Skip to main content

Advertisement

SpringerLink
Log in

Effect of Long-Term Normobaric Hyperoxia on Oxidative Stress in Mitochondria of the Guinea Pig Brain

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

Abstract

Normobaric hyperoxia (NBO) is applied for treatment of various clinical conditions related to hypoxia, but it can potentially also induce generation of reactive oxygen species, causing cellular damage. In this study, we examined the effects of 60 h NBO treatment on lipid and protein oxidative damage and activity of superoxide dismutase (Mn-SOD) in brain mitochondria of guinea pigs. Despite significant stimulation of Mn-SOD expression and activity the NBO treatment resulted in accumulation of markers of oxidative lesions, including lipid peroxidation (conjugated dienes, thiobarbituric acid reactive substances) and protein modification (bityrosines, adducts with lipid peroxidation products, oxidized thiols). When inhaled O2 was enriched with oxygen cation, O •+2 , the Mn-SOD expression and activity were stimulated to similar extend, but lipid peroxidation and protein oxidation were prevented. These results suggest that long-term NBO treatment causes oxidative stress, but enrichment of inhaled oxygen by oxygen cation can protect the brain again adverse effects of hyperoxia.

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
Fig. 3
Fig. 4

Similar content being viewed by others

References

  1. Singhal AB (2007) A review of oxygen therapy in ischemic stroke. Neurol Res 29:173–183

    Article  PubMed  Google Scholar 

  2. Kumaria A, Tolias CM (2009) Normobaric hyperoxia therapy for traumatic brain injury and stroke: a review. Br J Neurosurg 26:576–584

    Article  Google Scholar 

  3. Chen Y, Nadi NS, Chavko M et al (2009) Microarray analysis of gene expression in rat cortical neurons exposed to hyperbaric air and oxygen. Neurochem Res 34:1047–1056

    Article  PubMed  CAS  Google Scholar 

  4. Matchett GA, Martin RD, Zhang JH (2009) Hyperbaric oxygen therapy and cerebral ischemia: neuroprotective mechanisms. Neurol Res 31:114–121

    Article  PubMed  CAS  Google Scholar 

  5. Brutus NA, Hanley S, Ashraf QM et al (2009) Effect of hyperoxia on serine phosphorylation of apoptotic proteins in mitochondrial membranes of the cerebral cortex of newborn piglets. Neurochem Res 34:1219–1225

    Article  PubMed  CAS  Google Scholar 

  6. Mudduluru M, Zubrow AB, Ashraf QM et al (2010) Tyrosine phosphorylation of apoptotic proteins during hyperoxia in mitochondria of the cerebral cortex of newborn piglets Neurochem Res 35:1003–1009

    CAS  Google Scholar 

  7. Thom SR (2009) Oxidative stress is fundamental to hyperbaric oxygen therapy. J Appl Physiol 106:988–995

    Article  PubMed  CAS  Google Scholar 

  8. Henseley K, Howard BJ, Carney JM et al (1995) Membrane protein alterations in rodent erythrocytes and synaptosomes due to aging and hyperoxia. Biochim Biophys Acta 1270:203–206

    Google Scholar 

  9. Dundar K, Topal T, Ay H et al (2005) Protective effects of exogenously administrated or endogenously produced melatonin on hyperbaric oxygen-induced oxidative stress in the rat brain. Clin Exp Pharmacol Physiol 32:926–930

    Article  PubMed  CAS  Google Scholar 

  10. Bader N, Bosy-Westphal A, Koch A et al (2007) Effect of hyperbaric oxygen and vitamin C and E supplementation on biomarkers of oxidative stress in healthy men. Br J Nutr 98:826–833

    Article  PubMed  CAS  Google Scholar 

  11. Brozmanova M, Plevkova J, Bartos V et al (2008) The interaction of dietary antioxidant vitamins and oxidative stress on cough reflex in guinea-pigs after long term oxygen therapy J Physiol Pharmacol 57:45–54

    Google Scholar 

  12. Calderón Guzmán D, Trujillo Jiménez F, Hernández García E et al (2007) Assessment of antioxidant effect of 2, 5-dihydroxybenzoic acid and vitamin A in brains of rats with induced hyperoxia. Neurochem Res 32:1036–1040

    Article  PubMed  Google Scholar 

  13. Mollaoglu H, Topal T, Ozler M et al (2007) Antioxidant effects of melatonin in rats during chronic exposure to hyperbaric oxygen. J Pineal Res 42:50–54

    Article  PubMed  CAS  Google Scholar 

  14. Calkovska A, Engler I, Mokra D et al (2008) Differences in oxidative status, lung function, and pulmonary surfactant during long-term inhalation of medical oxygen and partially ionized oxygen in guinea pigs. J Physiol Pharmacol 59:173–181

    PubMed  Google Scholar 

  15. Kaplan P, Tatarkova Z, Engler I et al (2009) Effects of long-term oxygenation treatments on α-ketoglutarate dehydrogenase activity and oxidative modifications in mitochondria of guinea pig heart. Eur J Med Res 14:116–120

    PubMed  Google Scholar 

  16. Engler I, Atzmüeller C, Donic V et al (2009) Reactive oxygen species, especially O +•2 in cancer mechanisms. J Exp Therapeut Oncol 8(2):157–165

    CAS  Google Scholar 

  17. Babusikova E, Hatok J, Dobrota D et al (2007) Age-related oxidative modifications of proteins and lipids in rat brain. Neurochem Res 32:1351–1356

    Article  PubMed  CAS  Google Scholar 

  18. Dodd PR, Hardy JA, Oakley AE (1981) A rapid method for preparing synaptosomes: comparison with alternative procedures. Brain Res 226:107–118

