Smoothened-mediated Hedgehog signalling is required for the maintenance of the anterior-posterior lineage restriction in the developing wing of Drosophila

Development

Volumn 124, Issue 20, 1997, Pages 4053-4063

  Blair, Seth S ^a   Ralston, Amy ^a  

^a UNIVERSITY OF WISCONSIN MADISON   (United States)

Author keywords

Appendage patterning; Cell lineage; Compartment; Cubitus interuptus; Engrailed; Hedgehog; Invected; Selector gene; Smoothened

Indexed keywords

ANIMAL TISSUE; ARTICLE; CELL CLONE; CELL COMPARTMENTALIZATION; CELL LINEAGE; DEVELOPMENTAL GENETICS; DROSOPHILA; EMBRYO; IMAGINAL DISC; LARVAL DEVELOPMENT; LIMB DEVELOPMENT; NONHUMAN; PRIORITY JOURNAL; SIGNAL TRANSDUCTION;

ANIMALIA; CUBITUS; ERINACEIDAE;

EID: 0030729232     PISSN: 09501991     EISSN: None     Source Type: Journal    
DOI: 10.1242/dev.124.20.4053     Document Type: Article

References (66)

1. Abbott, L. C., Karpen, G. H. and Schubiger, G. (1981). Compartmental restrictions and blastema formation during pattern regulation in Drosophila imaginal discs. Dev. Biol. 87, 64-75.
2. Affolter, M., Montagne, J., Walldorf, U., Groppe, J., Kloter, U., de la Rosa, M. E. and Gehring, W. J. (1994). The Drosophila SRF homolog is expressed in a subset of tracheal cells and maps within a genomic region required for tracheal development. Development 120, 743-753.
3. Alcedo, J., Ayzenzon, M., Von Ohlen, T., Noll, M. and Hooper, J. E. (1996). The Drosophila smoothened gene encodes a seven-pass membrane protein, a putative receptor for the hedgehog signal. Cell 86, 221-232.
4. Basler, K. and Struhl, G. (1994). Compartment boundaries and the control of Drosophila limb pattern by hedgehog protein. Nature 368, 208-214.
5. Blair, S. S. (1992). engrailed expression in the anterior lineage compartment of the developing wing blade of Drosophila. Development 115, 21-34.
6. Blair, S. S. (1995). Compartments and appendage development in Drosophila. BioEssays 17, 299-309.
7. Blair, S. S., Brower, D. L., Thomas, J. B. and Zavortink, M. (1994). The role of apterous in the control of dorso-venlral compartmentalization and PS integrin gene expression in the developing wing of Drosophila. Development 120, 1805-1814.
8. Brook, W. J., Ostafichuk, L. M., Piorecky, J., Wilkinson, M. D., Hodgetts, D. J. and Russell, M. A. (1993). Gene expression during imaginal disc regeneration detected using enhancer-sensitive P-elements. Development 117, 1287-1297.
9. Brower, D. L. (1986). engrailed gene expression in Drosophila imaginal discs. EMBO J. 5, 2649-2656.
10. Brower, D. L. and Jaffe, S. M. (1989). Requirements for integrins during Drosophila wing development. Nature 342, 285-287.
11. Brower, D. L., Piovant, M. and Reger, L. A. (1985). Developmental analysis of Drosophila position-specific antigens. Dev. Biol. 108, 120-130.
12. Burke, R. and Basler, K. (1996). Dpp receptors are autonomously required for cell proliferation in the entire developing Drosophila wing. Development 122, 2261-2269.
13. Capdevila, J., Estrada, M. P., Sanchez-Herrero, E. and Guerrero, I. (1994). The Drosophila segment polarity gene patched interacts with decapentaplegic in wing development. EMBO J. 13, 71-82.
14. Chen, Y. and Struhl, G. (1996). Dual roles for Patched in sequestering and transducing Hedgehog. Cell 87, 553-563.
15. Cohen, S. M. (1993). Imaginal disc development. In The Development of Drosophila melanogaster (ed. M. Bate and A. Martinez Arias), pp. 747-841. Plainview: Cold Spring Harbor Laboratory Press.
16. Coleman, K. G., Poole, S. J., Weir, M. P., Soeller, W. C. and Kornberg, T. (1987). The invected gene of Drosophila: Sequence analysis and expression studies reveal a close kinship to the engrailed gene. Genes Dev. 1, 19-28.
17. Crick, F. H. C. and Lawrence, P. A. (1975). Compartments and polyclones in insect development. Science 189, 340-347.
18. de Celis, J. F. and Garcia-Bellido, A. (1994). Roles of the Notch gene in Drosophila wing morphogenesis. Mech. Dev. 46, 109-122.
19. de Celis, J. F. and Ruiz-Gomez, M. (1995. groucho and hedgehog regulate engrailed expression in the anterior compartment of the Drosophila wing. Development 121, 3467-3476.
20. Diaz-Benjumea, F. J. and Cohen, S. M. (1993). Interaction between dorsal and ventral cells in the imaginal disc directs wing development in Drosophila. Cell 75, 741-752.
