Pathogenesis of brain edema and investigation into anti-edema drugs

International Journal of Molecular Sciences

Volumn 16, Issue 5, 2015, Pages 9949-9975

  Michinaga, Shotaro ^a   Koyama, Yutaka ^a  

^a OSAKA OHTANI UNIVERSITY   (Japan)

Author keywords

Aquaporin; Blood brain barrier; Cold injury; Cytotoxic edema; ETB receptor; Fluid percussion injury; Matrix metalloproteinase; Vascular endothelial growth factor; Vasogenic edema

Indexed keywords

AQUAPORIN; CATION CHANNEL; DEXAMETHASONE; ENDOTHELIN B RECEPTOR; GLUCOCORTICOID RECEPTOR; MATRIX METALLOPROTEINASE; SODIUM POTASSIUM CHLORIDE COTRANSPORTER 1; SULFONYLUREA RECEPTOR 1; VASCULOTROPIN; GLUCOCORTICOID; LOOP DIURETIC AGENT; MATRIX METALLOPROTEINASE INHIBITOR; NEUROPROTECTIVE AGENT; VASCULOTROPIN A;

ANIMAL MODEL; BLOOD VESSEL PERMEABILITY; BRAIN EDEMA; BRAIN HEMORRHAGE; BRAIN INJURY; CELL SWELLING; COLD INJURY; DISORDERS OF MITOCHONDRIAL FUNCTIONS; DRY WEIGHT; GRAVIMETRY; LIVER FAILURE; NONHUMAN; NUCLEAR MAGNETIC RESONANCE IMAGING; OXIDATIVE STRESS; PATHOGENESIS; REVIEW; TRAUMATIC BRAIN INJURY; WATER INTOXICATION; ANIMAL; ANTAGONISTS AND INHIBITORS; HUMAN; METABOLISM; PATHOLOGY;

ANIMALIA;

ANIMALS; BRAIN EDEMA; GLUCOCORTICOIDS; HUMANS; MATRIX METALLOPROTEINASE INHIBITORS; NEUROPROTECTIVE AGENTS; SODIUM POTASSIUM CHLORIDE SYMPORTER INHIBITORS; VASCULAR ENDOTHELIAL GROWTH FACTOR A;

EID: 84929379633     PISSN: 16616596     EISSN: 14220067     Source Type: Journal    
DOI: 10.3390/ijms16059949     Document Type: Review

References (193)

1. Nag, S.; Manias, J.L.; Stewart, D.J. Pathology and new players in the pathogenesis of brain edema. Acta Neuropathol. 2009, 118, 197–217.
2. Bosoi, C.R.; Rose, C.F. Brain edema in acute liver failure and chronic liver disease: Similarities and differences. Neurochem. Int. 2013, 62, 446–457.
3. Raboel, P.H.; Bartek, J., Jr.; Andresen, M.; Bellander, B.M.; Romner, B. Intracranial pressure monitoring: Invasive versus non-invasive method—A review. Crit. Care Res. Pract. 2012, 2012, 950393.
4. Unterberg, A.W.; Stover J.; Kress, B.; Kiening, K.L. Edema and brain trauma. Neuroscience 2004, 4, 1021–1029.
5. Simard, J.M.; Kent, T.A.; Chen, M.; Tarasov, K.V.; Gerzanich, V. Brain oedema in focal ischaemia: Molecular pathophysiology and theoretical implications. Lancet Neurol. 2007, 6, 258–268.
6. Kuramatsu, J.B.; Huttner, H.B.; Schwab, S. Advances in the management of intracerebral hemorrhage. J. Neural Transm. 2013, 120, S35–S41.
7. Wright, G.; Sharifi, Y.; Jover-Cobos, M.; Jalan, R. The brain in acute on chronic liver failure. Metab. Brain Dis. 2014, 4, 965–973.
8. Rabinstein, A.A. Treatment of cerebral edema. Neurologist 2006, 12, 59–73.
9. Raslan, A.; Bhardwaj, A. Medical management of cerebral edema. Neurosurg. Focus 2007, 5, E12.
10. Walcott, B.P.; Kahle, K.T.; Simard, J.M. Novel treatment targets for cerebral edema. Neurotherapeutics 2012, 9, 65–72.
11. Thrane, A.S.; Rangroo Thrane, V.; Nedergaard, M. Drowning stars: Reassessing the role of astrocytes in brain edema. Trends Neurosci. 2014, 11, 620–628.
12. Abbott, N.J.; Rönnbäck, L.; Hansson, E. Astrocyte-endothelial interactions at the blood-brain barrier. Nat. Rev. Neurosci. 2006, 7, 41–53.
13. Wolburg, H.; Noell, S.; Mack, A.; Wolburg-Buchholz, K.; Fallier-Becker, P. Brain endothelial cells and the glio-vascular complex. Cell Tissue Res. 2009, 335, 75–96.
14. Ballabh, P.; Braun, A.; Nedergaard, M. The blood-brain barrier: An overview: Structure, regulation, and clinical implications. Neurobiol. Dis. 2004, 1, 1–13.
15. Paschen, W. Glutamate excitotoxicity in transient global cerebral ischemia. Acta Neurobiol. Exp. (Wars) 1996, 1, 313–322.
16. Cheng, G.; Kong, R.H.; Zhang, L.M.; Zhang, J.N. Mitochondria in traumatic brain injury and mitochondrial-targeted multipotential therapeutic strategies. Br. J. Pharmacol. 2012, 4, 699–719.
17. Walker, K.R.; Tesco, G. Molecular mechanisms of cognitive dysfunction following traumatic brain injury. Front. Aging Neurosci. 2013, 5, 29.
18. Weiss, N.; Miller, F.; Cazaubon, S.; Couraud, P.O. The blood-brain barrier in brain homeostasis and neurological diseases. Biochim. Biophys. Acta 2009, 4, 842–857.
19. Nedergaard, M.; Dirnagl, U. Role of glial cells in cerebral ischemia. Glia 2005, 4, 281–286.
20. Dimitrijevic, O.B.; Stamatovic, S.M.; Keep, R.F.; Andjelkovic, A.V. Absence of the chemokine receptor CCR2 protects against cerebral ischemia/reperfusion injury in mice. Stroke 2007, 4, 1345–1353.
21. Argaw, A.T.; Gurfein, B.T.; Zhang, Y.; Zameer, A.; John, G.R. VEGF-mediated disruption of endothelial CLN-5 promotes blood-brain barrier breakdown. Proc. Natl. Acad. Sci. USA 2009, 6, 977–982.
