Chapter 6 Reperfusion injury after stroke: neurovascular proteases and the blood-brain barrier

Handbook of Clinical Neurology

Volumn 92, Issue , 2008, Pages 117-136

  Ning, MingMing ^a   Wang, Xiaoying ^a   Lo, Eng H ^a  

^a MASSACHUSETTS GENERAL HOSPITAL   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

EID: 66049117375     PISSN: 00729752     EISSN: None     Source Type: Book Series    
DOI: 10.1016/S0072-9752(08)01906-4     Document Type: Review

References (206)

1. Abe K., Yoshidomi M., and Kogure K. Arachidonic acid metabolism in ischemic neuronal damage. Ann N Y Acad Sci 559 (1989) 259-268
2. Abilleira S., Montaner J., Molina C.A., et al. Matrix metalloproteinase-9 concentration after spontaneous intracerebral hemorrhage. J Neurosurg 99 (2003) 65-70
3. Abrahamson D.R. Recent studies on the structure and pathology of basement membranes. J Pathol 149 (1986) 257-278
4. Adamson P., Etienne S., Couraud P.O., et al. Lymphocyte migration through brain endothelial cell monolayers involves signaling through endothelial ICAM-1 via a rho-dependent pathway. J Immunol 162 (1999) 2964-2973
5. Ahn M.Y., Zhang Z.G., Tsang W., et al. Endogenous plasminogen activator expression after embolic focal cerebral ischemia in mice. Brain Res 837 (1999) 169-176
6. Akassoglou K., Kombrinck K.W., Degen J.L., et al. Tissue plasminogen activator-mediated fibrinolysis protects against axonal degeneration and demyelination after sciatic nerve injury. J Cell Biol 149 (2000) 1157-1166
7. Allport J.R., Ding H., Collins T., et al. Endothelial-dependent mechanisms regulate leukocyte transmigration: a process involving the proteasome and disruption of the vascular endothelial-cadherin complex at endothelial cell-to-cell junctions. J Exp Med 186 (1997) 517-527
8. Alvarez-Sabin J., Molina C.A., Montaner J., et al. Effects of admission hyperglycemia on stroke outcome in reperfused tissue plasminogen activator-treated patients. Stroke 34 (2003) 1235-1241
9. Ames III A., Wright R.L., Kowada M., et al. Cerebral ischemia. II. The no-reflow phenomenon. Am J Pathol 52 (1968) 437-453
10. Anthony D.C., Miller K.M., Fearn S., et al. Matrix metalloproteinase expression in an experimentally-induced DTH model of multiple sclerosis in the rat CNS. J Neuroimmunol 87 (1998) 62-72
11. Aoki T., Sumii T., Mori T., et al. Blood-brain barrier disruption and matrix metalloproteinase-9 expression during reperfusion injury: mechanical versus embolic focal ischemia in spontaneously hypertensive rats. Stroke 33 (2002) 2711-2717
12. Armao D., Kornfeld M., Estrada E.Y., et al. Neutral proteases and disruption of the blood-brain barrier in rat. Brain Res 767 (1997) 259-264
13. Armstead W.M., Nassar T., Akkawi S., et al. Neutralizing the neurotoxic effects of exogenous and endogenous tPA. Nat Neurosci 9 (2006) 1150-1155
14. Aronowski J., Strong R., and Grotta J.C. Reperfusion injury: demonstration of brain damage produced by reperfusion after transient focal ischemia in rats. J Cereb Blood Flow Metab 17 (1997) 1048-1056
15. Arrell D.K., Neverova I., and Van Eyk J.E. Cardiovascular proteomics: evolution and potential. Circ Res 88 (2001) 763-773
16. Arvidsson A., Collin T., Kirik D., et al. Neuronal replacement from endogenous precursors in the adult brain after stroke. Nat Med 8 (2002) 963-970
17. Asahi M., Asahi K., Jung J.C., et al. 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 (2000) 1681-1689
18. Asahi M., Asahi K., Wang X., et al. Reduction of tissue plasminogen activator-induced hemorrhage and brain injury by free radical spin trapping after embolic focal cerebral ischemia in rats. J Cereb Blood Flow Metab 20 (2000) 452-457
19. Asahi M., Wang X., Mori T., et al. 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 (2001) 7724-7732
20. Asahi M., Rammohan R., Sumii T., et al. Antiactin-targeted immunoliposomes ameliorate tissue plasminogen activator-induced hemorrhage after focal embolic stroke. J Cereb Blood Flow Metab 23 (2003) 895-899
21. Backstrom J.R., Lim G.P., Cullen M.J., et al. Matrix metalloproteinase-9 (MMP-9) is synthesized in neurons of the human hippocampus and is capable of degrading the amyloid-beta peptide (1-40). J Neurosci 16 (1996) 7910-7919
22. Baggiolini M. Chemokines and leukocyte traffic. Nature 392 (1998) 565-568
23. Bajetto A., Bonavia R., Barbero S., et al. Characterization of chemokines and their receptors in the central nervous system: physiopathological implications. J Neurochem 82 (2002) 1311-1329
