The programming of cardiac hypertrophy in the offspring by maternal obesity is associated with hyperinsulinemia, AKT, ERK, and mTOR activation
Open accessAbstract
Human and animal studies suggest that suboptimal early nutrition during critical developmental periods impacts long-term health. For example, maternal overnutrition during pregnancy and lactation in mice programs insulin resistance, obesity, and endothelial dysfunction in the offspring. Here we investigated the effects of diet-induced maternal obesity on the offspring cardiac phenotype and explored potential underlying molecular mechanisms. Dams fed the obesogenic diet were heavier (P < 0.01) and fatter (P < 0.0001) than controls throughout pregnancy and lactation. There was no effect of maternal obesity on offspring body weight or body composition up to 8 wk of age. However, maternal obesity resulted in increased offspring cardiac mass (P < 0.05), increased heart-body weight (P < 0.01), heart weight-tibia length (P < 0.05), increased left ventricular free wall thickness and area (P < 0.01 and P < 0.05, respectively), and increased myocyte width (P < 0.001). Consistent with these structural changes, the expression of molecular markers of cardiac hypertrophy were also increased [Nppb(BNP), Myh7-Myh6(βMHC-αMHC) (both P < 0.05) and mir-133a (P < 0.01)]. Offspring were hyperinsulinemic and displayed increased insulin action through AKT (P < 0.01), ERK (P < 0.05), and mammalian target of rapamycin (P < 0.05). p38MAPK phosphorylation was also increased (P < 0.05), suggesting pathological remodeling. Increased Ncf2(p67(phox)) expression (P < 0.05) and impaired manganese superoxide dismutase levels (P < 0.01) suggested oxidative stress, which was consistent with an increase in levels of 4-hydroxy-2-trans-nonenal (a measure of lipid peroxidation). We propose that maternal diet-induced obesity leads to offspring cardiac hypertrophy, which is independent of offspring obesity but is associated with hyperinsulinemia-induced activation of AKT, mammalian target of rapamycin, ERK, and oxidative stress.
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Young adult male offspring at 3 and 8 weeks of age from obese dams have increased heart weight, left ventricular wall thickness and increased heart weight to body weight ratio, compared to offspring from control dams.
“the Ozanne group showed that young adult male offspring (at 3 and 8 weeks of age) from obese dams have increased heart weight, LV wall thickness and increased heart weight to body weight ratio, compared to offspring from control dams [93,112].”
From Recent Experimental Studies of Maternal Obesity, Diabetes during Pregnancy and the Developmental Origins of Cardiovascular Disease (2022) · cites this paper as [93]
The Results (Effects of maternal obesity on offspring; Structural and molecular indices of cardiac hypertrophy; page unavailable) report greater heart weight, heart-weight-to-body-weight ratio, and left ventricular wall thickness in male offspring of obese dams at 8 weeks. The Materials and Methods (Animals; page unavailable) say offspring were weaned at 21 days and selected for cardiac analysis at 8 weeks; this paper does not report those cardiac findings at 3 weeks. (LLM, conf=0.90)
Experimental — accuracy not yet measuredIncreased expression of Nppb, Acta1 and the ratio of Myh7:Myh6 gene expression were observed in the offspring of obese dams.
“In line with cardiac hypertrophy, increased expression of Nppb, Acta1 and the ratio of Myh7:Myh6 gene expression were observed in the offspring of obese dams [93,112].”
From Recent Experimental Studies of Maternal Obesity, Diabetes during Pregnancy and the Developmental Origins of Cardiovascular Disease (2022) · cites this paper as [93]
The Results section (‘Structural and molecular indices of cardiac hypertrophy’; page unavailable) reports increased Nppb expression and an increased Myh7:Myh6 transcript ratio in offspring of obese dams. It does not report increased Acta1 expression; a search for Acta1 found no matching passage in our copy. (LLM, conf=0.90)
Experimental — accuracy not yet measuredThe effect of maternal obesity on cellular cardiomyocyte hypertrophy was only observed in the 3- and 8-week-old offspring and not 12-week-old offspring.
“Moreover, the effect of maternal obesity on cellular cardiomyocyte hypertrophy were only observed in the 3- and 8-week-old offspring [93,112] and not 12-week-old offspring [112].”
