Functions of ephrin/Eph interactions in the development of the nervous system: Emphasis on the hippocampal system

Allison, 1998, Role of actin in anchoring postsynaptic receptors in cultured hippocampal neurons: differential attachment of NMDA versus AMPA receptors, J. Neurosci., 18, 2423, 10.1523/JNEUROSCI.18-07-02423.1998 Amaral, 1995, The hippocampal formation, 443 Baker, 2003, Ephs and ephrins during early stages of chick embryogenesis, Dev. Dyn., 228, 128, 10.1002/dvdy.10354 Barallobre, 2000, Aberrant development of hippocampal circuits and altered neural activity in netrin 1-deficient mice, Development, 127, 4797, 10.1242/dev.127.22.4797 Bartley, 1994, B61 is a ligand for the ECK receptor protein-tyrosine kinase, Nature, 368, 558, 10.1038/368558a0 Becker, 1994, Several receptor tryosine kinase genes of the Eph family are segmentally expressed in the developing hindbrain, Mech. Dev., 47, 3, 10.1016/0925-4773(94)90091-4 Bergemann, 1995, ELF-2, a new member of the Eph ligand family, is segmentally expressed in the region of the hindbrain and newly forming somites, Mol. Cell. Biol., 15, 4921, 10.1128/MCB.15.9.4921 Blasco-Ibañez, 1997, Distribution, ultrastructure, and connectivity of calretinin-immunoreactive mossy cells of the mouse dentate gyrus, Hippocampus, 7, 307, 10.1002/(SICI)1098-1063(1997)7:3<307::AID-HIPO6>3.0.CO;2-H Bohme, 1996, Cell–cell adhesion mediated by binding of membrane-anchored ligand LERK-2 to the EPH-related receptor human embryonal kinase 2 promotes tyrosine kinase activity, J. Biol. Chem., 271, 24747, 10.1074/jbc.271.40.24747 Borrell, 1999, Reelin regulates the development and synaptogenesis of the layer-specific entorhino-hippocampal connections, J. Neurosci., 19, 1345, 10.1523/JNEUROSCI.19-04-01345.1999 Borrell, 1999, Development of commissural connections in the hippocampus of reeler mice: evidence of an inhibitory influence of Cajal–Retzius cells, Exp. Neurol., 156, 268, 10.1006/exnr.1999.7022 Braisted, 1997, Graded and lamina-specific distributions of ligands of EphB receptor tyrosine kinases in the developing retinotectal system, Dev. Biol., 191, 14, 10.1006/dbio.1997.8706 Brittis, 2002, Axonal protein synthesis provides a mechanism for localized regulation at an intermediate target, Cell, 110, 223, 10.1016/S0092-8674(02)00813-9 Bronner-Fraser, 1986, Analysis of the early stages of trunk neural crest migration in avian embryos using monoclonal antibody HNK-1, Dev. Biol., 115, 44, 10.1016/0012-1606(86)90226-5 Brownlee, 2000, Multiple ephrins regulate hippocampal neurite outgrowth, J. Comp. Neurol., 425, 315, 10.1002/1096-9861(20000918)425:2<315::AID-CNE12>3.0.CO;2-# Bruckner, 1997, Tyrosine phosphorylation of transmembrane ligands for Eph receptors, Science, 275, 1640, 10.1126/science.275.5306.1640 Bruckner, 1999, EphrinB ligands recruit GRIP family PDZ adaptor proteins into raft membrane microdomains, Neuron, 22, 511, 10.1016/S0896-6273(00)80706-0 Buchert, 1999, The junction-associated protein AF-6 interacts and clusters with specific Eph receptor tyrosine kinases at specialized sites of cell–cell contact in the brain, J. Cell Biol., 144, 361, 10.1083/jcb.144.2.361 Calakos, 1996, Synaptic vesicle biogenesis, docking, and fusion: a molecular description, Physiol. Rev., 76, 1, 10.1152/physrev.1996.76.1.1 Castellani, 1998, Dual action of a ligand for Eph receptor tyrosine kinases on specific populations of axons during the development of cortical circuits, J. Neurosci., 18, 4663, 10.1523/JNEUROSCI.18-12-04663.1998 Chedotal, 1998, Semaphorins III and IV repel hippocampal axons via two distinct receptors, Development, 125, 4313, 10.1242/dev.125.21.4313 Chen, 2004, Abnormal