24. Baranes D., Lederfein D., Huang Y.Y., et al. Tissue plasminogen activator contributes to the late phase of LTP and to synaptic growth in the hippocampal mossy fiber pathway. Neuron 21 (1998) 813-825
25. Barone F.C., and Feuerstein G.Z. Inflammatory mediators and stroke: new opportunities for novel therapeutics. J Cereb Blood Flow Metab 19 (1999) 819-834
26. Batjer H.H., Devous Sr. M.D., Meyer Y.J., et al. Cerebrovascular hemodynamics in arteriovenous malformation complicated by normal perfusion pressure breakthrough. Neurosurgery 22 (1988) 503-509
27. Bergers G., Brekken R., McMahon G., et al. Matrix metalloproteinase-9 triggers the angiogenic switch during carcinogenesis. Nat Cell Biol 2 (2000) 737-744
28. Bignami A., Cella G., and Chi N.H. Plasminogen activators in rat neural tissues during development and in Wallerian degeneration. Acta Neuropathol (Berl) 58 (1982) 224-228
29. Bolton S.J., Anthony D.C., and Perry V.H. Loss of the tight junction proteins occludin and zonula occludens-1 from cerebral vascular endothelium during neutrophil-induced blood-brain barrier breakdown in vivo. Neuroscience 86 (1998) 1245-1257
30. Brown R.C., and Davis T.P. Calcium modulation of adherens and tight junction function: a potential mechanism for blood-brain barrier disruption after stroke. Stroke 33 (2002) 1706-1711
31. Bruno A., Biller J., Adams Jr. H.P., et al. Acute blood glucose level and outcome from ischemic stroke. Trial of ORG 10172 in Acute Stroke Treatment (TOAST) Investigators. Neurology 52 (1999) 280-284
32. Calabresi P., Napolitano M., Centonze D., et al. Tissue plasminogen activator controls multiple forms of synaptic plasticity and memory. Eur J Neurosci 12 (2000) 1002-1012
33. Cannon III R.O. Mechanisms, management and future directions for reperfusion injury after acute myocardial infarction. Nat Clin Pract Cardiovasc Med 2 (2005) 88-94
34. Carroll P.M., Tsirka S.E., Richards W.G., et al. The mouse tissue plasminogen activator gene 5′ flanking region directs appropriate expression in development and a seizure-enhanced response in the CNS. Development 120 (1994) 3173-3183
35. Castellanos M., Leira R., Serena J., et al. Plasma metalloproteinase-9 concentration predicts hemorrhagic transformation in acute ischemic stroke. Stroke 34 (2003) 40-46
36. Chan P.H. Oxygen radicals in focal cerebral ischemia. Brain Pathol 4 (1994) 59-65
37. Chan P.H. Role of oxidants in ischemic brain damage. Stroke 27 (1996) 1124-1129
38. Chan P.H. Reactive oxygen radicals in signaling and damage in the ischemic brain. J Cereb Blood Flow Metab 21 (2001) 2-14
39. Che X., Ye W., Panga L., et al. Monocyte chemoattractant protein-1 expressed in neurons and astrocytes during focal ischemia in mice. Brain Res 902 (2001) 171-177
40. Chen Z.L., and Strickland S. Neuronal death in the hippocampus is promoted by plasmin-catalyzed degradation of laminin. Cell 91 (1997) 917-925
41. Chen Z.L., Yoshida S., Kato K., et al. Expression and activity-dependent changes of a novel limbic-serine protease gene in the hippocampus. J Neurosci 15 (1995) 5088-5097
42. Couraud P.O. Infiltration of inflammatory cells through brain endothelium. Pathol Biol (Paris) 46 (1998) 176-180
43. Coutts S.B., Hill M.D., and Hu W.Y. Hyperperfusion syndrome: toward a stricter definition. Neurosurgery 53 (2003) 1053-1058 discussion 1058-1060
44. Croll S.D., and Wiegand S.J. Vascular growth factors in cerebral ischemia. Mol Neurobiol 23 (2001) 121-135
45. Cserr H.F., and Bundgaard M. The neuronal microenvironment: a comparative view. Ann N Y Acad Sci 481 (1986) 1-6
46. Davies B.J., Pickard B.S., Steel M., et al. Serine proteases in rodent hippocampus. J Biol Chem 273 (1998) 23004-23011
47. De Crespigny A.J., Wendland M.F., Derugin N., et al. Real-time observation of transient focal ischemia and hyperemia in cat brain. Magn Reson Med 27 (1992) 391-397
48. Del Zoppo G.J., and Hallenbeck J.M. Advances in the vascular pathophysiology of ischemic stroke. Thromb Res 98 (2000) 73-81
49. Demchuk A.M., Morgenstern L.B., Krieger D.W., et al. Serum glucose level and diabetes predict tissue plasminogen activator-related intracerebral hemorrhage in acute ischemic stroke. Stroke 30 (1999) 34-39
50. Diener H.C., Lees K.R., Lyden P., et al. NXY-059 for the treatment of acute stroke. Pooled Analysis of the SAINT I and II Trials. Stroke (2008) Mar 2008. [Epub]
51. Eberhardt W., Beck K.F., and Pfeilschifter J. Cytokine-induced expression of tPA is differentially modulated by NO and reactive oxygen species in rat mesangial cells. Kidney Int 61 (2002) 20-30
52. Egeblad M., and Werb Z. New functions for the matrix metalloproteinases in cancer progression. Nat Rev Cancer 2 (2002) 161-174
