar
Voehringer, D., van Rooijen, N. & Locksley, R. M. Eosinophils develop in distinct stages and are recruited to peripheral sites by alternatively activated macrophages. J. Leukoc. Biol.81, 1434–1444 (2007). CASPubMed Google Scholar
Throsby, M., Herbelin, A., Pleau, J. M. & Dardenne, M. CD11c+ eosinophils in the murine thymus: developmental regulation and recruitment upon MHC class I-restricted thymocyte deletion. J. Immunol.165, 1965–1975 (2000). CASPubMed Google Scholar
Jung, Y. & Rothenberg, M. E. Roles and regulation of gastrointestinal eosinophils in immunity and disease. J. Immunol.193, 999–1005 (2014). CASPubMedPubMed Central Google Scholar
Percopo, C. M. et al. SiglecF+Gr1hi eosinophils are a distinct subpopulation within the lungs of allergen-challenged mice. J. Leukoc. Biol.101, 321–328 (2017). CASPubMed Google Scholar
Le-Carlson, M. et al. Markers of antigen presentation and activation on eosinophils and T cells in the esophageal tissue of patients with eosinophilic esophagitis. J. Pediatr. Gastroenterol. Nutr.56, 257–262 (2013). CASPubMedPubMed Central Google Scholar
Patel, A. J. et al. Increased HLA-DR expression on tissue eosinophils in eosinophilic esophagitis. J. Pediatr. Gastroenterol. Nutr.51, 290–294 (2010). CASPubMed Google Scholar
Sedgwick, J. B. et al. Comparison of airway and blood eosinophil function after in vivo antigen challenge. J. Immunol.149, 3710–3718 (1992). CASPubMed Google Scholar
Cagnoni, E. F. et al. Bronchopulmonary lymph nodes and large airway cell trafficking in patients with fatal asthma. J. Allergy Clin. Immunol.135, 1352–1357.e9 (2015). PubMed Google Scholar
Mesnil, C. et al. Lung-resident eosinophils represent a distinct regulatory eosinophil subset. J. Clin. Invest.126, 3279–3295 (2016). PubMedPubMed Central Google Scholar
Bettigole, S. E. et al. The transcription factor XBP1 is selectively required for eosinophil differentiation. Nat. Immunol.16, 829–837 (2015). This study implicates IRE1α–XBP1 signalling, a key component of the unfolded protein response pathway, in the terminal maturation of eosinophil progenitors. These data provide a link between eosinophilopoiesis and physiological endoplasmic reticulum stress in eosinophil-committed precursors. CASPubMedPubMed Central Google Scholar
Matthews, S. P., McMillan, S. J., Colbert, J. D., Lawrence, R. A. & Watts, C. Cystatin F ensures eosinophil survival by regulating granule biogenesis. Immunity44, 795–806 (2016). CASPubMedPubMed Central Google Scholar
Doyle, A. D. et al. Expression of the secondary granule proteins major basic protein 1 (MBP-1) and eosinophil peroxidase (EPX) is required for eosinophilopoiesis in mice. Blood122, 781–790 (2013). This study shows that concomitant loss of two of the main granule-derived cationic proteins (MBP1 and EPX) results in selective loss of eosinophil lineage-committed progenitors. This provides, for the first time, a link between granule protein expression and eosinophilopoiesis. CASPubMedPubMed Central Google Scholar
Spencer, L. A. et al. Human eosinophils constitutively express multiple Th1, Th2, and immunoregulatory cytokines that are secreted rapidly and differentially. J. Leukoc. Biol.85, 117–123 (2009). This study shows that blood eosinophils from healthy humans constitutively contain preformed stores of various cytokines that are rapidly and differentially released in response to specific agonists. CASPubMed Google Scholar
Moqbel, R. et al. Identification of messenger RNA for IL-4 in human eosinophils with granule localization and release of the translated product. J. Immunol.155, 4939–4947 (1995). CASPubMed Google Scholar
Beil, W. J., Weller, P. F., Tzizik, D. M., Galli, S. J. & Dvorak, A. M. Ultrastructural immunogold localization of tumor necrosis factor-alpha to the matrix compartment of eosinophil secondary granules in patients with idiopathic hypereosinophilic syndrome. J. Histochem. Cytochem.41, 1611–1615 (1993). CASPubMed Google Scholar
Liu, L. Y. et al. Generation of Th1 and Th2 chemokines by human eosinophils: evidence for a critical role of TNF-alpha. J. Immunol.179, 4840–4848 (2007). CASPubMed Google Scholar
