Disruption of ephrin-A/EphA binding alters synaptogenesis and neural connectivity in the hippocampus

Neuroscience

Volumn 135, Issue 2, 2005, Pages 451-461

  Martinez A ^a   Otal, R ^a   Sieber, B A ^b,c   Ibanez C ^c   Soriano, E ^a  

^a UNIVERSITY OF BARCELONA   (Spain)

^b NATIONAL INSTITUTE OF MENTAL HEALTH   (United States)

^c KAROLINSKA INSTITUTE   (Sweden)

Author keywords

Anterograde tracers; Calbindin; Hippocampal afferents; Mossy fibers; Transgenic mice

Indexed keywords

EPHRIN A1;

ANIMAL CELL; ARTICLE; BRAIN COMMISSURE; BRAIN REGION; CELL MATURATION; CONTROLLED STUDY; DENSITY; DENTATE GYRUS; ENTORHINAL CORTEX; GRANULE CELL; HIPPOCAMPUS; HUMAN; HUMAN CELL; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN DEGRADATION; PROTEIN EXPRESSION; PROTEIN PROTEIN INTERACTION; REDUCTION; SYNAPTIC TRANSMISSION; SYNAPTOGENESIS; TRANSGENIC MOUSE;

AGE FACTORS; ANIMALS; ANIMALS, NEWBORN; DENDRITES; EPHRINS; GENE EXPRESSION REGULATION, DEVELOPMENTAL; GLIAL FIBRILLARY ACIDIC PROTEIN; HIPPOCAMPUS; IMMUNOHISTOCHEMISTRY; MICE; MICE, TRANSGENIC; MICROSCOPY, ELECTRON, TRANSMISSION; NEURONS; PROTEIN BINDING; RECEPTOR, EPHA5; SYNAPSES;

EID: 24944552858     PISSN: 03064522     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.neuroscience.2005.06.052     Document Type: Article

References (68)

