Neurochemical Research

, 36:1056 | Cite as

Cigarette Smoke Inhibits Brain Mitochondrial Adaptations of Exercised Mice

  • Ana Elisa Speck
  • Daiane Fraga
  • Priscila Soares
  • Débora L. Scheffer
  • Luciano A. Silva
  • Aderbal S. AguiarJr.
  • Emílio L. Estreck
  • Ricardo A. Pinho
Original Paper
First Online:
Accepted:

Abstract

Physical exercise and smoking are environmental factors that generally cause opposite health-promoting adaptations. Both physical exercise and smoking converge on mitochondrial adaptations in various tissues, including the pro-oxidant nervous system. Here, we analyzed the impact of cigarette smoking on exercise-induced brain mitochondrial adaptations in the hippocampus and pre-frontal cortex of adult mice. The animals were exposed to chronic cigarette smoke followed by 8 weeks of moderate-intensity physical exercise that increased mitochondrial activity in the hippocampus and pre-frontal cortex in the non-smoker mice. However, mice previously exposed to cigarette smoke did not present these exercise-induced mitochondrial adaptations. Our results suggest that smoking can inhibit some brain health-promoting changes induced by physical exercise.

Keywords

Exercise Cigarette smoke Mitochondria Cortex Hippocampus 
This is a preview of subscription content, log in to check access.

