Lines is required for normal operation of Wingless, Hedgehog and Notch pathways during wing development.

The regulatory Lines/Drumstick/Bowl gene network is implicated in the integration of patterning information at several stages during development. Here, we show that during Drosophila wing development, Lines prevents Bowl accumulation in the wing primordium, confining its expression to the peripodial...

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Authors: Benítez, Elvira, Bray, Sarah J., Rodríguez Enríquez, Isabel, Guerrero Vega, Isabel
Format: article
Publication Date:2009
Country:España
Institution:Consejo Superior de Investigaciones Científicas (CSIC)
Repository:DIGITAL.CSIC. Repositorio Institucional del CSIC
OAI Identifier:oai:digital.csic.es:10261/24451
Online Access:http://hdl.handle.net/10261/24451
Access Level:Open access
Keyword:Wingless
Hedgehog
Notch
Wing development
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spelling Lines is required for normal operation of Wingless, Hedgehog and Notch pathways during wing development.Benítez, ElviraBray, Sarah J.Rodríguez Enríquez, IsabelGuerrero Vega, IsabelWinglessHedgehogNotchWing developmentThe regulatory Lines/Drumstick/Bowl gene network is implicated in the integration of patterning information at several stages during development. Here, we show that during Drosophila wing development, Lines prevents Bowl accumulation in the wing primordium, confining its expression to the peripodial epithelium. In cells that lack lines or over-expressing Drumstick, Bowl stabilization is responsible for alterations such as dramatic overgrowths and cell identity changes in the proximodistal patterning owing to aberrant responses to signaling pathways. The complex phenotypes are explained by Bowl repressing the Wingless pathway, the earliest effect seen. In addition, Bowl sequesters the general co-repressor Groucho from repressor complexes functioning in the Notch pathway and in Hedgehog expression, leading to ectopic activity of their targets. Supporting this model, elimination of the Groucho interaction domain in Bowl prevents the activation of the Notch and Hedgehog pathways, although not the repression of the Wingless pathway. Similarly, the effects of ectopic Bowl are partially rescued by co-expression of either Hairless or Master of thickveins, co-repressors that act with Groucho in the Notch and Hedgehog pathways, respectively. We conclude that by preventing Bowl accumulation in the wing, primordial Lines permits the correct balance of nuclear co-repressors that control the activity of the Wingless, Notch and Hedgehog pathways.We thank Aphrodite Bilioni and Fernando Díaz-Benjumea for critical reading of the manuscript, and members of the Bray and Guerrero laboratories for discussions and advice, especially Maki Daniels and Ainhoa Callejo. We are very grateful to Carmen Ibáñez, Emma Harrison and Marie Quick for excellent technical assistance; to A. Betz, N. Azpiazu, H. Bellen, C. Delidakis, F. J. Diaz- Benjumea, S. Kerridge, J. Modolell, T. Tabata and the Developmental Studies Hybridoma Bank for providing antibodies; and to V. Hatini, M. Calleja, S. DiNardo, C. Delidakis, J. Lengyel, C. Rauskolb, S. Shashidara, T. Tabata, A. Martinez-Arias, Vienna Drosophila RNAi Center and the Bloomington Stock Center for Drosophila stocks. This work has been supported by grants BFU2005-04183 and CSD2007-00008 from the Spanish MEC by an institutional grant from Fundación Areces given to the Centro de Biología Molecular ‘Severo Ochoa’ to I.G. and MEC fellowship (BMC2002-03839) to E.B. Work in the Bray laboratory was supported by a Programme Grant from the Medical Research Council (MRC) to S.J.B., with additional funding from EMBO Short Term Fellowship (ASTF 143-2006) to E.B. and Royal Society Travelling Fellowship to I.G. Deposited in PMC for release after 6 months.Peer reviewedCompany of BiologistsMinisterio de Educación y Ciencia (España)Fundación Ramón ArecesMedical Research Council (UK)EMBORoyal Society (UK)201020102009info:eu-repo/semantics/articlehttp://purl.org/coar/resource_type/c_65015845992 bytesapplication/pdfhttp://hdl.handle.net/10261/24451reponame:DIGITAL.CSIC. Repositorio Institucional del CSICinstname:Consejo Superior de Investigaciones Científicas (CSIC)Ingléshttp://dx.doi.org/10.1242/dev.021428info:eu-repo/semantics/openAccessoai:digital.csic.es:10261/244512026-05-22T06:33:51Z
dc.title.none.fl_str_mv Lines is required for normal operation of Wingless, Hedgehog and Notch pathways during wing development.
title Lines is required for normal operation of Wingless, Hedgehog and Notch pathways during wing development.
spellingShingle Lines is required for normal operation of Wingless, Hedgehog and Notch pathways during wing development.
