The Eph family of receptors

Current Opinion in Cell Biology

Volumn 9, Issue 5, 1997, Pages 608-615

  Pasquale, Elena B ^a  

^a BURNHAM INSTITUTE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

LIGAND; PROTEIN TYROSINE KINASE;

CELL ADHESION; CELL MEMBRANE; CELL MOTION; GROWTH CONE; PRIORITY JOURNAL; REVIEW; SIGNAL TRANSDUCTION;

EID: 0030874979     PISSN: 09550674     EISSN: None     Source Type: Journal    
DOI: 10.1016/S0955-0674(97)80113-5     Document Type: Article

References (57)

1. Tessier-Lavigne M, Goodman CS: The molecular biology of axon guidance. Science 1996, 274:1123-1133.
2. Van der Geer P, Hunter T, Lindberg RA: Receptor protein-tyrosine kinases and their signal transduction pathways. Annu Rev Cell Biol 1994, 10:251-337.
3. Connor RJ, Pasquale EB: Genomic organization and alternatively processed forms of Cek5, a receptor protein-tyrosine kinase of the Eph subfamily. Oncogene 1995, 11:2429-2438.
4. Gurniak CB, Berg LJ: A new member of the Eph family of receptors that lacks protein tyrosine kinase activity. Oncogene 1996, 13:777-786.
5. Eph Nomenclature Committee: Flanagan JG, Gale NW, Hunter T, Pasquale EB, Tessier-Lavigne M: Unified nomenclature for Eph receptors and their ligands, the ephrins. Cell 1997, 90:403-404.
6. Davis S, Gale NW, Aldrich TH, Maisonpierre PC, Lhotak V, Pawson T, Goldfarb M, Yancopoulos GD: Ligands for EPH-related receptor tyrosine kinases that require membrane attachment or clustering for activity. Science 1994, 266:816-819.
7. Soans C, Holash JA, Pasquale EB: Characterization of the expression of the Cek8 receptor-type tyrosine kinase during development and in tumor cell lines. Oncogene 1994, 9:3353-3361.
8. Bartley TD, Hunt RW, Welcher AA, Boyle W, Parker VP, Lindberg RA, Lu HS, Colombero AM, Elliot RL, Guthrie BA et al.: Receptor affinity techniques: identification of a ligand for the ECK receptor protein-tyrosine kinase. Nature 1994, 368:558-560.
9. Sperry RW: Chemoaffinity in the orderly growth of nerve fiber patterns and connections. Proc Natl Acad Sci USA 1963, 50:703-710.
10. Walter J, Kem-Veits B, Huf J, Stolze B, Bonhoeffer F: Recognition of position-specific properties of tectal cell membranes by retinal axons in vitro. Development 1987, 101:685-696.
11. Cheng HJ, Nakamoto M, Bergemann AD, Flanagan JG: Complementary gradients in expression and binding of ELF-1 and Mek4 in development of the topographic retinotectal projection map. Cell 1995, 82:371-381.
12. Drescher U, Kremoser C, Handwerker C, Loschinger J, Noda M, Bonhoeffer F: 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.
13. Monschau B, Kremoser C, Ohta K, Tanaka H, Handwerked C, Hornberger MR, Loschinger J, Pasquale EB, Siever DA, Verderame MF et al.: Shared and distinct functions of RAGS and ELF-1 in guiding retinal axons. EMBO J 1997, 16:1258-1267.
14. Nakamoto M, Cheng HJ, Friedman GC, McLaughlin T, Hansen MJ, Yoon CH, O'Leary DD, Flanagan JG: Topographically specific effects of ELF-1 on retinal axon guidance in vitro and retinal axon mapping in vivo. Cell 1996, 86:755-766. The ability of the ligand ELF-1 to influence the trajectories in the optic tectum of retinal ganglion cell axons expressing the receptor Cek4 was demonstrated for the first time.
15. Keynes RJ, Stern CD: Segmentation in the vertebrate nervous system. Nature 1984, 310:413-429.
