Table of Contents Author Guidelines Submit a Manuscript
Oxidative Medicine and Cellular Longevity
Volume 2015, Article ID 370312, 10 pages
http://dx.doi.org/10.1155/2015/370312
Review Article

Traumatic Brain Injury and NADPH Oxidase: A Deep Relationship

1Department for Life Quality Studies, Alma Mater Studiorum-University of Bologna, C.so Augusto 237, 47921 Rimini, Italy
2Department of Pharmacy and Biotechnology, Alma Mater Studiorum-University of Bologna, Via Irnerio 48, 40126 Bologna, Italy
3Neurorehabilitation Unit, Emergency Department, AUSL of Bologna, Via B. Nigrisoli 2, 40133 Bologna, Italy

Received 15 January 2015; Accepted 18 March 2015

Academic Editor: Javier Egea

Copyright © 2015 Cristina Angeloni 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. J. León-Carrión, M. D. R. Domínguez-Morales, J. M. Barroso y Martín, and F. Murillo-Cabezas, “Epidemiology of traumatic brain injury and subarachnoid hemorrhage,” Pituitary, vol. 8, no. 3-4, pp. 197–202, 2005. View at Publisher · View at Google Scholar · View at Scopus
  2. C. J. L. Murray and A. D. Lopez, “Alternative projections of mortality and disability by cause 1990-2020: global burden of disease study,” The Lancet, vol. 349, no. 9064, pp. 1498–1504, 1997. View at Publisher · View at Google Scholar · View at Scopus
  3. A. A. Hyder, C. A. Wunderlich, P. Puvanachandra, G. Gururaj, and O. C. Kobusingye, “The impact of traumatic brain injuries: a global perspective,” NeuroRehabilitation, vol. 22, no. 5, pp. 341–353, 2007. View at Google Scholar · View at Scopus
  4. F. Tagliaferri, C. Compagnone, M. Korsic, F. Servadei, and J. Kraus, “A systematic review of brain injury epidemiology in Europe,” Acta Neurochirurgica, vol. 148, no. 3, pp. 255–268, 2006. View at Publisher · View at Google Scholar · View at Scopus
  5. J. H. Adams, D. I. Graham, and T. A. Gennarelli, “Head injury in man and experimental animals: neuropathology,” Acta Neurochirurgica, Supplement, vol. 32, pp. 15–30, 1983. View at Publisher · View at Google Scholar · View at Scopus
  6. K. E. Saatman, A.-C. Duhaime, R. Bullock et al., “Classification of traumatic brain injury for targeted therapies,” Journal of Neurotrauma, vol. 25, no. 7, pp. 719–738, 2008. View at Publisher · View at Google Scholar · View at Scopus
  7. A. I. Maas, N. Stocchetti, and R. Bullock, “Moderate and severe traumatic brain injury in adults,” The Lancet Neurology, vol. 7, no. 8, pp. 728–741, 2008. View at Publisher · View at Google Scholar · View at Scopus
  8. J. J. Donkin and R. Vink, “Mechanisms of cerebral edema in traumatic brain injury: therapeutic developments,” Current Opinion in Neurology, vol. 23, no. 3, pp. 293–299, 2010. View at Publisher · View at Google Scholar · View at Scopus
  9. E. Motori, J. Puyal, N. Toni et al., “Inflammation-induced alteration of astrocyte mitochondrial dynamics requires autophagy for mitochondrial network maintenance,” Cell Metabolism, vol. 18, no. 6, pp. 844–859, 2013. View at Publisher · View at Google Scholar · View at Scopus
  10. S. Signoretti, A. Marmarou, B. Tavazzi et al., “The protective effect of Cyclosporin A upon N-acetylaspartate and mitochondrial dysfunction following experimental diffuse traumatic brain injury,” Journal of Neurotrauma, vol. 21, no. 9, pp. 1154–1167, 2004. View at Publisher · View at Google Scholar · View at Scopus
  11. A. Lewén, P. Matz, and P. H. Chan, “Free radical pathways in CNS injury,” Journal of Neurotrauma, vol. 17, no. 10, pp. 871–890, 2000. View at Publisher · View at Google Scholar · View at Scopus
  12. R. A. Floyd and J. M. Carney, “Free radical damage to protein and DNA: mechanisms involved and relevant observations on brain undergoing oxidative stress,” Annals of Neurology, vol. 32, pp. S22–S27, 1992. View at Publisher · View at Google Scholar · View at Scopus
  13. A. J. Lambert and M. D. Brand, “Reactive oxygen species production by mitochondria,” Methods in Molecular Biology, vol. 554, pp. 165–181, 2009. View at Publisher · View at Google Scholar · View at Scopus
  14. M. A. Ansari, K. N. Roberts, and S. W. Scheff, “A time course of NADPH-oxidase up-regulation and endothelial nitric oxide synthase activation in the hippocampus following neurotrauma,” Free Radical Biology and Medicine, vol. 77, pp. 21–29, 2014. View at Publisher · View at Google Scholar
