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The Influence of Microbiome Dysbiosis and Bacterial Biofilms On International Journal of Molecular Sciences Review The Influence of Microbiome Dysbiosis and Bacterial Biofilms on Epidermal Barrier Function in Atopic Dermatitis—An Update Leszek Blicharz 1,*, Lidia Rudnicka 1, Joanna Czuwara 1, Anna Wa´skiel-Burnat 1, Mohamad Goldust 2 , Małgorzata Olszewska 1 and Zbigniew Samochocki 1 1 Department of Dermatology, Medical University of Warsaw, 02-008 Warsaw, Poland; [email protected] (L.R.); [email protected] (J.C.); [email protected] (A.W.-B.); [email protected] (M.O.); [email protected] (Z.S.) 2 Department of Dermatology, University Medical Center of the Johannes Gutenberg University, 55131 Mainz, Germany; [email protected] * Correspondence: [email protected] Abstract: Atopic dermatitis (AD) is a common inflammatory dermatosis affecting up to 30% of children and 10% of adults worldwide. AD is primarily driven by an epidermal barrier defect which triggers immune dysregulation within the skin. According to recent research such phenomena are closely related to the microbial dysbiosis of the skin. There is growing evidence that cutaneous microbiota and bacterial biofilms negatively affect skin barrier function, contributing to the onset and exacerbation of AD. This review summarizes the latest data on the mechanisms leading to microbiome dysbiosis and biofilm formation in AD, and the influence of these phenomena on skin barrier function. Citation: Blicharz, L.; Rudnicka, L.; Keywords: atopic dermatitis; biofilms; microbiome; staphylococci; skin barrier Czuwara, J.; Wa´skiel-Burnat,A.; Goldust, M.; Olszewska, M.; Samochocki, Z. The Influence of Microbiome Dysbiosis and Bacterial Biofilms on Epidermal Barrier 1. Introduction Function in Atopic Dermatitis—An Atopic dermatitis (AD) is a chronic inflammatory skin disorder characterized by Update. Int. J. Mol. Sci. 2021, 22, 8403. a highly heterogenous clinical picture [1,2]. No specific tests ensure the diagnosis of AD. https://doi.org/10.3390/ijms22168403 Therefore, it is based on clinical criteria (i.e., UK Working Party criteria and the Hanifin and Rajka criteria applicable to the pediatric and adult populations, respectively) [3,4]. The Academic Editor: Kyung-Min Lim essential features of AD include the presence of eczematous lesions, itch, and a chronic or relapsing disease course [2,5]. The distribution and morphology of skin lesions reveals age- Received: 21 July 2021 dependent variations. Children under 2 years of age typically present with poorly defined, Accepted: 2 August 2021 exudative erythematous lesions located on the trunk, face, and cheeks. The majority Published: 5 August 2021 of pediatric patients >2 years of age exhibit a more localized eczema affecting flexor surfaces and the lichenification of chronic lesions. As regards adults, AD most commonly Publisher’s Note: MDPI stays neutral manifests as chronic hand eczema, flexural dermatitis, and/or head and neck dermatitis. with regard to jurisdictional claims in A recently published paper describing the prevalence of AD in adults revealed that the published maps and institutional affil- classic adult type, with lichenified/exudative flexural dermatitis frequently associated iations. with head and neck eczema or hand eczema was the most common AD phenotype [6]. Furthermore, the predominant manifestations of adult-onset AD included nummular eczema-like and prurigo-like phenotypes, whereas childhood-onset AD was more often characterized by lichenified/exudative flexural dermatitis alone and/or in association with Copyright: © 2021 by the authors. portrait dermatitis. Licensee MDPI, Basel, Switzerland. The lack of causative treatment, significant psychosocial impact, and high prevalence This article is an open access article reaching 10% of adults and 30% of children make AD a considerable challenge for public distributed under the terms and health worldwide [7,8]. conditions of the Creative Commons The current view on AD pathogenesis encompasses the following factors [2,9,10]: Attribution (CC BY) license (https:// creativecommons.org/licenses/by/ 1. An epidermal barrier defect; 4.0/). 2. Immune dysregulation; Int. J. Mol. Sci. 2021, 22, 8403. https://doi.org/10.3390/ijms22168403 https://www.mdpi.com/journal/ijms Int. J. Mol. Sci. 2021, 22, x FOR PEER REVIEW 2 of 20 Int. J. Mol. Sci. 2021, 22, 8403 2 of 19 1. An epidermal barrier defect; 2. Immune dysregulation; 3. Skin microbial dysbiosis; 3. Skin microbial dysbiosis; 4. The itch/scratch cycle. 