Recombinant tissue plasminogen activator induces blood-brain barrier breakdown by a matrix metalloproteinase-9-independent pathway after transient focal cerebral ischemia in mouse

European Journal of Neuroscience

Volumn 34, Issue 7, 2011, Pages 1085-1092

  Copin, Jean Christophe ^a,b,c   Bengualid, Daniel Jiménez ^a,b   Da Silva, Rafaela F ^d,e   Kargiotis, Odysseas ^a   Schaller, Karl ^a,b   Gasche, Yvan ^a,b  

^a GENEVA UNIVERSITY HOSPITALS   (Switzerland)

^b UNIVERSITY OF GENEVA   (Switzerland)

^c Centre Médical Universitaire   (Switzerland)

^d EPFL   (Switzerland)

^e FEDERAL UNIVERSITY OF MINAS GERAIS   (Brazil)

Author keywords

Brain edema; Matrix metalloproteinase; Stroke; Thrombolysis

Indexed keywords

4 AMINOBENZOYL GLYCYLPROLINE DEXTRO LEUCINE DEXTRO ALANINE HYDROXAMATE; ALTEPLASE; GELATINASE B; HYDROXAMIC ACID DERIVATIVE; UNCLASSIFIED DRUG;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BLOOD BRAIN BARRIER; BRAIN INFARCTION; BRAIN ISCHEMIA; BRAIN SIZE; CONTROLLED STUDY; DISSOCIATION; DRUG EFFICACY; DRUG SAFETY; ENZYME INHIBITION; MEMBRANE PERMEABILITY; MIDDLE CEREBRAL ARTERY OCCLUSION; MORTALITY; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN DEGRADATION; TREATMENT RESPONSE; ZYMOGRAPHY;

ANIMALS; BLOOD-BRAIN BARRIER; BRAIN ISCHEMIA; COLLAGEN TYPE IV; FIBRINOLYTIC AGENTS; LAMININ; MALE; MATRIX METALLOPROTEINASE 9; MICE; MICE, KNOCKOUT; STROKE; TISSUE PLASMINOGEN ACTIVATOR;

EID: 80053566544     PISSN: 0953816X     EISSN: 14609568     Source Type: Journal    
DOI: 10.1111/j.1460-9568.2011.07843.x     Document Type: Article

References (42)