53. Etienne-Manneville S., Manneville J.B., Adamson P., et al. ICAM-1-coupled cytoskeletal rearrangements and transendothelial lymphocyte migration involve intracellular calcium signaling in brain endothelial cell lines. J Immunol 165 (2000) 3375-3383
54. Fernandez-Monreal M., Lopez-Atalaya J.P., Benchenane K., et al. Is tissue-type plasminogen activator a neuromodulator?. Mol Cell Neurosci 25 (2004) 594-601
55. Fingleton B., Vargo-Gogola T., Crawford H.C., et al. Matrilysin (MMP-7) expression selects for cells with reduced sensitivity to apoptosis. Neoplasia 3 (2001) 459-468
56. Fini M.E., Cook J.R., Mohan R., et al. Regulation of matrix metalloproteinase gene expression. In: Parkers W.C., and Mecham R.P. (Eds). Matrix Metalloproteinases (1998), Academic Press, New York 299-356
57. Fischer S., Clauss M., Wiesnet M., et al. Hypoxia induces permeability in brain microvessel endothelial cells via VEGF and NO. Am J Physiol 276 (1999) C812-C820
58. Fischer S., Wobben M., Kleinstuck J., et al. Effect of astroglial cells on hypoxia-induced permeability in PBMEC cells. Am J Physiol Cell Physiol 279 (2000) C935-C944
59. Fishman R.A. Brain edema. N Engl J Med 293 (1975) 706-711
60. Franko J., Pomfy M., Novakova B., et al. Stobadine protects against ischemia-reperfusion induced morphological alterations of cerebral microcirculation in dogs. Life Sci 65 (1999) 1963-1967
61. Frey U., Muller M., and Kuhl D. A different form of long-lasting potentiation revealed in tissue plasminogen activator mutant mice. J Neurosci 16 (1996) 2057-2063
62. Friedman G.C., and Seeds N.W. Tissue plasminogen activator mRNA expression in granule neurons coincides with their migration in the developing cerebellum. J Comp Neurol 360 (1995) 658-670
63. Frisch S.M., and Francis H. Disruption of epithelial cell-matrix interactions induces apoptosis. J Cell Biol 124 (1994) 619-626
64. Fujimura M., Gasche Y., Morita-Fujimura Y., et al. Early appearance of activated matrix metalloproteinase-9 and blood-brain barrier disruption in mice after focal cerebral ischemia and reperfusion. Brain Res 842 (1999) 92-100
65. Gao E., Young W.L., Ornstein E., et al. A theoretical model of cerebral hemodynamics: application to the study of arteriovenous malformations. J Cereb Blood Flow Metab 17 (1997) 905-918
66. Gasche Y., Copin J.C., Sugawara T., et al. Matrix metalloproteinase inhibition prevents oxidative stress-associated blood-brain barrier disruption after transient focal cerebral ischemia. J Cereb Blood Flow Metab 21 (2001) 1393-1400
67. Geng J.G., Bevilacqua M.P., Moore K.L., et al. Rapid neutrophil adhesion to activated endothelium mediated by GMP-140. Nature 343 (1990) 757-760
68. Gingrich M.B., Junge C.E., Lyuboslavsky P., et al. Potentiation of NMDA receptor function by the serine protease thrombin. J Neurosci 20 (2000) 4582-4595
69. Giulian D., Woodward J., Young D.G., et al. Interleukin-1 injected into mammalian brain stimulates astrogliosis and neovascularization. J Neurosci 8 (1988) 2485-2490
70. Glaser K.B., Mobilio D., Chang J.Y., et al. Phospholipase A2 enzymes: regulation and inhibition. Trends Pharmacol Sci 14 (1993) 92-98
71. Gschwend T.P., Krueger S.R., Kozlov S.V., et al. Neurotrypsin, a novel multidomain serine protease expressed in the nervous system. Mol Cell Neurosci 9 (1997) 207-219
72. Gu Z., Kaul M., Yan B., et al. S-nitrosylation of matrix metalloproteinases: signaling pathway to neuronal cell death. Science 297 (2002) 1186-1190
73. Gualandris A., Jones T.E., Strickland S., et al. Membrane depolarization induces calcium-dependent secretion of tissue plasminogen activator. J Neurosci 16 (1996) 2220-2225
74. Haddad J.J. Redox regulation of pro-inflammatory cytokines and iκb-α/NF-κb nuclear translocation and activation. Biochem Biophys Res Commun 296 (2002) 847-856
75. Hallenbeck J.M., and Dutka A.J. Background review and current concepts of reperfusion injury. Arch Neurol 47 (1990) 1245-1254
76. Hamann G.F., Okada Y., Fitridge R., et al. Microvascular basal lamina antigens disappear during cerebral ischemia and reperfusion. Stroke 26 (1995) 2120-2126
77. Hamann G.F., Okada Y., and del Zoppo G.J. Hemorrhagic transformation and microvascular integrity during focal cerebral ischemia/reperfusion. J Cereb Blood Flow Metab 16 (1996) 1373-1378
78. Haraldsen G., Kvale D., Lien B., et al. Cytokine-regulated expression of E-selectin, intercellular adhesion molecule-1 (ICAM-1), and vascular cell adhesion molecule-1 (VCAM-1) in human microvascular endothelial cells. J Immunol 156 (1996) 2558-2565
