Home LiteratureArticle Details
PMID: 10611251 Published · ppublish English Journal Article Research Support, U.S. Gov't, P.H.S.

Fibroblast growth factor receptor-mediated rescue of x-ephrin B1-induced cell dissociation in Xenopus embryos.

Molecular and cellular biology ·Vol. 20 ·No. 2 ·2000-01-00 ·Pages 724-34

Chong LD, Park EK, Latimer E, Friesel R, Daar IO

Abstract

The Eph family of receptor tyrosine kinases and their membrane-bound ligands, the ephrins, have been implicated in regulating cell adhesion and migration during development by mediating cell-to-cell signaling events. Genetic evidence suggests that ephrins may transduce signals and become tyrosine phosphorylated during embryogenesis. However, the induction and functional significance of ephrin phosphorylation is not yet clear. Here, we report that when we used ectopically expressed proteins, we found that an activated fibroblast growth factor (FGF) receptor associated with and induced the phosphorylation of ephrin B1 on tyrosine. Moreover, this phosphorylation reduced the ability of overexpressed ephrin B1 to reduce cell adhesion. In addition, we identified a region in the cytoplasmic tail of ephrin B1 that is critical for interaction with the FGF receptor; we also report FGF-induced phosphorylation of ephrins in a neural tissue. This is the first demonstration of communication between the FGF receptor family and the Eph ligand family and implicates cross talk between these two cell surface molecules in regulating cell adhesion.

