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Reelin and apoE actions on signal transduction, synaptic function and memory formation

Published online by Cambridge University Press:  13 August 2009

Justin T. Rogers
Affiliation:
Department of Molecular Pharmacology and Physiology, Johnnie B Byrd Sr. Alzheimer's Center & Research Institute, University of South Florida, 4001 East Fletcher Ave., Tampa FL 33613, USA
Edwin J. Weeber*
Affiliation:
Department of Molecular Pharmacology and Physiology, Johnnie B Byrd Sr. Alzheimer's Center & Research Institute, University of South Florida, 4001 East Fletcher Ave., Tampa FL 33613, USA
*
Correspondence should be addressed to: Edwin J. Weeber, Department of Molecular Pharmacology and Physiology, Johnnie B Byrd Sr. Alzheimer's Center & Research Institute, University of South Florida, 4001 East Fletcher Ave., Tampa FL 33613, USA email: eweeber@health.usf.edu

Abstract

Low-density-lipoprotein receptors (LDLRs) are an evolutionarily ancient surface protein family with the ability to activate a diversity of extracellular signals across the cellular membrane in the adult central nervous system (CNS). Their intimate roles in modulating synaptic plasticity and their necessity in hippocampal-dependent learning and memory have only recently come to light. Two known LDLR ligands, specifically apolipoprotein E (apoE) and reelin, have been the most widely investigated in this regard. Most of our understanding of synaptic plasticity comes from investigation of both pre- and postsynaptic alterations. Therefore, it is interesting to note that neurons and glia that do not contribute to the synaptic junction in question can secrete signaling molecules that affect synaptic plasticity. Notably, reelin and apoE have been shown to modulate hippocampal long-term potentiation in general, and affect NMDA receptor and AMPA receptor regulation specifically. Furthermore, these receptors and signaling molecules have significant roles in neuronal degenerative diseases such as Alzheimer's disease. The recent production of recombinant proteins, knockout and transgenic mice for receptors and ligands and the development of human ApoE targeted replacement mice have significantly expanded our understanding of the roles LDLRs and their ligands have in certain disease states and the accompanying initiation of specific signaling pathways. This review describes the role LDLRs, apoE and reelin have in the regulation of hippocampal synaptic plasticity.

Type
Research Article
Copyright
Copyright © Cambridge University Press 2009

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References

REFERENCES

Abraham, W.C. and Mason, S.E. (1988) Effects of the NMDA receptor/channel antagonists CPP and MK801 on hippocampal field potentials and long-term potentiation in anesthetized rats. Brain Research 462, 4046.CrossRefGoogle ScholarPubMed
Aguilo, A., Schwartz, T.H., Kumar, V.S., Peterlin, Z.A., Tsiola, A., Soriano, E. et al. (1999) Involvement of Cajal-Retzius neurons in spontaneous correlated activity of embryonic and postnatal layer 1 from wild-type and reeler mice. Journal of Neuroscience 19, 1085610868.CrossRefGoogle ScholarPubMed
Anderson, R., Barnes, J.C., Bliss, T.V., Cain, D.P., Cambon, K., Davies, H.A. et al. (1998) Behavioural, physiological and morphological analysis of a line of apolipoprotein E knockout mouse. Neuroscience 85, 93110.CrossRefGoogle ScholarPubMed
Ang, L.S., Cruz, R.P., Hendel, A. and Granville, D.J. (2008) Apolipoprotein E, an important player in longevity and age-related diseases. Experimental Gerontology 43, 615622.CrossRefGoogle ScholarPubMed
Arnaud, L., Ballif, B.A., Forster, E. and Cooper, J.A. (2003) Fyn tyrosine kinase is a critical regulator of disabled-1 during brain development. Current Biology 13, 917.CrossRefGoogle ScholarPubMed
Bales, K.R., Verina, T., Dodel, R.C., Du, Y., Altstiel, L., Bender, M. et al. (1997) Lack of apolipoprotein E dramatically reduces amyloid beta-peptide deposition. Nature Genetics 17, 263264.CrossRefGoogle ScholarPubMed
Ballif, B.A., Arnaud, L. and Cooper, J.A. (2003) Tyrosine phosphorylation of Disabled-1 is essential for Reelin-stimulated activation of Akt and Src family kinases. Brain Research Molecular Brain Research 117, 152159.CrossRefGoogle ScholarPubMed
Banke, T.G., Bowie, D., Lee, H., Huganir, R.L., Schousboe, A. and Traynelis, S.F. (2000) Control of GluR1 AMPA receptor function by cAMP-dependent protein kinase. Journal of Neuroscience 20, 89102.CrossRefGoogle ScholarPubMed