Shen, Z. J., Esnault, S. & Malter, J. S. The peptidyl-prolyl isomerase Pin1 regulates the stability of granulocyte-macrophage colony-stimulating factor mRNA in activated eosinophils. Nat. Immunol.6, 1280–1287 (2005). CASPubMed Google Scholar
Chu, V. T. & Berek, C. Immunization induces activation of bone marrow eosinophils required for plasma cell survival. Eur. J. Immunol.42, 130–137 (2012). This study suggests that antigen-dependent activation primes eosinophils to provide pro-survival signals to plasma cells within bone marrow niches. CASPubMed Google Scholar
Rose, C. E. Jr. et al. Murine lung eosinophil activation and chemokine production in allergic airway inflammation. Cell. Mol. Immunol.7, 361–374 (2010). CASPubMedPubMed Central Google Scholar
Kanda, A. et al. Th2-activated eosinophils release Th1 cytokines that modulate allergic inflammation. Allergol. Int.64 (Suppl.), S71–S73 (2015). PubMed Google Scholar
Gessner, A., Mohrs, K. & Mohrs, M. Mast cells, basophils, and eosinophils acquire constitutive IL-4 and IL-13 transcripts during lineage differentiation that are sufficient for rapid cytokine production. J. Immunol.174, 1063–1072 (2005). CASPubMed Google Scholar
Melo, R. C. et al. Human eosinophils secrete preformed, granule-stored interleukin-4 through distinct vesicular compartments. Traffic6, 1047–1057 (2005). CASPubMedPubMed Central Google Scholar
Melo, R. C., Dvorak, A. M. & Weller, P. F. Electron tomography and immunonanogold electron microscopy for investigating intracellular trafficking and secretion in human eosinophils. J. Cell. Mol. Med.12, 1416–1419 (2008). PubMedPubMed Central Google Scholar
Melo, R. C. et al. Vesicle-mediated secretion of human eosinophil granule-derived major basic protein. Lab. Invest.89, 769–781 (2009). CASPubMedPubMed Central Google Scholar
Melo, R. C., Spencer, L. A., Dvorak, A. M. & Weller, P. F. Mechanisms of eosinophil secretion: large vesiculotubular carriers mediate transport and release of granule-derived cytokines and other proteins. J. Leukoc. Biol.83, 229–236 (2008). CASPubMed Google Scholar
Melo, R. C. & Weller, P. F. Vesicular trafficking of immune mediators in human eosinophils revealed by immunoelectron microscopy. Exp. Cell Res.347, 385–390 (2016). CASPubMedPubMed Central Google Scholar
Scepek, S., Moqbel, R. & Lindau, M. Compound exocytosis and cumulative degranulation by eosinophils and their role in parasite killing. Parasitol. Today10, 276–278 (1994). CASPubMed Google Scholar
Persson, C. & Uller, L. Primary lysis of eosinophils as a major mode of activation of eosinophils in human diseased tissues. Nat. Rev. Immunol.13, 902 (2013). CASPubMed Google Scholar
Ueki, S. et al. Eosinophil extracellular trap cell death-derived DNA traps: their presence in secretions and functional attributes. J. Allergy Clin. Immunol.137, 258–267 (2016). CASPubMed Google Scholar
Ueki, S. et al. Eosinophil extracellular DNA trap cell death mediates lytic release of free secretion-competent eosinophil granules in humans. Blood121, 2074–2083 (2013). CASPubMedPubMed Central Google Scholar
Persson, C. G. & Erjefalt, J. S. “Ultimate activation” of eosinophils in vivo: lysis and release of clusters of free eosinophil granules (Cfegs). Thorax52, 569–574 (1997). CASPubMedPubMed Central Google Scholar
Persson, C. G. & Erjefalt, J. S. Eosinophil lysis and free granules: an in vivo paradigm for cell activation and drug development. Trends Pharmacol. Sci.18, 117–123 (1997). CASPubMed Google Scholar
Persson, C. G. Centennial notions of asthma as an eosinophilic, desquamative, exudative, and steroid-sensitive disease. Lancet350, 1021–1024 (1997). CASPubMed Google Scholar
Erjefalt, J. S. & Persson, C. G. New aspects of degranulation and fates of airway mucosal eosinophils. Am. J. Respir. Crit. Care Med.161, 2074–2085 (2000). CASPubMed Google Scholar
Erjefalt, J. S. et al. Allergen-induced eosinophil cytolysis is a primary mechanism for granule protein release in human upper airways. Am. J. Respir. Crit. Care Med.160, 304–312 (1999). CASPubMed Google Scholar
