The association between ambient particulate matter exposure and the telomere–mitochondrial axis of aging in newborns

Background: Particulate matter (PM) is associated with aging markers at birth, including telomeres and mitochondria. It is unclear whether markers of the core-axis of aging, i.e. tumor suppressor p53 (p53) and peroxisome proliferator-activated receptor gamma co-activator 1 alpha (PGC-1α), are associ...

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Main Authors: Charlotte Van Der Stukken, Tim S Nawrot, Congrong Wang, Wouter Lefebvre, Charlotte Vanpoucke, Michelle Plusquin, Harry A Roels, Bram G Janssen, Dries S. Martens
Format: Article
Language:English
Published: Elsevier 2023-01-01
Series:Environment International
Subjects:
Online Access:http://www.sciencedirect.com/science/article/pii/S0160412022006225
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author Charlotte Van Der Stukken
Tim S Nawrot
Congrong Wang
Wouter Lefebvre
Charlotte Vanpoucke
Michelle Plusquin
Harry A Roels
Bram G Janssen
Dries S. Martens
author_facet Charlotte Van Der Stukken
Tim S Nawrot
Congrong Wang
Wouter Lefebvre
Charlotte Vanpoucke
Michelle Plusquin
Harry A Roels
Bram G Janssen
Dries S. Martens
author_sort Charlotte Van Der Stukken
collection DOAJ
description Background: Particulate matter (PM) is associated with aging markers at birth, including telomeres and mitochondria. It is unclear whether markers of the core-axis of aging, i.e. tumor suppressor p53 (p53) and peroxisome proliferator-activated receptor gamma co-activator 1 alpha (PGC-1α), are associated with prenatal air pollution and whether there are underlying mechanisms. Methods: 556 mother-newborn pairs from the ENVIRONAGE birth cohort were recruited at the East Limburg Hospital in Genk (Belgium). In placenta and cord blood, telomere length (TL) and mitochondrial DNA content (mtDNAc) were measured using quantitative real-time polymerase chain reaction (qPCR). In cord plasma, p53 and PGC-1α protein levels were measured using ELISA. Daily ambient PM2.5 concentrations during gestation were calculated using a spatial temporal interpolation model. Distributed lag models (DLMs) were applied to assess the association between prenatal PM2.5 exposure and each molecular marker. Mediation analysis was performed to test for underlying mechanisms. Results: A 5 µg/m3 increment in PM2.5 exposure was associated with −11.23 % (95 % CI: −17.36 % to −4.65 %, p = 0.0012) and −7.34 % (95 % CI: −11.56 % to −2.92 %, p = 0.0014) lower placental TL during the entire pregnancy and second trimester respectively, and with −12.96 % (95 % CI: −18.84 % to −6.64 %, p < 0.001) lower placental mtDNAc during the third trimester. Furthermore, PM2.5 exposure was associated with a 12.42 % (95 % CI: −1.07 % to 27.74 %, p = 0.059) higher cord plasma p53 protein level and a −3.69 % (95 % CI: −6.97 % to −0.31 %, p = 0.033) lower cord plasma PGC-1α protein level during the third trimester. Placental TL mediated 65 % of the negative and 17 % of the positive association between PM2.5 and placental mtDNAc and cord plasma p53 protein levels, respectively. Conclusion: Ambient PM2.5 exposure during pregnancy is associated with markers of the core-axis of aging, with TL as a mediating factor. This study strengthens the hypothesis of the air pollution induced core-axis of aging, and may unravel a possible underlying mediating mechanism in an early-life epidemiological context.