Bar, I., Lambert De Rouvroit, C., Royaux, I., Krizman, D.B., Dernoncourt, C., Ruelle, D. et al. (1995) A YAC contig containing the reeler locus with preliminary characterization of candidate gene fragments. Genomics 26, 543549.CrossRefGoogle ScholarPubMed
Barria, A. and Malinow, R. (2005) NMDA receptor subunit composition controls synaptic plasticity by regulating binding to CaMKII. Neuron 48, 289301.CrossRefGoogle ScholarPubMed
Barria, A., Muller, D., Derkach, V., Griffith, L.C. and Soderling, T.R. (1997) Regulatory phosphorylation of AMPA-type glutamate receptors by CaM-KII during long-term potentiation. Science 276, 20422045.CrossRefGoogle ScholarPubMed
Beffert, U., Weeber, E.J., Durudas, A., Qiu, S., Masiulis, I., Sweatt, J.D. et al. (2005) Modulation of synaptic plasticity and memory by Reelin involves differential splicing of the lipoprotein receptor Apoer2. Neuron 47, 567579.CrossRefGoogle ScholarPubMed
Benhayon, D., Magdaleno, S. and Curran, T. (2003) Binding of purified Reelin to ApoER2 and VLDLR mediates tyrosine phosphorylation of Disabled-1. Brain Research Molecular Brain Research 112, 3345.CrossRefGoogle ScholarPubMed
Bock, H.H. and Herz, J. (2003) Reelin activates SRC family tyrosine kinases in neurons. Current Biology 13, 1826.CrossRefGoogle ScholarPubMed
Bock, H.H., Jossin, Y., Liu, P., Forster, E., May, P., Goffinet, A.M. et al. (2003) Phosphatidylinositol 3-kinase interacts with the adaptor protein Dab1 in response to Reelin signaling and is required for normal cortical lamination. Journal of Biological Chemistry 278, 3877238779.CrossRefGoogle ScholarPubMed
Carmignoto, G. and Vicini, S. (1992) Activity-dependent decrease in NMDA receptor responses during development of the visual cortex. Science 258, 10071011.CrossRefGoogle ScholarPubMed
Chavis, P. and Westbrook, G. (2001) Integrins mediate functional pre- and postsynaptic maturation at a hippocampal synapse. Nature 411, 317321.CrossRefGoogle Scholar
Chen, Y., Beffert, U., Ertunc, M., Tang, T.S., Kavalali, E.T., Bezprozvanny, I. et al. (2005) Reelin modulates NMDA receptor activity in cortical neurons. Journal of Neuroscience 25, 82098216.CrossRefGoogle ScholarPubMed
Chung, H.J., Huang, Y.H., Lau, L.F. and Huganir, R.L. (2004) Regulation of the NMDA receptor complex and trafficking by activity-dependent phosphorylation of the NR2B subunit PDZ ligand. Journal of Neuroscience 24, 1024810259.CrossRefGoogle ScholarPubMed
Clark, G.D., Mizuguchi, M., Antalffy, B., Barnes, J. and Armstrong, D. (1997) Predominant localization of the LIS family of gene products to Cajal-Retzius cells and ventricular neuroepithelium in the developing human cortex. Journal of Neuropathology & Experimental Neurology 56, 10441052.CrossRefGoogle ScholarPubMed
Corder, E.H., Saunders, A.M., Strittmatter, W.J., Schmechel, D.E., Gaskell, P.C., Small, G.W. et al. (1993) Gene dose of apolipoprotein E type 4 allele and the risk of Alzheimer’s disease in late onset families. Science 261, 921923.CrossRefGoogle ScholarPubMed
D'Arcangelo, G. (2005) Apoer2: a reelin receptor to remember. Neuron 47, 471473.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
Del Rio, J.A., Heimrich, B., Borrell, V., Forster, E., Drakew, A., Alcantara, S. et al. (1997) A role for Cajal-Retzius cells and reelin in the development of hippocampal connections. Nature 385, 7074.CrossRefGoogle ScholarPubMed
Depboylu, C., Lohmuller, F., Du, Y., Riemenschneider, M., Kurz, A., Gasser, T. et al. (2006) Alpha2-macroglobulin, lipoprotein receptor-related protein and lipoprotein receptor-associated protein and the genetic risk for developing Alzheimer’s disease. Neuroscience Letters 400, 187190.CrossRefGoogle ScholarPubMed
Drakew, A., Deller, T., Heimrich, B., Gebhardt, C., Del Turco, D., Tielsch, A. et al. (2002) Dentate granule cells in reeler mutants and VLDLR and ApoER2 knockout mice. Experimental Neurology 176, 1224.CrossRefGoogle ScholarPubMed
Fagan, A.M., Bu, G., Sun, Y., Daugherty, A. and Holtzman, D.M. (1996) Apolipoprotein E-containing high density lipoprotein promotes neurite outgrowth and is a ligand for the low density lipoprotein receptor-related protein. Journal of Biological Chemistry 271, 3012130125.CrossRefGoogle ScholarPubMed
Forster, E., Tielsch, A., Saum, B., Weiss, K.H., Johanssen, C., Graus-Porta, D. et al. (2002) Reelin, Disabled 1, and beta 1 integrins are required for the formation of the radial glial scaffold in the hippocampus. Proceedings of the National Academy of Sciences of the U.S.A. 99, 1317813183.CrossRefGoogle ScholarPubMed