16. Gale NW, Holland SJ, Valenzuela DM, Flenniken A, Pan L, Ryan TE, Henkemeyer M, Strebhardt K, Hirai H, Wilkinson DG et al.: Eph receptors and ligands comprise two major specificity subclasses and are reciprocally compartmentalized during embryogenesis. Neuron 1996, 17:9-19. This was the first report to point out that the Eph receptors can be divided into two groups on the basis of sequence homologies and binding specificities for either transmembrane or glycosylphosphatidylinositol-linked ligands. The authors also show that expression patterns of receptors and their ligands are often complementary in the embryo.
17. Wang HU, Anderson DJ: Eph family transmembrane ligands can mediate repulsive guidance of trunk neural crest migration and motor axon outgrowth. Neuron 1997, 18:383-396. The authors of this paper are the first to indicate that the Eph family transmembrane ligands can mediate repulsive cell interactions. The authors describe the segmented expression of transmembrane ligands for Eph receptors in the caudal somite halves and show that, in vitro, these ligands can guide both spinal axons and trunk neural crest cells, both of which express receptors for these ligands.
18. Henkemeyer M, Marengere LE, McGlade J, Olivier JP, Conlon RA, Holmyard DP, Letwin K, Pawson T: Immunolocalization of the Nuk receptor tyrosine kinase suggests roles in segmental patterning of the brain and axonogenesis. Oncogene 1994, 9:1001-1014.
19. Krull CE, Lansford R, Gale NW, Collazo A, Marcelle C, Yancopoulos GD, Fraser SE, Bronner-Fraser M: Interactions of Eph-related receptors and ligands confer rostrocaudal pattern to trunk neural crest migration. Curr Biol 1997, 7:571-580. The authors are the first to demonstrate in vivo the functional significance of the asymmetric expression of transmembrane ligands for Eph receptors in the developing somites.
20. Smith A, Robinson V, Patel K, Wilkinson DG: The EphA4 and EphB1 receptor tyrosine kinases and ephrin-B2 ligand regulate the targeted migration of branchial neural crest cells. Curr Biol 1997, 7:561-570. The authors show that in vivo inhibition of Sek1 and Elk receptor function, or ectopic activation by overexpression of one of their ligands, Htk-L, disrupts the targeting of third arch crest cells in Xenopus embryos.
21. Xu Q, Alldus G, Holder N, Wilkinson DG: Expression of truncated Sek-1 receptor tyrosine kinase disrupts the segmental restriction of gene expression in the Xenopus and zebrafish hindbrain. Development 1995, 121:4005-4016.
22. Pasquale EB, Connor RJ, Rocholl D, Schnurch H, Risau W: Cek5, a tyrosine kinase of the Eph subclass, is activated during neural retina differentiation. Dev Biol 1994, 163:491-502.
23. Holash JA, Soans C, Chong LD, Shao H, Dixit VM, Pasquale EB: Reciprocal expression of the eph receptor Cek5 and its ligand(s) in the early retina. Dev Biol 1997, 182:256-269.
24. Soans C, Holash JA, Pavlova Y, Pasquale EB: Developmental expression and distinctive tyrosine phosphorylation of the Eph-related receptor tyrosine kinase Cek9. J Cell Biol 1996, 135:781-795.
25. Flenniken AM, Gale NW, Yancopoulos GD, Wilkinson DG: Distinct and overlapping expression patterns of ligands for Eph-related receptor tyrosine kinases during mouse embryogenesis. Dev Biol 1996, 179:382-401.
26. Donoghue MJ, Lewis RM, Merlie JP, Sanes JR: The Eph kinase ligand AL-1 is expressed by rostral muscles and inhibits outgrowth from caudal neurons. Mol Cell Neurosci 1996, 8:185-198.
27. Gao PP, Zhang JH, Yokoyama M, Racey B, Dreyfus CF, Black IB, Zhou R: Regulation of topographic projection in the brain: Elf-1 in the hippocamposeptal system. Proc Natl Acad Sci USA 1996, 93:11161-11166.
28. Winslow JW, Moran P, Valverde J, Shin A, Yuan JQ, Wong SC, Tsai SP, Goddard A, Henzel WJ, Hefti F et al.: Cloning of AL-1, a ligand for an Eph-related tyrosine kinase receptor involved in axon bundle formation. Neuron 1995, 14:973-981.
