Advertisement

Sports Medicine

, Volume 48, Issue 6, pp 1369–1387 | Cite as

The Influence of Post-Exercise Cold-Water Immersion on Adaptive Responses to Exercise: A Review of the Literature

  • James R. Broatch
  • Aaron Petersen
  • David J. Bishop
Review Article

Abstract

Post-exercise cold-water immersion (CWI) is used extensively in exercise training as a means to minimise fatigue and expedite recovery between sessions. However, debate exists around its merit in long-term training regimens. While an improvement in recovery following a single session of exercise may improve subsequent training quality and stimulus, reports have emerged suggesting CWI may attenuate long-term adaptations to exercise training. Recent developments in the understanding of the molecular mechanisms governing the adaptive response to exercise in human skeletal muscle have provided potential mechanistic insight into the effects of CWI on training adaptations. Preliminary evidence suggests that CWI may blunt resistance signalling pathways following a single exercise session, as well as attenuate key long-term resistance training adaptations such as strength and muscle mass. Conversely, CWI may augment endurance signalling pathways and the expression of genes key to mitochondrial biogenesis following a single endurance exercise session, but have little to no effect on the content of proteins key to mitochondrial biogenesis following long-term endurance training. This review explores current evidence regarding the underlying molecular mechanisms by which CWI may alter cellular signalling and the long-term adaptive response to exercise in human skeletal muscle.

Notes

Compliance with Ethical Standards

Funding

The authors acknowledge the funding of Exercise and Sports Science Australia and their Applied Sports Science research Grant (received 2011).

Conflict of interest

James Broatch, Aaron Petersen, and David Bishop have no conflicts of interest to declare that are directly relevant to the content of this review.