79. Heiss W.D. Experimental evidence of ischemic thresholds and functional recovery. Stroke 23 (1992) 1668-1672
80. Heissig B., Rafii S., Akiyama H., et al. Low-dose irradiation promotes tissue revascularization through VEGF release from mast cells and MMP-9-mediated progenitor cell mobilization. J Exp Med 202 (2005) 739-750
81. Heo J.H., Lucero J., Abumiya T., et al. Matrix metalloproteinases increase very early during experimental focal cerebral ischemia. J Cereb Blood Flow Metab 19 (1999) 624-633
82. Hoffman K.B., Larson J., Bahr B.A., et al. Activation of NMDA receptors stimulates extracellular proteolysis of cell adhesion molecules in hippocampus. Brain Res 811 (1998) 152-155
83. Holmin S., and Mathiesen T. Intracerebral administration of interleukin-1beta and induction of inflammation, apoptosis, and vasogenic edema. J Neurosurg 92 (2000) 108-120
84. Hosomi N., Lucero J., Heo J.H., et al. Rapid differential endogenous plasminogen activator expression after acute middle cerebral artery occlusion. Stroke 32 (2001) 1341-1348
85. Huang Y.Y., Bach M.E., Lipp H.P., et al. Mice lacking the gene encoding tissue-type plasminogen activator show a selective interference with late-phase long-term potentiation in both Schaffer collateral and mossy fiber pathways. Proc Natl Acad Sci USA 93 (1996) 8699-8704
86. Huber J.D., Egleton R.D., and Davis T.P. Molecular physiology and pathophysiology of tight junctions in the blood-brain barrier. Trends Neurosci 24 (2001) 719-725
87. Inoue N., Takeshita S., Gao D., et al. Lysophosphatidylcholine increases the secretion of matrix metalloproteinase 2 through the activation of NADH/NADPH oxidase in cultured aortic endothelial cells. Atherosclerosis 155 (2001) 45-52
88. Janoff A., and Scherer J. Mediators of inflammation in leukocyte lysosomes. IX. Elastinolytic activity in granules of human polymorphonuclear leukocytes. J Exp Med 128 (1968) 1137-1155
89. Jiang X., Namura S., and Nagata I. Matrix metalloproteinase inhibitor KB-R7785 attenuates brain damage resulting from permanent focal cerebral ischemia in mice. Neurosci Lett 305 (2001) 41-44
90. Karlsson B.R., Grogaard B., Gerdin B., et al. The severity of postischemic hypoperfusion increases with duration of cerebral ischemia in rats. Acta Anaesthesiol Scand 38 (1994) 248-253
91. Kase C.S., Furlan A.J., Wechsler L.R., et al. Cerebral hemorrhage after intra-arterial thrombolysis for ischemic stroke: the PROACT II trial. Neurology 57 (2001) 1603-1610
92. Kaur J., Zhao Z., Klein G.M., et al. The neurotoxicity of tissue plasminogen activator?. J Cereb Blood Flow Metab 24 (2004) 945-963
93. Kelly P.J., Morrow J.D., Ning M., et al. Oxidative stress and matrix metalloproteinase-9 in acute ischemic stroke: the Biomarker Evaluation for Antioxidant Therpay in Stroke (BEAT-Stroke) Study. Stroke 39 (2008) 100-104
94. Kim G.W., Lewen A., Copin J., et al. The cytosolic antioxidant, copper/zinc superoxide dismutase, attenuates blood-brain barrier disruption and oxidative cellular injury after photothrombotic cortical ischemia in mice. Neuroscience 105 (2001) 1007-1018
95. Kondo T., Kinouchi H., Kawase M., et al. Astroglial cells inhibit the increasing permeability of brain endothelial cell monolayer following hypoxia/reoxygenation. Neurosci Lett 208 (1996) 101-104
96. Kondo T., Reaume A.G., Huang T.T., et al. Reduction of CuZn-superoxide dismutase activity exacerbates neuronal cell injury and edema formation after transient focal cerebral ischemia. J Neurosci 17 (1997) 4180-4189
97. Krystosek A., and Seeds N.W. Plasminogen activator release at the neuronal growth cone. Science 213 (1981) 1532-1534
98. Krystosek A., and Seeds N.W. Peripheral neurons and Schwann cells secrete plasminogen activator. J Cell Biol 98 (1984) 773-776
99. Kuroiwa T., Ting P., Martinez H., et al. The biphasic opening of the blood-brain barrier to proteins following temporary middle cerebral artery occlusion. Acta Neuropathol (Berl) 68 (1985) 122-129
100. Lapchak P.A. Hemorrhagic transformation following ischemic stroke: significance, causes, and relationship to therapy and treatment. Curr Neurol Neurosci Rep 2 (2002) 38-43
101. Lapchak P.A., Chapman D.F., and Zivin J.A. Metalloproteinase inhibition reduces thrombolytic (tissue plasminogen activator)-induced hemorrhage after thromboembolic stroke. Stroke 31 (2000) 3034-3040
102. Lapchak P.A., Chapman D.F., and Zivin J.A. Pharmacological effects of the spin trap agents N-t-butyl-phenylnitrone (PBN) and 2,2,6, 6-tetramethylpiperidine-N-oxyl (TEMPO) in a rabbit thromboembolic stroke model: combination studies with the thrombolytic tissue plasminogen activator. Stroke 32 (2001) 147-153
