Microglial activation as a compelling target for treating acute traumatic brain injury

Current Medicinal Chemistry

Volumn 22, Issue 6, 2015, Pages 759-770

  Chio, Chung Ching ^a   Lin, Mao Tsun ^a   Chang, Ching Ping ^a  

^a SOUTHERN TAIWAN UNIVERSITY OF SCIENCE AND TECHNOLOGY   (Taiwan)

Author keywords

Brain; Cytokines; Free radicals; Microglia; Traumatic injury

Indexed keywords

2 CHLORO 5 HYDROXYPHENYLGLYCINE; AGMATINE; CENTRAL NERVOUS SYSTEM AGENTS; ERYTHROPOIETIN; ETANERCEPT; INTERLEUKIN 10; METABOTROPIC RECEPTOR 5; MNOZAC; NICOTINAMIDE ADENINE DINUCLEOTIDE ADENOSINE DIPHOSPHATE RIBOSYLTRANSFERASE 1; NICOTINAMIDE ADENINE DINUCLEOTIDE ADENOSINE DIPHOSPHATE RIBOSYLTRANSFERASE INHIBITOR; SIMVASTATIN; TROFINETIDE; TUMOR NECROSIS FACTOR ALPHA; TUMOR NECROSIS FACTOR RECEPTOR 1; UNCLASSIFIED DRUG;

ARTICLE; BRAIN CONTUSION; BRAIN REGION; BRAIN SIZE; CELL ACTIVATION; CELL COMMUNICATION; CELL CULTURE; CELL DIFFERENTIATION; CELL MATURATION; CELL SURVIVAL; CLINICAL EFFECTIVENESS; CLINICAL EVALUATION; COGNITION; COOLING; CYTOKINE PRODUCTION; DISEASE SEVERITY; ENZYME ACTIVATION; HUMAN; HYPERBARIC OXYGEN; MESENCHYMAL STEM CELL; MICROGLIA; NERVE REGENERATION; NERVOUS SYSTEM DEVELOPMENT; NEUROLOGIC DISEASE; NONHUMAN; PHAGOCYTE; STEM CELL TRANSPLANTATION; TRAUMATIC BRAIN INJURY; ACUTE DISEASE; ANIMAL; BRAIN INJURIES; DRUG EFFECTS; METABOLISM; MOLECULARLY TARGETED THERAPY; PATHOLOGY; PROCEDURES;

ACUTE DISEASE; ANIMALS; BRAIN INJURIES; HUMANS; MICROGLIA; MOLECULAR TARGETED THERAPY;

EID: 84931272233     PISSN: 09298673     EISSN: 1875533X     Source Type: Journal    
DOI: 10.2174/0929867321666141106124657     Document Type: Article

References (128)

1. Williams, A.J.; Hartings, J.A.; Lu, X.C.; Rolli, M.L.; Dave, J.R.; Tortella, F.C. Characterization of a new rat model of penetrating ballistic brain injury. J. Neurotrauma, 2005, 22, 313-331.
2. Wei, H.H.; Lu, X.C.; Shear, D.A.; Waghray, A.; Yao, C.; Tortella, F.C.; Dave, J.R. NNZ-2566 treatment inhibits neuroinflammation and pro-inflammatory cytokine expression induced by experimental penetrating ballistic-like brain injury in rats. J. Neuroinflam., 2009, 6, 19-29.
3. Chio, C.C.; Kuo, J.R.; Hsiao, S.H.; Chang, C.P.; Lin, M.T. Effect of brain cooling on brain ischemia and damage markers after fluid percussion brain injury in rats. Shock, 2007, 28, 284-290.
4. Lawson, L.J.; Perry, V.H.; Gordon, S. Turnover of resident microglia in the normal adult mouse brain. Neuroscience, 1992, 48, 405-415.
5. Xu, H.; Chen, M.; Mayer, E.J.; Forrester, J.V.; Dick, A.D. Turnover of resident retinal microglia in the normal adult mouse. Glia, 2007, 55, 1189-1198.
6. Long, J.M.; Kalehua, A.N.; Muth, N.J.; Calhoun, M.E.; Jucker, M.; Hengemihle, J.M.; Ingram, D.K.; Mouton, P.R. Stereological analysis of astrocyte and microglia in aging mouse hippocampus. Neurobiol. Aging, 1998, 19, 497-503.
7. Vaughan, D.W.; Peters, A. Neuroglial cells in the cerebral cortex of rats from young adulthood to old age: An electron microscope study. J. Neurocytol., 1974, 3, 405-429.
8. Tremblay, M.È.; Zettel, M.L.; Ison, J.R.; Allen, P.D.; Majewska, A.K. Effects of aging and sensory loss on glial cells in mouse visual and auditory cortices. Glia, 2012, 60, 541-558.
