Tissue-type plasminogen activator induces opening of the blood-brain barrier via the LDL receptor-related protein

Journal of Clinical Investigation

Volumn 112, Issue 10, 2003, Pages 1533-1540

  Yepes, Manuel ^a,b   Sandkvist, Maria ^a   Moore, Elizabeth G ^a   Bugge, Thomas H ^c   Strickland, Dudley K ^a   Lawrence, Daniel A ^a  

^a HOLLAND LABORATORY   (United States)

^b GEORGETOWN UNIVERSITY HOSPITAL   (United States)

^c NATIONAL INSTITUTE OF DENTAL AND CRANIOFACIAL RESEARCH   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

GELATINASE B; LOW DENSITY LIPOPROTEIN RECEPTOR RELATED PROTEIN; PLASMINOGEN; TISSUE PLASMINOGEN ACTIVATOR; UROKINASE RECEPTOR;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BLOOD BRAIN BARRIER; BLOOD VESSEL PERMEABILITY; BRAIN BLOOD VESSEL; BRAIN ISCHEMIA; CELL COMMUNICATION; CONCENTRATION RESPONSE; CONTROLLED STUDY; HOMEOSTASIS; INTRACRANIAL HYPERTENSION; NONHUMAN; PATHOGENESIS; PRIORITY JOURNAL; PROTEIN FUNCTION; RAT; SIGNAL TRANSDUCTION; TRANSGENIC MOUSE;

ANIMALS; ANTIBODIES; BLOOD-BRAIN BARRIER; BRAIN; BRAIN ISCHEMIA; CAPILLARY PERMEABILITY; COLORING AGENTS; DOSE-RESPONSE RELATIONSHIP, DRUG; EVANS BLUE; EXTRAVASATION OF DIAGNOSTIC AND THERAPEUTIC MATERIALS; HOMEOSTASIS; HUMANS; INFARCTION, MIDDLE CEREBRAL ARTERY; LDL-RECEPTOR RELATED PROTEIN 1; MATRIX METALLOPROTEINASE 9; MICE; MICE, INBRED C57BL; MICE, KNOCKOUT; NEUROPEPTIDES; PLASMINOGEN; RATS; RATS, SPRAGUE-DAWLEY; SERINE PROTEINASE INHIBITORS; SERPINS; TISSUE PLASMINOGEN ACTIVATOR;

EID: 0345824713     PISSN: 00219738     EISSN: None     Source Type: Journal    
DOI: 10.1172/JCI200319212     Document Type: Article

References (48)