103. Larsen P.H., DaSilva A.G., Conant K., et al. Myelin formation during development of the CNS is delayed in matrix metalloproteinase-9 and -12 null mice. J Neurosci 26 (2006) 2207-2214
104. Lee S.R., and Lo E.H. Induction of caspase-mediated cell death by matrix metalloproteinases in cerebral endothelial cells after hypoxia-reoxygenation. J Cereb Blood Flow Metab 24 (2004) 720-727
105. Lee S.R., Kim H.Y., Rogowska J., et al. Involvement of matrix metalloproteinase in neuroblast cell migration from the subventricular zone after stroke. J Neurosci 26 (2006) 3491-3495
106. Lees K.R., Zivin J.A., Ashwood T., et al. NXY-059 for acute ischemic stroke. N Engl J Med 354 (2006) 588-600
107. Lien Y.H., Lai L.W., and Silva A.L. Pathogenesis of renal ischemia/reperfusion injury: lessons from knockout mice. Life Sci 74 (2003) 543-552
108. Lijnen H.R. Plasmin and matrix metalloproteinases in vascular remodeling. Thromb Haemost 86 (2001) 324-333
109. Liotta L.A., Ferrari M., and Petricoin E. Clinical proteomics: written in blood. Nature 425 (2003) 905
110. Lo E.H. A haemodynamic analysis of intracranial arteriovenous malformations. Neurol Res 15 (1993) 51-55
111. Lo E.H., Wang X., and Cuzner M.L. Extracellular proteolysis in brain injury and inflammation: role for plasminogen activators and matrix metalloproteinases. J Neurosci Res 69 (2002) 1-9
112. Lo E.H., Dalkara T., and Moskowitz M.A. Mechanisms, challenges and opportunities in stroke. Nat Rev Neurosci 4 (2003) 399-415
113. Lo E.H., Broderick J.P., and Moskowitz M.A. tPA and proteolysis in the neurovascular unit. Stroke 35 (2004) 354-356
114. Lopez-Otin C., and Overall C.M. Protease degradomics: a new challenge for proteomics. Nat Rev Mol Cell Biol 3 (2002) 509-519
115. McCord J.M. Oxygen-derived free radicals in postischemic tissue injury. N Engl J Med 312 (1985) 159-163
116. McQuibban G.A., Gong J.H., Tam E.M., et al. Inflammation dampened by gelatinase A cleavage of monocyte chemoattractant protein-3. Science 289 (2000) 1202-1206
117. McQuibban G.A., Butler G.S., Gong J.H., et al. Matrix metalloproteinase activity inactivates the CXC chemokine stromal cell-derived factor-1. J Biol Chem 276 (2001) 43503-43508
118. Madani R., Hulo S., Toni N., et al. Enhanced hippocampal long-term potentiation and learning by increased neuronal expression of tissue-type plasminogen activator in transgenic mice. EMBO J 18 (1999) 3007-3012
119. Maeda M., Furuichi Y., Ueyama N., et al. A combined treatment with tacrolimus (FK506) and recombinant tissue plasminogen activator for thrombotic focal cerebral ischemia in rats: increased neuroprotective efficacy and extended therapeutic time window. J Cereb Blood Flow Metab 22 (2002) 1205-1211
120. Maier C.M., Hsieh L., Yu F., et al. Matrix metalloproteinase-9 and myeloperoxidase expression: quantitative analysis by antigen immunohistochemistry in a model of transient focal cerebral ischemia. Stroke 35 (2004) 1169-1174
121. Mark K.S., and Davis T.P. Cerebral microvascular changes in permeability and tight junctions induced by hypoxia-reoxygenation. Am J Physiol Heart Circ Physiol 282 (2002) H1485-H1494
122. Marti H.J., Bernaudin M., Bellail A., et al. Hypoxia-induced vascular endothelial growth factor expression precedes neovascularization after cerebral ischemia. Am J Pathol 156 (2000) 965-976
123. Martini S.R., Hill M.D., Alexandrov A.V., et al. Outcome in hyperglycemic stroke with ultrasound-augmented thrombolytic therapy. Neurology 67 (2006) 700-702
124. Memezawa H., Smith M.L., and Siesjo B.K. Penumbral tissues salvaged by reperfusion following middle cerebral artery occlusion in rats. Stroke 23 (1992) 552-559
125. Mohan P.S., and Spiro R.G. Macromolecular organization of basement membranes. Characterization and comparison of glomerular basement membrane and lens capsule components by immunochemical and lectin affinity procedures. J Biol Chem 261 (1986) 4328-4336
126. Molina C.A., Alvarez-Sabin J., Montaner J., et al. Thrombolysis-related hemorrhagic infarction: a marker of early reperfusion, reduced infarct size, and improved outcome in patients with proximal middle cerebral artery occlusion. Stroke 33 (2002) 1551-1556
127. Montaner J., Alvarez-Sabin J., Molina C.A., et al. Matrix metalloproteinase expression is related to hemorrhagic transformation after cardioembolic stroke. Stroke 32 (2001) 2762-2767