9. Damani, M.R.; Zhao, L.; Fontainhas, A.M.; Amaral, J.; Fariss, R.N.; Wong, W.T. Age-related alterations in the dynamic behavior of microglia. Aging Cell, 2011, 10, 263-276.
10. Mosher, K.I.; Wyss-Coray, T. Microglial dysfunction in brain aging and Alzheimer's disease. Biochem. Pharmacol., 2014, 88, 594-604.
11. Walker, F.R.; Beynon, S.B.; Jones, K.A.; Zhao, Z.; Kongsui, R.; Cairns, M.; Nilsson, M. Dynamic structural remodelling of microglia in health and disease: A review of the models, the signals and the mechanisms. Brain Behav. Immun., 2014, 37C, 1-14.
12. Hernandez-Ontiveros, D.G.; Tajiri, N.; Acosta, S.; Giunta, B.; Tan, J.; Borlongan, C.V. Microglia activation as a biomarker for traumatic brain injury. Front. Neurol., 2013, 4, 30.
13. Rivest, S. Regulation of innate immune responses in the brain. Nat. Rev. Immunol., 2009, 9, 429-439.
14. d'Avila, J.C.; Lam, T.I.; Bingham, D.; Shi, J.; Won, S.J.; Kauppinen, T.M.; Massa, S.; Liu, J.; Swanson, R.A. Microglial activation induced by brain trauma is suppressed by post-injury treatment with a PARP inhibitor. J. Neuroinflam., 2012, 9, 31.
15. Lucas, S.M.; Rothwell, N.J.; Gibson, R.M. The role of inflammation in CNS injury and disease. Br. J. Pharmacol., 2006, 147, S232-S240.
16. Vilhardt, F. Microglia: phagocyte and glia cell. Int. J. Biochem. Cell Biol., 2005, 37, 17-21.
17. Chio, C.C.; Lin, J.W.; Chang, M.W.; Wang, C.C.; Kuo, J.R.; Yang, C.Z.; Chang, C.P. Therapeutic evaluation of etanercept in a model of traumatic brain injury. J. Neurochem., 2010, 115, 921-929.
18. Davalos, D.; Grutzendler, J.; Yang, G.; Kim, J.V.; Zuo, Y.; Jung, S.; Littman, D.R.; Dustin, M.L.; Gan, W.B. ATP mediates rapid microglial response to local brain injury in vivo. Nat. Neurosci., 2005, 8, 752-758.
19. Cheong, C.U.; Chang, C.P.; Chao, C.M.; Cheng, B.C.; Yang, C.Z.; Chio, C.C. Etanercept attenuates traumatic brain injury in rats by reducing brain TNF-contents and by stimulating newly formed neurogenesis. Mediators Inflamm., 2013, 2013, 620837.
20. Meda, L.; Cassatella, M.A.; Szendrei, G.I.; Otvos L, Jr.; Baron, P.; Villalba, M.; Ferrari, D.; Rossi, F. Activation of microglial cells by beta-amyloid protein and interferon-gamma. Nature, 1995, 374, 647-650.
21. Bezzi, P.; Volterra, A. A neuron-glia signalling network in the active brain. Curr. Opin. Neurobiol., 2001, 11, 387-394. Review.
22. Perry, S.W.; Dewhurst, S.; Bellizzi, M.J.; Gelbard, H.A. Tumor necrosis factor-alpha in normal and diseased brain: Conflicting effects via intraneuronal receptor crosstalk? J. Neurovirol., 2002, 8, 611-624.
23. Shohami, E.; Novikov, M.; Bass, R.; Yamin, A.; Gallily, R. Closed head injury triggers early production of TNF and IL-6 by brain tissue. J. Cereb. Blood Flow Metab., 1994, 14, 615-619.
24. Taupin, V.; Toulmond, S.; Serrano, A.; Benavides, J.; Zavala, F. Increase in IL-6, IL-1 and TNF levels in rat brain following traumatic lesion. Influence of pre-and post-traumatic treatment with Ro5 4864, a peripheral-type (p site) benzodiazepine ligand. J. Neuroimmunol., 1993, 42, 177-185.
25. Yakovlev, A.G..; Faden, A.I. Molecular strategies in CNS injury. J. Neurotrauma, 1995, 12, 767-777.
26. Fan, L.; Young, P.R.; Barone, F.C.; Feverstein, G..Z.; Smith, D.H.; McIntosh, T.K. Experimental brain injury induces differential expression of tumor necrosis factor-alpha mRNA in the CNS. Mol. Brain Res., 1996, 36, 287-291.
27. Knoblach, S.M.; Fan, L.; Faden, A.I. Early neuronal expression of tumor necrosis factor-alpha after experimental brain injury contributes to neurological impairment. J. Neuroimmunol., 1999, 95, 115-125.
28. Chio, C.C.; Chang, C.H.; Wang, C.C.; Cheong, C.U.; Chao, C.M.; Cheng, B.C.; Yang, C.Z.; Chang, C.P. Etanercept attenuates traumatic brain injury in rats by reducing early microglial expression of tumor necrosis factor. BMC Neurosci., 2013, 14, 33.
