tPA in the injured central nervous system: different scenarios starring the same actor?

Abbott, 2010, Structure and function of the blood-brain barrier, Neurobiol. Dis., 37, 13, 10.1016/j.nbd.2009.07.030 Abe, 2003, Decreased neural damage after spinal cord injury in tPA-deficient mice, J. Neurotrauma, 20, 43, 10.1089/08977150360517173 Adibhatla, 2008, Tissue plasminogen activator (tPA) and matrix metalloproteinases in the pathogenesis of stroke: therapeutic strategies, CNS Neurol. Disord. Drug Targets, 7, 243, 10.2174/187152708784936608 Akassoglou, 2000, Tissue plasminogen activator-mediated fibrinolysis protects against axonal degeneration and demyelination after sciatic nerve injury, J. Cell Biol., 149, 1157, 10.1083/jcb.149.5.1157 An, 2008, Tissue-type plasminogen activator and the low-density lipoprotein receptor-related protein induce Akt phosphorylation in the ischemic brain, Blood, 112, 2787, 10.1182/blood-2008-02-141630 Aoki, 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, 10.1161/01.STR.0000033932.34467.97 Baron, 2010, NR2D containing NMDA receptors mediate tissue plasminogen activator-promoted neuronal excitotoxicity, Cell Death Differ., 17, 860, 10.1038/cdd.2009.172 Baron, 2010, Tissue-type plasminogen activator induces plasmin-dependent proteolysis of intracellular neuronal nitric oxide synthase, Biol. Cell., 102, 539, 10.1042/BC20100072 Benarroch, 2007, Tissue plasminogen activator: beyond thrombolysis, Neurology, 69, 799, 10.1212/01.wnl.0000269668.08747.78 Benchenane, 2007, Anti-NR1 N-terminal-domain vaccination unmasks the crucial action of tPA on NMDA-receptor-mediated toxicity and spatial memory, J. Cell Sci., 120, 578, 10.1242/jcs.03354 Cammer, 1978, Degradation of basic protein in myelin by neutral proteases secreted by stimulated macrophages: a possible mechanism of inflammatory demyelination, Proc. Natl. Acad. Sci. USA, 75, 1554, 10.1073/pnas.75.3.1554 Chen, 1997, Neuronal death in the hippocampus is promoted by plasmin-catalyzed degradation of laminin, Cell, 91, 917, 10.1016/S0092-8674(00)80483-3 Claudio, 1995, Evidence of persistent blood-brain barrier abnormalities in chronic-progressive multiple sclerosis, Acta Neuropathol., 90, 228, 10.1007/BF00296505 Correa, 2011, Tissue plasminogen activator prevents white matter damage following stroke, J. Exp. Med., 208, 1229, 10.1084/jem.20101880 Cuadrado, 2008, Tissue plasminogen activator (t-PA) promotes neutrophil degranulation and MMP-9 release, J. Leukoc. Biol., 84, 207, 10.1189/jlb.0907606 Cunningham, 2005, Multiple roles for MMPs and TIMPs in cerebral ischemia, Glia, 50, 329, 10.1002/glia.20169 del Zoppo, 2003, Cerebral microvessel responses to focal ischemia, J. Cereb. Blood Flow Metab., 23, 879, 10.1097/01.WCB.0000078322.96027.78 Docagne, 2007, Excitotoxicity in a chronic model of multiple sclerosis: neuroprotective effects of cannabinoids through CB1 and CB2 receptor activation, Mol. Cell. Neurosci., 34, 551, 10.1016/j.mcn.2006.12.005 Docagne, 1999, Transforming growth factor-beta1 as a regulator of the serpins/t-PA axis in cerebral ischemia, FASEB J., 13, 1315, 10.1096/fasebj.13.11.1315 East, 2005, A role for the plasminogen activator system in inflammation and neurodegeneration in the central nervous system during experimental allergic encephalomyelitis, Am. J. Pathol., 167, 545, 10.1016/S0002-9440(10)62996-3 East, 2008, Chronic relapsing experimental allergic encephalomyelitis (CREAE) in