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Journal of Physiology and Biochemistry

, Volume 74, Issue 2, pp 235–246 | Cite as

Physical exercise mitigates high-fat diet-induced adiposopathy and related endocrine alterations in an animal model of obesity

  • Sílvia Rocha-RodriguesEmail author
  • Inês O. Gonçalves
  • Jorge Beleza
  • António Ascensão
  • José Magalhães
Original Article

Abstract

The dysregulation of adipokine secretion owing to adiposopathy can contribute to the pathogenesis of obesity-related disorders. Being that exercise is an advised strategy against obesity-induced adiposopathy, we aimed to analyze the role of physical exercise as a preventive and therapeutic strategy against high-fat diet (HFD)-induced adipokine and ghrelin alterations. Rats were pair-fed the Lieber De Carli standard diet (S, 35 Kcal% fat) or HFD (71 Kcal% fat) over 17 weeks. Animals were assigned into four groups as follows: standard diet sedentary (SS), standard diet voluntary physical activity (SVPA), high-fat diet sedentary (HS), and high-fat diet voluntary physical activity (HVPA). After 9 weeks of dietary treatment, half of the SS and HS animals were submitted to an 8-week endurance training program, standard diet endurance training (SET), and high-fat-diet endurance training (HET) groups, maintaining the respective diets. Although there were no changes in body weight, HFD increased visceral adiposity, percentage of large adipocytes, hypoxia inducible factor (HIF)-1α, and leptin contents in epididymal adipose tissue (eWAT) and decreased plasma content of adiponectin (AdipQ). Both VPA and ET decreased visceral adiposity and percentage of large adipocytes in HFD-fed animals, but ET also increased the percentage of small- to medium-sized adipocytes. VPA increased plasma growth hormone secretagogue receptor (GHS-R) and decreased leptin protein in HVPA group. ET decreased plasma insulin and leptin levels and eWAT HIF-1α and leptin expression in HET group. Moreover, ET improved insulin sensitivity, plasma high molecular weight, and AdipQ and ghrelin levels and increased eWAT and GHS-R expression. Our data suggest that exercise, particularly ET, reverted adiposopathy and related endocrine alterations induced by an isocaloric HFD pair-fed diet.

Keywords

Obesity Adiposopathy Endurance training High molecular weight adiponectin Ghrelin Leptin 

Notes

Acknowledgements

We are thankful to Alexandra Holy, MPP/MBA, Mills College, Oakland, CA, USA, for proofreading the English language of the manuscript.

Funding sources

This work was supported by a grant from the Portuguese Foundation for Science and Technology (FCT) to the Research Center in Physical Activity, Health and Leisure, UID/DTP/00617/2013; to JM PTDC/DTP-DES/7087/2014, POCI-01-0145-FEDER-016690; and to S.R-R, SFRH/BD/89807/2012.

Compliance with ethical standards

Conflict of interest

The authors declare that they have no conflict of interest.

