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Mast Cells: From Host Defense to Pathology

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A special issue of International Journal of Molecular Sciences (ISSN 1422-0067). This special issue belongs to the section "Molecular Immunology".

Deadline for manuscript submissions: closed (31 December 2021) | Viewed by 53287

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Prof. Dr. Margarita Martín

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Head of Biochemistry and Molecular Biology Unit, Biomedicine Department, Faculty of Medicine and Health Sciences, University of Barcelona, Carrer de Casanova 143, E-08036 Barcelona, Spain
Interests: immunoreceptors; adaptor molecules; signal transduction; regulation of immune system; mast cells; allergy; anaphylaxis; KIT oncogenic disorders
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Dear Colleagues,

For this Special Issue of the International Journal of Molecular Sciences, we invite you to contribute either an original research article or a review article on any aspect of the subject of “Mast Cells: From Host Defense to Pathology”. Articles that provide mechanistic and functional insights at either a cellular or a molecular level, both in vitro and in vivo, are particularly welcome.
The evolutionary role of mast cells has been to act as a first line of defense against parasites and venoms. For this reason, they are found predominantly at the interface between the host and the external environment, at places of potential entry of pathogens or that are in contact with harmful substances. They express a wide spectrum of cell surface receptors, including immunoglobulin Fc receptors, toll-like receptors for pattern recognition, and other innate receptors, that enable them to respond to endogenous mediators and exogenous stimuli to release immune mediators to overcome the insult. However, mast cells are best known and widely recognized for their role in pathology as they are the main effector cell in allergies and anaphylaxis, a severe allergic reaction that may cause death. In the last few decades, the incidence of allergies and anaphylaxis has risen at an alarming rate and continues to rise. Therefore, a better understanding of the molecular basis for mast cell function will have repercussions that range from host defense to pathology.

Prof. Dr. Margarita Martín
Guest Editor

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Keywords

mast cells
bacteria
virus
host defense
allergy
anaphylaxis
molecular mechanisms

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Mast Cells: From Host Defense to Pathology 2.0 in International Journal of Molecular Sciences (16 articles)

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Editorial

Jump to: Research, Review

4 pages, 602 KiB

Open AccessEditorial

Mast Cells: When the Best Defense Is an Attack?

by Margarita Martin

Int. J. Mol. Sci. 2022, 23(7), 3570; https://doi.org/10.3390/ijms23073570 - 25 Mar 2022

Cited by 1 | Viewed by 1796

Abstract

The main goal of this Special Issue was to highlight the recent advances made on the role of mast cells (MCs) in host defense and pathology [...] Full article

(This article belongs to the Special Issue Mast Cells: From Host Defense to Pathology)

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Research

Jump to: Editorial, Review

12 pages, 1544 KiB

Open AccessArticle

Resveratrol Is a Natural Inhibitor of Human Intestinal Mast Cell Activation and Phosphorylation of Mitochondrial ERK1/2 and STAT3

by Sabrina Bilotta, Lakshmi Bhargavi Paruchuru, Katharina Feilhauer, Jörg Köninger and Axel Lorentz

Int. J. Mol. Sci. 2021, 22(14), 7640; https://doi.org/10.3390/ijms22147640 - 16 Jul 2021

Cited by 21 | Viewed by 2534

Abstract

Mast cells play a critical role as main effector cells in allergic and other inflammatory diseases. Usage of anti-inflammatory nutraceuticals could be of interest for affected patients. Resveratrol, a natural polyphenol found in red grapes, is known for its positive properties. Here, we analyzed the effects of resveratrol on FcεRI-mediated activation of mature human mast cells isolated from intestinal tissue (hiMC). Resveratrol inhibited degranulation and expression of cytokines and chemokines such as CXCL8, CCL2, CCL3, CCL4, and TNF-α in a dose-dependent manner. Further, resveratrol inhibited the phosphorylation of extracellular signal-regulated kinase (ERK) 1/2 and signal transducer and activator of transcription (STAT) 3. ERK1/2 is known to be involved in cytokine expression of hiMC and to directly interact with STAT3. Mitochondrial STAT3 is phosphorylated by ERK1/2 and contributes to mast cell degranulation. We were able to isolate mitochondrial fractions from small hiMC numbers and could show that activation of mitochondrial STAT3 and ERK1/2 in hiMC was also inhibited by resveratrol. Our results indicate that resveratrol inhibits hiMC activation by inhibiting the phosphorylation of mitochondrial and nuclear ERK1/2 and STAT3, and it could be considered as an anti-inflammatory nutraceutical in the treatment of mast cell-associated diseases. Full article

