A time course of NADPH-oxidase up-regulation and endothelial nitric oxide synthase activation in the hippocampus following neurotrauma

Free Radical Biology and Medicine

Volumn 77, Issue , 2014, Pages 21-29

  Ansari, Mubeen A ^a   Roberts, Kelly N ^a   Scheff, Stephen W ^a  

^a UNIVERSITY OF KENTUCKY   (United States)

Author keywords

Free radicals; NADPH oxidase; Secondary injury cascades; Traumatic brain injury

Indexed keywords

ENDOTHELIAL NITRIC OXIDE SYNTHASE; NITRIC OXIDE; REACTIVE NITROGEN SPECIES; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE PHOSPHATE OXIDASE; NEUTROPHIL CYTOSOL FACTOR 40K; NEUTROPHIL CYTOSOLIC FACTOR 1; NOS3 PROTEIN, RAT; OXIDOREDUCTASE; P67PHOX PROTEIN, RAT; PHOSPHOPROTEIN; PROTEIN SUBUNIT; SUPEROXIDE;

AEROBIC METABOLISM; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; APOPTOSIS; ARTICLE; CELL DEATH; CYTOSOLIC FRACTION; ENZYME ACTIVATION; ENZYME ACTIVITY; ENZYME INDUCTION; HIPPOCAMPUS; MALE; MODULATION; NERVOUS SYSTEM INJURY; NONHUMAN; OXIDATIVE STRESS; RAT; WESTERN BLOTTING; ANIMAL; BRAIN INJURY; CELL MEMBRANE; ENZYMOLOGY; METABOLISM; PROTEIN SUBUNIT; PROTEIN TRANSPORT; SPRAGUE DAWLEY RAT; UPREGULATION;

ANIMALS; BRAIN INJURIES; CELL MEMBRANE; ENZYME ACTIVATION; HIPPOCAMPUS; MALE; NADH, NADPH OXIDOREDUCTASES; NADPH OXIDASE; NITRIC OXIDE; NITRIC OXIDE SYNTHASE TYPE III; PHOSPHOPROTEINS; PROTEIN SUBUNITS; PROTEIN TRANSPORT; RATS, SPRAGUE-DAWLEY; SUPEROXIDES; UP-REGULATION;

EID: 84908571619     PISSN: 08915849     EISSN: 18734596     Source Type: Journal    
DOI: 10.1016/j.freeradbiomed.2014.08.025     Document Type: Article

References (94)

