Crossref journal-article
The Company of Biologists
Development (237)
Abstract

ABSTRACT Genes of the ventrolateral group in Drosophila are dedicated to developmental regulation of Egfr signaling in multiple processes including wing vein development. Among these genes, Egfr encodes the Drosophila EGF-Receptor, spitz (spi) and vein (vn) encode EGF-related ligands, and rhomboid (rho) and Star (S) encode membrane proteins. In this study, we show that rho-mediated hyperactivation of the EGFR/MAPK pathway is required for vein formation throughout late larval and early pupal development. Consistent with this observation, rho activity is necessary and sufficient to activate MAPK in vein primordium during late larval and early pupal stages. Epistasis studies using a dominant negative version of Egfr and a ligand-independent activated form of Egfr suggest that rho acts upstream of the receptor. We show that rho and S function in a common aspect of vein development since loss-of-function clones of rho or S result in nearly identical non-autonomous loss-of-vein phenotypes. Furthermore, mis-expression of rho and S in wild-type and mutant backgrounds reveals that these genes function in a synergistic and co-dependent manner. In contrast, spi does not play an essential role in the wing. These data indicate that rho and S act in concert, but independently of spi, to promote vein development through the EGFR/MAPK signaling pathway.

Bibliography

Guichard, A., Biehs, B., Sturtevant, M. A., Wickline, L., Chacko, J., Howard, K., & Bier, E. (1999). rhomboid and Star interact synergistically to promote EGFR/MAPK signaling during Drosophila wing vein development. Development, 126(12), 2663–2676.

