Hidden route of protein damage through oxygen-confined photooxidation

Abstract Oxidative modifications can disrupt protein folds and functions, and are strongly associated with human aging and diseases. Conventional oxidation pathways typically involve the free diffusion of reactive oxygen species (ROS), which primarily attack the protein surface. Yet, it remains uncl...

Full description

Saved in:
Bibliographic Details
Main Authors: Seoyoon Kim, Eojin Kim, Mingyu Park, Seong Ho Kim, Byung-Gyu Kim, Seungjin Na, Victor W. Sadongo, W. C. Bhashini Wijesinghe, Yu-Gon Eom, Gwangsu Yoon, Hannah Jeong, Eunhye Hwang, Chaiheon Lee, Kyungjae Myung, Chae Un Kim, Jeong-Mo Choi, Seung Kyu Min, Tae-Hyuk Kwon, Duyoung Min
Format: Article
Language:English
Published: Nature Portfolio 2024-12-01
Series:Nature Communications
Online Access:https://doi.org/10.1038/s41467-024-55168-z
Tags: Add Tag
No Tags, Be the first to tag this record!
_version_ 1841559294718246912
author Seoyoon Kim
Eojin Kim
Mingyu Park
Seong Ho Kim
Byung-Gyu Kim
Seungjin Na
Victor W. Sadongo
W. C. Bhashini Wijesinghe
Yu-Gon Eom
Gwangsu Yoon
Hannah Jeong
Eunhye Hwang
Chaiheon Lee
Kyungjae Myung
Chae Un Kim
Jeong-Mo Choi
Seung Kyu Min
Tae-Hyuk Kwon
Duyoung Min
author_facet Seoyoon Kim
Eojin Kim
Mingyu Park
Seong Ho Kim
Byung-Gyu Kim
Seungjin Na
Victor W. Sadongo
W. C. Bhashini Wijesinghe
Yu-Gon Eom
Gwangsu Yoon
Hannah Jeong
Eunhye Hwang
Chaiheon Lee
Kyungjae Myung
Chae Un Kim
Jeong-Mo Choi
Seung Kyu Min
Tae-Hyuk Kwon
Duyoung Min
author_sort Seoyoon Kim
collection DOAJ
description Abstract Oxidative modifications can disrupt protein folds and functions, and are strongly associated with human aging and diseases. Conventional oxidation pathways typically involve the free diffusion of reactive oxygen species (ROS), which primarily attack the protein surface. Yet, it remains unclear whether and how internal protein folds capable of trapping oxygen (O2) contribute to oxidative damage. Here, we report a hidden pathway of protein damage, which we refer to as O2-confined photooxidation. In this process, O2 is captured in protein cavities and subsequently converted into multiple ROS, primarily mediated by tryptophan residues under blue light irradiation. The generated ROS then attack the protein interior through constrained diffusion, causing protein damage. The effects of this photooxidative reaction appear to be extensive, impacting a wide range of cellular proteins, as supported by whole-cell proteomic analysis. This photooxidative mechanism may represent a latent oxidation pathway in human tissues directly exposed to visible light, such as skin and eyes.
format Article
id doaj-art-82444e44a71940509a8247999224af02
institution Kabale University
issn 2041-1723
language English
publishDate 2024-12-01
publisher Nature Portfolio
record_format Article
series Nature Communications
spelling doaj-art-82444e44a71940509a8247999224af022025-01-05T12:35:30ZengNature PortfolioNature Communications2041-17232024-12-0115111910.1038/s41467-024-55168-zHidden route of protein damage through oxygen-confined photooxidationSeoyoon Kim0Eojin Kim1Mingyu Park2Seong Ho Kim3Byung-Gyu Kim4Seungjin Na5Victor W. Sadongo6W. C. Bhashini Wijesinghe7Yu-Gon Eom8Gwangsu Yoon9Hannah Jeong10Eunhye Hwang11Chaiheon Lee12Kyungjae Myung13Chae Un Kim14Jeong-Mo Choi15Seung Kyu Min16Tae-Hyuk Kwon17Duyoung Min18Department of Chemistry, Ulsan National Institute of Science and TechnologyDepartment of Chemistry, Ulsan National Institute of Science and TechnologyDepartment of Chemistry, Ulsan National Institute of Science and TechnologyDepartment of Chemistry, Ulsan National Institute of Science and TechnologyCenter for Genomic Integrity, Institute for Basic ScienceDigital Omics Research Center, Korea Basic Science InstituteDepartment of Chemistry, Ulsan National Institute of Science and TechnologyDepartment of Chemistry, Ulsan National Institute of Science and TechnologyDepartment of Chemistry, Pusan National UniversityDepartment of Chemistry, Ulsan National Institute of Science and TechnologyDepartment of Physics, Ulsan National Institute