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      Topical bismuth oxide-manganese composite nanospheres alleviate atopic dermatitis-like inflammation

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          Abstract

          Atopic dermatitis (AD) is a common skin disease involving important immune mechanisms. There is an unmet need for a treatment for this condition. Herein, we focused on elucidating the role of Bi 2-xMn xO 3 nanospheres (BM) in alleviating skin inflammation in AD-like C57BL/6 mice. The BM was fabricated via sacrificial templates and its biosafety was systematically evaluated. The BM was applied topically to skin lesions of AD-like C57BL/6 mice. The phenotypic and histological changes in the skin were examined carefully. The responses of barrier proteins, inflammatory cytokines and cells to BM were evaluated in HaCaT cells and AD mouse models. The data demonstrated that BM treatment alleviated the AD phenotypes and decreased the level of inflammatory factors, while increasing the expression of the barrier proteins filaggrin/involucrin in the skin. BM effectively reduced the expression of phosphorylated STAT6, which in turn reduced the expression of GATA3, and further decreased the differentiation ratio of Th2 cells, thereby reducing the expression of IL-4. In conclusion, topical drug therapy with BM provides a safe and effective treatment modality for AD by reducing IL-4 and increasing barrier proteins.

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          Supplementary Information

          The online version contains supplementary material available at 10.1186/s12951-023-02207-4.

          Highlights

          This study was the first to explore the feasibility of Bi 2-xMnxO 3 nanospheres (BM) in agar gel as STAT phosphorylation regulators to improve the clinical manifestations in MC903-induced atopic dermatitis (AD)—like C57BL/6 mice, and to evaluate their immunomodulatory effects in vitro and in vivo. BM showed good skin penetration and system safety. BM reduced the expression of IL-4, IL-13 and p-STAT6 in TNF-α/IFN-γ-induced HaCaT inflammatory cells and in the MC903-induced mouse AD model, thereby effectively improving the expression of the barrier protein FLG/IVL and promoting the recovery of damaged skin. Moreover, the ratio of Th2 cells in the skin and spleen was considerably decreased after BM administration in MC903-induced AD mice, indicating that the as-prepared BM inhibits the Th2 cells response in the AD mouse model. BM has the potential to be an innovative therapeutic strategy for AD.

          Supplementary Information

          The online version contains supplementary material available at 10.1186/s12951-023-02207-4.

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          Most cited references49

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          Atopic dermatitis

          Stephan Weidinger, Kenji Kabashima, Alan D. Irvine … (2018)
          Atopic dermatitis (AD) is the most common chronic inflammatory skin disease, with a lifetime prevalence of up to 20% and substantial effects on quality of life. AD is characterized by intense itch, recurrent eczematous lesions and a fluctuating course. AD has a strong heritability component and is closely related to and commonly co-occurs with other atopic diseases (such as asthma and allergic rhinitis). Several pathophysiological mechanisms contribute to AD aetiology and clinical manifestations. Impairment of epidermal barrier function, for example, owing to deficiency in the structural protein filaggrin, can promote inflammation and T cell infiltration. The immune response in AD is skewed towards T helper 2 cell-mediated pathways and can in turn favour epidermal barrier disruption. Other contributing factors to AD onset include dysbiosis of the skin microbiota (in particular overgrowth of Staphylococcus aureus), systemic immune responses (including immunoglobulin E (IgE)-mediated sensitization) and neuroinflammation, which is involved in itch. Current treatments for AD include topical moisturizers and anti-inflammatory agents (such as corticosteroids, calcineurin inhibitors and cAMP-specific 3',5'-cyclic phosphodiesterase 4 (PDE4) inhibitors), phototherapy and systemic immunosuppressants. Translational research has fostered the development of targeted small molecules and biologic therapies, especially for moderate-to-severe disease.
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            Atopic dermatitis.

            Sinead Langan, Alan D. Irvine, Stephan Weidinger (2020)
            Atopic dermatitis is a common inflammatory skin disorder characterised by recurrent eczematous lesions and intense itch. The disorder affects people of all ages and ethnicities, has a substantial psychosocial impact on patients and relatives, and is the leading cause of the global burden from skin disease. Atopic dermatitis is associated with increased risk of multiple comorbidities, including food allergy, asthma, allergic rhinitis, and mental health disorders. The pathophysiology is complex and involves a strong genetic predisposition, epidermal dysfunction, and T-cell driven inflammation. Although type-2 mechanisms are dominant, there is increasing evidence that the disorder involves multiple immune pathways. Currently, there is no cure, but increasing numbers of innovative and targeted therapies hold promise for achieving disease control, including in patients with recalcitrant disease. We summarise and discuss advances in our understanding of the disease and their implications for prevention, management, and future research.
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              Atopic Dermatitis: Global Epidemiology and Risk Factors

