Resistance Training Suppresses Intra-abdominal Fatty Acid Synthesis in Ovariectomized Rats

Abstract

Ovarian hormone loss is associated with a shift in fat distribution to intra-abdomin al adipose tissue (intra-AAT) depots and with lipid metabolism disorders, which predisposes individuals to developing insulin resistance. Resistance training (RT) prevents increases in intra-AAT after ovarian hormone loss. However, the molecular mechanisms underlying these changes remain unclear. We investigated the effects of ovariectomy and RT on gene expression related to lipogenesis and fat oxidation in the intra-AAT of ovariectomized rats. Sprague-Dawley rats (n=6/group) were divided into the groups: sham-sedentary, ovariectomized-sedentary, sham-RT and ovariectomized-RT. RT groups performed a 10-week climbing program on a ladder with progressive overload. Intra-AAT was subjected to morphometric and mRNA analysis. Ovariectomized-sedentary group had larger adipocytes and higher expression of peroxisome proliferator-activated receptor-γ (PPAR-γ), sterol regulatory element-binding protein-1c (SREBP-1c), stearoyl-CoA desaturase-1 (SCD-1), acetyl-CoA carboxylase (ACC), hormone-sensitive lipase (HSL) and lower expression of the oxidative carnitinepalmitoyltransferase-I (CPT-1). RT counteracted OVX-induced increases in PPAR-γ and SCD-1 and decreased SREBP-1c. ACC and HSL were downregulated in ovariectomized-RT compared with the ovariectomized-sedentary group. Ovariectomized-RT group had the highest CPT-1 gene expression. Adipocyte size decreased in ovariectomized-RT group. Results suggest that RT reduces intra-AAT adipocyte size in ovariectomized rats by suppressing intra-AAT fatty acid synthesis and enhancing fatty acid β-oxidation.

Key words

exercise training - lipid metabolism - visceral adipose tissue - ovarian hormone deficiency

