The expression and regulation of chick EphA7 suggests roles in limb patterning and innervation

Development

Volumn 125, Issue 21, 1998, Pages 4195-4204

  Araujo, María ^a   Piedra, M Elisa ^b   Herrera, M Teresa ^a   Ros, María A ^b   Nieto, M Angela ^a  

^a INSTITUTO CAJAL   (Spain)

^b UNIVERSITY OF CANTABRIA   (Spain)

Author keywords

Apical ectodermal ridge; Axon guidance; Cek11; Chick; Dorsal ectoderm; Eph; EphA7; Ephrins; Limb patterning; Lmx 1; Mesenchyme; Neural tube; Sclerotome; Wnt7a

Indexed keywords

PROTEIN TYROSINE KINASE; RECEPTOR;

ANIMAL TISSUE; ARTICLE; BRAIN COMMISSURE; CELL CONTACT; CONTROLLED STUDY; DEVELOPMENTAL GENETICS; ECTODERM; EMBRYO; EMBRYO PATTERN FORMATION; GENE EXPRESSION REGULATION; INNERVATION; LIMB DEVELOPMENT; MESENCHYME; MOTOR NERVE; NERVOUS SYSTEM DEVELOPMENT; NEURAL CREST CELL; NONHUMAN; PRIORITY JOURNAL; SOMITE;

ANIMALS; AXONS; BODY PATTERNING; CHICK EMBRYO; ECTODERM; EPHRIN-A5; EXTREMITIES; GENE EXPRESSION REGULATION, DEVELOPMENTAL; HOMEODOMAIN PROTEINS; IMMUNOHISTOCHEMISTRY; IN SITU HYBRIDIZATION; MEMBRANE PROTEINS; NERVE TISSUE PROTEINS; RECEPTOR PROTEIN-TYROSINE KINASES; RECEPTOR, EPHA7; SPINAL CORD;

ANIMALIA; AVES; VERTEBRATA;

EID: 0031735912     PISSN: 09501991     EISSN: None     Source Type: Journal    
DOI: None     Document Type: Article

References (75)

