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Cell Stress and Chaperones

, Volume 21, Issue 6, pp 1021–1035 | Cite as

Hsp72 and Hsp90α mRNA transcription is characterised by large, sustained changes in core temperature during heat acclimation

  • Oliver R. GibsonEmail author
  • James A. Tuttle
  • Peter W. Watt
  • Neil S. Maxwell
  • Lee Taylor
Original Paper

Abstract

Increased intracellular heat shock protein-72 (Hsp72) and heat shock protein-90α (Hsp90α) have been implicated as important components of acquired thermotolerance, providing cytoprotection during stress. This experiment determined the physiological responses characterising increases in Hsp72 and Hsp90α mRNA on the first and tenth day of 90-min heat acclimation (in 40.2 °C, 41.0 % relative humidity (RH)) or equivalent normothermic training (in 20 °C, 29 % RH). Pearson’s product-moment correlation and stepwise multiple regression were performed to determine relationships between physiological [e.g. (Trec, sweat rate (SR) and heart rate (HR)] and training variables (exercise duration, exercise intensity, work done), and the leukocyte Hsp72 and Hsp90α mRNA responses via reverse transcription quantitative polymerase chain reaction (RT-QPCR) (n = 15). Significant (p < 0.05) correlations existed between increased Hsp72 and Hsp90α mRNA (r = 0.879). Increased core temperature was the most important criteria for gene transcription with ΔTrec (r = 0.714), SR (r = 0.709), Trecfinal45 (r = 0.682), area under the curve where Trec ≥ 38.5 °C (AUC38.5 °C; r = 0.678), peak Trec (r = 0.661), duration Trec ≥ 38.5 °C (r = 0.650) and ΔHR (r = 0.511) each demonstrating a significant (p < 0.05) correlation with the increase in Hsp72 mRNA. The Trec AUC38.5 °C (r = 0.729), ΔTrec (r = 0.691), peak Trec (r = 0.680), Trecfinal45 (r = 0.678), SR (r = 0.660), duration Trec ≥ 38.5 °C (r = 0.629), the rate of change in Trec (r = 0.600) and ΔHR (r = 0.531) were the strongest correlate with the increase in Hsp90α mRNA. Multiple regression improved the model for Hsp90α mRNA only, when Trec AUC38.5 °C and SR were combined. Training variables showed insignificant (p > 0.05) weak (r < 0.300) relationships with Hsp72 and Hsp90α mRNA. Hsp72 and Hsp90α mRNA correlates were comparable on the first and tenth day. When transcription of the related Hsp72 and Hsp90α mRNA is important, protocols should rapidly induce large, prolonged changes in core temperature.

Keywords

Heat shock proteins Hyperthermia Core temperature Heat acclimation Thermotolerance 

Notes

Compliance with ethical standards

All protocols, procedures and methods were approved by the institutional ethics committee. Participants completed medical questionnaires and written informed consent following the principles outlined by the Declaration of Helsinki as revised in 2013 prior to commencing any preliminary or experimental sessions.

