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Synaptic plasticity-associated proteases and protease inhibitors in the brain linked to the processing of extracellular matrix and cell adhesion molecules

Published online by Cambridge University Press:  13 August 2009

Tet Woo Lee
Affiliation:
School of Biological Sciences, University of Auckland, Private Bag 92019, Auckland, New Zealand
Vicky W.K. Tsang
Affiliation:
School of Biological Sciences, University of Auckland, Private Bag 92019, Auckland, New Zealand
Nigel P. Birch*
Affiliation:
School of Biological Sciences, University of Auckland, Private Bag 92019, Auckland, New Zealand
*
Correspondence should be addressed to: Nigel P. Birch, School of Biological Sciences, Level 2 Thomas BuildingUniversity of Auckland, Private Bag 92019, Auckland 1010, New Zealand phone: +64 9 373 7599 ex 88239 fax: +64 9 373 7414 email: n.birch@auckland.ac.nz

Abstract

Research on the molecular and cellular basis of learning and memory has focused on the mechanisms that underlie the induction and expression of synaptic plasticity. There is increasing evidence that structural changes at the synapse are associated with synaptic plasticity and that extracellular matrix (ECM) components and cell adhesion molecules are associated with these changes. The functions of both groups of molecules can be regulated by proteolysis. In this article we review the roles of selected proteases and protease inhibitors in perisynaptic proteolysis of the ECM and synaptic adhesion proteins and the impact of proteolysis on synaptic modification and cognitive function.

Type
Research Article
Copyright
Copyright © Cambridge University Press 2009

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References

REFERENCES

Abe, K., Chisaka, O., Roy, F.V. and Takeichi, M. (2004) Stability of dendritic spines and synaptic contacts is controlled by alpha N-catenin. Nature Neuroscience 7, 357363.CrossRefGoogle ScholarPubMed
Alberini, C.M. (2009) Transcription factors in long-term memory and synaptic plasticity. Physiological Reviews 89, 121145.CrossRefGoogle ScholarPubMed
Aonurm-Helm, A., Zharkovsky, T., Jürgenson, M., Kalda, A. and Zharkovsky, A. (2008) Dysregulated CREB signaling pathway in the brain of neural cell adhesion molecule (NCAM)-deficient mice. Brain Research 1243, 104112.CrossRefGoogle ScholarPubMed
Aoto, J. and Chen, L. (2007) Bidirectional ephrin/Eph signaling in synaptic functions. Brain Research 1184, 7280.CrossRefGoogle ScholarPubMed
Arikkath, J., Peng, I.-F., Ng, Y.G., Israely, I., Liu, X., Ullian, E.M. et al. (2009) Delta-catenin regulates spine and synapse morphogenesis and function in hippocampal neurons during development. Journal of Neuroscience 29, 54355442.CrossRefGoogle ScholarPubMed
Arikkath, J. and Reichardt, L.F. (2008) Cadherins and catenins at synapses: roles in synaptogenesis and synaptic plasticity. Trends in Neurosciences 31, 487494.CrossRefGoogle ScholarPubMed
Bamji, S.X., Shimazu, K., Kimes, N., Huelsken, J., Birchmeier, W., Lu, B. et al. (2003) Role of beta-catenin in synaptic vesicle localization and presynaptic assembly. Neuron 40, 719731.CrossRefGoogle ScholarPubMed
Baranes, D., Lederfein, D., Huang, Y.Y., Chen, M., Bailey, C.H. and Kandel, E.R. (1998) Tissue plasminogen activator contributes to the late phase of LTP and to synaptic growth in the hippocampal mossy fiber pathway. Neuron 21, 813825.CrossRefGoogle Scholar
Barker-Carlson, K., Lawrence, D.A. and Schwartz, B.S. (2002) Acyl-enzyme complexes between tissue-type plasminogen activator and neuroserpin are short-lived in vitro. Journal of Biological Chemistry 277, 4685246857.CrossRefGoogle ScholarPubMed
Bell, K.F.S., Zheng, L., Fahrenholz, F. and Cuello, A.C. (2008) ADAM-10 over-expression increases cortical synaptogenesis. Neurobiology of Aging 29, 554565.CrossRefGoogle ScholarPubMed
Berezovska, O., McLean, P., Knowles, R., Frosh, M., Lu, F.M., Lux, S.E. et al. (1999) Notch1 inhibits neurite outgrowth in postmitotic primary neurons. Neuroscience 93, 433439.CrossRefGoogle ScholarPubMed
