Skip to main content

Advertisement

SpringerLink
Log in

Oxidative Stress Parameters in Different Brain Structures Following Lateral Fluid Percussion Injury in the Rat

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

Abstract

Free radicals mediated damage of phospholipids, proteins and nucleic acids results in subsequent neuronal degeneration and cell loss. Aim of this study was to evaluate the existence of lipid and protein oxidative damage and the activities of superoxide dismutase (SOD) and glutathione peroxidase (GSH-Px) in various rat brain structures 24 h after lateral fluid percussion brain injury (LFPI). Parietal cortex, hippocampus, thalamus, entorhinal cortex, and cerebellum from the ipsilateral hemisphere were processed for analyses of the thiobarbituric acid reactive substances (TBARS) and oxidized protein levels as well as for the SOD and GSH-Px activities. Immunohistochemical detection of oxidized proteins was also performed. Results of our study showed that LFPI caused significant oxidative stress in the parietal cortex and hippocampus while other brain regions tested in this study were not oxidatively altered by LFPI. GSH-Px activities were significantly increased in the parietal cortex and hippocampus, while the SOD activities remained unchanged following LFPI in all regions investigated.

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. Zaloshnja E, Miller T, Langlois JA et al (2008) Prevalence of long-term disability from traumatic brain injury in the civilian population of the United States, 2005. J Head Trauma Rehabil 23(6):394–400

    Article  PubMed  Google Scholar 

  2. Corrigan JD, Selassie AW, Orman JA (2010) The epidemiology of traumatic brain injury. J Head Trauma Rehabil 25(2):72–80

    Article  PubMed  Google Scholar 

  3. Coles J (2004) Regional ischemia after head injury. Curr Opin Crit Care 10(2):120–125

    Article  PubMed  Google Scholar 

  4. Yi JH, Hazell AS (2006) Excitotoxic mechanisms and the role of astrocytic glutamate transporters in traumatic brain injury. Neurochem Int 48(5):394–403

    Article  PubMed  CAS  Google Scholar 

  5. Israelsson C, Bengtsson H, Kylberg A et al (2008) Distinct cellular patterns of upregulated chemokine expression supporting a prominent inflammatory role in traumatic brain injury. J Neurotrauma 25(8):959–974

    Article  PubMed  Google Scholar 

  6. Donkin JJ, Nimmo AJ, Cernak I et al (2009) Substance P is associated with the development of brain edema and functional deficits after traumatic brain injury. J Cereb Blood Flow Metab 29(8):1388–1398

    Article  PubMed  CAS  Google Scholar 

  7. Zhang D, Dhillon HS, Mattson MP et al (1999) Immunohistochemical detection of the lipid peroxidation product 4-hydroxynonenal after experimental brain injury in the rat. Neurosci Lett 272(1):57–61

    Article  PubMed  CAS  Google Scholar 

  8. Tyurin VA, Tyurina YY, Borisenko GG et al (2000) Oxidative stress following traumatic brain injury in rats: quantitation of biomarkers and detection of free radical intermediates. J Neurochem 75(5):2178–2189

    Article  PubMed  CAS  Google Scholar 

  9. Shao C, Roberts KN, Markesbery WR et al (2006) Oxidative stress in head trauma in aging. Free Radic Biol Med 41(1):77–85

    Article  PubMed  CAS  Google Scholar 

  10. Ansari MA, Roberts KN, Scheff SW (2008) Oxidative stress and modification of synaptic proteins in hippocampus after traumatic brain injury. Free Radic Biol Med 45(4):443–452

    Article  PubMed  CAS  Google Scholar 

  11. Wu A, Ying Z, Gomez-Pinilla F (2004) Dietary omega-3 fatty acids normalize BDNF levels, reduce oxidative damage, and counteract learning disability after traumatic brain injury in rats. J Neurotrauma 21(10):1457–1467

    Article  PubMed  Google Scholar 

  12. Wu A, Ying Z, Gomez-Pinilla F (2006) Dietary curcumin counteracts the outcome of traumatic brain injury on oxidative stress, synaptic plasticity, and cognition. Exp Neurol 197(2):309–317

