Carbon monoxide differentially modulates STAT1 and STAT3 and inhibits apoptosis via a phosphatidylinositol 3-kinase/Akt and p38 kinase-dependent STAT3 pathway during anoxia-reoxygenation injury
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Carbon monoxide (CO), previously considered a toxic waste product of heme catabolism, is emerging as an important gaseous molecule. In addition to its important role in neurotransmission, exogenous CO protects against vascular injury, transplant rejection, and acute lung injury. However, little is known regarding the precise signaling mechanisms of CO. We have recently shown that CO attenuates endothelial cell apoptosis during anoxia-reoxygenation injury by activating MKK3/p38alpha mitogen-activated protein kinase (MAPK) pathways. Our current study is the first to demonstrate that CO can differentially modulate STAT1 and STAT3 activation and, specifically, that STAT3 activation by CO is responsible for the anti-apoptotic effect in endothelial cells. In addition, we show that the anti-apoptotic effects of CO depend upon both phosphatidylinositol 3-kinase/Akt and p38 MAPK signaling pathways in endothelial cells, whereas previous reports have implicated only the MKK3/p38 MAPK pathway. Using chemical inhibitors and dominant negative constructs, we show that CO enhances STAT3 activation via phosphatidylinositol 3-kinase/Akt and p38 MAPK pathways with subsequent attenuation of Fas expression and caspase 3 activity. These data highlight the anti-apoptotic signaling mechanisms of CO and, importantly, delineate potential therapeutic strategies to prevent ischemia-reperfusion or anoxia-reoxygenation injury in the vasculature.
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In lung models of in vitro anoxia-reoxygenation and in vivo I/R, carbon monoxide attenuates endothelial cell apoptosis through enhanced STAT3 activation via PI3K/Akt and p38 MAPK pathways.
“In studies of lung models of in vitro anoxia–reoxygenation and in vivo I/R, carbon monoxide attenuated endothelial cell apoptosis presumably through enhanced STAT3 activation via PI3K/Akt and p38 MAPK pathways (Zhang et al., 2003, 2005).”
From Targeting Janus Kinases and Signal Transducer and Activator of Transcription 3 To Treat Inflammation, Fibrosis, and Cancer: Rationale, Progress, and Caution (2020) · cites this paper as Zhang et al., 2005
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- Authors
- Zhang, X., Shan, P., Alam, J., Fu, X.-Y., & Lee, P. J.
- Affiliations
- Yale University (US)
- Ochsner Medical Center (US)
- Indiana University Indianapolis (US)
- Corresponding author
- Lee, Patty J.
- Venue
- Journal of Biological Chemistry
- Publisher
- Elsevier BV
- Published
- 2005-03
- Volume
- 280
- Issue
- 10
- Pages
- 8714-8721
- ISSN
- 0021-9258 (ISSN-L)
- OpenAlex
- W2076019855
- Cited by
- 198
- References
- 32
- Citations by year
- 2026: 3 · 2025: 2 · 2024: 3 · 2023: 7 · 2022: 9 · 2021: 6 · 2020: 7 · 2019: 6 · 2018: 6 · 2017: 8 · 2016: 6 · 2015: 9 · 2014: 8 · 2013: 11 · 2012: 12
- FWCI
- 5.70
- Type
- journal article
- Language
- en
- Open access
- hybrid
- doi.org
- Licence
- Locations
- Journal of Biological Chemistry (publishedVersion, cc-by)
- PubMed (publishedVersion)
- Funders
- National Institutes of Health (5r01dk043135-07)
- National Heart, Lung, and Blood Institute (R01HL071595, HL 071595-01)
- National Institute of Allergy and Infectious Diseases (AI-34522, R01AI034522)
- National Institute of Diabetes and Digestive and Kidney Diseases (DK43135)
- Topics
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Heme Oxygenase-1 and Carbon Monoxide
- Health Sciences › Medicine › Oncology › Cytokine Signaling Pathways and Interactions
- Health Sciences › Medicine › Physiology › Nitric Oxide and Endothelin Effects
- Keywords
- carbon monoxide, STAT1, STAT3, apoptosis, anoxia/reoxygenation injury, ischemia-reperfusion injury, endothelial cells, phosphatidylinositol 3-kinase/Akt signaling, p38 MAPK signaling, Fas, caspase-3, anti-apoptotic signaling
- MeSH terms
- Animals, Carbon Monoxide, Cell Survival, DNA-Binding Proteins, Endothelium, Vascular, Protein-Tyrosine Kinases, Proto-Oncogene Proteins, Pulmonary Artery, Trans-Activators, Cell Hypoxia, Apoptosis, Protein Serine-Threonine Kinases, Phosphatidylinositol 3-Kinases, MAP Kinase Signaling System, p38 Mitogen-Activated Protein Kinases, STAT1 Transcription Factor, STAT3 Transcription Factor, Proto-Oncogene Proteins c-akt, Rats
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