Shared and distinct functions of RAGS and ELF-1 in guiding retinal axons

EMBO Journal

Volumn 16, Issue 6, 1997, Pages 1258-1267

  Monschau, Bruno ^a   Kremoser, Claus ^a   Ohta, Kunimasa ^b   Tanaka, Hideaki ^b   Kaneko, Tomomi ^b   Yamada, Tomoko ^b   Handwerker, Claudia ^a   Hornberger, Martin R ^a   Löschinger, Jürgen ^a   Pasquale, Elena B ^c   Siever, Doyle A ^d   Verderame, Michael F ^d   Müller, Bernhard K ^a   Bonhoeffer, Friedrich ^a   Drescher, Uwe ^a  

^a MAX PLANCK INSTITUTE FOR DEVELOPMENTAL BIOLOGY   (Germany)

^b KUMAMOTO UNIVERSITY   (Japan)

^c BURNHAM INSTITUTE   (United States)

^d PENN STATE COLLEGE OF MEDICINE   (United States)

Author keywords

Axon guidance; Eph related RTKs and ligands; Gradients; Retinotectal projection

Indexed keywords

PROTEIN TYROSINE KINASE;

ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; EMBRYO; NERVE FIBER; NERVOUS SYSTEM DEVELOPMENT; NONHUMAN; OPTIC TECTUM; PRIORITY JOURNAL; RECEPTOR BINDING; RETINA GANGLION CELL; RETINA NERVE CELL; RETINOTECTAL PROJECTION;

ANIMALS; AXONS; BASE SEQUENCE; CHICK EMBRYO; COS CELLS; DNA PRIMERS; DNA, COMPLEMENTARY; DNA-BINDING PROTEINS; EPHRIN-A2; GENE EXPRESSION REGULATION, DEVELOPMENTAL; MICE; NUCLEAR PROTEINS; RECEPTOR PROTEIN-TYROSINE KINASES; RETINA; RETINAL GANGLION CELLS; RNA; SUPERIOR COLLICULUS; TRANSCRIPTION FACTORS; TRANSFECTION; VISUAL PATHWAYS;

ANIMALIA;

EID: 0031003116     PISSN: 02614189     EISSN: None     Source Type: Journal    
DOI: 10.1093/emboj/16.6.1258     Document Type: Article

References (61)