hippocampal axon bundling in EphB receptor mutant mice, J. Neurosci., 24, 2366, 10.1523/JNEUROSCI.4711-03.2004 Cheng, 1995, Complementary gradients in expression and binding of ELF-1 and Mek4 in development of the topographic retinotectal projection map, Cell, 82, 371, 10.1016/0092-8674(95)90426-3 Chin-Sang, 1999, The ephrin VAB-2/EFN-1 functions in neuronal signaling to regulate epidermal morphogenesis in C. elegans, Cell, 99, 781, 10.1016/S0092-8674(00)81675-X Chong, 2000, Fibroblast growth factor receptor-mediated rescue of x-ephrin B1-induced cell dissociation in Xenopus embryos, Mol. Cell. Biol., 20, 724, 10.1128/MCB.20.2.724-734.2000 Ciossek, 1995, Identification of alternatively spliced mRNAs encoding variants of MDK1, a novel receptor tyrosine kinase expressed in the murine nervous system, Oncogene, 10, 97 Connor, 1998, Expression and tyrosine phosphorylation of Eph receptors suggest multiple mechanisms in patterning of the visual system, Dev. Biol., 193, 21, 10.1006/dbio.1997.8786 Contractor, 2002, Trans-synaptic Eph receptor-ephrin signaling in hippocampal mossy fiber LTP, Science, 296, 1864, 10.1126/science.1069081 Cowan, 2001, The SH2/SH3 adaptor Grb4 transduces B-ephrin reverse signals, Nature, 413, 174, 10.1038/35093123 Cutforth, 2003, Axonal ephrin-As and odorant receptors: coordinate determination of the olfactory sensory map, Cell, 114, 311, 10.1016/S0092-8674(03)00568-3 Dai, 1995, Abi-2, a novel SH3-containing protein interacts with the c-Abl tyrosine kinase and modulates c-Abl transforming activity, Genes Dev., 9, 2569, 10.1101/gad.9.21.2569 Dalva, 2000, EphB receptors interact with NMDA receptors and regulate excitatory synapse formation, Cell, 103, 945, 10.1016/S0092-8674(00)00197-5 Davis, 1994, Ligands for EPH-related receptor tyrosine kinases that require membrane attachment or clustering for activity, Science, 266, 816, 10.1126/science.7973638 Davy, 2000, Ephrin-A5 modulates cell adhesion and morphology in an integrin-dependent manner, EMBO J., 19, 5396, 10.1093/emboj/19.20.5396 Davy, 1999, Compartmentalized signaling by GPI-anchored ephrin-A5 requires the Fyn tyrosine kinase to regulate cellular adhesion, Genes Dev., 13, 3125, 10.1101/gad.13.23.3125 Del Rio, 1997, A role for Cajal–Retzius cells and reelin in the development of hippocampal connections, Nature, 385, 70, 10.1038/385070a0 Dergham, 2002, Rho signaling pathway targeted to promote spinal cord repair, J. Neurosci., 22, 6570, 10.1523/JNEUROSCI.22-15-06570.2002 Dodelet, 1999, A novel signaling intermediate, SHEP1, directly couples Eph receptors to R-Ras and Rap1A, J. Biol. Chem., 274, 31941, 10.1074/jbc.274.45.31941 Dottori, 1998, EphA4 (Sek1) receptor tyrosine kinase is required for the development of the corticospinal tract, Proc. Natl. Acad. Sci. U. S. A., 95, 13248, 10.1073/pnas.95.22.13248 Drescher, 1995, In vitro guidance of retinal ganglion cell axons by RAGS, a 25 kDa tectal protein related to ligands for Eph receptor tyrosine kinases, Cell, 82, 359, 10.1016/0092-8674(95)90425-5 Dufour, 2003, Area specificity and topography of thalamocortical projections are controlled by ephrin/Eph genes, Neuron, 39, 453, 10.1016/S0896-6273(03)00440-9 Durbin, 1998, Eph signaling is required for segmentation and differentiation of the somites, Genes Dev., 12, 3096, 10.1101/gad.12.19.3096 Dutting, 1999, Topographic targeting and pathfinding errors of retinal axons following overexpression of ephrinA ligands on retinal ganglion cell axons, Dev. Biol., 216, 297, 10.1006/dbio.1999.9489 Eberhart, 2004, Ephrin-A5 exerts positive or inhibitory effects on distinct subsets of EphA4-positive motor neurons, J. Neurosci., 24, 1070, 