Maternal diet-induced obesity during pregnancy alters lipid supply to mouse E18.5 fetuses and changes the cardiac tissue lipidome in a sex-dependent manner

  1. Lucas C Pantaleão  Is a corresponding author
  2. Isabella Inzani  Is a corresponding author
  3. Samuel Furse
  4. Elena Loche
  5. Antonia Hufnagel
  6. Thomas Ashmore
  7. Heather L Blackmore
  8. Benjamin Jenkins
  9. Asha A M Carpenter
  10. Ania Wilczynska
  11. Martin Bushell
  12. Albert Koulman
  13. Denise S Fernandez-Twinn
  14. Susan E Ozanne  Is a corresponding author
  1. Wellcome-MRC Institute of Metabolic Science and Medical Research Council Metabolic Diseases Unit, University of Cambridge, Addenbrooke’s Hospital, United Kingdom
  2. Core Metabolomics and Lipidomics Laboratory, Wellcome-MRC Institute of Metabolic Science, University of Cambridge, Addenbrooke’s Treatment Centre, United Kingdom
  3. Cancer Research UK Beatson Institute, United Kingdom
  4. Institute of Cancer Sciences, University of Glasgow, United Kingdom
6 figures, 3 tables and 4 additional files

Figures

Figure 1 with 2 supplements
Fetal characteristics at gestational day 18.5.

(A) Body weight of male and female fetuses from healthy control (CTL) and obese (OB) mouse dams at gestational day 18.5. Male CTL n = 6, male OB n = 6, female CTL n = 7, female OB n = 6. (B–C) Heart weight and heart weight/litter average body weight ratio of male and female fetuses from CTL and OB dams at gestational day 18.5. Male CTL n = 10, male OB n = 10, female CTL n = 12, female OB n = 12. (D) Histological sections stained with eosin of male and female fetuses from CTL and OB dams at gestational day 18.5 used in cardiac stereology (see also Figure 1—figure supplement 1). Scale bar indicates 500 µm. (E–H) Left and right ventricular wall volume and ventricular wall volume/body weight ratio of male and female fetuses from healthy control (CTL) and obese (OB) mouse dams at gestational day 18.5. Male CTL n = 4, male OB n = 6, female CTL n = 4, female OB n = 5. (I) Boxplot showing median and quartiles of cardiomyocyte area distribution in male and female fetuses from CTL and OB dams at gestational day 18.5. Under the boxplot a beeswarm plot shows individual area of each cardiomyocyte analysed. Male CTL n = 6, male OB n = 7, female CTL n = 6, female OB n = 6 (see Figure 1—figure supplement 2 for a representative image of stained cardiomyocytes). (J) Nuclear PCNA-positive cells percentage in hearts of male and female fetuses from CTL and OB dams at gestational day 18.5. Male CTL n = 6, male OB n = 5, female CTL n = 3, female OB n = 5. In panels A-H and J, p-values were calculated by Student t-test. In panel I, p-values were calculated using linear mixed-effects model followed by Tukey’s post-hoc test.

Figure 1—source data 1

Sex-specific fetal body weight at E18.5 (Figure 1A).

https://cdn.elifesciences.org/articles/69078/elife-69078-fig1-data1-v3.csv
Figure 1—source data 2

Fetal heart weight at E18.5 (Figure 1B).

https://cdn.elifesciences.org/articles/69078/elife-69078-fig1-data2-v3.csv
Figure 1—source data 3

Fetal heart weight at E18.5 relative to the average litter weight (Figure 1C).

https://cdn.elifesciences.org/articles/69078/elife-69078-fig1-data3-v3.csv
Figure 1—source data 4

Left ventricle wall volume (Figure 1E).

https://cdn.elifesciences.org/articles/69078/elife-69078-fig1-data4-v3.csv
Figure 1—source data 5

Right ventricle wall volume (Figure 1F).

https://cdn.elifesciences.org/articles/69078/elife-69078-fig1-data5-v3.csv
Figure 1—source data 6

Relative left ventricle wall volume (Figure 1G).

https://cdn.elifesciences.org/articles/69078/elife-69078-fig1-data6-v3.csv
Figure 1—source data 7

Relative right ventricle wall volume (Figure 1H).

https://cdn.elifesciences.org/articles/69078/elife-69078-fig1-data7-v3.csv
Figure 1—source data 8

Fetal cardiomyocyte area (Figure 1I).

https://cdn.elifesciences.org/articles/69078/elife-69078-fig1-data8-v3.csv
Figure 1—source data 9

% Nuclear PCNA-positive cardiac cells (Figure 1J).

https://cdn.elifesciences.org/articles/69078/elife-69078-fig1-data9-v3.csv
Figure 1—figure supplement 1
Stereological analysis of the gestational day 18.5 fetal heart.

