Hostname: page-component-cd9895bd7-gxg78 Total loading time: 0 Render date: 2024-12-23T04:25:31.917Z Has data issue: false hasContentIssue false

Bidirectional signaling of ErbB and Eph receptors at synapses

Published online by Cambridge University Press:  29 September 2009

Yu Chen
Affiliation:
Department of Biochemistry, Molecular Neuroscience Center and Biotechnology Research Institute, Hong Kong University of Science and Technology, Clear Water Bay, Hong Kong, China
Amy K.Y. Fu
Affiliation:
Department of Biochemistry, Molecular Neuroscience Center and Biotechnology Research Institute, Hong Kong University of Science and Technology, Clear Water Bay, Hong Kong, China
Nancy Y. Ip*
Affiliation:
Department of Biochemistry, Molecular Neuroscience Center and Biotechnology Research Institute, Hong Kong University of Science and Technology, Clear Water Bay, Hong Kong, China
*
Correspondence should be addressed to: Nancy Y. IP, Department of Biochemistry, Hong Kong University of Science and Technology, Clear Water Bay, Hong Kong, China phone: 852-2358-7289 fax: 852-2358-2765 email: [email protected]

Abstract

Synapse development and remodeling are regulated by a plethora of molecules such as receptor tyrosine kinases (RTKs), a family of cell surface receptors that play critical roles in neural development. Two families of RTKs implicated in synaptic functions, ErbBs and Ephs, share similar characteristics in terms of exhibiting forward and reverse signaling. In this review, we will discuss the latest advances in the functions of ErbBs and Ephs at the synapse, including dendritic spine morphogenesis, synapse formation and maturation, and synaptic transmission and plasticity. In addition to signaling at interneuronal synapses, communication between neuron and glia is increasingly implicated in the control of synaptic functions. Studies on RTKs and their cognate ligands in glial cells enhance our understanding on the nature of ‘tripartite synapse’. Implications of these signaling events in human diseases will be discussed.

Type
Research Article
Copyright
Copyright © Cambridge University Press 2009

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

REFERENCES

Adlkofer, K. and Lai, C. (2000) Role of neuregulins in glial cell development. GLIA 29, 104111.3.0.CO;2-2>CrossRefGoogle ScholarPubMed
Alford, S.C., Bazowski, J., Lorimer, H., Elowe, S. and Howard, P.L. (2007) Tissue transglutaminase clusters soluble A-type ephrins into functionally active high molecular weight oligomers. Experimental Cell Research 313, 41704179.CrossRefGoogle ScholarPubMed
Anton, E.S., Marchionni, M.A., Lee, K.F. and Rakic, P. (1997) Role of GGF/neuregulin signaling in interactions between migrating neurons and radial glia in the developing cerebral cortex. Development 124, 35013510.CrossRefGoogle ScholarPubMed
Armstrong, J.N., Saganich, M.J., Xu, N.J., Henkemeyer, M., Heinemann, S.F. and Contractor, A. (2006) B-ephrin reverse signaling is required for NMDA-independent long-term potentiation of mossy fibers in the hippocampus. Journal of Neuroscience 26, 34743481.CrossRefGoogle ScholarPubMed
Bamburg, J.R. (1999) Proteins of the ADF/cofilin family: essential regulators of actin dynamics. Annual Review of Cell & Developmental Biology 15, 185230.CrossRefGoogle ScholarPubMed
Bao, J., Lin, H., Ouyang, Y., Lei, D., Osman, A., Kim, T.W. et al. (2004) Activity-dependent transcription regulation of PSD-95 by neuregulin-1 and Eos. Nature Neuroscience 7, 12501258.CrossRefGoogle ScholarPubMed
