Skip to main content

Advertisement

Log in

Effects of whole-body heat acclimation on cell injury and cytokine responses in peripheral blood mononuclear cells

  • Original Article
  • Published:
European Journal of Applied Physiology Aims and scope Submit manuscript

Abstract

To test the hypothesis that whole-body heat acclimation (HA) would increase peripheral blood mononuclear cells’ (PBMC) tolerance to heat shock (HS) and/or alter the release of cytokines (IL-1β, IL-6, IL-10 and TNF-α) to bacterial lipopolysaccharide (LPS), we heat acclimated nine subjects by exercising them for 100 min in a hot environment for 10 days. The subjects’ PBMC were separated and cultured on days 1 and 10 of HA pre- and post-exercise. Pre-exercise PBMC were allocated to three treatments: control (PRE, 37°C), HS (42.5°C for 2 h), or LPS (1 ng mL−1 for 24 h). Post-exercise samples were incubated at 37°C. PBMC lactate dehydrogenase release increased (p < 0.05) after HS but it was not different (p > 0.05) between days 1 and 10 (0.100 ± 0.012 and 0.102 ± 0.16 abs., respectively). LPS treatment induced an increased (p < 0.05) release of cytokines but HA did not alter this response (p > 0.05). Pre-exercise intracellular heat shock protein 72 (Hsp72) was higher (p < 0.05) on day 10 compared to day 1 of HA (13 ± 5 and 8 ± 5 ng mL−1, respectively). HS treatment caused a greater increase (p < 0.05) in Hsp72 than the exercise sessions on HA days 1 and 10. In addition, after HA, the Hsp72 response to HS was reduced (day 1, 129 ± 46; day 10, 80 ± 32 ng mL−1, p < 0.05). In conclusion, HA increases PBMC Hsp72 but it does not reduce cellular damage to HS or alter cytokine response to LPS. We speculate that the stress applied during HA is not sufficient to modify the PBMC response.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6
Fig. 7

Similar content being viewed by others

References

  • American College of Sports Medicine (2000) ACSM’s guidelines for exercise testing and prescription. Lippincott Williams and Wilkins, New York

    Google Scholar 

  • Asai K, Hiki N, Mimura Y, Ogawa T, Unou K, Kaminishi M (2001) Gender differences in cytokine secretion by human peripheral blood mononuclear cells: role of estrogen in modulating LPS-induced cytokine secretion in an ex vivo septic model. Shock 16:340–343

    Article  PubMed  CAS  Google Scholar 

  • Bouchama A, Parhar RS, el-Yazigi A, Sheth K, al-Sedairy S (1991) Endotoxemia and release of tumor necrosis factor and interleukin 1 alpha in acute heatstroke. J Appl Physiol 70:2640–2644

    PubMed  CAS  Google Scholar 

  • Bouchama A, Knochel JP (2002) Heat stroke. N Engl J Med 346:1978–1988

    Article  PubMed  CAS  Google Scholar 

  • Chen D, Pan J, Du B, Sun D (2005) Induction of the heat shock response in vivo inhibits NF-kappaB activity and protects murine liver from endotoxemia-induced injury. J Clin Immunol 25:452–461

    Article  PubMed  CAS  Google Scholar 

  • Chang DM (1993) The role of cytokines in heat stroke. Immunol Invest 22:553–561

    Article  PubMed  CAS  Google Scholar 

  • Ding XZ, Fernandez-Prada CM, Bhattacharjee AK, Hoover DL (2001) Over-expression of hsp-70 inhibits bacterial lipopolysaccharide-induced production of cytokines in human monocyte-derived macrophages. Cytokine 16:210–219

    Article  PubMed  CAS  Google Scholar 

  • Dokladny K, Moseley PL, Ma TY (2006) Physiologically relevant increase in temperature causes an increase in intestinal epithelial tight junction permeability. Am J Physiol Gastrointest Liver Physiol 290:G204–G212

