Eph receptors, ephrins, and synaptic function

Neuroscientist

Volumn 10, Issue 4, 2004, Pages 304-314

  Murai, Keith K ^a   Pasquale, Elena B ^b,c  

^a MONTREAL GENERAL HOSPITAL   (Canada)

^b BURNHAM INSTITUTE   (United States)

^c UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

Dendritic spine; Neuropathologies; NMDA receptor; Plasticity; Tyrosine kinase

Indexed keywords

EPHRIN; EPHRIN RECEPTOR; LIGAND; N METHYL DEXTRO ASPARTIC ACID RECEPTOR; PROTEIN TYROSINE KINASE;

CELL CONTACT; CELL SURFACE; DENDRITIC SPINE; EXCITATION; GEOMETRY; HUMAN; MEMORY; MOLECULAR BIOLOGY; NERVE CELL PLASTICITY; NEUROPATHOLOGY; NONHUMAN; PRIORITY JOURNAL; REVIEW; SYNAPSE;

ANIMALS; CENTRAL NERVOUS SYSTEM; EPHRINS; HUMANS; NEURAL PATHWAYS; NEURONAL PLASTICITY; RECEPTOR AGGREGATION; RECEPTORS, EPH FAMILY; RECEPTORS, N-METHYL-D-ASPARTATE; SYNAPSES; SYNAPTIC TRANSMISSION;

EID: 3242781607     PISSN: 10738584     EISSN: None     Source Type: Journal    
DOI: 10.1177/1073858403262221     Document Type: Review

References (88)

