Antagonistic interactions between wingless and decapentaplegic responsible for dorsal-ventral pattern in the Drosophila leg

Science

Volumn 273, Issue 5280, 1996, Pages 1373-1377

  Brook, William J ^a   Cohen, Stephen M ^a  

^a EUROPEAN MOLECULAR BIOLOGY LABORATORY   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

ARTICLE; CELL INTERACTION; DROSOPHILA; GENE EXPRESSION; GENE REPRESSION; LEG; NONHUMAN; PRIORITY JOURNAL; SIGNAL TRANSDUCTION;

EID: 0029795757     PISSN: 00368075     EISSN: None     Source Type: Journal    
DOI: 10.1126/science.273.5280.1373     Document Type: Article

References (45)

1. S. S. Blair, Bioessays 17, 299 (1995).
2. K. Basler and G. Struhl, Nature 368, 208 (1994).
3. T. Tabata and T. Kornberg, Cell 76, 89 (1994).
4. J. Capdevila and I. Guerrero, EMBO J. 13, 4459 (1994).
5. P. W. Ingham and M. J. Fietz, Curr. Biol. 5, 432 (1995).
6. M. Zacca, K. Basler, G. Struhl, Development 121, 2265(1995).
7. D. Nellen, R. Burke, G. Struhl, K. Basler, Cell 85, 357 (1996).
8. T. Lecuit et al., Nature 381, 387 (1996).
9. F. J. Diaz-Benjumea, B. Cohen, S. M. Cohen, ibid. 372, 175 (1994).
10. L. I. J. Held, M. A, Heup, J. M. Sappington, S. D. Peters, Roux's Archiv. Dev. Biol. 203, 310 (1994).
11. F. J. Diaz-Benjumea and S M. Cohen, Cell 75, 741 (1993).
12. S. S. Blair, D. L. Brower, J. B.Thomas, M. Zavortink, Development 120, 1805 (1994).
13. E. Steiner, Wilhelm Roux's Archiv. 180, 9 (1976). Clones induced during mid-second instar (60 ± 12 hours wild-type age) or early third instar (76 ± 12 hours wild-type age) can cross between dorsal and ventral quadrants in the anterior compartment, though most clones do not. Thus, unlike the wing, there does not appear to be a robust restriction of cell lineage between dorsal and ventral leg. However, the initial subdivision of the disc into a ventral-anterior WG-expressing domain and dorsal-anterior domain that does not express WG is already in place when the disc primordium is specified in the embryo (40), thus predating the weak lineage restriction described for second instar discs. We found little support for the existence of a D-V selector gene in the leg because dorsal versus ventral fate can be reprogrammed by expression of WG dorsally or by DPP ventrally.
14. N. E. Baker, Dev. Biol. 125, 96 (1988b).
15. M. Peifer, C. Rauskolb, M. Williams, B. Riggleman, E. Wieschaus, Development 111, 1029 (1991).
16. J. P. Couso, M. Bate, A. Martínez-Arias, Science 259, 484 (1993).
17. J. Klingensmith, R. Nusse, N. Perrimon, Genes Dev. 8, 118 (1994).
18. H. Theisen et al., Development 120, 347 (1994).
19. G. Struhl and K. Basler, Cell 72, 527 (1993). Act5C is a constitutive promoter, and the > sign designates a flanking flp recombination target site (FRT).
20. G. Campbell, T. Weaver, A. Tomlinson, ibid. 74, 1113 (1993).
21. F. J, Diaz-Benjumea and S. M. Cohen. Development 120, 1661 (1994).
22. E. L Wilder and N. Perrimon, ibid. 121, 477 (1995).
23. J. D. Masucci, R. J. Mittenberger, F. M. Hoffmann, Genes Dev. 4, 2011 (1990).
24. R. K. Blackman, M. Sanicola, L. A. Raftery, T. Gillevet, W. M. Gelbart, Development 111, 657 (1991).
25. c×3 leg discs with antibody to WG (anti-WG) reveals a much reduced but detectable amount of WG protein in a normal pattern in the leg (32).
26. c×3 leg discs with antibody to WG (anti-WG) reveals a much reduced but detectable amount of WG protein in a normal pattern in the leg (32).
