Glutathione Adducts on Sarcoplasmic/Endoplasmic Reticulum Ca2+ ATPase Cys-674 Regulate Endothelial Cell Calcium Stores and Angiogenic Function as Well as Promote Ischemic Blood Flow Recovery
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The sarco/endoplasmic reticulum Ca(2+) ATPase (SERCA) is key to Ca(2+) homeostasis and is redox-regulated by reversible glutathione (GSH) adducts on the cysteine (C) 674 thiol that stimulate Ca(2+) uptake activity and endothelial cell angiogenic responses in vitro. We found that mouse hind limb muscle ischemia induced S-glutathione adducts on SERCA in both whole muscle tissue and endothelial cells. To determine the role of S-glutathiolation, we used a SERCA 2 C674S heterozygote knock-in (SKI) mouse lacking half the key thiol. Following hind limb ischemia, SKI animals had decreased SERCA S-glutathione adducts and impaired blood flow recovery. We studied SKI microvascular endothelial cells in which total SERCA 2 expression was unchanged. Cultured SKI microvascular endothelial cells showed impaired migration and network formation compared with wild type (WT). Ca(2+) studies showed decreased nitric oxide (·NO)-induced (45)Ca(2+) uptake into the endoplasmic reticulum (ER) of SKI cells, while Fura-2 studies revealed lower Ca(2+) stores and decreased vascular endothelial growth factor (VEGF)- and ·NO-induced Ca(2+) influx. Adenoviral overexpression of calreticulin, an ER Ca(2+) binding protein, increased ionomycin-releasable stores, VEGF-induced Ca(2+) influx and endothelial cell migration. Taken together, these data indicate that the redox-sensitive Cys-674 thiol on SERCA 2 is required for normal endothelial cell Ca(2+) homeostasis and ischemia-induced angiogenic responses, revealing a novel redox control of angiogenesis via Ca(2+) stores.
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Ca2+ can directly activate antioxidant enzymes such as GSH reductase, catalase, and SOD, through which ROS clearance is mediated.
“Ca2+ can directly activate antioxidant enzymes such as GSH reductase and catalase and SOD through which ROS clearance is mediated (Thompson et al. 2014).”
From Reactive Oxygen Species, Toxicity, Oxidative Stress, and Antioxidants: Chronic Diseases and Aging (2023) · cites this paper as Thompson et al. 2014
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Self-citation
- Authors
- Thompson, M. D., Mei, Y., Weisbrod, R. M., Silver, M., Shukla, P. C., Bolotina, V. M., Cohen, R. A., & Tong, X.
- Affiliations
- Boston University (US)
- Corresponding author
- Cohen, Richard A.
- Tong, Xiaoyong
- ORCID
- Venue
- Journal of Biological Chemistry
- Publisher
- Elsevier BV
- Published
- 2014-07
- Volume
- 289
- Issue
- 29
- Pages
- 19907-19916
- ISSN
- 0021-9258 (ISSN-L)
- PMC
- PMC4106311
- OpenAlex
- W2083447870
- Cited by
- 70
- References
- 24
- Citations by year
- 2026: 5 · 2025: 6 · 2024: 4 · 2023: 10 · 2022: 8 · 2021: 3 · 2020: 12 · 2019: 7 · 2018: 2 · 2017: 3 · 2016: 5 · 2015: 1 · 2014: 4
- FWCI
- 1.78
- Type
- journal article
- Language
- en
- Open access
- hybrid
- doi.org
- Licence
- Locations
- Journal of Biological Chemistry (publishedVersion, cc-by)
- PubMed Central (publishedVersion)
- PubMed (publishedVersion)
- Funders
- National Institutes of Health (HL031607-30, R37 HL104017, R01-HL071793, HL07969)
- 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 › Neuroscience › Sensory Systems › Ion Channels and Receptors
- Keywords
- SERCA2, S-glutathionylation, glutathione adducts, redox regulation, endoplasmic reticulum calcium stores, angiogenesis, hindlimb ischemia, blood flow recovery, microvascular endothelial cells, calreticulin, nitric oxide, vascular endothelial growth factor, endothelial cell migration
- MeSH terms
- Animals, Hypoxia, Calcium, Female, Glutathione, Hemodynamics, Hindlimb, Ischemia, Male, Mice, Inbred C57BL, Mice, Mutant Strains, Mice, Transgenic, Nitric Oxide, Oxidation-Reduction, Pregnancy, Muscle, Skeletal, Neovascularization, Physiologic, Calcium Signaling, Vascular Endothelial Growth Factor A, Endothelial Cells, Mutant Proteins, Mice, Sarcoplasmic Reticulum Calcium-Transporting ATPases, Gene Knock-In Techniques
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