References

  1. 1.
    Asada K, Yoshiji H, Noguchi R, Ikenaka Y, Kitade M, Kaji K, Yoshii J, Yanase K, Namisaki T, Yamazaki M, Tsujimoto T, Akahane T, Uemura M, Fukui H (2007) Crosstalk between high-molecular-weight adiponectin and T-cadherin during liver fibrosis development in rats. Int J Mol Med 20(5):725–729PubMedGoogle Scholar
  2. 2.
    Bays HE, Gonzalez-Campoy JM, Henry RR, Bergman DA, Kitabchi AE, Schorr AB, Rodbard HW (2008) Is adiposopathy (sick fat) an endocrine disease? Int J Clin Pract 62(10):1474–1483.  https://doi.org/10.1111/j.1742-1241.2008.01848.x CrossRefPubMedPubMedCentralGoogle Scholar
  3. 3.
    Berg AH, Combs TP, Scherer PE (2002) ACRP30/adiponectin: an adipokine regulating glucose and lipid metabolism. Trends Endocrinol Metab 13(2):84–89.  https://doi.org/10.1016/S1043-2760(01)00524-0 CrossRefPubMedGoogle Scholar
  4. 4.
    Betz MJ, Bielohuby M, Mauracher B, Abplanalp W, Muller HH, Pieper K, Ramisch J, Tschop MH, Beuschlein F, Bidlingmaier M, Slawik M (2012) Isoenergetic feeding of low carbohydrate-high fat diets does not increase brown adipose tissue thermogenic capacity in rats. PLoS One 7(6):e38997.  https://doi.org/10.1371/journal.pone.0038997 CrossRefPubMedPubMedCentralGoogle Scholar
  5. 5.
    Bluher M, Brennan AM, Kelesidis T, Kratzsch J, Fasshauer M, Kralisch S, Williams CJ, Mantzoros CS (2007) Total and high-molecular weight adiponectin in relation to metabolic variables at baseline and in response to an exercise treatment program: comparative evaluation of three assays. Diabetes Care 30(2):280–285.  https://doi.org/10.2337/dc06-1362 CrossRefPubMedGoogle Scholar
  6. 6.
    Cacho J, Sevillano J, de Castro J, Herrera E, Ramos MP (2008) Validation of simple indexes to assess insulin sensitivity during pregnancy in Wistar and Sprague-Dawley rats. Am J Phys Endocrinol Metab 295(5):E1269–E1276.  https://doi.org/10.1152/ajpendo.90207.2008 CrossRefGoogle Scholar
  7. 7.
    Delporte C (2013) Structure and physiological actions of ghrelin. Scientifica 2013:518909–518925.  https://doi.org/10.1155/2013/518909 CrossRefPubMedPubMedCentralGoogle Scholar
  8. 8.
    Ebrahimi M, Rahmani-Nia F, Damirchi A, Mirzaie B, Asghar Pur S (2013) Effect of short-term exercise on appetite, energy intake and energy-regulating hormones. Iran J Basic Med Sci 16(7):829–834PubMedPubMedCentralGoogle Scholar
  9. 9.
    Espelund U, Hansen TK, Hojlund K, Beck-Nielsen H, Clausen JT, Hansen BS, Orskov H, Jorgensen JO, Frystyk J (2005) Fasting unmasks a strong inverse association between ghrelin and cortisol in serum: studies in obese and normal-weight subjects. J Clin Endocrinol Metab 90(2):741–746.  https://doi.org/10.1210/jc.2004-0604 CrossRefPubMedGoogle Scholar
  10. 10.
    Ghanbari-Niaki A, Jafari A, Moradi M, Kraemer RR (2011) Short-,moderate-, and long-term treadmill training protocols reduce plasma, fundus, but not small intestine ghrelin concentrations in male rats. J Endocrinol Investig 34(6):439–443.  https://doi.org/10.3275/7437.10.1007/bf03346710 CrossRefGoogle Scholar
  11. 11.
    Gollisch KS, Brandauer J, Jessen N, Toyoda T, Nayer A, Hirshman MF, Goodyear LJ (2009) Effects of exercise training on subcutaneous and visceral adipose tissue in normal- and high-fat diet-fed rats. Am J Phys Endocrinol Metab 297(2):E495–E504.  https://doi.org/10.1152/ajpendo.90424.2008 CrossRefGoogle Scholar
  12. 12.
    Goncalves IO, Passos E, Rocha-Rodrigues S, Torrella JR, Rizo D, Santos-Alves E, Portincasa P, Martins MJ, Ascensao A, Magalhaes J (2014) Physical exercise antagonizes clinical and anatomical features characterizing Lieber-DeCarli diet-induced obesity and related metabolic disorders. Clinical Nutrition (Edinburgh, Scotland) 34(2):241–247.  https://doi.org/10.1016/j.clnu.2014.03.010 CrossRefGoogle Scholar
  13. 13.
    Holland AM, Kephart WC, Mumford PW, Mobley CB, Lowery RP, Shake JJ, Patel RK, Healy JC, McCullough DJ, Kluess HA, Huggins KW, Kavazis AN, Wilson JM, Roberts MD (2016) Effects of a ketogenic diet on adipose tissue, liver, and serum biomarkers in sedentary rats and rats that exercised via resisted voluntary wheel running. Am J Physiol Regul Integr Comp Physiol 311(2):R337–R351.  https://doi.org/10.1152/ajpregu.00156.2016 CrossRefPubMedGoogle Scholar