29. Winning RS, Scales JB, Sargent TD: Disruption of cell adhesion in Xenopus embryos by Pagliaccio, an Eph-class receptor tyrosine kinase. Dev Biol 1996, 179:309-319.
30. Zisch AH, Stallcup WB, Chong LD, Dahlin-Hippe K, Voshol J, Schachner M, Pasquale EB: Tyrosine phosphorylation of L1 family adhesion molecules: implication of the Eph kinase Cek5. J Neurosci Res 1997, 47:655-665.
31. Daniel TO, Stein E, Cerretti DP, St John PL, Robert B, Abrahamson DR: ELK and LERK-2 in developing kidney and microvascular endothelial assembly. Kidney Int 1996, Suppl 57:73-81.
32. Pandey A, Shao H, Marks RM, Polverini PJ, Dixit VM: Role of B61, the ligand for the Eck receptor tyrosine kinase, in TNF-alpha-induced angiogenesis. Science 1995, 268:567-569.
33. Heaysman JEM: Contact inhibition of locomotion: a reappraisal. Int Rev Cytol 1978, 55:49-66.
34. Meima L, Kljavin IJ, Moran P, Shih A, Winslow JW, Caras I: AL-1-induced growth cone collapse of rat cortical neurons is correlated with REK7 expression and rearrangement of the actin cytoskeleton. Eur J Neurosci 1997, 9:177-188.
35. Lhotak V, Pawson T: Biological and biochemical activities of a chimeric epidermal growth factor-Elk receptor tyrosine kinase. Mol Cell Biol 1993, 13:7071-7079.
36. Pandey A, Lazar DF, Saltiel AR, Dixit VM: Activation of the Eck receptor protein tyrosine kinase stimulates phosphatidylinositol 3-kinase activity. J Biol Chem 1994, 269:30154-30157.
37. Pandey A, Duan H, Dixit VM: Characterization of a novel Src-like adapter protein that associates with the Eck receptor tyrosine kinase. J Biol Chem 1995, 270:19201-19204.
38. Bixby JL, Jabvala P: Tyrosine phosphorylation in early embryonic growth cones. J Neurosci 1993, 13:3421-3432.
39. Brambilla R, Schnapp A, Casagranda F, Labrador JP, Bergemann AD, Flanagan JG, Pasquale EB, Klein R: Membrane-bound LERK2 ligand can signal through three different Eph-related receptor tyrosine kinases. EMBO J 1995, 14:3116-3126.
40. Brückner K, Pasquale EB, Klein R: Tyrosine phosphorylation of transmembrane ligands for Eph receptors. Science 1997, 275:1640-1643. This article reports that the cytoplasmic domain of the Eph receptor ligand Lerk2 inhibits tyrosine kinase signaling pathways in the ligand-bearing cells, suggesting a direct signaling function for this ligand.
41. Holland SJ, Gale NW, Mbamalu G, Yancopoulos GD, Henkemeyer M, Pawson T: Bidirectional signalling through the EPH-family receptor Nuk and its transmembrane ligands. Nature 1996, 383:722-725. This was the first report indicating that the transmembrane ligands for Eph receptors become tyrosine-phosphorylated as a consequence of interacting with the Eph receptors.
42. Henkemeyer M, Orioli D, Henderson JT, Saxton TM, Roder J, Pawson T, Klein R: Nuk controls pathfinding of commissural axons in the mammalian central nervous system. Cell 1996, 86:35-46. This is the first report of inactivation of an Eph receptor gene, the Nuk gene. Defects in the trajectories of anterior commissure neurons indicated a role for the Nuk receptor in axon pathfinding. Unexpectedly, Nuk was detected not in these axons but in the brain regions surrounding their pathway. It is a ligand for Nuk, Lerk2, that is present in the axons and which may respond to guidance cues provided by the Nuk extracellular domain.
