Peripheral blood mitochondrial DNA content in relation to circulating metabolites and inflammatory markers: A population study

Mitochondrial DNA (mtDNA) content might undergo significant changes caused by metabolic derangements, oxidative stress and inflammation that lead to development and progression of cardiovascular diseases. We, therefore, investigated in a general population the association of peripheral blood mtDNA c...

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Veröffentlicht in:PloS one 2017-07, Vol.12 (7), p.e0181036-e0181036
Hauptverfasser: Knez, Judita, Marrachelli, Vannina G, Cauwenberghs, Nicholas, Winckelmans, Ellen, Zhang, Zhenyu, Thijs, Lutgarde, Brguljan-Hitij, Jana, Plusquin, Michelle, Delles, Christian, Monleon, Daniel, Redón, Josep, Staessen, Jan A, Nawrot, Tim S, Kuznetsova, Tatiana
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container_issue 7
container_start_page e0181036
container_title PloS one
container_volume 12
creator Knez, Judita
Marrachelli, Vannina G
Cauwenberghs, Nicholas
Winckelmans, Ellen
Zhang, Zhenyu
Thijs, Lutgarde
Brguljan-Hitij, Jana
Plusquin, Michelle
Delles, Christian
Monleon, Daniel
Redón, Josep
Staessen, Jan A
Nawrot, Tim S
Kuznetsova, Tatiana
description Mitochondrial DNA (mtDNA) content might undergo significant changes caused by metabolic derangements, oxidative stress and inflammation that lead to development and progression of cardiovascular diseases. We, therefore, investigated in a general population the association of peripheral blood mtDNA content with circulating metabolites and inflammatory markers. We examined 310 subjects (50.6% women; mean age, 53.3 years) randomly selected from a Flemish population. Relative mtDNA content was measured by quantitative real-time PCR in peripheral blood cells. Peak circulating metabolites were quantified using nuclear magnetic resonance spectroscopy. The level of inflammation was assessed via established inflammatory markers. Using Partial Least Squares analysis, we constructed 3 latent factors from the 44 measured metabolites that explained 62.5% and 8.5% of the variance in the contributing metabolites and the mtDNA content, respectively. With adjustments applied, mtDNA content was positively associated with the first latent factor (P = 0.002). We identified 6 metabolites with a major impact on the construction of this latent factor including HDL3 apolipoproteins, tyrosine, fatty acid with αCH2, creatinine, β-glucose and valine. We summarized them into a single composite metabolite score. We observed a negative association between the composite metabolic score and mtDNA content (P = 0.001). We also found that mtDNA content was inversely associated with inflammatory markers including hs-CRP, hs-IL6, white blood cell and neutrophil counts as well as neutrophil-to-lymphocyte ratio (P≤0.0024). We demonstrated that in a general population relative peripheral blood mtDNA content was associated with circulating metabolites indicative of perturbed lipid metabolism and with inflammatory biomarkers.
doi_str_mv 10.1371/journal.pone.0181036
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Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>Knez, Judita</au><au>Marrachelli, Vannina G</au><au>Cauwenberghs, Nicholas</au><au>Winckelmans, Ellen</au><au>Zhang, Zhenyu</au><au>Thijs, Lutgarde</au><au>Brguljan-Hitij, Jana</au><au>Plusquin, Michelle</au><au>Delles, Christian</au><au>Monleon, Daniel</au><au>Redón, Josep</au><au>Staessen, Jan A</au><au>Nawrot, Tim S</au><au>Kuznetsova, Tatiana</au><au>Samuels, David C.</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>Peripheral blood mitochondrial DNA content in relation to circulating metabolites and inflammatory markers: A population study</atitle><jtitle>PloS one</jtitle><addtitle>PLoS One</addtitle><date>2017-07-13</date><risdate>2017</risdate><volume>12</volume><issue>7</issue><spage>e0181036</spage><epage>e0181036</epage><pages>e0181036-e0181036</pages><issn>1932-6203</issn><eissn>1932-6203</eissn><abstract>Mitochondrial DNA (mtDNA) content might undergo significant changes caused by metabolic derangements, oxidative stress and inflammation that lead to development and progression of cardiovascular diseases. We, therefore, investigated in a general population the association of peripheral blood mtDNA content with circulating metabolites and inflammatory markers. We examined 310 subjects (50.6% women; mean age, 53.3 years) randomly selected from a Flemish population. Relative mtDNA content was measured by quantitative real-time PCR in peripheral blood cells. Peak circulating metabolites were quantified using nuclear magnetic resonance spectroscopy. The level of inflammation was assessed via established inflammatory markers. Using Partial Least Squares analysis, we constructed 3 latent factors from the 44 measured metabolites that explained 62.5% and 8.5% of the variance in the contributing metabolites and the mtDNA content, respectively. With adjustments applied, mtDNA content was positively associated with the first latent factor (P = 0.002). We identified 6 metabolites with a major impact on the construction of this latent factor including HDL3 apolipoproteins, tyrosine, fatty acid with αCH2, creatinine, β-glucose and valine. We summarized them into a single composite metabolite score. We observed a negative association between the composite metabolic score and mtDNA content (P = 0.001). We also found that mtDNA content was inversely associated with inflammatory markers including hs-CRP, hs-IL6, white blood cell and neutrophil counts as well as neutrophil-to-lymphocyte ratio (P≤0.0024). We demonstrated that in a general population relative peripheral blood mtDNA content was associated with circulating metabolites indicative of perturbed lipid metabolism and with inflammatory biomarkers.</abstract><cop>United States</cop><pub>Public Library of Science</pub><pmid>28704533</pmid><doi>10.1371/journal.pone.0181036</doi><tpages>e0181036</tpages><orcidid>https://orcid.org/0000-0003-4293-4576</orcidid><oa>free_for_read</oa></addata></record>
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source MEDLINE; DOAJ Directory of Open Access Journals; Public Library of Science (PLoS) Journals Open Access; EZB-FREE-00999 freely available EZB journals; PubMed Central; Free Full-Text Journals in Chemistry
subjects Adolescent
Adult
Aged
Aged, 80 and over
Apolipoproteins
Biological markers
Biology and life sciences
Biomarkers
Biomarkers - blood
Blood
Blood cells
Blood circulation
C-Reactive Protein - metabolism
Cardiovascular disease
Cardiovascular diseases
Composite materials
Construction
Creatinine
Deoxyribonucleic acid
DNA
DNA, Mitochondrial - blood
Fatty acids
Female
Heart diseases
Humans
Inflammation
Inflammation - blood
Inflammation - genetics
Inflammation - metabolism
Interleukin 6
Interleukin-6 - blood
Least-Squares Analysis
Lipid metabolism
Lymphocytes
Magnetic resonance
Magnetic resonance spectroscopy
Male
Medicine and Health Sciences
Metabolism
Metabolites
Metabolomics - methods
Middle Aged
Mitochondria - genetics
Mitochondrial DNA
NMR
Nuclear magnetic resonance
Oxidative stress
Peripheral blood
Physical Sciences
Polymerase chain reaction
Population studies
Proton Magnetic Resonance Spectroscopy - methods
Spectroscopic analysis
Spectroscopy
Tyrosine
Valine
Young Adult
title Peripheral blood mitochondrial DNA content in relation to circulating metabolites and inflammatory markers: A population study
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