Signalling by the Drosophila epidermal growth factor receptor is required for the specification and diversification of embryonic muscle progenitors

Development

Volumn 125, Issue 11, 1998, Pages 2075-2086

  Buff, Eugene ^a   Carmena, Ana ^b   Gisselbrecht, Stephen ^a   Jiménez, Fernando ^b   Michelson, Alan M ^a  

^a BRIGHAM AND WOMEN S HOSPITAL   (United States)

^b UNIVERSIDAD AUTÓNOMA DE MADRID   (Spain)

Author keywords

Drosophila; Epidermal growth factor receptor; Myogenesis; Progenitor cell

Indexed keywords

EPIDERMAL GROWTH FACTOR RECEPTOR;

ANIMAL TISSUE; APOPTOSIS; ARTICLE; CONTROLLED STUDY; DROSOPHILA; EMBRYO; GENE EXPRESSION; GENE INDUCTION; MESODERM; MUSCLE DEVELOPMENT; NONHUMAN; PRIORITY JOURNAL; RECEPTOR UPREGULATION; STEM CELL;

ANIMALS; APOPTOSIS; CELL DIFFERENTIATION; DROSOPHILA; DROSOPHILA PROTEINS; EMBRYONIC INDUCTION; EPIDERMAL GROWTH FACTOR; LIGANDS; MEMBRANE PROTEINS; MESODERM; MUSCLES; PHOSPHOPROTEINS; RECEPTOR, EPIDERMAL GROWTH FACTOR; STEM CELLS; TIME FACTORS;

EID: 0031805618     PISSN: 09501991     EISSN: None     Source Type: Journal    
DOI: None     Document Type: Article

References (87)