(This article belongs to the Special Issue Mast Cells: From Host Defense to Pathology)

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12 pages, 4008 KiB

Open AccessArticle

Effect of a Cytoprotective Dose of Dehydroleucodine, Xanthatin, and 3-Benzyloxymethyl-5H-furan-2-one on Gastric Mucosal Lesions Induced by Mast Cell Activation

by Mariano Ezequiel Vera, María Laura Mariani, Cristina Aguilera and Alicia Beatriz Penissi

Int. J. Mol. Sci. 2021, 22(11), 5983; https://doi.org/10.3390/ijms22115983 - 1 Jun 2021

Cited by 6 | Viewed by 2254

Abstract

The aim of this study was to determine whether the lactones dehydroleucodine, xanthatin and 3-benzyloxymethyl-5H-furan-2-one, would be effective in an animal model of gastric ulcer induced by mast cell activation. Rats were divided into ten groups. Treatments were repeated for four days. The degree of gastric erosion was assessed with a scoring system and histological preparations. Gastric mast cell morphology was analyzed by histological procedures. Serum serotonin levels were determined as markers of mast cell activation. Statistical analyses were done using ANOVA and Tukey–Kramer test. We demonstrated that the repeated administration of compound 48/80 results in extensive mucosal lesions in the gastric mucosa and that such lesions occurred in association with mast cell degranulation and a significant increase of serum serotonin. We showed that these lesions were prevented by dehydroleucodine, xanthatin, and 3-benzyloxymethyl-5H-furan-2-one and that this effect was similar to that obtained with sodium cromoglycate. In conclusion, the results of the present study indicate that the optimal gastric cytoprotective dose of dehydroleucodine, xanthatin, and 3-benzyloxymethyl-5H-furan-2-one is efficacious in an animal model of gastric ulcer induced by mast cell activation. Our findings suggest that these lactones could be valuable tools for designing novel therapeutic agents for digestive disorders associated with inappropriate mast cell activation. Full article

(This article belongs to the Special Issue Mast Cells: From Host Defense to Pathology)

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20 pages, 2680 KiB

Open AccessArticle

Mast Cell Proteases Tryptase and Chymase Induce Migratory and Morphological Alterations in Bronchial Epithelial Cells

by Frida Berlin, Sofia Mogren, Julia Tutzauer and Cecilia K. Andersson

Int. J. Mol. Sci. 2021, 22(10), 5250; https://doi.org/10.3390/ijms22105250 - 16 May 2021

Cited by 12 | Viewed by 3819

Abstract

Chronic respiratory diseases are often characterized by impaired epithelial function and remodeling. Mast cells (MCs) are known to home into the epithelium in respiratory diseases, but the MC-epithelial interactions remain less understood. Therefore, this study aimed to investigate the effect of MC proteases on bronchial epithelial morphology and function. Bronchial epithelial cells were stimulated with MC tryptase and/or chymase. Morphology and epithelial function were performed using cell tracking analysis and holographic live-cell imaging. Samples were also analyzed for motility-associated gene expression. Immunocytochemistry was performed to compare cytoskeletal arrangement. Stimulated cells showed strong alterations on gene, protein and functional levels in several parameters important for maintaining epithelial function. The most significant increases were found in cell motility, cellular speed and cell elongation compared to non-stimulated cells. Also, cell morphology was significantly altered in chymase treated compared to non-stimulated cells. In the current study, we show that MC proteases can induce cell migration and morphological and proliferative alterations in epithelial cells. Thus, our data imply that MC release of proteases may play a critical role in airway epithelial remodeling and disruption of epithelial function. Full article

