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Maternal exposure to a Western-style diet causes differences in intestinal microbiota composition and gene expression of suckling mouse pups.

ABSTRACT: The long-lasting consequences of nutritional programming during the early phase of life have become increasingly evident. The effects of maternal nutrition on the developing intestine are still underexplored. In this study, we observed (1) altered microbiota composition of the colonic luminal content, and (2) differential gene expression in the intestinal wall in 2-week-old mouse pups born from dams exposed to a Western-style (WS) diet during the perinatal period. A sexually dimorphic effect was found for the differentially expressed genes in the offspring of WS diet-exposed dams but no differences between male and female pups were found for the microbiota composition. Integrative analysis of the microbiota and gene expression data revealed that the maternal WS diet independently affected gene expression and microbiota composition. However, the abundance of bacterial families not affected by the WS diet (Bacteroidaceae, Porphyromonadaceae, and Lachnospiraceae) correlated with the expression of genes playing a key role in intestinal development and functioning (e.g. Pitx2 and Ace2). Our data reveal that maternal consumption of a WS diet during the perinatal period alters both gene expression and microbiota composition in the intestinal tract of 2-week-old offspring.

SUBMITTER: Steegenga WT

PROVIDER: S-EPMC5215441 | biostudies-literature | 2017 Jan

REPOSITORIES: biostudies-literature

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Maternal exposure to a Western-style diet causes differences in intestinal microbiota composition and gene expression of suckling mouse pups.

Steegenga Wilma T WT Mischke Mona M Lute Carolien C Boekschoten Mark V MV Lendvai Agnes A Pruis Maurien G M MG Verkade Henkjan J HJ van de Heijning Bert J M BJ Boekhorst Jos J Timmerman Harro M HM Plösch Torsten T Müller Michael M Hooiveld Guido J E J GJ

Molecular nutrition & food research 20160712 1

<h4>Scope</h4>The long-lasting consequences of nutritional programming during the early phase of life have become increasingly evident. The effects of maternal nutrition on the developing intestine are still underexplored.<h4>Methods and results</h4>In this study, we observed (1) altered microbiota composition of the colonic luminal content, and (2) differential gene expression in the intestinal wall in 2-week-old mouse pups born from dams exposed to a Western-style (WS) diet during the perinata ...[more]

PMID: 27129739

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Project description:ObjectiveIn humans, offspring of women who are overweight or obese are more likely to develop metabolic disease later in life. Studies in lower animal species reveal that a calorically-dense maternal diet is associated with alterations in islet cell mass and function. The long-term effects of maternal diet on the structure and function of offspring islets with characteristics similar to humans are unknown. We used a well-established non-human primate (NHP) model to determine the consequences of exposure to Western-Style Diet (WSD) in utero and during lactation on islet cell mass and function in the offspring.MethodsFemale Japanese Macaques (Macaca fuscata) were fed either control (CTR) or WSD before and throughout pregnancy and lactation. Offspring were weaned onto CTR or WSD to generate four different groups based on maternal/offspring diets: CTR/CTR, WSD/CTR, CTR/WSD, and WSD/WSD. Offspring were analyzed at three years of age. Pancreatic tissue sections were immunolabelled to measure α- and β-cell mass and proliferation as well as islet vascularization. Live islets were also isolated to test the effects of WSD-exposure on islet function ex vivo. Offspring glucose tolerance was correlated with various maternal characteristics.Resultsα-cell mass was reduced as a result of maternal WSD exposure. α-cell proliferation was reduced in response to offspring WSD. Islet vasculature did not differ among the diet groups. Islets from WSD/CTR offspring secreted a greater amount of insulin in response to glucose ex vivo. We also found that maternal glucose tolerance and parity correlated with offspring glucose tolerance.ConclusionsMaternal WSD exposure results in persistently decreased α-cell mass in the three-year old offspring. WSD/CTR islets secreted greater amounts of insulin ex vivo, suggesting that these islets are primed to hyper-secrete insulin under certain metabolic stressors. Although WSD did not induce overt impaired glucose tolerance in dams or offspring, offspring born to mothers with higher glucose excursions during a glucose tolerance test were more likely to also show higher glucose excursions.

Project description:Current study evaluated the effect of a fine and coarsely ground insoluble dietary fibre source on the gastrointestinal development of suckling pigs. Oat hulls (OH) were selected as a model feedstuff, rich in cellulose, lignin, and insoluble dietary fibre. Three experimental supplemental diets were formulated: a finely ground, low fibre and nutrient dense diet served as control (CON). For the 2 high fibre diets, 15% heat-treated starch in CON was exchanged with OH, either finely (OH-f) or coarsely ground (OH-c). Litters of 10 primi- and multiparous sows (mean litter size 14.6 ± 0.84) were used. Within a litter, experimental diets were allotted to triplets of 4 piglets. From approximately 12 d of age, piglets' individual feed intakes were recorded 2 times per day when separated from their dam for 70 min. Piglets could suckle with their dam for the remainder of the day. On d 24 and 25, from the total pool of 120 piglets, seven healthy well-eating piglets per treatment were selected for post-mortem evaluation, resulting in 14 replicates per treatment. Consumption of OH-c and OH-f did not impede clinical health and production performance of piglets. The full stomach weights tended to be greater for OH-c compared to OH-f whereas CON was intermediate (P = 0.083). Supplementing OH significantly increased ileal villus height and caecal dry matter concentration (P < 0.05). For the colon, OH increased its length, contents weight, short-chain fatty acid concentration and reduced total bacterial count as well as γ-proteobacteria count and proportion (P < 0.05). The OH-c treatment specifically increased full gastrointestinal tract weight and caecum contents weight compared to piglets fed CON and OH-f. Furthermore, OH-c reduced colonic crypt depth when compared to OH-f (P = 0.018). In conclusion, supplementing OH to a diet for suckling piglets exerted subtle developmental effects on gastrointestinal morphology and colonic microbial community. These effects were largely independent from the particle size of the OH.

Dataset Information

Maternal exposure to a Western-style diet causes differences in intestinal microbiota composition and gene expression of suckling mouse pups.

Publications

Maternal exposure to a Western-style diet causes differences in intestinal microbiota composition and gene expression of suckling mouse pups.

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