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Mediators of Inflammation
Volume 2015, Article ID 498405, 17 pages
http://dx.doi.org/10.1155/2015/498405
Research Article

Repetitive Hyperbaric Oxygenation Attenuates Reactive Astrogliosis and Suppresses Expression of Inflammatory Mediators in the Rat Model of Brain Injury

1Department of Neurobiology, Institute for Biological Research “Sinisa Stankovic”, University of Belgrade, 11060 Belgrade, Serbia
2Institute of Medical Physiology “Richard Burian”, School of Medicine, University of Belgrade, 11000 Belgrade, Serbia
3Centre for Hyperbaric Medicine, 11040 Belgrade, Serbia
4Institute of Physiology and Biochemistry, Faculty of Biology, University of Belgrade, 11001 Belgrade, Serbia

Received 3 December 2014; Revised 5 February 2015; Accepted 8 March 2015

Academic Editor: Amos Douvdevani

Copyright © 2015 Irena Lavrnja et al. This is an open access article distributed under the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.

Linked References

  1. K. E. Saatman, K. J. Feeko, R. L. Pape, and R. Raghupathi, “Differential behavioral and histopathological responses to graded cortical impact injury in mice,” Journal of Neurotrauma, vol. 23, no. 8, pp. 1241–1253, 2006. View at Publisher · View at Google Scholar · View at Scopus
  2. S. Pekovic, S. Subasic, N. Nedeljkovic et al., “Molecular basis of brain injury and repair,” in Neurobiological Studies—From Genes to Behaviour, S. Ruzdijic and L. Rakic, Eds., pp. 143–165, Research Signpost, Kerala, India, 2006. View at Google Scholar
  3. D. Cederberg and P. Siesjö, “What has inflammation to do with traumatic brain injury?” Child's Nervous System, vol. 26, no. 2, pp. 221–226, 2010. View at Publisher · View at Google Scholar · View at Scopus
  4. P. M. Lenzlinger, M.-C. Morganti-Kossmann, H. L. Laurer, and T. K. McIntosh, “The duality of the inflammatory response to traumatic brain injury,” Molecular Neurobiology, vol. 24, no. 1–3, pp. 169–181, 2001. View at Publisher · View at Google Scholar · View at Scopus
  5. S. C. Hellewell and M. C. Morganti-Kossmann, “Guilty molecules, guilty minds? The conflicting roles of the innate immune response to traumatic brain injury,” Mediators of Inflammation, vol. 2012, Article ID 356494, 18 pages, 2012. View at Publisher · View at Google Scholar · View at Scopus
  6. K. Chen, J. Huang, W. Gong, L. Zhang, P. Yu, and J. M. Wang, “CD40/CD40L dyad in the inflammatory and immune responses in the central nervous system,” Cellular & Molecular Immunology, vol. 3, no. 3, pp. 163–169, 2006. View at Google Scholar · View at Scopus
  7. E. N. Benveniste, V. T. Nguyen, and D. R. Wesemann, “Molecular regulation of CD40 gene expression in macrophages and microglia,” Brain, Behavior, and Immunity, vol. 18, no. 1, pp. 7–12, 2004. View at Publisher · View at Google Scholar · View at Scopus
  8. G. Yilmaz and D. N. Granger, “Leukocyte recruitment and ischemic brain injury,” NeuroMolecular Medicine, vol. 12, no. 2, pp. 193–204, 2010. View at Publisher · View at Google Scholar · View at Scopus
  9. N. Y. Calingasan, H. A. Erdely, and C. Anthony Altar, “Identification of CD40 ligand in Alzheimer's disease and in animal models of Alzheimer's disease and brain injury,” Neurobiology of Aging, vol. 23, no. 1, pp. 31–39, 2002. View at Publisher · View at Google Scholar · View at Scopus
  10. C. D. Garlichs, S. Kozina, S. Fateh-Moghadam et al., “Upregulation of CD40-CD40 ligand (CD154) in patients with acute cerebral ischemia,” Stroke, vol. 34, no. 6, pp. 1412–1418, 2003. View at Publisher · View at Google Scholar · View at Scopus
  11. M. Ishikawa, T. Vowinkel, K. Y. Stokes et al., “CD40/CD40 ligand signaling in mouse cerebral microvasculature after focal ischemia/reperfusion,” Circulation, vol. 111, no. 13, pp. 1690–1696, 2005. View at Publisher · View at Google Scholar · View at Scopus
