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

Developmental Biology

Volumn 177, Issue 2, 1996, Pages 397-412

  Taneja, Reshma ^a   Thisse, Bernard ^a   Rijli, Filippo M ^a   Thisse, Christine ^a   Bouillet, Philippe ^a   Dollé, Pascal ^a   Chambon, Pierre ^a  

^a l'alimentation et l'Environnement   (France)

Author keywords

[No Author keywords available]

Indexed keywords

PROTEIN TYROSINE KINASE; ZINC FINGER PROTEIN;

ANIMAL CELL; ARTICLE; BRAIN DEVELOPMENT; EMBRYO; GENE EXPRESSION; GENE EXPRESSION REGULATION; HOMEOBOX; MORPHOGENESIS; MOUSE; NONHUMAN; PRIORITY JOURNAL; RHOMBENCEPHALON; SIGNAL TRANSDUCTION; ZEBRA FISH;

ANIMALIA; DANIO RERIO; VERTEBRATA;

EID: 0030221204     PISSN: 00121606     EISSN: None     Source Type: Journal    
DOI: 10.1006/dbio.1996.0173     Document Type: Article

References (79)

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., Hoist, 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 characterization of a family of ligands for eph-related tyrosine kinase receptors. EMBO J. 13, 3757-3762.
4. Bennett, B. D., Zeigler, F. C., Gu, Q., 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.
5. 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 mouse embryo in regions of the hindbrain and newly forming somites. Mol. Cell. Biol. 15, 4921-4929.
6. Birgbauer, E., and Fraser, S. E. (1994). Violation of cell lineage restriction compartments in the chick hindbrain. Development 120, 1347-1356.
7. Bouillet, P., Oulad-Abdelghani, M., Vicaire, S., Garnier, J-M., Schuhbaur, B., Dollé, 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 Stra1 (Mouse LERK-2/Eplg2). Dev. Biol. 170, 420-433.
8. Carpenter, E. M., Goddard, J. M., Chisaka, O., Manley, N. R., and Capecchi, M. R. (1993). Loss of Hox-A1 (Hox-1.6) function results in the reorganization of the murine hindbrain. Development 118, 1063-1075.
9. Chabot, B., Stephenson, D. A., Chapman, V. M., Besmer, P., and Bernstein, A. (1988). The proto-oncogene c-kit encoding a transmembrane tyrosine kinase receptor maps to the mouse W locus. Nature 335, 88-89.
10. Chan, J., and Watt, V. M. (1991). eek and erk, new members of the eph subclass of receptor protein-tyrosine kinases. Oncogene 6, 1057-1061.
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. Chisaka, O., Musci, T. S., and Capecchi, M. R. (1992). Developmental defects of the ear, cranial nerves and hindbrain resulting from targeted disruption of the mouse homeobox gene Hox-1.6. Nature 355, 516-520.
14. Ciossek, T., Millauer, B., and Ullrich, A. (1995). Identification of alternatively spliced mRN As encoding variants of MDK1, a novel receptor tyrosine kinase expressed in the murine nervous system. Oncogene 10, 97-108.
15. Conlon, R. A. (1995). Retinoic acid and pattern formation in vertebrates. Trends Genet. 11, 314-319.
16. Conlon, R. A., and Rossant, J. (1992). Exogenous retinoic acid rapidly induces anterior ectopic expression of murine Hox-2 genes in vivo. Development 116, 357-368.
17. Davis, S., Gale, N. W., Aldrich, T. H., Maisonpierre, P. C., Lohtak, 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.
18. Décimo, D., Georges-Labouesse, E., and Dollé, P. (1995). In situ hybridization of nucleic acid probes to cellular RNA. In "Gene Probes: A Practical Approach Book" (B. D. Hames and S. Higgins, Eds.), Vol. II. Oxford Univ. Press, London, in press.
19. Dollé, P., Lufkin, T., Krumlauf, R., Mark, M., Duboule, D., and Chambon, P. (1993). Local alterations of Krox-20 and Hox gene expression in the hindbrain suggest lack of rhombomeres 4 and 5 in homozygote null Hoxa-1 (Hox-1.6) mutant embryos. Proc. Natl. Acad. Sci. USA 90, 7666-7670.