Watanabe, K., Misu, T., Inoue, S. & Edamatsu, H. Cytolysis of eosinophils in nasal secretions. Ann. Otol. Rhinol. Laryngol.112, 169–173 (2003). PubMed Google Scholar
Greiff, L., Erjefalt, J. S., Andersson, M., Svensson, C. & Persson, C. G. Generation of clusters of free eosinophil granules (Cfegs) in seasonal allergic rhinitis. Allergy53, 200–203 (1998). CASPubMed Google Scholar
Uller, L., Andersson, M., Greiff, L., Persson, C. G. & Erjefalt, J. S. Occurrence of apoptosis, secondary necrosis, and cytolysis in eosinophilic nasal polyps. Am. J. Respir. Crit. Care Med.170, 742–747 (2004). PubMed Google Scholar
Gonzalez, E. B., Swedo, J. L., Rajaraman, S., Daniels, J. C. & Grant, J. A. Ultrastructural and immunohistochemical evidence for release of eosinophilic granules in vivo: cytotoxic potential in chronic eosinophilic pneumonia. J. Allergy Clin. Immunol.79, 755–762 (1987). CASPubMed Google Scholar
Grantham, J. G., Meadows, J. A., 3rd & Gleich, G. J. Chronic eosinophilic pneumonia. Evidence for eosinophil degranulation and release of major basic protein. Am. J. Med.80, 89–94 (1986). CASPubMed Google Scholar
Tajirian, A., Ross, R., Zeikus, P. & Robinson-Bostom, L. Subcutaneous fat necrosis of the newborn with eosinophilic granules. J. Cutan. Pathol.34, 588–590 (2007). PubMed Google Scholar
Chikwava, K. R., Savell, V. H. Jr & Boyd, T. K. Fatal cephalosporin-induced acute hypersensitivity myocarditis. Pediatr. Cardiol.27, 777–780 (2006). PubMed Google Scholar
Gutierrez-Pena, E. J., Knab, J. & Buttner, D. W. Immunoelectron microscopic evidence for release of eosinophil granule matrix protein onto microfilariae of Onchocerca volvulus in the skin after exposure to amocarzine. Parasitol. Res.84, 607–615 (1998). CASPubMed Google Scholar
Daneshpouy, M. et al. Activated eosinophils in upper gastrointestinal tract of patients with graft-versus-host disease. Blood99, 3033–3040 (2002). CASPubMed Google Scholar
Aceves, S. S., Newbury, R. O., Dohil, R., Bastian, J. F. & Broide, D. H. Esophageal remodeling in pediatric eosinophilic esophagitis. J. Allergy Clin. Immunol.119, 206–212 (2007). CASPubMed Google Scholar
Mueller, S., Aigner, T., Neureiter, D. & Stolte, M. Eosinophil infiltration and degranulation in oesophageal mucosa from adult patients with eosinophilic oesophagitis: a retrospective and comparative study on pathological biopsy. J. Clin. Pathol.59, 1175–1180 (2006). CASPubMedPubMed Central Google Scholar
Saffari, H. et al. Electron microscopy elucidates eosinophil degranulation patterns in patients with eosinophilic esophagitis. J. Allergy Clin. Immunol.133, 1728–1734.e1 (2014). This electron microscopy study used more than 1,500 images obtained from specimens taken from nine patients with eosinophilic oesophagitis to quantitatively assess degranulation patterns in human eosinophilsin vivo. It showed that more than 80% of eosinophils have signs of cytolytic release of free granules. CASPubMed Google Scholar
Shamri, R. et al. CCL11 elicits secretion of RNases from mouse eosinophils and their cell-free granules. FASEB J.26, 2084–2093 (2012). CASPubMedPubMed Central Google Scholar
Boyer, D., Vargas, S. O., Slattery, D., Rivera-Sanchez, Y. M. & Colin, A. A. Churg–Strauss syndrome in children: a clinical and pathologic review. Pediatrics118, e914–e920 (2006). PubMed Google Scholar
Neves, J. S. et al. Eosinophil granules function extracellularly as receptor-mediated secretory organelles. Proc. Natl Acad. Sci. USA105, 18478–18483 (2008). CASPubMed Google Scholar
Neves, J. S., Radke, A. L. & Weller, P. F. Cysteinyl leukotrienes acting via granule membrane expressed receptors elicit secretion from within cell-free human eosinophil granules. J. Allergy Clin. Immunol.125, 477–482 (2010). This paper provides the first demonstration that extracellular, cell-free eosinophil granules express outwardly oriented, functional cytokine receptors and G protein-coupled receptors, as well as intragranular signal transduction molecules, and are competent to undergo differential, stimulus-induced secretion. CASPubMedPubMed Central Google Scholar
