Endothelial-specific Nox2 overexpression increases vascular superoxide and macrophage recruitment in ApoE−/− mice

Douglas, Gillian; Bendall, Jennifer K.; Crabtree, Mark J.; Tatham, Amy L.; Carter, Emma E.; Hale, Ashley B.; Channon, Keith M.

doi:10.1093/cvr/cvs026

Cited by 111Nitric Oxide and Endothelin EffectsAtherosclerosis and Cardiovascular DiseasesNeutrophil, Myeloperoxidase and Oxidative Mechanisms

Endothelial-specific Nox2 overexpression increases vascular superoxide and macrophage recruitment in ApoE−/− mice

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Douglas, Gillian, Bendall, Jennifer K., Crabtree, Mark J., Tatham, Amy L., Carter, Emma E., Hale, Ashley B., Channon, Keith M.·2012·Cardiovascular Research

DOI 10.1093/cvr/cvs026PMC PMC3307381

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Abstract

AIMS: Vascular disease states are associated with endothelial dysfunction and increased production of reactive oxygen species derived from NADPH oxidases. However, it remains unclear whether a primary increase in superoxide production specifically in the endothelium alters the initiation or progression of atherosclerosis. METHODS AND RESULTS: Mice overexpressing Nox2 specifically in the endothelium (Nox2-Tg) were crossed with ApoE(-/-) mice to produce Nox2-Tg ApoE(-/-) mice and ApoE(-/-) littermates. Endothelial overexpression of Nox2 in ApoE(-/-) mice did not alter blood pressure, but significantly increased vascular superoxide production compared with ApoE(-/-) littermates, measured using both lucigenin chemiluminescence and 2-hydroxyethidium production (ApoE(-/-), 19.9 ± 6.3 vs. Nox2-Tg ApoE(-/-), 47.0 ± 7.0 nmol 2-hydroxyethidium/aorta, P< 0.05). Increased endothelial superoxide production increased endothelial levels of vascular cell adhesion protein 1 and enhanced macrophage recruitment in early lesions in the aortic roots of 9-week-old mice, indicating increased atherosclerotic plaque initiation. However, endothelial-specific Nox2 overexpression did not alter native or angiotensin II-driven atherosclerosis in either the aortic root or the descending aorta. CONCLUSION: Endothelial-targeted Nox2 overexpression in ApoE(-/-) mice is sufficient to increase vascular superoxide production and increase macrophage recruitment possible via activation of endothelial cells. However, this initial increase in macrophage recruitment did not alter the progression of atherosclerosis. These results indicate that Nox-mediated reactive oxygen species signalling has important cell-specific and distinct temporal roles in the initiation and progression of atherosclerosis.

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In other cases, increased expression of endothelial NOX2 has not been linked to pathological conditions even though increased production of superoxide and macrophage recruitment was observed.
“However, in other cases, an increased expression of endothelial NOX2 has not been linked to pathological conditions even though an increased production of superoxide and macrophage recruitment was observed (243, 443).”
From Sources of Vascular Nitric Oxide and Reactive Oxygen Species and Their Regulation (2019) · cites this paper as [243]
Subsequent progress of the atherosclerotic lesion is dependent on immune cells.
“The current paradigm indicates that macrophage NOX2 is more detrimental in the development of cardiovascular disease (395, 876), with endothelial NOX2 probably involved in the initiation, but not so much in the development of the disease, and a subsequent progress of the atherosclerotic lesion dependent on immune cells (243, 573, 976).”
From Sources of Vascular Nitric Oxide and Reactive Oxygen Species and Their Regulation (2019) · cites this paper as [243]
Endothelial NOX2 is probably involved in the initiation, but not so much in the development of cardiovascular disease.
“The current paradigm indicates that macrophage NOX2 is more detrimental in the development of cardiovascular disease (395, 876), with endothelial NOX2 probably involved in the initiation, but not so much in the development of the disease, and a subsequent progress of the atherosclerotic lesion dependent on immune cells (243, 573, 976).”
From Sources of Vascular Nitric Oxide and Reactive Oxygen Species and Their Regulation (2019) · cites this paper as [243]

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Endothelial-specific Nox2 over-expression increases vascular superoxide production but does not alter atherosclerotic plaque or AngII-dependent aneurysm formation
Douglas, G., Bendall, J. K., & Channon, K. M. (2010) · Atherosclerosis · doi:10.1016/j.atherosclerosis.2010.08.025 · Cited by 2 · see citing works
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Direct evidence of a role for Nox2 in superoxide production, reduced nitric oxide bioavailability, and early atherosclerotic plaque formation in ApoE−/−mice
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Excessive Superoxide Production And Endothelial Dysfunction In Cerebral Arteries Of Atherosclerotic Mice Occur In The Absence Of Lesions And Are Due To The Activity Of Nox2‐Containing NADPH Oxidase
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Authors: Douglas, G., Bendall, J. K., Crabtree, M. J., Tatham, A. L., Carter, E. E., Hale, A. B., & Channon, K. M.
Affiliations: John Radcliffe Hospital (GB)
University of Oxford (GB)
Corresponding author: Douglas, Gillian
ORCID: Douglas, Gillian
Crabtree, Mark J.
Channon, Keith M.
Venue: Cardiovascular Research
Publisher: Oxford University Press (OUP)
Published: 2012-01-27
Volume: 94
Issue: 1
Pages: 20-29
ISSN: 0008-6363 (ISSN-L)
1755-3245
DOI: 10.1093/cvr/cvs026
PMC: PMC3307381
OpenAlex: W1988097865
Cited by: 111
References: 28
Citations by year: 2026: 5 · 2025: 5 · 2024: 8 · 2023: 7 · 2022: 12 · 2021: 5 · 2020: 1 · 2019: 6 · 2018: 8 · 2017: 13 · 2016: 10 · 2015: 6 · 2014: 10 · 2013: 10 · 2012: 5
FWCI: 6.65
Type: journal article
Language: en
Open access: hybrid
doi.org
Licence: other-oa
Locations: Cardiovascular Research (publishedVersion, other-oa)
PubMed Central (publishedVersion, cc-by-nc)
PubMed (publishedVersion)
Funders: Wellcome Trust (090532)
British Heart Foundation (PG/05/141/20098, RG/07/003/23133, RG/12/5/29576)
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: NOX2, NADPH oxidase, atherosclerosis initiation, macrophage recruitment, ApoE-deficient mice, VCAM-1, reactive oxygen species, endothelial dysfunction, angiotensin II, aortic root lesions
MeSH terms: NADPH Oxidase 2, Angiotensin II, Animals, Aortic Diseases, Apolipoproteins E, Blood Pressure, Chemotaxis, Disease Models, Animal, Humans, Macrophages, Membrane Glycoproteins, Mice, Transgenic, Superoxides, Time Factors, Signal Transduction, Up-Regulation, Mice, Knockout, Disease Progression, Vascular Cell Adhesion Molecule-1, NADPH Oxidases, Endothelial Cells, Atherosclerosis, Mice

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Endothelial-specific Nox2 overexpression increases vascular superoxide and macrophage recruitment in ApoE−/− mice

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