Bilousova, T.V., Rusakov, D.A., Ethell, D.W. and Ethell, I.M. (2006) Matrix metalloproteinase-7 disrupts dendritic spines in hippocampal neurons through NMDA receptor activation. Journal of Neurochemistry 97, 4456.CrossRefGoogle ScholarPubMed
Bozdagi, O., Nagy, V., Kwei, K.T. and Huntley, G.W. (2007) In vivo roles for matrix metalloproteinase-9 in mature hippocampal synaptic physiology and plasticity. Journal of Neurophysiology 98, 334344.CrossRefGoogle ScholarPubMed
Bozdagi, O., Shan, W., Tanaka, H., Benson, D.L. and Huntley, G.W. (2000) Increasing numbers of synaptic puncta during late-phase LTP: N-cadherin is synthesized, recruited to synaptic sites, and required for potentiation. Neuron 28, 245259.CrossRefGoogle ScholarPubMed
Brou, C., Logeat, F., Gupta, N., Bessia, C., LeBail, O., Doedens, J.R. et al. (2000) A novel proteolytic cleavage involved in Notch signaling: the role of the disintegrin-metalloprotease TACE. Molecular Cell 5, 207216.CrossRefGoogle ScholarPubMed
Cao, C., Lawrence, D.A., Li, Y., Arnim, C.A.F.V., Herz, J., Su, E.J. et al. (2006) Endocytic receptor LRP together with tPA and PAI-1 coordinates Mac-1-dependent macrophage migration. EMBO Journal 25, 18601870.CrossRefGoogle ScholarPubMed
Chaillan, F.A., Rivera, S., Marchetti, E., Jourquin, J., Werb, Z., Soloway, P.D. et al. (2006) Involvement of tissue inhibition of metalloproteinases-1 in learning and memory in mice. Behavioural Brain Research 173, 191198.CrossRefGoogle ScholarPubMed
Chen, Q., Nakajima, A., Choi, S.H., Xiong, X. and Tang, Y.-P. (2008) Loss of presenilin function causes Alzheimer’s disease-like neurodegeneration in the mouse. Journal of Neuroscience Research 86, 16151625.CrossRefGoogle ScholarPubMed
Chen, Z.L. and Strickland, S. (1997) Neuronal death in the hippocampus is promoted by plasmin-catalyzed degradation of laminin. Cell 91, 917925.CrossRefGoogle ScholarPubMed
Chen, Z.L., Yoshida, S., Kato, K., Momota, Y., Suzuki, J., Tanaka, T. et al. (1995) Expression and activity-dependent changes of a novel limbic-serine protease gene in the hippocampus. Journal of Neuroscience 15, 50885097.CrossRefGoogle ScholarPubMed
Costa, R.M., Honjo, T. and Silva, A.J. (2003) Learning and memory deficits in Notch mutant mice. Current Biology 13, 13481354.CrossRefGoogle ScholarPubMed
Dalva, M.B., McClelland, A.C. and Kayser, M.S. (2007) Cell adhesion molecules: signalling functions at the synapse. Nature Reviews Neuroscience 8, 206220.CrossRefGoogle ScholarPubMed
D'Arcangelo, G., Miao, G.G., Chen, S.C., Soares, H.D., Morgan, J.I. and Curran, T. (1995) A protein related to extracellular matrix proteins deleted in the mouse mutant reeler. Nature 374, 719723.CrossRefGoogle ScholarPubMed
Dash, P.K., Moore, A.N. and Orsi, S.A. (2005) Blockade of gamma-secretase activity within the hippocampus enhances long-term memory. Biochemical and Biophysical Research Communications 338, 777782.CrossRefGoogle ScholarPubMed
de Rouvroit, C.L., de Bergeyck, V., Cortvrindt, C., Bar, I., Eeckhout, Y. and Goffinet, A.M. (1999) Reelin, the extracellular matrix protein deficient in reeler mutant mice, is processed by a metalloproteinase. Experimental Neurology 156, 214217.CrossRefGoogle Scholar
Diestel, S., Hinkle, C.L., Schmitz, B. and Maness, P.F. (2005) NCAM140 stimulates integrin-dependent cell migration by ectodomain shedding. Journal of Neurochemistry 95, 17771784.CrossRefGoogle ScholarPubMed
Dityatev, A. and Schachner, M. (2003) Extracellular matrix molecules and synaptic plasticity. Nature Reviews Neuroscience 4, 456468.CrossRefGoogle ScholarPubMed
Doyle, E., Nolan, P.M., Bell, R. and Regan, C.M. (1992) Intraventricular infusions of anti-neural cell adhesion molecules in a discrete posttraining period impair consolidation of a passive avoidance response in the rat. Journal of Neurochemistry 59, 15701573.CrossRefGoogle Scholar
