Marine pollutant exposures and human milk extracellular vesicle-microRNAs in a mother-infant cohort from the Faroe Islands.


Journal

Environment international
ISSN: 1873-6750
Titre abrégé: Environ Int
Pays: Netherlands
ID NLM: 7807270

Informations de publication

Date de publication:
01 2022
Historique:
received: 27 08 2021
revised: 29 10 2021
accepted: 15 11 2021
entrez: 7 1 2022
pubmed: 8 1 2022
medline: 11 1 2022
Statut: ppublish

Résumé

Early life exposures to marine contaminants can adversely impact child health but modes of action are unclear. Human milk contains extracellular vesicles (EVs) that can transport biologically relevant cargo from mother to infant, including microRNAs (miRNAs), and may partly mediate the effects of pollutants on child health. However, the role of marine pollutants on miRNA expression in milk EVs is unexplored. We isolated EV RNA from 333 milk samples collected between 2 and 74 days postpartum from a Faroese birth cohort born 1997-2000 and sequenced 2083 miRNAs using a targeted library preparation method. We quantified five perfluoroalkyl substances (PFAS), pesticide metabolite p,p'-dichlorodiphenyldichloroethylene (DDE), and the sum of three major polychlorinated biphenyls (ΣPCBs) in maternal serum at 34 weeks of gestation and maternal hair total mercury (Hg) at birth. We used negative binomial regressions to estimate associations between individual pollutants and 418 reliably expressed EV-miRNAs adjusted for potential confounders. We performed sparse principal components (PCs) analysis to derive the first four components of the EV-miRNA data and examined associations between pollutants and PCs using Bayesian kernel machine regression (BKMR). We observed no associations between pollutants and individual EV-miRNA expression after controlling the false discovery rate at 0.1. However, BKMR suggested that Hg was positively associated with PC1 and negatively associated with PC3, while ΣPCBs was negatively associated with PC3, and two PFAS were associated with PC4. Exploration of PC loadings followed by pathway analyses suggested that miRNAs in PC1 (miR-200b-3p, miR-664a-3p, miR-6738-5p, miR-429, miR-1236-5p, miR-4464, and miR-30b-5p) may be related to Hg neurotoxicity, while remaining PCs require further research. Our findings suggest that groups of milk EV-miRNAs may better serve as environmental biomarkers than individual miRNAs. Future studies are needed to elucidate the role of milk EV-miRNAs in child health following prenatal exposures.

Sections du résumé

BACKGROUND/AIMS
Early life exposures to marine contaminants can adversely impact child health but modes of action are unclear. Human milk contains extracellular vesicles (EVs) that can transport biologically relevant cargo from mother to infant, including microRNAs (miRNAs), and may partly mediate the effects of pollutants on child health. However, the role of marine pollutants on miRNA expression in milk EVs is unexplored.
METHODS
We isolated EV RNA from 333 milk samples collected between 2 and 74 days postpartum from a Faroese birth cohort born 1997-2000 and sequenced 2083 miRNAs using a targeted library preparation method. We quantified five perfluoroalkyl substances (PFAS), pesticide metabolite p,p'-dichlorodiphenyldichloroethylene (DDE), and the sum of three major polychlorinated biphenyls (ΣPCBs) in maternal serum at 34 weeks of gestation and maternal hair total mercury (Hg) at birth. We used negative binomial regressions to estimate associations between individual pollutants and 418 reliably expressed EV-miRNAs adjusted for potential confounders. We performed sparse principal components (PCs) analysis to derive the first four components of the EV-miRNA data and examined associations between pollutants and PCs using Bayesian kernel machine regression (BKMR).
RESULTS
We observed no associations between pollutants and individual EV-miRNA expression after controlling the false discovery rate at 0.1. However, BKMR suggested that Hg was positively associated with PC1 and negatively associated with PC3, while ΣPCBs was negatively associated with PC3, and two PFAS were associated with PC4. Exploration of PC loadings followed by pathway analyses suggested that miRNAs in PC1 (miR-200b-3p, miR-664a-3p, miR-6738-5p, miR-429, miR-1236-5p, miR-4464, and miR-30b-5p) may be related to Hg neurotoxicity, while remaining PCs require further research.
CONCLUSIONS
Our findings suggest that groups of milk EV-miRNAs may better serve as environmental biomarkers than individual miRNAs. Future studies are needed to elucidate the role of milk EV-miRNAs in child health following prenatal exposures.