43. Orioli D, Henkemeyer M, Lemke G, Klein R, Pawson T: Sek4 and Nuk receptors cooperate in guidance of commissural axons and in palate formation. EMBO J 1996, 15:6035-6049. This is the first report of the simultaneous inactivation of two Eph receptor genes, Nuk and Sek4. Defects in axon pathfinding and fasciculation and in palate formation were observed. Double mutant mice were more severely affected than would be expected from the phenotypes of single receptor mutants, indicating that the two Eph receptor genes have redundant functions during development. Both transmembrane ligands and their Eph receptors were found to be expressed in cortical neurons.
44. Inada T, Iwama A, Sakano S, Ohno M, Sawada K, Suda T: Selective expression of the receptor tyrosine kinase, HTK, on human erythroid progenitor cells. Blood 1997, 89:2757-2765.
45. Zhang JH, Cerretti DP, Yu T, Flanagan JG, Zhou R: Detection of ligands in regions anatomically connected to neurons expressing the Eph receptor Bsk: potential roles in neuron-target interaction. J Neurosci 1996, 16:7182-7192. This report indicates that Eph receptors and their ligands may specify topographic projections in various regions of the nervous system, in addition to in the visual system.
46. Ohta K, Nakamura M, Hirokawa K, Tanaka S, Iwama A, Suda T, Ando M, Tanaka H: The receptor tyrosine kinase, CekB, is transiently expressed on subtypes of motoneurons in the spinal cord during development Mech Dev 1996, 54:59-69.
47. Kilpatrick TJ, Brown A, Lai C, Gassmann M, Goulding M, Lemke G: Expression of the Tyro4/Mek4/Cek4 gene specifically marks a subset of embryonic motor neurons and their muscle targets. Mol Cell Neurosci 1996, 7:62-74.
48. Bergemann AD, Cheng HJ, Brambilla R, Klein R, Flanagan JG: ELF-2, a new member of the Eph ligand family, is segmentally expressed in mouse embryos in the region of the hindbrain and newly forming somites. Mol Cell Biol 1995, 15:4921-4929.
49. Gilardi-Hebenstreit P, Nieto MA, Frain M, Mattei MG, Chestier A, Wilkinson DG, Charnay P: An Eph-related receptor protein tyrosine kinase gene segmentally expressed in the developing mouse hindbrain. Oncogene 1992, 7:2499-2506. [Published erratum appears in Oncogene 1993, 8:1103.]
50. Gale NW, Flenniken A, Compton DC, Jenkins N, Copeland NG, Gilbert DJ, Davis S, Wilkinson DG, Yancopoulos GD: 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 1996, 13:1343-1352.
51. Cheng HJ, Flanagan JG: Identification and cloning of ELF-1, a developmentally expressed ligand for the Mek4 and Sek receptor tyrosine kinases. Cell 1994, 79:157-168.
52. Patel K, Nittenberg R, D'Souza D, Irving C, Burl D, Wilkinson DG, Tickle C: Expression and regulation of Cek-8, a cell to cell signalling receptor in developing chick limb buds. Development 1996, 122:1147-1155.
53. Holash JA, Pasquale EB: Polarized expression of the receptor protein tyrosine kinase Cek5 in the developing avian visual system. Dev Biol 1995, 172:683-693.
54. Marcus RC, Gale NW, Morrison ME, Mason CA, Yancopoulos GD: Eph family receptors and their ligands distribute in opposing gradients in the developing mouse retina. Dev Biol 1996, 180:786-789.
55. Stein E, Cerretti DP, Daniel TO: Ligand activation of ELK receptor tyrosine kinase promotes its association with GrblO and Grb2 in vascular endothelial cells. J Biol Chem 1996, 271:23588-23593.
56. Ellis C, Kasmi F, Ganju P, Walls E, Panayotou G, Reith AD: A juxtamembrane autophosphorylation site in the Eph family receptor tyrosine kinase, Sek, mediates high affinity interaction with p59fyn. Oncogene 1996, 12:1727-1736.
57. Holland SJ, Gale NW, Gish GD, Roth RA, Songyang Z, Cantley LC, Henkemeyer M, Yancopoulos GD, Pawson T: Juxtamembrane tyrosine residues couple the Eph family receptor EphB2/Nuk to specific SH2 domain proteins in neuronal cells. EMBO J 1997, 13:3877-3888.