Dreier, L., Burbea, M. and Kaplan, J.M. (2005) LIN-23-mediated degradation of beta-catenin regulates the abundance of GLR-1 glutamate receptors in the ventral nerve cord of C. elegans. Neuron 46, 5164.CrossRefGoogle ScholarPubMed
Dzwonek, J., Rylski, M. and Kaczmarek, L. (2004) Matrix metalloproteinases and their endogenous inhibitors in neuronal physiology of the adult brain. FEBS Letters 567, 129135.CrossRefGoogle ScholarPubMed
Edbauer, D., Winkler, E., Regula, J.T., Pesold, B., Steiner, H. and Haass, C. (2003) Reconstitution of gamma-secretase activity. Nature Cell Biology 5, 486488.CrossRefGoogle ScholarPubMed
Edwards, D.R., Handsley, M.M. and Pennington, C.J. (2008) The ADAM metalloproteinases. Molecular Aspects of Medicine 29, 258289.CrossRefGoogle ScholarPubMed
Elia, L.P., Yamamoto, M., Zang, K. and Reichardt, L.F. (2006) p120 catenin regulates dendritic spine and synapse development through Rho-family GTPases and cadherins. Neuron 51, 4356.CrossRefGoogle ScholarPubMed
Endo, A., Nagai, N., Urano, T., Takada, Y., Hashimoto, K. and Takada, A. (1999) Proteolysis of neuronal cell adhesion molecule by the tissue plasminogen activator-plasmin system after kainate injection in the mouse hippocampus. Neuroscience Research 33, 18.CrossRefGoogle ScholarPubMed
Ethell, I.M. and Ethell, D.W. (2007) Matrix metalloproteinases in brain development and remodeling: synaptic functions and targets. Journal of Neuroscience Research 85, 28132823.CrossRefGoogle ScholarPubMed
Fernández-Monreal, M., López-Atalaya, J.P., Benchenane, K., Cacquevel, M., Dulin, F., Caer, J.-P.L. et al. (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. Journal of Biological Chemistry 279, 5085050856.CrossRefGoogle ScholarPubMed
Fukata, Y., Adesnik, H., Iwanaga, T., Bredt, D.S., Nicoll, R.A. and Fukata, M. (2006) Epilepsy-related ligand/receptor complex LGI1 and ADAM22 regulate synaptic transmission. Science 313, 17921795.CrossRefGoogle ScholarPubMed
Gahmberg, C.G., Tian, L., Ning, L. and Nyman-Huttunen, H. (2008) ICAM-5–a novel two-facetted adhesion molecule in the mammalian brain. Immunology Letters 117, 131135.CrossRefGoogle ScholarPubMed
Georgakopoulos, A., Marambaud, P., Efthimiopoulos, S., Shioi, J., Cui, W., Li, H.C. et al. (1999) Presenilin-1 forms complexes with the cadherin/catenin cell–cell adhesion system and is recruited to intercellular and synaptic contacts. Molecular Cell 4, 893902.CrossRefGoogle ScholarPubMed
Gutwein, P., Mechtersheimer, S., Riedle, S., Stoeck, A., Gast, D., Joumaa, S. et al. (2003) ADAM10-mediated cleavage of L1 adhesion molecule at the cell surface and in released membrane vesicles. FASEB Journal 17, 292294.CrossRefGoogle ScholarPubMed
Hartmann, D., de Strooper, B., Serneels, L., Craessaerts, K., Herreman, A., Annaert, W. et al. (2002) The disintegrin/metalloprotease ADAM 10 is essential for Notch signalling but not for alpha-secretase activity in fibroblasts. Human Molecular Genetics 11, 26152624.CrossRefGoogle Scholar
Hattori, M., Osterfield, M. and Flanagan, J.G. (2000) Regulated cleavage of a contact-mediated axon repellent. Science 289, 13601365.CrossRefGoogle ScholarPubMed
Hübschmann, M.V., Skladchikova, G., Bock, E. and Berezin, V. (2005) Neural cell adhesion molecule function is regulated by metalloproteinase-mediated ectodomain release. Journal of Neuroscience Research 80, 826837.CrossRefGoogle ScholarPubMed
Hino, H., Akiyama, H., Iseki, E., Kato, M., Kondo, H., Ikeda, K. et al. (2001) Immunohistochemical localization of plasminogen activator inhibitor-1 in rat and human brain tissues. Neuroscience Letters 297, 105108.CrossRefGoogle ScholarPubMed
Hodkinson, P.S., Elliott, P.A., Lad, Y., McHugh, B.J., MacKinnon, A.C., Haslett, C. et al. (2007) Mammalian NOTCH-1 activates beta1 integrins via the small GTPase R-Ras. Journal of Biological Chemistry 282, 2899129001.CrossRefGoogle ScholarPubMed
Hoffman, K.B., Martinez, J. and Lynch, G. (1998) Proteolysis of cell adhesion molecules by serine proteases: a role in long term potentiation? Brain Research 811, 2933.CrossRefGoogle ScholarPubMed
