Does inhibiting Sur1 complement rt-PA in cerebral ischemia?

Annals of the New York Academy of Sciences

Volumn 1268, Issue 1, 2012, Pages 95-107

  Simard, J Marc ^a   Geng, Zhihua ^a   Silver, Frank L ^b   Sheth, Kevin N ^a   Kimberly, W Taylor ^c   Stern, Barney J ^a   Colucci, Mario ^d   Gerzanich, Volodymyr ^a  

^a UNIVERSITY OF MARYLAND SCHOOL OF MEDICINE   (United States)

^b UNIVERSITY OF TORONTO   (Canada)

^c MASSACHUSETTS GENERAL HOSPITAL   (United States)

^d UNIVERSITY OF BARI   (Italy)

Author keywords

Cerebral ischemia; Glyburide; MMP 9; Rt PA; Stroke; Sur1

Indexed keywords

ALTEPLASE; BATIMASTAT; BB 1101; DIMETHYLSULOXIDE; DIPHENYLIODONIUM SALT; DOXYCYCLINE; FN 439; GELATINASE B; GLIBENCLAMIDE; MATRIX METALLOPROTEINASE INHIBITOR; MINOCYCLINE; NORPHENAZONE; QUERCETIN; RESVERATROL; SB 3CT; SULFONYLUREA RECEPTOR 1; TETRACYCLINE DERIVATIVE; UNCLASSIFIED DRUG;

ARTICLE; BLEEDING; BRAIN ISCHEMIA; DIABETES MELLITUS; DIABETIC PATIENT; EDEMA; GENE REPRESSION; HUMAN; NONHUMAN; STROKE; SWELLING; TREATMENT OUTCOME;

EID: 84866002705     PISSN: 00778923     EISSN: 17496632     Source Type: Book Series    
DOI: 10.1111/j.1749-6632.2012.06705.x     Document Type: Article

References (116)