22. Kahle, K.T.; Simard, J.M.; Staley, K.J.; Nahed, B.V.; Jones, P.S.; Sun, D. Molecular mechanisms of ischemic cerebral edema: Role of electroneutral ion transport. Physiology (Bethesda) 2009, 24, 257–265.
23. Rabinstein, A.A. Treatment of brain edema in acute liver failure. Curr. Treat. Opt. Neurol. 2010, 2, 129–141.
24. Liang, D.; Bhatta, S.; Gerzanich, V.; Simard, J.M. Cytotoxic edema: Mechanisms of pathological cell swelling. jocus 2007, 5, E2.
25. Oury, T.D.; Piantadosi, C.A.; Crapo, J.D. Cold-induced brain edema in mice. Involvement of extracellular superoxide dismutase and nitric oxide. J. Biol. Chem. 1993, 268, 15394–15398.
26. Nag, S. Cold-injury of the cerebral cortex: Immunolocalization of cellular proteins and blood-brain barrier permeability studies. J. Neuropathol. Exp. Neurol. 1996, 55, 880–888.
27. Murakami, K.; Kondo, T.; Yang, G.; Chen, S.F.; Morita-Fujimura, Y.; Chan, P.H. Cold injury in mice: A model to study mechanisms of brain edema and neuronal apoptosis. Prog. Neurobiol. 1999, 57, 289–299.
28. Raslan, F.; Schwarz, T.; Meuth, S.G.; Austinat, M.; Bader, M.; Renné, T.; Roosen, K.; Stoll, G.; Sirén, A.L.; Kleinschnitz, C. Inhibition of bradykinin receptor B1 protects mice from focal brain injury by reducing blood-brain barrier leakage and inflammation. J. Cereb. Blood Flow Metab. 2010, 8, 1477–1486.
29. Pifarré, P.; Prado, J.; Giralt, M.; Molinero, A.; Hidalgo, J.; Garcia, A. Cyclic GMP phosphodiesterase inhibition alters the glial inflammatory response, reduces oxidative stress and cell death and increases angiogenesis following focal brain injury. J. Neurochem. 2010, 3, 807–817.
30. Donkin, J.J.; Vink, R. Mechanisms of cerebral edema in traumatic brain injury: Therapeutic developments. Curr. Opin. Neurol. 2010, 3, 293–299.
31. Xu, M.; Su, W.; Xu, Q.P. Aquaporin-4 and traumatic brain edema. Chin. J. Traumatol. 2010, 2, 103–110.
32. Chodobski, A.; Zink, B.J.; Szmydynger-Chodobska, J. Blood-brain barrier pathophysiology in traumatic brain injury. Transl. Stroke Res. 2011, 4, 492–516.
33. Nag, S.; Kapadia, A.; Stewart, D.J. Review: Molecular pathogenesis of blood-brain barrier breakdown in acute brain injury. Neuropathol. Appl. Neurobiol. 2011, 1, 3–23.
34. Albert-Weissenberger, C.; Sirén, A.L. Experimental traumatic brain injury. Exp. Transl. Stroke Med. 2010, 2, 16.
35. Xiong, Y.; Mahmood, A.; Chopp, M. Animal models of traumatic brain injury. Nat. Rev. Neurosci. 2013, 14, 128–142.
36. Thompson, H.J.; Lifshitz, J.; Marklund, N.; Grady, M.S.; Graham, D.I.; Hovda, D.A.; McIntosh, T.K. Lateral fluid percussion brain injury: A 15-year review and evaluation. J. Neurotrauma 2005, 1, 42–75.
37. Alder, J.; Fujioka, W.; Lifshitz, J.; Crockett, D.P.; Thakker-Varia, S. Lateral fluid percussion: Model of traumatic brain injury in mice. J. Vis. Exp. 2011, 54, doi:10.3791/3063.
38. Maegele, M.; Stuermer, E.K.; Hoeffgen, A.; Uhlenkueken, U.; Mautes, A.; Schaefer, N.; Lippert-Gruener, M.; Schaefer, U.; Hoehn, M. Multimodal MR imaging of acute and subacute experimental traumatic brain injury: Time course and correlation with cerebral energy metabolites. Acta Radiol. Short Rep. 2015, 4, doi:10.1177/2047981614555142.
39. Schmidt, R.H.; Grady, M.S. Regional patterns of blood-brain barrier breakdown following central and lateral fluid percussion injury in rodents. J. Neurotrauma 1993, 4, 415–430.
40. Fukuda, K.; Tanno, H.; Okimura, Y.; Nakamura, M.; Yamaura, A. The blood-brain barrier disruption to circulating proteins in the early period after fluid percussion brain injury in rats. J. Neurotrauma 1995, 3, 315–324.
41. Louin, G.; Marchand-Verrecchia, C.; Palmier, B.; Plotkine, M.; Jafarian-Tehrani, M. Selective inhibition of inducible nitric oxide synthase reduces neurological deficit but not cerebral edema following traumatic brain injury. Neuropharmacology 2006, 2, 182–190.
42. Simard, J.M.; Kilbourne, M.; Tsymbalyuk, O.; Tosun, C.; Caridi, J.; Ivanova, S.; Keledjian, K.; Bochicchio, G.; Gerzanich, V. Key role of sulfonylurea receptor 1 in progressive secondary hemorrhage after brain contusion. J. Neurotrauma 2009, 12, 2257–2267.
43. Lin, Y.; Pan, Y.; Wang, M.; Huang, X.; Yin, Y.; Wang, Y.; Jia, F.; Xiong, W.; Zhang, N.; Jiang, J.Y. Blood-brain barrier permeability is positively correlated with cerebral microvascular perfusion in the early fluid percussion-injured brain of the rat. Lab. Investig. 2012, 11, 1623–1634.
44. Knoblach, S.M.; Faden, A.I. Interleukin-10 improves outcome and alters proinflammatory cytokine expression after experimental traumatic brain injury. Exp. Neurol. 1998, 1, 143–151.
45. Farias, S.; Frey, L.C.; Murphy, R.C.; Heidenreich, K.A. Injury-related production of cysteinyl leukotrienes contributes to brain damage following experimental traumatic brain injury. J. Neurotrauma 2009, 11, 1977–1986.
46. Lotocki, G.; de Rivero Vaccari, J.P.; Perez, E.R.; Sanchez-Molano, J.; Furones-Alonso, O.; Bramlett, H.M.; Dietrich, W.D. Alterations in blood-brain barrier permeability to large and small molecules and leukocyte accumulation after traumatic brain injury: Effects of post-traumatic hypothermia. J. Neurotrauma 2009, 7, 1123–1134.
