Andrijana Nešić

Lidija Burazer

Rajna Minić

Sabine Flicker

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TYPE EditorialPUBLISHED 12 August 2024| DOI 10.3389/falgy.2024.1466954EDITED AND REVIEWED BYNikolaos (Nikos) G. Papadopoulos,National and Kapodistrian University of Athens,Greece*CORRESPONDENCERajna Minićrminic@torlak.rsRECEIVED 18 July 2024ACCEPTED 23 July 2024PUBLISHED 12 August 2024CITATIONMinić R, Burazer L, Nešić A and Flicker S (2024)Editorial: Allergen source-specific mucosalbarrier disruptors.Front. Allergy 5:1466954.doi: 10.3389/falgy.2024.1466954COPYRIGHT© 2024 Minić, Burazer, Nešić and Flicker. Thisis an open-access article distributed under theterms of the Creative Commons AttributionLicense (CC BY). The use, distribution orreproduction in other forums is permitted,provided the original author(s) and thecopyright owner(s) are credited and that theoriginal publication in this journal is cited, inaccordance with accepted academic practice.No use, distribution or reproduction ispermitted which does not comply withthese terms.Frontiers in AllergyEditorial: Allergen source-specificmucosal barrier disruptorsRajna Minić1*, Lidija Burazer1, Andrijana Nešić2 and Sabine Flicker31Institute of Virology, Vaccines and Sera “Torlak”, Belgrade, Serbia, 2Department of Biochemistry, Facultyof Chemistry, University of Belgrade, Belgrade, Serbia, 3Institute of Pathophysiology and AllergyResearch, Center for Pathophysiology, Infectiology and Immunology, Medical University of Vienna,Vienna, AustriaKEYWORDSmucosal barrier, barrier hypothesis, mucosal barrier disruptors, functional dyspepsia,epithelial–mesenchymal transition, deoxynivalenolEditorial on the Research TopicAllergen source-specific mucosal barrier disruptorsThe rise of allergic diseases has concerned medical doctors and scientists for years, andseveral hypotheses on the causation have been presented. The “hygiene hypothesis” (1)was the first theory to explain the increase in the prevalence of allergies, stating that thelack of diverse microbial stimulation contributes to the growing incidence of allergicdisorders. Yet, of greater significance to this topic is the “barrier hypothesis,” coined byPothoven and Schleimer (2) in 2017, and the “extended epithelial barrier hypothesis”presented by Cezmi Akdiş in 2021 (3). Akdiş lecture, during the ECI 2021 congressraised concern among participants about the future trend. Namely, the “extendedepithelial barrier hypothesis” states that the massive introduction of surface-activemolecules abundant in hygiene products, detergents, and cleaners can damage theepithelial barrier, leading to allergen penetration. However, this loss of barrier integritynot only triggers allergic sensitization but also affects the clinical course of autoimmuneand neuropsychiatric diseases.The translation of this hypothesis to the mechanisms of “classical” allergenicity impliesthat natural mucosal barrier disruptors are also present in conventional allergen sources,causing similar injury to the epithelial barrier. Among these allergenic sources, allergenswith proteolytic activity are considered the most notorious (4). However, there islimited research on the involvement of lipids and other hydrophobic molecules inpollen sensitization (5, 6).This Special Research Topic offers a comprehensive picture of the current researchfocusing on allergen source-specific mucosal barrier disruptors and beyond.The five articles published within this Special Research Topic are quite diversecovering the subject from different points of view. The review by Parron-Ballesteroset al. offered a carefully prepared global view of the epithelial barrier-damagingexposomes impairing the airways and the intestinal compartment. Special focus wasgiven on the microbiota composition, its role as producers of short-chain fatty acids,powerful anti-inflammatory agents, and the gut–lung axis, a hot topic influencing theclinical outcome not only of allergic diseases.Raith and Swoboda presented an exquisitely written review focused on birch pollenand birch pollen allergy. Current knowledge about internal and external influencesimpacting the allergenicity of birch pollen and its interactions with the epithelial barrier01 frontiersin.orgMinić et al. 10.3389/falgy.2024.1466954shows that there are still several challenges that need to beaddressed. Furthermore, this contribution raises the awarenessthat the recombinant Bet v 1 alone might not be the bestsurrogate when studying the influence of birch pollen on theintegrity of airway epithelial cells. The authors conclude that acombination of different approaches is required, such as cellculture models and patient studies, to uncover the molecularpathology and hopefully bring more effective treatments andprevention measures.Epidermal barrier dysfunction is also an important aspect ofatopic dermatitis pathogenesis, yet disease management iscurrently limited to topical corticosteroids to alleviate symptoms.Further insights into the pathogenesis are needed to reveal noveltreatment options. One innovative approach to support tissuerepair is the application of epithelial cells that can transform intoa migratory mesenchymal phenotype, in a process known as theepithelial–mesenchymal transition (EMT). Although EMT hasbeen highlighted as a possible mechanism for the remodelingprocess in asthma, the literature investigating atopic dermatitisand EMT is scarce. In their actual review article, Anderson et al.focused on this knowledge gap and identified the induction ofthe EMT pathway as a promising therapeutical target for atopicdermatitis and the inhibition of the same pathway in thetreatment of asthma.Moreover, a dysregulated epithelial barrier plays an importantrole in functional dyspepsia, a gastrointestinal disorder. Within thistopic, Hari et al. conducted a broad PubMed search for theirnarrative