1. Paciaroni, M., G. Agnelli, F. Corea, et al 2008. Early hemorrhagic transformation of brain infarction: rate, predictive factors, and influence on clinical outcome: results of a prospective multicenter study. Stroke 39: 2249-2256.
2. Lindley, R.I., J.M. Wardlaw, P.A. Sandercock, et al 2004. Frequency and risk factors for spontaneous hemorrhagic transformation of cerebral infarction. J. Stroke Cerebrovasc. Dis. 13: 235-246.
3. The Ninds t-PA Stroke Study Group. 1997. Intracerebral hemorrhage after intravenous t-PA therapy for ischemic stroke. Stroke 28: 2109-2118.
4. Khatri, P., L.R. Wechsler & J.P. Broderick 2007. Intracranial hemorrhage associated with revascularization therapies. Stroke 38: 431-440.
5. Larrue, V., R. Von Kummer, G.J. Del Zoppo & E. Bluhmki 1997. Hemorrhagic transformation in acute ischemic stroke. Potential contributing factors in the European Cooperative Acute Stroke Study. Stroke 28: 957-960.
6. Terruso, V., M. D'Amelio, B.N. Di, et al 2009. Frequency and determinants for hemorrhagic transformation of cerebral infarction. Neuroepidemiology 33: 261-265.
7. Woo, S.K., M.S. Kwon, Z. Geng, et al 2012. Sequential activation of hypoxia-inducible factor 1 and specificity protein 1 is required for hypoxia-induced transcriptional stimulation of Abcc8. J. Cereb. Blood Flow Metab. 32: 525-536.
8. Simard, J.M., M. Chen, K.V. Tarasov, et al 2006. Newly expressed SUR1-regulated NC(Ca-ATP) channel mediates cerebral edema after ischemic stroke. Nat. Med. 12: 433-440.
9. Simard, J.M., V. Yurovsky, N. Tsymbalyuk, et al 2009. Protective effect of delayed treatment with low-dose glibenclamide in three models of ischemic stroke. Stroke 40: 604-609.
10. Simard, J.M., N. Tsymbalyuk, O. Tsymbalyuk, et al 2010. Glibenclamide is superior to decompressive craniectomy in a rat model of malignant stroke. Stroke 41: 531-537.
11. Chen, M. & J.M. Simard 2001. Cell swelling and a nonselective cation channel regulated by internal Ca2+ and ATP in native reactive astrocytes from adult rat brain. J. Neurosci. 21: 6512-6521.
12. Simard, J.M., Z. Geng, S.K. Woo, et al 2009. Glibenclamide reduces inflammation, vasogenic edema, and caspase-3 activation after subarachnoid hemorrhage. J. Cereb. Blood Flow Metab. 29: 317-330.
13. Simard, J.M., T.A. Kent, M. Chen, et al 2007. Brain oedema in focal ischaemia: molecular pathophysiology and theoretical implications. Lancet Neurol. 6: 258-268.
14. Kaur, J., Z. Zhao, G.M. Klein, et al 2004. The neurotoxicity of tissue plasminogen activator? J. Cereb. Blood Flow Metab. 24: 945-963.
15. Nicole, O., F. Docagne, C. Ali, et al 2001. The proteolytic activity of tissue-plasminogen activator enhances NMDA receptor-mediated signaling. Nat. Med. 7: 59-64.
16. Fernandez-Monreal, M., J.P. Lopez-Atalaya, K. Benchenane, et al 2004. Arginine 260 of the amino-terminal domain of NR1 subunit is critical for tissue-type plasminogen activator-mediated enhancement of N-methyl-D-aspartate receptor signaling. J. Biol. Chem. 279: 50850-50856.
17. Siao, C.J. & S.E. Tsirka 2002. Tissue plasminogen activator mediates microglial activation via its finger domain through annexin II. J. Neurosci. 22: 3352-3358.
18. Wang, X., K. Tsuji, S.R. Lee, et al 2004. Mechanisms of hemorrhagic transformation after tissue plasminogen activator reperfusion therapy for ischemic stroke. Stroke 35: 2726-2730.
19. Lo, E.H., J.P. Broderick & M.A. Moskowitz 2004. tPA and proteolysis in the neurovascular unit. Stroke 35: 354-356.
20. Asahi, M., X. Wang, T. Mori, et al 2001. Effects of matrix metalloproteinase-9 gene knock-out on the proteolysis of blood-brain barrier and white matter components after cerebral ischemia. J. Neurosci. 21: 7724-7732.
21. Fujimura, M., Y. Gasche, Y. Morita-Fujimura, et al 1999. Early appearance of activated matrix metalloproteinase-9 and blood-brain barrier disruption in mice after focal cerebral ischemia and reperfusion. Brain Res. 842: 92-100.