Melo, R. C., Morgan, E., Monahan-Earley, R., Dvorak, A. M. & Weller, P. F. Pre-embedding immunogold labeling to optimize protein localization at subcellular compartments and membrane microdomains of leukocytes. Nat. Protoc.9, 2382–2394 (2014). CASPubMedPubMed Central Google Scholar
Melo, R. C., Perez, S. A., Spencer, L. A., Dvorak, A. M. & Weller, P. F. Intragranular vesiculotubular compartments are involved in piecemeal degranulation by activated human eosinophils. Traffic6, 866–879 (2005). CASPubMedPubMed Central Google Scholar
Melo, R. C., Dvorak, A. M. & Weller, P. F. Contributions of electron microscopy to understand secretion of immune mediators by human eosinophils. Microsc. Microanal.16, 653–660 (2010). CASPubMedPubMed Central Google Scholar
Spencer, L. A. et al. Cytokine receptor-mediated trafficking of preformed IL-4 in eosinophils identifies an innate immune mechanism of cytokine secretion. Proc. Natl Acad. Sci. USA103, 3333–3338 (2006). This study shows that a granule-derived cytokine can be mobilized into secretory vesicles and chaperoned through the vesicular compartment bound to its cognate receptor during eosinophil PMD. CASPubMed Google Scholar
Bagnasco, D. et al. Targeting interleukin-5 or interleukin-5Ralpha: safety considerations. Drug Saf.40, 559–570 (2017). PubMed Google Scholar
Diefenbach, A., Colonna, M. & Romagnani, C. The ILC world revisited. Immunity46, 327–332 (2017). CASPubMed Google Scholar
Jacobsen, E. A., Zellner, K. R., Colbert, D., Lee, N. A. & Lee, J. J. Eosinophils regulate dendritic cells and Th2 pulmonary immune responses following allergen provocation. J. Immunol.187, 6059–6068 (2011). CASPubMedPubMed Central Google Scholar
Jacobsen, E. A. et al. Allergic pulmonary inflammation in mice is dependent on eosinophil-induced recruitment of effector T cells. J. Exp. Med.205, 699–710 (2008). CASPubMedPubMed Central Google Scholar
Kondo, Y. et al. Administration of IL-33 induces airway hyperresponsiveness and goblet cell hyperplasia in the lungs in the absence of adaptive immune system. Int. Immunol.20, 791–800 (2008). CASPubMed Google Scholar
Klose, C. S. & Artis, D. Innate lymphoid cells as regulators of immunity, inflammation and tissue homeostasis. Nat. Immunol.17, 765–774 (2016). CASPubMed Google Scholar
Molofsky, A. B. et al. Innate lymphoid type 2 cells sustain visceral adipose tissue eosinophils and alternatively activated macrophages. J. Exp. Med.210, 535–549 (2013). CASPubMedPubMed Central Google Scholar
van Rijt, L., von Richthofen, H. & van Ree, R. Type 2 innate lymphoid cells: at the cross-roads in allergic asthma. Semin. Immunopathol.38, 483–496 (2016). CASPubMedPubMed Central Google Scholar
Dhariwal, J. et al. Mucosal type 2 innate lymphoid cells are a key component of the allergic response to aeroallergen. Am. J. Respir. Crit. Care Med.195, 1586–1596 (2017). CASPubMedPubMed Central Google Scholar
Smith, S. G. et al. Increased numbers of activated group 2 innate lymphoid cells in the airways of patients with severe asthma and persistent airway eosinophilia. J. Allergy Clin. Immunol.137, 75–86.e8 (2016). CASPubMed Google Scholar
Rosenberg, H. F., Dyer, K. D. & Foster, P. S. Eosinophils: changing perspectives in health and disease. Nat. Rev. Immunol.13, 9–22 (2013). CASPubMed Google Scholar
Mitchell, P. D. & O'Byrne, P. M. Epithelial-derived cytokines in asthma. Chest151, 1338–1344 (2017). PubMed Google Scholar
Esnault, S. & Kelly, E. A. Essential mechanisms of differential activation of eosinophils by IL-3 compared to GM-CSF and IL-5. Crit. Rev. Immunol.36, 429–444 (2016). PubMedPubMed Central Google Scholar
Egea, L., Hirata, Y. & Kagnoff, M. F. GM-CSF: a role in immune and inflammatory reactions in the intestine. Expert Rev. Gastroenterol. Hepatol.4, 723–731 (2010). CASPubMedPubMed Central Google Scholar
Sugawara, R. et al. Small intestinal eosinophils regulate Th17 cells by producing IL-1 receptor antagonist. J. Exp. Med.213, 555–567 (2016). CASPubMedPubMed Central Google Scholar