Authors 7
  1. Annabel Guichard (first)
  2. Brian Biehs (additional)
  3. Mark A. Sturtevant (additional)
  4. Laura Wickline (additional)
  5. Julie Chacko (additional)
  6. Katherine Howard (additional)
  7. Ethan Bier (additional)
References 54 Referenced 124
  1. 10.1101/gad.6.9.1752 / Genes Dev. / The Drosophila gene Hairless encodes a novel basic protein that controls alternative cell fates in adult sensory organ development by Bang (1992)
  2. 10.1242/dev.125.21.4245 / Development / Boundaries in the Drosophila wing imaginal disc organize vein-specific genetic programs by Biehs (1998)
  3. {'key': '2023090607371984700_DEVELOP_126_12_2663C3', 'first-page': '19', 'article-title': 'EGF-Receptor and TGF-β-like Dpp signaling during Drosophila development', 'volume-title': 'Hormones and Growth Factors in Development and Neoplasia. (ed', 'author': 'Bier', 'year': '1998'} / Hormones and Growth Factors in Development and Neoplasia. (ed / EGF-Receptor and TGF-β-like Dpp signaling during Drosophila development by Bier (1998)
  4. 10.1002/(SICI)1521-1878(199803)20:3<189::AID-BIES1>3.0.CO;2-N / BioEssays / Localized activation of RTK/MAPK pathways during Drosophila development by Bier (1998)
  5. 10.1101/gad.4.2.190 / Genes Dev. / rhomboid, a gene required for dorsoventral axis establishment and peripheral nervous system development in Drosophila melanogaster by Bier (1990)
  6. 10.1242/dev.118.2.401 / Development / Targeted gene expression as a means of altering cell fates and generating dominant phenotypes by Brand (1993)
  7. 10.1242/dev.125.11.2075 / Development / Signaling by the Drosophila epidermal growth factor receptor is required for the specification and diversification of embryonic muscle progenitors by Buff (1998)
  8. 10.1002/j.1460-2075.1994.tb06768.x / EMBO J / Targeted expression of the signaling molecule decapentaplegic induces pattern duplications and growth alterations in Drosophila wings by Capdevila (1994)
  9. {'key': '2023090607371984700_DEVELOP_126_12_2663C9', 'first-page': '531', 'article-title': 'Molecular analysis of the Drosophila EGF receptor homolog reveals that several genetically defined classes of alleles cluster in subdomains of the receptor protein', 'volume-title': 'Genetics', 'author': 'Clifford', 'year': '1994'} / Genetics / Molecular analysis of the Drosophila EGF receptor homolog reveals that several genetically defined classes of alleles cluster in subdomains of the receptor protein by Clifford (1994)
  10. 10.1098/rspb.1990.0100 / Proc. R Soc. Lond. B Biol. Sci. / Behaviour of cells mutant for an EGF receptor homologue of Drosophila in genetic mosaics by Díaz-Benjumea (1990)
  11. 10.1242/dev.120.3.569 / Development / The sevenless signalling cassette mediates Drosophila EGF receptor function during epidermal development by Díaz-Benjumea (1994)
  12. 10.1242/dev.116.2.335 / Development / Identifying targets of the rough homeobox gene of Drosophila: evidence that rhomboid functions in eye development by Freeman (1992)
  13. 10.1016/S0092-8674(00)81385-9 / Cell / Reiterative use of the EGF receptor triggers differentiation of all cell types in the Drosophila eye by Freeman (1996)
  14. 10.1126/science.277.5329.1103 / Science / In situ activation pattern of Drosophila EGF receptor pathway during development by Gabay (1997)
  15. 10.1242/dev.124.18.3535 / Development / MAP kinase in situ activation atlas during Drosophila embryogenesis by Gabay (1997)
  16. 10.1007/BF00848050 / Roux’s Arch. Dev. Biol. / Inductive mechanisms in the process of wing vein formation in Drosophila by García-Bellido (1977)
  17. 10.1073/pnas.91.21.10222 / Proc. Natl. Acad. Sci. USA / Cell interactions in the control of size in Drosophila wings by García-Bellido (1994)
  18. 10.1242/dev.122.11.3363 / Development / The Drosophila embryonic midline is the site of Spitz processing, and induces activation of the EGF receptor in the ventral ectoderm by Golembo (1996)
  19. 10.1016/0925-4773(94)90070-1 / Mech. Dev. / Cell proliferation patterns in the wing imaginal disc of Drosophila by González-Gaitán (1994)
  20. 10.1006/dbio.1993.1285 / Dev. Biol. / Star is required for neuronal differentiation in the Drosophila retina and displays dosage-sensitive interactions with Ras1 by Heberlein (1993)
  21. 10.1242/dev.100.2.201 / Development / Expression of Drosophila epidermal growth factor homologue in mitotic cell populations by Kammermeyer (1987)
  22. {'key': '2023090607371984700_DEVELOP_126_12_2663C22', 'first-page': '1454', 'article-title': 'A dominant negative mutation suppresses the function of normal epidermal growth factor receptors by heterodimerization', 'volume': '11', 'author': 'Kashles', 'year': '1991', 'journal-title': 'Mol. Cell. Biol.'} / Mol. Cell. Biol. / A dominant negative mutation suppresses the function of normal epidermal growth factor receptors by heterodimerization by Kashles (1991)
  23. 10.1016/0012-1606(91)90127-O / Dev. Biol. / Expression during Drosophila development of DER, a gene related to erbB-1 and neu: correlations with mutant phenotypes by Katzen (1991)
  24. 10.1242/dev.118.3.893 / Development / Influence of Drosophila ventral epidermal development by the CNS midline cells and spitz class genes by Kim (1993)
  25. 10.1242/dev.120.7.1731 / Development / Characterization of Star and its interactions with sevenless and EGF receptor during photoreceptor cell development in Drosophila by Kolodkin (1994)
  26. 10.1016/S0960-9822(97)70087-3 / Curr. Biol. / Requirement for EGF receptor signalling in neural recruitment during formation of Drosophila chordotonal sense organ clusters by Lage (1997)
  27. {'key': '2023090607371984700_DEVELOP_126_12_2663C27', 'volume-title': 'Genetic variations in Drosophila melanogaster', 'author': 'Lindsley', 'year': '1968'} / Genetic variations in Drosophila melanogaster by Lindsley (1968)