10.1523/JNEUROSCI.4719-03.2004 Ellis, 1996, A juxtamembrane autophosphorylation site in the Eph family receptor tyrosine kinase, Sek, mediates high affinity interaction with p59fyn, Oncogene, 12, 1727 Elowe, 2001, Downregulation of the Ras-mitogen-activated protein kinase pathway by the EphB2 receptor tyrosine kinase is required for ephrin-induced neurite retraction, Mol. Cell. Biol., 21, 7429, 10.1128/MCB.21.21.7429-7441.2001 1997, Unified nomenclature for Eph family receptors and their ligands, the ephrins, Cell, 90, 403, 10.1016/S0092-8674(00)80500-0 Ethell, 2001, EphB/syndecan-2 signaling in dendritic spine morphogenesis, Neuron, 31, 1001, 10.1016/S0896-6273(01)00440-8 Feldheim, 1998, Topographic guidance labels in a sensory projection to the forebrain, Neuron, 21, 1303, 10.1016/S0896-6273(00)80650-9 Feldheim, 2000, Genetic analysis of ephrin-A2 and ephrin-A5 shows their requirement in multiple aspects of retinocollicular mapping, Neuron, 25, 563, 10.1016/S0896-6273(00)81060-0 Feldheim, 2004, Loss-of-function analysis of EphA receptors in retinotectal mapping, J. Neurosci., 24, 2542, 10.1523/JNEUROSCI.0239-03.2004 Feng, 2000, Roles for ephrins in positionally selective synaptogenesis between motor neurons and muscle fibers, Neuron, 25, 295, 10.1016/S0896-6273(00)80895-8 Flenniken, 1996, Distinct and overlapping expression patterns of ligands for Eph-related receptor tyrosine kinases during mouse embryogenesis, Dev. Biol., 179, 382, 10.1006/dbio.1996.0269 Forcet, 2002, Netrin-1-mediated axon outgrowth requires deleted in colorectal cancer-dependent MAPK activation, Nature, 417, 443, 10.1038/nature748 Fournier, 2003, Rho kinase inhibition enhances axonal regeneration in the injured CNS, J. Neurosci., 23, 1416, 10.1523/JNEUROSCI.23-04-01416.2003 Frisen, 1998, Ephrin-A5 (AL-1/RAGS) is essential for proper retinal axon guidance and topographic mapping in the mammalian visual system, Neuron, 20, 235, 10.1016/S0896-6273(00)80452-3 Gale, 1996, Eph receptors and ligands comprise two major specificity subclasses and are reciprocally compartmentalized during embryogenesis, Neuron, 17, 9, 10.1016/S0896-6273(00)80276-7 Gao, 1996, Regulation of topographic projection in the brain: Elf-1 in the hippocamposeptal system, Proc. Natl. Acad. Sci. U. S. A., 93, 11161, 10.1073/pnas.93.20.11161 Gao, 1998, Regulation of thalamic neurite outgrowth by the Eph ligand ephrin-A5: implications in the development of thalamocortical projections, Proc. Natl. Acad. Sci. U. S. A., 95, 5329, 10.1073/pnas.95.9.5329 Gao, 1998, Regulation of hippocampal synaptic plasticity by the tyrosine kinase receptor, REK7/EphA5, and its ligand, AL-1/Ephrin-A5, Mol. Cell. Neurosci., 11, 247, 10.1006/mcne.1998.0696 Gao, 1999, Ephrin-dependent growth and pruning of hippocampal axons, Proc. Natl. Acad. Sci. U. S. A., 96, 4073, 10.1073/pnas.96.7.4073 Gebhardt, 2002, Abnormal positioning of granule cells alters afferent fiber distribution in the mouse fascia dentata: morphologic evidence from reeler, apolipoprotein E receptor 2-, and very low density lipoprotein receptor knockout mice, J. Comp. Neurol., 445, 278, 10.1002/cne.10172 Gerlai, 2002, EphB and NMDA receptors: components of synaptic plasticity coming together, Trends Neurosci., 25, 180, 10.1016/S0166-2236(02)02165-3 Gerlai, 2000, Anesthesia induced retrograde amnesia is ameliorated by ephrinA5-IgG in mice: EphA receptor tyrosine kinases are involved in mammalian memory, Behav. Brain Res., 108, 133, 10.1016/S0166-4328(99)00139-4 Gerlai, 1999, Regulation of learning by EphA receptors: a protein targeting study, J. Neurosci., 19, 9538, 10.1523/JNEUROSCI.19-21-09538.1999 Grant, 1996, Analysis of