1. Bugge, T.H., et al. 1996. Loss of fibrinogen rescues mice from the pleiotropic effects of plasminogen deficiency. Cell. 87:709-719.
2. Qian, Z., Gilbert, M.E., Colicos, M.A., Kandel, E.R., and Kuhl, D. 1993. Tissue-plasminogen activator is induced as an immediate-early gene during seizure, kindling and long-term potentiation. Nature. 361:453-457.
3. Seeds, N.W., Williams, B.L., and Bickford, P.C. 1995. Tissue plasminogen activator induction in Purkinje neurons after cerebellar motor learning. Science. 270:1992-1994.
4. Yepes, M., et al. 2002. Regulation of seizure spreading by neuroserpin and tissue-type plasminogen activator is plasminogen-independent. J. Clin. Invest. 109:1571-1578. doi:10.1172/JCI200214308.
5. Mataga, N., Nagai, N., and Hensch, T.K. 2002. Permissive proteolytic activity for visual cortical plasticity. Proc. Natl. Acad. Sci. U. S. A. 99:7717-7721.
6. Tsirka, S.E., Gualandris, A., Amaral, D.G., and Strickland, S. 1995. Excitotoxin-induced neuronal degeneration and seizure are mediated by tissue plasminogen activator. Nature. 377:340-344.
7. Yepes, M., et al. 2000. Neuroserpin reduces cerebral infarct volume and protects neurons from ischemia-induced apoptosis. Blood. 96:569-576.
8. Wang, Y.F., 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.
9. Kim, Y.H., Park, J.H., Hong, S.H., and Koh, J.Y. 1999. Nonproteolytic neuroprotection by human recombinant tissue plasminogen activator. Science. 284:647-650.
10. Tabrizi, P., et al. 1999. Tissue plasminogen activator (tPA) deficiency exacerbates cerebrovascular fibrin deposition and brain injury in a murine stroke model: studies in tPA-deficient mice and wild-type mice on a matched genetic background. Arterioscler. Thromb. Vasc. Biol. 19:2801-2806.
11. Nagai, N., De Mol, M., Lijnen, H.R., Carmeliet, P., and Collen, D. 1999. Role of plasminogen system components in focal cerebral ischemic infarction: a gene targeting and gene transfer study in mice. Circulation. 99:2440-2444.
12. Cinelli, P., et al. 2001. Neuroserpin, a neuroprotective factor in focal ischemic stroke. Mol. Cell. Neurosci. 18:443-457.
13. 1995. Tissue plasminogen activator for acute ischemic stroke. The National Institute of Neurological Disorders and Stroke rt-PA Stroke Study Group. N. Engl. J. Med. 333:1581-1587.
14. Zhang, Z., et al. 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.
15. Aoki, T., Sumii, T., Mori, T., Wang, X., and Lo, E.H. 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.
16. Rubin, L.L., and Staddon J.M., 1999. The cell biology of the blood-brain barrier. Annu. Rev. Neurosci. 22:11-28.
17. Garcia, J.H., Lossinsky, A.S., Kauffman, F.C., and Conger, K.A. 1978. Neuronal ischemic injury: light microscopy, ultrastructure and biochemistry. Acta Neuropathol. (Berl.) 43:85-95.
18. Baker, R.N., Cancilla, P.A., Pollock, S., and Frommes, S.P. 1971. The movement of exogenous protein in experimental cerebral edema. An electron microscopic study after freeze-injury. J. Neuropathol. Exp. Neurol. 30:668-679.
19. Romanic, A.M., and Madri, J.A. 1994. Extracellular matrix-degrading proteinases in the nervous system. Brain Pathol. 4:145-156.
20. Rosenberg, G.A., Navratil, M., Barone, F., and Feuerstein, G. 1996. Proteolytic cascade enzymes increase in focal cerebral ischemia in rat. J. Cereb. Blood Flow Metab. 16:360-366.
21. Asahi, M., 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.
22. Asahi, M., et al. 2001. Effects of matrix metalloproteinase-9 gene knockout on the proteolysis of blood-brain barrier and white matter components after cerebral ischemia. J. Neurosci. 21:7724-7732.
23. Herz, J., et al. 1988. Surface location and high affinity for calcium of a 500-kd liver membrane protein closely related to the LDL-receptor suggest a physiological role as lipoprotein receptor. EMBO J. 7:4119-4127.
24. Bu, G., Williams, S., Strickland, D.K., and Schwartz, A.L. 1992. Low density lipoprotein receptor-related protein/alpha 2-macroglobulin receptor is an hepatic receptor for tissue-type plasminogen activator. Proc. Natl. Acad. Sci. U. S. A. 89:7427-7431.