• References

• 1 Andersson T, Soderstrom I, Simonyte K, Olsson T. Estrogen reduces 11beta-hydroxysteroid dehydrogenase type 1 in liver and visceral, but not subcutaneous, adipose tissue in rats. Obesity (Silver Spring) 2010; 18: 470-475
• 2 Bea JW, Cussler EC, Going SB, Blew RM, Metcalfe LL, Lohman TG. Resistance training predicts 6-yr body composition change in postmenopausal women. Med Sci Sports Exerc 2010; 42: 1286-1295
• 3 Berkemeyer S. Acid-base balance and weight gain: are there crucial links via protein and organic acids in understanding obesity?. Med Hypotheses 2009; 73: 347-356
• 4 Bouwman FG, Wang P, van Baak M, Saris WH, Mariman EC. Increased beta-oxidation with improved glucose uptake capacity in adipose tissue from obese after weight loss and maintenance. Obesity (Silver Spring) 2013; 22: 819-827
• 5 Camporez JP, Jornayvaz FR, Lee HY, Kanda S, Guigni BA, Kahn M, Samuel VT, Carvalho CR, Petersen KF, Jurczak MJ, Shulman GI. Cellular mechanism by which estradiol protects female ovariectomized mice from high-fat diet-induced hepatic and muscle insulin resistance. Endocrinology 2013; 154: 1021-1028
• 6 Cao YK, Zhang SF, Zou SE, Xia X. Daidzein improves insulin resistance in ovariectomized rats. Climacteric 2013; 16: 111-116
• 7 Cedernaes J, Alsio J, Vastermark A, Riserus U, Schioth HB. Adipose tissue stearoyl-CoA desaturase 1 index is increased and linoleic acid is decreased in obesity-prone rats fed a high-fat diet. Lipids Health Dis 2013; 12: 1-11
• 8 Czech MP, Tencerova M, Pedersen DJ, Aouadi M. Insulin signalling mechanisms for triacylglycerol storage. Diabetologia 2013; 56: 949-964
• 9 D'Eon TM, Souza SC, Aronovitz M, Obin MS, Fried SK, Greenberg AS. Estrogen regulation of adiposity and fuel partitioning. Evidence of genomic and non-genomic regulation of lipogenic and oxidative pathways. J Biol Chem 2005; 280: 35983-35991
• 10 Enevoldsen LH, Stallknecht B, Langfort J, Petersen LN, Holm C, Ploug T, Galbo H. The effect of exercise training on hormone-sensitive lipase in rat intra-abdominal adipose tissue and muscle. J Physiol 2001; 536: 871-877
• 11 Flachs P, Rossmeisl M, Kuda O, Kopecky J. Stimulation of mitochondrial oxidative capacity in white fat independent of UCP1: A key to lean phenotype. Biochim Biophys Acta 2013; 986-1003
• 12 Harriss DJ, Atkinson G. Ethical standards in sport and exercise science research: 2014 update. Int J Sports Med 2013; 34: 1025-1028
• 13 Hirsch J, Gallian E. Methods for the determination of adipose cell size in man and animals. J Lipid Res 1968; 9: 110-119
• 14 Hornberger TA, Farrar RP. Physiological hypertrophy of the FHL muscle following 8 weeks of progressive resistance exercise in the rat. Can J Appl Physiol 2004; 29: 16-31
• 15 Isken F, Pfeiffer AF, Nogueiras R, Osterhoff MA, Ristow M, Thorens B, Tschop MH, Weickert MO. Deficiency of glucose-dependent insulinotropic polypeptide receptor prevents ovariectomy-induced obesity in mice. Am J Physiol 2008; 295: E350-E355
• 16 Iwata T, Taniguchi H, Kuwajima M, Taniguchi T, Okuda Y, Sukeno A, Ishimoto K, Mizusawa N, Yoshimoto K. The action of D-dopachrome tautomerase as an adipokine in adipocyte lipid metabolism. PLoS One 2012; 7: e33402
• 17 Kalu DN. The ovariectomized rat model of postmenopausal bone loss. Bone Miner 1991; 15: 175-191
• 18 Kusminski CM, Scherer PE. Mitochondrial dysfunction in white adipose tissue. Trends Endocrinol Metab 2012; 23: 435-443
• 19 Leite RD, Prestes J, Bernardes CF, Shiguemoto GE, Pereira GB, Duarte JO, Domingos MM, Baldissera V, de Andrade Perez SE. Effects of ovariectomy and resistance training on lipid content in skeletal muscle, liver, and heart; fat depots; and lipid profile. Appl Physiol Nutr Metab 2009; 34: 1079-1086
• 20 Leite RD, Prestes J, Pereira GB, Shiguemoto GE, Perez SE. Menopause: highlighting the effects of resistance training. Int J Sports Med 2010; 31: 761-767
• 21 Livak KJ, Schmittgen TD. Analysis of relative gene expression data using real-time quantitative PCR and the 2(-Delta Delta C(T)) Method. Methods 2001; 25: 402-408
• 22 Lovejoy JC, Champagne CM, de Jonge L, Xie H, Smith SR. Increased visceral fat and decreased energy expenditure during the menopausal transition. Int J Obes (Lond) 2008; 32: 949-958
• 23 Lundholm L, Zang H, Hirschberg AL, Gustafsson JA, Arner P, Dahlman-Wright K. Key lipogenic gene expression can be decreased by estrogen in human adipose tissue. Fertil Steril 2008; 90: 44-48
• 24 Mauvais-Jarvis F, Clegg DJ, Hevener AL. The Role of Estrogens in Control of Energy Balance and Glucose Homeostasis. Endocr Rev 2013; 34: 309-338
• 25 Messier V, Rabasa-Lhoret R, Barbat-Artigas S, Elisha B, Karelis AD, Aubertin-Leheudre M. Menopause and sarcopenia: A potential role for sex hormones. Maturitas 2011; 68: 331-336
