Download PDF
Int J Sports Med 2015; 36(03): 226-233
DOI: 10.1055/s-0034-1390494
Training & Testing
© Georg Thieme Verlag KG Stuttgart · New York

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

U. S. Stotzer
1   Department of Physiological Sciences, Federal University of São Carlos, São Carlos, Brazil
,
M. F. C. Rodrigues
1   Department of Physiological Sciences, Federal University of São Carlos, São Carlos, Brazil
,
M. M. Domingos
1   Department of Physiological Sciences, Federal University of São Carlos, São Carlos, Brazil
,
G. H. G. Silva
1   Department of Physiological Sciences, Federal University of São Carlos, São Carlos, Brazil
,
F. O. Duarte
1   Department of Physiological Sciences, Federal University of São Carlos, São Carlos, Brazil
,
C. V. G. Gatto
2   Department of Physical Education and Human Motricity, Federal University of São Carlos, São Carlos, Brazil
,
A. C. G. O. Duarte
2   Department of Physical Education and Human Motricity, Federal University of São Carlos, São Carlos, Brazil
,
G. E. Shiguemoto
1   Department of Physiological Sciences, Federal University of São Carlos, São Carlos, Brazil
,
S. E. A. Perez
1   Department of Physiological Sciences, Federal University of São Carlos, São Carlos, Brazil
,
H. S. Selistre-de-Araujo
1   Department of Physiological Sciences, Federal University of São Carlos, São Carlos, Brazil
› Author Affiliations
Further Information

Publication History



accepted after revision 13 August 2014

Publication Date:
21 November 2014 (online)

Also available at
    Permissions and Reprints

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
    CrossrefPubMedGoogle Scholar
  • 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
    CrossrefPubMedGoogle Scholar
  • 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
    CrossrefPubMedGoogle Scholar
  • 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
    PubMedGoogle Scholar
  • 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
    CrossrefPubMedGoogle Scholar
  • 6 Cao YK, Zhang SF, Zou SE, Xia X. Daidzein improves insulin resistance in ovariectomized rats. Climacteric 2013; 16: 111-116
    CrossrefPubMedGoogle Scholar
  • 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
    CrossrefPubMedGoogle Scholar
  • 8 Czech MP, Tencerova M, Pedersen DJ, Aouadi M. Insulin signalling mechanisms for triacylglycerol storage. Diabetologia 2013; 56: 949-964
    CrossrefPubMedGoogle Scholar
  • 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
    CrossrefPubMedGoogle Scholar
  • 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
    CrossrefPubMedGoogle Scholar
  • 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
    PubMedGoogle Scholar
  • 12 Harriss DJ, Atkinson G. Ethical standards in sport and exercise science research: 2014 update. Int J Sports Med 2013; 34: 1025-1028
    Article in Thieme ConnectPubMedGoogle Scholar
  • 13 Hirsch J, Gallian E. Methods for the determination of adipose cell size in man and animals. J Lipid Res 1968; 9: 110-119
    PubMedGoogle Scholar
  • 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
    CrossrefPubMedGoogle Scholar
  • 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
    CrossrefPubMedGoogle Scholar
  • 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
    CrossrefPubMedGoogle Scholar
  • 17 Kalu DN. The ovariectomized rat model of postmenopausal bone loss. Bone Miner 1991; 15: 175-191
    CrossrefPubMedGoogle Scholar
  • 18 Kusminski CM, Scherer PE. Mitochondrial dysfunction in white adipose tissue. Trends Endocrinol Metab 2012; 23: 435-443
    CrossrefPubMedGoogle Scholar
  • 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
    CrossrefPubMedGoogle Scholar
  • 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
    Article in Thieme ConnectPubMedGoogle Scholar
  • 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
    CrossrefPubMedGoogle Scholar
  • 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
    CrossrefPubMedGoogle Scholar
  • 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
    CrossrefPubMedGoogle Scholar
  • 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
    CrossrefPubMedGoogle Scholar
  • 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
    CrossrefPubMedGoogle Scholar
  • 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
    CrossrefPubMedGoogle Scholar
  • 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
    CrossrefPubMedGoogle Scholar
  • 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
    CrossrefPubMedGoogle Scholar
  • 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
    PubMedGoogle Scholar
  • 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
    CrossrefPubMedGoogle Scholar
  • 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
    Article in Thieme ConnectPubMedGoogle Scholar
  • 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
    CrossrefPubMedGoogle Scholar
  • 33 Rosano GM, Vitale C, Marazzi G, Volterrani M. Menopause and cardiovascular disease: the evidence. Climacteric 2007; 10: 19-24
    CrossrefPubMedGoogle Scholar
  • 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
    CrossrefPubMedGoogle Scholar
  • 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
    CrossrefPubMedGoogle Scholar
  • 36 Spriet LL. New insights into the interaction of carbohydrate and fat metabolism during exercise. Sports Med 2014; 44 (Suppl. 01) S87-S96
    CrossrefPubMedGoogle Scholar
  • 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
    CrossrefPubMedGoogle Scholar
  • 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
    CrossrefPubMedGoogle Scholar
  • 39 Tchernof A, Despres JP. Pathophysiology of human visceral obesity: an update. Physiol Rev 2013; 93: 359-404
    CrossrefPubMedGoogle Scholar
  • 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
    CrossrefPubMedGoogle Scholar
  • 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
    PubMedGoogle Scholar
  • 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
    CrossrefPubMedGoogle Scholar
  • 43 White UA, Stephens JM. Transcriptional factors that promote formation of white adipose tissue. Mol Cell Endocrinol 2010; 318: 10-14
    CrossrefPubMedGoogle Scholar
  • 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
    PubMedGoogle Scholar
  • 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
    CrossrefPubMedGoogle Scholar
  • 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
    PubMedGoogle Scholar
  • 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
    CrossrefPubMedGoogle Scholar
  • 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
    CrossrefPubMedGoogle Scholar