The role of neuroinflammation in traumatic brain injury

European Journal of Trauma

Volumn 30, Issue 3, 2004, Pages 135-149

  Schmidt, Oliver I ^a   Infanger, Manfred ^a   Heyde, Christoph E ^a   Ertel, Wolfgang ^a   Stahel, Philip F ^a  

^a CHARITÉ UNIVERSITÄTSMEDIZIN BERLIN   (Germany)

Author keywords

Blood brain barrier; Complement; Cytokines; Neuroinflammation; Secondary brain damage; Traumatic brain injury

Indexed keywords

CANNABINOID; CELL ADHESION MOLECULE; COMPLEMENT; CORTICOSTEROID; CYTOKINE; DEXANABINOL; FREE RADICAL;

ANTIINFLAMMATORY ACTIVITY; ANTIOXIDANT ACTIVITY; BLOOD BRAIN BARRIER; BRAIN EDEMA; BRAIN HYPOXIA; BRAIN INJURY; BRAIN PROTECTION; CLINICAL TRIAL; COMPLEMENT ACTIVATION; CORTICOSTEROID THERAPY; DEVELOPED COUNTRY; DRUG EFFICACY; HUMAN; HYPOTENSION; IMMUNOCOMPETENT CELL; INFLAMMATION; INTRACRANIAL HYPERTENSION; LEUKOCYTE MIGRATION; MEDIATOR RELEASE; NEUROINFLAMMATION; NEUROPATHOLOGY; NEUROTOXICITY; OXIDATIVE STRESS; REPERFUSION INJURY; RESUSCITATION; REVIEW; SECONDARY BRAIN INJURY; TISSUE REPAIR;

EID: 3042805103     PISSN: 14390590     EISSN: None     Source Type: Journal    
DOI: 10.1007/s00068-004-1394-9     Document Type: Review

References (196)

1. Firsching R, Woischneck D. Present status of neurosurgical trauma in Germany. World J Surg 2001;25:1221-3.
2. Bouillon B, Raum M, Fach H, et al. The incidence and outcome of severe brain trauma: design and first results of an epidemiological study in an urban area. Restor Neurol Neurosci 1999;14:85-92.
3. Kossmann T, Stahel PF. Closed head injury. In: Bland KI, Sarr MG, eds. The practice of general surgery. Philadelphia: Saunders, 2001:101-8.
4. Masson F, Thicoipe M, Aye P, et al. Epidemiology of severe brain injuries: a prospective population-based study. J Trauma 2001;51:481-9.
5. Andersson EH, Björklund R, Emanuelson I, et al. Epidemiology of traumatic brain injury: a population based study in western Sweden. Acta Neurol Scand 2003;107:256-9.
6. Engberg AW, Teasdale TW. Traumatic brain injury in Denmark 1979-1996. A national study of incidence and mortality. Eur J Epidemiol 2001;17:437-42.
7. Murray GD, Teasdale GM, Braakman R, et al. The European Brain Injury Consortium survey of head injuries. Acta Neurochir (Wien) 1999;141:223-36.
8. Eisenberg HM, Gary HE Jr, Aldrich EF, et al. Initial CT findings in 753 patients with severe head injury. A report from the NIH Traumatic Coma Data Bank. J Neurosurg 1990;73:688-98.
9. Bayir H, Clark RS, Kochanek PM. Promising strategies to minimize secondary brain injury after head trauma. Crit Care Med 2003;31:S112-7.
10. Chesnut RM, Marshall LF, Klauber MR, et al. The role of secondary brain injury in determining outcome from severe head injury. J Trauma 1993;34:216-22.
11. Golding EM. Sequelae following traumatic brain injury: the cerebrovascular perspective. Brain Res Rev 2002;38:377-88.
12. Wahl M, Schilling L, Unterberg A, et al. Mediators of vascular and parenchymal mechanisms in secondary brain damage. Acta Neurochir Suppl (Wien) 1993;57:64-72.
13. Rosomoff HL, Kochanek PM, Clark R, et al. Resuscitation from severe brain trauma. Crit Care Med 1996;24:S48-56.
14. Leker RR, Shohami E. Cerebral ischemia and trauma - different etiologies yet similar mechanisms: neuroprotective opportunities. Brain Res Rev 2002;39:55-73.
15. Farooqui AA, Yi Ong W, Lu XR, et al. Neurochemical consequences of kainate-induced toxicity in brain: involvement of arachidonic acid release and prevention of toxicity by phospholipase A(2) inhibitors. Brain Res Rev 2001;38:61-78.
16. Skaper SD, Floreani M, Ceccon M, et al. Excitotoxicity, oxidative stress, and the neuroprotective potential of melatonin. Ann N Y Acad Sci 1999;890:107-18.
17. Liou AK, Clark RS, Henshall DC, et al. To die or not to die for neurons in ischemia, traumatic brain injury and epilepsy: a review on the stress-activated signaling pathways and apoptotic pathways. Prog Neurobiol 2003;69:103-42.