  15. X.-Y. Lu, H.-D. Wang, J.-G. Xu, K. Ding, and T. Li, “NADPH oxidase inhibition improves neurological outcome in experimental traumatic brain injury,” Neurochemistry International, vol. 69, no. 1, pp. 14–19, 2014. View at Publisher · View at Google Scholar · View at Scopus
  16. I. N. Singh, P. G. Sullivan, Y. Deng, L. H. Mbye, and E. D. Hall, “Time course of post-traumatic mitochondrial oxidative damage and dysfunction in a mouse model of focal traumatic brain injury: implications for neuroprotective therapy,” Journal of Cerebral Blood Flow and Metabolism, vol. 26, no. 11, pp. 1407–1418, 2006. View at Publisher · View at Google Scholar · View at Scopus
  17. S.-X. Song, J.-L. Gao, K.-J. Wang et al., “Attenuation of brain edema and spatial learning deficits by the inhibition of NADPH oxidase activity using apocynin following diffuse traumatic brain injury in rats,” Molecular Medicine Reports, vol. 7, no. 1, pp. 327–331, 2013. View at Publisher · View at Google Scholar · View at Scopus
  18. Q. G. Zhang, M. D. Laird, D. Han et al., “Critical role of NADPH oxidase in neuronal oxidative damage and microglia activation following traumatic brain injury,” PLoS ONE, vol. 7, no. 4, Article ID e34504, 2012. View at Publisher · View at Google Scholar · View at Scopus
  19. B. Y. Choi, B. G. Jang, J. H. Kim et al., “Prevention of traumatic brain injury-induced neuronal death by inhibition of NADPH oxidase activation,” Brain Research, vol. 1481, pp. 49–58, 2012. View at Publisher · View at Google Scholar · View at Scopus
  20. C. L. Harrison and M. Dijkers, “Traumatic brain injury registries in the United States: an overview,” Brain Injury, vol. 6, no. 3, pp. 203–212, 1992. View at Publisher · View at Google Scholar · View at Scopus
  21. G. Teasdale and B. Jennett, “Assessment of coma and impaired consciousness. A practical scale,” The Lancet, vol. 2, no. 7872, pp. 81–84, 1974. View at Google Scholar · View at Scopus
  22. B. Jennett, “Epidemiology of head injury,” Journal of Neurology Neurosurgery and Psychiatry, vol. 60, no. 4, pp. 362–369, 1996. View at Publisher · View at Google Scholar · View at Scopus
  23. J. T. Povlishock and D. I. Katz, “Update of neuropathology and neurological recovery after traumatic brain injury,” Journal of Head Trauma Rehabilitation, vol. 20, no. 1, pp. 76–94, 2005. View at Publisher · View at Google Scholar · View at Scopus
  24. T. A. Gennarelli, L. E. Thibault, J. H. Adams, D. I. Graham, C. J. Thompson, and R. P. Marcincin, “Diffuse axonal injury and traumatic coma in the primate,” Annals of Neurology, vol. 12, no. 6, pp. 564–574, 1982. View at Publisher · View at Google Scholar · View at Scopus
  25. J. M. Meythaler, J. D. Peduzzi, E. Eleftheriou, and T. A. Novack, “Current concepts: diffuse axonal injury-associated traumatic brain injury,” Archives of Physical Medicine and Rehabilitation, vol. 82, no. 10, pp. 1461–1471, 2001. View at Publisher · View at Google Scholar · View at Scopus
  26. T. Skandsen, K. A. Kvistad, O. Solheim, I. H. Strand, M. Folvik, and V. Anne, “Prevalence and impact of diffuse axonal injury in patients with moderate and severe head injury: a cohort study of early magnetic resonance imaging findings and 1-year outcome: Clinical article,” Journal of Neurosurgery, vol. 113, no. 3, pp. 556–563, 2010. View at Publisher · View at Google Scholar · View at Scopus
  27. J. H. Adams, D. Doyle, I. Ford, T. A. Gennarelli, D. I. Graham, and D. R. McLellan, “Diffuse axonal injury in head injury: definition, diagnosis and grading,” Histopathology, vol. 15, no. 1, pp. 49–59, 1989. View at Publisher · View at Google Scholar · View at Scopus
  28. A. Büki and J. T. Povlishock, “All roads lead to disconnection?—Traumatic axonal injury revisited,” Acta Neurochirurgica, vol. 148, no. 2, pp. 181–193, 2006. View at Publisher · View at Google Scholar · View at Scopus
  29. J. Y. Wang, K. Bakhadirov, H. Abdi et al., “Longitudinal changes of structural connectivity in traumatic axonal injury,” Neurology, vol. 77, no. 9, pp. 818–826, 2011. View at Publisher · View at Google Scholar · View at Scopus
  30. C. B. Hutson, C. R. Lazo, F. Mortazavi, C. C. Giza, D. Hovda, and M. F. Chesselet, “Traumatic brain injury in adult rats causes progressive nigrostriatal dopaminergic cell loss and enhanced vulnerability to the pesticide paraquat,” Journal of Neurotrauma, vol. 28, no. 9, pp. 1783–1801, 2011. View at Publisher · View at Google Scholar · View at Scopus
  31. T. C. Lye and E. A. Shores, “Traumatic brain injury as a risk factor for Alzheimer's disease: a review,” Neuropsychology Review, vol. 10, no. 2, pp. 115–129, 2000. View at Publisher · View at Google Scholar · View at Scopus
