Convergent evolution of monocyte differentiation in adult skin instructs Langerhans cell identity

IF 17.6 1区 医学 Q1 IMMUNOLOGY
Anna Appios, James Davies, Sofia Sirvent, Stephen Henderson, Sébastien Trzebanski, Johannes Schroth, Morven L. Law, Inês Boal Carvalho, Marlene Magalhaes Pinto, Cyril Carvalho, Howard Yuan-Hao Kan, Shreya Lovlekar, Christina Major, Andres Vallejo, Nigel J. Hall, Michael Ardern-Jones, Zhaoyuan Liu, Florent Ginhoux, Sian M. Henson, Rebecca Gentek, Elaine Emmerson, Steffen Jung, Marta E. Polak, Clare L. Bennett
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Abstract

Langerhans cells (LCs) are distinct among phagocytes, functioning both as embryo-derived, tissue-resident macrophages in skin innervation and repair and as migrating professional antigen-presenting cells, a function classically assigned to dendritic cells (DCs). Here, we demonstrate that both intrinsic and extrinsic factors imprint this dual identity. Using ablation of embryo-derived LCs in the murine adult skin and tracking differentiation of incoming monocyte-derived replacements, we found intrinsic intraepidermal heterogeneity. We observed that ontogenically distinct monocytes give rise to LCs. Within the epidermis, Jagged-dependent activation of Notch signaling, likely within the hair follicle niche, provided an initial site of LC commitment before metabolic adaptation and survival of monocyte-derived LCs. In the human skin, embryo-derived LCs in newborns retained transcriptional evidence of their macrophage origin, but this was superseded by DC-like immune modules after postnatal expansion. Thus, adaptation to adult skin niches replicates conditioning of LC at birth, permitting repair of the embryo-derived LC network.
成人皮肤中单核细胞分化的趋同进化指示朗格汉斯细胞的特性。
朗格汉斯细胞(Langerhans cells,LCs)在吞噬细胞中是与众不同的,它既能作为胚胎衍生的组织驻留巨噬细胞在皮肤神经支配和修复中发挥作用,又能作为迁移的专业抗原递呈细胞发挥作用,而这一功能通常是由树突状细胞(DCs)承担的。在这里,我们证明了内在和外在因素对这种双重身份的影响。通过在小鼠成年皮肤中消融胚胎衍生的 LCs 并跟踪单核细胞衍生的替代细胞的分化,我们发现了表皮内的内在异质性。我们观察到,本体上不同的单核细胞会产生 LCs。在表皮内,Jagged 依赖性激活的 Notch 信号(可能在毛囊龛内)在单核细胞衍生的 LCs 代谢适应和存活之前提供了 LC 承诺的初始位置。在人类皮肤中,新生儿胚胎衍生的 LC 保留了其巨噬细胞来源的转录证据,但在出生后扩增后被类似 DC 的免疫模块所取代。因此,对成人皮肤龛位的适应复制了出生时 LC 的调节,允许修复胚胎衍生的 LC 网络。
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来源期刊
Science Immunology
Science Immunology Immunology and Microbiology-Immunology
CiteScore
32.90
自引率
2.00%
发文量
183
期刊介绍: Science Immunology is a peer-reviewed journal that publishes original research articles in the field of immunology. The journal encourages the submission of research findings from all areas of immunology, including studies on innate and adaptive immunity, immune cell development and differentiation, immunogenomics, systems immunology, structural immunology, antigen presentation, immunometabolism, and mucosal immunology. Additionally, the journal covers research on immune contributions to health and disease, such as host defense, inflammation, cancer immunology, autoimmunity, allergy, transplantation, and immunodeficiency. Science Immunology maintains the same high-quality standard as other journals in the Science family and aims to facilitate understanding of the immune system by showcasing innovative advances in immunology research from all organisms and model systems, including humans.
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