References

  1. 1.
    Versey NG, Halson SL, Dawson BT. Water immersion recovery for athletes: effect on exercise performance and practical recommendations. Sports Med. 2013;43(11):1101–30.PubMedCrossRefGoogle Scholar
  2. 2.
    Wilcock IM, Cronin JB, Hing WA. Physiological response to water immersion: a method for sport recovery? Sports Med. 2006;36(9):747–65.PubMedCrossRefGoogle Scholar
  3. 3.
    Pournot H, Bieuzen F, Duffield R, Lepretre PM, Cozzolino C, Hausswirth C. Short term effects of various water immersions on recovery from exhaustive intermittent exercise. Eur J Appl Physiol. 2011;111(7):1287–95.PubMedCrossRefGoogle Scholar
  4. 4.
    Skurvydas A, Sipaviciene S, Krutulyte G, Gailiuniene A, Stasiulis A, Marnkus G, et al. Cooling leg muscles affects dynamics of indirect indicators of skeletal muscle damage. J Back Musculoskel. 2006;19(4):141–51.CrossRefGoogle Scholar
  5. 5.
    Bailey DM, Erith SJ, Griffin PJ, Dowson A, Brewer DS, Gant N, et al. Influence of cold-water immersion on indices of muscle damage following prolonged intermittent shuttle running. J Sport Sci. 2007;25(11):1163–70.CrossRefGoogle Scholar
  6. 6.
    Vaile J, Halson S, Gill N, Dawson B. Effect of hydrotherapy on the signs and symptoms of delayed onset muscle soreness. Eur J Appl Physiol. 2008;102(4):447–55.PubMedCrossRefGoogle Scholar
  7. 7.
    Vaile J, Halson S, Gill N, Dawson B. Effect of cold water immersion on repeat cycling performance and thermoregulation in the heat. J Sport Sci. 2008;26(5):431–40.CrossRefGoogle Scholar
  8. 8.
    Peiffer JJ, Abbiss CR, Watson G, Nosaka K, Laursen PB. Effect of a 5-min cold-water immersion recovery on exercise performance in the heat. Br J Sports Med. 2010;44(6):461–5.PubMedCrossRefGoogle Scholar
  9. 9.
    Yeargin SW, Casa DJ, McClung JM, Knight JC, Healey JC, Goss PJ, et al. Body cooling between two bouts of exercise in the heat enhances subsequent performance. J Strength Cond Res. 2006;20(2):383–9.PubMedGoogle Scholar
  10. 10.
    Leeder J, Gissane C, van Someren K, Gregson W, Howatson G. Cold water immersion and recovery from strenuous exercise: a meta-analysis. Br J Sports Med. 2011;46(4):233–40.PubMedCrossRefGoogle Scholar
  11. 11.
    Eston R, Peters D. Effects of cold water immersion on the symptoms of exercise-induced muscle damage. J Sport Sci. 1999;17(3):231–8.CrossRefGoogle Scholar
  12. 12.
    Stacey DL, Gibala MJ, Martin Ginis KA, Timmons BW. Effects of recovery method after exercise on performance, immune changes, and psychological outcomes. J Orthop Sports Phys Ther. 2010;40(10):656–65.PubMedCrossRefGoogle Scholar
  13. 13.
    Peake J, Peiffer JJ, Abbiss CR, Nosaka K, Okutsu M, Laursen PB, et al. Body temperature and its effect on leukocyte mobilization, cytokines and markers of neutrophil activation during and after exercise. Eur J Appl Physiol. 2008;102(4):391–401.PubMedCrossRefGoogle Scholar
  14. 14.
    Montgomery PG, Pyne DB, Cox AJ, Hopkins WG, Minahan CL, Hunt PH. Muscle damage, inflammation, and recovery interventions during a 3-day basketball tournament. Eur J Sport Sci. 2008;8(5):241–50.CrossRefGoogle Scholar
  15. 15.
    Ingram J, Dawson B, Goodman C, Wallman K, Beilby J. Effect of water immersion methods on post-exercise recovery from simulated team sport exercise. J Sci Med Sport. 2009;12(3):417–21.PubMedCrossRefGoogle Scholar
  16. 16.
    Stanley J, Buchheit M, Peake JM. The effect of post-exercise hydrotherapy on subsequent exercise performance and heart rate variability. Eur J Appl Physiol. 2011;112(3):951–61.PubMedCrossRefGoogle Scholar
  17. 17.
    Rowsell GJ, Coutts AJ, Reaburn P, Hill-Haas S. Effect of post-match cold-water immersion on subsequent match running performance in junior soccer players during tournament play. J Sport Sci. 2011;29(1):1–6.CrossRefGoogle Scholar
  18. 18.
    Parouty J, Al Haddad H, Quod M, Lepretre PM, Ahmaidi S, Buchheit M. Effect of cold water immersion on 100-m sprint performance in well-trained swimmers. Eur J Appl Physiol. 2010;109(3):483–90.PubMedCrossRefGoogle Scholar
  19. 19.
    Peiffer JJ, Abbiss CR, Watson G, Nosaka K, Laursen PB. Effect of cold-water immersion duration on body temperature and muscle function. J Sport Sci. 2009;27(10):987–93.CrossRefGoogle Scholar
  20. 20.
    Coffey V, Leveritt M, Gill N. Effect of recovery modality on 4-hour repeated treadmill running performance and changes in physiological variables. J Sci Med Sport. 2004;7(1):1–10.PubMedCrossRefGoogle Scholar
  21. 21.
    Peiffer JJ, Abbiss CR, Watson G, Nosaka K, Laursen PB. Effect of cold water immersion on repeated 1-km cycling performance in the heat. J Sci Med Sport. 2010;13(1):112–6.PubMedCrossRefGoogle Scholar
  22. 22.
    Buchheit M, Peiffer JJ, Abbiss CR, Laursen PB. Effect of cold water immersion on postexercise parasympathetic reactivation. Am J Physiol-Heart C. 2009;296(2):H421–7.CrossRefGoogle Scholar
  23. 23.
    Howatson G, Goodall S, van Someren KA. The influence of cold water immersions on adaptation following a single bout of damaging exercise. Eur J Appl Physiol. 2009;105(4):615–21.PubMedCrossRefGoogle Scholar
  24. 24.
    Sellwood KL, Brukner P, Williams D, Nicol A, Hinman R. Ice-water immersion and delayed-onset muscle soreness: a randomised controlled trial. Br J Sports Med. 2007;41(6):392–7.PubMedPubMedCentralCrossRefGoogle Scholar
  25. 25.
    Paddon-Jones DJ, Quigley BM. Effect of cryotherapy on muscle soreness and strength following eccentric exercise. Int J Sports Med. 1997;18(8):588–93.PubMedCrossRefGoogle Scholar
  26. 26.
    Kinugasa T, Kilding AE. A comparison of post-match recovery strategies in youth soccer players. J Strength Cond Res. 2009;23(5):1402–7.PubMedCrossRefGoogle Scholar
  27. 27.
    Jakeman JR, Macrae R, Eston R. A single 10-min bout of cold-water immersion therapy after strenuous plyometric exercise has no beneficial effect on recovery from the symptoms of exercise-induced muscle damage. Ergonomics. 2009;52(4):456–60.PubMedCrossRefGoogle Scholar
  28. 28.
    Goodall S, Howatson G. The effects of multiple cold water immersions on indices of muscle damage. J Sport Sci Med. 2008;7(2):235–41.Google Scholar
  29. 29.
    King M, Duffield ROB. The effects of recovery interventions on consecutive days of intermittent sprint exercise. J Strength Cond Res. 2009;23(6):1795–802.PubMedCrossRefGoogle Scholar
  30. 30.
