Melatonin alleviates inflammation-induced apoptosis in human umbilical vein endothelial cells via suppression of Ca2+-XO-ROS-Drp1-mitochondrial fission axis by activation of AMPK/SERCA2a pathway
Open accessAbstract
Endothelia inflammation damage is vital to the development and progression of chronic venous disease. In the present study, we explored the protective effect of melatonin on endothelia apoptosis induced by LPS, particularly focusing on the mitochondrial fission. We demonstrated that human umbilical vein endothelial cells (HUVEC) subjected to LPS for 12 h exhibited a higher apoptotic rate. However, melatonin (1–20 μM) treatment 12 h before LPS had the ability to protect HUVEC cell against LPS-mediated apoptosis in a dose-dependent manner. Furthermore, LPS induced the cytoplasmic calcium overload which was responsible for the upregulation of calcium-dependent xanthine oxidase (XO). Higher XO expression was associated with reactive oxygen species (ROS) overproduction, leading to the Drp1 phosphorylation at the Ser616 site and migration on the surface of mitochondria. Furthermore, phosphorylated Drp1 initiated the mitochondrial fission contributing to the caspase9-dependent mitochondrial apoptosis as evidenced by lower membrane potential, more cyt-c leakage into the nuclear, and higher expression of proapoptotic proteins. However, melatonin treatment could trigger the AMPK pathway, which was followed by the increased SERCA2a expression. Activation of AMPK/SERCA2a by melatonin inhibited the calcium overload, XO-mediated ROS outburst, Drp1-required mitochondrial fission, and final mitochondrial apoptosis. In summary, this study confirmed that LPS induced HUVEC apoptosis through Ca 2+ -XO-ROS-Drp1-mitochondrial fission axis and that melatonin reduced the apoptosis of HUVEC through activation of the AMPK/SERCA2a pathway.
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DRP1-dependent mitochondrial fission triggered mitochondrial apoptotic pathway, as shown by the caspase 9 cleavage, ΔΨm decline, cytochrome c leakage, as well as increased expression of proapoptotic proteins.
“DRP1-dependent mitochondrial fission triggered mitochondrial apoptotic pathway, as shown by the caspase 9 cleavage, ΔΨm decline, cytochrome c leakage, as well as increased expression of proapoptotic proteins [140].”
From AMPK, Mitochondrial Function, and Cardiovascular Disease (2020) · cites this paper as [140]
Melatonin-activated AMPK-sarcoplasmic/endoplasmic reticulum calcium ATPase 2a axis prevented calcium overload, XO-dependent ROS overproduction, DRP1-mediated mitochondrial fission, and apoptosis in lipopolysaccharide-treated cells.
“Further, melatonin-activated AMPK-sarcoplasmic/endoplasmic reticulum calcium ATPase 2a axis prevented calcium overload, XO-dependent ROS overproduction, DRP1-mediated mitochondrial fission, and apoptosis in lipopolysaccharide-treated cells [140].”
From AMPK, Mitochondrial Function, and Cardiovascular Disease (2020) · cites this paper as [140]
Melatonin induced endothelial cell apoptosis through activation of the AMPK-sarcoplasmic/endoplasmic reticulum calcium ATPase 2a pathway under conditions of inflammation.
“Collectively, this study demonstrated that melatonin induced endothelial cell apoptosis through activation of the AMPK-sarcoplasmic/endoplasmic reticulum calcium ATPase 2a pathway under conditions of inflammation [140].”
From AMPK, Mitochondrial Function, and Cardiovascular Disease (2020) · cites this paper as [140]
Melatonin protected HUVECs against lipopolysaccharide-mediated apoptosis.
“For instance, melatonin protected HUVECs against lipopolysaccharide-mediated apoptosis [140].”
From AMPK, Mitochondrial Function, and Cardiovascular Disease (2020) · cites this paper as [140]
Lipopolysaccharide triggered cytosolic calcium overload, and in turn upregulated XO, whose activity is calcium-dependent.
“Lipopolysaccharide triggered cytosolic calcium overload, and in turn upregulated XO, whose activity is calcium-dependent [140].”
From AMPK, Mitochondrial Function, and Cardiovascular Disease (2020) · cites this paper as [140]
Upregulation of XO was accompanied by excessive ROS production, resulting in the Ser616 phosphorylation as well as the mitochondrial migration of DRP1.
“Upregulation of XO was accompanied by excessive ROS production, resulting in the Ser616 phosphorylation as well as the mitochondrial migration of DRP1 [140].”
From AMPK, Mitochondrial Function, and Cardiovascular Disease (2020) · cites this paper as [140]
Melatonin activated AMPK, which was associated with the upregulation of sarcoplasmic/endoplasmic reticulum calcium ATPase 2a.
“Importantly, melatonin activated AMPK, which was associated with the upregulation of sarcoplasmic/endoplasmic reticulum calcium ATPase 2a [140].”
From AMPK, Mitochondrial Function, and Cardiovascular Disease (2020) · cites this paper as [140]
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- Authors
- Cui, J., Li, Z., Zhuang, S., Qi, S., Li, L., Zhou, J., Zhang, W., & Zhao, Y.
- Affiliations
- Fudan University (CN)
- Corresponding author
- Cui, Jiasen
- Venue
- Cell Stress and Chaperones
- Publisher
- Elsevier BV
- Published
- 2018-03
- Volume
- 23
- Issue
- 2
- Pages
- 281-293
- ISSN
- 1355-8145 (ISSN-L)
- PMC
- PMC5823809
- OpenAlex
- W2755416799
- Cited by
- 65
- References
- 61
- Citations by year
- 2026: 3 · 2025: 9 · 2024: 6 · 2023: 4 · 2022: 10 · 2021: 5 · 2020: 12 · 2019: 6 · 2018: 10
- FWCI
- 4.70
- Type
- journal article
- Language
- en
- Open access
- hybrid
- doi.org
- Licence
- Locations
- Cell Stress and Chaperones (publishedVersion, cc-by-nc-nd)
- Europe PMC (PubMed Central) (publishedVersion)
- PubMed Central (publishedVersion)
- PubMed (publishedVersion)
- Topics
- Life Sciences › Neuroscience › Endocrine and Autonomic Systems › Circadian rhythm and melatonin
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Mitochondrial Function and Pathology
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Cell death mechanisms and regulation
- Keywords
- melatonin, endothelial cell apoptosis, human umbilical vein endothelial cells, lipopolysaccharide, mitochondrial fission, Drp1 phosphorylation, xanthine oxidase, reactive oxygen species, calcium overload, AMPK, SERCA2a, mitochondrial apoptosis, caspase-9, chronic venous disease, endothelial inflammation
- MeSH terms
- Adenylate Kinase, Calcium, Humans, Inflammation, Lipopolysaccharides, Melatonin, Mitochondria, Xanthine Oxidase, Signal Transduction, Up-Regulation, Apoptosis, Reactive Oxygen Species, Caspase 9, Sarcoplasmic Reticulum Calcium-Transporting ATPases, Human Umbilical Vein Endothelial Cells, Mitochondrial Dynamics
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