29. McCoy, M.K.; Tansey, M.G. TNF signaling inhibition in the CNS: implications for normal brain function and neurodegenerative disease. J. Neuroinflam., 2008, 5, 45.
30. Iosif, R.E.; Ahlenius, H.; Ekdahl, C.T.; Darsalia, V.; Thored, P.; Jovinge, S.; Kokaia, Z.; Lindvall, O. Suppression of stroke-induced progenitor proliferation in adult subventricular zone by tumor necrosis factor receptor 1. J. Cereb. Blood Flow Metab., 2008, 28, 1574-1587.
31. Scherbel, U.; Raghupathi, R.; Nakamura, M.; Saatman, K.; McIntosh, T.K. Evaluation of neurobehavioral deficits in brain-injured tumor necrosis factor-dificent (TNF-1) mice after experimental brain injury. J. Neurotrauma, 1997, 14, 781.
32. Oshima, T.; Lee, S.; Sato, A.; Oda, S.; Hirasawa, H.; Yamashita, T. TNF-alpha contributes to axonal sprouting and functional recovery following traumatic brain injury. Brain Res., 2009, 1290, 102-110.
33. Chirumamilla, S.; Sun, D.; Bullock, M.R.; Colello, R.J. Traumatic brain injury induced cell proliferation in the adult mammalian central nervous system. J. Neurotrauma, 2002, 19, 693-703.
34. Rice, A.C.; Khaldi, A.; Harvey, H.B.; Salman, N.J.; White, F.; Fillmore, H.; Bullock, M.R. Proliferation and neuronal differentiation of mitotically active cells following traumatic brain injury. Exp. Neurol., 2003, 183, 406-417.
35. Itoh, T.; Satou, T.; Nishida, S.; Hashimoto, S.; Ito, H. Immature and mature neurons coexist among glial scars after rat traumatic brain injury. Neurol. Res., 2007, 29, 734-742.
36. Azbill, R.D.; Mu, X.; Bruce-Keller, A.J.; Mattson, M.P.; Springer, J.E. Impaired mitochondrial function, oxidative stress and altered antioxidant enzyme activities following traumatic spinal cord injury. Brain Res., 1997, 765, 283-290.
37. Kawamata, T.; Katayama, Y.; Hovda, D.A.; Yoshino, A.; Becker, D.P. Lactate accumulation following concussive brain injury: The role of ionic fluxes induced by excitatory amino acids. Brain Res., 1995, 674, 196-204.
38. Xiong, Y.; Gu, Q.; Peterson, P.L.; Muizelaar, J.P.; Lee, C.P. Mitochondrial dysfunction and calcium perturbation induced by traumatic brain injury. J. Neurotrauma, 1997, 14, 23-34.
39. Gage, F.H. Mammalian neural stem cells. Science, 2000, 287, 1433-1438.
40. Mckay, R. Stem cells in the central nervous system. Science, 1997, 276, 66-71.
41. Brown, J.P.; Couillard-Després, S.; Cooper-Kuhn, C.M.; Winkler, J.; Aigner, L.; Kuhn, H.G. Transient expression of doublecortin during adult neurogenesis. J. Comp. Neurol., 2003, 467, 1-10.
42. Nacher, J.; Crespo, C.; McEwen, B.S. Doublecortin expression in the adult rat telencephalon. Eur. J. Neurosci., 2001, 14, 629-644.
43. Couillard-Despres, S.; Winner, B.; Schaubeck, S.; Aigner, R.; Vroemen, M.; Weidner, N.; Bogdahn, U.; Winkler, J.; Kuhn, H.G.; Aigner, L. Doublecortin expression levels in adult brain reflect neurogenesis. Eur. J. Neurosci., 2005, 21, 1-14.
44. Chiaretti, A.; Antonelli, A.; Genovese, O.; Pezzotti, P.; Rocco, C.D.; Viola, L.; Riccardi, R. Nerve growth factor and doublecortin expression correlates with improved outcome in children with severe traumatic brain injury. J. Trauma, 2008, 65, 80-85.
45. Rola, R.; Mizumatsu, S.; Otsuka, S.; Morhardt, D.R.; Noble-Haeusslein, L.J.; Fishman, K.; Potts, M.B.; Fike, J.R. Alterations in hippocampal neurogenesis following traumatic brain injury in mice. Exp. Neurol., 2006, 202, 189-199.
46. Elliott, M.J.; Maini, R.N.; Feldmann, M.; Long-Fox, A.; Charles, P.; Katsikis, P.; Brennan, F.M.; Walker, J.; Bijl, H.; Ghrayeb, J.; Woody, J.N. Treatment of rheumatoid arthritis with chimeric monoclonal antibodies to tumor necrosis factor alpha. Arthritis Rheum., 1993, 36, 1681-1690.