    Peiffer JJ, Abbiss CR, Nosaka K, Peake JM, Laursen PB. Effect of cold water immersion after exercise in the heat on muscle function, body temperatures, and vessel diameter. J Sci Med Sport. 2009;12(1):91–6.PubMedCrossRefGoogle Scholar
  31. 31.
    Yamane M, Teruya H, Nakano M, Ogai R, Ohnishi N, Kosaka M. 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. 2006;96(5):572–80.PubMedCrossRefGoogle Scholar
  32. 32.
    Schniepp J, Campbell TS, Powell KL, Pincivero DM. The effects of cold-water immersion on power output and heart rate in elite cyclists. J Strength Cond Res. 2002;16(4):561–6.PubMedGoogle Scholar
  33. 33.
    Crowe MJ, O’Connor D, Rudd D. Cold water recovery reduces anaerobic performance. Int J Sports Med. 2007;28(12):994–8.PubMedCrossRefGoogle Scholar
  34. 34.
    White GE, Rhind SG, Wells GD. The effect of various cold-water immersion protocols on exercise-induced inflammatory response and functional recovery from high-intensity sprint exercise. Eur J Appl Physiol. 2014;114(11):2353–67.PubMedCrossRefGoogle Scholar
  35. 35.
    Broatch JR, Petersen A, Bishop DJ. Postexercise cold water immersion benefits are not greater than the placebo effect. Med Sci Sports Exerc. 2014;46(11):2139–47.PubMedCrossRefGoogle Scholar
  36. 36.
    Nakamura K, Takahashi H, Shimai S, Tanaka M. Effects of immersion in tepid bath water on recovery from fatigue after submaximal exercise in man. Ergonomics. 1996;39(2):257–66.PubMedCrossRefGoogle Scholar
  37. 37.
    Howatson G, van Someren KA. The prevention and treatment of exercise-induced muscle damage. Sports Med. 2008;38(6):483–503.PubMedCrossRefGoogle Scholar
  38. 38.
    Gulick DT, Kimura IF, Sitler M, Paolone A, Kelly JD. Various treatment techniques on signs and symptoms of delayed onset muscle soreness. J Athl Training. 1996;31(2):145–52.Google Scholar
  39. 39.
    Barnett A. Using recovery modalities between training sessions in elite athletes: does it help? Sports Med. 2006;36(9):781–96.PubMedCrossRefGoogle Scholar
  40. 40.
    Kellmann M. Preventing overtraining in athletes in high-intensity sports and stress/recovery monitoring. Scand J Med Sci Spor. 2010;20(Suppl 2):95–102.CrossRefGoogle Scholar
  41. 41.
    Halson SL, Bartram J, West N, Stephens J, Argus CK, Driller MW, et al. Does hydrotherapy help or hinder adaptation to training in competitive cyclists? Med Sci Sports Exerc. 2014;46(8):1631–9.PubMedCrossRefGoogle Scholar
  42. 42.
    Baar K. Training for endurance and strength: lessons from cell signaling. Med Sci Sports Exerc. 2006;38(11):1939–44.PubMedCrossRefGoogle Scholar
  43. 43.
    Coffey VG, Hawley JA. The molecular bases of training adaptation. Sports Med. 2007;37(9):737–63.PubMedCrossRefGoogle Scholar
  44. 44.
    Egan B, Zierath JR. Exercise metabolism and the molecular regulation of skeletal muscle adaptation. Cell Metab. 2013;17(2):162–84.PubMedCrossRefGoogle Scholar
  45. 45.
    Hood DA, Uguccioni G, Vainshtein A, D’Souza D. Mechanisms of exercise-induced mitochondrial biogenesis in skeletal muscle: implications for health and disease. Compr Physiol. 2011;1(3):1119–34.PubMedGoogle Scholar
  46. 46.
    Ars E, Serra E, de la Luna S, Estivill X, Lazaro C. Cold shock induces the insertion of a cryptic exon in the neurofibromatosis type 1 (NF1) mRNA. Nucleic Acids Res. 2000;28(6):1307–12.PubMedPubMedCentralCrossRefGoogle Scholar
  47. 47.
    Kaitsuka T, Tomizawa K, Matsushita M. Transformation of eEF1Bdelta into heat-shock response transcription factor by alternative splicing. EMBO Rep. 2011;12(7):673–81.PubMedPubMedCentralCrossRefGoogle Scholar
  48. 48.
    Sonna LA, Fujita J, Gaffin SL, Lilly CM. Invited review: Effects of heat and cold stress on mammalian gene expression. J Appl Physiol. 2002;92(4):1725–42.PubMedCrossRefGoogle Scholar
  49. 49.
    Plesofsky N, Brambl R. Glucose metabolism in Neurospora is altered by heat shock and by disruption of HSP30. Biochim Biophys Acta. 1999;1449(1):73–82.PubMedCrossRefGoogle Scholar
  50. 50.
    Neutelings T, Lambert CA, Nusgens BV, Colige AC. Effects of mild cold shock (25 degrees C) followed by warming up at 37 degrees C on the cellular stress response. PLoS ONE. 2013;8(7):e69687.PubMedPubMedCentralCrossRefGoogle Scholar
  51. 51.
    Slivka DR, Dumke CL, Tucker TJ, Cuddy JS, Ruby B. Human mRNA response to exercise and temperature. Int J Sports Med. 2012;33(2):94–100.PubMedCrossRefGoogle Scholar
  52. 52.
    Manfredi LH, Zanon NM, Garofalo MA, Navegantes LC, Kettelhut IC. Effect of short-term cold exposure on skeletal muscle protein breakdown in rats. J Appl Physiol (1985). 2013;115(10):1496–505.Google Scholar
  53. 53.
    Samuels SE, Thompson JR, Christopherson RJ. Skeletal and cardiac muscle protein turnover during short-term cold exposure and rewarming in young rats. Am J Physiol. 1996;270(6 Pt 2):R1231–9.PubMedGoogle Scholar
  54. 54.
    Lindquist S. The heat-shock response. Annu Rev Biochem. 1986;55:1151–91.PubMedCrossRefGoogle Scholar
  55. 55.
    Dresios J, Aschrafi A, Owens GC, Vanderklish PW, Edelman GM, Mauro VP. Cold stress-induced protein Rbm3 binds 60S ribosomal subunits, alters microRNA levels, and enhances global protein synthesis. Proc Natl Acad Sci USA. 2005;102(6):1865–70.PubMedPubMedCentralCrossRefGoogle Scholar
  56. 56.
    Liu AY, Bian H, Huang LE, Lee YK. Transient cold shock induces the heat shock response upon recovery at 37 degrees C in human cells. J Biol Chem. 1994;269(20):14768–75.PubMedGoogle Scholar
  57. 57.
    Laios E, Rebeyka IM, Prody CA. Characterization of cold-induced heat shock protein expression in neonatal rat cardiomyocytes. Mol Cell Biochem. 1997;173(1–2):153–9.PubMedCrossRefGoogle Scholar
  58. 58.
    Parsell DA, Lindquist S. The function of heat-shock proteins in stress tolerance: degradation and reactivation of damaged proteins. Annu Rev Genet. 1993;27:437–96.PubMedCrossRefGoogle Scholar
  59. 59.
    Georgopoulos C, Welch WJ. Role of the major heat shock proteins as molecular chaperones. Annu Rev Cell Biol. 1993;9:601–34.PubMedCrossRefGoogle Scholar
  60. 60.
    Otterbein LE, Choi AM. Heme oxygenase: colors of defense against cellular stress. Am J Physiol-Lung C. 2000;279(6):L1029–37.CrossRefGoogle Scholar
  61. 61.
    Asea A, Kraeft SK, Kurt-Jones EA, Stevenson MA, Chen LB, Finberg RW, et al. HSP70 stimulates cytokine production through a CD14-dependant pathway, demonstrating its dual role as a chaperone and cytokine. Nat Med. 2000;6(4):435–42.PubMedCrossRefGoogle Scholar
