{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,7,15]],"date-time":"2026-07-15T06:57:31Z","timestamp":1784098651753,"version":"3.55.0"},"reference-count":51,"publisher":"The Company of Biologists","issue":"10","content-domain":{"domain":[],"crossmark-restriction":false},"short-container-title":[],"published-print":{"date-parts":[[2002,5,15]]},"abstract":"<jats:p>The wing imaginal disc comprises the primordia of the adult wing and the dorsal thoracic body wall. During second larval instar, the wing disc is subdivided into distinct domains that correspond to the presumptive wing and body wall. Early activity of the signaling protein Wingless has been implicated in the specification of the wing primordium. Wingless mutants can produce animals in which the wing is replaced by a duplication of thoracic structures. Specification of wing fate has been visualized by expression of the POU-homeodomain protein Nubbin in the presumptive wing territory and by repression of the homeodomain protein Homothorax. We report that repression of the zinc-finger transcription factor Teashirt (Tsh) is the earliest event in wing specification. Repression of Tsh by the combined action of Wingless and Decapentaplegic is required for wing pouch formation and for subsequent repression of Hth. Thus, repression of Tsh defines the presumptive wing earlier in development than repression of Hth, which must therefore be considered a secondary event.<\/jats:p>","DOI":"10.1242\/dev.129.10.2411","type":"journal-article","created":{"date-parts":[[2021,4,26]],"date-time":"2021-04-26T04:53:29Z","timestamp":1619412809000},"page":"2411-2418","source":"Crossref","is-referenced-by-count":72,"title":["Repression of Teashirt marks the initiation of wing development"],"prefix":"10.1242","volume":"129","author":[{"given":"Jun","family":"Wu","sequence":"first","affiliation":[{"name":"Present address: Mount Sinai School of Medicine, 1 Gustav Levy Place, New York, NY, USA"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Stephen M.","family":"Cohen","sequence":"additional","affiliation":[{"name":"Present address: Mount Sinai School of Medicine, 1 Gustav Levy Place, New York, NY, USA"}],"role":[{"vocabulary":"crossref","role":"author"}]}],"member":"237","reference":[{"key":"2021042604183229600_ABU-SHAAR-AND-MANN-1998","doi-asserted-by":"crossref","unstructured":"Abu-Shaar, M. and Mann, R. (1998). Generation of multiple antagonistic domains along the proximodistal axis during Drosophila leg development. Development125, 3821-3830.","DOI":"10.1242\/dev.125.19.3821"},{"key":"2021042604183229600_AVEROF-AND-COHEN-1997","doi-asserted-by":"crossref","unstructured":"Averof, M. and Cohen, S. M. (1997). Evolutionary origin of insect wings from ancestral gills. Nature385, 627-630.","DOI":"10.1038\/385627a0"},{"key":"2021042604183229600_AXELROD-ETAL-1996","doi-asserted-by":"crossref","unstructured":"Axelrod, J. D., Matsuno, K., Artavanis-Tsakonas, S. and Perrimon, N. (1996). Interaction between wingless and Notch signaling pathways mediated by Dishevelled. Science271, 1826-1832.","DOI":"10.1126\/science.271.5257.1826"},{"key":"2021042604183229600_AZPIAZU-AND-MORATA-2000","doi-asserted-by":"crossref","unstructured":"Azpiazu, N. and Morata, G. (2000). Function and regulation of homothorax in the wing imaginal disc of Drosophila. Development127, 2685-2693.","DOI":"10.1242\/dev.127.12.2685"},{"key":"2021042604183229600_BRAND-AND-PERRIMON-1993","doi-asserted-by":"crossref","unstructured":"Brand, A. H. and Perrimon, N. (1993). Targeted gene expression as a means of altering cell fates and generating dominant phenotypes. Development118, 401-415.","DOI":"10.1242\/dev.118.2.401"},{"key":"2021042604183229600_BROOK-AND-COHEN-1996","doi-asserted-by":"crossref","unstructured":"Brook, W. J. and