Eph receptors and ephrin ligands in axon guidance

Advances in Experimental Medicine and Biology

Volumn 621, Issue , 2007, Pages 32-49

  Reber, Michael ^a   Hindges, Robert ^b   Lemke, Greg ^c  

^a CENTRE DE NEUROCHIMIE   (France)

^b KING'S COLLEGE LONDON   (United Kingdom)

^c SALK INSTITUTE FOR BIOLOGICAL STUDIES   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

EPHRIN; EPHRIN A1; EPHRIN A2; EPHRIN A3; EPHRIN A4; EPHRIN A5; EPHRIN A6; EPHRIN B1; EPHRIN B2; EPHRIN B3; EPHRIN RECEPTOR; EPHRIN RECEPTOR A1; EPHRIN RECEPTOR A2; EPHRIN RECEPTOR A3; EPHRIN RECEPTOR A4; EPHRIN RECEPTOR A5; EPHRIN RECEPTOR A6; EPHRIN RECEPTOR A7; EPHRIN RECEPTOR A8; EPHRIN RECEPTOR B1; EPHRIN RECEPTOR B2; EPHRIN RECEPTOR B3; EPHRIN RECEPTOR B4; EPHRIN RECEPTOR B5; EPHRIN RECEPTOR B6; PROTEIN TYROSINE KINASE; RAS PROTEIN; RHO GUANINE NUCLEOTIDE BINDING PROTEIN; TYROSINE KINASE RECEPTOR; UNCLASSIFIED DRUG; LIGAND;

ANGIOGENESIS; AUDITORY NERVOUS SYSTEM; AUDITORY SYSTEM; BRAIN CORTEX; BRAIN MAPPING; CELL FUNCTION; CELL MIGRATION; DENDRITIC SPINE; ENDOCYTOSIS; GENE INACTIVATION; GENE MAPPING; GENICULATE BODY; HUMAN; LATERAL GENICULATE BODY; LIGAND BINDING; MOTONEURON; NERVE CELL; NERVE FIBER; NERVE REGENERATION; NERVOUS SYSTEM DEVELOPMENT; NEURAL CREST CELL; NEUROMERE; NONHUMAN; OLFACTORY SYSTEM; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN CLEAVAGE; PROTEIN INTERACTION; PROTEIN LOCALIZATION; PROTEIN PHOSPHORYLATION; PROTEIN PROTEIN INTERACTION; PROTEIN STRUCTURE; PROTEOMICS; PYRAMIDAL TRACT; RECEPTOR BINDING; RETINOTECTAL PROJECTION; REVIEW; RHOMBENCEPHALON; SIGNAL TRANSDUCTION; SYNAPSE; THALAMUS; ANIMAL; CHEMISTRY; METABOLISM; MORPHOGENESIS; PHYSIOLOGY;

ANIMALS; AXONS; EPHRINS; HUMANS; LIGANDS; MORPHOGENESIS; RECEPTORS, EPH FAMILY; SIGNAL TRANSDUCTION;

EID: 40549085775     PISSN: 00652598     EISSN: None     Source Type: Book Series    
DOI: 10.1007/978-0-387-76715-4_3     Document Type: Review

References (138)

1. Flanagan JG, Vanderhaeghen P. The ephrins and Eph receptors in neural development. Annu Rev Neurosci 1998; 21:309-345.
2. Drescher U. Eph family functions from an evolutionary perspective. Curr Opin Genet Dev 2002; 12:397-402.
3. Dodelet Vc, Pasquale EB. Eph receptors and ephrin ligands: Embryogenesis to tumorigenesis. Oncogene 2000; 19:5614-5619.
4. Kullander K, Klein R. Mechanisms and functions of Eph and ephrin signalling. Nat Rev Mol Cell Biol 2002; 3:475-486.
5. Lemke G, Reber M. Retinotectal mapping: New insights from molecular genetics. Annu Rev Cell Dev Biol 2005; 21:551-580.
6. McLaughlin T, O'Leary DD. Molecular gradients and development of retinotopic maps. Annu Rev Neurosci 2005; 28:327-355.