47. Van Putten, H.P.; Bouwhuis, M.G.; Muizelaar, J.P.; Lyeth, B.G.; Berman, R.F. Diffusion-weighted imaging of edema following traumatic brain injury in rats: Effects of secondary hypoxia. J. Neurotrauma 2005, 8, 857–872.
48. Claassen, J.; Carhuapoma, J.R.; Kreiter, K.T.; Du, E.Y.; Connolly, E.S.; Mayer, S.A. Global cerebral edema after subarachnoid hemorrhage: Frequency, predictors, and impact on outcome. Stroke 2002, 5, 1225–1232.
49. Qureshi, A.I.; Mendelow, A.D.; Hanley, D.F. Intracerebral haemorrhage. Lancet 2009, 373, 1632–1644.
50. Qureshi, A.I.; Tuhrim, S.; Broderick, J.P.; Batjer, H.H.; Hondo, H.; Hanley, D.F. Spontaneous intracerebral hemorrhage. N. Engl. J. Med. 2001, 344, 1450–1460.
51. Yang, G.Y.; Betz, A.L.; Chenevert, T.L.; Brunberg, J.A.; Hoff, J.T. Experimental intracerebral hemorrhage: Relationship between brain edema, blood flow, and blood-brain barrier permeability in rats. J. Neurosurg. 1994, 1, 93–102.
52. Katsuki, H. Exploring neuroprotective drug therapies for intracerebral hemorrhage. J. Pharmacol. Sci. 2010, 4, 366–378.
53. Keep, R.F.; Xiang, J.; Ennis, S.R.; Andjelkovic, A.; Hua, Y.; Xi, G.; Hoff, J.T. Blood-brain barrier function in intracerebral hemorrhage. Acta Neurochir. Suppl. 2008, 105, 73–77.
54. Keep, R.F.; Zhou, N.; Xiang, J.; Andjelkovic, A.V.; Hua, Y.; Xi, G. Vascular disruption and blood-brain barrier dysfunction in intracerebral hemorrhage. Fluids Barriers CNS 2014, 10, 18.
55. Kreiter, K.T.; Copeland, D.; Bernardini, G.L.; Bates, J.E.; Peery, S.; Claassen, J.; Du, Y.E.; Stern, Y.; Connolly, E.S.; Mayer, S.A. Predictors of cognitive dysfunction after subarachnoid hemorrhage. Stroke 2002, 1, 200–208.
56. Bodmer, D.; Vaughan, K.A.; Zacharia, B.E.; Hickman, Z.L.; Connolly, E.S. The Molecular Mechanisms that Promote Edema after Intracerebral Hemorrhage. Transl. Stroke Res. 2012, 3, S52–S61.
57. Kirkman, M.A.; Allan, S.M.; Parry-Jones, A.R. Experimental intracerebral hemorrhage: Avoiding pitfalls in translational research. J. Cereb. Blood Flow Metab. 2011, 11, 2135–2151.
58. Manaenko, A.; Chen, H.; Zhang, J.H.; Tang, J. Comparison of different preclinical models of intracerebral hemorrhage. Acta Neurochir. Suppl. 2011, 111, 9–14.
59. Kooijman, E.; Nijboer, C.H.; van Velthoven, C.T.; Kavelaars, A.; Kesecioglu, J.; Heijnen, C.J. The rodent endovascular puncture model of subarachnoid hemorrhage: Mechanisms of brain damage and therapeutic strategies. J. Neuroinflamm. 2014, 11, 2.
60. Carpenter, J.; Weinstein, S.; Myseros, J.; Vezina, G.; Bell, M.J. Inadvertent hyponatremia leading to acute cerebral edema and early evidence of herniation. Neurocrit. Care 2007, 3, 195–199.
61. Papadopoulos, M.C.; Verkman, A.S. Aquaporin-4 and brain edema. Pediatr. Nephrol. 2007, 6, 778–784.
62. Yamaguchi, M.; Wu, S.; Ehara, K.; Nagashima, T.; Tamaki, N. Cerebral blood flow of rats with water-intoxicated brain edema. Acta Neurochir. Suppl. (Wien) 1994, 60, 190–192.
63. Manley, G.T.; Fujimura, M.; Ma, T.; Noshita, N.; Filiz, F.; Bollen, A.W.; Chan, P.; Verkman, A.S. Aquaporin-4 deletion in mice reduces brain edema after acute water intoxication and ischemic stroke. Nat. Med. 2000, 6, 159–163.
64. Yang, B.; Zador, Z.; Verkman, A.S. Glial cell aquaporin-4 overexpression in transgenic mice accelerates cytotoxic brain swelling. J. Biol. Chem. 2008, 22, 15280–15286.
65. Yeung, P.K.; Lo, A.C.; Leung, J.W.; Chung, S.S.; Chung, S.K. Targeted overexpression of endothelin-1 in astrocytes leads to more severe cytotoxic brain edema and higher mortality. J. Cereb. Blood Flow Metab. 2009, 12, 1891–1902.
66. Kozler, P.; Riljak, V.; Pokorný, J. Both water intoxication and osmotic BBB disruption increase brain water content in rats. Physiol. Res. 2013, 62, S75–S80.
67. Mpabanzi, L.; Jalan, R. Neurological complications of acute liver failure: Pathophysiological basis of current management and emerging therapies. Neurochem. Int. 2012, 60, 736–742.
68. Häussinger, D. Low grade cerebral edema and the pathogenesis of hepatic encephalopathy in cirrhosis. Hepatology 2006, 43, 1187–1190.
69. Larsen, F.S.; Wendon, J. Brain edema in liver failure: Basic physiologic principles and management. Liver Transpl. 2002, 8, 983–989.
70. Wendon, J.; Lee, W. Encephalopathy and cerebral edema in the setting of acute liver failure: Pathogenesis and management. Neurocrit. Care 2008, 1, 97–102.
71. Scott, T.R.; Kronsten, V.T.; Hughes, R.D.; Shawcross, D.L. Pathophysiology of cerebral oedema in acute liver failure. World J. Gastroenterol. 2013, 48, 9240–9255.
72. Larsen, F.S.; Wendon, J. Prevention and management of brain edema in patients with acute liver failure. Liver Transpl. 2008, 14, S90–S96.
73. Wright, G.; Davies, N.A.; Shawcross, D.L.; Hodges, S.J.; Zwingmann, C.; Brooks, H.F.; Mani, A.R.; Harry, D.; Stadlbauer, V.; Zou, Z. et al. Endotoxemia produces coma and brain swelling in bile duct ligated rats. Hepatology 2007, 45, 1517–1526.