MeSH Terms
Amino Acid Sequence Animals Binding Sites Cell Adhesion/drug effects Chick Embryo Conserved Sequence Embryo, Nonmammalian/cytology,drug effects,metabolism Ephrin-B1 Fibroblast Growth Factors/pharmacology Gene Expression Membrane Proteins/chemistry,genetics,metabolism Mitogen-Activated Protein Kinases/metabolism Molecular Sequence Data Mutation/genetics Phosphorylation/drug effects Phosphotyrosine/metabolism Protein Binding Receptor Cross-Talk/drug effects Receptors, Fibroblast Growth Factor/genetics,metabolism Receptors, Platelet-Derived Growth Factor/physiology Retina/drug effects,embryology,metabolism Signal Transduction/drug effects Xenopus laevis/embryology
Chemicals
Ephrin-B1 Membrane Proteins Receptors, Fibroblast Growth Factor Phosphotyrosine Fibroblast Growth Factors Receptors, Platelet-Derived Growth Factor Mitogen-Activated Protein Kinases
Authors & Affiliations
5 authors, click to expand affiliations / ORCID
Chong L D
Basic Research Laboratory, National Cancer Institute, Frederick, Maryland 21702, USA.
Park E K
Latimer E
Friesel R
Daar I O
References (80)
80 references, click to expand
  1. Localization of MAP kinase activity in early Xenopus embryos: implications for endogenous FGF signaling.
    Dev Biol. 1997 Mar 1;183(1):9-20 PMID: 9119118
  2. Tyrosine phosphorylation of L1 family adhesion molecules: implication of the Eph kinase Cek5.
    J Neurosci Res. 1997 Mar 15;47(6):655-65 PMID: 9089215
  3. Identification of XLerk, an Eph family ligand regulated during mesoderm induction and neurogenesis in Xenopus laevis.
    Oncogene. 1997 May 8;14(18):2159-66 PMID: 9174051
  4. The N-terminal globular domain of Eph receptors is sufficient for ligand binding and receptor signaling.
    EMBO J. 1997 Jul 1;16(13):3889-97 PMID: 9233799
  5. The EphA4 and EphB1 receptor tyrosine kinases and ephrin-B2 ligand regulate targeted migration of branchial neural crest cells.
    Curr Biol. 1997 Aug 1;7(8):561-70 PMID: 9259557
  6. Interactions of Eph-related receptors and ligands confer rostrocaudal pattern to trunk neural crest migration.
    Curr Biol. 1997 Aug 1;7(8):571-80 PMID: 9259560
  7. The Eph family: a multitude of receptors that mediate cell recognition signals.
    Cell Tissue Res. 1997 Nov;290(2):217-26 PMID: 9321683
  8. Ephrins and their receptors: a repulsive topic?
    Cell Tissue Res. 1997 Nov;290(2):227-41 PMID: 9321684
  9. Multiple roles of Eph-like kinases and their ligands during development.
    Cell Tissue Res. 1997 Nov;290(2):243-50 PMID: 9321685
  10. CAMs and the FGF receptor: an interacting role in axonal growth.
    Cell Tissue Res. 1997 Nov;290(2):451-5 PMID: 9321709
  11. The Eph family of receptors.
    Curr Opin Cell Biol. 1997 Oct;9(5):608-15 PMID: 9330863
  12. Transplanted oligodendrocyte progenitor cells expressing a dominant-negative FGF receptor transgene fail to migrate in vivo.
    J Neurosci. 1997 Dec 1;17(23):9122-32 PMID: 9364059
  13. The Eph family in the patterning of neural development.
    Curr Biol. 1997 Dec 1;7(12):R799-807 PMID: 9382835
  14. Syntenin, a PDZ protein that binds syndecan cytoplasmic domains.
    Proc Natl Acad Sci U S A. 1997 Dec 9;94(25):13683-8 PMID: 9391086
  15. Loss of cell adhesion in Xenopus laevis embryos mediated by the cytoplasmic domain of XLerk, an erythropoietin-producing hepatocellular ligand.
    Proc Natl Acad Sci U S A. 1998 Jan 20;95(2):576-81 PMID: 9435234
  16. The VAB-1 Eph receptor tyrosine kinase functions in neural and epithelial morphogenesis in C. elegans.
    Cell. 1998 Mar 6;92(5):633-43 PMID: 9506518
  17. Topographically specific effects of ELF-1 on retinal axon guidance in vitro and retinal axon mapping in vivo.
    Cell. 1996 Sep 6;86(5):755-66 PMID: 8797822
  18. Ligand-independent activation of fibroblast growth factor receptors by point mutations in the extracellular, transmembrane, and kinase domains.
    J Biol Chem. 1996 Oct 4;271(40):25049-57 PMID: 8798788
  19. Regulation of topographic projection in the brain: Elf-1 in the hippocamposeptal system.
    Proc Natl Acad Sci U S A. 1996 Oct 1;93(20):11161-6 PMID: 8855326
  20. Bidirectional signalling through the EPH-family receptor Nuk and its transmembrane ligands.
    Nature. 1996 Oct 24;383(6602):722-5 PMID: 8878483
  21. The molecular biology of axon guidance.
    Science. 1996 Nov 15;274(5290):1123-33 PMID: 8895455
  22. Disruption of cell adhesion in Xenopus embryos by Pagliaccio, an Eph-class receptor tyrosine kinase.
    Dev Biol. 1996 Nov 1;179(2):309-19 PMID: 8903347
  23. Mesoderm induction in early Xenopus embryos by heparin-binding growth factors.
    Nature. 1987 Mar 12-18;326(6109):197-200 PMID: 3821895
  24. Synergistic induction of mesoderm by FGF and TGF-beta and the identification of an mRNA coding for FGF in the early Xenopus embryo.