1. Beckmann, M.P. (1994) Molecular characterization of a family of ligands for eph-related tyrosine kinase receptors. EMBO J., 13, 3757-3762.
2. Bennett, B.D., Zeigler, F.C., Gu, Q.M., Fendly, B., Goddard, A.D., Gillett, N. and Matthews, W. (1995) Molecular-cloning of a ligand for the eph-related receptor protein-tyrosine kinase htk. Proc. Natl Acad. Sci. USA, 92, 1866-1870.
3. 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 mouse embryos in the region of the hindbrain and newly forming somites. Mol. Cell. Biol., 15, 4921-4929.
4. Brambilla, R. and Klein, R. (1995) Telling axons where to grow: a role for Eph receptor tyrosine kinases in guidance. Mol. Cell Neurosci., 6, 487-495.
5. Brambilla, R., Schnapp, A., Casagranda, F., Labrador, J.P., Bergemann, A.D., Flanagan, J.G., Pasquale, E.B. and Klein, R. (1995) Membrane-bound Lerk2 ligand can signal through three different Eph-related receptor tyrosine kinases. EMBO J., 14, 3116-3126.
6. Chen, C. and Okayama, H. (1987) High-efficiency transformation of mammalian cells by plasmid DNA. Mol. Cell Biol., 8, 2745-2752.
7. 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.
8. 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.
9. Ciossek, T., Millauer, B. and Ullrich, A. (1995) Identification of alternatively spliced mRNAs encoding variants of MDK1, a novel receptor tyrosine kinase expressed in the murine nervous system. Oncogene, 10, 97-108.
10. Colamarino, S.A. and Tessier-Lavigne, M. (1995) The role of the floor plate in axon guidance. Ann. Rev. Neurosci., 18, 497-529.
11. Cox, E.C., Müller, B. and Bonhoeffer, F. (1990) Axonal guidance in the chick visual system: posterior rectal membranes induce collapse of growth cones from the temporal retina. Neuron, 2, 31-37.
12. 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 receptor tyrosine kinases that require membrane attachment or clustering for activity. Science, 266, 816-819.
13. Drescher, U., Kremoser, C., Handwerker, C., Löschinger, 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.
14. Fan, J.H. and Raper, J.A. (1995) Localized collapsing cues can steer growth cones without inducing their full collapse. Neuron, 14, 263-274.
15. Flanagan, J.G. and Leder, P. (1990) The kit ligand: a cell surface molecule altered in steel mutant fibroblasts. Cell, 63, 185-194.
16. Gale, N.W. et al. (1996) Eph receptors and ligands comprise two major specificity subclasses and are reciprocally compartmentalized during embryogenesis. Neuron, 17, 9-19.
17. 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.
18. Gierer, A. (1983) Model for the retino-tectal projection. Proc. R. Soc. Lond. B, 218, 77-93.
19. Gierer, A. (1988) Spatial organization and genetic information in brain development. Biol. Cybern., 59, 13-21.
20. Goodman, C.S. (1996) Mechanisms and molecules that control growth cone guidance. Ann. Rev. Neurosci., 19, 341-377.
21. Harlow, E. and Lane, D. (1988) Monoclonal antibodies. In Harlow, E. and Lane, D. (eds), Antibodies. A Laboratory Manual. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NY, pp. 139-244.
22. Holash, J.A. and Pasquale, E.B. (1995) Polarized expression of the receptor protein tyrosine kinase Cek5 in the developing avian visual system. Dev. Biol., 172, 683-693.
23. Holt, C.E. and Harris, W.A. (1993) Position, guidance, and mapping in the developing visual system. J. Neurobiol., 24, 1400-1422.
24. Jesuthasan, S. (1996) Contact inhibition/collapse and pathfinding of neural crest cells in the zebrafish trunk. Development, 122, 381-389.
25. Kenny, D., Bronner-Frazer, M. and Marcelle, C. (1995) The receptor tyrosine kinase qek5 mRNA is expressed in a gradient within the neural retina and the tectum. Dev. Biol., 172, 708-716.
26. Keynes, R. and Cook, G. (1990) Cell-cell repulsion: clues from the growth cone? Cell, 62, 609-610.
27. Kozlosky, C.J. et al. (1995) Ligands for the receptor tyrosine kinases hek and elk-isolation of cDNAs encoding a family of proteins. Oncogene, 10, 299-306.
28. Lindberg, R.A. and Hunter, T. (1990) cDNA cloning and characterization of eck, an epithelial cell receptor protein-tyrosine kinase in the eph/elk family of protein kinases. Mol. Cell. Biol., 10, 6316-6324.
29. Lumsden, A. (1990) The cellular basis of segmentation in the developing hindbrain. Trends Neurosci., 13, 329-335.
30. Maisonpierre, P.C., Barrezueta, N.X. and Yancopoulos, G.D. (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.
31. McLoon, S.C. (1991) A monoclonal antibody that distinguishes between nasal and temporal retinal axons. J. Neurosci., 11, 1470-1477.