(This article belongs to the Special Issue Mast Cells: From Host Defense to Pathology)

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15 pages, 2465 KiB

Open AccessArticle

Thapsigargin-Stimulated LAD2 Human Mast Cell Line Is a Potent Cellular Adjuvant for the Maturation of Monocyte-Derived Dendritic Cells for Adoptive Cellular Immunotherapy

by Pavla Taborska, Dmitry Stakheev, Jirina Bartunkova and Daniel Smrz

Int. J. Mol. Sci. 2021, 22(8), 3978; https://doi.org/10.3390/ijms22083978 - 12 Apr 2021

Cited by 7 | Viewed by 2538

Abstract

The preparation of dendritic cells (DCs) for adoptive cellular immunotherapy (ACI) requires the maturation of ex vivo-produced immature(i) DCs. This maturation ensures that the antigen presentation triggers an immune response towards the antigen-expressing cells. Although there is a large number of maturation agents capable of inducing strong DC maturation, there is still only a very limited number of these agents approved for use in the production of DCs for ACI. In seeking novel DC maturation agents, we used differentially activated human mast cell (MC) line LAD2 as a cellular adjuvant to elicit or modulate the maturation of ex vivo-produced monocyte-derived iDCs. We found that co-culture of iDCs with differentially activated LAD2 MCs in serum-containing media significantly modulated polyinosinic:polycytidylic acid (poly I:C)-elicited DC maturation as determined through the surface expression of the maturation markers CD80, CD83, CD86, and human leukocyte antigen(HLA)-DR. Once iDCs were generated in serum-free conditions, they became refractory to the maturation with poly I:C, and the LAD2 MC modulatory potential was minimized. However, the maturation-refractory phenotype of the serum-free generated iDCs was largely overcome by co-culture with thapsigargin-stimulated LAD2 MCs. Our data suggest that differentially stimulated mast cells could be novel and highly potent cellular adjuvants for the maturation of DCs for ACI. Full article

(This article belongs to the Special Issue Mast Cells: From Host Defense to Pathology)

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20 pages, 7265 KiB

Open AccessArticle

Type I Interferon α/β Receptor-Mediated Signaling Negatively Regulates Antiviral Cytokine Responses in Murine Bone-Marrow-Derived Mast Cells and Protects the Cells from Virus-Induced Cell Death

by Maedeh Darzianiazizi, Yeganeh Mehrani, Lily Chan, Robert C. Mould, Raveendra R. Kulkarni, Shayan Sharif, Byram W. Bridle and Khalil Karimi

Int. J. Mol. Sci. 2020, 21(23), 9041; https://doi.org/10.3390/ijms21239041 - 27 Nov 2020

Cited by 4 | Viewed by 3268

Abstract

Mast cells (MCs) are critical for initiating inflammatory responses to pathogens including viruses. Type I interferons (IFNs) that exert their antiviral functions by interacting with the type I IFN receptor (IFNAR) play a central role in host cellular responses to viruses. Given that virus-induced excessive toxic inflammatory responses are associated with aberrant IFNAR signaling and considering MCs are an early source of inflammatory cytokines during viral infections, we sought to determine whether IFNAR signaling plays a role in antiviral cytokine responses of MCs. IFNAR-intact, IFNAR-blocked, and IFNAR-knockout (IFNAR^−/−) bone-marrow-derived MCs (BMMCs) were treated in vitro with a recombinant vesicular stomatitis virus (rVSVΔm51) to assess cytokine production by these cells. All groups of MCs produced the cytokines interleukin-6 and tumor necrosis factor-α in response to rVSVΔm51. However, production of the cytokines was lowest in IFNAR-intact cells as compared with IFNAR^−/− or IFNAR-blocked cells at 20 h post-stimulation. Surprisingly, rVSVΔm51 was capable of infecting BMMCs, but functional IFNAR signaling was able to protect these cells from virus-induced death. This study showed that BMMCs produced pro-inflammatory cytokines in response to rVSVΔm51 and that IFNAR signaling was required to down-modulate these responses and protect the cells from dying from viral infection. Full article