    Cell. 1987 Dec 4;51(5):869-77 PMID: 3479265
  25. Expression of a novel FGF in the Xenopus embryo. A new candidate inducing factor for mesoderm formation and anteroposterior specification.
    Development. 1992 Mar;114(3):711-20 PMID: 1618138
  26. breathless, a Drosophila FGF receptor homolog, is essential for migration of tracheal and specific midline glial cells.
    Genes Dev. 1992 Sep;6(9):1668-78 PMID: 1325393
  27. Developmental expression of the Xenopus int-2 (FGF-3) gene: activation by mesodermal and neural induction.
    Development. 1992 Jul;115(3):695-702 PMID: 1425349
  28. Structural and functional diversity in the FGF receptor multigene family.
    Adv Cancer Res. 1993;60:1-41 PMID: 8417497
  29. Biochemical analysis of torso and D-raf during Drosophila embryogenesis: implications for terminal signal transduction.
    Mol Cell Biol. 1993 Feb;13(2):1163-72 PMID: 8423783
  30. FGF signalling in the early specification of mesoderm in Xenopus.
    Development. 1993 Jun;118(2):477-87 PMID: 8223274
  31. Adhesion molecules of the nervous system.
    Curr Opin Neurobiol. 1993 Oct;3(5):709-15 PMID: 8260819
  32. Eph receptors discriminate specific ligand oligomers to determine alternative signaling complexes, attachment, and assembly responses.
    Genes Dev. 1998 Mar 1;12(5):667-78 PMID: 9499402
  33. Axon guidance to and from choice points.
    Curr Opin Neurobiol. 1998 Feb;8(1):64-72 PMID: 9568393
  34. Adhesion and signaling in axonal fasciculation.
    Curr Opin Neurobiol. 1998 Feb;8(1):80-6 PMID: 9568395
  35. The Eph family receptors and ligands.
    Pharmacol Ther. 1998 Mar;77(3):151-81 PMID: 9576626
  36. Dual action of a ligand for Eph receptor tyrosine kinases on specific populations of axons during the development of cortical circuits.
    J Neurosci. 1998 Jun 15;18(12):4663-72 PMID: 9614241
  37. Molecular distinction and angiogenic interaction between embryonic arteries and veins revealed by ephrin-B2 and its receptor Eph-B4.
    Cell. 1998 May 29;93(5):741-53 PMID: 9630219
  38. Distinct subdomains of the EphA3 receptor mediate ligand binding and receptor dimerization.
    J Biol Chem. 1998 Aug 7;273(32):20228-37 PMID: 9685371
  39. Impaired cerebral cortex development and blood pressure regulation in FGF-2-deficient mice.
    EMBO J. 1998 Aug 3;17(15):4213-25 PMID: 9687490
  40. Eph signaling is required for segmentation and differentiation of the somites.
    Genes Dev. 1998 Oct 1;12(19):3096-109 PMID: 9765210
  41. Interaction of EphB2-tyrosine kinase receptor and its ligand conveys dorsalization signal in Xenopus laevis development.
    Oncogene. 1998 Sep 24;17(12):1509-16 PMID: 9794228
  42. DCC and netrins.
    Curr Opin Cell Biol. 1998 Oct;10(5):609-13 PMID: 9818171
  43. Requirement for EphA receptor signaling in the segregation of Xenopus third and fourth arch neural crest cells.
    Mech Dev. 1998 Nov;78(1-2):63-79 PMID: 9858686
  44. The carboxyl terminus of B class ephrins constitutes a PDZ domain binding motif.
    J Biol Chem. 1999 Feb 5;274(6):3726-33 PMID: 9920925
  45. Roles of ephrinB ligands and EphB receptors in cardiovascular development: demarcation of arterial/venous domains, vascular morphogenesis, and sprouting angiogenesis.
    Genes Dev. 1999 Feb 1;13(3):295-306 PMID: 9990854
  46. Eph receptors and ephrins restrict cell intermingling and communication.
    Nature. 1999 Jul 1;400(6739):77-81 PMID: 10403252
  47. PDGF signalling is required for gastrulation of Xenopus laevis.
    Development. 1995 Sep;121(9):3099-110 PMID: 7555734
  48. Functions of fibroblast growth factors and their receptors.
    Curr Biol. 1995 May 1;5(5):500-7 PMID: 7583099
  49. An FGF receptor signaling pathway is required for the normal cell migrations of the sex myoblasts in C. elegans hermaphrodites.
    Cell. 1995 Nov 17;83(4):611-20 PMID: 7585964
  50. Expression of truncated Sek-1 receptor tyrosine kinase disrupts the segmental restriction of gene expression in the Xenopus and zebrafish hindbrain.
    Development. 1995 Dec;121(12):4005-16 PMID: 8575301
  51. Receptor tyrosine phosphatases are required for motor axon guidance in the Drosophila embryo.
    Cell. 1996 Feb 23;84(4):599-609 PMID: 8598046
  52. The transmembrane tyrosine phosphatase DLAR controls motor axon guidance in Drosophila.
    Cell. 1996 Feb 23;84(4):611-22 PMID: 8598047
  53. Growth factors and neural connectivity.
    Genet Eng (N Y). 1996;18:33-47 PMID: 8785125
  54. Nuk controls pathfinding of commissural axons in the mammalian central nervous system.
    Cell. 1996 Jul 12;86(1):35-46 PMID: 8689685
  55. Eph receptors and ligands comprise two major specificity subclasses and are reciprocally compartmentalized during embryogenesis.