1. Langlois, J. A.; Marr, A.; Mitchko, J.; Johnson, R. L. Tracking the silent epidemic and educating the public: CDC's traumatic brain injury-associated activities under the TBI Act of 1996 and the Children's Health Act of 2000. J. Head Trauma Rehabil. 20:196-204; 2005.
2. Bayir, H.; Kagan, V. E.; Clark, R. S.; Janesko-Feldman, K.; Rafikov, R.; Huang, Z.; Zhang, X.; Vagni, V.; Billiar, T. R.; Kochanek, P. M. Neuronal NOS-mediated nitration and inactivation of manganese superoxide dismutase in brain after experimental and human brain injury. J. Neurochem. 101:168-181; 2007.
3. Hall, E. D.; Detloff, M. R.; Johnson, K.; Kupina, N. C. Peroxynitrite-mediated protein nitration and lipid peroxidation in a mouse model of traumatic brain injury. J. Neurotrauma 21:9-20; 2004.
4. Siesjo, B. K. Calcium-mediated processes in neuronal degeneration. Ann. N. Y. Acad. Sci 747:140-161; 1994.
5. Gilmer, L. K.; Ansari, M. A.; Roberts, K. N.; Scheff, S. W. Age-related mitochondrial changes after traumatic brain injury. J. Neurotrauma 27:939-950; 2010.
6. Gilmer, L. K.; Ansari, M. A.; Roberts, K. N.; Scheff, S. W. Age-related changes in mitochondrial respiration and oxidative damage in the cerebral cortex of the Fischer 344 rat. Mech. Ageing Dev. 131:133-143; 2010.
7. Singh, I. N.; Sullivan, P. G.; Hall, E. D. Peroxynitrite-mediated oxidative damage to brain mitochondria: protective effects of peroxynitrite scavengers. J. Neurosci. Res. 85:2216-2223; 2007.
8. Sullivan, P. G.; Rabchevsky, A. G.;Waldmeier, P. C.; Springer, J. E. Mitochondrial permeability transition in CNS trauma: cause or effect of neuronal cell death? J. Neurosci. Res 79:231-239; 2005.
9. Biegon, A.; Fry, P. A.; Paden, C. M.; Alexandrovich, A.; Tsenter, J.; Shohami, E. Dynamic changes in N-methyl-D-aspartate receptors after closed head injury in mice: implications for treatment of neurological and cognitive deficits. Proc. Natl. Acad. Sci. USA 101:5117-5122; 2004.
10. Ansari, M. A.; Roberts, K. N.; Scheff, S. Dose and time dependent neuroprotective effects of Pycnogenol following traumatic brain injury. J. Neurotrauma 30:1542-1549; 2013.
11. Ansari, M. A.; Roberts, K. N.; Scheff, S. W. Oxidative stress and modification of synaptic proteins in hippocampus after traumatic brain injury. Free Radic. Biol. Med. 45:443-452; 2008.
12. Ansari, M. A.; Roberts, K. N.; Scheff, S. W. A time course of contusion-induced oxidative stress and synaptic proteins in cortex in a rat model of TBI. J. Neurotrauma 25:513-526; 2008.
13. Holmin, S.; Schalling, M.; Hojeberg, B.; Nordqvist, A. C.; Skeftruna, A. K.; Mathiesen, T. Delayed cytokine expression in rat brain following experimental contusion. J. Neurosurg. 86:493-504; 1997.
14. Liu, B.; Hong, J. S. Role of microglia in inflammation-mediated neurodegenerative diseases: mechanisms and strategies for therapeutic intervention. J. Pharmacol. Exp. Ther. 304:1-7; 2003.
15. Scheff, S. W.; Ansari, M. A.; Roberts, K. N. Neuroprotective effect of Pycnogenol (R) following traumatic brain injury. Exp. Neurol. 239:183-191; 2013.
16. Shohami, E.; Bass, R.; Wallach, D.; Yamin, A.; Gallily, R. Inhibition of tumor necrosis factor alpha (TNFalpha) activity in rat brain is associated with cerebroprotection after closed head injury. J. Cereb. Blood Flow Metab. 16:378-384; 1996.