From Recent Experimental Studies of Maternal Obesity, Diabetes during Pregnancy and the Developmental Origins of Cardiovascular Disease (2022) · cites this paper as [93]
The Results (Structural and molecular indices of cardiac hypertrophy; page not supplied) report significantly greater myocyte width in offspring of obese dams studied at 8 weeks. The paper does not report cellular hypertrophy measurements at 3 or 12 weeks, so it cannot establish that the effect was present at 3 weeks or absent at 12 weeks. (LLM, conf=0.88)
Experimental — accuracy not yet measuredThe elevated Akt Ser-473 phosphorylation in hearts of offspring from obese dams appears to be mediated by increased p38-MAPK signalling through Erk and mTOR.
“Interestingly, phosphorylation of Akt at the activating Ser-473 site was elevated in hearts of offspring from obese dams, although this appeared to be mediated by increased p38-Mitogen-activated protein kinase signalling through Erk and mTOR [93]”
From Recent Experimental Studies of Maternal Obesity, Diabetes during Pregnancy and the Developmental Origins of Cardiovascular Disease (2022) · cites this paper as [93]
The Results section reports elevated AKT1 Ser-473 phosphorylation in hearts of offspring from obese dams, alongside increased phosphorylation of ERK1/2, mTOR, and p38MAPK. The Discussion does not say that p38MAPK mediates AKT phosphorylation through ERK and mTOR; it describes AKT phosphorylation as an insulin-signaling event and proposes a separate role for p38MAPK in pathological remodeling. No page number is available in our copy. (LLM, conf=0.90)
Experimental — accuracy not yet measuredIn hearts of offspring from obese dams, phosphorylation of Akt at the activating Ser-473 site is elevated.
“Interestingly, phosphorylation of Akt at the activating Ser-473 site was elevated in hearts of offspring from obese dams, although this appeared to be mediated by increased p38-Mitogen-activated protein kinase signalling through Erk and mTOR [93]”
From Recent Experimental Studies of Maternal Obesity, Diabetes during Pregnancy and the Developmental Origins of Cardiovascular Disease (2022) · cites this paper as [93]
Levels of mitochondrial localized superoxide dismutase-2 are reduced in the hearts of offspring of obese dams.
“Reduced levels of mitochondrial localized superoxide dismutase-2 in the hearts of offspring of obese dams [93] suggest that maternal obesity increases the sensitivity of the offspring myocardium to oxidative damage.”
From Recent Experimental Studies of Maternal Obesity, Diabetes during Pregnancy and the Developmental Origins of Cardiovascular Disease (2022) · cites this paper as [93]
In 8-week-old offspring of obese dams, cardiac expression of insulin receptor-β is reduced.
“In 8-week-old offspring of obese dams, the expression of insulin receptor-β, a key component for mediating insulin signalling in the heart, was reduced [93].”
From Recent Experimental Studies of Maternal Obesity, Diabetes during Pregnancy and the Developmental Origins of Cardiovascular Disease (2022) · cites this paper as [93]
Exposure to maternal obesity reduces mRNA expression of Gata-4 in the offspring heart.
“Fernandez-Twinn et al. [93] discovered that exposure of the offspring to maternal obesity increased the cardiac expression of miR-133 and reduced the mRNA expression of one of its putative targets, Gata-4, which is upregulated in cardiac hypertrophy.”
From Recent Experimental Studies of Maternal Obesity, Diabetes during Pregnancy and the Developmental Origins of Cardiovascular Disease (2022) · cites this paper as [93]
Gata-4 is upregulated in cardiac hypertrophy.
“Fernandez-Twinn et al. [93] discovered that exposure of the offspring to maternal obesity increased the cardiac expression of miR-133 and reduced the mRNA expression of one of its putative targets, Gata-4, which is upregulated in cardiac hypertrophy.”
From Recent Experimental Studies of Maternal Obesity, Diabetes during Pregnancy and the Developmental Origins of Cardiovascular Disease (2022) · cites this paper as [93]
Exposure to maternal obesity increases cardiac expression of miR-133 in offspring.
