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Mild-cold water swimming does not exacerbate white adipose tissue browning and brown adipose tissue activation in mice

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Abstract

The present study investigated the effects of swimming physical training either thermoneutral or below thermoneutral water temperature on white (WAT) and brown (BAT) adipose tissue metabolism, morphology, and function. C57BL/6J male mice (n = 40; weight 25.3 ± 0.1 g) were divided into control (CT30), cold control (CT20), trained (TR30), and cold trained (TR20) groups. Swimming training consisted of 30-min exercise at 30°C (control) or 20°C (cold) water temperature. After 8-week training, adipose tissues were excised and inguinal (ingWAT) and BAT were processed for histology, lipolysis, and protein contents of total OXPHOS, PGC1α, and UCP1 by western blotting analysis. Swimming training reduced body weight gain independently of water temperature (P < 0.05). ingWAT mass was decreased for TR30 in comparison to other groups (P < 0.05), while for BAT, there was a significant increase in CT20 in relation to CT30, and both trained groups were significantly increased in relation to control groups (P < 0.05). ingWAT mean adipocyte area was smaller for trained groups, and seemed to present multilocular adipocytes. Lipolytic activity and protein content of UCP1, PGC1α, and mitochondrial markers were increased in trained groups for ingWAT (P < 0.05), independent of water temperature (P > 0.05), and these patterns were not observed for BAT (P > 0.05). Our findings suggest that mild-cold water exposure and swimming physical exercise seem to, independently, promote browning in ingWAT with no effects on BAT; however, the association of exercise and mild-cold water did not exacerbate these effects.

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Abbreviations

BAT:

Brown adipose tissue

bm:

Body mass

CT20:

Cold control

CT30:

Control

ECL:

Enhanced chemiluminescence

epiWAT:

Epididymal

IL-6:

Interleukine 6

ingWAT:

Inguinal

NaCl:

Sodium chloride

NaF:

Sodium fluoride

PGC1α:

Peroxisome proliferator-activated receptor gamma coactivator 1 alpha

PVDF:

Polyvinylidene difluoride

rpWAT:

Retroperitoneal

TR20:

Cold training

TR30:

Training

UCP1:

Uncoupling protein 1

WAT:

White adipose tissue

References

  1. Aldiss P, Betts J, Sale C, Pope M, Budge H, Symonds ME (2018) Exercise-induced ‘browning’ of adipose tissues. Metabolism 81:63–70. https://doi.org/10.1016/j.metabol.2017.11.009

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  2. Almeida WS, Lima LC, Cunha VN, Cunha R, Araújo RC, Barros CC, Simões HG, Campbell CS (2011) Assessment of aerobic capacity during swimming exercise in ob/ob mice. Cell Biochem Funct 29(8):666–672. https://doi.org/10.1002/cbf.1803

    Article  CAS  PubMed  Google Scholar 

  3. Boström P, Wu J, Jedrychowski MP, Korde A, Ye L, Lo JC, Rasbach KA, Boström EA, Choi JH, Long JZ, Kajimura S, Zingaretti MC, Vind BF, Tu H, Cinti S, Højlund K, Gygi SP, Spiegelman BM (2012) A PGC1-α-dependent myokine that drives brown-fat-like development of white fat and thermogenesis. Nature 481(7382):463–468. https://doi.org/10.1038/nature10777

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  4. Cannon B, Nedergaard J (2004) Brown adipose tissue: function and physiological significance. Physiol Rev 84(1):277–359. https://doi.org/10.1152/physrev.00015.2003

    Article  CAS  PubMed  Google Scholar 

  5. Cao L, Choi EY, Liu X, Martin A, Wang C, Xu X, During MJ (2011) White to brown fat phenotypic switch induced by genetic and environmental activation of a hypothalamic-adipocyte axis. Cell Metab 14(3):324–338. https://doi.org/10.1016/j.cmet.2011.06.020