27. d12 are regulatory mutations that delete control elements needed for dpp expression in the distal region of the imaginal discs [D. St. Johnston et a/., Genes Dev. 4, 1114 (1990); (24)]. Their effects on leg patterning have been described [F. Spencer et al., Cell 28, 451 (1982); (10)]. These alleles are considered here as hypomorphic because they do not remove dpp function at all stages but only in specific regions of the imaginai discs.
28. d12 disc runs along the anterior side of the A-P compartment boundary, as it normally does on the ventral side (32).
29. V. Wiersdorff, T. Lecuit, S. M. Cohen, M. Mlodzik, Development 122, 2153 (1996). Note that A-P. D-V, and P-D patterning of the antenna disc are controlled by the same intercellular signals as in the leg disc (9).
30. A. Brand and N. Perrimon, ibid. 118, 401 (1993).
31. P. A. Lawrence, R. Bodmer, J. P. Vincent, ibid. 121, 4303 (1995).
32. G. O. Pflugfelder, H. Roth, B. Poeck, Biochem. Biophys. Res. Commun. 186, 918 (1992).
33. W. J. Brook and S. M. Cohen, data not shown.
34. S. Grimm and G. Pflugfelder, Science 271, 1601 (1996).
35. The H 15 locus was identified as a P element enhancertrap insertion at 25D6 [W. J. Brook et al., Development 117, 1287 (1993)]. Genomic DNA flanking the insertion was cloned by plasmid rescue. Coding sequences expressed in the H15 pattern were identified with genomic DNA fragments as in situ hybridization probes on leg discs. The sequence of a partial cDNA revealed an open reading frame encoding a predicted T-box protein (accession number: X98766). OMB (M81796), human TBX2 (U28049), and mouse TBX2 (U15566) were selected by a BLAST search as the rearest relatives of H15. omb-lacZ is a P element enhancer-trap insertion at the omb locus (8, 33). Expression of omb is absent in leg discs where dpp activity is reduced, indicating that omb expression is DPP-dependent in the leg (32). Loss-of-function mutants in either gene develop with only slight defects in the leg (32).
36. W. Li, J. T. Ohlmeyer, M. E. Lane, D. Kalderon, Cell 80, 553 (1995).
37. J. Jiang and G. Struhl, ibid., p. 563.
38. T. Lepage, S. M. Cohen, F. J. Diaz-Benjumea, S. M. Parkhurst, Nature 373, 711 (1995).
39. D. J. Pan and G. Rubin, Cell 180, 543 (1995).
40. +) transgene. Although not sufficient to repress WG in all cases, it is possible that the low level of DPP activity provided by the transgene prevents WG expression in some clones.
41. B. Cohen, A. A. Simcox, S. M. Cohen, Development 117, 597 (1993).
42. M. van den Heuvel, R. Nusse, P. Johnston, P. A. Lawrence, Cell 59, 739 (1989).
43. M. Frasch, Nature 374, 464 (1995).
44. + >wg/h15-LacZ were subjected to a 90-min heat shock at 38°C at 60 ± 12 hours of age (second instar). This treatment causes excision of the flip-out cassette (a segment of DNA bounded by direct FRT repeats) in virtually all cells, resulting in low-level ubiquitous WG expression. This level of WG expression is sufficient to direct H15 expression but does not repress DPP expression (20). The GAL30A driver is described in (29). Larval genotypes: (Fig. 3C) GAL30A/+; UAS-wg/+; (Fig. 3D) GAL30A/H15-lacZ; UAS-wg/+ ; (Fig. 3E) GAL30A/+; UAS-wg UAS-dpp/+; and (Fig, 3F) GAL30A/H15-lacZ; UAS-wg UAS-dpp/+.
45. We thank C. Pfeifle for help in molecular characterization of H15 and for isolation of H15 mutants; A.-M. Voie for producing the WG monoclonal antibody: W. Norris and P. Ingham for mouse antibody to PTC protein; F. Diaz-Benjumea and V. Wiersdorff for sharing unpublished results; and S, Eaton, M. Averof, M. Ng, and an anonymous reviewer for suggesting improvements to the manuscript. W.J.B. is the recipient of an EMBO longterm fellowship in molecular biology.