The Eph family: A multitude of receptors that mediate cell recognition signals

Cell and Tissue Research

Volumn 290, Issue 2, 1997, Pages 217-226

  Zisch, Andreas H ^a   Pasquale, Elena B ^a  

^a BURNHAM INSTITUTE   (United States)

Author keywords

Axon pathfinding; L1; Neural development; Receptor tyrosine kinase; Src family kinases

Indexed keywords

CELL RECEPTOR; NERVE CELL ADHESION MOLECULE; PROTEIN TYROSINE KINASE;

ARTICLE; CELL ADHESION; CYTOSKELETON; EMBRYO DEVELOPMENT; LIGAND BINDING; NERVE FIBER GROWTH; NEURITE; PRIORITY JOURNAL; RECEPTOR GENE; SIGNAL TRANSDUCTION;

ANIMALS; CELL COMMUNICATION; HUMANS; NEURONS; RECEPTOR PROTEIN-TYROSINE KINASES; SIGNAL TRANSDUCTION;

EID: 0030807905     PISSN: 0302766X     EISSN: None     Source Type: Journal    
DOI: 10.1007/s004410050926     Document Type: Article

References (95)

1. Bartley TD et al (1994) Receptor affinity techniques: identification of a ligand for the ECK receptor protein-tyrosine kinase. Nature 368:558-560
2. Becker N et al. (1994) Several receptor tyrosine kinase genes of the Eph family are segmentally expressed in the developing hindbrain. Mech Dev 47:3-17
3. Bergemann AD, Cheng H-J, Brambilla R, Klein R, Flanagan JG (1995) ELF-2, a new member of the Eph ligand family, is segmentally expressed in mouse embryos in the region of the hindbrain and newly formed somites. Mol Cell Biol 15:4921-4929
4. Bixby JL, Jhabvala P (1993) Tyrosine phosphorylation in early embryonic growth cones. J Neurosci 13:3421-3432
5. Bohme B, Vanden Bos T, Cerretti DP, Park LS, Holtrich U, Ruebsamen-Waigmann H, Strebhardt K (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 271:24747-24752
6. Brambilla R, Schnapp A, Casagranda F, Labrador JP, Bergemann AD, Flanagan JG, Pasqualle EB, Klein R (1995) Membrane-bound LERK2 ligand can signal through three different Eph-related receptor lyrosine kinases. EMBO J 14:3116-3126
7. Brückner K, Pasquale EB, Klein R (1997) Tyrosine phosphorylation of transmembrane ligands for Eph receptors suggest a role for the ligands in signal transduction. Science: 1640-1643
8. Cervello M, Lemmon V, Landreth G, Rutishauser U (1991) Phosphorylation-dependent regulation of axon fasciculation. Proc Natl Acad Sci 88: 10548-10552
9. Cheng H-J, Flanagan JG (1994) Identification and cloning of ELF-1, a developmentally expressed ligand for the Mek4 and Sek receptor tyrosine kinases. Cell 79:157-168
10. Cheng H-J, Nakamoto M, Bergemann AD, Flanagan JG (1995) Complementary gradients in expression and binding of ELF-1 and Mek4 in development of the topographic retinotectal projection map. Cell 82:371-381
11. Ciossek T, Millauer B, Ullrich A (1995) Identification of alternatively spliced mRNAs encoding variants of MDK1, a novel receptor tyrosine kinase expressed in the murine nervous system. Oncogene 9:97-108
12. Connor RJ, Pasquale EB (1995) Genomic organization and alternatively processed forms of Cek5, a receptor protein-tyrosine kinase of the Eph family. Oncogene 11:2429-2438
13. Davis JQ, Bennett V (1994) Ankyrin-binding activity shared by the neurofascin/L1/NrCAM family of nervous system cell adhesion molecules. J Biol Chem 262:27163-27166
14. Doherty P, Walsh FS (1996) CAM-FGF receptor interactions: a model for axonal growth. Mol Cell Neurosci 8:99-111
15. Drescher U, Kremoser C, Handwerker C, Löschinger J, Noda M, Bonhoeffer F (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 82:359-370
16. Drscher U, Bonhoeffer F, Mueller BK (1997) The Eph family in retinal axon guidance. Curr Opin Neurobiol 7:75-80