47. Bell, S.; Kamm, M.A. Antibodies to tumor necrosis factor alpha as treatment for crohn's disease. Lancet, 2000, 355, 858-860.
48. Zou, J.X.; Braun, J.; Sieper, J. Immunological basis for the use of TNFalpha-blocking agents in ankylosing spondylitis and immunological changes during treatment. Clin. Exp. Rheumatol., 2002, 20, S34-S37.
49. Howarth, P.H.; Babu, K.S.; Arshad, H.S.; Lau, L.; Buckley, M.; McConnell, W.; Beckett, P.; Al Ali. M.; Chauhan, A.; Wilson, S.J.; Reynolds, A.; Davies, D.E.; Holgate, S.T. Tumour necrosis factor (TNFalpha) as a novel therapeutic target in symptomatic corticosteroid dependent asthma. Thorax, 2005, 60, 1012-1018.
50. Forrest, E.H.; Oien, K.A.; Dickson, S.; Galloway, D.; Mills, P.R. Improvement in cholestasis associated with total parenteral nutrition after treatment with an antibody against tumour necrosis factor alpha. Liver, 2002, 22, 317-320.
51. Francis, J.; Chu, Y.; Johnson, A.K.; Weiss, R.M.; Felder, R.B. Acute myocardial infarction induces hypothalamic cytokine synthesis. Am. J. Physiol. Heart Circ. Physiol., 2004, 286, H2264-H2271.
52. Genovese, T.; Mazzon, E.; Crisafulli, C.; Di Paola, R.; Muià, C.; Bramanti, P.; Cuzzocrea, S. Immunomodulatory effects of etanercept in an experimental model of spinal cord injury. J. Pharmacol. Exp. Ther., 2006, 316, 1006-1016.
53. Hosomi, N.; Ban, C.R.; Naya, T.; Takahashi, T.; Guo, P.; Song, X.Y.; Kohno, M. Tumor necrosis factor-alpha neutralization reduced cerebral edema through inhibition of matrix metalloproteinase production after transient focal cerebral ischemia. J. Cereb. Blood Flow Metab., 2005, 25, 959-967.
54. Caso, J.R.; Lizasoain, I.; Lorenzo, P.; Moro, M.A.; Leza, J.C. The role of tumor necrosis factor-alpha in stress-induced worsening of cerebral ischemia in rats. Neuroscience, 2006, 142, 59-69.
55. Campbell, S.J.; Jiang, Y.; Davis, A.E.; Farrands, R.; Holbrook, J.; Leppert, D.; Anthony, D.C. Immunomodulatory effects of etanercept in a model of brain injury act through attenuation of the acutephase response. J. Neurochem., 2007, 103, 2245-2255.
56. Chio, C.C.; Kuo, J.R.; Hsiao, S.H.; Chang, C.P.; Lin, M.T. Effect of brain cooling on brain ischemia and damage markers after fluid percussion brain injury in rats. Shock, 2007, 28, 284-290.
57. Kuo, J.R.; Lo, C.J.; Chio, C.C.; Chang, C.P.; Lin, M.T. Resuscitation from experimental traumatic brain injury by agmatine therapy. Resuscitation, 2007, 75, 506-514.
58. Chen, S.H.; Chang, C.Y.; Chang, H.K.; Chen, W.C.; Lin, M.T.; Wang, J.J.; Chen, J.C.; Chang, F.M. Premarin stimulates estrogen receptor-alpha to protect against traumatic brain injury in male rats. Crit. Care Med., 2009, 37, 3097-3106.
59. Lindvall, O.; Kokaia, Z.; Martinez-Serrano, A. Stem cell therapy for human neurodegenerative disorders-how to make it work. Nat. Med., 2004, 10, S42-S50.
60. Taguchi, A.; Soma, T.; Tanaka, H.; Kanda, T.; Nishimura, H.; Yoshikawa, H.; Tsukamoto, Y.; Iso, H.; Fujimori, Y.; Stern, D.M.; Naritomi, H.; Matsuyama, T. Administration of CD34+ cells after stroke enhances neurogenesis via angiogenesis in a mouse model. J. Clin. Invest., 2004, 114, 330-338.
61. Chen, S.H.; Chang, F.M.; Tsai, Y.C.; Huang, K.F.; Lin, M.T. Resuscitation from experimental heatstroke by transplantation of human umbilical cord blood cells. Crit. Care Med., 2005, 33, 1377-1383.
62. Chen, J.; Sanberg, P.R.; Li, Y.; Wang, L.; Lu, M.; Willing, A.E.; Sanchez-Ramos, J.; Chopp, M. Intravenous administration of human umbilical cord blood reduces behavioral deficits after stroke in rats. Stroke, 2001, 32, 2682-2688.
63. Willing, A.E.; Vendrame, M.; Mallery, J.; Cassady, C.J.; Davis, C.D.; Sanchez-Ramos, J.; Sanberg, P.R. Mobilized peripheral blood cells administered intravenously produce functional recovery in stroke. Cell Transplant., 2003, 12, 449-454.
