Abstract
This study examined the relationship between exhaustive exercise in the heat at moderate and high intensities on the intracellular heat shock protein 72 (iHsp72) response. Twelve male subjects cycled to exhaustion at 60 and 75 % of maximal oxygen uptake in hot conditions (40 °C, 50 % RH). iHsp72 concentration was measured in monocytes before, at exhaustion and 24 h after exercise. Rectal temperature, heart rate and oxygen uptake were recorded during exercise. Volitional exhaustion occurred at 58.9 ± 12.1 and 27.3 ± 9.5 min (P < 0.001) and a rectal temperature of 39.8 ± 0.4 and 39.2 ± 0.6 °C (P = 0.002), respectively, for 60 and 75 %. The area under the curve above a rectal temperature of 38.5 °C was greater at 60 % (17.5 ± 6.6 °C min) than 75 % (3.4 ± 4.8 °C min; P < 0.001), whereas the rate of increase in rectal temperature was greater at 75 % (5.1 ± 1.7 vs. 2.2 ± 1.4 °C h−1; P < 0.001). iHsp72 concentration increased similarly at exhaustion relative to pre-exercise (P = 0.044) and then increased further at 24 h (P < 0.001). Multiple regression analysis revealed no predictor variables associated with iHsp72 expression; however, a correlation was observed between exercise intensities for the increase in iHsp expression at exhaustion and 24 h (P < 0.05). These results suggest that iHsp72 expression increased in relation to the level of hyperthermia attained and sustained at 60 % and the higher metabolic rate and greater rate of increase in core temperature at 75 %, with the further increase in iHsp72 concentration 24 h after exercise reinforcing its role as a chaperone and cytoprotective agent.
References
Asea A (2007) Mechanisms of HSP72 release. J Biosci 32:579–584
Asea A, Kraeft S-T, Kurt-Jones EA, Stevenson MA, Chen LB, Finberg RW, Koo GC, Calderwood SK (2000) HSP70 stimulates cytokine production through a CD14-dependant pathway, demonstrating its dual role as a chaperone and cytokine. Nat Med 6:435–442
Donati YR, Slosman DO, Polla BS (1990) Oxidative injury and the heat shock response. Biochem Pharmacol 40:2571–2577
Febbraio MA, Koukoulas I (2000) HSP72 gene expression progressively increases in human skeletal muscle during prolonged, exhaustive exercise. J Appl Physiol 89:1055–1060
Febbraio MA, Ott P, Nielsen HB, Steensberg A, Keller C, Krustrup P, Secher NH, Pedersen BK (2002) Exercise induces hepatosplanchnic release of heat shock protein 72 in humans. J Physiol 544:957–962
Fehrenbach E, Niess AM, Schlotz E, Passek F, Dickhuth H-H, Northoff H (2000a) Transcriptional and translational regulation of heat shock proteins in leukocytes of endurance runners. J Appl Physiol 89:704–710
Fehrenbach E, Passek F, Niess AM, Pohla H, Weinstock C, Dickhuth H-H, Northoff H (2000b) HSP expression in human leukocytes is modulated by endurance exercise. Med Sci Sports Exerc 32:592–600
Fehrenbach E, Niess AM, Veith R, Dickhuth H-H, Northoff H (2001) Changes of HSP72-expression in leukocytes are associated with adaptation to exercise under conditions of high environmental temperature. J Leukoc Biol 69:747–754
Fehrenbach E, Veith R, Schmid M, Dickhuth HH, Northoff H, Niess AM (2003) Inverse response of leukocyte heat shock proteins and DNA damage to exercise and heat. Free Radic Res 37:975–982
Flanagan SW, Ryan AJ, Gisolfi CV, Moseley PL (1995) Tissue-specific HSP70 response in animals undergoing heat stress. Am J Physiol 268:R28–R32
Fleshner M, Johnson JD (2005) Endogenous extra-cellular heat shock protein 72: releasing signal(s) and function. Int J Hyperther 21:457–471
Gibson OR, Dennis A, Parfitt T, Taylor L, Watt PW, Maxwell NS (2013) Extracellular Hsp72 concentration relates to a minimum endogenous criteria during acute exercise-heat exposure. Cell Stress Chaperones
Graziani-Bowering GM, Graham JM, Filion LG (1997) A quick, easy and inexpensive method for the isolation of human peripheral blood monocytes. J Immunol Methods 207:157–168
Heck TG, Scholer CM, de Bittencourt PI (2011) HSP70 expression: does it a novel fatigue signalling factor from immune system to the brain? Cell Biochem Funct 29:215–226
Hom LL, Lee EC, Apicella JM, Wallace SD, Emmanuel H, Klau JF, Poh PY, 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 17:29–39
Kregel KC (2002) Heat shock proteins: modifying factors in physiological stress responses and acquired thermotolerance. J Appl Physiol (1985) 92:2177–2186
Kwak DJ, Augustine NH, Borges WG, Joyner JL, Green WF, Hill HR (2000) Intracellular and extracellular cytokine production by human mixed mononuclear cells in response to group B streptococci. Infect Immun 68:320–327