    Article  PubMed  CAS  Google Scholar 

  19. Kaplan P, Babusikova E, Lehotsky J et al (2003) Free radical-induced protein modification and inhibition of Ca2+-ATPase of cardiac sarcoplasmic reticulum. Mol Cell Biochem 248:41–47

    Article  PubMed  CAS  Google Scholar 

  20. Gonzales R, Auclair C, Voisin E et al (1984) Superoxide dismutase, catalase, and glutathione peroxidase in red blood cells from patients with malignant diseases. Cancer Res 44:4137–4139

    PubMed  CAS  Google Scholar 

  21. Powell CS, Jackson RM (2003) Mitochondrial complex I, aconitase, and succinate dehydrogenase during hypoxia-reoxygenation: Modulation of enzyme activities by MnSOD. Am J Physiol Lung Cell Mol Physiol 285:L189–L198

    PubMed  CAS  Google Scholar 

  22. Hink J, Jansen E (2001) Are superoxide and/or hydrogen peroxide responsible for some of the beneficial effects of hyperbaric oxygen therapy? Med Hypotheses 57:764–769

    Article  PubMed  CAS  Google Scholar 

  23. Ay H, Topal T, Özler M et al (2007) Persistence of hyperbaric oxygen-induced oxidative effects after exposure in rat brain cortex tissue. Life Sci 80:2025–2029

    Article  PubMed  CAS  Google Scholar 

  24. Nemoto EM, Betterman K (2007) Basic physiology of hyperbaric oxygen in brain. Neurol Res 29:116–126

    Article  PubMed  CAS  Google Scholar 

  25. Xue L, Yu Q, Zhang H et al (2008) Effect of large dose hyperbaric oxagenation therapy on prognosis and oxidative stress of acute pemanet cerebral ischemic stroke in rats. Neurol Res 30:389–393

    Article  PubMed  Google Scholar 

  26. Singhal AB, Wang X, Sumii T et al (2002) Effect of normobaric hyperoxia in a rat moedl of focal cerebral ischemia-reperfusion. J Cereb Blood Flow Metab 22:861–868

    Article  PubMed  Google Scholar 

  27. Puccio AM, Hoffman LA, Bayir H et al (2009) Effect of short periods of normobaric hyperoxia on local brain tissue oxygenation and cerebrospinal fluid oxidative stress markers in severe traumatic brain injury. J Neurotrauma 26:1241–1249

    Article  PubMed  Google Scholar 

  28. Liu W, Sood R, Chen Q et al (2008) Normobaric hyperoxia inhibits NADPH oxidase-mediated matrix metalloproteinase-9 induction in cerebral microvessels in experimental stroke. J Neurochem 107:1196–1205

    Article  PubMed  CAS  Google Scholar 

  29. Ahotupa M, Mantyla E, Peltola V et al (1992) Pro-oxidant effects of normobaric hyperoxia in rat tissues. Acta Physiol Scand 145:151–157

    Article  PubMed  CAS  Google Scholar 

  30. Bigdeli MR, Rahnema M (2009) The effect of normobaric hyperoxia on superoxide dismutase activity and neurological deficits in an animal model of Huntington disease. Physiol Pharmacol 13:18–27

    Google Scholar 

  31. Boveris A, Chance B (1973) The mitochondrial generation of hydrogen peroxide. General properties and effect of hyperbaric oxygen. Biochem J 134:707–716

    PubMed  CAS  Google Scholar 

  32. McLennan HR, Esposti MD (2000) The contribution of mitochondrial respiratory complexes to the production of reactive oxygen species. J. Bioenerg Biomembr 32:153–162

    Article  CAS  Google Scholar 

  33. Lenaz G (2002) The mitochondrial production of reactive oxygen species: Mechanisms and implications in human pathology. IUBMB Life 52:159–164

    Article  Google Scholar 

  34. Tang X, Liu KJ, Ramu J et al (2010) Inhibition of gp91phox contributes towards normobaric hyperoxia afforded neuroprotection in focal cerebral ischemia. Brain Res 1348:174–180

    Article  PubMed  CAS  Google Scholar 

Download references

Acknowledgments

This work was partially supported by grants VEGA 1/0028/11 and VVCE APVV 0064/07 from the Ministry of Education and Science of the Slovak Republic and project “Identification of Novel Markers in Diagnostic Panel of Neurological Diseases”, code:26220220114 co-financed from EC sources and European Regional Development Fund.

Author information

Authors and Affiliations

  1. Department of Medical Biochemistry, Jessenius Faculty of Medicine, Comenius University, Mala Hora 4, 036 01, Martin, Slovak Republic

    Zuzana Tatarkova, Anna Drgova, Peter Hodas, Jan Lehotsky, Dusan Dobrota & Peter Kaplan

  2. Department of Physiology, Medical Faculty, PJ Safarik University, Kosice, Slovak Republic

    Ivan Engler

  3. Department of Physiology, Jessenius Faculty of Medicine, Comenius University, Martin, Slovak Republic

    Andrea Calkovska & Daniela Mokra

Authors
  1. Zuzana Tatarkova
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Ivan Engler
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Andrea Calkovska
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Daniela Mokra
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Anna Drgova
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Peter Hodas
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Jan Lehotsky
    View author publications

    You can also search for this author in PubMed Google Scholar

  8. Dusan Dobrota
    View author publications

    You can also search for this author in PubMed Google Scholar

  9. Peter Kaplan
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Peter Kaplan.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Tatarkova, Z., Engler, I., Calkovska, A. et al. Effect of Long-Term Normobaric Hyperoxia on Oxidative Stress in Mitochondria of the Guinea Pig Brain. Neurochem Res 36, 1475–1481 (2011). https://doi.org/10.1007/s11064-011-0473-7

Download citation

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11064-011-0473-7

Keywords

Search

Navigation