64. Saporta, S.; Kim, J.J.; Willing, A.E.; Fu, E.S.; Davis, C.D.; Sanberg, P.R. Human umbilical cord blood stem cells infusion in spinal cord injury: engraftment and beneficial influence on behavior. J. Hematother. Stem Cell Res., 2003, 12, 271-278.
65. Lu, D.; Sanberg, P.R.; Mahmood, A.; Li, Y.; Wang, L.; Sanchez-Ramos, J.; Chopp, M. Intravenous administration of human umbilical cord blood reduces neurological deficit in the rat after traumatic brain injury. Cell Transplant., 2002, 11, 275-281.
66. Chen, S.H.; Wang, J.J.; Chen, C.H.; Chang, H.K.; Lin, M.T.; Chang, F.M.; Chio, C.C. Umbilical cord blood-derived CD34+ cells improve outcomes of traumatic brain injury in rats by stimulating angiogenesis and neurogenesis. Cell Transplant., 2014, 23, 959-979.
67. Mahmood, A.; Lu, D.; Chopp, M. Intravenous administration of marrow stromal cells (MSCs) increases the expression of growth factors in rat brain after traumatic brain injury. J. Neurotrauma, 2004, 21, 33-39.
68. Kim, H.J.; Lee, J.H.; Kim, S.H. Therapeutic effects of human mesenchymal stem cells on traumatic brain injury in rats: secretion of neurotrophic factors and inhibition of apoptosis. J. Neurotrauma, 2010, 27, 131-138.
69. Kinnaird, T.; Stabile, E.; Burnett, M.S.; Lee, C.W.; Barr, S.; Fuchs, S.; Epstein, S.E. Marrow-derived stromal cells express genes encoding a broad spectrum of arteriogenic cytokines and promote in vitro and in vivo arteriogenesis through paracrine mechanisms. Circ. Res., 2004, 94, 678-685.
70. Chio, C.C.; Chang, C.P.; Lin, M.T. Hypoxic preconditioning enhances the potentially therapeutic secretome from cultured human mesenchymal stem cells in experimental traumatic brain injury. Science, 2012, 338(6113): 1485 (Suppl) 59-60.
71. Chang, C.P.; Chio, C.C.; Cheong, C.U.; Chao, C.M.; Cheng, B.C.; Lin, M.T. Hypoxic preconditioning enhances the therapeutic potential of the secretome from cultured human mesenchymal stem cells in experimental traumatic brain injury. Clin. Sci. (Lond), 2013, 124, 165-176.
72. Daugherty, W.P.; Levasseur, J.E.; Sun, D.; Rockswold, G.L.; Bullock, M.R. Effects of hyperbaric oxygen therapy on cerebral oxygenation and mitochondrial function following moderate lateral fluid-percussion injury in rats. J. Neurosurg., 2004, 101, 499-504.
73. Palzur, E.; Zaaroor, M.; Vlodavsky, E.; Milman, F.; Soustiel, J.F. Neuroprotective effect of hyperbaric oxygen therapy in brain injury is mediated by preservation of mitochondrial membrane properties. Brain Res., 2008, 1221, 126-133.
74. Ren, H.; Wang, W.; Ge, Z. Glasgow Coma Scale, brain electric activity mapping and Glasgow Outcome Scale after hyperbaric oxygen treatment of severe brain injury. Chin. J. Traumatol., 2001, 4, 239-241.
75. Rockswold, S.B.; Rockswold, G.L.; Vargo, J.M.; Erickson, C.A.; Sutton, R.L.; Bergman, T.A.; Biros, M.H. Effects of hyperbaric oxygenation therapy on cerebral metabolism and intracranial pressure in severely brain injured patients. J. Neurosurg., 2001, 94, 403-411.
76. Niklas, A.; Brock, D.; Schober, R.; Schulz, A.; Schneider, D. Continuous measurements of cerebral tissue oxygen pressure during hyperbaric oxygenation-HBO effects on brain edema and necrosis after severe brain trauma in rabbits. J. Neurol. Sci., 2004, 219, 77-82.
77. Tinianow, C.L.; Tinianow, T.K.; Wilcox, M. Effects of hyperbaric oxygen on focal brain contusions. Biomed. Sci. Instrum., 2000, 36, 275-281.
78. Vlodavsky, E.; Palzur, E.; Soustiel, J.F. Hyperbaric oxygen therapy reduces neuroinflammation and expression of matrix metalloproteinase-9 in the rat model of traumatic brain injury. Neuropathol. Appl. Neurobiol., 2006, 32, 40-50.
79. Zhou, Z.; Daugherty, W.P.; Sun, D.; Levasseur, J.E.; Altememi, N.; Hamm, R.J.; Rockswold, G.L.; Bullock, M.R. Protection of mitochondrial function and improvement in cognitive recovery in rats treated with hyperbaric oxygen following lateral fluid-percussion injury. J. Neurosurg., 2007, 106, 687-694.