  62. 62.
    Hood DA, Takahashi M, Connor MK, Freyssenet D. Assembly of the cellular powerhouse: current issues in muscle mitochondrial biogenesis. Exerc Sport Sci Rev. 2000;28(2):68–73.PubMedGoogle Scholar
  63. 63.
    Jansky L. Shivering. In: Blattheis CM, editor. Physiology and pathophysiology of temperature regulation. Singapore: World Scientific; 1998.Google Scholar
  64. 64.
    Slivka D, Heesch M, Dumke C, Cuddy J, Hailes W, Ruby B. Effects of post-exercise recovery in a cold environment on muscle glycogen, PGC-1alpha, and downstream transcription factors. Cryobiology. 2013;66(3):250–5.PubMedCrossRefGoogle Scholar
  65. 65.
    Bruton JD, Aydin J, Yamada T, Shabalina IG, Ivarsson N, Zhang SJ, et al. Increased fatigue resistance linked to Ca2+ -stimulated mitochondrial biogenesis in muscle fibres of cold-acclimated mice. J Physiol. 2010;588(Pt 21):4275–88.PubMedPubMedCentralCrossRefGoogle Scholar
  66. 66.
    Cannon B, Nedergaard J. Brown adipose tissue: function and physiological significance. Physiol Rev. 2004;84(1):277–359.PubMedCrossRefGoogle Scholar
  67. 67.
    Mall S, Broadbridge R, Harrison SL, Gore MG, Lee AG, East JM. The presence of sarcolipin results in increased heat production by Ca(2+)-ATPase. J Biol Chem. 2006;281(48):36597–602.PubMedCrossRefGoogle Scholar
  68. 68.
    Lichtenbelt WvM, Kingma B, van der Lans A, Schellen L. Cold exposure—an approach to increasing energy expenditure in humans. Trends Endocrin Met. 2014;25(4):165–7.Google Scholar
  69. 69.
    Wijers SL, Schrauwen P, Saris WH, van Marken Lichtenbelt WD. Human skeletal muscle mitochondrial uncoupling is associated with cold induced adaptive thermogenesis. PLoS One. 2008;3(3):e1777.PubMedPubMedCentralCrossRefGoogle Scholar
  70. 70.
    Handschin C, Rhee J, Lin J, Tarr PT, Spiegelman BM. An autoregulatory loop controls peroxisome proliferator-activated receptor gamma coactivator 1alpha expression in muscle. Proc Natl Acad Sci USA. 2003;100(12):7111–6.PubMedPubMedCentralCrossRefGoogle Scholar
  71. 71.
    Irrcher I, Ljubicic V, Kirwan AF, Hood DA. AMP-activated protein kinase-regulated activation of the PGC-1alpha promoter in skeletal muscle cells. PLoS One. 2008;3(10):e3614.PubMedPubMedCentralCrossRefGoogle Scholar
  72. 72.
    Ito N, Ruegg UT, Kudo A, Miyagoe-Suzuki Y, Takeda S. Activation of calcium signaling through Trpv1 by nNOS and peroxynitrite as a key trigger of skeletal muscle hypertrophy. Nat Med. 2013;19(1):101–6.PubMedCrossRefGoogle Scholar
  73. 73.
    Wenz T. Regulation of mitochondrial biogenesis and PGC-1alpha under cellular stress. Mitochondrion. 2013;13(2):134–42.PubMedCrossRefGoogle Scholar
  74. 74.
    Halliwell B. Mechanisms involved in the generation of free radicals. Pathol Biol. 1996;44(1):6–13.PubMedGoogle Scholar
  75. 75.
    Bleakley CM, Davison GW. What is the biochemical and physiological rationale for using cold-water immersion in sports recovery? A systematic review. Br J Sports Med. 2010;44(3):179–87.PubMedCrossRefGoogle Scholar
  76. 76.
    Alessio HM. Exercise-induced oxidative stress. Med Sci Sports Exerc. 1993;25(2):218–24.PubMedCrossRefGoogle Scholar
  77. 77.
    Wallace SS. Biological consequences of free radical-damaged DNA bases. Free Radic Bio Med. 2002;33(1):1–14.CrossRefGoogle Scholar
  78. 78.
    Radak Z, Kaneko T, Tahara S, Nakamoto H, Ohno H, Sasvari M, et al. The effect of exercise training on oxidative damage of lipids, proteins, and DNA in rat skeletal muscle: evidence for beneficial outcomes. Free Radic Bio Med. 1999;27(1–2):69–74.CrossRefGoogle Scholar
  79. 79.
    Jackson MJ, O’Farrell S. Free radicals and muscle damage. Br Med Bull. 1993;49(3):630–41.PubMedCrossRefGoogle Scholar
  80. 80.
    Jenkins RR. Free radical chemistry. Relationship to exercise. Sports Med. 1988;5(3):156–70.PubMedCrossRefGoogle Scholar
  81. 81.
    Szweda PA, Friguet B, Szweda LI. Proteolysis, free radicals, and aging. Free Radic Bio Med. 2002;33(1):29–36.CrossRefGoogle Scholar
  82. 82.
    Renke J, Popadiuk S, Korzon M, Bugajczyk B, Wozniak M. Protein carbonyl groups’ content as a useful clinical marker of antioxidant barrier impairment in plasma of children with juvenile chronic arthritis. Free Radic Bio Med. 2000;29(2):101–4.CrossRefGoogle Scholar
  83. 83.
    Levine RL. Carbonyl modified proteins in cellular regulation, aging, and disease. Free Radic Bio Med. 2002;32(9):790–6.CrossRefGoogle Scholar
  84. 84.
    Finaud J, Lac G, Filaire E. Oxidative stress: relationship with exercise and training. Sports Med. 2006;36(4):327–58.PubMedCrossRefGoogle Scholar
  85. 85.
    Thomas MJ. The role of free radicals and antioxidants. Nutrition. 2000;16(7–8):716–8.Google Scholar
  86. 86.
    Smith MA, Reid MB. Redox modulation of contractile function in respiratory and limb skeletal muscle. Respir Physiol Neurobiol. 2006;151(2–3):229–41.PubMedCrossRefGoogle Scholar
  87. 87.
    Reid MB. Nitric oxide, reactive oxygen species, and skeletal muscle contraction. Med Sci Sports Exerc. 2001;33(3):371–6.PubMedCrossRefGoogle Scholar
  88. 88.
    Reid MB. Invited Review: redox modulation of skeletal muscle contraction: what we know and what we don’t. J Appl Physiol. 2001;90(2):724–31.PubMedCrossRefGoogle Scholar
  89. 89.
    Droge W. Free radicals in the physiological control of cell function. Physiol Rev. 2002;82(1):47–95.PubMedCrossRefGoogle Scholar
  90. 90.
    Sendowski I, Savourey G, Launay JC, Besnard Y, Cottet-Emard JM, Pequignot JM, et al. Sympathetic stimulation induced by hand cooling alters cold-induced vasodilatation in humans. Eur J Appl Physiol. 2000;81(4):303–9.PubMedCrossRefGoogle Scholar
  91. 91.
    Puigserver P, Wu Z, Park CW, Graves R, Wright M, Spiegelman BM. A cold-inducible coactivator of nuclear receptors linked to adaptive thermogenesis. Cell. 1998;92(6):829–39.PubMedCrossRefGoogle Scholar
  92. 92.
    Liang H, Ward WF. PGC-1alpha: a key regulator of energy metabolism. Adv Physiol Educ. 2006;30(4):145–51.PubMedCrossRefGoogle Scholar
  93. 93.
    Kim YS, Sainz RD. Beta-adrenergic agonists and hypertrophy of skeletal muscles. Life Sci. 1992;50(6):397–407.PubMedCrossRefGoogle Scholar
  94. 94.
    Kline WO, Panaro FJ, Yang H, Bodine SC. Rapamycin inhibits the growth and muscle-sparing effects of clenbuterol. J Appl Physiol. 2007;102(2):740–7.PubMedCrossRefGoogle Scholar
  95. 95.
