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Cell Stress and Chaperones

, Volume 21, Issue 5, pp 793–804 | Cite as

Post-exercise cold water immersion does not alter high intensity interval training-induced exercise performance and Hsp72 responses, but enhances mitochondrial markers

  • Paula Fernandes Aguiar
  • Sílvia Mourão Magalhães
  • Ivana Alice Teixeira Fonseca
  • Vanessa Batista da Costa Santos
  • Mariana Aguiar de Matos
  • Marco Fabrício Dias Peixoto
  • Fábio Yuzo Nakamura
  • Craig Crandall
  • Hygor Nunes Araújo
  • Leonardo Reis Silveira
  • Etel Rocha-Vieira
  • Flávio de Castro Magalhães
  • Fabiano Trigueiro AmorimEmail author
Original Paper

Abstract

This study aims to evaluate the effect of regular post-exercise cold water immersion (CWI) on intramuscular markers of cellular stress response and signaling molecules related to mitochondria biogenesis and exercise performance after 4 weeks of high intensity interval training (HIIT). Seventeen healthy subjects were allocated into two groups: control (CON, n = 9) or CWI (n = 8). Each HIIT session consisted of 8–12 cycling exercise stimuli (90–110 % of peak power) for 60 s followed by 75 s of active recovery three times per week, for 4 weeks (12 HIIT sessions). After each HIIT session, the CWI had their lower limbs immersed in cold water (10 °C) for 15 min and the CON recovered at room temperature. Exercise performance was evaluated before and after HIIT by a 15-km cycling time trial. Vastus lateralis biopsies were obtained pre and 72 h post training. Samples were analyzed for heat shock protein 72 kDa (Hsp72), adenosine monophosphate-activated protein kinase (AMPK), and phosphorylated p38 mitogen-activated protein kinase (p-p38 MAPK) assessed by western blot. In addition, the mRNA expression of heat shock factor-1 (HSF-1), peroxisome proliferator-activated receptor gamma coactivator-1α (PGC-1α), nuclear respiratory factor 1 and 2 (NRF1 and 2), mitochondrial transcription factor A (Tfam), calcium calmodulin-dependent protein kinase 2 (CaMK2) and enzymes citrate synthase (CS), carnitine palmitoyltransferase I (CPT1), and pyruvate dehydrogenase kinase (PDK4) were assessed by real-time PCR. Time to complete the 15-km cycling time trial was reduced with training (p < 0.001), but was not different between groups (p = 0.33). The Hsp72 (p = 0.01), p38 MAPK, and AMPK (p = 0.04) contents increased with training, but were not different between groups (p > 0.05). No differences were observed with training or condition for mRNA expression of PGC-1α (p = 0.31), CPT1 (p = 0.14), CS (p = 0.44), and NRF-2 (p = 0.82). However, HFS-1 (p = 0.007), PDK4 (p = 0.03), and Tfam (p = 0.03) mRNA were higher in CWI. NRF-1 decrease in both groups after training (p = 0.006). CaMK2 decreased with HIIT (p = 0.003) but it was not affected by CWI (p = 0.99). Cold water immersion does not alter HIIT-induced Hsp72, AMPK, p38 MAPK, and exercise performance but was able to increase some markers of cellular stress response and signaling molecules related to mitochondria biogenesis.

Keywords

Post-exercise recovery Cold water immersion Heat shock protein High intensity interval training Mitochondria biogenesis 

Notes

Acknowledgments

The authors wish to acknowledge Dr. Miguel Proença for performing the muscle biopsy and all the volunteers that participated in the present study. This work was supported by CAPES (PNPD-2455/2011), FAPEMIG (APQ-01382-12), and CNPq (407252/2013-4 and 445096/2014-4) grants.