Bao, J., Wolpowitz, D., Role, L.W. and Talmage, D.A. (2003) Back signaling by the Nrg-1 intracellular domain. Journal of Cell Biology 161, 11331141.CrossRefGoogle ScholarPubMed
Barros, C.S., Calabrese, B., Chamero, P., Roberts, A.J., Korzus, E., Lloyd, K. et al. (2009) Impaired maturation of dendritic spines without disorganization of cortical cell layers in mice lacking NRG1/ErbB signaling in the central nervous system. Proceedings of the National Academy of Sciences of the U.S.A. 106, 45074512.CrossRefGoogle ScholarPubMed
Beattie, E.C., Stellwagen, D., Morishita, W., Bresnahan, J.C., Ha, B.K., Von Zastrow, M. et al. (2002) Control of synaptic strength by glial TNFalpha. Science 295, 22822285.CrossRefGoogle ScholarPubMed
Beg, A.A., Sommer, J.E., Martin, J.H. and Scheiffele, P. (2007) alpha2-Chimaerin is an essential EphA4 effector in the assembly of neuronal locomotor circuits. Neuron 55, 768778.CrossRefGoogle ScholarPubMed
Bjarnadottir, M., Misner, D.L., Haverfield-Gross, S., Bruun, S., Helgason, V.G., Stefansson, H. et al. (2007) Neuregulin1 (NRG1) signaling through Fyn modulates NMDA receptor phosphorylation: differential synaptic function in NRG1+/− knock-outs compared with wild-type mice. Journal of Neuroscience 27, 45194529.CrossRefGoogle ScholarPubMed
Bourgin, C., Murai, K.K., Richter, M. and Pasquale, E.B. (2007) The EphA4 receptor regulates dendritic spine remodeling by affecting beta1-integrin signaling pathways. Journal of Cell Biology 178, 12951307.CrossRefGoogle ScholarPubMed
Bourne, J.N. and Harris, K.M. (2008) Balancing structure and function at hippocampal dendritic spines. Annual Review of Neuroscience 31, 4767.CrossRefGoogle ScholarPubMed
Buonanno, A. and Fischbach, G.D. (2001) Neuregulin and ErbB receptor signaling pathways in the nervous system. Current Opinion in Neurobiology 11, 287296.CrossRefGoogle ScholarPubMed
Carmona, M.A., Murai, K.K., Wang, L., Roberts, A.J. and Pasquale, E.B. (2009) Glial ephrin-A3 regulates hippocampal dendritic spine morphology and glutamate transport. Proceedings of the National Academy of Sciences of the U.S.A. doi: 10.1073 (106, 1252412529).CrossRefGoogle ScholarPubMed
Chang, Q. and Fischbach, G.D. (2006) An acute effect of neuregulin 1 beta to suppress alpha 7-containing nicotinic acetylcholine receptors in hippocampal interneurons. Journal of Neuroscience 26, 1129511303.CrossRefGoogle ScholarPubMed
Cheung, Z.H., Fu, A.K. and Ip, N.Y. (2006) Synaptic roles of Cdk5: implications in higher cognitive functions and neurodegenerative diseases. Neuron 50, 1318.CrossRefGoogle ScholarPubMed
Christopherson, K.S., Ullian, E.M., Stokes, C.C., Mullowney, C.E., Hell, J.W., Agah, A. et al. (2005) Thrombospondins are astrocyte-secreted proteins that promote CNS synaptogenesis. Cell 120, 421433.CrossRefGoogle ScholarPubMed
Contractor, A., Rogers, C., Maron, C., Henkemeyer, M., Swanson, G.T. and Heinemann, S.F. (2002) Trans-synaptic Eph receptor-ephrin signaling in hippocampal mossy fiber LTP. Science 296, 18641869.CrossRefGoogle ScholarPubMed
Corfas, G., Roy, K. and Buxbaum, J.D. (2004) Neuregulin 1-erbB signaling and the molecular/cellular basis of schizophrenia. Nature Neuroscience 7, 575580.CrossRefGoogle ScholarPubMed
Cowan, C.A. and Henkemeyer, M. (2001) The SH2/SH3 adaptor Grb4 transduces B-ephrin reverse signals. Nature 413, 174179.CrossRefGoogle ScholarPubMed
Dalva, M.B., Takasu, M.A., Lin, M.Z., Shamah, S.M., Hu, L., Gale, N.W. et al. (2000) EphB receptors interact with NMDA receptors and regulate excitatory synapse formation. Cell 103, 945956.CrossRefGoogle ScholarPubMed