18. Raghupathi R, Graham DI, McIntosh TK. Apoptosis after traumatic brain injury. J Neurotrauma 2000;17:927-38.
19. Bredesen DE. Apoptosis: overview and signal transduction pathways. J Neurotrauma 2000;17:801-10.
20. Neugebauer E, Hensler T, Rose S, et al. [Severe craniocerebral trauma in multiple trauma. An assessment of the interaction of local and systemic mediator responses.] Unfallchirurg 2000;103:122-31.
21. Shohami E, Beit-Yannai E, Horowitz M, et al. Oxidative stress in closed-head injury: brain antioxidant capacity as an indicator of functional outcome. J Cereb Blood Flow Metab 1997;17:1007-19.
22. Lu J, Moochhala S, Kaur C, et al. Cellular inflammatory response associated with breakdown of the blood-brain barrier after closed head injury in rats. J Neurotrauma 2001;18:399-408.
23. Kossmann T, Lenzlinger PM, Stover JF, et al. [Neurochemical changes and current pharmacological approaches in craniocerebral trauma.] Unfallchirurg 1997;100:613-22.
24. Morganti-Kossmann MC, Rancan M, Otto VI, et al. Role of cerebral inflammation after traumatic brain injury: a revisited concept. Shock 2001;16:165-77.
25. Stahel PF, Morganti-Kossmann MC, Kossmann T. The role of the complement system in traumatic brain injury. Brain Res Rev 1998;27:243-56.
26. Barnum SR. Complement in central nervous system inflammation. Immunol Res 2002;26:7-13.
27. Morgan BP, Gasque P, Singhrao S, et al. The role of complement in disorders of the nervous system. Immunopharmacology 1997;38:43-50.
28. Ransohoff RM. The chemokine system in neuroinflammation: an update. J Infect Dis 2002;186:Suppl 2:S152-6.
29. Feuerstein GZ, Wang X, Barone FC. The role of cytokines in the neuropathology of stroke and neurotrauma. Neuroimmunomodulation 1998;5:143-59.
30. Bayir H, Kagan VE, Tyurina YY, et al. Assessment of antioxidant reserves and oxidative stress in cerebrospinal fluid after severe traumatic brain injury in infants and children. Pediatr Res 2002;51:571-8.
31. Tyurin VA, Tyurina YY, Borisenko GG, et al. Oxidative stress following traumatic brain injury in rats: quantitation of biomarkers and detection of free radical intermediates. J Neurochem 2000;75:2178-89.
32. Schoettle RJ, Kochanek PM, Magargee MJ, et al. Early polymorphonuclear leukocyte accumulation correlates with the development of posttraumatic cerebral edema in rats. J Neurotrauma 1990;7:207-17.
33. Carlos TM, Clark RS, Franicola-Higgins D, et al. Expression of endothelial adhesion molecules and recruitment of neutrophils after traumatic brain injury in rats. J Leukoc Biol 1997;61:279-85.
34. Whalen MJ, Carlos TM, Dixon CE, et al. Reduced brain edema after traumatic brain injury in mice deficient in P-selectin and intercellular adhesion molecule-1. J Leukoc Biol 2000;67:160-8.
35. Shohami E, Gati I, Beit-Yannai E, et al. Closed head injury in the rat induces whole body oxidative stress: overall reducing antioxidant profile. J Neurotrauma 1999;16:365-76.
36. Morgan BP, Gasque P. Expression of complement in the brain: role in health and disease. Immunol Today 1996;17:461-6.
37. Hopkins SJ, Rothwell NJ. Cytokines and the nervous system. I: Expression and recognition. Trends Neurosci 1995;18:83-8.
38. Asensio VC, Campbell IL. Chemokines in the CNS: plurifunctional mediators in diverse states. Trends Neurosci 1999;22:504-12.
39. Ransohoff RM. Chemokines in neurological trauma models. Ann N Y Acad Sci 2002;961:346-9.
40. Shohami E, Ginis I, Hallenbeck JM. Dual role of tumor necrosis factor alpha in brain injury. Cytokine Growth Factor Rev 1999;10:119-30.
41. Scherbel U, Raghupathi R, Nakamura M, et al. Differential acute and chronic responses of tumor necrosis factor-deficient mice to experimental brain injury. Proc Natl Acad Sci U S A 1999;96:8721-6.
42. Merrill JE, Benveniste EN. Cytokines in inflammatory brain lesions: helpful and harmful. Trends Neurosci 1996;19:331-8.
43. Morganti-Kossmann MC, Rancan M, Stahel PF, et al. Inflammatory response in acute traumatic brain injury: a double-edged sword. Curr Opin Crit Care 2002;8:101-5.
44. Lenzlinger PM, Morganti-Kossmann MC, Laurer HL, et al. The duality of the inflammatory response to traumatic brain injury. Mol Neurobiol 2001;24:169-81.
45. Narayan RK, Michel ME, Ansell B, et al. Clinical trials in head injury. J Neurotrauma 2002;19:503-57.
46. Reinert MM, Bullock R. Clinical trials in head injury. Neurol Res 1999;21:330-8.
47. Bullock MR, Lyeth BG, Muizelaar JP. Current status of neuroprotection trials for traumatic brain injury: lessons from animal models and clinical studies. Neurosurgery 1999;45:207-17, discussion 17-20.