Identifiants

pubmed: 34991248
pii: S0160-4120(21)00611-5
doi: 10.1016/j.envint.2021.106986
pmc: PMC8742869
mid: NIHMS1759571
pii:
doi:

Substances chimiques

Environmental Pollutants 0
MIRN1236 microRNA, human 0
MicroRNAs 0

Types de publication

Journal Article Research Support, N.I.H., Extramural Research Support, Non-U.S. Gov't Research Support, U.S. Gov't, Non-P.H.S.

Langues

eng

Sous-ensembles de citation

IM

Pagination

106986

Subventions

Organisme : NIEHS NIH HHS
ID : R21 ES027087
Pays : United States
Organisme : NIEHS NIH HHS
ID : T32 ES007142
Pays : United States
Organisme : NIEHS NIH HHS
ID : K99 ES030749
Pays : United States
Organisme : NIEHS NIH HHS
ID : P30 ES009089
Pays : United States
Organisme : NIEHS NIH HHS
ID : R21 ES029328
Pays : United States
Organisme : NIEHS NIH HHS
ID : R00 ES030749
Pays : United States

Informations de copyright

Copyright © 2021 The Authors. Published by Elsevier Ltd.. All rights reserved.

Références

Theranostics. 2021 Apr 3;11(12):5986-6005
pubmed: 33897894
Protein Sci. 2019 Nov;28(11):1947-1951
pubmed: 31441146
Elife. 2015 Aug 12;4:
pubmed: 26267216
Chemosphere. 2018 Mar;195:156-165
pubmed: 29268174
Bioinformatics. 2012 Mar 15;28(6):882-3
pubmed: 22257669
Nucleic Acids Res. 2015 Jul 1;43(W1):W460-6
pubmed: 25977294
J Nutr. 2014 Oct;144(10):1495-500
pubmed: 25122645
Nutrients. 2021 Mar 27;13(4):
pubmed: 33801634
Environ Health Perspect. 1994 Jan;102(1):74-7
pubmed: 9719671
Nucleic Acids Res. 2018 Jan 4;46(D1):D239-D245
pubmed: 29156006
Environ Epidemiol. 2019 Oct;3(5):
pubmed: 32051926
Neuroscience. 2017 Jan 26;341:112-153
pubmed: 27889578
BMC Bioinformatics. 2010 Feb 18;11:94
pubmed: 20167110
Biostatistics. 2015 Jul;16(3):493-508
pubmed: 25532525
Adv Nutr. 2018 May 1;9(suppl_1):278S-294S
pubmed: 29846526
Toxicol In Vitro. 2020 Jun;65:104787
pubmed: 32004541
J Appl Toxicol. 2020 Sep;40(9):1166-1182
pubmed: 32125006
J Transl Med. 2019 Jul 22;17(1):236
pubmed: 31331349
Nat Cell Biol. 2011 Apr;13(4):423-33
pubmed: 21423178
Food Chem Toxicol. 2021 Jan;147:111918
pubmed: 33301842
Front Mol Neurosci. 2014 Apr 23;7:28
pubmed: 24795562
Environ Health Perspect. 2015 Oct;123(10):1015-21
pubmed: 25910281
Environ Health. 2005 Jul 14;4:12
pubmed: 16014177
Adv Exp Med Biol. 2020;1252:3-7
pubmed: 32816256
Environ Int. 2020 Mar;136:105446
pubmed: 31926437
Sci Rep. 2021 Mar 12;11(1):5840
pubmed: 33712635
Environ Res. 1995 Oct;71(1):29-38
pubmed: 8757236
Am J Epidemiol. 1999 Aug 1;150(3):301-5
pubmed: 10430235
Cell Death Dis. 2019 May 21;10(6):399
pubmed: 31113939
Am J Geriatr Psychiatry. 2016 Oct;24(10):903-12
pubmed: 27591915
Cell Rep. 2018 Oct 30;25(5):1346-1358
pubmed: 30380423
J Extracell Vesicles. 2012 Apr 16;1:
pubmed: 24009879
Cell. 2017 Mar 9;168(6):960-976
pubmed: 28283069
Nutrients. 2019 Oct 28;11(11):
pubmed: 31661820
Nucleic Acids Res. 2021 Jan 8;49(D1):D545-D551
pubmed: 33125081
Epigenetics. 2021 Apr;16(4):389-404
pubmed: 32777999
Bioinformatics. 2010 Jan 1;26(1):139-40
pubmed: 19910308
Nat Cell Biol. 2007 Jun;9(6):654-9
pubmed: 17486113
Pediatrics. 2005 Feb;115(2):496-506
pubmed: 15687461
Cortex. 2016 Jan;74:358-69
pubmed: 26109549
Toxicol Appl Pharmacol. 2001 Jul 1;174(1):49-59
pubmed: 11437648
J Thorac Dis. 2016 May;8(5):833-41
pubmed: 27162656
Front Genet. 2018 Mar 27;9:92
pubmed: 29636770
PLoS One. 2016 Apr 13;11(4):e0152610
pubmed: 27074017
Environ Health Perspect. 2011 Oct;119(10):1429-35
pubmed: 21719373
Sci Rep. 2016 Feb 08;6:20680
pubmed: 26854194
Cell. 2005 Jan 14;120(1):15-20
pubmed: 15652477
Bioinformatics. 2012 Mar 15;28(6):771-6
pubmed: 22285563
Environ Health. 2013 Jan 07;12:3
pubmed: 23289875
Environ Sci Technol. 2012 Sep 4;46(17):9274-81
pubmed: 22862179
Environ Sci Technol. 2015 Sep 1;49(17):10466-73
pubmed: 26291735
Arch Toxicol. 2018 Jan;92(1):513-527
pubmed: 28821999
Chemosphere. 2020 Apr;244:125400
pubmed: 31809933
Neurotoxicol Teratol. 2012 Jul;34(4):466-72
pubmed: 22705177
Mol Cell Biochem. 2014 Jun;391(1-2):117-25
pubmed: 24526524
Reprod Toxicol. 2017 Mar;68:164-170
pubmed: 27421579
Nucleic Acids Res. 2000 Jan 1;28(1):27-30
pubmed: 10592173
Front Cell Dev Biol. 2021 Jun 25;9:693534
pubmed: 34249944
Am J Ind Med. 2007 Oct;50(10):712-9
pubmed: 17492658
Cell Physiol Biochem. 2015;36(2):585-98
pubmed: 25997722
Cell. 2004 Jan 23;116(2):281-97
pubmed: 14744438
Nucleic Acids Res. 2013 Jul;41(Web Server issue):W169-73
pubmed: 23680784
Sci Rep. 2016 Oct 21;6:35729
pubmed: 27767083
Arch Environ Contam Toxicol. 2014 Jul;67(1):9-20
pubmed: 24435476
Environ Health Prev Med. 2013 May;18(3):205-14
pubmed: 23054994
Reprod Toxicol. 2017 Mar;68:145-153
pubmed: 27496715
Environ Res. 2021 Apr;195:110825
pubmed: 33545124
Environ Health Perspect. 2017 Jun 26;125(6):067015
pubmed: 28669934
Sci Rep. 2017 Aug 23;7(1):9262
pubmed: 28835693