  14. 14.
    Hopkins M, Blundell JE (2016) Energy balance, body composition, sedentariness and appetite regulation: pathways to obesity. Clin Sci 130(18):1615–1628.  https://doi.org/10.1042/cs20160006 CrossRefPubMedGoogle Scholar
  15. 15.
    Jacobs K, Brouha S, Bettencourt R, Barrett-Connor E, Sirlin C, Loomba R (2016) Association of nonalcoholic fatty liver disease with visceral adiposity but not coronary artery calcification in the elderly. Clin Gastroenterol Hepatol 14:1337–1344 e1333.  https://doi.org/10.1016/j.cgh.2016.01.010 CrossRefPubMedGoogle Scholar
  16. 16.
    Kang J, Robertson RJ, Hagberg JM, Kelley DE, Goss FL, DaSilva SG, Suminski RR, Utter AC (1996) Effect of exercise intensity on glucose and insulin metabolism in obese individuals and obese NIDDM patients. Diabetes Care 19(4):341–349.  https://doi.org/10.2337/diacare.19.4.341 CrossRefPubMedGoogle Scholar
  17. 17.
    Kim DY, Seo BD, Kim DJ (2014) Effect of walking exercise on changes in cardiorespiratory fitness, metabolic syndrome markers, and high-molecular-weight adiponectin in obese middle-aged women. J Phys Ther Sci 26(11):1723–1727.  https://doi.org/10.1589/jpts.26.1723 CrossRefPubMedPubMedCentralGoogle Scholar
  18. 18.
    Klimcakova E, Polak J, Moro C, Hejnova J, Majercik M, Viguerie N, Berlan M, Langin D, Stich V (2006) Dynamic strength training improves insulin sensitivity without altering plasma levels and gene expression of adipokines in subcutaneous adipose tissue in obese men. J Clin Endocrinol Metab 91(12):5107–5112.  https://doi.org/10.1210/jc.2006-0382 CrossRefPubMedGoogle Scholar
  19. 19.
    Krskova K, Eckertova M, Kukan M, Kuba D, Kebis A, Olszanecki R, Suski M, Gajdosechova L, Zorad S (2012) Aerobic training lasting for 10 weeks elevates the adipose tissue FABP4, Gialpha, and adiponectin expression associated by a reduced protein oxidation. Endocr Regul 46(03):137–146.  https://doi.org/10.4149/endo_2012_03_137 CrossRefPubMedGoogle Scholar
  20. 20.
    Lara-Castro C, Luo N, Wallace P, Klein RL, Garvey WT (2006) Adiponectin multimeric complexes and the metabolic syndrome trait cluster. Diabetes 55(1):249–259.  https://doi.org/10.2337/diabetes.55.01.06.db05-1105 CrossRefPubMedGoogle Scholar
  21. 21.
    Li X, Lian F, Liu C, Hu KQ, Wang XD (2015) Isocaloric pair-fed high-carbohydrate diet induced more hepatic steatosis and inflammation than high-fat diet mediated by miR-34a/SIRT1 axis in mice. Sci Rep 5(1):16774.  https://doi.org/10.1038/srep16774 CrossRefPubMedPubMedCentralGoogle Scholar
  22. 22.
    Linden MA, Pincu Y, Martin SA, Woods JA, Baynard T (2014) Moderate exercise training provides modest protection against adipose tissue inflammatory gene expression in response to high-fat feeding. Physiol Rep 2(7):e12071.  https://doi.org/10.14814/phy2.12071 CrossRefPubMedPubMedCentralGoogle Scholar
  23. 23.
    Magalhaes J, Goncalves IO, Lumini-Oliveira J, Marques-Aleixo I, Passos E, Rocha-Rodrigues S, Machado NG, Moreira AC, Rizo D, Viscor G, Oliveira PJ, Torrella JR, Ascensao A (2014) Modulation of cardiac mitochondrial permeability transition and apoptotic signaling by endurance training and intermittent hypobaric hypoxia. Int J Cardiol 173(1):40–45.  https://doi.org/10.1016/j.ijcard.2014.02.011 CrossRefPubMedGoogle Scholar
  24. 24.
    Mason C, Xiao L, Imayama I, Duggan CR, Campbell KL, Kong A, Wang CY, Alfano CM, Blackburn GL, Foster-Schubert KE, McTiernan A (2015) The effects of separate and combined dietary weight loss and exercise on fasting ghrelin concentrations in overweight and obese women: a randomized controlled trial. Clin Endocrinol 82(3):369–376.  https://doi.org/10.1111/cen.12483 CrossRefGoogle Scholar
  25. 25.
    Mihalache L, Gherasim A, Nita O, Ungureanu MC, Padureanu SS, Gavril RS, Arhire LI (2016) Effects of ghrelin in energy balance and body weight homeostasis. Hormones (Athens) 15(2):186–196.  https://doi.org/10.14310/horm.2002.1672 CrossRefGoogle Scholar
  26. 26.
    Miyatake N, Takahashi K, Wada J, Nishikawa H, Morishita A, Suzuki H, Kunitomi M, Makino H, Kira S, Fujii M (2004) Changes in serum leptin concentrations in overweight Japanese men after exercise. Diabetes Obes Metab 6(5):332–337.  https://doi.org/10.1111/j.1462-8902.2004.00351.x CrossRefPubMedGoogle Scholar
