Enhanced hippocampal long-term potentiation and learning by increased neuronal expression of tissue-type plasminogen activator in transgenic mice

EMBO Journal

Volumn 18, Issue 11, 1999, Pages 3007-3012

  Madani, Rime ^a   Hulo, Sophie ^a   Toni, Nicolas ^a   Madani, Hala ^a   Steimer, Thierry ^b   Muller, Dominique ^a   Vassalli, Jean Dominique ^a  

^a UNIVERSITY OF GENEVA   (Switzerland)

^b Faculty of Medicine   (Switzerland)

Author keywords

LTP; Memory; Synaptic plasticity; tPA; Transgenic mice

Indexed keywords

PLASMINOGEN ACTIVATOR; PROTEINASE;

ANIMAL TISSUE; ARTICLE; BRAIN CELL; CATALYSIS; CONTROLLED STUDY; EXTRACELLULAR SPACE; GENE OVEREXPRESSION; HIPPOCAMPUS POTENTIAL; LEARNING; LONG TERM POTENTIATION; MOUSE; NERVE CELL PLASTICITY; NONHUMAN; PRIORITY JOURNAL; PROTEIN DEGRADATION; PROTEIN EXPRESSION; SPATIAL ORIENTATION; SYNAPTIC MEMBRANE; TRANSGENIC MOUSE;

ANIMALS; ELECTROPHYSIOLOGY; GENE EXPRESSION; HIPPOCAMPUS; LEARNING; LONG-TERM POTENTIATION; MEMORY; MICE; MICE, TRANSGENIC; NEURONS; SPACE PERCEPTION; SWIMMING; SYNAPSES; TISSUE PLASMINOGEN ACTIVATOR; TRANSGENES;

ANIMALIA; HIPPOCAMPUS HIPPOCAMPUS; MUS MUSCULUS;

EID: 0033151831     PISSN: 02614189     EISSN: None     Source Type: Journal    
DOI: 10.1093/emboj/18.11.3007     Document Type: Article

References (34)

