Strength training and aerobic exercise alter mitochondrial parameters in brown adipose tissue and equally reduce body adiposity in aged rats

  • Anand Thirupathi
  • Bruno Luiz da Silva Pieri
  • João Annibal Milano Peixoto Queiroz
  • Matheus Scarpatto Rodrigues
  • Gustavo de Bem Silveira
  • Daniela Roxo de Souza
  • Thais Fernandes Luciano
  • Paulo Cesar Lock Silveira
  • Claudio Teodoro De SouzaEmail author
Original Article


With aging, there is a reduction in mitochondrial activity, and several changes occur in the body composition, including increased adiposity. The dysfunction of mitochondrial activity causes changes and adaptations in tissue catabolic characteristics. Among them, we can mention brown adipose tissue (BAT). BAT’s main function is lipid oxidation for heat production, hence playing a role in adaptive thermogenesis induced by environmental factors such as exercise. It is known that exercise causes a series of metabolic changes, including loss body fat; however, there is still no consensus in the academic community about whether both strength and aerobic exercise equally reduces adiposity. Therefore, this study aimed to evaluate the effects of strength training and aerobic exercise regimes on adiposity, proteins regulating mitochondrial activity, and respiratory complexes in BAT of old rats. The rats were divided in two control groups: young control (YC; N = 5), and old control (OC; N = 5), and two exercise groups: strength training (OST; N = 5), and aerobic treadmill training (OAT; N = 5). Rats were subjected to an 8-week exercise regime, and their body composition parameters were evaluated (total body weight, adiposity index, and BAT weight). In addition, mitochondrial biogenesis proteins (PGC-1α, SIRT1, and pAMPK) and respiratory chain activity (complexes I, II/III, III, and IV) were evaluated. Results showed that OST and OAT exercise protocols significantly increased the mitochondrial regulatory molecules and respiratory chain activity, while body fat percentage and adiposity index significantly decreased. Taken together, both OST and OAT exercise increased BAT weight, activity of respiratory complexes, and regulatory proteins in BAT and equally reduced body adiposity.


Aging Physical exercise Brown adipose tissue Adiposity Metabolism 



Adenosine monophosphate-activated protein kinase


Brown adipose tissue




Ethylenediaminetetraacetic acid


Nicotinamide adenine dinucleotide dehydrogenase


Nuclear respiratory factor 1


Nuclear respiratory factor 2


Aerobic treadmill training


Old control


Strength training


Peroxisome proliferator-activated receptor gamma coactivator 1-alpha


Phenylmethylsulfonyl fluoride


Reactive oxygen species


Sodium dodecyl sulfate polyacrylamide gel electrophoresis


Sirtuin 1


Sympathetic nervous system


Vascular endothelial growth factor


Young control



This work was supported by the Universidade do Extremo Sul Catarinense, Criciuma, SC, Brazil. The Authors thanks professor Fernando Antonio Basile Colugnati of the Health Graduate Program of Juiz de Fora Federal University for statistical support.

Compliance with ethical standards

The study protocol was reviewed and approved by the local ethics committee according to the Guidelines for Animal Care and Experimentation (number 16/2013).

Conflict of interest

The authors declare that they have no conflicts of interest.