plasminogen activator inhibitor-1 knockout mice: the effect of fibrinolysis during neuroinflammation, Neuropathol. Appl. Neurobiol., 34, 216, 10.1111/j.1365-2990.2007.00889.x Echeverry, 2010, Tissue-type plasminogen activator is a neuroprotectant in the mouse hippocampus, J. Clin. Invest., 120, 2194, 10.1172/JCI41722 Fernández-Monreal, 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, 10.1074/jbc.M407069200 Fernández-Monreal, 2004, Is tissue-type plasminogen activator a neuromodulator?, Mol. Cell. Neurosci., 25, 594, 10.1016/j.mcn.2003.11.002 Fitch, 2008, CNS injury, glial scars, and inflammation: inhibitory extracellular matrices and regeneration failure, Exp. Neurol., 209, 294, 10.1016/j.expneurol.2007.05.014 Flavin, 2000, Microglial tissue plasminogen activator (tPA) triggers neuronal apoptosis in vitro, Glia, 29, 347, 10.1002/(SICI)1098-1136(20000215)29:4<347::AID-GLIA5>3.0.CO;2-8 Fukuda, 2004, Focal cerebral ischemia induces active proteases that degrade microvascular matrix, Stroke, 35, 998, 10.1161/01.STR.0000119383.76447.05 Gijbels, 1993, Gelatinase B is present in the cerebrospinal fluid during experimental autoimmune encephalomyelitis and cleaves myelin basic protein, J. Neurosci. Res., 36, 432, 10.1002/jnr.490360409 Gveric, 2001, Plasminogen activators in multiple sclerosis lesions: implications for the inflammatory response and axonal damage, Brain, 124, 1978, 10.1093/brain/124.10.1978 Gveric, 2003, Impaired fibrinolysis in multiple sclerosis: a role for tissue plasminogen activator inhibitors, Brain, 126, 1590, 10.1093/brain/awg167 Hacke, 2008, Thrombolysis with alteplase 3 to 4.5 hours after acute ischemic stroke, N. Engl. J. Med., 359, 1317, 10.1056/NEJMoa0804656 Jin, 2010, Molecular insights and therapeutic targets for blood-brain barrier disruption in ischemic stroke: critical role of matrix metalloproteinases and tissue-type plasminogen activator, Neurobiol. Dis., 38, 376, 10.1016/j.nbd.2010.03.008 Kidwell, 2008, Thrombolytic toxicity: blood brain barrier disruption in human ischemic stroke, Cerebrovasc. Dis., 25, 338, 10.1159/000118379 Kim, 1999, Nonproteolytic neuroprotection by human recombinant tissue plasminogen activator, Science, 284, 647, 10.1126/science.284.5414.647 Kozai, 2007, Tissue type plasminogen activator induced in rat dorsal horn astrocytes contributes to mechanical hypersensitivity following dorsal root injury, Glia, 55, 595, 10.1002/glia.20483 Kvajo, 2004, Regulation of brain proteolytic activity is necessary for the in vivo function of NMDA receptors, J. Neurosci., 24, 9734, 10.1523/JNEUROSCI.3306-04.2004 Lee, 2007, Matrix metalloproteinase-9 inhibition attenuates vascular endothelial growth factor-induced intracerebral hemorrhage, Stroke, 38, 2563, 10.1161/STROKEAHA.106.481515 Lee, 2007, Non-proteolytic neurotrophic effects of tissue plasminogen activator on cultured mouse cerebrocortical neurons, J. Neurochem., 101, 1236, 10.1111/j.1471-4159.2007.04417.x Lemons, 1999, Chondroitin sulfate proteoglycan immunoreactivity increases following spinal cord injury and transplantation, Exp. Neurol., 160, 51, 10.1006/exnr.1999.7184 Levin, 1997, The expression of endothelial tissue plasminogen activator in vivo: a function defined by vessel size and anatomic location, J. Cell Sci., 110, 139, 10.1242/jcs.110.2.139 Ling, 2006, Disruption of tissue plasminogen activator gene reduces macrophage migration, Biochem. Biophys. Res. Commun., 