Skip to main content
SpringerLink
Log in

The Dose-Dependent Antioxidant Effects of Physical Exercise in the Hippocampus of Mice

  • Original Paper
  • Published:
Neurochemical Research Aims and scope Submit manuscript

Abstract

Exercise increases both the consumption of oxygen and the production of reactive species in biological tissues, and this is counterbalanced by antioxidant adaptations to regular physical training. When the intensity of exercise fluctuates between mild and moderate, it improves the status of reduction–oxidation balance in the brain and induces neuroplasticity. However, intense exercise can oxidize the brain and impair neurological function. The effect of the frequency of exercise, which is an important factor in physical training, is still unknown. The effect of periodic exercise on biomarkers of oxidative stress in the hippocampus of mice was evaluated in this study. Mice were made to run on a treadmill for 8 weeks, two, three, or five times per week, and their hippocampi and quadriceps femoris muscles were then dissected. Biomarkers of oxidative damage were negatively correlated with the frequency of exercise and mitochondrial muscular activity, while the sulfhydryl contents were positively correlated with exercise frequency. A logistic analysis revealed a dose-dependent effect of exercise on these biomarkers. In summary, these results suggested that manipulating the frequency of physical exercise could induce antioxidant-related adaptations in the hippocampi of adult mice.

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

Access this article

Log in via an institution

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

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2

Similar content being viewed by others

References

  1. Droge W (2002) Free radicals in the physiological control of cell function. Physiol Rev 82:47–95

    CAS  PubMed  Google Scholar 

  2. Aguiar AS Jr., Tuon T, Pinho CA, Silva LA, Andreazza AC, Kapczinski F, Quevedo J, Streck EL, Pinho RA (2008) Intense exercise induces mitochondrial dysfunction in mice brain. Neurochem Res 33:51–58

    Article  CAS  PubMed  Google Scholar 

  3. Camiletti-Moiron D, Aparicio VA, Aranda P, Radak Z (2013) Does exercise reduce brain oxidative stress? a systematic review. Scand J Med Sci Sports 23:e202–e212

    Article  CAS  PubMed  Google Scholar 

  4. Aguiar AS Jr., Tuon T, Soares FS, da Rocha LG, Silveira PC, Pinho RA (2008) The effect of n-acetylcysteine and deferoxamine on exercise-induced oxidative damage in striatum and hippocampus of mice. Neurochem Res 33:729–736

    Article  CAS  PubMed  Google Scholar 

  5. Mattson MP (2000) Neuroprotective signaling and the aging brain: take away my food and let me run. Brain Res 886:47–53

    Article  CAS  PubMed  Google Scholar 

  6. Radak Z, Toldy A, Szabo Z, Siamilis S, Nyakas C, Silye G, Jakus J, Goto S (2006) The effects of training and detraining on memory, neurotrophins and oxidative stress markers in rat brain. Neurochem Int 49:387–392

    Article  CAS  PubMed  Google Scholar 

  7. Kayser B (2003) Exercise starts and ends in the brain. Eur J Appl Physiol 90:411–419

    Article  PubMed  Google Scholar 

  8. Cotman CW, Berchtold NC (2002) Exercise: a behavioral intervention to enhance brain health and plasticity. Trends Neurosci 25:295–301

    Article  CAS  PubMed  Google Scholar 

  9. Stranahan AM, Lee K, Becker KG, Zhang Y, Maudsley S, Martin B, Cutler RG, Mattson MP (2010) Hippocampal gene expression patterns underlying the enhancement of memory by running in aged mice. Neurobiol Aging 31:1937–1949

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  10. Nakajima S, Ohsawa I, Ohta S, Ohno M, Mikami T (2010) Regular voluntary exercise cures stress-induced impairment of cognitive function and cell proliferation accompanied by increases in cerebral IGF-1 and GST activity in mice. Behav Brain Res 211:178–184