1. Armstead, W.M., Nassar, T., Akkawi, S., Smith, D.H., Chen, X.H., Cines, D.B. & Higazi, A.A. (2006) Neutralizing the neurotoxic effects of exogenous and endogenous tPA. Nat. Neurosci., 9, 1150-1155.
2. Benchenane, K., Berezowski, V., Ali, C., Fernandez-Monreal, M., Lopez-Atalaya, J.P., Brillault, J., Chuquet, J., Nouvelot, A., MacKenzie, E.T., Bu, G.J., Cecchelli, R., Touzani, O. & Vivien, D. (2005) Tissue-type plasminogen activator crosses the intact blood-brain barrier by low-density lipoprotein receptor-related protein-mediated transcytosis. Circulation, 111, 2241-2249.
3. Benchenane, K., Castel, H., Boulouard, M., Bluthe, R., Fernandez-Monreal, M., Roussel, B.D., Lopez-Atalaya, J.P., Butt-Gueulle, S., Agin, V., Maubert, E., Dantzer, R., Touzani, O., Dauphin, F., Vivien, D. & Ali, C. (2007) Anti-NR1N-terminal-domain vaccination unmasks the crucial action of tPA on NMDA-receptor-mediated toxicity and spatial memory. J. Cell Sci., 120, 578-585.
4. Cheng, T., Petraglia, A.L., Li, Z., Thiyagarajan, M., Zhong, Z., Wu, Z., Liu, D., Maggirwar, S.B., Deane, R., Fernandez, J.A., LaRue, B., Griffin, J.H., Chopp, M. & Zlokovic, B.V. (2006) Activated protein C inhibits tissue plasminogen activator-induced brain hemorrhage. Nat. Med., 12, 1278-1285.
5. Connolly, E.S. Jr, Winfree, C.J., Stern, D.M., Solomon, R.A. & Pinsky, D.J. (1996) Procedural and strain-related variables significantly affect outcome in a murine model of focal cerebral ischemia. Neurosurgery, 38, 523-531; discussion 532.
6. Copin, J.C., Goodyear, M.C., Gidday, J.M., Shah, A.R., Gascon, E., Dayer, A., Morel, D.M. & Gasche, Y. (2005) Role of matrix metalloproteinases in apoptosis after transient focal cerebral ischemia in rats and mice. Eur. J. Neurosci., 22, 1597-1608.
7. Copin, J.C., Merlani, P., Sugawara, T., Chan, P.H. & Gasche, Y. (2008) Delayed matrix metalloproteinase inhibition reduces intracerebral hemorrhage after embolic stroke in rats. Exp. Neurol., 213, 196-201.
8. Cuadrado, E., Ortega, L., Hernandez-Guillamon, M., Penalba, A., Fernandez-Cadenas, I., Rosell, A. & Montaner, J. (2008) Tissue plasminogen activator (t-PA) promotes neutrophil degranulation and MMP-9 release. J. Leukoc. Biol., 84, 207-214.
9. Cuadrado, E., Rosell, A., Penalba, A., Slevin, M., Alvarez-Sabin, J., Ortega-Aznar, A. & Montaner, J. (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.
10. Fujimura, M., Gasche, Y., Morita-Fujimura, Y., Massengale, J., Kawase, M. & Chan, P.H. (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.
11. Gasche, Y., Fujimura, M., Morita-Fujimura, Y., Copin, J.C., Kawase, M., Massengale, J. & Chan, P.H. (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.
12. Gasche, Y., Soccal, P.M., Kanemitsu, M. & Copin, J.C. (2006) Matrix metalloproteinases and diseases of the central nervous system with a special emphasis on ischemic brain. Front Biosci., 11, 1289-1301.
13. Gidday, J.M., Gasche, Y.G., Copin, J.C., Shah, A.R., Perez, R.S., Shapiro, S.D., Chan, P.H. & Park, T.S. (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.
14. Hacke, W., Donnan, G., Fieschi, C., Kaste, M., von Kummer, R., Broderick, J.P., Brott, T., Frankel, M., Grotta, J.C., Haley, E.C. Jr, Kwiatkowski, T., Levine, S.R., Lewandowski, C., Lu, M., Lyden, P., Marler, J.R., Patel, S., Tilley, B.C., Albers, G., Bluhmki, E., Wilhelm, M. & Hamilton, S. (2004) Association of outcome with early stroke treatment: pooled analysis of ATLANTIS, ECASS, and NINDS rt-PA stroke trials. Lancet, 363, 768-774.
15. Haelewyn, B., Risso, J.J. & Abraini, J.H. (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.
16. Horstmann, S., Kalb, P., Koziol, J., Gardner, H. & Wagner, S. (2003) Profiles of matrix metalloproteinases, their inhibitors, and laminin in stroke patients: influence of different therapies. Stroke, 34, 2165-2170.
17. Korninger, C. & Collen, D. (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.
18. Macrez, R., Bezin, L., Le Mauff, B., Ali, C. & Vivien, D. (2010) Functional occurrence of the interaction of tissue plasminogen activator with the NR1 Subunit of N-methyl-D-aspartate receptors during stroke. Stroke, 41, 2950-2955.
19. Matys, T. & Strickland, S. (2003) Tissue plasminogen activator and NMDA receptor cleavage. Nat. Med., 9, 371-372.
20. McCawley, L.J. & Matrisian, L.M. (2001) Matrix metalloproteinases: they're not just for matrix anymore!. Curr. Opin. Cell Biol., 13, 534-540.
21. Medina, M.G., Ledesma, M.D., Dominguez, J.E., Medina, M., Zafra, D., Alameda, F., Dotti, C.G. & Navarro, P. (2005) Tissue plasminogen activator mediates amyloid-induced neurotoxicity via Erk1/2 activation. EMBO J., 24, 1706-1716.