48. Clifton GL, Miller ER, Choi SC, et al. Lack of effect of induction of hypothermia after acute brain injury. N Engl J Med 2001;344:556-63.
49. Morris GF, Bullock R, Marshall SB, et al. Failure of the competitive N-methyl-D-aspartate antagonist Selfotel (CGS 19755) in the treatment of severe head injury: results of two phase III clinical trials. The Selfotel Investigators. J Neurosurg 1999;91:737-43.
50. Ward JD, Becker DP, Miller JD, et al. Failure of prophylactic barbiturate coma in the treatment of severe head injury. J Neurosurg 1985;62:383-8.
51. Wang CX, Shuaib A. Involvement of inflammatory cytokines in central nervous system injury. Prog Neurobiol 2002;67:161-72.
52. Allan SM, Rothwell NJ. Cytokines and acute neurodegeneration. Nat Rev Neurosci 2001;2:734-44.
53. Morganti-Kossman MC, Lenzlinger PM, Hans V, et al. Production of cytokines following brain injury: beneficial and deleterious for the damaged tissue. Mol Psychiatry 1997;2:133-6.
54. Rothwell N. Interleukin-1 and neuronal injury: mechanisms, modification, and therapeutic potential. Brain Behav Immun 2003;17:152-7.
55. Ghirnikar RS, Lee YL, Eng LF. Inflammation in traumatic brain injury: role of cytokines and chemokines. Neurochem Res 1998;23:329-40.
56. Ott L, McClain CJ, Gillespie M, et al. Cytokines and metabolic dysfunction after severe head injury. J Neurotrauma 1994;11:447-72.
57. Kim KS, Wass CA, Cross AS, et al. Modulation of blood-brain barrier permeability by tumor necrosis factor and antibody to tumor necrosis factor in the rat. Lymphokine Cytokine Res 1992;11:293-8.
58. Ramilo O, Saez-Llorens X, Mertsola J, et al. Tumor necrosis factor alpha/cachectin and interleukin 1 beta initiate meningeal inflammation. J Exp Med 1990;172:497-507.
59. Megyeri P, Abraham CS, Temesvari P, et al. Recombinant human tumor necrosis factor alpha constricts pial arterioles and increases blood-brain barrier permeability in newborn piglets. Neurosci Lett 1992;148:137-40.
60. De Vries HE, Blom-Roosemalen MC, van Oosten M, et al. The influence of cytokines on the integrity of the blood-brain barrier in vitro. J Neuroimmunol 1996;64:37-43.
61. Lavine SD, Hofman FM, Zlokovic BV. Circulating antibody against tumor necrosis factor-alpha protects rat brain from reperfusion injury. J Cereb Blood Flow Metab 1998;18:52-8.
62. Shohami E, Novikov M, Bass R, et al. Closed head injury triggers early production of TNF alpha and IL-6 by brain tissue. J Cereb Blood Flow Metab 1994;14:615-9.
63. Fan L, Young PR, Barone FC, et al. Experimental brain injury induces differential expression of tumor necrosis factor-alpha mRNA in the CNS. Mol Brain Res 1996;36:287-91.
64. Knoblach SM, Fan L, Faden AI. Early neuronal expression of tumor necrosis factor-alpha after experimental brain injury contributes to neurological impairment. J Neuroimmunol 1999;95:115-25.
65. Taupin V, Toulmond S, Serrano A, et al. Increase in IL-6, IL-1 and TNF levels in rat brain following traumatic lesion. Influence of pre- and post-traumatic treatment with R05 4864, a peripheral-type (p site) benzodiazepine ligand. J Neuroimmunol 1993;42:177-85.
66. Tchelingerian JL, Quinonero J, Booss J, et al. Localization of TNFα and IL-1α immunoreactivities in striatal neurons after surgical injury to the hippocampus. Neuron 1993;10S:213-24.
67. Gourin CG, Shackford SR. Production of tumor necrosis factor-alpha and interleukin-1beta by human cerebral microvascular endothelium after percussive trauma. J Trauma 1997;42:1101-7.
68. Goodman JC, Robertson CS, Grossman RG, et al. Elevation of tumor necrosis factor in head injury. J Neuroimmunol 1990;30:213-7.
69. Ross SA, Halliday MI, Campbell GC, et al. The presence of tumour necrosis factor in CSF and plasma after severe head injury. Br J Neurosurg 1994;8:419-25.
70. Csuka E, Morganti-Kossmann MC, Lenzlinger PM, et al. IL-10 levels in cerebrospinal fluid and serum of patients with severe traumatic brain injury: relationship to IL-6, TNF-alpha, TGF-beta1 and blood-brain barrier function. J Neuroimmunol 1999;101:211-21.
71. Trembovler V, Beit-Yannai E, Younis F, et al. Antioxidants attenuate acute toxicity of tumor necrosis factor-alpha induced by brain injury in rat. J Interferon Cytokine Res 1999;19:791-5.