1. D.G. Amaral, J.A. Dent Development of the mossy fibers of the dentate gyrus: I. A light and electron microscopic study of the mossy fibers and their expansions J Comp Neurol 195 1981 51 86
2. A. Bagri, H.J. Cheng, A. Yaron, S.J. Pleasure, M. Tessier-Lavigne Stereotyped pruning of long hippocampal axon branches triggered by retraction inducers of the semaphorin family Cell 113 2003 285 299
3. M. Brenner Structure and transcriptional regulation of the GFAP gene Brain Pathol 4 1994 245 257
4. M. Brenner, A. Messing GFAP transgenic mice Methods 10 1996 351 364
5. H. Brownlee, P.P. Gao, J. Frisen, C. Dreyfus, R. Zhou, I.B. Black Multiple ephrins regulate hippocampal neurite outgrowth J Comp Neurol 425 2000 315 322
6. M. Buchert, S. Schneider, V. Meskenaite, M.T. Adams, E. Canaani, T. Baechi, K. Moelling, C.M. Hovens 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 1999 361 371
7. V. Castellani, Y. Yue, P.P. Gao, R. Zhou, J. Bolz Dual action of a ligand for Eph receptor tyrosine kinases on specific populations of axons during the development of cortical circuits J Neurosci 18 1998 4663 4672
8. H. Chen, A. Bagri, J.A. Zupicich, Y. Zou, E. Stoeckli, S.J. Pleasure, D.H. Lowenstein, W.C. Skarnes, A. Chedotal, M. Tessier-Lavigne Neuropilin-2 regulates the development of selective cranial and sensory nerves and hippocampal mossy fiber projections Neuron 25 2000 43 56
9. H.J. Cheng, M. Nakamoto, A.D. Bergemann, J.G. Flanagan Complementary gradients in expression and binding of ELF-1 and Mek4 in development of the topographic retinotectal projection map Cell 82 1995 371 381
10. H.J. Cheng, A. Bagri, A. Yaron, E. Stein, S.J. Pleasure, M. Tessier-Lavigne Plexin-A3 mediates semaphorin signaling and regulates the development of hippocampal axonal projections Neuron 32 2001 249 263
11. W.M. Cowan, B.B. Stanfield, K. Kishi The development of the dentate gyrus Curr Top Dev Biol 1 1980 103 157
12. T. Cutforth, L. Moring, M. Mendelsohn, A. Nemes, N.M. Shah, M.M. Kim, J. Frisen, R. Axel Axonal ephrin-As and odorant receptors coordinate determination of the olfactory sensory map Cell 114 2003 311 322
13. M.B. Dalva, M.A. Takasu, M.Z. Lin, S.M. Shamah, L. Hu, N.W. Gale, M.E. Greenberg EphB receptors interact with NMDA receptors and regulate excitatory synapse formation Cell 103 2000 945 956
14. S. Davis, N.W. Gale, T.H. Aldrich, P.C. Maisonpierre, V. Lhotak, T. Pawson, M. Goldfarb, G.D. Yancopoulos Ligands for EPH-related receptor tyrosine kinases that require membrane attachment or clustering for activity Science 266 1994 816 819
15. U. Drescher, C. Kremoser, C. Handwerker, J. Loschinger, M. Noda, F. Bonhoeffer 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 1995 359 370
16. A. Dufour, J. Seibt, L. Passante, V. Depaepe, T. Ciossek, J. Frisen, K. Kullander, J.G. Flanagan, F. Polleux, P. Vanderhaeghen Area specificity and topography of thalamocortical projections are controlled by ephrin/Eph genes Neuron 39 2003 453 465
17. J. Eberhart, J. Barr, S. O'Connell, A. Flagg, M.E. Swartz, K.S. Cramer, K.W. Tosney, E.B. Pasquale, C.E. Krull Ephrin-A5 exerts positive or inhibitory effects on distinct subsets of EphA4-positive motor neurons J Neurosci 24 2004 1070 1078
18. D.A. Feldheim, Y.I. Kim, A.D. Bergemann, J. Frisen, M. Barbacid, J.G. Flanagan Genetic analysis of ephrin-A2 and ephrin-A5 shows their requirement in multiple aspects of retinocollicular mapping Neuron 25 2000 563 574
19. D.A. Feldheim, M. Nakamoto, M. Osterfield, N.W. Gale, T.M. DeChiara, R. Rohatgi, G.D. Yancopoulos, J.G. Flanagan Loss-of-function analysis of EphA receptors in retinotectal mapping J Neurosci 24 2004 2542 2550
20. G. Feng, M.B. Laskowski, D.A. Feldheim, H. Wang, R. Lewis, J. Frisen, J.G. Flanagan, J.R. Sanes Roles for ephrins in positionally selective synaptogenesis between motor neurons and muscle fibers Neuron 25 2000 295 306
21. K.B.J. Franklin, G. Paxinos The mouse brain in stereotaxic coordinates 1997 Academic Press New York
22. J. Frisen, P.A. Yates, T. McLaughlin, G.C. Friedman, D.D. O'Leary, M. Barbacid Ephrin-A5 (AL-1/RAGS) is essential for proper retinal axon guidance and topographic mapping in the mammalian visual system Neuron 20 1998 235 243
