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Docosahexaenoic acid increases accumulation of adipocyte triacylglycerol through up-regulation of lipogenic gene expression in pigs.

ABSTRACT: Changing dietary fatty acid composition in modern diet influences the prevalence of obesity. Increasing evidences suggest favorable effects of n-3 PUFA for protecting against obesity and the metabolic syndrome. However, the regulation of n-3 PUFA in adipose is still unclear. Thus, this study addressed metabolism of different dietary fats in the adipose tissue of porcine model.Eight-week-old cross-bred pigs were randomly assigned to three groups and fed a 2% fat diet for 30 days from either soybean oil (SBO), docosahexaenoic acid (DHA) or beef tallow. An in vitro experiment was conducted in which linoleic acid (LA), DHA or oleic acid (OA) were added to represent the major fatty acid in the SBO-, DHA- or BT- diets, respectively. Adipocytes size and lipid metabolism related genes were analyzed.Plasma triacylglycerol (TAG) was lower in DHA- than in BT-fed pigs, and the product of lipolysis, glycerol was highest in BT-fed pigs. In addition, expression of the lipolytic genes, adipose triglyceride lipase and hormone sensitive lipase was higher in BT-fed pigs and with OA treatment in vitro. DHA promoted protein kinase A activity in pigs without affecting lipolytic genes. Adipocyte cell sizes, TAG content and expression of lipogenic-related genes including, adipose differentiated related protein (ADRP) and diacylglycerol acyltransferase 1 (DGAT1) were elevated by DHA in vivo and in vitro, indicating DHA promoted adipogenesis to trap TAG in adipose tissue. Fatty acid ?-oxidation genes were increased in the DHA-fed pigs.This effect was partly explained by the effect of DHA to promote adipogenesis to trap TAG in adipocytes and also increase expression of genes involved in adipocyte fatty acid oxidation. Therefore, our results suggest a direct effect of DHA on adipocyte metabolism, resulting in TAG turnover and fatty acid dissipation to facilitate plasma lipid uptake from the circulation.

SUBMITTER: Huang CW

PROVIDER: S-EPMC5297193 | biostudies-literature | 2017 Feb

REPOSITORIES: biostudies-literature

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Docosahexaenoic acid increases accumulation of adipocyte triacylglycerol through up-regulation of lipogenic gene expression in pigs.

Huang Chao-Wei CW Chen Yu-Jen YJ Yang Jui-Ting JT Chen Ching-Yi CY Ajuwon Kolapo M KM Chen Shuen-Ei SE Su Nan-Wei NW Chen Yu-Shan YS Mersmann Harry J HJ Ding Shih-Torng ST

Lipids in health and disease 20170207 1

<h4>Background</h4>Changing dietary fatty acid composition in modern diet influences the prevalence of obesity. Increasing evidences suggest favorable effects of n-3 PUFA for protecting against obesity and the metabolic syndrome. However, the regulation of n-3 PUFA in adipose is still unclear. Thus, this study addressed metabolism of different dietary fats in the adipose tissue of porcine model.<h4>Methods</h4>Eight-week-old cross-bred pigs were randomly assigned to three groups and fed a 2% fat ...[more]

PMID: 28173868

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Project description:Although docosahexaenoic acid (DHA), an important dietary omega-3 polyunsaturated fatty acid (PUFA), is at present primarily sourced from marine fish, bioengineered crops producing DHA may offer a more sustainable and cost-effective source. DHA has been produced in transgenic oilseed crops, however, DHA in seed oil primarily occupies the sn-1/3 positions of triacylglycerol (TAG) with relatively low amounts of DHA in the sn-2 position. To increase the amount of DHA in the sn-2 position of TAG and in seed oil, putative lysophosphatidic acid acyltransferases (LPAATs) were identified and characterized from the DHA-producing alga Schizochytrium sp. and from soybean (Glycine max). The affinity-purified proteins were confirmed to have LPAAT activity. Expression of the Schizochytrium or soybean LPAATs in DHA-producing Arabidopsis expressing the Schizochytrium PUFA synthase system significantly increased the total amount of DHA in seed oil. A novel sensitive band-selective heteronuclear single quantum coherence (HSQC) NMR method was developed to quantify DHA at the sn-2 position of glycerolipids. More than two-fold increases in sn-2 DHA were observed for Arabidopsis lines expressing Schizochytrium or soybean LPAATs, with one Schizochytrium LPAAT driving DHA accumulation in the sn-2 position to 61% of the total DHA. Furthermore, expression of a soybean LPAAT led to a redistribution of DHA-containing TAG species, with two new TAG species identified. Our results demonstrate that transgenic expression of Schizochytrium or soybean LPAATs can increase the proportion of DHA at the sn-2 position of TAG and the total amount of DHA in the seed oil of a DHA-accumulating oilseed plant. Additionally, the band-selective HSQC NMR method that we developed provides a sensitive and robust method for determining the regiochemistry of DHA in glycerolipids. These findings will benefit the advancement of sustainable sources of DHA via transgenic crops such as canola and soybean.

