The lectin ArtinM activates RBL-2H3 mast cells without inducing degranulation

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Abstract

Mast cells are connective tissue resident cells with morphological and functional characteristics that contribute to their role in allergic and inflammatory processes, host defense and maintenance of tissue homeostasis. Mast cell activation results in the release of pro-inflammatory mediators which are largely responsible for the physiological functions of mast cells. The lectin ArtinM, extracted from Artocarpus heterophyllus (jackfruit), binds to D-manose, thus inducing degranulation of mast cells. ArtinM has several immunomodulatory properties including acceleration of wound healing, and induction of cytokine release. The aim of the present study was to investigate the role of ArtinM in the activation and proliferation of mast cells. The rat mast cell line RBL-2H3 was used throughout this study. At a low concentration (0.25μg/mL), ArtinM induced mast cell activation and the release of IL-6 without stimulating the release of pre-formed or newly formed mediators. Additionally, when the cells were activated by ArtinM protein tyrosine phosphorylation was stimulated. The low concentration of ArtinM also activated the transcription factor NFkB, but not NFAT. ArtinM also affected the cell cycle and stimulated cell proliferation. Therefore, ArtinM may have therapeutic applications by modulating immune responses due to its ability to activate mast cells and promote the release of newly synthesized mediators. Additionally, ArtinM could have beneficial effects at low concentrations without degranulating mast cells and inducing allergic reactions.

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Most cited references 63

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Mast cells are so widely recognized as critical effector cells in allergic disorders and other immunoglobulin E-associated acquired immune responses that it can be difficult to think of them in any other context. However, mast cells also can be important as initiators and effectors of innate immunity. In addition, mast cells that are activated during innate immune responses to pathogens, or in other contexts, can secrete products and have cellular functions with the potential to facilitate the development, amplify the magnitude or regulate the kinetics of adaptive immune responses. Thus, mast cells may influence the development, intensity and duration of adaptive immune responses that contribute to host defense, allergy and autoimmunity, rather than simply functioning as effector cells in these settings.

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Mast cells are well known for their role in allergic and anaphylactic reactions, as well as their involvement in acquired and innate immunity. Increasing evidence now implicates mast cells in inflammatory diseases where they are activated by non-allergic triggers, such as neuropeptides and cytokines, often exerting synergistic effects as in the case of IL-33 and neurotensin. Mast cells can also release pro-inflammatory mediators selectively without degranulation. In particular, IL-1 induces selective release of IL-6, while corticotropin-releasing hormone secreted under stress induces the release of vascular endothelial growth factor. Many inflammatory diseases involve mast cells in cross-talk with T cells, such as atopic dermatitis, psoriasis and multiple sclerosis, which all worsen by stress. How mast cell differential responses are regulated is still unresolved. Preliminary evidence suggests that mitochondrial function and dynamics control mast cell degranulation, but not selective release. Recent findings also indicate that mast cells have immunomodulatory properties. Understanding selective release of mediators could explain how mast cells participate in numerous diverse biologic processes, and how they exert both immunostimulatory and immunosuppressive actions. Unraveling selective mast cell secretion could also help develop unique mast cell inhibitors with novel therapeutic applications. This article is part of a Special Issue entitled: Mast cells in inflammation. Copyright © 2010 Elsevier B.V. All rights reserved.

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Author and article information

Contributors

Patricia A. A. Buranello: Role: ConceptualizationRole: Formal analysisRole: Funding acquisitionRole: InvestigationRole: MethodologyRole: ValidationRole: Writing – original draftRole: Writing – review & editing

Valéria C. Barbosa-Lorenzi: Role: Formal analysisRole: InvestigationRole: MethodologyRole: Writing – review & editing

Marcelo R. Pinto: Role: Formal analysisRole: Writing – original draftRole: Writing – review & editing

Gabriela Pereira-da-Silva: Role: Formal analysisRole: MethodologyRole: Writing – review & editing

Maria Cristina R. A. Barreira:

ORCID: http://orcid.org/0000-0001-7425-0908

Role: ConceptualizationRole: Funding acquisitionRole: MethodologyRole: ResourcesRole: Writing – review & editing

Maria Célia Jamur: Role: ConceptualizationRole: Formal analysisRole: Funding acquisitionRole: ResourcesRole: SupervisionRole: Writing – review & editing

Constance Oliver:

ORCID: http://orcid.org/0000-0002-8633-4612

Role: ConceptualizationRole: Data curationRole: Formal analysisRole: Funding acquisitionRole: InvestigationRole: MethodologyRole: Project administrationRole: ResourcesRole: SupervisionRole: Writing – review & editing

Bruno Lourenco Diaz: Role: Editor

Journal

Journal ID (nlm-ta): PLoS One

Journal ID (iso-abbrev): PLoS ONE

Journal ID (publisher-id): plos

Journal ID (pmc): plosone

Title: PLoS ONE

Publisher: Public Library of Science (San Francisco, CA USA )

ISSN (Electronic): 1932-6203

Publication date (Electronic): 24 March 2020

Publication date Collection: 2020

Volume: 15

Issue: 3

Electronic Location Identifier: e0230633

Affiliations

[1 ] Department of Cell and Molecular Biology and Pathogenic Bioagents, Ribeirão Preto Medical School, University of São Paulo, Ribeirão Preto, São Paulo, Brazil

[2 ] Department of Maternal-Infant Nursing and Public Health, Escola de Enfermagem de Ribeirão Preto, University of São Paulo, Ribeirão Preto, São Paulo, Brazil

Universidade Federal do Rio de Janeiro, BRAZIL

Author notes

Competing Interests: The authors have declared that no competing interests exist.

[¤a]

Current address: Department of Biological Sciences, Universidade Federal do Triangulo Mineiro, Uberaba, Minas Gerais, Brazil

[¤b]

Current address: Laboratory of Biopathology and Molecular Biology, University of Uberaba, Uberaba, Minas Gerais, Brazil

* E-mail: coliver@ 123456fmrp.usp.br

Author information

Maria Cristina R. A. Barreira http://orcid.org/0000-0001-7425-0908

Constance Oliver http://orcid.org/0000-0002-8633-4612

Article

Publisher ID: PONE-D-19-31092

DOI: 10.1371/journal.pone.0230633

PMC ID: 7092976

PubMed ID: 32208440

SO-VID: edfbf360-9787-4956-8507-526c810c9e80

License:

This is an open access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.

History

Date received : 7 November 2019

Date accepted : 4 March 2020