(A–B) Representative images of fetal torso prior (A) and after (B) blinded identification of cardiac structures by a trained histologist.

Figure 1—figure supplement 2
Representative image of immunofluorescence identifying cardiomyocytes using a mAb anti-Cardiac Troponin I IgG followed by incubation with an Alexa Fluor 488-conjugated secondary IgG.
Figure 2 with 2 supplements
Maternal and fetal serum lipidome measured by direct infusion mass spectrometry.

(A–B) Relative changes in serum lipid classes abundance in obese dams (A) and in obese fetuses (B). Values are mean + SE. *p < 0.05 calculated by Student t-test or Mann-Whitney test. (C) Influence of maternal diet and sex on fetal serum lipid classes abundance as calculated by factorial ANOVA. (D) Regulation of maternal and fetal serum lipid species ranked according to their abundance. Coloured dots represent statistically regulated species as calculated by univariate Student t-test (p < 0.05) and PLS-DA VIP (vip score >1) in maternal or fetal OB serum compared to CTL. (E–G) Serum levels of regulated lipids from obese dams (E) and from male (F) and female (G) fetuses of obese dams at gestational day 18.5. Each dot represents a result from one obese fetus' serum relative to the average of results for individual lipids in the control group (straight line). Dam CTL n = 9, dam OB n = 6, male fetuses CTL n = 10, male fetuses OB n = 8, female fetuses CTL n = 10, female fetuses OB n = 7; * p < 0.05, ** p < 0.01, *** p < 0.001 calculated by Student t-test. In figures A-C: PE, phosphatidylethanolamines/odd chain phosphatidylcholines; PC, phosphatidylcholines/odd-chain phosphatidylethanolamines; PG, phosphatidylglycerols; PS, phosphatidylserines; PA, phosphatidic acids; PI, phosphatidylinositols; TG, monoglycerides, diglycerides and triglycerides; SM, sphingomyelins; CE, cholesteryl esters; Cer, ceramides; PL, phospholipids. In figures D-G, other isobaric lipids can contribute to these signals (Supplementary file 1). See also Figure 2—figure supplement 1 and Figure 2—figure supplement 2.

Figure 2—source data 1

Relative lipid classes abundance in maternal serum (Figure 2A).

https://cdn.elifesciences.org/articles/69078/elife-69078-fig2-data1-v3.csv
Figure 2—source data 2

Relative lipid classes abundance in fetal serum (Figure 2B).

https://cdn.elifesciences.org/articles/69078/elife-69078-fig2-data2-v3.csv
Figure 2—source data 3

Direct infusion high-resolution mass spectrometry of the serum (positive mode only) (Figure 2D–G).

Scaled raw data and statistical significance.

https://cdn.elifesciences.org/articles/69078/elife-69078-fig2-data3-v3.csv
Figure 2—figure supplement 1
Multivariate analysis of the maternal and fetal serum lipid profiles.

(A) PCA plots showing the PC1 and PC2 scores for individual dam and fetal serum lipidomes at gestational day 18.5. (B–C) PCA plots showing the PC1 and PC2 scores for individual dam (B) or fetal (C) serum lipidomes.

Figure 2—figure supplement 2
Serum levels of lipid groups.

(A) Heatmap showing lipid classes serum levels in male and female E18.5 fetuses. (B–C) Pearson’s correlation between individual lipid species in maternal serum and male (B) and female (C) fetal serum at gestational day 18.5. Blue dots represent positively correlated lipid species between maternal and fetal serum deemed statistically significant (p < 0.05). Red dots represent negatively correlated lipid species between maternal and fetal serum deemed statistically significant (p < 0.05). (D) Relative abundance of different lipid classes in maternal and fetal control serum.

Figure 3 with 2 supplements
Fatty acid composition of serum phospholipids measured by direct infusion mass spectrometry using in-source CID fragmentation.