Cohen, S. M. (1996). Antagonistic interactions between wingless and decapentaplegic responsible for dorsal-ventral pattern in the Drosophila Leg. Science273, 1373-1377.","DOI":"10.1126\/science.273.5280.1373"},{"key":"2021042604183229600_CADIGAN-ETAL-1998","doi-asserted-by":"crossref","unstructured":"Cadigan, K. M., Fish, M. P., Rulifson, E. J. and Nusse, R. (1998). Wingless repression of Drosophila frizzled 2 expression shapes the Wingless morphogen gradient in the wing. Cell93, 767-777.","DOI":"10.1016\/S0092-8674(00)81438-5"},{"key":"2021042604183229600_CASARES-AND-MANN-2000","doi-asserted-by":"crossref","unstructured":"Casares, F. and Mann, R. S. (2000). A dual role for homothorax in inhibiting wing blade development and specifying proximal wing identities in Drosophila. Development127, 1499-1508.","DOI":"10.1242\/dev.127.7.1499"},{"key":"2021042604183229600_COHEN-ETAL-1992","doi-asserted-by":"crossref","unstructured":"Cohen, B., McGuffin, M. E., Pfeifle, C., Segal, D. and Cohen, S. M. (1992). apterous, a gene required for imaginal disc development in Drosophila encodes a member of the LIM family of developmental regulatory proteins. Genes Dev.6, 715-729.","DOI":"10.1101\/gad.6.5.715"},{"key":"2021042604183229600_COHEN-ETAL-1989","doi-asserted-by":"crossref","unstructured":"Cohen, S. M., Bronner, G., Kuttner, F., Jurgens, G. and Jackle, H. (1989). Distal-less encodes a homoeodomain protein required for limb development in Drosophila. Nature338, 432-434.","DOI":"10.1038\/338432a0"},{"key":"2021042604183229600_COHEN-AND-JUUMLRGENS-1989","doi-asserted-by":"crossref","unstructured":"Cohen, S. M. and Ju\u0308rgens, G. (1989). Proximal-distal pattern formation in Drosophila: cell autonomous requirement for Distal-less gene activity in limb development. EMBO J.8, 2045-2055.","DOI":"10.1002\/j.1460-2075.1989.tb03613.x"},{"key":"2021042604183229600_COUSO-ETAL-1993","doi-asserted-by":"crossref","unstructured":"Couso, J. P., Bate, M. and Martinez Arias, A. (1993). A wingless-dependent polar coordinate system in the imaginal discs of Drosophila. Science259, 484-489.","DOI":"10.1126\/science.8424170"},{"key":"2021042604183229600_COUSO-ETAL-1995","doi-asserted-by":"crossref","unstructured":"Couso, J. P., Knust, E. and Martinez Arias, A. (1995). Serrate and wingless cooperate to induce vestigial gene expression and wing formation in Drosophila. Curr. Biol.5, 1437-1448.","DOI":"10.1016\/S0960-9822(95)00281-8"},{"key":"2021042604183229600_DE-CELIS-AND-BRAY-1997","doi-asserted-by":"crossref","unstructured":"de Celis, J. F. and Bray, S. (1997). Feed-back mechanisms affecting Notch activation at the dorsoventral boundary in the Drosophila wing. Development124, 3241-3251.","DOI":"10.1242\/dev.124.17.3241"},{"key":"2021042604183229600_DE-CELIS-ETAL-1996","doi-asserted-by":"crossref","unstructured":"de Celis, J. F., Garcia-Bellido, A. and Bray, S. J. (1996). Activation and function of Notch at the dorsal-ventral boundary of the wing imaginal disc. Development122, 359-369.","DOI":"10.1242\/dev.122.1.359"},{"key":"2021042604183229600_DIAZ-BENJUMEA-ETAL-1994","doi-asserted-by":"crossref","unstructured":"Diaz-Benjumea, F. J., Cohen, B. and Cohen, S. M. (1994). Cell interactions between compartments establishes the proximal-distal axis of Drosophila limbs. Nature372, 175-179.","DOI":"10.1038\/372175a0"},{"key":"2021042604183229600_DIAZ-BENJUMEA-AND-COHEN-1995","doi-asserted-by":"crossref","unstructured":"Diaz-Benjumea, F. J. and Cohen, S. M. (1995). Serrate signals through Notch to establish a Wingless-dependent organizer at the dorsal\/ventral compartment boundary of the Drosophila wing. Development121, 4215-4225.","DOI":"10.1242\/dev.121.12.4215"},{"key":"2021042604183229600_DOHERTY-ETAL-1996","doi-asserted-by":"crossref","unstructured":"Doherty, D., Fenger, G., Younger-Shepherd, S., Jan, L.