Frotscher, M., Haas, C.A. and Forster, E. (2003) Reelin controls granule cell migration in the dentate gyrus by acting on the radial glial scaffold. Cerebral Cortex 13, 634640.CrossRefGoogle ScholarPubMed
Fryer, J.D., Taylor, J.W., DeMattos, R.B., Bales, K.R., Paul, S.M., Parsadanian, M. et al. (2003) Apolipoprotein E markedly facilitates age-dependent cerebral amyloid angiopathy and spontaneous hemorrhage in amyloid precursor protein transgenic mice. Journal of Neuroscience 23, 78897896.CrossRefGoogle ScholarPubMed
Games, D., Adams, D., Alessandrini, R., Barbour, R., Berthelette, P., Blackwell, C. et al. (1995) Alzheimer-type neuropathology in transgenic mice overexpressing V717F beta-amyloid precursor protein. Nature 373, 523527.CrossRefGoogle ScholarPubMed
Gouni-Berthold, I., Seewald, S., Hescheler, J. and Sachinidis, A. (2004) Regulation of mitogen-activated protein kinase cascades by low density lipoprotein and lysophosphatidic acid. Cellular Physiology and Biochemistry 14, 167176.CrossRefGoogle ScholarPubMed
Grosshans, D.R., Clayton, D.A., Coultrap, S.J. and Browning, M.D. (2002) LTP leads to rapid surface expression of NMDA but not AMPA receptors in adult rat CA1. Nature Neuroscience 5, 2733.CrossRefGoogle Scholar
Grover, L.M. and Teyler, T.J. (1990) Two components of long-term potentiation induced by different patterns of afferent activation. Nature 347, 477479.CrossRefGoogle ScholarPubMed
Gu, Y., McIlwain, K.L., Weeber, E.J., Yamagata, T., Xu, B., Antalffy, B.A. et al. (2002) Impaired conditioned fear and enhanced long-term potentiation in Fmr2 knock-out mice. Journal of Neuroscience 22, 27532763.CrossRefGoogle ScholarPubMed
Guo, H., Liu, D., Gelbard, H., Cheng, T., Insalaco, R., Fernandez, J.A. et al. (2004a) Activated protein C prevents neuronal apoptosis via protease activated receptors 1 and 3. Neuron 41, 563572.CrossRefGoogle Scholar
Guo, L., LaDu, M.J. and Van Eldik, L.J. (2004b) A dual role for apolipoprotein e in neuroinflammation: anti- and pro-inflammatory activity. Journal of Molecular Neuroscience 23, 205212.CrossRefGoogle ScholarPubMed
Haass, C. and Steiner, H. (2001) Protofibrils, the unifying toxic molecule of neurodegenerative disorders? Nature Neuroscience 4, 859860.CrossRefGoogle ScholarPubMed
Harris, E.W. and Cotman, C.W. (1986) Long-term potentiation of guinea pig mossy fiber responses is not blocked by N-methyl D-aspartate antagonists. Neuroscience Letters 70, 132137.CrossRefGoogle Scholar
Harris, E.W., Ganong, A.H. and Cotman, C.W. (1984) Long-term potentiation in the hippocampus involves activation of N-methyl-D-aspartate receptors. Brain Research 323, 132137.CrossRefGoogle ScholarPubMed
Hayashi, T. and Huganir, R.L. (2004) Tyrosine phosphorylation and regulation of the AMPA receptor by SRC family tyrosine kinases. Journal of Neuroscience 24, 61526160.CrossRefGoogle ScholarPubMed
Hayashi, Y., Shi, S.H., Esteban, J.A., Piccini, A., Poncer, J.C. and Malinow, R. (2000) Driving AMPA receptors into synapses by LTP and CaMKII: requirement for GluR1 and PDZ domain interaction. Science 287, 22622267.CrossRefGoogle ScholarPubMed
Herz, J. (2001) The LDL receptor gene family: (un)expected signal transducers in the brain. Neuron 29, 571581.CrossRefGoogle ScholarPubMed
Hiesberger, T., Trommsdorff, M., Howell, B.W., Goffinet, A., Mumby, M.C., Cooper, J.A. et al. (1999) Direct binding of Reelin to VLDL receptor and ApoE receptor 2 induces tyrosine phosphorylation of disabled-1 and modulates tau phosphorylation. Neuron 24, 481489.CrossRefGoogle ScholarPubMed
Hoe, H.S., Harris, D.C. and Rebeck, G.W. (2005) Multiple pathways of apolipoprotein E signaling in primary neurons. Journal of Neurochemistry 93, 145155.CrossRefGoogle ScholarPubMed
Hoe, H.S., Pocivavsek, A., Dai, H., Chakraborty, G., Harris, D.C. and Rebeck, G.W. (2006) Effects of apoE on neuronal signaling and APP processing in rodent brain. Brain Research 1112, 7079.CrossRefGoogle ScholarPubMed
Holtzman, D.M., Bales, K.R., Wu, S., Bhat, P., Parsadanian, M., Fagan, A.M. et al. (1999) Expression of human apolipoprotein E reduces amyloid-beta deposition in a mouse model of Alzheimer's disease. Journal of Clinical Investigation 103, R15R21.CrossRefGoogle Scholar
Howell, B.W., Hawkes, R., Soriano, P. and Cooper, J.A. (1997) Neuronal position in the developing brain is regulated by mouse disabled-1. Nature 389, 733737.CrossRefGoogle ScholarPubMed
Isaac, J.T., Nicoll, R.A. and Malenka, R.C. (1995) Evidence for silent synapses: implications for the expression of LTP. Neuron 15, 427434.CrossRefGoogle ScholarPubMed