128. Montaner J., Alvarez-Sabin J., Molina C., et al. Matrix metalloproteinase expression after human cardioembolic stroke: temporal profile and relation to neurological impairment. Stroke 32 (2001) 1759-1766
129. Montaner J., Molina C.A., Monasterio J., et al. Matrix metalloproteinase-9 pretreatment level predicts intracranial hemorrhagic complications after thrombolysis in human stroke. Circulation 107 (2003) 598-603
130. Montaner J., Molina C.A., Arenillas J.F., et al. Proteolytic modifications on the metalloproteinase system (MMP-9-Laminin-TIMP-1) induced by t-PA treatment for acute cerebral ischemia in humans. Stroke 35 (2004) 339
131. Mori T., Wang X., Kline A.E., et al. Reduced cortical injury and edema in tissue plasminogen activator knockout mice after brain trauma. Neuroreport 12 (2001) 4117-4120
132. Morita-Fujimura Y., Fujimura M., Gasche Y., et al. 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 20 (2000) 130-138
133. Moulin T., Tatu L., Crepin-Leblond T., et al. The Besancon Stroke Registry: an acute stroke registry of 2,500 consecutive patients. Eur Neurol 38 (1997) 10-20
134. Mun-Bryce S., and Rosenberg G.A. Matrix metalloproteinases in cerebrovascular disease. J Cereb Blood Flow Metab 18 (1998) 1163-1172
135. Murphy G., Atkinson S., Ward R., et al. The role of plasminogen activators in the regulation of connective tissue metalloproteinases. Ann N Y Acad Sci 667 (1992) 1-12
136. Nagase H., and Woessner Jr. J.F. Matrix metalloproteinases. J Biol Chem 274 (1999) 21491-21494
137. Nakatomi H., Kuriu T., Okabe S., et al. Regeneration of hippocampal pyramidal neurons after ischemic brain injury by recruitment of endogenous neural progenitors. Cell 110 (2002) 429-441
138. Neuhoff H., Roeper J., and Schweizer M. Activity-dependent formation of perforated synapses in cultured hippocampal neurons. Eur J Neurosci 11 (1999) 4241-4250
139. Ning M., Lo E.H., Furie K., et al. T-PA-mediated increase in matrix metalloproteinase-9 in acute ischemic stroke. Stroke 35 (2004) 298
140. Ning M., Menezes N., Furie K., et al. MMP-9, TIMP-1 and ADC reduction on MRI-A comparison of serum and radiographic markers in acute ischemic stroke. Stroke 36 (2005) 517
141. Ning M., Montaner J., Wang X., et al. Matrix metalloproteinases (MMPs) and tissue Plasminogen Activator (t-PA) reperfusion therapy for stroke. In: Chan P., Johnson D., and Lajtha A. (Eds). Acute Ischemic Injury and Repair in the Nervous System. Handbook of Neurochemistry and Molecular Neurobiology 23 (2006), Kluwer Academic Publishers, New York
142. Ning M., Furie K.L., Koroshetz W.J., et al. Association between tPA therapy and raised early matrix metalloproteinase-9 in acute stroke. Neurology 66 (2006) 1550-1555
143. Ning M., Sarracino D., Buonanno F., et al. Plasma protease substrate profiling of tPA treatment in acute ischemic stroke patients: a step toward pharmacoproteomics at the bedside. Mol Cell Proteomics 5 (2006) 176s
144. Nishibori M., Ohtsuka A., Kawabata M., et al. A novel serpin-like protein, B-43, exists in both neurons and astrocytes: an immunohistochemical study in the parietal region of the bovine brain. Neurosci Lett 200 (1995) 125-128
145. Opdenakker G., Van den Steen P.E., Dubois B., et al. Gelatinase B functions as regulator and effector in leukocyte biology. J Leukoc Biol 69 (2001) 851-859
146. Opie L.H. Reperfusion injury and its pharmacologic modification. Circulation 80 (1989) 1049-1062
147. Overall C.M. Matrix metalloproteinase substrate binding domains, modules and exosites. Overview and experimental strategies. Methods Mol Biol 151 (2001) 79-120
148. Petty M.A., and Lo E.H. Junctional complexes of the blood-brain barrier: permeability changes in neuroinflammation. Prog Neurobiol 68 (2002) 311-323
149. Petty M.A., and Wettstein J.G. Elements of cerebral microvascular ischaemia. Brain Res Brain Res Rev 36 (2001) 23-34
150. Pfefferkorn T., and Rosenberg G.A. Closure of the blood-brain barrier by matrix metalloproteinase inhibition reduces rtPA-mediated mortality in cerebral ischemia with delayed reperfusion. Stroke 34 (2003) 2025-2030
151. Piepgras D.G., Morgan M.K., Sundt Jr. T.M., et al. Intracerebral hemorrhage after carotid endarterectomy. J Neurosurg 68 (1988) 532-536
152. Qian Z., Gilbert M.E., Colicos M.A., et al. Tissue-plasminogen activator is induced as an immediate-early gene during seizure, kindling and long-term potentiation. Nature 361 (1993) 453-457
153. Romanic A.M., White R.F., Arleth A.J., et al. Matrix metalloproteinase expression increases after cerebral focal ischemia in rats: inhibition of matrix metalloproteinase-9 reduces infarct size. Stroke 29 (1998) 1020-1030