349, 906, 10.1016/j.bbrc.2006.08.111 Liot, 2006, Tissue-type plasminogen activator rescues neurones from serum deprivation-induced apoptosis through a mechanism independent of its proteolytic activity, J. Neurochem., 98, 1458, 10.1111/j.1471-4159.2006.03982.x Liu, 2004, Tissue plasminogen activator neurovascular toxicity is controlled by activated protein C, Nat. Med., 10, 1379, 10.1038/nm1122 Lu, 2002, Involvement of tissue plasminogen activator in onset and effector phases of experimental allergic encephalomyelitis, J. Neurosci., 22, 10781, 10.1523/JNEUROSCI.22-24-10781.2002 Macrez, 2009 Matys, 2003, Tissue plasminogen activator and NMDA receptor cleavage, Nat. Med., 9, 371, 10.1038/nm0403-371 Medina, 2005, Tissue plasminogen activator mediates amyloid-induced neurotoxicity via Erk1/2 activation, EMBO J., 24, 1706, 10.1038/sj.emboj.7600650 Minor, 2009, Tissue plasminogen activator promotes axonal outgrowth on CNS myelin after conditioned injury, J. Neurochem., 109, 706, 10.1111/j.1471-4159.2009.05977.x Minor, 2008, Plasminogen activator induction facilitates recovery of respiratory function following spinal cord injury, Mol. Cell. Neurosci., 37, 143, 10.1016/j.mcn.2007.09.005 Miranda, 2006, Neuroserpin: a serpin to think about, Cell. Mol. Life Sci., 63, 709, 10.1007/s00018-005-5077-4 Nicole, 2001, The proteolytic activity of tissue-plasminogen activator enhances NMDA receptor-mediated signaling, Nat. Med., 7, 59, 10.1038/83358 Nolin, 2008, tPA-mediated generation of plasmin is catalyzed by the proteoglycan NG2, Glia, 56, 177, 10.1002/glia.20603 Pang, 2004, Cleavage of proBDNF by tPA/plasmin is essential for long-term hippocampal plasticity, Science, 306, 487, 10.1126/science.1100135 Parathath, 2006, Nitric oxide mediates neurodegeneration and breakdown of the blood-brain barrier in tPA-dependent excitotoxic injury in mice, J. Cell. Sci., 119, 339, 10.1242/jcs.02734 Park, 2008, Key role of tissue plasminogen activator in neurovascular coupling, Proc. Natl. Acad. Sci. USA, 105, 1073, 10.1073/pnas.0708823105 Pennica, 1983, Cloning and expression of human tissue-type plasminogen activator cDNA in E. coli, Nature, 301, 214, 10.1038/301214a0 Pitt, 2000, Glutamate excitotoxicity in a model of multiple sclerosis, Nat. Med., 6, 67, 10.1038/71555 Polavarapu, 2008, Regulated intramembrane proteolysis of the low-density lipoprotein receptor-related protein mediates ischemic cell death, Am. J. Pathol., 172, 1355, 10.2353/ajpath.2008.070975 Profyris, 2004, Degenerative and regenerative mechanisms governing spinal cord injury, Neurobiol. Dis., 15, 415, 10.1016/j.nbd.2003.11.015 Reijerkerk, 2010, The NR1 subunit of NMDA receptor regulates monocyte transmigration through the brain endothelial cell barrier, J. Neurochem., 113, 447, 10.1111/j.1471-4159.2010.06598.x Reijerkerk, 2008, Tissue-type plasminogen activator is a regulator of monocyte diapedesis through the brain endothelial barrier, J. Immunol., 181, 3567, 10.4049/jimmunol.181.5.3567 Rijken, 1988, Relationships between structure and function of tissue-type plasminogen activator, Klin. Wochenschr., 66, 33 Rogove, 1999, Activation of microglia reveals a non-proteolytic cytokine function for tissue plasminogen activator in the central nervous system, J. Cell Sci., 112, 4007, 10.1242/jcs.112.22.4007 Salles, 2002, Localization and regulation of the tissue plasminogen activator plasmin system in the hippocampus, J. Neurosci., 22, 