1. Adams RH, Wilkinson GA, Weiss C, Diella F, Gale NW, Deutsch U, and others. 1999. Roles of ephrinB ligands and EphB receptors in cardiovascular development: demarcation of arterial/venous domains, vascular morphogenesis, and sprouting angiogenesis. Genes Dev 13:295-306.
2. Annunziata I, Lanzara C, Conte I, Zullo A, Ventruto V, Rinaldi MM, and others. 2003. Mapping of MRX81 in Xp11.2-Xq12 suggests the presence of a new gene involved in nonspecific X-linked mental retardation. Am J Med Genet 118A:217-22.
3. Bruckner K, Pablo Labrador J, Scheiffele P, Herb A, Seeburg PH, and Klein R. 1999. EphrinB ligands recruit GRIP family PDZ adaptor proteins into raft membrane microdomains. Neuron 22:511-24.
4. Buchert M, Schneider S, Meskenaite V, Adams MT, Canaani E, Baechi T, and others. 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 144:361-71.
5. Bundesen LQ, Scheel TA, Bregman BS, Kromer LF. 2003. Ephrin-B2 and EphB2 regulation of astrocyte-meningeal fibroblast interactions in response to spinal cord lesions in adult rats. J Neurosci 23:7789-800.
6. Chelly J, Mandel JL. 2001. Monogenic causes of X-linked mental retardation. Nat Rev Genet 2:669-80.
7. Choquet D, Triller A. 2003. The role of receptor diffusion in the organization of the postsynaptic membrane. Nat Rev Neurosci 4:251-65.
8. Ciossek T, Ullrich A, West E, Rogers JH. 1999. Segregation of the receptor EphA7 from its tyrosine kinase-negative isoform on neurons in adult mouse brain. Mol Brain Res 74:231-6.
9. Contractor A, Rogers C, Maron C, Henkemeyer M, Swanson GT, Heinemann SF. 2002. Trans-synaptic Eph receptor-ephrin signaling in hippocampal mossy fiber LTP. Science 296:1864-9.
10. Cowan CA, Henkemeyer M. 2001. The SH2/SH3 adaptor Grb4 transduces B-ephrin reverse signals. Nature 413:174-9.
11. Cowan WM, Kopnisky KL, Hyman SE. 2002. The human genome project and its impact on psychiatry. Annu Rev Neurosci 25:1-50.
12. Dalva MB, Takasu MA, Lin MZ, Shamah SM, Hu L, Gale NW, and others. 2000. EphB receptors interact with NMDA receptors and regulate excitatory synapse formation. Cell 103:945-56.
13. Davenport RW, Thies E, Zhou R, Nelson PG. 1998. Cellular localization of ephrin-A2, ephrin-A5, and other functional guidance cues underlies retinotopic development across species. J Neurosci 18:975-986.
14. Davy A, Gale NW, Murray EW, Klinghoffer RA, Soriano P, Feuerstein C, and others. 1999. Compartmentalized signaling by GPI-anchored ephrin-A5 requires the Fyn tyrosine kinase to regulate cellular adhesion. Genes Dev 13:3125-35.
15. Davy A, Robbins SM. 2000. Ephrin-A5 modulates cell adhesion and morphology in an integrin-dependent manner. EMBO J 19:5396-405.
16. Dunaevsky A, Blazeski R, Yuste R, Mason C. 2001. Spine motility with synaptic contact. Nat Neurosci 4:685-6.
17. Dunaevsky A, Tashiro A, Majewska A, Mason C, Yuste R. 1999. Developmental regulation of spine motility in the mammalian central nervous system. Proc Natl Acad Sci U S A 96:13438-43.
18. Ethell IM, Irie F, Kalo MS, Couchman JR, Pasquale EB, Yamaguchi Y. 2001. EphB/syndecan-2 signaling in dendritic spine morphogenesis. Neuron 31:1001-13.
19. Feldheim DA, Kim YI, Bergemann AD, Frisen J, Barbacid M, Flanagan JG. 2000. Genetic analysis of ephrin-A2 and ephrin-A5 shows their requirement in multiple aspects of retinocollicular mapping. Neuron 25:563-74.
20. Fiala JC, Feinberg M, Popov V, Harris KM. 1998. Synaptogenesis via dendritic filopodia in developing hippocampal area CA1. J Neurosci 18:8900-11.
21. Fiala JC, Spacek J, Harris KM. 2002. Dendritic spine pathology: cause or consequence of neurological disorders? Brain Res Brain Res Rev 39:29-54.