References

  1. Amorim FT, Fonseca IT, Machado-Moreira CA, Magalhães FC (2015) Insights into the role of heat shock proteins 72 to whole-body heat acclimation in humans. Temperature 2:499–505CrossRefGoogle Scholar
  2. Amorim FT, Yamada PM, Robergs RA, Schneider SM, Moseley PL (2008) The effect of the rate of heat storage on serum heat shock protein 72 in humans. Eur J Appl Physiol 104:965–972CrossRefPubMedGoogle Scholar
  3. Anckar J, Sistonen L (2011) Regulation of HSF1 function in the heat stress response: implications in aging and disease. Annu Rev Biochem 80:1089–1115CrossRefPubMedGoogle Scholar
  4. Asea A (2003) Chaperokine-induced signal transduction pathways. Exerc Immunol Rev 9:25–33PubMedPubMedCentralGoogle Scholar
  5. Atamaniuk J, Stuhlmeier KM, Vidotto C, Tschan H, Dossenbach-Glaninger A, Mueller MM (2008) Effects of ultra-marathon on circulating DNA and mRNA expression of pro- and anti-apoptotic genes in mononuclear cells. Eur J Appl Physiol 104:711–717CrossRefPubMedGoogle Scholar
  6. Bruce CR, Carey AL, Hawley JA, Febbraio MA (2003) Intramuscular heat shock protein 72 and heme oxygenase-1 mRNA are reduced in patients with type 2 diabetes: evidence that insulin resistance is associated with a disturbed antioxidant defense mechanism. Diabetes 52:2338–2345CrossRefPubMedGoogle Scholar
  7. Byrne C, Lee JKW, Chew SAN, Lim CL, Tan EYM (2006) Continuous thermoregulatory responses to mass-participation distance running in heat. Med Sci Sports Exerc 38:803–810CrossRefPubMedGoogle Scholar
  8. Carter MR, Mcginn R, Barrera-Ramirez J, Sigal RJ, Kenny GP (2014) Impairments in local heat loss in type 1 diabetes during exercise in the heat. Med Sci Sport Exerc 46:2224–2233CrossRefGoogle Scholar
  9. Chomczynski P, Sacchi N (1987) Single-step method of RNA isolation by acid guanidinium thiocyanate-phenol-chloroform extraction. Anal Biochem 162:156–159CrossRefPubMedGoogle Scholar
  10. Connolly PH, Caiozzo VJ, Zaldivar F, Nemet D, Larson J, Hung S-P, Heck JD, Hatfield GW, Cooper DM (2004) Effects of exercise on gene expression in human peripheral blood mononuclear cells. J Appl Physiol 97:1461–1469CrossRefPubMedGoogle Scholar
  11. Davis SL, Wilson TE, White AT, Frohman EM (2010) Thermoregulation in multiple sclerosis. J Appl Physiol 109:1531–1537CrossRefPubMedPubMedCentralGoogle Scholar
  12. Dokladny K, Zuhl MN, Moseley PL (2016) Intestinal epithelial barrier function and tight junction proteins with heat and exercise. J Appl Physiol 120:692–701CrossRefPubMedGoogle Scholar
  13. Duncan RF (2005) Inhibition of Hsp90 function delays and impairs recovery from heat shock. FEBS J 272:5244–5256CrossRefPubMedGoogle Scholar
  14. Erekat N, Al-Khatib A, Al-Jarrah M (2014) Heat shock protein 90 is a potential therapeutic target for ameliorating skeletal muscle abnormalities in Parkinson’s disease. Neural Regen Res 9:616–621CrossRefPubMedPubMedCentralGoogle Scholar
  15. Erlejman AG, Lagadari M, Toneatto J, Piwien-Pilipuk G, Galigniana MD (2014) Regulatory role of the 90-kDa-heat-shock protein (Hsp90) and associated factors on gene expression. Biochim Biophys Acta 1839:71–87CrossRefPubMedGoogle Scholar
  16. Febbraio MA, Koukoulas I (2000) HSP72 gene expression progressively increases in human skeletal muscle during prolonged, exhaustive exercise. J Appl Physiol 89:1055–1060PubMedGoogle Scholar
  17. Febbraio MA, Steensberg A, Walsh R, Koukoulas I, van Hall G, Saltin B, Pedersen BK (2002) Reduced glycogen availability is associated with an elevation in HSP72 in contracting human skeletal muscle. J Physiol 538:911–917CrossRefPubMedPubMedCentralGoogle Scholar
