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

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Abstract

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.

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Abbreviations

AMPK:

Adenosine monophosphate-activated protein kinase

BAT:

Brown adipose tissue

DTT:

Dithiothreitol

EDTA:

Ethylenediaminetetraacetic acid

NADH:

Nicotinamide adenine dinucleotide dehydrogenase

NRF-1:

Nuclear respiratory factor 1

NRF-2:

Nuclear respiratory factor 2

OAT:

Aerobic treadmill training

OC:

Old control

OST:

Strength training

PGC-1α:

Peroxisome proliferator-activated receptor gamma coactivator 1-alpha

PMSF:

Phenylmethylsulfonyl fluoride

ROS:

Reactive oxygen species

SDS-PAGE:

Sodium dodecyl sulfate polyacrylamide gel electrophoresis

SIRT1:

Sirtuin 1

SNS:

Sympathetic nervous system

VEGF:

Vascular endothelial growth factor

YC:

Young control

References

  1. Bernlohr DA (2014) Exercise and mitochondrial function in adipose biology: all roads lead to NO. Diabetes 63(8):2606–2608

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  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 481:463–468

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  3. Boudina S, Graham TE (2014) Mitochondrial function/dysfunction in white adipose tissue. Exp Physiol 99(9):1168–1178

    Article  PubMed  Google Scholar 

  4. Bratic A, Larsson NG (2013) The role of mitochondria in ageing. J Clin Invest 123(3):951–957

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  5. Cannon B, Nedergaard J (2004) Brown adipose tissue: function and physiological significance. Physiol Rev 84(1):277–359

    Article  CAS  PubMed  Google Scholar 

  6. Canto and Auwerx (2009) PGC-1alpha, SIRT1 and AMPK, an energy sensing network that controls energy expenditure. Currr Opin Lipidol 20(2):98–105

    Article  CAS  Google Scholar 

  7. Cassina A, Radi R (1996) Differential inhibitory action of nitric oxide and peroxynitrite on mitochondrial electron transport. Arch Biochem Biophys 328(2):309–316

    Article  CAS  PubMed  Google Scholar 

  8. Cloos PA, Christgau S (2004) Post-translational modification of proteins: implications for aging antigen recognition, and autoimmunity. Biogerontology 5(3):139–158

    Article  CAS  PubMed  Google Scholar 

  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 38:796–805

    Article  CAS  PubMed  Google Scholar 

  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 31:181–190

    Article  CAS  PubMed  Google Scholar 

  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 145:89–100

    Article  CAS  PubMed  Google Scholar 

  12. Fulco M, Sartorelli V (2008) Comparing and contrasting the roles of AMPK and SIRT1 in metabolic tissues. Cell Cycle 7(23):3669–3679

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  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):1913–1923

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  14. Habinowski SA, Witters LA (2001) The effects of AICAR on adipocyte differentiation of 3T3-L1 cells. Biochem Biophys Res Commun 286(5):852–856

    Article  CAS  PubMed  Google Scholar 

  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):16–31

    Article  CAS  PubMed  Google Scholar 

  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 48:963–970

    Article  CAS  Google Scholar 

  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):271–277

    Article  PubMed  PubMed Central  Google Scholar 

  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):832–837

    Article  CAS  PubMed  Google Scholar 

  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):371–378

    Article  CAS  PubMed  Google Scholar 

  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):1109–1122

    Article  CAS  PubMed  Google Scholar 

  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):e00065

    Google Scholar 

  22. Lowry O, Rosebrough NJ, Farr AL, Randall RJ (1951) Protein measurement with the Folin phenol reagent. J Biol Chem 193(1):265–275

    CAS  Google Scholar 

  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 69:1060–1068

    Article  CAS  PubMed  Google Scholar 

  24. Niederberger E, King TS, Russe OQ, Geisslinger G (2015) Activation of AMPK and its impact on exercise capacity. Sports Med 45(11):1497–1509

    Article  PubMed  Google Scholar 

  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 6:174

    Article  Google Scholar 

  26. Picard F, Guarente L (2005) Molecular links between aging and adipose tissue. Int J Obes 29:S36–S39

    Article  CAS  Google Scholar 

  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):771–776

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  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 8:971–982

    Article  CAS  PubMed  Google Scholar 

  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 228:35–51

    Article  CAS  PubMed  Google Scholar 

  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):21–32

    Article  CAS  PubMed  Google Scholar 

  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):1239–1246

    Article  CAS  PubMed  Google Scholar 

  32. Stanford KI, Middelbeek RJ, Goodyear LJ (2015) Exercise effects on white adipose tissue: beiging and metabolic adaptations. Diabetes 64(7):2361–2368

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  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 95:960–968

    Article  CAS  PubMed  Google Scholar 

  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 73:487–494

    Article  CAS  PubMed  Google Scholar 

  35. Thirupathi A, Pinho R (2018) Effects of reactive oxygen species and interplay of antioxidants during physical exercise in skeletal muscles. J Physiol Biochem 74:359–367

  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 54:7928–7937

    Article  CAS  Google Scholar 

  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 106:21–27

    Article  CAS  PubMed  Google Scholar 

  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):45

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  39. Woods JA, Wilund KR, Martin SA, Kistler BM (2012) Exercise, inflammation and aging. Aging Dis 3(1):130–140

    Google Scholar 

  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):194–199

    Article  CAS  PubMed  Google Scholar 

Download references

Acknowledgements

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.

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Authors and Affiliations

  1. Laboratory of Exercise Biochemistry and Physiology, Graduate Program in Health Sciences, Universidade do Extremo Sul Catarinense, Av. Universitária, 1105 Bairro Universitário, Criciúma, Santa Catarina, 88806-000, Brazil

    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

  2. Laboratory of Molecular Iron metabolism, College of Life Science, Hebei Normal University, Shijiazhuang, Hebei, China

    Anand Thirupathi

  3. Department of Internal Medicine, Medicine School, Federal University of Juiz de Fora, Juiz de Fora, MG, Brazil

    Claudio Teodoro De Souza

  4. Programa de Pós-Graduação em Saúde, Departamento de Clínica Médica, Faculdade de Medicina, Universidade Federal de Juiz de Fora, Av. Eugenio do Nascimento, s/n, Bairro Dom Bosco, CEP, Juiz de Fora, MG, 36038-330, Brazil

    Claudio Teodoro De Souza

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  1. Anand Thirupathi
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  2. Bruno Luiz da Silva Pieri
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Correspondence to Claudio Teodoro De Souza.

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

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Thirupathi, A., da Silva Pieri, B.L., Queiroz, J.A.M.P. et al. Strength training and aerobic exercise alter mitochondrial parameters in brown adipose tissue and equally reduce body adiposity in aged rats. J Physiol Biochem 75, 101–108 (2019). https://doi.org/10.1007/s13105-019-00663-x

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