-Y. and Jan, Y.-N. (1996). Dorsal and ventral cells respond differently to the Notch ligands Delta and Serrate during Drosophila wing development. Genes Dev.10, 421-434.","DOI":"10.1101\/gad.10.4.421"},{"key":"2021042604183229600_FLEMING-ETAL-1997","doi-asserted-by":"crossref","unstructured":"Fleming, R. J., Gu, Y. and Hukriede, N. A. (1997). Serrate-mediated activation of Notch is specifically blocked by the product of the gene fringe in the dorsal compartment of the Drosophila wing imaginal disc. Development124, 2973-2981.","DOI":"10.1242\/dev.124.15.2973"},{"key":"2021042604183229600_HALDER-ETAL-1998","doi-asserted-by":"crossref","unstructured":"Halder, G., Polaczyk, P., Kraus, M. E., Hudson, A., Kim, J., Laughon, A. and Carroll, S. (1998). The Vestigial and Scalloped proteins act together to directly regulate wing-specific gene expression in Drosophila. Genes Dev.12, 3900-3909.","DOI":"10.1101\/gad.12.24.3900"},{"key":"2021042604183229600_HELD-ETAL-1994","doi-asserted-by":"crossref","unstructured":"Held, L. I. J., Heup, M. A., Sappington, J. M. and Peters, S. D. (1994). Interactions of decapentaplegic, wingless and Distal-less in the Drosophila leg. Roux\u2019 Arch. Dev. Biol.203, 310-319.","DOI":"10.1007\/BF00457802"},{"key":"2021042604183229600_JIANG-AND-STRUHL-1996","doi-asserted-by":"crossref","unstructured":"Jiang, J. and Struhl, G. (1996). Complementary and mutually exclusive activities of Decapentaplegic and Wingless organize axial pattern during Drosophila limb development. Cell86, 401-409.","DOI":"10.1016\/S0092-8674(00)80113-0"},{"key":"2021042604183229600_JOHNSTON-AND-EDGAR-1998","doi-asserted-by":"crossref","unstructured":"Johnston, L. A. and Edgar, B. A. (1998). Wingless and Notch regulate cell-cycle arrest in the developing Drosophila wing. Nature394, 82-84.","DOI":"10.1038\/27925"},{"key":"2021042604183229600_KIM-ETAL-1995","doi-asserted-by":"crossref","unstructured":"Kim, J., Irvine, K. D. and Carroll, S. B. (1995). Cell recognition, signal induction, and symmetrical gene activation at the dorsal-ventral boundary of the developing Drosophila wing. Cell82, 795-802.","DOI":"10.1016\/0092-8674(95)90476-X"},{"key":"2021042604183229600_KIM-ETAL-1996","doi-asserted-by":"crossref","unstructured":"Kim, J., Sebring, A., Esch, J. J., Kraus, M. E., Vorwerk, K., Magee, J. and Carroll, S. B. (1996). Integration of positional signals and regulation of wing formation by Drosophila vestigial gene. Nature382, 133-138.","DOI":"10.1038\/382133a0"},{"key":"2021042604183229600_KLEIN-AND-MARTINEZ-ARIAS-1998","doi-asserted-by":"crossref","unstructured":"Klein, T. and Martinez-Arias, A. (1998). Different spatial and temporal interactions between Notch, wingless, and vestigial specify proximal and distal pattern elements of the wing in Drosophila. Dev. Biol.194, 196-212.","DOI":"10.1006\/dbio.1997.8829"},{"key":"2021042604183229600_KURANT-ETAL-1998","doi-asserted-by":"crossref","unstructured":"Kurant, E., Pai, C. Y., Sharf, R., Halachmi, N., Sun, Y. H. and Salzberg, A. (1998). Dorsotonals\/homothorax, the Drosophila homologue of meis1, interacts with extradenticle in patterning of the embryonic PNS. Development125, 1037-1048.","DOI":"10.1242\/dev.125.6.1037"},{"key":"2021042604183229600_LECUIT-ETAL-1996","doi-asserted-by":"crossref","unstructured":"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. Nature381, 387-393.","DOI":"10.1038\/381387a0"},{"key":"2021042604183229600_LECUIT-AND-COHEN-1997","doi-asserted-by":"crossref","unstructured":"Lecuit, T. and Cohen, S. M. (1997). Proximal-distal axis formation in the Drosophila leg. Nature388, 139-145.","DOI":"10.1038\/40563"},{"key":"2021042604183229600_LIU-ETAL-2000","doi-asserted-by":"crossref","unstructured":"Liu, X., Grammont, M. and Irvine, K. D. (2000). Roles