17. Ellis C, Kasmi F, Ganju P, Walls E Panayotou G, Reith AD (1996) A juxtamembrane autophosphorylation site in the Eph family receptor tyrosine kinase, Sek, mediates high affinity interaction with p59fyn. Oncogene 12:1727-1736
18. Eph Nomenclature Committee (1997) Unified nomenclature for Eph family receptors and their ligands, the ephrins. Cell 90:403-404
19. Fields S, Song O (1989) A novel genetic system to detect protein-protein interactions. Nature 340:245-246
20. Fischer G, Kuenemund V, Schachner M (1986) Neunte outgrowth patterns in cerebellar microexplant cultures are affected by antibodies to the cell surface glycoprotein L1. J Neurosci 6:605-612
21. Flenniken AM, Gale NW, Yancopoulos GD, Wilkinson DG (1996) Distinct and overlapping expression patterns of ligands for Eph-related receptor tyrosine kinases during mouse embryogenesis. Dev Biol 179:382-401
22. Friedmann GC, O'Leary DDM (1996) Eph receptor tyrosine kinases and their ligands in neural development. Curr Opin Neurobiol 6:127-133
23. c-src in developing cerebellum. Mol Cell Biol 5:27-32
24. Gale NW, Holland SJ, Valenzuela DM, Flenniken A, Pan L, Ryan TE, Henkemeyer M, Strebhardt K, Hirai HS, Wilkinson DG, Pawson T, Davis S, Yancopoulos GD (1996a) Eph receptors and ligands comprise two major specificity subclasses and are reciprocally compartmentalized during embryogenesis. Neuron 17:9-19
25. Gale NW, Flenniken A, Compton DC, Jenkins N, Copeland NG, Gilbert DJ, Davis S, Wilkinson DG, Yancopoulos GD (1996b) Elk-L3, a novel transmembrane ligand for the Eph family of receptor tyrosine kinases, expressed in embryonic floor plate, roof plate and hindbrain segments. Oncogene 13:1343-1352
26. Gilardi-Hebenstreit P, Nieto MA, Frain M, Mattei M-G, Chestier A, Wilkinson DG, Charnay P (1992) An Eph-related receptor protein tyrosine kinase segmentally expressed in the developing mouse hindbrain. Oncogene 7:2499-2506
27. Gurniak CB, Berg LJ (1996) A new member of the Eph family of receptors that lacks protein tyrosine kinase activity. Oncogene 13:777-786
28. Hall H, Walsh FS, Doherty P (1996) Review: a role for the FGF receptor in the axonal growth response stimulated by cell adhesion molecules? Cell Adhes Commun 3:441-450
29. Heiland PC, Hertlein B, Traub O, Griffith LS, Schmitz B (1996) The neural cell adhesion molecule L1 is phosphorylated on tyrosine and serine residues. Neuroreport 7:2675-2678
30. Henkemeyer M, Marengere LEM, McGlade J, Olivier JP, Conlon RA, Holmyard DP, Letwin K, Pawson T (1994) Immunolocalization of the Nuk receptor tyrosine kinase suggests roles in segmental patterning of the brain and axonogenesis. Oncogene 9:1001-1014
31. Henkemeyer M, Orioli D, Henderson JT, Saxton TM, Roder J, Pawson T, Klein R (1996) Nuk controls pathfinding of commissural axons in the mammalian central nervous system. Cell 86:35-46
32. Hlavin M, Lemmon V (1991) Molecular and functional testing of human L1 CAM: an interspecies comparison. Genomics 11:416-423
33. Holash JA, Pasquale EB (1995) Polarized expression of the receptor protein-tyrosine kinase Cek5 in the developing avian visual system. Dev Biol 172:683-693
34. Holash JA, Soans C, Chong LD, Shao H, Dixit VM, Pasquale EB (1997) Reciprocal expression of the Eph receptor Cek5 and its ligand(s) in the early retina. Dev Biol 182:256-269
35. Holland SJ, Gale NW, Mbamalu G, Yancopoulos GD, Henkemeyer M, Pawson T (1996) Bidirectional signaling through the EPH-family receptor Nuk and its transmembrane ligands. Nature 383:722-725
36. Ignelzi MA, Miller DR, Soriano P, Maness PF (1994) Impaired neurite outgrowth of src-minus cerebellar neurons on the cell adhesion molecule L1. Neuron 12:873-884