Davy, A., Gale, N.W., Murray, E.W., Klinghoffer, R.A., Soriano, P., Feuerstein, C. et al. (1999) Compartmentalized signaling by GPI-anchored ephrin-A5 requires the Fyn tyrosine kinase to regulate cellular adhesion. Genes & Development 13, 31253135.CrossRefGoogle ScholarPubMed
Erickson, S.L., O'Shea, K.S., Ghaboosi, N., Loverro, L., Frantz, G., Bauer, M. et al. (1997) ErbB3 is required for normal cerebellar and cardiac development: a comparison with ErbB2-and heregulin-deficient mice. Development 124, 49995011.CrossRefGoogle ScholarPubMed
Essmann, C.L., Martinez, E., Geiger, J.C., Zimmer, M., Traut, M.H., Stein, V. et al. (2008) Serine phosphorylation of ephrinB2 regulates trafficking of synaptic AMPA receptors. Nature Neuroscience 11, 10351043.CrossRefGoogle ScholarPubMed
Ethell, I.M. and Pasquale, E.B. (2005) Molecular mechanisms of dendritic spine development and remodeling. Progress in Neurobiology 75, 161205.CrossRefGoogle ScholarPubMed
Falls, D.L. (2003) Neuregulins: functions, forms, and signaling strategies. Experimental Cell Research 284, 1430.CrossRefGoogle ScholarPubMed
Fellin, T., Pascual, O., Gobbo, S., Pozzan, T., Haydon, P.G. and Carmignoto, G. (2004) Neuronal synchrony mediated by astrocytic glutamate through activation of extrasynaptic NMDA receptors. Neuron 43, 729743.CrossRefGoogle ScholarPubMed
Fiala, J.C., Spacek, J. and Harris, K.M. (2002) Dendritic spine pathology: cause or consequence of neurological disorders? Brain Research – Brain Research Reviews 39, 2954.CrossRefGoogle ScholarPubMed
Flanagan, J.G. and Vanderhaeghen, P. (1998) The ephrins and Eph receptors in neural development. Annual Review of Neuroscience 21, 309345.CrossRefGoogle ScholarPubMed
Fu, A.K., Fu, W.Y., Cheung, J., Tsim, K.W., Ip, F.C., Wang, J.H. et al. (2001) Cdk5 is involved in neuregulin-induced AChR expression at the neuromuscular junction. Nature Neuroscience 4, 374381.CrossRefGoogle ScholarPubMed
Fu, A.Y., Hung, K.W., Shen, C., Xia, J., Fu, W.Y. and Ip, N.Y. (2008) EphA4-dependent signaling regulates the synaptic strength of glutamatergic synapses Program No. 325.8. Neuroscience 2008 Abstracts. Society for Neuroscience, Washington, DC, 2008. Online.Google Scholar
Fu, W.Y., Chen, Y., Sahin, M., Zhao, X.S., Shi, L., Bikoff, J.B. et al. (2007) Cdk5 regulates EphA4-mediated dendritic spine retraction through an ephexin1-dependent mechanism. Nature Neuroscience 10, 6776.CrossRefGoogle ScholarPubMed
Gajendran, N., Kapfhammer, J.P., Lain, E., Canepari, M., Vogt, K., Wisden, W. et al. (2009) Neuregulin signaling is dispensable for NMDA- and GABA(A)-receptor expression in the cerebellum in vivo. Journal of Neuroscience 29, 24042413.CrossRefGoogle ScholarPubMed
Gao, W.Q., Shinsky, N., Armanini, M.P., Moran, P., Zheng, J.L., Mendoza-Ramirez, J.L. et al. (1998) Regulation of hippocampal synaptic plasticity by the tyrosine kinase receptor, REK7/EphA5, and its ligand, AL-1/Ephrin-A5. Molecular & Cellular Neurosciences 11, 247259.CrossRefGoogle ScholarPubMed
Garcia, R.A., Vasudevan, K. and Buonanno, A. (2000) The neuregulin receptor ErbB-4 interacts with PDZ-containing proteins at neuronal synapses. Proceedings of the National Academy of Sciences of the U.S.A. 97, 35963601.CrossRefGoogle ScholarPubMed
Gassmann, M., Casagranda, F., Orioli, D., Simon, H., Lai, C., Klein, R. et al. (1995) Aberrant neural and cardiac development in mice lacking the ErbB4 neuregulin receptor. Nature 378, 390394.CrossRefGoogle ScholarPubMed
Georgakopoulos, A., Litterst, C., Ghersi, E., Baki, L., Xu, C., Serban, G. et al. (2006) Metalloproteinase/Presenilin1 processing of ephrinB regulates EphB-induced Src phosphorylation and signaling. EMBO Journal 25, 12421252.CrossRefGoogle ScholarPubMed