1. Araujo, M. and Nieto, M. A. (1997). The expression of EphA7 during segmentation of the central and peripheral nervous system. Mech. Dev. 68, 173-177.
2. Bambrilla, R., Schnapp, A., Casagranda, F., Labrador, J. P., Bergemann, A. D., Flanagan, J. G., Pasquale, E. and Klein, R. (1995). Membrane-bound LERK2 ligand can signal through different Eph-related receptor tyrosine kinases. EMBO J. 14, 3116-3126.
3. 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.
4. Brückner, K., Pasquale, E. B. and Klein, R. (1997). Tyrosine phosphorylation of transmembrane ligands for Eph receptors. Science 275, 1640-1643.
5. Chang, D. T., López, A., Von Kessler, D. P., Chang, C., Simandl, B. K., Zhao, R., Selding, M. F., Fallon, J. F. and Beachy, P. A. (1994). Products, genetic linkage and limb patterning activity of a murine hedgehog gene. Development 120, 3339-3353.
6. Cheng, H.-J. and Flanagan, J. G. (1994). Identification and cloning of ELF-1, a developmentally expressed ligand for the mek-4 and Sek receptor tyrosine kinases. Cell 79, 157-168.
7. Cheng, H.-J., Nakamotu, M., Bergeman, A. D. and Flanagan, J. G. (1995). Complementary gradients in expression and binding of ELF-1 and Mek-4 in development of the topographic retinotectal projection map. Cell 82, 371-381.
8. Conn, M. J. and Tickle, C. (1996). Limbs: a model for pattern formation within the vertebrate body plan. Trends Genet. 12, 253-257.
9. Crossley, P. H., Minowada, G., MacArthur, C. A. and Martin, G. (1996). Roles for FGF8 in the induction, initiation and maintenance of chick limb development. Cell 84, 127-136.
10. 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 require membrane attachment or clustering for activity. Science 266, 816-819.
11. Drescher, U. (1997). The Eph family in the patterning of neural development. Current Biol. 7, 799-807.
12. Drescher, U., Kremoser, C., Handwerker, C., Löschingen J., Noda, M. and Bonhoeffer, F. (1995) In vitro guidance of retinal ganglion cell axons by RAGS, a 25kDa tectal protein related to ligands for Eph receptor tyrosine kinases. Cell 82, 359-370.
13. Ebens, A., Brose, K., Leonardo, E. D., Hanson Jr, M. G., Bladt, F., Birchmeier, C., Bares, B. A. and Tessier-Lavigne, M. (1996). Hepatocyte growth factor/Scatter factor is an axonal chemosttractant and a neurotrophic factor for spinal motor neurons. Neuron 17, 1157-1172.
14. Ellis, J., Liu, Q., Breitman, M., Jenkins, N. A., Gilbert, D. J., Copeland, N. G., Tempest, H. V., Warren, S., Muir, E., Schilling, H., Fletcher, F. A., Ziegler, S. F. and Rogers, J. H. (1995). Embryo brain kinase: a novel gene of the eph/elk recptor tyrosine kinase family. Mech. Dev. 52, 319-341.
15. Eph Nomenclature Committee. (1997). Unified nomenclature for the Eph family recptors and their ligands, the ephrins. Cell 90, 403-404.
16. Ensini, M., Tsuchida, T. N., Belting, H.-G. and Jessell, T. M. (1998). The control of rostro-caudal pattern in the developing spinal cord: Specification of motor neuron subtype identity is initiated by signals from puraxial mesoderm. Development 125, 969-982.
17. Faivre-Sarrailh, C. and Rougon, G. (1997). Axonal molecules of the immunoglobulin superfamily bearing a GPI anchor: Their role in controlling neurite outgrowth. Mol. Cell. Neurosci. 9, 109-115.
18. Fallon, J. F., López, A., Ros, M. A., Savage, M., Olwin, B. and Simandl, B. K. (1994). FGF2: apical ectodermal ridge growth signal for the chick limb development. Science 264, 104-107.
19. Flenniken, A. M., Gale, N. W., Yancopoulos, G. D. and Wilkinson, D. G. (1996). Distinct and overlapping expression patterns of ligands for Eph-related receptor tyrosine kinases during mouse embryogenesis. Dev. Biol. 179, 382-401.
20. Frisen, J., Yates, P. A., McLaughlin, T., Friedman, G. C., O'Leary, D. D. and Barbacid, M. (1998). Ephrin-A5 (AL-1/RAGS) is essential for proper retinal axon guidance and topographic mapping in the mammalian visual system. Neuron 20, 235-243.
21. Gale, N. W., Holland, S. J., Valenzuela, D. M., Flenniken, A., Pan, L., Ryan, T. E., Henkemeyer, M., Strebhardt, K., Hirai, H., Wilkinson, D. G., Pawson, T., Davis, S. and Yancopoulos, G. D. (1996). Eph receptors and ligands comprise two major specificity subclasses and are reciprocally compartmentalized during embryogenesis. Neuron 17, 9-19.
22. Gale, N. W. and Yancopoulos, G. D. (1997). Ephrins and their receptors: a repulsive topic? Cell Tissue Res. 290, 227-241.
23. Ganju, P., Shigemoto, K., Brennan, J., Entwistle, A., 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.
24. Gao, P.-P., Zhang, J.-H., Yokoyama, M., Dreyfus, C. F., Black, I. B. and Zhou, R. (1996). Regulation of topographic projection in the brain: Elf-1 in the hippocamposeptal system. Proc. Natl. Acd. Sci. USA 93, 11161-11166.