  1. 1.
    Bernlohr DA (2014) Exercise and mitochondrial function in adipose biology: all roads lead to NO. Diabetes 63(8):2606–2608CrossRefGoogle Scholar
  2. 2.
    Bostrom P, Wu J, Jedrychowski MP, Korde A, Ye L, Lo JC, Rasbach KA, Boström EA, Choi JH, Long JZ et al (2012) A PGC1-α-dependent myokine that drives brown-fat-like development of white fat and thermogenesis. Nature 481:463–468CrossRefGoogle Scholar
  3. 3.
    Boudina S, Graham TE (2014) Mitochondrial function/dysfunction in white adipose tissue. Exp Physiol 99(9):1168–1178CrossRefGoogle Scholar
  4. 4.
    Bratic A, Larsson NG (2013) The role of mitochondria in ageing. J Clin Invest 123(3):951–957CrossRefGoogle Scholar
  5. 5.
    Cannon B, Nedergaard J (2004) Brown adipose tissue: function and physiological significance. Physiol Rev 84(1):277–359CrossRefGoogle Scholar
  6. 6.
    Canto and Auwerx (2009) PGC-1alpha, SIRT1 and AMPK, an energy sensing network that controls energy expenditure. Currr Opin Lipidol 20(2):98–105CrossRefGoogle Scholar
  7. 7.
    Cassina A, Radi R (1996) Differential inhibitory action of nitric oxide and peroxynitrite on mitochondrial electron transport. Arch Biochem Biophys 328(2):309–316CrossRefGoogle Scholar
  8. 8.
    Cloos PA, Christgau S (2004) Post-translational modification of proteins: implications for aging antigen recognition, and autoimmunity. Biogerontology 5(3):139–158CrossRefGoogle Scholar
  9. 9.
    Cocco T, Sgobbo P, Clemente M, Lopriore B, Grattagliano I, Di Paola M, Villani G (2005) Tissue specific changes of mitochondrial functions in aged rats: effect of a long-term dietary treatment with N-acetylcysteine. Free Radic Biol Med 38:796–805CrossRefGoogle Scholar
  10. 10.
    Davies SM, Poljak A, Duncan MW, Smythe GA, Murphy MP (2001) Measurements of protein carbonyls, ortho and meta-tyrosine and oxidative phosphorylation complex activity in mitochondria from young and old rats. Free Radic Biol Med 31:181–190CrossRefGoogle Scholar
  11. 11.
    Fischer JC, Ruitenbeek W, Stadhouders AM, Trijbels JMF, Sengers RCA, Janssen AJM, Veerkamp JH (1985) Investigation of mitochondrial metabolism small human skeletal muscle biopsy specimens. Clin Chim Acta 145:89–100CrossRefGoogle Scholar
  12. 12.
    Fulco M, Sartorelli V (2008) Comparing and contrasting the roles of AMPK and SIRT1 in metabolic tissues. Cell Cycle 7(23):3669–3679CrossRefGoogle Scholar
  13. 13.
    Gerhart-Hines Z, Rodgers JT, Bare O, Lerin C, Kim SH, Mostoslavsky R, Alt FW, Wu Z, Puigserver P (2007) Metabolic control of muscle mitochondrial function and fatty acid oxidation through SIRT1/PGC-1 alpha. EMBO J 26(7):1913–1923CrossRefGoogle Scholar
  14. 14.
    Habinowski SA, Witters LA (2001) The effects of AICAR on adipocyte differentiation of 3T3-L1 cells. Biochem Biophys Res Commun 286(5):852–856CrossRefGoogle Scholar
  15. 15.
    Hornberger TA Jr, Farrar RP (2004) Physiological hypertrophy of the FHL muscle following 8 weeks of progressive resistance exercise in the rat. Can J Appl Physiol 29(1):16–31CrossRefGoogle Scholar
  16. 16.
    Igbal S, Ostojic O, Singh K, Joseph AM, Hood DA (2013) Expression of mitochondrial fission and fusion regulatory proteins in skeletal muscle during chronic use and disuse. Muscle Nerve 48:963–970CrossRefGoogle Scholar
  17. 17.
    Kim HS, Kim DG (2013) Effect of long-term resistance exercise on body composition, blood lipid factors, and vascular compliance in the hypertensive elderly men. J Exerc Rehabil 9(2):271–277CrossRefGoogle Scholar
  18. 18.
    Kohrt WM, Malley MT, Dalsky GP, Holloszy JO (1992) Body composition of healthy sedentary and trained, young and older men and women. Med Sci Sports Exerc 24(7):832–837CrossRefGoogle Scholar
  19. 19.
    Konopka AR, Miranda Suer K, Christopher Wolff A, Matthew Harber P (2014) Markers of human skeletal muscle mitochondrial biogenesis and quality control: effect of age and aerobic exercise training. J Gerontol A Biol Sci Med Sci 69(4):371–378CrossRefGoogle Scholar
  20. 20.
    Lagouge M, Argmann C, Gerhart-Hines Z, Meziane H, Lerin C, Daussin F, Messadeq N, Milne J, Lambert P, Elliott P, Geny B, Laakso M, Puigserver P, Auwerx J (2006) Resveratrol improves mitochondrial function and protects against metabolic disease by activating SIRT1 and PGC-1 alpha. Cell 127(6):1109–1122CrossRefGoogle Scholar
  21. 21.
    Lo KA, Sun L (2013) Turning WAT into BAT: a review on regulators controlling the browning of white adipocytes. Bio Sci Rep 33(5):e00065Google Scholar
  22. 22.
    Lowry O, Rosebrough NJ, Farr AL, Randall RJ (1951) Protein measurement with the Folin phenol reagent. J Biol Chem 193(1):265–275Google Scholar
  23. 23.
    Mennes E, Dungan CM, Frendo-Cumbo S, Williamson DL, Wright DC (2014) Aging-associated reductions in lipolytic and mitochondrial proteins in mouse adipose tissue are not rescued by metformin treatment. J Gerontol A Biol Sci Med Sci 69:1060–1068CrossRefGoogle Scholar
  24. 24.