23. N.W. Gale, S.J. Holland, D.M. Valenzuela, A. Flenniken, L. Pan, T.E. Ryan, M. Henkemeyer, K. Strebhardt, H. Hirai, D.G. Wilkinson, T. Pawson, S. Davis, G.D. Yancopoulos Eph receptors and ligands comprise two major specificity subclasses and are reciprocally compartmentalized during embryogenesis Neuron 17 1996 9 19
24. P.P. Gao, J.H. Zhang, M. Yokoyama, B. Racey, C.F. Dreyfus, I.B. Black, R. Zhou Regulation of topographic projection in the brain Elf-1 in the hippocamposeptal system Proc Natl Acad Sci U S A 93 1996 11161 11166
25. P.P. Gao, Y. Yue, J.H. Zhang, D.P. Cerretti, P. Levitt, R. Zhou 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 1998 5329 5334
26. W.Q. Gao, N. Shinsky, M.P. Armanini, P. Moran, J.L. Zheng, J.L. Mendoza-Ramirez, H.S. Phillips, J.W. Winslow, I.W. Caras Regulation of hippocampal synaptic plasticity by the tyrosine kinase receptor, REK7/EphA5, and its ligand, AL-1/Ephrin-A5 Mol Cell Neurosci 11 1998 247 259
27. P.P. Gao, Y. Yue, D.P. Cerretti, C. Dreyfus, R. Zhou Ephrin-dependent growth and pruning of hippocampal axons Proc Natl Acad Sci U S A 96 1999 4073 4077
28. R. Gerlai, N. Shinsky, A. Shih, P. Williams, J. Winer, M. Armanini, B. Cairns, J. Winslow, W. Gao, H.S. Phillips Regulation of learning by EphA receptors a protein targeting study J Neurosci 19 1999 9538 9549
29. R.J. Giger, J.F. Cloutier, A. Sahay, R.K. Prinjha, D.V. Levengood, S.E. Moore, S. Pickering, D. Simmons, S. Rastan, F.S. Walsh, A.L. Kolodkin, D.D. Ginty, M. Geppert Neuropilin-2 is required in vivo for selective axon guidance responses to secreted semaphorins Neuron 25 2000 29 41
30. M.J. Hansen, G.E. Dallal, J.G. Flanagan Retinal axon response to ephrin-as shows a graded, concentration-dependent transition from growth promotion to inhibition Neuron 42 2004 717 730
31. J. Holmberg, D.L. Clarke, J. Frisen Regulation of repulsion versus adhesion by different splice forms of an Eph receptor Nature 408 2000 203 206
32. J. Holmberg, J. Frisen Ephrins are not only unattractive Trends Neurosci 25 2002 239 243
33. W.M. Jurney, G. Gallo, P.C. Letourneau, S.C. McLoon Rac1-mediated endocytosis during ephrin-A2- and semaphorin 3A-induced growth cone collapse J Neurosci 22 2002 6019 6028
34. B. Knoll, K. Zarbalis, W. Wurst, U. Drescher A role for the EphA family in the topographic targeting of vomeronasal axons Development 128 2001 895 906
35. K. Kullander, R. Klein Mechanisms and functions of Eph and ephrin signalling Nat Rev Mol Cell Biol 3 2002 475 486
36. D.J. Liebl, C.J. Morris, M. Henkemeyer, L.F. Parada mRNA expression of ephrins and Eph receptor tyrosine kinases in the neonatal and adult mouse central nervous system J Neurosci Res 71 2003 7 22
37. K. Mackarehtschian, C.K. Lau, I. Caras, S.K. McConnell Regional differences in the developing cerebral cortex revealed by ephrin-A5 expression Cereb Cortex 9 1999 601 610
38. F. Mann, C. Peuckert, F. Dehner, R. Zhou, J. Bolz Ephrins regulate the formation of terminal axonal arbors during the development of thalamocortical projections Development 129 2002 3945 3955
39. R.C. Marcus, G.A. Matthews, N.W. Gale, G.D. Yancopoulos, C.A. Mason Axon guidance in the mouse optic chiasm retinal neurite inhibition by ephrin "A"-expressing hypothalamic cells in vitro Dev Biol 221 2000 132 147
40. M.E. Martone, J.A. Holash, A. Bayardo, E.B. Pasquale, M.H. Ellisman Immunolocalization of the receptor tyrosine kinase EphA4 in the adult rat central nervous system Brain Res 771 1997 238 250
41. L. Meima, I.J. Kljavin, P. Moran, A. Shih, J.W. Winslow, I.W. Caras 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 1997 177 188
42. P. Menzel, F. Valencia, P. Godement, V.C. Dodelet, E.B. Pasquale Ephrin-A6, a new ligand for EphA receptors in the developing visual system Dev Biol 230 2001 74 88
43. T. Mori, A. Wanaka, A. Taguchi, K. Matsumoto, M. Tohyama 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 1995 325 335
44. K.K. Murai, E.B. Pasquale Can Eph receptors stimulate the mind? Neuron 33 2002 159 162
45. K.K. Murai, L.N. Nguyen, F. Irie, Y. Yamaguchi, E.B. Pasquale Control of hippocampal dendritic spine morphology through ephrin-A3/EphA4 signaling Nat Neurosci 6 2003 153 160
46. B.N. Patel, D.L. Van Vactor Axon guidance the cytoplasmic tail Curr Opin Cell Biol 14 2002 221 229
47. M. Rickmann, D.G. Amaral, W.M. Cowan Organization of radial glial cells during the development of the rat dentate gyrus J Comp Neurol 264 1987 449 479