22. Fisher SE, DeFries JC. 2002. Developmental dyslexia: genetic dissection of a complex cognitive trait. Nat Rev Neurosci 3:767-80.
23. Fleischmann A, Hvalby O, Jensen V, Strekalova T, Zacher C, Layer LE, and others. 2003. Impaired long-term memory and NR2A-type NMDA receptor-dependent synaptic plasticity in mice lacking c-Fos in the CNS. J Neurosci 23:9116-22.
24. Gao WQ, Shinsky N, Armanini MP, Moran P, Zheng JL, Mendoza-Ramirez JL, and others. 1998. Regulation of hippocampal synaptic plasticity by the tyrosine kinase receptor, REK7/EphA5, and its ligand, AL-1/Ephrin-A5. Mol Cell Neurosci 11:247-59.
25. Gerlai R. 2001. Eph receptors and neural plasticity. Nat Rev Neurosci 2:205-9.
26. Gerlai R, McNamara A. 2000. Anesthesia induced retrograde amnesia is ameliorated by ephrinA5-IgG in mice: EphA receptor tyrosine kinases are involved in mammalian memory. Behav Brain Res 108:133-43.
27. Gerlai R, Shinsky N, Shih A, Williams P, Winer J, Armanini M, and others. 1999. Regulation of learning by EphA receptors: a protein targeting study. J Neurosci 19:9538-49.
28. Grigorenko EL, Wood FB, Meyer MS, Pauls JE, Hart LA, Pauls DL. 2001. Linkage studies suggest a possible locus for developmental dyslexia on chromosome 1p. Am J Med Genet 105:120-9.
29. Grunwald IC, Korte M, Wolfer D, Wilkinson GA, Unsicker K, Lipp HP, and others. 2001. Kinase-independent requirement of EphB2 receptors in hippocampal synaptic plasticity. Neuron 32:1027-40.
30. Halpain S. 2000. Actin and the agile spine: how and why do dendritic spines dance? Trends Neurosci 23:141-6.
31. Hattori M, Osterfield M, Flanagan JG. 2000. Regulated cleavage of a contact-mediated axon repellent. Science 289:1360-5.
32. Haydon PG. 2001. GLIA: listening and talking to the synapse. Nat Rev Neurosci 2:185-93.
33. Henderson JT, Georgiou J, Jia ZP, Robertson J, Elowe S, Roder JC, and others. 2001. The receptor tyrosine kinase EphB2 regulates NMDA-dependent synaptic function. Neuron 32:1041-56.
34. Hering H, Lin C-C, Sheng M. 2003. Lipid rafts in the maintenance of synapses, dendritic spines, and surface AMPA receptor stability, J Neurosci 23:3262-71.
35. Himanen JP, Rajashankar KR, Lackmann M, Cowan CA, Henkemeyer M, Nikolov DB. 2001. Crystal structure of an Eph receptor-ephrin complex. Nature 414:933-8.
36. Holmberg J, Clarke DL, Frisen J. 2000. Regulation of repulsion versus adhesion by different splice forms of an Eph receptor. Nature 408:203-6.
37. Irie F, Yamaguchi Y. 2002. EphB receptors regulate dendritic spine development via intersectin, Cdc42 and N-WASP. Nat Neurosci 5:1117-8.
38. Kaech S, Brinkhaus H, Matus A. 1999. Volatile anesthetics block actin-based motility in dendritic spines. Proc Natl Acad Sci U S A 96:10433-7.
39. Kalo MS, Pasquale EB. 1999. Multiple in vivo tyrosine phosphorylation sites in EphB receptors. Biochemistry 38:14396-408.
40. Kaufmann WE, Moser HW. 2000. Dendritic anomalies in disorders associated with mental retardation. Cereb Cortex 10:981-91.
41. Koolpe M, Dail M, Pasquale EB. 2002. An ephrin mimetic peptide that selectively targets the EphA2 receptor. J Biol Chem 277:46974-9.
42. Kullander K, Klein R. 2002. Mechanisms and functions of Eph and ephrin signalling. Nat Rev Mol Cell Biol 3:475-86.
43. Lackmann M, Oates AC, Dottori M, Smith FM, Do C, Power M, and others. 1998. Distinct subdomains of the EphA3 receptor mediate ligand binding and receptor dimerization. J Biol Chem 273:20228-37.
44. Lai KO, Ip FCF, Cheung J, Fu AKY, Ip NY. 2001. Expression of Eph receptors in skeletal muscle and their localization at the neuromuscular junction. Mol Cell Neurosci 17:1034-47.