Gerlai, R., Shinsky, N., Shih, A., Williams, P., Winer, J., Armanini, M. et al. (1999) Regulation of learning by EphA receptors: a protein targeting study. Journal of Neuroscience 19, 95389549.CrossRefGoogle ScholarPubMed
Govek, E.E., Newey, S.E. and Van Aelst, L. (2005) The role of the Rho GTPases in neuronal development. Genes & Development 19, 149.CrossRefGoogle ScholarPubMed
Grunwald, I.C., Korte, M., Adelmann, G., Plueck, A., Kullander, K., Adams, R.H. et al. (2004) Hippocampal plasticity requires postsynaptic ephrinBs. Nature Neuroscience 7, 3340.CrossRefGoogle ScholarPubMed
Grunwald, I.C., Korte, M., Wolfer, D., Wilkinson, G.A., Unsicker, K., Lipp, H.P. et al. (2001) Kinase-independent requirement of EphB2 receptors in hippocampal synaptic plasticity. Neuron 32, 10271040.CrossRefGoogle ScholarPubMed
Gu, Z., Jiang, Q., Fu, A.K., Ip, N.Y. and Yan, Z. (2005) Regulation of NMDA receptors by neuregulin signaling in prefrontal cortex. Journal of Neuroscience 25, 49744984.CrossRefGoogle ScholarPubMed
Guy, P.M., Platko, J.V., Cantley, L.C., Cerione, R.A. and Carraway, K.L. 3rd (1994) Insect cell-expressed p180erbB3 possesses an impaired tyrosine kinase activity. Proceedings of the National Academy of Sciences of the U.S.A. 91, 81328136.CrossRefGoogle ScholarPubMed
Hama, H., Hara, C., Yamaguchi, K. and Miyawaki, A. (2004) PKC signaling mediates global enhancement of excitatory synaptogenesis in neurons triggered by local contact with astrocytes. Neuron 41, 405415.CrossRefGoogle ScholarPubMed
Hattori, M., Osterfield, M. and Flanagan, J.G. (2000) Regulated cleavage of a contact-mediated axon repellent. Science 289, 13601365.CrossRefGoogle ScholarPubMed
Henderson, J.T., Georgiou, J., Jia, Z., Robertson, J., Elowe, S., Roder, J.C. et al. (2001) The receptor tyrosine kinase EphB2 regulates NMDA-dependent synaptic function. Neuron 32, 10411056.CrossRefGoogle ScholarPubMed
Henkemeyer, M., Itkis, O.S., Ngo, M., Hickmott, P.W. and Ethell, I.M. (2003) Multiple EphB receptor tyrosine kinases shape dendritic spines in the hippocampus. Journal of Cell Biology 163, 13131326.CrossRefGoogle ScholarPubMed
Huang, Y.Z., Wang, Q., Xiong, W.C. and Mei, L. (2001) Erbin is a protein concentrated at postsynaptic membranes that interacts with PSD-95. Journal of Biological Chemistry 276, 1931819326.CrossRefGoogle ScholarPubMed
Huang, Y.Z., Won, S., Ali, D.W., Wang, Q., Tanowitz, M., Du, Q.S. et al. (2000) Regulation of neuregulin signaling by PSD-95 interacting with ErbB4 at CNS synapses. Neuron 26, 443455.CrossRefGoogle ScholarPubMed
Inoue, E., Deguchi-Tawarada, M., Togawa, A., Matsui, C., Arita, K., Katahira-Tayama, S. et al. (2009) Synaptic activity prompts {gamma}-secretase-mediated cleavage of EphA4 and dendritic spine formation. Journal of Cell Biology 185, 551564.CrossRefGoogle ScholarPubMed
Irie, F., Okuno, M., Pasquale, E.B. and Yamaguchi, Y. (2005) EphrinB-EphB signalling regulates clathrin-mediated endocytosis through tyrosine phosphorylation of synaptojanin 1. Nature Cell Biology 7, 501509.CrossRefGoogle ScholarPubMed
Irie, F. and Yamaguchi, Y. (2002) EphB receptors regulate dendritic spine development via intersectin, Cdc42 and N-WASP. Nature Neuroscience 5, 11171118.CrossRefGoogle ScholarPubMed
Iwasato, T., Katoh, H., Nishimaru, H., Ishikawa, Y., Inoue, H., Saito, Y.M. et al. (2007) Rac-GAP alpha-chimerin regulates motor-circuit formation as a key mediator of EphrinB3/EphA4 forward signaling. Cell 130, 742753.CrossRefGoogle ScholarPubMed