7. Gale NW, Holland SJ, Valenzuela DM et al. Eph receptors and ligands comprise two major specificity subclasses and are reciprocally compartmentalized during embryogenesis. Neuron 1996; 17:9-19.
8. Himanen JP, Chumley MJ, Lackmann M et al. Repelling class discrimination: Ephrin-A5 binds to and activates EphB2 receptor signaling. Nat Neurosci 2004; 7:501-509.
9. Murai KK, Pasquale EB. 'Eph'ective signaling: Forward, reverse and crosstalk. J Cell Sci 2003; 116:2823-2832.
10. Koolpe M, Dail M, Pasquale EB. An ephrin mimetic peptide that selectively targets the EphA2 receptor. J Biol Chem 2002; 277:46974-46979.
11. Himanen JP, Nikolov DB. Eph signaling: A structural view. Trends Neurosci 2003; 26:46-51.
12. Himanen JP, Nikolov DB. Eph receptors and ephrins. Int J Biochem Cell Biol 2003; 35:130-134.
13. Day B, To C, Himanen JP et al. Three distinct molecular surfaces in ephrin-A5 are essential for a functional interaction with EphA3. J Biol Chem 2005; 280:26526-26532.
14. Egea J, Nissen UV, Dufour A et al. Regulation of EphA 4 kinase activity is required for a subset of axon guidance decisions suggesting a key role for receptor clustering in Eph function. Neuron 2005; 47:515-528.
15. Dickson BJ. Rho GTPases in growth cone guidance. Curr Opin Neurobiol 2001; 11:103-110.
16. Yuan XB, Jin M, Xu X et al. Signalling and crosstalk of Rho GTPases in mediating axon guidance. Nat Cell Biol 2003; 5:38-45.
17. Kozma R, Sarner S, Ahmed S et al. Rho family GTPases and neuronal growth cone remodelling: Relationship between increased complexity induced by Cdc42Hs, Rac1 , and acetylcholine and collapse induced by RhoA and lysophosphatidic acid. Mol Cell Biol 1997; 17:1201-1211.
18. Shamah SM, Lin MZ, Goldberg JL et al. EphA receptors regulate growth cone dynamics through the novel guanine nucleotide exchange factor ephexin. Cell 2001; 105:233-244.
19. Sahin M, Greer PL, Lin MZ et al. Eph-dependent tyrosine phosphorylation of ephexin1 modulates growth cone collapse. Neuron 2005; 46:191-204.
20. Cowan CW, Shao YR, Sahin M et al. Vav family GEFs link activated Ephs to endocytosis and axon guidance. Neuron 2005; 46:205-217.
21. Tanaka M, Ohashi R, Nakamura R et al. Tiam1 mediates neurite outgrowth induced by ephrin-B1 and EphA2. EMBO J 2004; 23:1075-1088.
22. Knöll B, Drescher U. Src family kinases are involved in EphA receptor-mediated retinal axon guidance. J Neurosci 2004; 24:6248-6257.
23. Jurney WM, Gallo G, Letourneau PC et al. Rac1-mediated endocytosis during ephrin-A2- and semaphorin 3A-induced growth cone collapse. J Neurosci 2002; 22:6019-6028.
24. Wahl S, Barth H, Ciossek T et al. Ephrin-A5 induces collapse of growth cones by activating Rho and Rho kinase. J Cell Biol 2000; 149:263-270.
25. Noren NK, Pasquale EB. Eph receptor-ephrin bidirectional signals that target Ras and Rho proteins. Cell Signal 2004; 16:655-666.
26. Miao H, Wei BR, Peehl DM et al. Activation of EphA receptor tyrosine kinase inhibits rhe Ras/MAPK pathway. Nat Cell Biol 2001; 3:527-530.
27. Marquardt T, Shirasaki R, Ghosh S et al. Coexpressed EphA receptors and ephrin-A ligands mediate opposing actions on growth cone navigarion from distinct membrane domains. Cell 2005; 121:127-139.
28. Davy A, Gale NW, Murray EW et al. Compartmentalized signaling by GPI-anchored ephrin-A5 requires the Fyn tyrosine kinase to regulate cellular adhesion. Genes Dev 1999; 13:3125-3135.
29. Davy A, Robbins SM. Ephrin-A5 modulates cell adhesion and morphology in an integrin-dependent manner. EMBO J 2000; 19:5396-5405.
