Adipose tissue protects against skin photodamage through CD151- and AdipoQ- EVs

Abstract To clarify the protective effects of subcutaneous adipose tissue (SAT) against photodamage, we utilized nude mouse skin with or without SAT. Skin and fibroblasts were treated with adipose tissue-derived extracellular vesicles (AT-EVs) or extracellular vesicles derived from adipose-derived s...

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Main Authors: Yan-Wen Wang, Poh-Ching Tan, Qing-Feng Li, Xue-Wen Xu, Shuang-Bai Zhou
Format: Article
Language:English
Published: BMC 2024-12-01
Series:Cell Communication and Signaling
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Online Access:https://doi.org/10.1186/s12964-024-01978-z
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author Yan-Wen Wang
Poh-Ching Tan
Qing-Feng Li
Xue-Wen Xu
Shuang-Bai Zhou
author_facet Yan-Wen Wang
Poh-Ching Tan
Qing-Feng Li
Xue-Wen Xu
Shuang-Bai Zhou
author_sort Yan-Wen Wang
collection DOAJ
description Abstract To clarify the protective effects of subcutaneous adipose tissue (SAT) against photodamage, we utilized nude mouse skin with or without SAT. Skin and fibroblasts were treated with adipose tissue-derived extracellular vesicles (AT-EVs) or extracellular vesicles derived from adipose-derived stem cells (ADSC-EVs) to demonstrate that SAT protects the overlying skin from photodamage primarily through AT-EVs. Surprisingly, AT-EVs stimulated fibroblast proliferation more rapidly than ADSC-EVs did. The yield of AT-EVs from the same volume of AT was 200 times greater than that of ADSC-EVs. To compare the differences between AT-EVs and ADSC-EVs, we used a proximity barcoding assay (PBA) to analyze the surface proteins on individual particles of these two types of EVs. PBA analysis revealed that AT-EVs contain diverse subpopulations, with 83.42% expressing CD151, compared to only 1.98% of ADSC-EVs. Furthermore, AT-EVs are internalized more rapidly by cells than ADSC-EVs, as our study demonstrated that CD151-positive AT-EVs were endocytosed more quickly than their CD151-negative counterparts. Additionally, adiponectin in AT-EVs activated the AMPK pathway and inhibited the NF-κB pathway, enhancing fibroblast protection against photodamage. The significantly higher yield and faster acquisition of AT-EVs compared to ADSC-EVs underscore their potential for broader applications. Graphical Abstract AT mitigates skin photoaging via AT-EVs, which consist of 14 subpopulations and express more CD151 and APN on their surface, as determined by PBA sequencing. CD151 facilitates faster cellular recognition and uptake of AT-EVs. APN activates AdipoR to stimulate the AMPK pathway and inhibit the NF-κB pathway, reducing ROS and DNA damage in fibroblasts. This results in improved skin histology, increased collagen production, a reduction in senescent cells, and decreased ROS accumulation. (Created with BioRender.com)
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institution Kabale University
issn 1478-811X
language English
publishDate 2024-12-01
publisher BMC
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series Cell Communication and Signaling
spelling doaj-art-02c9050aee454b99bb421d2e595d34ae2024-12-22T12:37:40ZengBMCCell Communication and Signaling1478-811X2024-12-0122111410.1186/s12964-024-01978-zAdipose tissue protects against skin photodamage through CD151- and AdipoQ- EVsYan-Wen Wang0Poh-Ching Tan1Qing-Feng Li2Xue-Wen Xu3Shuang-Bai Zhou4Department of Plastic & Reconstructive Surgery, Ninth People’s Hospital, Shanghai Jiao Tong University School of MedicineDepartment of Plastic & Reconstructive Surgery, Ninth People’s Hospital, Shanghai Jiao Tong University School of MedicineDepartment of Plastic & Reconstructive Surgery, Ninth People’s Hospital, Shanghai Jiao Tong University School of MedicineDepartment of Plastic and Burn Surgery, West China Hospital, Sichuan UniversityDepartment of Plastic & Reconstructive Surgery, Ninth People’s Hospital, Shanghai Jiao Tong University School of MedicineAbstract To clarify the protective effects of subcutaneous adipose tissue (SAT) against photodamage, we utilized nude mouse skin with or without SAT. Skin and fibroblasts were treated with adipose tissue-derived extracellular vesicles (AT-EVs) or extracellular vesicles derived from adipose-derived stem cells (ADSC-EVs) to demonstrate that SAT protects the overlying skin from photodamage primarily through AT-EVs. Surprisingly, AT-EVs stimulated fibroblast proliferation more rapidly than ADSC-EVs did. The yield of AT-EVs from the same volume of AT was 200 times greater than that of ADSC-EVs. To compare the differences between AT-EVs and ADSC-EVs, we used a proximity barcoding assay (PBA) to analyze the surface proteins on individual particles of these two types of EVs. PBA analysis revealed that AT-EVs contain diverse subpopulations, with 83.42% expressing CD151, compared to only 1.98% of ADSC-EVs. Furthermore, AT-EVs are internalized more rapidly by cells than ADSC-EVs, as our study demonstrated that CD151-positive AT-EVs were endocytosed more quickly than their CD151-negative counterparts. Additionally, adiponectin in AT-EVs activated the AMPK pathway and inhibited the NF-κB pathway, enhancing fibroblast protection against photodamage. The significantly higher yield and faster acquisition of AT-EVs compared to ADSC-EVs underscore their potential for broader applications. Graphical Abstract AT mitigates skin photoaging via AT-EVs, which consist of 14 subpopulations and express more CD151 and APN on their surface, as determined by PBA sequencing. CD151 facilitates faster cellular recognition and uptake of AT-EVs. APN activates AdipoR to stimulate the AMPK pathway and inhibit the NF-κB pathway, reducing ROS and DNA damage in fibroblasts. This results in improved skin histology, increased collagen production, a reduction in senescent cells, and decreased ROS accumulation. (Created with BioRender.com)https://doi.org/10.1186/s12964-024-01978-zAdipose tissueAdipose tissue-derived extracellular vesiclesUVBSkin photoagingCD151Endocytosis
spellingShingle Yan-Wen Wang
Poh-Ching Tan
Qing-Feng Li
Xue-Wen Xu
Shuang-Bai Zhou
Adipose tissue protects against skin photodamage through CD151- and AdipoQ- EVs
Cell Communication and Signaling
Adipose tissue
Adipose tissue-derived extracellular vesicles
UVB
Skin photoaging
CD151
Endocytosis
title Adipose tissue protects against skin photodamage through CD151- and AdipoQ- EVs
title_full Adipose tissue protects against skin photodamage through CD151- and AdipoQ- EVs
title_fullStr Adipose tissue protects against skin photodamage through CD151- and AdipoQ- EVs
title_full_unstemmed Adipose tissue protects against skin photodamage through CD151- and AdipoQ- EVs
title_short Adipose tissue protects against skin photodamage through CD151- and AdipoQ- EVs
title_sort adipose tissue protects against skin photodamage through cd151 and adipoq evs
topic Adipose tissue
Adipose tissue-derived extracellular vesicles
UVB
Skin photoaging
CD151
Endocytosis
url https://doi.org/10.1186/s12964-024-01978-z
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AT qingfengli adiposetissueprotectsagainstskinphotodamagethroughcd151andadipoqevs
AT xuewenxu adiposetissueprotectsagainstskinphotodamagethroughcd151andadipoqevs
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