Ji, Y., Gong, Y., Gan, W., Beach, T., Holtzman, D.M. and Wisniewski, T. (2003) Apolipoprotein E isoform-specific regulation of dendritic spine morphology in apolipoprotein E transgenic mice and Alzheimer's disease patients. Neuroscience 122, 305315.CrossRefGoogle ScholarPubMed
Jordan, J., Galindo, M.F., Miller, R.J., Reardon, C.A., Getz, G.S. and LaDu, M.J. (1998) Isoform-specific effect of apolipoprotein E on cell survival and beta-amyloid-induced toxicity in rat hippocampal pyramidal neuronal cultures. Journal of Neuroscience 18, 195204.CrossRefGoogle ScholarPubMed
Kerchner, G.A. and Nicoll, R.A. (2008) Silent synapses and the emergence of a postsynaptic mechanism for LTP. Nature Reviews Neuroscience 9, 813825.CrossRefGoogle ScholarPubMed
Kitamura, H.W., Hamanaka, H., Watanabe, M., Wada, K., Yamazaki, C., Fujita, S.C. et al. (2004) Age-dependent enhancement of hippocampal long-term potentiation in knock-in mice expressing human apolipoprotein E4 instead of mouse apolipoprotein E. Neuroscience Letters 369, 173178.CrossRefGoogle ScholarPubMed
Klein, W.L., Krafft, G.A. and Finch, C.E. (2001) Targeting small Abeta oligomers: the solution to an Alzheimer's disease conundrum? Trends in Neurosciences 24, 219224.CrossRefGoogle Scholar
Ko, J., Humbert, S., Bronson, R.T., Takahashi, S., Kulkarni, A.B., Li, E. et al. (2001) p35 and p39 are essential for cyclin-dependent kinase 5 function during neurodevelopment. Journal of Neuroscience 21, 67586771.CrossRefGoogle ScholarPubMed
Koch, S., Strasser, V., Hauser, C., Fasching, D., Brandes, C., Bajari, T.M. et al. (2002) A secreted soluble form of ApoE receptor 2 acts as a dominant-negative receptor and inhibits Reelin signaling. EMBO Journal 21, 59966004.CrossRefGoogle ScholarPubMed
Koistinaho, M., Lin, S., Wu, X., Esterman, M., Koger, D., Hanson, J. et al. (2004) Apolipoprotein E promotes astrocyte colocalization and degradation of deposited amyloid-beta peptides. Nature Medicine 10, 719726.CrossRefGoogle ScholarPubMed
Kopan, R. and Ilagan, M.X. (2004) Gamma-secretase: proteasome of the membrane? Nature Reviews Molecular Cell Biology 5, 499504.CrossRefGoogle ScholarPubMed
Korwek, K., Trotter, J., LaDu, M., Sullivan, P. and Weeber, E.J. (2009) ApoE isoform-dependent changes in hippocampal synaptic function. Molecular Neurodegeneration 4, 21.CrossRefGoogle ScholarPubMed
Kuo, Y.M., Emmerling, M.R., Vigo-Pelfrey, C., Kasunic, T.C., Kirkpatrick, J.B., Murdoch, G.H. et al. (1996) Water-soluble Abeta (N-40, N-42) oligomers in normal and Alzheimer disease brains. Journal of Biological Chemistry 271, 40774081.CrossRefGoogle ScholarPubMed
LaDu, M.J., Falduto, M.T., Manelli, A.M., Reardon, C.A., Getz, G.S. and Frail, D.E. (1994) Isoform-specific binding of apolipoprotein E to beta-amyloid. Journal of Biological Chemistry 269, 2340323406.CrossRefGoogle ScholarPubMed
LaDu, M.J., Pederson, T.M., Frail, D.E., Reardon, C.A., Getz, G.S. and Falduto, M.T. (1995) Purification of apolipoprotein E attenuates isoform-specific binding to beta-amyloid. Journal of Biological Chemistry 270, 90399042.CrossRefGoogle ScholarPubMed
LaDu, M.J., Reardon, C., Van Eldik, L., Fagan, A.M., Bu, G., Holtzman, D. et al. (2000a) Lipoproteins in the central nervous system. Annals of the New York Academy of Sciences 903, 167175.CrossRefGoogle ScholarPubMed
LaDu, M.J., Shah, J.A., Reardon, C.A., Getz, G.S., Bu, G., Hu, J. et al. (2000b) Apolipoprotein E receptors mediate the effects of beta-amyloid on astrocyte cultures. Journal of Biological Chemistry 275, 3397433980.CrossRefGoogle ScholarPubMed
Lahiri, D.K., Sambamurti, K. and Bennett, D.A. (2004) Apolipoprotein gene and its interaction with the environmentally driven risk factors: molecular, genetic and epidemiological studies of Alzheimer's disease. Neurobiology of Aging 25, 651660.CrossRefGoogle ScholarPubMed
Lansbury, P.T. Jr. (1999) Evolution of amyloid: what normal protein folding may tell us about fibrillogenesis and disease. Proceedings of the National Academy of Sciences of the U.S.A. 96, 33423344.CrossRefGoogle ScholarPubMed
Laskowitz, D.T., Thekdi, A.D., Thekdi, S.D., Han, S.K., Myers, J.K., Pizzo, S.V. et al. (2001) Downregulation of microglial activation by apolipoprotein E and apoE-mimetic peptides. Experimental Neurology 167, 7485.CrossRefGoogle ScholarPubMed
Lau, L.F. and Huganir, R.L. (1995) Differential tyrosine phosphorylation of N-methyl-D-aspartate receptor subunits. Journal of Biological Chemistry 270, 2003620041.CrossRefGoogle ScholarPubMed