30. Huai J, Drescher U. An ephrin-A-dependent signaling pathway controls integrin function and is linked to the tyrosine phosphorylation of a 120-kDa protein. J Biol Chem 2001; 276:6689-6694.
31. Connor RJ, Menzel P, Pasquale EB. Expression and tyrosine phosphorylation of Eph receptors suggesr multiple mechanisms in patterning of the visual system. Dev Biol 1998; 193:21-35.
32. Hornberger MR, Dütting D, Ciossek T et al. Modulation of EphA receptor function by coexpressed ephrinA ligands on retinal ganglion cell axons. Neuron 1999; 22:731-742.
33. Yin Y, Yamashita Y, Noda H et al. EphA receptor tyrosine kinases interact with coexpressed ephrin-A ligands in cis. Neurosci Res 2004; 48:285-296.
34. Carvalho RF, Beutler M, Marler KJ et al. Silencing of EphA3 through a cis interaction with ephrinA5. Nat Neurosci 2006; 9:322-330.
35. Hattori M, Osterfield M, Flanagan JG. Regulated cleavage of a contact-mediated axon repellent. Science 2000; 289:1360-1365.
36. Janes PW, Saha N, Barton WA et al. Adam meets Eph: An ADAM substrate recognition module acts as a molecular switch for ephrin cleavage in trans. Cell 2005; 123:291-304.
37. Penzes P, Beeser A, Chernoff J et al. Rapid induction of dendritic spine morphogenesis by trans-synaptic ephrinB-EphB receptor activation of the Rho-GEF kalirin. Neuron 2003; 37:263-274.
38. Irie F, Yamaguchi Y. EphB receptors regulate dendritic spine development via inrersectin, Cdc42 and N-WASP. Nat Neurosci 2002; 5:1117-1118.
39. Murai KK, Pasquale EB. Eph receptors, ephrins, and synaptic function. Neuroscientist 2004; 10:304-314.
40. Tong J, Elowe S, Nash P et al. Manipulation of EphB2 regulatory motifs and SH2 binding sites switches MAPK signaling and biological activity. J Biol Chem 2003; 278:6111-6119.
41. Zou JX, Wang B, Kalo MS et al. An Eph receptor regulates inregrin activity through R-Ras. Proc Natl Acad Sci USA 1999; 96:13813-13818.
42. Nagashima K, Endo A, Ogita H et al. Adaptor protein Crk is required for ephrin-B1-induced membrane ruffling and focal complex assembly of human aortic endothelial cells. Mol Biol Cell 2002; 13:4231-4242.
43. Stein E, Lane AA, Cerretti DP et al. Eph receptors discriminate specific ligand oligomers to determine alternative signaling complexes, attachment, and assembly responses. Genes Dev 1998; 12:667-678.
44. Becker E, Huynh-Do U, Holland S et al. Nck-interacting Ste20 kinase couples Eph receptors to c-Jun N-terminal kinase and integrin activation. Mol Cell Biol 2000; 20:1537-1545.
45. Stein E, Huynh-Do U, Lane AA et al. Nck recruitment to Eph receptor, EphB1/ELK, couples ligand activation to c-jun kinase. J Biol Chem 1998; 273:1303-1308.
46. Holland SJ, Gale NW, Mbamalu G et al. Bidirectional signalling through the EPH-family receptor Nuk and its transmembrane ligands. Nature 1996; 383:722-725.
47. Brückner K, Pasquale EB, Klein R. Tyrosine phosphorylation of transmembrane ligands for Eph receptors. Science 1997; 275:1640-1643.
48. Wilkinson DG. Multiple roles of EPH receptors and ephrins in neural developmenr. Nat Rev Neurosci 2001; 2:155-164.
49. Cowan CA, Henkemeyer M. The SH2/SH3 adaptor Grb4 transduces B-ephrin reverse signals. Nature 2001; 413:174-179.
50. Garrity PA, Rao Y, Salecker I et al. Drosophila photoreceptor axon guidance and targeting requires the dreadlocks SH2/SH3 adapter protein. Cell 1996; 85:639-650.