154. Rosenberg G.A. Matrix metalloproteinases in brain injury. J Neurotrauma 12 (1995) 833-842
155. Rosenberg G.A. Matrix metalloproteinases in neuroinflammation. Glia 39 (2002) 279-291
156. Rosenberg G.A., Kornfeld M., Estrada E., et al. TIMP-2 reduces proteolytic opening of blood-brain barrier by type IV collagenase. Brain Res 576 (1992) 203-207
157. Rosenberg G.A., Estrada E.Y., Dencoff J.E., et al. Tumor necrosis factor-alpha-induced gelatinase B causes delayed opening of the blood-brain barrier: an expanded therapeutic window. Brain Res 703 (1995) 151-155
158. Rosenberg G.A., Navratil M., Barone F., et al. Proteolytic cascade enzymes increase in focal cerebral ischemia in rat. J Cereb Blood Flow Metab 16 (1996) 360-366
159. Rosenberg G.A., Estrada E.Y., and Dencoff J.E. Matrix metalloproteinases and TIMPs are associated with blood-brain barrier opening after reperfusion in rat brain. Stroke 29 (1998) 2189-2195
160. Salles F.J., and Strickland S. Localization and regulation of the tissue plasminogen activator-plasmin system in the hippocampus. J Neurosci 22 (2002) 2125-2134
161. Sappino A.P., Madani R., Huarte J., et al. Extracellular proteolysis in the adult murine brain. J Clin Invest 92 (1993) 679-685
162. Savitz S.I., and Fisher M. Future of neuroprotection for acute stroke: In the aftermath of the SAINT Trial. Ann Neurol 61 (2007) 396-402
163. Scarisbrick I.A., Isackson P.J., Ciric B., et al. MSP, a trypsin-like serine protease, is abundantly expressed in the human nervous system. J Comp Neurol 431 (2001) 347-361
164. Schaller B., and Graf R. Cerebral ischemia and reperfusion: the pathophysiologic concept as a basis for clinical therapy. J Cereb Blood Flow Metab 24 (2004) 351-371
165. Schmid-Elsaesser R., Zausinger S., Hungerhuber E., et al. Superior neuroprotective efficacy of a novel antioxidant (U-101033E) with improved blood-brain barrier permeability in focal cerebral ischemia. Stroke 28 (1997) 2018-2024
166. Shafer R.A., and Murphy S. Activated astrocytes induce nitric oxide synthase-2 in cerebral endothelium via tumor necrosis factor alpha. Glia 21 (1997) 370-379
167. Shuaib A., Lees K.R., Lyden P., et al. NXY-059 for the treatment of Acute Ischemic Stroke. NEJM 357 (2007) 562-571
168. Siao C.J., Fernandez S.R., and Tsirka S.E. Cell type-specific roles for tissue plasminogen activator released by neurons or microglia after excitotoxic injury. J Neurosci 23 (2003) 3234-3242
169. Siflinger-Birnboim A., Del Vecchio P.J., Cooper J.A., et al. Molecular sieving characteristics of the cultured endothelial monolayer. J Cell Physiol 132 (1987) 111-117
170. Sondell M., Sundler F., and Kanje M. Vascular endothelial growth factor is a neurotrophic factor which stimulates axonal outgrowth through the flk-1 receptor. Eur J Neurosci 12 (2000) 4243-4254
171. Stanimirovic D., and Satoh K. Inflammatory mediators of cerebral endothelium: a role in ischemic brain inflammation. Brain Pathol 10 (2000) 113-126
172. Study Group. Tissue plasminogen activator for acute ischemic stroke. The National Institute of Neurological Disorders and Stroke rt-PA Stroke Study Group. N Engl J Med 333 (1995) 1581-1587
173. Sumii T., and Lo E.H. Involvement of matrix metalloproteinase in thrombolysis-associated hemorrhagic transformation after embolic focal ischemia in rats. Stroke 33 (2002) 831-836
174. Thored P., Arvidsson A., Cacci E., et al. Persistent production of neurons from adult brain stem cells during recovery after stroke. Stem Cells 24 (2006) 739-747
175. Traupe H., Kruse E., and Heiss W.D. Reperfusion of focal ischemia of varying duration: postischemic hyper- and hypo-perfusion. Stroke 13 (1982) 615-622
176. Tsirka S.E., Gualandris A., Amaral D.G., et al. Excitotoxin-induced neuronal degeneration and seizure are mediated by tissue plasminogen activator. Nature 377 (1995) 340-344
177. Vaillant C., Meissirel C., Mutin M., et al. MMP-9 deficiency affects axonal outgrowth, migration, and apoptosis in the developing cerebellum. Mol Cell Neurosci 24 (2003) 395-408
178. Van Bruggen N., Thibodeaux H., Palmer J.T., et al. VEGF antagonism reduces edema formation and tissue damage after ischemia/reperfusion injury in the mouse brain. J Clin Invest 104 (1999) 1613-1620
179. Wagner D.D. The Weibel-Palade body: the storage granule for von Willebrand factor and P-selectin. Thromb Haemost 70 (1993) 105-110
180. Wang X., and Lo E.H. Triggers and mediators of hemorrhagic transformation in cerebral ischemia. Mol Neurobiol 28 (2003) 229-244