  32. A. C. McKee, R. C. Cantu, C. J. Nowinski et al., “Chronic traumatic encephalopathy in athletes: progressive tauopathy after repetitive head injury,” Journal of Neuropathology & Experimental Neurology, vol. 68, no. 7, pp. 709–735, 2009. View at Publisher · View at Google Scholar · View at Scopus
  33. K. Beauchamp, H. Mutlak, W. R. Smith, E. Shohami, and P. F. Stahel, “Pharmacology of traumatic brain injury: where is the ‘golden bullet’?” Molecular Medicine, vol. 14, no. 11-12, pp. 731–740, 2008. View at Publisher · View at Google Scholar · View at Scopus
  34. H. Bayir, V. E. Kagan, R. S. B. Clark et al., “Neuronal NOS-mediated nitration and inactivation of manganese superoxide dismutase in brain after experimental and human brain injury,” Journal of Neurochemistry, vol. 101, no. 1, pp. 168–181, 2007. View at Publisher · View at Google Scholar · View at Scopus
  35. E. D. Hall, M. R. Detloff, K. Johnson, and N. C. Kupina, “Peroxynitrite-mediated protein nitration and lipid peroxidation in a mouse model of traumatic brain injury,” Journal of Neurotrauma, vol. 21, no. 1, pp. 9–20, 2004. View at Publisher · View at Google Scholar · View at Scopus
  36. G. Lotocki, J. P. de Rivero Vaccari, E. R. Perez et al., “Alterations in blood-brain barrier permeability to large and small molecules and leukocyte accumulation after traumatic brain injury: effects of post-traumatic hypothermia,” Journal of Neurotrauma, vol. 26, no. 7, pp. 1123–1134, 2009. View at Publisher · View at Google Scholar · View at Scopus
  37. P. B. L. Pun, J. Lu, and S. Moochhala, “Involvement of ROS in BBB dysfunction,” Free Radical Research, vol. 43, no. 4, pp. 348–364, 2009. View at Publisher · View at Google Scholar · View at Scopus
  38. H. Z. Toklu, T. Hakan, N. Biber, S. Solakoğlu, A. V. Öğünç, and G. Şener, “The protective effect of alpha lipoic acid against traumatic brain injury in rats,” Free Radical Research, vol. 43, no. 7, pp. 658–667, 2009. View at Publisher · View at Google Scholar · View at Scopus
  39. B. K. Siesjo, “Calcium-mediated processes in neuronal degeneration,” Annals of the New York Academy of Sciences, vol. 747, pp. 140–161, 1994. View at Google Scholar · View at Scopus
  40. A. Biegon, P. A. Fry, C. M. Paden, A. Alexandrovich, J. Tsenter, and E. Shohami, “Dynamic changes in N-methyl-D-aspartate receptors after closed head injury in mice: implications for treatment of neurological and cognitive deficits,” Proceedings of the National Academy of Sciences of the United States of America, vol. 101, no. 14, pp. 5117–5122, 2004. View at Publisher · View at Google Scholar · View at Scopus
  41. A. W. Unterberg, J. Stover, B. Kress, and K. L. Kiening, “Edema and brain trauma,” Neuroscience, vol. 129, no. 4, pp. 1021–1029, 2004. View at Publisher · View at Google Scholar · View at Scopus
  42. B. Liu and J. S. Hong, “Role of microglia in inflammation-mediated neurodegenerative diseases: mechanisms and strategies for therapeutic intervention,” Journal of Pharmacology and Experimental Therapeutics, vol. 304, no. 1, pp. 1–7, 2003. View at Publisher · View at Google Scholar · View at Scopus
  43. E. Shohami, R. Bass, D. Wallach, A. Yamin, and R. Gallily, “Inhibition of tumor necrosis factor alpha (TNFalpha) activity in rat brain is associated with cerebroprotection after closed head injury,” Journal of Cerebral Blood Flow and Metabolism, vol. 16, no. 3, pp. 378–384, 1996. View at Google Scholar · View at Scopus
  44. M. A. Ansari, K. N. Roberts, and S. W. Scheff, “Oxidative stress and modification of synaptic proteins in hippocampus after traumatic brain injury,” Free Radical Biology and Medicine, vol. 45, no. 4, pp. 443–452, 2008. View at Publisher · View at Google Scholar · View at Scopus
  45. C. Shao, K. N. Roberts, W. R. Markesbery, S. W. Scheff, and M. A. Lovell, “Oxidative stress in head trauma in aging,” Free Radical Biology and Medicine, vol. 41, no. 1, pp. 77–85, 2006. View at Publisher · View at Google Scholar · View at Scopus
  46. M. Prins, T. Greco, D. Alexander, and C. C. Giza, “The pathophysiology of traumatic brain injury at a glance,” Disease Models & Mechanisms, vol. 6, no. 6, pp. 1307–1315, 2013. View at Publisher · View at Google Scholar · View at Scopus