    Article  CAS  PubMed  Google Scholar 

  11. Moreira EL, Aguiar AS Jr., de Carvalho CR, Santos DB, de Oliveira J, de Bem AF, Xikota JC, Walz R, Farina M, Prediger RD (2013) Effects of lifestyle modifications on cognitive impairments in a mouse model of hypercholesterolemia. Neurosci Lett 541:193–198

    CAS  PubMed  Google Scholar 

  12. Chodzko-Zajko WJ, Proctor DN, Fiatarone Singh MA, Minson CT, Nigg CR, Salem GJ, Skinner JS (2009) American college of sports medicine position stand. exercise and physical activity for older adults. Med Sci Sports Exerc 41:1510–1530

    Article  PubMed  Google Scholar 

  13. Fischer JC, Ruitenbeek W, Berden JA, Trijbels JM, Veerkamp JH, Stadhouders AM, Sengers RC, Janssen AJ (1985) Differential investigation of the capacity of succinate oxidation in human skeletal muscle. Clin Chim Acta 153:23–36

    Article  CAS  PubMed  Google Scholar 

  14. Draper HH, Hadley M (1990) Malondialdehyde determination as index of lipid-peroxidation. Method Enzymol 186:421–431

    Article  CAS  Google Scholar 

  15. Levine RL, Garland D, Oliver CN, Amici A, Climent I, Lenz AG, Ahn BW, Shaltiel S, Stadtman ER (1990) Determination of carbonyl content in oxidatively modified proteins. Method Enzymol 186:464–478

    Article  CAS  Google Scholar 

  16. Lowry OH, Rosebrough NJ, Farr AL, Randall RJ (1951) Protein measurement with the Folin phenol reagent. J Biol Chem 193:265–275

    CAS  PubMed  Google Scholar 

  17. Robergs RA, Ghiasvand F, Parker D (2004) Biochemistry of exercise-induced metabolic acidosis. Am J Physiol Regul Integr Comp Physiol 287:R502–R516

    Article  CAS  PubMed  Google Scholar 

  18. Radak Z, Chung HY, Goto S (2008) Systemic adaptation to oxidative challenge induced by regular exercise. Free Radic Bio Med 44:153–159

    Article  CAS  Google Scholar 

  19. Di Meo S, Venditti P (2001) Mitochondria in exercise-induced oxidative stress. Biol Signals Recept 10:125–140

    Article  PubMed  Google Scholar 

  20. Calabrese V, Lodi R, Tonon C, D’Agata V, Sapienza M, Scapagnini G, Mangiameli A, Pennisi G, Stella AM, Butterfield DA (2005) Oxidative stress, mitochondrial dysfunction and cellular stress response in Friedreich’s ataxia. J Neurol Sci 233:145–162

    Article  CAS  PubMed  Google Scholar 

  21. Floyd RA (1999) Antioxidants, oxidative stress, and degenerative neurological disorders. Proc Soc Exp Biol Med 222:236–245

    Article  CAS  PubMed  Google Scholar 

  22. Sen CK (1995) Oxidants and antioxidants in exercise. J Appl Physiol 79:675–686

    CAS  PubMed  Google Scholar 

  23. Ozkaya YG, Agar A, Yargicoglu P, Hacioglu G, Bilmen-Sarikcioglu S, Ozen I, Aliciguzel Y (2002) The effect of exercise on brain antioxidant status of diabetic rats. Diabetes Metab 28:377–384

    CAS  PubMed  Google Scholar 

  24. Halliwell B (1992) Reactive oxygen species and the central nervous system. J Neurochem 59:1609–1623

    Article  CAS  PubMed  Google Scholar 

  25. Navarro A, Gomez C, Lopez-Cepero JM, Boveris A (2004) Beneficial effects of moderate exercise on mice aging: survival, behavior, oxidative stress, and mitochondrial electron transfer. Am J Physiol Regul Integr Comp Physiol 286:R505–R511

    Article  CAS  PubMed  Google Scholar 

  26. Kiraly MA, Kiraly SJ (2005) The effect of exercise on hippocampal integrity: review of recent research. Int J Psychiatry Med 35:75–89

