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Eosinophils in Immunity and Disease Roles and Regulation of Gastrointestinal Roles and Regulation of Gastrointestinal Eosinophils in Immunity and Disease YunJae Jung and Marc E. Rothenberg This information is current as J Immunol 2014; 193:999-1005; ; of September 29, 2021. doi: 10.4049/jimmunol.1400413 http://www.jimmunol.org/content/193/3/999 Downloaded from References This article cites 88 articles, 31 of which you can access for free at: http://www.jimmunol.org/content/193/3/999.full#ref-list-1 Why The JI? Submit online. http://www.jimmunol.org/ • Rapid Reviews! 30 days* from submission to initial decision • No Triage! Every submission reviewed by practicing scientists • Fast Publication! 4 weeks from acceptance to publication *average by guest on September 29, 2021 Subscription Information about subscribing to The Journal of Immunology is online at: http://jimmunol.org/subscription Permissions Submit copyright permission requests at: http://www.aai.org/About/Publications/JI/copyright.html Email Alerts Receive free email-alerts when new articles cite this article. Sign up at: http://jimmunol.org/alerts The Journal of Immunology is published twice each month by The American Association of Immunologists, Inc., 1451 Rockville Pike, Suite 650, Rockville, MD 20852 Copyright © 2014 by The American Association of Immunologists, Inc. All rights reserved. Print ISSN: 0022-1767 Online ISSN: 1550-6606. Th eJournal of Brief Reviews Immunology Roles and Regulation of Gastrointestinal Eosinophils in Immunity and Disease YunJae Jung*,† and Marc E. Rothenberg* Eosinophils have historically been considered to be de- using eosinophil-specific surface markers was established (5). structive end-stage effector cells that have a role in Additionally, the development of eosinophil-deficient mouse parasitic infections and allergic reactions by the release strains has expanded the understanding of the role of intes- of their granule-derived cytotoxic proteins. However, an tinal eosinophils from dogmatic antiparasitic effector cells to increasing number of experimental observations indi- immune modulatory cells. In this article, we discuss emerg- cate that eosinophils also are multifunctional leukocytes ing advances in the understanding of intestinal eosino- involved in diverse inflammatory and physiologic immune phils at baseline and during inflammatory gastrointestinal responses. Under homeostatic conditions, eosinophils disorders, including primary eosinophilic gastrointestinal dis- Downloaded from are particularly abundant in the lamina propria of orders (EGIDs), such as eosinophilic esophagitis (EoE) (6). the gastrointestinal tract, where their involvement in Developmental properties of eosinophils various biological processes within the gastrointestinal tract has been posited. In this review, we summarize the Eosinophils develop in the bone marrow from pluripotent molecular steps involved in eosinophil development and stem cells that become eosinophil progenitors marked by + + http://www.jimmunol.org/ describe eosinophil trafficking to the gastrointestinal CD34 CD125 expression. Eosinophil lineage specification is tract. We synthesize the current findings on the pheno- determined by the interplay of several transcription factors, typic and functional properties of gastrointestinal eo- including the zinc finger transcription factor GATA-binding protein 1 (GATA-1), the E26 transformation-specific family sinophils and the accumulating evidence that they member PU.1, IFN consensus sequence binding protein, and have a contributory role in gastrointestinal disorders, C/EBP family members (2, 7, 8), as well as by regulation by with a focus on primary eosinophilic gastrointestinal dis- microRNAs, including miR-21 and miR-223 (9, 10). Of the orders. Finally, we discuss the potential role of eosino- transcription factors, GATA-1 is the most important; targeted phils as modulators of the intestinal immune system. deletion of the high-affinity double palindromic GATA-1 by guest on September 29, 2021 The Journal of Immunology, 2014, 193: 999–1005. binding site in the Gata1 promoter results in eosinophil- depleted mice, referred to as ΔdblGATA mice (11). ΔdblGATA osinophils are multifunctional proinflammatory leu- mice, along with another eosinophil-deficient strain gener- kocytes involved in the pathogenesis of allergic dis- ated using a promoter of the eosinophil peroxidase gene to E orders and are implicated in the protection against drive expression of cytocidal diphtheria toxin A (referred to helminth infections (1, 2). Eosinophils are generally thought as PHIL mice) (12), are being used to uncover the function of as proinflammatory cells because they release pleotropic of eosinophils (13). Eosinophil development is guided by cytokines, chemokines, and lipid mediators, as well as toxic