Reactive Oxygen Species Can Provide Atheroprotection via NOX4-Dependent Inhibition of Inflammation and Vascular Remodeling
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Objective—: Oxidative stress is considered a hallmark of atherosclerosis. In particular, the superoxide-generating type 1 NADPH oxidase (NOX1) has been shown to be induced and play a pivotal role in early phases of mouse models of atherosclerosis and in the context of diabetes mellitus. Here, we investigated the role of the most abundant type 4 isoform (NOX4) in human and mouse advanced atherosclerosis. Approach and Results—: Plaques of patients with cardiovascular events or established diabetes mellitus showed a surprising reduction in expression of the most abundant but hydrogen peroxide (H 2 O 2 )-generating type 4 isoform (Nox4), whereas Nox1 mRNA was elevated, when compared with respective controls. As these data suggested that NOX4-derived reactive oxygen species may convey a surprisingly protective effect during plaque progression, we examined a mouse model of accelerated and advanced diabetic atherosclerosis, the streptozotocin-treated ApoE −/− mouse, with ( NOX4 −/− ) and without genetic deletion of Nox4. Similar to the human data, advanced versus early plaques of wild-type mice showed reduced Nox4 mRNA expression. Consistent with a rather protective role of NOX4-derived reactive oxygen species, NOX4 −/− mice showed increased atherosclerosis when compared with wild-type mice. Deleting NOX4 was associated with reduced H 2 O 2 forming activity and attenuation of the proinflammatory markers, monocyte chemotratic protein-1, interleukin-1β, and tumor necrosis factor-α, as well as vascular macrophage accumulation. Furthermore, there was a greater accumulation of fibrillar collagen fibres within the vascular wall and plaque in diabetic Nox4 −/− ApoE −/− mice, indicative of plaque remodeling. These data could be replicated in human aortic endothelial cells in vitro, where Nox4 overexpression increased H 2 O 2 and reduced the expression of pro-oxidants and profibrotic markers. Interestingly, Nox4 levels inversely correlated with Nox2 gene and protein levels. Although NOX2 is not constitutively active unlike NOX4 and forms rather superoxide, this opens up the possibility that at least some effects of NOX4 deletion are mediated by NOX2 activation. Conclusions—: Thus, the appearance of reactive oxygen species in atherosclerosis is apparently not always a nondesirable oxidative stress, but can also have protective effects. Both in humans and in mouse, the H 2 O 2 -forming NOX4, unlike the superoxide-forming NOX1, can act as a negative modulator of inflammation and remodeling and convey atheroprotection. These results have implications on how to judge reactive oxygen species formation in cardiovascular disease and need to be considered in the development of NOX inhibitory drugs.
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In general, NOX4 shows protective effects in ApoE−/− mice.
“In general, NOX4 shows protective effects in ApoE−/− mice (194, 229, 230, 379, 552, 838).”
From Sources of Vascular Nitric Oxide and Reactive Oxygen Species and Their Regulation (2019) · cites this paper as [379]
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- Authors
- Gray, S. P., Di Marco, E., Kennedy, K., Chew, P., Okabe, J., El-Osta, A., Calkin, A. C., Biessen, E. A. L., Touyz, R. M., Cooper, M. E., Schmidt, H. H. H. W., & Jandeleit-Dahm, K. A. M.
- Affiliations
- Baker Heart and Diabetes Institute (AU)
- From the Diabetic Complications Laboratory (S.P.G., E.D.M., K.K., P.C., M.E.C., K.A.M.J.-D.), Epigenetics Laboratory (J.O., A.E.-O.), and Diabetes and Dyslipidaemia Group (A.C.C.), Baker IDI Heart and Diabetes Institute, Melbourne, Australia; Faculty of Medicine, Monash University, Melbourne, Australia (S.P.G., E.D.M., K.A.M.J.-D.); Department of Pathology, Maastricht University Medical Center, Maastricht, The Netherlands (E.A.L.B.); Institute of Cardiovascular and Medical Sciences, University of...
- Corresponding author
- Schmidt, Harald H.H.W.
- Jandeleit-Dahm, Karin A.M.
- ORCID
- Venue
- Arteriosclerosis, Thrombosis, and Vascular Biology
- Published
- 2016-02
- Volume
- 36
- Issue
- 2
- Pages
- 295-307
- ISSN
- 1079-5642 (ISSN-L)
- 1524-4636
- OpenAlex
- W2209633084
- Cited by
- 189
- References
- 58
- Citations by year
- 2026: 7 · 2025: 14 · 2024: 17 · 2023: 14 · 2022: 18 · 2021: 13 · 2020: 21 · 2019: 15 · 2018: 22 · 2017: 27 · 2016: 20
- FWCI
- 16.94
- Type
- journal article
- Language
- en
- Open access
- bronze
- doi.org
- Locations
- Arteriosclerosis Thrombosis and Vascular Biology (publishedVersion)
- PubMed (publishedVersion)
- Research Publications (Maastricht University) (publishedVersion, other-oa)
- Padua Research Archive (University of Padova) (submittedVersion)
- Research Publications (Maastricht University) (submittedVersion, other-oa)
- Funders
- Diabetes Australia Research Trust
- British Heart Foundation (RG/13/7/30099)
- Diabetes Australia
- Australian Diabetes Society
- State Government of Victoria
- Université de Genève
- National Health and Medical Research Council
- Topics
- Health Sciences › Medicine › Physiology › Nitric Oxide and Endothelin Effects
- Life Sciences › Immunology and Microbiology › Immunology › Atherosclerosis and Cardiovascular Diseases
- Life Sciences › Immunology and Microbiology › Immunology › Neutrophil, Myeloperoxidase and Oxidative Mechanisms
- Keywords
- NOX4, reactive oxygen species, atherosclerosis, atheroprotection, oxidative stress, hydrogen peroxide, NADPH oxidase, NOX2, inflammation, vascular remodeling, plaque remodeling, diabetes mellitus, ApoE-deficient mice, macrophage accumulation, collagen fibrosis, aortic endothelial cells
- MeSH terms
- NADPH Oxidase 1, NADPH Oxidase 2, NADPH Oxidase 4, Animals, Aorta, Aortic Diseases, Apolipoproteins E, Cells, Cultured, Disease Models, Animal, Humans, Hydrogen Peroxide, Inflammation, Male, Membrane Glycoproteins, NADH, NADPH Oxidoreductases, Superoxides, Time Factors, Transfection, Signal Transduction, Case-Control Studies, Cytokines, Mice, Knockout, Oxidative Stress, Inflammation Mediators, NADPH Oxidases, Fibrillar Collagens, RNA Interference, Endothelial Cells, Atherosclerosis, Plaque, Atherosclerotic, Vascular Remodeling
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