20. 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 25kDa tectal protein related to ligands for Eph receptor tyrosine kinases. Cell 82, 359-370.
21. Ekker, M., Wegner, J., Akimenko, M. A., and Westerfield, M. (1992). Coordinate embryonic expression of three zebrafish engrailed genes. Development 116, 1001-1010.
22. 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 receptor tyrosine kinase family. Mech. Dev. 52, 319-341.
23. Fantl, W. J., Johnson, D. E., and Williams, L. T. (1993). Signalling by receptor tyrosine kinases. Annu. Rev. Biochem. 62, 453-481.
24. Fraser, S., Keynes, R., and Lumsden, A. (1990). Segmentation in the chick embryo hindbrain is defined by cell lineage restriction. Nature 344, 431-435.
25. Frohman, M. A., Boyle, M., and Martin, G. R. (1990). Isolation of the mouse Hox-2.9 gene: Analysis of embryonic expression suggests that positional information along the anterior-posterior axis is specified by mesoderm. Development 110, 589-607.
26. 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.
27. Geissler, E. N., Ryan, M. A., and Housman, D. E. (1988). The dominant-white spotting (W) locus of the mouse encodes the c-kit proto-oncogene. Cell 55, 185-192.
28. Gendron-Maguire, M., Mallo, M., Zhang, M., and Gridley, T. (1993). Hoxa-2 mutant mice exhibit homeotic transformation of skeletal elements derived from cranial neural crest. Cell 75, 1317-1331.
29. Gilardi-Hebenstreit, P., Nieto, M. A., Frain, M., Mattei, M. G., Chestier, A., Wilkinson, D. G., and Charnay, P. (1992). An Eph-related receptor protein tyrosine kinase gene segmentally expressed in the developing mouse hindbrain. Oncogene 7, 2499-2506.
30. Guthrie, S. (1995). The status of the neural segment. Trends Neurosci. 18, 74-79.
31. Hauptmann, G., and Gerster, T. (1994). Two color whole-mount in situ hybridizations on zebrafish and Drosophila embryos. Trends Genet. 10, 266.
32. Henkemeyer, M., Marengere, L. E., McGlade, J., Olivier, J. P., Conlon, R. A., Holmyard, 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.
33. Hirsch, M-R., Gaugler, L., Deagostini-Bazin, H., Bally-Cuif, L., and Goridis, C. (1990). Identification of positive and negative regulatory elements governing cell-type specific expression of the neural cell adhesion molecule gene. Mol. Cell. Biol. 10, 1959-1968.
34. Hunt, P., Gulisano, M., Cook, M., Sham, M. H., Faiella, A., Wilkinson, D., Boncinelli, E., and Krumlauf, R. (1991). A distinct Hox code for the branchial region of the vertebrate head. Nature 353, 861-864.
35. Jones, F. S., Crossin, K. L., Cunningham, B. A., and Edelman, G. M. (1990). Identification and characterization of the promoter for the cytotactin gene. Proc. Natl. Acad. Sci. USA 87, 6497-6501.
36. Jones, F. S., Prediger, E. A., Bittner, D. A., Robertis, E. M., and Edelman, G. M. (1992). Cell adhesion molecules as targets for Hox genes: Neural cell adhesion molecule promoter activity is modulated by cotransfection with Hox-2.5 and -2.4. Proc. Natl. Acad. Sci. USA 89, 2086-2090.
37. Jones, F. S., Holst, B. D., Minowa, O., DeRobertis, E. M., and Edelman, G. M. (1993). Binding and transcriptional activation of the promoter for the neural cell adhesion molecule by HoxC6 (Hox-3.3). Proc. Natl. Acad. Sci. USA 90, 6557-6561.
38. Kozlosky, C. J., Maraskovsky, E., McGrew, J. T., Vanden Bos, T., Teepe, M., Lyman, S. D., Srinivasan, S., Fletcher, F. A., Gayle, R. B., III, Cerretti, D. P., and Beckmann, M. P. (1995). Ligands for the receptor tyrosine kinases hek and elk: Isolation of cDNAs encoding a family of proteins. Oncogene 10, 299-306.