NMDA receptor mediated synaptic plasticity using gene targeting: roles of Fyn and FAK non-receptor tyrosine kinases, J. Physiol., 90, 337 Grant, 1992, Impaired long-term potentiation, spatial learning, and hippocampal development in fyn mutant mice, Science, 258, 1903, 10.1126/science.1361685 Grunwald, 2001, Kinase-independent requirement of EphB2 receptors in hippocampal synaptic plasticity, Neuron, 32, 1027, 10.1016/S0896-6273(01)00550-5 Grunwald, 2004, Hippocampal plasticity requires postsynaptic ephrinBs, Nat. Neurosci., 7, 33, 10.1038/nn1164 Gu, 2003, Neuropilin-1 conveys semaphorin and VEGF signaling during neural and cardiovascular development, Dev. Cell, 5, 45, 10.1016/S1534-5807(03)00169-2 Hansen, 2004, Retinal axon response to ephrin-as shows a graded, concentration-dependent transition from growth promotion to inhibition, Neuron, 42, 717, 10.1016/j.neuron.2004.05.009 Hattori, 2000, Regulated cleavage of a contact-mediated axon repellent, Science, 289, 1360, 10.1126/science.289.5483.1360 Hayashi, 1996, Modulatory role of drebrin on the cytoskeleton within dendritic spines in the rat cerebral cortex, J. Neurosci., 16, 7161, 10.1523/JNEUROSCI.16-22-07161.1996 Helmbacher, 2000, Targeting of the EphA4 tyrosine kinase receptor affects dorsal/ventral pathfinding of limb motor axons, Development, 127, 3313, 10.1242/dev.127.15.3313 Henderson, 2001, The receptor tyrosine kinase EphB2 regulates NMDA-dependent synaptic function, Neuron, 32, 1041, 10.1016/S0896-6273(01)00553-0 Henkemeyer, 1994, Immunolocalization of the Nuk receptor tyrosine kinase suggests roles in segmental patterning of the brain and axonogenesis, Oncogene, 9, 1001 Henkemeyer, 1996, Nuk controls pathfinding of commissural axons in the mammalian central nervous system, Cell, 86, 35, 10.1016/S0092-8674(00)80075-6 Henkemeyer, 2003, Multiple EphB receptor tyrosine kinases shape dendritic spines in the hippocampus, J. Cell Biol., 163, 1313, 10.1083/jcb.200306033 Himanen, 2003, Eph receptors and ephrins, Int. J. Biochem. Cell Biol., 35, 130, 10.1016/S1357-2725(02)00096-1 Himanen, 1998, Crystal structure of the ligand-binding domain of the receptor tyrosine kinase EphB2, Nature, 396, 486, 10.1038/24904 Himanen, 2001, Crystal structure of an Eph receptor–ephrin complex, Nature, 414, 933, 10.1038/414933a Himanen, 2004, Repelling class discrimination: ephrin-A5 binds to and activates EphB2 receptor signalling, Nat. Neurosci., 2, 501, 10.1038/nn1237 Hindges, 2002, EphB forward signaling controls directional branch extension and arborization required for dorsal–ventral retinotopic mapping, Neuron, 35, 475, 10.1016/S0896-6273(02)00799-7 Hirai, 1987, A novel putative tyrosine kinase receptor encoded by the eph gene, Science, 238, 1717, 10.1126/science.2825356 Holash, 1995, Polarized expression of the receptor protein tyrosine kinase Cek5 in the developing avian visual system, Dev. Biol., 172, 683, 10.1006/dbio.1995.8039 Holash, 1997, Reciprocal expression of the Eph receptor Cek5 and its ligand(s) in the early retina, Dev. Biol., 182, 256, 10.1006/dbio.1996.8496 Holland, 1996, Bi-directional signalling through the EPH-family receptor Nuk and its transmembrane ligands, Nature, 383, 722, 10.1038/383722a0 Holmberg, 2000, Regulation of repulsion versus adhesion by different splice forms of an Eph receptor, Nature, 408, 203, 10.1038/35041577 Holzman, 1990, A novel immediate-early response gene of endothelium is induced by cytokines and encodes a secreted protein, Mol. Cell. Biol., 10, 5830, 10.1128/MCB.10.11.5830 Hornberger, 1999, Modulation of EphA receptor function by coexpressed ephrinA ligands on retinal ganglion cell axons, Neuron, 22, 731, 