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Regulatory T Cells Do Not Suppress Rather Activate Human Basophils by IL-3 and STAT5-Dependent Mechanisms Mrinmoy Das, Emmanuel Stephen-Victor, Jagadeesh Bayry

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Regulatory T Cells Do Not Suppress Rather Activate Human Basophils by IL-3 and STAT5-Dependent Mechanisms Mrinmoy Das, Emmanuel Stephen-Victor, Jagadeesh Bayry Regulatory T cells do not suppress rather activate human basophils by IL-3 and STAT5-dependent mechanisms Mrinmoy Das, Emmanuel Stephen-Victor, Jagadeesh Bayry To cite this version: Mrinmoy Das, Emmanuel Stephen-Victor, Jagadeesh Bayry. Regulatory T cells do not suppress rather activate human basophils by IL-3 and STAT5-dependent mechanisms. OncoImmunology, Taylor & Francis, 2020, 9, pp.1773193. 10.1080/2162402X.2020.1773193. inserm-02879887 HAL Id: inserm-02879887 https://www.hal.inserm.fr/inserm-02879887 Submitted on 24 Jun 2020 HAL is a multi-disciplinary open access L’archive ouverte pluridisciplinaire HAL, est archive for the deposit and dissemination of sci- destinée au dépôt et à la diffusion de documents entific research documents, whether they are pub- scientifiques de niveau recherche, publiés ou non, lished or not. The documents may come from émanant des établissements d’enseignement et de teaching and research institutions in France or recherche français ou étrangers, des laboratoires abroad, or from public or private research centers. publics ou privés. Distributed under a Creative Commons Attribution - NonCommercial| 4.0 International License OncoImmunology ISSN: (Print) (Online) Journal homepage: https://www.tandfonline.com/loi/koni20 Regulatory T cells do not suppress rather activate human basophils by IL-3 and STAT5-dependent mechanisms Mrinmoy Das , Emmanuel Stephen-Victor & Jagadeesh Bayry To cite this article: Mrinmoy Das , Emmanuel Stephen-Victor & Jagadeesh Bayry (2020) Regulatory T cells do not suppress rather activate human basophils by IL-3 and STAT5-dependent mechanisms, OncoImmunology, 9:1, 1773193, DOI: 10.1080/2162402X.2020.1773193 To link to this article: https://doi.org/10.1080/2162402X.2020.1773193 © 2020 The Author(s). Published with license by Taylor & Francis Group, LLC. Published online: 05 Jun 2020. Submit your article to this journal Article views: 109 View related articles View Crossmark data Full Terms & Conditions of access and use can be found at https://www.tandfonline.com/action/journalInformation?journalCode=koni20 ONCOIMMUNOLOGY 2020, VOL. 9, NO. 1, 1–3 https://doi.org/10.1080/2162402X.2020.1773193 AUTHOR’S VIEW Regulatory T cells do not suppress rather activate human basophils by IL-3 and STAT5-dependent mechanisms Mrinmoy Dasa*, Emmanuel Stephen-Victora*, and Jagadeesh Bayry b aDivision of Immunology, Boston Children’s Hospital, Harvard Medical School, Boston, MA, USA; bInstitut National de la Santé et de la Recherche Médicale, Centre de Recherche des Cordeliers, Equipe - Immunopathologie et Immunointervention Thérapeutique, Sorbonne Université, Université de Paris, Paris, France ABSTRACT ARTICLE HISTORY Basophils play an important role in orienting Th2 immune response, and in the pathogenesis of allergic Received 19 May 2020 and inflammatory disorders. However, the mechanism by which basophils are kept in check remains Accepted 20 May 2020 unclear and hence we explored the role of regulatory T cells (Treg cells) in this process. We demonstrate KEYWORDS that human Treg cells do not suppress rather induce activation of basophils, and promote Th2 responses Basophil; CD4+CD25+FoxP3+ by IL-3 and STAT5-dependent mechanism. regulatory T cell; cancer; immune evasion; Tregs; Th2 response Basophils are rare granulocytes representing approximately 1% cells, they are the targets to boost protective immune response to of peripheral blood leukocytes. Basophils are reported to play cancer.2 a role in regulating acquired immunity, particularly by pro­ In order to explore the regulation of human basophils moting Th2 cell differentiation as well as amplifying humoral functions by Treg cells, we activated basophils with IL-3 and memory response.1 Several studies have also uncovered a role anti-IgE antibodies that induce basophil activation via IL-3 for basophils in protective immunity to pathogens. But dysre­ receptor (IL-3R, a heterodimer composed of IL-3-specific α- gulated functions of basophils are associated with many pathol­ subunit and a common β-subunit) and FcεRI-mediated signal­ ogies and in particular allergic and inflammatory diseases. ing respectively. Interestingly, we found that basophils were Main reason for the exceptional role of basophils in various refractory to Treg cell-mediated suppression. Despite being pathologies despite their low frequency, is the expression of an under the influence of Treg cells, basophils had undergone array of receptors including FcεRI and cytokine receptors that activation and anti-IgE-induced degranulation as analyzed by sense signals derived