Distinct and overlapping expression patterns of ligands for Eph-related receptor tyrosine kinases during mouse embryogenesis

Developmental Biology

Volumn 179, Issue 2, 1996, Pages 382-401

  Flenniken, Ann M ^a   Gale, Nicholas W ^b   Yancopoulos, George D ^b   Wilkinson, David G ^a  

^a NATIONAL INSTITUTE FOR MEDICAL RESEARCH   (United Kingdom)

^b REGENERON PHARMACEUTICALS INC   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

LIGAND; PROTEIN TYROSINE KINASE;

AMINO ACID SEQUENCE; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; EMBRYO; EMBRYO DEVELOPMENT; IN SITU HYBRIDIZATION; LIGAND BINDING; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; SEQUENCE HOMOLOGY;

ANIMALIA; CERVUS ELAPHUS;

EID: 0030296943     PISSN: 00121606     EISSN: None     Source Type: Journal    
DOI: 10.1006/dbio.1996.0269     Document Type: Article

References (53)

1. Bartley, T. D., Hunt, R. W., Welcher, A. A., Boyle, W. J., Parker, V. P., Lindberg, R. A., Lu, H. S., Colombero, A. M., Elliott, R. L., Guthrie, B. A., Holst, P. L., Skrine, J. D., Toso, R. J., Zhang, M., Fernandez, E., Trail, G., Varnum, B., Yarden, Y., Hunter, T., and Fox, G. M. (1994). B61 is a ligand for the ECK receptor protein-tyrosine kinase. Nature 368, 558-560.
2. Becker, N., Seitanidou, T., Murphy, P., Mattei, M.-G., Topilko, P., Nieto, M. A., Wilkinson, D. G., Charnay, P., and Gilardi-Hebenstreit, P. (1994). Several receptor tyrosine kinase genes of the Eph family are segmentally expressed in the developing hindbrain. Mech. Dev. 47, 3-17.
3. Beckmann, M. P., Cerretti, D. P., Baum, P., Vanden Bos, T., James, L., Farrah, T., Kozlosky, C., Hollingsworth, T., Shilling, H., Maraskovsky, E., Fletcher, F. A., Lhotak, V., Pawson, T., and Lyman, S. D. (1994). Molecular characterisation of a family of ligands for eph-related tyrosine kinase receptors. EMBO J. 13, 3757-3762.
4. Bergemann, A. D., Cheng, H.-J., Brambilla, R., Klein, R., and Flanagan, J. G. (1995). ELF-2, a new member of the Eph ligand family, is segmentally expressed in the region of the hindbrain and newly formed somites. Mol. Cell. Biol. 15, 4921-4929.
5. Biffo, S., Offenhauser, N., Carter, B. D., and Barde, Y. A. (1995). Selective binding and internalisation by truncated receptors restrict the availability of BDNF during development. Development 121, 2461-2470.
6. Birgbauer, E., Sechrist, J., Bronner-Fraser, M., and Fraser, S. (1995). Rhombomeric origin and rostrocaudal assortment of neural crest cells revealed by intravital microscopy. Development 121, 935-945.
7. Bouillet, P., Oulad-Abdelghani, M., Vicaire, S., Garnier, J.-M., Schuhbaur, B., Dolle, P., and Chambon, P. (1995). Efficient cloning of cDNAs of retinoic acid-responsive genes in P19 embryonal carcinoma cells and characterization of a novel mouse gene, Stra 1, (mouse Lerk2/Eplg2). Dev. Biol. 170, 420-433.
8. Brambilla, R., and Klein, R. (1995). Telling axons where to grow -a role for Eph receptor tyrosine kinases in guidance. Mol. Cell. Neurosci. 6, 487-492.
9. Brambilla, R., Schnapp, A., Casagranda, F., Labrador, J., Bergemann, A., Flanagan, J., Pasquale, E., and Klein, R. (1995). Membrane-bound LERK2 ligand can signal through three different Eph-related receptor tyrosine kinases. EMBO J. 14, 3116-3126.
10. Chen, J., Nachabah, A., Scherer, C., Ganju, P., Reith, A., Bronson, R., and Ruley, H. (1996). Germ-line inactivation of the murine Eck receptor tyrosine kinase by gene trap retroviral insertion. Oncogens 12, 979-988.
11. Cheng, H.-J., and Flanagan, J. G. (1994). Identification and cloning of ELF-1, a developmentally expressed ligand for the Mek4 and Sek receptor tyrosine kinases. Cell 79, 157-168.
12. Cheng, H.-J., Nakamoto, M., Bergemann, A. D., and Flanagan, J. G. (1995). Complementary gradients in expression and binding of ELF-1 and Mek4 in development of the topographic retinotectal projection map. Cell 82, 371-381.
13. Chirgwin, J., Przybyla, A., MacDonald, R., and Rutter, W. (1979). Isolation of biologically active ribonucleic acid from sources enriched in ribonuclease. Biochemistry 18, 5294-5299.
14. Davis, S., Gale, N. W., Aldrich, T. H., Maisonpierre, P. C., Lhotak, V., Pawson, T., Goldfarb, M., and Yancopoulos, G. D. (1994). Ligands for EPH-related receptors that require membrane attachment or clustering for activity. Science 266, 816-819.