181. Wang Y.F., Tsirka S.E., Strickland S., et al. Tissue plasminogen activator (tPA) increases neuronal damage after focal cerebral ischemia in wild-type and tPA-deficient mice. Nat Med 4 (1998) 228-231
182. Wang X., Li X., Yaish-Ohad S., et al. Molecular cloning and expression of the rat monocyte chemotactic protein-3 gene: a possible role in stroke. Brain Res Mol Brain Res 71 (1999) 304-312
183. Wang X., Jung J., Asahi M., et al. Effects of matrix metalloproteinase-9 gene knock-out on morphological and motor outcomes after traumatic brain injury. J Neurosci 20 (2000) 7037-7042
184. Wang X., Mori T., Jung J.C., et al. Secretion of matrix metalloproteinase-2 and -9 after mechanical trauma injury in rat cortical cultures and involvement of MAP kinase. J Neurotrauma 19 (2002) 615-625
185. Wang X., Lee S.R., Arai K., et al. Lipoprotein receptor-mediated induction of matrix metalloproteinase by tissue plasminogen activator. Nat Med 9 (2003) 1313-1317
186. Wang X., Tsuji K., Lee S.R., et al. Mechanisms of hemorrhagic transformation after tissue plasminogen activator reperfusion therapy for ischemic stroke. Stroke 35 (2004) 2726-2730
187. Warach S., and Latour L.L. Evidence of reperfusion injury, exacerbated by thrombolytic therapy, in human focal brain ischemia using a novel imaging marker of early blood-brain barrier disruption. Stroke 35 (2004) 2659-2661
188. Wasinger V.C., Cordwell S.J., Cerpa-Poljak A., et al. Progress with gene-product mapping of the Mollicutes: Mycoplasma genitalium. Electrophoresis 16 (1995) 1090-1094
189. Wei E.P., Christman C.W., Kontos H.A., et al. Effects of oxygen radicals on cerebral arterioles. Am J Physiol 248 (1985) H157-H162
190. Weir C.J., Murray G.D., Dyker A.G., et al. Is hyperglycaemia an independent predictor of poor outcome after acute stroke? Results of a long-term follow up study. Br Med J 314 (1997) 1303-1306
191. Weiss S.J., Peppin G., Ortiz X., et al. Oxidative autoactivation of latent collagenase by human neutrophils. Science 227 (1985) 747-749
192. Wolburg H., and Lippoldt A. Tight junctions of the blood-brain barrier: development, composition and regulation. Vascul Pharmacol 38 (2002) 323-337
193. Wong D., and Dorovini-Zis K. Upregulation of intercellular adhesion molecule-1 (ICAM-1) expression in primary cultures of human brain microvessel endothelial cells by cytokines and lipopolysaccharide. J Neuroimmunol 39 (1992) 11-21
194. Wu Y.P., Siao C.J., Lu W., et al. The tissue plasminogen activator (tPA)/plasmin extracellular proteolytic system regulates seizure-induced hippocampal mossy fiber outgrowth through a proteoglycan substrate. J Cell Biol 148 (2000) 1295-1304
195. Yepes M., Sandkvist M., Wong M.K., et al. Neuroserpin reduces cerebral infarct volume and protects neurons from ischemia-induced apoptosis. Blood 96 (2000) 569-576
196. Yepes M., Sandkvist M., Coleman T.A., et al. Regulation of seizure spreading by neuroserpin and tissue-type plasminogen activator is plasminogen-independent. J Clin Invest 109 (2002) 1571-1578
197. Yong V.W. Metalloproteinases: mediators of pathology and regeneration in the CNS. Nat Rev Neurosci 6 (2005) 931-944
198. Yong V.W., Power C., Forsyth P., et al. Metalloproteinases in biology and pathology of the nervous system. Nat Rev Neurosci 2 (2001) 502-511
199. Yurchenco P.D., and Schittny J.C. Molecular architecture of basement membranes. FASEB J 4 (1990) 1577-1590
200. Zhang W., and Stanimirovic D. Current and future therapeutic strategies to target inflammation in stroke. Curr Drug Targets Inflamm Allergy 1 (2002) 151-166
201. Zhang R., Chopp M., Zhang Z., et al. The expression of P- and E-selectins in three models of middle cerebral artery occlusion. Brain Res 785 (1998) 207-214
202. Zhang Z.G., Zhang L., Jiang Q., et al. VEGF enhances angiogenesis and promotes blood-brain barrier leakage in the ischemic brain. J Clin Invest 106 (2000) 829-838
203. Zhang Z.G., Zhang L., Tsang W., et al. Correlation of VEGF and angiopoietin expression with disruption of blood-brain barrier and angiogenesis after focal cerebral ischemia. J Cereb Blood Flow Metab 22 (2002) 379-392
204. Zhao B.Q., Ikeda Y., Ihara H., et al. 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 (2004) 2610-2616
205. Zhao B.Q., Wang S., Kim H.Y., et al. Role of matrix metalloproteinases in delayed cortical responses after stroke. Nat Med 12 (2006) 441-445
206. Zweier J.L., Kuppusamy P., and Lutty G.A. Measurement of endothelial cell free radical generation: evidence for a central mechanism of free radical injury in postischemic tissues. Proc Natl Acad Sci USA 85 (1988) 4046-4050