25. Hamburger, V. and Hamilton, H. (1951). A series of normal stages in the development of the chick embryos. J. Morphol. 88, 49-92.
26. Henkemeyer, M., Marengere, L. E. M., McGlade, L. E., Olivier, J. P., Conlon, R. A., Hulmyard, D. P., Letwin, K. and Pawson, T. (1994) Immunolocalization of the Nuk receptor tyrosine kinase suggests roles in segmental patterning of the brain and axonogenesis. Oncogene 9, 1001-1014.
27. Henkemeyer, M., Orioli, D., Henderson, J. T., Sxaton, 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.
28. Holland, S. J., Gale, N. W., Mbamalu, G., Yancopoulos, G. D., Henkemeyer, M. and Pawson, T. (1996). Bidirectional signalling trough the Eph family receptor Nuk and its transmeinbrane ligands. Nature 383, 722-725.
29. Holland, S. J., Peles, E., Pawson, T. and Schlessinger, J. (1998). Cell-contact-dependent signalling in axon growth and guidance: Eph receptor tyrosine kinases and recptor tyrosine phosphatase β. Curr. Opin. Neurobiol. 8, 117-127.
30. Hollyday, M. (1995). Chick wing innervation. I. Time course of innervation and early differentiation of the peripheral nerve pattern. J. Comp. Neurol. 357, 242-253.
31. 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.
32. Irving, C., Nieto, M. A., DasGupta, R., Charnay, P. and Wilkinson, D. G. (1996) Progressive spatial restriction of Sek-1 and Kros-20 gene expression during hindbrain segmentation. Dev. Biol. 173, 26-38.
33. Kitsukawa, T., Shimizu, M., Sanbo, M., Hirata, T., Taniguchi, M., Bekku, Y., Vagi, T. and Fujisawa, H. (1997). Neuropilin-SemaphorinIII/Dmediated chemorepulsive signals play a crucial role in peripheral nerve projection in mice. Neuron 19, 995-1005.
34. Krull, C. E., Landsford, R., Gale, N. W., Collazo, A., Marcelle, C., Yancopoulos, G. D., Fraser, S. E. and Bronner-Fraser, M. (1997). Interactions of Eph-related receptors and ligands confer rostrocaudal pattern to trunk neural crest migration. Current Biol. 7, 571-580.
35. Laufer, E., Dahn, R., Orozco, O. E., Yeo, C. Y., Pisenti, J., Henrique, D., Abott, U. K., Fallon, J. F. and Tabin, C. (1997). Expression of radical Fringe in limb-bud ectoderm regulates apical ectodermal ridge formation. Nature 386, 366-373.
36. Logan, C., Hornbruch, A., Campbell, I. and Lumsden, A. (1997). The role of Engrailed in establishing the dorsoventral axis of the chick limb. Development 124, 2317-2324.
37. Loomis, C. A., Harris, E., Michaud, J., Wurst, W., Hanks, M. and Joyner, A. L. (1996). The mouse Engrailed-1 gene and ventral limb patterning. Nature 382, 360-363.
38. Loomis, C. A., Kimmel, R. A., Tong, C. X., Michaud, J. and Joyner, A. L. (1998). Analysis of the genetic pathway leading to formation of ectopic apical ectodermal ridges in mouse Engrailed-1 mutant limbs. Development, 125, 1137-1148.
39. López-Martínez, A., Chang, D. T., Chiang, C., Porter, J. A., Ros, M. A., Simandl, B. K., Beachy, P. A. and Fallon, J. F. (1995). Limb-patterning activity and restricted posterior localization of the amino terminal product of Sonic hedgehog cleavage. Curr. Biol. 5, 791-796.
40. Lewis, J., Chevalier, A., Kieny, M. and Wolpert, L. (1981). Muscle nerve branches do not develop in chick wings devoid of muscle. J. Embryol. Exp. Morph. 64, 211-232.
41. Mahmood, R., Bresnick, J., Hornbruch, A., Mahony, C., Morton, N., Colquhoun, K., Martin. P., Lumsden, A., Dickson, C. and Mason, I. (1995). A role for FGF8 in the initiation and maintenance of vertebrate limb bud outgrowth. Curr. Biol. 5, 797-806.
42. Marcus, R. C., Gale, N. W., Morrison, M. E., Mason, C. A. and Yancopoulos, G. D. (1996). Eph family receptors and their ligands distribute in the developing mouse retina. Dev. Biol. 180, 786-789.
43. Martin, P. and Lewis, J. (1986). Normal development of the skeleton in chick limb buds devoid of dorsal ectoderm. Dev. Biol. 118, 233-246.
44. Moody, S. A., Quigg, M. S. and Frankfurter, A. (1989) Development of the peripheral trigeminal system in the chick revealed by an isotype-specific anti-beta-tubulin monoclonal antibody. J. Comp. Neurol. 279, 567-580.
45. Nakamoto, M., Cheng, H.-J., Friedman, G. C., McLaughlin, T., Hansen, M. J., Yoon, C. H., O'Leary, D. D. M. and Flanagan, J. G. (1996). Topographically specific effects of ELF-1 on retinal axon guidance in vitro and retinal axon guidance in vivo. Cell 86, 755-766.
46. Nieto, M. A. (1996). Molecular biology of axon guidance. Neuron 17, 1039-1048.
47. 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 the mesoderm. Development 116, 1137-1150.
48. Nieto, M. A., Patel, K. and Wilkinson D. G. (1996). In situ hybridization analysis of chick embryos in whole mount and tissue sections. Methods Cell Biol. 51, 220-235.