15. Dodd, J., and Jessell, T. M. (1988). Axon guidance and the patterning of neuronal projections in vertebrates. Science 242, 692-699.
16. Drescher, U., Kremoser, C., Handwerker, C., Loschinger, J., Noda, M., and 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.
17. Ellis, J., Liu, Q., Breitman, M., Jenkins, N., Gilbert, D., Copeland, N., Tempest, H., Warren, S., Muir, E., Schilling, H., Fletcher, F., Ziegler, S., and Rogers, J. (1995). Embryo brain kinase: a novel gene of the eph/elk receptor tyrosine kinase family. Mech. Dev. 52, 319-349.
18. Fletcher, F. A., Renshaw, B., Hollingsworth, T., Baum, P., Lyman, S. D., Jenkins, N. A., Gilbert, D. J., Copeland, N. G., and Davison, B. L. (1994). Genomic organization and chromosomal localization of mouse Eplg2, a gene encoding a binding protein for the receptor tyrosine kinase Elk. Genomics 24, 127-132.
19. Gale, N. W., Holland, S., Valenzuela, D., Flenniken, A., Pan, L., Henkemeyer, M., Strebhardt, K., Hirai, H., Wilkinson, D. G., Pawson, T., Davis, S., and Yancopoulos, G. D. (1996a). Eph receptors and ligands comprise two major specificity subclasses, and are reciprocally compartmentalized during embryogenesis. Neuron 17, 9-19.
20. Gale, N. W., Flenniken, A., Wang, H., Compton, D. C., Jenkins, N., Davis, S., Anderson, D. J., Wilkinson, D. G., and Yancopoulos, G. D. (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, in press.
21. Ganju, P., Shigemoto, K., Brennan, J., Entwistle, A., and Reith, A. D. (1994). The Eck receptor tyrosine kinase is implicated in pattern formation during gastrulation, hindbrain segmentation and limb development. Oncogene 9, 1613-1624.
22. Henkemeyer, M., Marengere, L. E., McGlade, J., Olivier, J. P., Conlon, R. A., Holmyard, D. P., Letwin, K., and Pawson, T. (1994). Immunolocalisation of the Nuk receptor tyrosine kinase suggests roles in segmental patterning of the brain and axonogenesis. Oncogene 9, 1001-1014.
23. Henkemeyer, M., Orioli, D., Henderson, J. T., Saxton, T. M., Roder, J., Pawson, T., and Klein, R. (1996). Nuk controls pathfinding of commissural axons in the mammalian central nervous system. Cell 86, 35-46.
24. Heyman, I., Kent, A., and Lumsden, A. (1993). Cellular morphology and extracellular space at rhombomere boundaries in the chick embryo hindbrain. Dev. Dynamics 198, 241-253.
25. Ide, H., Wada, N., and Uchiyama, K. (1994). Sorting out of cells from different parts and stages of the chick limb bud. Dev. Biol. 162, 71-76.
26. Irving, C., Nieto, M. A., DasGupta, R., Charnay, P., and Wilkinson, D. G. (1996). Progressive spatial restriction of Sek-1 and Krox-20 gene expression during hindbrain segmentation. Dev. Biol. 173, 26-38.
27. Kaufman, M. (1992). "The Atlas of Mouse Development." Academic Press, London.
28. Kilpatrick, T. J., Brown, A., Lai, C., Gassmann, M., Goulding, M., and Lemke, G. (1996). Expression of the Tyro4/Mek4/Cek4 gene specifically marks a subset of embryonic motor neurons and their muscle targets. Mol. Cell. Neurosci. 7, 62-74.
29. Kozlosky, D., Maraskovsky, E., McGrew, J., VandenBos, T., Teepe, M., Lyman, S., Srinivasan, S., Fletcher, F., Gayle, R., Cerretti, D., and Beckmann, M. (1995). Ligands for the receptor tyrosine kinases hek and elk: Isolation of cDNAs encoding a family of proteins. Oncogene 10, 299-306.
30. Lhotak, V., and Pawson, T. (1993). Biological and biochemical activities of a chimeric epidermal growth factor-Elk receptor tyrosine kinase. Mol. Cell. Biol. 13, 7071-7079.
31. Morgan, B., Conlon, F., Manzanares, M., Millar, J., Kanuga, N., Sharpe, J., Krumlauf, R., Smith, J., and Sedgwick, S. (1996). Transposon tools for recombinant DNA manipulation: characterization of transcriptional regulators from yeast, Xenopus, and mouse. Proc. Natl. Acad. Sci. USA 93, 2801-2806.
32. Nieto, M. A., Gilardi-Hebenstreit, P., Charnay, P., and Wilkinson, D. G. (1992). A receptor protein tyrosine kinase implicated in the segmental patterning of the hindbrain and mesoderm. Development 116, 1137-1150.
33. Nieto, M. A., Patel, K., and Wilkinson, D. G. (1995). In situ hybridisation analysis of chick embryos in whole mount and tissue sections. In "Methods in Avian Embryology" (M. Bronner-Fraser, Ed.). Academic Press, San Diego.