Munitz, A. & Levi-Schaffer, F. Inhibitory receptors on eosinophils: a direct hit to a possible Achilles heel? J. Allergy Clin. Immunol.119, 1382–1387 (2007). CASPubMed Google Scholar
Nutku, E., Aizawa, H., Hudson, S. A. & Bochner, B. S. Ligation of Siglec-8: a selective mechanism for induction of human eosinophil apoptosis. Blood101, 5014–5020 (2003). CASPubMed Google Scholar
Ben Baruch-Morgenstern, N. et al. Paired immunoglobulin-like receptor A is an intrinsic, self-limiting suppressor of IL-5-induced eosinophil development. Nat. Immunol.15, 36–44 (2014). PubMed Google Scholar
Tedla, N. et al. Activation of human eosinophils through leukocyte immunoglobulin-like receptor 7. Proc. Natl Acad. Sci. USA100, 1174–1179 (2003). CASPubMed Google Scholar
Munitz, A. et al. The inhibitory receptor IRp60 (CD300a) suppresses the effects of IL-5, GM-CSF, and eotaxin on human peripheral blood eosinophils. Blood107, 1996–2003 (2006). CASPubMed Google Scholar
Lee, J. J. & Rosenberg, H. F. (eds) Eosinophils in Health and Disease Ch. 5.6 111–119 (Elsevier, 2013). Google Scholar
Yu, C. et al. Targeted deletion of a high-affinity GATA-binding site in the GATA-1 promoter leads to selective loss of the eosinophil lineage in vivo. J. Exp. Med.195, 1387–1395 (2002). CASPubMedPubMed Central Google Scholar
Lee, J. J. et al. Defining a link with asthma in mice congenitally deficient in eosinophils. Science305, 1773–1776 (2004). CASPubMed Google Scholar
Jacobsen, E. A. et al. Eosinophil activities modulate the immune/inflammatory character of allergic respiratory responses in mice. Allergy69, 315–327 (2014). CASPubMed Google Scholar
Doyle, A. D. et al. Homologous recombination into the eosinophil peroxidase locus generates a strain of mice expressing Cre recombinase exclusively in eosinophils. J. Leukoc. Biol.94, 17–24 (2013). CASPubMedPubMed Central Google Scholar
Croxford, A. L. & Buch, T. Cytokine reporter mice in immunological research: perspectives and lessons learned. Immunology132, 1–8 (2011). CASPubMedPubMed Central Google Scholar
Mohrs, M., Shinkai, K., Mohrs, K. & Locksley, R. M. Analysis of type 2 immunity in vivo with a bicistronic IL-4 reporter. Immunity15, 303–311 (2001). CASPubMed Google Scholar
Voehringer, D., Shinkai, K. & Locksley, R. M. Type 2 immunity reflects orchestrated recruitment of cells committed to IL-4 production. Immunity20, 267–277 (2004). CASPubMed Google Scholar
Mohrs, K., Wakil, A. E., Killeen, N., Locksley, R. M. & Mohrs, M. A two-step process for cytokine production revealed by IL-4 dual-reporter mice. Immunity23, 419–429 (2005). CASPubMedPubMed Central Google Scholar
Aupperlee, M. D. et al. Epidermal growth factor receptor (EGFR) signaling is a key mediator of hormone-induced leukocyte infiltration in the pubertal female mammary gland. Endocrinology155, 2301–2313 (2014). PubMedPubMed Central Google Scholar
Gouon-Evans, V., Lin, E. Y. & Pollard, J. W. Requirement of macrophages and eosinophils and their cytokines/chemokines for mammary gland development. Breast Cancer Res.4, 155–164 (2002). PubMedPubMed Central Google Scholar
Gouon-Evans, V., Rothenberg, M. E. & Pollard, J. W. Postnatal mammary gland development requires macrophages and eosinophils. Development127, 2269–2282 (2000). CASPubMed Google Scholar
Gouon-Evans, V. & Pollard, J. W. Eotaxin is required for eosinophil homing into the stroma of the pubertal and cycling uterus. Endocrinology142, 4515–4521 (2001). CASPubMed Google Scholar
Sferruzzi-Perri, A. N., Robertson, S. A. & Dent, L. A. Interleukin-5 transgene expression and eosinophilia are associated with retarded mammary gland development in mice. Biol. Reprod.69, 224–233 (2003). CASPubMed Google Scholar
Zhang, J., Lathbury, L. J. & Salamonsen, L. A. Expression of the chemokine eotaxin and its receptor, CCR3, in human endometrium. Biol. Reprod.62, 404–411 (2000). CASPubMed Google Scholar