49. Niswander, L., Tickle, C., Vogel, A., Booth, I. and Martin, G. R. (1993). FGF4 replaces the apical ectodermal ridge and directs outgrowth and patterning of the limb. Cell 75, 579-587.
50. 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 dvelopment. Mech. Dev. 54, 59-69.
51. Ohta, K., Iwamasa, H., Drescher, U., Terasaki, H. and Tanaka, H. (1997). The inhibitory effect on neurite outgrowth of motoneurons exerted by the ligands ELF-1 and RAGS. Mech. Dev. 64, 127-135.
52. Orioli, D., Henkemeyer, M., Lemke, G., Klein, R. and Pawson, T. (1996). Sek4 and Nuk receptors cooperate in guidance of commissural axons and in palate formation. EMBO J. 15, 6035-6049.
53. Orioli, D. and Klein, R. (1997). The Eph receptor family: axonal guidance by contact repulsion. Trends. Genet. 13, 354-359.
54. Park, S., Frisen, J. and Barbacid, M. (1997). Aberrant axonal projections in mice lacking EphA8 (Eek) tyrosine protein kinase receptors. EMBO J. 16, 3106-3114.
55. Parr, B. A. and McMahon, A. P. (1995). Dorsalizing signal Wnt-7a required for normal polarity of D-V and A-P axes in mouse limb. Nature 374, 350-353.
56. Patel, K., Nittenberg, R., D'Souza, D., Irving, C., Burt, D., Wilkinson, D. G. and Tickle, C. (1996). Expression and regulation of Cek-8, a cell to cell signalling receptor in developing chick limb buds. Development 122
57. Peles, E., Nativ, M., Lustig, M., Grumet, M., Schilling, J., Martinez, R., Plowman, G. D., and Schlessinger, J. (1997). Identification of a novel contactin-associated transmembrane receptor with multiple domains implicated in protein-protein interactions. EMBO J. 16, 978-988.
58. Riddle, R. D., Johnson, R. L., Laufer, E. and Tabin, C. (1993). Sonic hedgehog mediates the polarizing activity of the ZPA. Cell 75, 1401-1416.
59. Riddle, R. D., Ensini, M., Nelson, C., Tsuchida, T., Jessell, T. M. and Tabin, C. (1995). Induction of the LIM homeobox gene Lmx1 by Wnt7a establishes dorsoventral pattern in the vertebrate limb. Cell 83, 631-640.
60. Rodriguez-Esteban, C., Schwabe, J. W., De la Peña, J., Foys, B., Eshelman, B. and Izpisua-Belmonte, J. C. (1997). Radical fringe positions the apical ectodermal ridge at the dorsoventral boundary of the vertebrate limb. Nature 386, 360-366.
61. Rowe, D. A. and Fallon, J. F. (1982). The proximodistal determination of skeletal parts in the developing chick leg. J. Embryol. Exp. Morph. 68, 1-7.
62. 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.
63. Saunders, J. W. (1948). The proximo-distal sequence of origin of the parts of the chick wing and the role of the ectoderm. J. Exp. Zool. 108, 363-403.
64. Sefton, M., Araujo, M. and Nieto, M. A. (1997). Novel expression gradients of Eph-like receptor tyrosine kinases in the developing chick retina. Dev. Biol. 188, 363-368.
65. Sefton, M. and Nieto, M. A. (1997). Multiple role of Eph kinases and their ligands during development. Cell Tissue Res. 290, 243-250.
66. Smith, A., Robinson, V., Patel, K. and Wilkinson, D. G. (1997). The EphA4 and EphB1 receptor tyrosine kinases and ephrin-B2 ligand regulate targeted migration of branchial neural crest. Current Biol. 7, 561-570.
67. Taneja, R., Thisse, B., Rijli, F. M., Thisse, C., Bouillet, P., Dollé, P. And Chambon, P. (1996). The expression pattern of the mouse receptor tyrosine kinase gene MDK1 is conserved through evolution and requires Hoxa-2 for rhombomere-specific expression in mouse embryos. Mech. Dev. 177, 397-412.
68. Tsuchida, T., Ensini, M., Morton, S. B., Baldassare, M., Edlund, T., Jessel, T. M. and Pfaff, S. L. (1994). Topographic organization of embryonic motor neurons defined by expression of LIM homeobox genes. Cell 79, 957-970.
69. Vogel, A., Rodriguez, C., Warnken, W. and Izpisúa-Belmonte, J. C. (1995). Dorsal cell fate specified by chick Lmx1 during vertebrate limb development. Nature 378, 716-720.
70. Vogel, A., Rodriguez, C. and Izpisúa-Belmonte, J. C. (1996). Involvement of FGF-8 in initiation, outgrowth and patterning of the vertebrate limb. Development 122, 1737-1750.
71. Wang, H. U. and Anderson, D. J. (1997). Eph family transmembrane ligands can mediate repulsive guidance of trunk neural crest migration and motor axon outgrowth. Neuron 18, 383-396.
72. Wilkinson, D. G. and Nieto, M. A. (1993). Detection of messenger RNA by in situ hybridization to tissues sections and whole mounts. Methods Enzymol. 225, 361-373.
73. Yang, Y. and Niswander, L. (1995). Interaction between the signalling molecules WNT7a and SHH during vertebrate limb development: dorsal signals regulate anteroposterior patterning. Cell 80, 939-947.
74. 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.
75. Xu, Q., Alldus, G., Macdonald, R., Wilkinson, D. G. and Holder, N. (1996). Function of the Eph-related kinase rtk1 in patterning of the zebrafish forebrain. Nature 381, 319-321.