80. Wang, G.H.; Zhang, X.G.; Jiang, Z.L.; Li, X.; Peng, L.L.; Li, Y.C.; Wang, Y. Neuroprotective effects of hyperbaric oxygen treatment on traumatic brain injury in the rat. J. Neurotrauma, 2010, 27, 1733-1743.
81. Lin, K.C.; Niu, K.C.; Tsai, K.J.; Kuo, J.R.; Wang, L.C.; Chio, C.C.; Chang, C.P. Attenuating inflammation but stimulating both angiogenesis and neurogenesis using hyperbaric oxygen in rats with traumatic brain injury. J. Trauma Acute Care Surg., 2012, 72, 650-659.
82. Clifton, G.L.; Miller, E.R.; Choi, S.C.; Levin, H.S.; McCauley, S.R.; Smith, K.R.; Muizellar, J.P.; Marion, D.W.; Luerssen, T.G. Hypothermia on admission in patients with severe brain injury. J. Neurotrauma, 2002, 19, 293-301.
83. Markgraf, C.G.; Clifton, G.L.; Moody, M.R. Treatment window for hypothermia in brain injury. J. Neurosurg, 2001, 95, 979-983.
84. Wen, Y.S.; Huang, M.S.; Lin, M.T.; Lee, C.H. Rapid brain cooling by hypothermic retrograde jugular vein flush. J. Trauma, 2005, 58, 577-581.
85. Kuo, J.R.; Lo, C.J.; Chang, C.P.; Lin, M.T.; Chio, C.C. Attenuation of brain nitrostative and oxidative damage by brain cooling during experimental traumatic brain injury. J. Biomed. Biotechnol., 2011, 2011, 145214.
86. Kuo, J.R.; Lo, C.J.; Chang, C.P.; Lin, H.J.; Lin, M.T.; Chio, C.C. Brain cooling-stimulated angiogenesis and neurogenesis attenuated traumatic brain injury in rats. J. Trauma, 2010, 69, 1467-1472.
87. Tsuji, M.; Higuchi, Y.; Shiraishi, K.; Kume, T.; Akaike, A.; Hattori, H. Protective effect of aminoguanidine on hypoxicischemic brain damage and temporal profile of brain nitric oxide in neonatal rat. Pediatr. Res., 2000, 47, 79-83.
88. Cai, Z.; Xiao, F.; Fratkin, J.D.; Rhodes, P.G. Protection of neonatal rat brain from hypoxic-ischemic injury by LY379268, a Group II metabotropic glutamate receptor agonist. Neuroreport, 1999, 10, 3927-3931.
89. Yang, X.C.; Reis, D.J. Agmatine selectively blocks the N-methyl-D-aspartate subclass of glutamate receptor channels in rat hippocampal neurons. J. Pharmacol. Exp. Ther., 1999, 288, 544-549.
90. Olmos, G.; DeGregorio-Rocasolano, N.; Paz Regalado, M.; Gasull, T.; Assumpció Boronat, M.; Trullas, R.; Villarroel, A.; Lerma, J.; García-Sevilla, J.A. Protection by imidazol(ine) drugs and agmatine of glutamate-induced neurotoxicity in cultured cerebellar granule cells through blockade of NMDA receptor. Br. J. Pharmacol., 1999, 127, 1317-1326.
91. Gilad, G.M.; Salame, K.; Rabey, J.M.; Gilad, V.H. Agmatine treatment is neuroprotective in rodent brain injury models. Life Sci., 1996, 58, PL41-PL46.
92. Yu, C.G.; Marcillo, A.E.; Fairbanks, C.A.; Wilcox, G.L.; Yezierski, R.P., Agmatine improves locomotor function and reduces tissue damage following spinal cord injury. Neuroreport, 2000, 11, 3203-3207.
93. Kuo, J.R.; Lo, C.J.; Chang, C.P.; Lin, K.C.; Lin, M.; Chio, C.C. Agmatine-promoted angiogenesis, neurogenesis, and inhibition of gliosis-reduced traumatic brain injury in rats. J. Trauma, 2011, 71, E87-E93.
94. Somera-Molina, K.C.; Robin, B.; Somera, C.A.; Anderson, C.; Stine, C.; Koh, S.; Behanna, H.A.; Van Eldik, L.J.; Watterson, D.M.; Wainwright, M.S. Glial activation links early-life seizures and long-term neurologic dysfunction: evidence using a small molecule inhibitor of proinflammatory cytokine upregulation. Epilepsia, 2007, 48, 1785-1800.
95. Hu, W.; Ralay Ranaivo, H.; Roy, S.M.; Behanna, H.A.; Wing, L.K.; Munoz, L.; Guo, L.; Van Eldik, L.J.; Watterson, D.M. Development of a novel therapeutic suppressor of brain proinflammatory cytokine up-regulation that attenuates synaptic dysfunction and behavioral deficits. Bioorg. Med. Chem. Lett., 2007, 17, 414-418.