    Article  PubMed  CAS  Google Scholar 

  • 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 69:747–754

    PubMed  CAS  Google Scholar 

  • Gething MJ, Sambrook J (1992) Protein folding in the cell. Nature 355:33–45

    Article  PubMed  CAS  Google Scholar 

  • Heyward V (2006) Advanced fitness assessment and exercise prescription, 5th edn. Human Kinetics, Champaign, IL

    Google Scholar 

  • Hung CH, Chang NC, Cheng BC, Lin MT (2005) Progressive exercise preconditioning protects against circulatory shock during experimental heatstroke. Shock 23:426–433

    Article  PubMed  Google Scholar 

  • Jo SK, Ko GJ, Boo CS, Cho WY, Kim HK (2006) Heat preconditioning attenuates renal injury in ischemic ARF in rats: role of heat-shock protein 70 on NF-{kappa}B-mediated inflammation and on tubular cell injury. J Am Soc Nephrol 17:3082–3092

    Article  PubMed  CAS  Google Scholar 

  • King YT, Lin CS, Lin JH, Lee WC (2002) Whole-body hyperthermia-induced thermotolerance is associated with the induction of heat shock protein 70 in mice. J Exp Biol 205:273–278

    PubMed  CAS  Google Scholar 

  • Kregel KC (2002) Heat shock proteins: modifying factors in physiological stress responses and acquired thermotolerance. J Appl Physiol 92:2177–2186

    PubMed  CAS  Google Scholar 

  • Lee JI, Burckart GJ (1998) Nuclear factor kappa B: important transcription factor and therapeutic target. J Clin Pharmacol 38:981–993

    Article  PubMed  CAS  Google Scholar 

  • Leon LR, Helwig BG (2010) Heat stroke: role of the systemic inflammatory response. J Appl Physiol; Jun 3 [Epub ahead of print]

  • Leoni S, Brambilla D, Risuleo G, de Feo G, Scarsella G (2000) Effect of different whole body hyperthermic sessions on the heat shock response in mice liver and brain. Mol Cell Biochem 204:41–47

    Article  PubMed  CAS  Google Scholar 

  • Lim CL, Mackinnon LT (2006) The roles of exercise-induced immune system disturbances in the pathology of heat stroke: the dual pathway model of heat stroke. Sports Med 36:39–64

    Article  PubMed  Google Scholar 

  • Lu KC, Wang JY, Lin SH, Chu P, Lin YF (2004) Role of circulating cytokines and chemokines in exertional heatstroke. Crit Care Med 32:399–403

    Article  PubMed  CAS  Google Scholar 

  • Maloyan A, Palmon A, Horowitz M (1999) Heat acclimation increases the basal HSP72 level and alters its production dynamics during heat stress. Am J Physiol 276:R1506–R1515

    PubMed  CAS  Google Scholar 

  • Magalhães FD, Amorim FT, Passos RL, Fonseca MA, Oliveira KP, Lima MR, Guimarães JB, Ferreira-Júnior 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; Apr 23 [Epub ahead of print]

  • 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

    Article  PubMed  CAS  Google Scholar 

  • Myrianthefs P, Venetsanou k, Grouzi E, Boutzouka E, Evagelopoulou P, Fildissis G, Spiliotopoulou I, Baltopoulos G (2002) Monocyte normal immune response to LPS stimulation. Crit Care 6(Suppl 1):101

    Article  Google Scholar 

  • Mizzen LA, Welch WJ (1988) Characterization of the thermotolerant cell. I. Effects on protein synthesis activity and the regulation of heat-shock protein 70 expression. J Cell Biol 106:1105–1116

    Article  PubMed  CAS  Google Scholar 

  • Moseley PL, Gisolfi CV (1993) New frontiers in thermoregulation and exercise. Sports Med 16:163–167