22. Gasche, Y., M. Fujimura, Y. Morita-Fujimura, et al 1999. Early appearance of activated matrix metalloproteinase-9 after focal cerebral ischemia in mice: a possible role in blood-brain barrier dysfunction. J. Cereb. Blood Flow Metab. 19: 1020-1028.
23. Rosenberg, G.A., M. Navratil, F. Barone & G. Feuerstein 1996. Proteolytic cascade enzymes increase in focal cerebral ischemia in rat. J. Cereb. Blood Flow Metab. 16: 360-366.
24. Heo, J.H., J. Lucero, T. Abumiya, et al 1999. Matrix metalloproteinases increase very early during experimental focal cerebral ischemia. J. Cereb. Blood Flow Metab. 19: 624-633.
25. Cunningham, L.A., M. Wetzel & G.A. Rosenberg 2005. Multiple roles for MMPs and TIMPs in cerebral ischemia. Glia 50: 329-339.
26. Adibhatla, R.M. & J.F.Hatcher 2008. Tissue plasminogen activator (tPA) and matrix metalloproteinases in the pathogenesis of stroke: therapeutic strategies. CNS Neurol. Disord. Drug Targets 7: 243-253.
27. Rosenberg, G.A. 2002. Matrix metalloproteinases in neuroinflammation. Glia 39: 279-291.
28. Del Zoppo, G.J. & T. Mabuchi 2003. Cerebral microvessel responses to focal ischemia. J. Cereb. Blood Flow Metab. 23: 879-894.
29. Yong, V.W., C. Power, P. Forsyth & D.R. Edwards 2001. Metalloproteinases in biology and pathology of the nervous system. Nat. Rev. Neurosci. 2: 502-511.
30. Lo, E.H., X. Wang & M.L. Cuzner 2002. Extracellular proteolysis in brain injury and inflammation: role for plasminogen activators and matrix metalloproteinases. J. Neurosci. Res. 69: 1-9.
31. Copin, J.C., P. Merlani, T. Sugawara, et al 2008. Delayed matrix metalloproteinase inhibition reduces intracerebral hemorrhage after embolic stroke in rats. Exp. Neurol. 213: 196-201.
32. Gidday, J.M., Y.G. Gasche, J.C. Copin, et al 2005. Leukocyte-derived matrix metalloproteinase-9 mediates blood-brain barrier breakdown and is proinflammatory after transient focal cerebral ischemia. Am. J. Physiol. Heart Circ. Physiol. 289: H558-H568.
33. Castellanos, M., R. Leira, J. Serena, et al 2003. Plasma metalloproteinase-9 concentration predicts hemorrhagic transformation in acute ischemic stroke. Stroke 34: 40-46.
34. Ramos-Fernandez, M., M.F. Bellolio & L.G. Stead 2011. Matrix metalloproteinase-9 as a marker for acute ischemic stroke: a systematic review. J. Stroke Cerebrovasc. Dis. 20: 47-54.
35. Morancho, A., A. Rosell, L. Garcia-Bonilla & J. Montaner 2010. Metalloproteinase and stroke infarct size: role for anti-inflammatory treatment? Ann. N.Y. Acad. Sci 1207: 123-133.
36. Ning, M., K.L. Furie, W.J. Koroshetz, et al 2006. Association between tPA therapy and raised early matrix metalloproteinase-9 in acute stroke. Neurology 66: 1550-1555.
37. Sumii, T. & E.H. Lo 2002. Involvement of matrix metalloproteinase in thrombolysis-associated hemorrhagic transformation after embolic focal ischemia in rats. Stroke 33: 831-836.
38. Kanazawa, M., H. Igarashi, K. Kawamura, et al 2011. Inhibition of VEGF signaling pathway attenuates hemorrhage after tPA treatment. J. Cereb. Blood Flow Metab. 31: 1461-1474.
39. Murata, Y., A. Rosell, R.H. Scannevin, et al 2008. Extension of the thrombolytic time window with minocycline in experimental stroke. Stroke 39: 3372-3377.
40. Tsuji, K., T. Aoki, E. Tejima, et al 2005. Tissue plasminogen activator promotes matrix metalloproteinase-9 upregulation after focal cerebral ischemia. Stroke 36: 1954-1959.
41. Yagi, K., K.T. Kitazato, M. Uno, et al 2009. Edaravone, a free radical scavenger, inhibits MMP-9-related brain hemorrhage in rats treated with tissue plasminogen activator. Stroke 40: 626-631.
42. Pfefferkorn, T. & G.A. Rosenberg 2003. Closure of the blood-brain barrier by matrix metalloproteinase inhibition reduces rt-PA-mediated mortality in cerebral ischemia with delayed reperfusion. Stroke 34: 2025-2030.