45. Li Z, Sheng M. 2003. Some assembly required: the development of neuronal synapses. Nature Mol Cell Biol 4:833-41.
46. Liebl DJ, Morris CJ, Henkemeyer M, Parada LF. 2003. mRNA expression of ephrins and Eph receptor tyrosine kinases in the neonatal and adult mouse central nervous system. J Neurosci Res 71:7-22.
47. Lin D, Gish GD, Songyang Z, Pawson I. 1999. The carboxyl terminus of B class ephrins constitutes a PDZ domain binding motif. J Biol Chem 274:3726-33.
48. Malenka RC. 2003. Opinion: the long-term potential of LTP. Nat Rev Neurosci 4:923-6.
49. Mann F, Miranda E, Weinl C, Harmer E, Holt CE. 2003. B-type Eph receptors and ephrins induce growth cone collapse through distinct intracellular pathways. J Neurobiol 57:323-36.
50. Manning G, Whyte DB, Martinez R, Hunter T, Sudarsanam S. 2002. The protein kinase complement of the human genome. Science 298:1912-34.
51. Marston DJ, Dickinson S, Nobes CD. 2003. Rac-dependent transendocytosis of ephrinBs regulates Eph-ephrin contact repulsion. Nat Cell Biol 5:879-88.
52. Martone ME, Holash JA, Bayardo A, Pasquale EB, Ellisman MH. 1997. Immunolocalization of the receptor tyrosine kinase EphA4 in the adult rat central nervous system. Brain Res 771:238-50.
53. Matus A, Brinkhaus H, Wagner U. 2000. Actin dynamics in dendritic spines: a form of regulated plasticity at excitatory synapses. Hippocampus 10:555-60.
54. McLaughlin T, Hindges R, O'Leary DD. 2003. Regulation of axial patterning of the retina and its topographic mapping in the brain. Curr Opin Neurobiol 13:57-69.
55. Murai KK, Nguyen LN, Irie F, Yamaguchi Y, Pasquale EB. 2003. Control of hippocampal dendritic spine morphology through ephrin-A3/EphA4 signaling. Nat Neurosci 6:153-60.
56. Murai KK, Nguyen LN, Koolpe M, McLennan R, Krull CE, Pasquale EB. 2003. Targeting the EphA4 receptor in the nervous system with biologically active peptides. Mol Cell Neurosci 24: 1000-11.
57. Murai KK, Pasquale EB. 2003. "Eph"ective signaling: forward, reverse and crosstalk. J Cell Sci 116:2823-32.
58. Murthy VN, De Camilli P. 2003. Cell biology of the presynaptic terminal. Annu Rev Neurosci 26:701-28.
59. Nimchinsky EA, Sabatini BL, Svoboda K. 2002. Structure and function of dendritic spines. Annu Rev Physiol 64:313-53.
60. Noebels JL. 2003. The biology of epilepsy genes. Annu Rev Neurosci 26:599-625.
61. Noren NK, Pasquale EB. 2004. Eph receptor-ephrin bidirectional signals that target Ras and Rho proteins. Cell Signal. Forthcoming.
62. Orioli D, Henkemeyer M, Lemke G, Klein R, Pawson T. 1996. Sek4 and Nuk receptors cooperate in guidance of commissural axons and in palate formation. EMBO J 15:6035-49.
63. Palmer A, Klein R. 2003. Multiple roles of ephrins in morphogenesis, neuronal networking, and brain function. Genes Dev 17:1429-50.
64. Palmer A, Zimmer M, Erdmann KS, Eulenburg V, Porthin A, Heumann R, and others. 2002. EphrinB phosphorylation and reverse signaling: regulation by Src kinases and PTP-BL phosphatase. Mol Cell 9:725-37.
65. Penzes P, Beeser A, Chernoff J, Schiller MR, Eipper BA, Mains RE, and others. 2003. Rapid induction of dendritic spine morphogenesis by trans-synaptic ephrinB-EphB receptor activation of the Rho-GEF Kalirin. Neuron 37:263-74.
66. Ramakers GJ. 2002. Rho proteins, mental retardation and the cellular basis of cognition. Trends Neurosci 25:191-9.
67. Salter MW. 1998. Src, N-methyl-D-aspartate (NMDA) receptors, and synaptic plasticity. Biochem Pharmacol 56:789-98.
