Nrf2 deficiency causes lipid oxidation, inflammation, and matrix-protease expression in DHA-supplemented and UVA-irradiated skin fibroblasts
Abstract
Fish oil rich in docosahexaenoic acid (DHA) has beneficial effects on human health. Omega-3 polyunsaturated fatty acids are precursors of eicosanoids and docosanoids, signaling molecules that control inflammation and immunity, and their dietary uptake improves a range of disorders including cardiovascular diseases, ulcerative colitis, rheumatoid arthritis, and psoriasis. The unsaturated nature of these fatty acids, however, makes them prone to oxidation, especially when they are incorporated into (membrane) phospholipids. The skin is an organ strongly exposed to oxidative stress, mainly due to solar ultraviolet radiation. Thus, increased levels of PUFA in combination with oxidative stress could cause increased local generation of oxidized lipids, whose action spectrum reaches from signaling molecules to reactive carbonyl compounds that can crosslink biomolecules. Here, we investigated whether PUFA supplements to fibroblasts are incorporated into membrane phospholipids and whether an increase of PUFA within phospholipids affects the responses of the cells to UV exposure. The redox-sensitive transcription factor Nrf2 is the major regulator of the fibroblast stress response to ultraviolet radiation or exposure to oxidized lipids. Here we addressed how Nrf2 signaling would be affected in PUFA-supplemented human dermal fibroblasts and mouse dermal fibroblasts from Nrf2-deficient and wild type mice. We found, using HPLC-tandem MS, that DHA supplements to culture media of human and murine fibroblasts were readily incorporated into phospholipids and that subsequent irradiation of the supplemented cells with UVA resulted in an increase in 1-palmitoyl-2-(epoxyisoprostane-E2)-sn-glycero-3-phosphorylcholine and Oxo-DHA esterified to phospholipid, both of which are Nrf2 agonists. Also, induction of Nrf2 target genes was enhanced in the DHA-supplemented fibroblasts after UVA irradiation. In Nrf2-deficient murine fibroblasts, the expression of the target genes was, as expected, decreased, but surprisingly, expression of TNFα and MMP13 was strongly induced in DHA-supplemented, UVA-irradiated cells. Also, Nrf2-deficient cells had increased levels of oxidized phospholipids relative to the unoxidized precursors after UVA irradiation. Our data suggest that under ultraviolet stress a functioning Nrf2 system is required to prevent DHA-induced inflammation and matrix degradation in dermal fibroblasts.
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Nrf2 deficiency or Nrf2-knockdown causes lipid oxidation, inflammation, and ECM-protease expression (e.g., MMPs, Cox) in UVA-irradiated skin fibroblasts or heat shock-induced human dermal fibroblasts.
“For example, Nrf2 deficiency or Nrf2-knockdown is known to cause lipid oxidation, inflammation, and extracellular matrix-protease expression (e.g., MMPs, cyclo-oxygenases (Cox) in UVA-irradiated skin fibroblasts or heat shock-induced human dermal fibroblasts [74,75].”
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- Authors
- Gruber, F., Ornelas, C. M., Karner, S., Narzt, M.-S., Nagelreiter, I. M., Gschwandtner, M., Bochkov, V., & Tschachler, E.
- Affiliations
- Medical University of Vienna (AT)
- ORCID
- Venue
- Free Radical Biology and Medicine
- Publisher
- Elsevier BV
- Published
- 2015-11
- Volume
- 88
- Issue
- Pt B
- Pages
- 439-451
- ISSN
- 0891-5849 (ISSN-L)
- OpenAlex
- W287343231
- Cited by
- 44
- References
- 84
- Citations by year
- 2026: 1 · 2025: 4 · 2024: 4 · 2023: 6 · 2022: 7 · 2021: 2 · 2020: 3 · 2019: 7 · 2018: 3 · 2017: 2 · 2016: 5
- FWCI
- 1.45
- Type
- journal article
- Language
- en
- Open access
- closed
- Locations
- Free Radical Biology and Medicine (publishedVersion)
- PubMed (publishedVersion)
- Funders
- Federal Ministry of Science, Research and Economy
- the National Foundation for Research, Technology, and Development
- Topics
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Genomics, phytochemicals, and oxidative stress
- Health Sciences › Medicine › Dermatology › Skin Protection and Aging
- Health Sciences › Nursing › Nutrition and Dietetics › Fatty Acid Research and Health
- Keywords
- docosahexaenoic acid, omega-3 polyunsaturated fatty acids, UVA irradiation, dermal fibroblasts, lipid peroxidation, oxidized phospholipids, Nrf2 target genes, TNF-α, MMP-13, matrix metalloproteinases, inflammation, oxidative stress, fish oil supplementation
- MeSH terms
- Animals, Chromatography, High Pressure Liquid, Docosahexaenoic Acids, Fibroblasts, Humans, Immunoenzyme Techniques, Inflammation, Skin, Ultraviolet Rays, Blotting, Western, Lipid Peroxidation, Reverse Transcriptase Polymerase Chain Reaction, NF-E2-Related Factor 2, Mice, Tandem Mass Spectrometry
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