References

  1. ACSM (2014) In: Linda S Pescatello, Ross Arena, Deborah Riebe, Paul D Thompson (eds). ACSM’s Guidelines for Exercise Testing and Prescription. 9th Ed. Philadelphia: Wolters Kluwer/Lippincott Williams & WilkinsGoogle Scholar
  2. Bailey DM, Erith SJ, Griffin PJ, Dowson A, Brewer DS, Gant N, Williams C (2007) Influence of cold-water immersion on indices of muscle damage following prolonged intermittent shuttle running. J Sports Sci 25:1163–1170CrossRefPubMedGoogle Scholar
  3. Bergström J, Hultman E (1966) Muscle glycogen synthesis after exercise: an enhancing factor localized to the muscle cells in man. Nature 210:309–310CrossRefPubMedGoogle Scholar
  4. Borg GA (1982) Psychophysical bases of perceived exertion. Med Sci Sports Exerc 14:377–381PubMedGoogle Scholar
  5. Bradford MM (1976) A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal Biochem 72:248–254CrossRefPubMedGoogle Scholar
  6. Broatch JR, Petersen A, Bishop DJ (2014) Postexercise cold-water immersion benefits are not greater than the placebo effect. Med Sci Sports Exerc 46:2139–2147CrossRefPubMedGoogle Scholar
  7. Bruton JD, Aydin J, Yamada T, Shabalina IG, Ivarsson N, Zhang SJ, Wada M, Tavi P, Nedergaard J, Katz A, Westerblad H (2010) Increased fatigue resistance linked to Ca2+-stimulated mitochondrial biogenesis in muscle fibres of cold-acclimated mice. J Physiol 588(Pt 21):4275–4288. doi: 10.1113/jphysiol.2010.198598 CrossRefPubMedPubMedCentralGoogle Scholar
  8. Buck MJ, Squire TL, Andrews MT (2002) Coordinate expression of the PDK4 gene: a means of regulating fuel selection in a hibernating mammal. Physiol Genomics 8(1):5–13CrossRefPubMedGoogle Scholar
  9. Burgomaster KA, Heigenhauser GJ, Gibala MJ (2006) Effect of short-term sprint interval training on human skeletal muscle carbohydrate metabolism during exercise and time-trial performance. J Appl Physiol 100:2041–2047CrossRefPubMedGoogle Scholar
  10. Crampton D, Donne B, Warmington SA, Egaña M (2013) Cycling time to failure is better maintained by cold than contrast or thermoneutral lower-body water immersion in normothermia. Eur J Appl Physiol 113:3059–3067CrossRefPubMedGoogle Scholar
  11. De Matos MA, de Oliveira Ottone V, Duarte TC, Sampaio PF, Costa KB, Fonseca CA, Neves MP, Schneider SM, Moseley P, Coimbra CC, Magalhães FC, Rocha-Vieira E, Amorim FT (2014) Exercise reduces cellular stress related to skeletal muscle insulin resistance. Cell Stress Chaperones 19:263–270CrossRefPubMedGoogle Scholar
  12. Dunne A, Crampton D, Egaña M (2013) Effect of post-exercise hydrotherapy water temperature on subsequent exhaustive running performance in normothermic conditions. J Sci Med Sport 16:466–471CrossRefPubMedGoogle Scholar
  13. Guttman SD, Glover CV, Allis CD, Gorovsky MA (1980) Heat shock, deciliation and release from anoxia induce the synthesis of the same set of polypeptides in starved T. pyriformis. Cell 22:299–307CrossRefPubMedGoogle Scholar
  14. Haddad HA, Parouty J, Buchheit M (2012) Effect of daily cold water immersion on heart rate variability and subjective ratings of well-being in highly trained swimmers. Int J Sports Physiol Perform 7:33–38CrossRefPubMedGoogle Scholar
  15. Halson SL, Bartram J, West N, Stephens J, Argus CK, Driller MW, Sargent C, Lastella M, Hopkins WG, Martin DT (2014) Does hydrotherapy help or hinder adaptation to training in competitive cyclists. Med Sci Sports Exerc 46:1631–1639CrossRefPubMedGoogle Scholar
  16. Henstridge DC, Bruce CR, Drew BG, Tory K, Kolonics A, Estevez E, Chung J, Watson N, Gardner T, Lee-Young RS, Connor T, Watt MJ, Carpenter K, Hargreaves M, McGee SL, Hevener AL, Febbraio MA (2014) Activating HSP72 in rodent skeletal muscle increases mitochondrial number and oxidative capacity and decreases insulin resistance. Diabetes 63:1881–1894CrossRefPubMedGoogle Scholar
  17. Ihsan M, Watson G, Lipski M, Abbiss CR (2013) Influence of postexercise cooling on muscle oxygenation and blood volume changes. Med Sci Sports Exerc 45:876–882CrossRefPubMedGoogle Scholar