Benítez, Elvira
Wingless
Hedgehog
Notch
Wing development
title_short Lines is required for normal operation of Wingless, Hedgehog and Notch pathways during wing development.
title_full Lines is required for normal operation of Wingless, Hedgehog and Notch pathways during wing development.
title_fullStr Lines is required for normal operation of Wingless, Hedgehog and Notch pathways during wing development.
title_full_unstemmed Lines is required for normal operation of Wingless, Hedgehog and Notch pathways during wing development.
title_sort Lines is required for normal operation of Wingless, Hedgehog and Notch pathways during wing development.
dc.creator.none.fl_str_mv Benítez, Elvira
Bray, Sarah J.
Rodríguez Enríquez, Isabel
Guerrero Vega, Isabel
author Benítez, Elvira
author_facet Benítez, Elvira
Bray, Sarah J.
Rodríguez Enríquez, Isabel
Guerrero Vega, Isabel
author_role author
author2 Bray, Sarah J.
Rodríguez Enríquez, Isabel
Guerrero Vega, Isabel
author2_role author
author
author
dc.contributor.none.fl_str_mv Ministerio de Educación y Ciencia (España)
Fundación Ramón Areces
Medical Research Council (UK)
EMBO
Royal Society (UK)
dc.subject.none.fl_str_mv Wingless
Hedgehog
Notch
Wing development
topic Wingless
Hedgehog
Notch
Wing development
description The regulatory Lines/Drumstick/Bowl gene network is implicated in the integration of patterning information at several stages during development. Here, we show that during Drosophila wing development, Lines prevents Bowl accumulation in the wing primordium, confining its expression to the peripodial epithelium. In cells that lack lines or over-expressing Drumstick, Bowl stabilization is responsible for alterations such as dramatic overgrowths and cell identity changes in the proximodistal patterning owing to aberrant responses to signaling pathways. The complex phenotypes are explained by Bowl repressing the Wingless pathway, the earliest effect seen. In addition, Bowl sequesters the general co-repressor Groucho from repressor complexes functioning in the Notch pathway and in Hedgehog expression, leading to ectopic activity of their targets. Supporting this model, elimination of the Groucho interaction domain in Bowl prevents the activation of the Notch and Hedgehog pathways, although not the repression of the Wingless pathway. Similarly, the effects of ectopic Bowl are partially rescued by co-expression of either Hairless or Master of thickveins, co-repressors that act with Groucho in the Notch and Hedgehog pathways, respectively. We conclude that by preventing Bowl accumulation in the wing, primordial Lines permits the correct balance of nuclear co-repressors that control the activity of the Wingless, Notch and Hedgehog pathways.
publishDate 2009
dc.date.none.fl_str_mv 2009
2010
2010
dc.type.none.fl_str_mv info:eu-repo/semantics/article
http://purl.org/coar/resource_type/c_6501
format article
dc.identifier.none.fl_str_mv http://hdl.handle.net/10261/24451
url http://hdl.handle.net/10261/24451
dc.language.none.fl_str_mv Inglés
language_invalid_str_mv Inglés
dc.relation.none.fl_str_mv http://dx.doi.org/10.1242/dev.021428
dc.rights.none.fl_str_mv info:eu-repo/semantics/openAccess
eu_rights_str_mv openAccess
dc.format.none.fl_str_mv 5845992 bytes
application/pdf
dc.publisher.none.fl_str_mv Company of Biologists
publisher.none.fl_str_mv Company of Biologists
dc.source.none.fl_str_mv reponame:DIGITAL.CSIC. Repositorio Institucional del CSIC
instname:Consejo Superior de Investigaciones Científicas (CSIC)
instname_str Consejo Superior de Investigaciones Científicas (CSIC)
reponame_str DIGITAL.CSIC. Repositorio Institucional del CSIC
collection DIGITAL.CSIC. Repositorio Institucional del CSIC
repository.name.fl_str_mv
repository.mail.fl_str_mv
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