37. Ingraham CA, Cooke MP, Chuang Y-N, Perlmutter RM, Maness PF (1992) Cell type and development regulation of the fyn protooncogene in neural retina. Oncogene 7:95-100
38. Janmey PA, Stossel TP (1989) Gelsolin-polyphosphoinositide interaction. J Biol Chem 264:4825-4831
39. Jouet M, Rosenthal A, Armstrong G, MacFarlane J, Stevenson R, Paterson J, Metzenberg A, Ionasescu V, Temple K, Kenwrick S (1994) X-linked spastic paraplegia (SPG 1). MASA syndrome and X-linked hydrocephalus result from mutations in the L1 gene. Nat Genet 7:402-407
40. Kuhn TB, Stoeckli ET, Condrau MA, Rathjen FG, Sonderegger P (1991) Neunte outgrowth on immobilised axonin-1 is mediated by heterophilic interaction with L1(G4). J Cell Biol 115:113-1126
41. Kunz S, Ziegler U, Kunz B, Sonderegger P (1996) Intracellular signaling is changed after clustering of the neural cell adhesion molecules axonin-1 and Ng-CAM during neurite fasciculation. J Cell Biol 135:253-267
42. Lhotak V, Pawson T (1993) Biological and biochemical activities of a chimeric epidermal growth factor-Elk receptor tyrosine kinase. Mol Cell Biol 13:7071-7079
43. Lindner J, Rathjen FG, Schachner M (1983) L1 mono- and polyclonal antibodies modify cell migration in early postnatal mouse cerebellum. Nature 305:427-430
44. Magal E, Holash JA, Toso RJ, Chang D, Lindberg RA, Pasquale EB (1996) B61, a ligand for the Eck receptor protein-tyrosine kinase, exhibits neurotrophic activity in cultures of rat spinal cord neurons. J Neurosci Res 43:735-744
45. Maisonpierre PC, Barrezuta NX, Yancopoulos GD (1993) Ehk-1 and Ehk-2: two novel members of the Eph receptor-like tyrosine kinase family with distinctive structures and neuronal expression. Oncogene 8:3277-3288
46. 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 (in press)
47. Maru Y, Hirai H, Yoshida MC, Takaku F (1988) Evolution, expression, and chromosomal location of a novel receptor tyrosine kinase gene, eph. Mol Cell Biol 8:3770-3776
48. Monschau B, etal (1997) Shared and unique functions of RAGS and ELF-1 in guiding retinal axons. EMBO J 6:1258-1267
49. Nakamoto M, Cheng H-J, Friedman GC, McLaughlin T, Hansen MJ, Yoon CH, O'Leary DDM, Flanagan JG (1996) Topographically specific effects of ELF-1 on retinal axon guidance in vitro and retinal axon mapping in vivo. Cell 86:755-766
50. O'Bryan JP, Frye RA, Cogswell PC, Neubauer A, Kitch B, Prokop C, Espinosa R, LeBeau MM, Earp HS, Liu ET (1991) axl, a transforming gene isolated from primary human myeloid leukemia cells, encodes a novel receptor tyrosine kinase. Mol Cell Biol 11:5016-5031
51. Ohta K, Nakamura M, Hirokawa K, Tanaka S, Iwama A, Suda T, Ando M, Tanaka H (1996) The receptor tyrosine kinase, Cek8, is transiently expressed on subtypes of motoneurons in the spinal cord during development. Mech Dev 54:59-69
52. Ooi J, Yajnik V, Immanuel D, Gordon M, Moskow JJ, Buchberg AM, Margolis B (1995) The cloning of Grb10 reveals a new family of SH2 domains. Oncogene 10:1621-1630
53. 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 15:6035-6049
54. Pandey A, Lazar DF, Saltiel AR, Dixil VM (1994) Activation of the Eck-receptor protein tyrosine kinase stimulates phosphatidyl-inositol 3-kinase activity. J Biol Chem 269:30154-30157
55. Pandey A, Duan H, Dixit VM (1995a) Characterization of a novel Src-like adaptor protein that associates with the Eck receptor tyrosine kinase. J Biol Chem 270:19201-19204
56. Pandey A, Shao H, Marks RM, Polverini PJ, Dixit VM (1995b) Role of B61, the ligand for the Eck receptor tyrosine kinase, in TNF-α-induced angiogenesis. Science 268:567-569