10.1016/S0896-6273(00)80732-1 Hu, 2003, Corpus callosum deficiency in transgenic mice expressing a truncated Ephrin-a receptor, J. Neurosci., 23, 10963, 10.1523/JNEUROSCI.23-34-10963.2003 Huai, 2001, An ephrin-A-dependent signaling pathway controls integrin function and is linked to the tyrosine phosphorylation of a 120-kDa protein, J. Biol. Chem., 276, 6689, 10.1074/jbc.M008127200 Hughes, 1997, Suppression of integrin activation: a novel function of a Ras/Raf-initiated MAP kinase pathway, Cell, 88, 521, 10.1016/S0092-8674(00)81892-9 Huynh-Do, 1999, Surface densities of ephrin-B1 determine EphB1-coupled activation of cell attachment through alphaVbeta3 and alfa5beta1 integrins, EMBO J., 18, 2165, 10.1093/emboj/18.8.2165 Imondi, 2000, Complementary expression of transmembrane ephrins and their receptors in the mouse spinal cord: a possible role in constraining the orientation of longitudinally projecting axons, Development, 127, 1397, 10.1242/dev.127.7.1397 Irie, 2002, EphB receptors regulate dendritic spine development via intersectin, Cdc42 and N-WASP, Nat. Neurosci., 5, 1117, 10.1038/nn964 Jurney, 2002, Rac1-mediated endocytosis during ephrin-A2- and semaphorin 3A-induced growth cone collapse, J. Neurosci., 22, 6019, 10.1523/JNEUROSCI.22-14-06019.2002 Kalo, 2001, In vivo tyrosine phosphorylation sites of activated ephrin-B1 and ephB2 from neural tissue, J. Biol. Chem., 276, 38940, 10.1074/jbc.M105815200 Katso, 1999, Functional analysis of H-Ryk, an atypical member of the receptor tyrosine kinase family, Mol. Cell. Biol., 19, 6427, 10.1128/MCB.19.9.6427 Kim, 1999, A role of actin filament in synaptic transmission and long-term potentiation, J. Neurosci., 19, 4314, 10.1523/JNEUROSCI.19-11-04314.1999 Knoll, 2001, A role for the EphA family in the topographic targeting of vomeronasal axons, Development, 128, 895, 10.1242/dev.128.6.895 Kong, 2001, An evolutionarily conserved transmembrane protein that is a novel downstream target of neurotrophin and ephrin receptors, J. Neurosci., 21, 176, 10.1523/JNEUROSCI.21-01-00176.2001 Kozlosky, 1997, LERK-7: a ligand of the Eph-related kinases is developmentally regulated in the brain, Cytokine, 9, 540, 10.1006/cyto.1997.0199 Krull, 1997, Interactions of Eph-related receptors and ligands confer rostrocaudal pattern to trunk neural crest migration, Curr. Biol., 7, 571, 10.1016/S0960-9822(06)00256-9 Labrador, 1997, The N-terminal globular domain of Eph receptors is sufficient for ligand binding and receptor signalling, EMBO J., 16, 3889, 10.1093/emboj/16.13.3889 Lackmann, 1997, Ligand for EPH-related kinase (LERK) 7 is the preferred high affinity ligand for the HEK receptor, J. Biol. Chem., 27, 16521, 10.1074/jbc.272.26.16521 Lackmann, 1998, Distinct subdomains of the EphA3 receptor mediate ligand binding and receptor dimerization, J. Biol. Chem., 273, 20228, 10.1074/jbc.273.32.20228 Lai, 2001, Expression of Eph receptors in skeletal muscle and their localization at the neuromuscular junction, Mol. Cell. Neurosci., 17, 1034, 10.1006/mcne.2001.0997 Lehmann, 1999, Inactivation of Rho signaling pathway promotes CNS axon regeneration, J. Neurosci., 19, 7537, 10.1523/JNEUROSCI.19-17-07537.1999 Liebl, 2003, mRNA expression of ephrins and Eph receptor tyrosine kinases in the neonatal and adult mouse central nervous system, J. Neurosci. Res., 71, 7, 10.1002/jnr.10457 Linke, 1995, Development of the hippocamposeptal projection in the rat, J. Comp. Neurol., 351, 602, 10.1002/cne.903510409 Lu, 2001, Ephrin-B reverse signaling is mediated by a novel PDZ-RGS protein and selectively inhibits G protein-coupled chemoattraction, Cell, 105, 69, 10.1016/S0092-8674(01)00297-5 Mackarehtschian, 