  12. B. Zhang, T. Wu, M. Chen, Y. Zhou, D. Yi, and R. Guo, “The CD40/CD40L system: a new therapeutic target for disease,” Immunology Letters, vol. 153, no. 1-2, pp. 58–61, 2013. View at Publisher · View at Google Scholar · View at Scopus
  13. J. Silver and J. H. Miller, “Regeneration beyond the glial scar,” Nature Reviews Neuroscience, vol. 5, no. 2, pp. 146–156, 2004. View at Publisher · View at Google Scholar · View at Scopus
  14. M. V. Sofroniew, “Molecular dissection of reactive astrogliosis and glial scar formation,” Trends in Neurosciences, vol. 32, no. 12, pp. 638–647, 2009. View at Publisher · View at Google Scholar · View at Scopus
  15. M. V. Sofroniew and H. V. Vinters, “Astrocytes: biology and pathology,” Acta Neuropathologica, vol. 119, no. 1, pp. 7–35, 2010. View at Publisher · View at Google Scholar · View at Scopus
  16. C. Werner and K. Engelhard, “Pathophysiology of traumatic brain injury,” British Journal of Anaesthesia, vol. 99, no. 1, pp. 4–9, 2007. View at Publisher · View at Google Scholar · View at Scopus
  17. L. Huang and A. Obenaus, “Hyperbaric oxygen therapy for traumatic brain injury,” Medical Gas Research, vol. 1, no. 1, article 21, 2011. View at Publisher · View at Google Scholar
  18. P. Brkic, S. Pekovic, D. Krstic, and T. Jovanovic, “Hyperbaric oxygenation as an adjuvant therapy for traumatic brain injury: a review of literature,” Periodicum Biologorum, vol. 116, no. 1, pp. 29–36, 2014. View at Google Scholar
  19. K. Kraitsy, M. Uecal, S. Grossauer et al., “Repetitive long-term Hyperbaric Oxygen Treatment,(HBOT) administered after experimental traumatic brain injury in rats induces significant remyelination and a recovery of sensorimotor function,” PLoS ONE, vol. 9, no. 5, Article ID e97750, 2014. View at Publisher · View at Google Scholar · View at Scopus
  20. A. L. Gill and C. N. A. Bell, “Hyperbaric oxygen: its uses, mechanisms of action and outcomes,” Quarterly Journal of Medicine, vol. 97, no. 7, pp. 385–395, 2004. View at Publisher · View at Google Scholar · View at Scopus
  21. A. K. Helms, H. T. Whelan, and M. T. Torbey, “Hyperbaric oxygen therapy of cerebral ischemia,” Cerebrovascular Diseases, vol. 20, no. 6, pp. 417–426, 2005. View at Publisher · View at Google Scholar · View at Scopus
  22. N. S. Al-Waili, G. J. Butler, J. Beale et al., “Hyperbaric oxygen in the treatment of patients with cerebral stroke, brain trauma, and neurologic disease,” Advances in Therapy, vol. 22, no. 6, pp. 659–678, 2005. View at Publisher · View at Google Scholar · View at Scopus
  23. H. Bitterman, “Bench-to-bedside review: oxygen as a drug,” Critical Care, vol. 13, no. 1, p. 205, 2009. View at Publisher · View at Google Scholar · View at Scopus
  24. A. B. Parabucki, I. D. Božić, I. M. Bjelobaba et al., “Hyperbaric oxygenation alters temporal expression pattern of superoxide dismutase 2 after cortical stab injury in rats,” Croatian Medical Journal, vol. 53, no. 6, pp. 586–597, 2012. View at Publisher · View at Google Scholar · View at Scopus
  25. P. Brkic, M. Stojiljkovic, T. Jovanovic et al., “Hyperbaric oxygenation improves locomotor ability by enhancing neuroplastic responses after cortical ablation in rats,” Brain Injury, vol. 26, no. 10, pp. 1273–1284, 2012. View at Publisher · View at Google Scholar · View at Scopus
  26. G. Paxinos and C. Watson, The Rat Brain in Stereotaxic Coordinates, New York, NY, USA, Elsevier, 2005.
  27. P. Brkic, A. Mitrovic, M. Rakic, M. Grajic, and T. Jovanovic, “Hyperbaric oxygen therapy of angiopathic changes in patients with inherited gene imbalance,” Serbian Archives of Medicine, vol. 135, no. 11-12, pp. 669–671, 2007. View at Publisher · View at Google Scholar
  28. J. J. Feldmeier, Hyperbaric Oxygen Therapy: 2003 Committee Report, Undersea and Hyperbaric Medical Society, Kensington, Md, USA, 2003.
