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The effects of dietary fatty acids in the physiological outcomes of maternal high-fat diet on offspring energy homeostasis in mice

Published online by Cambridge University Press:  26 September 2019

Kyle J. Mamounis ,
Naomi R. Shvedov ,
Nicholas Margolies ,
Ali Yasrebi  and
Troy A. Roepke Open the ORCID record for Troy A. Roepke [Opens in a new window]
Kyle J. Mamounis
Affiliation:
Department of Animal Sciences, School of Environmental & Biological Sciences, Rutgers, The State University of New Jersey, New Brunswick, NJ, USA Nutritional Sciences Graduate Program, Rutgers, The State University of New Jersey, New Brunswick, NJ, USA
Naomi R. Shvedov
Affiliation:
Department of Animal Sciences, School of Environmental & Biological Sciences, Rutgers, The State University of New Jersey, New Brunswick, NJ, USA
Nicholas Margolies
Affiliation:
Department of Animal Sciences, School of Environmental & Biological Sciences, Rutgers, The State University of New Jersey, New Brunswick, NJ, USA
Ali Yasrebi
Affiliation:
Department of Animal Sciences, School of Environmental & Biological Sciences, Rutgers, The State University of New Jersey, New Brunswick, NJ, USA
Troy A. Roepke*
Affiliation:
Department of Animal Sciences, School of Environmental & Biological Sciences, Rutgers, The State University of New Jersey, New Brunswick, NJ, USA Nutritional Sciences Graduate Program, Rutgers, The State University of New Jersey, New Brunswick, NJ, USA New Jersey Institute for Food, Nutrition, and Health, Rutgers, The State University of New Jersey, New Brunswick, NJ, USA
*
Address for correspondence: Troy A. Roepke, Department of Animal Sciences, Rutgers University, SEBS, Bartlett Hall, 84 Lipman Drive, New Brunswick, NJ 08901, USA. Email: [email protected]
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Abstract

The early-life origins of disease hypothesis has been applied to obesity research and modeled through overnutrition, usually with a high-fat diet (HFD). Since the obesity epidemic coincided with societal change in dietary fat consumption, rather than amount, manipulation of fatty acid (FA) profile is an under-investigated area of study. Additionally, the binding of FAs to nuclear receptors may have persistent intergenerational, extranutritive endocrinological effects that interact with the actions of reproductive steroids causing sex-dependent effects. To determine the role of FA type in the effects underlying maternal HFD, we fed wild-type C57BL6/J mating pairs, from preconception through lactation, a HFD with high saturated fat levels from coconut oil or high linoleic acid (LA) levels from vegetable oil. Male and female offspring body weight and food intake were measured weekly for 25 weeks. Assays for glucose metabolism, body composition, and calorimetry were performed at 25 weeks. Plasma metabolic peptides and liver mRNA were measured terminally. Obesity was primarily affected by adult rather than maternal diet in males, yet in females, maternal HFD potentiated the effects of adult HFD. Maternal HFD high in LA impaired glucose disposal in males weaned onto HFD and insulin sensitivity of females. Plasma leptin correlated with adiposity, but insulin and insulin receptor expression in the liver were altered by maternal LA in males. Our results suggest that maternal FA profile is most influential on offspring glucose metabolism and that adult diet is more important than maternal diet for obesity and other parameters of metabolic syndrome.

Keywords

Obesitymaternalfatty acidslinoleic acidglucose
Type
Original Article
Information
Journal of Developmental Origins of Health and Disease , Volume 11 , Issue 3 , June 2020 , pp. 273 - 284
Copyright
© Cambridge University Press and the International Society for Developmental Origins of Health and Disease 2019

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Footnotes

Current address: Kyle J. Mamounis, Burnett School of Biomedical Sciences, College of Medicine, University of Central Florida, Orlando, FL 32827, USA.