74. Swain, M.; Butterworth, R.F.; Blei, A.T. Ammonia and related amino acids in the pathogenesis of brain edema in acute ischemic liver failure in rats. Hepatology 1992, 15, 449–453.
75. Norenberg, M.D.; Rao, K.V.; Jayakumar, A.R. Mechanisms of ammonia-induced astrocyte swelling. Metab. Brain Dis. 2005, 20, 303–318.
76. Rama Rao, K.V.; Verkman, A.S.; Curtis, K.M.; Norenberg, M.D. Aquaporin-4 deletion in mice reduces encephalopathy and brain edema in experimental acute liver failure. Neurobiol. Dis. 2014, 63, 222–228.
77. Jayakumar, A.R.; Rao, K.V.; Murthy, C.R.; Norenberg, M.D. Glutamine in the mechanism of ammonia-induced astrocyte swelling. Neurochem. Int. 2006, 6–7, 623–628.
78. Rama Rao, K.V.; Jayakumar, A.R.; Norenberg, M.D. Glutamine in the pathogenesis of acute hepatic encephalopathy. Neurochem. Int. 2012, 4, 575–580.
79. Jayakumar, A.R.; Bethea, J.R.; Tong, X.Y.; Gomez, J.; Norenberg, M.D. NF-κB in the mechanism of brain edema in acute liver failure: Studies in transgenic mice. Neurobiol. Dis. 2011, 2, 498–507.
80. Jayakumar, A.R.; Valdes, V.; Tong, X.Y.; Shamaladevi, N.; Gonzalez, W.; Norenberg, M.D. Sulfonylurea receptor 1 contributes to the astrocyte swelling and brain edema in acute liver failure. Transl. Stroke Res. 2014, 1, 28–37.
81. Rama Rao, K.V.; Jayakumar, A.R.; Tong, X.; Curtis, K.M.; Norenberg, M.D. Brain aquaporin-4 in experimental acute liver failure. J. Neuropathol. Exp. Neurol. 2010, 9, 869–879.
82. Rama Rao, K.V.; Reddy, P.V.; Tong, X.; Norenberg, M.D. Brain edema in acute liver failure: Inhibition by L-histidine. Am. J. Pathol. 2010, 3, 1400–1408.
83. Rama Rao, K.V.; Jayakumar, A.R.; Norenberg, M.D. Brain edema in acute liver failure: Mechanisms and concepts. Metab. Brain Dis. 2014, 4, 927–936.
84. Cauli, O.; López-Larrubia, P.; Rodrigo, R.; Agusti, A.; Boix, J.; Nieto-Charques, L.; Cerdán, S.; Felipo, V. Brain region-selective mechanisms contribute to the progression of cerebral alterations in acute liver failure in rats. Gastroenterology 2011, 140, 638–645.
85. Yamamoto, S.; Nguyen, J.H. TIMP-1/MMP-9 imbalance in brain edema in rats with fulminant hepatic failure. J. Surg. Res. 2006, 134, 307–314.
86. Chavarria, L.; Cordoba, J. Magnetic resonance of the brain in chronic and acute liver failure. Metab. Brain Dis. 2014, 29, 937–944.
87. Rama Rao, K.V.; Chen, M.; Simard, J.M.; Norenberg, M.D. Increased aquaporin-4 expression in ammonia-treated cultured astrocytes. Neuroreport 2003, 18, 2379–2382.
88. Jayakumar, A.R.; Liu, M.; Moriyama, M.; Ramakrishnan, R.; Forbush, B., 3rd.; Reddy, P.V.; Norenberg, M.D. Na–K–Cl cotransporter-1 in the mechanism of ammonia-induced astrocyte swelling. J. Biol. Chem. 2008, 49, 33874–33882.
89. Keep, R.F.; Hua, Y.; Xi, G. Brain water content. A misunderstood measurement? Transl. Stroke Res. 2012, 3, 263–265.
90. Marmarou, A.; Poll, W.; Shulman, K.; Bhagavan, H. A simple gravimetric technique for measurement of cerebral edema. J. Neurosurg. 1978, 49, 530–537.
91. Loubinoux, I.; Volk, A.; Borredon, J.; Guirimand, S.; Tiffon, B.; Seylaz, J.; Méric, P. Spreading of vasogenic edema and cytotoxic edema assessed by quantitative diffusion and T2 magnetic resonance imaging. Stroke 1997, 28, 419–426.
92. Badaut, J.; Ashwal, S.; Tone, B.; Regli, L.; Tian, H.R.; Obenaus, A. Temporal and regional evolution of aquaporin-4 expression and magnetic resonance imaging in a rat pup model of neonatal stroke. Pediatr. Res. 2007, 62, 248–254.
93. Rumpel, H.; Ferrini, B.; Martin, E. Lasting cytotoxic edema as an indicator of irreversible brain damage: A case of neonatal stroke. AJNR Am. J. Neuroradiol. 1998, 19, 1636–1638.
94. Roy H.; Bhardwaj, S.; Ylä-Herttuala, S. Biology of vascular endothelial growth factors. FEBS Lett. 2006, 12, 2879–2887.
95. Hayashi, T.; Abe, K.; Suzuki, H.; Itoyama, Y. Rapid induction of vascular endothelial growth factor gene expression after transient middle cerebral artery occlusion in rats. Stroke 1997, 28, 2039–2044.
96. Nag, S.; Eskandarian, M.R.; Davis, J.; Eubanks, J.H. Differential expression of vascular endothelial growth factor-A (VEGF-A) and VEGF-B after brain injury. J. Neuropathol. Exp. Neurol. 2002, 9, 778–788.
97. Sköld, M.K.; von Gertten, C.; Sandberg-Nordqvist, A.C.; Mathiesen, T.; Holmin, S. VEGF and VEGF receptor expression after experimental brain contusion in rat. J. Neurotrauma 2005, 22, 353–367.
98. Issa, R.; Krupinski, J.; Bujny, T.; Kumar, S.; Kaluza, J.; Kumar, P. Vascular endothelial growth factor and its receptor, KDR, in human brain tissue after ischemic stroke. Lab. Investig. 1999, 4, 417–425.
99. Plate, K.H.; Beck, H.; Danner, S.; Allegrini, P.R.; Wiessner, C. Cell type specific upregulation of vascular endothelial growth factor in an MCA-occlusion model of cerebral infarct. J. Neuropathol. Exp. Neurol. 1999, 6, 654–666.
100. Mărgăritescu, O.; Pirici, D.; Mărgăritescu, C. VEGF expression in human brain tissue after acute ischemic stroke. Rom. J. Morphol. Embryol. 2011, 4, 1283–1292.
