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Title: Dietary patterns influence epicardial adipose tissue fatty acid composition and inflammatory gene expression in the Ossabaw pig

Author
item WALKER, MAURA - Jean Mayer Human Nutrition Research Center On Aging At Tufts University
item MATTHAN, NIRUPA - Jean Mayer Human Nutrition Research Center On Aging At Tufts University
item GOLDBAUM, AUDREY - Jean Mayer Human Nutrition Research Center On Aging At Tufts University
item MENG, HUICUI - Jean Mayer Human Nutrition Research Center On Aging At Tufts University
item LAMON-FAVA, STEFANIA - Jean Mayer Human Nutrition Research Center On Aging At Tufts University
item Lakshman, Sukla
item Jang, Saebyeol
item Molokin, Aleksey
item Solano-Aguilar, Gloria
item Urban, Joseph
item LICHTENSTEIN, ALICE - Jean Mayer Human Nutrition Research Center On Aging At Tufts University

Submitted to: Journal of Nutritional Biochemistry
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 4/25/2019
Publication Date: 8/1/2019
Citation: Walker, M., Matthan, N., Goldbaum, A., Meng, H., Lamon-Fava, S., Lakshman, S., Jang, S., Molokin, A., Solano Aguilar, G., Urban Jr, J.F., Lichtenstein, A.H. 2019. Dietary patterns influence epicardial adipose tissue fatty acid composition and inflammatory gene expression in the Ossabaw pig. Journal of Nutritional Biochemistry. 70:138-146. https://doi.org/10.1016/j.jnutbio.2019.04.013.
DOI: https://doi.org/10.1016/j.jnutbio.2019.04.013

Interpretive Summary: Little is known about the influence of dietary fat and plasma cholesterol-lowering therapy on epicardial adipose tissue, a type of fat tissue that accumulates around blood vessels of the heart. This type of adipose tissue is of interest because it is thought to promote the development of heart disease. To gain insight into this relationship, our objective was to determine how dietary fat affects the epicardial adipose tissue fatty acid composition and gene expression. We used an animal model, the Ossabaw pig, fed either a Heart-Healthy diet or Western diet, with or without the most common cholesterol lowering drug, a statin (atorvastatin). The pigs were randomly allocated to one of the four groups and fed either the Heart-Healthy Diet (high in unsaturated fat, whole grain, fruits/vegetables) or Western Diet (high in saturated fat, cholesterol, refined grain) with or without atorvastatin. There was no significant effect of atorvastatin on the outcome measures; hence, the data are reported for the two dietary treatments. Epicardial adipose tissue fatty acid composition reflected, to some extent, that of the diet. The two diets resulted in differential expression of genes associated with interferon signaling, those genes involved with the inflammation. Saturated fatty acids, high in the Western diet, upregulated genes associated with inflammation and polyunsaturated fatty acids, high in the Heart-Healthy diet, upregulated the expression of two anti-inflammatory genes. Associations between epicardial adipose tissue saturated fatty acids and polyunsaturated fatty acids, and expression of genes related to inflammation provide a link between dietary type fat and epicardial adipose tissue inflammation.

Technical Abstract: Background: Little is known about the influence of dietary fat and statin therapy on epicardial adipose tissue (EAT). The Ossabaw pig produces a robust EAT depot and has been used as a translational model of human dietary patterns. Objective: To examine EAT fatty acid (FA) composition in pigs fed a Heart Healthy diet or Western diet, with or without atorvastatin (HHD, HHD+S, WD, and WD+S) and the associations of selected EAT saturated (SFAs) and polyunsaturated (PUFAs) FAs with inflammatory gene expression. Methods: Thirty-Two Ossabaw pigs were randomized to one of the four groups and fed either the HHD (high in unsaturated fat, whole grain, fruits/vegetables) or WD (high in saturated fat, cholesterol, refined grain) with/without atorvastatin. Diets were fed in isocaloric amounts for 6 months. Serum, and EAT adjacent to the left anterior descending coronary artery, were collected during necropsy. Gene expression was determined by RNA sequencing and FA composition by gas chromatography. Results: EAT FA composition largely reflected dietary fat composition. However, there was no significant effect of atorvastatin. SFAs (total SFAs, capric, lauric, palmitic and stearic acids) had positive associations with IRF7, IFIT1, and PTGS2. Total n-6 PUFAs, linoleic acid, and n-3 PUFAs (total n-3 PUFAs, x-linolenic, eicosapentaenoic, docosapentaenoic and docosahexaenoic acids) had strong positive associations with FFAR4 and PPARG, and weak to moderate positive associations with ALOX5. Docosahexaenoic acid was negatively associated with IL-1beta. Capric and lauric acids had weak negative associations with IL-6. Strong associations emerged between EAT and serum FAs. Conclusions: These data document, for the first time, that EAT FA composition is influenced by dietary fat type. Associations between EAT SFAs and PUFAs, and expression of genes related to inflammation provide a link between dietary type fat and EAT inflammation. Serum FAs could potentially serve as a surrogate marker of EAT FA composition.