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The results suggest that determination for bristle type does not depend on a prior determination decision for organ type. The results also provide an avenue for exploring the nature of 'competence' at cellular and molecular levels Scanga, It is of interest to investigate the regulatory basis of classic Antp alleles that give rise to antenna to leg transformations. The duplication gives the mutant gene three Antp promoters, and transcripts from each of these are correctly processed to yield functional ANTP proteins.
At least two of the promoters are ectopically active in the eye-antenna imaginal discs, leading to homeotic transformation of the adult head Talbert, A aa peptide corresponding to the homeodomain of Antennapedia protein can translocate through the membrane of neurons in culture, accumulate in neuronal nuclei, and promote neurite growth. Three mutant versions of ANTP were constructed that differ in their ability to translocate through the membrane and to bind specifically the cognate sequence for homeodomains present in the promoter of HoxA5.
Removing two hydrophobic residues of the third helix inhibits ANTP internalization and suppresses its neurotrophic activity.
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ANTP neurotrophic activity is lost when mutations are introduced in positions preserving its penetration and nuclear accumulation but abolishing its capacity to bind specifically the cognate DNA-binding motif for homeoproteins. These results suggest that Antennapedia protein neurotrophicity requires both its internalization and its specific binding to homeobox cognate sequences Le Roux, Control of the spineless antennal enhancer: direct repression of antennal target genes by Antennapedia It is currently thought that antennal target genes are activated in Drosophila by the combined action of Distal-less, homothorax , and extradenticle , and that the Hox gene Antennapedia prevents activation of antennal genes in the leg by repressing homothorax.
To test these ideas, a 62bp enhancer was isolated from the antennal gene spineless that is specific for the third antennal segment. This enhancer is activated by a tripartite complex of Distal-less, Homothorax, and Extradenticle. Surprisingly, Antennapedia represses the enhancer directly, at least in part by competing with Distal-less for binding.
Antennapedia is required in the leg only within a proximal ring that coexpresses Distal-less, Homothorax and Extradenticle.
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It is concluded that the function of Antennapedia in the leg is not to repress homothorax , as has been suggested, but to directly repress spineless and other antennal genes that would otherwise be activated within this ring Duncan, This report examines the regulation of an enhancer from the antennal gene ss that drives expression specifically in the third antennal segment A3. The work provides the first look at how the homeodomain proteins Dll, Hth, and Exd function in the antenna to activate antennal target genes. This work also reveals how the Hox protein Antp functions in the leg to repress antennal development.
The conventional view has been that the primary function of Antp is to repress hth in the distal leg, which then prevents the activation of all downstream antennal genes. However, this study found that Antp represses the ss A3 enhancer directly. This repression is essential within a proximal ring in the leg that coexpresses the antennal gene activators Dll, Hth, and Exd.
Antp competes with Dll for binding to the enhancer, and this competition is part of a molecular switch that allows the ss A3 element to be activated in the antenna, but represses its activation in the leg. The results suggest that repression of antenna-specific genes in the proximal ring is the sole function of Antp in the leg imaginal disc Duncan, The enhancer is also very specific, driving expression in A3 and nowhere else in imaginal discs. It has been proposed that antennal identity in Drosophila is determined by the combined action of Dll, Hth, and Exd.
Consistent with this proposal, all three of these factors were found to be required for D4 expression. A previous report Emmons, showed that the antennal expression pattern of ss is reproduced by lacZ reporters containing a bp fragment from the ss 5' region. Expression in the arista and the third antennal segment A3 prove to be under separate control; expression in the arista requires domains 1, 3 and 5, whereas expression in A3 is lost only when domain 4 is deleted. Moreover, reporters containing domain 4 alone show expression in A3 and nowhere else in imaginal discs.
Thus, domain 4 is both necessary and sufficient for A3-specific expression. The activators Hth and Exd bind with strong cooperativity to directly adjacent sites. Their joint binding site matches the optimum site for in vitro binding of the mammalian homologs of Hth and Exd Meis and Prep , consistent with the robust activity of the enhancer in vivo. Mutation of either of these sites abolishes activity of the enhancer. The coactivator Dll binds three sites in D4 ; one of these sites Dlla is required for almost all activity of the enhancer. Dll shows strong cooperativity with Hth and Exd for binding to D4 , indicating that Dll interacts physically with these proteins.