101. Shore, P.M.; Jackson, E.K.; Wisniewski, S.R.; Clark, R.S.; Adelson, P.D.; Kochanek, P.M. Vascular endothelial growth factor is increased in cerebrospinal fluid after traumatic brain injury in infants and children. Neurosurgery 2004, 3, 605–161.
102. Hirose, T.; Matsumoto, N.; Tasaki, O.; Nakamura, H.; Akagaki, F.; Shimazu, T. Delayed progression of edema formation around a hematoma expressing high levels of VEGF and MMP-9 in a patient with traumatic brain injury: Case report. Neurol. Med. Chir. (Tokyo) 2013, 9, 609–612.
103. Matsuo, R.; Ago, T.; Kamouchi, M.; Kuroda, J.; Kuwashiro, T.; Hata, J.; Sugimori, H.; Fukuda, K.; Gotoh, S.; Makihara, N. et al. Clinical significance of plasma VEGF value in ischemic stroke-research for biomarkers in ischemic stroke (REBIOS) study. BMC Neurol. 2013, 13, 32.
104. Park, E.; Bell, J.D.; Siddiq, I.P.; Baker, A.J. An analysis of regional microvascular loss and recovery following two grades of fluid percussion trauma: A role for hypoxia-inducible factors in traumatic brain injury. J. Cereb. Blood Flow Metab. 2009, 3, 575–584.
105. Lee, C.; Agoston, D.V. Vascular endothelial growth factor is involved in mediating increased de novo hippocampal neurogenesis in response to traumatic brain injury. J. Neurotrauma 2010, 3, 541–553.
106. Jośko, J. Cerebral angiogenesis and expression of VEGF after subarachnoid hemorrhage (SAH) in rats. Brain Res. 2003, 1–2, 58–69.
107. Li, Y.N.; Pan, R.; Qin, X.J.; Yang, W.L.; Qi, Z.; Liu, W.; Liu, K.J. Ischemic neurons activate astrocytes to disrupt endothelial barrier via increasing VEGF expression. J. Neurochem. 2014, 1, 120–129.
108. Bates, D.O. Vascular endothelial growth factors and vascular permeability. Cardiovasc. Res. 2010, 87, 262–271.
109. Argaw, A.T.; Asp, L.; Zhang, J.; Navrazhina, K.; Pham, T.; Mariani, J.N.; Mahase, S.; Dutta, D.J.; Seto, J.; Kramer, E.G. et al. Astrocyte-derived VEGF-A drives blood-brain barrier disruption in CNS inflammatory disease. J. Clin. Investig. 2012, 7, 2454–2468.
110. Jiang, S.; Xia, R.; Jiang, Y.; Wang, L.; Gao, F. Vascular endothelial growth factors enhance the permeability of the mouse blood-brain barrier. PLoS ONE 2014, 2, e86407.
111. Tsukita, S.; Furuse, M. Claudin-based barrier in simple and stratified cellular sheets. Curr. Opin. Cell Biol. 2002, 14, 531–536.
112. Nitta, T.; Hata, M.; Gotoh, S.; Seo, Y.; Sasaki, H.; Hashimoto, N.; Furuse, M.; Tsukita, S. Size-selective loosening of the blood-brain barrier in claudin-5-deficient mice. J. Cell Biol. 2003, 161, 653–660.
113. Furuse, M.; Hirase, T.; Itoh, M.; Nagafuchi, A.; Yonemura, S.; Tsukita, S.; Tsukita, S. Occludin: A novel integral membrane protein localizing at tight junctions. J. Cell Biol. 1993, 123, 1777–1788.
114. Kimura, R.; Nakase, H.; Tamaki, R.; Sakaki, T. Vascular endothelial growth factor antagonist reduces brain edema formation and venous infarction. Stroke 2005, 36, 1259–1263.
115. Van Bruggen, N.; Thibodeaux, H.; Palmer, J.T.; Lee, W.P.; Fu, L.; Cairns, B.; Tumas, D.; Gerlai, R.; Williams, S.P.; van Lookeren, C.M. et al. VEGF antagonism reduces edema formation and tissue damage after ischemia/reperfusion injury in the mouse brain. J. Clin. Investig. 1999, 104, 1613–1620.
116. Kumai, Y.; Ooboshi, H.; Ibayashi, S.; Ishikawa, E.; Sugimori, H.; Kamouchi, M.; Kitazono, T.; Egashira, K.; Iida, M. Postischemic gene transfer of soluble Flt-1 protects against brain ischemia with marked attenuation of blood-brain barrier permeability. J. Cereb. Blood Flow Metab. 2007, 6, 1152–1160.
117. Koyama, J.; Miyake, S.; Sasayama, T.; Kondoh, T.; Kohmura, E. Effect of VEGF receptor antagonist (VGA1155) on brain edema in the rat cold injury model. Kobe J. Med. Sci. 2007, 5, 199–207.
118. Mott, J.D.; Werb, Z. Regulation of matrix biology by matrix metalloproteinases. Curr. Opin. Cell Biol. 2004, 5, 558–564.
119. Pepper, M.S. Role of the matrix metalloproteinase and plasminogen activator-plasmin systems in angiogenesis. Arterioscler. Thromb. Vasc. Biol. 2001, 7, 1104–1017.
120. Seo, J.H.; Guo, S.; Lok, J.; Navaratna, D.; Whalen, M.J.; Kim, K.W.; Lo, E.H. Neurovascular matrix metalloproteinases and the blood-brain barrier. Curr. Pharm. Des. 2012, 25, 3645–3648.
121. Heo, J.H.; Lucero, J.; Abumiya, T.; Koziol, J.A.; Copeland, B.R.; del Zoppo, G.J. Matrix metalloproteinases increase very early during experimental focal cerebral ischemia. J. Cereb. Blood Flow Metab. 1999, 6, 624–633.
122. Grossetete, M.; Phelps, J.; Arko, L.; Yonas, H.; Rosenberg, G.A. Elevation of matrix metalloproteinases 3 and 9 in cerebrospinal fluid and blood in patients with severe traumatic brain injury. Neurosurgery 2009, 4, 702–708.
123. Zheng, K.; Li, C.; Shan, X.; Liu, H.; Fan, W.; Wang, Z.; Zheng, P. Matrix metalloproteinases and their tissue inhibitors in serum and cerebrospinal fluid of patients with moderate and severe traumatic brain injury. Neurol. India 2013, 6, 606–609.
124. Jia, F.; Pan, Y.H.; Mao, Q.; Liang, Y.M.; Jiang, J.Y. Matrix metalloproteinase-9 expression and protein levels after fluid percussion injury in rats: The effect of injury severity and brain temperature. J. Neurotrauma 2010, 6, 1059–1068.