(A) Grouped saturated, monounsaturated and polyunsaturated fatty acids content in maternal, male and female fetal serum at gestational day 18.5. Values are mean + SE. (B) Regulation of maternal and fetal serum fatty acids. Coloured dots represent statistically regulated fatty acids as calculated by univariate Student t-test or Mann-Whitney test (p < 0.05) in maternal or fetal OB serum compared to CTL. (C) Pearson’s correlation between maternal serum fatty acids and the same fatty acids detected in the fetal serum. Blue and red dots represent species with significant positive and negative association (p < 0.05). Dam CTL n = 8, dam OB n = 6, male fetuses CTL n = 10, male fetuses OB n = 8, female fetuses CTL n = 8, female fetuses OB n = 6. See also Figure 3—figure supplement 1 and Figure 3—figure supplement 2.

Figure 3—source data 1

Relative fatty acid classes abundance in maternal and fetal serum (Figure 3A).

https://cdn.elifesciences.org/articles/69078/elife-69078-fig3-data1-v3.csv
Figure 3—source data 2

Fatty acids abundance obtained by direct infusion high-resolution mass spectrometry of the serum (negative mode) (Figure 3B).

Scaled raw data and statistical significance.

https://cdn.elifesciences.org/articles/69078/elife-69078-fig3-data2-v3.csv
Figure 3—figure supplement 1
Radar plots showing regulation of fatty acids statistically changed in the serum or in the heart of fetuses from obese dams in different compartments.

Gray-shaded area indicates negative changes.

Figure 3—figure supplement 2
Correlation matrices showing Pearson’s correlation between cardiac fatty acids in dams and fetuses.

Fatty acids grouped following Euclidian clusterisation.

Figure 4 with 2 supplements
Maternal and fetal cardiac lipidome.

(A–B) Relative changes in cardiac lipid classes in male (A) and female (B) fetuses from obese dams. Values are mean + SE. *p < 0.05 calculated by Student t-test or Mann-Whitney test. (C–D) PCA plots showing the PC1 and PC2 scores for individual male (C) and female (D) cardiac lipidomes. (E) Regulation of fetal cardiac lipid species ranked according to their abundance. Coloured dots represent statistically regulated species as calculated by univariate Student t-test (p < 0.05) and PLS-DA VIP (vip score >1) in fetal OB hearts compared to CTL. (F–G) Cardiac levels of regulated lipids from male (F) and female (G) fetuses of obese dams at gestational day 18.5. Each dot represents a result from one obese heart, relative to the average of results for individual lipids in the control group (straight line). Male fetuses CTL n = 6, male fetuses OB n = 7, female fetuses CTL n = 7, female fetuses OB n = 6. * p < 0.05, ** p < 0.01, *** p < 0.001 calculated by Student t-test. (H) Cumulative frequency of cardiac lipid species according to the log2 of the fold change in abundance between male and female fetuses from obese and control dams. (I) Grouped saturated, monounsaturated and polyunsaturated fatty acids content in male and female fetal hearts at gestational day 18.5. (J) Regulation of maternal and fetal serum fatty acids. Coloured dots represent statistically regulated fatty acids as calculated by univariate Student t-test or Mann-Whitney test (p < 0.05) in fetal OB hearts compared to CTL. Male fetuses CTL n = 8, male fetuses OB n = 6, female fetuses CTL n = 7, female fetuses OB n = 7. In figures A-B: PE, phosphatidylethanolamines/odd chain phosphatidylcholines; PC, phosphatidylcholines/odd-chain phosphatidylethanolamines; PC, phosphatidylcholines; PG, phosphatidylglycerols; PS, phosphatidylserines; PA, phosphatidic acids; PI, phosphatidylinositols; TG, monoglycerides, diglycerides and triglycerides; SM, sphingomyelins; CE, cholesteryl esters; Cer, ceramides; PL, phospholipids. In figures E-G, other isobaric lipids can contribute to these signals (Supplementary file 2). See also Figure 4—figure supplement 1 and Figure 4—figure supplement 2.

Figure 4—source data 1

Relative lipid classes abundance in fetal heart (Figure 4A–B).

https://cdn.elifesciences.org/articles/69078/elife-69078-fig4-data1-v3.csv
Figure 4—source data 2

Direct infusion high-resolution mass spectrometry of the heart (positive mode only) (Figure 4E–H).