signals from the aforementioned transcription factors; sub- cytoplasmic granule constituents, including major basic pro- sequently, permissive proliferation and differentiation are tein, eosinophil cationic protein, eosinophil peroxidase, and regulated primarily by IL-5, although IL-3 and GM-CSF can eosinophil-derived neurotoxin (EDN) (3, 4). Although eosin- also contribute (2). Of these cytokines, IL-5 is the most ophils are recognized as circulating cells, composing 1–5% specific for selective differentiation of eosinophils, stimulat- of peripheral blood leukocytes, they are primarily resident in ing their migration from the bone marrow to the circula- the lamina propria of the small intestine, where they com- tion (2, 14). Eosinophils released into the blood migrate into pose a substantial fraction (e.g., 20–30%) of the cellular the thymus, mammary gland, uterus, and the gastrointes- population (2, 5). Recently, a standard protocol for the isola- tinal tract, with the last having the highest eosinophil levels tion of murine eosinophils from the intestinal lamina propria under homeostatic conditions (2). Levels of gastrointestinal *Division of Allergy and Immunology, Cincinnati Children’s Hospital Medical Center, Cincinnati College of Medicine, 3333 Burnet Avenue, ML7028, Cincinnati, OH University of Cincinnati College of Medicine, Cincinnati, OH 45229; and †Department 45229. E-mail address: [email protected] of Microbiology, Graduate School of Medicine, Gachon University, Incheon 406–799, Abbreviations used in this article: APRIL, a proliferation-inducing ligand; EDN, Republic of Korea eosinophil-derived neurotoxin; EGID, eosinophilic gastrointestinal disorder; EoE, eo- Received for publication February 12, 2014. Accepted for publication April 23, 2014. sinophilic esophagitis; GATA-1, GATA-binding protein 1; IBD, inflammatory bowel disease; ILC2, type 2 innate lymphoid cell; PIR, paired Ig-like receptor; Siglec, sialic This work was supported by National Institutes of Health Grants U19 AI066738, R37 acid–binding Ig-like lectin; SIRP-a, signal regulatory protein a. A1045898, and U19 AI070235 and by the Basic Science Research Program through the National Research Foundation of Korea funded by the Ministry of Education Ó (2013R1A1A2004820). Copyright 2014 by The American Association of Immunologists, Inc. 0022-1767/14/$16.00 Address correspondence and reprint requests to Dr. Marc E. Rothenberg, Division of Allergy and Immunology, Cincinnati Children’s Hospital Medical Center, University of www.jimmunol.org/cgi/doi/10.4049/jimmunol.1400413 1000 BRIEF REVIEWS: GASTROINTESTINAL EOSINOPHILS eosinophils were estimated to be $10-fold higher than in steady-state but are ready for conversion to proinflammatory the circulation (2, 3). Examination of the entire gastrointes- cells via downregulation of CD22. tinal tract reveals that only the esophagus is devoid of baseline Under homeostatic conditions, most eosinophils produced eosinophils and that eosinophil levels progressively increase in the bone marrow migrate to the small intestine; this pro- from the stomach to the colon, where they can be fairly high cess is regulated by eosinophil expression of CCR3 and a4b7 (i.e., as many as 50 eosinophils/high-power microscopic field integrin because their cognate ligands (eotaxin and mucosal [4003]) (15). vascular addressin cell adhesion molecule 1, respectively) are constitutively expressed in the intestine (15, 26). b7 integrin Unique characteristics of intestinal eosinophils appears to be particularly important in the large intestine, Until recently, no detailed phenotypic analysis of intestinal whereas eotaxins mediate eosinophil homing in the large and eosinophils had been performed because of the difficulties small intestine of mice (26, 27). Gastrointestinal eosinophils inherent in identifying and/or isolating sufficient numbers of are postmitotic and have limited survival in the absence of these cells from the gastrointestinal tract. However, phenotypic survival-promoting cytokine signals (28); conversely, cytokine characterization of murine eosinophils in the intestinal lamina signaling through the common g-chain increases the lifespan propria was reported recently by several groups (5, 16, 17). For of murine small intestinal eosinophils (Fig. 1A) (5). There- detection of eosinophils in mice, there are several available fore, in combination with a specialized influx mechanism, the markers, including CCR3, sialic acid–binding Ig-like lectin prolonged survival of eosinophils ($14 d) contributes to their (Siglec)-F (homolog of siglec-8 in humans), and CD125, predominance in the gastrointestinal tract (5). In addition, Downloaded from which encodes for IL-5Ra (18–20). Although these markers signal regulatory protein a (SIRP-a), highly expressed in are primarily expressed
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