Lee, H.K., Takamiya, K., Han, J.S., Man, H., Kim, C.H., Rumbaugh, G. et al. (2003) Phosphorylation of the AMPA receptor GluR1 subunit is required for synaptic plasticity and retention of spatial memory. Cell 112, 631643.CrossRefGoogle ScholarPubMed
Liao, D., Hessler, N.A. and Malinow, R. (1995) Activation of postsynaptically silent synapses during pairing-induced LTP in CA1 region of hippocampal slice. Nature 375, 400404.CrossRefGoogle ScholarPubMed
Liu, W.S., Pesold, C., Rodriguez, M.A., Carboni, G., Auta, J., Lacor, P. et al. (2001) Down-regulation of dendritic spine and glutamic acid decarboxylase 67 expressions in the reelin haploinsufficient heterozygous reeler mouse. Proceedings of the National Academy of Sciences of the U.S.A. 98, 34773482.CrossRefGoogle ScholarPubMed
Lu, W., Man, H., Ju, W., Trimble, W.S., MacDonald, J.F. and Wang, Y.T. (2001) Activation of synaptic NMDA receptors induces membrane insertion of new AMPA receptors and LTP in cultured hippocampal neurons. Neuron 29, 243254.CrossRefGoogle ScholarPubMed
Lu, Y.M., Roder, J.C., Davidow, J. and Salter, M.W. (1998) Src activation in the induction of long-term potentiation in CA1 hippocampal neurons. Science 279, 13631367.CrossRefGoogle ScholarPubMed
Lynch, J.R., Tang, W., Wang, H., Vitek, M.P., Bennett, E.R., Sullivan, P.M. et al. (2003) APOE genotype and an ApoE-mimetic peptide modify the systemic and central nervous system inflammatory response. Journal of Biological Chemistry 278, 4852948533.CrossRefGoogle Scholar
Ma, J., Brewer, H.B. Jr. and Potter, H. (1996) Alzheimer A beta neurotoxicity: promotion by antichymotrypsin, ApoE4; inhibition by A beta-related peptides. Neurobiology of Aging 17, 773780.CrossRefGoogle Scholar
Ma, J., Yee, A., Brewer, H.B. Jr., Das, S. and Potter, H. (1994) Amyloid-associated proteins alpha 1-antichymotrypsin and apolipoprotein E promote assembly of Alzheimer beta-protein into filaments. Nature 372, 9294.CrossRefGoogle ScholarPubMed
Mahley, R.W. (1988) Apolipoprotein E: cholesterol transport protein with expanding role in cell biology. Science 240, 622630.CrossRefGoogle ScholarPubMed
Manelli, A.M., Bulfinch, L.C., Sullivan, P.M. and LaDu, M.J. (2007) Abeta42 neurotoxicity in primary co-cultures: effect of apoE isoform and Abeta conformation. Neurobiology of Aging 28, 11391147.CrossRefGoogle ScholarPubMed
Marx, J.L. (1985) A potpourri of membrane receptors. Science 230, 649651.CrossRefGoogle ScholarPubMed
Masliah, E., Mallory, M., Ge, N., Alford, M., Veinbergs, I. and Roses, A.D. (1995) Neurodegeneration in the central nervous system of apoE-deficient mice. Experimental Neurology 136, 107122.CrossRefGoogle ScholarPubMed
Massey, P.V., Johnson, B.E., Moult, P.R., Auberson, Y.P., Brown, M.W., Molnar, E. et al. (2004) Differential roles of NR2A and NR2B-containing NMDA receptors in cortical long-term potentiation and long-term depression. Journal of Neuroscience 24, 78217828.CrossRefGoogle ScholarPubMed
Mauch, D.H., Nagler, K., Schumacher, S., Goritz, C., Muller, E.C., Otto, A. et al. (2001) CNS synaptogenesis promoted by glia-derived cholesterol. Science 294, 13541357.CrossRefGoogle ScholarPubMed
May, P., Herz, J. and Bock, H.H. (2005) Molecular mechanisms of lipoprotein receptor signalling. Cellular and Molecular Life Sciences 62, 23252338.CrossRefGoogle ScholarPubMed
Migaud, M., Charlesworth, P., Dempster, M., Webster, L.C., Watabe, A.M., Makhinson, M. et al. (1998) Enhanced long-term potentiation and impaired learning in mice with mutant postsynaptic density-95 protein. Nature 396, 433439.CrossRefGoogle ScholarPubMed
Miyata, M. and Smith, J.D. (1996) Apolipoprotein E allele-specific antioxidant activity and effects on cytotoxicity by oxidative insults and beta-amyloid peptides. Nature Genetics 14, 5561.CrossRefGoogle ScholarPubMed
Mizuguchi, M., Takashima, S., Kakita, A., Yamada, M. and Ikeda, K. (1995) Lissencephaly gene product. Localization in the central nervous system and loss of immunoreactivity in Miller-Dieker syndrome. American Journal of Pathology 147, 11421151.Google ScholarPubMed
Monyer, H., Burnashev, N., Laurie, D.J., Sakmann, B. and Seeburg, P.H. (1994) Developmental and regional expression in the rat brain and functional properties of four NMDA receptors. Neuron 12, 529540.CrossRefGoogle ScholarPubMed
Morris, R.G., Anderson, E., Lynch, G.S. and Baudry, M. (1986a) Selective impairment of learning and blockade of long-term potentiation by an N-methyl-D-aspartate receptor antagonist, AP5. Nature 319, 774776.CrossRefGoogle ScholarPubMed
Morris, R.G., Hagan, J.J. and Rawlins, J.N. (1986b) Allocentric spatial learning by hippocampectomised rats: a further test of the “spatial mapping” and “working memory” theories of hippocampal function. Quarterly Journal of Experimental Psychology B 38, 365395.Google ScholarPubMed
