Developmental programming of the metabolic syndrome by maternal nutritional imbalance: how strong is the evidence from experimental models in mammals?

Armitage, James A.; Khan, Imran Y; Taylor, Paul D.; Nathanielsz, Peter W.; Poston, Lucilla

doi:10.1113/jphysiol.2004.072009

Cited by 490 publications

(406 citation statements)

References 186 publications

(285 reference statements)

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“…The pregnant rat subjected to a modest protein deficiency has become widely used as an animal model in the study of metabolic programming [28] since this seemingly mild intervention produces long lasting changes in the offspring, including reduced glucose tolerance, defects in insulin secretion and raised blood pressure. [25,[29][30][31].…”

Section: Discussionmentioning

confidence: 99%

The effect of dietary protein on the amino acid supply and threonine metabolism in the pregnant rat

Rees¹,

Hay²,

Antipatis³

2006

Reprod. Nutr. Dev.

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-To characterise the effects of dietary protein content on threonine metabolism during pregnancy, rats were fed diets containing 18% or 9% protein and then killed at different stages of gestation. Serum threonine concentrations fell significantly faster in the animals fed the diet containing 9% protein when compared to those fed the diet containing 18% protein. On day 4 of gestation the rate of threonine oxidation was higher in maternal liver homogenates prepared from the animals fed the diet containing 18% protein. The rate of threonine oxidation by liver homogenates fell as gestation proceeded in both diet groups. The activity of threonine dehydrogenase in the maternal liver was unaffected by dietary protein content at all stages of gestation. Serine-threonine dehydratase activity in homogenates of the maternal liver was transiently increased during the early stages of gestation in the animals fed high protein diets but was unchanged in the low protein groups. There was an increase in serine-threonine dehydratase activity in the kidney during the later stages of gestation but this was unaffected by the protein content of the maternal diet. These data show that the changes in free threonine concentrations cannot be accounted for through changes in the oxidation rate and suggest that some other factor influences the unusual metabolism of this amino acid during gestation. threonine dehydratase / threonine dehydrogenase / protein metabolism / pregnancy / foetus / metabolic programming Abbreviations: SDH, serine/threonine dehydratase; TDH, threonine dehydrogenase; PCA, perchloric acid; TCA, trichloroacetic acid.

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Section: Discussionmentioning

confidence: 99%

The effect of dietary protein on the amino acid supply and threonine metabolism in the pregnant rat

Rees¹,

Hay²,

Antipatis³

2006

Reprod. Nutr. Dev.

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“…The fetus responds to this nutritional stress by programming its own growth in a way that could increase its risk of developing metabolic disorders in later life (6 -8). Considering that a typical Western diet is rich in dietary fat content (17), especially saturated fatty acids (SFA), some studies have investigated the role of high-fat feeding in the concept of developmental origins of health and disease (3)(4)(5). These studies indicate that maternal high-SFA consumption during pregnancy can induce features of metabolic syndrome including dyslipidemia (26,27,35), insulin resistance (57), and hypertension (36,35) in the adult offspring.…”

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confidence: 99%

Developmental programming of lipid metabolism and aortic vascular function in C57BL/6 mice: a novel study suggesting an involvement of LDL-receptor