72. Shohami E, Bass R, Wallach D, et al. Inhibition of tumor necrosis factor alpha (TNFalpha) activity in rat brain is associated with cerebroprotection after closed head injury. J Cereb Blood Flow Metab 1996;16:378-84.
73. Shohami E, Gallily R, Mechoulam R, et al. Cytokine production in the brain following closed head injury: dexanabinol (HU-211) is a novel TNF-alpha inhibitor and an effective neuroprotectant. J Neurolmmunol 1997;72:169-77.
74. Rosenberg GA, Estrada EY, Dencoff JE, et al. Tumor necrosis factor-alpha-induced gelatinase B causes delayed opening of the blood-brain barrier: an expanded therapeutic window. Brain Res 1995;703:151-5.
75. Akassoglou K, Bauer J, Kassiotis G, et al. Oligodendrocyte apoptosis and primary demyelination induced by local TNF/p55TNF receptor signaling in the central nervous system of transgenic mice: models for multiple sclerosis with primary oligodendrogliopathy. Am J Pathol 1998;153:801-13.
76. Sedgwick JD, Riminton DS, Cyster JG, et al. Tumor necrosis factor: a master-regulator of leukocyte movement. Immunol Today 2000;21:110-3.
77. Hurwitz AA, Lyman WD, Guida MP, et al. Tumor necrosis factor alpha induces adhesion molecule expression on human fetal astrocytes. J Exp Med 1992;176:1631-6.
78. Otto VI, Heinzel-Pleines UE, Gloor SM, et al. slCAM-1 and TNF-alpha induce MIP-2 with distinct kinetics in astrocytes and brain microvascular endothelial cells. J Neurosci Res 2000;6:733-42.
79. Probert L, Akassoglou K, Kassiotis G, et al. TNF-alpha transgenic and knockout models of CNS inflammation and degeneration. J Neuroimmunol 1997;72:137-41.
80. Stahel PF, Shohami E, Younis FM, et al. Experimental closed head injury: analysis of neurological outcome, blood-brain barrier dysfunction, intracranial neutrophil infiltration, and neuronal cell death in mice deficient in genes for pro-inflammatory cytokines. J Cereb Blood Flow Metab 2000;20:369-80.
81. Quagliarello VJ, Wispelwey B, Long J, et al. Recombinant human interleukin-1 induces meningitis and blood-brain barrier injury in the rat. J Clin Invest 1991;87:1360-6.
82. Patel HC, Boutin H, Allan SM. Interleukin-1 in the brain: mechanisms of action in acute neurodegeneration. Ann N Y Acad Sci 2003;992:39-47.
83. Allan SM, Parker LC, Collins B, et al. Cortical cell death induced by IL-1 is mediated via actions in the hypothalamus of the rat. Proc Natl Acad Sci U S A 2000;97:5580-5.
84. Boutin H, LeFeuvre RA, Horai R, et al. Role of IL-1alpha and IL-1beta in ischemic brain damage. J Neurosci 2001;21:5528-34.
85. Vecil GG, Larsen PH, Corley SM, et al. Interleukin-1 is a key regulator of matrix metalloproteinase-9 expression in human neurons in culture and following mouse brain trauma in vivo. J Neurosci Res 2000;61:212-24.
86. Woodroofe MN, Sarna GS, Wadhwa M, et al. Detection of interleukin-1 and interleukin-6 in adult rat brain, following mechanical injury, by in vivo microdialysis: evidence of a role for microglia in cytokine production. J Neuroimmunol 1991;33:227-36.
87. Yan HQ, Alcaros Banos M, Herregodts P, et al. Expression of interleukin (IL)-1beta, IL-6 and their respective receptors in the normal rat brain and after injury. Eur J Immunol 1992;22:2963-71.
88. Chao CC, Hu S, Ehrlich L, et al. Interleukin-1 and tumor necrosis factor-alpha synergistically mediate neurotoxicity: involvement of nitric oxide and of N-methyl-D-aspartate receptors. Brain Behav Immun 1995;9:355-65.
89. Toulmond S, Rothwell NJ. Interleukin-1 receptor antagonist inhibits neuronal damage caused by fluid percussion injury in the rat. Brain Res 1995;671:261-6.
90. Tehranian R, Andell-Jonsson S, Beni SM, et al. Improved recovery and delayed cytokine induction after closed head injury in mice with central overexpression of the secreted isoform of the interleukin-1 receptor antagonist. J Neurotrauma 2002;19:939-51.
91. Fassbender K, Mielke O, Bertsch T, et al. Interferon-gamma-inducing factor (IL-18) and interferon-gamma in inflammatory CNS diseases. Neurology 1999;53:1104-6.
92. Hedtjarn M, Leverin AL, Eriksson K, et al. Interleukin-18 involvement in hypoxic-ischemic brain injury. J Neurosci 2002;22:5910-9.
93. Jander S, Schroeter M, Stoll G. Interleukin-18 expression after focal ischemia of the rat brain: association with the late-stage inflammatory response. J Cereb Blood Flow Metab 2002;22:62-70.