Nakashima, Y., Plump, A.S., Raines, E.W., Breslow, J.L. and Ross, R. (1994) ApoE-deficient mice develop lesions of all phases of atherosclerosis throughout the arterial tree. Arteriosclerosis and Thrombosis 14, 133140.CrossRefGoogle ScholarPubMed
Namba, Y., Tomonaga, M., Kawasaki, H., Otomo, E. and Ikeda, K. (1991) Apolipoprotein E immunoreactivity in cerebral amyloid deposits and neurofibrillary tangles in Alzheimer's disease and kuru plaque amyloid in Creutzfeldt-Jakob disease. Brain Research 541, 163166.CrossRefGoogle ScholarPubMed
Nimpf, J. and Schneider, W.J. (2000) From cholesterol transport to signal transduction: low density lipoprotein receptor, very low density lipoprotein receptor, and apolipoprotein E receptor-2. Biochimica et Biophysica Acta 1529, 287298.CrossRefGoogle ScholarPubMed
Niu, S., Renfro, A., Quattrocchi, C.C., Sheldon, M. and D'Arcangelo, G. (2004) Reelin promotes hippocampal dendrite development through the VLDLR/ApoER2-Dab1 pathway. Neuron 41, 7184.CrossRefGoogle ScholarPubMed
Norris, C.M., Halpain, S. and Foster, T.C. (1998) Reversal of age-related alterations in synaptic plasticity by blockade of L-type Ca2+ channels. Journal of Neuroscience 18, 31713179.CrossRefGoogle ScholarPubMed
Norris, C.M., Korol, D.L. and Foster, T.C. (1996) Increased susceptibility to induction of long-term depression and long-term potentiation reversal during aging. Journal of Neuroscience 16, 53825392.CrossRefGoogle ScholarPubMed
Nykjaer, A., Dragun, D., Walther, D., Vorum, H., Jacobsen, C., Herz, J. et al. (1999) An endocytic pathway essential for renal uptake and activation of the steroid 25-(OH) vitamin D3. Cell 96, 507515.CrossRefGoogle Scholar
Ogawa, M., Miyata, T., Nakajima, K., Yagyu, K., Seike, M., Ikenaka, K. et al. (1995) The reeler gene-associated antigen on Cajal-Retzius neurons is a crucial molecule for laminar organization of cortical neurons. Neuron 14, 899912.CrossRefGoogle ScholarPubMed
Ohshima, T., Ward, J.M., Huh, C.G., Longenecker, G., Veeranna Pant, H.C., Brady, R.O. et al. (1996) Targeted disruption of the cyclin-dependent kinase 5 gene results in abnormal corticogenesis, neuronal pathology and perinatal death. Proceedings of the National Academy of Sciences of the U.S.A. 93, 1117311178.CrossRefGoogle ScholarPubMed
Panza, F., D'Introno, A., Colacicco, A.M., Capurso, C., Basile, A.M., Capurso, S. et al. (2004) Regional European differences in allele and genotype frequencies of low density lipoprotein receptor-related protein 1 polymorphism in Alzheimer's disease. American Journal of Medical Genetics Part B Neuropsychiatric Genetics 126B, 6973.CrossRefGoogle ScholarPubMed
Pesold, C., Impagnatiello, F., Pisu, M.G., Uzunov, D.P., Costa, E., Guidotti, A. et al. (1998) Reelin is preferentially expressed in neurons synthesizing gamma-aminobutyric acid in cortex and hippocampus of adult rats. Proceedings of the National Academy of Sciences of the U.S.A. 95, 32213226.CrossRefGoogle ScholarPubMed
Pickard, L., Noel, J., Duckworth, J.K., Fitzjohn, S.M., Henley, J.M., Collingridge, G.L. et al. (2001) Transient synaptic activation of NMDA receptors leads to the insertion of native AMPA receptors at hippocampal neuronal plasma membranes. Neuropharmacology 41, 700713.CrossRefGoogle Scholar
Pillot, T., Goethals, M., Najib, J., Labeur, C., Lins, L., Chambaz, J. et al. (1999) Beta-amyloid peptide interacts specifically with the carboxy-terminal domain of human apolipoprotein E: relevance to Alzheimer's disease. Journal of Neurochemistry 72, 230237.CrossRefGoogle ScholarPubMed
Qiu, S., Korwek, K.M., Pratt-Davis, A.R., Peters, M., Bergman, M.Y. and Weeber, E.J. (2006a) Cognitive disruption and altered hippocampus synaptic function in Reelin haploinsufficient mice. Neurobiology of Learning and Memory 85, 228242.CrossRefGoogle ScholarPubMed
Qiu, S., Korwek, K.M. and Weeber, E.J. (2006b) A fresh look at an ancient receptor family: emerging roles for low density lipoprotein receptors in synaptic plasticity and memory formation. Neurobiology of Learning and Memory 85, 1629.CrossRefGoogle Scholar
Qiu, S., Zhao, L.F., Korwek, K.M. and Weeber, E.J. (2006c) Differential reelin-induced enhancement of NMDA and AMPA receptor activity in the adult hippocampus. Journal of Neuroscience 26, 1294312955.CrossRefGoogle ScholarPubMed
Qiu, Z., Hyman, B.T. and Rebeck, G.W. (2004) Apolipoprotein E receptors mediate neurite outgrowth through activation of p44/42 mitogen-activated protein kinase in primary neurons. Journal of Biological Chemistry 279, 3494834956.CrossRefGoogle ScholarPubMed