51. Cowan CA, Henkemeyer M. Ephrins in reverse, park and drive. Trends Cell Biol 2002; 12:339-346.
52. Lu Q, Sun EE, Klein RS et al. Ephrin-B reverse signaling is mediated by a novel PDZ-RGS protein and selectively inhibits G protein-coupled chemoattraction. Cell 2001; 105:69-79.
53. Xu Z, Lai KO, Zhou HM et al. Ephtin-B1 reverse signaling activates JNK through a novel mechanism that is independent of tyrosine phosphorylation. J Biol Chem 2003; 278:24767-24775.
54. Tanaka M, Kamo T, Ota S et al. Association of Dishevelled with Eph tyrosine kinase receptor and ephrin mediates cell repulsion. EMBO J 2003; 22:847-858.
55. Lee HS, Bong YS, Moore KB et al. Dishevelled mediates ephrinBl signalling in the eye field through the planar cell polarity pathway. Nat Cell Biol 2006; 8:55-63.
56. Zimmer M, Palmer A, Köhler J et al. EphB-ephrinB bi-directional endocytosis terminates adhesion allowing contact mediated repulsion. Nat Cell Biol 2003; 5:869-878.
57. Marston DJ, Dickinson S, Nobes CD. Rac-dependent trans-endocytosis of ephrinBs regulates Eph-ephrin contact repulsion. Nat Cell Biol 2003; 5:879-888.
58. Palmer A, Klein R. Multiple roles of ephrins in morphogenesis, neuronal networking, and brain function. Genes Dev 2003; 17:1429-1450.
59. Yamaguchi Y, Pasquale EB. Eph receptors in the adult brain. Curr Opin Neurobiol 2004; 14:288-296.
60. Cooke JE, Moens CB. Boundary formation in the hindbrain: Eph only it were simple. Trends Neurosci 2002; 25:260-267.
61. Mellitzer G, Xu Q, Wilkinson DG. Eph receptors and ephrins restrict cell intermingling and communication. Nature 1999; 400:77-81.
62. Cooke JE, Kemp HA, Moens CB. EphA4 is required for cell adhesion and rhombomere-boundary formation in the zebrafish. Curr Biol 2005; 15:536-542.
63. Cooke J, Moens C, Roth L et al. Eph signalling functions downstream of Val to regulate cell sorting and boundary formation in the caudal hindbrain. Development 2001; 128:571-580.
64. Dottori M, Hartley L, Galea M et al. EphA4 (Sek1) receptor tyrosine kinase is required for the development of the corticospinal tract. Proc Natl Acad Sci USA 1998; 95:13248-13253.
65. Kullander K, Croll SD, Zimmer M et al. Ephrin-B3 is the midline barrier that prevents corticospinal tract axons from recrossing, allowing for unilateral motor control. Genes Dev 2001; 15:877-888.
66. Kullander K, Mather NK, Diella F et al. Kinase-dependent and kinase-independent functions of EphA4 receptors in major axon tract formation in vivo. Neuron 2001; 29:73-84.
67. Nakagawa S, Brennan C, Johnson KG et al. Ephrin-B regulates the Ipsilateral routing of retinal axons at the optic chiasm. Neuron 2000; 25:599-610.
68. Williams SE, Mann F, Erskine L et al. Ephrin-B2 and EphB1 mediate retinal axon divergence at the optic chiasm. Neuron 2003; 39:919-935.
69. Pak W, Hindges R, Lim YS et al. Magnitude of binocular vision controlled by islet-2 repression of a genetic program that specifies laterality of retinal axon pathfinding. Cell 2004; 119:567-578.
70. Williams SE, Mason CA, Herrera E. The optic chiasm as a midline choice point. Curr Opin Neurobiol 2004; 14:51-60.
71. Henkemeyer M, Orioli D, Henderson JT et al. Nuk controls pathfinding of commissural axons in the mammalian central nervous system. Cell 1996; 86:35-46.
72. Orioli D, Henkemeyer M, Lemke G et al. Sek4 and Nuk receptors cooperate in guidance of commissural axons and in palate formation. EMBO J 1996; 15:6035-6049.
73. Hu Z, Yue X, Shi G et al. Corpus callosum deficiency in transgenic mice expressing a truncated ephrin-A receptor. J Neurosci 2003; 23:10963-10970.