Horiuchi, K., Gall, S.L., Schulte, M., Yamaguchi, T., Reiss, K., Murphy, G. et al. (2007) Substrate selectivity of epidermal growth factor-receptor ligand sheddases and their regulation by phorbol esters and calcium influx. Molecular Biology of the Cell 18, 176188.CrossRefGoogle ScholarPubMed
Huang, Y.Y., Bach, M.E., Lipp, H.P., Zhuo, M., Wolfer, D.P., Hawkins, R.D. 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. Proceedings of the National Academy of Sciences of the U.S.A. 93, 86998704.CrossRefGoogle ScholarPubMed
Jossin, Y., Gui, L. and Goffinet, A.M. (2007) Processing of Reelin by embryonic neurons is important for function in tissue but not in dissociated cultured neurons. Journal of Neuroscience 27, 42434252.CrossRefGoogle ScholarPubMed
Jossin, Y., Ignatova, N., Hiesberger, T., Herz, J., de Rouvroit, C.L. and Goffinet, A.M. (2004) The central fragment of Reelin, generated by proteolytic processing in vivo, is critical to its function during cortical plate development. Journal of Neuroscience 24, 514521.CrossRefGoogle ScholarPubMed
Kalus, I., Bormann, U., Mzoughi, M., Schachner, M. and Kleene, R. (2006) Proteolytic cleavage of the neural cell adhesion molecule by ADAM17/TACE is involved in neurite outgrowth. Journal of Neurochemistry 98, 7888.CrossRefGoogle ScholarPubMed
Kato, K., Kishi, T., Kamachi, T., Akisada, M., Oka, T., Midorikawa, R. et al. (2001) Serine proteinase inhibitor 3 and murinoglobulin I are potent inhibitors of neuropsin in adult mouse brain. Journal of Biological Chemistry 276, 1456214571.CrossRefGoogle ScholarPubMed
Kim, D.Y., Ingano, L.A.M. and Kovacs, D.M. (2002) Nectin-1alpha, an immunoglobulin-like receptor involved in the formation of synapses, is a substrate for presenilin/gamma-secretase-like cleavage. Journal of Biological Chemistry 277, 4997649981.CrossRefGoogle ScholarPubMed
Kobayashi, D., Zeller, M., Cole, T., Buttini, M., McConlogue, L., Sinha, S. et al. (2008) BACE1 gene deletion: impact on behavioral function in a model of Alzheimer's disease. Neurobiology of Aging 29, 861873.CrossRefGoogle Scholar
Kohno, S., Kohno, T., Nakano, Y., Suzuki, K., Ishii, M., Tagami, H. et al. (2009) Mechanism and significance of specific proteolytic cleavage of Reelin. Biochemical and Biophysical Research Communications 380, 9397.CrossRefGoogle ScholarPubMed
Komai, S., Matsuyama, T., Matsumoto, K., Kato, K., Kobayashi, M., Imamura, K. et al. (2000) Neuropsin regulates an early phase of schaffer-collateral long-term potentiation in the murine hippocampus. European Journal of Neuroscience 12, 14791486.CrossRefGoogle ScholarPubMed
Krueger, S.R., Ghisu, G.P., Cinelli, P., Gschwend, T.P., Osterwalder, T., Wolfer, D.P. et al. (1997) Expression of neuroserpin, an inhibitor of tissue plasminogen activator, in the developing and adult nervous system of the mouse. Journal of Neuroscience 17, 89848996.CrossRefGoogle ScholarPubMed
Kulahin, N., Li, S., Hinsby, A., Kiselyov, V., Berezin, V. and Bock, E. (2008) Fibronectin type III (FN3) modules of the neuronal cell adhesion molecule L1 interact directly with the fibroblast growth factor (FGF) receptor. Molecular and Cellular Neurosciences 37, 528536.CrossRefGoogle ScholarPubMed
Laird, F.M., Cai, H., Savonenko, A.V., Farah, M.H., He, K., Melnikova, T. et al. (2005) BACE1, a major determinant of selective vulnerability of the brain to amyloid-beta amyloidogenesis, is essential for cognitive, emotional, and synaptic functions. Journal of Neuroscience 25, 1169311709.CrossRefGoogle Scholar
Lee, T.W., Coates, L.C. and Birch, N.P. (2008) Neuroserpin regulates N-cadherin-mediated cell adhesion independently of its activity as an inhibitor of tissue plasminogen activator. Journal of Neuroscience Research 86, 12431253.CrossRefGoogle ScholarPubMed
Leong, K.G., Hu, X., Li, L., Noseda, M., Larrivée, B., Hull, C. et al. (2002) Activated Notch4 inhibits angiogenesis: role of beta 1-integrin activation. Molecular and Cellular Biology 22, 28302841.CrossRefGoogle ScholarPubMed