1. Abrams, J. M., White, K., Fessier, L. I. and Steller, H. (1993). Programmed cell death during Drosophila embryogenesis. Development 117, 29-43.
2. Amaya, E., Musci, T. J. and Kirschner, M. W. (1991). Expression of a dominant negative mutant of the FGF receptor disrupts mesoderm formation in Xenopus embryos. Cell 66, 257-270.
3. Baker, R. and Schubiger, G. (1996). Autonomous and nonautonomous Notch functions for embryonic muscle and epidermis development in Drosophila. Development 122, 617-626.
4. Bate, M. (1990). The embryonic development of larval muscles in Drosophila. Development 110, 791-804.
5. Bate, M. (1993). The mesoderm and its derivatives. In The Development of Drosophila melanogaster (ed. M. Bate and A. Martinez Arias), pp. 1013-1090. Cold Spring Harbor Laboratory Press.
6. Bate, M. and Baylies, M. (1996). Intrinsic and extrinsic determinants of mesodermal differentiation in Drosophila. Semin. Cell Dev. Biol. 7, 103-111.
7. Bate, M., Rushton, E. and Frasch, M. (1993). A dual requirement for neurogenic genes in Drosophila myogenesis. Development 149-161.
8. Baylies, M. K., Arias, A. M. and Bate, M. (1995). wingless is required for the formation of a subset of muscle founder cells during Drosophila embryogenesis. Development 121, 3829-3837.
9. Baylies, M. K. and Bate, M. (1996). twist: A myogenic switch in Drosophila. Science 272, 1481-1484.
10. Beiman, M., Shilo, B. Z. and Volk, T. (1996). Heartless, a Drosophila FGF receptor homolog, is essential for cell migration and establishment of several mesodermal lineages. Genes Dev. 10, 2993-3002.
11. Bier, E., Jan, L. Y. and Jan, Y. N. (1990). rhomboid, a gene required for dorsoventral axis establishment and peripheral nervous system development in Drosophila melanogaster. Genes Dev. 4, 190-203.
12. Bourgouin, C., Lundgren, S. E. and Thomas, J. B. (1992). apterous is a Drosophila LIM domain gene required for the development of a subset of embryonic muscles. Neuron 9, 549-561.
13. Brand, A. H. and Perrimon, N. (1993). Targeted gene expression as a means of altering cell fates and generating dominant phenotypes. Development 118, 401-415.
14. Callahan, C. A., Bonkovsky, J. L., Scully, A. L. and Thomas, J. B. (1996). derailed is required for muscle attachment site selection in Drosophila. Development 122, 2761 -2767.
15. Carmena, A., Bate, M. and Jiménez, F. (1995). lethal of scute, a proneural gene, participates in the specification of muscle progenitors during Drosophila embryogenesis. Genes Der. 9, 2373-2383.
16. Carmena, A., Murugasu-Oei, B., Menon, D., Jimenéz, F. and Chia, W. (1998). inscuteable and numb mediate asymmetric muscle progenitor cell divisions during Drosophila myogenesis. Genes Dev. 12, 304-315.
17. Clifford, R. and Schüpbach, T. (1992). The torpedo (DER) receptor tyrosine kinase is required at multiple times during Drosophila embryogenesis. Development 115, 853-872.
18. Corbin, V., Michelson, A. M., Abmayr, S. M., Neel, V., Alcamo, E., Maniatis, T. and Young, M. W. (1991). A role for the Drosophila neurogenic genes in mesoderm differentiation. Cell 67, 311-323.
19. Cossu, G., Tajbakhsh, S. and Buckingham, M. (1996). How is myogenesis initiated in the embryo? Trends Genet. 12, 218-223.
20. Dohrmann, C., Azpiazu, N. and Frasch, M. (1990). A new Drosophila homeobox gene is expressed in mesodermal precursor cells of distinct muscles during embryogenesis. Genes Dev. 4, 2098-2111.
21. Dunin Borkowski, O. M., Brown, N. H. and Bate, M. (1995). Anteriorposterior subdivision and the diversification of the mesoderm in Drosophila. Development 121, 4183-4193.
22. Fantl, W. J., Johnson, D. E. and Williams, L. T. (1993). Signalling by receptor tryrosine kinases. Ann. Rev. Biochem. 62, 453-481.
23. Frasch, M. (1995). Induction of visceral and cardiac mesoderm by ectodermal Dpp in the early Drosophila embryo. Nature 374, 646-467.
24. Frasch, M., Hoey, T., Rushlow, C., Doyle, H. and Levine, M. (1987). Characterization and localization of the Even skipped prolein of Drosophila. EMBO J 6, 749-759.