74. Mendes SW, Henkemeyer M, Liebl DJ. Multiple Eph receptors and B-class ephrins regulate midline crossing of corpus callosum fibers in the developing mouse forebrain. J Neurosci 2006; 26:882-892.
75. Sperry RW. Chemoaffinity in the orderly growth of nerve fiber patterns and connections. Proc Natl Acad Sci USA 1963; 50:703-710.
76. Cheng HJ, Nakamoto M, Bergemann AD et al. Complementary gradients in expression and binding of ELF-l and Mek4 in development of the topographic retinotectal projection map. Cell 1995; 82:371-381.
77. Drescher U, Kremoser C, Handwerker C et al. In vitro guidance of retinal ganglion cell axons by RAGS, a 25 kDa tectal protein related to ligands for Eph receptor tyrosine kinases. Cell 1995; 82:359-370.
78. Feldheim DA, Kim YI, Bergemann AD et al. Genetic analysis of ephtin-A2 and ephrin-A5 shows their requirement in multiple aspects of retinocollicular mapping. Neuron 2000; 25:563-574.
79. Brown A, Yates PA, Burrola P et al. Topographic mapping from the retina to the midbrain is controlled by relative but not absolute levels of EphA receptor signaling. Cell 2000; 102:77-88.
80. Reber M, Burrola P, Lemke G. A relative signalling model for the formation of a topographic neural map. Nature 2004; 431:847-853.
81. Hansen MJ, Dallal GE, Flanagan JG. Retinal axon response to ephrin-as shows a graded, concentration-dependent transition from growth promotion to inhibition. Neuron 2004; 42:717-730.
82. Rashid T, Upton AL, Blentic A et al. Opposing gradients of ephrin-As and EphA7 in the superior colliculus are essential for topographic mapping in the mammalian visual system. Neuron 2005; 47:57-69.
83. Hindges R, McLaughlin T, Genoud N et al. EphB forward signaling controls directional branch extension and arborization required for dorsal-ventral retinotopic mapping. Neuron 2002: 35:475-487.
84. McLaughlin T, Hindges R, Yates PA et al. Bifunctional action of ephrin-B1 as a repellent and attractant to control bidirectional branch extension in dorsal-ventral retinotopic mapping. Development 2003; 130:2407-2418.
85. Mann F, Peuckert C, Dehner F et al. Ephrins regulate the formation of terminal axonal arbors during the development of thalamocortical ptojections. Development 2002; 129:3945-3955.
86. Brittis PA, Lu Q, Flanagan JG. Axonal protein synthesis provides a mechanism for localized regulation at an intermediate target. Cell 2002; 110:223-235.
87. Feldheim DA, Vanderhaeghen P, Hansen MJ et al. Topographic guidance labels in a sensory projection to the forebrain. Neuron 1998; 21:1303-1313.
88. Ellsworth CA, Lyckman AW, Feldheim DA et al. Ephrin-Az and -A5 influence patterning of normal and novel retinal projections to the thalamus: Conserved mapping mechanisms in visual and auditory thalamic targets. J Comp Neurol 2005; 488:140-151.
89. Pfeiffenberger C, Cutforth T, Woods G et al. Ephrin-As and neural activity are required for eye-specific patterning during retinogeniculate mapping. Nat Neurosci 2005; 8:1022-1027.
90. Huberman AD, Murray KD, Warland DK et al. Ephrin-As mediate targeting of eye-specific projections to the lateral geniculate nucleus. Nat Neurosci 2005; 8:1013-1021.
91. Bianchi LM, Gale NW. Distribution of Eph-related molecules in the developing and mature cochlea. Hear Res 1998; 117:161-172.
92. Nishida K, Flanagan JG, Nakamoto M. Domain-specific olivocerebellar projection regulated by the EphA-ephrin-A interaction. Development 2002; 129:5647-5658.
93. Lyckman AW, Jhaveri S, Feldheim DA et al. Enhanced plasticity of retinothalamic projections in an ephrin-AZ/A5 double mutant. J Neurosci 2001; 21:7684-7690.
94. Cramer KS. Eph proteins and the assembly of auditory circuits. Hear Res 2005; 206:42-51.
95. Bianchi LM, Gray NA. EphB receptors influence growth of ephrin-B1-positive statoacoustic nerve fibers. Eur J Neurosci 2002; 16:1499-1506.