from diverse sources, and immediate the expression of surface markers (CD203c, CD69, CD63 and release of inflammatory mediators including cytokines (IL-4, CD107a) and histamine in the culture supernatants.5 IL-13, IL-6, thymic stromal lymphopoietin and B-cell- We were surprised by the results and hence investigated rea­ activating factor), histamine and leukotriene that support sons for the refractoriness of human basophils toward Treg- hypersensitive and inflammatory responses.1 However, the mediated suppressive effects. As mentioned earlier, Treg cells mechanisms by which basophils are kept in check remains mediate suppression of target cells by contact-dependent and – unclear and hence recently we explored if independent mechanisms. However, we found that human baso­ CD4+CD25+Foxp3+ regulatory T cells (Treg cells) have the phils either in the circulation or residing at secondary lymphoid capacity to control the functions of human basophils. organs lack CD80 and CD86, the receptors for CTLA-4; and Treg cells play a pivotal role in maintaining the peripheral HLA-DR, the receptor for LAG-3.6 Furthermore, we also found tolerance by inhibiting autoimmune and inflammatory diseases. that human basophils do not express TGF-βRII. On the other Treg cells also play a major role in transplantation tolerance and hand, a subset of human basophils express IL-10Rα, but we found in suppressing tumor immunity.2 The cellular targets of Treg- that basophils are not responsive to IL-10.5 Together, these results mediated suppressor functions include T cells, dendritic cells, could explain underlying reasons for the refractoriness of human B cells, macrophages, monocytes, mast cells, NK cells and NKT basophils toward Treg cell-mediated suppression. cells.3 Treg cells exert their suppressive functions through several Next, we explored if Treg cells could suppress resting baso­ mechanisms that are mediated either by cell-cell contact through phils. We co-cultured resting basophils with activated memory inhibitory surface molecules (cytotoxic T lymphocyte antigen-4 Treg cells in the absence of any exogenous stimulation or (CTLA-4) and lymphocyte-activation gene-3 (LAG-3)), or by cytokines. Interestingly, we found that Treg cells induced acti­ secreting regulatory cytokines (TGF-β1 and IL-10) and cytolysis vation of human basophils characterized by the enhanced through cytotoxic molecules (granzyme and perforin).4 As Treg expression of surface markers associated with basophil activa­ cells suppress the activation of both innate and adaptive immune tion (CD203c, CD13 and CD69) and secretion of cytokines (IL- CONTACT Jagadeesh Bayry [email protected] Institut National de la Santé et de la Recherche Médicale Unité 1138, Centre de Recherche des Cordeliers, 15 Rue de l’Ecole de Médicine, Paris F-75006, France *These authors contributed equally to this work. © 2020 The Author(s). Published with license by Taylor & Francis Group, LLC. This is an Open Access article distributed under the terms of the Creative Commons Attribution-NonCommercial License (http://creativecommons.org/licenses/by-nc/4.0/), which permits unrestricted non-commercial use, distribution, and reproduction in any medium, provided the original work is properly cited. 2 M. DAS ET AL. Figure 1. Tumor cells secrete chemokines that recruit Treg cells to the tumor microenvironment. Our data suggest that tumor-associated Treg cells promote tumor survival and its immune escape by several mechanisms including secretion of IL-3 to activate basophils and to orchestrate Th2 responses. 8, IL-13 and IL-4). However, Treg-induced basophil activation malignant cells are surrounded by diverse nonmalignant cells was not associated with degranulation. Trans-well experiments (immune cells, stromal cells and endothelial cells) that coordinate and blocking studies targeting the intercellular adhesion mole­ and orchestrate the immune response to the malignant cells. cule-1 and inducible T cell costimulator ligand pathway in Treg Notably, tumor cells and innate immune cells secrete several cells failed to mitigate basophil activation. In contrast, cultur­ chemokines such as CCL17/22, CCL5, and CXCL9/10 to establish ing basophils with supernatants from the activated Treg cells a tolerogenic microenvironment by recruiting Treg cells.9 In recapitulated basophil activation similar to that observed in PDAC, chemokines such as CCL7 secreted by alternatively acti­ our co-culture studies.5 These results suggested that soluble vated monocytes recruit basophils to the tumor draining-lymph mediators released from the activated Treg cells but not cellular nodes. IL-3 secreted by T cells in the tumor microenvironment contact drive the activation of basophils. further activates basophils to orchestrate a Th2 responses by Notably, we found that activated Treg cells secrete IL-3 that secreting IL-4.8 Based on our observation it appears that Treg could potently activate basophils. To further
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