review to finally present a hypothesis on theinvolvement of hypoxia-inducible factors (HIFs) in functionaldyspepsia. What is especially interesting about this condition isthat it occurs with high frequency ranging from 7.2% (7) to 16%(8) and that 34% of functional dyspepsia patients suffer from apsychiatric condition (9), highlighting the strength of the gut–brain interaction, but what is even more interesting is thatalthough sounding pretty straightforward, the pathogenesis onthe molecular level is still elusive.As a highlight of this topic, Drønen et al. provided theiroriginal research which, through a series of well-planned andexecuted experiments, pinpointed the known mucosal barrierdisruptor deoxynivalenol (DON), a trichothecene mycotoxinproduced by common cereal crops fungal contaminants (10), asan adjuvant in a peanut allergy model. DON also has a moreprominent effect in comparison to the cholera toxin (CT), aknown activator of adenylate cyclase-cAMP system (11) onearly allergy markers such as IL-33 and thymic stromallymphopoietin (TSLP) levels in the intestines and ST2 levels inserum, showing that different kinds of mucosal barrierdisruptors, such as DON and CT, exert different activities at theearly stages of peanut sensitization.Frontiers in Allergy 02The results from this study clearly show that the increase inepithelial barrier-damaging agents linked to industrialization andmodern lifestyle contribute to the rise in allergic disorders.The collection of data within this Special Research Topicdemonstrates that maintenance and restoration of the epithelialbarrier integrity is a crucial factor affecting various underlyingpathways in allergic, autoimmune, and other chronic conditions.Gaining a deeper understanding of the consequences ofharmful environmental factors on the disruption of the epithelialbarrier will hopefully sensitize policymakers and individualsto prioritize less toxic alternatives to stop the progress ofinflammatory disorders.Author contributionsRM: Conceptualization, Writing – original draft, Writing –review & editing. LB: Writing – review & editing. AN: Writing –review & editing. SF: Conceptualization, Writing – original draft,Writing – review & editing.FundingThe author(s) declare financial support was received for theresearch, authorship, and/or publication of this article.Ministry of Science, Technological Development, andInnovations of The Republic of Serbia, Grant No. 200177 (ContractNo. 451-03-66/2024-03/200177) and Austria Science Fund (FWF)grant I3946-B33.Conflict of interestThe authors declare that the research was conducted in theabsence of any commercial or financial relationships that couldbe construed as potential conflict of interest.The authors declared that they were an editorial board memberof Frontiers, at the time of submission. This had no impact on thepeer review process and the final decision.Publisher’s noteAll claims expressed in this article are solely those of theauthors and do not necessarily represent those of their affiliatedorganizations, or those of the publisher, the editors and thereviewers. Any product that may be evaluated in this article, orclaim that may be made by its manufacturer, is not guaranteedor endorsed by the publisher.References1. Strachan DP. Hay fever, hygiene, and household size. BMJ (Clinical Research ed).(1989) 299(6710):1259–60. doi: 10.1136/bmj.299.6710.12592. Pothoven KL, Schleimer RP. The barrier hypothesis and oncostatin M: restorationof epithelial barrier function as a novel therapeutic strategy for the treatment of type 2frontiersin.orgMinić et al. 10.3389/falgy.2024.1466954inflammatory disease. Tissue Barriers. (2017) 5(3):e1341367. doi: 10.1080/21688370.2017.13413673. Akdis CA. Does the epithelial barrier hypothesis explain the increase in allergy,autoimmunity and other chronic conditions? Nat Rev Immunol. (2021) 21(11):739–51. doi: 10.1038/s41577-021-00538-74. Baglivo I, Quaranta NV, Dragonieri S, Colantuono S, Menzella F, Selvaggio D,et al. The new paradigm: the role of proteins and triggers in the evolution ofallergic asthma. Int. J Mol Sci. (2024) 25:5747. doi: 10.3390/ijms251157475. Bashir ME, Lui JH, Palnivelu R, Naclerio RM, Preuss D. Pollen lipidomics: lipidprofiling exposes a notable diversity in 22 allergenic pollen and potential biomarkersof the allergic immune response. PLoS One. (2013) 8(2):e57566. doi: 10.1371/journal.pone.00575666. Guryanova SV, Finkina EI, Melnikova DN, Bogdanov IV, Bohle B, OvchinnikovaTV. How do pollen allergens sensitize? Front Mol Biosci. (2022) 9:900533. doi: 10.3389/fmolb.2022.90053Frontiers in Allergy 037. Sperber AD, Bangdiwala SI, Drossman DA, Ghoshal UC, Simren M, Tack J, et al.Worldwide prevalence and burden of functional gastrointestinal disorders, results ofRome Foundation Global Study. Gastroenterology. (2021) 160(1):99–114.e3. doi: 10.1053/j.gastro.2020.04.0148. Ford AC, Mahadeva S, Carbone MF, Lacy BE, Talley NJ. Functional dyspepsia.Lancet (London England). (2020) 396(10263):1689–702. doi: 10.1016/S0140-6736(20)30469-49. Haug TT, Svebak S, Wilhelmsen I, Berstad A, Ursin H. Psychological factorsand somatic symptoms in functional dyspepsia. a comparison with duodenal ulcerand healthy controls. J Psychosomatic Res. (1994) 38:281–91. doi: 10.1016/0022-3999(94)90033-710. Bianchini A, Bullerman LB. Mycotoxins: classification. In: Batt CA, TortorelloML, editors. Encyclopedia of Food Microbiology. 2nd edn. Volume 2. Oxford:Academic Press (2014). p. 854–61. doi: 10.1016/B978-0-12-384730-0.00230-511. Ganguly NK, Kaur T. Mechanism of action of cholera toxin & other toxins.Indian J Med Res. (1996) 104:28–37.frontiersin.org

Editorial: Allergen source-specific mucosal barrier disruptors

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Editorial: Allergen source-specific mucosal barrier disruptors

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