96. Cowan CA, Yokoyama N, Bianchi LM et al. EphB2 guides axons at the midline and is necessary for normal vestibular function. Neuron 2000; 26:417-430.
97. Person AL, Cerretti DP, Pasquale EB et al. Tonotopic gradients of Eph family proteins in the chick nucleus laminaris during synaptogenesis. J Neurobiol 2004; 60:28-39.
98. Siddiqui SA, Cramer KS. Differential expression of Eph receptors and ephrins in the cochlear ganglion and eighth cranial nerve of the chick embryo. J Comp Neurol 2005; 482:309-319.
99. Brors D, Bodmer D, Pak K et al. EphA4 provides repulsive signals to developing cochlear ganglion neurites mediated through ephrin-B2 and -B3. J Comp Neurol 2003: 462:90-100.
100. St John JA, Pasquale EB, Key B. EphA receptors and ephrin-A ligands exhibit highly regulated spatial and temporal expression patterns in the developing olfactory system. Brain Res Dev Brain Res 2002: 138:1-14.
101. Cutforth T, Moring L, Mendelsohn M et al. Axonal ephrin-As and odorant receptors: Coordinate determination of the olfactory sensory map. Cell 2003; 114:311-322.
102. Knöll B, Zarbalis K, Wurst W et al. A role for the EphA family in the topographic targeting of vomeronasal axons. Development 2001; 128:895-906.
103. Vanderhaeghen P, Polleux F. Developmental mechanisms patterning thalamocortical projections: Intrinsic, extrinsic and in between. Trends Neurosci 2004; 27:384-391.
104. Dufour A, Seibt J, Passante L et al. Area specificity and topography of thalamocortical projections are controlled by ephrin/Eph genes. Neuron 2003; 39:453-465.
105. Torii M, Levitt P. Dissociation of corticothalamic and thalamocortical axon targeting by an EphA7-mediated mechanism. Neuron 2005: 48:563-575.
106. Cang J, Kaneko M, Yamada J et al. Ephrin-as guide the formation of functional maps in the visual cortex. Neuron 2005: 48:577-589.
107. Castellani V, Yue Y, Gao PP et al. Dual action of a ligand for Eph receptor tyrosine kinases on specific populations of axons during the development of cortical circuits. J Neurosci 1998; 18:4663-4672.
108. Bolz J, Uziel D, Mühlfriedel S et al. Multiple roles of ephrins during the formation of thalamocortical projections: Maps and more. J Neurobiol 2004; 59:82-94.
109. Takemoto M, Fukuda T, Sonoda R et al. Ephrin-B3-EphA4 interactions regulate the growth of specific thalamocortical axon populations in vitro. Eur J Neurosci 2002; 16:1168-1172.
110. Pfaff S, Kintner C. Neuronal diversification: Development of motor neuron subtypes. Curr Opin Neurobiol 1998; 8:27-36.
111. Helmbacher F. Schneider-Maunoury S, Topilko P et al. Targeting of the EphA4 tyrosine kinase receptor affects dorsal/ventral pathfinding of limb motor axons. Development 2000; 127:3313-3324.
112. Kania A. jessell TM. Topographic motor projections in the limb imposed by LIM homeodomain protein regulation of ephrin-A:EphA interactions. Neuron 2003; 38:581-596.
113. Eberhart J. Barr J. O'Connell S et al, Ephrin-A5 exerts positive or inhibitory effects on distinct subsets of EphA4-positive motor neurons. J Neurosci 2004; 24: 1070-1078.
114. Vaidya A, Pniak A, Lemke G et al. EphA3 null mutants do not demonstrate motor axon guidance defects. Mol Cell Biol 2003; 23:8092-8098.
115. Gerlai R, McNamara A. Anesthesia induced retrograde amnesia is ameliorated by ephrinA5 -IgG in mice: EphA receptor tyrosine kinases are involved in mammalian memory. Behav Brain Res 2000; 108:133-143.