“Fernandez-Twinn et al. [93] discovered that exposure of the offspring to maternal obesity increased the cardiac expression of miR-133 and reduced the mRNA expression of one of its putative targets, Gata-4, which is upregulated in cardiac hypertrophy.”
From Recent Experimental Studies of Maternal Obesity, Diabetes during Pregnancy and the Developmental Origins of Cardiovascular Disease (2022) · cites this paper as [93]
Maternal obesity increases the sensitivity of the offspring myocardium to oxidative damage.
“Reduced levels of mitochondrial localized superoxide dismutase-2 in the hearts of offspring of obese dams [93] suggest that maternal obesity increases the sensitivity of the offspring myocardium to oxidative damage.”
From Recent Experimental Studies of Maternal Obesity, Diabetes during Pregnancy and the Developmental Origins of Cardiovascular Disease (2022) · cites this paper as [93]
Protein translation supporting pathologic cardiac hypertrophy is activated in hearts of offspring from obese dams.
“suggesting that protein translation supporting pathologic cardiac hypertrophy was activated.”
From Recent Experimental Studies of Maternal Obesity, Diabetes during Pregnancy and the Developmental Origins of Cardiovascular Disease (2022) · cites this paper as [93]
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- Authors
- Fernandez-Twinn, D. S., Blackmore, H. L., Siggens, L., Giussani, D. A., Cross, C. M., Foo, R., & Ozanne, S. E.
- Affiliations
- Metabolic Research Laboratories (D.S.F.-T., H.L.B., S.E.O.), University of Cambridge, Institute of Metabolic Science, Addenbrooke's Hospital, Cambridge CB2 0QQ, United Kingdom
- University of Cambridge (GB)
- Venue
- Endocrinology
- Publisher
- The Endocrine Society
- Published
- 2012-12-01
- Volume
- 153
- Issue
- 12
- Pages
- 5961-5971
- ISSN
- 0013-7227 (ISSN-L)
- 1945-7170
- PMC
- PMC3568261
- OpenAlex
- W2075074527
- Cited by
- 141
- References
- 43
- Citations by year
- 2026: 4 · 2025: 8 · 2024: 5 · 2023: 8 · 2022: 17 · 2021: 7 · 2020: 10 · 2019: 7 · 2018: 18 · 2017: 9 · 2016: 14 · 2015: 11 · 2014: 13 · 2013: 10
- FWCI
- 9.53
- Type
- journal article
- Language
- en
- Open access
- hybrid
- doi.org
- Licence
- Locations
- Endocrinology (publishedVersion, cc-by-nc)
- Europe PMC (PubMed Central) (publishedVersion, cc-by-nc)
- PubMed Central (publishedVersion, cc-by-nc)
- PubMed (publishedVersion)
- Funders
- Wellcome Trust (EU-FP7-, 086797, 086797/Z/08/Z)
- British Heart Foundation (FS/09/050, FS/09/029/27902)
- European Commission (289346)
- Directorate for Biological Sciences
- Medical Research Council (EU FP7)
- Biotechnology and Biological Sciences Research Council (BB/F015364/1)
- Topics
- Health Sciences › Medicine › Pediatrics, Perinatology and Child Health › Birth, Development, and Health
- Health Sciences › Medicine › Cardiology and Cardiovascular Medicine › Cardiac Fibrosis and Remodeling
- Health Sciences › Medicine › Cardiology and Cardiovascular Medicine › Cardiovascular Function and Risk Factors
- Keywords
- maternal obesity, diet-induced obesity, cardiac hypertrophy, hyperinsulinemia, Akt signaling, ERK signaling, mTOR signaling, p38 MAPK, oxidative stress, manganese superoxide dismutase, lipid peroxidation, cardiomyocyte hypertrophy, developmental programming, cardiac remodeling
- MeSH terms
- Animals, Body Composition, Body Weight, Female, Cardiomegaly, Hyperinsulinism, Male, Mice, Inbred C57BL, Mothers, Obesity, Phenotype, Pregnancy, Pregnancy, Animal, Prenatal Exposure Delayed Effects, Lipid Peroxidation, Oxidative Stress, Maternal Nutritional Physiological Phenomena, Extracellular Signal-Regulated MAP Kinases, Proto-Oncogene Proteins c-akt, Mice, TOR Serine-Threonine Kinases
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