The Vestigial and Scalloped proteins act together to directly regulate wing-specific gene expression in <i>Drosophila</i>

Halder, Georg; Polaczyk, Patricia J.; Kraus, Mary Ellen; Hudson, Amy W.; Kim, Jaeseob; Laughon, Allen; Carroll, Sean B.

doi:10.1101/gad.12.24.3900

Cited by 216 publications

(265 citation statements)

References 46 publications

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“…However, this is at odds with the presumptive activating function mediated by an Sd-Vg complex that occurs in other tissues like the wing imaginal disk, where an Sd-Vg complex binds and activates the vg boundary enhancer (Halder et al, 1998). The differential activities of these proteins in muscle versus wing development may reflect a requirement for yet additional proteins within a presumptive Vg/Sd/Dmef2 complex to modify its activity in a tissue-specific manner.…”

Section: Discussioncontrasting

confidence: 41%

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Alternative Requirements for Vestigial, Scalloped, and Dmef2 during Muscle Differentiation inDrosophila melanogaster

Deng

Hughes

Bell³

et al. 2009

MBoC

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Vertebrate development requires the activity of the myocyte enhancer factor 2 (mef2) gene family for muscle cell specification and subsequent differentiation. Additionally, several muscle-specific functions of MEF2 family proteins require binding additional cofactors including members of the Transcription Enhancing Factor-1 (TEF-1) and Vestigiallike protein families. In Drosophila there is a single mef2 (Dmef2) gene as well single homologues of TEF-1 and vestigial-like, scalloped (sd), and vestigial (vg), respectively. To clarify the role(s) of these factors, we examined the requirements for Vg and Sd during Drosophila muscle specification. We found that both are required for muscle differentiation as loss of sd or vg leads to a reproducible loss of a subset of either cardiac or somatic muscle cells in developing embryos. This muscle requirement for Sd or Vg is cell specific, as ubiquitous overexpression of either or both of these proteins in muscle cells has a deleterious effect on muscle differentiation. Finally, using both in vitro and in vivo binding assays, we determined that Sd, Vg, and Dmef2 can interact directly. Thus, the muscle-specific phenotypes we have associated with Vg or Sd may be a consequence of alternative binding of Vg and/or Sd to Dmef2 forming alternative protein complexes that modify Dmef2 activity. INTRODUCTIONSpecification and differentiation of both vertebrate and invertebrate muscles requires a conserved cohort of transcription factors (Baylies et al., 1998;Cripps and Olson, 2002). Among these, myocyte enhancer factor-2 (MEF2) plays a key role in specification and subsequent differentiation of all muscle types (skeletal, smooth, and heart muscle; Lilly et al., 1995;. There are four different known vertebrate mef2 genes: mef2-a, -b, -c, and -d (Black and Olson, 1998). These four genes produce several different MEF2 isoforms involved in differentiation of all muscle types. In addition, it has been proposed that MEF2 proteins have a requirement for tissue-specific cofactors to confer additional specificity. For example, during mammalian heart development, GATA-4 (Charron and Nemer, 1999) helps to recruit MEF2 to the promoters of cardiac-specific genes including atrial natriuretic factor (ANF) and ␣-cardiac actin (␣-CA; Morin et al., 2000). MEF2 also interacts with another transcription factor, HAND1, during activation of ANF in cardiac cells (Morin et al., 2005). This complex interplay between MEF2 proteins and cofactors is not restricted to cardiac muscles as during skeletal muscle development; MEF2 interacts with MyoD during activation of specific structural genes (Molkentin et al., 1995;.In terms of MEF2 protein family activity, muscle differentiation in Drosophila is relatively less complex as there is only a single homologue mef2, Dmef2 (Lilly et al., 1994). Like vertebrates, Drosophila Dmef2 isoforms activate muscle-specific genes and also seems to interact with a conserved cohort of interacting proteins for muscle specification, including cardiogenesis. These include tinman (Azp...