References

  1. 1.
    Dröge W (2002) Free radicals in the physiological control of cell function. Physiol Rev 82:47–95PubMedGoogle Scholar
  2. 2.
    Aguiar Jr AS, Pinho RA (2010) The brain redox paradox of physical exercise. In: Kozyrev D, Slutsky V (ed) Handbook of free radicals: formation, types and effects. Nova Science, New York, pp 153–166Google Scholar
  3. 3.
    Aguiar AS Jr, Speck AE, Prediger RDS et al (2008) Downhill training upregulates mice hippocampal and striatal brain-derived neurotrophic factor levels. J Neural Transm 115:1251–1255PubMedCrossRefGoogle Scholar
  4. 4.
    Cotman CW, Engesser-Cesar C (2002) Exercise enhances and protects brain function. Exerc Sport Sci Rev 30:75–79PubMedCrossRefGoogle Scholar
  5. 5.
    Figueiredo CP, Pamplona FA, Mazzuco TL et al (2010) Role of the glucose-dependent insulinotropic polypeptide and its receptor in the central nervous system: therapeutic potential in neurological diseases. Behav Pharmacol 21:394–408PubMedCrossRefGoogle Scholar
  6. 6.
    van Praag H, Christie BR, Sejnowski TJ et al (1999) Running enhances neurogenesis, learning, and long-term potentiation in mice. Proc Natl Acad Sci USA 9:13427–13431CrossRefGoogle Scholar
  7. 7.
    Fowler JS, Volkow ND, Wang GJ et al (1996) Inhibition of monoamine oxidase B in the brains of smokers. Nature 379:733–736PubMedCrossRefGoogle Scholar
  8. 8.
    Menegali BT, Nesi RT, Souza PS et al (2009) The effects of physical exercise on the cigarette smoke-induced pulmonary oxidative response. Pulm Pharmacol Ther 22:567–573PubMedCrossRefGoogle Scholar
  9. 9.
    Wolf PA, D’Agostino RB, Belanger AJ, Kannel WB et al (1991) Probability of stroke: a risk profile from the Framingham study. Stroke 22:312–318PubMedGoogle Scholar
  10. 10.
    Thorgeirsson TE, Geller F, Sulem P (2008) A variant associated with nicotine dependence, lung cancer and peripheral arterial disease. Nature 452:638–642PubMedCrossRefGoogle Scholar
  11. 11.
    Cormier A, Morin C, Zini R et al (2003) Nicotine protects rat brain mitochondria against experimental injuries. Neuropharmacology 44:642–652PubMedCrossRefGoogle Scholar
  12. 12.
    Méndez-Alvarez E, Soto-Otero R, Sánchez-Sellero I et al (1998) In vitro inhibition of catalase activity by cigarette smoke: relevance for oxidative stress. J Appl Toxicol 18:443–448PubMedCrossRefGoogle Scholar
  13. 13.
    Hauptmann N, Shih JC (2001) 2-Naphthylamine, a compound found in cigarette smoke, decreases both monoamine oxidase A and B catalytic activity. Life Sci 68:1231–1241PubMedCrossRefGoogle Scholar
  14. 14.
    Anbarasi K, Vani G, Devi CS (2005) Protective effect of bacoside A on cigarette smoking-induced brain mitochondrial dysfunction in rats. J Environ Pathol Toxicol Oncol 24:225–234PubMedCrossRefGoogle Scholar
  15. 15.
    American Heart Association Nutrition Committee, Lichtenstein AH, Appel LJ et al (2006) Diet and lifestyle recommendations revision 2006: a scientific statement from the American Heart Association Nutrition Committee. Circulation 114:82–96PubMedCrossRefGoogle Scholar
  16. 16.
    West R, McNeill A, Raw M (2000) Smoking cessation guidelines for health professionals: an update. Health education authority. Thorax 55:987–999PubMedCrossRefGoogle Scholar
  17. 17.
    Jha P (2009) Avoidable global cancer deaths and total deaths from smoking. Nat Rev Cancer 9:655–664PubMedCrossRefGoogle Scholar
  18. 18.
    Patrick H, Canevello A (2011) Methodological overview of a self-determination theory-based computerized intervention to promote leisure-time physical activity. Psychol Sport Exerc 12:13–19PubMedCrossRefGoogle Scholar
  19. 19.
    Tuon T, Valvassori SS, Lopes-Borges J et al (2010) Effects of moderate exercise on cigarette smoke exposure-induced hippocampal oxidative stress values and neurological behaviors in mice. Neurosci Lett 475:16–19PubMedCrossRefGoogle Scholar
  20. 20.
    Aguiar AS Jr, Tuon T, Soares FS et al (2088) The effect of n-acetylcysteine and deferoxamine on exercise-induced oxidative damage in striatum and hippocampus of mice. Neurochem Res 33:729–736CrossRefGoogle Scholar
  21. 21.
    Radak Z, Taylor AW, Ohno H et al (2001) Adaptation to exercise-induced oxidative stress: from muscle to brain. Exerc Immunol Rev 7:90–107PubMedGoogle Scholar
  22. 22.
    Rueff-Barroso CR, Trajano ET, Alves JN et al. (2010) Organ-related cigarette smoke-induced oxidative stress is strain-dependent. Med Sci Monit 16:BR218-26Google Scholar
  23. 23.
    Beutler E, West C (1984) Simplified determination of carboxyhemoglobin. Clin Chem 30:871–874PubMedGoogle Scholar
  24. 24.
    Latini A, Rodriguez M, Borba Rosa R et al (2005) 3-Hydroxyglutaric acid moderately impairs energy metabolism in brain of young rats. Neuroscience 135:111–120PubMedCrossRefGoogle Scholar
  25. 25.
    Cassina A, Radi R (1996) Differential inhibitory action of nitric oxide and peroxynitrite on mitochondrial electron transport. Arch Biochem Biophys 328:309–316PubMedCrossRefGoogle Scholar
  26. 26.
    Fischer JC, Ruitenbeek W, Berden JA et al (1985) Differential investigation of the capacity of succinate oxidation in human skeletal muscle. Clin Chim Acta 153:23–36PubMedCrossRefGoogle Scholar
  27. 27.
