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Cited by 229Genetic Syndromes and ImprintingBirth, Development, and HealthEpigenetics and DNA Methylation

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Sex- and Diet-Specific Changes of Imprinted Gene Expression and DNA Methylation in Mouse Placenta under a High-Fat Diet

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Gallou-Kabani, Catherine, Gabory, Anne, Tost, Jörg, Karimi, Mohsen, Mayeur, Sylvain, Lesage, Jean, Boudadi, Elsa, Gross, Marie-Sylvie, Taurelle, Julien, Vigé, Alexandre, Breton, Christophe, Reusens, Brigitte, Remacle, Claude, Vieau, Didier, Ekström, Tomas J., Jais, Jean-Philippe, Junien, Claudine·2010·PLoS ONE
DOI 10.1371/journal.pone.0014398PMC PMC3006175
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Abstract

BACKGROUND: Changes in imprinted gene dosage in the placenta may compromise the prenatal control of nutritional resources. Indeed monoallelic behaviour and sensitivity to changes in regional epigenetic state render imprinted genes both vulnerable and adaptable. METHODS AND FINDINGS: We investigated whether a high-fat diet (HFD) during pregnancy modified the expression of imprinted genes and local and global DNA methylation patterns in the placenta. Pregnant mice were fed a HFD or a control diet (CD) during the first 15 days of gestation. We compared gene expression patterns in total placenta homogenates, for male and female offspring, by the RT-qPCR analysis of 20 imprinted genes. Sexual dimorphism and sensitivity to diet were observed for nine genes from four clusters on chromosomes 6, 7, 12 and 17. As assessed by in situ hybridization, these changes were not due to variation in the proportions of the placental layers. Bisulphite-sequencing analysis of 30 CpGs within the differentially methylated region (DMR) of the chromosome 17 cluster revealed sex- and diet-specific differential methylation of individual CpGs in two conspicuous subregions. Bioinformatic analysis suggested that these differentially methylated CpGs might lie within recognition elements or binding sites for transcription factors or factors involved in chromatin remodelling. Placental global DNA methylation, as assessed by the LUMA technique, was also sexually dimorphic on the CD, with lower methylation levels in male than in female placentae. The HFD led to global DNA hypomethylation only in female placenta. Bisulphite pyrosequencing showed that neither B1 nor LINE repetitive elements could account for these differences in DNA methylation. CONCLUSIONS: A HFD during gestation triggers sex-specific epigenetic alterations within CpG and throughout the genome, together with the deregulation of clusters of imprinted genes important in the control of many cellular, metabolic and physiological functions potentially involved in adaptation and/or evolution. These findings highlight the importance of studying both sexes in epidemiological protocols and dietary interventions.

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Figures

Figure 1 Linear discriminant supervised clustering analysis. The five genes mapping to chromosome 17 for which RT-qPCR was carried out (Slc22a1, Slc22a2, Slc22a3, Igf2r, Air) were studied by a linear discriminant approach. (A) Pooled results from individuals were projected onto the first two discriminant axes, which accounted for 99.6% of the inter-class variability. Inertia ellipses represent intra-class variability for each group. Discrimination power increases with the compactness and distance of the ellipses. (B) The correlation circle indicates the contribution of the five genes to the discriminant axes.
Figure 1 Linear discriminant supervised clustering analysis. The five genes mapping to chromosome 17 for which RT-qPCR was carried out (Slc22a1, Slc22a2, Slc22a3, Igf2r, Air) were studied by a linear discriminant approach. (A) Pooled results from individuals were projected onto the first two discriminant axes, which accounted for 99.6% of the inter-class variability. Inertia ellipses represent intra-class variability for each group. Discrimination power increases with the compactness and distance of the ellipses. (B) The correlation circle indicates the contribution of the five genes to the discriminant axes.CC BY · PubMed Central
Figure 2 Analysis of gene expression by in situ hybridization. Detection by in situ hybridisation of Slc22a3 (A), Dlk1 (B) and Rtl1 (C) in of the placentae of female (F) or male (M) mouse embryos from mothers fed a control (CD) or high fat (HFD) diet. No difference in the distribution of these RNAs was observed, all of which were restricted to the labyrinth layer. The histograms (D) show the proportion of the labyrinth, this area being similar between the four groups.
Figure 2 Analysis of gene expression by in situ hybridization. Detection by in situ hybridisation of Slc22a3 (A), Dlk1 (B) and Rtl1 (C) in of the placentae of female (F) or male (M) mouse embryos from mothers fed a control (CD) or high fat (HFD) diet. No difference in the distribution of these RNAs was observed, all of which were restricted to the labyrinth layer. The histograms (D) show the proportion of the labyrinth, this area being similar between the four groups.CC BY · PubMed Central
Figure 3 Schematic diagram of the Igf2r region on mouse chromosome 17. (A), Box plot representing global methylation (B), specific CpG2 (C), sexual dimorphism under HFD (D), and sexual dimorphism under CD (E) obtained by bisulphite sequencing analysis of the DMR Igf2r encompassing 30 CpGs. The 30 CpGs are underlined. CpGs displaying sex-specific methylation under HFD and CD are shown in bold. Differences between methylation profiles were analysed by Mann-Whitney tests (p<0.05). F = female, M = male.
Figure 3 Schematic diagram of the Igf2r region on mouse chromosome 17. (A), Box plot representing global methylation (B), specific CpG2 (C), sexual dimorphism under HFD (D), and sexual dimorphism under CD (E) obtained by bisulphite sequencing analysis of the DMR Igf2r encompassing 30 CpGs. The 30 CpGs are underlined. CpGs displaying sex-specific methylation under HFD and CD are shown in bold. Differences between methylation profiles were analysed by Mann-Whitney tests (p<0.05). F = female, M = male.CC BY · PubMed Central
Figure 4 Box plot representing global methylation of the genome. Results obtained by LUMA, in five different tissues from six-month-old mice on the CD (liver, muscle, kidney, testis and placenta) at E15.5 (A), and from the placentae of female and male foetuses from mothers fed the CD or the HFD (B). Differences between methylation profiles were analysed by Mann-Whitney tests (p<0.05). Completely unmethylated DNA would have an HpaII/MspI ratio of 1.0, whereas 100% methylated DNA would have an HpaII/MspI ratio close to zero [121].
Figure 4 Box plot representing global methylation of the genome. Results obtained by LUMA, in five different tissues from six-month-old mice on the CD (liver, muscle, kidney, testis and placenta) at E15.5 (A), and from the placentae of female and male foetuses from mothers fed the CD or the HFD (B). Differences between methylation profiles were analysed by Mann-Whitney tests (p<0.05). Completely unmethylated DNA would have an HpaII/MspI ratio of 1.0, whereas 100% methylated DNA would have an HpaII/MspI ratio close to zero [121].CC BY · PubMed Central