17. Shao, C.; Roberts, K. N.; Markesbery,W. R.; Scheff, S.W.; Lovell, M. A. Oxidative stress in head trauma in aging. Free Radic. Biol. Med. 41:77-85; 2006.
18. Ozdemir, D.; Uysal, N.; Gonenc, S.; Acikgoz, O.; Sonmez, A.; Topcu, A.; Ozdemir, N.; Duman, M.; Semin, I.; Ozkan, H. Effect of melatonin on brain oxidative damage induced by traumatic brain injury in immature rats. Physiol. Res. 54:631-637; 2005.
19. Ansari, M. A.; Ahmad, A. S.; Ahmad, M.; Salim, S.; Yousuf, S.; Ishrat, T.; Islam, F. Selenium protects cerebral ischemia in rat brain mitochondria. Biol. Trace Elem. Res. 101:73-86; 2004.
20. Gahm, C.; Holmin, S.; Mathiesen, T. Temporal profiles and cellular sources of three nitric oxide synthase isoforms in the brain after experimental contusion. Neurosurgery 46:169-177; 2000.
21. Jafarian-Tehrani, M.; Louin, G.; Royo, N. C.; Besson, V. C.; Bohme, G. A.; Plotkine, M.; Marchand-Verrecchia, C. 1400W, a potent selective inducible NOS inhibitor, improves histopathological outcome following traumatic brain injury in rats. Nitric Oxide 12:61-69; 2005.
22. Choi, B. Y.; Jang, B. G.; Kim, J. H.; Lee, B. E.; Sohn, M.; Song, H. K.; Suh, S. W. Prevention of traumatic brain injury-induced neuronal death by inhibition of NADPH oxidase activation. Brain Res. 1481:49-58; 2012.
23. Ferreira, A. P.; Rodrigues, F. S.; Della-Pace, I. D.; Mota, B. C.; Oliveira, S. M.; Velho Gewehr, C. D.; Bobinski, F.; de Oliveira, C. V.; Brum, J. S.; Oliveira, M. S.; Furian, A. F.; de Barros, C. S.; Ferreira, J.; Santos, A. R.; Fighera, M. R.; Royes, L. F. The effect of NADPH-oxidase inhibitor apocynin on cognitive impairment induced by moderate lateral fluid percussion injury: role of inflammatory and oxidative brain damage. Neurochem. Int. 63:583-593; 2013.
24. Loane, D. J.; Stoica, B. A.; Byrnes, K. R.; Jeong, W.; Faden, A. I. Activation of mGluR5 and inhibition of NADPH oxidase improves functional recovery after traumatic brain injury. J. Neurotrauma 30:403-412; 2013.
25. Zhang, Q. G.; Laird, M. D.; Han, D.; Nguyen, K.; Scott, E.; Dong, Y.; Dhandapani, K. M.; Brann, D. W. Critical role of NADPH oxidase in neuronal oxidative damage and microglia activation following traumatic brain injury. PLoS One 7; 2012e34504 7; 2012.
26. Block, M. L.; Zecca, L.; Hong, J. S. Microglia-mediated neurotoxicity: uncovering the molecular mechanisms. Nat. Rev. Neurosci. 8:57-69; 2007.
27. Lull, M. E.; Block, M. L. Microglial activation and chronic neurodegeneration. Neurotherapeutics 7:354-365; 2010.
28. Qin, L.; Liu, Y.; Wang, T.; Wei, S. J.; Block, M. L.; Wilson, B.; Liu, B.; Hong, J. S. NADPH oxidase mediates lipopolysaccharide-induced neurotoxicity and proin.ammatory gene expression in activated microglia. J. Biol. Chem. 279:1415-1421; 2004.
29. Brennan, A. M.; Suh, S. W.; Won, S. J.; Narasimhan, P.; Kauppinen, T. M.; Lee, H.; Edling, Y.; Chan, P. H.; Swanson, R. A. NADPH oxidase is the primary source of superoxide induced by NMDA receptor activation. Nat. Neurosci. 12:857-863; 2009.
30. Liu, X. X.; Zhou, H. J.; Cai, L.; Zhang, W.; Ma, J. L.; Tao, X. J.; Yu, J. N. NADPH oxidase-dependent formation of reactive oxygen species contributes to transforming growth factor beta1-induced epithelial-mesenchymal transition in rat peritoneal mesothelial cells, and the role of astragalus intervention. Chin. J. Integr. Med. ; 2012.