  47. U. Dirnagl, C. Iadecola, and M. A. Moskowitz, “Pathobiology of ischaemic stroke: an integrated view,” Trends in Neurosciences, vol. 22, no. 9, pp. 391–397, 1999. View at Publisher · View at Google Scholar · View at Scopus
  48. J. Sahuquillo, M. A. Poca, and S. Amoros, “Current aspects of pathophysiology and cell dysfunction after severe head injury,” Current Pharmaceutical Design, vol. 7, no. 15, pp. 1475–1503, 2001. View at Publisher · View at Google Scholar · View at Scopus
  49. T. I. Peng and M. J. Jou, “Oxidative stress caused by mitochondrial calcium overload,” Annals of the New York Academy of Sciences, vol. 1201, pp. 183–188, 2010. View at Publisher · View at Google Scholar · View at Scopus
  50. Y. Xiong, Q. Gu, P. L. Peterson, J. P. Muizelaar, and C. P. Lee, “Mitochondrial dysfunction and calcium perturbation induced by traumatic brain injury,” Journal of Neurotrauma, vol. 14, no. 1, pp. 23–34, 1997. View at Publisher · View at Google Scholar · View at Scopus
  51. F. Clausen, H. Lundqvist, S. Ekmark, A. Lewén, T. Ebendal, and L. Hillered, “Oxygen free radical-dependent activation of extracellular signal-regulated kinase mediates apoptosis-like cell death after traumatic brain injury,” Journal of Neurotrauma, vol. 21, no. 9, pp. 1168–1182, 2004. View at Publisher · View at Google Scholar · View at Scopus
  52. N. Marklund, F. Clausen, T. Lewander, and L. Hillered, “Monitoring of reactive oxygen species production after traumatic brain injury in rats with microdialysis and the 4-hydroxybenzoic acid trapping method,” Journal of Neurotrauma, vol. 18, no. 11, pp. 1217–1227, 2001. View at Publisher · View at Google Scholar · View at Scopus
  53. J. D. Lambeth and A. S. Neish, “Nox enzymes and new thinking on reactive oxygen: a double-edged sword revisited,” Annual review of pathology, vol. 9, pp. 119–145, 2014. View at Publisher · View at Google Scholar · View at Scopus
  54. N. Chaudhari, P. Talwar, A. Parimisetty, C. Lefebvre d'Hellencourt, and P. Ravanan, “A molecular web: endoplasmic reticulum stress, inflammation, and oxidative stress,” Frontiers in Cellular Neuroscience, vol. 8, article 213, 2014. View at Publisher · View at Google Scholar
  55. B. Halliwell, “The role of oxygen radicals in human disease, with particular reference to the vascular system,” Haemostasis, vol. 23, supplement 1, pp. 118–126, 1993. View at Google Scholar · View at Scopus
  56. H. L. Hsieh and C. M. Yang, “Role of redox signaling in neuroinflammation and neurodegenerative diseases,” BioMed Research International, vol. 2013, Article ID 484613, 18 pages, 2013. View at Publisher · View at Google Scholar
  57. N. Kaludercic, S. Deshwal, and F. Di Lisa, “Reactive oxygen species and redox compartmentalization,” Frontiers in Physiology, vol. 5, article 285, 2014. View at Publisher · View at Google Scholar
  58. S. I. Liochev, “Free radical paradoxes,” Free Radical Biology and Medicine, vol. 65, pp. 232–233, 2013. View at Publisher · View at Google Scholar · View at Scopus
  59. B. Uttara, A. V. Singh, P. Zamboni, and R. T. Mahajan, “Oxidative stress and neurodegenerative diseases: a review of upstream and downstream antioxidant therapeutic options,” Current Neuropharmacology, vol. 7, no. 1, pp. 65–74, 2009. View at Publisher · View at Google Scholar · View at Scopus
  60. M. L. Circu and T. Y. Aw, “Reactive oxygen species, cellular redox systems, and apoptosis,” Free Radical Biology and Medicine, vol. 48, no. 6, pp. 749–762, 2010. View at Publisher · View at Google Scholar · View at Scopus
  61. P. S. Hole, R. L. Darley, and A. Tonks, “Do reactive oxygen species play a role in myeloid leukemias?” Blood, vol. 117, no. 22, pp. 5816–5826, 2011. View at Publisher · View at Google Scholar · View at Scopus
  62. C. Cornelius, R. Crupi, V. Calabrese et al., “Traumatic brain injury: oxidative stress and neuroprotection,” Antioxidants & Redox Signaling, vol. 19, no. 8, pp. 836–853, 2013. View at Publisher · View at Google Scholar · View at Scopus
  63. K. Keyer, A. S. Gort, and J. A. Imlay, “Superoxide and the production of oxidative DNA damage,” Journal of Bacteriology, vol. 177, no. 23, pp. 6782–6790, 1995. View at Google Scholar · View at Scopus
  64. S. R. Thomas, P. K. Witting, and G. R. Drummond, “Redox control of endothelial function and dysfunction: molecular mechanisms and therapeutic opportunities,” Antioxidants and Redox Signaling, vol. 10, no. 10, pp. 1713–1765, 2008. View at Publisher · View at Google Scholar · View at Scopus