for scalloped and vestigial in regulating cell affinity and interactions between the wing blade and the wing hinge. Dev. Biol.228, 287-303.","DOI":"10.1006\/dbio.2000.9939"},{"key":"2021042604183229600_MICCHELLI-ETAL-1997","doi-asserted-by":"crossref","unstructured":"Micchelli, C. A., Rulifson, E. J. and Blair, S. S. (1997). The function and regulation of cut expression on the wing margin of Drosophila: Notch, Wingless and a dominant negative role for Delta and Serrate. Development124, 1485-1495.","DOI":"10.1242\/dev.124.8.1485"},{"key":"2021042604183229600_MORATA-AND-LAWRENCE-1977","doi-asserted-by":"crossref","unstructured":"Morata, G. and Lawrence, P. A. (1977). The development of wingless, a homeotic mutation of Drosophila. Dev. Biol.56, 227-240.","DOI":"10.1016\/0012-1606(77)90266-4"},{"key":"2021042604183229600_NEUMANN-AND-COHEN-1996A","doi-asserted-by":"crossref","unstructured":"Neumann, C. J. and Cohen, S. M. (1996a). Distinct mitogenic and cell fate specification functions of wingless in different regions of the wing Development. Development122, 1781-1789.","DOI":"10.1242\/dev.122.6.1781"},{"key":"2021042604183229600_NEUMANN-AND-COHEN-1996B","doi-asserted-by":"crossref","unstructured":"Neumann, C. J. and Cohen, S. M. (1996b). A hierarchy of cross-regulation involving Notch, wingless, vestigial and cut organizes the dorsal\/ventral axis of the Drosophila wing. Development122, 3477-3485.","DOI":"10.1242\/dev.122.11.3477"},{"key":"2021042604183229600_NEUMANN-AND-COHEN-1997","doi-asserted-by":"crossref","unstructured":"Neumann, C. J. and Cohen, S. M. (1997). Long-range action of Wingless organizes the dorsal-ventral axis of the Drosophila wing. Development124, 871-880.","DOI":"10.1242\/dev.124.4.871"},{"key":"2021042604183229600_NEUMANN-AND-COHEN-1998","doi-asserted-by":"crossref","unstructured":"Neumann, C. J. and Cohen, S. M. (1998). Boundary formation in the Drosophila wing: the POU-domain protein Nubbin attenuates Notch activity. Science281, 409-413.","DOI":"10.1126\/science.281.5375.409"},{"key":"2021042604183229600_NG-ETAL-1995","doi-asserted-by":"crossref","unstructured":"Ng, M., Diaz-Benjumea, F. J. and Cohen, S. M. (1995). Nubbin encodes a POU-domain protein required for proximal-distal patterning in the Drosophila wing. Development121, 589-599.","DOI":"10.1242\/dev.121.2.589"},{"key":"2021042604183229600_NG-ETAL-1996","doi-asserted-by":"crossref","unstructured":"Ng, M., Diaz-Benjumea, F. J., Vincent, J. P., Wu, J. and Cohen, S. M. (1996). Specification of the wing by localized expression of wingless protein. Nature381, 316-318.","DOI":"10.1038\/381316a0"},{"key":"2021042604183229600_PAI-ETAL-1997","doi-asserted-by":"crossref","unstructured":"Pai, L. M., Orsulic, S., Bejsovec, A. and Peifer, M. (1997). Negative regulation of Armadillo, a Wingless effector in Drosophila. Development124, 2255-2266.","DOI":"10.1242\/dev.124.11.2255"},{"key":"2021042604183229600_PANIN-ETAL-1997","doi-asserted-by":"crossref","unstructured":"Panin, V. M., Papayannopoulos, V., Wilson, R. and Irvine, K. D. (1997). Fringe modulates Notch-ligand interactions. Nature387, 908-913.","DOI":"10.1038\/43191"},{"key":"2021042604183229600_PIGNONI-AND-ZIPURSKY-1997","doi-asserted-by":"crossref","unstructured":"Pignoni, F. and Zipursky, S. L. (1997). Induction of Drosophila eye development by decapentaplegic. Development124, 271-278.","DOI":"10.1242\/dev.124.2.271"},{"key":"2021042604183229600_RULIFSON-AND-BLAIR-1995","doi-asserted-by":"crossref","unstructured":"Rulifson, E. J. and Blair, S. S. (1995). Notch regulates wingless expression and is not required for reception of the paracrine wingless signal during wing margin neurogenesis in Drosophila. Development121, 