43. Yepes, M., M. Sandkvist, E.G. Moore, et al 2003. Tissue-type plasminogen activator induces opening of the blood-brain barrier via the LDL receptor-related protein. J. Clin. Invest. 112: 1533-1540.
44. Zhang, C., J. An, W.B. Haile, et al 2009. Microglial low-density lipoprotein receptor-related protein 1 mediates the effect of tissue-type plasminogen activator on matrix metalloproteinase-9 activity in the ischemic brain. J. Cereb. Blood Flow Metab. 29: 1946-1954.
45. Asahi, M., K. Asahi, J.C. Jung, et al 2000. Role for matrix metalloproteinase 9 after focal cerebral ischemia: effects of gene knockout and enzyme inhibition with BB-94. J. Cereb. Blood Flow Metab. 20: 1681-1689.
46. Cuadrado, E., A. Rosell, A. Penalba, et al 2009. Vascular MMP-9/TIMP-2 and neuronal MMP-10 up-regulation in human brain after stroke: a combined laser microdissection and protein array study. J. Proteome. Res. 8: 3191-3197.
47. Haelewyn, B., J.J. Risso & J.H. Abraini 2010. Human recombinant tissue-plasminogen activator (alteplase): why not use the 'human' dose for stroke studies in rats? J. Cereb. Blood Flow Metab. 30: 900-903.
48. Simard, J.M., S.K. Woo, N. Tsymbalyuk, et al 2012. Glibenclamide - 10 hour treatment window in a clinically-relevant model of stroke. Transl. Stroke Res. 3: 286-295.
49. Kelly, M.A., A. Shuaib & K.G. Todd 2006. Matrix metalloproteinase activation and blood-brain barrier breakdown following thrombolysis. Exp. Neurol. 200: 38-49.
50. Li, M., Z. Zhang, W. Sun, et al 2011. 17beta-estradiol attenuates breakdown of blood-brain barrier and hemorrhagic transformation induced by tissue plasminogen activator in cerebral ischemia. Neurobiol. Dis. 44: 277-283.
51. Cheng, T., A.L. Petraglia, Z. Li, et al 2006. Activated protein C inhibits tissue plasminogen activator-induced brain hemorrhage. Nat. Med. 12: 1278-1285.
52. Ishiguro, M., K. Mishiro, Y. Fujiwara, et al 2010. Phosphodiesterase-III inhibitor prevents hemorrhagic transformation induced by focal cerebral ischemia in mice treated with tPA. PLoS. One 5: e15178.
53. Wang, X., S.R. Lee, K. Arai, et al 2003. Lipoprotein receptor-mediated induction of matrix metalloproteinase by tissue plasminogen activator. Nat. Med. 9: 1313-1317.
54. Copin, J.C., D.J. Bengualid, R.F. Da Silva, et al 2011. Recombinant tissue plasminogen activator induces blood-brain barrier breakdown by a matrix metalloproteinase-9-independent pathway after transient focal cerebral ischemia in mouse. Eur. J. Neurosci. 34: 1085-1092.
55. Kahles, T., C. Foerch, M. Sitzer, et al 2005. Tissue plasminogen activator mediated blood-brain barrier damage in transient focal cerebral ischemia in rats: relevance of interactions between thrombotic material and thrombolytic agent. Vascul. Pharmacol. 43: 254-259.
56. Hu, Q., C. Chen, N.H. Khatibi, et al 2011. Lentivirus-mediated transfer of MMP-9 shRNA provides neuroprotection following focal ischemic brain injury in rats. Brain Res. 1367: 347-359.
57. Hu, Q., C. Chen, J. Yan, et al 2009. Therapeutic application of gene silencing MMP-9 in a middle cerebral artery occlusion-induced focal ischemia rat model. Exp. Neurol. 216: 35-46.
58. Zhao, B.Q., Y. Ikeda, H. Ihara, et al 2004. Essential role of endogenous tissue plasminogen activator through matrix metalloproteinase 9 induction and expression on heparin-produced cerebral hemorrhage after cerebral ischemia in mice. Blood 103: 2610-2616.
59. Wang, Y.F., S.E. Tsirka, S. Strickland, et al 1998. Tissue plasminogen activator (tPA) increases neuronal damage after focal cerebral ischemia in wild-type and tPA-deficient mice. Nat. Med. 4: 228-231.
60. Park, C.H., T.K. Shin, H.Y. Lee, et al 2011. Matrix metalloproteinase inhibitors attenuate neuroinflammation following focal cerebral ischemia in mice Korean. J. Physiol. Pharmacol. 15: 115-122.