    Article  PubMed  CAS  Google Scholar 

  13. Opii WO, Nukala VN, Sultana R et al (2007) Proteomic identification of oxidized mitochondrial proteins following experimental traumatic brain injury. J Neurotrauma 24(5):772–789

    Article  PubMed  Google Scholar 

  14. Ansari MA, Roberts KN, Scheff SW (2008) A time course of contusion-induced oxidative stress and synaptic proteins in cortex in a rat model of TBI. J Neurotrauma 25(5):513–526

    Article  PubMed  Google Scholar 

  15. Üstün ME, Duman A, Oğun CO et al (2001) Effects of nimodipine and magnesium sulfate on endogenous antioxidant levels in brain tissue after experimental head trauma. J Neurosurg Anesthesiol 13(3):227–232

    Article  PubMed  Google Scholar 

  16. DeKosky ST, Taffe KM, Abrahamson EE et al (2004) Time course analysis of hippocampal nerve growth factor and antioxidant enzyme activity following lateral controlled cortical impact brain injury in the rat. J Neurotrauma 21(5):491–500

    Article  PubMed  Google Scholar 

  17. Laurer HL, McIntosh TK (1999) Experimental models of brain trauma. Curr Opin Neurol 12(6):715–721

    Article  PubMed  CAS  Google Scholar 

  18. Shohami E, Shapira Y, Rosenthal J et al (1991) Superoxide dismutase activity is not affected by closed head injury in rats. J Basic Clin Physiol Pharmacol 2(1–2):103–109

    Article  PubMed  CAS  Google Scholar 

  19. Goss JR, Taffe KM, Kochanek PM et al (1997) The antioxidant enzymes glutathione peroxidase and catalase increase following traumatic brain injury in the rat. Exp Neurol 146(1):291–294

    Article  PubMed  CAS  Google Scholar 

  20. Sullivan PG, Keller JN, Mattson MP (1998) Traumatic brain injury alters synaptic homeostasis: implications for impaired mitochondrial and transport function. J Neurotrauma 15(10):789–798

    Article  PubMed  CAS  Google Scholar 

  21. Vagnozzi R, Marmarou A, Tavazzi B et al (1999) Changes of cerebral energy metabolism and lipid peroxidation in rats leading to mitochondrial dysfunction after diffuse brain injury. J Neurotrauma 16(10):903–913

    Article  PubMed  CAS  Google Scholar 

  22. Hall ED, Detloff MR, Johnson K et al (2004) Peroxynitrite-mediated protein nitration and lipid peroxidation in a mouse model of traumatic brain injury. J Neurotrauma 21(1):9–20

    Article  PubMed  Google Scholar 

  23. Petronilho F, Feier G, de Souza B et al (2010) Oxidative stress in brain according to traumatic brain injury intensity. J Surg Res 164(2):316–320

    Article  PubMed  CAS  Google Scholar 

  24. McIntosh TK, Vink R, Noble L et al (1989) Traumatic brain injury in the rat: characterization of a lateral fluid-percussion model. Neuroscience 28(1):233–244

    Article  PubMed  CAS  Google Scholar 

  25. Thompson HJ, Lifshitz J, Marklund N et al (2005) Lateral fluid percussion brain injury: a 15-year review and evaluation. J Neurotrauma 22(1):42–75

    Article  PubMed  Google Scholar 

  26. Praticò D, Reiss P, Tang LX et al (2002) Local and systemic increase in lipid peroxidation after moderate experimental traumatic brain injury. J Neurochem 80(5):894–898

    Article  PubMed  Google Scholar 

  27. Lima FD, Souza MA, Furian AF et al (2008) Na+, K+-ATPase activity impairment after experimental traumatic brain injury: relationship to spatial learning deficits and oxidative stress. Behav Brain Res 193(2):306–310

    Article  PubMed  CAS  Google Scholar 

  28. Paolin A, Nardin L, Gaetani P et al (2002) Oxidative damage after severe head injury and its relationship to neurological outcome. Neurosurgery 51:949–954

