Oxidative stress-mediated NFκB phosphorylation upregulates p62/SQSTM1 and promotes retinal pigmented epithelial cell survival through increased autophagy
Open accessAbstract
p62 is a scaffolding adaptor implicated in the clearance of protein aggregates by autophagy. Reactive oxygen species (ROS) can either stimulate or inhibit NFκB-mediated gene expression influencing cellular fate. We studied the effect of hydrogen peroxide (H2O2)-mediated oxidative stress and NFκB signaling on p62 expression in the retinal pigment epithelium (RPE) and investigated its role in regulation of autophagy and RPE survival against oxidative damage. Cultured human RPE cell line ARPE-19 and primary human adult and fetal RPE cells were exposed to H2O2-induced oxidative stress. The human apolipoprotein E4 targeted-replacement (APOE4) mouse model of AMD was used to study expression of p62 and other autophagy proteins in the retina. p62, NFκB p65 (total, phosphorylated, nuclear and cytoplasmic) and ATG10 expression was assessed by mRNA and protein analyses. Cellular ROS and mitochondrial superoxide were measured by CM-H2DCFDA and MitoSOX staining respectively. Mitochondrial viability was determined using MTT activity. qPCR-array system was used to investigate autophagic genes affected by p62. Nuclear and cytoplasmic levels of NFκB p65 were evaluated after cellular fractionation by Western blotting. We report that p62 is up-regulated in RPE cells under H2O2-induced oxidative stress and promotes autophagic activity. Depletion of endogenous p62 reduces autophagy by downregulation of ATG10 rendering RPE more susceptible to oxidative damage. NFκB p65 phosphorylation at Ser-536 was found to be critical for p62 upregulation in response to oxidative stress. Proteasome inhibition by H2O2 causes p62-NFκB signaling as antioxidant pre-treatment reversed p62 expression and p65 phosphorylation when RPE was challenged by H2O2 but not when by Lactacystin. p62 protein but not RNA levels are elevated in APOE4-HFC AMD mouse model, suggesting reduction of autophagic flux in disease conditions. Our findings suggest that p62 is necessary for RPE cytoprotection under oxidative stress and functions, in part, by modulating ATG10 expression. NFκB p65 activity may be a critical upstream initiator of p62 expression in RPE cells under oxidative stress.
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The cytoprotective role of autophagy under stress and increased p62 likely favors pexophagy and mitophagy.
“thus the cytoprotective role of autophagy under stress and increased p62 likely favors these two LC3-dependent functions (Mitter et al., 2012; Wang et al., 2014; Song et al., 2017).”
From Microtubule-associated protein 1 light chain 3B, (LC3B) is necessary to maintain lipid-mediated homeostasis in the retinal pigment epithelium (2018) · cites this paper as Song et al., 2017
Pexophagy and mitophagy both utilize the LC3 adapter p62.
“Pexophagy and mitophagy both utilize the LC3 adapter p62”
From Microtubule-associated protein 1 light chain 3B, (LC3B) is necessary to maintain lipid-mediated homeostasis in the retinal pigment epithelium (2018) · cites this paper as Song et al., 2017
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Self-citation
- Authors
- Song, C., Mitter, S. K., Qi, X., Beli, E., Rao, H. V., Ding, J., Ip, C. S., Gu, H., Akin, D., Dunn, W. A., Bowes Rickman, C., Lewin, A. S., Grant, M. B., & Boulton, M. E.
- Affiliations
- University of Florida (US)
- Indiana University Indianapolis (US)
- Duke University (US)
- Corresponding author
- Boulton, Michael E.
- ORCID
- Venue
- PLoS ONE
- Publisher
- Public Library of Science (PLoS)
- Published
- 2017-02-21
- Volume
- 12
- Issue
- 2
- Pages
- e0171940
- ISSN
- 1932-6203 (ISSN-L)
- PMC
- PMC5319799
- OpenAlex
- W2591403620
- Cited by
- 100
- References
- 56
- Citations by year
- 2026: 4 · 2025: 8 · 2024: 6 · 2023: 10 · 2022: 9 · 2021: 16 · 2020: 14 · 2019: 12 · 2018: 12 · 2017: 9
- FWCI
- 12.53
- Type
- journal article
- Language
- en
- Open access
- gold
- doi.org
- Licence
- Locations
- PLoS ONE (publishedVersion, cc-by)
- PubMed Central (publishedVersion, cc-by)
- PubMed (publishedVersion)
- IUScholarWorks (Indiana University) (submittedVersion, cc-by-nc-nd)
- DOAJ (DOAJ: Directory of Open Access Journals) (submittedVersion, cc-by-sa)
- Purdue University Indianapolis (Indiana University) (submittedVersion, cc-by-nc-nd)
- PMC
- Funders
- National Eye Institute (EY019688, EY021626, EY020825, EY021721, EY019038, EY005722)
- Edward N. and Della L. Thome Memorial Foundation
- Research to Prevent Blindness (Unrestricted Grant)
- Topics
- Health Sciences › Medicine › Ophthalmology › Retinal Diseases and Treatments
- Health Sciences › Medicine › Epidemiology › Autophagy in Disease and Therapy
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Retinal Development and Disorders
- Keywords
- p62, p65 phosphorylation, oxidative stress, hydrogen peroxide, retinal pigment epithelium, autophagy, ATG10, reactive oxygen species, mitochondrial superoxide, age-related macular degeneration, APOE ε4, protein aggregation, cell survival, cytoprotection, autophagic flux, proteasome
- MeSH terms
- Sequestosome-1 Protein, Animals, Autophagy, Cell Line, Cell Survival, Disease Models, Animal, Fluorescent Antibody Technique, Macular Degeneration, Phosphorylation, Superoxides, Blotting, Western, Up-Regulation, NF-kappa B, RNA-Binding Proteins, Reactive Oxygen Species, Oxidative Stress, Mice, Retinal Pigment Epithelium, Real-Time Polymerase Chain Reaction
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