96. Lloyd, E.; Somera-Molina, K.; Van Eldik, L.J.; Watterson, D.M.; Wainwright, M.S. Suppression of acute proinflammatory cytokine and chemokine upregulation by post-injury administration of a novel small molecule improves long-term neurologic outcome in a mouse model of traumatic brain injury. J. Neuroinflam., 2008, 5, 28.
97. Moppett, I.K. Traumatic brain injury: Assessment, resuscitation and early management. Br. J. Anaesth., 2007, 99, 18-31.
98. Li, B.; Mahmood, A.; Lu, D.; Wu, H.; Xiong, Y.; Qu, C.; Chopp, M. Simvastatin attenuates microglial cells and astrocyte activation and decreases interleukin-1beta level after traumatic brain injury. Neurosurgery, 2009, 65, 179-186.
99. Lu, D.; Qu, C.; Goussev, A.; Jiang, H.; Lu, C.; Schallert, T.; Mahmood, A.; Chen, J.; Li, Y.; Chopp, M. Statins increase neurogenesis in the dentate gyrus, reduce delayed neuronal death in the hippocampal CA3 region, and improve spatial learning in rat after traumatic brain injury. J. Neurotrauma, 2007, 24, 1132-1146.
100. Alexi, T.; Hughes, P.E.; van Roon-Mom, W.M.; Faull, R.L.; Williams, C.E.; Clark, R.G.; Gluckman, P.D. The IGF-I aminoterminal tripeptide glycine-proline-glutamate (GPE) is neuroprotective to striatum in the quinolinic acid lesion animal model of Huntington's disease. Exp. Neurol., 1999, 159, 84-97.
101. Batchelor, D.C.; Lin, H.; Wen, J.Y.; Keven, C.; Van Ziji, P.L.; Breier, B.H.; Gluckman, P.D.; Thomas, G.B. Pharmacokinetics of glycin-proline-glutamate, the N-terminal tripeptide of insulin-like growth factor-1, in rats. Anal. Biochem., 2003, 323, 156-163.
102. Guan, J. Insulin-like growth factor-1 and its derivatives: potential pharmaceutical application for ischemic brain injury. Recent Patents CNS drug. Discov., 2008, 3, 112-127.
103. Lu, X.C.; Chen, R.W.; Yao, C.; Wei, H.; Yang, X.; Liao, Z.; Dave, J.R.; Tortella, F.C. NNZ-2566, a glypromate analog, improves functional recovery and attenuates apoptosis and inflammation in a rat model of penetrating ballistic-type brain injury. J. Neurotrauma, 2009, 26, 141-154.
104. Wei, H.H.; Lu, X.C.; Shear, D.A.; Waghray, A.; Yao, C.; Tortella, F.C.; Dave, J.R. NNZ-2566 treatment inhibits neuroinflammation and pro-inflammatory cytokine expression induced by experimental penetrating ballistic-like brain injury in rats. J. Neuroinflam., 2009, 6, 19.
105. Block, M.L.; Zecca, L.; Hong, J.S. Microglia-mediated neurotoxicity: uncovering the molecular mechanisms. Nat. Rev. Neurosci., 2007, 8, 57-69.
106. Aloisi, F. Immune function of microglia. Glia, 2001, 36, 165-179.
107. Block, M.L.; Hong, J.S. Microglia and inflammation-mediated neurodegeneration: multiple function of microglia. Prog. Neurobiol., 2005, 76, 77-98.
108. Loane, D.J.; Stoica, B.A.; Pajoohesh-Ganji, A.; Byrnes, K.R.; Faden, A.I. Activation of metabotropic glutamate receptor 5 modulates microglial reactivity and neurotoxicity by inhibiting NADPH oxidase. J. Biol. Chem., 2009, 284, 15629-15639.
109. Byrnes, K.R.; Stoica, B.; Loane, D.J.; Riccio, A.; Davis, M.I.; Faden, A.I. Metabotropic glutamate receptor 5 activation inhibits microglial associated inflammation and neurotoxicity. Glia, 2009, 57, 550-560.
110. Byrnes, K.R.; Stoica, B.; Riccio, A.; Pajoohesh-Ganji, A.; Loane, D.J.; Faden, A.I. Activation of metabotropic glutamate receptor 5 improves recovery after spinal cord injury in rodents. Ann. Neurol., 2009, 66, 63-74.
111. Byrnes, K.R.; Loane, D.J.; Stoica, B.A.; Zhang, J.; Faden, A.I. Delayed mGluR5 activation limits neuroinflammation and neurodegeneration after traumatic brain injury. J. Neuroinflam., 2012, 9, 43.
112. d'Avila, J.C.; Lam, T.I.; Bingham, D.; Shi, J.; Won, S.J.; Kauppinen, T.M.; Massa, S.; Liu, J.; Swanson, R.A. Microglial activation induced by brain trauma is suppressed by post-injury treatment with a PARP inhibitor. J. Neuroinflam., 2012, 9, 31-42.