  18. Ihsan M, Watson G, Choo HC, Lewandowski P, Papazzo A, Cameron-Smith D, Abbiss CR (2014) Postexercise muscle cooling enhances gene expression of PGC-1α. Med Sci Sports Exerc 46(10):1900–1907CrossRefPubMedGoogle Scholar
  19. Ihsan M, Markworth JF, Watson G, Choo HC, Govus A, Pham T, Hickey A, Cameron-Smith D, Abbiss CR (2015) Regular postexercise cooling enhances mitochondrial biogenesis through AMPK and p38 MAPK in human skeletal muscle. Am J Physiol-Regul Integr Comp Physiol 309:R286–R294CrossRefPubMedGoogle Scholar
  20. Kramer HF, Goodyear LJ (2007) Exercise, MAPK, and NF-kB signaling in skeletal muscle. J Appl Physiol 103:388–395CrossRefPubMedGoogle Scholar
  21. Kregel KC (2002) Invited review: heat shock proteins: modifying factors in physiological stress responses and acquired thermotolerance. J Appl Physiol 92:2177–2186CrossRefPubMedGoogle Scholar
  22. Little JP, Safdar A, Wilkin GP, Tarnopolsky MA, Gibala MJ (2010) A practical model of low-volume high-intensity interval training induces mitochondrial biogenesis in human skeletal muscle: potential mechanisms. J Physiol 588:1011–1022CrossRefPubMedPubMedCentralGoogle Scholar
  23. Liu Y, Mayr S, Opitz-Gress A, Zeller C, Lormes W, Baur S, Lehmann M, Steinacker JM (1999) Human skeletal muscle HSP70 response to training in highly trained rowers. J Appl Physiol 86:101–104PubMedGoogle Scholar
  24. Liu CC, Lin CH, Lee CC, Lin MT, Wen HC (2013) Transgenic overexpression of heat shock protein 72 in mouse muscle protects against exhaustive exercise-induced skeletal muscle damage. J Form Med Assoc 112:24e30Google Scholar
  25. Livak, K. J.; Schmittgen, T. D. Analysis of relative gene expression data using real time quantitative PCR and the 2-(ΔCT) method. Methods, v. 25, n. 4, p. 402-8, DEC, 2001.Google Scholar
  26. Locke M, Atkinson BG, Tanguay RM, Noble EG (1994) Shifts in type I fiber proportion in rat hindlimb muscle are accompanied by changes in HSP72 content. Am J Physiol-Cell Physiol 266:C1240–C1246Google Scholar
  27. Mawhinney C, Jones H, Joo CH, Low DA, Green DJ, Gregson W (2013) Influence of cold-water immersion on limb and cutaneous blood flow after exercise. Med Sci Sports Exerc 45:2277–2285CrossRefPubMedGoogle Scholar
  28. Miller BF, Konopka AR, Hamilton KL. (2016) The rigorous study of exercise adaptations: why mRNA might not be enough. J Appl Physiol (1985). Mar 24:jap.00137.2016. doi:  10.1152/japplphysiol.00137
  29. Peiffer JJ, Abbiss CR, Watson G, Nosaka K, Laursen PB (2009) Effect of cold-water immersion duration on body temperature and muscle function. J Sports Sci 27:987–993CrossRefPubMedGoogle Scholar
  30. Perry CG, Lally J, Holloway G, Heigenhauser GJ, Bonen A, Spriet LL (2010) Repeated transient mRNA bursts precede increases in transcriptional and mitochondrial proteins during training in human skeletal muscle. J Physiol 588(Pt 23):4795–4810. doi:  10.1113/jphysiol.2010.199448
  31. 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 92:829–839CrossRefPubMedGoogle Scholar
  32. Reid MB (2005) Response of the ubiquitin-proteasome pathway to changes in muscle activity. Am J Physiol-Regul Integr Comp Physiol 288:R1423–R1431CrossRefPubMedGoogle Scholar
  33. Reznick RM, Shulman GI (2006) The role of AMP-activated protein kinase in mitochondrial biogenesis. J Physiol 574:33–39CrossRefPubMedPubMedCentralGoogle Scholar
  34. Roberts LA, Nosaka K, Coombes JS, Peake JM (2014) Cold water immersion enhances recovery of submaximal muscle function after resistance exercise. Am J Physiol-Regul Integr Comp Physiol 307:R998–R1008CrossRefPubMedGoogle Scholar
  35. Rowsell GJ, Reaburn P, Toone R, Smith M, Coutts AJ (2014) Effect of run training and cold-water immersion on subsequent cycle training quality in high-performance triathletes. J Strength Cond Res 28:1664–1672CrossRefPubMedGoogle Scholar
  36. Sciandra JJ, Subjeck JR (1983) The effects of glucose on protein synthesis and thermosensitivity in Chinese hamster ovary cells. J Biol Chem 258:12091–12093PubMedGoogle Scholar