1999, Regional differences in the developing cerebral cortex revealed by ephrin-A5 expression, Cereb. Cortex, 9, 601, 10.1093/cercor/9.6.601 Mann, 2002, Ephrins regulate the formation of terminal axonal arbors during the development of thalamocortical projections, Development, 129, 3945, 10.1242/dev.129.16.3945 Mann, 2002, Topographic mapping in dorsoventral axis of the Xenopus retinotectal system depends on signaling through ephrin-B ligands, Neuron, 35, 461, 10.1016/S0896-6273(02)00786-9 Marcus, 1996, Eph family receptors and their ligands distribute in opposing gradients in the developing mouse retina, Dev. Biol., 180, 786, 10.1006/dbio.1996.0347 Marin, 2001, Differential expression of Eph receptors and ephrins correlates with the formation of topographic projections in primary and secondary visual circuits of the embryonic chick forebrain, Dev. Biol., 234, 289, 10.1006/dbio.2001.0268 Marshall, 1995, Specificity of receptor tyrosine kinase signaling: transient versus sustained extracellular signal-regulated kinase activation, Cell, 80, 179, 10.1016/0092-8674(95)90401-8 A. Martínez, R. Otal, B.A. Sieber, C. Ibañez, E. Soriano, Disruption of Ephrin-A/EphA binding alters synaptogenesis and neural connectivity in the hippocampus (In progress). Martone, 1997, Immunolocalization of the receptor tyrosine kinase EphA4 in the adult rat central nervous system, Brain Res., 771, 238, 10.1016/S0006-8993(97)00792-0 McLaughlin, 2003, Bifunctional action of ephrin-B1 as a repellent and attractant to control bidirectional branch extension in dorsal–ventral retinotopic mapping, Development, 130, 2407, 10.1242/dev.00467 Meima, 1997, AL-1-induced growth cone collapse of rat cortical neurons is correlated with REK7 expression and rearrangement of the actin cytoskeleton, Eur. J. Neurosci., 9, 177, 10.1111/j.1460-9568.1997.tb01365.x Mellitzer, 1999, Eph receptors and ephrins restrict cell intermingling and communication, Nature, 400, 77, 10.1038/21907 Menzel, 2001, Ephrin-A6, a new ligand for EphA receptors in the developing visual system, Dev. Biol., 230, 74, 10.1006/dbio.2000.0109 Monschau, 1997, Shared and distinct functions of RAGS and ELF-1 in guiding retinal axons, EMBO J., 16, 1258, 10.1093/emboj/16.6.1258 Moreno-Flores, 1999, Up-regulation of Eph tyrosine kinase receptors after excitotoxic injury in adult hippocampus, Neuroscience, 91, 193, 10.1016/S0306-4522(98)00568-5 Mori, 1995, Differential expressions of the eph family of receptor tyrosine kinase genes (sek, elk, eck) in the developing nervous system of the mouse, Brain Res., Mol. Brain Res., 29, 325, 10.1016/0169-328X(94)00263-E Morris, 1982, Place navigation impaired in rats with hippocampal lesions, Nature, 297, 681, 10.1038/297681a0 Murai, 2003, Control of hippocampal dendritic spine morphology through ephrin-A3/EphA4 signaling, Nat. Neurosci., 6, 153, 10.1038/nn994 Nakamoto, 1996, Topographically specific effects of ELF-1 on retinal axon guidance in vitro and retinal axon mapping in vivo, Cell, 86, 755, 10.1016/S0092-8674(00)80150-6 Nieto, 1992, A receptor protein tyrosine kinase implicated in the segmental patterning of the hindbrain and mesoderm, Development, 116, 1137, 10.1242/dev.116.4.1137 Orioli, 1996, Sek4 and Nuk receptors cooperate in guidance of commissural axons and in palate formation, EMBO J., 15, 6035, 10.1002/j.1460-2075.1996.tb00992.x R. Otal, J. Frisén, E. Soriano, A. Martínez, Ephrin-A5 modulates the topographic mapping and connectivity of commissural axons in murine hippocampus (Submitted for publication). Palmer, 2002, EphrinB phosphorylation and reverse signaling: regulation by Src kinases and PTP-BL phosphatase, Mol. Cell, 