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Dorsoventral lineage restriction in wing imaginal discs requires Notch

Abstract

The formation of boundaries that prevent the intermixing of cells is an important developmental patterning mechanism. The compartmental lineage restrictions that appear in the developing imaginal discs of Drosophila are striking examples of such boundaries1. However, little is known about the cellular mechanism underlying compartmental lineage restrictions. The dorsoventral (D/V) lineage restriction that arises late in the developing wing imaginal disc requires the dorsal expression of the transcription factor Apterous and it has been hypothesized that apterous (ap) maintains compartmentalization by directly regulating the expression of molecules that modify cell adhesion or affinity2. However, ap expression also regulates signalling between dorsal and ventral compartments, resulting in high levels of Notch signalling at the D/V boundary3,4,5,6,7,8,9,10,11,12,13,14,15,16,17. Here we show that the formation of Notch-dependent boundary cells is required for the D/V lineage restriction.

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Figure 1: Notch signalling along the dorsoventral (D/V) compartment boundary of the wing imaginal disc.
Figure 2: Late third-instar wing discs containing N- clones (N) generated at 72–60 h before pupariation, marked by the absence of a marker gene (green).
Figure 3: The role of signalling at compartment boundaries.
Figure 4: Model for the maintenance of the D/V lineage restriction.

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References

  1. Blair,S. S. in Development–Genetics, Epigenetics and Environmental Regulation (eds Russo, V. E. A., Cove, D., Edgar, L., Jaenisch, R. & Salamini, F.) 347–370 (Springer, Heidelberg, 1999).

    Google Scholar 

  2. Blair,S. S., Browser,D. L., Thomas,J. B. & Zavortink,M. The role of apterous in the control of dorso-ventral compartmentalization and PS integrin gene expression in the developing wing of Drosophila. Development 120, 1805–1814 (1994).

    CAS  PubMed  Google Scholar 

  3. Diaz-Benjumea,F. J. & Cohen,S. M. Interaction between dorsal and ventral cells in the imaginal disc directs wing development in Drosophila. Cell 75, 741–752 (1993).

    Article  CAS  Google Scholar 

  4. Rulifson,E. J. & Blair,S. S. Notch regulates wingless expression and is not required for the reception of paracrine wingless signals during wing margin development in Drosophila. Development 121, 2813–2824 (1995).

    CAS  PubMed  Google Scholar 

  5. Kim,J., Irvine,K. D. & Carroll,S. B. Cell recognition, signal induction, and symmetrical gene activation at the dorsal-ventral boundary of the developing Drosophila wing. Cell 82, 795–802 (1995).

    Article  CAS  Google Scholar 

  6. Couso,J. P., Knust,E. & Martinez Arias,A. Serrate and wingless cooperate to induce vestigial gene expression and wing formation in Drosophila. Curr. Biol. 5, 1437–1448 (1995).

    Article  CAS  Google Scholar 

  7. Diaz-Benuumea,F. J. & Cohen,S. M. Serrate signals through Notch to establish a Wingless-dependent organizer at the dorsal/ventral compartment boundary of the Drosophila wing. Development 121, 4215–4225 (1995).

    Google Scholar 

  8. de Celis,J. F., Garcia-Bellido,A. & Bray,S. J. Activation and function of Notch at the dorso-ventral boundary of the wing imaginal disc. Development 122, 359–369 (1996).

    CAS  PubMed  Google Scholar 

  9. Kim,J. et al. Integration of positional signals and regulation of wing formation and identity by Drosophila vestigial gene. Nature 382, 133–138 (1996).

    Article  ADS  CAS  Google Scholar 

  10. Doherty,D., Feger,G. Younger-Shepherd,S., Jan,L. Y. & Jan,Y. N. Delta is a ventral to dorsal signal complementary to Serrate, another Notch ligand, in Drosophila wing formation. Genes Dev. 10, 421–434 (1996).

    Article  CAS  Google Scholar 

  11. Klein,T. & Martinez Arias,A. Interactions among Delta, Serrate and fringe modulate Notch activity during Drosophila wing development. Development 125, 2951–2962 (1998).

    CAS  Google Scholar 

  12. Micchelli,C. A., Rulifson,E. J. & Blair,S. S. The function and regulation of cut expression on the wing margin of Drosophila. Notch, Wingles, and a dominant negative role for Delta and Serrate. Development 124, 1485–1495 (1997).

    CAS  PubMed  Google Scholar 

  13. de Celis,J. F. & Bray,S. Feed-back mechanisms affecting Notch activation at the dorsoventral boundary in the Drosophila wing. Development 124, 3241–3251 (1997).