Auteurs

Allison Kupsco (A)

Department of Environmental Health Sciences, Columbia University Mailman School of Public Health, New York, NY 10023, United States. Electronic address: ak4181@cumc.columbia.edu.

Jenny Jyoung Lee (JJ)

Department of Biostatistics, Harvard T.H Chan School of Public Health, Boston, MA, United States.

Diddier Prada (D)

Department of Environmental Health Sciences, Columbia University Mailman School of Public Health, New York, NY 10023, United States; Instituto Nacional de Cancerología, San Fernando 22, Colonia Seccion XVI, Tlalpan, Mexico City 14080, Mexico.

Damaskini Valvi (D)

Department of Environmental Medicine and Public Health, Icahn School of Medicine at Mount Sinai, New York, NY 10029, United States.

Lisa Hu (L)

Department of Environmental Health Sciences, Columbia University Mailman School of Public Health, New York, NY 10023, United States.

Maria Skaalum Petersen (MS)

Department of Occupational Medicine and Public Health, The Faroese Hospital System, Tórshavn, Faroe Islands; Center of Health Science, University of The Faroe Islands, Tórshavn, Faroe Islands.

Brent A Coull (BA)

Department of Biostatistics, Harvard T.H Chan School of Public Health, Boston, MA, United States; Department of Environmental Health, Harvard T.H. Chan School of Public Health, Boston, MA, United States.

Pal Weihe (P)

Department of Occupational Medicine and Public Health, The Faroese Hospital System, Tórshavn, Faroe Islands; Center of Health Science, University of The Faroe Islands, Tórshavn, Faroe Islands.

Philippe Grandjean (P)

Department of Environmental Health, Harvard T.H. Chan School of Public Health, Boston, MA, United States; Department of Environmental Medicine, University of Southern Denmark, Odense C, Denmark.

Andrea A Baccarelli (AA)

Department of Environmental Health Sciences, Columbia University Mailman School of Public Health, New York, NY 10023, United States.

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