94. Yatsiv I, Morganti-Kossmann MC, Perez D, et al. Elevated intracranial IL-18 in humans and mice after traumatic brain injury and evidence of neuroprotective effects of IL-18-binding protein after experimental closed head injury. J Cereb Blood Flow Metab 2002;22:971-8.
95. Menge T, Jander S, Stoll G. Induction of the pro-inflammatory cytokine interleukin-18 by axonal injury. J Neurosci Res 2001;65:332-9.
96. Trinchieri G. Interleukin-12 and the regulation of innate resistance and adaptive immunity. Nat Rev Immunol 2003;3:133-46.
97. Constantinescu CS, Frei K, Wysocka M, et al. Astrocytes and microglia produce interleukin-12 p40. Ann N Y Acad Sci 1996;795:328-33.
98. Kornelisse RF, Hack CE, Savelkoul HF, et al. Intrathecal production of interleukin-12 and gamma interferon in patients with bacterial meningitis. Infect Immun 1997;65:877-81.
99. Balashov KE, Smith DR, Khoury SJ, et al. Increased interleukin 12 production in progressive multiple sclerosis: induction by activated CD4+ cells via CD40 ligand. Proc Natl Acad Sci U S A 1997;94:599-603.
100. Stahel PF, Kossmann T, Joller H, et al. Increased interleukin-12 levels in human cerebrospinal fluid following severe head trauma. Neurosci Lett 1998;249:123-6.
101. Holmin S, Soderlund J, Biberfeld P, et al. Intracerebral inflammation after human brain contusion. Neurosurgery 1998;42:291-8, discussion 8-9.
102. Gruol DL, Nelson TE. Physiological and pathological roles of interleukin-6 in the central nervous system. Mol Neurobiol 1997;15:307-39.
103. Eugster HP, Frei K, Kopf M, et al. IL-6-deficient mice resist myelin oligodendrocyte glycoprotein-induced autoimmune encephalomyelitis. Eur J Immunol 1998;28:2178-87.
104. McClain C, Cohen D, Phillips R, et al. Increased plasma and ventricular fluid interleukin-6 levels in patients with head injury. J Lab Clin Med 1991;118:225-31.
105. Bell MJ, Kochanek PM, Doughty LA, et al. Interieukin-6 and interleukin-10 in cerebrospinal fluid after severe traumatic brain injury in children. J Neurotrauma 1997;14:451-7.
106. Kossmann T, Hans V, Imhof HG, et al. Interleukin-6 released in human cerebrospinal fluid following traumatic brain injury may trigger nerve growth factor production in astrocytes. Brain Res 1996;713:143-52.
107. Maier B, Schwerdtfeger K, Mautes A, et al. Differential release of interleukines 6, 8, and 10 in cerebrospinal fluid and plasma after traumatic brain injury. Shock 2001;15:421-6.
108. Kossmann T, Hans VH, Imhof HG, et al. Intrathecal and serum interleukin-6 and the acute-phase response in patients with severe traumatic brain injuries. Shock 1995;4:311-7.
109. Klein MA, Moller JC, Jones LL, et al. Impaired neuroglial activation in interleukin-6 deficient mice. Glia 1997;19:227-33.
110. Penkowa M, Moos T, Carrasco J, et al. Strongly compromised inflammatory response to brain injury in interleukin-6-deficient mice. Glia 1999;25:343-57.
111. Campbell IL, Abraham CR, Masliah E, et al. Neurologic disease induced in transgenic mice by cerebral overexpression of interleukin 6. Proc Natl Acad Sci U S A 1993;90:10061-5.
112. Penkowa M, Giralt M, Carrasco J, et al. Impaired inflammatory response and increased oxidative stress and neurodegeneration after brain injury in interleukin-6-deficient mice. Glia 2000;32:271-85.
113. Penkowa M, Camats J, Hadberg H, et al. Astrocyte-targeted expression of interleukin-6 protects the central nervous system during neuroglial degeneration induced by 6-aminonicotinamide. J Neurosci Res 2003;73:481-96.
114. Swartz KR, Liu F, Sewell D, et al. Interleukin-6 promotes posttraumatic healing in the central nervous system. Brain Res 2001;896:86-95.
115. Gasque P, Dean YD, McGreal EP, et al. Complement components of the innate immune system in health and disease in the CNS. Immunopharmacology 2000;49:171-86.
116. Barnum SR. Inhibition of complement as a therapeutic approach in inflammatory central nervous system (CNS) disease. Mol Med 1999;5:569-82.
117. Van Beek J, Elward K, Gasque P. Activation of complement in the central nervous system: roles in neurodegeneration and neuroprotection. Ann N Y Acad Sci 2003;992:56-71.
118. Elward K, Gasque P. "Eat me" and "don't eat me" signals govern the innate immune response and tissue repair in the CNS: emphasis on the critical role of the complement system. Mol Immunol 2003;40:85-94.
119. Stahel PF, Barnum SR. Bacterial meningitis: complement gene expression in the central nervous system. Immunopharmacology 1997;38:65-72.