Knudsen, U. B., Uldbjerg, N., Rechberger, T. & Fredens, K. Eosinophils in human cervical ripening. Eur. J. Obstetr., Gynecol., Reproductive Biol.72, 165–168 (1997). CAS Google Scholar
Timmons, B. C., Fairhurst, A. M. & Mahendroo, M. S. Temporal changes in myeloid cells in the cervix during pregnancy and parturition. J. Immunol.182, 2700–2707 (2009). CASPubMedPubMed Central Google Scholar
Robertson, S. A., Mau, V. J., Young, I. G. & Matthaei, K. I. Uterine eosinophils and reproductive performance in interleukin 5-deficient mice. J. Reprod. Fertil.120, 423–432 (2000). CASPubMed Google Scholar
Matthews, A. N. et al. Eotaxin is required for the baseline level of tissue eosinophils. Proc. Natl Acad. Sci. USA95, 6273–6278 (1998). CASPubMed Google Scholar
Hogan, S. P., Mishra, A., Brandt, E. B., Foster, P. S. & Rothenberg, M. E. A critical role for eotaxin in experimental oral antigen-induced eosinophilic gastrointestinal allergy. Proc. Natl Acad. Sci. USA97, 6681–6686 (2000). CASPubMed Google Scholar
Mishra, A., Hogan, S. P., Lee, J. J., Foster, P. S. & Rothenberg, M. E. Fundamental signals that regulate eosinophil homing to the gastrointestinal tract. J. Clin. Invest.103, 1719–1727 (1999). CASPubMedPubMed Central Google Scholar
Chu, V. T. et al. Eosinophils promote generation and maintenance of immunoglobulin-A-expressing plasma cells and contribute to gut immune homeostasis. Immunity40, 582–593 (2014). One of the first papers to show alterations in intestinal immune homeostasis (including alterations in IgA production, the intestinal T cell compartment and microbiota composition) in the absence of eosinophils. CASPubMed Google Scholar
Jung, Y. et al. IL-1beta in eosinophil-mediated small intestinal homeostasis and IgA production. Mucosal Immunol.8, 930–942 (2015). This paper implicates eosinophil-derived IL-1βin promoting intestinal homeostasis, including the maintenance of intestinal IgA levels and RORγ-expressing ILCs. CASPubMedPubMed Central Google Scholar
Goh, Y. P. et al. Eosinophils secrete IL-4 to facilitate liver regeneration. Proc. Natl Acad. Sci. USA110, 9914–9919 (2013). CASPubMed Google Scholar
Heredia, J. E. et al. Type 2 innate signals stimulate fibro/adipogenic progenitors to facilitate muscle regeneration. Cell153, 376–388 (2013). CASPubMedPubMed Central Google Scholar
Joe, A. W. et al. Muscle injury activates resident fibro/adipogenic progenitors that facilitate myogenesis. Nat. Cell Biol.12, 153–163 (2010). CASPubMedPubMed Central Google Scholar
Uezumi, A., Fukada, S., Yamamoto, N., Takeda, S. & Tsuchida, K. Mesenchymal progenitors distinct from satellite cells contribute to ectopic fat cell formation in skeletal muscle. Nat. Cell Biol.12, 143–152 (2010). CASPubMed Google Scholar
Lumeng, C. N., Bodzin, J. L. & Saltiel, A. R. Obesity induces a phenotypic switch in adipose tissue macrophage polarization. J. Clin. Invest.117, 175–184 (2007). CASPubMedPubMed Central Google Scholar
Weisberg, S. P. et al. Obesity is associated with macrophage accumulation in adipose tissue. J. Clin. Invest.112, 1796–1808 (2003). CASPubMedPubMed Central Google Scholar
Wu, D. et al. Eosinophils sustain adipose alternatively activated macrophages associated with glucose homeostasis. Science332, 243–247 (2011). This study implicates IL-4 and/or IL-13 derived from adipose tissue eosinophils in the maintenance of alternatively activated macrophages, thereby linking eosinophils to metabolic homeostasis. CASPubMedPubMed Central Google Scholar
Maizels, R. M. & Allen, J. E. Immunology. Eosinophils forestall obesity. Science332, 186–187 (2011). CASPubMed Google Scholar
Rao, R. R. et al. Meteorin-like is a hormone that regulates immune-adipose interactions to increase beige fat thermogenesis. Cell157, 1279–1291 (2014). CASPubMedPubMed Central Google Scholar
Qiu, Y. et al. Eosinophils and type 2 cytokine signaling in macrophages orchestrate development of functional beige fat. Cell157, 1292–1308 (2014). CASPubMedPubMed Central Google Scholar
Jordan, M. B., Mills, D. M., Kappler, J., Marrack, P. & Cambier, J. C. Promotion of B cell immune responses via an alum-induced myeloid cell population. Science304, 1808–1810 (2004). CASPubMed Google Scholar