• 26 Morgan K, Uyuni A, Nandgiri G, Mao L, Castaneda L, Kathirvel E, French SW, Morgan TR. Altered expression of transcription factors and genes regulating lipogenesis in liver and adipose tissue of mice with high fat diet-induced obesity and nonalcoholic fatty liver disease. Eur J Gastroenterol Hepatol 2008; 20: 843-854
• 27 Nakayama H, Otabe S, Ueno T, Hirota N, Yuan X, Fukutani T, Hashinaga T, Wada N, Yamada K. Transgenic mice expressing nuclear sterol regulatory element-binding protein 1c in adipose tissue exhibit liver histology similar to nonalcoholic steatohepatitis. Metabolism 2007; 56: 470-475
• 28 Orsatti FL, Nahas EA, Maesta N, Nahas-Neto J, Burini RC. Plasma hormones, muscle mass and strength in resistance-trained postmenopausal women. Maturitas 2008; 59: 394-404
• 29 Palou M, Priego T, Sanchez J, Rodriguez AM, Palou A, Pico C. Gene expression patterns in visceral and subcutaneous adipose depots in rats are linked to their morphologic features. Int J Exp Cell Physiol Biochem Pharmacol 2009; 24: 547-556
• 30 Palou M, Sanchez J, Priego T, Rodriguez AM, Pico C, Palou A. Regional differences in the expression of genes involved in lipid metabolism in adipose tissue in response to short- and medium-term fasting and refeeding. J Nutr Biochem 2010; 21: 23-33
• 31 Prestes J, Leite RD, Pereira GB, Shiguemoto GE, Bernardes CF, Asano RY, Sales MM, Bartholomeu Neto J, Perez SE. Resistance Training and Glycogen Content in Ovariectomized Rats. Int J Sports Med 2011; 33: 550-554
• 32 Rogers NH, Perfield 2nd JW, Strissel KJ, Obin MS, Greenberg AS. Reduced energy expenditure and increased inflammation are early events in the development of ovariectomy-induced obesity. Endocrinology 2009; 150: 2161-2168
• 33 Rosano GM, Vitale C, Marazzi G, Volterrani M. Menopause and cardiovascular disease: the evidence. Climacteric 2007; 10: 19-24
• 34 Saengsirisuwan V, Pongseeda S, Prasannarong M, Vichaiwong K, Toskulkao C. Modulation of insulin resistance in ovariectomized rats by endurance exercise training and estrogen replacement. Metabolism 2009; 58: 38-47
• 35 Shiguemoto GE, Prestes J, Leite RD, Pereira GB, Pontes CL, D’Avila FV, Botero JP, Baldissera V, Nonaka KO, Selistre-de-Araujo HS, Perez SE. Effects of resistance training on matrix metalloproteinase-2 activity and biomechanical and physical properties of bone in ovariectomized and intact rats. Scand J Med Sci Sports 2012; 22: 607-617
• 36 Spriet LL. New insights into the interaction of carbohydrate and fat metabolism during exercise. Sports Med 2014; 44 (Suppl. 01) S87-S96
• 37 Strasser B, Arvandi M, Siebert U. Resistance training, visceral obesity and inflammatory response: a review of the evidence. Obes Rev 2012; 13: 578-591
• 38 Stubbins RE, Najjar K, Holcomb VB, Hong J, Nunez NP. Oestrogen alters adipocyte biology and protects female mice from adipocyte inflammation and insulin resistance. Diabetes Obes Metab 2012; 14: 58-66
• 39 Tchernof A, Despres JP. Pathophysiology of human visceral obesity: an update. Physiol Rev 2013; 93: 359-404
• 40 Vieira Potter VJ, Strissel KJ, Xie C, Chang E, Bennett G, Defuria J, Obin MS, Greenberg AS. Adipose tissue inflammation and reduced insulin sensitivity in ovariectomized mice occurs in the absence of increased adiposity. Endocrinology 2012; 153: 4266-4277
• 41 Walsh NP, Gleeson M, Shephard RJ, Woods JA, Bishop NC, Fleshner M, Green C, Pedersen BK, Hoffman-Goetz L, Rogers CJ, Northoff H, Abbasi A, Simon P. Position statement. Part one: Immune function and exercise. Exerc Immunol Rev 2011; 17: 6-63
• 42 Watt MJ, Heigenhauser GJ, Spriet LL. Effects of dynamic exercise intensity on the activation of hormone-sensitive lipase in human skeletal muscle. J Physiol 2003; 547: 301-308
• 43 White UA, Stephens JM. Transcriptional factors that promote formation of white adipose tissue. Mol Cell Endocrinol 2010; 318: 10-14
• 44 Yang YK, Chen M, Clements RH, Abrams GA, Aprahamian CJ, Harmon CM. Human mesenteric adipose tissue plays unique role versus subcutaneous and omental fat in obesity related diabetes. Int J Exp Cell Physiol Biochem Pharmacol 2008; 22: 531-538
• 45 You T, Arsenis NC, Disanzo BL, Lamonte MJ. Effects of exercise training on chronic inflammation in obesity: current evidence and potential mechanisms. Sports Med 2013; 43: 243-256
• 46 Zamboni M, Rossi AP, Fantin F, Zamboni G, Chirumbolo S, Zoico E, Mazzali G. Adipose tissue, diet and aging. Mech Ageing Dev 2014; 136–137: 129-137
• 47 Zang Y, Wang T, Xie W, Wang-Fischer YL, Getty L, Han J, Corkey BE, Guo W. Regulation of acetyl CoA carboxylase and carnitine palmitoyl transferase-1 in rat adipocytes. Obes Res 2005; 13: 1530-1539
• 48 Zivkovic TB, Vuksanovic M, Jelic MA, Stojanovic J, Buric B, Jojic B, Milic N, Vujovic S. Obesity and metabolic syndrome during the menopause transition in Serbian women. Climacteric 2011; 14: 643-648