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Authors
Gallou-Kabani, C., Gabory, A., Tost, J., Karimi, M., Mayeur, S., Lesage, J., Boudadi, E., Gross, M.-S., Taurelle, J., Vigé, A., Breton, C., Reusens, B., Remacle, C., Vieau, D., Ekström, T. J., Jais, J.-P., & Junien, C.
Affiliations
  • Hôpital Necker-Enfants Malades (FR)
  • Commissariat à l'Énergie Atomique et aux Énergies Alternatives (FR)
  • Karolinska Institutet (SE)
  • Université de Lille (FR)
  • UCLouvain (BE)
Corresponding author
Junien, Claudine
ORCID
Venue
PLoS ONE
Publisher
Public Library of Science (PLoS)
Published
2010-12-21
Volume
5
Issue
12
Pages
e14398
ISSN
1932-6203 (ISSN-L)
DOI
10.1371/journal.pone.0014398
PMC
PMC3006175
OpenAlex
W2157038986
Cited by
229
References
124
Citations by year
2026: 1 · 2025: 9 · 2024: 5 · 2023: 5 · 2022: 10 · 2021: 11 · 2020: 16 · 2019: 13 · 2018: 27 · 2017: 22 · 2016: 14 · 2015: 24 · 2014: 12 · 2013: 31 · 2012: 23
FWCI
10.80
Type
journal article
Language
en
Open access
Licence
Locations
  • PLoS ONE (publishedVersion, cc-by)
  • PubMed Central (publishedVersion, cc-by)
  • PubMed (publishedVersion)
  • HAL (submittedVersion, other-oa)
  • Digital Access to Libraries (submittedVersion, other-oa)
  • DOAJ (DOAJ: Directory of Open Access Journals) (submittedVersion, cc-by-sa)
Funders
  • Agence Nationale de la Recherche (ANR-06-PNRA-0022)
  • Institut National de la Santé et de la Recherche Médicale
  • Cancerfonden
  • Institut National de la Recherche Agronomique
Topics
  • Life Sciences › Biochemistry, Genetics and Molecular Biology › Genetics › Genetic Syndromes and Imprinting
  • Health Sciences › Medicine › Pediatrics, Perinatology and Child Health › Birth, Development, and Health
  • Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Epigenetics and DNA Methylation
Keywords
genomic imprinting, imprinted gene expression, placenta, high-fat diet, maternal diet, sex differences, DNA methylation, differentially methylated regions, global DNA hypomethylation, monoallelic expression, epigenetic inheritance
MeSH terms
Alleles, Animals, Animal Feed, Dietary Fats, Female, Gene Expression Regulation, Male, Placenta, Pregnancy, Pregnancy, Animal, Sex Factors, Genomic Imprinting, Gene Dosage, DNA Methylation, Epigenesis, Genetic, Mice

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