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Originally published In Press as doi:10.1074/jbc.M205147200 on August 7, 2002

J. Biol. Chem., Vol. 277, Issue 42, 39944-39952, October 18, 2002
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Reelin and ApoE Receptors Cooperate to Enhance Hippocampal Synaptic Plasticity and Learning*

Edwin J. WeeberDagger , Uwe Beffert§, Chris Jones§, Jill M. ChristianDagger , Eckart Förster||, J. David SweattDagger , and Joachim Herz§**

From the Dagger  Division of Neuroscience, Baylor College of Medicine, Houston, Texas 77030, the § Department of Molecular Genetics, University of Texas Southwestern, Dallas, Texas 75390, and the || Anatomisches Institut, University of Freiburg, D-79001 Freiburg, Germany

Two apolipoprotein E (apoE) receptors, the very low density lipoprotein (VLDL) receptor and apoE receptor 2 (apoER2), are also receptors for Reelin, a signaling protein that regulates neuronal migration during brain development. In the adult brain, Reelin is expressed by GABA-ergic interneurons, suggesting a potential function as a modulator of neurotransmission. ApoE receptors have been indirectly implicated in memory and neurodegenerative disorders because their ligand, apoE, is genetically associated with Alzheimer disease. We have used knockout mice to investigate the role of Reelin and its receptors in cognition and synaptic plasticity. Mice lacking either the VLDL receptor or the apoER2 show contextual fear conditioning deficits. VLDL receptor-deficient mice also have a moderate defect in long term potentiation (LTP), and apoER2 knockouts have a pronounced one. The perfusion of mouse hippocampal slices with Reelin has no effect on baseline synaptic transmission but significantly enhances LTP in area CA1. This Reelin-dependent augmentation of LTP is abolished in VLDL receptor and apoER2 knockout mice. Our results reveal a role for Reelin in controlling synaptic plasticity in the adult brain and suggest that both of its receptors are necessary for Reelin-dependent enhancement of synaptic transmission in the hippocampus. Thus, the impairment of apoE receptor-dependent neuromodulation may contribute to cognitive impairment and synaptic loss in Alzheimer disease.

* This work was supported by National Institutes of Health Grants MH57014, NS37444, HD24064, HL20948, HL63762, and NS43408, the Alzheimer Association, the American Heart Association, and the Perot Family Foundation.The costs of publication of this article were defrayed in part by the payment of page charges. The article must therefore be hereby marked "advertisement" in accordance with 18 U.S.C. Section 1734 solely to indicate this fact.

Fellow of the Human Frontier Science Program and the Canadian Institute of Health Research.

** Investigator of the American Heart Association and Parke-Davis and recipient of the Wolfgang-Paul Award from the Humboldt Foundation. To whom correspondence should be addressed: Dept. of Molecular Genetics, University of Texas Southwestern, 5323 Harry Hines Blvd., Dallas, TX 75390-9046. Tel.: 214-648-5633; Fax: 214-648-8804; E-mail: Joachim.Herz@UTSouthwestern.edu.

Copyright © 2002 by The American Society for Biochemistry and Molecular Biology, Inc.
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