31. Zhou, H.; Zhang, F.; Chen, S. H.; Zhang, D.; Wilson, B.; Hong, J. S.; Gao, H. M. Rotenone activates phagocyte NADPH oxidase by binding to its membrane subunit gp91phox. Free Radic. Biol. Med. 52:303-313; 2012.
32. Block, M. L.; Hong, J. S. Microglia and inflammation-mediated neurodegeneration: multiple triggers with a common mechanism. Prog. Neurobiol. 76:77-98; 2005.
33. Rooker, S.; Jander, S.; Van Reempts, J.; Stoll, G.; Jorens, P. G.; Borgers, M.; Verlooy, J. Spatiotemporal pattern of neuroinflammation after impactacceleration closed head injury in the rat. Mediators Inflamm. 2006:90123; 2006.
34. Brown, G. C. Mechanisms of inflammatory neurodegeneration: iNOS and NADPH oxidase. Biochem. Soc. Trans. 35:1119-1121; 2007.
35. Duchen, M. R. Roles of mitochondria in health and disease. Diabetes 53(Suppl. 1): S96-S102; 2004.
36. Hortobagyi, T.; Gorlach, C.; Benyo, Z.; Lacza, Z.; Hortobagyi, S.; Wahl, M.; Harkany, T. Inhibition of neuronal nitric oxide synthase-mediated activation of poly(ADP-ribose) polymerase in traumatic brain injury: neuroprotection by 3-aminobenzamide. Neuroscience 121:983-990; 2003.
37. Fukui, T.; Lassegue, B.; Kai, H.; Alexander, R. W.; Griendling, K. K. Cytochrome b-558 alpha-subunit cloning and expression in rat aortic smooth muscle cells. Biochim. Biophys. Acta 1231:215-219; 1995.
38. Jones, S. A.; O'Donnell, V. B.; Wood, J. D.; Broughton, J. P.; Hughes, E. J.; Jones, O. T. Expression of phagocyte NADPH oxidase components in human endothelial cells. Am. J. Physiol. 271:H1626-H1634; 1996.
39. Brown, G. C.; Neher, J. J. Inflammatory neurodegeneration and mechanisms of microglial killing of neurons. Mol. Neurobiol. 41:242-247; 2010.
40. Chang, C. C.; Wang, Y. H.; Chern, C. M.; Liou, K. T.; Hou, Y. C.; Peng, Y. T.; Shen, Y. C. Prodigiosin inhibits gp91(phox) and iNOS expression to protect mice against the oxidative/nitrosative brain injury induced by hypoxia-ischemia. Toxicol. Appl. Pharmacol. 257:137-147; 2011.
41. Cooney, S. J.; Bermudez-Sabogal, S. L.; Byrnes, K. R. Cellular and temporal expression of NADPH oxidase (NOX) isotypes after brain injury. J. Neuroinflammation 10:155; 2013.
42. Hur, J.; Lee, P.; Kim, M. J.; Kim, Y.; Cho, Y. W. Ischemia-activated microglia induces neuronal injury via activation of gp91phox NADPH oxidase. Biochem. Biophys. Res. Commun. 391:1526-1530; 2010.
43. Loane, D. J.; Kumar, A.; Stoica, B. A.; Cabatbat, R.; Faden, A. I. Progressive neurodegeneration after experimental brain trauma: association with chronic microglial activation. J. Neuropathol. Exp. Neurol. 73:14-29; 2014.
44. Kim, Y. H.; Koh, J. Y. The role of NADPH oxidase and neuronal nitric oxide synthase in zinc-induced poly(ADP-ribose) polymerase activation and cell death in cortical culture. Exp. Neurol. 177:407-418; 2002.
45. Tammariello, S. P.; Quinn, M. T.; Estus, S. NADPH oxidase contributes directly to oxidative stress and apoptosis in nerve growth factor-deprived sympathetic neurons. J. Neurosci. 20:RC53; 2000.
46. Abramov, A. Y.; Jacobson, J.; Wientjes, F.; Hothersall, J.; Canevari, L.; Duchen, M. R. Expression and modulation of an NADPH oxidase in mammalian astrocytes. J. Neurosci. 25:9176-9184; 2005.
47. Abramov, A. Y.; Scorziello, A.; Duchen, M. R. Three distinct mechanisms generate oxygen free radicals in neurons and contribute to cell death during anoxia and reoxygenation. J. Neurosci. 27:1129-1138; 2007.