  65. T. Nishikawa, D. Edelstein, X. L. Du et al., “Normalizing mitochondrial superoxide production blocks three pathways of hyperglycaemic damage,” Nature, vol. 404, no. 6779, pp. 787–790, 2000. View at Publisher · View at Google Scholar · View at Scopus
  66. T. Maraldi, “Natural compounds as modulators of NADPH oxidases,” Oxidative Medicine and Cellular Longevity, vol. 2013, Article ID 271602, 10 pages, 2013. View at Publisher · View at Google Scholar · View at Scopus
  67. F. Vieceli Dalla Sega, L. Zambonin, D. Fiorentini et al., “Specific aquaporins facilitate Nox-produced hydrogen peroxide transport through plasma membrane in leukaemia cells,” Biochimica et Biophysica Acta, vol. 1843, no. 4, pp. 806–814, 2014. View at Publisher · View at Google Scholar · View at Scopus
  68. T. Finkel, “Signal transduction by reactive oxygen species,” The Journal of Cell Biology, vol. 194, no. 1, pp. 7–15, 2011. View at Publisher · View at Google Scholar · View at Scopus
  69. E. D. Hall and J. M. Braughler, “Free radicals in CNS injury,” Research Publications—Association for Research in Nervous and Mental Disease, vol. 71, pp. 81–105, 1993. View at Google Scholar · View at Scopus
  70. M. M. Zaleska and R. A. Floyd, “Regional lipid peroxidation in rat brain in vitro: possible role of endogenous iron,” Neurochemical Research, vol. 10, no. 3, pp. 397–410, 1985. View at Publisher · View at Google Scholar · View at Scopus
  71. A. Rodríguez-Rodríguez, J. J. Egea-Guerrero, F. Murillo-Cabezas, and A. Carrillo-Vico, “Oxidative stress in traumatic brain injury,” Current Medicinal Chemistry, vol. 21, no. 10, pp. 1201–1211, 2014. View at Publisher · View at Google Scholar · View at Scopus
  72. A. Tarozzi, C. Angeloni, M. Malaguti, F. Morroni, S. Hrelia, and P. Hrelia, “Sulforaphane as a potential protective phytochemical against neurodegenerative diseases,” Oxidative Medicine and Cellular Longevity, vol. 2013, Article ID 415078, 10 pages, 2013. View at Publisher · View at Google Scholar · View at Scopus
  73. A. Minarini, A. Milelli, V. Tumiatti et al., “Cystamine-tacrine dimer: a new multi-target-directed ligand as potential therapeutic agent for Alzheimer's disease treatment,” Neuropharmacology, vol. 62, no. 2, pp. 997–1003, 2012. View at Publisher · View at Google Scholar · View at Scopus
  74. Z.-G. Xiong, X.-M. Zhu, X.-P. Chu et al., “Neuroprotection in ischemia: Blocking calcium-permeable acid-sensing ion channels,” Cell, vol. 118, no. 6, pp. 687–698, 2004. View at Publisher · View at Google Scholar · View at Scopus
  75. C. Ikonomidou and L. Turski, “Why did NMDA receptor antagonists fail clinical trials for stroke and traumatic brain injury?” The Lancet Neurology, vol. 1, no. 6, pp. 383–386, 2002. View at Publisher · View at Google Scholar · View at Scopus
  76. J. Sastre, F. V. Pallardo, and J. Vina, “The role of mitochondrial oxidative stress in aging,” Free Radical Biology & Medicine, vol. 35, no. 1, pp. 1–8, 2003. View at Google Scholar
  77. H. A. Kontos and J. T. Povlishock, “Oxygen radicals in brain injury,” Central Nervous System Trauma, vol. 3, no. 4, pp. 257–263, 1986. View at Google Scholar · View at Scopus
  78. H. A. Kontos and E. P. Wei, “Superoxide production in experimental brain injury,” Journal of Neurosurgery, vol. 64, no. 5, pp. 803–807, 1986. View at Publisher · View at Google Scholar · View at Scopus
  79. G. Barreto, R. E. White, Y. Ouyang, L. Xu, and R. G. Giffard, “Astrocytes: targets for neuroprotection in stroke,” Central Nervous System Agents in Medicinal Chemistry, vol. 11, no. 2, pp. 164–173, 2011. View at Publisher · View at Google Scholar · View at Scopus
  80. M. L. Block and J. S. Hong, “Microglia and inflammation-mediated neurodegeneration: multiple triggers with a common mechanism,” Progress in Neurobiology, vol. 76, no. 2, pp. 77–98, 2005. View at Publisher · View at Google Scholar · View at Scopus
  81. J. M. C. Gutteridge, “Lipid peroxidation and antioxidants as biomarkers of tissue damage,” Clinical Chemistry, vol. 41, no. 12, pp. 1819–1828, 1995. View at Google Scholar · View at Scopus
  82. A. G. Mustafa, I. N. Singh, J. Wang, K. M. Carrico, and E. D. Hall, “Mitochondrial protection after traumatic brain injury by scavenging lipid peroxyl radicals,” Journal of Neurochemistry, vol. 114, no. 1, pp. 271–280, 2010. View at Publisher · View at Google Scholar · View at Scopus