    PubMed  Google Scholar 

  29. Ohkawa H, Ohishi N, Yagi K (1979) Assay for lipid peroxides in animal tissues by thiobarbituric acid reaction. Anal Biochem 95(2):351–358

    Article  PubMed  CAS  Google Scholar 

  30. Callaway JK, Beart PM, Jarrott B (1998) A reliable procedure for comparison of antioxidants in rat brain homogenates. J Pharmacol Toxicol Methods 39(3):155–162

    Article  PubMed  CAS  Google Scholar 

  31. McCord JM, Fridovich I (1969) Superoxide dismutase. An enzymic function for erythrocuprein (hemocuprein). J Biol Chem 244(22):6049–6055

    PubMed  CAS  Google Scholar 

  32. Paglia DE, Valentine WN (1967) Studies on the quantitative and qualitative characterization of erythrocyte glutathione peroxidase. J Lab Clin Med 70(1):158–169

    PubMed  CAS  Google Scholar 

  33. Bradford MM (1976) A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal Biochem 72:248–254

    Article  PubMed  CAS  Google Scholar 

  34. Hicks RR, Smith DH, Lowenstein DH et al (1993) Mild experimental brain injury in the rat induces cognitive deficits associated with regional neuronal loss in the hippocampus. J Neurotrauma 10(4):405–414

    Article  PubMed  CAS  Google Scholar 

  35. Hicks RR, Soares HD, Smith D et al (1996) Temporal and spatial characterization of neuronal injury following lateral fluid-percussion brain injury in the rat. Acta Neuropathol 91(3):236–246

    Article  PubMed  CAS  Google Scholar 

  36. Conti AC, Raghupathi R, Trojanowski JQ et al (1998) Experimental brain injury induces regionally distinct apoptosis during the acute and delayed post-traumatic period. J Neurosci 18(15):5663–5672

    PubMed  CAS  Google Scholar 

  37. Manoli LP, Gamaro GD, Silveira PP et al (2000) Effect of chronic variate stress on thiobarbituric-acid reactive species and on total radical-trapping potential in distinct regions of rat brain. Neurochem Res 25(7):915–921

    Article  PubMed  CAS  Google Scholar 

  38. Župan G, Pilipović K, Hrelja A et al (2008) Oxidative stress parameters in different rat brain structures after electroconvulsive shock-induced seizures. Prog Neuropsychopharmacol Biol Psychiatry 32(3):771–777

    Article  PubMed  Google Scholar 

  39. Peternel S, Pilipović K, Župan G (2009) Seizure susceptibility and the brain regional sensitivity to oxidative stress in male and female rats in the lithium-pilocarpine model of temporal lobe epilepsy. Prog Neuropsychopharmacol Biol Psychiatry 33(3):456–462

    Article  PubMed  CAS  Google Scholar 

  40. Riegel RE, Valvassori SS, Moretti M et al (2010) Intracerebroventricular ouabain administration induces oxidative stress in the rat brain. Int J Dev Neurosci 28:233–237

    Article  PubMed  CAS  Google Scholar 

  41. Leker RR, Shohami E (2002) Cerebral ischemia and trauma-different etiologies yet similar mechanisms: neuroprotective opportunities. Brain Res Brain Res Rev 39(1):55–73

    Article  PubMed  Google Scholar 

  42. Eraković V, Župan G, Varljen J et al (2000) Lithium plus pilocarpine induced status epilepticus-biochemical changes. Neurosci Res 36(2):157–166

    Article  PubMed  Google Scholar 

  43. Eraković V, Župan G, Varljen J et al (2000) Electroconvulsive shock in rats: changes in superoxide dismutase and glutathione peroxidase activity. Brain Res Mol Brain Res 76(2):266–274

    Article  PubMed  Google Scholar 

  44. Yunoki M, Kawauchi M, Ukita N et al (1997) Effects of lecithinized superoxide dismutase on traumatic brain injury in rats. J Neurotrauma 14(10):739–746

    Article  PubMed  CAS  Google Scholar 

  45. Ding JY, Kreipke CW, Speirs SL et al (2009) Hypoxia-inducible factor-1alpha signaling in aquaporin upregulation after traumatic brain injury. Neurosci Lett 453(1):68–72