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  6. Carrière A, Jeanson Y, Berger-Müller S, André M, Chenouard V, Arnaud E, Barreau C, Walther R, Galinier A, Wdziekonski B, Villageois P, Louche K, Collas P, Moro C, Dani C, Villarroya F, Casteilla L (2014) Browning of white adipose cells by intermediate metabolites: an adaptive mechanism to alleviate redox pressure. Diabetes 63(10):3253–3265. https://doi.org/10.2337/db13-1885

    Article  CAS  PubMed  Google Scholar 

  7. Castro É, Silva TEO, Festuccia WT (2017) Critical review of beige adipocyte thermogenic activation and contribution to whole-body energy expenditure. Horm Mol Biol Clin Invest 31(2)

  8. Cheng AJ, Willis SJ, Zinner C, Chaillou T, Ivarsson N, Ørtenblad N, Lanner JT, Holmberg HC, Westerblad H (2017) Post-exercise recovery of contractile function and endurance in humans and mice is accelerated by heating and slowed by cooling skeletal muscle. J Physiol 595(24):7413–7426

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  9. Chimin P, Andrade ML, Belchior T, Paschoal VA, Magdalon J, Yamashita AS, Castro É, Castoldi A, Chaves-Filho AB, Yoshinaga MY, Miyamoto S, Câmara NO, Festuccia WT (2017) Adipocyte mTORC1 deficiency promotes adipose tissue inflammation and NLRP3 inflammasome activation via oxidative stress and de novo ceramide synthesis. J Lipid Res 58(9):1797–1807. https://doi.org/10.1194/jlr.M074518

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  10. Chu Y, Huddleston GG, Clancy AN, Harris RB, Bartness TJ (2010) Epididymal fat is necessary for spermatogenesis, but not testosterone production or copulatory behavior. Endocrinology 151(12):5669–5679. https://doi.org/10.1210/en.2010-0772

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  11. De Matteis R, Lucertini F, Guescini M, Polidori E, Zeppa S, Stocchi V, Cinti S, Cuppini R (2013) Exercise as a new physiological stimulus for brown adipose tissue activity. Nutr Metab Cardiovasc Dis 23(6):582–590. https://doi.org/10.1016/j.numecd.2012.01.013

    Article  CAS  PubMed  Google Scholar 

  12. Dewal RS, Stanford KI (2018) Effects of exercise on brown and beige adipocytes. Biochimica et Biophysica Acta (BBA)-Molecular and Cell Biology of Lipids

  13. Fenzl A, Kiefer FW (2014) Brown adipose tissue and thermogenesis. Horm Mol Biol Clin Invest 19(1):25–37. https://doi.org/10.1515/hmbci-2014-0022

    Article  CAS  Google Scholar 

  14. Gaskill BN, Gordon CJ, Pajor EA, Lucas JR, Davis JK, Garner JP (2013) Impact of nesting material on mouse body temperature and physiology. Physiol Behav 110-111:87–95. https://doi.org/10.1016/j.physbeh.2012.12.018

    Article  CAS  PubMed  Google Scholar 

  15. 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 Physiol Endocrinol Metabol 297(2):E495–E504

    Article  CAS  Google Scholar 

  16. Handschin C, Spiegelman BM (2008) The role of exercise and PGC1α in inflammation and chronic disease. Nature 454(7203):463–469

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  17. Harri M, Kuusela P (1986) Is swimming exercise or cold exposure for rats? Acta Physiol Scand 126(2):189–197. https://doi.org/10.1111/j.1748-1716.1986.tb07805.x

    Article  CAS  PubMed  Google Scholar 

  18. Knudsen JG, Murholm M, Carey AL, Biensø RS, Basse AL, Allen TL, Hidalgo J, Kingwell BA, Febbraio MA, Hansen JB, Pilegaard H (2014) Role of IL-6 in exercise training- and cold-induced UCP1 expression in subcutaneous white adipose tissue. PLoS One 9(1):e84910. https://doi.org/10.1371/journal.pone.0084910