120. Emmerling MR, Watson MD, Raby CA, et al. The role of complement in Alzheimer's disease pathology. Biochim Biophys Acta 2000;1502:158-71.
121. Klein MA, Kaeser PS, Schwarz P, et al. Complement facilitates early prion pathogenesis. Nat Med 2001;7:488-92.
122. Kaczorowski SL, Schiding JK, Toth CA, et al. Effect of soluble complement receptor-1 on neutrophil accumulation after traumatic brain injury in rats. J Cereb Blood Flow Metab 1995;15:860-4.
123. Keeling KL, Hicks RR, Mahesh J, et al. Local neutrophil influx following lateral fluid-percussion brain injury in rats is associated with accumulation of complement activation fragments of the third component (C3) of the complement system. J Neuroimmunol 2000;105:20-30.
124. Nataf S, Stahel PF, Davoust N, et al. Complement anaphylatoxin receptors on neurons: newtricks for old receptors? Trends Neurosci 1999;22:397-402.
125. Stahel PF, Morganti-Kossmann MC, Perez D, et al. Intrathecal levels of complement-derived soluble membrane attack complex (sC5b-9) correlate with blood-brain barrier dysfunction in patients with traumatic brain injury. J Neurotrauma 2001;18:773-81.
126. Singhrao SK, Neal JW, Rushmere NK, et al. Spontaneous classical pathway activation and deficiency of membrane regulators render human neurons susceptible to complement lysis. Am J Pathol 2000;157:905-18.
127. Casarsa C, De Luigi A, Pausa M, et al. Intracerebroventricular injection of terminal complement complex causes inflammatory reaction in the rat brain. Eur J Immunol 2003;33:1260-70.
128. Xiong ZQ, Oian W, Suzuki K, et al. Formation of complement membrane attack complex in mammalian cerebral cortex evokes seizures and neurodegeneration. J Neurosci 2003;23:955-60.
129. Bellander BM, Holst H von, Fredman P, et al. Activation of the complement cascade and increase of clusterin in the brain following a cortical contusion in the adult rat. J Neurosurg 1996;85:468-75.
130. Bellander BM, Singhrao SK, Ohlsson M, et al. Complement activation in the human brain after traumatic head injury. J Neurotrauma 2001;18:1295-311.
131. Kossmann T, Stahel PF, Morganti-Kossmann MC, et al. Elevated levels of the complement components C3 and factor B in ventricular cerebrospinal fluid of patients with traumatic brain injury. J Neuroimmunol 1997;73:63-9.
132. Lindsberg PJ, Ohman J, Lehto T, et al. Complement activation in the central nervous system following blood-brain barrier damage in man. Ann Neurol 1996;40:587-96.
133. Gasque P, Singhrao SK, Neal JW, et al. The receptor for complement anaphylatoxin C3a is expressed by myeloid cells and nonmyeloid cells in inflamed human central nervous system: analysis in multiple sclerosis and bacterial meningitis. J Immunol 1998;160:3543-54.
134. Davoust N, Jones J, Stahel PF, et al. Receptor for the C3a anaphylatoxin is expressed by neurons and glial cells. Glia 1999;26:201-11.
135. Van Beek J, Nicole O, Ali C, et al. Complement anaphylatoxin C3a is selectively protective against NMDA-induced neuronal cell death. Neuroreport 2001;12:289-93.
136. Heese K, Hock C, Otten U. Inflammatory signals induce neurotrophin expression in human microglial cells. J Neurochem 1998;70:699-707.
137. Ember JA, Hugli TE. Complement factors and their receptors. Immunopharmacology 1997;38:3-15.
138. Mollnes TE, Song WC, Lambris JD. Complement in inflammatory tissue damage and disease. Trends Immunol 2002;23:61-4.
139. Farkas I, Baranyi L, Takahashi M, et al. A neuronal C5a receptor and an associated apoptotic signal transduction pathway. J Physiol (Lond) 1998;507:679-87.
140. Osaka H, Mukherjee P, Aisen PS, et al. Complement-derived anaphylatoxin C5a protects against glutamate-mediated neurotoxicity. J Cell Biochem 1999;73:303-11.
141. O'Barr SA, Caguioa J, Gruol D, et al. Neuronal expression of a functional receptor for the C5a complement activation fragment. J Immunol 2001;166:4154-62.
142. Lacy M, Jones J, Whittemore SR, et al. Expression of the receptors for the C5a anaphylatoxin, interleukin-8 and FMLP by human astrocytes and microglia. J Neuroimmunol 1995;61:71-8.
143. Nataf S, Levison SW, Barnum SR. Expression of the anaphylatoxin C5a receptor in the oligodendrocyte lineage. Brain Res 2001;894:321-6.
144. Gasque P, Chan P, Fontaine M, et al. Identification and characterization of the complement C5a anaphylatoxin receptor on human astrocytes. J Immunol 1995;155:4882-9.
145. Stahel PF, Kossmann T, Morganti-Kossmann MC, et al. Experimental diffuse axonal injury induces enhanced neuronal C5a receptor mRNA expression in rats. Brain Res Mol Brain Res 1997;50:205-12.