  18. Fehrenbach E, Niess AM, Schlotz E, Passek F, Dickhuth HH, Northoff H (2000) Transcriptional and translational regulation of heat shock proteins in leukocytes of endurance runners. J Appl Physiol 89:704–710PubMedGoogle Scholar
  19. Fehrenbach E, Niess AM, Veith R, Dickhuth HH, Northoff H (2001) Changes of HSP72-expression in leukocytes are associated with adaptation to exercise under conditions of high environmental temperature. J Leukoc Biol 69:747–754PubMedGoogle Scholar
  20. Fehrenbach E, Veith R, Schmid M, Dickhuth H-H, Northoff H, Niess AM (2003) Inverse response of leukocyte heat shock proteins and DNA damage to exercise and heat. Free Radic Res 37:975–982CrossRefPubMedGoogle Scholar
  21. Garrett AT, Goosens NG, Rehrer NJ, Patterson MJ, Harrison J, Sammut I, Cotter JD (2014) Short-term heat acclimation is effective and may be enhanced rather than impaired by dehydration. Am J Hum Biol 26:311–320CrossRefPubMedGoogle Scholar
  22. Gibson OR, Dennis A, Parfitt T, Taylor L, Watt PW, Maxwell NS (2014) Extracellular Hsp72 concentration relates to a minimum endogenous criteria during acute exercise-heat exposure. Cell Stress Chaperones 19:389–400CrossRefPubMedGoogle Scholar
  23. Gibson OR, Mee JA, Taylor L, Tuttle JA, Watt PW, Maxwell NS, Taylor L, Watt PW, Maxwell NS (2015a) Isothermic and fixed-intensity heat acclimation methods elicit equal increases in Hsp72 mRNA. Scand J Med Sci Sports 25:259–268CrossRefPubMedGoogle Scholar
  24. Gibson OR, Mee JA, Tuttle JA, Taylor L, Watt PW, Maxwell NS (2015b) Isothermic and fixed intensity heat acclimation methods induce similar heat adaptation following short and long-term timescales. J Therm Biol 49-50:55–65CrossRefPubMedGoogle Scholar
  25. Gibson OR, Turner G, Tuttle JA, Taylor L, Watt PW, Maxwell NS (2015c) Heat acclimation attenuates physiological strain and the HSP72, but not HSP90α, mRNA response to acute normobaric hypoxia. J Appl Physiol 119:889–899CrossRefPubMedGoogle Scholar
  26. Giraldo E, Multhoff G, Ortega E (2010) Noradrenaline increases the expression and release of Hsp72 by human neutrophils. Brain Behav Immun 24:672–677CrossRefPubMedGoogle Scholar
  27. Gupte AA, Bomhoff GL, Touchberry CD, Geiger PC (2011) Acute heat treatment improves insulin-stimulated glucose uptake in aged skeletal muscle. J Appl Physiol 110:451–457CrossRefPubMedGoogle Scholar
  28. 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 (2014a) Activating HSP72 in rodent skeletal muscle increases mitochondrial number and oxidative capacity and decreases insulin resistance. Diabetes 63:1881–1894CrossRefPubMedPubMedCentralGoogle Scholar
  29. Henstridge DC, Febbraio MA, Hargreaves M (2016) Heat shock proteins and exercise adaptations. Our knowledge thus far and the road still ahead. J Appl Physiol 120:683–691CrossRefPubMedGoogle Scholar
  30. Henstridge DC, Whitham M, Febbraio MA (2014b) Chaperoning to the metabolic party: the emerging therapeutic role of heat-shock proteins in obesity and type 2 diabetes. Mol Metab 3:781–793CrossRefPubMedPubMedCentralGoogle Scholar
  31. Hillman AR, Vince RV, Taylor L, McNaughton L, Mitchell N, Siegler J (2011) Exercise-induced dehydration with and without environmental heat stress results in increased oxidative stress. Appl Physiol Nutr Metab 36:698–706CrossRefPubMedGoogle Scholar