(This article belongs to the Special Issue Mast Cells: From Host Defense to Pathology)

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Review

Jump to: Editorial, Research

24 pages, 1733 KiB

Open AccessReview

Mast Cells in the Mammalian Testis and Epididymis—Animal Models and Detection Methods

by Marta Himelreich-Perić, Ana Katušić-Bojanac, Marko Hohšteter, Nino Sinčić, Vedrana Mužić-Radović and Davor Ježek

Int. J. Mol. Sci. 2022, 23(5), 2547; https://doi.org/10.3390/ijms23052547 - 25 Feb 2022

Cited by 5 | Viewed by 4074

Abstract

Mast cells (MCs) are an evolutionary well-conserved type of cells, mediating and modulating allergic responses in innate immunity and tissue remodeling after chronic inflammation. Among other tissues, they inhabit both the testis and epididymis. In the testis, MCs usually appear in the interstitial compartment in humans, but not in other standard experimental models, like rats and mice. MCs seem to be responsible for testicular tissue fibrosis in different causes of infertility. Although experimental animal models follow the effect on MC activation or penetration to the interstitial tissue like in humans to some extent, there is an inconsistency in the available literature regarding experimental design, animal strain, and detection methods used. This comprehensive review offers an insight into the literature on MCs in mammalian testes and epididymides. We aimed to find the most suitable model for research on MC and offer recommendations for future experimental designs. When using in vivo animal models, tunica albuginea incorporation and standard histological assessment need to be included. Domesticated boar strains kept in modified controlled conditions exhibit the highest similarity to the MC distribution in the human testis. 3D testicular models are promising but need further fine-tuning to become a valid model for MC investigation. Full article

(This article belongs to the Special Issue Mast Cells: From Host Defense to Pathology)

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8 pages, 1198 KiB

Open AccessReview

The pLysRS-Ap₄A Pathway in Mast Cells Regulates the Switch from Host Defense to a Pathological State

by Sharmila Govindaraj, Lakshmi Bhargavi Paruchuru and Ehud Razin

Int. J. Mol. Sci. 2021, 22(11), 5620; https://doi.org/10.3390/ijms22115620 - 25 May 2021

Cited by 3 | Viewed by 2723

Abstract

The innate and adaptive immune systems play an essential role in host defense against pathogens. Various signal transduction pathways monitor and balance the immune system since an imbalance may promote pathological states such as allergy, inflammation, and cancer. Mast cells have a central role in the regulation of the innate/adaptive immune system and are involved in the pathogenesis of many inflammatory and allergic diseases by releasing inflammatory mediators such as histamines, proteases, chemotactic factors, and cytokines. Although various signaling pathways are associated with mast cell activation, our discovery and characterization of the pLysRS-Ap₄A signaling pathway in these cells provided an additional important step towards a full understanding of the intracellular mechanisms involved in mast cell activation. In the present review, we will discuss in depth this signaling pathway’s contribution to host defense and the pathological state. Full article

(This article belongs to the Special Issue Mast Cells: From Host Defense to Pathology)

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11 pages, 10046 KiB

Open AccessReview

Adenosine Signaling in Mast Cells and Allergic Diseases

by Lucia Garcia-Garcia, Laia Olle, Margarita Martin, Jordi Roca-Ferrer and Rosa Muñoz-Cano

Int. J. Mol. Sci. 2021, 22(10), 5203; https://doi.org/10.3390/ijms22105203 - 14 May 2021