9, 725, 10.1016/S1097-2765(02)00488-4 Park, 1997, Aberrant axonal projections in mice lacking EphA8 (Eek) tyrosine protein kinase receptors, EMBO J., 16, 3106, 10.1093/emboj/16.11.3106 Pasquale, 1992, Cek5, a membrane receptor-type tyrosine kinase, is in neurons of the embryonic and postnatal avian brain, J. Neurosci., 12, 3956, 10.1523/JNEUROSCI.12-10-03956.1992 Penzes, 2003, Rapid induction of dendritic spine morphogenesis by trans-synaptic ephrinB-EphB receptor activation of the Rho-GEF kalirin, Neuron, 37, 263, 10.1016/S0896-6273(02)01168-6 Pozas, 2001, Age-dependent effects of secreted Semaphorins 3A, 3F, and 3E on developing hippocampal axons: in vitro effects and phenotype of Semaphorin 3A (−/−) mice, Mol. Cell. Neurosci., 18, 26, 10.1006/mcne.2001.0999 Rickmann, 1985, The migration of neural crest cells and the growth of motor axons through the rostral half of the chick somite, J. Embryol. Exp. Morphol., 90, 437 Roskies, 1994, Control of topographic retinal axon branching by inhibitory membrane-bound molecules, Science, 265, 799, 10.1126/science.8047886 Sasaki, 2003, ephA9, a novel avian receptor tyrosine kinase gene, Gene, 316, 103, 10.1016/S0378-1119(03)00743-1 Schmidt, 2001, Regulation of EphA4 expression in paraxial and lateral plate mesoderm by ectoderm-derived signals, Dev. Dyn., 220, 377, 10.1002/dvdy.1117 Sefton, 1997, Novel expression gradients of Eph-like receptor tyrosine kinases in the developing chick retina, Dev. Biol., 188, 363, 10.1006/dbio.1997.8638 Shamah, 2001, EphA receptors regulate growth cone dynamics through the novel guanine nucleotide exchange factor ephexin, Cell, 105, 233, 10.1016/S0092-8674(01)00314-2 Shi, 1995, Abl-interactor-1, a novel SH3 protein binding to the carboxy-terminal portion of the Abl protein, suppresses v-abl transforming activity, Genes Dev., 9, 2583, 10.1101/gad.9.21.2583 Smith, 1997, The EphA4 and EphB1 receptor tyrosine kinases and ephrin-B2 ligand regulate targeted migration of branchial neural crest cells, Curr. Biol., 7, 561, 10.1016/S0960-9822(06)00255-7 Soans, 1994, Characterization of the expression of the Cek8 receptor-type tyrosine kinase during development and in tumor cell lines, Oncogene, 9, 3353 Song, 2002, Solution structure and backbone dynamics of the functional cytoplasmic subdomain of human ephrin B2, a cell-surface ligand with bidirectional signaling properties, Biochemistry, 41, 10942, 10.1021/bi025815u Sperry, 1963, Chemoaffinity in the orderly growth of nerve fiber patterns and connections, Proc. Natl. Acad. Sci. U. S. A., 50, 703, 10.1073/pnas.50.4.703 Stein, 1999, A role for the Eph ligand ephrin-A3 in entorhino-hippocampal axon targeting, J. Neurosci., 19, 8885, 10.1523/JNEUROSCI.19-20-08885.1999 Steup, 1999, Semaphorin D acts as a repulsive factor for entorhinal and hippocampal neurons, Eur. J. Neurosci., 11, 729, 10.1046/j.1460-9568.1999.00517.x Steup, 2000, Sema3C and netrin-1 differentially affect axon growth in the hippocampal formation, Mol. Cell. Neurosci., 15, 141, 10.1006/mcne.1999.0818 Supèr, 1994, The organization of the embryonic and early postnatal murine hippocampus: II. Development of entorhinal, commissural, and septal connections studied with the lipophilic tracer DiI, J. Comp. Neurol., 344, 101, 10.1002/cne.903440108 Supèr, 1998, Involvement of distinct pioneer neurons in the formation of layer-specific connections in the hippocampus, J. Neurosci., 18, 4616, 10.1523/JNEUROSCI.18-12-04616.1998 Takasu, 2002, Modulation of NMDA receptor-dependent calcium influx and gene expression through EphB receptors, Science, 295, 491, 10.1126/science.1065983 Tanaka, 2004, Tiam1 mediates neurite outgrowth induced by