References

Ogden, CL, Carroll, MD, Kit, BK, Flegal, KM.Prevalence of childhood and adult obesity in the United States, 2011–2012. JAMA. 2014; 311, 806–814.CrossRefGoogle ScholarPubMed
Barker, DJ.The fetal and infant origins of adult disease. BMJ Br Med J. 1990; 301, 1111.CrossRefGoogle ScholarPubMed
Delahaye, F, Breton, C, Risold, PY, et al.Maternal perinatal undernutrition drastically reduces postnatal leptin surge and affects the development of arcuate nucleus proopiomelanocortin neurons in neonatal male rat pups. Endocrinology. 2008; 149, 470–475.CrossRefGoogle ScholarPubMed
Cripps, RL, Martin-Gronert, MS, Archer, ZA, Hales, CN, Mercer, JG, Ozanne, SE.Programming of hypothalamic neuropeptide gene expression in rats by maternal dietary protein content during pregnancy and lactation. Clin Sci. 2009; 117, 85–93.CrossRefGoogle ScholarPubMed
Howie, GJ, Sloboda, DM, Kamal, T, Vickers, MH.Maternal nutritional history predicts obesity in adult offspring independent of postnatal diet. J Physiol. 2009; 587, 905–915.CrossRefGoogle ScholarPubMed
Rother, E, Kuschewski, R, Angel, M, et al.Hypothalamic JNK1 and IKKβ activation and impaired early postnatal glucose metabolism after maternal perinatal high-fat feeding. Endocrinology. 2012; 153, 770–781.CrossRefGoogle ScholarPubMed
Velloso, LA, Araújo, EP, de Souza, CT.Diet-induced inflammation of the hypothalamus in obesity. Neuroimmunomodulation. 2008; 15, 189–193.10.1159/000153423CrossRefGoogle ScholarPubMed
Roepke, TA, Yasrebi, A, Villalobos, A, Krumm, EA, Yang, JA, Mamounis, KJ.Loss of ERα partially reverses the effects of maternal high-fat diet on energy homeostasis in female mice. Sci Rep. 2017; 7, 1–15.CrossRefGoogle ScholarPubMed
Taubes, G.The soft science of dietary fat. Science. 2001; 291, 1–16.CrossRefGoogle ScholarPubMed
Blasbalg, TL, Hibbeln, JR, Ramsden, CE, Majchrzak, SF, Rawlings, RR.Changes in consumption of omega-3 and omega-6 fatty acids in the United States during the 20th century. Am J Clin Nutr. 2011; 93, 950–962.CrossRefGoogle ScholarPubMed
Ailhaud, G, Guesnet, P.Fatty acid composition of fats is an early determinant of childhood obesity: a short review and an opinion. Obes Rev. 2004; 5, 21–26.10.1111/j.1467-789X.2004.00121.xCrossRefGoogle Scholar
Ikemoto, S, Takahashi, M, Tsunoda, N, Maruyama, K, Itakura, H, Ezaki, O.High-fat diet-induced hyperglycemia and obesity in mice: differential effects of dietary oils. Metabolism. 1996; 45, 1539–1546.CrossRefGoogle ScholarPubMed
Alvheim, AR, Malde, MK, Osei-Hyiaman, D, et al.Dietary linoleic acid elevates endogenous 2-AG and anandamide and induces obesity. Obesity. 2012; 20, 1984–1994.CrossRefGoogle ScholarPubMed
Wit, N De, Derrien, M, Bosch-Vermeulen, H, et al.Saturated fat stimulates obesity and hepatic steatosis and affects gut microbiota composition by an enhanced overflow of dietary fat to the distal intestine. AJP Gastrointest Liver Physiol. 2012; 303, G589–G599.CrossRefGoogle ScholarPubMed
Tsunoda, N, Ikemoto, S, Takahashi, M, et al.High-monounsaturated fat diet-induced obesity and diabetes in C57BL/6J mice. Metabolism. 1998; 47, 724–730.CrossRefGoogle ScholarPubMed
Masterjohn, C. Retrieved from https://chrismasterjohnphd.com/blog/2011/11/19/this-just-in-infamous-lard-based-hig/ 2011.Google Scholar
Mamounis, KJ, Yasrebi, A, Roepke, TA.Linoleic acid causes greater weight gain than saturated fat without hypothalamic inflammation in the male mouse. J Nutr Biochem. 2017; 40, 122–131.10.1016/j.jnutbio.2016.10.016CrossRefGoogle ScholarPubMed
Cabanes, A, Assis, D, Gustafsson, J.Maternal high n-6 polyunsaturated fatty acid intake during pregnancy increases voluntary alcohol intake and hypothalamic estrogen receptor alpha and beta levels among female. Dev Neurosci. 2000; 2197, 488–493.CrossRefGoogle Scholar