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  19. Magdalon J, Chimin P, Belchior T, Neves RX, Vieira-Lara MA, Andrade ML, Farias TS, Bolsoni-Lopes A, Paschoal VA, Yamashita AS, Kowaltowski AJ, Festuccia WT (2016) Constitutive adipocyte mTORC1 activation enhances mitochondrial activity and reduces visceral adiposity in mice. Biochim Biophys Acta 1861(5):430–438. https://doi.org/10.1016/j.bbalip.2016.02.023

    Article  CAS  PubMed  Google Scholar 

  20. Nedergaard J, Cannon B (2014) The browning of white adipose tissue: some burning issues. Cell Metab 20(3):396–407. https://doi.org/10.1016/j.cmet.2014.07.005

    Article  CAS  PubMed  Google Scholar 

  21. Oh-ishi S, Kizaki T, Toshinai K, Haga S, Fukuda K, Nagata N, Ohno H (1996) Swimming training improves brown-adipose-tissue activity in young and old mice. Mech Ageing Dev 89(2):67–78

    Article  CAS  PubMed  Google Scholar 

  22. Puigserver P, Wu Z, Park CW, Graves R, Wright M, Spiegelman BM (1998) A cold-inducible coactivator of nuclear receptors linked to adaptive thermogenesis. Cell 92(6):829–839. https://doi.org/10.1016/s0092-8674(00)81410-5

    Article  CAS  PubMed  Google Scholar 

  23. Rodrigues NA, Torsoni AS, Fante T, Dos Reis IG, Gobatto CA, Manchado-Gobatto FB (2017) Lactate minimum underestimates the maximal lactate steady-state in swimming mice. Appl Physiol Nutr Metab 42(1):46–52. https://doi.org/10.1139/apnm-2016-0198

    Article  CAS  PubMed  Google Scholar 

  24. Rosen ED, Spiegelman BM (2006) Adipocytes as regulators of energy balance and glucose homeostasis. Nature 444(7121):847–853. https://doi.org/10.1038/nature05483

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  25. Rosen ED, Spiegelman BM (2014) What we talk about when we talk about fat. Cell 156(1–2):20–44. https://doi.org/10.1016/j.cell.2013.12.012

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  26. Sanchez-Gurmaches J, Hung CM, Guertin DA (2016) Emerging complexities in adipocyte origins and identity. Trends Cell Biol 26(5):313–326. https://doi.org/10.1016/j.tcb.2016.01.004

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  27. Shirvani H, Arabzadeh E (2018) Metabolic cross-talk between skeletal muscle and adipose tissue in high-intensity interval training vs. moderate-intensity continuous training by regulation of PGC-1α. Eat Weight Disord. https://doi.org/10.1007/s40519-018-0491-4

  28. Stanford KI, Middelbeek RJ, Goodyear LJ (2015) Exercise effects on white adipose tissue: beiging and metabolic adaptations. Diabetes 64(7):2361–2368. https://doi.org/10.2337/db15-0227

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  29. Sutherland LN, Bomhof MR, Capozzi LC, Basaraba SA, Wright DC (2009) Exercise and adrenaline increase PGC-1α mRNA expression in rat adipose tissue. J Physiol 587(7):1607–1617

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  30. Uldry M, Yang W, St-Pierre J, Lin J, Seale P, Spiegelman BM (2006) Complementary action of the PGC-1 coactivators in mitochondrial biogenesis and brown fat differentiation. Cell Metab 3(5):333–341. https://doi.org/10.1016/j.cmet.2006.04.002

    Article  CAS  PubMed  Google Scholar 

  31. Waldén TB, Hansen IR, Timmons JA, Cannon B, Nedergaard J (2012) Recruited vs. nonrecruited molecular signatures of brown, “brite,” and white adipose tissues. Am J Physiol Endocrinol Metab 302(1):E19–E31. https://doi.org/10.1152/ajpendo.00249.2011