Cambier, J. C., Morrison, D. C., Chien, M. M. & Lehmann, K. R. Modeling of T cell contact-dependent B cell activation. IL-4 and antigen receptor ligation primes quiescent B cells to mobilize calcium in response to Ia cross-linking. J. Immunol.146, 2075–2082 (1991). CASPubMed Google Scholar
Lang, P. et al. TCR-induced transmembrane signaling by peptide/MHC class II via associated Ig-alpha/beta dimers. Science291, 1537–1540 (2001). CASPubMed Google Scholar
Tabata, H., Matsuoka, T., Endo, F., Nishimura, Y. & Matsushita, S. Ligation of HLA-DR molecules on B cells induces enhanced expression of IgM heavy chain genes in association with Syk activation. J. Biol. Chem.275, 34998–35005 (2000). CASPubMed Google Scholar
Lane, P. J., McConnell, F. M., Schieven, G. L., Clark, E. A. & Ledbetter, J. A. The role of class II molecules in human B cell activation. Association with phosphatidyl inositol turnover, protein tyrosine phosphorylation, and proliferation. J. Immunol.144, 3684–3692 (1990). CASPubMed Google Scholar
Wang, H. B. & Weller, P. F. Pivotal advance: eosinophils mediate early alum adjuvant-elicited B cell priming and IgM production. J. Leukoc. Biol.83, 817–821 (2008). CASPubMedPubMed Central Google Scholar
Berek, C. Eosinophils: important players in humoral immunity. Clin. Exp. Immunol.183, 57–64 (2016). CASPubMed Google Scholar
Wong, T. W., Doyle, A. D., Lee, J. J. & Jelinek, D. F. Eosinophils regulate peripheral B cell numbers in both mice and humans. J. Immunol.192, 3548–3558 (2014). CASPubMedPubMed Central Google Scholar
Chu, V. T. et al. Eosinophils are required for the maintenance of plasma cells in the bone marrow. Nat. Immunol.12, 151–159 (2011). CASPubMed Google Scholar
Mantis, N. J., Rol, N. & Corthesy, B. Secretory IgA's complex roles in immunity and mucosal homeostasis in the gut. Mucosal Immunol.4, 603–611 (2011). CASPubMedPubMed Central Google Scholar
Tulic, M. K. et al. Thymic indoleamine 2,3-dioxygenase-positive eosinophils in young children: potential role in maturation of the naive immune system. Am. J. Pathol.175, 2043–2052 (2009). CASPubMedPubMed Central Google Scholar
Odemuyiwa, S. O. et al. Cutting edge: human eosinophils regulate T cell subset selection through indoleamine 2,3-dioxygenase. J. Immunol.173, 5909–5913 (2004). CASPubMed Google Scholar
Kim, H. J., Alonzo, E. S., Dorothee, G., Pollard, J. W. & Sant'Angelo, D. B. Selective depletion of eosinophils or neutrophils in mice impacts the efficiency of apoptotic cell clearance in the thymus. PLoS ONE5, e11439 (2010). PubMedPubMed Central Google Scholar
Dajotoy, T. et al. Human eosinophils produce the T cell-attracting chemokines MIG and IP-10 upon stimulation with IFN-gamma. J. Leukoc. Biol.76, 685–691 (2004). CASPubMed Google Scholar
Yang, D. et al. Eosinophil-derived neurotoxin (EDN), an antimicrobial protein with chemotactic activities for dendritic cells. Blood102, 3396–3403 (2003). CASPubMed Google Scholar
Kambayashi, T. & Laufer, T. M. Atypical MHC class II-expressing antigen-presenting cells: can anything replace a dendritic cell? Nat. Rev. Immunol.14, 719–730 (2014). CASPubMed Google Scholar
Farhan, R. K. et al. Effective antigen presentation to helper T cells by human eosinophils. Immunology149, 413–422 (2016). CASPubMedPubMed Central Google Scholar
Carretero, R. et al. Eosinophils orchestrate cancer rejection by normalizing tumor vessels and enhancing infiltration of CD8+ T cells. Nat. Immunol.16, 609–617 (2015). CASPubMed Google Scholar
Noor, Z. et al. Role of eosinophils and tumor necrosis factor alpha in interleukin-25-mediated protection from amebic colitis. MBio8, e02329–e02316 (2017). CASPubMedPubMed Central Google Scholar
Guerra, E. S. et al. Central role of IL-23 and IL-17 producing eosinophils as immunomodulatory effector cells in acute pulmonary aspergillosis and allergic asthma. PLoS Pathog.13, e1006175 (2017). PubMedPubMed Central Google Scholar