  32. Hom LL, Lee EC-H, Apicella JM, Wallace SD, Emmanuel H, Klau JF, Poh PYS, Marzano S, Armstrong LE, Casa DJ, Maresh CM (2012) Eleven days of moderate exercise and heat exposure induces acclimation without significant HSP70 and apoptosis responses of lymphocytes in college-aged males. Cell Stress Chaperones 17:29–39CrossRefPubMedGoogle Scholar
  33. Hooper PL, Balogh G, Rivas E, Kavanagh K, Vigh L (2014) The importance of the cellular stress response in the pathogenesis and treatment of type 2 diabetes. Cell Stress Chaperones 19:447–464CrossRefPubMedPubMedCentralGoogle Scholar
  34. Horowitz M (2014) Heat acclimation, epigenetics, and cytoprotection memory. Compr Physiol 4:199–230CrossRefPubMedGoogle Scholar
  35. Horowitz M (2016) Epigenetics and cytoprotection with heat acclimation. J Appl Physiol 120:702–710CrossRefPubMedGoogle Scholar
  36. Hubbard RW, Bowers WD, Matthew WT, Curtis FC, Criss RE, Sheldon GM, Ratteree JW (1977) Rat model of acute heatstroke mortality. J Appl Physiol 42:809–816PubMedGoogle Scholar
  37. Kampinga HH, Hageman J, Vos MJ, Kubota H, Tanguay RM, Bruford EA, Cheetham ME, Chen B, Hightower LE (2009) Guidelines for the nomenclature of the human heat shock proteins. Cell Stress Chaperones 14:105–111CrossRefPubMedGoogle Scholar
  38. Kenny GP, Sigal RJ, McGinn R (2016) Body temperature regulation in diabetes. Temperature 3:119–145CrossRefGoogle Scholar
  39. Khassaf M, Child RB, McArdle A, Brodie DA, Esanu C, Jackson MJ (2001) Time course of responses of human skeletal muscle to oxidative stress induced by nondamaging exercise. J Appl Physiol 90:1031–1035PubMedGoogle Scholar
  40. Krause M, Heck TG, Bittencourt A, Scomazzon SP, Newsholme P, Curi R, Homem De Bittencourt PI (2015a) The chaperone balance hypothesis: the importance of the extracellular to intracellular HSP70 ratio to inflammation-driven type 2 diabetes, the effect of exercise, and the implications for clinical management. Mediat Inflamm 249205:12Google Scholar
  41. Krause M, Ludwig MS, Heck TG, Takahashi HK (2015b) Heat shock proteins and heat therapy for type 2 diabetes: pros and cons. Curr Opin Clin Nutr Metab Care 18:374–380CrossRefPubMedGoogle Scholar
  42. Kregel KC (2002) Heat shock proteins: modifying factors in physiological stress responses and acquired thermotolerance. J Appl Physiol 92:2177–2186CrossRefPubMedGoogle Scholar
  43. Kuennen M, Gillum T, Dokladny K, Bedrick E, Schneider S, Moseley P (2011) Thermotolerance and heat acclimation may share a common mechanism in humans. Am J Physiol Regul Integr Comp Physiol 301:R524–R533CrossRefPubMedPubMedCentralGoogle Scholar
  44. Kurucz I, Morva A, Vaag A, Eriksson K-F, Huang X, Groop L, Koranyi L (2002) Decreased expression of heat shock protein 72 in skeletal muscle of patients with type 2 diabetes correlates with insulin resistance. Diabetes 51:1102–1109CrossRefPubMedGoogle Scholar
  45. Lee BJ, Miller A, James RS, Thake CD (2016) Cross acclimation between heat and hypoxia: heat acclimation improves cellular tolerance and exercise performance in acute normobaric hypoxia. Front Physiol 7:78PubMedPubMedCentralGoogle Scholar
  46. Lee EC, Muñoz CX, McDermott BP, Beasley KN, Yamamoto LM, Hom LL, Casa DJ, Armstrong LE, Kraemer WJ, Anderson JM, Maresh CM (2015) Extracellular and cellular Hsp72 differ as biomarkers in acute exercise/environmental stress and recovery. Scand J Med Sci SportsGoogle Scholar
  47. 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
  48. Logan-Sprenger HM, Heigenhauser GJF, Jones GL, Spriet LL (2015) The effect of dehydration on muscle metabolism and time trial performance during prolonged cycling in males. Physiol Rep 3Google Scholar