  83. I. N. Singh, L. K. Gilmer, D. M. Miller, J. E. Cebak, J. A. Wang, and E. D. Hall, “Phenelzine mitochondrial functional preservation and neuroprotection after traumatic brain injury related to scavenging of the lipid peroxidation-derived aldehyde 4-hydroxy-2-nonenal,” Journal of Cerebral Blood Flow & Metabolism, vol. 33, no. 4, pp. 593–599, 2013. View at Publisher · View at Google Scholar · View at Scopus
  84. J. N. Keller, R. J. Mark, A. J. Bruce et al., “4-hydroxynonenal, an aldehydic product of membrane lipid peroxidation, impairs glutamate transport and mitochondrial function in synaptosomes,” Neuroscience, vol. 80, no. 3, pp. 685–696, 1997. View at Publisher · View at Google Scholar · View at Scopus
  85. W. A. Pedersen, N. R. Cashman, and M. P. Mattson, “The lipid peroxidation product 4-hydroxynonenal impairs glutamate and glucose transport and choline acetyltransferase activity in NSC-19 motor neuron cells,” Experimental Neurology, vol. 155, no. 1, pp. 1–10, 1999. View at Publisher · View at Google Scholar · View at Scopus
  86. R. Durmaz, G. Kanbak, F. Akyüz et al., “Lazaroid attenuates edema by stabilizing ATPase in the traumatized rat brain,” Canadian Journal of Neurological Sciences, vol. 30, no. 2, pp. 143–149, 2003. View at Google Scholar · View at Scopus
  87. P. Račay, P. Kaplán, V. Mézešová, and J. Lehotský, “Lipid peroxidation both inhibits Ca2+-ATPase and increases Ca2+ permeability of endoplasmic reticulum membrane,” Biochemistry and Molecular Biology International, vol. 41, no. 4, pp. 647–655, 1997. View at Google Scholar · View at Scopus
  88. K. Wada, K. Chatzipanteli, S. Kraydieh, R. Busto, and W. D. Dietrich, “Inducible nitric oxide synthase expression after traumatic brain injury and neuroprotection with aminoguanidine treatment in rats,” Neurosurgery, vol. 43, no. 6, pp. 1427–1436, 1998. View at Google Scholar · View at Scopus
  89. C. Mésenge, C. Charriaut-Marlangue, C. Verrecchia, M. Allix, R. R. Boulu, and M. Plotkine, “Reduction of tyrosine nitration after Nω-nitro-l-arginine-methylester treatment of mice with traumatic brain injury,” European Journal of Pharmacology, vol. 353, no. 1, pp. 53–57, 1998. View at Publisher · View at Google Scholar · View at Scopus
  90. Y. Deng-Bryant, I. N. Singh, K. M. Carrico, and E. D. Hall, “Neuroprotective effects of tempol, a catalytic scavenger of peroxynitrite-derived free radicals, in a mouse traumatic brain injury model,” Journal of Cerebral Blood Flow and Metabolism, vol. 28, no. 6, pp. 1114–1126, 2008. View at Publisher · View at Google Scholar · View at Scopus
  91. C. Gahm, S. Holmin, and T. Mathiesen, “Temporal profiles and cellular sources of three nitric oxide synthase isoforms in the brain after experimental contusion,” Neurosurgery, vol. 46, no. 1, pp. 169–177, 2000. View at Google Scholar · View at Scopus
  92. C. S. Cobbs, A. Fenoy, D. S. Bredt, and L. J. Noble, “Expression of nitric oxide synthase in the cerebral microvasculature after traumatic brain injury in the rat,” Brain Research, vol. 751, no. 2, pp. 336–338, 1997. View at Publisher · View at Google Scholar · View at Scopus
  93. V. L. Raghavendra Rao, A. Dogan, K. K. Bowen, and R. J. Dempsey, “Traumatic injury to rat brain upregulates neuronal nitric oxide synthase expression and l-[3H]nitroarginine binding,” Journal of Neurotrauma, vol. 16, no. 10, pp. 865–877, 1999. View at Publisher · View at Google Scholar · View at Scopus
  94. P. Ascenzi, A. Bocedi, P. Visca et al., “Hemoglobin and heme scavenging,” IUBMB Life, vol. 57, no. 11, pp. 749–759, 2005. View at Publisher · View at Google Scholar · View at Scopus
  95. T. Arai, N. Takeyama, and T. Tanaka, “Glutathione monoethyl ester and inhibition of the oxyhemoglobin-induced increase in cytosolic calcium in cultured smooth-muscle cells,” Journal of Neurosurgery, vol. 90, no. 3, pp. 527–532, 1999. View at Publisher · View at Google Scholar · View at Scopus
  96. T. Asano, “Oxyhemoglobin as the principal cause of cerebral vasospasm: a holistic view of its actions,” Critical Reviews in Neurosurgery, vol. 9, no. 5, pp. 303–318, 1999. View at Publisher · View at Google Scholar
  97. F. Marzatico, P. Gaetani, C. Cafe, G. Spanu, and R. Rodriguez y Baena, “Antioxidant enzymatic activities after experimental subarachnoid hemorrhage in rats,” Acta Neurologica Scandinavica, vol. 87, no. 1, pp. 62–66, 1993. View at Publisher · View at Google Scholar · View at Scopus
  98. F. Marzatico, P. Gaetani, V. Silvani, D. Lombardi, E. Sinforiani, and R. Baena, “Experimental isobaric subarachnoid hemorrhage: regional mitochondrial function during the acute and late phase,” Surgical Neurology, vol. 34, no. 5, pp. 294–300, 1990. View at Publisher · View at Google Scholar · View at Scopus
