Astaxanthin protects against environmentally persistent free radical-induced oxidative stress in well-differentiated respiratory epithelium

Environmentally persistent free radicals (EPFRs) are combustion products present in substantial numbers on atmospheric particulate matter with half-lives of days to years. The mechanisms linking EPFR exposure and respiratory diseases are unclear, but likely involve oxidative stress. We investigated...

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Main Authors: Ayaho Yamamoto, Peter D. Sly, Lavrent Khachatryan, Nelufa Begum, Abrey J. Yeo, Paul D. Robinson, Stephania A. Cormier, Emmanuelle Fantino
Format: Article
Language:English
Published: Elsevier 2025-04-01
Series:Redox Biology
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Online Access:http://www.sciencedirect.com/science/article/pii/S2213231725000552
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author Ayaho Yamamoto
Peter D. Sly
Lavrent Khachatryan
Nelufa Begum
Abrey J. Yeo
Paul D. Robinson
Stephania A. Cormier
Emmanuelle Fantino
author_facet Ayaho Yamamoto
Peter D. Sly
Lavrent Khachatryan
Nelufa Begum
Abrey J. Yeo
Paul D. Robinson
Stephania A. Cormier
Emmanuelle Fantino
author_sort Ayaho Yamamoto
collection DOAJ
description Environmentally persistent free radicals (EPFRs) are combustion products present in substantial numbers on atmospheric particulate matter with half-lives of days to years. The mechanisms linking EPFR exposure and respiratory diseases are unclear, but likely involve oxidative stress. We investigated the mechanisms by which EPFR exposure impact on well-differentiated primary human nasal epithelial cells from subjects sensitive or resistant to oxidant stressors, cultured at an air-liquid interface. We found that EPFR exposure induced mitochondrial reactive oxygen species (mtROS) production; increased mitochondrial DNA copy number; down-regulated mucus production gene, Mucin-5AC (MUC5AC); up-regulated detoxifying gene, cytochrome P450 1A1 (CYP1A1), nuclear factor erythroid 2-related factor 2 (NRF2)-regulated antioxidant pathways including Sirtuin 1 (SIRT1)-Forkhead box O3 (FOXO3), mitophagy, PTEN-induced kinase 1 (PINK1), apoptosis, cyclin-dependent kinase inhibitor p21 (p21), and inflammation, C–C motif chemokine ligand 5 (CCL5). These results indicate that the well-differentiated respiratory epithelium can respond and activate redox reactions when exposed to sublethal concentrations of EPFRs. Increased susceptibility to EPFR exposure is conferred by failure to upregulate the mucin gene, MUC5AC, expression. Pre-treatment with astaxanthin prevented most of the negative impacts caused by EPFRs. Our results demonstrate that EPFRs can induce oxidative stress and cause damage to respiratory epithelium. A dietary antioxidant, astaxanthin, protected cells from EPFR-induced oxidant stress.
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spelling doaj-art-7bc184090f224a7eb69a9dc992f8c2502025-08-20T03:02:29ZengElsevierRedox Biology2213-23172025-04-018110354210.1016/j.redox.2025.103542Astaxanthin protects against environmentally persistent free radical-induced oxidative stress in well-differentiated respiratory epitheliumAyaho Yamamoto0Peter D. Sly1Lavrent Khachatryan2Nelufa Begum3Abrey J. Yeo4Paul D. Robinson5Stephania A. Cormier6Emmanuelle Fantino7Child Health Research Centre, The University of Queensland, South Brisbane, Queensland, 4101, Australia; Corresponding author. Centre for Children's Health Research, 62 Graham Street, South Brisbane, Queensland, 4101, Australia.Child Health Research Centre, The University of Queensland, South Brisbane, Queensland, 4101, AustraliaDepartment of Chemistry, Louisiana State University, Baton Rouge, LA, 70803, United StatesChild Health Research Centre, The University of Queensland, South Brisbane, Queensland, 4101, AustraliaChild Health Research Centre, The University of Queensland, South Brisbane, Queensland, 4101, Australia; Centre for Clinical Research, The University of Queensland, Herston, Queensland, 4006, AustraliaChild Health Research Centre, The University of Queensland, South Brisbane, Queensland, 4101, AustraliaDepartment of Biological Sciences, and Pennington Biomedical Research Center, Louisiana State University, Baton Rouge, LA, 70803, United StatesChild Health Research Centre, The University of Queensland, South Brisbane, Queensland, 4101, AustraliaEnvironmentally persistent free radicals (EPFRs) are combustion products present in substantial numbers on atmospheric particulate matter with half-lives of days to years. The mechanisms linking EPFR exposure and respiratory diseases are unclear, but likely involve oxidative stress. We investigated the mechanisms by which EPFR exposure impact on well-differentiated primary human nasal epithelial cells from subjects sensitive or resistant to oxidant stressors, cultured at an air-liquid interface. We found that EPFR exposure induced mitochondrial reactive oxygen species (mtROS) production; increased mitochondrial DNA copy number; down-regulated mucus production gene, Mucin-5AC (MUC5AC); up-regulated detoxifying gene, cytochrome P450 1A1 (CYP1A1), nuclear factor erythroid 2-related factor 2 (NRF2)-regulated antioxidant pathways including Sirtuin 1 (SIRT1)-Forkhead box O3 (FOXO3), mitophagy, PTEN-induced kinase 1 (PINK1), apoptosis, cyclin-dependent kinase inhibitor p21 (p21), and inflammation, C–C motif chemokine ligand 5 (CCL5). These results indicate that the well-differentiated respiratory epithelium can respond and activate redox reactions when exposed to sublethal concentrations of EPFRs. Increased susceptibility to EPFR exposure is conferred by failure to upregulate the mucin gene, MUC5AC, expression. Pre-treatment with astaxanthin prevented most of the negative impacts caused by EPFRs. Our results demonstrate that EPFRs can induce oxidative stress and cause damage to respiratory epithelium. A dietary antioxidant, astaxanthin, protected cells from EPFR-induced oxidant stress.http://www.sciencedirect.com/science/article/pii/S2213231725000552Air-liquid interface cultureAir pollutionAntioxidantMitochondriaMitochondrial reactive oxygen speciesMucus
spellingShingle Ayaho Yamamoto
Peter D. Sly
Lavrent Khachatryan
Nelufa Begum
Abrey J. Yeo
Paul D. Robinson
Stephania A. Cormier
Emmanuelle Fantino
Astaxanthin protects against environmentally persistent free radical-induced oxidative stress in well-differentiated respiratory epithelium
Redox Biology
Air-liquid interface culture
Air pollution
Antioxidant
Mitochondria
Mitochondrial reactive oxygen species
Mucus
title Astaxanthin protects against environmentally persistent free radical-induced oxidative stress in well-differentiated respiratory epithelium
title_full Astaxanthin protects against environmentally persistent free radical-induced oxidative stress in well-differentiated respiratory epithelium
title_fullStr Astaxanthin protects against environmentally persistent free radical-induced oxidative stress in well-differentiated respiratory epithelium
title_full_unstemmed Astaxanthin protects against environmentally persistent free radical-induced oxidative stress in well-differentiated respiratory epithelium
title_short Astaxanthin protects against environmentally persistent free radical-induced oxidative stress in well-differentiated respiratory epithelium
title_sort astaxanthin protects against environmentally persistent free radical induced oxidative stress in well differentiated respiratory epithelium
topic Air-liquid interface culture
Air pollution
Antioxidant
Mitochondria
Mitochondrial reactive oxygen species
Mucus
url http://www.sciencedirect.com/science/article/pii/S2213231725000552
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