22. Nicole, O., Docagne, F., Ali, C., Margaill, I., Carmeliet, P., MacKenzie, E.T., Vivien, D. & Buisson, A. (2001) The proteolytic activity of tissue-plasminogen activator enhances NMDA receptor-mediated signaling. Nat. Med., 7, 59-64.
23. Ning, M., Furie, K.L., Koroshetz, W.J., Lee, H., Barron, M., Lederer, M., Wang, X., Zhu, M., Sorensen, A.G., Lo, E.H. & Kelly, P.J. (2006) Association between tPA therapy and raised early matrix metalloproteinase-9 in acute stroke. Neurology, 66, 1550-1555.
24. Odake, S., Morita, Y., Morikawa, T., Yoshida, N., Hori, H. & Nagai, Y. (1994) Inhibition of matrix metalloproteinases by peptidyl hydroxamic acids. Biochem. Biophys. Res. Commun., 199, 1442-1446.
25. Parathath, S.R., Parathath, S. & Tsirka, S.E. (2006) Nitric oxide mediates neurodegeneration and breakdown of the blood-brain barrier in tPA-dependent excitotoxic injury in mice. J. Cell Sci., 119, 339-349.
26. Reijerkerk, A., Kooij, G., van der Pol, S.M.A., Leyen, T., Lakeman, K., van het Hof, B., Vivien, D. & de Vries, H.E. (2010) The NR1 subunit of NMDA receptor regulates monocyte transmigration through the brain endothelial cell barrier. J. Neurochem., 113, 447-453.
27. Rosenberg, G.A. (2009) Matrix metalloproteinases and their multiple roles in neurodegenerative diseases. Lancet Neurol., 8, 205-216.
28. Sole, S., Petegnief, V., Gorina, R., Chamorro, A. & Planas, A.M. (2004) Activation of matrix metalloproteinase-3 and agrin cleavage in cerebral ischemia/reperfusion. J. Neuropathol. Exp. Neurol., 63, 338-349.
29. Su, E.J., Fredriksson, L., Geyer, M., Folestad, E., Cale, J., Andrae, J., Gao, Y., Pietras, K., Mann, K., Yepes, M., Strickland, D.K., Betsholtz, C., Eriksson, U. & Lawrence, D.A. (2008) Activation of PDGF-CC by tissue plasminogen activator impairs blood-brain barrier integrity during ischemic stroke. Nat. Med., 14, 731-737.
30. Su, E.J., Fredriksson, L., Schielke, G.P., Eriksson, U. & Lawrence, D.A. (2009) Tissue plasminogen activator-mediated PDGF signaling and neurovascular coupling in stroke. J. Thromb. Haemostasis, 7, 155-158.
31. Sumii, T. & Lo, E.H. (2002) Involvement of matrix metalloproteinase in thrombolysis-associated hemorrhagic transformation after embolic focal ischemia in rats. Stroke, 33, 831-836.
32. Suzuki, Y., Nagai, N., Yamakawa, K., Kawakami, J., Lijnen, H.R. & Umemura, K. (2009) Tissue-type plasminogen activator (t-PA) induces stromelysin-1 (MMP-3) in endothelial cells through activation of lipoprotein receptor-related protein. Blood, 114, 3352-3358.
33. Tsuji, K., Aoki, T., Tejima, E., Arai, K., Lee, S.R., Atochin, D.N., Huang, P.L., Wang, X.Y., Montaner, J. & Lo, E.H. (2005) Tissue plasminogen activator promotes matrix metalloproteinase-9 upregulation after focal cerebral ischemia. Stroke, 36, 1954-1959.
34. Van Lint, P. & Libert, C. (2006) Matrix metalloproteinase-8: cleavage can be decisive. Cytokine Growth Factor Rev., 17, 217-223.
35. Wang, Y.F., Tsirka, S.E., Strickland, S., Stieg, P.E., Soriano, S.G. & Lipton, S.A. (1998) Tissue plasminogen activator (tPA) increases neuronal damage after focal cerebral ischemia in wild-type and tPA-deficient mice. Nat. Med., 4, 228-231.
36. Wang, X., Lee, S.R., Arai, K., Lee, S.R., Tsuji, K., Rebeck, G.W. & Lo, E.H. (2003) Lipoprotein receptor-mediated induction of matrix metalloproteinase by tissue plasminogen activator. Nat. Med., 9, 1313-1317.
37. Yepes, M., Sandkvist, M., Moore, E.G., Bugge, T.H., Strickland, D.K. & Lawrence, D.A. (2003) Tissue-type plasminogen activator induces opening of the blood-brain barrier via the LDL receptor-related protein. J. Clin. Invest., 112, 1533-1540.
38. Yepes, M., Roussel, B.D., Ali, C. & Vivien, D. (2009) Tissue-type plasminogen activator in the ischemic brain: more than a thrombolytic. Trends Neurosci., 32, 48-55.
39. Zechariah, A., ElAli, A. & Hermann, D.M. (2010) Combination of tissue-plasminogen activator with erythropoietin induces blood-brain barrier permeability, extracellular matrix disaggregation, and DNA fragmentation after focal cerebral ischemia in mice. Stroke, 41, 1008-1012.
40. Zhang, Z., Zhang, L., Yepes, M., Jiang, Q., Li, Q., Arniego, P., Coleman, T.A., Lawrence, D.A. & Chopp, M. (2002) Adjuvant treatment with neuroserpin increases the therapeutic window for tissue-type plasminogen activator administration in a rat model of embolic stroke. Circulation, 106, 740-745.
41. Zhang, X.H., Polavarapu, R., She, H., Mao, Z.X. & Yepes, M. (2007) Tissue-type plasminogen activator and the low-density lipoprotein receptor-related protein mediate cerebral ischemia-induced nuclear factor-kappa B pathway activation. Am. J. Pathol., 171, 1281-1290.
42. Zhao, B.Q., Ikeda, Y., Ihara, H., Urano, T., Fan, W.F., Mikawa, S., Suzuki, Y., Kondo, K., Sato, K., Nagai, N. & Umemura, K. (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.