Dpp Represses eagle Expression at Short-Range, but Can Repress Its Expression at a Long-Range via EGFR Signal Repression

  • Kim, Se Young (Department of Biology Education, Seoul National University) ;
  • Jung, Keuk Il (Department of Biology Education, Seoul National University) ;
  • Kim, Sang Hee (Department of Chemistry, Konkuk University) ;
  • Jeon, Sang-Hak (Department of Biology Education, Seoul National University)
  • Received : 2008.07.11
  • Accepted : 2008.09.09
  • Published : 2008.12.31

Abstract

Nervous system development takes place after positional information has been established along the dorsal-ventral (D/V) axis. The initial subdivision provided by a gradient of nuclear dorsal protein is maintained by the zygotic genes expressed along the D/V axis. In this study, an investigation was conducted to determine the range of Dpp function in repressing the expression of eagle (eg) that is present in intermediate neuroblasts defective (ind) and muscle specific homeobox (msh) gene domain. eg is expressed in neuroblast (NB) 2-4, 3-3 and 6-4 of the msh domain, and NB7-3 of the ind domain at the embryonic stage 11. In decapentaplegic (dpp) loss-of-function mutant embryos, eg was ectopically expressed in the dorsal region, while in dpp gain-of-function mutants produced by sog or sca-GAL4/UAS-dpp, eg was repressed by Dpp. It is worthy of note that Dpp produced from sim;;dpp embryos showed that Dpp could function at long range. However, Dpp produced from en-GAL4/UAS-dpp or wg-GAL4/UAS-dpp primarily acted at short-range. This result demonstrated that this discrepancy seems to be due to the repression of Dpp to EGFR signaling in sim;;dpp embryos. Taken together, these results suggest that Dpp signaling works at short-range, but can function indirectly at long-range by way of repression of EGFR signaling during embryonic neurogenesis.