  29. M. F. Bijlsma, P. J. A. Leenders, B. J. A. Janssen, M. P. Peppelenbosch, H. T. Cate, and C. A. Spek, “Endogenous hedgehog expression contributes to myocardial ischemia-reperfusion-induced injury,” Experimental Biology and Medicine, vol. 233, no. 8, pp. 989–996, 2008. View at Publisher · View at Google Scholar · View at Scopus
  30. N. Pejnovic, M. Colic, B. Draskovic-Pavlovic, and A. Dujic, “A monoclonal antibody R-MC46 induces homotypic adhesion and activation of rat peripheral blood neutrophils,” in Immunoregulation in Health and Disease, M. L. Lukic, M. Colic, M. Mostarica-Stojkovic, and K. Cuperlovic, Eds., pp. 95–101, Academic Press, London, UK, 1997. View at Google Scholar
  31. J. W. Calvert, J. Cahill, and J. H. Zhang, “Hyperbaric oxygen and cerebral physiology,” Neurological Research, vol. 29, no. 2, pp. 132–141, 2007. View at Publisher · View at Google Scholar · View at Scopus
  32. E. Palzur, M. Zaaroor, E. Vlodavsky, F. Milman, and J. F. Soustiel, “Neuroprotective effect of hyperbaric oxygen therapy in brain injury is mediated by preservation of mitochondrial membrane properties,” Brain Research, vol. 1221, pp. 126–133, 2008. View at Publisher · View at Google Scholar · View at Scopus
  33. G.-H. Wang, X.-G. Zhang, Z.-L. Jiang et al., “Neuroprotective effects of hyperbaric oxygen treatment on traumatic brain injury in the rat,” Journal of Neurotrauma, vol. 27, no. 9, pp. 1733–1743, 2010. View at Publisher · View at Google Scholar · View at Scopus
  34. R. W. Smerz, “Incidence of oxygen toxicity during the treatment of dysbarism,” Undersea and Hyperbaric Medicine, vol. 31, no. 2, pp. 199–202, 2004. View at Google Scholar · View at Scopus
  35. T. Zhang, Q.-W. Yang, S.-N. Wang et al., “Hyperbaric oxygen therapy improves neurogenesis and brain blood supply in piriform cortex in rats with vascular dementia,” Brain Injury, vol. 24, no. 11, pp. 1350–1357, 2010. View at Publisher · View at Google Scholar · View at Scopus
  36. J. D. Wood, W. J. Watson, and G. W. Murray, “Correlation between decreases in brain gamma-aminobutyric acid levels and susceptibility to convulsions induced by hyperbaric oxygen,” Journal of Neurochemistry, vol. 16, no. 3, pp. 281–287, 1969. View at Publisher · View at Google Scholar · View at Scopus
  37. S. Benedetti, A. Lamorgese, M. Piersantelli, S. Pagliarani, F. Benvenuti, and F. Canestrari, “Oxidative stress and antioxidant status in patients undergoing prolonged exposure to hyperbaric oxygen,” Clinical Biochemistry, vol. 37, no. 4, pp. 312–317, 2004. View at Publisher · View at Google Scholar · View at Scopus
  38. D. W. Hampton, K. E. Rhodes, C. Zhao, R. J. M. Franklin, and J. W. Fawcett, “The responses of oligodendrocyte precursor cells, astrocytes and microglia to a cortical stab injury, in the brain,” Neuroscience, vol. 127, no. 4, pp. 813–820, 2004. View at Publisher · View at Google Scholar · View at Scopus
  39. M. T. Fitch and J. Silver, “CNS injury, glial scars, and inflammation: inhibitory extracellular matrices and regeneration failure,” Experimental Neurology, vol. 209, no. 2, pp. 294–301, 2008. View at Publisher · View at Google Scholar · View at Scopus
  40. N. J. Allen and B. A. Barres, “Neuroscience: Glia—more than just brain glue,” Nature, vol. 457, no. 7230, pp. 675–677, 2009. View at Publisher · View at Google Scholar · View at Scopus
  41. M. Pekny, U. Wilhelmsson, and M. Pekna, “The dual role of astrocyte activation and reactive gliosis,” Neuroscience Letters, vol. 565, pp. 30–38, 2014. View at Publisher · View at Google Scholar · View at Scopus
  42. M. A. Anderson, Y. Ao, and M. V. Sofroniew, “Heterogeneity of reactive astrocytes,” Neuroscience Letters, vol. 565, pp. 23–29, 2014. View at Publisher · View at Google Scholar · View at Scopus