    Article  PubMed  CAS  Google Scholar 

  46. Lawler JM, Song W (2002) Specificity of antioxidant enzyme inhibition in skeletal muscle to reactive nitrogen species donors. Biochem Biophys Res Commun 294(5):1093–1100

    Article  PubMed  CAS  Google Scholar 

  47. DeKosky ST, Goss JR, Miller PD et al (1994) Upregulation of nerve growth factor following cortical trauma. Exp Neurol 130:173–177

    Article  PubMed  CAS  Google Scholar 

  48. Goss JR, O’Malley ME, Zou L, Styren SD et al (1998) Astrocytes are the major source of nerve growth factor upregulation following traumatic brain injury in the rat. Exp Neurol 149:301–309

    Article  PubMed  CAS  Google Scholar 

  49. Fan P, Yamauchi T, Noble LJ et al (2003) Age-dependent differences in glutathione peroxidase activity after traumatic brain injury. J Neurotrauma 20(5):437–445

    Article  PubMed  Google Scholar 

  50. Hellmich HL, Garcia JM, Shimamura M et al (2005) Traumatic brain injury and hemorrhagic hypotension suppress neuroprotective gene expression in injured hippocampal neurons. Anesthesiology 102(4):806–814

    Article  PubMed  Google Scholar 

  51. Shimamura M, Garcia JM, Prough DS et al (2005) Analysis of long-term gene expression in neurons of the hippocampal subfields following traumatic brain injury in rats. Neuroscience 131(1):87–97

    Article  PubMed  CAS  Google Scholar 

  52. Xiong Y, Shie FS, Zhang J et al (2004) The protective role of cellular glutathione peroxidase against trauma-induced mitochondrial dysfunction in the mouse brain. J Stroke Cerebrovasc Dis 13(3):129–137

    Article  PubMed  Google Scholar 

  53. Tsuru-Aoyagi K, Potts MB, Trivedi A et al (2009) Glutathione peroxidase activity modulates recovery in the injured immature brain. Ann Neurol 65(5):540–549

    Article  PubMed  CAS  Google Scholar 

  54. Potts MB, Rola R, Claus CP et al (2009) Glutathione peroxidase overexpression does not rescue impaired neurogenesis in the injured immature brain. J Neurosci Res 87(8):1848–1857

    Article  PubMed  CAS  Google Scholar 

  55. Halliwell B, Gutteridge JM (1984) Oxygen toxicity, oxygen radicals, transition metals and disease. Biochem J 219(1):1–14

    PubMed  CAS  Google Scholar 

Download references

Acknowledgments

The authors would like to thank Vedran Frković, MD for his assistance in performing some of these experiments. This research was supported by Grants 062-0620529-0519 and 062-0620529-0518 from The Ministry of Science, Education and Sports of the Republic of Croatia.

Author information

Authors and Affiliations

  1. Department of Pharmacology, School of Medicine, University of Rijeka, Braće Branchetta 20, 51000, Rijeka, Croatia

    Kristina Pilipović, Jasenka Mršić-Pelčić & Gordana Župan

  2. Department of Anesthesiology, Reanimatology and Intensive Care Medicine, School of Medicine, University of Rijeka, Rijeka, Croatia

    Željko Župan

  3. Clinics of Anesthesiology, Reanimatology and Intensive Care Medicine, Clinical Hospital Center Rijeka, Rijeka, Croatia

    Željko Župan & Boban Dangubić

Authors
  1. Kristina Pilipović
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Željko Župan
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Boban Dangubić
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Jasenka Mršić-Pelčić
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Gordana Župan
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Gordana Župan.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Pilipović, K., Župan, Ž., Dangubić, B. et al. Oxidative Stress Parameters in Different Brain Structures Following Lateral Fluid Percussion Injury in the Rat. Neurochem Res 36, 913–921 (2011). https://doi.org/10.1007/s11064-011-0424-3

Download citation

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11064-011-0424-3

Keywords

Search

Navigation