Nox4- and Nox2-dependent oxidant production is required for VEGF-induced SERCA cysteine-674 S-glutathiolation and endothelial cell migration
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Endothelial cell (EC) migration in response to vascular endothelial growth factor (VEGF) is a critical step in both physiological and pathological angiogenesis. Although VEGF signaling has been extensively studied, the mechanisms by which VEGF-dependent reactive oxygen species (ROS) production affects EC signaling are not well understood. The aim of this study was to elucidate the involvement of Nox2- and Nox4-dependent ROS in VEGF-mediated EC Ca(2+) regulation and migration. VEGF induced migration of human aortic ECs into a scratch wound over 6 h, which was inhibited by overexpression of either catalase or superoxide dismutase (SOD). EC stimulation by micromolar concentrations of H2O2 was inhibited by catalase, but also unexpectedly by SOD. Both VEGF and H2O2 increased S-glutathiolation of SERCA2b and increased Ca(2+) influx into EC, and these events could be blocked by overexpression of catalase or overexpression of SERCA2b in which the reactive cysteine-674 was mutated to a serine. In determining the source of VEGF-mediated ROS production, our studies show that specific knockdown of either Nox2 or Nox4 inhibited VEGF-induced S-glutathiolation of SERCA, Ca(2+) influx, and EC migration. Treatment with H2O2 induced S-glutathiolation of SERCA and EC Ca(2+) influx, overcoming the knockdown of Nox4, but not Nox2, and Amplex red measurements indicated that Nox4 is the source of H2O2. These results demonstrate that VEGF stimulates EC migration through increased S-glutathiolation of SERCA and Ca(2+) influx in a Nox4- and H2O2-dependent manner, requiring Nox2 downstream.
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NOX4-derived ROS can induce the reversible glutathionylation of SERCA and increase Ca2+ levels, thus regulating VEGF-signaling cell migration.
“Consistent with this role of NOX4-derived ROS in angiogenesis (642, 989), it has been shown that NOX4 can modulate the role of VEGF-induced dimerization of CD146 necessary for cell adhesion (1065), and NOX4-derived ROS can induce the reversible glutathionylation of SERCA and increase Ca2+ levels, thus regulating VEGF-signaling cell migration (273).”
From Sources of Vascular Nitric Oxide and Reactive Oxygen Species and Their Regulation (2019) · cites this paper as [273]
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- Authors
- Evangelista, A. M., Thompson, M. D., Bolotina, V. M., Tong, X., & Cohen, R. A.
- Affiliations
- Boston University (US)
- Corresponding author
- Cohen, Richard A.
- Venue
- Free Radical Biology and Medicine
- Publisher
- Elsevier BV
- Published
- 2012-12
- Volume
- 53
- Issue
- 12
- Pages
- 2327-2334
- ISSN
- 0891-5849 (ISSN-L)
- PMC
- PMC3568680
- OpenAlex
- W2006496714
- Cited by
- 78
- References
- 33
- Citations by year
- 2026: 1 · 2025: 2 · 2024: 5 · 2023: 4 · 2022: 2 · 2021: 7 · 2020: 9 · 2019: 7 · 2018: 9 · 2017: 13 · 2016: 3 · 2015: 4 · 2014: 10 · 2013: 2
- FWCI
- 2.06
- Type
- journal article
- Language
- en
- Open access
- green
- europepmc.org
- Locations
- Free Radical Biology and Medicine (publishedVersion)
- PubMed (publishedVersion)
- Europe PMC (PubMed Central) (acceptedVersion)
- PubMed Central (acceptedVersion)
- Funders
- U.S. Department of Health and Human Services (HHSN268201000031C)
- National Institutes of Health (RO1-HL54150, HL031607-29, RO1-HL071793, HL007501-26)
- National Heart, Lung, and Blood Institute
- Boston University
- Montana Department of Transportation
- Topics
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Redox biology and oxidative stress
- Health Sciences › Medicine › Physiology › Nitric Oxide and Endothelin Effects
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Angiogenesis and VEGF in Cancer
- Keywords
- NOX4, NOX2, reactive oxygen species, VEGF signaling, endothelial cell migration, SERCA2b, calcium influx, hydrogen peroxide, catalase, superoxide dismutase, angiogenesis, NADPH oxidase
- MeSH terms
- NADPH Oxidase 2, NADPH Oxidase 4, Catalase, Cell Movement, Cells, Cultured, Cysteine, Glutathione, Humans, Hydrogen Peroxide, Membrane Glycoproteins, Oxidation-Reduction, Superoxides, Superoxide Dismutase, NADPH Oxidases, Calcium Signaling, Vascular Endothelial Growth Factor A, Endothelial Cells, Sarcoplasmic Reticulum Calcium-Transporting ATPases
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