DPP controls tracheal cell migration along the dorsoventral body axis of the <i>Drosophila</i> embryo

Vincent, Stéphane; Ruberte, Esther; Grieder, Nicole C.; Chen, Chao-Kung; Haerry, Theo; Schuh, Reinhard; Affolter, Markus

doi:10.1242/dev.124.14.2741

Cited by 97 publications

(13 citation statements)

References 36 publications

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“…The binding of Dpp to a type II and type I receptor complex [consisting primarily of the serine threonine kinases encoded by punt and thickveins (tkv); Brummel et al, 1994;Nellen et al, 1994;Penton et al, 1994;Letsou et al, 1995;Ruberte et al, 1995] leads to phosphorylation of receptor-speci®c Smads [such as the Mothers against dpp (Mad) gene product; Sekelsky et al, 1995]. The phosphorylated Smad then associates with a general Smad partner, such as the Medea (Med) gene product (Das et al, 1998;Hudson et al, 1998;Inoue et al, 1998;Wisotzkey et al, 1998), and the Smad complex translocates to the nucleus where it functions together with other transcription factors to regulate expression of target genes (Massague and Wotton, 2000). Drosophila Mad was the ®rst Smad demonstrated to possess direct DNA binding activity (Kim et al, 1997).…”

Section: Introductionmentioning

confidence: 99%

“…it can exert long‐range patterning effects and specify positional identities in a concentration‐dependent manner (Lecuit et al ., 1996; Nellen et al ., 1996; Podos and Ferguson, 1999). Dpp is required for multiple aspects of embryonic and adult development, such as specification of the dorsoventral axis in the embryo (Irish and Gelbart, 1987; Ferguson and Anderson, 1992; Podos and Ferguson, 1999), mesoderm and endoderm induction (Frasch, 1995; Bienz, 1997), tracheal cell migration (Vincent et al ., 1997) and patterning of the adult appendages (Spencer et al ., 1982; Capdevila and Guerrero, 1994; Zecca et al ., 1995).…”

Section: Introductionmentioning

confidence: 99%

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Direct transcriptional control of the Dpp target omb by the DNA binding protein Brinker

et al. 2000

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The gradient morphogen Decapentaplegic (Dpp) organizes pattern by inducing the transcription of different target genes at distinct threshold concentrations during Drosophila development. An important, albeit indirect, mode by which Dpp controls the spatial extent of its targets is via the graded downregulation of brinker, whose product in turn negatively regulates the expression of these targets. Here we report the molecular dissection of the cis-regulatory sequences of optomotor-blind (omb), a Dpp target gene in the wing. We identify a minimal 284 bp Dpp response element and demonstrate that it is subject to Brinker (Brk) repression. Using this omb wing enhancer, we show that Brk is a sequence-specific DNA binding protein. Mutations in the high-affinity Brk binding site abolish responsiveness of this omb enhancer to Brk and also compromise the input of an unknown transcriptional activator. Our results therefore identify Brk as a novel transcription factor antagonizing Dpp signalling by directly binding target genes and repressing their expression.

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Section: Introductionmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

Direct transcriptional control of the Dpp target omb by the DNA binding protein Brinker

et al. 2000

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“…Tracheal tdf expression, as shown here, coincides with the spatial limits of trh expression and is dependent on trh activity. This (Vincent et al, 1997). In contrast, TDF directs general tracheal cell migration independently of either signalling pathways.…”

Section: The Role Of Tdf In Tracheal System Formationmentioning

confidence: 91%

“…The second pathway is initiated by the morphogen Decapentaplegic (DPP), a member of the TGFβ superfamily, that is expressed on the dorsal and ventral side of the invaginating tracheal metameres (Affolter et al ., 1994; Vincent et al ., 1997). DPP signalling via receptor serine/threonine kinases (Ruberte et al ., 1995) directs tracheal cell migration along the dorsoventral body axis and it causes localized gene expression patterns in the developing tracheal placode (Vincent et al ., 1997). Such regionalized gene expression in response to DPP signalling is seen for the transcription factors knirps ( kni ) (Nauber et al ., 1988) and spalt ( sal ) (Kühnlein et al ., 1994).…”

Section: Introductionmentioning

confidence: 99%

The tracheae defective gene encodes a bZIP protein that controls tracheal cell movement during Drosophila embryogenesis