  99. E. D. Hall, R. A. Vaishnav, and A. G. Mustafa, “Antioxidant therapies for traumatic brain injury,” Neurotherapeutics, vol. 7, no. 1, pp. 51–61, 2010. View at Publisher · View at Google Scholar · View at Scopus
  100. S. Rehncrona, H. N. Hauge, and B. K. Siesjo, “Enhancement of iron-catalyzed free radical formation by acidosis in brain homogenates: differences in effect by lactic acid and CO2,” Journal of Cerebral Blood Flow and Metabolism, vol. 9, no. 1, pp. 65–70, 1989. View at Publisher · View at Google Scholar · View at Scopus
  101. J. D. Lambeth and A. S. Neish, “Nox enzymes and new thinking on reactive oxygen: a double-edged sword revisited,” Annual Review of Pathology, vol. 9, pp. 119–145, 2014. View at Publisher · View at Google Scholar · View at Scopus
  102. A. Panday, M. K. Sahoo, D. Osorio, and S. Batra, “NADPH oxidases: an overview from structure to innate immunity-associated pathologies,” Cellular and Molecular Immunology, vol. 12, no. 1, pp. 5–23, 2014. View at Publisher · View at Google Scholar
  103. H. Sumimoto, “Structure, regulation and evolution of Nox-family NADPH oxidases that produce reactive oxygen species,” FEBS Journal, vol. 275, no. 13, pp. 3249–3277, 2008. View at Publisher · View at Google Scholar · View at Scopus
  104. K. Bedard and K.-H. Krause, “The NOX family of ROS-generating NADPH oxidases: physiology and pathophysiology,” Physiological Reviews, vol. 87, no. 1, pp. 245–313, 2007. View at Publisher · View at Google Scholar · View at Scopus
  105. S. Sorce and K. H. Krause, “NOX enzymes in the central nervous system: from signaling to disease,” Antioxidants and Redox Signaling, vol. 11, no. 10, pp. 2481–2504, 2009. View at Publisher · View at Google Scholar · View at Scopus
  106. A. Y. Abramov, J. Jacobson, F. Wientjes, J. Hothersall, L. Canevari, and M. R. Duchen, “Expression and modulation of an NADPH oxidase in mammalian astrocytes,” The Journal of Neuroscience, vol. 25, no. 40, pp. 9176–9184, 2005. View at Publisher · View at Google Scholar · View at Scopus
  107. S. H. Choi, Y. L. Da, U. K. Seung, and K. J. Byung, “Thrombin-induced oxidative stress contributes to the death of hippocampal neurons in vivo: role of microglial NADPH oxidase,” The Journal of Neuroscience, vol. 25, no. 16, pp. 4082–4090, 2005. View at Publisher · View at Google Scholar · View at Scopus
  108. A. P. O. Ferreira, F. S. Rodrigues, I. D. Della-Pace et al., “The effect of NADPH-oxidase inhibitor apocynin on cognitive impairment induced by moderate lateral fluid percussion injury: role of inflammatory and oxidative brain damage,” Neurochemistry International, vol. 63, no. 6, pp. 583–593, 2013. View at Publisher · View at Google Scholar · View at Scopus
  109. D. J. Loane, B. A. Stoica, K. R. Byrnes, W. Jeong, and A. I. Faden, “Activation of mGluR5 and inhibition of NADPH oxidase improves functional recovery after traumatic brain injury,” Journal of Neurotrauma, vol. 30, no. 5, pp. 403–412, 2013. View at Publisher · View at Google Scholar · View at Scopus
  110. K. Dohi, H. Ohtaki, T. Nakamachi et al., “Gp91phox (NOX2) in classically activated microglia exacerbates traumatic brain injury,” Journal of Neuroinflammation, vol. 7, article 41, 2010. View at Publisher · View at Google Scholar · View at Scopus
  111. J. Stolk, T. J. Hiltermann, J. H. Dijkman, and A. J. Verhoeven, “Characteristics of the inhibition of NADPH oxidase activation in neutrophils by apocynin, a methoxy-substituted catechol,” American Journal of Respiratory Cell and Molecular Biology, vol. 11, no. 1, pp. 95–102, 1994. View at Publisher · View at Google Scholar · View at Scopus
  112. E. van den Worm, C. J. Beukelman, A. J. J. van den Berg, B. H. Kroes, R. P. Labadie, and H. van Dijk, “Effects of methoxylation of apocynin and analogs on the inhibition of reactive oxygen species production by stimulated human neutrophils,” European Journal of Pharmacology, vol. 433, no. 2-3, pp. 225–230, 2001. View at Publisher · View at Google Scholar · View at Scopus
  113. T. Hayashi, P. A. R. Juliet, H. Kano-Hayashi et al., “NADPH oxidase inhibitor, apocynin, restores the impaired endothelial-dependent and -independent responses and scavenges superoxide anion in rats with type 2 diabetes complicated by NO dysfunction,” Diabetes, Obesity and Metabolism, vol. 7, no. 4, pp. 334–343, 2005. View at Publisher · View at Google Scholar · View at Scopus