Levenson, J.M., Qiu, S. and Weeber, E.J. (2008) The role of reelin in adult synaptic function and the genetic and epigenetic regulation of the reelin gene. Biochimica et Biophysica Acta 1779, 422431.CrossRefGoogle ScholarPubMed
Lochner, J.E., Honigman, L.S., Grant, W.F., Gessford, S.K., Hansen, A.B., Silverman, M.A. et al. (2006) Activity-dependent release of tissue plasminogen activator from the dendritic spines of hippocampal neurons revealed by live-cell imaging. Journal of Neurobiology 66, 564577.CrossRefGoogle ScholarPubMed
Lüthi, A., der Putten, H.V., Botteri, F.M., Mansuy, I.M., Meins, M., Frey, U. et al. (1997) Endogenous serine protease inhibitor modulates epileptic activity and hippocampal long-term potentiation. Journal of Neuroscience 17, 46884699.CrossRefGoogle ScholarPubMed
Lüthi, A., Mohajeri, H., Schachner, M. and Laurent, J.P. (1996) Reduction of hippocampal long-term potentiation in transgenic mice ectopically expressing the neural cell adhesion molecule L1 in astrocytes. Journal of Neuroscience Research 46, 16.3.0.CO;2-P>CrossRefGoogle ScholarPubMed
Lüthl, A., Laurent, J.P., Figurov, A., Muller, D. and Schachner, M. (1994) Hippocampal long-term potentiation and neural cell adhesion molecules L1 and NCAM. Nature 372, 777779.CrossRefGoogle Scholar
Madani, R., Hulo, S., Toni, N., Madani, H., Steimer, T., Muller, D. et al. (1999) Enhanced hippocampal long-term potentiation and learning by increased neuronal expression of tissue-type plasminogen activator in transgenic mice. EMBO Journal 18, 30073012.CrossRefGoogle ScholarPubMed
Madani, R., Kozlov, S., Akhmedov, A., Cinelli, P., Kinter, J., Lipp, H.-P. et al. (2003) Impaired explorative behavior and neophobia in genetically modified mice lacking or overexpressing the extracellular serine protease inhibitor neuroserpin. Molecular and Cellular Neurosciences 23, 473494.CrossRefGoogle ScholarPubMed
Maness, P.F. and Schachner, M. (2007) Neural recognition molecules of the immunoglobulin superfamily: signaling transducers of axon guidance and neuronal migration. Nature Neuroscience 10, 1926.CrossRefGoogle ScholarPubMed
Marambaud, P., Wen, P.H., Dutt, A., Shioi, J., Takashima, A., Siman, R. et al. (2003) A CBP binding transcriptional repressor produced by the PS1/epsilon-cleavage of N-cadherin is inhibited by PS1 FAD mutations. Cell 114, 635645.Google ScholarPubMed
Maretzky, T., Schulte, M., Ludwig, A., Rose-John, S., Blobel, C., Hartmann, D. et al. (2005) L1 is sequentially processed by two differently activated metalloproteases and presenilin/gamma-secretase and regulates neural cell adhesion, cell migration, and neurite outgrowth. Molecular and Cellular Biology 25, 90409053.CrossRefGoogle ScholarPubMed
Mataga, N., Mizuguchi, Y. and Hensch, T.K. (2004) Experience-dependent pruning of dendritic spines in visual cortex by tissue plasminogen activator. Neuron 44, 10311041.CrossRefGoogle ScholarPubMed
Mataga, N., Nagai, N. and Hensch, T.K. (2002) Permissive proteolytic activity for visual cortical plasticity. Proceedings of the National Academy of Sciences of the U.S.A. 99, 77177721.CrossRefGoogle ScholarPubMed
Matsumoto-Miyai, K., Ninomiya, A., Yamasaki, H., Tamura, H., Nakamura, Y. and Shiosaka, S. (2003) NMDA-dependent proteolysis of presynaptic adhesion molecule L1 in the hippocampus by neuropsin. Journal of Neuroscience 23, 77277736.CrossRefGoogle ScholarPubMed
Matsuno, M., Horiuchi, J., Tully, T. and Saitoe, M. (2009) The Drosophila cell adhesion molecule klingon is required for long-term memory formation and is regulated by Notch. Proceedings of the National Academy of Sciences of the U.S.A. 106, 310315.CrossRefGoogle ScholarPubMed
Meighan, P.C., Meighan, S.E., Davis, C.J., Wright, J.W. and Harding, J.W. (2007) Effects of matrix metalloproteinase inhibition on short- and long-term plasticity of schaffer collateral/CA1 synapses. Journal of Neurochemistry 102, 20852096.CrossRefGoogle Scholar