  28. {'key': '2023090607371984700_DEVELOP_126_12_2663C28', 'volume-title': 'The Genome of Drosophila melanogaster', 'author': 'Lindsley', 'year': '1992'} / The Genome of Drosophila melanogaster by Lindsley (1992)
  29. 10.1242/dev.125.21.4145 / Development / The knirps and knirps-related genes organize development of the second wing-vein in Drosophila by Lunde (1998)
  30. 10.1101/gad.2.11.1496 / Genes Dev. / A group of genes required for pattern formation in the ventral ectoderm of the Drosophila embryo by Mayer (1988)
  31. 10.1242/dev.120.8.2329 / Development / New functions of the Drosophila rhomboid gene during embryonic and adult development are revealed by a novel genetic method, enhancer piracy by Noll (1994)
  32. {'key': '2023090607371984700_DEVELOP_126_12_2663C32', 'first-page': '874', 'article-title': 'Double-label in situ hybridization using biotin and digoxigenin-tagged RNA probes', 'volume': '870', 'author': 'O’Neill', 'year': '1994', 'journal-title': 'BioTechniques'} / BioTechniques / Double-label in situ hybridization using biotin and digoxigenin-tagged RNA probes by O’Neill (1994)
  33. 10.1016/0955-0674(94)90145-7 / Current Opinion in Cell Biology / Signalling pathways initiated by receptor protein tyrosine kinases in Drosophila by Perrimon (1994)
  34. 10.1016/S0092-8674(00)80177-4 / Cell / There must be 50 ways to rule the signal: The case of the Drosophila EGF receptor by Perrimon (1997)
  35. 10.1006/dbio.1998.9119 / Dev. Biol / The role of Star in the production of an activated ligand for the EGF Receptor signaling pathway by Pickup (1999)
  36. 10.1016/0092-8674(89)90641-7 / Cell / The maternal ventralizing locus torpedo is allelic to faint little ball, an embryonic lethal, and encodes the Drosophila EGF receptor homolog by Price (1989)
  37. 10.1242/dev.124.19.3871 / Development / Ectopic activation of torpedo/Egfr, a Drosophila receptor tyrosine kinase, dorsalizes both the eggshell and the embryo by Queenan (1997)
  38. 10.1101/gad.7.10.1937 / Genes Dev. / Establishment of ventral cell fates in the Drosophila embryonic ectoderm requires DER, the EGF receptor homolog by Raz (1993)
  39. 10.1242/dev.125.10.1823 / Development / Genetic interactions and cell behaviour in blistered mutants during proliferation and differentiation of the Drosophila wing by Roch (1998)
  40. 10.1016/0092-8674(93)90273-S / Cell / Spatially localized rhomboid is required for establishment of the dorsal-ventral axis in Drosophila oogenesis by Ruohola-Baker (1993)
  41. 10.1101/gad.6.8.1503 / Genes Dev. / The Drosophila spitz gene encodes a putative EGF-like growth factor involved in dorsal-ventral axis formation and neurogenesis by Rutledge (1992)
  42. 10.1242/dev.125.2.191 / Development / Sequential activation of the EGF receptor pathway during Drosophila oogenesis establishes the dorsoventral axis by Sapir (1998)
  43. 10.1016/0092-8674(89)90642-9 / Cell / The Drosophila EGF receptor homolog (DER) gene is allelic to faint little ball, a locus essential for embryonic development by Schejter (1989)
  44. 10.1101/gad.12.7.908 / Genes Dev / EGF domain swap converts a Drosophila EGF receptor activator into an inhibitor by Schnepp (1998)
  45. 10.1101/gad.10.18.2302 / Genes Dev. / Vein is a novel component in the Drosophila epidermal growth factor receptor pathway with similarity to the neuregulins by Schnepp (1996)
  46. 10.1101/gad.9.12.1518 / Genes Dev. / Secreted Spitz triggers the DER signaling pathway and is a limiting component in embryonic ventral ectoderm determination by Schweitzer (1995)
  47. 10.1016/S0168-9525(97)01091-3 / Trends Genet. / A thousand and one roles for the Drosophila EGF receptor by Schweitzer (1997)
  48. 10.1006/dbio.1996.0179 / Dev. Biol. / tMolecular, phenotypic, and expression analysis of vein, a gene required for growth of the Drosophila wing disc by Simcox (1996)
  49. 10.1016/S0925-4773(96)00643-0 / Mech. Dev. / Differential requirement for EGF-like ligands in Drosophila wing development by Simcox (1997)
  50. 10.1101/gad.7.6.961 / Genes Dev. / The Drosophila rhomboid gene mediates the localized formation of wing veins and interacts genetically with components of the Egf-R signaling pathway by Sturtevant (1993)
  51. 10.1242/dev.120.9.2593 / Development / Down-regulation of Drosophila Egf-r mRNA levels following hyperactivated receptor signaling by Sturtevant (1994)
  52. 10.1242/dev.121.3.785 / Development / Analysis of the genetic hierarchy guiding wing vein development in Drosophila by Sturtevant (1995)
  53. 10.1242/dev.124.22.4707 / Development / Interactions between the EGF receptor and DPP pathways establish distinct cell fates in the tracheal placodes by Wappner (1997)
  54. 10.1016/0012-1606(92)90299-V / Dev. Biol. / Localization of DER and the pattern of cell divisions in wild-type and Ellipse eye imaginal discs by Zak (1992)
Dates
Type When
Created 4 years, 4 months ago (April 23, 2021, 3:38 p.m.)
Deposited 1 year, 11 months ago (Sept. 6, 2023, 3:37 a.m.)
Indexed 3 weeks, 1 day ago (Aug. 7, 2025, 4:41 p.m.)
Issued 26 years, 2 months ago (June 15, 1999)
Published 26 years, 2 months ago (June 15, 1999)
Published Online 26 years, 2 months ago (June 15, 1999)
Published Print 26 years, 2 months ago (June 15, 1999)
Funders 0

None

@article{Guichard_1999, title={rhomboid and Star interact synergistically to promote EGFR/MAPK signaling during Drosophila wing vein development}, volume={126}, ISSN={1477-9129}, url={http://dx.doi.org/10.1242/dev.126.12.2663}, DOI={10.1242/dev.126.12.2663}, number={12}, journal={Development}, publisher={The Company of Biologists}, author={Guichard, Annabel and Biehs, Brian and Sturtevant, Mark A. and Wickline, Laura and Chacko, Julie and Howard, Katherine and Bier, Ethan}, year={1999}, month=jun, pages={2663–2676} }