    Article  CAS  PubMed  Google Scholar 

  32. Wolfe RR, Klein S, Carraro F, Weber JM (1990) Role of triglyceride-fatty acid cycle in controlling fat metabolism in humans during and after exercise. Am J Phys 258(2 Pt 1):E382–E389. https://doi.org/10.1152/ajpendo.1990.258.2.E382

    Article  CAS  Google Scholar 

  33. Wu J, Boström P, Sparks LM, Ye L, Choi JH, Giang AH, Khandekar M, Virtanen KA, Nuutila P, Schaart G, Huang K, Tu H, van Marken Lichtenbelt WD, Hoeks J, Enerbäck S, Schrauwen P, Spiegelman BM (2012) Beige adipocytes are a distinct type of thermogenic fat cell in mouse and human. Cell 150(2):366–376. https://doi.org/10.1016/j.cell.2012.05.016

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  34. Wu MV, Bikopoulos G, Hung S, Ceddia RB (2014) Thermogenic capacity is antagonistically regulated in classical brown and white subcutaneous fat depots by high fat diet and endurance training in rats: impact on whole-body energy expenditure. J Biol Chem 289(49):34129–34140. https://doi.org/10.1074/jbc.M114.591008

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  35. Xu X, Ying Z, Cai M, Xu Z, Li Y, Jiang SY, Tzan K, Wang A, Parthasarathy S, He G, Rajagopalan S, Sun Q (2011) Exercise ameliorates high-fat diet-induced metabolic and vascular dysfunction, and increases adipocyte progenitor cell population in brown adipose tissue. Am J Phys Regul Integr Comp Phys 300(5):R1115–R1125. https://doi.org/10.1152/ajpregu.00806.2010

    Article  CAS  Google Scholar 

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Funding

This work was supported by Fundação Araucária de Apoio ao Desenvolvimento Científico e Tecnológico do Estado do Paraná (FA).

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Authors and Affiliations

  1. Department of Physical Education, Physical Education and Sports Center, Londrina State University – UEL, Rodovia Celso Garcia Cid, Pr 445 Km 380, Campus Universitário, Cx Postal 6001, Londrina, PR, 86051-990, Brazil

    Jhonattan Toniatto da Silva, Paola Sanches Cella, Mayra Tardelli de Jesus Testa, Luiz Augusto Perandini, Rafael Deminice & Patricia Chimin

  2. Department of Physiology and Biophysics, Institute of Biomedical Sciences, University of São Paulo – USP, São Paulo, Brazil

    Luiz Augusto Perandini & William T. Festuccia

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  1. Jhonattan Toniatto da Silva
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Contributions

J.T.S., P.S.C., and M.T.J.T. designed and performed the research, analyzed data, performed histological analysis, carried analysis of adipose tissue lipolysis, and performed western blotting analysis. L.A.P., R.D., W.T.F., and P.C. designed and performed the research, analyzed data, and wrote the manuscript. All authors revised the manuscript and approved the final version.

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Correspondence to Patricia Chimin.

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The authors declare that they have no conflict of interest.

Research involving human participants and/or animals

All procedures and protocols used in the study were in accordance with the National Council of Animal Experimentation (CONCEA) and were approved by the Ethical Committee for Animal Research (CEUA) of the Londrina State University, Brazil (Protocol CEUA n0 18153.2016.34).

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Key points

Swimming training increases thermogenesis of ingWAT independently of mild-cold water. ingWAT is more responsive than BAT to mild-cold swimming training.

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da Silva, J.T., Cella, P.S., Testa, M.T. et al. Mild-cold water swimming does not exacerbate white adipose tissue browning and brown adipose tissue activation in mice. J Physiol Biochem 76, 663–672 (2020). https://doi.org/10.1007/s13105-020-00771-z

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