    CAS  PubMed  Google Scholar 

  14. Irvine,K. & Weischaus,E. F. fringe, a boundary-specific signaling molecule, mediate interactions between dorsal and ventral cells during Drosophila wing development. Cell 79, 595–606 (1994).

    Article  CAS  Google Scholar 

  15. Panin,V. M., Papayannopoulos,V., Wilson,R. & Irvine,K. Fringe modulates Notch–ligand interactions. Nature 387, 908–912 (1997).

    Article  ADS  CAS  Google Scholar 

  16. Fleming,R. J., Gu,Y. & Hukriede,N. A. Serrate-mediated activation of Notch is specifically blocked by the product of the gene fringe in the dorsal compartment of the Drosophila wing disc. Development 124, 2973–2981 (1997).

    CAS  Google Scholar 

  17. Blair,S. S. Marginal Fringe benefits. Curr. Biol. 7, R686–R690 (1997).

    Article  CAS  Google Scholar 

  18. Blair,S. S. Mechanisms of compartment formation: evidence that non-proliferating cells do not play a critical role in defining the D/V lineage restriction in the developing wing of Drosophila. Development 119, 339–351 (1993).

    CAS  PubMed  Google Scholar 

  19. Kidd,S., Kelley,M. R. & Young,M. W. Sequence of the Notch locus of Drosophila: relationship of the encoded protein to mammalian clotting and growth factors. Mol. Cell. Biol. 6, 3094–3108 (1986).

    Article  CAS  Google Scholar 

  20. Brower,D. L. Piovant,M. & Reger,L. A. Development analysis of Drosophila position-specific antigens. Dev. Biol. 108, 120–130 (1985).

    Article  CAS  Google Scholar 

  21. de Celis,J. F. & Garcia-Bellido,A. Roles of the Notch gene in Drosophila wing morphogenesis. Mech. Dev. 46, 109–122 (1994).

    Article  CAS  Google Scholar 

  22. Shellenbarger,D. L. & Mohler,J. D. Temperature sensitive periods and autonomy of pleiotropic effects of l(l)Nts, a conditional Notch lethal in Drosophila. Dev. Biol. 62, 432–446 (1978).

    Article  CAS  Google Scholar 

  23. Rebay,I., Fehon,R. G. & Artavanis Tsakonas,S. Specific truncations of Drosophila Notch define dominant activated and dominant negative forms of the receptor. Cell 74, 319–329 (1993).

    Article  CAS  Google Scholar 

  24. Artavanis-Tsakonas,S., Rand,M. D. & Lake,R. J. Notch signaling: Cell fate control and signal integration in development. Science 284, 770–776 (1999).

    Article  ADS  CAS  Google Scholar 

  25. Neumann,C. J. & Cohen,S. M. A hierarchy of cross-regulation involving Notch, wingless, vestigial and cut organizes the dorsal/ventral axis of the Drosophila wing. Development 122, 3477–3485 (1996).

    CAS  PubMed  Google Scholar 

  26. Gho,M., Lecourtois,M., Geraud,G., Posakony,J. W. & Schweisguth,F. Subcellular localization of Suppressor of Hairless in Drosophila sense organ cells during Notch signaling. Development 122, 1673–1682 (1996).

    CAS  PubMed  Google Scholar 

  27. Fehon,R. G. et al. Molecular interactions between the protein products of the neurogenic loci Notch and Delta, two EGF-homologous genes in Drosophila. Cell 61, 523–534 (1991).

    Article  Google Scholar 

  28. Brennan,K., Tateson,R., Lewis,K. & Martinez Arias,A. A functional analysis of Notch mutations in Drosophila. Genetics 147, 177–188 (1997).

    CAS  PubMed  PubMed Central  Google Scholar 

  29. Blair,S. S. & Ralston,A. Smoothened-mediated Hedgehog signaling is required for the maintenance of the anterior-posterior lineage restriction in the developing wing of Drosophila. Development 124, 4053–4063 (1997).

    CAS  PubMed  Google Scholar 

  30. Rodriguez,I. & Basler,K. Control of compartmental affinity boundaries by Hedgehog. Nature 389, 614–617 (1997).

    Article  ADS  CAS  Google Scholar 

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Acknowledgements

We thank the Keck Neural Imaging Center for use of its confocal microscope. This work was supported by research grants from NSF and NIH, and a fellowship to C.A.M. from the Neuroscience Training Program at the University of Wisconsin.

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Correspondence to Seth S. Blair.

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Micchelli, C., Blair, S. Dorsoventral lineage restriction in wing imaginal discs requires Notch. Nature 401, 473–476 (1999). https://doi.org/10.1038/46779

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