Scaled raw data and statistical significance.

https://cdn.elifesciences.org/articles/69078/elife-69078-fig4-data2-v3.csv
Figure 4—source data 3

Relative fatty acids classes abundance in fetal heart (Figure 4I).

https://cdn.elifesciences.org/articles/69078/elife-69078-fig4-data3-v3.csv
Figure 4—source data 4

Fatty acids abundance obtained by direct infusion high-resolution mass spectrometry of the heart (negative mode) (Figure 4J).

Scaled raw data and statistical significance.

https://cdn.elifesciences.org/articles/69078/elife-69078-fig4-data4-v3.csv
Figure 4—figure supplement 1
Radar plots showing regulation of most abundant statistically regulated lipids in the heart of fetuses from obese pregnancies in different compartments.

Grey-shaded area indicates negative regulation.

Figure 4—figure supplement 2
Scatterplots showing enrichment score (ES) and statistical significance of lipid ontology pathways from LION.
Fetal cardiac transcriptomics.

(A) Volcano plot showing up and downregulated genes in the heart of obese fetuses. p < 0.05 and FDR < 0.1 by generalised linear models with quasi-likelihood tests. Full statistical data is available in Figure 5—source data 1. (B) Top five regulated Ingenuity Canonical Pathways predicted by analysis of cardiac transcriptome from male fetuses from obese dams compared to fetuses from control dams. A p-value cut-off of 0.01 calculated by likelihood-ratio test was used to select regulated genes included in the IPA analysis. Bars represent activation z-score per pathway; points represent p-value of enriched pathways estimated by IPA algorithm. (C) Activation z-score of top Ingenuity Upstream Regulators predicted by analysis of cardiac transcriptome from male fetuses from obese dams compared to fetuses from control dams. The complete lists of regulated IPA canonical pathways and IPA upstream regulators are available in Figure 5—source data 2 and Figure 5—source data 3, respectively (D) Heatmap showing mRNA levels of genes regulated by PPAR-alpha activity (red bar), and genes mapped to ‘Superpathway of Cholesterol Biosynthesis’ (green bar), ‘Oleate Biosynthesis II’ (blue bar), ‘Superpathway of Geranylgeranyldiphosphate Biosynthesis I’ (yellow bar), ‘Cholecystokinin/Gastrin-mediated Signalling’ (pink bar) and ‘IGF-1 Signalling’ (light blue bar) Ingenuity Canonical Pathways in male E18.5 hearts as analysed by RNA Seq. CTL n = 4 and OB n = 4. (E) mRNA levels of selected markers of lipid metabolism in male and female fetal heats. Male CTL n = 8, male OB n = 8, female CTL n = 6, female OB n = 11. *p < 0.05, **p < 0.01, ***p < 0.001 by Student t-test. Diet ***p < 0.001 by factorial ANOVA. Primer sequences are available in Table 1.

Figure 5—source data 1

Quasi-likelihood general linear models generated from the analysis of E18.5 fetal cardiac transcriptomes (obese versus control) (Figure 5A).

https://cdn.elifesciences.org/articles/69078/elife-69078-fig5-data1-v3.csv
Figure 5—source data 2

List of IPA canonical pathways with mapped E18.5 fetal cardiac genes confidently regulated by maternal obesity (Figure 5B).

https://cdn.elifesciences.org/articles/69078/elife-69078-fig5-data2-v3.csv
Figure 5—source data 3

List of IPA upstream regulators with mapped E18.5 fetal cardiac genes confidently regulated by maternal obesity (Figure 5C).

https://cdn.elifesciences.org/articles/69078/elife-69078-fig5-data3-v3.csv
Figure 5—source data 4

Counts per million of selected genes (Figure 5D).

https://cdn.elifesciences.org/articles/69078/elife-69078-fig5-data4-v3.csv
Figure 5—source data 5

Fetal cardiac mRNA levels by qPCR (Figure 5E).

https://cdn.elifesciences.org/articles/69078/elife-69078-fig5-data5-v3.csv
Figure 6 with 1 supplement
Acyl-carnitine levels in fetal hearts measured by LC-MS.

