DNA methylation signatures to predict the cervicovaginal microbiome status.


Journal

Clinical epigenetics
ISSN: 1868-7083
Titre abrégé: Clin Epigenetics
Pays: Germany
ID NLM: 101516977

Informations de publication

Date de publication:
23 11 2020
Historique:
received: 29 07 2020
accepted: 03 11 2020
entrez: 24 11 2020
pubmed: 25 11 2020
medline: 27 10 2021
Statut: epublish

Résumé

The composition of the microbiome plays an important role in human health and disease. Whether there is a direct association between the cervicovaginal microbiome and the host's epigenome is largely unexplored. Here we analyzed a total of 448 cervicovaginal smear samples and studied both the DNA methylome of the host and the microbiome using the Illumina EPIC array and next-generation sequencing, respectively. We found that those CpGs that are hypo-methylated in samples with non-lactobacilli (O-type) dominating communities are strongly associated with gastrointestinal differentiation and that a signature consisting of 819 CpGs was able to discriminate lactobacilli-dominating (L-type) from O-type samples with an area under the receiver operator characteristic curve (AUC) of 0.84 (95% CI = 0.77-0.90) in an independent validation set. The performance found in samples with more than 50% epithelial cells was further improved (AUC 0.87) and in women younger than 50 years of age was even higher (AUC 0.91). In a subset of 96 women, the buccal but not the blood cell DNA showed the same trend as the cervicovaginal samples in discriminating women with L- from O-type cervicovaginal communities. These findings strongly support the view that the epithelial epigenome plays an essential role in hosting specific microbial communities.

Sections du résumé

BACKGROUND
The composition of the microbiome plays an important role in human health and disease. Whether there is a direct association between the cervicovaginal microbiome and the host's epigenome is largely unexplored.
RESULTS
Here we analyzed a total of 448 cervicovaginal smear samples and studied both the DNA methylome of the host and the microbiome using the Illumina EPIC array and next-generation sequencing, respectively. We found that those CpGs that are hypo-methylated in samples with non-lactobacilli (O-type) dominating communities are strongly associated with gastrointestinal differentiation and that a signature consisting of 819 CpGs was able to discriminate lactobacilli-dominating (L-type) from O-type samples with an area under the receiver operator characteristic curve (AUC) of 0.84 (95% CI = 0.77-0.90) in an independent validation set. The performance found in samples with more than 50% epithelial cells was further improved (AUC 0.87) and in women younger than 50 years of age was even higher (AUC 0.91). In a subset of 96 women, the buccal but not the blood cell DNA showed the same trend as the cervicovaginal samples in discriminating women with L- from O-type cervicovaginal communities.
CONCLUSIONS
These findings strongly support the view that the epithelial epigenome plays an essential role in hosting specific microbial communities.

Identifiants

pubmed: 33228781
doi: 10.1186/s13148-020-00966-7
pii: 10.1186/s13148-020-00966-7
pmc: PMC7686703
doi:

Types de publication

Journal Article Multicenter Study Research Support, Non-U.S. Gov't

Langues

eng

Sous-ensembles de citation

IM

Pagination

180

Références

Nat Med. 2019 Oct;25(10):1500-1504
pubmed: 31591599
Nat Commun. 2016 Jan 29;7:10478
pubmed: 26823093
Nat Methods. 2018 Dec;15(12):1059-1066
pubmed: 30504870
N Engl J Med. 2020 May 14;382(20):1906-1915
pubmed: 32402161
PLoS One. 2009 Dec 18;4(12):e8274
pubmed: 20019873
Clin Microbiol Infect. 2016 Feb;22(2):178.e1-178.e9
pubmed: 26482265
J Transl Med. 2019 Jul 15;17(1):225
pubmed: 31307469
Lancet Oncol. 2019 Aug;20(8):1171-1182
pubmed: 31300207
PLoS One. 2014 Aug 22;9(8):e105998
pubmed: 25148517
J Eukaryot Microbiol. 2015 May-Jun;62(3):338-45
pubmed: 25312509
Lancet. 2019 Aug 3;394(10196):420-431
pubmed: 31379333
J Natl Cancer Inst. 2014 Jun 28;106(7):
pubmed: 24973978
Epigenomics. 2018 Jul;10(7):925-940
pubmed: 29693419
J Mol Biol. 1990 Oct 5;215(3):403-10
pubmed: 2231712
Genome Res. 2010 Apr;20(4):440-6
pubmed: 20219944
J Infect Dis. 2014 Dec 1;210(11):1723-33
pubmed: 24943724
Bioinformatics. 2006 Jul 1;22(13):1658-9
pubmed: 16731699
JAMA Oncol. 2015 Jul;1(4):476-85
pubmed: 26181258
Front Microbiol. 2019 Feb 14;10:193
pubmed: 30837959
Int J Cancer. 2012 Jun 1;130(11):2495-504
pubmed: 21792894
Nucleic Acids Res. 2012 Jan;40(Database issue):D136-43
pubmed: 22139910
BMC Bioinformatics. 2016 Apr 22;17:178
pubmed: 27103033
Nature. 2017 Jan 5;541(7635):81-86
pubmed: 28002404
Bioinformatics. 2011 Nov 1;27(21):2957-63
pubmed: 21903629
Nature. 2019 Jul;571(7766):489-499
pubmed: 31341302
Nat Commun. 2016 May 24;7:11620
pubmed: 27216078
Proc Natl Acad Sci U S A. 2011 Mar 15;108 Suppl 1:4680-7
pubmed: 20534435
Nat Microbiol. 2020 Apr;5(4):610-619
pubmed: 32015497
N Engl J Med. 2018 Jun 28;378(26):2535-2536
pubmed: 29860912
Nature. 2013 Dec 5;504(7478):153-7
pubmed: 24185009
J Physiol. 2017 Jan 15;595(2):451-463
pubmed: 27373840
Lab Invest. 2012 Jun;92(6):802-11
pubmed: 22488153
Nucleic Acids Res. 2009 Jan;37(Database issue):D141-5
pubmed: 19004872
Lancet Oncol. 2013 Nov;14(12):1226-32
pubmed: 24140203
Nat Rev Clin Oncol. 2018 May;15(5):292-309
pubmed: 29485132
Nucleic Acids Res. 2017 Feb 28;45(4):e22
pubmed: 27924034
Bioinformatics. 2011 Aug 15;27(16):2194-200
pubmed: 21700674
Nature. 2018 Mar 8;555(7695):210-215
pubmed: 29489753

Auteurs

Nuno R Nené (NR)

Department of Women's Cancer, EGA Institute for Women's Health, University College London, London, UK.
Department of Mathematics, University College London, London, UK.

James Barrett (J)

Department of Women's Cancer, EGA Institute for Women's Health, University College London, London, UK.
European Translational Oncology Prevention and Screening (EUTOPS) Institute, 6060, Hall in Tirol, Austria.
Research Institute for Biomedical Aging Research, Universität Innsbruck, 6020, Innsbruck, Austria.

Allison Jones (A)

Department of Women's Cancer, EGA Institute for Women's Health, University College London, London, UK.

Iona Evans (I)

Department of Women's Cancer, EGA Institute for Women's Health, University College London, London, UK.

Daniel Reisel (D)

Department of Women's Cancer, EGA Institute for Women's Health, University College London, London, UK.

John F Timms (JF)

Department of Women's Cancer, EGA Institute for Women's Health, University College London, London, UK.

Tobias Paprotka (T)

Eurofins Genomics Europe Sequencing, Constance, Germany.

Andreas Leimbach (A)

Eurofins Genomics Europe Sequencing, Constance, Germany.

Dorella Franchi (D)

Europeo Di Oncologia, IRCCS, Milan, Italy.

Nicoletta Colombo (N)

Europeo Di Oncologia, IRCCS, Milan, Italy.
University of Milano-Bicocca, Milan, Italy.

Line Bjørge (L)

Department of Obstetrics and Gynecology, Haukeland University Hospital, Bergen, Norway.
Centre for Cancer Biomarkers, Department of Clinical Science, CCBIO, University of Bergen, Bergen, Norway.

Michal Zikan (M)

Hospital Na Bulovce, Prague, Czech Republic.
Department of Obstetrics and Gynecology, General University Hospital in Prague, First Faculty of Medicine, Charles University, Prague, Czech Republic.

David Cibula (D)

Department of Obstetrics and Gynecology, General University Hospital in Prague, First Faculty of Medicine, Charles University, Prague, Czech Republic.

Martin Widschwendter (M)

Department of Women's Cancer, EGA Institute for Women's Health, University College London, London, UK. m.widschwendter@ucl.ac.uk.
European Translational Oncology Prevention and Screening (EUTOPS) Institute, 6060, Hall in Tirol, Austria. m.widschwendter@ucl.ac.uk.
Research Institute for Biomedical Aging Research, Universität Innsbruck, 6020, Innsbruck, Austria. m.widschwendter@ucl.ac.uk.

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