ephrin-B1 and EphA2, EMBO J., 23, 1075, 10.1038/sj.emboj.7600128 Taylor, 1994, Expression and developmental regulation of Ehk-1, a neuronal Elk-like receptor tyrosine kinase in brain, Neuroscience, 63, 163, 10.1016/0306-4522(94)90014-0 Torres, 1998, PDZ proteins bind, cluster, and synaptically colocalize with Eph receptors and their ephrin ligands, Neuron, 21, 1453, 10.1016/S0896-6273(00)80663-7 Toth, 2001, Crystal structure of an ephrin ectodomain, Dev. Cell, 1, 83, 10.1016/S1534-5807(01)00002-8 Tuzi, 1994, Eph, the largest known family of putative growth factor receptors, Br. J. Cancer, 69, 417, 10.1038/bjc.1994.77 Vanderhaeghen, 2000, A mapping label required for normal scale of body representation in the cortex, Nat. Neurosci., 3, 358, 10.1038/73929 Wahl, 2000, Ephrin-A5 induces collapse of growth cones by activating Rho and Rho kinase, J. Cell Biol., 149, 263, 10.1083/jcb.149.2.263 Wang, 1997, Eph family transmembrane ligands can mediate repulsive guidance of trunk neural crest migration and motor axon outgrowth, Neuron, 18, 383, 10.1016/S0896-6273(00)81240-4 Wang, 1999, Multiple ephrins control cell organization in C. elegans using kinase-dependent and -independent functions of the VAB-1 Eph receptor, Mol. Cell, 4, 903, 10.1016/S1097-2765(00)80220-8 Wimmer-Kleikamp, 2004, Recruitment of Eph receptors into signaling clusters does not require ephrin contact, J. Cell Biol., 164, 661, 10.1083/jcb.200312001 Winslow, 1995, Cloning of AL-1, a ligand for an Eph-related tyrosine kinase receptor involved in axon bundle formation, Neuron, 14, 973, 10.1016/0896-6273(95)90335-6 Xu, 1995, Expression of truncated Sek-1 receptor tyrosine kinase disrupts the segmental restriction of gene expression in the Xenopus and zebrafish hindbrain, Development, 121, 4005, 10.1242/dev.121.12.4005 Xu, 1999, In vivo cell sorting in complementary segmental domains mediated by Eph receptors and ephrins, Nature, 399, 267, 10.1038/20452 Xu, 2003, Ephrin-B1 reverse signaling activates JNK through a novel mechanism that is independent of tyrosine phosphorylation, J. Biol. Chem., 278, 24767, 10.1074/jbc.M302454200 Yu, 1997, NMDA channel regulation by channel-associated protein tyrosine kinase Src, Science, 275, 674, 10.1126/science.275.5300.674 Yu, 2001, Multiple signaling interactions of Abl and Arg kinases with the EphB2 receptor, Oncogene, 20, 3995, 10.1038/sj.onc.1204524 Yue, 2002, Mistargeting hippocampal axons by expression of a truncated Eph receptor, Proc. Natl. Acad. Sci. U. S. A., 99, 10777, 10.1073/pnas.162354599 Yun, 2003, EphA family gene expression in the developing mouse neocortex: regional patterns reveal intrinsic programs and extrinsic influence, J. Comp. Neurol., 456, 203, 10.1002/cne.10498 Zhang, 2002, Developmentally regulated changes in cellular compartmentation and synaptic distribution of actin in hippocampal neurons, J. Neurosci. Res., 69, 427, 10.1002/jnr.10313 Zhang, 1996, Detection of ligands in regions anatomically connected to neurons expressing the Eph receptor Bsk: potential roles in neuron–target interaction, J. Neurosci., 16, 7182, 10.1523/JNEUROSCI.16-22-07182.1996 Zhang, 1997, Dynamic expression suggests multiple roles of the eph family receptor brain-specific kinase (Bsk) during mouse neurogenesis, Brain Res., Mol. Brain Res., 47, 202, 10.1016/S0169-328X(97)00051-X Zhou, 1997, Regulation of topographic projection by the Eph family receptor Bsk (EphA5) and its ligands, Cell Tissue Res., 290, 251, 10.1007/s004410050929 Zhou, 1994, Isolation and characterization of Bsk, a growth factor receptor-like tyrosine kinase associated with the limbic system, J. Neurosci. Res., 37, 129, 10.1002/jnr.490370117