    Bishop DJ, Granata C, Eynon N. Can we optimise the exercise training prescription to maximise improvements in mitochondria function and content? BBM-Gen Subj. 2014;1840(4):1266–75.CrossRefGoogle Scholar
  96. 96.
    Puigserver P, Spiegelman BM. Peroxisome proliferator-activated receptor-gamma coactivator 1 alpha (PGC-1 alpha): transcriptional coactivator and metabolic regulator. Endocr Rev. 2003;24(1):78–90.PubMedCrossRefGoogle Scholar
  97. 97.
    Puigserver P, Rhee J, Lin J, Wu Z, Yoon JC, Zhang CY, et al. Cytokine stimulation of energy expenditure through p38 MAP kinase activation of PPARgamma coactivator-1. Mol Cell. 2001;8(5):971–82.PubMedCrossRefGoogle Scholar
  98. 98.
    Ljubicic V, Joseph AM, Saleem A, Uguccioni G, Collu-Marchese M, Lai RY, et al. Transcriptional and post-transcriptional regulation of mitochondrial biogenesis in skeletal muscle: effects of exercise and aging. Biochim Biophys Acta. 2010;1800(3):223–34.PubMedCrossRefGoogle Scholar
  99. 99.
    Matoba S, Kang JG, Patino WD, Wragg A, Boehm M, Gavrilova O, et al. p53 regulates mitochondrial respiration. Science. 2006;312(5780):1650–3.PubMedCrossRefGoogle Scholar
  100. 100.
    Park JY, Wang PY, Matsumoto T, Sung HJ, Ma W, Choi JW, et al. p53 improves aerobic exercise capacity and augments skeletal muscle mitochondrial DNA content. Circ Res. 2009;105(7):705–12 (11 p following 12).Google Scholar
  101. 101.
    Saleem A, Adhihetty PJ, Hood DA. Role of p53 in mitochondrial biogenesis and apoptosis in skeletal muscle. Physiol Genom. 2009;37(1):58–66.CrossRefGoogle Scholar
  102. 102.
    Saleem A, Carter HN, Iqbal S, Hood DA. Role of p53 within the regulatory network controlling muscle mitochondrial biogenesis. Exerc Sport Sci Rev. 2011;39(4):199–205.PubMedGoogle Scholar
  103. 103.
    Saleem A, Hood DA. Acute exercise induces tumour suppressor protein p53 translocation to the mitochondria and promotes a p53-Tfam-mitochondrial DNA complex in skeletal muscle. J Physiol. 2013;591(Pt 14):3625–36.PubMedPubMedCentralCrossRefGoogle Scholar
  104. 104.
    Hood DA, Tryon LD, Carter HN, Kim Y, Chen CCW. Unravelling the mechanisms regulating muscle mitochondrial biogenesis. Biochem J. 2016;473(15):2295–314.PubMedCrossRefGoogle Scholar
  105. 105.
    McKinsey TA, Zhang CL, Lu J, Olson EN. Signal-dependent nuclear export of a histone deacetylase regulates muscle differentiation. Nature. 2000;408(6808):106–11.PubMedPubMedCentralCrossRefGoogle Scholar
  106. 106.
    Jorgensen SB, Wojtaszewski JF, Viollet B, Andreelli F, Birk JB, Hellsten Y, et al. Effects of alpha-AMPK knockout on exercise-induced gene activation in mouse skeletal muscle. FASEB J. 2005;19(9):1146–8.PubMedCrossRefGoogle Scholar
  107. 107.
    Oliveira RL, Ueno M, de Souza CT, Pereira-da-Silva M, Gasparetti AL, Bezzera RM, et al. Cold-induced PGC-1alpha expression modulates muscle glucose uptake through an insulin receptor/Akt-independent. AMPK-dependent pathway. Am J Physiol-Endoc M. 2004;287(4):E686–95.Google Scholar
  108. 108.
    Seebacher F, Glanville EJ. Low levels of physical activity increase metabolic responsiveness to cold in a rat (Rattus fuscipes). PLoS One. 2010;5(9):e13022.PubMedPubMedCentralCrossRefGoogle Scholar
  109. 109.
    Ijiri D, Kanai Y, Hirabayashi M. Possible roles of myostatin and PGC-1alpha in the increase of skeletal muscle and transformation of fiber type in cold-exposed chicks: expression of myostatin and PGC-1alpha in chicks exposed to cold. Domest Anim Endocrinol. 2009;37(1):12–22.PubMedCrossRefGoogle Scholar
  110. 110.
    Wu Z, Puigserver P, Andersson U, Zhang C, Adelmant G, Mootha V, et al. Mechanisms controlling mitochondrial biogenesis and respiration through the thermogenic coactivator PGC-1. Cell. 1999;98(1):115–24.PubMedCrossRefGoogle Scholar
  111. 111.
    Ihsan M, Watson G, Choo HC, Lewandowski P, Papazzo A, Cameron-Smith D, et al. Postexercise muscle cooling enhances gene expression of PGC-1alpha. Med Sci Sports Exerc. 2014;46(10):1900–7.PubMedCrossRefGoogle Scholar
  112. 112.
    Joo CH, Allan R, Drust B, Close GL, Jeong TS, Bartlett JD, et al. Passive and post-exercise cold-water immersion augments PGC-1alpha and VEGF expression in human skeletal muscle. Eur J Appl Physiol. 2016;116(11–12):2315–26.PubMedPubMedCentralCrossRefGoogle Scholar
  113. 113.
    Allan R, Sharples AP, Close GL, Drust B, Shepherd SO, Dutton J, et al. Post-exercise cold-water immersion modulates skeletal muscle PGC-1alpha mRNA expression in immersed and non-immersed limbs: evidence of systemic regulation. J Appl Physiol. 2017;123(2):451–9.PubMedCrossRefGoogle Scholar
  114. 114.
    Olesen J, Kiilerich K, Pilegaard H. PGC-1alpha-mediated adaptations in skeletal muscle. Pflugers Arch. 2010;460(1):153–62.PubMedCrossRefGoogle Scholar
  115. 115.
    Christiansen D, Murphy RM, Broatch JR, Bangsbo J, McKenna MJ, Kuang J, et al. Post-exercise cold-water immersion increases Na+,K+-ATPase α2-isoform mRNA content in parallel with elevated Sp1 expression in human skeletal muscle. bioRxiv. 2017.  https://doi.org/10.1101/151100.
  116. 116.
    Christiansen D, Murphy RM, Broatch JR, Bangsbo J, McKenna MJ, Bishop DJ. Regulation of Na+,K+-ATPase isoforms and phospholemman (FXYD1) in skeletal muscle fibre types by exercise training and cold-water immersion in men. bioRxiv. 2017.  https://doi.org/10.1101/151035.
  117. 117.
    Broatch JR, Petersen A, Bishop DJ. Cold-water immersion following sprint interval training does not alter endurance signaling pathways or training adaptations in human skeletal muscle. Am J Physiol-Reg I. 2017;313(4):R372–84.Google Scholar
  118. 118.
    Shute R, Heesch M, Laursen T, Slivka D. Local muscle cooling does not impact expression of mitochondrial-related genes. J Therm Biol. 2017;67:35–9.PubMedCrossRefGoogle Scholar
  119. 119.
    Aguiar PF, Magalhaes SM, Fonseca IA, da Costa Santos VB, de Matos MA, Peixoto MF, et al. Post-exercise cold water immersion does not alter high intensity interval training-induced exercise performance and Hsp72 responses, but enhances mitochondrial markers. Cell Stress Chaperon. 2016;21(5):793–804.CrossRefGoogle Scholar
  120. 120.
    Ihsan M, Markworth JF, Watson G, Choo HC, Govus A, Pham T, et al. Regular postexercise cooling enhances mitochondrial biogenesis through AMPK and p38 MAPK in human skeletal muscle. Am J Physiol-Reg I. 2015;309(3):R286–94.Google Scholar
