Acute exposure to ultraviolet radiation targets proteins involved in collagen fibrillogenesis

Introduction: Exposure to chronic, low-dose UV irradiation (UVR) can lead to premature ageing of the skin. Understanding which proteins are affected by acute UVR and photo-dynamically produced reactive oxygen species (ROS) could help to inform strategies to delay photoageing. Conventional biochemica...

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Main Authors: Christopher I. Platt, Callum Stewart-McGuinness, Alexander Eckersley, Loren Wilkins, Michael J. Sherratt
Format: Article
Language:English
Published: Frontiers Media S.A. 2024-03-01
Series:Frontiers in Physiology
Subjects:
Online Access:https://www.frontiersin.org/articles/10.3389/fphys.2024.1352161/full
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author Christopher I. Platt
Callum Stewart-McGuinness
Alexander Eckersley
Loren Wilkins
Michael J. Sherratt
author_facet Christopher I. Platt
Callum Stewart-McGuinness
Alexander Eckersley
Loren Wilkins
Michael J. Sherratt
author_sort Christopher I. Platt
collection DOAJ
description Introduction: Exposure to chronic, low-dose UV irradiation (UVR) can lead to premature ageing of the skin. Understanding which proteins are affected by acute UVR and photo-dynamically produced reactive oxygen species (ROS) could help to inform strategies to delay photoageing. Conventional biochemical analyses can be used to characterize UVR/ROS-induced damage on a protein-by-protein basis and we have previously shown using SDS-PAGE that collagen I and plasma fibronectin are respectively resistant and susceptible to physiological doses of UVR. The aim of this study was to screen a complex proteome for UVR-affected proteins.Methods: This study employed a sensitive mass spectrometry technique (peptide location fingerprinting: PLF) which can identify structure associated differences following trypsin digestion to characterize the impact of UVR exposure on purified collagen I and tissue fibronectin and to identify UVR-susceptible proteins in an ECM-enriched proteome.Results: Using LC/MS-MS and PLF we show that purified mature type-I collagen is resistant to UVR, whereas purified tissue fibronectin is susceptible. UV irradiation of a human dermal fibroblast-deposited ECM-enriched proteome in vitro, followed by LC/MS-MS and PLF analysis revealed two protein cluster groups of UV susceptible proteins involved in i) matrix collagen fibril assembly and ii) protein translation and motor activity. Furthermore, PLF highlighted UV susceptible domains within targeted matrix proteins, suggesting that UV damage of matrix proteins is localized.Discussion: Here we show that PLF can be used to identify protein targets of UVR and that collagen accessory proteins may be key targets in UVR exposed tissues.
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spelling doaj.art-7e2599b059c9427280d3811756f5583b2024-03-15T04:54:52ZengFrontiers Media S.A.Frontiers in Physiology1664-042X2024-03-011510.3389/fphys.2024.13521611352161Acute exposure to ultraviolet radiation targets proteins involved in collagen fibrillogenesisChristopher I. Platt0Callum Stewart-McGuinness1Alexander Eckersley2Loren Wilkins3Michael J. Sherratt4Division of Cell Matrix Biology & Regenerative Medicine, School of Biological Science, Faculty of Biology, Medicine and Health, The University of Manchester, Manchester, United KingdomDivision of Cell Matrix Biology & Regenerative Medicine, School of Biological Science, Faculty of Biology, Medicine and Health, The University of Manchester, Manchester, United KingdomDivision of Musculoskeletal & Dermatological Sciences, School of Biological Sciences, Faculty of Biology, Medicine and Health, The University of Manchester, Manchester, United KingdomSchool of Medical Sciences, The University of Manchester, Manchester, United KingdomDivision of Cell Matrix Biology & Regenerative Medicine, School of Biological Science, Faculty of Biology, Medicine and Health, The University of Manchester, Manchester, United KingdomIntroduction: Exposure to chronic, low-dose UV irradiation (UVR) can lead to premature ageing of the skin. Understanding which proteins are affected by acute UVR and photo-dynamically produced reactive oxygen species (ROS) could help to inform strategies to delay photoageing. Conventional biochemical analyses can be used to characterize UVR/ROS-induced damage on a protein-by-protein basis and we have previously shown using SDS-PAGE that collagen I and plasma fibronectin are respectively resistant and susceptible to physiological doses of UVR. The aim of this study was to screen a complex proteome for UVR-affected proteins.Methods: This study employed a sensitive mass spectrometry technique (peptide location fingerprinting: PLF) which can identify structure associated differences following trypsin digestion to characterize the impact of UVR exposure on purified collagen I and tissue fibronectin and to identify UVR-susceptible proteins in an ECM-enriched proteome.Results: Using LC/MS-MS and PLF we show that purified mature type-I collagen is resistant to UVR, whereas purified tissue fibronectin is susceptible. UV irradiation of a human dermal fibroblast-deposited ECM-enriched proteome in vitro, followed by LC/MS-MS and PLF analysis revealed two protein cluster groups of UV susceptible proteins involved in i) matrix collagen fibril assembly and ii) protein translation and motor activity. Furthermore, PLF highlighted UV susceptible domains within targeted matrix proteins, suggesting that UV damage of matrix proteins is localized.Discussion: Here we show that PLF can be used to identify protein targets of UVR and that collagen accessory proteins may be key targets in UVR exposed tissues.https://www.frontiersin.org/articles/10.3389/fphys.2024.1352161/fullskinextracellular matrixultravioletcollagen fibrillogenesismass spectrometrypost-translational modification
spellingShingle Christopher I. Platt
Callum Stewart-McGuinness
Alexander Eckersley
Loren Wilkins
Michael J. Sherratt
Acute exposure to ultraviolet radiation targets proteins involved in collagen fibrillogenesis
Frontiers in Physiology
skin
extracellular matrix
ultraviolet
collagen fibrillogenesis
mass spectrometry
post-translational modification
title Acute exposure to ultraviolet radiation targets proteins involved in collagen fibrillogenesis
title_full Acute exposure to ultraviolet radiation targets proteins involved in collagen fibrillogenesis
title_fullStr Acute exposure to ultraviolet radiation targets proteins involved in collagen fibrillogenesis
title_full_unstemmed Acute exposure to ultraviolet radiation targets proteins involved in collagen fibrillogenesis
title_short Acute exposure to ultraviolet radiation targets proteins involved in collagen fibrillogenesis
title_sort acute exposure to ultraviolet radiation targets proteins involved in collagen fibrillogenesis
topic skin
extracellular matrix
ultraviolet
collagen fibrillogenesis
mass spectrometry
post-translational modification
url https://www.frontiersin.org/articles/10.3389/fphys.2024.1352161/full
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AT alexandereckersley acuteexposuretoultravioletradiationtargetsproteinsinvolvedincollagenfibrillogenesis
AT lorenwilkins acuteexposuretoultravioletradiationtargetsproteinsinvolvedincollagenfibrillogenesis
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