Project description:The objectives of this study were as follows: 1) to establish whether feeding a source of eicosapentaenoic acid (EPA) and docosahexaenoic acid (DHA) to ewes during late gestation changes the fatty acid profile of colostrum, milk, ewe adipose tissue, and plasma and subsequently lamb plasma and red blood cells (RBC), and 2) to investigate the effects of EPA and DHA on mRNA expression in ewe adipose tissue. Eighty-four gestating ewes (28 pens, three per pen) were blocked by lambing day and assigned to a diet with an addition of fat at 0.39% of the DM during the last 50 d of gestation using Ca salts of a palm fatty acid distillate (PFAD) high in palmitic and oleic acids or EPA + DHA. Blood samples were taken from ewes on days 20, 1 (parturition), and 30 and from lambs on days 1 and 30 for plasma fatty acid analysis. Fatty analysis of lamb RBC was performed on day 1. Colostrum samples were taken at lambing and milk samples on day 30 for fatty acid analysis. Subcutaneous adipose tissue biopsies were taken from one ewe per pen on day 20 for fatty acid analysis and gene expression analysis of 27 genes. Treatment × day interactions (P < 0.10) were observed for several isomers of C18:1, with concentrations that were greater in plasma of EPA + DHA ewes on day 20, but were not different on day 1 or 30. Plasma concentrations of EPA tended to be greater (P = 0.07), whereas DHA was greater (P < 0.001) in EPA + DHA ewes compared with PFAD ewes. There was no difference in EPA or DHA in adipose tissue with EPA + DHA vs. PFAD supplementation (P > 0.10). Concentrations of fatty acids with 6 to 10 carbons were significantly increased (P < 0.05) in colostrum and milk of EPA + DHA ewes. There was a treatment × day interaction with EPA + DHA ewes yielding greater EPA (P = 0.03) and DHA (P = 0.04) concentrations than PFAD in colostrum, but not in milk. Treatment × day interactions (P < 0.05) were observed for several C18:1 isomers with concentrations that were greater in EPA + DHA ewe colostrum, but were not different between treatments in milk. In lamb plasma and RBC, EPA and DHA were not different between treatments (P > 0.10). The expression of fatty acid synthase and leptin was significantly increased (P < 0.05), whereas the expression of diacylglycerol acyltransferase 2 tended to be increased (P = 0.08) by supplementation of EPA + DHA vs. PFAD. These results suggest that supplementation with EPA and DHA to ewes during late gestation alters the fatty acid profile of plasma, colostrum, and milk and may increase lipogenesis.

Project description:BackgroundExcessive fat accumulation of pigs is undesirable, as it severely affects economic returns in the modern pig industry. Studies in humans and mice have examined the role of the gut microbiome in host energy metabolism. Commercial Duroc pigs are often fed formula diets with high energy and protein contents. Whether and how the gut microbiome under this type of diet regulates swine fat accumulation is largely unknown.ResultsIn the present study, we systematically investigated the correlation of gut microbiome with pig lean meat percentage (LMP) in 698 commercial Duroc pigs and found that Prevotella copri was significantly associated with fat accumulation of pigs. Fat pigs had significantly higher abundance of P. copri in the gut. High abundance of P. copri was correlated with increased concentrations of serum metabolites associated with obesity, e.g., lipopolysaccharides, branched chain amino acids, aromatic amino acids, and the metabolites of arachidonic acid. Host intestinal barrier permeability and chronic inflammation response were increased. A gavage experiment using germ-free mice confirmed that the P. copri isolated from experimental pigs was a causal species increasing host fat accumulation and altering serum metabolites. Colon, adipose tissue, and muscle transcriptomes in P. copri-gavaged mice indicated that P. copri colonization activated host chronic inflammatory responses through the TLR4 and mTOR signaling pathways and significantly upregulated the expression of the genes related to lipogenesis and fat accumulation, but attenuated the genes associated with lipolysis, lipid transport, and muscle growth.ConclusionsTaken together, the results proposed that P. copri in the gut microbial communities of pigs fed with commercial formula diets activates host chronic inflammatory responses by the metabolites through the TLR4 and mTOR signaling pathways, and increases host fat deposition significantly. The results provide fundamental knowledge for reducing fat accumulation in pigs through regulating the gut microbial composition. Video Abstract.

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Docosahexaenoic acid increases accumulation of adipocyte triacylglycerol through up-regulation of lipogenic gene expression in pigs.

Publications

Docosahexaenoic acid increases accumulation of adipocyte triacylglycerol through up-regulation of lipogenic gene expression in pigs.

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