48. Choi, S. H.; Lee, D. Y.; Kim, S. U.; Jin, B. K. Thrombin-induced oxidative stress contributes to the death of hippocampal neurons in vivo: role of microglial NADPH oxidase. J. Neurosci. 25:4082-4090; 2005.
49. Song, S. X.; Gao, J. L.; Wang, K. J.; Li, R.; Tian, Y. X.; Wei, J. Q.; Cui, J. Z. Attenuation of brain edema and spatial learning deficits by the inhibition of NADPH oxidase activity using apocynin following diffuse traumatic brain injury in rats. Mol. Med. Rep 7:327-331; 2013.
50. Ansari, M. A.; Keller, J. N.; Scheff, S. W. Protective effect of Pycnogenol in human neuroblastoma SH-SY5Y cells following acrolein-induced cytotoxicity. Free Radic. Biol. Med. 45:1510-1519; 2008.
51. Babior, B. M. NADPH oxidase: an update. Blood 93:1464-1476; 1999.
52. Ozaki, M.; Deshpande, S. S.; Angkeow, P.; Bellan, J.; Lowenstein, C. J.; Dinauer, M. C.; Goldschmidt-Clermont, P. J.; Irani, K. Inhibition of the Rac1 GTPase protects against nonlethal ischemia/reperfusion-induced necrosis and apoptosis in vivo. FASEB J. 14:418-429; 2000.
53. Reeves, E. P.; Dekker, L. V.; Forbes, L. V.; Wientjes, F. B.; Grogan, A.; Pappin, D. J.; Segal, A. W. Direct interaction between p47phox and protein kinase C: evidence for targeting of protein kinase C by p47phox in neutrophils. Biochem. J. 344(Pt 3):859-866; 1999.
54. Cross, A. R.; Segal, A. W. The NADPH oxidase of professional phagocytes-prototype of the NOX electron transport chain systems. Biochim. Biophys. Acta 1657:1-22; 2004.
55. Anantharam, V.; Kaul, S.; Song, C.; Kanthasamy, A.; Kanthasamy, A. G. Pharmacological inhibition of neuronal NADPH oxidase protects against 1-methyl-4-phenylpyridinium (MPP+)-induced oxidative stress and apoptosis in mesencephalic dopaminergic neuronal cells. Neurotoxicology 28:988-997; 2007.
56. Ansari, M. A.; Scheff, S. W. NADPH-oxidase activation and cognition in Alzheimer disease progression. Free Radic. Biol. Med. 51:171-178; 2011.
57. McCann, S. K.; Dusting, G. J.; Roulston, C. L. Early increase of Nox4 NADPH oxidase and superoxide generation following endothelin-1-induced stroke in conscious rats. J. Neurosci. Res. 86:2524-2534; 2008.
58. Droge, W. Free radicals in the physiological control of cell function. Physiol. Rev. 82:47-95; 2002.
59. Gao, H. M.; Zhou, H.; Hong, J. S. NADPH oxidases: novel therapeutic targets for neurodegenerative diseases. Trends Pharmacol. Sci. 33:295-303; 2012.
60. Kim, J. H.; Jang, B. G.; Choi, B. Y.; Kim, H. S.; Sohn, M.; Chung, T. N.; Choi, H. C.; Song, H. K.; Suh, S. W. Post-treatment of an NADPH oxidase inhibitor prevents seizure-induced neuronal death. Brain Res. 1499:163-172; 2013.
61. Cherian, L.; Hlatky, R.; Robertson, C. S. Nitric oxide in traumatic brain injury. Brain Pathol. 14:195-201; 2004.
62. Hall, E. D.; Wang, J. A.; Miller, D. M. Relationship of nitric oxide synthase induction to peroxynitrite-mediated oxidative damage during the first week after experimental traumatic brain injury. Exp. Neurol. 238:176-182; 2012.
63. Wada, K.; Chatzipanteli, K.; Busto, R.; Dietrich, W. D. Role of nitric oxide in traumatic brain injury in the rat. J. Neurosurg. 89:807-818; 1998.
64. Zhou, Y. F.; Li, W. T.; Han, H. C.; Gao, D. K.; He, X. S.; Li, L.; Song, J. N.; Fei, Z. Allicin protects rat cortical neurons against mechanical trauma injury by regulating nitric oxide synthase pathways. Brain Res. Bull. 100:14-21; 2014.