116. Murai KK. Pasquale EB. Can Eph receptors stimulate the mind? Neuron 2002; 33:159-162.
117. Murai KK. Nguyen LN. Irie F et al. Control of hippocampal dendritic spine morphology through ephrin-A3/EphA4 signaling. Nat Neurosci 2003; 6:153-160.
118. Dalva MB. Takasu MA, Lin MZ et al. EphB receptors interact with NMDA receptors and regulate excitatory synapse formation. Cell 2000; 103:945-956.
119. Takasu MA, Dalva MB, Zigmond RE et al. Modulation of NMDA receptor-dependent calcium influx and gene expression through EphB receptors. Science 2002; 295:491-495.
120. Henkemeyer M, Itkis OS, Ngo M et al, Multiple EphB receptor tyrosine kinases shape dendritic spines in the hippocampus. J Cell Biol 2003; 163:1313-1326.
121. Ethell IM, Irie F. Kalo MS et al. EphB/syndecan-2 signaling in dendritic spine morphogenesis. Neuron 2001; 31:1001-1013.
122. Holmberg J. Armulik A, Senti KA et al. Ephrin-A2 reverse signaling negatively regulates neural progenitor proliferation and neurogenesis. Genes Dev 2005; 19:462-471.
123. Depaepe V, Suarez-Gonzalez N. Dufour A et al. Ephrin signalling controls brain size by regulating apoptosis of neural progenitors. Nature 2005; 435:1244-1250.
124. Koeberle PD, Bähr M. Growth and guidance cues for regenerating axons: Where have they gone? J Neurobiol 2004; 59:162-180.
125. Rodger J, Bartlett CA. Beazley LD et al. Transient upregulation of the rostrocaudal gradient of ephrin A2 in the tectum coincides with reestablishment of orderly projections during optic nerve regeneration in goldfish. Exp Neurol 2000; 166:196-200.
126. Symonds AC, Rodger J, Tan MM et al. Reinnervation of the superior colliculus delays down-regulation of ephrin A2 in neonatal rat. Exp Neurol 2001; 170:364-370.
127. Rodger J, Lindsey KA, Leaver SG et al. Expression of ephrin-A2 in the superior colliculus and EphA5 in the retina following optic nerve section in adult rat. Eur J Neurosci 2001; 14:1929-1936.
128. Rodger J, Vitale PN, Tee LB et al. EphA/ephrin-A interactions during optic nerve regeneration: Restoration of topography and regulation of ephrin-A2 expression . Mol Cell Neurosci 2004; 25:56-68.
129. Goldshmit Y, Galea MP, Wise G et al. Axonal regeneration and lack of astroeytic gliosis in EphA4-deficient mice. J Neurosci 2004; 24: 10064-10073.
130. Irizarry-Ramírez M, Willson CA, Cruz-Orengo L et al. Upregularion of EphA3 receptor after spinal cord injury. J Neurotrauma 2005; 22:929-935.
131. Klagsbrun M. Eichmann A. A role for axon guidance receptors and ligands in blood vessel development and tumor angiogenesis. Cytokine Growth Factor Rev 2005; 16:535-548.
132. Tammela T, Petrova TV. Alitalo K. Molecular lymphangiogenesis: New players. Trends Cell Biol 2005; 15:434-441.
133. Wu J, Luo H. Recent advances on T-cell regulation by receptor tyrosine kinases. Curr Opin Hematol 2005; 12:292-297.
134. Wimmer-Kleikamp SH. Lackmann M. Eph-rnodulared cell morphology. adhesion and motility in carcinogenesis. IUBMB Life 2005; 57:421-431.
135. Surawska H, Ma PC, Salgia R. The role of ephrins and Eph receptors in cancer. Cytokine Growth Factor Rev 2004; 15:419-433.
136. Negrete OA, Levroney EL, Aguilar HC et al. EphrinB2 is the entry receptor for Nipah virus, an emergent deadly paramyxovirus. Nature 2005; 436:401-405.
137. Negrete OA, Wolf MC, Aguilar HC et al. Two key residues in Ephrinb3 are critical for its use as an alternative receptor for Nipah virus. PLoS Pathog 2006; 2:e7.
138. Dravis C. Yokoyama N, Chumley MJ et al. Bidirectional signaling mediated by ephrin-B2 and EphB2 controls urorectal development. Dev Biol 2004; 271:272-290.