146. Stahel PF, Kariya K, Shohami E, et al. Intracerebral complement C5a receptor (CD88) expression is regulated by TNF and lymphotoxin-alpha following closed head injury in mice. J Neuroimmunol 2000;109:164-72.
147. Hicks RR, Keeling KL, Yang MY, et al. Vaccinia virus complement control protein enhances functional recovery after traumatic brain injury. J Neurotrauma 2002;19:705-14.
148. Rancan M, Morganti-Kossmann MC, Barnum SR, et al. Central nervous system-targeted complement inhibition mediates neuroprotection after closed head injury in transgenic mice. J Cereb Blood Flow Metab 2003;23:1070-4.
149. Ransohoff RM, Tani M. Do chemokines mediate leukocyte recruitment in post-traumatic CNS inflammation? Trends Neurosci 1998;21:154-9.
150. Clark RS, Carlos TM, Schiding JK, et al. Antibodies against Mac-1 attenuate neutrophil accumulation after traumatic brain injury in rats. J Neurotrauma 1996;13:333-41.
151. Glabinski AR, Ransohoff RM. Chemokines and chemokine receptors in CNS pathology. J Neurovirol 1999;5:3-12.
152. Kossmann T, Stahel PF, Lenzlinger PM, et al. Interleukin-8 released into the cerebrospinal fluid after brain injury is associated with blood-brain barrier dysfunction and nerve growth factor production. J Cereb Blood Flow Metab 1997;17:280-9.
153. Whalen MJ, Carlos TM, Kochanek PM, et al. Interleukin-8 is increased in cerebrospinal fluid of children with severe head injury. Crit Care Med 2000;28:929-34.
154. Bell MD, Taub DD, Perry VH. Overriding the brain's intrinsic resistance to leukocyte recruitment with intraparenchymal injections of recombinant chemokines. Neuroscience 1996;74:283-92.
155. Otto VI, Stahel PF, Rancan M, et al. Regulation of chemokines and chemokine receptors after experimental closed head injury. Neuroreport 2001;12:2059-64.
156. Glabinski A, Bielecki B, Kolodziejski P, et al. TNF-alpha microinjection upregulates chemokines and chemokine receptors in the central nervous system without inducing leukocyte infiltration. J Interferon Cytokine Res 2003;23:457-66.
157. Horuk R, Martin AW, Wang Z, et al. Expression of chemokine receptors by subsets of neurons in the central nervous system. J Immunol 1997;158:2882-90.
158. Berman JW, Guida MP, Warren J, et al. Localization of monocyte chemoattractant peptide-1 expression in the central nervous system in experimental autoimmune encephalomyelitis and trauma in the rat. J Immunol 1996;156:3017-23.
159. Rancan M, Otto VI, Hans VH, et al. Upregulation of ICAM-1 and MCP-1 but not of MIP-2 and sensorimotor deficit in response to traumatic axonal injury in rats. J Neurosci Res 2001;63:438-46.
160. Balabanov R, Goldman H, Murphy S, et al. Endothelial cell activation following moderate traumatic brain injury. Neurol Res 2001;23:175-82.
161. Pleines UE, Stover JF, Kossmann T, et al. Soluble ICAM-1 in CSF coincides with the extent of cerebral damage in patients with severe traumatic brain injury. J Neurotrauma 1998;15:399-409.
162. Whalen MJ, Carlos TM, Dixon CE, et al. Effect of traumatic brain injury in mice deficient in intercellular adhesion molecule-1: assessment of histopathologic and functional outcome. J Neurotrauma 1999;16:299-309.
163. Grady MS, Cody RF Jr, Maris DO, et al. P-selectin blockade following fluid-percussion injury: behavioral and immunochemical sequelae. J Neurotrauma 1999;16:13-25.
164. Redl H, Gasser H, Schlag G, et al. Involvement of oxygen radicals in shock related cell injury. Br Med Bull 1993;49:556-65.
165. Evans PH. Free radicals in brain metabolism and pathology. Br Med Bull 1993;49:577-87.
166. D'Ambrosio AL, Pinsky DJ, Connolly ES. The role of the complement cascade in ischemia/reperfusion injury: implications for neuroprotection. Mol Med 2001;7:367-82.
167. Granger DN. Role of xanthine oxidase and granulocytes in ischemia-reperfusion injury. Am J Physiol 1988;255:H1269-75.
168. Riedemann NC, Ward PA. Complement in ischemia reperfusion injury. Am J Pathol 2003;162:363-7.
169. Beit-Yannai E, Kohen R, Horowitz M, et al. Changes of biological reducing activity in rat brain following closed head injury: a cyclic voltammetry study in normal and heat-acclimated rats. J Cereb Blood Flow Metab 1997;17:273-9.
170. Cherian L, Goodman JC, Robertson CS. Brain nitric oxide changes after controlled cortical impact injury in rats. J Neurophysiol 2000;83:2171-8.
171. 3H]nitroarginine binding. J Neurotrauma 1999;16:865-77.