61. Lapchak, P.A., D.F. Chapman & J.A. Zivin 2000. Metalloproteinase inhibition reduces thrombolytic (tissue plasminogen activator)-induced hemorrhage after thromboembolic stroke. Stroke 31: 3034-3040.
62. Rosenberg, G.A., E.Y. Estrada & J.E. Dencoff 1998. Matrix metalloproteinases and TIMPs are associated with blood-brain barrier opening after reperfusion in rat brain. Stroke 29: 2189-2195.
63. Rosenberg, G.A., L.A. Cunningham, J. Wallace, et al 2001. Immunohistochemistry of matrix metalloproteinases in reperfusion injury to rat brain: activation of MMP-9 linked to stromelysin-1 and microglia in cell cultures. Brain Res. 893: 104-112.
64. Sood, R.R., S. Taheri, E. Candelario-Jalil, et al 2008. 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. 28: 431-438.
65. Yang, Y., E.Y. Estrada, J.F. Thompson, et al 2007. Matrix metalloproteinase-mediated disruption of tight junction proteins in cerebral vessels is reversed by synthetic matrix metalloproteinase inhibitor in focal ischemia in rat. J. Cereb. Blood Flow Metab. 27: 697-709.
66. Kang, S.S., J.H. Kook, S. Hwang, et al 2008. Inhibition of matrix metalloproteinase-9 attenuated neural progenitor cell migration after photothrombotic ischemia. Brain Res. 1228: 20-26.
67. Gu, Z., J. Cui, S. Brown, et al 2005. A highly specific inhibitor of matrix metalloproteinase-9 rescues laminin from proteolysis and neurons from apoptosis in transient focal cerebral ischemia. J. Neurosci. 25: 6401-6408.
68. Lee, S.R., H.Y. Kim, J. Rogowska, et al 2006. Involvement of matrix metalloproteinase in neuroblast cell migration from the subventricular zone after stroke. J. Neurosci. 26: 3491-3495.
69. Barkho, B.Z., A.E. Munoz, X. Li, et al 2008. Endogenous matrix metalloproteinase (MMP)-3 and MMP-9 promote the differentiation and migration of adult neural progenitor cells in response to chemokines. Stem Cells 26: 3139-3149.
70. Zhao, B.Q., E. Tejima & E.H. Lo 2007. Neurovascular proteases in brain injury, hemorrhage and remodeling after stroke. Stroke 38: 748-752.
71. Griffin, M.O., E. Fricovsky, G. Ceballos & F. Villarreal 2010. Tetracyclines: a pleitropic family of compounds with promising therapeutic properties. Review of the literature. Am. J. Physiol. Cell Physiol. 299: C539-C548.
72. Wang, Z., Y. Xue, H. Jiao, et al 2012. Doxycycline-mediated protective effect against focal cerebral ischemia-reperfusion injury through the modulation of tight junctions and PKCdelta signaling in rats. J. Mol. Neurosci. 47: 89-100.
73. Lee, H., J.W. Park, S.P. Kim, et al 2009. Doxycycline inhibits matrix metalloproteinase-9 and laminin degradation after transient global cerebral ischemia. Neurobiol. Dis. 34: 189-198.
74. Koistinaho, M., T.M. Malm, M.I. Kettunen, et al 2005. Minocycline protects against permanent cerebral ischemia in wild type but not in matrix metalloprotease-9-deficient mice. J. Cereb. Blood Flow Metab. 25: 460-467.
75. Machado, L.S., I.Y. Sazonova, A. Kozak, et al 2009. Minocycline and tissue-type plasminogen activator for stroke: assessment of interaction potential. Stroke 40: 3028-3033.
76. Nagel, S., Y. Su, S. Horstmann, et al 2008. Minocycline and hypothermia for reperfusion injury after focal cerebral ischemia in the rat: effects on BBB breakdown and MMP expression in the acute and subacute phase. Brain Res. 1188: 198-206.
77. Machado, L.S., A. Kozak, A. Ergul, et al 2006. Delayed minocycline inhibits ischemia-activated matrix metalloproteinases 2 and 9 after experimental stroke. BMC Neurosci. 7: 56.
78. Switzer, J.A., D.C. Hess, A. Ergul, et al 2011. Matrix metalloproteinase-9 in an exploratory trial of intravenous minocycline for acute ischemic stroke. Stroke 42: 2633-2635.
79. Kolev, K., J. Skopal, L. Simon, et al 2003. Matrix metalloproteinase-9 expression in post-hypoxic human brain capillary endothelial cells: H2O2 as a trigger and NF-kappaB as a signal transducer. Thromb. Haemost. 90: 528-537.