34. Ohta, K., Nakamura, M., Hirokawa, K., Tanaka, S., Iwama, A., Suda, T., Ando, M., and 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.
35. Pandey, A., Lazar, D., Saltiel, A., and Dixit, V. (1994). Activation of the Eck receptor protein tyrosine kinase stimulates phosphatidylinositol 3-kinase activity. J. Biol. Chem. 269, 30154-30157.
36. Pandey, A., Lindberg, R. A., and Dixit, V. M. (1995a). Receptor orphans find a family. Curr. Biol. 5, 986-989.
37. Pandey, A., Shao, H., Marks, R., Polverini, P., and Dixit, V. (1995b). Role of B61, the ligand of the Eck receptor tyrosine kinase, in TNF-a-induced angiogenesis. Science 268, 567-569.
38. Pasquale, E. B., Deerinck, T. J., Singer, S. J., and Ellisman, M. H. (1992). Cek5, a membrane receptor-type tyrosine kinase, is in neurons of the embryonic and postnatal avian brain. J. Neurosci. 12, 3956-3967.
39. Patel, K., Nittenberg, R., D'Souza, D., Irving, C., Burt, D., Wilkinson, D., and Tickle, C. (1996). Expression and regulation of Cek-8, a cell to cell signalling receptor, in developing chick limb buds. Dev. Biol. 122, 1147-1155.
40. Ruiz, J., and Robertson, E. J. (1994). The expression of the receptor-protein tyrosine kinase gene, eck, is highly restricted during early mouse development. Mech. Dev. 46, 87-100.
41. Sambrook, J., Fritsch, E. F., and Maniatis, T. (1989). "Molecular Cloning - A Laboratory Manual." Cold Spring Harbor Laboratory Press, New York.
42. Schaeren Wiemers, N., and Gerfin Moser, A. (1993). A single protocol to detect transcripts of various types and expression levels in neural tissue and cultured cells: in situ hybridisation using digoxigenin-labelled cRNA probes. Histochemistry 100, 431-440.
43. Serbedzija, G. N., Bronner-Fraser, M., and Fraser, S. E. (1992). Vital dye analysis of cranial neural crest cell migration in the mouse embryo. Development 116, 297-307.
44. Shao, H., Lou, L., Pandey, A., Pasquale, E. B., and Dixit, V. M. (1994). cDNA cloning and characterization of a ligand for the Cek5 receptor protein -tyrosine kinase. J Biol. Chem. 269, 26606-26609.
45. Shao, H., Pandey, A., O'Shea, K., Seldin, M., and Dixit, V. (1995). Characterization of B61, the ligand for the Eck receptor protein tyrosine kinase. J. Biol. Chem. 270, 5636-5641.
46. Snow, D., Steindler, D., and Silver, J. (1990). Molecular and cellular characterisation of the glial roof plate of the spinal cord and optic tectum: a possible role for a proteoglycan in the development of an axon barrier. Dev. Biol. 138, 359-376.
47. Takahashi, H., and Ikeda, T. (1995). Molecular cloning and expression of rat and mouse B61: implications on organogenesis. Oncogene 11, 879-883.
48. Tsuchida, T., Ensini, M., Morton, S. B., Baldassare, M., Edlund, T., Jessell, T. M., and Pfaff, S. L. (1994). Topographic organization of embryonic motor neurons defined by expression of LIM homeobox genes. Cell 79, 957-970.
49. van der Geer, P., Hunter, T., and Lindberg, R. A. (1994). Receptor protein tyrosine kinases and their signal transduction pathways. Annu. Rev. Cell Biol. 10, 251-337.
50. Winslow, J. W., Moran, P., Valverde, J., Shih, A., Yuan, J. Q., Wong, S. C., Tsai, S. P., Goddard, A., Henzel, W. J., Heftl, F., Beck, K. D., and Caras, I. W. (1995). Cloning of AL-1, a ligand for an Eph-related tyrosine kinase receptor involved in axon bundle formation. Neuron 14, 973-981.
51. Xu, Q., Holder, N., Patient, R., and Wilson, S. W. (1994). Spatially regulated expression of three receptor tyrosine kinase genes during gastrulation in the zebrafish. Development 120, 287-299.
52. Xu, Q., Alldus, G., Holder, N., and Wilkinson, D. G. (1995). Expression of truncated Sek-1 receptor tyrosine kinase disrupts the segmental restriction of gene expression in the Xenopus and zebrafish hindbrain. Development 121, 4005-4016.
53. Yaginuma, H., Shiga, T., Homma, S., Ishihara, R., and Oppenheim, R. W. (1990). Identification of early developing axon projections from spinal interneurons in the chick embryo with a neuron specific β-tubulin antibody: evidence for a new "pioneer" pathway in the spinal cord. Development 108, 705-716.