125. Rosenberg, G.A.; Navratil, M. Metalloproteinase inhibition blocks edema in intracerebral hemorrhage in the rat. Neurology 1997, 4, 921–926.
126. Planas, A.M.; Solé, S.; Justicia, C. Expression and activation of matrix metalloproteinase-2 and -9 in rat brain after transient focal cerebral ischemia. Neurobiol. Dis. 2001, 8, 834–846.
127. Rosenberg, G.A.; Cunningham, L.A.; Wallace, J.; Alexander, S.; Estrada, E.Y.; Grossetete, M.; Razhagi, A.; Miller, K.; Gearing, A. Immunohistochemistry of matrix metalloproteinases in reperfusion injury to rat brain: Activation of MMP9 linked to stromelysin-1 and microglia in cell cultures. Brain Res. 2001, 893, 104–112.
128. Muir, E.M.; Adcock, K.H.; Morgenstern, D.A.; Clayton, R.; von Stillfried, N.; Rhodes, K.; Ellis, C.; Fawcett, J.W.; Rogers, J.H. Matrix metalloproteases and their inhibitors are produced by overlapping populations of activated astrocytes. Brain Res. Mol. Brain Res. 2002, 100, 103–117.
129. Lee, S.R.; Tsuji, K.; Lee, S.R.; Lo, E.H. Role of matrix metalloproteinases in delayed neuronal damage after transient global cerebral ischemia. J. Neurosci. 2004, 3, 671–678.
130. Morita-Fujimura, Y.; Fujimura, M.; Gasche, Y.; Copin, J.C.; Chan, P.H. Overexpression of copper and zinc superoxide dismutase in transgenic mice prevents the induction and activation of matrix metalloproteinases after cold injury-induced brain trauma. J. Cereb. Blood Flow Metab. 2000, 1, 130–138.
131. Gasche, Y.; Copin, J.C.; Sugawara, T.; Fujimura, M.; Chan, P.H. Matrix metalloproteinase inhibition prevents oxidative stress-associated blood-brain barrier disruption after transient focal cerebral ischemia. J. Cereb. Blood Flow Metab. 2001, 12, 1393–400.
132. Rivera, S.; Ogier, C.; Jourquin, J.; Timsit, S.; Szklarczyk, A.W.; Miller, K.; Gearing, A.J.; Kaczmarek, L.; Khrestchatisky, M. Gelatinase B and TIMP-1 are regulated in a cell- and time-dependent manner in association with neuronal death and glial reactivity after global forebrain ischemia. Eur. J. Neurosci. 2002, 15, 19–32.
133. Asahi, M.; Wang, X.; Mori, T.; Sumii, T.; Jung, J.C.; Moskowitz, M.A.; Fini, M.E.; Lo, E.H. Effects of matrix metalloproteinase-9 gene knock-out on the proteolysis of blood-brain barrier and white matter components after cerebral ischemia. J. Neurosci. 2001, 21, 7724–7732.
134. Wang, J.; Tsirka, S.E. Neuroprotection by inhibition of matrix metalloproteinases in a mouse model of intracerebral haemorrhage. Brain 2005, 128, 1622–1633.
135. Shigemori, Y.; Katayama, Y.; Mori, T.; Maeda, T.; Kawamata, T. Matrix metalloproteinase-9 is associated with blood-brain barrier opening and brain edema formation after cortical contusion in rats. Acta Neurochir. Suppl. 2006, 96,130–133.
136. Rosenberg, G.A.; Estrada, E.Y.; Dencoff, J.E. Matrix metalloproteinases and TIMPs are associated with blood-brain barrier opening after reperfusion in rat brain. Stroke 1998, 10, 2189–2195.
137. Sood, R.R.; Taheri, S.; Candelario-Jalil, E.; Estrada, E.Y.; Rosenberg, G.A. Early beneficial effect of matrix metalloproteinase inhibition on blood-brain barrier permeability as measured by magnetic resonance imaging countered by impaired long-term recovery after stroke in rat brain. J. Cereb. Blood Flow Metab. 2008, 28, 431–438.
138. Kawai, N.; Kawanishi, M.; Okada, M.; Matsumoto, Y.; Nagao, S. Treatment of cold injury-induced brain edema with a nonspecific matrix metalloproteinase inhibitor MMI270 in rats. J. Neurotrauma 2003, 7, 649–657.
139. Agre, P.; King, L.S.; Yasui, M.; Guggino, W.B.; Ottersen, O.P.; Fujiyoshi, Y.; Engel, A.; Nielsen, S. Aquaporin water channels—From atomic structure to clinical medicine. J. Physiol. 2002, 1, 3–16.
140. Papadopoulos, M.C.; Verkman, A.S. Aquaporin water channels in the nervous system. Nat. Rev. Neurosci. 2013, 4, 265–277.
141. Fukuda, A.M.; Badaut, J. Aquaporin 4: A player in cerebral edema and neuroinflammation. J. Neuroinflamm. 2012, 9, 279.
142. Oshio, K.; Watanabe, H.; Song, Y.; Verkman, A.S.; Manley, G.T. Reduced cerebrospinal fluid production and intracranial pressure in mice lacking choroid plexus water channel Aquaporin-1. FASEB J. 2005, 19, 76–78.
143. Badaut, J.; Hirt, L.; Granziera, C.; Bogousslavsky, J.; Magistretti, P.J.; Regli, L. Astrocyte-specific expression of aquaporin-9 in mouse brain is increased after transient focal cerebral ischemia. J. Cereb. Blood Flow Metab. 2001, 21, 477–482.
144. Hu, H.; Yao, H.T.; Zhang, W.P.; Zhang, L.; Ding, W.; Zhang, S.H.; Chen, Z.; Wei, E.Q. Increased expression of aquaporin-4 in human traumatic brain injury and brain tumors. J. Zhejiang Univ. Sci. B 2005, 1, 33–37.
145. Kimbler, D.E.; Shields, J.; Yanasak, N.; Vender, J.R.; Dhandapani, K.M. Activation of P2X7 promotes cerebral edema and neurological injury after traumatic brain injury in mice. PLoS ONE 2012, 7, e41229.
146. Qing, W.G.; Dong, Y.Q.; Ping, T.Q.; Lai, L.G.; Fang, L.D.; Min, H.W.; Xia, L.; Heng, P.Y. Brain edema after intracerebral hemorrhage in rats: The role of iron overload and aquaporin4. J. Neurosurg. 2009, 3, 462–468.