25. Freeman, M. (I994). The spitz gene is required for photoreceptor determination in the Drosophila eye where it interacts with the EGF receptor. Mech. Dev. 48, 25-33.
26. Freeman, M. (1996). Reiterative use of the EGF receptor triggers differentiation of all cell types in the Drosophila eye. Cell 87, 651-660.
27. Freeman, M. (1997). Cell determination strategies in the Drosophila eye. Development 124, 261-270.
28. Gabay, L., Scholz, H., Golembo, M., Klaes, A., Shilo, B. Z. and Klambt, C. (1996). EGF receptor signalling induces pointed PI transcription and inactivates Van protein in the Drosophila embryonic ventral ectoderm. Development 122, 3355-3362.
29. Garcia-Bellido, A. (1977). Inductive mechanisms in the process of wing vein formation in Drosophila. Roux's Arch. Dev. Biol. 182, 93-106.
30. Gaul, U., Seifert, E., Schuh, R. and Jackle, H. (1987). Analysis of Krüppel protein distribution during early Drosophila development reveals posttranscriptional regulation. Cell 50, 639-647.
31. Gisselbrecht, S., Skeath, J. B., Doe, C. Q. and Michelson, A. M. (1996). 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. 10, 3003-3017.
32. Golembo, M., Raz, E. and Shilo, B.-Z. ( 1996a). The Drosophila embryonic midline is the site of Spitz processing, and induces activation of the EGF receptor in the ventral ectoderm. Development 122, 3363-3370.
33. Golembo, M., Schweitzer, R., Freeman, M. and Shilo, B.-Z. (1996b). argos transcription is induced by the Drosophila EGF receptor pathway to form an inhibitory feedback loop. Development 122, 223-230.
34. Greenwood, S. and Struhl, G. (1997). Different levels of Ras activity can specify distinct transcriptional and morphological consequences in early Drosophila embryos. Development 124, 4879-4886.
35. Greig, S. and Akam, M. (1993). Homeotic genes autonomously specify one aspect of pattern in the Drosophila mesoderm. Nature 362, 630-632.
36. Heberlein, U., Hariharan, I. K. and Rubin, G. M. (1993). Star is required for neuronal differentiation in the Drosophila retina and displays dosagesensitive interactions with Rasl. Dev. Biol. 160, 51-63.
37. Katz, W. S., Hill, R. J., Clandinin, T. R. and Sternberg, P. W. (1995). Different levels of the C. elegans growth factor LIN-3 promote distinct vulval precursor fates. Cell 82, 297-307.
38. Keller, C. A., Erickson, M. S. and Abmayr, S. M. (1997). Misexpression of nautilus induces myogenesis in cardioblasts and alters the pattern of somatic muscle fibers. Dev. Biol. 181, 197-212.
39. Klambt, C. (1993). The Drosophila gene pointed encodes two ETS-like proteins which are involved in the development of midline glial cells. Development 111, 163-176.
40. Kolodkin, A. L., Pickup, A. T., Lin, D. M., Goodman, C. S. and Banerjee, U. (1994). Characterization of Star and its interactions with sevenless and EGF receptor during photoreceptor cell development in Drosophila. Development 120, 1731-1745.
41. Lage, P. Z., Jan, Y. N. and Jarman, A. P. (1997). Requirement for EGF receptor signalling in neural recruitment during formation of Drosophila chordotonal sense organ clusters. Curr. Biol. 7, 166-175.
42. Lawrence, P. A., Bodmer, R. and Vincent, J.-P. (1995). Segmental patterning of heart precursors in Drosophila. Development 121, 4303-4308.
43. Lee, Y. M., Park, T., Schulz, R. A. and Kim, Y. (1997). Twist-mediated activation of the NK-4 homeobox gene in the visceral mesoderm of Drosophila requires two distinct clusters of E-box regulatory elements. J. Biol. Chem. 272, 17531-17541.
44. Lillien, L. (1995). Changes in retinal cell fate induced by overexpression of EGF receptor. Nature 377, 158-162.
45. Lilly, B., Zhao, B., Ranganayakulu, G., Paterson, B. M., Schultz, R. A. and Olson, E. N. (1995). Requirement of MADS domain transcription factor DMEF2 for muscle formation in Drosophila. Science 267, 688-693.