Meighan, S.E., Meighan, P.C., Choudhury, P., Davis, C.J., Olson, M.L., Zornes, P.A. et al. (2006) Effects of extracellular matrix-degrading proteases matrix metalloproteinases 3 and 9 on spatial learning and synaptic plasticity. Journal of Neurochemistry 96, 12271241.CrossRefGoogle ScholarPubMed
Miller, C.A. and Sweatt, J.D. (2007) Covalent modification of DNA regulates memory formation. Neuron 53, 857869.CrossRefGoogle ScholarPubMed
Miranda, E. and Lomas, D.A. (2006) Neuroserpin: a serpin to think about. Cellular and Molecular Life Sciences 63, 709722.CrossRefGoogle ScholarPubMed
Monea, S., Jordan, B.A., Srivastava, S., DeSouza, S. and Ziff, E.B. (2006) Membrane localization of membrane type 5 matrix metalloproteinase by AMPA receptor binding protein and cleavage of cadherins. Journal of Neuroscience 26, 23002312.CrossRefGoogle ScholarPubMed
Müller, C.M. and Griesinger, C.B. (1998) Tissue plasminogen activator mediates reverse occlusion plasticity in visual cortex. Nature Neuroscience 1, 4753.CrossRefGoogle ScholarPubMed
Mumm, J.S., Schroeter, E.H., Saxena, M.T., Griesemer, A., Tian, X., Pan, D.J. et al. (2000) A ligand-induced extracellular cleavage regulates gamma-secretase-like proteolytic activation of Notch1. Molecular Cell 5, 197206.CrossRefGoogle ScholarPubMed
Nagai, N., Urano, T., Endo, A., Takahashi, H., Takada, Y. and Takada, A. (1999) Neuronal degeneration and a decrease in laminin-like immunoreactivity is associated with elevated tissue-type plasminogen activator in the rat hippocampus after kainic acid injection. Neuroscience Research 33, 147154.CrossRefGoogle Scholar
Nagy, V., Bozdagi, O. and Huntley, G.W. (2007) The extracellular protease matrix metalloproteinase-9 is activated by inhibitory avoidance learning and required for long-term memory. Learning & Memory 14, 655664.CrossRefGoogle ScholarPubMed
Nagy, V., Bozdagi, O., Matynia, A., Balcerzyk, M., Okulski, P., Dzwonek, J. et al. (2006) Matrix metalloproteinase-9 is required for hippocampal late-phase long-term potentiation and memory. Journal of Neuroscience 26, 19231934.CrossRefGoogle ScholarPubMed
Nakagami, Y., Abe, K., Nishiyama, N. and Matsuki, N. (2000) Laminin degradation by plasmin regulates long-term potentiation. Journal of Neuroscience 20, 20032010.CrossRefGoogle ScholarPubMed
Nakamura, Y., Tamura, H., Horinouchi, K. and Shiosaka, S. (2006) Role of neuropsin in formation and maturation of Schaffer-collateral L1cam-immunoreactive synaptic boutons. Journal of Cell Science 119, 13411349.CrossRefGoogle ScholarPubMed
Nayeem, N., Silletti, S., Yang, X., Lemmon, V.P., Reisfeld, R.A., Stallcup, W.B. et al. (1999) A potential role for the plasmin(ogen) system in the posttranslational cleavage of the neural cell adhesion molecule L1. Journal of Cell Science 112, 47394749.CrossRefGoogle ScholarPubMed
Ohno, M., Chang, L., Tseng, W., Oakley, H., Citron, M., Klein, W.L. et al. (2006) Temporal memory deficits in Alzheimer's mouse models: rescue by genetic deletion of BACE1. European Journal of Neuroscience 23, 251260.CrossRefGoogle ScholarPubMed
Ohno, M., Sametsky, E.A., Younkin, L.H., Oakley, H., Younkin, S.G., Citron, M. et al. (2004) BACE1 deficiency rescues memory deficits and cholinergic dysfunction in a mouse model of Alzheimer's disease. Neuron 41, 2733.CrossRefGoogle Scholar
Okuda, T., Yu, L.M.Y., Cingolani, L.A., Kemler, R. and Goda, Y. (2007) beta-Catenin regulates excitatory postsynaptic strength at hippocampal synapses. Proceedings of the National Academy of Sciences of the U.S.A. 104, 1347913484.CrossRefGoogle ScholarPubMed
Okulski, P., Jay, T.M., Jaworski, J., Duniec, K., Dzwonek, J., Konopacki, F.A. et al. (2007) TIMP-1 abolishes MMP-9-dependent long-lasting long-term potentiation in the prefrontal cortex. Biological Psychiatry 62, 359362.CrossRefGoogle ScholarPubMed
Oray, S., Majewska, A. and Sur, M. (2004) Dendritic spine dynamics are regulated by monocular deprivation and extracellular matrix degradation. Neuron 44, 10211030.CrossRefGoogle ScholarPubMed