Cited by 13 | Viewed by 3595

Abstract

Adenosine is a nucleoside involved in the pathogenesis of allergic diseases. Its effects are mediated through its binding to G protein-coupled receptors: A1, A2a, A2b and A3. The receptors differ in the type of G protein they recruit, in the effect on adenylyl cyclase (AC) activity and the downstream signaling pathway triggered. Adenosine can produce both an enhancement and an inhibition of mast cell degranulation, indicating that adenosine effects on these receptors is controversial and remains to be clarified. Depending on the study model, A1, A2b, and A3 receptors have shown anti- or pro-inflammatory activity. However, most studies reported an anti-inflammatory activity of A2a receptor. The precise knowledge of the adenosine mechanism of action may allow to develop more efficient therapies for allergic diseases by using selective agonist and antagonist against specific receptor subtypes. Full article

(This article belongs to the Special Issue Mast Cells: From Host Defense to Pathology)

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17 pages, 1598 KiB

Open AccessReview

Anaphylaxis: Focus on Transcription Factor Activity

by Yanru Guo, Elizabeth Proaño-Pérez, Rosa Muñoz-Cano and Margarita Martin

Int. J. Mol. Sci. 2021, 22(9), 4935; https://doi.org/10.3390/ijms22094935 - 6 May 2021

Cited by 8 | Viewed by 4451

Abstract

Anaphylaxis is a severe allergic reaction, rapid in onset, and can lead to fatal consequences if not promptly treated. The incidence of anaphylaxis has risen at an alarming rate in past decades and continues to rise. Therefore, there is a general interest in understanding the molecular mechanism that leads to an exacerbated response. The main effector cells are mast cells, commonly triggered by stimuli that involve the IgE-dependent or IgE-independent pathway. These signaling pathways converge in the release of proinflammatory mediators, such as histamine, tryptases, prostaglandins, etc., in minutes. The action and cell targets of these proinflammatory mediators are linked to the pathophysiologic consequences observed in this severe allergic reaction. While many molecules are involved in cellular regulation, the expression and regulation of transcription factors involved in the synthesis of proinflammatory mediators and secretory granule homeostasis are of special interest, due to their ability to control gene expression and change phenotype, and they may be key in the severity of the entire reaction. In this review, we will describe our current understanding of the pathophysiology of human anaphylaxis, focusing on the transcription factors’ contributions to this systemic hypersensitivity reaction. Host mutation in transcription factor expression, or deregulation of their activity in an anaphylaxis context, will be updated. So far, the risk of anaphylaxis is unpredictable thus, increasing our knowledge of the molecular mechanism that leads and regulates mast cell activity will enable us to improve our understanding of how anaphylaxis can be prevented or treated. Full article

(This article belongs to the Special Issue Mast Cells: From Host Defense to Pathology)

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12 pages, 874 KiB

Open AccessReview

New Insights into the Pathogenesis of Systemic Mastocytosis

by Zhixiong Li

Int. J. Mol. Sci. 2021, 22(9), 4900; https://doi.org/10.3390/ijms22094900 - 5 May 2021

Cited by 12 | Viewed by 3561

Abstract

Mastocytosis is a type of myeloid neoplasm characterized by the clonal, neoplastic proliferation of morphologically and immunophenotypically abnormal mast cells that infiltrate one or more organ systems. Systemic mastocytosis (SM) is a more aggressive variant of mastocytosis with extracutaneous involvement, which might be associated with multi-organ dysfunction or failure and shortened survival. Over 80% of patients with SM carry the KIT D816V mutation. However, the KIT D816V mutation serves as a weak oncogene and appears to be a late event in the pathogenesis of mastocytosis. The management of SM is highly individualized and was largely palliative for patients without a targeted form of therapy in past decades. Targeted therapy with midostaurin, a multiple kinase inhibitor that inhibits KIT, has demonstrated efficacy in patients with advanced SM. This led to the recent approval of midostaurin by the United States Food and Drug Administration and European Medicines Agency. However, the overall survival of patients treated with midostaurin remains unsatisfactory. The identification of genetic and epigenetic alterations and understanding their interactions and the molecular mechanisms involved in mastocytosis is necessary to develop rationally targeted therapeutic strategies. This review briefly summarizes recent developments in the understanding of SM pathogenesis and potential treatment strategies for patients with SM. Full article

(This article belongs to the Special Issue Mast Cells: From Host Defense to Pathology)

