Systemic and local vascular inflammation and arterial reactive oxygen species generation in patients with advanced cardiovascular diseases

BackgroundSystemic inflammation may cause endothelial activation, mediate local inflammation, and accelerate progression of atherosclerosis. We examined whether the levels of circulating inflammatory cytokines reflect local vascular inflammation and oxidative stress in two types of human arteries.Me...

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Main Authors: Joanna Sulicka-Grodzicka, Piotr Szczepaniak, Ewelina Jozefczuk, Karol Urbanski, Mateusz Siedlinski, Łukasz Niewiara, Bartłomiej Guzik, Grzegorz Filip, Bogusław Kapelak, Karol Wierzbicki, Mariusz Korkosz, Tomasz J. Guzik, Tomasz P. Mikolajczyk
Format: Article
Language:English
Published: Frontiers Media S.A. 2023-09-01
Series:Frontiers in Cardiovascular Medicine
Subjects:
Online Access:https://www.frontiersin.org/articles/10.3389/fcvm.2023.1230051/full
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author Joanna Sulicka-Grodzicka
Joanna Sulicka-Grodzicka
Piotr Szczepaniak
Piotr Szczepaniak
Ewelina Jozefczuk
Ewelina Jozefczuk
Karol Urbanski
Mateusz Siedlinski
Mateusz Siedlinski
Łukasz Niewiara
Bartłomiej Guzik
Grzegorz Filip
Bogusław Kapelak
Karol Wierzbicki
Mariusz Korkosz
Tomasz J. Guzik
Tomasz J. Guzik
Tomasz J. Guzik
Tomasz P. Mikolajczyk
Tomasz P. Mikolajczyk
Tomasz P. Mikolajczyk
author_facet Joanna Sulicka-Grodzicka
Joanna Sulicka-Grodzicka
Piotr Szczepaniak
Piotr Szczepaniak
Ewelina Jozefczuk
Ewelina Jozefczuk
Karol Urbanski
Mateusz Siedlinski
Mateusz Siedlinski
Łukasz Niewiara
Bartłomiej Guzik
Grzegorz Filip
Bogusław Kapelak
Karol Wierzbicki
Mariusz Korkosz
Tomasz J. Guzik
Tomasz J. Guzik
Tomasz J. Guzik
Tomasz P. Mikolajczyk
Tomasz P. Mikolajczyk
Tomasz P. Mikolajczyk
author_sort Joanna Sulicka-Grodzicka
collection DOAJ
description BackgroundSystemic inflammation may cause endothelial activation, mediate local inflammation, and accelerate progression of atherosclerosis. We examined whether the levels of circulating inflammatory cytokines reflect local vascular inflammation and oxidative stress in two types of human arteries.MethodsHuman internal mammary artery (IMA) was obtained in 69 patients undergoing coronary artery bypass graft (CABG) surgery and left anterior descending (LAD) artery was obtained in 17 patients undergoing heart transplantation (HTx). Plasma levels of tumor necrosis factor α (TNF-α), interleukin-6 (IL-6) and interleukin-1β (IL-1β) were measured using ELISA, high-sensitivity C-reactive protein (hs-CRP) was measured using Luminex, and mRNA expression of proinflammatory cytokines in the vascular tissues was assessed. Furthermore, formation of superoxide anion was measured in segments of IMA using 5 uM lucigenin-dependent chemiluminescence. Vascular reactivity was measured using tissue organ bath system.ResultsTNF-α, IL-6 and IL-1β mRNAs were expressed in all studied IMA and LAD segments. Plasma levels of inflammatory cytokines did not correlate with vascular cytokine mRNA expression neither in IMA nor in LAD. Plasma TNF-α and IL-6 correlated with hs-CRP level in CABG group. Hs-CRP also correlated with TNF-α in HTx group. Neither vascular TNF-α, IL-6 and IL-1β mRNA expression, nor systemic levels of either TNF-α, IL-6 and IL-1β were correlated with superoxide generation in IMAs. Interestingly, circulating IL-1β negatively correlated with maximal relaxation of the internal mammary artery (r = −0.37, p = 0.004). At the same time the mRNA expression of studied inflammatory cytokines were positively associated with each other in both IMA and LAD. The positive correlations were observed between circulating levels of IL-6 and TNF-α in CABG cohort and IL-6 and IL-1β in HTx cohort.ConclusionsThis study shows that peripheral inflammatory cytokine measurements may not reflect local vascular inflammation or oxidative stress in patients with advanced cardiovascular disease (CVD). Circulating pro-inflammatory cytokines generally correlated positively with each other, similarly their mRNA correlated in the arterial wall, however, these levels were not correlated between the studied compartments.