    Article  PubMed  Google Scholar 

  27. Radak Z, Sasvari M, Nyakas CB, Kaneko T, Tahara S, Ohno H, Goto S (2001) Single bout of exercise eliminates the immobilization-induced oxidative stress in rat brain. Neurochem Int 39:33–38

    Article  CAS  PubMed  Google Scholar 

  28. Somani SM, Ravi R, Rybak LP (1995) Effect of exercise training on antioxidant system in brain regions of rat. Pharmacol Biochem Behav 50:635–639

    Article  CAS  PubMed  Google Scholar 

  29. Aguiar AS Jr., Boemer G, Rial D, Cordova FM, Mancini G, Walz R, de Bem AF, Latini A, Leal RB, Pinho RA, Prediger RD (2010) High-intensity physical exercise disrupts implicit memory in mice: involvement of the striatal glutathione antioxidant system and intracellular signaling. Neuroscience 171:1216–1227

    Article  CAS  PubMed  Google Scholar 

  30. Rosa EF, Takahashi S, Aboulafia J, Nouailhetas VL, Oliveira MG (2007) Oxidative stress induced by intense and exhaustive exercise impairs murine cognitive function. J Neurophysiol 98:1820–1826

    Article  PubMed  Google Scholar 

  31. Kenakin T (2004) Principles: receptor theory in pharmacology. Trends Pharmacol Sci 25:186–192

    Article  CAS  PubMed  Google Scholar 

  32. Liu J, Yeo HC, Overvik-Douki E, Hagen T, Doniger SJ, Chyu DW, Brooks GA, Ames BN (2000) Chronically and acutely exercised rats: biomarkers of oxidative stress and endogenous antioxidants. J Appl Physiol 89:21–28

    CAS  PubMed  Google Scholar 

Download references

Acknowledgments

This work was financially supported by the following Brazilian agencies: CNPq, CAPES, FAPESC, and NENASC Projects (PRONEX program CNPq/FAPESC).

Author information

Authors and Affiliations

  1. Programa de Pós-Graduação em Neurociências (PPGNeuro), Centro de Ciências Biológicas–CCB, Universidade Federal de Santa Catarina–UFSC, Florianópolis, SC, 88040-900, Brazil

    Ana Elisa Speck & Aderbal Silva Aguiar Jr.

  2. Laboratory of Exercise Biochemistry and Physiology (LAFIBE), Graduate Program in Health Sciences, Health Sciences Unit, Unidade de Ciências da Saúde, Universidade do Extremo Sul Catarinense–UNESC, Criciúma, Santa Catarina, 88806-000, Brazil

    Camila Baumer Tromm, Bruna Gianatassio Pozzi, Carla Souza Paganini, Talita Tuon, Paulo C. L. Silveira, Aderbal Silva Aguiar Jr. & Ricardo Aurino Pinho

  3. Departamento de Fisioterapia, Universidade Federal de Santa Catarina–UFSC, Araranguá, SC, 88906-072, Brazil

    Ana Elisa Speck, Camila Baumer Tromm, Bruna Gianatassio Pozzi, Carla Souza Paganini, Talita Tuon, Paulo C. L. Silveira, Aderbal Silva Aguiar Jr. & Ricardo Aurino Pinho

Authors
  1. Ana Elisa Speck
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Camila Baumer Tromm
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Bruna Gianatassio Pozzi
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Carla Souza Paganini
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Talita Tuon
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Paulo C. L. Silveira
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Aderbal Silva Aguiar Jr.
    View author publications

    You can also search for this author in PubMed Google Scholar

  8. Ricardo Aurino Pinho
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding authors

Correspondence to Aderbal Silva Aguiar Jr. or Ricardo Aurino Pinho.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Speck, A.E., Tromm, C.B., Pozzi, B.G. et al. The Dose-Dependent Antioxidant Effects of Physical Exercise in the Hippocampus of Mice. Neurochem Res 39, 1496–1501 (2014). https://doi.org/10.1007/s11064-014-1339-6

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11064-014-1339-6

Keywords

Search

Navigation