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Cytokine Diversity in Human Peripheral Blood Eosinophils: Profound Variability of IL-16

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Cytokine Diversity in Human Peripheral Blood Eosinophils: Profound Variability of IL-16 Cytokine Diversity in Human Peripheral Blood Eosinophils: Profound Variability of IL-16 This information is current as Michelle Ma, Caroline M. Percopo, Daniel E. Sturdevant, of September 28, 2021. Albert C. Sek, Hirsh D. Komarow and Helene F. Rosenberg J Immunol 2019; 203:520-531; Prepublished online 10 June 2019; doi: 10.4049/jimmunol.1900101 http://www.jimmunol.org/content/203/2/520 Downloaded from Supplementary http://www.jimmunol.org/content/suppl/2019/06/07/jimmunol.190010 Material 1.DCSupplemental http://www.jimmunol.org/ References This article cites 84 articles, 14 of which you can access for free at: http://www.jimmunol.org/content/203/2/520.full#ref-list-1 Why The JI? Submit online. • Rapid Reviews! 30 days* from submission to initial decision by guest on September 28, 2021 • No Triage! Every submission reviewed by practicing scientists • Fast Publication! 4 weeks from acceptance to publication *average 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 All rights reserved. Print ISSN: 0022-1767 Online ISSN: 1550-6606. The Journal of Immunology Cytokine Diversity in Human Peripheral Blood Eosinophils: Profound Variability of IL-16 Michelle Ma,* Caroline M. Percopo,* Daniel E. Sturdevant,† Albert C. Sek,* Hirsh D. Komarow,‡ and Helene F. Rosenberg* Eosinophilic leukocytes develop in the bone marrow and migrate from peripheral blood to tissues, where they maintain homeostasis and promote dysfunction via release of preformed immunomodulatory mediators. In this study, we explore human eosinophil heterogeneity with a specific focus on naturally occurring variations in cytokine content. We found that human eosinophil-associated cytokines varied on a continuum from minimally (coefficient of variation [CV] £ 50%) to moderately variable (50% < CV £ 90%). Within the moderately variable group, we detected immunoreactive IL-27 (953 6 504 pg/mg lysate), a mediator not previously associated with human eosinophils. However, our major finding was the distinct and profound variability of eosinophil-associated IL-16 (CV = 103%). Interestingly, eosinophil IL-16 content correlated directly with body mass index (R2 = 0.60, ***p < 0.0001) in one donor subset. We found Downloaded from no direct correlation between eosinophil IL-16 content and donor age, sex, total leukocytes, lymphocytes, or eosinophils (cells per microliter), nor was there any relationship between IL-16 content and the characterized 2295T/C IL-16 promoter polymorphism. Likewise, although eosinophil IL-1b,IL-1a, and IL-6 levels correlated with one another, there was no direct association between any of these cytokines and eosinophil IL-16 content. Finally, a moderate increase in total dietary fat resulted in a 2.7-fold reduction in eosinophil IL-16 content among C57BL/6-IL5tg mice. Overall, these results suggest that relationships between energy metabolism, eosinophils, and IL-16 content are not direct or straightforward. Nonetheless, given our current understanding of the connections http://www.jimmunol.org/ between asthma and obesity, these findings suggest important eosinophil-focused directions for further exploration. The Journal of Immunology, 2019, 203: 520–531. osinophils have been historically perceived as end-stage, spectrum of allergic and nonallergic disorders (3–7), evolution tells cytotoxic cells with a limited range of effector responses. us that the ability to induce pathologic conditions cannot be the E Numerous observations have profoundly altered these views “raison d’eˆtre” for any existing cell lineage (1). Recent studies that and have provided a spotlight on eosinophils as complex cells with explore the role of eosinophils at homeostasis in the gastrointestinal critical immunomodulatory functions (1, 2). Whereas eosinophils tract (8, 9), which identify distinct eosinophil-mediated antimicro- by guest on September 28, 2021 are activated in and contribute to the pathophysiology of a wide bial activities (10, 11) and that reveal specific eosinophil subtypes (12, 13), suggest that there are new and profound complexities remaining to be unraveled. *Inflammation Immunobiology Section, Laboratory of Allergic Diseases, National Among the most prominent features of eosinophils are their Institute of Allergy and Infectious Diseases, National Institutes of Health, Bethesda, MD 20892; †Genomics Unit, Research Technologies Branch, National Institute of distinct cytoplasmic granules, which contain unique cationic proteins