46. Marshall, C. J. (1995). Specificity of receptor tyrosine kinase signalling: transient versus sustained extracellular signal-regulated kinase activation. Cell 80, 179-185.
47. Mayer, U. and Nüsslein-Volhard, C. (1988). A group of genes required for pattern formation in the ventral ectoderm of the Drosophila embryo. Genes Dev. 2, 1496-1511.
48. Michelson, A. M. (1994). Muscle pattern diversification in Drosophila is determined by the autonomous function of homeotic genes in the embryonic mesoderm. Development 120, 755-768.
49. Michelson, A. M., Abmayr, S. M., Bate, M., Martinez Arias, A. and Maniatis, T. (1990). Expression of a MyoD family member prefigures muscle pattern in Drosophila embryos. Genes Der. 4, 2086-2097.
50. Michelson, A. M., Gisselbrecht, S., Zhou, Y., Back, K.-H. and Buff, E. M. (1998). Dual functions of the Heartless fibroblast growth factor receptor in development of the Drosophila embryonic mesoderm. Dev. Genet, (in press).
51. Molkentin, J. D. and Olson, E. N. (1996). Defining the regulatory networks for muscle development. Curr: Opin. Genet. Dev. 6, 445-453.
52. Nelson, R. E., Fessier, L. I.,Takagi, Y., Blumberg, B., Keene, D. R., Olson, P. F., Parker, C. G. and Fessier, J. H. (1994). Peroxidasin: a novel enzymematrix protein of Drosophila development. EMBO J. 13, 3438-3447.
53. Noll, R., Sturtevant, M. A., Gollapudi, R. R. and Bier, E. (1994).New functions of the Drosophila rhomboid gene during embryonic and adult development are revealed by a novel genetic method, enhancer piracy. Development 120, 2329-2338.
54. Okabe, M. and Okano, H, (1997). Two-step induction of chordotonal organ precursors in Drosophila embryogenesis. Development 124, 1045-1053.
55. O'Neill, J. W. and Bier, E. (1994). Double-label in situ hybridization using biotin and digoxigenin-tagged RNA probes. Biotechniques 17, 870-875.
56. Park, M., Wu, X., Golden, K., Axelrod, J. D. and Bodmer, R. (1996). The Wingless signalling pathway is directly involved in Drosophila heart development. Dev. Biol. 177, 104-116.
57. Paterson, B. M., Walldorf, U., Eldridge, J., Dubendorfer, A., Frasch, M. and Gehring, W. J. (1991). The Drosophila homologue of vertebrate myogenic-determination genes encodes a transiently expressed nuclear protein marking primary myogenic cells. Proc. Nat. Acad. Sci. USA 88, 3782-3786.
58. Perrimon, N. and Perkins, L. A. (1997). There must be 50 ways to rule the signal: the case of the Drosophila EGF receptor. Cell 89, 13-16.
59. Queenan, A. M., Ghabrial, A. and Schüpbach, T. (1997). Ectopic activation of torpedo/Egfr, a Drosophila receptor tyrosine kinase, dorsalizes both the eggshell and the embryo. Development 124, 3871-3880.
60. Ranganayakulu, G., Schulz, R. A. and Olson, E. N. (1996). Wingless signalling induces nautilus expression in the ventral mesoderm of the Drosophila embryo. Dev. Biol, 176, 143-148.
61. Rawls, A. and Olson, E. N. (1997). MyoD meets its maker. Cell 89, 5-8.
62. Raz, E. and Shilo, B.-Z. (1992). Dissection of the faint little ball (flb) phenotype: determination of the development of the Drosophila central nervous system by early interactions in the ectoderm. Development 114, 113-123.
63. Ruiz Gomez, M. and Bate, M. (1997). Segregation of myogenic lineages in Drosophila requires Numb. Development 124, 4857-4866.
64. Ruiz Gomez, M., Romani, S., Hartmann, C., Jackle, H. and Bate, M. (1997). Specific muscle identities are regulated by Krüppel during Drosophila embryogenesis. Development 124, 3407-3414.
65. Ruohola-Baker, H., Grell, E., Chou, T.-B., Baker, D., Jan, L. Y. and Nung, J. Y. (1993). Spatially localized rhomboid is required for establishment of the dorsal-ventral axis in Drosophila oogenesis. Cell 73, 953-965.
66. Rushton, E., Drysdale, R., Abmayr, S. M., Michelson, A. M. and Bate, M. (1995). Mutations in a novel gene, myobfast city, provide evidence in support of the founder cell hypothesis for Drosophila muscle development. Development 121, 1979-1988.