  121. 121.
    Xing JQ, Zhou Y, Chen JF, Li SB, Fang W, Yang J. Effect of cold adaptation on activities of relevant enzymes and antioxidant system in rats. Int J Clin Exp Med. 2014;7(11):4232–7.PubMedPubMedCentralGoogle Scholar
  122. 122.
    Camargo MZ, Siqueira CPCM, Preti MCP, Nakamura FY, de Lima FM, Dias IFL, et al. Effects of light emitting diode (LED) therapy and cold water immersion therapy on exercise-induced muscle damage in rats. Lasers Med Sci. 2012;27(5):1051–8.PubMedCrossRefGoogle Scholar
  123. 123.
    Watkins AM, Cheek DJ, Harvey AE, Goodwin JD, Blair KE, Mitchell JB. Heat shock protein (HSP-72) levels in skeletal muscle following work in heat. Aviat Space Envir Md. 2007;78(9):901–5.Google Scholar
  124. 124.
    Schaeffer PJ, Villarin JJ, Lindstedt SL. Chronic cold exposure increases skeletal muscle oxidative structure and function in Monodelphis domestica, a marsupial lacking brown adipose tissue. Physiological and biochemical zoology: PBZ. 2003;76(6):877–87.Google Scholar
  125. 125.
    Young AJ, Sawka MN, Quigley MD, Cadarette BS, Neufer PD, Dennis RC, et al. Role of thermal factors on aerobic capacity improvements with endurance training. J Appl Physiol. 1993;75(1):49–54.PubMedCrossRefGoogle Scholar
  126. 126.
    Mitchell CR, Harris MB, Cordaro AR, Starnes JW. Effect of body temperature during exercise on skeletal muscle cytochrome c oxidase content. J Appl Physiol. 2002;93(2):526–30.PubMedCrossRefGoogle Scholar
  127. 127.
    Aydin J, Shabalina IG, Place N, Reiken S, Zhang SJ, Bellinger AM, et al. Nonshivering thermogenesis protects against defective calcium handling in muscle. FASEB J. 2008;22(11):3919–24.PubMedPubMedCentralCrossRefGoogle Scholar
  128. 128.
    Arruda AP, Ketzer LA, Nigro M, Galina A, Carvalho DP, de Meis L. Cold tolerance in hypothyroid rabbits: role of skeletal muscle mitochondria and sarcoplasmic reticulum Ca2+ ATPase isoform 1 heat production. Endocrinology. 2008;149(12):6262–71.PubMedCrossRefGoogle Scholar
  129. 129.
    Scheele C, Nielsen S, Pedersen BK. ROS and myokines promote muscle adaptation to exercise. Trends Endocrinol Metab. 2009;20(3):95–9.PubMedCrossRefGoogle Scholar
  130. 130.
    Acin-Perez R, Salazar E, Brosel S, Yang H, Schon EA, Manfredi G. Modulation of mitochondrial protein phosphorylation by soluble adenylyl cyclase ameliorates cytochrome oxidase defects. EMBO Mol Med. 2009;1(8–9):392–406.PubMedPubMedCentralCrossRefGoogle Scholar
  131. 131.
    Ristow M, Zarse K. How increased oxidative stress promotes longevity and metabolic health: the concept of mitochondrial hormesis (mitohormesis). Exp Gerontol. 2010;45(6):410–8.PubMedCrossRefGoogle Scholar
  132. 132.
    Kulisz A, Chen N, Chandel NS, Shao Z, Schumacker PT. Mitochondrial ROS initiate phosphorylation of p38 MAP kinase during hypoxia in cardiomyocytes. Am J Physiol-Lung C. 2002;282(6):L1324–9.CrossRefGoogle Scholar
  133. 133.
    Beeson CC, Beeson GC, Buff H, Eldridge J, Zhang A, Seth A, et al. Integrin-dependent Akt1 activation regulates PGC-1 expression and fatty acid oxidation. J Vasc Res. 2012;49(2):89–100.PubMedPubMedCentralCrossRefGoogle Scholar
  134. 134.
    Kabe Y, Ando K, Hirao S, Yoshida M, Handa H. Redox regulation of NF-kappaB activation: distinct redox regulation between the cytoplasm and the nucleus. Antioxid Redox Signal. 2005;7(3–4):395–403.Google Scholar
  135. 135.
    Bakkar N, Wang J, Ladner KJ, Wang H, Dahlman JM, Carathers M, et al. IKK/NF-kB regulates skeletal myogenesis via a signaling switch to inhibit differentiation and promote mitochondrial biogenesis. J Cell Biol. 2013;202(5):825.PubMedCentralCrossRefGoogle Scholar
  136. 136.
    McKenna MJ, Bangsbo J, Renaud JM. Muscle K+, Na+, and Cl disturbances and Na+-K+ pump inactivation: implications for fatigue. J Appl Physiol. 2008;104(1):288–95.PubMedCrossRefGoogle Scholar
  137. 137.
    Thomassen M, Christensen PM, Gunnarsson TP, Nybo L, Bangsbo J. Effect of 2-wk intensified training and inactivity on muscle Na+ -K+ pump expression, phospholemman (FXYD1) phosphorylation, and performance in soccer players. J Appl Physiol. 2010;108(4):898–905.PubMedCrossRefGoogle Scholar
  138. 138.
    Siems WG, Brenke R, Sommerburg O, Grune T. Improved antioxidative protection in winter swimmers. QJM. 1999;92(4):193–8.PubMedCrossRefGoogle Scholar
  139. 139.
    Siems WG, van Kuijk FJ, Maass R, Brenke R. Uric acid and glutathione levels during short-term whole body cold exposure. Free Radic Bio Med. 1994;16(3):299–305.CrossRefGoogle Scholar
  140. 140.
    Dugue B, Smolander J, Westerlund T, Oksa J, Nieminen R, Moilanen E, et al. Acute and long-term effects of winter swimming and whole-body cryotherapy on plasma antioxidative capacity in healthy women. Scand J Clin Lab Invest. 2005;65(5):395–402.PubMedCrossRefGoogle Scholar
  141. 141.
    Bartlett JD, Louhelainen J, Iqbal Z, Cochran AJ, Gibala MJ, Gregson W, et al. Reduced carbohydrate availability enhances exercise-induced p53 signaling in human skeletal muscle: implications for mitochondrial biogenesis. Am J Physiol-Reg I. 2013;304(6):R450–8.Google Scholar
  142. 142.
    Berkers CR, Maddocks OD, Cheung EC, Mor I, Vousden KH. Metabolic regulation by p53 family members. Cell Metab. 2013;18(5):617–33.PubMedPubMedCentralCrossRefGoogle Scholar
  143. 143.
    Bergeaud M, Mathieu L, Guillaume A, Moll UM, Mignotte B, Le Floch N, et al. Mitochondrial p53 mediates a transcription-independent regulation of cell respiration and interacts with the mitochondrial F(1)F0-ATP synthase. Cell Cycle. 2013;12(17):2781–93.PubMedPubMedCentralCrossRefGoogle Scholar
  144. 144.
    Ermolenko DN, Makhatadze GI. Bacterial cold-shock proteins. Cell Mol Life Sci. 2002;59(11):1902–13.PubMedCrossRefGoogle Scholar
  145. 145.
    Costello JT, Culligan K, Selfe J, Donnelly AE. Muscle, skin and core temperature after − 110 degrees c cold air and 8 degrees c water treatment. PLoS One. 2012;7(11):e48190.PubMedPubMedCentralCrossRefGoogle Scholar
  146. 146.
    Gregson W, Allan R, Holden S, Phibbs P, Doran D, Campbell I, et al. Postexercise cold-water immersion does not attenuate muscle glycogen resynthesis. Med Sci Sports Exerc. 2013;45(6):1174–81.PubMedCrossRefGoogle Scholar
  147. 147.
    Folland JP, Williams AG. The adaptations to strength training: morphological and neurological contributions to increased strength. Sports Med. 2007;37(2):145–68.PubMedCrossRefGoogle Scholar