68. Schueler MG, Higgins AW, Nagaraja R, Tentler D, Dahl N, Gustashaw K, and others. 2000. Large-insert clone/STS contigs in Xq11-q12, spanning deletions in patients with androgen insensitivity and mental retardation. Genomics 66:104-9.
69. Shamah SM, Lin MZ, Goldberg JL, Estrach S, Sahin M, Hu L, and others. 2001. EphA receptors regulate growth cone dynamics through the novel guanine nucleotide exchange factor ephexin. Cell 105:233-44.
70. Shima DT, Mailhos C. 2000. Vascular developmental biology: getting nervous. Curr Opin Gen Dev 10:536-42.
71. Simons K, Toomre D. 2000. Lipid rafts and signal transduction. Nat Rev Mol Cell Biol 1:31-9.
72. Smalla M, Schmieder P, Kelly M, Ter Laak A, Krause G, Ball L, and others. 1999. Solution structure of the receptor tyrosine kinase EphB2 SAM domain and identification of two distinct homotypic interaction sites. Protein Sci 8:1954-61.
73. Stapleton D, Balan I, Pawson T, Sicheri F. 1999. The crystal structure of an Eph receptor SAM domain reveals a mechanism for modular dimerization. Nat Struct Biol 6:44-9.
74. Takasu MA, Dalva MB, Zigmond RE, Greenberg ME. 2002. Modulation of NMDA receptor-dependent calcium influx and gene expression through EphB receptors. Science 295:491-5.
75. Thanos CD, Goodwill KE, Bowie JU. 1999. Oligomeric structure of the human EphB2 receptor SAM domain. Science 283:833-6.
76. Torres R, Firestein BL, Dong H, Staudinger J, Olson EN, Huganir RL, and others. 1998. PDZ proteins bind, cluster, and synaptically colocalize with Eph receptors and their ephrin ligands. Neuron 21:1453-63.
77. Toth J, Cutforth T, Gelinas AD, Bethoney KA, Bard J, Harrison CJ. 2001. Crystal structure of an ephrin ectodomain. Dev Cell 1:83-92.
78. Trachtenberg JT, Chen BE, Knott GW, Feng G, Sanes JR, Welker E, and others. 2002. Long-term in vivo imaging of experience-dependent synaptic plasticity in adult cortex. Nature 420:788-94.
79. Weeber EJ, Sweatt JD. 2002. Molecular neurobiology of human cognition. Neuron 33:845-8.
80. Wilkinson DG. 2001. Multiple roles of Eph receptors and ephrins in neural development. Nat Rev Neurosci 2:155-64.
81. Winslow JW, Moran P, Valverde J, Shih A, Yuan JQ, Wong SC, and others. 1995. Cloning of AL-1, a ligand for an Eph-related tyrosine kinase receptor involved in axon bundle formation. Neuron 14:973-81.
82. Wu C, Butz S, Ying Y, and Anderson RG. 1997. Tyrosine kinase receptors concentrated in caveolae-like domains from neuronal plasma membrane. J Biol Chem 272:3554-9.
83. Wybenga-Groot LE, Baskin B, Ong SH, Tong JF, Pawson T, Sicheri F. 2001. Structural basis for autoinhibition of the EphB2 receptor tyrosine kinase by the unphosphorylated juxtamembrane region. Cell 106:745-7.
84. Yue Y, Chen Z-Y, Gale NW, Blair-Flynn J, Hu T-J, Yue X, and others. 2002. Mistargeting hippocampal axons by expression of a truncated Eph receptor. Proc Natl Acad U S A 99:10777-82.
85. Yun ME, Johnson RR, Antic A, Donoghue MJ. 2003. EphA family gene expression in the developing mouse neocortex: regional patterns reveal intrinsic programs and extrinsic influence. J Comp Neurol 456:203-16.
86. Yuste R, Bonhoeffer T. 2001. Morphological changes in dendritic spines associated with long-term synaptic plasticity. Annu Rev Neurosci 24:1071-89.
87. Zhang JH, Pimenta AF, Levitt P, Zhou R. 1997. Dynamic expression suggests multiple roles of the eph family receptor brain-specific kinase (Bsk) during mouse neurogenesis. Brain Res Mol Brain Res 47:202-14.
88. Zimmer M, Palmer A, Kohler J, Klein R. 2003. EphB-ephrinB bidirectional endocytosis terminates adhesion allowing contact mediated repulsion. Nat Cell Biol 5:869-78.