67. Rutledge, B. J., Zhang, K., Bier, E., Jan, Y. N. and Perrimon, N. (1992). The Drosophila spitz gene encodes a putative EGF-Iike growth factor involved in dorsal-ventral axis formation and neurogenesis. Genes Dev. 6, 1503-1517.
68. Schweitzer, R., Howes, R., Smith, R., Shilo, B.-Z. and Freeman, M. (1995a). Inhibition of Drosophila EGF receptor activation by the secreted protein Argos. Nature 376, 699-702.
69. Schweitzer, R., Shaharabany, M., Seger, R. and Shilo, B.-Z. (1995b). Secreted Spitz triggers the DER signalling pathway and is a limiting component in embryonic ventral ectoderm determination. Genes Dev. 9, 1518-1529.
70. Schweitzer, R. and Shilo, B.-Z. (1997). A thousand and one roles for the Drosophila EGF receptor. Trends Genet. 13, 191-196.
71. Shishido, E., Ono, N., Kojima, T. and Saigo, K. (1997). Requirements of DFR1/Heartless, a mesoderm-specific Drosophila FGF-receptor, for the formation of heart, visceral and somatic muscles, and ensheathing of longitudinal axon tracts in CNS. Development 124, 2119-2128.
72. Spradling, A. C. (1986). P Element-Mediated Transformation. In Drosophila: A Practical Approach (ed. D. B. Roberts), pp. 175-197. IRL Press: Oxford, Washington DC.
73. Staehling-Hampton, K., Hoffmann, F. M., Baylies, M. K., Rushton, E. and Bate, M. (1994). dpp induces mesodermal gene expression in Drosophila. Nature 372, 783-786.
74. Sturtevant, M. A., Roark, M. and Bier, E. (1993). The Drosophila rhomboid gene mediates the localized formation of wing veins and interacts genetically with components of the EGFR signalling pathway. Genes Dev. 7, 961-973.
75. Sturtevant, M. A., Roark, M., O'Neill, J. W., Biehs, B., Colley, N. and Bier, E. (1996). The Drosophila Rhomboid protein is concentrated in patches at the apical cell surface. Dev. Biol 174, 298-309.
76. Sziits, D., Freeman, M. and Bienz, M. (1997). Antagonism between EGFR and Wingless signalling in the larval cuticle of Drosophila. Development 124, 3209-3219.
77. Tajbakhsh, S. and Cossu, G. (1997). Establishing myogenic identity during somitogenesis. Curr. Opin. Genet. Dev: 7, 634-641.
78. Tautz, D. and Pfeifle, C. (1989). A nonradioactive in situ hybridization method for the localization of specific RNAs in Drosophila embryos reveals a translational control of the segmentation gene hunchback. Chromosoma 98, 81-85.
79. Tio, M., Ma, C. and Moses, K. (1994). spitz, a Drosophila homolog of transforming growth factor-α, is required in the founding photoreceptor cells of the compound eye facets. Mech. Dev. 48, 13-23.
80. Tio, M. and Moses, K. (1997). The Drosophila TGF-α homolog spitz acts in photoreceptor recruitment in the developing retina. Development 124, 343-351.
81. van der Geer, P., Hunter, T. and Lindberg, R. A. (1994). Receptor-protein tyrosine kinases and their signal transduction pathways. Ann. Rev. Cell Biol 10, 251-337.
82. White, K., Grether, M. E., Abrams, J. M., Young, L., Farrell, K. and Steiler, H. (1994). Genetic control of programmed cell death in Drosophila. Science 264, 677-683.
83. Wieschaus, E. and Nüsslein-Volhard, C. (1986). Looking at Embryos. In Drosophila: A Practical Approach (ed. D. B. Roberts), pp. 199-227. IRL Press: Oxford, Washington DC.
84. Williams, J. A., Bell, J. B. and Carroll, S. B. (1991). Control of Drosophila wing and haltere development by the nuclear vestigial gene product. Genes Dev. 5, 2481-2495.
85. Yarnitzky, T., Min, L. and Volk, T. (1997). The Drosophila neureguhn homolog Vein mediates inductive interactions between myotubes and their epidermal attachment cells. Genes Dev. 11, 2691-2700.
86. Yin, Z., Xu, X.-L. and Frasch, M. (1997). Regulation of the Twist target gene tinman by modular cis-regulatory elements during early mesoderm development. Development 124, 4971-4982.
87. Zak, N. B., Wides, R. J., Schejter, E. D., Raz, E, and Shilo, B.-Z. (1990). Localization of the DER/flb protein in embryos: implications on the faint little ball lethal phenotype. Development 109, 865-874.