Ikutani, M. et al. Prolonged activation of IL-5-producing ILC2 causes pulmonary arterial hypertrophy. JCI Insight2, e90721 (2017). PubMedPubMed Central Google Scholar
Withers, S. B. et al. Eosinophils are key regulators of perivascular adipose tissue and vascular functionality. Sci. Rep.7, 44571 (2017). CASPubMedPubMed Central Google Scholar
Luna-Gomes, T., Bozza, P. T. & Bandeira-Melo, C. Eosinophil recruitment and activation: the role of lipid mediators. Front. Pharmacol.4, 27 (2013). CASPubMedPubMed Central Google Scholar
Liu, Y., Beyer, A. & Aebersold, R. On the dependency of cellular protein levels on mRNA abundance. Cell165, 535–550 (2016). CASPubMed Google Scholar
Dyer, K. D., Garcia-Crespo, K. E., Percopo, C. M., Sturm, E. M. & Rosenberg, H. F. Protocols for identifying, enumerating, and assessing mouse eosinophils. Methods Mol. Biol.1032, 59–77 (2013). CASPubMed Google Scholar
Behzad, A. R. et al. Localization of DNA and RNA in eosinophil secretory granules. Int. Arch. Allergy Immunol.152, 12–27 (2010). CASPubMed Google Scholar
Wickramasinghe, S. N. & Hughes, M. High resolution autoradiographic studies of RNA, protein and DNA synthesis during human eosinophil granulocytopoiesis: evidence for the presence of RNA on or within eosinophil granules. Br. J. Haematol.38, 179–183 (1978). CASPubMed Google Scholar
Bandeira-Melo, C., Woods, L. J., Phoofolo, M. & Weller, P. F. Intracrine cysteinyl leukotriene receptor-mediated signaling of eosinophil vesicular transport-mediated interleukin-4 secretion. J. Exp. Med.196, 841–850 (2002). CASPubMedPubMed Central Google Scholar
Carulli, G. et al. Detection of eosinophils in whole blood samples by flow cytometry. Cytometry34, 272–279 (1998). CASPubMed Google Scholar
Ethier, C., Lacy, P. & Davoine, F. Identification of human eosinophils in whole blood by flow cytometry. Methods Mol. Biol.1178, 81–92 (2014). PubMed Google Scholar
Barnig, C. et al. Circulating human eosinophils share a similar transcriptional profile in asthma and other hypereosinophilic disorders. PLoS ONE10, e0141740 (2015). PubMedPubMed Central Google Scholar
Zhang, J. Q., Biedermann, B., Nitschke, L. & Crocker, P. R. The murine inhibitory receptor mSiglec-E is expressed broadly on cells of the innate immune system whereas mSiglec-F is restricted to eosinophils. Eur. J. Immunol.34, 1175–1184 (2004). CASPubMed Google Scholar
de Bruin, A. M. et al. Eosinophil differentiation in the bone marrow is inhibited by T cell-derived IFN-gamma. Blood116, 2559–2569 (2010). CASPubMed Google Scholar
Dyer, K. D. et al. Functionally competent eosinophils differentiated ex vivo in high purity from normal mouse bone marrow. J. Immunol.181, 4004–4009 (2008). CASPubMedPubMed Central Google Scholar
Satoh, T. et al. Critical role of Trib1 in differentiation of tissue-resident M2-like macrophages. Nature495, 524–528 (2013). CASPubMed Google Scholar
Carlens, J. et al. Common gamma-chain-dependent signals confer selective survival of eosinophils in the murine small intestine. J. Immunol.183, 5600–5607 (2009). CASPubMed Google Scholar
Smith, K. M., Rahman, R. S. & Spencer, L. A. Humoral immunity provides resident intestinal eosinophils access to luminal antigen via eosinophil-expressed low-affinity Fcgamma receptors. J. Immunol.197, 3716–3724 (2016). CASPubMedPubMed Central Google Scholar
Cheng, L. E. et al. IgE-activated basophils regulate eosinophil tissue entry by modulating endothelial function. J. Exp. Med.212, 513–524 (2015). CASPubMedPubMed Central Google Scholar
Esnault, S. et al. Semaphorin 7A is expressed on airway eosinophils and upregulated by IL-5 family cytokines. Clin. Immunol.150, 90–100 (2014). CASPubMed Google Scholar
Stevens, W. W., Kim, T. S., Pujanauski, L. M., Hao, X. & Braciale, T. J. Detection and quantitation of eosinophils in the murine respiratory tract by flow cytometry. J. Immunol. Methods327, 63–74 (2007). CASPubMedPubMed Central Google Scholar
Grimaldi, J. C. et al. Depletion of eosinophils in mice through the use of antibodies specific for C-C chemokine receptor 3 (CCR3). J. Leukoc. Biol.65, 846–853 (1999). CASPubMed Google Scholar