  49. Lyashko VN, Vikulova VK, Chernicov VG, Ivanov VI, Ulmasov KA, Zatsepina OG, Evgen’ev MB (1994) Comparison of the heat shock response in ethnically and ecologically different human populations. Proc Natl Acad Sci U S A 91:12492–12495CrossRefPubMedPubMedCentralGoogle Scholar
  50. Magalhães FDC, Amorim FT, Passos RLF, Fonseca MA, Oliveira KPM, Lima MRM, Guimarães JB, Ferreira-Júnior JB, Martini ARP, Lima NRV, Soares DD, Oliveira EM, Rodrigues LOC (2010) Heat and exercise acclimation increases intracellular levels of Hsp72 and inhibits exercise-induced increase in intracellular and plasma Hsp72 in humans. Cell Stress Chaperones 15:885–895CrossRefPubMedCentralGoogle Scholar
  51. Maloyan A, Horowitz M (2002) Beta-adrenergic signaling and thyroid hormones affect HSP72 expression during heat acclimation. J Appl Physiol 93:107–115CrossRefPubMedGoogle Scholar
  52. Marshall HC, Campbell SA, Roberts CW, Nimmo MA (2007) Human physiological and heat shock protein 72 adaptations during the initial phase of humid-heat acclimation. J Therm Biol 32:341–348CrossRefGoogle Scholar
  53. Maughan RJ, Otani H, Watson P (2012) Influence of relative humidity on prolonged exercise capacity in a warm environment. Eur J Appl Physiol 112:2313–2321CrossRefPubMedGoogle Scholar
  54. McClung JP, Hasday JD, He J-RR, Montain SJ, Cheuvront SN, Sawka MN, Singh IS (2008) Exercise-heat acclimation in humans alters baseline levels and ex vivo heat inducibility of HSP72 and HSP90 in peripheral blood mononuclear cells. Am J Physiol Regul Integr Comp Physiol 294:R185–R191CrossRefPubMedGoogle Scholar
  55. Mestre-Alfaro A, Ferrer MD, Banquells M, Riera J, Drobnic F, Sureda A, Tur JA, Pons A (2012) Body temperature modulates the antioxidant and acute immune responses to exercise. Free Radic Res 46:799–808CrossRefPubMedGoogle Scholar
  56. Mohr M, Nybo L, Grantham J, Racinais S (2012) Physiological responses and physical performance during football in the heat. PLoS One 7:e39202CrossRefPubMedPubMedCentralGoogle Scholar
  57. Moran DS, Eli-Berchoer L, Heled Y, Mendel L, Schocina M, Horowitz M (2006) Heat intolerance: does gene transcription contribute? J Appl Physiol 100:1370–1376CrossRefPubMedGoogle Scholar
  58. Morton JP, Holloway K, Woods P, Cable NT, Burniston J, Evans L, Kayani AC, McArdle A (2009) Exercise training-induced gender-specific heat shock protein adaptations in human skeletal muscle. Muscle Nerve 39:230–233CrossRefPubMedGoogle Scholar
  59. Morton JP, Maclaren DPM, Cable NT, Campbell IT, Evans L, Bongers T, Griffiths RD, Kayani AC, McArdle A, Drust B (2007) Elevated core and muscle temperature to levels comparable to exercise do not increase heat shock protein content of skeletal muscle of physically active men. Acta Physiol (Oxf) 190:319–327CrossRefGoogle Scholar
  60. Moseley PL (2000) Exercise, stress, and the immune conversation. Exerc Sport Sci Rev 28:128–132PubMedGoogle Scholar
  61. Moseley PL (1997) Heat shock proteins and heat adaptation of the whole organism. J Appl Physiol 83:1413–1417PubMedGoogle Scholar
  62. Noble EG, Shen GX (2012) Impact of exercise and metabolic disorders on heat shock proteins and vascular inflammation. Autoimmune Dis 2012:836519PubMedPubMedCentralGoogle Scholar
  63. Ortega E (2003) Neuroendocrine mediators in the modulation of phagocytosis by exercise: physiological implications. Exerc Immunol Rev 9:70–93PubMedGoogle Scholar
  64. Peart D, McNaughton L, Midgley A (2011) Pre-exercise alkalosis attenuates the heat shock protein 72 response to a single-bout of anaerobic exercise. J Sci 14:435–440Google Scholar