Massiera, F, Saint-Marc, P, Seydoux, J, et al.Arachidonic acid and prostacyclin signaling promote adipose tissue development: a human health concern? J Lipid Res. 2003; 44, 271–279.CrossRefGoogle ScholarPubMed
Pouteau, E, Aprikian, O, Grenot, C, et al.A low alpha-linolenic intake during early life increases adiposity in the adult guinea pig. Nutr Metab (Lond). 2010; 7, 1–9.CrossRefGoogle ScholarPubMed
Muhlhausler, BS, Ailhaud, GP.Omega-6 polyunsaturated fatty acids and the early origins of obesity. Curr Opin Endocrinol Diabetes Obes. 2013; 20, 56–61.CrossRefGoogle ScholarPubMed
Rebholz, SL, Jones, T, Burke, KT, et al.Multiparity leads to obesity and inflammation in mothers and obesity in male offspring. AJP Endocrinol Metab. 2012; 302, E449–E457.CrossRefGoogle ScholarPubMed
Livak, KJ, Schmittgen, TD.Analysis of relative gene expression data using real-time quantitative PCR and the 2-ÄÄCT method. Methods. 2001; 25, 402–408.CrossRefGoogle Scholar
Pfaffl, MW.A new mathematical model for relative quantification in real-time RT-PCR. Nucleic Acids Res. 2001; 29, 2002–2007.CrossRefGoogle ScholarPubMed
Samuelsson, A-M, Matthews, PA, Argenton, M, et al.Diet-induced obesity in female mice leads to offspring hyperphagia, adiposity, hypertension, and insulin resistance: a novel murine model of developmental programming. Hypertension. 2008; 51, 383–392.CrossRefGoogle ScholarPubMed
Kotarsky, K, Nilsson, NE, Flodgren, E, Owman, C, Olde, B.A human cell surface receptor activated by free fatty acids and thiazolidinedione drugs. Biochem Biophys Res Commun. 2003; 301, 406–410.CrossRefGoogle ScholarPubMed
Georgiadi, A, Kersten, S.Mechanisms of gene regulation by fatty acids. Adv Nutr. 2012; 3, 127–134.10.3945/an.111.001602CrossRefGoogle ScholarPubMed
National Research Council Nutrient Requirements of Laboratory Animals: Fourth Revised Edition, 1995. Washington, DC: The National Academies Press. https://doi.org/10.17226/4758.Google Scholar
Alvheim, AR, Torstensen, BE, Lin, YH, et al.Dietary linoleic acid elevates the endocannabinoids 2-AG and anandamide and promotes weight gain in mice fed a low fat diet. Lipids. 2014; 49, 59–69.CrossRefGoogle ScholarPubMed
Grygiel-Górniak, B.Peroxisome proliferator-activated receptors and their ligands: nutritional and clinical implications – a review. Nutr J. 2014; 13, 1–10.CrossRefGoogle ScholarPubMed
Massiera, F, Weill, P, Legrand, P, Alessandri, J, Guesnet, P.Temporal changes in dietary fats: role of n-6 polyunsaturated fatty acids in excessive adipose tissue development and relationship to obesity. Prog Lipid Res. 2006; 45, 203–236.Google Scholar
Jo, J, Gavrilova, O, Pack, S, et al.Hypertrophy and/or hyperplasia: dynamics of adipose tissue growth. PLoS Comput Biol. 2009; 5, 1–11.CrossRefGoogle ScholarPubMed
Sugii, S, Evans, RM.Epigenetic codes of PPARy in metabolic disease. FEBS Lett. 2011; 585, 2121–2128.CrossRefGoogle Scholar
Wang, P, Mariman, E, Renes, J, Keijer, J.The secretory function of adipocytes in the physiology of white adipose tissue. J Cell Physiol. 2008; 216, 3–13.CrossRefGoogle ScholarPubMed
Mamounis, KJ, Hernandez, MR, Margolies, N, Yasrebi, A, Roepke, TA.Interaction of 17β-estradiol and dietary fatty acids on energy and glucose homeostasis in female mice. Nutr Neurosci. 2017; 1–14.CrossRefGoogle Scholar
Power, GW, Yaqoob, P, Harvey, DJJ, Newsholme, EAA, Calder, PCC.The effect of dietary lipid manipulation on hepatic mitochondrial phospholipid fatty acid composition and carnitine palmitoyltransferase I activity. Biochem Mol Biol Int. 1994; 34, 671–684.Google ScholarPubMed
Yin, H, Xu, L, Porter, NA.Free radical lipid peroxidation: mechanisms and analysis. Chem Rev. 2011; 111, 5944–5972.CrossRefGoogle ScholarPubMed
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