              Sophie Nutten (2015)
              Atopic dermatitis (AD) is a chronic inflammatory skin disease posing a significant burden on health-care resources and patients' quality of life. It is a complex disease with a wide spectrum of clinical presentations and combinations of symptoms. AD affects up to 20% of children and up to 3% of adults; recent data show that its prevalence is still increasing, especially in low-income countries. First manifestations of AD usually appear early in life and often precede other allergic diseases such as asthma or allergic rhinitis. Individuals affected by AD usually have genetically determined risk factors affecting the skin barrier function or the immune system. However, genetic mutations alone might not be enough to cause clinical manifestations of AD, and it is merely the interaction of a dysfunctional epidermal barrier in genetically predisposed individuals with harmful effects of environmental agents which leads to the development of the disease. AD has been described as an allergic skin disease, but today, the contribution of allergic reactions to the initiation of AD is challenged, and it is proposed that allergy is rather a consequence of AD in subjects with a concomitant underlying atopic constitution. Treatment at best achieves symptom control rather than cure; there is thus a strong need to identify alternatives for disease prevention.
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                Author and article information

                Contributors
                Haisheng Qian: shqian@ahmu.edu.cn
                Fengli Xiao: xiaofengli@126.com
                Journal
                Journal ID (nlm-ta): J Nanobiotechnology
                Journal ID (iso-abbrev): J Nanobiotechnology
                Title: Journal of Nanobiotechnology
                Publisher: BioMed Central (London )
                ISSN (Electronic): 1477-3155
                Publication date (Electronic): 16 November 2023
                Publication date PMC-release: 16 November 2023
                Publication date Collection: 2023
                Volume: 21
                Electronic Location Identifier: 430
                Affiliations
                [1 ]Department of Dermatology of First Affiliated Hospital, and Institute of Dermatology, Anhui Medical University, ( https://ror.org/03xb04968) Hefei, 230032 Anhui China
                [2 ]Key Laboratory of Dermatology, Anhui Medical University, Ministry of Education, ( https://ror.org/03xb04968) Hefei, Anhui China
                [3 ]The Center for Scientific Research of Anhui Medical University, ( https://ror.org/03xb04968) Hefei, Anhui China
                [4 ]School of Biomedical Engineering, Research and Engineering Center of Biomedical Materials, Anhui Provincial Institute of Translational Medicine, Anhui Medical University, ( https://ror.org/03xb04968) Hefei, 230032 Anhui China
                [5 ]GRID grid.186775.a, ISNI 0000 0000 9490 772X, Inflammation and Immune Mediated Diseases Laboratory of Anhui Province, ; Hefei, China
                Article
                Publisher ID: 2207
                DOI: 10.1186/s12951-023-02207-4
                PMC ID: 10655471
                PubMed ID: 37974268
                SO-VID: 2fd08f99-bfe9-4706-89fe-f0846712ca0a
                Copyright © © The Author(s) 2023
                License:

                Open Access This article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons licence, and indicate if changes were made. The images or other third party material in this article are included in the article's Creative Commons licence, unless indicated otherwise in a credit line to the material. If material is not included in the article's Creative Commons licence and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this licence, visit http://creativecommons.org/licenses/by/4.0/. The Creative Commons Public Domain Dedication waiver ( http://creativecommons.org/publicdomain/zero/1.0/) applies to the data made available in this article, unless otherwise stated in a credit line to the data.

                History
                Date received : 19 September 2023
                Date accepted : 8 November 2023
                Funding
                Funded by: Anhui Provincial Institute of Translational Medicine
                Award ID: 2021zhyx-B15
                Award Recipient :
                Funded by: FundRef http://dx.doi.org/10.13039/501100001809, National Natural Science Foundation of China;
                Award ID: 81972926
                Award Recipient :
                Categories
                Subject: Research
                Custom metadata
                issue-copyright-statement © BioMed Central Ltd., part of Springer Nature 2023

                ScienceOpen disciplines: Biotechnology
                Keywords: atopic dermatitis,skin inflammation,il-4,stat6,bi2-xmnxo3 nanospheres
                Data availability:
                ScienceOpen disciplines: Biotechnology
                Keywords: atopic dermatitis, skin inflammation, il-4, stat6, bi2-xmnxo3 nanospheres

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