Distribution of the wingless gene product in drosophila embryos: A protein involved in cell-cell communication

Heuvel, Marcel van den; Nusse, Roel; Johnston, Paul R.; Lawrence, Peter A.

doi:10.1016/0092-8674(89)90020-2

Cited by 434 publications

(131 citation statements)

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“…2E). Wingless, best known for its role in establishing and maintaining segment polarity during embryogenesis, is a highly pleiotropic signaling protein with many independent roles in development (29)(30)(31)(32). Most relevant, Wg is required for pattern formation in the adult Drosophila abdominal epidermis (33).…”

Section: Sex-specific Regulation Of the Morphogen Wingless Is Correlatedmentioning

confidence: 99%

Sexually dimorphic regulation of the Wingless morphogen controls sex-specific segment number in Drosophila

Wang

Kidd

Carroll

et al. 2011

Proc. Natl. Acad. Sci. U.S.A.

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Sexual dimorphism is widespread throughout the metazoa and plays important roles in mate recognition and preference, sexbased niche partitioning, and sex-specific coadaptation. One notable example of sex-specific differences in insect body morphology is presented by the higher diptera, such as Drosophila, in which males develop fewer abdominal segments than females. Because diversity in segment number is a distinguishing feature of major arthropod clades, it is of fundamental interest to understand how different numbers of segments can be generated within the same species. Here we show that sex-specific and segment-specific regulation of the Wingless (Wg) morphogen underlies the development of sexually dimorphic adult segment number in Drosophila. Wg expression is repressed in the developing terminal male abdominal segment by the combination of the Hox protein Abdominal-B (Abd-B) and the sex-determination regulator Doublesex (Dsx). The subsequent loss of the terminal male abdominal segment during pupation occurs through a combination of developmental processes including segment compartmental transformation, apoptosis, and suppression of cell proliferation. Furthermore, we show that ectopic expression of Wg is sufficient to rescue this loss. We propose that dimorphic Wg regulation, in concert with monomorphic segment-specific programmed cell death, are the principal mechanisms of sculpting the sexually dimorphic abdomen of Drosophila.morphogenesis | segmentation | homeotic | epithelia B rachycera, higher diptera that include drosophilidae, exhibit an evolutionary trend toward reduced abdominal size that contributes to swift, maneuverable flight (1). Such reduction is especially pronounced within the infraorder Muscomorpha. Within this group of flies, abdominal reduction is sexually dimorphic such that adult males have fewer segments than females. Lower diptera, which includes mosquitoes and midges, retain ancestral morphology with respect to segment number; both adult males and females generate eight abdominal segments. In Muscomorpha the most posterior adult abdominal segments (all or a subset of segments A5-A8) are modified in females, usually as a telescoping ovipositor, whereas corresponding segments are absent in males (2). In all diptera, segment number is monomorphic during embryogenesis and larval development, reflecting the basal insect body plan of three head, three thoracic, and 11 abdominal segments. For most diptera, only embryonic abdominal segments 1-8 generate adult abdominal tissue (only segments 1-7 in the drosophilidae). The more posterior embryonic segments contribute to the adult genitalia. During pupation, sex-specific developmental programs are deployed that sculpt sexually dimorphic segment morphology and number.The posterior abdomen of Drosophila melanogaster serves as an excellent model to study the development of these sex-specific morphologies. Posterior abdominal segment identity, morphology, and number in both sexes is regulated by the Hox protein Abdominal-B (Abd-B) (3, 4). Abd-B ex...

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Section: Sex-specific Regulation Of the Morphogen Wingless Is Correlatedmentioning

confidence: 99%

Sexually dimorphic regulation of the Wingless morphogen controls sex-specific segment number in Drosophila

Wang

Kidd

Carroll

et al. 2011

Proc. Natl. Acad. Sci. U.S.A.

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“…This input is provided by the wingless (wg) gene, expressed in segmentally repeated stripes of cells that lie next to en-expressing cells 8,9 . The wg protein, which is homologous to the product of the proto-oncogene Wnt-1 ( ref.…”

Section: Introductionmentioning

confidence: 99%

“…This restriction requires expression of en by posterior cells 3,4,7 . But it seems that the onset of localized en expression in early embryos is not sufficient to irreversibly determine posterior compartment identity because en requires at least one cell-extrinsic input at this time.This input is provided by the wingless (wg) gene, expressed in segmentally repeated stripes of cells that lie next to en-expressing cells 8,9 . The wg protein, which is homologous to the product of the proto-oncogene Wnt-1 ( ref.…”

mentioning

confidence: 99%

Multiple modes of engrailed regulation in the progression towards cell fate determination