Kadotani, H., Hirano, T., Masugi, M., Nakamura, K., Nakao, K., Katsuki, M. et al. (1996) Motor discoordination results from combined gene disruption of the NMDA receptor NR2A and NR2C subunits, but not from single disruption of the NR2A or NR2C subunit. Journal of Neuroscience 16, 78597867.CrossRefGoogle ScholarPubMed
Kayser, M.S., McClelland, A.C., Hughes, E.G. and Dalva, M.B. (2006) Intracellular and trans-synaptic regulation of glutamatergic synaptogenesis by EphB receptors. Journal of Neuroscience 26, 1215212164.CrossRefGoogle ScholarPubMed
Kayser, M.S., Nolt, M.J. and Dalva, M.B. (2008) EphB receptors couple dendritic filopodia motility to synapse formation. Neuron 59, 5669.CrossRefGoogle ScholarPubMed
Kim, E. and Sheng, M. (2004) PDZ domain proteins of synapses. Nature Reviews Neuroscience 5, 771781.CrossRefGoogle ScholarPubMed
Klein, R. (2009) Bidirectional modulation of synaptic functions by Eph/ephrin signaling. Nature Neuroscience 12, 1520.CrossRefGoogle ScholarPubMed
Krivosheya, D., Tapia, L., Levinson, J.N., Huang, K., Kang, Y., Hines, R. et al. (2008) ErbB4-neuregulin signaling modulates synapse development and dendritic arborization through distinct mechanisms. Journal of Biological Chemistry 283, 3294432956.CrossRefGoogle ScholarPubMed
Kwon, O.B., Longart, M., Vullhorst, D., Hoffman, D.A. and Buonanno, A. (2005) Neuregulin-1 reverses long-term potentiation at CA1 hippocampal synapses. Journal of Neuroscience 25, 93789383.CrossRefGoogle ScholarPubMed
Kwon, O.B., Paredes, D., Gonzalez, C.M., Neddens, J., Hernandez, L., Vullhorst, D. et al. (2008) Neuregulin-1 regulates LTP at CA1 hippocampal synapses through activation of dopamine D4 receptors. Proceedings of the National Academy of Sciences of the U.S.A. 105, 1558715592.CrossRefGoogle ScholarPubMed
Lai, K.O., Ip, F.C., Cheung, J., Fu, A.K. and Ip, N.Y. (2001) Expression of Eph receptors in skeletal muscle and their localization at the neuromuscular junction. Molecular & Cellular Neurosciences 17, 10341047.CrossRefGoogle ScholarPubMed
Lauterbach, J. and Klein, R. (2006) Release of full-length EphB2 receptors from hippocampal neurons to cocultured glial cells. Journal of Neuroscience 26, 1157511581.CrossRefGoogle ScholarPubMed
Lee, H.J., Jung, K.M., Huang, Y.Z., Bennett, L.B., Lee, J.S., Mei, L. et al. (2002) Presenilin-dependent gamma-secretase-like intramembrane cleavage of ErbB4. Journal of Biological Chemistry 277, 63186323.CrossRefGoogle ScholarPubMed
Lewis, D.A. and Moghaddam, B. (2006) Cognitive dysfunction in schizophrenia: convergence of gamma-aminobutyric acid and glutamate alterations. Archives of Neurology 63, 13721376.CrossRefGoogle ScholarPubMed
Li, B., Woo, R.S., Mei, L. and Malinow, R. (2007) The neuregulin-1 receptor erbB4 controls glutamatergic synapse maturation and plasticity. Neuron 54, 583597.CrossRefGoogle ScholarPubMed
Li, Y., Tennekoon, G.I., Birnbaum, M., Marchionni, M.A. and Rutkowski, J.L. (2001) Neuregulin signaling through a PI3K/Akt/Bad pathway in Schwann cell survival. Molecular & Cellular Neurosciences 17, 761767.CrossRefGoogle ScholarPubMed
Linggi, B. and Carpenter, G. (2006) ErbB receptors: new insights on mechanisms and biology. Trends in Cell Biology 16, 649656.CrossRefGoogle ScholarPubMed
Litterst, C., Georgakopoulos, A., Shioi, J., Ghersi, E., Wisniewski, T., Wang, R. et al. (2007) Ligand binding and calcium influx induce distinct ectodomain/gamma-secretase-processing pathways of EphB2 receptor. Journal of Biological Chemistry 282, 1615516163.CrossRefGoogle ScholarPubMed