1. Carmeliet, P. et al. (1994) Physiological consequences of loss of plasminogen activator gene function in mice. Nature, 368, 419-424.
2. Chen, Z.L. and Strickland, S. (1997) Neuronal death in the hippocampus is promoted by plasmin-catalyzed degradation of laminin. Cell, 91, 917-925.
3. Davies, B.J., Pickard, B.S., Steel, M., Morris, R.G.M. and Lathe, R. (1998) Serine proteases in rodent hippocampus. J. Biol. Chem., 273, 23004-23011.
4. Endo, A., Nagai, N., Urano, T., Ihara, H., Takada, Y., Hashimoto, K. and Takada, A. (1998) Proteolysis of highly polysialylated NCAM by the tissue plasminogen activator-plasmin system in rats. Neurosci. Lett., 246, 37-40.
5. Evans, G.A., Ingraham, H.A., Lewis, K., Cunningham, K., Seki, T., Moriuchi, T., Chang, H.C., Silver, J. and Hyman, R. (1984) Expression of the Thy-1 glycoprotein gene by DNA-mediated gene transfer. Proc. Natl Acad. Sci. USA, 81, 5532-5536.
6. Frey, U., Muller, M. and Kuhl, D. (1996) A different form of long-lasting potentiation revealed in tissue plasminogen activator mutant mice. J. Neurosci., 16, 2057-2063.
7. Gschwend, T.P., Krueger, S.R., Kozlov, S.V., Wolfer, D.P. and Sonderegger, P. (1997) Neurotrypsin, a novel multidomain serine protease expressed in the nervous system. Mol. Cell. Neurosci., 9, 207-219.
8. Guzowski, J.F. and McGaugh, J.L. (1997) Antisense oligodeoxynucleotide-mediated disruption of hippocampal cAMP response element binding protein levels impairs consolidation of memory for water maze training. Proc. Natl Acad. Sci. USA, 94, 2693-2698.
9. Hogan, B., Beddington, R., Costantini, F. and Lacy, E. (1994) Manipulating the Mouse Embryo: A Laboratory Manual. 2nd edn. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NY.
10. Huang, Y.Y. et al. (1996) 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, 8699-8704.
11. Kelley, K.A., Friedrich, V.L., Jr, Sonshine, A., Hu, Y., Lax, J., Li, J., Drinkwater, D., Dressler, H. and Herrup, K. (1994) Expression of Thy-1/lacZ fusion genes in the CNS of transgenic mice. Brain Res. Mol. Brain Res., 24, 261-274.
12. Manabe, T. et al. (1998) Facilitation of long-term potentiation and memory in mice lacking nociceptin receptors. Nature, 394, 577-581.
13. Mars, W., Zarnegra, R. and Michalopoulos, G. (1993) Activation of hepatocyte growth factor by the plasminogen activators uPA and tPA. Am. J. Pathol. 143, 949-958.
14. Morris, R. (1984) Developments of a water-maze procedure for studying spatial learning in the rat, J. Neurosci. Methods, 11, 47-60.
15. Müller, C.M. and Griesinger, C.B. (1998) Tissue plasminogen activator mediates reverse occlusion plasticity in visual cortex. Nature Neurosci., 1, 47-53.
16. Muller, D., Wang, C., Skibo, G., Toni, N., Cremer, H., Calaora, V., Rougon, G. and Kiss, J.Z. (1996) PSA-NCAM is required for activity-induced synaptic plasticity. Neuron, 17, 413-422.
17. Ohlsson, M., Hsueh, A. J. and Ny, T. (1988) Hormonal regulation of tissue-type plasminogen activator messenger ribonucleic acid levels in rat granulosa cells: mechanisms of induction by follicle-stimulating hormone and gonadotropin releasing hormone. Mol. Endocrinol., 2, 854-861.
18. Osterwalder, T, Cinelli, P., Baici, A., Pennella, A., Krueger, S.R., Schrimpf, S.P., Meins, M. and Sonderegger, P. (1998) The axonally secreted serine proteinase inhibitor, neuroserpin, inhibits plasminogen activators and plasmin but not thrombin. J. Biol. Chem., 273, 2312-2321.
19. 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.
20. Rickles, R.J., Darrow, A.L. and Strickland, S. (1988) Molecular cloning of complementary DNA to mouse tissue plasminogen activator mRNA and its expression during F9 teratocarcinoma cell differentiation. J. Biol. Chem., 263, 1563-1569.
21. Saksela, O. and Rifkin, D.B. (1988) Cell-associated plasminogen activation: regulation and physiological functions. Annu. Rev. Cell Biol., 4, 93-126.
22. Sappino, A.P., Huarte, J., Vassalli, J.D. and Belin, D. (1991) Sites of synthesis of urokinase and tissue-type plasminogen activators in the murine kidney. J. Clin. Invest., 87, 962-970.
23. Sappino, A.P., Madani, R., Huarte, J., Belin, D., Kiss, J.Z., Wohlwend, A. and Vassalli, J.D. (1993) Extracellular proteolysis in the adult murine brain. J. Clin. Invest., 92, 679-685.
24. Scarisbrick, I.A., Towner, M.D. and Isackson, P.J. (1997) Nervous system-specific expression of a novel serine protease: regulation in the adult rat spinal cord by excitotoxic injury. J. Neurosci., 17, 8156-8168.
25. Schenk, F. (1989) A homing procedure for studying spatial memory in immature and adult rodents. J. Neurosci. Methods, 26, 249-258.
26. 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.
27. Stone, S.R., Nick, H., Hofsteenge, J. and Monard, D. (1987) Glial-derived neurite-promoting factor is a slow-binding inhibitor of trypsin, thrombin and urokinase. Arch. Biochem. Biophys., 252, 237-244.
28. Thewke, D.P. and Seeds, N.W. (1996) Expression of hepatocyte growth factor/scatter factor, its receptor, c-met and tissue-type plasminogen activator during development of the murine olfactory system. J. Neurosci., 16, 6933-6944.
29. 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.
30. Tsirka, S.E., Rogove, A.D. and Strickland, S. (1996) Neuronal cell death and tPA. Nature, 384, 123-124.
31. Tsirka, S.E., Rogove, A.D., Bugge, T.H., Degen, J.L. and Strickland, S. (1997) An extracellular proteolytic cascade promotes neuronal degeneration in the mouse hippocampus. J. Neurosci., 17, 543-552.
32. Vassalli, J.D., Sappino, A.P. and Belin, D. (1991) The plasminogen activator/plasmin system. J. Clin. Invest., 88, 1067-1072.
33. Vidal, M., Morris, R., Grosveld, F. and Spanopoulou, E. (1990) Tissue-specific control elements of the Thy-1 gene. EMBO J., 9, 833-840.
34. Yamashiro, K., Tsuruoka, N., Kodama, S., Tsujimoto, M., Yamamura, Y., Tanaka, T., Nakazato, H. and Yamaguchi, N. (1997) Molecular cloning of a novel trypsin-like serine protease (neurosin) preferentially expressed in brain. Biochim. Biophys. Acta, 1350, 11-14.