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31 pages, 3706 KiB

Open AccessReview

Mast Cells in the Skin: Defenders of Integrity or Offenders in Inflammation?

by Martin Voss, Johanna Kotrba, Evelyn Gaffal, Konstantinos Katsoulis-Dimitriou and Anne Dudeck

Int. J. Mol. Sci. 2021, 22(9), 4589; https://doi.org/10.3390/ijms22094589 - 27 Apr 2021

Cited by 53 | Viewed by 11396

Abstract

Mast cells (MCs) are best-known as key effector cells of immediate-type allergic reactions that may even culminate in life-threatening anaphylactic shock syndromes. However, strategically positioned at the host–environment interfaces and equipped with a plethora of receptors, MCs also play an important role in the first-line defense against pathogens. Their main characteristic, the huge amount of preformed proinflammatory mediators embedded in secretory granules, allows for a rapid response and initiation of further immune effector cell recruitment. The same mechanism, however, may account for detrimental overshooting responses. MCs are not only detrimental in MC-driven diseases but also responsible for disease exacerbation in other inflammatory disorders. Focusing on the skin as the largest immune organ, we herein review both beneficial and detrimental functions of skin MCs, from skin barrier integrity via host defense mechanisms to MC-driven inflammatory skin disorders. Moreover, we emphasize the importance of IgE-independent pathways of MC activation and their role in sustained chronic skin inflammation and disease exacerbation. Full article

(This article belongs to the Special Issue Mast Cells: From Host Defense to Pathology)

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15 pages, 2253 KiB

Open AccessReview

The Multifaceted Mas-Related G Protein-Coupled Receptor Member X2 in Allergic Diseases and Beyond

by Paola Leonor Quan, Marina Sabaté-Brescó, Yanru Guo, Margarita Martín and Gabriel Gastaminza

Int. J. Mol. Sci. 2021, 22(9), 4421; https://doi.org/10.3390/ijms22094421 - 23 Apr 2021

Cited by 31 | Viewed by 5776

Abstract

Recent research on mast cell biology has turned its focus on MRGPRX2, a new member of the Mas-related G protein-coupled subfamily of receptors (Mrgprs), originally described in nociceptive neurons of the dorsal root ganglia. MRGPRX2, a member of this group, is present not only in neurons but also in mast cells (MCs), specifically, and potentially in other cells of the immune system, such as basophils and eosinophils. As emerging new functions for this receptor are studied, a variety of both natural and pharmacologic ligands are being uncovered, linked to the ability to induce receptor-mediated MC activation and degranulation. The diversity of these ligands, characterized in their human, mice, or rat homologues, seems to match that of the receptor’s interactions. Natural ligands include host defense peptides, basic molecules, and key neuropeptides such as substance P and vasointestinal peptide (known for their role in the transmission of pain and itch) as well as eosinophil granule-derived proteins. Exogenous ligands include MC secretagogues such as compound 48/80 and mastoparan, a component of bee wasp venom, and several peptidergic drugs, among which are members of the quinolone family, neuromuscular blocking agents, morphine, and vancomycin. These discoveries shed light on its capacity as a multifaceted participant in naturally occurring responses within immunity and neural stimulus perception, as in responses at the center of immune pathology. In host defense, the mice Mrgprb2 has been proven to aid mast cells in the detection of peptidic molecules from bacteria and in the release of peptides with antimicrobial activities and other immune mediators. There are several potential actions described for it in tissue homeostasis and repair. In the realm of pathologic response, there is evidence to suggest that this receptor is also involved in chronic inflammation. Furthermore, MRGPRX2 has been linked to the pathophysiology of non-IgE-mediated immediate hypersensitivity drug reactions. Different studies have shown its possible role in other allergic diseases as well, such as asthma, atopic dermatitis, contact dermatitis, and chronic spontaneous urticaria. In this review, we sought to cover its function in physiologic processes and responses, as well as in allergic and nonallergic immune disease. Full article

(This article belongs to the Special Issue Mast Cells: From Host Defense to Pathology)

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