2125, 10.1523/JNEUROSCI.22-06-02125.2002 Samson, 2006, Tissue-type plasminogen activator: a multifaceted modulator of neurotransmission and synaptic plasticity, Neuron, 50, 673, 10.1016/j.neuron.2006.04.013 Samson, 2008, Tissue-type plasminogen activator requires a co-receptor to enhance NMDA receptor function, J. Neurochem., 107, 1091 Sappino, 1993, Extracellular proteolysis in the adult murine brain, J. Clin. Invest., 92, 679, 10.1172/JCI116637 Seeds, 1997, Neuronal extracellular proteases facilitate cell migration, axonal growth, and pathfinding, Cell Tissue Res., 290, 367, 10.1007/s004410050942 Sheehan, 2007, Proteolytic activation of monocyte chemoattractant protein-1 by plasmin underlies, excitotoxic neurodegeneration in mice, J. Neurosci., 27, 1738, 10.1523/JNEUROSCI.4987-06.2007 Siao, 2003, Cell type-specific roles for tissue plasminogen activator released by neurons or microglia after excitotoxic injury, J. Neurosci., 23, 3234, 10.1523/JNEUROSCI.23-08-03234.2003 Siao, 2002, Tissue plasminogen activator mediates microglial activation via its finger domain through annexin II, J. Neurosci., 22, 3352, 10.1523/JNEUROSCI.22-09-03352.2002 Su, 2008, Activation of PDGF-CC by tissue plasminogen activator impairs blood-brain barrier integrity during ischemic stroke, Nat. Med., 14, 731, 10.1038/nm1787 Suzuki, 2007, Stromelysin-1 (MMP-3) is critical for intracranial bleeding after t-PA treatment of stroke in mice, J. Thromb. Haemost., 5, 1732, 10.1111/j.1538-7836.2007.02628.x Tanswell, 1991, Pharmacokinetics and hepatic catabolism of tissue-type plasminogen activator, Arzneimittelforschung, 41, 1310 The National Institute of Neurological Disorders and Stroke rt-PA Stroke Study Group, 1995, Tissue plasminogen activator for acute ischemic stroke, N. Engl. J. Med., 333, 1581, 10.1056/NEJM199512143332401 Tsirka, 1995, Excitotoxin-induced neuronal degeneration and seizure are mediated by tissue plasminogen activator, Nature, 377, 340, 10.1038/377340a0 van den Berg, 2010, Incidence of spinal cord injury worldwide: a systematic review, Neuroepidemiology, 34, 184, 10.1159/000279335 Veeravalli, 2009, Stem cells downregulate the elevated levels of tissue plasminogen activator in rats after spinal cord injury, Neurochem. Res., 34, 1183, 10.1007/s11064-008-9894-3 Yeo, 2009, Spinal epidural hematoma after intravenous thrombolysis for acute ischemic stroke, J. Neurol. Sci., 284, 190, 10.1016/j.jns.2009.04.016 Yepes, 2009, Tissue-type plasminogen activator in the ischemic brain: more than a thrombolytic, Trends Neurosci., 32, 48, 10.1016/j.tins.2008.09.006 Yepes, 2003, Tissue-type plasminogen activator induces opening of the blood-brain barrier via the LDL receptor-related protein, J. Clin. Invest., 112, 1533, 10.1172/JCI200319212 Yepes, 2000, Neuroserpin reduces cerebral infarct volume and protects neurons from ischemia-induced apoptosis, Blood, 96, 569, 10.1182/blood.V96.2.569 Zhang, 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, 10.1038/jcbfm.2009.174 Zhang, 2007, Tissue-type plasminogen activator and the low-density lipoprotein receptor-related protein mediate cerebral ischemia-induced nuclear factor-kappaB pathway activation, Am. J. Pathol., 171, 1281, 10.2353/ajpath.2007.070472 Zlokovic, 1995, Expression of tissue plasminogen activator in cerebral capillaries: possible fibrinolytic function of the blood-brain barrier, Neurosurgery, 37, 955, 10.1227/00006123-199511000-00015