Eulenberg¹,

Schuh

1997

The EMBO Journal

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The tracheae defective (tdf) gene is required for the formation of the tracheal system during Drosophila embryogenesis. It encodes a putative bZIP transcription factor (TDF). Antibodies directed against TDF detect a nuclear protein in all tracheal cells before invagination and throughout tracheal system morphogenesis. Examination of tdf mutants revealed that tdf activity is not necessary for determining tracheal cell identity but for subsequent morphogenetic cell movements. tdf activity is under the control of trachealess, the key regulator gene for tracheal development. In contrast, tdf activity is not dependent on and does not interfere with the fibroblast growth factor- (FGF) and Decapentaplegic- (DPP) mediated signalling that direct guided tracheal cell migration. Our results suggest that lack of tdf activity affects tracheal cell migration in general rather than specific aspects of cell migration. tdf activity involves a maternal and zygotic component and its requirement is not limited to tracheal system formation. The complex spatiotemporal patterns of TDF expression in the embryo correspond to defects, suggesting that cell migration is impaired. We propose that the bZIP protein TDF functions as a co-regulator of target genes that provide cells with the ability to migrate.

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“…It is a network of epithelial tubes with a monolayer of tightly-adhered polarized cells surrounding a central apical lumen. Previous research has revealed the mechanisms of the early steps of tube formation, including the specification of branch identities [1][2][3][4][5][6][7][8][9], the migration of tracheal cells [10][11][12][13], as well as branch fusion led by fusion cells at the tips of the branch to form an interconnected tubular network [14][15][16][17][18]. Tracheal tube maturation is a sequential process in which: (a) an apical secretion pulse deposits extracellular matrix components to form aECM [19].…”

Section: Introductionmentioning

confidence: 99%

The Osiris family genes function as novel regulators of the tube maturation process in the Drosophila trachea

et al. 2023

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Drosophila trachea is a premier model to study tube morphogenesis. After the formation of continuous tubes, tube maturation follows. Tracheal tube maturation starts with an apical secretion pulse that deposits extracellular matrix components to form a chitin-based apical luminal matrix (aECM). This aECM is then cleared and followed by the maturation of taenidial folds. Finally, air fills the tubes. Meanwhile, the cellular junctions are maintained to ensure tube integrity. Previous research has identified several key components (ER, Golgi, several endosomes) of protein trafficking pathways that regulate the secretion and clearance of aECM, and the maintenance of cellular junctions. The Osiris (Osi) gene family is located at the Triplo-lethal (Tpl) locus on chromosome 3R 83D4-E3 and exhibits dosage sensitivity. Here, we show that three Osi genes (Osi9, Osi15, Osi19), function redundantly to regulate adherens junction (AJ) maintenance, luminal clearance, taenidial fold formation, tube morphology, and air filling during tube maturation. The localization of Osi proteins in endosomes (Rab7-containing late endosomes, Rab11-containing recycling endosomes, Lamp-containing lysosomes) and the reduction of these endosomes in Osi mutants suggest the possible role of Osi genes in tube maturation through endosome-mediated trafficking. We analyzed tube maturation in zygotic rab11 and rab7 mutants, respectively, to determine whether endosome-mediated trafficking is required. Interestingly, similar tube maturation defects were observed in rab11 but not in rab7 mutants, suggesting the involvement of Rab11-mediated trafficking, but not Rab7-mediated trafficking, in this process. To investigate whether Osi genes regulate tube maturation primarily through the maintenance of Rab11-containing endosomes, we overexpressed rab11 in Osi mutant trachea. Surprisingly, no obvious rescue was observed. Thus, increasing endosome numbers is not sufficient to rescue tube maturation defects in Osi mutants. These results suggest that Osi genes regulate other aspects of endosome-mediated trafficking, or regulate an unknown mechanism that converges or acts in parallel with Rab11-mediated trafficking during tube maturation.

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DPP controls tracheal cell migration along the dorsoventral body axis of the Drosophila embryo

Cited by 97 publications

References 36 publications

Direct transcriptional control of the Dpp target omb by the DNA binding protein Brinker

Direct transcriptional control of the Dpp target omb by the DNA binding protein Brinker

The tracheae defective gene encodes a bZIP protein that controls tracheal cell movement during Drosophila embryogenesis

The Osiris family genes function as novel regulators of the tube maturation process in the Drosophila trachea

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