Liu, Y., Ford, B., Mann, M.A. and Fischbach, G.D. (2001) Neuregulins increase alpha7 nicotinic acetylcholine receptors and enhance excitatory synaptic transmission in GABAergic interneurons of the hippocampus. Journal of Neuroscience 21, 56605669.CrossRefGoogle ScholarPubMed
Ma, L., Huang, Y.Z., Pitcher, G.M., Valtschanoff, J.G., Ma, Y.H., Feng, L.Y. et al. (2003) Ligand-dependent recruitment of the ErbB4 signaling complex into neuronal lipid rafts. Journal of Neuroscience 23, 31643175.CrossRefGoogle ScholarPubMed
Marler, K.J., Becker-Barroso, E., Martinez, A., Llovera, M., Wentzel, C., Poopalasundaram, S. et al. (2008) A TrkB/EphrinA interaction controls retinal axon branching and synaptogenesis. Journal of Neuroscience 28, 1270012712.CrossRefGoogle ScholarPubMed
Marston, D.J., Dickinson, S. and Nobes, C.D. (2003) Rac-dependent trans-endocytosis of ephrinBs regulates Eph-ephrin contact repulsion. Nature Cell Biology 5, 879888.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
Mei, L. and Xiong, W.C. (2008) Neuregulin 1 in neural development, synaptic plasticity and schizophrenia. Nature Reviews Neuroscience 9, 437452.CrossRefGoogle ScholarPubMed
Meyer, D. and Birchmeier, C. (1995) Multiple essential functions of neuregulin in development. Nature 378, 386390.CrossRefGoogle ScholarPubMed
Murai, K.K., Nguyen, L.N., Irie, F., Yamaguchi, Y. and Pasquale, E.B. (2003) Control of hippocampal dendritic spine morphology through ephrin-A3/EphA4 signaling. Nature Neuroscience 6, 153160.CrossRefGoogle ScholarPubMed
Naisbitt, S., Kim, E., Tu, J.C., Xiao, B., Sala, C., Valtschanoff, J. et al. (1999) Shank, a novel family of postsynaptic density proteins that binds to the NMDA receptor/PSD-95/GKAP complex and cortactin. Neuron 23, 569582.CrossRefGoogle Scholar
Nakazawa, T., Komai, S., Tezuka, T., Hisatsune, C., Umemori, H., Semba, K. et al. (2001) Characterization of Fyn-mediated tyrosine phosphorylation sites on GluR epsilon 2 (NR2B) subunit of the N-methyl-D-aspartate receptor. Journal of Biological Chemistry 276, 693699.CrossRefGoogle ScholarPubMed
Nestor, M.W., Mok, L.P., Tulapurkar, M.E. and Thompson, S.M. (2007) Plasticity of neuron–glial interactions mediated by astrocytic EphARs. Journal of Neuroscience 27, 1281712828.CrossRefGoogle ScholarPubMed
Ni, C.Y., Murphy, M.P., Golde, T.E. and Carpenter, G. (2001) gamma-Secretase cleavage and nuclear localization of ErbB-4 receptor tyrosine kinase. Science 294, 21792181.CrossRefGoogle ScholarPubMed
Nishida, H. and Okabe, S. (2007) Direct astrocytic contacts regulate local maturation of dendritic spines. Journal of Neuroscience 27, 331340.CrossRefGoogle ScholarPubMed
Okada, M. and Corfas, G. (2004) Neuregulin1 downregulates postsynaptic GABAA receptors at the hippocampal inhibitory synapse. Hippocampus 14, 337344.CrossRefGoogle ScholarPubMed
Ozaki, M., Sasner, M., Yano, R., Lu, H.S. and Buonanno, A. (1997) Neuregulin-beta induces expression of an NMDA-receptor subunit. Nature 390, 691694.CrossRefGoogle ScholarPubMed
Pasquale, E.B. (2005) Eph receptor signalling casts a wide net on cell behaviour. Nature Reviews Molecular Cell Biology 6, 462475.CrossRefGoogle ScholarPubMed
Penzes, P., Beeser, A., Chernoff, J., Schiller, M.R., Eipper, B.A., Mains, R.E. et al. (2003) Rapid induction of dendritic spine morphogenesis by trans-synaptic ephrinB-EphB receptor activation of the Rho-GEF kalirin. Neuron 37, 263274.CrossRefGoogle ScholarPubMed
Pitcher, G.M., Beggs, S., Woo, R.S., Mei, L. and Salter, M.W. (2008) ErbB4 is a suppressor of long-term potentiation in the adult hippocampus. Neuroreport 19, 139143.CrossRefGoogle ScholarPubMed