65. Oddi, S.; Latini, L.; Viscomi, M. T.; Bisicchia, E.; Molinari, M.; Maccarrone, M. Distinct regulation of nNOS and iNOS by CB2 receptor in remote delayed neurodegeneration. J. Mol. Med. (Berl.) 90:371-387; 2012.
66. Nathan, C.; Xie, Q. W. Nitric oxide synthases: roles, tolls, and controls. Cell 78:915-918; 1994.
67. DeWitt, D. S.; Smith, T. G.; Deyo, D. J.; Miller, K. R.; Uchida, T.; Prough, D. S. L-Arginine and superoxide dismutase prevent or reverse cerebral hypoperfusion after fluid-percussion traumatic brain injury. J. Neurotrauma 14:223-233; 1997.
68. Lee, S. T.; Chu, K.; Sinn, D. I.; Jung, K. H.; Kim, E. H.; Kim, S. J.; Kim, J. M.; Ko, S. Y.; Kim, M.; Roh, J. K. Erythropoietin reduces perihematomal inflammation and cell death with eNOS and STAT3 activations in experimental intracerebral hemorrhage. J. Neurochem. 96:1728-1739; 2006.
69. Zhan, X.; Li, D.; Johns, R. A. Expression of endothelial nitric oxide synthase in ciliated epithelia of rats. J. Histochem. Cytochem. 51:81-87; 2003.
70. Yoshitomi, H.; Xu, Q.; Gao, M.; Yamori, Y. Phosphorylated endothelial NOS Ser1177 via the PI3K/Akt pathway is depressed in the brain of stroke-prone spontaneously hypertensive rat. J. Stroke Cerebrovasc. Dis 20:406-412; 2011.
71. Sastry, K. V.; Moudgal, R. P.; Mohan, J.; Tyagi, J. S.; Rao, G. S. Spectrophotometric determination of serum nitrite and nitrate by copper-cadmium alloy. Anal. Biochem. 306:79-82; 2002.
72. Mathis, D. M.; Furman, J. L.; Norris, C. M. Preparation of acute hippocampal slices from rats and transgenic mice for the study of synaptic alterations during aging and amyloid pathology. J. Vis. Exp ; 2011.
73. Norris, C. M.; Scheff, S. W. Recovery of afferent function and synaptic strength in hippocampal CA1 following traumatic brain injury. J. Neurotrauma 26:2269-2278; 2009.
74. Pierce, J. E.; Smith, D. H.; Trojanowski, J. Q.; McIntosh, T. K. Enduring cognitive, neurobehavioral and histopathological changes persist for up to one year following severe experimental brain injury in rats. Neuroscience 87:359-369; 1998.
75. Shapira, M.; Licht, A.; Milman, A.; Pick, C. G.; Shohami, E.; Eldar-Finkelman, H. Role of glycogen synthase kinase-3beta in early depressive behavior induced by mild traumatic brain injury. Mol. Cell. Neurosci. 34:571-577; 2007.
76. Tejada-Simon, M. V.; Serrano, F.; Villasana, L. E.; Kanterewicz, B. I.; Wu, G. Y.; Quinn, M. T.; Klann, E. Synaptic localization of a functional NADPH oxidase in the mouse hippocampus. Mol. Cell. Neurosci. 29:97-106; 2005.
77. Singh, I. N.; Sullivan, P. G.; Deng, Y.; Mbye, L. H.; Hall, E. D. Time course of posttraumatic mitochondrial oxidative damage and dysfunction in a mouse model of focal traumatic brain injury: implications for neuroprotective therapy. J. Cereb. Blood Flow Metab. 26:1407-1418; 2006.
78. Kuhlmann, C. R.; Tamaki, R.; Gamerdinger, M.; Lessmann, V.; Behl, C.; Kempski, O. S.; Luhmann, H. J. Inhibition of the myosin light chain kinase prevents hypoxia-induced blood-brain barrier disruption. J. Neurochem. 102:501-507; 2007.
79. Mohazzab, K. M.; Kaminski, P. M.; Wolin, M. S. NADH oxidoreductase is a major source of superoxide anion in bovine coronary artery endothelium. Am. J. Physiol. 266:H2568-H2572; 1994.