Keywords

Dpp signaling;Drosophila melanogaster;eagle;EGFR signaling;neuroectoderm

Acknowledgement

Supported by : Korea Science and Engineering Foundation

References

  1. Chang, J.K., Kim, 1.0., Ahn, I.S., and Kim, S.H. (2001). The CNS midline cells control the spitz class and Egfr signaling genes to establish the proper cell fate of the Drosophila ventral neuroectoderm. lnt, J. Dev. BioI. 45,715-724
  2. Chang, 1., Shy, D., and Hartenstein, V. (2003). Antagonistic relationship between Dpp and EGFR signaling in Drosophila head patteming. Dev. BioI. 263,103-113 https://doi.org/10.1016/S0012-1606(03)00448-2
  3. Chu, H., Parras, C., White, K., and Jimenez, F. (1998). Formation and specification of ventral neuroblasts is controlled by vnd in Drosophila neurogenesis. Genes Dev. 12,3613-3624 https://doi.org/10.1101/gad.12.22.3613
  4. Dittrich, R., Bossing, T., Gould, AP., Technau, G.M., and Urban, J. (1997). The differentiation of the serotonergic neurons in the Drosophila ventral nerve cord depends on the combined function of the zinc finger proteins Eagle and Huckebein. Development 124,2515-2525
  5. Gabay, L., Seger, R., and Shilo, B.Z. (1997). In situ activation pattern of Drosophila EGF Receptor pathway during development. Science 277, 1103-1106 https://doi.org/10.1126/science.277.5329.1103
  6. Oh, CT., Kwon, S.H., Jeon, K.J., Han, P.L., Kim, S.H., and Jeon, S.H. (2002). Local inhibition of Drosophila homeobox-containing neural dorsoventral patteming genes by Dpp. FEBS Lett. 531, 427-431 https://doi.org/10.1016/S0014-5793(02)03573-1
  7. Shilo, B.Z. (2003). Signaling by the Drosophila epidermal growth factor receptor pathway during development. Exp. Cell Res. 284, 140-149 https://doi.org/10.1016/S0014-4827(02)00094-0
  8. Campos-Ortega, JA (1995). Genetic mechanisms of early neurogenesis in Drosophila melanogaster. Mol. Neurobiol. 10, 75-89 https://doi.org/10.1007/BF02740668
  9. Mlodzik, ME., and Rubin, G.M. (1990). Isolation and expression of scabrous, a gene regulating neurogenesis in Drosophila. Genes Dev. 4, 1848-1861 https://doi.org/10.1101/gad.4.11.1848
  10. Dumstrei, K., Nassif, C., Abboud, G., Aryai, A, and Hartenstein, V. (1998). EGFR signaling is required for the differentiation and maintenance of neural progenitors along the dorsal midline of the Drosophila embryonic head. Development 125, 3417-3426
  11. Rusch, J., and Levine, M. (1996). Threshold responses to the dorsal regulatory gradient and the subdivision of primary tissue territories in the Drosophila embryo. Curro Opin. Genet. Dev. 6, 416-423 https://doi.org/10.1016/S0959-437X(96)80062-1
  12. Skeath, J.B., and Carroll, S.B. (1992). Regulation of proneural gene expression and cell fate during neuroblast segregation. Development 114, 939-946
  13. Truman, J'w., and Bate, C.M. (1988). Spatial and temporal patterns of neurogenesis in the CNS of Drosophila melanogaster. Dev. BioI. 125,145-157 https://doi.org/10.1016/0012-1606(88)90067-X
  14. Isshiki, T., Takeichi, M., and Nose, A (1997). The role of the rnsh homsobox gene during Drosophila neurogenesis: implication for the dorsoventral specification of the neuroectoderm. Development 124, 3099-3109
  15. Ohlen, TV., and Doe, C.O. (2000). Convergence of Dorsal, Dpp, and Egfr signaling pathways subdivideded the Dorsophila neuroectoderm into three dorsal-ventral columns. Dev. BioI. 224, 362-372 https://doi.org/10.1006/dbio.2000.9789
  16. Hartenstein, V., and Campos-Ortega, J.A. (1984). Early neurogenesis in wild-type Drosophila melanogaster. Wilhelm Roux' Arch. Dev. BioI. 193,308-325
  17. Biehs, B., Francois, V., and Bier, E. (1996). The Drosophila short gastrulation gene prevents Dpp from autoactivating and suppressing neurogenesis in the neuroectoderm. Genes Dev. 10, 2922-2934 https://doi.org/10.1101/gad.10.22.2922
  18. Decotto, E., and Ferguson, E.L. (2001). A positive role for short gastrulation in modulating BMP signaling during dorsoventral patteming in the Drosophila embryo. Development 128, 3831-3841
  19. St. Johnston, R.D., Hoffmann, F.M., Blackman, RK, Segal, D., Grimaila, R., Padgett, RW., Irick, HA, and Gelbart, W.M. (1990). Molecular organization of the decapentaplegic gene in Drosophila melanogaster. Genes Dev. 4, 1114-1127 https://doi.org/10.1101/gad.4.7.1114
  20. D'Alessio, M., and Frasch, M. (1996). msh may playa conserved role in dorsoventral patteming of the neuroectoderm and mesoderm. Mech. Dev. 58, 217-231 https://doi.org/10.1016/S0925-4773(96)00583-7
  21. Rutledge, B.J., Zhang, K., Bier, E., Jan, Y.N., and Perrimon, N. (1992). The Drosophila spitz gene encodes a putative EGF-like growth factor involved in dorsal-ventral axis formation and neurogenesis. Genes Dev. 6, 1503-1517 https://doi.org/10.1101/gad.6.8.1503
  22. Skeath, J.B. (1999). At the nexus between pattern formation and cell-type specification: the generation of individual neuroblast fates in the Drosophila embryonic central nervous system. Bioessays 21, 922-931 https://doi.org/10.1002/(SICI)1521-1878(199911)21:11<922::AID-BIES4>3.0.CO;2-T
  23. Bernardoni, R., Kammerer, M., Vonesch, J.L., and Giangrande, A. (1999). Gliogenesis depends on glide/gem through asymmetric division of neuroglioblasts. Dev. BioI. 216, 265-275 https://doi.org/10.1006/dbio.1999.9511
  24. Higashijim, S.I., Shishido, E., Matsuzaki, M., and Saigo, K. (1996). eagle, a member of the steroid receptor gene superfamily, is expressed in a subset of neuroblasts and regulates the fate of their putative progeny in the Drosophila CNS. Development 122, 527-536
  25. Tautz, D., and Pfeifle, C. (1989). A non-radioactive in situ hybridization method for the localization of specific RNAs in Drosophila embryos reveals translational control of the segmentation gene hunchback. Chromosoma 98, 81-85 https://doi.org/10.1007/BF00291041
  26. Weiss, J.B., Ohlen, T.V., Mellerick, D.M., Dressler, G., Doe, C.O., and Scott, M.P. (1998). Dorsoventral patterning in the Drosophila central nervous system: the intermediate neuroblasts defective homeobox gene specifies intermediate column identiy. Genes Dev. 22, 3591-3602
  27. Franc, N.C., Heitzler, P., Ezekowitz, RAB., and Kirstin, W. (1999). Requirement for croquemort in phagocytosis of apoptotic cells in Drosophila. Science 284,1991-1994 https://doi.org/10.1126/science.284.5422.1991
  28. 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
  29. Doe, C.O. (1992). Molecular markers for identified neuroblasts and ganglion mother cells in the Drosophila central nervous system. Development 116, 855-863
  30. Irish, V.F., and Gelbart, W.M. (1987). The decapentaplegic gene is required for dorsal-ventral patteming of the Drosophila embryo. Genes Dev. 1,868-879 https://doi.org/10.1101/gad.1.8.868
  31. Udolph, G., Urban, J., Rusing, G., Luer, K., and Technau, G.M. (1998). Differential effects of EGF receptor signaling on neuroblast lineages along the dorsoventral axis of the Drosophila CNS. Development 125, 3291-3299
  32. Furguson, E.L., and Anderson, KV. (1992). Localized enhancement and repression of the activity of the TGF-13 family member, decapentaplegic, is necessary for dorsal-ventral pattern formation in the Drosophila embryo. Development 114,583-597
  33. Lanoue, B.R., Gordon, M.D., Battye, R., and Jacobs, J.R. (2000). Genetic analysis of vein function in the Drosophila embryonic nervous system. Genome 43, 564-573 https://doi.org/10.1139/gen-43-3-564
  34. Akiyama-Oda, Y., Hosoya, T., and Hotta, Y. (1999). Asymmetric cell division of thoracic neuroblast 6-4 to bifurcate glial and neuronal lineage in Drosophila. Development 126,1967-1974
  35. Nellen, D., Burke, R., Struhl, G., and Basler, K. (1996). Direct and long-range action of a DPP morphogen gradient. Cell 85, 357-368 https://doi.org/10.1016/S0092-8674(00)81114-9
  36. Kwon, S.H., Kim, S.H., Chung, H.M., Girton, J.R., and Jeon, S.H. (2003). The Drosophila pleionomeotc mutation enhances the Polycomblike and Polycomb mutant phenotypes during embryogenesis and in the adult. Int. J. Dev. BioI. 47, 389-395
  37. Nambu, J.R., Franks, R.G., Hu, S., and Crews, S.T. (1990). The single-minded gene of Drosophila is required for the expression of genes important for the development of CNS midline cells. Cell 63, 1157-1167