Allergy and Infectious Diseases, National Institutes of Health, Hamilton, MT 59840; (14) and immunomodulatory mediators (15–17). Moqbel, Lacy, and and ‡Mast Cell Biology Section, Laboratory of Allergic Diseases, National Institute of Allergy and Infectious Diseases, National Institutes of Health, Bethesda, MD colleagues (18, 19) were among the first to characterize these me- 20892 diators in eosinophils, which include cytokines, chemokines, lipids, ORCIDs: 0000-0002-1497-8128 (C.M.P.); 0000-0002-8170-3749 (A.C.S.); 0000- and growth factors and their receptors (20). Physiologic roles for 0001-7012-9406 (H.D.K.). these mediators and their importance in eosinophil function was Received for publication January 24, 2019. Accepted for publication May 20, 2019. highlighted by Lee and colleagues (21) in their manuscript entitled This work was supported by the National Institute of Allergy and Infectious Diseases “Eosinophils in Health and Disease: The LIAR Hypothesis,” in which Division of Intramural Research (Z01-AI000941-14 to H.F.R.). they proposed that eosinophils were recruited to tissues to promote M.M. performed most of the experimental work, optimized the eosinophil isolation local immunity, remodeling, and repair. This hypothesis has been and cytokine profiling, coordinated the donor samples with the National Institutes of Health Clinical Center Blood Bank, and reviewed the methods for the manuscript. strongly supported by recent studies on eosinophil function in health C.M.P. performed additional experimental work and provided input on the first draft and disease in vivo [e.g., studies featured in reviews on eosinophil of the manuscript. D.E.S. performed multivariate analysis of the cytokine profiling function in helminth infection and innate immunity (22–24)]. data and reviewed the revised manuscript. A.C.S. assisted with experimental work and prepared photographic images for the manuscript. H.D.K. was instrumental in As such, a better understanding of eosinophil mediators and the obtaining normal donor samples via the Laboratory of Allergic Diseases protocol and mechanisms that promote their synthesis and release is currently a provided input on the first and subsequent drafts of the manuscript. H.F.R. concep- topic of significant interest (25–27). Toward this end, Melo and tualized the project, performed data analysis, and wrote the first and subsequent drafts of the manuscript. colleagues (28) have characterized the tubulovesicular networks Address correspondence and reprint requests to Dr. Helene F. Rosenberg, Inflamma- that serve as conduits for mediator secretion, and Lacy and col- tion Immunobiology Section, 50 South Drive, Room 6241 MSC 8014, National leagues (29, 30) have examined signaling factors that pro- Institute of Allergy and Infectious Diseases/National Institutes of Health, Bethesda, mote degranulation. The potential for distinct cytokine profiles MD 20892. E-mail address: [email protected] (i.e., differences among eosinophils from human subjects) was The online version of this article contains supplemental material. first addressed by Spencer and colleagues (31), who focused on Abbreviations used in this article: BMI, body mass index; CV, coefficient of varia- tion; LAD, Laboratory of Allergic Diseases; mpd, mean pixel density; npd, normal- seven individual cytokines identified in eosinophil lysates from 18 ized pixel density. nonallergic and allergic donors. Among their findings, the Th1 www.jimmunol.org/cgi/doi/10.4049/jimmunol.1900101 The Journal of Immunology 521 cytokine IFN-g was identified as a prominent component of hu- on-site (14BS vivarium, National Institute of Allergy and Infectious Dis- man eosinophils, although no significant differences were reported eases/National Institutes of Health). Mice were maintained on normal in comparisons between allergic versus nonallergic donors. house diets (LabDiet, Advanced Protocol 5V0T, 12.5% kcal from fat) or a diet with moderately increased fat (LabDiet, Select Mouse 5B0G, 22% In this manuscript, we build on these findings using dual-Ab kcal from fat), the latter for 5–6 wk prior to evaluation. The National proteome profiling technology. With this method we examined Institute of Allergy and Infectious Diseases Division of Intramural Re- differential expression of 36 cytokines in lysates prepared from search Animal Care and Use Committee, as part of the National Institutes peripheral blood eosinophils purified from whole blood from normal of Health Intramural Research Program, approved all the experimental procedures as per protocols LAD7 and LAD 8E. donors. As a component of this study, we identified naturally oc- curring variations in cytokine
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