147. Kiening, K.L.; van Landeghem, F.K.; Schreiber, S.; Thomale, U.W.; von Deimling, A.; Unterberg, A.W.; Stover, J.F. Decreased hemispheric Aquaporin-4 is linked to evolving brain edema following controlled cortical impact injury in rats. Neurosci. Lett. 2002, 2, 105–108.
148. Hoshi, A.; Yamamoto, T.; Shimizu, K.; Sugiura, Y.; Ugawa, Y. Chemical preconditioning-induced reactive astrocytosis contributes to the reduction of post-ischemic edema through aquaporin-4 downregulation. Exp. Neurol. 2011, 1, 89–95.
149. Papadopoulos, M.C.; Manley, G.T.; Krishna, S.; Verkman, A.S. Aquaporin-4 facilitates reabsorption of excess fluid in vasogenic brain edema. FASEB J. 2004, 18, 1291–1293.
150. Tang, Y.; Wu, P.; Su, J.; Xiang, J.; Cai, D.; Dong, Q. Effects of A quaporin-4 on edema formation following intracerebral hemorrhage. Exp. Neurol. 2010, 2, 485–495.
151. Igarashi, H.; Huber, V.J.; Tsujita, M.; Nakada, T. Pretreatment with a novel aquaporin 4 inhibitor, TGN-020, significantly reduces ischemic cerebral edema. Neurol. Sci. 2011, 32, 113–116.
152. Bhattacharya, P.; Pandey, A.K.; Paul, S.; Patnaik, R.; Yavagal, D.R. Aquaporin-4 inhibition mediates piroxicam-induced neuroprotection against focal cerebral ischemia/reperfusion injury in rodents. PLoS ONE 2013, 8, e73481.
153. Jayakumar, A.R.; Norenberg, M.D. The Na–K–Cl co-transporter in astrocyte swelling. Metab. Brain Dis. 2010, 1, 31–38.
154. Yan, Y.; Dempsey, R.J.; Flemmer, A.; Forbush, B.; Sun, D. Inhibition of Na+–K+–Cl− cotransporter during focal cerebral ischemia decreases edema and neuronal damage. Brain Res. 2003, 1, 22–31.
155. Simard, J.M.; Kahle, K.T.; Gerzanich, V. Molecular mechanisms of microvascular failure in CNS injury—Synergistic roles of NKCC1 and SUR1/TRPM4. J. Neurosurg. 2010, 3, 622–629.
156. Chechneva, O.; Yuen, N.; Tsai, Y.-C.; Chen, Y.J.; Anderson, S.; O’Donnell, M. Evidence for blood-brain barrier Na–K–Cl cotransport, Na/H exchange and Na–HCO3 cotransport involvement in hyperglycemia exacerbation of cerebral edema formation in ischemic stroke. FASEB J. 2014, 28, S685.3.
157. Su, G.; Kintner, D.B.; Flagella, M.; Shull, G.E.; Sun, D. Astrocytes from Na+–K+–Cl− cotransporter-null mice exhibit absence of swelling and decrease in EAA release. Am. J. Physiol. Cell Physiol. 2002, 5, C1147–C1160.
158. Chen, H.; Luo, J.; Kintner, D.B.; Shull, G.E.; Sun, D. Na+-dependent chloride transporter (NKCC1)-null mice exhibit less gray and white matter damage after focal cerebral ischemia. J. Cereb. Blood Flow Metab. 2005, 1, 54–66.
159. O’Donnell, M.E.; Tran, L.; Lam, T.I.; Liu, X.B.; Anderson, S.E. Bumetanide inhibition of the blood-brain barrier Na–K–Cl cotransporter reduces edema formation in the rat middle cerebral artery occlusion model of stroke. J. Cereb. Blood Flow Metab. 2004, 9, 1046–1056.
160. Lu, K.T.; Cheng, N.C.; Wu, C.Y.; Yang, Y.L. NKCC1-mediated traumatic brain injury-induced brain edema and neuron death via Raf/MEK/MAPK cascade. Crit. Care Med. 2008, 3, 917–922.
161. Jayakumar, A.R.; Valdes, V.; Norenberg, M.D. The Na–K–Cl cotransporter in the brain edema of acute liver failure. J. Hepatol. 2011, 2, 272–278.
162. Chen, M.; Simard, J.M. Cell swelling and a nonselective cation channel regulated by internal Ca2+ and ATP in native reactive astrocytes from adult rat brain. J. Neurosci. 2001, 17, 6512–6521.
163. Simard, J.M.; Chen, M.; Tarasov, K.V.; Bhatta, S.; Ivanova, S.; Melnitchenko, L.; Tsymbalyuk, N.; West, G.A.; Gerzanich, V. Newly expressed SUR1-regulated NCCa-ATP channel mediates cerebral edema after ischemic stroke. Nat. Med. 2006, 4, 433–440.
164. Simard, J.M.; Woo, S.K.; Schwartzbauer, G.T.; Gerzanich, V. Sulfonylurea receptor 1 in central nervous system injury: A focused review. J. Cereb. Blood Flow Metab. 2012, 9, 699–717.
165. Simard, J.M.; Tsymbalyuk, O.; Ivanov, A.; Ivanova, S.; Bhatta, S.; Geng, Z.; Woo, S.K.; Gerzanich, V. Endothelial sulfonylurea receptor 1-regulated NCCa-ATP channels mediate progressive hemorrhagic necrosis following spinal cord injury. J. Clin. Investig. 2007, 8, 2105–2013.
166. Zweckberger, K.; Hackenberg, K.; Jung, C.S.; Hertle, D.N.; Kiening, K.L.; Unterberg, A.W.; Sakowitz, O.W. Glibenclamide reduces secondary brain damage after experimental traumatic brain injury. Neuroscience 2014, 272, 199–206.
167. Simard, J.M.; Woo, S.K.; Tsymbalyuk, N.; Voloshyn, O.; Yurovsky, V.; Ivanova, S.; Lee, R.; Gerzanich, V. Glibenclamide-10-h treatment window in a clinically relevant model of stroke. Transl. Stroke Res. 2012, 2, 286–295.
168. Simard, J.M.; Sheth, K.N.; Kimberly, W.T.; Stern, B.J.; del Zoppo, G.J.; Jacobson, S.; Gerzanich, V. Glibenclamide in cerebral ischemia and stroke. Neurocrit. Care 2014, 2, 319–333.
169. Goto, K.; Hama, H.; Kasuya, Y. Molecular pharmacology and pathophysiological significance of endothelin. Jpn. J. Pharmacol. 1996, 72, 261–290.
170. Schinelli, S. Pharmacology and physiopathology of the brain endothelin system: An overview. Curr. Med. Chem. 2006, 13, 627–638.