39. Krumlauf, R. (1993). Hox genes and pattern formation in the branchial region of the vertebrate head. Trends Genet. 9, 106-112.
40. Letwin, K., Yee, S. P., and Pawson, T. (1988). Novel protein-tyrosine kinase cDNAs related to fps/fes and eph cloned using antiphosphotyrosine antibody. Oncogene 3, 621-627.
41. Lufkin, T., Dierich, A., LeMeur, M., Mark, M., and Chambon, P. (1991). Disruption of the Hox-1.6 homeobox gene results in defects in a region corresponding to its rostral domain of expression. Cell 66, 1105-1119.
42. Lumsden, A. (1990). The cellular basis of segmentation in the developing hindbrain. Trends Neurosci. 13, 329-335.
43. Lumsden, A., and Keynes, R. (1989). Segmental patterns of neuronal development in the chick hindbrain. Nature 337, 424-428.
44. Maden, M., and Holder, N. (1992). Retinoic acid and development of the central nervous system. BioEssays 14, 431-438.
45. Maden, M., Horton, C., Graham, A., Leonard, L., Pizzey, J., Siegenthaler, G., Lumsden, A., and Eriksson, U. (1992). Domains of cellular retinoic acid-binding protein I (CRABP I) expression in the hindbrain and neural crest of the mouse embryo. Mech. Dev. 37, 13-23.
46. Maden, M., Hunt, P., Eriksson, U., Kuroiwa, A., Krumlauf, R., and Summerbell, D. (1991). Retinoic acid-binding protein, rhombomeres and the neural crest. Development 111, 35-43.
47. 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.
48. Mark, M., Lufkin, T., Vonesch, J. L., Ruberte, E., Olivo, J. C., Dollé, P., Gorry, P., Lumsden, A., and Chambon, P. (1993). Two rhombomeres are altered in Hoxa-1 mutant mice. Development 119, 319-328.
49. Marshall, H., Nonchev, S., Sham, M. H., Muchamore, I., Lumsden, A., and Krumlauf, R. (1992). Retinoic acid alters hindbrain Hox code and induces transformation of rhombomeres 2/3 into a 4/5 identity. Nature 360, 737-741.
50. Murphy, P., Davidson, D. R., and Hill, R. E. (1989). Segment-specific expression of a homoeobox-containing gene in the mouse hindbrain. Nature 341, 156-159.
51. Murphy, P., and Hill, R. E. (1991). Expression of the mouse labial-like homeobox-containing genes, Hox 2.9 and Hox 1.6, during segmentation of the hindbrain. Development 111, 61-74.
52. 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.
53. Oxtoby, E., and Jowett, T. (1993). Cloning of the zebrafish Krox-20 gene (krx-20) and its expression during hindbrain development. Nucleic Acids Res. 21, 1087-1095.
54. Pasquale, E. B. (1991). Identification of chicken embryo kinase 5, a developmentally regulated receptor-type tyrosine kinase of the Eph family. Cell Regul. 2, 523-534.
55. Pawson, T., and Bernstein, A. (1990). Receptor tyrosine kinases: Genetic evidence for their role in Drosophila and mouse development. Trends Genet. 6, 350-356.
56. Rijli, F. M., Mark, M., Lakkaraju, S., Dierich, A., Dollé, P., and Chambon, P. (1993). A homeotic transformation is generated in the rostral branchial region of the head by disruption of Hoxa-2, which acts as a selector gene. Cell 75, 1333-1349.
57. Roy, B., Taneja, R., and Chambon, P. (1995). Synergistic activation of retinoic acid (RA)-responsive genes and induction of embryonal carcinoma cell differentiation by an RA receptor a (RARα)-, RARβ, or RARγ-selective ligand in combination with a retinoid X receptor-specific ligand. Mol. Cell. Biol. 15, 6481-6487.
58. Ruberte, E., Dollé, P., Chambon, P., and Morriss-Kay, G. (1991). Retinoic acid receptors and cellular retinoid binding proteins. II. Their differential pattern of transcription during early morphogenesis in mouse embryos. Development 111, 45-60.