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spelling doaj.art-9bf6ced2b3e64c1a805ed49714dc23a62023-09-07T17:42:47ZengFrontiers Media S.A.Frontiers in Cardiovascular Medicine2297-055X2023-09-011010.3389/fcvm.2023.12300511230051Systemic and local vascular inflammation and arterial reactive oxygen species generation in patients with advanced cardiovascular diseasesJoanna Sulicka-Grodzicka0Joanna Sulicka-Grodzicka1Piotr Szczepaniak2Piotr Szczepaniak3Ewelina Jozefczuk4Ewelina Jozefczuk5Karol Urbanski6Mateusz Siedlinski7Mateusz Siedlinski8Łukasz Niewiara9Bartłomiej Guzik10Grzegorz Filip11Bogusław Kapelak12Karol Wierzbicki13Mariusz Korkosz14Tomasz J. Guzik15Tomasz J. Guzik16Tomasz J. Guzik17Tomasz P. Mikolajczyk18Tomasz P. Mikolajczyk19Tomasz P. Mikolajczyk20Department of Rheumatology and Immunology, Jagiellonian University Medical College, Krakow, PolandSchool of Infection and Immunity, University of Glasgow, Glasgow, United KingdomDepartment of Internal and Agricultural Medicine, Faculty of Medicine, Jagiellonian University Medical College, Krakow, PolandCenter for Medical Genomics OMICRON, Jagiellonian University Medical College, Krakow, PolandDepartment of Internal and Agricultural Medicine, Faculty of Medicine, Jagiellonian University Medical College, Krakow, PolandCenter for Medical Genomics OMICRON, Jagiellonian University Medical College, Krakow, PolandDepartment of Internal and Agricultural Medicine, Faculty of Medicine, Jagiellonian University Medical College, Krakow, PolandDepartment of Internal and Agricultural Medicine, Faculty of Medicine, Jagiellonian University Medical College, Krakow, PolandCenter for Medical Genomics OMICRON, Jagiellonian University Medical College, Krakow, PolandDepartment of Interventional Cardiology, Jagiellonian University Medical College, John Paul II Hospital, Kraków, PolandDepartment of Interventional Cardiology, Jagiellonian University Medical College, John Paul II Hospital, Kraków, PolandDepartment of Cardiovascular Surgery and Transplantology, Jagiellonian University, John Paul II Hospital, Krakow, PolandDepartment of Cardiovascular Surgery and Transplantology, Jagiellonian University, John Paul II Hospital, Krakow, PolandDepartment of Cardiovascular Surgery and Transplantology, Jagiellonian University, John Paul II Hospital, Krakow, PolandDepartment of Rheumatology and Immunology, Jagiellonian University Medical College, Krakow, PolandDepartment of Internal and Agricultural Medicine, Faculty of Medicine, Jagiellonian University Medical College, Krakow, PolandCenter for Medical Genomics OMICRON, Jagiellonian University Medical College, Krakow, PolandBHF Centre for Research Excellence, Centre for Cardiovascular Sciences, The University of Edinburgh, Edinburgh, United KingdomSchool of Infection and Immunity, University of Glasgow, Glasgow, United KingdomDepartment of Internal and Agricultural Medicine, Faculty of Medicine, Jagiellonian University Medical College, Krakow, PolandCenter for Medical Genomics OMICRON, Jagiellonian University Medical College, Krakow, PolandBackgroundSystemic inflammation may cause endothelial activation, mediate local inflammation, and accelerate progression of atherosclerosis. We examined whether the levels of circulating inflammatory cytokines reflect local vascular inflammation and oxidative stress in two types of human arteries.MethodsHuman internal mammary artery (IMA) was obtained in 69 patients undergoing coronary artery bypass graft (CABG) surgery and left anterior descending (LAD) artery was obtained in 17 patients undergoing heart transplantation (HTx). Plasma levels of tumor necrosis factor α (TNF-α), interleukin-6 (IL-6) and interleukin-1β (IL-1β) were measured using ELISA, high-sensitivity C-reactive protein (hs-CRP) was measured using Luminex, and mRNA expression of proinflammatory cytokines in the vascular tissues was assessed. Furthermore, formation of superoxide anion was measured in segments of IMA using 5 uM lucigenin-dependent chemiluminescence. Vascular reactivity was measured using tissue organ bath system.ResultsTNF-α, IL-6 and IL-1β mRNAs were expressed in all studied IMA and LAD segments. Plasma levels of inflammatory cytokines did not correlate with vascular cytokine mRNA expression neither in IMA nor in LAD. Plasma TNF-α and IL-6 correlated with hs-CRP level in CABG group. Hs-CRP also correlated with TNF-α in HTx group. Neither vascular TNF-α, IL-6 and IL-1β mRNA expression, nor systemic levels of either TNF-α, IL-6 and IL-1β were correlated with superoxide generation in IMAs. Interestingly, circulating IL-1β negatively correlated with maximal relaxation of the internal mammary artery (r = −0.37, p = 0.004). At the same time the mRNA expression of studied inflammatory cytokines were positively associated with each other in both IMA and LAD. The positive correlations were observed between circulating levels of IL-6 and TNF-α in CABG cohort and IL-6 and IL-1β in HTx cohort.ConclusionsThis study shows that peripheral inflammatory cytokine measurements may not reflect local vascular inflammation or oxidative stress in patients with advanced cardiovascular disease (CVD). Circulating pro-inflammatory cytokines generally correlated positively with each other, similarly their mRNA correlated in the arterial wall, however, these levels were not correlated between the studied compartments.https://www.frontiersin.org/articles/10.3389/fcvm.2023.1230051/fullcardiovascular diseasecytokineinflammationoxidative stresssuperoxidehs-CRP
spellingShingle Joanna Sulicka-Grodzicka
Joanna Sulicka-Grodzicka
Piotr Szczepaniak
Piotr Szczepaniak
Ewelina Jozefczuk
Ewelina Jozefczuk
Karol Urbanski
Mateusz Siedlinski
Mateusz Siedlinski
Łukasz Niewiara
Bartłomiej Guzik
Grzegorz Filip
Bogusław Kapelak
Karol Wierzbicki
Mariusz Korkosz
Tomasz J. Guzik
Tomasz J. Guzik
Tomasz J. Guzik
Tomasz P. Mikolajczyk
Tomasz P. Mikolajczyk
Tomasz P. Mikolajczyk
Systemic and local vascular inflammation and arterial reactive oxygen species generation in patients with advanced cardiovascular diseases
Frontiers in Cardiovascular Medicine
cardiovascular disease
cytokine
inflammation
oxidative stress
superoxide
hs-CRP
title Systemic and local vascular inflammation and arterial reactive oxygen species generation in patients with advanced cardiovascular diseases
title_full Systemic and local vascular inflammation and arterial reactive oxygen species generation in patients with advanced cardiovascular diseases
title_fullStr Systemic and local vascular inflammation and arterial reactive oxygen species generation in patients with advanced cardiovascular diseases
title_full_unstemmed Systemic and local vascular inflammation and arterial reactive oxygen species generation in patients with advanced cardiovascular diseases
title_short Systemic and local vascular inflammation and arterial reactive oxygen species generation in patients with advanced cardiovascular diseases
title_sort systemic and local vascular inflammation and arterial reactive oxygen species generation in patients with advanced cardiovascular diseases
topic cardiovascular disease
cytokine
inflammation
oxidative stress
superoxide
hs-CRP
url https://www.frontiersin.org/articles/10.3389/fcvm.2023.1230051/full
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