171. Dashwood, M.R.; Loesch, A. Endothelin-1 as a neuropeptide: Neurotransmitter or neurovascular effects? J. Cell Commun. Signal. 2010, 4, 51–62.
172. Kaundal, R.K.; Deshpande, T.A.; Gulati, A.; Sharma, S.S. Targeting endothelin receptors for pharmacotherapy of ischemic stroke: Current scenario and future perspectives. Drug Discov. Today 2012, 17, 793–804.
173. Peters, C.M.; Rogers, S.D.; Pomonis, J.D.; Egnaczyk, G.F.; Keyser, C.P.; Schmidt, J.A.; Ghilardi, J.R.; Maggio, J.E.; Mantyh, P.W. Endothelin receptor expression in the normal and injured spinal cord: Potential involvement in injury-induced ischemia and gliosis. Exp. Neurol. 2003, 180, 1–13.
174. Rogers, S.D.; Peters, C.M.; Pomonis, J.D.; Hagiwara, H.; Ghilardi, J.R.; Mantyh, P.W. Endothelin B receptors are expressed by astrocytes and regulate astrocyte hypertrophy in the normal and injured CNS. Glia 2003, 41, 180–190.
175. Wilhelmsson, U.; Li, L.; Pekna, M.; Berthold, C.H.; Blom, S.; Eliasson, C.; Renner, O.; Bushong, E.; Ellisman, M.; Morgan, T.E. et al. Absence of glial fibrillary acidic protein and vimentin prevents hypertrophy of astrocytic processes and improves post-traumatic regeneration. J. Neurosci. 2004, 24, 5016–5021.
176. Ishikawa, N.; Takemura, M.; Koyama, Y.; Shigenaga, Y.; Okada, T.; Baba, A. Endothelins promote the activation of astrocytes in rat neostriatum through ETB receptors. Eur. J. Neurosci. 1997, 9, 895–901.
177. Koyama, Y.; Tsujikawa, K.; Matsuda, T.; Baba, A. Intracerebroventricular administration of an endothelin ETB receptor agonist increases expressions of GDNF and BDNF in rat brain. Eur. J. Neurosci. 2003, 18, 887–894.
178. Koyama, Y.; Tanaka, K. Intracerebroventricular administration of an endothelin ETB-receptor agonist increases expression of matrix metalloproteinase-2 and -9 in rat brain. J. Pharmacol. Sci. 2010, 114, 433–443.
179. Koyama, Y.; Nagae, R.; Tokuyama, S.; Tanaka, K. I.c.v. administration of an endothelin ETB receptor agonist stimulates vascular endothelial growth factor-A production and activates vascular endothelial growth factor receptors in rat brain. Neuroscience 2011, 192, 689–698.
180. Koyama, Y.; Maebara, Y.; Hayashi, M.; Nagae, R.; Tokuyama, S.; Michinaga, S. Endothelins reciprocally regulate VEGF-A and angiopoietin-1 production in cultured rat astrocytes: Implications on astrocytic proliferation. Glia 2012, 60, 1954–1963.
181. Michinaga, S.; Nagase, M.; Matsuyama, E.; Yamanaka, D.; Seno, N.; Fuka, M.; Yamamoto, Y.; Koyama, Y. Amelioration of cold injury-induced cortical brain edema formation by selective endothelin ETB receptor antagonists in mice. PLoS ONE 2014, 9, e102009.
182. Kim, J.E.; Ryu, H.J.; Kang, T.C. Status epilepticus induces vasogenic edema via tumor necrosis factor-α/endothelin-1-mediated two different pathways. PLoS ONE 2013, 9, e74458.
183. Moldes, O.; Sobrino, T.; Blanco, M.; Agulla, J.; Barral, D.; Ramos-Cabrer, P.; Castillo, J. Neuroprotection afforded by antagonists of endothelin-1 receptors in experimental stroke. Neuropharmacology 2012, 63, 279–285.
184. Kaal, E.C.; Vecht, C.J. The management of brain edema in brain tumors. Curr. Opin. Oncol. 2004, 6, 593–600.
185. Sinha, S.; Bastin, M.E.; Wardlaw, J.M.; Armitage, P.A.; Whittle, I.R. Effects of dexamethasone on peritumoral oedematous brain: A DT-MRI study. J. Neurol. Neurosurg. Psychiatry 2004, 75, 1632–1635.
186. Betz, A.L.; Coester, H.C. Effect of steroids on edema and sodium uptake of the brain during focal ischemia in rats. Stroke 1990, 8, 1199–1204.
187. Hortobágyi, T.; Hortobágyi, S.; Görlach, C.; Harkany, T.; Benyó, Z.; Görögh, T.; Nagel, W.; Wahl, M. A novel brain trauma model in the mouse: Effects of dexamethasone treatment. Pflugers Arch. 2000, 2–3, 409–415.
188. Vachon, P.; Moreau, J.P. Low doses of dexamethasone decrease brain water content of collagenase-induced cerebral hematoma. Can. J. Vet. Res. 2003, 2, 157–159.
189. Yang, J.T.; Lee, T.H.; Lee, I.N.; Chung, C.Y.; Kuo, C.H.; Weng, H.H. Dexamethasone inhibits ICAM-1 and MMP-9 expression and reduces brain edema in intracerebral hemorrhagic rats. Acta Neurochir. (Wien) 2011, 11, 2197–2203.
190. Stamatovic, S.M.; Dimitrijevic, O.B.; Keep, R.F.; Andjelkovic, A.V. Inflammation and brain edema: New insights into the role of chemokines and their receptors. Acta Neurochir. Suppl. 2006, 96, 444–450.
191. Kim, H.; Lee, J.M.; Park, J.S.; Jo, S.A.; Kim, Y.O.; Kim, C.W.; Jo, I. Dexamethasone coordinately regulates angiopoietin-1 and VEGF: A mechanism of glucocorticoid-induced stabilization of blood-brain barrier. Biochem. Biophys. Res. Commun. 2008, 1, 243–248.
192. Romero, I.A.; Radewicz, K.; Jubin, E.; Michel, C.C.; Greenwood, J.; Couraud, P.O., Adamson, P. Changes in cytoskeletal and tight junctional proteins correlate with decreased permeability induced by dexamethasone in cultured rat brain endothelial cells. Neurosci. Lett. 2003, 2, 112–116.
193. Kimberly, W.T.; Battey, T.W.; Pham, L.; Wu, O.; Yoo, A.J.; Furie, K.L.; Singhal, A.B.; Elm, J.J.; Stern, B.J.; Sheth, K.N. Glyburide is associated with attenuated vasogenic edema in stroke patients. Neurocrit. Care 2014, 2, 193–201.