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Previous Article | Next Article
The Journal of Neuroscience, January 15, 2000, 20(2):542-549
Role of Tissue Plasminogen Activator Receptor LRP in Hippocampal Long-Term Potentiation
Min Zhuo1, David M. Holtzman2, 3, Yonghe Li4, Hiroshi Osaka4, Joe DeMaro2, Mark Jacquin2, and Guojun Bu4, 5 Departments of 1 Anesthesiology, 2 Neurology, 3 Molecular Biology and Pharmacology, 4 Pediatrics, and 5 Cell Biology and Physiology, Washington University School of Medicine, St. Louis, Missouri 63110
The low-density lipoprotein (LDL) receptor-related protein (LRP) is a multifunctional endocytic receptor that is expressed abundantly in neurons of the CNS. Both LRP and several of its ligands, including tissue plasminogen activator (tPA), apolipoprotein E/lipoproteins,
2-macroglobulin, and the
-amyloid precursor protein, have been implicated in various neuronal functions and in the pathogenesis of Alzheimer's disease. It has been reported that induction of tPA expression may contribute to activity-dependent synaptic plasticity in the hippocampus and cerebellum. In addition, long-term potentiation (LTP) is significantly decreased in mice lacking tPA. Here we demonstrate that tPA receptor LRP is abundantly expressed in hippocampal neurons and participates in hippocampal LTP. Perfusion of hippocampal slices with receptor-associated protein (RAP), an antagonist for ligand interactions with LRP, significantly reduced late-phase LTP (L-LTP). In addition, RAP also blocked the enhancing effect of synaptic potentiation by exogenous tPA in hippocampal slices prepared from tPA knock-out mice. Metabolic labeling and ligand binding analyses showed that both tPA and LRP are synthesized by hippocampal neurons and that LRP is the major cell surface receptor that binds tPA. Finally, we found that tPA binding to LRP in hippocampal neurons enhances the activity of cyclic AMP-dependent protein kinase, a key molecule that is known to be involved in L-LTP. Taken together, our results demonstrate that interactions between tPA and cell surface LRP are important for hippocampal L-LTP.
Key words: LRP; tPA; LTP; PKA; Alzheimer's disease; hippocampus
Copyright © 2000 Society for Neuroscience 0270-6474/00/202542-08$05.00/0
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[Abstract] [Full Text] [PDF]
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[Abstract] [Full Text] [PDF]
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