(A) Relative changes in cardiac carnitine classes levels in male and female fetuses from obese dams. (B) Influence of maternal diet and sex on fetal cardiac carnitine classes levels as calculated by factorial ANOVA. (C) Relative fold change of individual acyl-carnitine levels in the heart of E18.5 fetuses from obese dams according to their abundance. Larger figures are acyl-carnitine species deemed as regulated with p < 0.05 by Student t-test or Mann-Whitney test. SCAC: small-chain acyl-carnitine; MCAC: medium-chain acyl-carnitine; LCAC: long-chain acyl-carnitine; S.MCAM.OH: small- and medium-chain hydroxy acyl-carnitine, LCAC.OH: Long-chain hydroxy acyl-carnitine; Odd Chain: acyl-carnitines with an odd chain number; DCAC: dicarboxylic acyl-carnitines. (D–E) Individual acyl-carnitine species levels in male (D) and female (E) fetal hearts at 18.5 days of pregnancy. See Supplementary file 3 for list of full names. *p < 0.05 by Student t-test or Mann-Whitney test. Male fetuses CTL n = 7, male fetuses OB n = 7, female fetuses CTL n = 7, female fetuses OB n = 6.

Figure 6—source data 1

Acyl-carnitine classes abundance in fetal heart (Figure 6A).

https://cdn.elifesciences.org/articles/69078/elife-69078-fig6-data1-v3.csv
Figure 6—source data 2

Acyl-carnitines abundance obtained by spectrometry of the heart (negative mode) (Figure 6C–E).

Raw data and statistical significance.

https://cdn.elifesciences.org/articles/69078/elife-69078-fig6-data2-v3.csv
Figure 6—source data 3

Estimated pmol [14C]-CO2/ nmol [1-14C]-oleate produced by male and female fetal cardiomyocytes from CTL and OB dams at gestational day 18.5 (Figure 6—figure supplement 1).

https://cdn.elifesciences.org/articles/69078/elife-69078-fig6-data3-v3.csv
Figure 6—figure supplement 1
Estimated pmol [14C]-CO2/ nmol [1-14C]-oleate produced by male and female fetal cardiomyocytes from CTL and OB dams at gestational day 18.5.

Male CTL n = 3, male OB n = 6, female CTL n = 2, female OB n = 5.

Tables

Key resources table
Reagent type (species) or resourceDesignationSource or referenceIdentifiersAdditional information
Biological sample (Mus musculus)Murine cardiac ventriclesUBS, Cambridge, UKExcised and frozen from Mus musculus
Biological sample (Mus musculus)Whole murine cardiac torsosUBS, Cambridge, UKFixed Mus musculus torsos after culling
Biological sample (Mus musculus)Primary murine cardiomyocytesUBS, Cambridge, UKFreshly isolated from Mus musculus
AntibodyAnti-Cardiac Troponin I(mouse monoclonal)AbcamCat# ab8295IF(1:50)
AntibodyAnti-mouse IgG (FITC)(goat polyclonal)AbcamCat# ab6785IF(1:1000)
AntibodyAnti-PCNA(mouse monoclonal)AbcamCat# ab29IHC(1:10,000)
Commercial assay or kitPierce Primary Cardiomyocyte Isolation KitThermo-FisherCat# 88,281
Commercial assay or kitHRP/DAB (AMB) detection IHC kitAbcamab64264
Commercial assay or kitmiRNeasy mini kitQiagen217,004
Commercial assay or kitTruSeq RNA Library Preparation kit v2IlluminaRS-122–2001
Commercial assay or kitHigh-Capacity cDNA Reverse Transcription KitThermo-Fisher4368814
Software, algorithmBowtieBowtieRRID:SCR_005476V 1.2.3
Software, algorithmIngenuity Pathways Analysis (IPA)QiagenRRID:SCR_008653V 42012434
Software, algorithmedgeRBioconductor (R)RRID:SCR_012802V 3.36.0
Software, algorithmRStudioRStudioRRID:SCR_000432V 1.4
Software, algorithmPrismGraphPadRRID:SCR_002798V 9.3.0
Software, algorithmQuPathQuPathRRID:SCR_018257V 0.3.0
Software, algorithmXcaliburThermoRRID:SCR_014593V 4.3
Software, algorithmInkscapeInkscapeRRID:SCR_014479V 1.1.1
Software, algorithmHarmonyPerkinElmerRRID:SCR_018809V 5.0
Software, algorithmImageJImageJRRID:SCR_003070V 1.53 n
Software, algorithmXCMSBioconductor (R)RRID:SCR_015538V 3.16.1
Software, algorithmPeakpickerRHarshfield et al., 2019V 2.0
OtherHorse Serum, heat inactivatedThermo-FisherCat# 26050070
OtherFetal bovine serum (FBS) for standard applicationsThermo-FisherCat#26,140
OtherParaformaldehyde Solution, 4% in PBSThermo-FisherCat# 15670799
OtherAnimal-free blocking bufferVector laboratoriesCat# SP-5030–250
OtherFormalin solution, neutral buffered, 10%MerckHT501128
OtherHaematoxylin QS CounterstainVector laboratoriesH-3404–100
OtherHepesMerckCat# H3375
OtherDAPI solutionMerck10236276001(1 µg/mL)
OtherGuanidineMerckCAS 50-01-1
OtherThioureaMerckCAS 62-56-6
OtherDichloromethaneMerckCAS 75-09-2
OtherMethanolMerckCAS 67-56-1
OtherTriethylammonium chlorideMerckCAS 554-68-7
OtherAmmonium AcetateMerckCAS 631-61-8
OtherChloroformMerck34854–2.5 L-M
OtherButyryl-d7-L-carnitineQMX laboratoryD-7761/0.05
OtherHexadecanoyl-L-carnitine-d3QMX laboratoryD-6646/0.05
OtherAcetoneMerckA/0560/17
OtherAcetonitrileMerck2856–25
OtherPower SYBR Green PCR Master MixThermo-Fisher4367659
OtherFatty acid-free bovine serum albumin (BSA)MerckA9205
OtherDMEM – low glucoseMerckD6046
OtherL-CarnitineMerckCAS 541-15-1
OtherOleic Acid, [1–14 C]-, 50 µCiPerkinElmerNEC317050UC
Table 1
Sequence-specific primers for qPCR.
GeneForward primer (5’ to 3’)Reverse primer (5’ to 3’)
Acot2GCCACCCCGAGGTAAAAGGACCACGACATCCAAGAGACCAT
Cpt1TCCGCTCGCTCATTCCGCTGCCATTCTTGAATCGGATGAACT
Cpt2TCGTACCCACCATGCACTACGTTTAGGGATAGGCAGCCTGG
MvkCGGGGCAGAAGTCTCAGAAGTTCTCAAGTTCAAGGCCGCT
PparaTGCAGCCTCAGCCAAGTTGAACCCGAACTTGACCAGCCACA
Author response table 1
LipidDirectionCTLOBP.value
Cer 34:1;O2_[M + H-H2O]+Low520.6083916
High44
Cer 42:1;O2_[M + H-H2O]+Low520.6083916
High44
Cer 42:2;O2_[M + H-H2O]+Low431