Pang, P.T., Teng, H.K., Zaitsev, E., Woo, N.T., Sakata, K., Zhen, S. et al. (2004) Cleavage of proBDNF by tPA/plasmin is essential for long-term hippocampal plasticity. Science 306, 487491.CrossRefGoogle ScholarPubMed
Parkin, E. and Harris, B. (2009) A disintegrin and metalloproteinase (ADAM)-mediated ectodomain shedding of ADAM10. Journal of Neurochemistry 108, 14641479.CrossRefGoogle ScholarPubMed
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, 453457.CrossRefGoogle ScholarPubMed
Reinhard, E., Suidan, H.S., Pavlik, A. and Monard, D. (1994) Glia-derived nexin/protease nexin-1 is expressed by a subset of neurons in the rat brain. Journal of Neuroscience Research 37, 256270.CrossRefGoogle ScholarPubMed
Reiss, K., Maretzky, T., Ludwig, A., Tousseyn, T., de Strooper, B., Hartmann, D. et al. (2005) ADAM10 cleavage of N-cadherin and regulation of cell-cell adhesion and beta-catenin nuclear signalling. EMBO Journal 24, 742752.CrossRefGoogle ScholarPubMed
Sagane, K., Hayakawa, K., Kai, J., Hirohashi, T., Takahashi, E., Miyamoto, N. et al. (2005) Ataxia and peripheral nerve hypomyelination in ADAM22-deficient mice. BMC Neuroscience 6, 33.CrossRefGoogle ScholarPubMed
Samson, A.L., Nevin, S.T., Croucher, D., Niego, B., Daniel, P.B., Weiss, T.W. et al. (2008) Tissue-type plasminogen activator requires a co-receptor to enhance NMDA receptor function. Journal of Neurochemistry 107, 10911101.CrossRefGoogle ScholarPubMed
Saura, C.A., Choi, S.Y., Beglopoulos, V., Malkani, S., Zhang, D., Rao, B.S.S. et al. (2004) Loss of presenilin function causes impairments of memory and synaptic plasticity followed by age-dependent neurodegeneration. Neuron 42, 2336.CrossRefGoogle ScholarPubMed
Schmitt, U., Hiemke, C., Fahrenholz, F. and Schroeder, A. (2006) Over-expression of two different forms of the alpha-secretase ADAM10 affects learning and memory in mice. Behavioural Brain Research 175, 278284.CrossRefGoogle ScholarPubMed
Scott, R.W., Bergman, B.L., Bajpai, A., Hersh, R.T., Rodriguez, H., Jones, B.N. et al. (1985) Protease nexin. Properties and a modified purification procedure. Journal of Biological Chemistry 260, 70297034.CrossRefGoogle Scholar
Seeds, N.W., Basham, M.E. and Ferguson, J.E. (2003) Absence of tissue plasminogen activator gene or activity impairs mouse cerebellar motor learning. Journal of Neuroscience 23, 73687375.CrossRefGoogle ScholarPubMed
Seeds, N.W., Williams, B.L. and Bickford, P.C. (1995) Tissue plasminogen activator induction in Purkinje neurons after cerebellar motor learning. Science 270, 19921994.CrossRefGoogle ScholarPubMed
Selkoe, D.J. and Wolfe, M.S. (2007) Presenilin: running with scissors in the membrane. Cell 131, 215221.CrossRefGoogle ScholarPubMed
Sestan, N., Artavanis-Tsakonas, S. and Rakic, P. (1999) Contact-dependent inhibition of cortical neurite growth mediated by notch signaling. Science 286, 741746.CrossRefGoogle ScholarPubMed
Shapiro, L., Love, J. and Colman, D.R. (2007) Adhesion molecules in the nervous system: structural insights into function and diversity. Annual Review of Neuroscience 30, 451474.CrossRefGoogle ScholarPubMed
Shimizu, C., Yoshida, S., Shibata, M., Kato, K., Momota, Y., Matsumoto, K. et al. (1998) Characterization of recombinant and brain neuropsin, a plasticity-related serine protease. Journal of Biological Chemistry 273, 1118911196.CrossRefGoogle ScholarPubMed
Specht, C.G. and Triller, A. (2008) The dynamics of synaptic scaffolds. Bioessays 30, 10621074.CrossRefGoogle ScholarPubMed
Szklarczyk, A., Lapinska, J., Rylski, M., McKay, R.D.G. and Kaczmarek, L. (2002) Matrix metalloproteinase-9 undergoes expression and activation during dendritic remodeling in adult hippocampus. Journal of Neuroscience 22, 920930.CrossRefGoogle ScholarPubMed
Tai, C.-Y., Kim, S.A. and Schuman, E.M. (2008) Cadherins and synaptic plasticity. Current Opinion in Cell Biology 20, 567575.CrossRefGoogle ScholarPubMed
Takahashi, E., Sagane, K., Nagasu, T. and Kuromitsu, J. (2006) Altered nociceptive response in ADAM11-deficient mice. Brain Research 1097, 3942.CrossRefGoogle ScholarPubMed
