Tension as a key factor in skin responses to pollution

Abstract Being the more apparent organ exposed to the outdoor stressors, the effect of pollution on the skin has been widely studied in the last few decades. Although UV light is known as the most aggressive stressor to which our cutaneous tissue is daily exposed, other components of the tropospheri...

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Main Authors: Erika Pambianchi, Zachary Hagenberg, Alessandra Pecorelli, Arianna Pasqui, Jean-Philippe Therrien, Giuseppe Valacchi
Format: Article
Language:English
Published: Nature Portfolio 2023-09-01
Series:Scientific Reports
Online Access:https://doi.org/10.1038/s41598-023-42629-6
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author Erika Pambianchi
Zachary Hagenberg
Alessandra Pecorelli
Arianna Pasqui
Jean-Philippe Therrien
Giuseppe Valacchi
author_facet Erika Pambianchi
Zachary Hagenberg
Alessandra Pecorelli
Arianna Pasqui
Jean-Philippe Therrien
Giuseppe Valacchi
author_sort Erika Pambianchi
collection DOAJ
description Abstract Being the more apparent organ exposed to the outdoor stressors, the effect of pollution on the skin has been widely studied in the last few decades. Although UV light is known as the most aggressive stressor to which our cutaneous tissue is daily exposed, other components of the tropospheric pollution have also shown to affect skin health and functionality. Among them, ozone has been proven to be one of the most toxic due to its high reactivity with the epidermal lipids. Studying the cutaneous effect of pollution in a laboratory setting presents challenges, therefore it becomes critical to employ appropriate and tailored models that aim to answer specific questions. Several skin models are available nowadays: in vitro models (2D cell lines and 3D cutaneous tissues), ex vivo skin explants and in vivo approaches (animals and humans). Although in the last 20 years researchers developed skin models that closely resemble human skin (3D cutaneous tissues), ex vivo skin explants still remain one of the best models to study cutaneous responses. Unfortunately, one important cutaneous property that is not present in the traditional ex vivo human skin explants is the physiological tension, which has been shown to be a cardinal player in skin structure, homeostasis, functional properties and responses to external stimuli. For this reason, in this study, to confirm and further comprehend the harmful mechanism of ozone exposure on the integumentary system, we have performed experiments using the state of art in cutaneous models: the innovative TenSkin™ model in which ex vivo human skin explants are cultured under physiologically relevant tension during the whole experimental procedure. Specifically, we were interested in corroborating previous findings showing that ozone exposure modulates the expression of cutaneous antimicrobial peptides (AMPs). The present work demonstrates that cutaneous exposure to ozone induces AMPs gene and protein levels (CAMP/LL-37, hBD2, hBD3) and that the presence of tension can further modulate their expression. In addition, different responses between tension and non-tension cultured skin were also observed during the evaluation of OxInflammatory markers [cyclooxygenase-2 (COX2), aryl hydrocarbon receptor (AhR), matrix-metallo-proteinase 9 (MMP9) and 4-hydroxy-nonenal (4HNE)]. This current study supports our previous findings confirming the ability of pollution to induce the cutaneous expression of AMPs via redox signaling and corroborates the principle that skin explants are a good and reliable model to study skin responses even though it underlines the need to holistically consider the role of skin tension before extrapolating the data to real life.
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spelling doaj.art-101b0d8331984d9facc58cd84c9e47642023-11-26T13:20:26ZengNature PortfolioScientific Reports2045-23222023-09-0113111310.1038/s41598-023-42629-6Tension as a key factor in skin responses to pollutionErika Pambianchi0Zachary Hagenberg1Alessandra Pecorelli2Arianna Pasqui3Jean-Philippe Therrien4Giuseppe Valacchi5Department of Animal Science, Plants for Human Health Institute, North Carolina State UniversityDepartment of Animal Science, Plants for Human Health Institute, North Carolina State UniversityDepartment of Animal Science, Plants for Human Health Institute, North Carolina State UniversityDepartment of Biotechnologies, Chemistry and Pharmacy, University of SienaDepartment of Food, Bioprocessing and Nutrition Sciences, Plants for Human Health Institute, North Carolina State UniversityDepartment of Animal Science, Plants for Human Health Institute, North Carolina State UniversityAbstract Being the more apparent organ exposed to the outdoor stressors, the effect of pollution on the skin has been widely studied in the last few decades. Although UV light is known as the most aggressive stressor to which our cutaneous tissue is daily exposed, other components of the tropospheric pollution have also shown to affect skin health and functionality. Among them, ozone has been proven to be one of the most toxic due to its high reactivity with the epidermal lipids. Studying the cutaneous effect of pollution in a laboratory setting presents challenges, therefore it becomes critical to employ appropriate and tailored models that aim to answer specific questions. Several skin models are available nowadays: in vitro models (2D cell lines and 3D cutaneous tissues), ex vivo skin explants and in vivo approaches (animals and humans). Although in the last 20 years researchers developed skin models that closely resemble human skin (3D cutaneous tissues), ex vivo skin explants still remain one of the best models to study cutaneous responses. Unfortunately, one important cutaneous property that is not present in the traditional ex vivo human skin explants is the physiological tension, which has been shown to be a cardinal player in skin structure, homeostasis, functional properties and responses to external stimuli. For this reason, in this study, to confirm and further comprehend the harmful mechanism of ozone exposure on the integumentary system, we have performed experiments using the state of art in cutaneous models: the innovative TenSkin™ model in which ex vivo human skin explants are cultured under physiologically relevant tension during the whole experimental procedure. Specifically, we were interested in corroborating previous findings showing that ozone exposure modulates the expression of cutaneous antimicrobial peptides (AMPs). The present work demonstrates that cutaneous exposure to ozone induces AMPs gene and protein levels (CAMP/LL-37, hBD2, hBD3) and that the presence of tension can further modulate their expression. In addition, different responses between tension and non-tension cultured skin were also observed during the evaluation of OxInflammatory markers [cyclooxygenase-2 (COX2), aryl hydrocarbon receptor (AhR), matrix-metallo-proteinase 9 (MMP9) and 4-hydroxy-nonenal (4HNE)]. This current study supports our previous findings confirming the ability of pollution to induce the cutaneous expression of AMPs via redox signaling and corroborates the principle that skin explants are a good and reliable model to study skin responses even though it underlines the need to holistically consider the role of skin tension before extrapolating the data to real life.https://doi.org/10.1038/s41598-023-42629-6
spellingShingle Erika Pambianchi
Zachary Hagenberg
Alessandra Pecorelli
Arianna Pasqui
Jean-Philippe Therrien
Giuseppe Valacchi
Tension as a key factor in skin responses to pollution
Scientific Reports
title Tension as a key factor in skin responses to pollution
title_full Tension as a key factor in skin responses to pollution
title_fullStr Tension as a key factor in skin responses to pollution
title_full_unstemmed Tension as a key factor in skin responses to pollution
title_short Tension as a key factor in skin responses to pollution
title_sort tension as a key factor in skin responses to pollution
url https://doi.org/10.1038/s41598-023-42629-6
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AT ariannapasqui tensionasakeyfactorinskinresponsestopollution
AT jeanphilippetherrien tensionasakeyfactorinskinresponsestopollution
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