  27. 27.
    Miyazaki S, Izawa T, Ogasawara JE, Sakurai T, Nomura S, Kizaki T, Ohno H, Komabayashi T (2010) Effect of exercise training on adipocyte-size-dependent expression of leptin and adiponectin. Life Sci 86(17-18):691–698.  https://doi.org/10.1016/j.lfs.2010.03.004 CrossRefPubMedGoogle Scholar
  28. 28.
    Nogueiras R, Tschop MH, Zigman JM (2008) Central nervous system regulation of energy metabolism: ghrelin versus leptin. Ann N Y Acad Sci 1126(1):14–19.  https://doi.org/10.1196/annals.1433.054 CrossRefPubMedPubMedCentralGoogle Scholar
  29. 29.
    Novelli EL, Diniz YS, Galhardi CM, Ebaid GM, Rodrigues HG, Mani F, Fernandes AA, Cicogna AC, Novelli Filho JL (2007) Anthropometrical parameters and markers of obesity in rats. Lab Anim 41(1):111–119.  https://doi.org/10.1258/002367707779399518 CrossRefPubMedGoogle Scholar
  30. 30.
    Numao S, Katayama Y, Hayashi Y, Matsuo T, Tanaka K (2011) Influence of acute aerobic exercise on adiponectin oligomer concentrations in middle-aged abdominally obese men. Metab Clin Exp 60(2):186–194.  https://doi.org/10.1016/j.metabol.2009.12.011 CrossRefPubMedGoogle Scholar
  31. 31.
    O'Leary VB, Jorett AE, Marchetti CM, Gonzalez F, Phillips SA, Ciaraldi TP, Kirwan JP (2007) Enhanced adiponectin multimer ratio and skeletal muscle adiponectin receptor expression following exercise training and diet in older insulin-resistant adults. Am J Phys Endocrinol Metab 293(1):E421–E427.  https://doi.org/10.1152/ajpendo.00123.2007 CrossRefGoogle Scholar
  32. 32.
    Purnell JQ, Weigle DS, Breen P, Cummings DE (2003) Ghrelin levels correlate with insulin levels, insulin resistance, and high-density lipoprotein cholesterol, but not with gender, menopausal status, or cortisol levels in humans. J Clin Endocrinol Metab 88(12):5747–5752.  https://doi.org/10.1210/jc.2003-030513 CrossRefPubMedGoogle Scholar
  33. 33.
    Reseland JE, Anderssen SA, Solvoll K, Hjermann I, Urdal P, Holme I, Drevon CA (2001) Effect of long-term changes in diet and exercise on plasma leptin concentrations. Am J Clin Nutr 73(2):240–245CrossRefPubMedGoogle Scholar
  34. 34.
    Sun Y (2015) Ghrelin receptor controls obesity by fat burning. Oncotarget 6(9):6470–6471.  https://doi.org/10.18632/oncotarget.3668 CrossRefPubMedPubMedCentralGoogle Scholar
  35. 35.
    Tiryaki-Sonmez G, Ozen S, Bugdayci G, Karli U, Ozen G, Cogalgil S, Schoenfeld B, Sozbir K, Aydin K (2013) Effect of exercise on appetite-regulating hormones in overweight women. Biol Sport 30(2):75–80.  https://doi.org/10.5604/20831862.1044220 CrossRefPubMedPubMedCentralGoogle Scholar
  36. 36.
    Vilela BS, Vasques AC, Cassani RS, Forti AC, Pareja JC, Tambascia MA, Geloneze B (2016) The HOMA-adiponectin (HOMA-AD) closely mirrors the HOMA-IR index in the screening of insulin resistance in the Brazilian Metabolic Syndrome Study (BRAMS). PLoS One 11(8):e0158751.  https://doi.org/10.1371/journal.pone.0158751 CrossRefPubMedPubMedCentralGoogle Scholar
  37. 37.
    Yamauchi T, Kamon J, Ito Y, Tsuchida A, Yokomizo T, Kita S, Sugiyama T, Miyagishi M, Hara K, Tsunoda M, Murakami K, Ohteki T, Uchida S, Takekawa S, Waki H, Tsuno NH, Shibata Y, Terauchi Y, Froguel P, Tobe K, Koyasu S, Taira K, Kitamura T, Shimizu T, Nagai R, Kadowaki T (2003) Cloning of adiponectin receptors that mediate antidiabetic metabolic effects. Nature 423(6941):762–769.  https://doi.org/10.1038/nature01705 CrossRefPubMedGoogle Scholar
  38. 38.
    Ye J, Gao Z, Yin J, He Q (2007) Hypoxia is a potential risk factor for chronic inflammation and adiponectin reduction in adipose tissue of ob/ob and dietary obese mice. Am J Phys Endocrinol Metab 293(4):E1118–E1128.  https://doi.org/10.1152/ajpendo.00435.2007 CrossRefGoogle Scholar

Copyright information

© University of Navarra 2018

Authors and Affiliations

  • Sílvia Rocha-Rodrigues
    • 1
    Email author
  • Inês O. Gonçalves
    • 1
  • Jorge Beleza
    • 1
  • António Ascensão
    • 1
  • José Magalhães
    • 1
  1. 1.CIAFEL—Research Centre in Physical Activity, Health and Leisure, Faculty of Sport SciencesUniversity of PortoPortoPortugal

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