  43. A. Günther, L. Küppers-Tiedt, P.-M. Schneider et al., “Reduced infarct volume and differential effects on glial cell activation after hyperbaric oxygen treatment in rat permanent focal cerebral ischaemia,” European Journal of Neuroscience, vol. 21, no. 11, pp. 3189–3194, 2005. View at Publisher · View at Google Scholar · View at Scopus
  44. B.-S. Zhao, L.-X. Meng, Y.-Y. Ding, and Y.-Y. Cao, “Hyperbaric oxygen treatment produces an antinociceptive response phase and inhibits astrocyte activation and inflammatory response in a rat model of neuropathic pain,” Journal of Molecular Neuroscience, vol. 53, no. 2, pp. 251–261, 2014. View at Publisher · View at Google Scholar · View at Scopus
  45. J. Hui, Z.-J. Zhang, X. Zhang, Y. Shen, and Y.-J. Gao, “Repetitive hyperbaric oxygen treatment attenuates complete Freund's adjuvant-induced pain and reduces glia-mediated neuroinflammation in the spinal cord,” Journal of Pain, vol. 14, no. 7, pp. 747–758, 2013. View at Publisher · View at Google Scholar · View at Scopus
  46. Y.-S. Lee, C.-C. Chio, C.-P. Chang et al., “Long course hyperbaric oxygen stimulates neurogenesis and attenuates inflammation after ischemic stroke,” Mediators of Inflammation, vol. 2013, Article ID 512978, 13 pages, 2013. View at Publisher · View at Google Scholar · View at Scopus
  47. E. Dardiotis, V. Karanikas, K. Paterakis, K. Fountas, and M. G. Hadjigeorgiou, “Traumatic brain injury and inflammation: emerging role of innate and adaptive immunity,” in Brain Injury—Pathogenesis, Monitoring, Recovery and Management, A. Agrawal, Ed., pp. 23–38, InTech, 2012. View at Google Scholar
  48. C. Lawson and S. Wolf, “ICAM-1 signaling in endothelial cells,” Pharmacological Reports, vol. 61, no. 1, pp. 22–32, 2009. View at Publisher · View at Google Scholar · View at Scopus
  49. T. L. Cunningham, C. M. Cartagena, X.-C. M. Lu et al., “Correlations between blood-brain barrier disruption and neuroinflammation in an experimental model of penetrating ballistic-like brain injury,” Journal of Neurotrauma, vol. 31, no. 5, pp. 505–514, 2014. View at Publisher · View at Google Scholar · View at Scopus
  50. X. Wang, A.-L. Siren, Y. Liu, T.-L. Yue, F. C. Barone, and G. Z. Feuerstein, “Upregulation of intercellular adhesion molecule 1 (ICAM-1) on brain microvascular endothelial cells in rat ischemic cortex,” Molecular Brain Research, vol. 26, no. 1-2, pp. 61–68, 1994. View at Publisher · View at Google Scholar · View at Scopus
  51. C. Gong, J. T. Hoff, and R. F. Keep, “Acute inflammatory reaction following experimental intracerebral hemorrhage in rat,” Brain Research, vol. 871, no. 1, pp. 57–65, 2000. View at Publisher · View at Google Scholar · View at Scopus
  52. C. H. Hang, J.-X. Shi, J.-S. Li, W. Wu, and X. Y. Hong, “Concomitant upregulation of nuclear factor-κB activity, proinflammatory cytokines and ICAM-1 in the injured brain after cortical contusion trauma in a rat model,” Neurology India, vol. 53, no. 3, pp. 312–317, 2005. View at Publisher · View at Google Scholar · View at Scopus
  53. H. J. Bidmon, K. Kato, A. Schleicher, O. W. Witte, and K. Zilles, “Transient increase of manganese-superoxide dismutase in remote brain ares focal photothrombotic cortical lesion,” Stroke, vol. 29, no. 1, pp. 203–211, 1998. View at Publisher · View at Google Scholar · View at Scopus
  54. T. M. Carlos, R. S. B. Clark, D. Franicola-Higgins, J. K. Schiding, and P. M. Kochanek, “Expression of endothelial adhesion molecules and recruitment of neutrophils after traumatic brain injury in rats,” Journal of Leukocyte Biology, vol. 61, no. 3, pp. 279–285, 1997. View at Google Scholar · View at Scopus
  55. M. Hartlage-Rübsamen and R. Schliebs, “Sequential upregulation of cell adhesion molecules in degenerating rat basal forebrain cholinergic neurons and in phagocytotic microglial cells,” Brain Research, vol. 897, no. 1-2, pp. 20–26, 2001. View at Publisher · View at Google Scholar · View at Scopus