57. Parsons JT, Parsons SJ (1997) Src family protein tyrosine kinases: cooperating with growth factor and adhesion signaling pathways. Curr Opin Cell Biol 9:187-192
58. Pasquale EB (1991) Identification of chicken embryo kinase 5, a developmentally regulated receptor-type tyrosine kinase of the Eph family. Cell Regul 2:523-534
59. Pasquale EB, Deenrick TJ, Singer SJ, Ellismann MH (1992) Cek5, a membrane receptor-type tyrosine kinase, is in neurons of the embryonic and postnatal avian brain. J Neurosci 12:3956-3967
60. Pasquale EB, Connor RJ, Rocholl D, Schnürch H, Risau W (1994) Cek5, a tyrosine kinase of the Eph subclass, is activated during neural retina differentiation. Dev Biol 163:491-502
61. Pawson T, Schlessinger J (1993) SH2 and SH3 domains. Curr Biol 3:434-442
62. Rose SPR (1995) Cell-adhesion molecules, glucocorticoids and long term-memory formation. Trends Neurosci 18:502-506
63. Rosenthal A, Jouet M, Kenwrick S (1992) Aberrant splicing of L1CAM mRNA associated with X-linked hydrocephalus. Nat Genet 2:107-112
64. Sadoul R, Kirchhoff F, Schachner M (1989) A protein kinase activity is associated with and specifically phosphorylates the neural cell adhesion molecule L1. J Neurochem 53:1471-1478
65. Sajjadi FG, Pasquale EB (1993) Five novel avian Eph-related tyrosine kinases are differentially expressed. Oncogene 8: 1807-1813
66. Sajjadi FG, Pasquale EB, Subramani S (1991) Identification of a new eph-related receptor tyrosine kinase gene from mouse and chicken that is developmentally regulated and encodes at least two forms of the receptor. New Biol 3:769-778
67. Salton SRJ, Shelanski ML, Greene LA (1983) Biochemical properties of the nerve growth factor inducible large external (NILE) glycoprotein. J Neurosci 3:2420-2430
68. Shao H, Lou L, Pandey A, Pasquale EB, Dixit VM (1994) cDNA cloning and characterization of a ligand for the Cek5 receptor protein-tyrosine kinase. J Biol Chem 269:26606-26609
69. Shao H, Lou L, Pandey A, Verderame MF, Siever DA, Dixit VM (1995) cDNA cloning and characterization of a EphA5 receptor protein tyrosine-kinase ligand that is identical to the ligand (ELF-1) for the Mek-4 and Sek receptor protein-tyrosine kinases. J Biol Chem 270:3467-3470
70. Siever DA, Verderame MF (1994) Identification of a complete Cek7 receptor protein tyrosine kinase coding sequence and cDNAs of alternatively spliced transcripts. Gene 148:219-226
71. Soans C, Holash JA, Pasquale EB (1994) Characterization of the expression of the Cek8 receptor-type tyrosine kinase during development and in tumor cell lines. Oncogene 9:3353-3361
72. Soans C, Holash JA, Pavlova Y, Pasquale EB (1996) Developmental expression and distinctive tyrosine phosphorylation of the Eph-related receptor tyrosine kinase, Cek9. J Cell Biol 135:781-795
73. c-src is developmentally regulated in the neural retina. Cell 36:249-257
74. Stallcup WB, Beasley L (1985) Involvement of the nerve growth factor-inducible large external glycoprotein (NILE) in neurite fasciculation in primary cultures of rat brain. Proc Natl Acad Sci USA 82:1276-1280
75. Stein E, Cerretti DP, Daniel TO (1996) Ligand activation of ELK receptor tyrosine kinase promotes its association with Grb10 and Grb2 in vascular endothelial cells. J Biol Chem 271:23588-23593
76. Superti-Furga G, Courtneidge SA (1995) Structure-function relationships in Src family and related protein tyrosine kinases. Bioessays 17:321-330