32. Mey, J. and Thanos, S. (1992) Development of the visual system of the chick - a review. J. Hirnforsch., 33, 673-702.
33. 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 motorneurons in the spinal cord during development. Mech. Dev., 54, 59-69.
34. Pandey, A., Lindberg, R.A. and Dixit, V.M. (1995a) Receptor orphans find a family. Curr. Biol., 5, 986-989.
35. Pandey, A., Shao, H.N., Marks, R.M., Polverini, P.J. and Dixit, V.M. (1995b) Role of B61, the ligand for the eck receptor tyrosine kinase, in TNF-alpha-induced angiogenesis. Science, 268, 567-569.
36. Pfenninger, K.H. (1986) Of nerve growth cones, leukocytes and memory: second messenger systems and growth regulated proteins. Trends Neurosci., 11, 562-565.
37. Rager, G. (1976) Morphogenesis and physiogenesis of the retinotectal connection in the chicken. II. The retinotectal synapse. Proc. R. Soc. Lond. B, 192, 353-370.
38. Rager, U., Rager, G. and Frei, B. (1993) Central retinal area is not the site where ganglion cells are generated first. J. Comp. Neurol., 334, 529-544.
39. Raper, J.A. and Kapfhammer, J. (1990) The enrichment of a neuronal growth cone collapsing activity from embryonic chick brain. Neuron, 4, 21-29.
40. Roskies, A., Friedmann, G.C. and O'Leary, D.D.M. (1995) Mechanisms and molecules controlling the development of retinal maps. Perspect. Dev. Neurobiol., 3, 61-15.
41. Ruiz, J.C. 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.
42. Sajjadi, F.G. and Pasquale, E.B. (1993) Five novel avian Eph-related tyrosine kinases are differentially expressed. Oncogene, 8, 1807-1813.
43. Sajjadi, F.G., Pasquale, E.B. and 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, 169-718.
44. AP: a topographically graded protein in the developing chick visual system. Neuron, 14, 253-261.
45. Scatchard, G. (1949) The attractions of protein for small molecules and ions. Ann. N. Y. Acad. Sci, 51, 660-672.
46. Shao, H.N., Lou, L.D., Pandey, A., Verderame, M.F., Siever, D.A. and Dixit, V.M. (1995) cDNA cloning and characterization of a cek7 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.
47. Siever, D.A. and Verderame, M.F. (1994) Identification of a complete cek7 receptor protein-tyrosine kinase coding sequence and cDNAs of alternatively spliced transcripts. Gene, 148, 219-226.
48. Sperry, R.W. (1963) Chemoaffinity in the orderly growth of nerve fiber patters and connections. Proc. Natl Acad. Sci. USA, 50, 703-710.
49. Stahl, B., Muller, B., von Boxberg, Y., Cox, E.C. and Bonhoeffer, F. (1990) Biochemical characterization of a putative axonal guidance molecule of the chick visual system. Neuron, 5, 733-743.
50. Tessier-Lavigne, M. (1995) Eph receptor tyrosine kinases, axon repulsion, and the development of topographic maps. Cell, 82, 345-348.
51. Udin, S.B. and Fawcett, J.W. (1988) Formation of topographic maps. Ann. Rev. Neurosci., 11, 289-327.
52. Valenzuela, D.M., Rojas, E., Griffiths, J.A., Compton, D.L., Gisser, M., Ip, N.Y., Goldfarb, M. and Yancopoulos, G.D. (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.
53. Walter, J., Kern-Veits, B., Huf, J., Stolze, B. and Bonhoeffer, F. (1987) Recognition of position-specific properties of tectal cell membranes by retinal axons in vitro. Development, 101, 685-696.
54. Walter, J., Allsopp, T.E. and Bonhoeffer, F. (1990) A common denominator of growth cone guidance and collapse? Trends Neurosci., 13, 447-452.
55. Whitelaw, V.A. and Cowan, J.D. (1981) Specificity and plasticity of retinotectal connections: a computational model. J. Neurosci., 1, 1369-1387.
56. Wilkinson, D.G. (1995) RNA detection using non-radioactive in situ hybridization. Curr. Opin. Biotechnol., 6, 20-23.
57. Willshaw, D.J. and Malsburg, C.v. (1976) How patterned neural connections can be set up by self-organization. Proc. R. Soc. Lond. B, 194, 431-445.
58. Willshaw, D.J. and Malsburg, C.v. (1979) A marker induction mechanism for the establishment of ordered neural mappings: its application to the retinotectal problem. Philos. Trans. R. Soc. Lond. B, 287, 203-243.
59. Winslow, J.W. et al. (1995) Cloning of Al-1, a ligand for an Eph-related tyrosine kinase receptor involved in axon bundle formation. Neuron, 14, 973-981.
60. Xu, Q., Alldus, G., Holder, N. and Wilkinson, D.G. (1996a) Expression of truncated Sek-1 receptor tyrosine kinase disrupts the segmental restriction of gene expression in the Xenopus and zebrafish hindbrain. Development, 121, 4005-1016.
61. Xu, Q., Alldus, G., Macdonald, R., Wilkinson, D.G. and Holder, N. (1996b) Function of the Eph-related kinase rtk1 in patterning of the zebrafish forebrain. Nature, 381, 319-322.