Rieff, H.I., Raetzman, L.T., Sapp, D.W., Yeh, H.H., Siegel, R.E. and Corfas, G. (1999) Neuregulin induces GABA(A) receptor subunit expression and neurite outgrowth in cerebellar granule cells. Journal of Neuroscience 19, 1075710766.CrossRefGoogle ScholarPubMed
Rio, C., Buxbaum, J.D., Peschon, J.J. and Corfas, G. (2000) Tumor necrosis factor-alpha-converting enzyme is required for cleavage of erbB4/HER4. Journal of Biological Chemistry 275, 1037910387.CrossRefGoogle ScholarPubMed
Rio, C., Rieff, H.I., Qi, P., Khurana, T.S. and Corfas, G. (1997) Neuregulin and erbB receptors play a critical role in neuronal migration. Neuron 19, 3950.CrossRefGoogle ScholarPubMed
Rodenas-Ruano, A., Perez-Pinzon, M.A., Green, E.J., Henkemeyer, M. and Liebl, D.J. (2006) Distinct roles for ephrinB3 in the formation and function of hippocampal synapses. Developmental Biology 292, 3445.CrossRefGoogle Scholar
Role, L.W. and Talmage, D.A. (2007) Neurobiology: new order for thought disorders. Nature 448, 263265.CrossRefGoogle ScholarPubMed
Sardi, S.P., Murtie, J., Koirala, S., Patten, B.A. and Corfas, G. (2006) Presenilin-dependent ErbB4 nuclear signaling regulates the timing of astrogenesis in the developing brain. Cell 127, 185197.CrossRefGoogle ScholarPubMed
Segura, I., Essmann, C.L., Weinges, S. and Acker-Palmer, A. (2007) Grb4 and GIT1 transduce ephrinB reverse signals modulating spine morphogenesis and synapse formation. Nature Neuroscience 10, 301310.CrossRefGoogle ScholarPubMed
Shamah, S.M., Lin, M.Z., Goldberg, J.L., Estrach, S., Sahin, M., Hu, L. et al. (2001) EphA receptors regulate growth cone dynamics through the novel guanine nucleotide exchange factor ephexin. Cell 105, 233244.CrossRefGoogle ScholarPubMed
Shi, L., Fu, W.Y., Hung, K.W., Porchetta, C., Hall, C., Fu, A.K. et al. (2007) Alpha2-chimaerin interacts with EphA4 and regulates EphA4-dependent growth cone collapse. Proceedings of the National Academy of Sciences of the U.S.A. 104, 1634716352.CrossRefGoogle ScholarPubMed
Shi, Y., Pontrello, C.G., DeFea, K.A., Reichardt, L.F. and Ethell, I.M. (2009) Focal adhesion kinase acts downstream of EphB receptors to maintain mature dendritic spines by regulating cofilin activity. Journal of Neuroscience 29, 4681–4608.CrossRefGoogle ScholarPubMed
Simón, A.M., de Maturana, R.L., Ricobaraza, A., Escribano, L., Schiapparelli, L., Cuadrado-Tejedor, M. et al. (2009) Early changes in hippocampal Eph receptors precede the onset of memory decline in mouse models of Alzheimer's disease. Journal of Alzheimer's Disease DOI: 10.3233/JAD-2009-1096.CrossRefGoogle ScholarPubMed
Stevens, B. (2008) Neuron–astrocyte signaling in the development and plasticity of neural circuits. NeuroSignals 16, 278288.CrossRefGoogle ScholarPubMed
Tada, T. and Sheng, M. (2006) Molecular mechanisms of dendritic spine morphogenesis. Current Opinion in Neurobiology 16, 95101.CrossRefGoogle ScholarPubMed
Takahashi, T., Feldmeyer, D., Suzuki, N., Onodera, K., Cull-Candy, S.G., Sakimura, K. et al. (1996) Functional correlation of NMDA receptor epsilon subunits expression with the properties of single-channel and synaptic currents in the developing cerebellum. Journal of Neuroscience 16, 43764382.CrossRefGoogle ScholarPubMed
Takasu, M.A., Dalva, M.B., Zigmond, R.E. and Greenberg, M.E. (2002) Modulation of NMDA receptor-dependent calcium influx and gene expression through EphB receptors. Science 295, 491495.CrossRefGoogle ScholarPubMed
Thompson, S.M. (2003) Ephrins keep dendritic spines in shape. Nature Neuroscience 6, 103104.CrossRefGoogle ScholarPubMed
