Control of angiogenesis dictated by picomolar superoxide levels

Bir, Shyamal C.; Shen, Xinggui; Kavanagh, Terrance J.; Kevil, Christopher G.; Pattillo, Christopher B.

doi:10.1016/j.freeradbiomed.2013.05.015

Cited by 30Angiogenesis and VEGF in CancerNitric Oxide and Endothelin EffectsRedox biology and oxidative stress

Control of angiogenesis dictated by picomolar superoxide levels

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Bir, Shyamal C., Shen, Xinggui, Kavanagh, Terrance J., Kevil, Christopher G., Pattillo, Christopher B.·2013·Free Radical Biology and Medicine

DOI 10.1016/j.freeradbiomed.2013.05.015PMC PMC3732119

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Abstract

Control of vascular insufficiencies due to various cardiovascular pathologies is important for developing specific and effective treatments. Fluctuations in oxidative stress significantly alter the progression of angiogenesis under physiological and pathological conditions. However, the precise amount of reactive oxygen species (ROS) required to influence subsequent signaling pathways for ischemic angiogenesis remains undefined. Here, we have determined the effect of ROS-mediated molecular mechanisms on angiogenesis in a murine model of peripheral artery disease using Gclm mutant mice (a model of compromised glutathione synthesis and therefore reduced antioxidant capacity). Left femoral artery ligation and excision were performed in Gclm WT (+/+), heterozygous (+/-), and null (-/-) mice. Blood flow (laser Doppler), angiogenic index (CD31/DAPI), and proliferation index (Ki67/DAPI) were significantly increased in Gclm(+/-) mice but not in Gclm(+/+) or Gclm(-/-) mice. Measurements of reactive oxygen species suggest that the amount of superoxide required to stimulate angiogenesis after the induction of ischemia is 9.82 pmol/mg of tissue. Protein carbonyl levels increased in a manner consistent with increasing oxidative stress. Superoxide and protein carbonyl levels were reduced by the addition of the nitroxide tempol, a known superoxide dismutase mimetic. Finally, restoration of blood flow in Gclm(+/-) mice was attenuated by a VEGF164 aptamer, verifying that slightly elevated levels of ROS restore blood flow by stimulating endothelial cell proliferation through a VEGF-dependent pathway. The results of this study reveal new information on the amount of ROS necessary for angiogenic activity and provide the foundation of critical redox parameters for vascular remodeling responses. The information obtained from this study on vascular ischemia, using a model of decreased antioxidant capacity, has provided insight into the control of revascularization and is a step forward in our ability to regulate angiogenic therapies.

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Generation of superoxide and hydrogen peroxide mediates critical processes such as angiogenesis, hypoxic adaptation, and energy homeostasis.
“Indeed, the generation of superoxide and hydrogen peroxide, among others, has been shown to mediate critical processes such as angiogenesis, hypoxic adaptation, and energy homeostasis (96, 249, 291, 720, 778, 825, 960).”
From Sources of Vascular Nitric Oxide and Reactive Oxygen Species and Their Regulation (2019) · cites this paper as [96]

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Authors: Bir, S. C., Shen, X., Kavanagh, T. J., Kevil, C. G., & Pattillo, C. B.
Affiliations: Louisiana State University Health Sciences Center Shreveport (US)
University of Washington (US)
Corresponding author: Pattillo, Christopher B.
ORCID: Bir, Shyamal C.
Shen, Xinggui
Kavanagh, Terrance J.
Kevil, Christopher G.
Pattillo, Christopher B.
Venue: Free Radical Biology and Medicine
Publisher: Elsevier BV
Published: 2013-10
Volume: 63
Pages: 135-142
ISSN: 0891-5849 (ISSN-L)
DOI: 10.1016/j.freeradbiomed.2013.05.015
PMC: PMC3732119
OpenAlex: W1971835411
Cited by: 30
References: 43
Citations by year: 2023: 3 · 2022: 5 · 2021: 1 · 2020: 2 · 2019: 1 · 2018: 3 · 2017: 6 · 2016: 3 · 2015: 4 · 2014: 2
FWCI: 1.34
Type: journal article
Language: en
Open access: green
www.ncbi.nlm.nih.gov
Licence: www.elsevier.com/tdm/userlicense/1.0/ (tdm)
www.elsevier.com/legal/tdmrep-license (tdm)
Locations: Free Radical Biology and Medicine (publishedVersion)
PubMed (publishedVersion)
Europe PMC (PubMed Central) (acceptedVersion)
PubMed Central (acceptedVersion)
Funders: NIH (R01HL080482, F32HL094021, R01ES010849, P50ES015915)
ADA Basic Science (1-10-BS-84)
Topics: Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Angiogenesis and VEGF in Cancer
Health Sciences › Medicine › Physiology › Nitric Oxide and Endothelin Effects
Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Redox biology and oxidative stress
Keywords: angiogenesis, superoxide, reactive oxygen species, oxidative stress, peripheral arterial disease, glutathione synthesis, antioxidant capacity, ischemia, revascularization, protein carbonylation, endothelial cell proliferation, blood flow
MeSH terms: Animals, Disease Models, Animal, Glutamate-Cysteine Ligase, Ischemia, Mice, Transgenic, Neovascularization, Pathologic, Regional Blood Flow, Superoxides, Signal Transduction, Reactive Oxygen Species, Oxidative Stress, Neovascularization, Physiologic, NADPH Oxidases, Vascular Endothelial Growth Factor A, Mice, Peripheral Arterial Disease

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Control of angiogenesis dictated by picomolar superoxide levels

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