21. DiNardo, S., Kuner, J. M., Theis, J. and O'Farrell, P. H. (1985). Development of embryonic pattern in D. melanogaster as revealed by accumulation of the nuclear engrailed protein. Cell 43, 59-69.
22. Fausto-Sterling, A. and Hsieh, L. (1987). In vitro culture of Drosophila imaginal disc cells: Aggregation, sorting out, and differentiative abilities. Dev. Biol. 120, 284-293.
23. Fehon, R. G., Gauger, A. and Schubiger, G. (1987). Cellular recognition and adhesion in embryos and imaginal discs of Drosophila melanogaster. In Genetic Regulation of Development (ed. W. F. Loomis), pp. 141-170. New York: Alan R, Liss, Inc.
24. Garcia-Bellido, A. (1975). Genetic control of wing disc development in Drosophila. In Cell Patterning. CIBA Symposium 29, pp. 161-183, Boston: Little. Brown.
25. Gomez-Skarmeta, J. L. and Modolell, J. (1996). araucan and caupolican provide a link between compartment subdivisions and patterning of sensory organs and veins the Drosophila wing. Genes Dev. 10, 2935-2945.
26. Gubb, D. (1985). Domains, compartments and determinative switches in Drosophila development. BioEssays 2, 27-31.
27. Guillen, I., Mullor, J. L., Capdevila, J., Sanchez-Herrero, E., Morata, G. and Guerrero, I. (1995). The function of engrailed and the specification of Drosophila wing pattern. Development 121, 3447-3456.
28. Gustavson, E., Goldsborough, A. S., Ali, Z. and Kornberg, T. B. (1996). The Drosophila engrailed and invected genes; partners in regulation, expression and function. Genetics 142, 893-906.
29. Hidalgo, A. (1994). Three distinct roles for the engrailed gene in Drosophila wing development. Curr. Biol. 4, 1087-1098.
30. Hooper, J. E. and Scott, M. P. (1989). The Drosophila patched gene encodes a putative membrane protein required for segmental patterning. Cell 59, 751-765.
31. Ingham, P. W. (1993). Localized hedgehog activity controls spatial limits of wingless transcription in the Drosophila embryo. Nature 366, 560-562.
32. Jiang, J. and Struhl, G. (1995). Protein kinase A and hedgehog signaling in Drosophila limb development. Cell 80, 563-572.
33. Karlsson, J. (1984). Morphogenesis and compartments in Drosophila. In Pattern Formation : A Primer in Developmental Biology (ed. G. M. Malacinski and S. V. Bryant), pp. 323-337, New York: Macmillan Pub. Co.
34. Kornberg, T., Siden, I., O'Farrell, P. and Simon, M. (1985). The engrailed locus of Drosophila: In situ localization of transcripts reveals compartment-specific expression. Cell 40, 45-53.
35. Kornberg, T. (1981). engrailed: A gene controlling compartment and segment formation in Drosophila. Proc. Natn. Acad. Sci. USA 78, 1095-1099.
36. Lawrence, P. A. and Morata, G. (1976a). The compartment hypothesis. In Insect Development (ed. P. A. Lawrence), pp. 132-147. Oxford: Blackwell Scientific Publishing.
37. Lawrence, P. A. and Morata, G. (1976b). Compartments in the wing of Drosophila: A study of the engrailed gene. Dev. Biol. 50, 321-337.
38. Lawrence, P. A. and Struhl, G. (1982). Further studies of the engrailed phenotype in Drosophila. EMBO J. 1, 827-833.
39. Lecuit, T., Brook, W. J., Ng, M., Calleja, M., Sun, H. and Cohen, S. M. (1996). Two distinct mechanisms for long-range patterning by decapentaplegic in the Drosophila wing. Nature 381, 387-393.
40. Lee, J. J., von Kessler, D. P., Parks, S. and Beachy, P. A. (1992). Secretion and localized transcription suggest a role in positional signaling for products of the segmentation gene hedgehog. Cell 71, 33050.
41. Lepage, T., Cohen, S. M., Diaz-Benjumea, F. J. and Parkhurst, S. M. (1995). Signal transduction by cAMP-dependent protein kinase A in Drosophila limb patterning. Nature 373, 711-715.
42. Li, W., Ohlmeyer, J. T., Lane, M. E. and Kalderon, D. (1995). Function of protein kinase A in hedgehog signal transduction and Drosophila imaginal disc development. Cell 80, 553-562.
43. Marigo, V., Davey, R. A., Zuo, Y., Cunningham, J. M. and Tabin, C. J. (1996). Biochemical evidence that Patched is the Hedgehog receptor. Nature 384, 176-178.
44. Mohler, J. and Vani, K. (1992). Molecular organization and embryonic expression of the hedgehog gene involved in cell-cell communication in segmental patterning of Drosophila. Development 115, 957-971.