Lancaster GI, Moller K, Nielsen B, Secher NH, Febbraio MA, Nybo L (2004) Exercise induces the release of heat shock protein 72 from the human brain in vivo. Cell Stress Chaperones 9:276–280
Lee BJ, Emery-Sincliar EL, Mackenzie RWA, Hussain A, Taylor L, James RS, Thake CD (2014) The impact of submaximal exercise during heat and/or hypoxia on the cardiovascular and monocyte HSP72 responses to subsequent (post 24 h) exercise in hypoxia. Extreme Physiol Med 3:1–16
Lee BJ, Mackenzie RW, Cox V, James RS, Thake CD (2015) Human monocyte heat shock protein 72 responses to acute hypoxic exercise after 3 days of exercise heat acclimation. BioMed Res Int 2015:849809
Locke M (1997) The cellular stress response to exercise: role of stress proteins. Exerc Sport Sci Rev 25:105–136
Lovell R, Madden L, McNaughton LR, Carroll S (2008) Effects of active and passive hyperthermia on heat shock protein 70 (HSP70). Amino Acids 34:203–211
Magalhaes FC, Amorim FT, Passos RL, Fonseca MA, Oliveira KP, Lima MR, Guimaraes JB, Ferreira-Junior JB, Martini AR, Lima NR, Soares DD, Oliveira EM, Rodrigues LO (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 15:885–895
Marshall HC, Ferguson RA, Nimmo MA (2006) Human resting extracellular heat shock protein 72 concentration decreases during the initial adaptation to exercise in a hot, humid environment. Cell Stress Chaperones 11:129–134
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 32:341–348
McClung JP, Hasday JD, He JR, 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–R191
Noble EG, Milne KJ, Melling CW (2008) Heat shock proteins and exercise: a primer. Appl Physiol, Nutr Metab 33:1050–1065
Oehler R, Pusch E, Zellner M, Dungel P, Hergovics N, Homoncik M, Eliasen MM, Brabec M, Roth E (2001) Cell type-specific variations in the induction of hsp70 in human leukocytes by feverlike whole body hyperthermia. Cell Stress Chaperones 6:306–315
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 17:375–383
Pockley AG (2003) Heat shock proteins as regulators of the immune response. Lancet 362:469–476
Ruell PA, Hoffman KM, Chow CM, Thompson MW (2004) Effect of temperature and duration of hyperthermia on HSP72 induction in rat tissues. Mol Cell Biochem 267:187–194
Ruell PA, Thompson MW, Hoffman KM, Brotherhood JR, Richards DAB (2007) Lymphocyte HSP72 following exercise in hyperthermic runners: the effect of temperature. J Therm Biol 32:406–412
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–R586
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 29:769–774
Skidmore R, Gutierrez JA, Guerriero V Jr, Kregel KC (1995) HSP70 induction during exercise and heat stress in rats: role of internal temperature. Am J Physiol 268:R92–R97
Sonna LA, Gaffin SL, Pratt RE, Cullivan ML, Angel KC, Lilly CM (2001) Selected Contribution: effect of acute heat shock on gene expression by human peripheral blood mononuclear cells. J Appl Physiol 92:2208–2220.
Walters TJ, Ryan KL, Tehrany MR, Jones MB, Paulus LA, Mason PA (1998) HSP70 expression in the CNS in response to exercise and heat stress in rats. J Appl Physiol 84:1269–1277
Watkins AM, Cheek DJ, Harvey AE, Blair KE, Mitchell JB (2008) Heat acclimation and HSP-72 expression in exercising humans. Int J Sports Med 29:269–276
Whitham M, Fortes MB (2008) Heat shock protein 72: release and biological significance during exercise. Front Biosci 1:1328–1339
Whitham M, Halson SL, Lancaster GI, Gleeson M, Jeukendrup AE, Blannin AK (2004) Leukocyte heat shock protein expression before and after intensified training. Int J Sports Med 25:522–527
Yamada PM, Amorim FT, Moseley P, Robergs R, Schneider SM (2007) Effect of heat acclimation on heat shock protein 72 and interleukin-10 in humans. J Appl Physiol (1985) 103:1196–1204
Acknowledgments
The authors thank all the subjects that participated in this investigation. The authors also thank Rhys Philips, Madeline Lynch, Colin Tuohy, Carl Cheah, Angelina Tan and Thomas Wüthrich for their help with the data collection. This work was supported by the University of Sydney Faculty of Health Sciences.
Author information
Authors and Affiliations
Corresponding author
Rights and permissions
About this article
Cite this article
Périard, J.D., Ruell, P.A., Thompson, M.W. et al. Moderate- and high-intensity exhaustive exercise in the heat induce a similar increase in monocyte Hsp72. Cell Stress and Chaperones 20, 1037–1042 (2015). https://doi.org/10.1007/s12192-015-0631-y
Received:
Revised:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s12192-015-0631-y