Tamura, H., Ishikawa, Y., Hino, N., Maeda, M., Yoshida, S., Kaku, S. et al. (2006) Neuropsin is essential for early processes of memory acquisition and Schaffer collateral long-term potentiation in adult mouse hippocampus in vivo. Journal of Physiology 570, 541551.CrossRefGoogle ScholarPubMed
Thinakaran, G. and Koo, E.H. (2008) Amyloid precursor protein trafficking, processing, and function. Journal of Biological Chemistry 283, 2961529619.CrossRefGoogle ScholarPubMed
Tian, L., Stefanidakis, M., Ning, L., Lint, P.V., Nyman-Huttunen, H., Libert, C. et al. (2007) Activation of NMDA receptors promotes dendritic spine development through MMP-mediated ICAM-5 cleavage. Journal of Cell Biology 178, 687700.CrossRefGoogle ScholarPubMed
Togashi, H., Abe, K., Mizoguchi, A., Takaoka, K., Chisaka, O. and Takeichi, M. (2002) Cadherin regulates dendritic spine morphogenesis. Neuron 35, 7789.CrossRefGoogle ScholarPubMed
Trommsdorff, M., Gotthardt, M., Hiesberger, T., Shelton, J., Stockinger, W., Nimpf, J. et al. (1999) Reeler/Disabled-like disruption of neuronal migration in knockout mice lacking the VLDL receptor and ApoE receptor 2. Cell 97, 689701.CrossRefGoogle ScholarPubMed
Uemura, K., Kihara, T., Kuzuya, A., Okawa, K., Nishimoto, T., Ninomiya, H. et al. (2006) Characterization of sequential N-cadherin cleavage by ADAM10 and PS1. Neuroscience Letters 402, 278283.CrossRefGoogle ScholarPubMed
Utsunomiya-Tate, N., Kubo, K., Tate, S., Kainosho, M., Katayama, E., Nakajima, K. et al. (2000) Reelin molecules assemble together to form a large protein complex, which is inhibited by the function-blocking CR-50 antibody. Proceedings of the National Academy of Sciences of the U.S.A. 97, 97299734.CrossRefGoogle Scholar
Wang, X.B., Bozdagi, O., Nikitczuk, J.S., Zhai, Z.W., Zhou, Q. and Huntley, G.W. (2008) Extracellular proteolysis by matrix metalloproteinase-9 drives dendritic spine enlargement and long-term potentiation coordinately. Proceedings of the National Academy of Sciences of the U.S.A. 105, 1952019525.CrossRefGoogle ScholarPubMed
Wang, Y., Chan, S.L., Miele, L., Yao, P.J., Mackes, J., Ingram, D.K. et al. (2004) Involvement of Notch signaling in hippocampal synaptic plasticity. Proceedings of the National Academy of Sciences of the U.S.A. 101, 94589462.CrossRefGoogle ScholarPubMed
Weeber, E.J., Beffert, U., Jones, C., Christian, J.M., Forster, E., Sweatt, J.D. et al. (2002) Reelin and ApoE receptors cooperate to enhance hippocampal synaptic plasticity and learning. Journal of Biological Chemistry 277, 3994439952.CrossRefGoogle ScholarPubMed
White, J.M. (2003) ADAMs: modulators of cell-cell and cell-matrix interactions. Current Opinion in Cell Biology 15, 598606.CrossRefGoogle ScholarPubMed
Wright, J.W., Brown, T.E. and Harding, J.W. (2007) Inhibition of hippocampal matrix metalloproteinase-3 and -9 disrupts spatial memory. Neural Plasticity 2007, 73813.CrossRefGoogle ScholarPubMed
Wright, J.W., Masino, A.J., Reichert, J.R., Turner, G.D., Meighan, S.E., Meighan, P.C. et al. (2003) Ethanol-induced impairment of spatial memory and brain matrix metalloproteinases. Brain Research 963, 252261.CrossRefGoogle ScholarPubMed
Wu, Y.P., Siao, C.J., Lu, W., Sung, T.C., Frohman, M.A., Milev, P. et al. (2000) The tissue plasminogen activator (tPA)/plasmin extracellular proteolytic system regulates seizure-induced hippocampal mossy fiber outgrowth through a proteoglycan substrate. Journal of Cell Biology 148, 12951304.CrossRefGoogle ScholarPubMed
Yepes, M., Roussel, B.D., Ali, C. and Vivien, D. (2009) Tissue-type plasminogen activator in the ischemic brain: more than a thrombolytic. Trends in Neurosciences 32, 4855.CrossRefGoogle ScholarPubMed
Yu, H., Saura, C.A., Choi, S.Y., Sun, L.D., Yang, X., Handler, M. et al. (2001) APP processing and synaptic plasticity in presenilin-1 conditional knockout mice. Neuron 31, 713726.CrossRefGoogle ScholarPubMed
Zheng, H. and Koo, E.H. (2006) The amyloid precursor protein: beyond amyloid. Molecular Neurodegeneration 1, 5.CrossRefGoogle ScholarPubMed