  56. H. H. Birdsall, “Induction of ICAM-1 on human neural cells and mechanisms of neutrophil-mediated injury,” The American Journal of Pathology, vol. 139, no. 6, pp. 1341–1350, 1991. View at Google Scholar · View at Scopus
  57. F. Giuliani, C. G. Goodyer, J. P. Antel, and V. Wee Yong, “Vulnerability of human neurons to T cell-mediated cytotoxicity,” Journal of Immunology, vol. 171, no. 1, pp. 368–379, 2003. View at Publisher · View at Google Scholar · View at Scopus
  58. J. A. Buras, G. L. Stahl, K. K. H. Svoboda, and W. R. Reenstra, “Hyperbaric oxygen downregulates ICAM-1 expression induced by hypoxia and hypoglycemia: the role of NOS,” The American Journal of Physiology—Cell Physiology, vol. 278, no. 2, pp. C292–C302, 2000. View at Google Scholar · View at Scopus
  59. D. N. Atochin, D. Fisher, I. T. Demchenko, and S. R. Thom, “Neutrophil sequestration and the effect of hyperbaric oxygen in a rat model of temporary middle cerebral artery occlusion,” Undersea and Hyperbaric Medicine, vol. 27, no. 4, pp. 185–190, 2000. View at Google Scholar · View at Scopus
  60. M. Miljkovic-Lolic, R. Silbergleit, G. Fiskum, and R. E. Rosenthal, “Neuroprotective effects of hyperbaric oxygen treatment in experimental focal cerebral ischemia are associated with reduced brain leukocyte myeloperoxidase activity,” Brain Research, vol. 971, no. 1, pp. 90–94, 2003. View at Publisher · View at Google Scholar · View at Scopus
  61. E. Vlodavsky, E. Palzur, and J. F. Soustiel, “Hyperbaric oxygen therapy reduces neuroinflammation and expression of matrix metalloproteinase-9 in the rat model of traumatic brain injury,” Neuropathology and Applied Neurobiology, vol. 32, no. 1, pp. 40–50, 2006. View at Publisher · View at Google Scholar · View at Scopus
  62. K. M. Omari and K. Dorovini-Zis, “CD40 expressed by human brain endothelial cells regulates CD4+ T cell adhesion to endothelium,” Journal of Neuroimmunology, vol. 134, no. 1-2, pp. 166–178, 2003. View at Publisher · View at Google Scholar · View at Scopus
  63. Z.-J. Ke, N. Y. Calingasan, L. A. DeGiorgio, B. T. Volpe, and G. E. Gibson, “CD40-CD40L interactions promote neuronal death in a model of neurodegeneration due to mild impairment of oxidative metabolism,” Neurochemistry International, vol. 47, no. 3, pp. 204–215, 2005. View at Publisher · View at Google Scholar · View at Scopus
  64. T. Town, J. Tan, and M. Mullan, “CD40 signaling and Alzheimer's disease pathogenesis,” Neurochemistry International, vol. 39, no. 5-6, pp. 371–380, 2001. View at Publisher · View at Google Scholar · View at Scopus
  65. J. Tan, T. Town, T. Mori et al., “CD40 is expressed and functional on neuronal cells,” EMBO Journal, vol. 21, no. 4, pp. 643–652, 2002. View at Publisher · View at Google Scholar · View at Scopus
  66. A. L. Du, T. L. Ji, B. Yang et al., “Neuroprotective effect of AG490 in experimental traumatic brain injury of rats,” Chinese Medical Journal, vol. 126, no. 15, pp. 2934–2937, 2013. View at Google Scholar
  67. A. L. Peters, L. L. Stunz, and G. A. Bishop, “CD40 and autoimmunity: the dark side of a great activator,” Seminars in Immunology, vol. 21, no. 5, pp. 293–300, 2009. View at Publisher · View at Google Scholar · View at Scopus
  68. U. Schönbeck, F. Mach, and P. Libby, “CD154 (CD40 ligand),” International Journal of Biochemistry and Cell Biology, vol. 32, no. 7, pp. 687–693, 2000. View at Publisher · View at Google Scholar · View at Scopus
  69. V. Henn, J. R. Slupsky, M. Gräfe et al., “CD40 ligand on activated platelets triggers an inflammatory reaction of endothelial cells,” Nature, vol. 391, no. 6667, pp. 591–594, 1998. View at Publisher · View at Google Scholar · View at Scopus