4. The itch/scratch cycle. These pathogenic events are strictly related and trigger the occurrence and exacerba- These pathogenic events are strictly related and trigger the occurrence and exacer- tions of AD, making it a model disease for the study of interactions between the skin bar- bations of AD, making it a model disease for the study of interactions between the skin rier and cutaneous microbiome (Figure 1). barrier and cutaneous microbiome (Figure1). FigureFigure 1. AA graphical graphical representation representation of of the the interactions interactions between between the the epidermal epidermal barrier, barrier, microbiota, microbiota, andand the immune the immune sys- system.tem. In Inhealthy healthy individuals, individuals, the the epider epidermismis constitutes constitutes a abarrier barrier preventing preventing the the uncontrolled uncontrolled proliferation proliferation of potentially harmfulharmful microorganisms.microorganisms. AA diversediverse array array of of microbes microbes participates participates in in the the crosstalk crosstal withk with the the immune immune system system and and ensures ensures its maturationits maturation to maintain to maintain immune immune balance balance within within the skin. the skin In AD,. In theAD, epidermal the epidermal barrier barrier defect defect and dysregulation and dysregulation of innate of andinnate acquired and acquired immunity immunity result in theresult enhanced in the adhesionenhanced and adhesion proliferation and proliferation of some bacterial of some species, bacterial especially species, staphylococci. especially staphylococci. Microbial dysbiosis subsequently aggravates the skin defect by degrading the components of the epidermal Microbial dysbiosis subsequently aggravates the skin defect by degrading the components of the epidermal barrier and barrier and potentiating Th2-skewing. potentiating Th2-skewing. Literature data suggest that an epidermal barrierbarrier defectdefect isis thethe primaryprimary factorfactor drivingdriving AD symptoms [[11,12].11,12]. Individuals withwith ADAD exhibitexhibit highlyhighly variablevariable congenitalcongenital abnormali-abnormal- tiesities that that translate translate intointo epidermalepidermal barrierbarrier impairment.impairment. TheThe mostmost frequentfrequent polymorphismspolymorphisms affect thethe expressionexpression ofof filaggrin, filaggrin, tight tight junctions, junctions, epidermal epidermal lipids, lipids, and and endothelial endothelial protease prote- activityase activity [13 –[13–18].18]. The The epidermal epidermal barrier barrier may ma alsoy also be be secondarily secondarily damaged damaged by by epigeneticepigenetic changes and environmental factorsfactors [[2,13,19].2,13,19]. Recent research in the fieldfield of the microbiome hashas highlighted thethe crucialcrucial rolerole ofof skinskin microbes in preserving preserving the the intact intact skin skin barri barrierer [20,21]. [20,21 ].Commensal Commensal microorganisms microorganisms are arein- involvedvolved in inconstant constant crosstalk crosstalk with with the the keratinocytes keratinocytes and and the theimmune immune system, system, mediate mediate the theformation formation of tight of tight junctions, junctions, maintain maintain immune immune homeostasis, homeostasis, and and“teach” “teach” the host the host to rec- to recognizeognize and and combat combat pathogens pathogens capable capable of causing of causing a potential a potential skin skininfection. infection. Furthermore, Further- more,the physiological the physiological microbiome microbiome constitutes constitutes an additional an additional physiological physiological barrier barrier against against path- pathogenicogenic microbes microbes by competing by competing for the for niches the niches favoring favoring their their growth growth [22]. [ 22]. Microbes may function in a sessile form, but in most cases they form complex multi- species communities communities within within the the biofilms biofilms [23]. [23 ].A growing A growing body body of evidence of evidence points points to bac- to bacterialterial biofilms biofilms as the as primary the primary pathogenic pathogenic factor factor in a number in a number of dermatological of dermatological conditions, con- ditions,e.g., in acne e.g., vulgaris in acne vulgaris[24] and [chronic24] and wounds chronic wounds[25]. The [ 25importance]. The importance of bacterial of bacterialbiofilms biofilmsfor the skin for barrier the skin in barrier AD has in also AD hasbeen also recently been recentlysuggested. suggested. The aim of this narrative review is to summarize the recent insights into the interac- tions between cutaneouscutaneous microbes,microbes, theirtheir biofilms,biofilms, andand skinskin barrierbarrier functionfunction inin AD.AD. 2. Materials and Methods The literature search was performed with the use of the following databases: PubMed, Scopus and Web of Science. The keywords used to perform the search were “atopic dermatitis”, “biofilm”, “microbiome”, “S. aureus”, “epidermal
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