  37. Sonna LA, Fujita J, Gaffin SL, Lilly CM (2002) Effects of heat and cold stress on mammalian gene expression. J Appl Physiol 92:1725–1742. doi: 10.1152/japplphysiol.01143.2001 CrossRefPubMedGoogle Scholar
  38. Stanley J, Peake JM, Coombes JS, Buchheit M (2014) Central and peripheral adjustments during high-intensity exercise following cold water immersion. Eur J Appl Physiol 114:147–163CrossRefPubMedGoogle Scholar
  39. Takahashi M, Chesley A, Freyssenet D, Hood DA (1998) Contractile activity-induced adaptations in the mitochondrial protein import system. Am J Physiol-Cell Physiol 274:C1380–C1387Google Scholar
  40. Tupling AR, Gramolini AO, Duhamel TA, Kondo H, Asahi M, Tsuchiya SC, Borrelli MJ, Lepock JR, Otsu K, Hori M, MacLennan DH, Green HJ (2004) HSP70 binds to the fast-twitch skeletal muscle sarco (endo) plasmic reticulum Ca2+-ATPase (SERCA1a) and prevents thermal inactivation. J Biol Chem 279:52382–52389CrossRefPubMedGoogle Scholar
  41. Vaile J, Halson S, Gill N, Dawson B (2008) Effect of hydrotherapy on the signs and symptoms of delayed onset muscle soreness. Eur J Appl Physiol 102:447–455CrossRefPubMedGoogle Scholar
  42. Vandesompele, J.; De Preter, K.; Pattyn, F.; Poppe, B.; Van Roy, N.; De Paepe, A.; Speleman, F. Accurate normalization of real-time quantitative RT-PCR data by geometric averaging of multiple internal control genes. Genome Biol., v. 3, n. 7, JUN, 2002.Google Scholar
  43. Versey NG, Halson SL, Dawson BT (2013) Water immersion recovery for athletes: effect on exercise performance and practical recommendations. Sports Med 43:1101–1130CrossRefPubMedGoogle Scholar
  44. Vogt M, Puntschart A, Geiser J, Zuleger C, Billeter R, Hoppeler H (2001) Molecular adaptations in human skeletal muscle to endurance training under simulated hypoxic conditions. J Appl Physiol 91:173–182PubMedGoogle Scholar
  45. Wende AR, Huss JM, Schaeffer PJ, Giguère V, Kelly DP (2005) PGC-1alpha coactivates PDK4 gene expression via the orphan nuclear receptor ERRalpha: a mechanism for transcriptional control of muscle glucose metabolism. Mol Cell Biol 25(24):10684–10694CrossRefPubMedPubMedCentralGoogle Scholar
  46. Wu Z, Puigserver P, Andersson U, Zhang C, Adelmant G, Mootha V, Troy A, Cinti S, Lowell B, Scarpulla RC, Spiegelman BM (1999) Mechanisms controlling mitochondrial biogenesis and respiration through the thermogenic coactivator PGC-1. Cell 98:115–124CrossRefPubMedGoogle Scholar
  47. Yamane M, Teruya H, Nakano M, Ogai R, Ohnishi N, Kosaka M (2006) Post-exercise leg and forearm flexor muscle cooling in humans attenuates endurance and resistance training effects on muscle performance and on circulatory adaptation. Eur J Appl Physiol 96:572–580CrossRefPubMedGoogle Scholar
  48. Yamane M, Ohnishi N, Matsumoto T (2015) Does regular post-exercise cold application attenuate trained muscle adaptation? Int J Sports Med 36(8):647–653CrossRefPubMedGoogle Scholar

Copyright information

© Cell Stress Society International 2016

Authors and Affiliations

  • Paula Fernandes Aguiar
    • 1
  • Sílvia Mourão Magalhães
    • 1
  • Ivana Alice Teixeira Fonseca
    • 1
  • Vanessa Batista da Costa Santos
    • 2
  • Mariana Aguiar de Matos
    • 1
  • Marco Fabrício Dias Peixoto
    • 1
  • Fábio Yuzo Nakamura
    • 2
  • Craig Crandall
    • 3
  • Hygor Nunes Araújo
    • 4
  • Leonardo Reis Silveira
    • 4
  • Etel Rocha-Vieira
    • 1
  • Flávio de Castro Magalhães
    • 1
  • Fabiano Trigueiro Amorim
    • 1
    Email author
  1. 1.Programa Multicêntrico de Pós Graduação em Ciências Fisiológicas, Faculdade de Ciências Básicas e da SaúdeUniversidade Federal dos Vales do Jequitinhonha e MucuriDiamantinaBrazil
  2. 2.Universidade Estadual de LondrinaLondrinaBrazil
  3. 3.University of Texas Southwestern Medical CenterDallasUSA
  4. 4.Universidade de CampinasCampinasBrazil

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