    Article  PubMed  CAS  Google Scholar 

  • Moseley PL (1997) Heat shock proteins and heat adaptation of the whole organism. J Appl Physiol 83:1413–1417

    PubMed  CAS  Google Scholar 

  • Shi Y, Tu Z, Tang D, Zhang H, Liu M, Wang K, Calderwood SK, Xiao X (2006) The inhibition of LPS-induced production of inflammatory cytokines by HSP70 involves inactivation of the NF-kappaB pathway but not the MAPK pathways. Shock 26:277–284

    Article  PubMed  CAS  Google Scholar 

  • Sonna LA, Gaffin SL, Pratt RE, Cullivan ML, Angel KC, Lilly CM (2002) Effect of acute heat shock on gene expression by human peripheral blood mononuclear cells. J Appl Physiol 92:2208–2220

    PubMed  CAS  Google Scholar 

  • Sun D, Chen D, Du B, Pan J (2005) Heat shock response inhibits NF-kappaB activation and cytokine production in murine Kupffer cells. J Surg Res 129:114–121

    Article  PubMed  CAS  Google Scholar 

  • Téllez-Gil L, Mansilla-Roselló A, Collado-Torres A, Villar-del-Moral J, Garrote-Lara D, Villegas-Herrera T, Alvarez-Martín MJ, Ferrón-Orihuela JÁ (2002) Effect of pretreatment with interleukin-1 beta on inflammatory infiltrates and tissue damage after experimental endotoxic challenge. Crit Care Med 30:1820–1825

    Article  PubMed  Google Scholar 

  • Wang JL, Ke DS, Lin MT (2005) Heat shock pretreatment may protect against heatstroke-induced circulatory shock and cerebral ischemia by reducing oxidative stress and energy depletion. Shock 23:161–167

    Article  PubMed  Google Scholar 

  • 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(4):269–276

    Article  PubMed  CAS  Google Scholar 

  • Wyndham CH (1967) Effect of acclimatization on the sweat rate-rectal temperature relationship. J Appl Physiol 22:27–30

    PubMed  CAS  Google Scholar 

  • Wyndham CH, Rogers GG, Senay LC, Mitchell D (1976) Acclimization in a hot, humid environment: cardiovascular adjustments. J Appl Physiol 40:779–785

    PubMed  CAS  Google Scholar 

  • Wischmeyer PE, Riehm J, Singleton KD, Ren H, Musch MW, Kahana M, Chang EB (2003) Glutamine attenuates tumor necrosis factor-alpha release and enhances heat shock protein 72 in human peripheral blood mononuclear cells. Nutrition 19:1–6

    Article  PubMed  CAS  Google Scholar 

  • 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 103:1196–1204

    Article  PubMed  CAS  Google Scholar 

  • Zheng Z, Kim JY, Ma H, Lee JE, Yenari MA (2008) Anti-inflammatory effects of the 70 kDa heat shock protein in experimental stroke. J Cereb Blood Flow Metab 28:53–63

    Article  PubMed  CAS  Google Scholar 

Download references

Acknowledgments

We thank the volunteers for their participation. We acknowledge technical assistance of Lou Stevenson, Carol Morris, Walker Wharton, Karol Dokladny and Rebecca Lobb. The first author gratefully acknowledges the financial support by the Brazilian Government under CAPES-scholarship. This study was partially funded by National Institute of Arthritis and Musculoskeletal and Skin Diseases Grant AR40771 and by the Gatorade Student Award to Fabiano Amorim. The authors declare that they have no conflict of interest.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Fabiano Amorim.

Additional information

Communicated by Susan Ward.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Amorim, F., Yamada, P., Robergs, R. et al. Effects of whole-body heat acclimation on cell injury and cytokine responses in peripheral blood mononuclear cells. Eur J Appl Physiol 111, 1609–1618 (2011). https://doi.org/10.1007/s00421-010-1780-4

Download citation

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00421-010-1780-4

Keywords

Navigation