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Section: Discussioncontrasting

confidence: 41%

“…In fact, ectopic expression of Vg, in the cells of the developing eye that also express Sd, leads to a respecification of these cells to a wing phenotype (Halder et al, 1998;Simmonds et al, 1998). Vg has two domains that influence transcriptional activation activity (MacKay et al, 2003) al., 2002).…”

Section: Introductionmentioning

confidence: 99%

Alternative Requirements for Vestigial, Scalloped, and Dmef2 during Muscle Differentiation inDrosophila melanogaster

Deng

Hughes

Bell³

et al. 2009

MBoC

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“…6,9 It has been shown that vg interacts genetically and molecularly with the scalloped (sd) gene product. [10][11][12] vg and sd are coexpressed in the wing imaginal disc and dimerization of VG and SD seems to be a prerequisite for translocation of the dimer to the nucleus, where it acts as a functional transcription factor. [12][13][14] In fact, in the heterodimer, SD contains the transcription enhancer activator (TEA) DNA binding domain, while VG provides the transcriptional activation domain.…”

Section: Introductionmentioning

confidence: 99%

“…[10][11][12] vg and sd are coexpressed in the wing imaginal disc and dimerization of VG and SD seems to be a prerequisite for translocation of the dimer to the nucleus, where it acts as a functional transcription factor. [12][13][14] In fact, in the heterodimer, SD contains the transcription enhancer activator (TEA) DNA binding domain, while VG provides the transcriptional activation domain. 10,12,14 It has been shown that ectopic expression of vg in other imaginal discs induces wing outgrowths, this being dependent on the presence of SD.…”

Section: Introductionmentioning

confidence: 99%

“…[12][13][14] In fact, in the heterodimer, SD contains the transcription enhancer activator (TEA) DNA binding domain, while VG provides the transcriptional activation domain. 10,12,14 It has been shown that ectopic expression of vg in other imaginal discs induces wing outgrowths, this being dependent on the presence of SD. 4,11 Therefore, vg seems to be required for both wing identity and cell proliferation, suggesting that the VG-SD dimer could be one of the links between signalling genes and genes involved in cell proliferation.…”

Section: Introductionmentioning

confidence: 99%

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The Drosophila wing differentiation factor Vestigial–Scalloped is required for cell proliferation and cell survival at the dorso-ventral boundary of the wing imaginal disc

et al. 2003

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Links between genes involved in development, proliferation and apoptosis have been difficult to establish. In the Drosophila wing disc, the vestigial (vg) and the scalloped (sd) gene products dimerize to form a functional transcription factor. Ectopic expression of vg in other imaginal discs induces outgrowth and wing tissue specification. We investigated the role of the VG-SD dimer in proliferation and showed that vg antagonizes the effect of dacapo, the cyclin-cdk inhibitor. Moreover, ectopic vg drives cell cycle progression and in HeLa cultured cells, the VG-SD dimer induces cell proliferation per se. In Drosophila, ectopic vg induces expression of dE2F1 and its targets dRNR2 and string. In addition vg, but not dE2F1, interacts with and induces expression of dihydrofolate reductase (DHFR). Moreover, a decrease in VG or addition of aminopterin, a specific DHFR inhibitor, shift the dorso-ventral boundary cells of the disc to a cell death sensitive state that is correlated with reaper induction and DIAP1 downregulation. This indicates that vg in interaction with dE2F1 and DHFR is a critical player for both cell proliferation and cell survival in the presumptive wing margin area.

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The function of vestigial in Drosophila wing development: How are tissue-specific responses to signalling pathways specified?

Celis

1999

Bioessays

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The activities of conserved signal transduction pathways are central to the development of Drosophila wings, legs, and eyes. Yet, all these structures have characteristic morphologies, suggesting that additional factors provide organ‐specific information. One excellent candidate for such a function is Vestigial, which activity promotes the formation of wings. The biochemical function of Vestigial is unknown, however, since no homologies with other proteins have been identified. Two recent reports show that Vestigial interacts with the transcription factor Scalloped,(1,2) forming an active complex that binds to specific DNA sequences and regulates gene expression in cooperation with several signalling pathways.(3) These results illustrate how tissue‐specific transcription factors cooperate with general signalling pathways to regulate gene expression in a tissue‐specific manner. BioEssays 21:542–545, 1999. © 1999 John Wiley & Sons, Inc.

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The Vestigial and Scalloped proteins act together to directly regulate wing-specific gene expression in Drosophila

Cited by 216 publications

References 46 publications

Alternative Requirements for Vestigial, Scalloped, and Dmef2 during Muscle Differentiation inDrosophila melanogaster

Alternative Requirements for Vestigial, Scalloped, and Dmef2 during Muscle Differentiation inDrosophila melanogaster

The Drosophila wing differentiation factor Vestigial–Scalloped is required for cell proliferation and cell survival at the dorso-ventral boundary of the wing imaginal disc

The function of vestigial in Drosophila wing development: How are tissue-specific responses to signalling pathways specified?

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