  65. Périard JD, Ruell P, Caillaud C, Thompson MW (2012) Plasma Hsp72 (HSPA1A) and Hsp27 (HSPB1) expression under heat stress: influence of exercise intensity. Cell Stress Chaperones 17:375–383CrossRefPubMedPubMedCentralGoogle Scholar
  66. Périard JD, Ruell PA, Thompson MW, Caillaud C (2015) Moderate- and high-intensity exhaustive exercise in the heat induce a similar increase in monocyte Hsp72. Cell Stress Chaperones 20:1037–1042CrossRefPubMedPubMedCentralGoogle Scholar
  67. Price MJ (2006) Thermoregulation during exercise in individuals with spinal cord injuries. Sports Med 36:863–879CrossRefPubMedGoogle Scholar
  68. Racinais S, Alonso JM, Coutts AJ, Flouris AD, Girard O, González-Alonso J, Hausswirth C, Jay O, Lee JKW, Mitchell N, Nassis GP, Nybo L, Pluim BM, Roelands B, Sawka MN, Wingo JE, Périard JD (2015) Consensus recommendations on training and competing in the heat. Scand J Med Sci Sports 25:6–19CrossRefPubMedGoogle Scholar
  69. Romberg A, Ikonen A, Ruutiainen J, Virtanen A, Hämäläinen P (2012) The effects of heat stress on physical functioning in persons with multiple sclerosis. J Neurol Sci 319:42–46CrossRefPubMedGoogle Scholar
  70. Ruell PA, Simar D, Périard JD, Best S, Caillaud C, Thompson MW (2014) Plasma and lymphocyte Hsp72 responses to exercise in athletes with prior exertional heat illness. Amino Acids 46:1491–1499CrossRefPubMedGoogle Scholar
  71. Sawka MN, Burke LM, Eichner ER, Maughan RJ, Montain SJ, Stachenfeld NS (2007) American College of Sports Medicine position stand. Exercise and fluid replacement. Med Sci Sports Exerc 39:377–390CrossRefPubMedGoogle Scholar
  72. Sawka MN, Latzka WA, Montain SJ, Cadarette BS, Kolka MA, Kraning KK 2nd, Gonzalez RR (2001) Physiologic tolerance to uncompensable heat: intermittent exercise, field vs laboratory. Med Sci Sport Exerc 33:422–430CrossRefGoogle Scholar
  73. Selkirk GA, McLellan TM, Wright HE, Rhind SG (2009) Expression of intracellular cytokines, HSP72, and apoptosis in monocyte subsets during exertional heat stress in trained and untrained individuals. Am J Physiol Regul Integr Comp Physiol 296:R575–R586CrossRefPubMedGoogle Scholar
  74. Shin Y-O, Oh J-K, Sohn H-S, Bae J-S, Lee M-Y, Lee J-B, Yang H-M, Min Y-K, Song H-Y, Ko K-K, Matsumoto T (2004) Expression of exercise-induced HSP70 in long-distance runner’s leukocytes. J Therm Biol 29:769–774CrossRefGoogle Scholar
  75. Silver JT, Noble EG (2012) Regulation of survival gene hsp70. Cell Stress Chaperones 17:1–9CrossRefPubMedGoogle Scholar
  76. Sonna LA, Hawkins L, Lissauer ME, Maldeis P, Towns M, Johnson SB, Moore R, Singh IS, Cowan MJ, Hasday JD (2010) Core temperature correlates with expression of selected stress and immunomodulatory genes in febrile patients with sepsis and noninfectious SIRS. Cell Stress Chaperones 15:55–66CrossRefPubMedGoogle Scholar
  77. Stary CM, Hogan MC (2016) Cytosolic calcium transients are a determinant of contraction-induced HSP72 transcription in single skeletal muscle fibers. J Appl Physiol. doi: 10.1152/japplphysiol.01060.2015 Google Scholar
  78. Stary CM, Walsh BJ, Knapp AE, Brafman D, Hogan MC (2008) Elevation in heat shock protein 72 mRNA following contractions in isolated single skeletal muscle fibers. Am J Physiol Regul Integr Comp Physiol 295:R642–R648CrossRefPubMedPubMedCentralGoogle Scholar
  79. Subbarao Sreedhar A, Kalmár É, Csermely P, Shen Y-F (2004) Hsp90 isoforms: functions, expression and clinical importance. FEBS Lett 562:11–15CrossRefGoogle Scholar