59. Ruberte, E., Friederich, V., Morriss-Kay, G., and Chambon, P. (1992). Differential distribution patterns of CRABP I and CRABP II transcripts during mouse embryogenesis. Development 115, 973-987.
60. Sajjadi, F. G., and Pasquale, E. B. (1993). Five novel avian Eph-related tyrosine kinases are differentially expressed. Oncogene 8, 1807-1813.
61. 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, 769-778.
62. Schlessinger, J., and Ullrich, A. (1992). Growth factor signaling by receptor tyrosine kinases. Neuron 9, 383-391.
63. Schneider-Maunoury, S., Topilko, P., Seitandou, T., Levi, G., Cohen-Tannoudji, M., Pournin, S., Babinet, C., and Charnay, P. (1993). Disruption of Krox-20 results in alteration of rhombomeres 3 and 5 in the developing hindbrain. Cell 75, 1199-1214.
64. Schulte-Merker, S., Hammerschmidt, M., Beuchle, D., Cho, K. W., De Robertis, E. M., and Nüsslein-Volhard, C. (1994). Expression of the zebrafish goosecoid and no tail gene products in wild-type and mutant no tail embryos. Development 120, 843-852.
65. Sham, M. H., Vesque, C., Nonchev, S., Marshall, H., Frain, M., Gupta, R. D., Whiting, J., Wilkinson, D., Charnay, P., and Krumlauf, R. (1993). The zinc finger gene Krox20 regulates HoxB2 (Hox2.8) during hindbrain segmentation. Cell 72, 183-196.
66. Skorstengaard, K., Jensen, M. S., Sahl, P., Petersen, T. E., and Magnusson, S. (1986). Complete primary structure of bovine plasma fibronectin. Eur. J. Biochem. 161, 441-453.
67. Snider, W. D. (1994). Function s of the neurotrophins during nervous system development: What the knockouts are teaching us. Cell 77, 627-638.
68. Stachel, S. E., Grunwald, D. J., and Myers, P. Z. (1993). Lithium perturbation and goosecoid expression identify a dorsal specification pathway in the pregastrula zebrafish. Development 117, 1261-1274.
69. Sundin, O. H., and Eichele, G. (1990). A homeo domain protein reveals the metameric nature of the developing chick hindbrain. Genes Dev. 4, 1267-1276.
70. Swiatek, P. J., and Gridley, T. (1993). Perinatal lethality and defects in hindbrain development in mice homozygous for a targeted mutation of the zinc finger gene Krox20. Genes Dev. 7, 2071-2084.
71. Taneja, R., Bouillet, P., Boylan, J. F., Gaub, M-P., Roy, B., Gudas, L. J., and Chambon, P. (1995). Reexpression of retinoic acid receptor (RAR)γ or overexpression of RARα or RAR/3 in RARγ-null F9 cells reveals a partial functional redundancy between the three RAR types. Proc. Natl. Acad. Sci. USA 92, 7854-7858.
72. Thisse, B., Thisse, C., and Weston, J. A. (1995). Novel FGF receptor (Z-FGFR4) is dynamically expressed in mesoderm and neurectoderm during early zebrafish embryogenesis. Dev. Dyn. 203, 377-391.
73. Thisse, C., Thisse, B., Halpern, M., and Postlethwait, J. H. (1994). Goosecoid expression in neurectoderm and mesendoderm is disrupted in zebrafish Cyclops gastrulas. Dev. Biol. 164, 420-429.
74. Ullrich, A., and Schlessinger, J. (1990). Signal transduction by receptors with tyrosine kinase activity. Cell 6, 203-212.
75. 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.
76. Wilkinson, D., Bhatt, S., Chavier, P., Bravo, R., and Charnay, P. (1989a). Segment-specific expression of a zinc finger gene in the developing nervous system of the mouse. Nature 337, 461-464.
77. Wilkinson, D. G., Bhatt, S., Cook, M., Boncinelli, E., and Krumlauf, R. (1989b). Segmental expression of Hox-2 homeobox-containing genes in the developing mouse hindbrain. Nature 341, 405-409.
78. 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.
79. 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.