Heemskerk

DiNardo

Kostriken³

et al. 1991

Nature

246

147

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The engrailed gene product of Drosophila specifies the fate of a subset of cells in each segment. Our studies of engrailed regulation suggest that fate determination is an elaborate, multistep process. At the time in embryogenesis when the engrailed-dependent cell fate is probably determined, four modes of control act in an overlapping progression to govern engrailed expression. After activation by pairrule genes, both an extracellular signal, wingless, and autoregulation are required for engrailed expression. Autoregulation graduates to wingless independence, but is transient, and is superseded by an engrailed-independent mode of maintenance.Two levels of commitment have been defined for the choice of cell fate 1 . Early in development, fate can be instructed by environmental cues. This fate specification is flexible and allows fate to change in response to extracellular signals. But cells can undergo a transition from this type of specification to one which is determined and therefore irreversible. Because a determined cell maintains a particular fate independent of its environment, the transition to a determined state requires that development comes under cell-intrinsic, rather than cell-extrinsic control. The identification of selector genes in Drosophila provides an opportunity to study the basis of both types of cell-fate control. Selector genes encode regulators whose function defines the fate of a cell, and whose continued expression stably maintains cell fate 2,3 . Where the choice of cell fate is initially dependent on the environment, selector gene expression must be sensitive to extracellular signals. By contrast, once cell fate is determined, expression of these genes must be governed exclusively by cell-intrinsic factors.The engrailed (en) gene is a selector gene that distinguishes two populations of cells in each developing embryonic segment, the progenitors of the anterior and posterior compartments 3,4 . This distinction can be seen as a lineage restriction when individual embryonic cells are marked by mitotic recombination 5,6 . These give rise to clonal patches in the adult that never span the boundary between the anterior and posterior compartments, demonstrating that, from the time of marking, the progeny of a given cell only contribute to one compartment. This restriction requires expression of en by posterior cells 3,4,7 . But it seems that the onset of localized en expression in early embryos is not sufficient to irreversibly determine posterior compartment identity because en requires at least one cell-extrinsic input at this time.This input is provided by the wingless (wg) gene, expressed in segmentally repeated stripes of cells that lie next to en-expressing cells 8,9 . The wg protein, which is homologous to the product of the proto-oncogene Wnt-1 ( ref. 10 ), is secreted and appears to be taken up by en-expressing cells 9 . In wg mutant embryos, en expression is initiated in a normal striped pattern but soon stops, indicating that continued en expression in wild-type embryos r...

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“…En effet, par immunolocalisation et analyse en microscopie électronique, Wingless est majoritairement détecté dans les endosomes des cellules épidermiques embryonnaires de la drosophile [8,9]. Sur la base de cette observation, il a donc été suggéré que ce morphogène se propage au sein de ce tissu par transcytose « planaire » (c'est-à-dire dans le plan de l'épithé-lium), par analogie à la transcytose trans-épithéliale qui désigne le transport vésiculaire entre le domaine basal et le domaine apical des cellules épithéliales [10].…”

Section: Endocytose Et Transport Des Morphogènesunclassified

Morphogènes et endocytose

Dubois

2003

Med Sci (Paris)

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Au cours du développement, chaque cellule au sein d'un tissu sait où elle se trouve, et adopte un destin approprié à la position qu'elle occupe: on dit qu'elle possède une information de position. Généralement, cette information de position est fournie par un groupe de cellules particulières, l'organisateur, sous la forme d'un signal morphogène formant un gradient de concentration au sein du tissu. Ainsi, les cellules « mesurent » la distance qui les sépare de l'organisateur grâce à la concentration locale du signal morphogène à laquelle elles sont soumises [1]. Dès le début du siècle dernier, plusieurs embryologistes ont suspecté l'existence de ces gradients. Mais ce n'est qu'au cours de ces quinze dernières années que quelques molécules ont pu être qualifiées de morphogènes. À l'heure actuelle, une molécule sécrétée est qualifiée de morphogène si elle agit directement sur des cellules distantes de sa source et si elle induit, au niveau de ces cellules, des réponses distinctes selon sa concentration. Chez la drosophile, les protéines sécrétées Wingless, Hedgehog et Decapentaplegic (Dpp) (membre de la famille des TGF-β) remplissent ces conditions. Par exemple, les disques imaginaux de la larve, qui formeront les appendices de l'adulte, sont constitués d'un compartiment antérieur et d'un compartiment posté-rieur. Dpp est exprimé dans le compartiment antérieur au sein d'une fine bande de cellules située le long de la frontière antéro-postérieure (Figure 1). Dpp est absolument requis pour l'organisation des disques et le développement des appendices(➜). Dans les cellules voisines de son lieu de production, Dpp active l'expression des gènes spalt et optomotorblind (omb). Mais la concentration de Dpp requise pour activer spalt est plus forte que celle requise pour activer optomotorblind. Il en résulte que spalt est exprimé dans les cellules situées près de la source de Dpp, alors que optomotorblind est exprimé dans un domaine cellulaire plus large, également centré sur les cellules exprimant Dpp (Figure 1). La présence du récep-teur de Dpp Thikvein (Tkv) est nécessaire pour activer spalt et optomotorblind dans tous leurs domaines d'expression. Ce résultat indique que l'activation de ces gènes dépend de la réception du signal Dpp, y compris dans les cellules les plus distantes de son lieu de production, suggérant que Dpp doit atteindre directement ces cellules. C'est sur la base de ces observations que Dpp a été qualifié de morphogène [2,3]. Cependant, même si Dpp se définit fonctionnellement comme un MEDECINE/SCIENCES 2003 ; 19 : 351-7 REVUES MINI-SYNTHÈSE > Les protéines signalisatrices des familles Wingless/Wnt, Hedgehog et Decapentaplegic (Dpp)/Bone morphogenic protein (BMP) agissent comme des morphogènes au cours du développe-ment. On sait aujourd'hui que ces molécules sécrétées agissent directement sur des cellules pourtant distantes de leurs sites de production, mais peu de choses sont connues sur la façon dont ces molécules se propagent au sein d'un tissu, et sur les mécanismes contrôlant cette propagation....

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Distribution of the wingless gene product in drosophila embryos: A protein involved in cell-cell communication

Cited by 434 publications

References 47 publications

Sexually dimorphic regulation of the Wingless morphogen controls sex-specific segment number in Drosophila

Sexually dimorphic regulation of the Wingless morphogen controls sex-specific segment number in Drosophila

Multiple modes of engrailed regulation in the progression towards cell fate determination

Morphogènes et endocytose

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