Quattrocchi, C.C., Wannenes, F., Persico, A.M., Ciafre, S.A., D'Arcangelo, G., Farace, M.G. et al. (2002) Reelin is a serine protease of the extracellular matrix. Journal of Biological Chemistry 277, 303309.CrossRefGoogle ScholarPubMed
Quinlan, E.M., Lebel, D., Brosh, I. and Barkai, E. (2004) A molecular mechanism for stabilization of learning-induced synaptic modifications. Neuron 41, 185192.CrossRefGoogle ScholarPubMed
Racine, R.J., Milgram, N.W. and Hafner, S. (1983) Long-term potentiation phenomena in the rat limbic forebrain. Brain Research 260, 217231.CrossRefGoogle ScholarPubMed
Rebeck, G.W., LaDu, M.J., Estus, S., Bu, G. and Weeber, E.J. (2006) The generation and function of soluble apoE receptors in the CNS. Molecular Neurodegeneration 1, 15.CrossRefGoogle ScholarPubMed
Rebeck, G.W., Reiter, J.S., Strickland, D.K. and Hyman, B.T. (1993) Apolipoprotein E in sporadic Alzheimer's disease: allelic variation and receptor interactions. Neuron 11, 575580.CrossRefGoogle ScholarPubMed
Salter, M.W. and Kalia, L.V. (2004) Src kinases: a hub for NMDA receptor regulation. Nature Reviews Neuroscience 5, 317328.CrossRefGoogle ScholarPubMed
Sanan, D.A., Weisgraber, K.H., Russell, S.J., Mahley, R.W., Huang, D., Saunders, A. et al. (1994) Apolipoprotein E associates with beta amyloid peptide of Alzheimer's disease to form novel monofibrils. Isoform apoE4 associates more efficiently than apoE3. Journal of Clinical Investigation 94, 860869.CrossRefGoogle ScholarPubMed
Schmechel, D.E., Saunders, A.M., Strittmatter, W.J., Crain, B.J., Hulette, C.M., Joo, S.H. et al. (1993) Increased amyloid beta-peptide deposition in cerebral cortex as a consequence of apolipoprotein E genotype in late-onset al.zheimer disease. Proceedings of the National Academy of Sciences of the U.S.A. 90, 96499653.CrossRefGoogle Scholar
Schonbaum, C.P., Lee, S. and Mahowald, A.P. (1995) The Drosophila yolkless gene encodes a vitellogenin receptor belonging to the low density lipoprotein receptor superfamily. Proceedings of the National Academy of Sciences of the U.S.A. 92, 14851489.CrossRefGoogle Scholar
Selkoe, D.J. (1997) Alzheimer's disease: genotypes, phenotypes, and treatments. Science 275, 630631.CrossRefGoogle ScholarPubMed
Senokuchi, T., Matsumura, T., Sakai, M., Matsuo, T., Yano, M., Kiritoshi, S. et al. (2004) Extracellular signal-regulated kinase and p38 mitogen-activated protein kinase mediate macrophage proliferation induced by oxidized low-density lipoprotein. Atherosclerosis 176, 233245.CrossRefGoogle ScholarPubMed
Sheng, M., Cummings, J., Roldan, L.A., Jan, Y.N. and Jan, L.Y. (1994) Changing subunit composition of heteromeric NMDA receptors during development of rat cortex. Nature 368, 144147.CrossRefGoogle ScholarPubMed
Shi, S.H., Hayashi, Y., Petralia, R.S., Zaman, S.H., Wenthold, R.J., Svoboda, K. et al. (1999) Rapid spine delivery and redistribution of AMPA receptors after synaptic NMDA receptor activation. Science 284, 18111816.CrossRefGoogle ScholarPubMed
Siest, G., Henny, J., Galteau, M.M., Schiele, F., Steinmetz, J. and Visvikis, S. (1995) Lipid and lipoprotein genetic variability: an important contribution from the French health examination centers. Clinical Biochemistry 28, 3138.CrossRefGoogle ScholarPubMed
Sinagra, M., Verrier, D., Frankova, D., Korwek, K.M., Blahos, J., Weeber, E.J. et al. (2005) Reelin, very-low-density lipoprotein receptor, and apolipoprotein E receptor 2 control somatic NMDA receptor composition during hippocampal maturation in vitro. Journal of Neuroscience 25, 61276136.CrossRefGoogle ScholarPubMed
Small, D.H. (1998) The Sixth International Conference on Alzheimer's disease, Amsterdam, The Netherlands, July 1998. The amyloid cascade hypothesis debate: emerging consensus on the role of A beta and amyloid in Alzheimer's disease. Amyloid 5, 301304.CrossRefGoogle ScholarPubMed
Soda, T., Nakashima, R., Watanabe, D., Nakajima, K., Pastan, I. and Nakanishi, S. (2003) Segregation and coactivation of developing neocortical layer 1 neurons. Journal of Neuroscience 23, 62726279.CrossRefGoogle ScholarPubMed
Staubli, U. and Lynch, G. (1987) Stable hippocampal long-term potentiation elicited by ‘theta' pattern stimulation. Brain Research 435, 227234.CrossRefGoogle ScholarPubMed
Strasser, V., Fasching, D., Hauser, C., Mayer, H., Bock, H.H., Hiesberger, T. et al. (2004) Receptor clustering is involved in Reelin signaling. Molecular and Cellular Biology 24, 13781386.CrossRefGoogle ScholarPubMed