45. Montagne, J., Groppe, J., Guillemin, K., Krasnow, M. A., Gehring, W. J. and Affolter, M. (1996). The Drosophila Serum Response Factor gene is required for the formation of intervein tissue of the wing and is allelic to blistered. Development 122, 2589-2597.
46. Morata, G. and Lawrence, P. A. (1975). Control of compartment development by the engrailed gene of Drosophila. Nature 255, 614-617.
47. Mullor, J. L., Calleja, M., Capdevila, J. and Guerrero, I (1997). Hedgehog activity, independent of Decapentaplegic, participates in wing disc patterning. Development 124, 1227-1237.
48. Murray, M. A., Schubiger, M. and Palka, J. (1984). Neuron differentiation and axon growth in the developing wing of Drosophila melanogaster. Dev. Biol. 104, 159-173.
49. Nankano, Y., Guerrero, I., Hidalgo, A., Taylor, A., Whittle, J. R. S. and Ingham, P. W. (1989). A protein with several possible membrane-spanning domains encoded by the Drosophila segment polarity gent patched. Nature 341, 508-513.
50. Nellen, D., Burke, R., Struhl, G. and Basler, K. (1996). Direct and long range action of a DPP morphogen gradient. Cell 85, 357-368.
51. Nestoras, K, Lee, H. and Mohler, J. (1997). Role of knot (kn) in wing patterning in Drosophila. Genetics (in press).
52. Pan, D. and Rubin, G. M. (1995). cAMP-dependent protein kinase and hedgehog act antagonistically in regulating decapentaplegic transcription in Drosophila imaginal discs. Cell 80, 543-552.
53. Patel, N. H., Martin-Blanco, E., Coleman, K. G., Poole, S. J., Ellis, M. G., Kornberg, T. B. and Goodman, C. S. (1989). Expression of engrailed proteins in arthropods, annelids, and chordates. Cell 58, 955-968.
54. Phillips, R. G., Roberts, I. G. H., Ingham, P. W. and Whittle, J. R. S. (1990). The Drosophila segment polarity gene patched is involved in a positional signalling mechanism in imaginal discs. Development 110, 105-114.
55. Sanchez-Herrero, E., Couso, J. P., Capdevila, J., Guerrero, I. (1996). The fu gene discriminates between pathways to control dpp expression in Drosophila imaginal discs. Mech Dev. 55, 159-170.
56. Sanicola, M., Sekelsky, J., Elson, S. and Gelbart, W. M. (1995). Drawing a stripe in Drosophila imaginal disks: negative regulation of decapentaplegic and patched by engrailed. Genetics 139, 745-756.
57. Schwartz, C., Locke, J., Nishida, C. and Kornberg, T. B. (1995). Analysis of cubitus interruptus regulation in Drosophila embryos and imaginal disks. Development 121, 1625-1635.
58. Simonds, A. J., Brook, W. J., Cohen, S. M. and Bell, J. B. (1995). Distinguishable functions for engrailed and invected in anterior-posterior patterning in the Drosophila wing. Nature 376, 424-427.
59. Slusarski, D. C., Motzny, C. K. and Holmgren, R. (1995). Mutations that alter the timing and pattern of cubitus interruptus gene expression in Drosophila melanogaster. Genetics 139, 229-240.
60. Stone, D. M., Hynes, M., Armanini, M., Swanson, T.A., Gu, Q., Johnson, R. L., Scott, M. P., Pennica, D., Goddard, A., Phillips, H., Noll, M., Hooper, J. E., de Sauvage, F. and Rosenthal, A. (1996). The tumour-suppressor gene patched encodes a candidate receptor for Sonic hedgehog. Nature 384, 129-133.
61. Tabata, T. and Kornberg, T. B. (1994). Hedgehog is a signaling protein with a key role in patterning Drosophila imaginal discs. Cell 76, 89-102.
62. Tabata, T., Eaton, S. E., and Kornberg, T. B. (1992). The Drosophila hedgehog gene is expressed specifically in posterior compartment cells and is a target of engrailed expression. Genes Dev. 6, 2635-2645.
63. Tabata, T., Schwartz, C., Gustavson, E., Ali, Z. and Kornberg, T. B. (1995). Creating a Drosophila wing de novo, the role of engrailed, and the compartment border hypothesis. Development 121, 3359-3369.
64. van den Heuvel, M. and Ingham, P. W. (1996). smoothened encodes a receptor-like serpentine protein required for hedgehog signalling. Nature 382, 547-551.
65. Xu, T. and Rubin, G. M. (1993). Analysis of genetic mosaics in developing and adult Drosophila tissues. Development 117, 1223-1237.
66. Zecca, M., Basler, K. and Struhl, G. (1995). Sequential organizing activities of engrailed, hedgehog, and decapentaplegic in the Drosophila wing. Development 121, 2265-2278.