80. Liu, N., J. Shang, F. Tian, et al 2011. In vivo optical imaging for evaluating the efficacy of edaravone after transient cerebral ischemia in mice. Brain Res. 1397: 66-75.
81. Lee, J.K., H.J. Kwak, M.S. Piao, et al 2011. Quercetin reduces the elevated matrix metalloproteinases-9 level and improves functional outcome after cerebral focal ischemia in rats. Acta Neurochir. (Wien.) 153: 1321-1329.
82. Nagel, S., J. Genius, S. Heiland, et al 2007. Diphenyleneiodonium and dimethylsulfoxide for treatment of reperfusion injury in cerebral ischemia of the rat. Brain Res. 1132: 210-217.
83. Gao, D., X. Zhang, X. Jiang, et al 2006. Resveratrol reduces the elevated level of MMP-9 induced by cerebral ischemia-reperfusion in mice. Life Sci. 78: 2564-2570.
84. Yamashita, T., T. Kamiya, K. Deguchi, et al 2009. Dissociation and protection of the neurovascular unit after thrombolysis and reperfusion in ischemic rat brain. J. Cereb. Blood Flow Metab. 29: 715-725.
85. Zhang, W., K. Sato, T. Hayashi, et al 2004. Extension of ischemic therapeutic time window by a free radical scavenger, Edaravone, reperfused with tPA in rat brain. Neurol. Res. 26: 342-348.
86. Lapchak, P.A. 2010. A critical assessment of edaravone acute ischemic stroke efficacy trials: is edaravone an effective neuroprotective therapy? Expert Opin. Pharmacother. 11: 1753-1763.
87. Isahaya, K., K. Yamada, M. Yamatoku, et al 2012. Effects of Edaravone, a free radical scavenger, on serum levels of inflammatory biomarkers in acute brain infarction. J. Stroke Cerebrovasc. Dis. 21: 102-107.
88. Abumiya, T., C. Yokota, Y. Kuge & K. Minematsu 2005. Aggravation of hemorrhagic transformation by early intraarterial infusion of low-dose vascular endothelial growth factor after transient focal cerebral ischemia in rats. Brain Res. 1049: 95-103.
89. Valable, S., J. Montaner, A. Bellail, et al 2005. VEGF-induced BBB permeability is associated with an MMP-9 activity increase in cerebral ischemia: both effects decreased by Ang-1. J. Cereb. Blood Flow Metab. 25: 1491-1504.
90. Tu, X.K., W.Z. Yang, S.S. Shi, et al 2009. 5-lipoxygenase inhibitor zileuton attenuates ischemic brain damage: involvement of matrix metalloproteinase 9. Neurol. Res. 31: 848-852.
91. Liu, X.S., Z.G. Zhang, L. Zhang, et al 2006. Atorvastatin downregulates tissue plasminogen activator-aggravated genes mediating coagulation and vascular permeability in single cerebral endothelial cells captured by laser microdissection. J. Cereb. Blood Flow Metab. 26: 787-796.
92. Zhang, L., Z.G. Zhang, G.L. Ding, et al 2005. Multitargeted effects of statin-enhanced thrombolytic therapy for stroke with recombinant human tissue-type plasminogen activator in the rat. Circulation 112: 3486-3494.
93. Kawai, H., S. Deguchi, K. Deguchi, et al 2011. Protection against ischemic stroke damage by synergistic treatment with amlodipine plus atorvastatin in Zucker metabolic rat. Brain Res. 1382: 308-314.
94. Liu, R., Y. Wen, E. Perez, et al 2005. 17beta-Estradiol attenuates blood-brain barrier disruption induced by cerebral ischemia-reperfusion injury in female rats. Brain Res. 1060: 55-61.
95. Liu, R., Q. Liu, S. He, et al 2010. Combination therapy of 17beta-estradiol and recombinant tissue plasminogen activator for experimental ischemic stroke. J. Pharmacol. Exp. Ther. 332: 1006-1012.
96. Hung, Y.C., T.Y. Chen, E.J. Lee, et al 2008. Melatonin decreases matrix metalloproteinase-9 activation and expression and attenuates reperfusion-induced hemorrhage following transient focal cerebral ischemia in rats. J. Pineal Res. 45: 459-467.
97. Tai, S.H., H.Y. Chen, E.J. Lee, et al 2010. Melatonin inhibits postischemic matrix metalloproteinase-9 (MMP-9) activation via dual modulation of plasminogen/plasmin system and endogenous MMP inhibitor in mice subjected to transient focal cerebral ischemia. J. Pineal Res. 49: 332-341.