172. Hall ED, Kupina NC, Althaus JS. Peroxynitrite scavengers for the acute treatment of traumatic brain injury. Ann N Y Acad Sci 1999;890:462-8.
173. Marklund N, Clausen F, McIntosh TK, et al. Free radical scavenger posttreatment improves functional and morphological outcome after fluid percussion injury in the rat. J Neurotrauma 2001;18:821-32.
174. Yang Y, Li O, Shuaib A. Neuroprotection by 2-h postischemia administration of two free radical scavengers, alpha-phenyl-n-tert-butyl-nitrone (PBN) and N-tert-butyl-(2-sulfophenyl)-nitrone (S-PBN), in rats subjected to focal embolic cerebral ischemia. Exp Neurol 2000;163:39-45.
175. Galasso JM, Wang P, Martin D, et al. Inhibition of TNF-alpha can attenuate or exacerbate excitotoxic injury in neonatal rat brain. Neuroreport 2000;11:231-5.
176. Sullivan PG, Bruce-Keller AJ, Rabchevsky AG, et al. Exacerbation of damage and altered NF-kappaB activation in mice lacking tumor necrosis factor receptors after traumatic brain injury. J Neurosci 1999;19:6248-56.
177. Arnett HA, Mason J, Marino M, et al. TNF alpha promotes proliferation of oligodendrocyte progenitors and remyelination. Nat Neurosci 2001;4:1116-22.
178. Loddick SA, Turnbull AV, Rothwell NJ. Cerebral interleukin-6 is neuroprotective during permanent focal cerebral ischemia in the rat. J Cereb Blood Flow Metab 1998;18:176-9.
179. Strijbos PJ, Rothwell NJ. Interleukin-1 beta attenuates excitatory amino acid-induced neurodegeneration in vitro: involvement of nerve growth factor. J Neurosci 1995;15:3468-74.
180. Herx LM, Rivest S, Yong VW. Central nervous system-initiated inflammation and neurotrophism in trauma: IL-1 beta is required for the production of ciliary neurotrophic factor. J Immunol 2000;165:2232-9.
181. Penkowa M, Camats J, Giralt M, et al. Metallothionein-I overexpression alters brain inflammation and stimulates brain repair in transgenic mice with astrocyte-targeted interleukin-6 expression. Glia 2003;42:287-306.
182. Mukherjee P, Pasinetti GM. Complement anaphylatoxin C5a neuroprotects through mitogen-activated protein kinase-dependent inhibition of caspase 3. J Neurochem 2001;77:43-9.
183. DeGraba TJ, Pettigrew LC. Why do neuroprotective drugs work in animals but not humans? Neurol Clin 2000;18:475-93.
184. Alderson P, Roberts I. Corticosteroids in acute traumatic brain injury: systematic review of randomised controlled trials. Br Med J 1997;314:1855-9.
185. Fisher CJ Jr, Agosti J, Opal SM, et al. Treatment of septic shock with the tumor necrosis factor receptor:Fc fusion protein. The Soluble TNF Receptor Sepsis Study Group. N Engl J Med 1996;334:1697-702.
186. Knoblach SM, Faden AI. Interleukin-10 improves outcome and alters proinflammatory cytokine expression after experimental traumatic brain injury. Exp Neurol 1998;153:143-51.
187. Strle K, Zhou JH, Shen WH, et al. Interleukin-10 in the brain. Crit Rev Immunol 2001;21:427-49.
188. Balasingam V, Yong VW. Attenuation of astroglial reactivity by interleukin-10. J Neurosci 1996;16:2945-55.
189. National Coordinators of the Medical Research Council CRASH Trial. Update on progress in the international, multicenter, randomized, controlled trial for corticosteroids after significant head injury (Medical Research Council CRASH Trial). Curr Opin Crit Care 2003;9:92-7.
190. Shohami E, Novikov M, Mechoulam R. A nonpsychotropic cannabinoid, HU-211, has cerebroprotective effects after closed head injury in the rat. J Neurotrauma 1993;10:109-19.
191. Panikashvili D, Simeonidou C, Ben-Shabat S, et al. An endogenous cannabinoid (2-AG) is neuroprotective after brain injury. Nature 2001;413:527-31.
192. Mechoulam R, Panikashvili D, Shohami E. Cannabinoids and brain injury: therapeutic implications. Trends Mol Med 2002;8:58-61.
193. Royo NC, Shimizu S, Schouten JW, et al. Pharmacology of traumatic brain injury. Curr Opin Pharmacol 2003;3:27-32.
194. Leker RR, Shohami E, Abramsky O, et al. Dexanabinol; a novel neuroprotective drug in experimental focal cerebral ischemia. J Neurol Sci 1999;162:114-9.
195. Knoller N, Levi L, Shoshan I, et al. Dexanabinol (HU-211) in the treatment of severe closed head injury: a randomized, placebo-controlled, phase II clinical trial. Crit Care Med 2002;30:548-54.
196. Bracken MB. Methylprednisolone and acute spinal cord injury: an update of the randomized evidence. Spine 2001;26: Suppl:S47-54.