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spelling doaj.art-906d8a9bc9a448d9bded683a2dc4aedb2023-01-19T04:16:17ZengElsevierEnvironment International0160-41202023-01-01171107695The association between ambient particulate matter exposure and the telomere–mitochondrial axis of aging in newbornsCharlotte Van Der Stukken0Tim S Nawrot1Congrong Wang2Wouter Lefebvre3Charlotte Vanpoucke4Michelle Plusquin5Harry A Roels6Bram G Janssen7Dries S. Martens8Centre for Environmental Sciences, Hasselt University, Hasselt, BelgiumCentre for Environmental Sciences, Hasselt University, Hasselt, Belgium; Department of Public Health &amp; Primary Care, Occupational &amp; Environmental Medicine, Leuven University, Leuven, BelgiumCentre for Environmental Sciences, Hasselt University, Hasselt, BelgiumFlemish Institute for Technological Research (VITO), Mol, BelgiumBelgian Interregional Environment Agency, Brussels, BelgiumCentre for Environmental Sciences, Hasselt University, Hasselt, BelgiumCentre for Environmental Sciences, Hasselt University, Hasselt, Belgium; Louvain Centre for Toxicology and Applied Pharmacology, Université catholique de Louvain, Brussels, BelgiumCentre for Environmental Sciences, Hasselt University, Hasselt, BelgiumCentre for Environmental Sciences, Hasselt University, Hasselt, Belgium; Corresponding author at: Centre for Environmental Sciences, Hasselt University, Agoralaan gebouw D, 3590 Diepenbeek, Belgium.Background: Particulate matter (PM) is associated with aging markers at birth, including telomeres and mitochondria. It is unclear whether markers of the core-axis of aging, i.e. tumor suppressor p53 (p53) and peroxisome proliferator-activated receptor gamma co-activator 1 alpha (PGC-1α), are associated with prenatal air pollution and whether there are underlying mechanisms. Methods: 556 mother-newborn pairs from the ENVIRONAGE birth cohort were recruited at the East Limburg Hospital in Genk (Belgium). In placenta and cord blood, telomere length (TL) and mitochondrial DNA content (mtDNAc) were measured using quantitative real-time polymerase chain reaction (qPCR). In cord plasma, p53 and PGC-1α protein levels were measured using ELISA. Daily ambient PM2.5 concentrations during gestation were calculated using a spatial temporal interpolation model. Distributed lag models (DLMs) were applied to assess the association between prenatal PM2.5 exposure and each molecular marker. Mediation analysis was performed to test for underlying mechanisms. Results: A 5 µg/m3 increment in PM2.5 exposure was associated with −11.23 % (95 % CI: −17.36 % to −4.65 %, p = 0.0012) and −7.34 % (95 % CI: −11.56 % to −2.92 %, p = 0.0014) lower placental TL during the entire pregnancy and second trimester respectively, and with −12.96 % (95 % CI: −18.84 % to −6.64 %, p < 0.001) lower placental mtDNAc during the third trimester. Furthermore, PM2.5 exposure was associated with a 12.42 % (95 % CI: −1.07 % to 27.74 %, p = 0.059) higher cord plasma p53 protein level and a −3.69 % (95 % CI: −6.97 % to −0.31 %, p = 0.033) lower cord plasma PGC-1α protein level during the third trimester. Placental TL mediated 65 % of the negative and 17 % of the positive association between PM2.5 and placental mtDNAc and cord plasma p53 protein levels, respectively. Conclusion: Ambient PM2.5 exposure during pregnancy is associated with markers of the core-axis of aging, with TL as a mediating factor. This study strengthens the hypothesis of the air pollution induced core-axis of aging, and may unravel a possible underlying mediating mechanism in an early-life epidemiological context.http://www.sciencedirect.com/science/article/pii/S0160412022006225Telomere lengthMitochondrial DNA contentp53PGC-1αParticulate matter
spellingShingle Charlotte Van Der Stukken
Tim S Nawrot
Congrong Wang
Wouter Lefebvre
Charlotte Vanpoucke
Michelle Plusquin
Harry A Roels
Bram G Janssen
Dries S. Martens
The association between ambient particulate matter exposure and the telomere–mitochondrial axis of aging in newborns
Environment International
Telomere length
Mitochondrial DNA content
p53
PGC-1α
Particulate matter
title The association between ambient particulate matter exposure and the telomere–mitochondrial axis of aging in newborns
title_full The association between ambient particulate matter exposure and the telomere–mitochondrial axis of aging in newborns
title_fullStr The association between ambient particulate matter exposure and the telomere–mitochondrial axis of aging in newborns
title_full_unstemmed The association between ambient particulate matter exposure and the telomere–mitochondrial axis of aging in newborns
title_short The association between ambient particulate matter exposure and the telomere–mitochondrial axis of aging in newborns
title_sort association between ambient particulate matter exposure and the telomere mitochondrial axis of aging in newborns
topic Telomere length
Mitochondrial DNA content
p53
PGC-1α
Particulate matter
url http://www.sciencedirect.com/science/article/pii/S0160412022006225
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