  148. 148.
    Gabriel DA, Kamen G, Frost G. Neural adaptations to resistive exercise: mechanisms and recommendations for training practices. Sports Med. 2006;36(2):133–49.PubMedCrossRefGoogle Scholar
  149. 149.
    Pansarasa O, Rinaldi C, Parente V, Miotti D, Capodaglio P, Bottinelli R. Resistance training of long duration modulates force and unloaded shortening velocity of single muscle fibres of young women. J Electromyogr Kinesiol. 2009;19(5):e290–300.PubMedCrossRefGoogle Scholar
  150. 150.
    Erskine RM, Jones DA, Maffulli N, Williams AG, Stewart CE, Degens H. What causes in vivo muscle specific tension to increase following resistance training? Exp Physiol. 2011;96(2):145–55.PubMedCrossRefGoogle Scholar
  151. 151.
    Peake JM, Roberts LA, Figueiredo VC, Egner I, Krog S, Aas SN, et al. The effects of cold water immersion and active recovery on inflammation and cell stress responses in human skeletal muscle after resistance exercise. J Physiol. 2017;595(3):695–711.PubMedCrossRefGoogle Scholar
  152. 152.
    Figueiredo VC, Roberts LA, Markworth JF, Barnett MP, Coombes JS, Raastad T, et al. Impact of resistance exercise on ribosome biogenesis is acutely regulated by post-exercise recovery strategies. Physiol Rep. 2016;4(2):e12670.  https://doi.org/10.14814/phy2.12670.PubMedPubMedCentralCrossRefGoogle Scholar
  153. 153.
    Roberts LA, Raastad T, Markworth JF, Figueiredo VC, Egner IM, Shield A, et al. Post-exercise cold water immersion attenuates acute anabolic signalling and long-term adaptations in muscle to strength training. J Physiol. 2015;593(18):4285–301.PubMedPubMedCentralCrossRefGoogle Scholar
  154. 154.
    Yamane M, Ohnishi N, Matsumoto T. Does regular post-exercise cold application attenuate trained muscle adaptation? Int J Sports Med. 2015;36(8):647–53.PubMedCrossRefGoogle Scholar
  155. 155.
    Tipton KD, Hamilton DL, Gallagher IJ. Assessing the role of muscle protein breakdown in response to nutrition and exercise in humans. Sports Med. 2018;48(Suppl 1):53–64.PubMedPubMedCentralCrossRefGoogle Scholar
  156. 156.
    Miller BF, Olesen JL, Hansen M, Dossing S, Crameri RM, Welling RJ, et al. Coordinated collagen and muscle protein synthesis in human patella tendon and quadriceps muscle after exercise. J Physiol. 2005;567(Pt 3):1021–33.PubMedPubMedCentralCrossRefGoogle Scholar
  157. 157.
    Biolo G, Tipton KD, Klein S, Wolfe RR. An abundant supply of amino acids enhances the metabolic effect of exercise on muscle protein. Am J Physiol Endocrinol Metab. 1997;273(1):E122–9.Google Scholar
  158. 158.
    Phillips SM, Tipton KD, Aarsland A, Wolf SE, Wolfe RR. Mixed muscle protein synthesis and breakdown after resistance exercise in humans. American journal of physiology Endocrinology and metabolism. 1997;273(1):E99–107.Google Scholar
  159. 159.
    Goodman CA, Frey JW, Mabrey DM, Jacobs BL, Lincoln HC, You JS, et al. The role of skeletal muscle mTOR in the regulation of mechanical load-induced growth. J Physiol. 2011;589(Pt 22):5485–501.PubMedPubMedCentralCrossRefGoogle Scholar
  160. 160.
    Bodine SC, Stitt TN, Gonzalez M, Kline WO, Stover GL, Bauerlein R, et al. Akt/mTOR pathway is a crucial regulator of skeletal muscle hypertrophy and can prevent muscle atrophy in vivo. Nat Cell Biol. 2001;3(11):1014–9.PubMedCrossRefGoogle Scholar
  161. 161.
    Leger B, Cartoni R, Praz M, Lamon S, Deriaz O, Crettenand A, et al. Akt signalling through GSK-3β, mTOR and Foxo1 is involved in human skeletal muscle hypertrophy and atrophy. J Physiol. 2006;576(3):923–33.Google Scholar
  162. 162.
    Figueiredo VC, Caldow MK, Massie V, Markworth JF, Cameron-Smith D, Blazevich AJ. Ribosome biogenesis adaptation in resistance training-induced human skeletal muscle hypertrophy. Am J Physiol Endocrinol Metab. 2015;309(1):E72–83.PubMedCrossRefGoogle Scholar
  163. 163.
    Fyfe JJ, Bishop DJ, Bartlett JD, Hanson ED, Anderson MJ, Garnham AP, et al. Enhanced skeletal muscle ribosome biogenesis, yet attenuated mTORC1 and ribosome biogenesis-related signalling, following short-term concurrent versus single-mode resistance training. Scientific reports. 2018;8(1):560.PubMedPubMedCentralCrossRefGoogle Scholar
  164. 164.
    Schuelke M, Wagner KR, Stolz LE, Hubner C, Riebel T, Komen W, et al. Myostatin mutation associated with gross muscle hypertrophy in a child. N Engl J Med. 2004;350(26):2682–8.PubMedCrossRefGoogle Scholar
  165. 165.
    McPherron AC, Lawler AM, Lee SJ. Regulation of skeletal muscle mass in mice by a new TGF-beta superfamily member. Nature. 1997;387(6628):83–90.PubMedCrossRefGoogle Scholar
  166. 166.
    MacKenzie MG, Hamilton DL, Pepin M, Patton A, Baar K. Inhibition of myostatin signaling through Notch activation following acute resistance exercise. PLoS One. 2013;8(7):e68743.PubMedPubMedCentralCrossRefGoogle Scholar
  167. 167.
    Mawhinney C, Jones H, Joo CH, Low DA, Green DJ, Gregson W. Influence of cold-water immersion on limb and cutaneous blood flow after exercise. Med Sci Sports Exerc. 2013;45(12):2277–85.PubMedCrossRefGoogle Scholar
  168. 168.
    Menetrier A, Beliard S, Ravier G, Mourot L, Bouhaddi M, Regnard J, et al. Changes in femoral artery blood flow during thermoneutral, cold, and contrast-water therapy. J Sports Med Phys Fit. 2015;55(7–8):768–75.Google Scholar
  169. 169.
    Gregson W, Black MA, Jones H, Milson J, Morton J, Dawson B, et al. Influence of cold water immersion on limb and cutaneous blood flow at rest. Am J Sports Med. 2011;39(6):1316–23.PubMedCrossRefGoogle Scholar
  170. 170.
    Fujita S, Rasmussen BB, Cadenas JG, Grady JJ, Volpi E. Effect of insulin on human skeletal muscle protein synthesis is modulated by insulin-induced changes in muscle blood flow and amino acid availability. Am J Physiol Endocrinol Metab. 2006;291(4):E745–54.PubMedPubMedCentralCrossRefGoogle Scholar
  171. 171.
    Timmerman KL, Lee JL, Fujita S, Dhanani S, Dreyer HC, Fry CS, et al. Pharmacological vasodilation improves insulin-stimulated muscle protein anabolism but not glucose utilization in older adults. Diabetes. 2010;59(11):2764–71.PubMedPubMedCentralCrossRefGoogle Scholar
  172. 172.
    Hofmann S, Cherkasova V, Bankhead P, Bukau B, Stoecklin G. Translation suppression promotes stress granule formation and cell survival in response to cold shock. Mol Biol Cell. 2012;23(19):3786–800.PubMedPubMedCentralCrossRefGoogle Scholar
  173. 173.