  114. Y. Jinnouchi, S.-I. Yamagishi, T. Matsui et al., “Administration of pigment epithelium-derived factor (PEDF) inhibits cold injury-induced brain edema in mice,” Brain Research, vol. 1167, no. 1, pp. 92–100, 2007. View at Publisher · View at Google Scholar · View at Scopus
  115. D. J. Loane, A. Kumar, B. A. Stoica, R. Cabatbat, and A. I. Faden, “Progressive neurodegeneration after experimental brain trauma: association with chronic microglial activation,” Journal of Neuropathology and Experimental Neurology, vol. 73, no. 1, pp. 14–29, 2014. View at Publisher · View at Google Scholar · View at Scopus
  116. L. Qin, Y. Liu, J. S. Hong, and F. T. Crews, “NADPH oxidase and aging drive microglial activation, oxidative stress, and dopaminergic neurodegeneration following systemic LPS administration,” Glia, vol. 61, no. 6, pp. 855–868, 2013. View at Publisher · View at Google Scholar · View at Scopus
  117. M. E. Lull and M. L. Block, “Microglial activation and chronic neurodegeneration,” Neurotherapeutics, vol. 7, no. 4, pp. 354–365, 2010. View at Publisher · View at Google Scholar · View at Scopus
  118. A. Kumar, B. A. Stoica, B. Sabirzhanov, M. P. Burns, A. I. Faden, and D. J. Loane, “Traumatic brain injury in aged animals increases lesion size and chronically alters microglial/macrophage classical and alternative activation states,” Neurobiology of Aging, vol. 34, no. 5, pp. 1397–1411, 2013. View at Publisher · View at Google Scholar · View at Scopus
  119. S. J. Cooney, S. L. Bermudez-Sabogal, and K. R. Byrnes, “Cellular and temporal expression of NADPH oxidase (NOX) isotypes after brain injury,” Journal of Neuroinflammation, vol. 10, article 155, 2013. View at Publisher · View at Google Scholar · View at Scopus
  120. N. B. Chauhan, “Chronic neurodegenerative consequences of traumatic brain injury,” Restorative Neurology and Neuroscience, vol. 32, no. 2, pp. 337–365, 2014. View at Google Scholar
  121. S. Shimohama, H. Tanino, N. Kawakami et al., “Activation of NADPH oxidase in Alzheimer's disease brains,” Biochemical and Biophysical Research Communications, vol. 273, no. 1, pp. 5–9, 2000. View at Publisher · View at Google Scholar · View at Scopus
  122. D. Zekry, T. Kay Epperson, and K.-H. Krause, “A role for NOX NADPH oxidases in Alzheimer's disease and other types of dementia?” IUBMB Life, vol. 55, no. 6, pp. 307–313, 2003. View at Publisher · View at Google Scholar · View at Scopus
  123. W. Zhang, T. Wang, L. Qin et al., “Neuroprotective effect of dextromethorphan in the MPTP Parkinson's disease model: role of NADPH oxidase,” The FASEB journal, vol. 18, no. 3, pp. 589–591, 2004. View at Google Scholar · View at Scopus
  124. C. Angeloni, L. Zambonin, and S. Hrelia, “Role of methylglyoxal in alzheimer's disease,” BioMed Research International, vol. 2014, Article ID 238485, 12 pages, 2014. View at Publisher · View at Google Scholar · View at Scopus
  125. H. M. Bramlett and W. D. Dietrich, “Pathophysiology of cerebral ischemia and brain trauma: similarities and differences,” Journal of Cerebral Blood Flow & Metabolism, vol. 24, no. 2, pp. 133–150, 2004. View at Google Scholar · View at Scopus
  126. C. van den Heuvel, E. Thornton, and R. Vink, “Traumatic brain injury and Alzheimer's disease: a review,” Progress in Brain Research, vol. 161, pp. 303–316, 2007. View at Publisher · View at Google Scholar · View at Scopus
  127. K. Beyer, M. Domingo-Sàbat, and A. Ariza, “Molecular pathology of Lewy body diseases,” International Journal of Molecular Sciences, vol. 10, no. 3, pp. 724–745, 2009. View at Publisher · View at Google Scholar · View at Scopus
  128. T. Yasuda, Y. Nakata, and H. Mochizuki, “α-Synuclein and neuronal cell death,” Molecular neurobiology, vol. 47, no. 2, pp. 466–483, 2013. View at Publisher · View at Google Scholar · View at Scopus
  129. S. A. Acosta, N. Tajiri, I. de la Pena et al., “Alpha-synuclein as a pathological link between chronic traumatic brain injury and Parkinson's disease,” Journal of Cellular Physiology, vol. 230, no. 5, pp. 1024–1032, 2015. View at Publisher · View at Google Scholar
  130. A. C. Cristóvão, S. Guhathakurta, E. Bok et al., “Nadph oxidase 1 mediates alpha-synucleinopathy in Parkinson's disease,” The Journal of Neuroscience, vol. 32, no. 42, pp. 14465–14477, 2012. View at Publisher · View at Google Scholar · View at Scopus