25. Hahn-Dantona, E., Ruiz, J.F., Bornstein, P., and Strickland, D.K. 2001. The low density lipoprotein receptor-related protein modulates levels of matrix metalloproteinase 9 (MMP-9) by mediating its cellular catabolism. J. Biol. Chem. 276:15498-15503.
26. Dehouck, B., et al. 1997. A new Function for the LDL receptor: transcytosis of LDL across the blood-brain barrier. J. Cell Biol. 138:877-889.
27. Demeule, M., et al. 2002. High transcytosis of melanoctransferrin (P97) across the blood-brain barrier. J. Neurochem. 83:924-933.
28. Herz, J., and Bock, H.H. 2002. Lipoprotein receptors in the nervous system. Annu. Rev. Biochem. 71:405-434.
29. Zhuo, M., et al. 2000. Role of tissue plasminogen activator receptor LRP in hippocampal long-term potentiation. J. Neurosci. 20:542-549.
30. Boucher, P., Gotthardt, M., Li, W.P., Anderson, R.G., and Herz, J. 2003. LRP: role in vascular wall integrity and protection from atherosclerosis. Science. 300:329-332.
31. Netzel-Arnett, S., et al. 2002. Collagen dissolution by keratinocytes requires cell surface plasminogen activation and matrix metalloproteinase activity. J. Biol. Chem. 277:45154-45161.
32. Vu, T.H., et al. 1998. MMP-9/gelatinase B is a key regulator of growth plate angiogenesis and apoptosis of hypertrophic chondrocytes. Cell. 93:411-422.
33. Betsuyaku, T., Shipley, J.M., Liu, Z., and Senior, R.M. 1999. Neutrophil emigration in the lungs, peritoneum, and skin does nor require gelatinase B. Am. J. Respir. Cell Mol. Biol. 20:1303-1309.
34. Paxinos, G., and Franklin, K.B.J. 2001. The mouse brain in stereotaxic coordinates. Academic Press Inc. San Diego, California, USA. 1-93.
35. Rosenberg, G.A., Estrada, E.Y., Dencoff, J.E., and Stetler-Stevenson, W.G. 1995. Tumor necrosis factor-alpha-induced gelatinase B causes delayed opening of the blood-brain barrier: an expanded therapeutic window. Brain Res. 703:151-155.
36. Nicole, O., et al. 2001. The proteolytic activity of tissue-plasminogen activator enhances NMDA receptor-mediated signaling. Nat. Med. 7:59-64.
37. Matys, T., and Strickland, S. 2003. Tissue plasminogen activator and NMDA receptor cleavage. Nat. Med. 9:371-372.
38. Wong, E.H., et al. 1986. The anticonvulsant MK-801 is a potent N-methyl-D-aspartate antagonist. Proc. Natl. Acad Sci. U. S. A. 83:7104-7108.
39. Bu, G. 1998. Receptor-associated protein: a specialized chaperone and antagonist for members of the LDL receptor gene family. Curr. Opin. Lipidol. 9:149-155.
40. Wolburg, H., and Lippoldt, A. 2002. Tight junctions of the blood-brain barrier: development, composition and regulation. Vascul. Pharmacol. 38:323-337.
41. Rubin, L.L., and Staddon, J.M. 1999. The cell biology of the blood-brain barrier. Annu. Rev. Neurosci 22:11-28.
42. Castellanos, M., et al. 2003. Plasma metalloproteinase-9 concentration predicts hemorrhagic transformation in acute ischemic stroke. Stroke. 34:40-46.
43. Siao, C.J., Fernandez, S.R., and Tsirka, S.E. 2003. Cell type-specific roles for tissue plasminogen activator released by neurons or microglia after excitotoxic injury. J. Neurosci. 23:3224-3242.
44. May, P., Reddy, Y.K., and Herz, J. 2002. Proteolytic processing of low density lipoprotein receptor-related protein mediates regulated release of its intracellular domain. J. Biol. Chem. 277:18736-18743.
45. Coughlin, S.R. 2002. Protease-activated receptors in the cardiovascular system. Cold Spring Harb. Symp. Quant. Biol. 67:197-208.
46. Sobey, C.G., and Cocks, T.M. 1998. Activation of protease-activated receptor-2 (PAR-2) elicits nitric oxide-dependent dilatation of the basilar artery in vivo. Stroke. 29:1439-1444.
47. Jiang, X., et al. 2002. Storage and release of tissue plasminogen activator by sympathetic axons in resistance vessel walls. Microvasc. Res. 64:438-447.
48. Llorente-Cortes, V., Martinez-Gonzalez, J., and Badimon, L. 2000. LDL receptor-related protein mediates uptake of aggregated LDL in human vascular smooth muscle cells. Arterioscler. Thromb. Vasc. Biol. 20:1572-1579.