Tolias, K.F., Bikoff, J.B., Kane, C.G., Tolias, C.S., Hu, L. and Greenberg, M.E. (2007) The Rac1 guanine nucleotide exchange factor Tiam1 mediates EphB receptor-dependent dendritic spine development. Proceedings of the National Academy of Sciences of the U.S.A. 104, 72657270.CrossRefGoogle ScholarPubMed
Tomita, T., Tanaka, S., Morohashi, Y. and Iwatsubo, T. (2006) Presenilin-dependent intramembrane cleavage of ephrin-B1. Molecular Neurodegeneration 1, 2.CrossRefGoogle ScholarPubMed
Torres, R., Firestein, B.L., Dong, H., Staudinger, J., Olson, E.N., Huganir, R.L. et al. (1998) PDZ proteins bind, cluster, and synaptically colocalize with Eph receptors and their ephrin ligands. Neuron 21, 14531463.CrossRefGoogle ScholarPubMed
Tzahar, E., Waterman, H., Chen, X., Levkowitz, G., Karunagaran, D., Lavi, S. et al. (1996) A hierarchical network of interreceptor interactions determines signal transduction by Neu differentiation factor/neuregulin and epidermal growth factor. Molecular & Cellular Biology 16, 52765287.CrossRefGoogle ScholarPubMed
Vecchi, M. and Carpenter, G. (1997) Constitutive proteolysis of the ErbB-4 receptor tyrosine kinase by a unique, sequential mechanism. Journal of Cell Biology 139, 9951003.CrossRefGoogle ScholarPubMed
Wang, J.Y., Frenzel, K.E., Wen, D. and Falls, D.L. (1998) Transmembrane neuregulins interact with LIM kinase 1, a cytoplasmic protein kinase implicated in development of visuospatial cognition. Journal of Biological Chemistry 273, 2052520534.CrossRefGoogle ScholarPubMed
Watanabe, M., Inoue, Y., Sakimura, K. and Mishina, M. (1992) Developmental changes in distribution of NMDA receptor channel subunit mRNAs. Neuroreport 3, 11381140.CrossRefGoogle ScholarPubMed
Wegmeyer, H., Egea, J., Rabe, N., Gezelius, H., Filosa, A., Enjin, A. et al. (2007) EphA4-dependent axon guidance is mediated by the RacGAP alpha2-chimaerin. Neuron 55, 756767.CrossRefGoogle ScholarPubMed
Wilkinson, D.G. (2001) Multiple roles of EPH receptors and ephrins in neural development. Nature Reviews Neuroscience 2, 155164.CrossRefGoogle ScholarPubMed
Woo, R.S., Li, X.M., Tao, Y., Carpenter-Hyland, E., Huang, Y.Z., Weber, J. et al. (2007) Neuregulin-1 enhances depolarization-induced GABA release. Neuron 54, 599610.CrossRefGoogle ScholarPubMed
Xie, F., Padival, M. and Siegel, R.E. (2007) Association of PSD-95 with ErbB4 facilitates neuregulin signaling in cerebellar granule neurons in culture. Journal of Neurochemistry 100, 6272.CrossRefGoogle ScholarPubMed
Xie, F., Raetzman, L.T. and Siegel, R.E. (2004) Neuregulin induces GABAA receptor beta2 subunit expression in cultured rat cerebellar granule neurons by activating multiple signaling pathways. Journal of Neurochemistry 90, 15211529.CrossRefGoogle ScholarPubMed
Zhong, C., Du, C., Hancock, M., Mertz, M., Talmage, D.A. and Role, L.W. (2008) Presynaptic type III neuregulin 1 is required for sustained enhancement of hippocampal transmission by nicotine and for axonal targeting of alpha7 nicotinic acetylcholine receptors. Journal of Neuroscience 28, 91119116.CrossRefGoogle ScholarPubMed
Zhou, L., Martinez, S.J., Haber, M., Jones, E.V., Bouvier, D., Doucet, G. et al. (2007) EphA4 signaling regulates phospholipase Cgamma1 activation, cofilin membrane association, and dendritic spine morphology. Journal of Neuroscience 27, 51275138.CrossRefGoogle ScholarPubMed
Zimmer, M., Palmer, A., Kohler, J. and Klein, R. (2003) EphB-ephrinB bi-directional endocytosis terminates adhesion allowing contact mediated repulsion. Nature Cell Biology 5, 869878.CrossRefGoogle ScholarPubMed