77. Taylor V, Micscher GC, Pfarr S, Honegger P, Breitschopf H, Lassmann H, Steck A (1994) Expression and developmental regulation of Ehk-1, a neuronal Elk-like receptor tyrosine kinase in brain. Neuroscience 63:163-178
78. Tessier-Lavigne M, Goodman C (1996) The molecular biology of axon guidance. Science 274:1123-1133
79. Valenzuela DM, Rojas E, Griffiths JA, Compton DL, Gisser M, Ip NY, Goldfarb M, Yancopoulos GD (1995) Identification of full-length and truncated forms of Ehk-3, a novel member of the Eph receptor tyrosine kinase family. Oncogene 10:1573-1580
80. Valius M, Kazlauskas A (1993) Phospholipase C-γl and phosphatidylinositol 3 kinase are the downstream mediators of the PDGF receptors's mitogenic signal. Cell 73:321-334
81. Van der Geer P, Hunter T, Lindberg RA (1994) Receptor protein-tyrosine kinases and their signal transduction pathways. Annu Rev Cell Biol 10:251-337
82. Vits L, Van Camp G, Coucke P, Fransen E, De Boulle K, Reyniers K, Korn B, Poustka A, Wilson G, Schrander-Stumpel C, Winter RM, Schwartz C, Willems PJ (1994) MASA syndrome is due to mutations in the neural cell adhesion gene L1CAM. Nat Genet 7:408-412
83. Wang HU, Anderson DJ (1997) Eph family transmembrane ligands can mediate repulsive guidance of trunk neural crest migration and motor axon outgrowth. Neuron 18:383-396
84. Wennström S, Siegbahn A, Yokote K, Arvidsson A-K, Heldin C-H, Mori S, Claesson-Welsh L (1994) Membrane ruffling and chemotaxis transduced by the PDGF β-receptor require the binding site for phosphatidylinositol 3′ kinase. Oncogene 9:651-660
85. Williams EJ, Doherty P, Turner G, Reid RA, Hemperly JJ, Walsh FS (1992) Calcium influx into neurons can solely account for cell contact-dependent neurite outgrowth stimulated by transfected L1. J Cell Biol 119:883-892
86. Williams EJ, Walsh FS, Doherty P (1994a) Tyrosine kinase inhibitors can differentially inhibit integrin-dependent and CAM-stimulated neurite outgrowth. J Cell Biol 124:1029-1037
87. Williams EJ, Furness J, Walsh FS, Doherty P (1994b) Activation of the FGF receptor underlies neurite outgrowth stimulated by L1, N-CAM, and N-cadherin. Neuron 13:583-594
88. Williams EJ, Furness J, Walsh FS, Doherty P (1994c) Characterisation of the second messenger pathway underlying neurite outgrowth stimulated by FGF. Development 120:1685-1693
89. Winslow JW, Moran P, Valverde J, Shih A, Yuan JQ, Wong SC, Tsai SP, Goddard A, Henzel WJ, Hefti F, Beck KD, Caras IW (1995) Cloning of AL-1, a ligand for an Eph-related tyrosine kinase receptor involved in axon bundle formation. Neuron 14:973-981
90. Wong E, Kenwrick S, Willems P, Lemmon V (1995) Mutations in the cell adhesion molecule L1 cause mental retardation. Trends Neurosci 18:168-172
91. rsk in neurite outgrowth mediated by the cell adhesion molecule L1. J Biol Chem 271:18217-18223
92. Wong EV, Schaefer AW, Landreth G, Lemmon V (1996b) Casein kinase 11 phosphorylates the neural cell adhesion molecule L1. J Ncuroehem 66:779-786
93. Xu Q, Alldus G, Holder N, Wilkinson DG (1995) Expression of truncated Sek-1 receptor disrupts the segmental restriction of gene expression in the Xenopus and zebrafish hindbrain. Development 121:4005-4016
94. Zhang J-H, Cerreti DP, Yu T, Flagan JG, Zhou R (1996) Detection of ligands in regions anatomically connected to neurons expressing the Eph receptor Bsk: potential roles in neuron-target interaction. J Neurosci 16:7182-7192
95. Zisch AH, Stallcup WB, Chong LD, Dahlin-Huppe K, Voshol J, Schachner M, Pasquale EB (1997) Tyrosine phosphorylation of L1 family adhesion molecules: implication of the Eph kinase Cek5. J Neurosci Res 47:655-665