98. Guan, W., A. Kozak, A.B. El-Remessy, et al 2011. Acute treatment with Candesartan reduces early injury after permanent middle cerebral artery occlusion. Transl. Stroke Res. 2: 179-185.
99. Simard, J.M., S.K. Woo, S. Bhatta & V. Gerzanich 2008. Drugs acting on SUR1 to treat CNS ischemia and trauma. Curr. Opin. Pharmacol. 8: 42-49.
100. Simard, J.M., O. Tsymbalyuk, A. Ivanov, et al 2007. Endothelial sulfonylurea receptor 1-regulated NC Ca-ATP channels mediate progressive hemorrhagic necrosis following spinal cord injury. J. Clin. Invest. 117: 2105-2113.
101. Colucci, M., S. Scopece, A.V. Gelato, et al 1997. In vitro clot lysis as a potential indicator of thrombus resistance to fibrinolysis-study in healthy subjects and correlation with blood fibrinolytic parameters. Thromb. Haemost. 77: 725-729.
102. Korninger, C. & D. Collen 1981. Studies on the specific fibrinolytic effect of human extrinsic (tissue-type) plasminogen activator in human blood and in various animal species in vitro. Thromb. Haemost. 46: 561-565.
103. Del Zoppo, G.J., K. Poeck, M.S. Pessin, et al 1992. Recombinant tissue plasminogen activator in acute thrombotic and embolic stroke. Ann. Neurol. 32: 78-86.
104. Von, K.R., R. Holle, L. Rosin, et al 1995. Does arterial recanalization improve outcome in carotid territory stroke? Stroke 26: 581-587.
105. Del Zoppo, G.J., J.L. Saver, E.C. Jauch & H.P. Adams, Jr. 2009. Expansion of the time window for treatment of acute ischemic stroke with intravenous tissue plasminogen activator: a science advisory from the American Heart Association/American Stroke Association. Stroke 40: 2945-2948.
106. Del Zoppo, G.J., R. Milner, T. Mabuchi, et al 2007. Microglial activation and matrix protease generation during focal cerebral ischemia. Stroke 38: 646-651.
107. Del Zoppo, G.J., H. Frankowski, Y.H. Gu, et al 2012. Microglial cell activation is a source of metalloproteinase generation during hemorrhagic transformation. J. Cereb. Blood Flow Metab. 32: 919-932.
108. Aoki, T., T. Sumii, T. Mori, et al 2002. Blood-brain barrier disruption and matrix metalloproteinase-9 expression during reperfusion injury: mechanical versus embolic focal ischemia in spontaneously hypertensive rats. Stroke 33: 2711-2717.
109. Rosell, A., A. Ortega-Aznar, J. Alvarez-Sabin, et al 2006. Increased brain expression of matrix metalloproteinase-9 after ischemic and hemorrhagic human stroke. Stroke 37: 1399-1406.
110. Kunte, H., S. Schmidt, M. Eliasziw, et al 2007. Sulfonylureas improve outcome in patients with type 2 diabetes and acute ischemic stroke. Stroke 38: 2526-2530.
111. Weih, M., N. Amberger, S. Wegener, et al 2001. Sulfonylurea drugs do not influence initial stroke severity and in-hospital outcome in stroke patients with diabetes. Stroke 32: 2029-2032.
112. Silver, F.L., J. Fang, A.C. Robertson, et al 2009. Possible neuroprotective effects of sufonylureas in diabetic patients with acute ischemic stroke. Abstracts from the 2009 International Stroke Conference. Stroke 40: e156 [P19, http://stroke.ahajournals.org/cgi/reprint/40/4/e105].
113. Callahan, A., P. Amarenco, L.B. Goldstein, et al 2011. Risk of stroke and cardiovascular events after ischemic stroke or transient ischemic attack in patients with type 2 diabetes or metabolic syndrome: secondary analysis of the Stroke Prevention by Aggressive Reduction in Cholesterol Levels (SPARCL) trial. Arch. Neurol. 68: 1245-1251.
114. Ergul, A., A. Kelly-Cobbs, M. Abdalla & S.C. Fagan 2011. Cerebrovascular complications of diabetes: focus on stroke. Transl. Stroke Res. 2: 391-398.
115. Martini, S.R. & T.A. Kent 2007. Hyperglycemia in acute ischemic stroke: a vascular perspective. J. Cereb. Blood Flow Metab. 27: 435-451.
116. Elgebaly, M.M., S. Ogbi, W. Li, et al 2011. Neurovascular injury in acute hyperglycemia and diabetes: a comparative analysis in experimental stroke. Transl. Stroke Res. 2: 391-398.