    Niederberger E, King TS, Russe OQ, Geisslinger G (2015) Activation of AMPK and its impact on exercise capacity. Sports Med 45(11):1497–1509CrossRefGoogle Scholar
  25. 25.
    Peng XR, Gennemark P, O’Mahony G, Bartesaghi S (2015) Unlock the thermogenic potential of adipose tissue: pharmacological modulation and implication for treatment of diabetes and obesity. Front Endocrinol 6:174CrossRefGoogle Scholar
  26. 26.
    Picard F, Guarente L (2005) Molecular links between aging and adipose tissue. Int J Obes 29:S36–S39CrossRefGoogle Scholar
  27. 27.
    Picard F, Kurtev M, Chung N, Topark-Ngarm A, Senawong T, Machado De Oliveira R, Leid M, McBurney MW, Guarente L (2004) Sirt1 promotes fat mobilization in white adipocytes by repressing PPAR-gamma. Nature 429(6993):771–776CrossRefGoogle Scholar
  28. 28.
    Puigserver P, Rhee J, Lin J, Wu Z, Yoon JC, Zhang CY, Krauss S, Mootha VK, Lowell BB, Spiegelman BM (2001) Cytokine stimulation of energy expenditure through p38 MAP kinase activation of PPAR gamma coactivator-1. Mol Cell 8:971–982CrossRefGoogle Scholar
  29. 29.
    Rustin P, Chretien D, Gerard B, Bourgeron T, Rotig A, Saudubray JM, Munnich A (1994) Biochemical and molecular investigations in respiratory chain deficiencies. Clin Chim Acta 228:35–51CrossRefGoogle Scholar
  30. 30.
    Sanchez-Delgado G, Martinez-Tellez B, Olza J, Aguilera CM, Gil A, Ruiz JR (2015) Role of exercise in the activation of brown adipose tissue. Ann Nutr Metab 67(1):21–32CrossRefGoogle Scholar
  31. 31.
    Scheffer DL, Silva LA, Tromm CB, da Rosa GL, Silveiira PC, de Souza CT, Latini A, Pinho RA (2012) Impact of different resistance training protocols on muscular oxidative stress parameters. Appl Physiol Nutr Metab 37(6):1239–1246CrossRefGoogle Scholar
  32. 32.
    Stanford KI, Middelbeek RJ, Goodyear LJ (2015) Exercise effects on white adipose tissue: beiging and metabolic adaptations. Diabetes 64(7):2361–2368CrossRefGoogle Scholar
  33. 33.
    Suwa M, Nakano H, Kumagai S (2003) Effects of chronic AICAR treatment on fiber composition, enzyme activity, UCP3, and PGC-1 in rat muscles. J Appl Physiol 95:960–968CrossRefGoogle Scholar
  34. 34.
    Thirupathi A, de Souza CT (2017) Multi-regulatory network of ROS: the interconnection of ROS, PGC-1 alpha, and AMPK-SIRT1 during exercise. J Physiol Biochem 73:487–494CrossRefGoogle Scholar
  35. 35.
    Thirupathi A, Pinho R (2018) Effects of reactive oxygen species and interplay of antioxidants during physical exercise in skeletal muscles. J Physiol Biochem 74:359–367Google Scholar
  36. 36.
    Vilela TC, Muller AP, Damiani AP, Macan TP, da Silva S, Canteiro PB, de Sena Casagrande A, Pedroso GDS, Nesi RT, de Andrade VM, de Pinho RA (2017) Strength and aerobic exercises improve spatial memory in aging rats through stimulating distinct neuroplasticity mechanisms. Mol Neurobiol 54:7928–7937CrossRefGoogle Scholar
  37. 37.
    Vilela TC, Effting PS, Dos Santos Pedroso G, Farias H, Paganini L, Rebelo Sorato H, Nesi RT, de Andrade VM, de Pinho RA (2018) Aerobic and strength training induce changes in oxidative stress parameters and elicit modifications of various cellular components in skeletal muscle of aged rats. Exp Gerontol 106:21–27CrossRefGoogle Scholar
  38. 38.
    White Z, Terrill J, White RB, McMahon C, Sheard P, Grounds MD, Shavlakadze T (2016) Voluntary resistance wheel exercise from mid-life prevents sarcopenia and increases markers of mitochondrial function and autophagy in muscles of old male and female C57BL/6J mice. Skelet Muscle 6(1):45CrossRefGoogle Scholar
  39. 39.
    Woods JA, Wilund KR, Martin SA, Kistler BM (2012) Exercise, inflammation and aging. Aging Dis 3(1):130–140Google Scholar
  40. 40.
    Wright DC, Han DH, Garcia-Roves PM, Geiger PC, Jones TE, Holloszy JO (2007) Exercise induced mitochondrial biogenesis begins before the increase in muscle PGC-1 alpha expression. J Biol Chem 282(1):194–199CrossRefGoogle Scholar

Copyright information

© University of Navarra 2019

Authors and Affiliations

  • Anand Thirupathi
    • 1
    • 2
  • Bruno Luiz da Silva Pieri
    • 1
  • João Annibal Milano Peixoto Queiroz
    • 1
  • Matheus Scarpatto Rodrigues
    • 1
  • Gustavo de Bem Silveira
    • 1
  • Daniela Roxo de Souza
    • 1
  • Thais Fernandes Luciano
    • 1
  • Paulo Cesar Lock Silveira
    • 1
  • Claudio Teodoro De Souza
    • 3
    • 4
    Email author
  1. 1.Laboratory of Exercise Biochemistry and Physiology, Graduate Program in Health SciencesUniversidade do Extremo Sul CatarinenseCriciúmaBrazil
  2. 2.Laboratory of Molecular Iron metabolism, College of Life ScienceHebei Normal UniversityShijiazhuangChina
  3. 3.Department of Internal Medicine, Medicine SchoolFederal University of Juiz de ForaJuiz de ForaBrazil
  4. 4.Programa de Pós-Graduação em Saúde, Departamento de Clínica Médica, Faculdade de MedicinaUniversidade Federal de Juiz de ForaJuiz de ForaBrazil

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