Modulation of rat monocyte/macrophage innate functions by increasing intensities of swimming exercise is associated with heat shock protein status

Abstract

Moderate exercise positively impacts innate immune functions, bringing about a better resistance against infections and general immunosurveillance. Exercise of high workloads (i.e., high intensity and/or duration) such as elite marathon, on the other hand, may have detrimental effects over immune function, but neither how long nor how intense should be the exercise sessions to be deleterious is known, this being a matter of intense dispute. Exercise is, at the same time, one of the most powerful inducers of the 70 kDa family of heat shock proteins (HSPAs, formerly known as HSP70s), which are protein chaperones characterized by a marked anti-inflammatory potency, when located intracellularly (iHSPA), but may act as pro-inflammatory cytokines if in the extracellular space (eHSPA). The above observations led us to suppose that short-term exercise could impose long-lasting effects on macrophage function that should be related to the eHSPA-to-iHSPA ratio, viz. H-index. Sedentary adult male Wistar rats were then submitted to 20 min swimming sessions with an overload (as a percentage of body weight attached to the tail base) of either 2, 4, 6, or 8 %. Control animals were maintained at rest in shallow water. Monocyte/macrophage functions (phagocytic capacity, nitric oxide [NO], and hydrogen peroxide [H2O2]) were assessed just after and 12 h after exercise and compared with HSPA status and oxidative stress markers. The results showed that exercise increased phagocytosis and H2O2 immediately after the bouts in a workload-dependent way. This was accompanied by increased H-index but no alteration in the redox status. Enhanced phagocytic capacity persisted for up to 12 h, when a marked rise in NO production was also observed, but H-index resumes its control values, suggesting that immune alertness returned to basal levels. Of note was the detection of the cognate form of eHSPA (encoded by hspa8 gene and formerly known as HSP73) in the rat sera. In total, acute exercise may evoke 12 h long workload-dependent effects associated with HSPA status.

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Acknowledgements and funding

PIHBJ is responsible for grant support with respect to Brazilian National Council for Scientific and Technological Development (CNPq, Grants #402626/2012–5 and #402364/2012–0). TGH was supported by CNPq [#382692/2011–0] and State of Rio Grande do Sul Foundation for Research Support (FAPERGS, grant # 002106–2551/13–5). CMS was recipient of a scholarship from CAPES (The Brazilian Ministry of Education Coordination for the Improvement of Higher Education Personnel).

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Correspondence to Paulo Ivo Homem de Bittencourt Jr..

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CMS, TGH, LPOJ, and PIHBJ designed the study. CMS, CVM, GSS, and TGH completed all the experiments described in this manuscript. CMS, LPOJ, TGH, and PIHBJ analyzed the results. CMS and PIHBJ co-wrote the article. PIHBJ provided experimental advice and revised the final version of the manuscript. All the authors had final approval of the submitted and published versions.

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The authors declare no conflict of interest and no competing interests such as consultancies, financial involvement, patent ownership, etc. in relation to the work described herein. CNPq, FAPERGS and CAPES (the funding organisms) had no involvement in the propositions presented in this manuscript.

Ethical approval

All the procedures performed in studies involving the animals followed the ethical rules established by Arouca’s Act (Federal Law 11794/2008) and the Guide for Care and Use of Experimental Animals published by the National Institutes of Health (NIH publication no. 85-23, revised in 1996). The procedures were approved by the Federal University of Rio Grande do Sul Ethics Committee on Animal Experimentation (CEUA #23451), according to the guidelines of the Brazilian National Council for the Control of Animal Experimentation (CONCEA).

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Schöler, C.M., Marques, C.V., da Silva, G.S. et al. Modulation of rat monocyte/macrophage innate functions by increasing intensities of swimming exercise is associated with heat shock protein status. Mol Cell Biochem 421, 111–125 (2016). https://doi.org/10.1007/s11010-016-2791-1

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Keywords

  • Exercise
  • Monocyte/macrophage
  • Heat shock protein
  • Phagocytosis
  • Hydrogen peroxide
  • Nitric oxide