113. Brines, M.L.; Ghezzi, P.; Keenan, S.; Agnello, D.; de Lanerolle, N.C.; Cerami, C.; Itri, L.M.; Cerami, A. Erythropoietin crosses the blood-brain barrier to protect against experimental brain injury. Proc. Natl. Acad Sci. U S A, 2000, 97, 10526-10531.
114. Cherian, L.; Goodman, C.J.; Robertson, C.S. Neuroprotection with erythropoietin administration following controlled cortical impact injury in rat. J. Pharmacol. Exp. Ther., 2007, 322, 789-794.
115. Lu, F.; Mshmoof, S.; Vhsnhdhrnh, Q.; Goussev, A.; Schallert, T.; Chopp, M. Erythropoietin enhances neurogenesis and restores spatial memory in rat after traumatic brain injury. J. Neurotrauma, 2005, 22, 1011-1017.
116. Marti, H.H.; Bernaudin, M.; Petit, E.; Bauer, C. Neuroprotection and Angiogenesis: Dual Role of Erythropoietin in Brain Ischemia. News Physiol. Sci., 2000, 15, 225-229.
117. Sirén, A.L.; Fratelli, M.; Brines, M.; Goemans, C.; Casagrande, S.; Lewczuk, P.; Keenan, S.; Gleiter, C.; Pasquali, C.; Capobianco, A.; Mennini, T.; Heumann, R.; Cerami, A.; Ehrenreich, H.; Ghezzi, P. Erythropoietin prevents neuronal apoptosis after cerebral ischemia and metabolic stress. Proc. Natl. Acad. Sci. U S A, 2001, 98, 4044-4049.
118. Villa, P.; Bigini, P.; Mennini, T.; Agnello, D.; Laragione, T.; Cagnotto, A.; Viviani, B.; Marinovich, M.; Cerami, A.; Coleman, T.R.; Brines, M.; Ghezzi, P. Erythropoietin selectively attenuates cytokine production and inflammation in cerebral ischemia by targeting neuronal apoptosis. J. Exp. Med., 2003, 198, 971-975.
119. Wang, L.; Zhang, Z.; Wang, Y.; Zhang, R.; Chopp, M. Treatment of stroke with erythropoietin enhances neurogenesis and angiogenesis and improves neurological function in rats. Stroke, 2004, 35, 1732-1737.
120. Yatsiv, I.; Grigoriadis, N.; Simeonidou, C.; Stahel, P.F.; Schmidt, O.I.; Alexandrovitch, A.G.; Tsenter, J.; Shohami, E. Erythropoietin is neuroprotective, improves functional recovery, and reduces neuronal apoptosis and inflammation in a rodent model of experimental closed head injury. FASEB J., 2005, 19, 1701-1703.
121. Robertson, C.S.; Garcia, R.; Gaddam, S.S.; Grill, R.J.; Hand, C.C.; Tian, T.S.; Hannay, H.J. Treatment of mild traumatic brain injury with an erythropoietin-mimetic peptide. J. Neurotrauma, 2013, 30, 765-774.
122. Brines, M.; Patel, N.S.; Villa, P.; Brines, C.; Mennini, T.; De Paola, M.; Erbayraktar, Z.; Erbayraktar, S.; Sepodes, B.; Thiemermann, C.; Ghezzi, P.; Yamin, M.; Hand, C.C.; Xie, Q.W.; Coleman, T.; Cerami, A. Nonerythropoietic, tissue-protective peptides derived from the tertiary structure of erythropoietin. Proc. Natl. Acad. Sci. U S A, 2008, 105, 10925-10930.
123. Wyss-Coray, T.; Mucke, L. Inflammation in neurodegenerative disease-a double-edged sword. Neuron, 2002, 35, 419-432.
124. Hernandez-Ontiveras, D.G.; Tajiri, N.; Acosta, S.; Giunta, B.; Tan, J.; Borlonga, C.V. Microglia activation as a biomarker for traumatic brain injury. Front. Neurol., 2013, 30, 1-9.
125. Yirmiya, R.; Goshen, I. Immune modulation of learning, memory, neural plasticity and neurogenesis. Brain Behav. Immun., 2011, 25, 181-213.
126. Das, S.; Basu, A. Inflammation: A new candidate in modulating adult neurogenesis. J. Neurosci. Res., 2008, 86, 1199-1208.
127. Ekdahl, C.T.; Kokaia, Z.; Lindvall, O. Brain inflammation and adult neurogenesis: The dual role of microglia. Neuroscience, 2009, 158, 1021-1029.
128. Welser, J.V.; Li, L.; Milner, R. Microglial activation state exerts a biphasic influence on brain endothelial proliferation by regulating the balance of TNF and TGF-1. J. Neuroinflam., 2010, 7, 89-96.