of Science and TechnologyDepartment of Chemistry, Ulsan National Institute of Science and TechnologyDepartment of Chemistry, Ulsan National Institute of Science and TechnologyCenter for Genomic Integrity, Institute for Basic ScienceDepartment of Physics, Ulsan National Institute of Science and TechnologyDepartment of Chemistry, Pusan National UniversityDepartment of Chemistry, Ulsan National Institute of Science and TechnologyDepartment of Chemistry, Ulsan National Institute of Science and TechnologyDepartment of Chemistry, Ulsan National Institute of Science and TechnologyAbstract Oxidative modifications can disrupt protein folds and functions, and are strongly associated with human aging and diseases. Conventional oxidation pathways typically involve the free diffusion of reactive oxygen species (ROS), which primarily attack the protein surface. Yet, it remains unclear whether and how internal protein folds capable of trapping oxygen (O2) contribute to oxidative damage. Here, we report a hidden pathway of protein damage, which we refer to as O2-confined photooxidation. In this process, O2 is captured in protein cavities and subsequently converted into multiple ROS, primarily mediated by tryptophan residues under blue light irradiation. The generated ROS then attack the protein interior through constrained diffusion, causing protein damage. The effects of this photooxidative reaction appear to be extensive, impacting a wide range of cellular proteins, as supported by whole-cell proteomic analysis. This photooxidative mechanism may represent a latent oxidation pathway in human tissues directly exposed to visible light, such as skin and eyes.https://doi.org/10.1038/s41467-024-55168-z
spellingShingle Seoyoon Kim
Eojin Kim
Mingyu Park
Seong Ho Kim
Byung-Gyu Kim
Seungjin Na
Victor W. Sadongo
W. C. Bhashini Wijesinghe
Yu-Gon Eom
Gwangsu Yoon
Hannah Jeong
Eunhye Hwang
Chaiheon Lee
Kyungjae Myung
Chae Un Kim
Jeong-Mo Choi
Seung Kyu Min
Tae-Hyuk Kwon
Duyoung Min
Hidden route of protein damage through oxygen-confined photooxidation
Nature Communications
title Hidden route of protein damage through oxygen-confined photooxidation
title_full Hidden route of protein damage through oxygen-confined photooxidation
title_fullStr Hidden route of protein damage through oxygen-confined photooxidation
title_full_unstemmed Hidden route of protein damage through oxygen-confined photooxidation
title_short Hidden route of protein damage through oxygen-confined photooxidation
title_sort hidden route of protein damage through oxygen confined photooxidation
url https://doi.org/10.1038/s41467-024-55168-z
work_keys_str_mv AT seoyoonkim hiddenrouteofproteindamagethroughoxygenconfinedphotooxidation
AT eojinkim hiddenrouteofproteindamagethroughoxygenconfinedphotooxidation
AT mingyupark hiddenrouteofproteindamagethroughoxygenconfinedphotooxidation
AT seonghokim hiddenrouteofproteindamagethroughoxygenconfinedphotooxidation
AT byunggyukim hiddenrouteofproteindamagethroughoxygenconfinedphotooxidation
AT seungjinna hiddenrouteofproteindamagethroughoxygenconfinedphotooxidation
AT victorwsadongo hiddenrouteofproteindamagethroughoxygenconfinedphotooxidation
AT wcbhashiniwijesinghe hiddenrouteofproteindamagethroughoxygenconfinedphotooxidation
AT yugoneom hiddenrouteofproteindamagethroughoxygenconfinedphotooxidation
AT gwangsuyoon hiddenrouteofproteindamagethroughoxygenconfinedphotooxidation
AT hannahjeong hiddenrouteofproteindamagethroughoxygenconfinedphotooxidation
AT eunhyehwang hiddenrouteofproteindamagethroughoxygenconfinedphotooxidation
AT chaiheonlee hiddenrouteofproteindamagethroughoxygenconfinedphotooxidation
AT kyungjaemyung hiddenrouteofproteindamagethroughoxygenconfinedphotooxidation
AT chaeunkim hiddenrouteofproteindamagethroughoxygenconfinedphotooxidation
AT jeongmochoi hiddenrouteofproteindamagethroughoxygenconfinedphotooxidation
AT seungkyumin hiddenrouteofproteindamagethroughoxygenconfinedphotooxidation
AT taehyukkwon hiddenrouteofproteindamagethroughoxygenconfinedphotooxidation
AT duyoungmin hiddenrouteofproteindamagethroughoxygenconfinedphotooxidation