Additional files

Supplementary file 1

Isobars and main predicted classes for m/z detected in direct infusion high-resolution mass spectrometry of the serum (positive mode only).

Isobar annotations were obtained from LIPID MAPS Structure Database and a mass tolerance (m/z) threshold:±0.001 was used. For multiple isobars per m/z, biological likelihood was employed to predict the likely identification. Main classes were predicted according to the likely identification.

https://cdn.elifesciences.org/articles/69078/elife-69078-supp1-v3.csv
Supplementary file 2

Isobars and main predicted classes for m/z detected in direct infusion high-resolution mass spectrometry of the heart (positive mode only).

Isobar annotations were obtained from LIPID MAPS Structure Database and a mass tolerance (m/z) threshold:±0.001 was used. For multiple isobars per m/z, biological likelihood was employed to predict the likely identification. Main classes were predicted according to the likely identification.

https://cdn.elifesciences.org/articles/69078/elife-69078-supp2-v3.csv
Supplementary file 3

List of names for acyl-carnitines identified in E18.5 fetal hearts by LCMS.

https://cdn.elifesciences.org/articles/69078/elife-69078-supp3-v3.csv
Transparent reporting form
https://cdn.elifesciences.org/articles/69078/elife-69078-transrepform1-v3.pdf

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  1. Lucas C Pantaleão
  2. Isabella Inzani
  3. Samuel Furse
  4. Elena Loche
  5. Antonia Hufnagel
  6. Thomas Ashmore
  7. Heather L Blackmore
  8. Benjamin Jenkins
  9. Asha A M Carpenter
  10. Ania Wilczynska
  11. Martin Bushell
  12. Albert Koulman
  13. Denise S Fernandez-Twinn
  14. Susan E Ozanne
(2022)
Maternal diet-induced obesity during pregnancy alters lipid supply to mouse E18.5 fetuses and changes the cardiac tissue lipidome in a sex-dependent manner
eLife 11:e69078.
https://doi.org/10.7554/eLife.69078