48. A. Sahay, M.E. Molliver, D.D. Ginty, A.L. Kolodkin Semaphorin 3F is critical for development of limbic system circuitry and is required in neurons for selective CNS axon guidance events J Neurosci 23 2003 6671 6680
49. T. Sakurai, E. Wong, U. Drescher, H. Tanaka, D.G. Jay Ephrin-A5 restricts topographically specific arborization in the chick retinotectal projection in vivo Proc Natl Acad Sci U S A 99 2002 10795 10800
50. B.A. Sieber, A. Kuzmin, J.M. Canals, A. Danielsson, G. Paratcha, E. Arenas, J. Alberch, S.O. Ogren, C.F. Ibanez Disruption of EphA/ephrin-a signaling in the nigrostriatal system reduces dopaminergic innervation and dissociates behavioral responses to amphetamine and cocaine Mol Cell Neurosci 26 2004 418 428
51. E. Stein, N.E. Savaskan, O. Ninnemann, R. Nitsch, R. Zhou, T. Skutella A role for the Eph ligand ephrin-A3 in entorhino-hippocampal axon targeting J Neurosci 19 1999 8885 8893
52. H. Supèr, E. Soriano 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 1994 101 120
53. H. Supèr, A. Martínez, J.A. Del Rio, E. Soriano Involvement of distinct pioneer neurons in the formation of layer-specific connections in the hippocampus J Neurosci 18 1998 4616 4626
54. M.A. Takasu, M.B. Dalva, R.E. Zigmond, M.E. Greenberg Modulation of NMDA receptor-dependent calcium influx and gene expression through EphB receptors Science 295 2002 491 495
55. V. Taylor, G.C. Miescher, S. Pfarr, P. Honegger, H. Breitschopf, H. Lassmann, A.J. Steck Expression and developmental regulation of Ehk-1, a neuronal Elk-like receptor tyrosine kinase in brain Neuroscience 63 1994 163 178
56. R. Torres, B.L. Firestein, H. Dong, J. Staudinger, E.N. Olson, R.L. Huganir, D.S. Bredt, N.W. Gale, G.D. Yancopoulos PDZ proteins bind, cluster, and synaptically colocalize with Eph receptors and their ephrin ligands Neuron 21 1998 1453 1463
57. D. Uziel, S. Muhlfriedel, K. Zarbalis, W. Wurst, P. Levitt, J. Bolz Miswiring of limbic thalamocortical projections in the absence of ephrin-A5 J Neurosci 22 2002 9352 9357
58. P. Vanderhaeghen, Q. Lu, N. Prakash, J. Frisen, C.A. Walsh, R.D. Frostig, J.G. Flanagan A mapping label required for normal scale of body representation in the cortex Nat Neurosci 3 2000 358 365
59. K.H. Weiss, C. Johanssen, A. Tielsch, J. Herz, T. Deller, M. Frotscher, E. Forster Malformation of the radial glial scaffold in the dentate gyrus of reeler mice, scrambler mice, and ApoER2/VLDLR-deficient mice J Comp Neurol 460 2003 56 65
60. J.W. Winslow, P. Moran, J. Valverde, A. Shih, J.Q. Yuan, S.C. Wong, S.P. Tsai, A. Goddard, W.J. Henzel, F. Hefti Cloning of AL-1, a ligand for an Eph-related tyrosine kinase receptor involved in axon bundle formation Neuron 14 1995 973 981
61. P.L. Woodhams, E. Basco, F. Hajos, A. Csillag, R. Balazs Radial glia in the developing mouse cerebral cortex and hippocampus Anat Embryol 163 1981 331 343
62. B. Xu, S. Li, A. Brown, R. Gerlai, M. Fahnestock, R.J. Racine EphA/ephrin-A interactions regulate epileptogenesis and activity-dependent axonal sprouting in adult rats Mol Cell Neurosci 24 2003 984 999
63. Y. Yue, Z.Y. Chen, N.W. Gale, J. Blair-Flynn, T.J. Hu, X. Yue, M. Cooper, D.P. Crockett, G.D. Yancopoulos, L. Tessarollo, R. Zhou Mistargeting hippocampal axons by expression of a truncated Eph receptor Proc Natl Acad Sci U S A 99 2002 10777 10782
64. M.E. Yun, R.R. Johnson, A. Antic, M.J. Donoghue EphA family gene expression in the developing mouse neocortex regional patterns reveal intrinsic programs and extrinsic influence J Comp Neurol 456 2003 203 216
65. J.H. Zhang, D.P. Cerretti, T. Yu, J.G. Flanagan, R. Zhou Detection of ligands in regions anatomically connected to neurons expressing the Eph receptor Bsk potential roles in neuron-target interaction J Neurosci 16 1996 7182 7192
66. J.H. Zhang, A.F. Pimenta, P. Levitt, R. Zhou Dynamic expression suggests multiple roles of the eph family receptor brain-specific kinase (Bsk) during mouse neurogenesis Brain Res Mol Brain Res 47 1997 202 214
67. R. Zhou, T.D. Copeland, L.F. Kromer, N.T. Schulz Isolation and characterization of Bsk, a growth factor receptor-like tyrosine kinase associated with the limbic system J Neurosci Res 37 1994 129 143
68. R. Zhou Regulation of topographic projection by the Eph family receptor Bsk (EphA5) and its ligands Cell Tissue Res 290 1997 251 259