    Trappe TA, White F, Lambert CP, Cesar D, Hellerstein M, Evans WJ. Effect of ibuprofen and acetaminophen on postexercise muscle protein synthesis. Am J Physiol Endocrinol Metab. 2002;282(3):E551–E6.Google Scholar
  174. 174.
    Pournot H, Bieuzen F, Louis J, Mounier R, Fillard JR, Barbiche E, et al. Time-course of changes in inflammatory response after whole-body cryotherapy multi exposures following severe exercise. PLoS One. 2011;6(7):e22748.PubMedPubMedCentralCrossRefGoogle Scholar
  175. 175.
    Navegantes LC, Migliorini RH, do Carmo Kettelhut I. Adrenergic control of protein metabolism in skeletal muscle. Curr Opin Clin Nutr Metab Care. 2002;5(3):281–6.PubMedCrossRefGoogle Scholar
  176. 176.
    Morgan SA, Hassan-Smith ZK, Doig CL, Sherlock M, Stewart PM, Lavery GG. Glucocorticoids and 11β-HSD1 are major regulators of intramyocellular protein metabolism. J Endocrinol. 2016;229(3):277–86.Google Scholar
  177. 177.
    Šrámek P, Šimečková M, Janský L, Šavlíková J, Vybíral S. Human physiological responses to immersion into water of different temperatures. Eur J Appl Physiol. 2000;81(5):436–42.PubMedCrossRefGoogle Scholar
  178. 178.
    Ferry AL, Vanderklish PW, Dupont-Versteegden EE. Enhanced survival of skeletal muscle myoblasts in response to overexpression of cold shock protein RBM3. Am J Physiol Cell Physiol. 2011;301(2):C392–C402.Google Scholar
  179. 179.
    Goll DE, Neti G, Mares SW, Thompson VF. Myofibrillar protein turnover: the proteasome and the calpains. J Anim Sci. 2008;86(14 Suppl):E19–35.PubMedCrossRefGoogle Scholar
  180. 180.
    Murton AJ, Constantin D, Greenhaff PL. The involvement of the ubiquitin proteasome system in human skeletal muscle remodelling and atrophy. Biochem Biophys Acta. 2008;1782(12):730–43.PubMedGoogle Scholar
  181. 181.
    Stefanetti RJ, Lamon S, Rahbek SK, Farup J, Zacharewicz E, Wallace MA, et al. Influence of divergent exercise contraction mode and whey protein supplementation on atrogin-1, MuRF1, and FOXO1/3A in human skeletal muscle. J Appl Physiol (1985). 2014;116(11):1491–502.Google Scholar
  182. 182.
    Paulsen G, Hamarsland H, Cumming KT, Johansen RE, Hulmi JJ, Borsheim E, et al. Vitamin C and E supplementation alters protein signalling after a strength training session, but not muscle growth during 10 weeks of training. J Physiol. 2014;592(24):5391–408.PubMedPubMedCentralCrossRefGoogle Scholar
  183. 183.
    Sandri M, Lin J, Handschin C, Yang W, Arany ZP, Lecker SH, et al. PGC-1α protects skeletal muscle from atrophy by suppressing FoxO3 action and atrophy-specific gene transcription. Proc Natl Acad Sci. 2006;103(44):16260–5.Google Scholar
  184. 184.
    McCarthy JJ, Mula J, Miyazaki M, Erfani R, Garrison K, Farooqui AB, et al. Effective fiber hypertrophy in satellite cell-depleted skeletal muscle. Development. 2011;138(17):3657–66.Google Scholar
  185. 185.
    Fry CS, Lee JD, Jackson JR, Kirby TJ, Stasko SA, Liu H, et al. Regulation of the muscle fiber microenvironment by activated satellite cells during hypertrophy. FASEB J. 2014;28(4):1654–65.Google Scholar
  186. 186.
    Petrella JK, Kim J-s, Mayhew DL, Cross JM, Bamman MM. Potent myofiber hypertrophy during resistance training in humans is associated with satellite cell-mediated myonuclear addition: a cluster analysis. J Appl Physiol. 2008;104(6):1736–42.Google Scholar
  187. 187.
    Snijders T, Smeets JS, van Kranenburg J, Kies AK, van Loon LJ, Verdijk LB. Changes in myonuclear domain size do not precede muscle hypertrophy during prolonged resistance-type exercise training. Acta Physiol (Oxf). 2016;216(2):231–9.CrossRefGoogle Scholar
  188. 188.
    Takagi R, Fujita N, Arakawa T, Kawada S, Ishii N, Miki A. Influence of icing on muscle regeneration after crush injury to skeletal muscles in rats. J Appl Physiol (1985). 2011;110(2):382–8.Google Scholar
  189. 189.
    Shima A, Matsuda R. The expression of myogenin, but not of MyoD, is temperature-sensitive in mouse skeletal muscle cells. Zool Sci. 2008;25(11):1066–74.PubMedCrossRefGoogle Scholar
  190. 190.
    Charge SBP, Rudnicki MA. Cellular and molecular regulation of muscle regeneration. Physiol Rev. 2004;84(1):209–38.Google Scholar
  191. 191.
    Bandell M, Story GM, Hwang SW, Viswanath V, Eid SR, Petrus MJ, et al. Noxious cold ion channel TRPA1 is activated by pungent compounds and bradykinin. Neuron. 2004;41(6):849–57.PubMedCrossRefGoogle Scholar
  192. 192.
    Osterloh M, Böhm M, Kalbe B, Osterloh S, Hatt H. Identification and functional characterization of TRPA1 in human myoblasts. Pflügers Arch Eur J Physiol. 2016;468(2):321–33.CrossRefGoogle Scholar
  193. 193.
    Larsen S, Nielsen J, Hansen CN, Nielsen LB, Wibrand F, Stride N, et al. Biomarkers of mitochondrial content in skeletal muscle of healthy young human subjects. J Physiol. 2012;590(Pt 14):3349–60.PubMedPubMedCentralCrossRefGoogle Scholar
  194. 194.
    Stancic A, Buzadzic B, Korac A, Otasevic V, Jankovic A, Vucetic M, et al. Regulatory role of PGC-1α/PPAR signaling in skeletal muscle metabolic recruitment during cold acclimation. J Exp Biol. 2013;216(22):4233–41.PubMedCrossRefGoogle Scholar
  195. 195.
    Frohlich M, Faude O, Klein M, Pieter A, Emrich E, Meyer T. Strength training adaptations after cold-water immersion. J Strength Cond Res. 2014;28(9):2628–33.PubMedCrossRefGoogle Scholar
  196. 196.
    Ohnishi N, Yamane M, Uchiyama N, Shirasawa S, Kosaka M, Shiono H, et al. Adaptive changes in muscular performance and circulation by resistance training with regular cold application. J Therm Biol. 2004;29(7–8):839–43.CrossRefGoogle Scholar
  197. 197.
    Spiering BA, Kraemer WJ, Anderson JM, Armstrong LE, Nindl BC, Volek JS, et al. Effects of elevated circulating hormones on resistance exercise-induced Akt signaling. Med Sci Sports Exerc. 2008;40(6):1039–48.PubMedCrossRefGoogle Scholar
  198. 198.
    Smith DJ. A framework for understanding the training process leading to elite performance. Sports Med. 2003;33(15):1103–26.PubMedCrossRefGoogle Scholar

Copyright information

© Springer International Publishing AG, part of Springer Nature 2018

Authors and Affiliations

  1. 1.Institute for Health and SportVictoria UniversityMelbourneAustralia
  2. 2.Department of PhysiologyAustralian Institute of SportCanberraAustralia
  3. 3.School of Medical and Health SciencesEdith Cowan UniversityJoondalupAustralia

Personalised recommendations