80. Shin, H. K.; Hong, K. W. Importance of calcitonin gene-related peptide, adenosine and reactive oxygen species in cerebral autoregulation under normal and diseased conditions. Clin. Exp. Pharmacol. Physiol. 31:1-7; 2004.
81. Hsieh, H. L.; Lin, C. C.; Shih, R. H.; Hsiao, L. D.; Yang, C. M. NADPH oxidase-mediated redox signal contributes to lipoteichoic acid-induced MMP-9 upregulation in brain astrocytes. J. Neuroinflammation 9:110; 2012.
82. Hsieh,H. L.;Wang, H. H.;Wu, C. Y.; Yang, C. M. Reactive oxygen species-dependent c-Fos/activator protein 1 induction upregulates heme oxygenase-1 expression by bradykinin in brain astrocytes. Antioxid. Redox Signal. 13:1829-1844; 2010.
83. Wu, D. M.; Lu, J.; Zheng, Y. L.; Zhang, Y. Q.; Hu, B.; Cheng,W.; Zhang, Z. F.; Li, M. Q. Small interfering RNA-mediated knockdown of protein kinase C zeta attenuates domoic acid-induced cognitive deficits in mice. Toxicol. Sci. 128:209-222; 2012.
84. Chern, C. M.; Liou, K. T.; Wang, Y. H.; Liao, J. F.; Yen, J. C.; Shen, Y. C. Andrographolide inhibits PI3K/AKT-dependent NOX2 and iNOS expression protecting mice against hypoxia/ischemia-induced oxidative brain injury. Planta Med. 77:1669-1679; 2011.
85. Grzybicki, D.; Moore, S. A.; Schelper, R.; Glabinski, A. R.; Ransohoff, R. M.; Murphy, S. Expression of monocyte chemoattractant protein (MCP-1) and nitric oxide synthase-2 following cerebral trauma. Acta Neuropathol. 95:98-103; 1998.
86. Egea, J.; Martin-de-Saavedra, M. D.; Parada, E.; Romero, A.; Del Barrio, L.; Rosa, A. O.; Garcia, A. G.; Lopez, M. G. Galantamine elicits neuroprotection by inhibiting iNOS, NADPH oxidase and ROS in hippocampal slices stressed with anoxia/reoxygenation. Neuropharmacology 62:1082-1090; 2012.
87. Jin, R.; Song, Z.; Yu, S.; Piazza, A.; Nanda, A.; Penninger, J. M.; Granger, D. N.; Li, G. Phosphatidylinositol-3-kinase gamma plays a central role in blood-brain barrier dysfunction in acute experimental stroke. Stroke 42:2033-2044; 2011.
88. Hwang, J. J.; Choi, S. Y.; Koh, J. Y. The role of NADPH oxidase, neuronal nitric oxide synthase and poly(ADP ribose) polymerase in oxidative neuronal death induced in cortical cultures by brain-derived neurotrophic factor and neurotrophin- 4/5. J. Neurochem. 82:894-902; 2002.
89. Kim, S. M.; Byun, J. S.; Jung, Y. D.; Kang, I. C.; Choi, S. Y.; Lee, K. Y. The effects of oxygen radicals on the activity of nitric oxide synthase and guanylate cyclase. Exp. Mol. Med. 30:221-226; 1998.
90. Fabian, R. H.; Perez-Polo, J. R.; Kent, T. A. Perivascular nitric oxide and superoxide in neonatal cerebral hypoxia-ischemia. Am. J. Physiol. Heart Circ. Physiol 295:H1809-H1814; 2008.
91. Kandasamy, R.; Kanti Pal, H.; Swamy, M.; Abdullah, J. Cerebrospinal fluid nitric oxide metabolite levels as a biomarker in severe traumatic brain injury. Int. J. Neurosci. 123:385-391; 2013.
92. Stoffel, M.; Rinecker, M.; Plesnila, N.; Eriskat, J.; Baethmann, A. Role of nitric oxide in the secondary expansion of a cortical brain lesion from cold injury. J. Neurotrauma 18:425-434; 2001.
93. Campese, V. M.; Sindhu, R. K.; Ye, S.; Bai, Y.; Vaziri, N. D.; Jabbari, B. Regional expression of NO synthase, NAD(P)H oxidase and superoxide dismutase in the rat brain. Brain Res. 1134:27-32; 2007.
94. Vallance, P.; Collier, J.; Moncada, S. Effects of endothelium-derived nitric oxide on peripheral arteriolar tone in man. Lancet 2:997-1000; 1989.