Strittmatter, W.J., Weisgraber, K.H., Huang, D.Y., Dong, L.M., Salvesen, G.S., Pericak-Vance, M. et al. (1993) Binding of human apolipoprotein E to synthetic amyloid beta peptide: isoform-specific effects and implications for late-onset Alzheimer disease. Proceedings of the National Academy of Sciences of the U.S.A. 90, 80988102.CrossRefGoogle ScholarPubMed
Sullivan, P.M., Mezdour, H., Aratani, Y., Knouff, C., Najib, J., Reddick, R.L. et al. (1997) Targeted replacement of the mouse apolipoprotein E gene with the common human APOE3 allele enhances diet-induced hypercholesterolemia and atherosclerosis. Journal of Biological Chemistry 272, 1797217980.CrossRefGoogle ScholarPubMed
Tanzi, R.E. and Bertram, L. (2005) Twenty years of the Alzheimer's disease amyloid hypothesis: a genetic perspective. Cell 120, 545555.CrossRefGoogle ScholarPubMed
Terry, R.D. (2001) An honorable compromise regarding amyloid in Alzheimer disease. Annals of Neurology 49, 684.CrossRefGoogle ScholarPubMed
Teyler, T.J. (1987) Long-term potentiation and memory. International Journal of Neurology 21–22, 163171.Google Scholar
Teyler, T.J. and DiScenna, P. (1987) Long-term potentiation. Annual Review of Neuroscience 10, 131161.CrossRefGoogle ScholarPubMed
Teyler, T.J. and Fountain, S.B. (1987) Neuronal plasticity in the mammalian brain: relevance to behavioral learning and memory. Child Development 58, 698712.CrossRefGoogle ScholarPubMed
Tokuda, T., Calero, M., Matsubara, E., Vidal, R., Kumar, A., Permanne, B. et al. (2000) Lipidation of apolipoprotein E influences its isoform-specific interaction with Alzheimer's amyloid beta peptides. Biochemical Journal 348, 359365.CrossRefGoogle ScholarPubMed
Trommer, B.L., Shah, C., Yun, S.H., Gamkrelidze, G., Pasternak, E.S., Stine, W.B. et al. (2005) ApoE isoform-specific effects on LTP: blockade by oligomeric amyloid-beta1–42. Neurobiology of Disease 18, 7582.CrossRefGoogle ScholarPubMed
Trommer, B.L., Shah, C., Yun, S.H., Gamkrelidze, G., Pasternak, E.S., Ye, G.L. et al. (2004) ApoE isoform affects LTP in human targeted replacement mice. Neuroreport 15, 26552658.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
Wahrle, S.E. and Holtzman, D.M. (2003) Differential metabolism of ApoE isoforms in plasma and CSF. Experimental Neurology 183, 46.CrossRefGoogle ScholarPubMed
Wang, Y.T. and Salter, M.W. (1994) Regulation of NMDA receptors by tyrosine kinases and phosphatases. Nature 369, 233235.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
Westerlund, J.A. and Weisgraber, K.H. (1993) Discrete carboxyl-terminal segments of apolipoprotein E mediate lipoprotein association and protein oligomerization. Journal of Biological Chemistry 268, 1574515750.CrossRefGoogle ScholarPubMed
Whitson, J.S., Mims, M.P., Strittmatter, W.J., Yamaki, T., Morrisett, J.D. and Appel, S.H. (1994) Attenuation of the neurotoxic effect of A beta amyloid peptide by apolipoprotein E. Biochemical and Biophysical Research Communications 199, 163170.CrossRefGoogle ScholarPubMed
Willnow, T.E., Nykjaer, A. and Herz, J. (1999) Lipoprotein receptors: new roles for ancient proteins. Nature Cell Biology 1, E157E162.CrossRefGoogle ScholarPubMed
Wisniewski, T., Castano, E.M., Golabek, A., Vogel, T. and Frangione, B. (1994) Acceleration of Alzheimer's fibril formation by apolipoprotein E in vitro. American Journal of Pathology 145, 10301035.Google ScholarPubMed
Wisniewski, T., Golabek, A., Matsubara, E., Ghiso, J. and Frangione, B. (1993) Apolipoprotein E: binding to soluble Alzheimer's beta-amyloid. Biochemical and Biophysical Research Communications 192, 359365.CrossRefGoogle ScholarPubMed
Xu, Q., Bernardo, A., Walker, D., Kanegawa, T., Mahley, R.W. and Huang, Y. (2006) Profile and regulation of apolipoprotein E (ApoE) expression in the CNS in mice with targeting of green fluorescent protein gene to the ApoE locus. Journal of Neuroscience 26, 49854994.CrossRefGoogle Scholar
Yochem, J. and Greenwald, I. (1993) A gene for a low density lipoprotein receptor-related protein in the nematode Caenorhabditis elegans. Proceedings of the National Academy of Sciences of the U.S.A. 90, 45724576.CrossRefGoogle ScholarPubMed
Yu, X.M., Askalan, R., Keil, G.J. 2nd and Salter, M.W. (1997) NMDA channel regulation by channel-associated protein tyrosine kinase Src. Science 275, 674678.CrossRefGoogle ScholarPubMed
Zhao, S., Chai, X., Forster, E. and Frotscher, M. (2004) Reelin is a positional signal for the lamination of dentate granule cells. Development 131, 51175125.CrossRefGoogle ScholarPubMed