    Rustin P, Chretien D, Bourgeron T et al (1994) Biochemical and molecular investigations in respiratory chain deficiencies. Clin Chim Acta 228:35–51PubMedCrossRefGoogle Scholar
  28. 28.
    Lowry OH, Rosebrough NJ, Farr AL et al (1951) Protein measurement with the Folin phenol reagent. J Biol Chem 193:265–275PubMedGoogle Scholar
  29. 29.
    Aguiar AS Jr, Tuon T, Pinho CA et al (2007) Mitochondrial IV complex and brain neurothrophic derived factor responses of mice brain cortex after downhill training. Neurosci Lett 22:171–174CrossRefGoogle Scholar
  30. 30.
    Aguiar AS Jr, Boemer G, Rial D et al (2010) High-intensity physical exercise disrupts implicit memory in mice: involvement of the striatal glutathione antioxidant system and intracellular signaling. Neuroscience 29:1216–1227CrossRefGoogle Scholar
  31. 31.
    Vaynman S, Ying Z, Wu A et al (2006) Coupling energy metabolism with a mechanism to support brain-derived neurotrophic factor-mediated synaptic plasticity. Neuroscience 139:1221–1234PubMedCrossRefGoogle Scholar
  32. 32.
    Stranahan AM, Lee K, Becker KG et al (2010) Hippocampal gene expression patterns underlying the enhancement of memory by running in aged mice. Neurobiol Aging 31:1937–1949PubMedCrossRefGoogle Scholar
  33. 33.
    Linert W, Bridge MH, Huber M et al (1999) In vitro and in vivo studies investigating possible antioxidant actions of nicotine: relevance to Parkinson’s and Alzheimer’s diseases. Biochim Biophys Acta 1454:143–152PubMedGoogle Scholar
  34. 34.
    Cotman CW, Berchtold NC (2002) Exercise: a behavioral intervention to enhance brain health and plasticity. Trends Neurosci 25:295–301PubMedCrossRefGoogle Scholar
  35. 35.
    Navarro A, Gomez C, López-Cepero JM et al (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–R511PubMedCrossRefGoogle Scholar
  36. 36.
    Mattson MP, Chan SL, Duan W (2002) Modification of brain aging and neurodegenerative disorders by genes, diet, and behavior. Physiol Rev 82:637–672PubMedGoogle Scholar
  37. 37.
    Aguiar AS Jr, Tuon T, Pinho CA et al (2008) Intense exercise induces mitochondrial dysfunction in mice brain. Neurochem Res 33:51–58PubMedCrossRefGoogle Scholar
  38. 38.
    Powers SK, Duarte J, Kavazis AN et al (2010) Reactive oxygen species are signaling molecules for skeletal muscle adaptation. Exp Physiol 95:1–9PubMedCrossRefGoogle Scholar
  39. 39.
    Valko M, Leibfritz D, Moncol J et al (2007) Free radicals and antioxidants in normal physiological functions and human disease. Int J Biochem Cell Biol 39:44–84PubMedCrossRefGoogle Scholar
  40. 40.
    Liu HT, Akita T, Shimizu T et al (2009) Bradykinin-induced astrocyte-neuron signaling: glutamate release is mediated by ROS-activated volume-sensitive outwardly rectifying anion channels. J Physiol 587:2197–2209PubMedCrossRefGoogle Scholar
  41. 41.
    Calabrese V, Signorile A, Cornelius C et al (2008) Practical approaches to investigate redox regulation of heat shock protein expression and intracellular glutathione redox state. Methods Enzymol 441:83–110PubMedCrossRefGoogle Scholar
  42. 42.
    Barreiro E, Peinado VI, Galdiz JB et al (2010) Cigarette smoke-induced oxidative stress: a role in chronic obstructive pulmonary disease skeletal muscle dysfunction. Am J Respir Crit Care Med 182:477–488PubMedCrossRefGoogle Scholar
  43. 43.
    Florek E, Ignatowicz E, Piekoszewski W (2009) Effect of pregnancy and tobacco smoke on the antioxidant activity of rutin in an animal model. Pharmacol Rep 61:935–940PubMedGoogle Scholar
  44. 44.
    Luchese C, Pinton S, Nogueira CW (2009) Brain and lungs of rats are differently affected by cigarette smoke exposure: antioxidant effect of an organoselenium compound. Pharmacol Res 59:194–201PubMedCrossRefGoogle Scholar
  45. 45.
    Reilly M, Delanty N, Lawson JA et al (1996) Modulation of oxidant stress in vivo in chronic cigarette smokers. Circulation 94:19–25PubMedGoogle Scholar
  46. 46.
    Ristow M, Zarse K, Oberbach A et al (2009) Antioxidants prevent health-promoting effects of physical exercise in humans. Proc Natl Acad Sci USA 106:8665–8670PubMedCrossRefGoogle Scholar
  47. 47.
    Conway TL, Cronan TA (1992) Smoking, exercise, and physical fitness. Prev Med 21:723–734PubMedCrossRefGoogle Scholar
  48. 48.
    Altarac M, Gardner JW, Popovich RM et al (2000) Cigarette smoking and exercise-related injuries among young men and women. Am J Prev Med 18:96–102PubMedCrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media, LLC 2011

Authors and Affiliations

  • Ana Elisa Speck
    • 1
  • Daiane Fraga
    • 2
  • Priscila Soares
    • 3
  • Débora L. Scheffer
    • 3
  • Luciano A. Silva
    • 2
  • Aderbal S. AguiarJr.
    • 1
    • 3
  • Emílio L. Estreck
    • 2
  • Ricardo A. Pinho
    • 3
  1. 1.Laboratório Experimental de Doenças Neurodegenerativas, Departamento de FarmacologiaUniversidade Federal de Santa CatarinaFlorianópolisBrazil
  2. 2.Experimental Laboratory of Physiopathology, Postgraduate Program in Health Sciences, Health Sciences UnitUniversidade do Extremo Sul CatarinenseCriciúmaBrazil
  3. 3.Laboratory of Exercise Biochemistry and Physiology, Postgraduate Program in Health Sciences, Health Sciences UnitUniversidade do Extremo Sul CatarinenseCriciúmaBrazil

Personalised recommendations