2813-2824.","DOI":"10.1242\/dev.121.9.2813"},{"key":"2021042604183229600_RYOO-ETAL-1999","doi-asserted-by":"crossref","unstructured":"Ryoo, H. D., Marty, T., Casares, F., Affolter, M. and Mann, R. S. (1999). Regulation of Hox target genes by a DNA bound Homothorax\/Hox\/Extradenticle complex. Development126, 5137-5148.","DOI":"10.1242\/dev.126.22.5137"},{"key":"2021042604183229600_SHARMA-AND-CHOPRA-1976","doi-asserted-by":"crossref","unstructured":"Sharma, R. P. and Chopra, V. L. (1976). Effect of the wingless (wg1) mutation on wing and haltere development in Drosophila melanogaster. Dev. Biol.48, 461-465.","DOI":"10.1016\/0012-1606(76)90108-1"},{"key":"2021042604183229600_SCHNEPP-ETAL-1996","doi-asserted-by":"crossref","unstructured":"Schnepp, B., Grumbling, G., Donaldson, T. and Simcox, A. (1996). Vein is a novel component in the Drosophila epidermal growth factor receptor pathway with similarity to the neuregulins. Genes Dev.10, 2302-2313.","DOI":"10.1101\/gad.10.18.2302"},{"key":"2021042604183229600_THEISEN-ETAL-1996","doi-asserted-by":"crossref","unstructured":"Theisen, H., Haerry, T. E., O\u2019Connor, M. B. and Marsh, J. L. (1996). Developmental territories created by mutual antagonism between Wingless and Decapentaplegic. Development122, 3939-3948.","DOI":"10.1242\/dev.122.12.3939"},{"key":"2021042604183229600_WANG-ETAL-2000","doi-asserted-by":"crossref","unstructured":"Wang, S. H., Simcox, A. and Campbell, G. (2000). Dual role for Drosophila epidermal growth factor receptor signaling in early wing disc development. Genes Dev.14, 2271-2276.","DOI":"10.1101\/gad.827000"},{"key":"2021042604183229600_WILLIAMS-ETAL-1993","doi-asserted-by":"crossref","unstructured":"Williams, J. A., Paddock, S. W. and Carroll, S. B. (1993). Pattern formation in a secondary field: a hierarchy of regulatory genes subdivides the developing Drosophila wing disc into discrete subregions. Development117, 571-584.","DOI":"10.1242\/dev.117.2.571"},{"key":"2021042604183229600_WU-AND-COHEN-1999","unstructured":"Wu, J. and Cohen, S. M. (1999). Proximal distal axis formation in the Drosophila leg: primary subdivision into proximal and distal domains by Homothorax, Teashirt and Distal-less expression. Development126, 109-117."},{"key":"2021042604183229600_WU-AND-COHEN-2000","doi-asserted-by":"crossref","unstructured":"Wu, J. and Cohen, S. M. (2000). Proximal distal axis formation in the Drosophila leg: distinct functions of Teashirt and Homothorax in the proximal leg. Mech. Dev.94, 47-56.","DOI":"10.1016\/S0925-4773(00)00311-7"},{"key":"2021042604183229600_ZECCA-ETAL-1996","doi-asserted-by":"crossref","unstructured":"Zecca, M., Basler, K. and Struhl, G. (1996). Direct and long-range action of a Wingless morphogen gradient. Cell87, 833-844.","DOI":"10.1016\/S0092-8674(00)81991-1"}],"container-title":["Development"],"original-title":[],"language":"en","link":[{"URL":"http:\/\/journals.biologists.com\/dev\/article-pdf\/129\/10\/2411\/1138932\/2411.pdf","content-type":"application\/pdf","content-version":"vor","intended-application":"syndication"},{"URL":"http:\/\/journals.biologists.com\/dev\/article-pdf\/129\/10\/2411\/1138932\/2411.pdf","content-type":"unspecified","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2022,12,25]],"date-time":"2022-12-25T11:59:01Z","timestamp":1671969541000},"score":1,"resource":{"primary":{"URL":"https:\/\/journals.biologists.com\/dev\/article\/129\/10\/2411\/41714\/Repression-of-Teashirt-marks-the-initiation-of"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2002,5,15]]},"references-count":51,"journal-issue":{"issue":"10","published-print":{"date-parts":[[2002,5,15]]}},"URL":"https:\/\/doi.org\/10.1242\/dev.129.10.2411","relation":{},"ISSN":["1477-9129","0950-1991"],"issn-type":[{"value":"1477-9129","type":"electronic"},{"value":"0950-1991","type":"print"}],"subject":[],"published":{"date-parts":[[2002,5,15]]}}}