Chechi

McGuire²,

Cheema³

2009

American Journal of Physiology-Regulatory, Integrative and Comp

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Chechi K, McGuire JJ, Cheema SK. Developmental programming of lipid metabolism and aortic vascular function in C57BL/6 mice: a novel study suggesting an involvement of LDL-receptor. Am J Physiol Regul Integr Comp Physiol 296: R1029 -R1040, 2009. First published February 4, 2009 doi:10.1152/ajpregu.90932.2008We have previously shown that a maternal high-fat diet, rich in saturated fatty acids (SFA), alters the lipid metabolism of their adult offspring. The present study was designed to investigate 1) whether alterations in hepatic LDL-receptor (LDL-r) expression may serve as a potential mechanism of developmental programming behind the altered lipid metabolism of the offspring, 2) whether altered lipid metabolism leads to aortic vascular dysfunction in the offspring, 3) whether deleterious effects of SFA exposure preweaning are influenced by postweaning diet, and 4) whether gender-specific programming effects are observed. Female C57Bl/6 mice were fed a high-SFA diet or regular chow during gestation and lactation while their pups, both male and female, received either SFA or a chow diet after weaning. Male offspring obtained from mothers fed an SFA diet and those who continued on chow postweaning had higher plasma triglycerides and total cholesterol, whereas female offspring had higher plasma total and LDL cholesterol levels, lower hepatic LDL-r mRNA expression, and reduced aortic contractile responses compared with the offspring that were fed chow throughout the study. A comparison of the postweaning diet revealed significantly lower hepatic LDL-r expression along with significantly higher plasma LDL-cholesterol concentration in the female offspring that were obtained from mothers fed an SFA diet and who continued on an SFA diet postweaning, compared with the female offspring that were obtained from mothers fed an SFA diet but who continued on chow postweaning. In conclusion, we report a novel observation of hepatic LDL-r-mediated programming of altered lipid metabolism, along with aortic vascular dysfunction, in the female offspring of mothers fed a high-SFA diet. Male offspring only exhibited dyslipidemia, suggesting gender-mediated programming. This study further highlighted the role of postweaning diets in overriding the effects of maternal programming. fetal programming; plasma lipids; hepatic LDL-receptor; dietary fats; cardiovascular disease RECENT EVIDENCE BASED ON THE developmental origins of health and disease hypothesis suggests that early nutrition can be critical in determining the cardiovascular health of an individual (43, 44). According to this hypothesis, which was originally known as Barker's hypothesis, an adverse maternal nutrition during gestation can create a stressed environment for the developing fetus. The fetus responds to this nutritional stress by programming its own growth in a way that could increase its risk of developing metabolic disorders in later life (6 -8). Considering that a typical Western diet is rich in dietary fat content (17), especially saturated fatty acids (SFA), s...

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“…This is reflected by a 'U'-shaped relationship between birth weight and adult BMI, suggesting that both low-and high-birth weights are risk factors for future obesity (Demmelmair et al 2006, Martin-Gronert & Ozanne 2010. In addition, weight gain from the first week to 2 years of life may be a critical determinant for the development of obesity and metabolic syndrome several decades later (Armitage et al 2004, Toschke et al 2004, Patel & Srinivasan 2010. Therefore, both pre-and postnatal nutrition have significant effects on the long-term regulation of body weight and energy homeostasis in adulthood.…”

Section: Introductionmentioning

confidence: 99%

Neonatal overnutrition in mice exacerbates high-fat diet-induced metabolic perturbations

Liu¹,

Lim²,

Su³

et al. 2013

Journal of Endocrinology

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Neonatal overnutrition results in accelerated development of high-fat diet (HFD)-induced metabolic defects in adulthood. To understand whether the increased susceptibility was associated with aggravated inflammation and dysregulated lipid metabolism, we studied metabolic changes and insulin signaling in a chronic postnatal overnutrition (CPO) mouse model. Male Swiss Webster pups were raised with either three pups per litter to induce CPO or ten pups per litter as control (CTR) and weaned to either low-fat diet (LFD) or HFD. All animals were killed on the postnatal day 150 (P150) except for a subset of mice killed on P15 for the measurement of stomach weight and milk composition. CPO mice exhibited accelerated body weight gain and increased body fat mass prior to weaning and the difference persisted into adulthood under conditions of both LFD and HFD. As adults, insulin signaling was more severely impaired in epididymal white adipose tissue (WAT) from HFD-fed CPO (CPO-HFD) mice. In addition, HFD-induced upregulation of pro-inflammatory cytokines was exaggerated in CPO-HFD mice. Consistent with greater inflammation, CPO-HFD mice showed more severe macrophage infiltration than HFD-fed CTR (CTR-HFD) mice. Furthermore, when compared with CTR-HFD mice, CPO-HFD mice exhibited reduced levels of several lipogenic enzymes in WAT and excess intramyocellular lipid accumulation. These data indicate that neonatal overnutrition accelerates the development of insulin resistance and exacerbates HFD-induced metabolic defects, possibly by worsening HFD-induced inflammatory response and impaired lipid metabolism.

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Developmental programming of the metabolic syndrome by maternal nutritional imbalance: how strong is the evidence from experimental models in mammals?

Cited by 490 publications

References 186 publications

The effect of dietary protein on the amino acid supply and threonine metabolism in the pregnant rat

The effect of dietary protein on the amino acid supply and threonine metabolism in the pregnant rat

Developmental programming of lipid metabolism and aortic vascular function in C57BL/6 mice: a novel study suggesting an involvement of LDL-receptor

Neonatal overnutrition in mice exacerbates high-fat diet-induced metabolic perturbations

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