    Neuron. 1996 Jul;17(1):9-19 PMID: 8755474
  56. Inhibition of FGF receptor activity in retinal ganglion cell axons causes errors in target recognition.
    Neuron. 1996 Aug;17(2):245-54 PMID: 8780648
  57. The Eck receptor tyrosine kinase is implicated in pattern formation during gastrulation, hindbrain segmentation and limb development.
    Oncogene. 1994 Jun;9(6):1613-24 PMID: 8183555
  58. Basic fibroblast growth factor promotes adhesive interactions of neuroepithelial cells from chick neural tube with extracellular matrix proteins in culture.
    Development. 1993 Nov;119(3):943-56 PMID: 8187649
  59. Characterization of recombinant Xenopus MAP kinase kinases mutated at potential phosphorylation sites.
    Oncogene. 1994 Jul;9(7):1891-8 PMID: 8208535
  60. Association of fibroblast growth factor receptor-1 with c-Src correlates with association between c-Src and cortactin.
    J Biol Chem. 1994 Aug 12;269(32):20221-4 PMID: 7519605
  61. Characterization of the expression of the Cek8 receptor-type tyrosine kinase during development and in tumor cell lines.
    Oncogene. 1994 Nov;9(11):3353-61 PMID: 7936661
  62. Several receptor tyrosine kinase genes of the Eph family are segmentally expressed in the developing hindbrain.
    Mech Dev. 1994 Jul;47(1):3-17 PMID: 7947319
  63. Axon guidance. Growth cones say no.
    Curr Biol. 1994 Feb 1;4(2):131-3 PMID: 7953512
  64. Ligands for EPH-related receptor tyrosine kinases that require membrane attachment or clustering for activity.
    Science. 1994 Nov 4;266(5186):816-9 PMID: 7973638
  65. fgfr-1 is required for embryonic growth and mesodermal patterning during mouse gastrulation.
    Genes Dev. 1994 Dec 15;8(24):3032-44 PMID: 8001822
  66. Regulation of growth cone motility by substratum bound molecules and cytoplasmic [Ca2+].
    Prog Brain Res. 1994;103:85-98 PMID: 7886224
  67. Localization of PDGF A and PDGFR alpha mRNA in Xenopus embryos suggests signalling from neural ectoderm and pharyngeal endoderm to neural crest cells.
    Mech Dev. 1994 Dec;48(3):165-74 PMID: 7893600
  68. Expression of an amphibian homolog of the Eph family of receptor tyrosine kinases is developmentally regulated.
    Oncogene. 1995 Mar 16;10(6):1111-7 PMID: 7700636
  69. Role of B61, the ligand for the Eck receptor tyrosine kinase, in TNF-alpha-induced angiogenesis.
    Science. 1995 Apr 28;268(5210):567-9 PMID: 7536959
  70. 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 Aug 11;82(3):359-70 PMID: 7634326
  71. Complementary gradients in expression and binding of ELF-1 and Mek4 in development of the topographic retinotectal projection map.
    Cell. 1995 Aug 11;82(3):371-81 PMID: 7634327
  72. 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 Sep;15(9):4921-9 PMID: 7651410
  73. CAM-FGF receptor interactions: a model for axonal growth.
    Mol Cell Neurosci. 1996;8(2-3):99-111 PMID: 8918827
  74. Neuronal pathfinding and recognition: roles of cell adhesion molecules.
    Dev Biol. 1996 Dec 15;180(2):424-32 PMID: 8954715
  75. Cell contact-dependent signaling.
    Dev Biol. 1996 Dec 15;180(2):445-54 PMID: 8954717
  76. heartless encodes a fibroblast growth factor receptor (DFR1/DFGF-R2) involved in the directional migration of early mesodermal cells in the Drosophila embryo.
    Genes Dev. 1996 Dec 1;10(23):3003-17 PMID: 8957001
  77. Expression of a dominant negative FGF receptor inhibits axonal growth and FGF receptor phosphorylation stimulated by CAMs.
    Neuron. 1997 Feb;18(2):231-42 PMID: 9052794
  78. Tyrosine phosphorylation of transmembrane ligands for Eph receptors.
    Science. 1997 Mar 14;275(5306):1640-3 PMID: 9054357
  79. Reciprocal expression of the Eph receptor Cek5 and its ligand(s) in the early retina.
    Dev Biol. 1997 Feb 15;182(2):256-69 PMID: 9070326
  80. Eph family transmembrane ligands can mediate repulsive guidance of trunk neural crest migration and motor axon outgrowth.
    Neuron. 1997 Mar;18(3):383-96 PMID: 9115733
Article Info
Journal
Molecular and cellular biology
Abbr.
Mol Cell Biol
ISSN
0270-7306
Published
2000-01-00
Pages
724-34
Language
English
Region
United States
NLM ID
8109087
PMCID
PMC85187
Subset
IM
Grants
NIDCR NIH HHS · R01 DE013248 · United States
NIDCR NIH HHS · DE 13248 · United States
NCI NIH HHS · N01-CO-5600 · United States
Analysis Services
Analysis Services

Contact

No. 2 Wenbo Road, Zhangqiu District, Jinan, Shandong

Qilu Normal University · Genelibs Bioinformatics Lab

750 Shunhua Rd, Jinan

2F, Bldg F, University Science Park

Tel: 0531-88819269

WeChat Official Account

Follow our WeChat subscription account for real-time updates and the latest in medical and biological research.


Business Email

E-mail: [email protected]