  80. Sureda A, Tauler P, Aguiló A, Cases N, Fuentespina E, Córdova A, Tur JA, Pons A (2005) Relation between oxidative stress markers and antioxidant endogenous defences during exhaustive exercise. Free Radic Res 39:1317–1324CrossRefPubMedGoogle Scholar
  81. Taipale M, Jarosz DF, Lindquist S (2010) HSP90 at the hub of protein homeostasis: emerging mechanistic insights. Nat Rev Mol Cell Biol 11:515–528CrossRefPubMedGoogle Scholar
  82. Taylor HL, Buskirk E, Henschel A (1955) Maximal oxygen intake as an objective measure of cardio-respiratory performance. J Appl Physiol 8:73–80PubMedGoogle Scholar
  83. Taylor L, Midgley A, Chrismas B (2010a) The effect of acute hypoxia on heat shock protein 72 expression and oxidative stress in vivo. Eur J Appl Physiol 109:849–855CrossRefPubMedGoogle Scholar
  84. Taylor L, Midgley AW, Chrismas B, Hilman AR, Madden LA, Vince RV, McNaughton LR (2011) Daily hypoxia increases basal monocyte HSP72 expression in healthy human subjects. Amino Acids 40:393–401CrossRefPubMedGoogle Scholar
  85. Taylor L, Midgley AW, Chrismas B, Madden LA, Vince RV, McNaughton LR (2010b) Daily quadratic trend in basal monocyte expressed HSP72 in healthy human subjects. Amino Acids 38:1483–1488CrossRefPubMedGoogle Scholar
  86. Taylor NAS, Cotter JD (2006) Heat adaptation: guidelines for the optimisation of human performance. Int Sport Med J 7:33–57Google Scholar
  87. Tintinger GR, Theron AJ, Anderson R, Ker JA (2001) The anti-inflammatory interactions of epinephrine with human neutrophils in vitro are achieved by cyclic AMP-mediated accelerated resequestration of cytosolic calcium. Biochem Pharmacol 61:1319–1328CrossRefPubMedGoogle Scholar
  88. Tuttle JA, Castle PC, Metcalfe AJ, Midgley AW, Taylor L, Lewis MP (2015) Downhill running and exercise in hot environments increase leukocyte Hsp 72 (HSPA1A) and Hsp90α (HSPC1) gene transcripts. J Appl Physiol 118:996–1005CrossRefPubMedGoogle Scholar
  89. Vihervaara A, Sistonen L (2014) HSF1 at a glance. J Cell Sci 127:261–266CrossRefPubMedGoogle Scholar
  90. Watkins AM, Cheek DJ, Harvey AE, Goodwin JD, Blair KE, Mitchell JB (2007) Heat shock protein (HSP-72) levels in skeletal muscle following work in heat. Aviat Sp Environ Med 78:901–905Google Scholar
  91. Whitham M, Laing SJ, Jackson A, Maassen N, Walsh NP (2007) Effect of exercise with and without a thermal clamp on the plasma heat shock protein 72 response. J Appl Physiol 103:1251–1256CrossRefPubMedGoogle Scholar

Copyright information

© Cell Stress Society International 2016

Authors and Affiliations

  • Oliver R. Gibson
    • 1
    • 2
    Email author
  • James A. Tuttle
    • 3
  • Peter W. Watt
    • 2
  • Neil S. Maxwell
    • 2
  • Lee Taylor
    • 4
    • 5
  1. 1.Centre for Human Performance, Exercise and Rehabilitation (CHPER)Brunel University LondonUxbridgeUK
  2. 2.Centre for Sport and Exercise Science and Medicine (SESAME), Environmental Extremes Laboratory, Welkin Human Performance LaboratoriesUniversity of BrightonEastbourneUK
  3. 3.Muscle Cellular and Molecular Physiology (MCMP) and Applied Sport and Exercise Science (ASEP) Research Groups, Institute of Sport and Physical Activity Research (ISPAR)University of BedfordshireBedfordUK
  4. 4.Athlete Health and Performance Research CentreASPETAR, Qatar Orthopaedic and Sports Medicine HospitalDohaQatar
  5. 5.School of Sport, Exercise and Health SciencesLoughborough UniversityLoughboroughUK

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