This interaction requires DNA binding, as Dll protein containing a missense change that blocks DNA binding a change of asn51 to ala in the homeodomain shows no ability to associate with D4 -bound Hth and Exd. A curious feature of the cooperativity seen in the binding studies is that although Hth and Exd increase the affinity of Dll for D4 , Dll appears to have little effect on the affinity of Hth and Exd for the enhancer.
Since Hth and Exd already bind cooperatively with one another, it may be that additional cooperative interactions with Dll have little effect.
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If so, Hth and Exd would be expected to increase Dll binding to D4 , but Dll would have little effect on the binding of Hth and Exd, as observed. Interactions between Dll and Hth in the absence of DNA have been reported in immunoprecipitation experiments. However, this study was unable to repeat these observations. Moreover, the finding that the asn51 mutant of Dll fails to associate with D4 -bound Hth and Exd argues strongly against such interactions Duncan, The repressor Cut also acts directly upon D4. These binding sites suggest that D4 is controlled by Cut in much the same way that a structurally similar Abdominal-A Abd-A regulated enhancer from the rhomboid gene is controlled by the repressor Senseless Sens.
In the rhomboid enhancer, adjacent Hth and Exd sites are also present, and these create a binding site for Sens. Activity of the rhomboid enhancer is controlled by a competition between binding of the Sens repressor and binding of the activators Abd-A, Hth, and Exd.
It seems likely that D4 is controlled similarly, with the repressor Cut competing for binding with the activators Dll, Hth, and Exd. It will be of interest to determine whether enhancers similar to D4 are used more widely to control Cut targets involved in its role as an external sense organ determinant Duncan, A key finding in this work is that Antp represses D4 by direct interaction. Antp binds a single site in D4 , which overlaps or is identical to the Dlla binding site. Like Dll, Antp binds cooperatively with Hth and Exd. Using purified proteins, it was showm that binding of Dll and Antp to the Dlla site is mutually exclusive.
This indicates that Antp represses the enhancer at least in part by competing with Dll for binding. Similar competition may occur at other enhancers; when Antp expression is driven artificially in the distal leg, variable deletions of the tarsal segments occur. These defects might arise because Antp competes with Dll for binding to its target genes in the distal leg. In most other contexts examined, Antp is an activator of transcription; why it fails to activate D4 is not clear. The similar behavior of Dll and Antp in binding to D4 supports the idea that Dll behaves like a Hox protein in activating D4 Duncan, Although the initial focus of this study was on the antenna, the finding that Antp interacts directly with D4 led to an examination of D4 regulation in the leg, where Antp is normally expressed.
In second leg imaginal discs, Antp is required only in a proximal ring of cells that coexpresses Dll and Hth. This ring appears in the early third instar, and is of uncertain function. Importantly, such clones have no effect on the expression of Dll or Hth within the ring. Second, many such clones begin expressing the antennal markers Ss and Cut, indicating a transformation to antenna, and round up as if they have lost affinity for neighboring cells. Third, such clones appear to extend and move distally in the disc Duncan, The finding that only clones that overlap the proximal ring undergo transformation accounts for this observation.
Most importantly, these observations provide an explanation for why ss is controlled directly by Antp. Therefore, Antp must function in the ring at the target gene level to repress antennal genes that would otherwise be activated by combined Hth and Dll and Exd. Since several such targets are known, it seems likely that several, perhaps many, antennal genes in addition to ss are repressed directly by Antp Duncan, If hth is not directly controlled by Antp in the leg, as this study suggests, then why is hth ectopically expressed within such clones?
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A likely explanation is that downstream antennal genes that have become activated in such clones feed back to activate hth. This interpretation is strongly supported by the finding that ectopic expression of the antennal genes ss , dan , or danr in the distal leg causes ectopic activation of hth. Whether repression of hth in the antenna by ectopic Antp is also indirect is not clear. The function of the proximal Dll- and Hth-expressing ring in the proximal leg is not well understood.
The ring is highly conserved among the insects, and may serve as a boundary between the proximal and distal portions of the legs. In the context of this work, a striking feature of the ring is that it contains a microcosm of gene expression domains corresponding to the three major antennal segments. These expression combinations are characteristic of the A1, A2, and A3 antennal segments, respectively. Looked at in this way, the ring would appear to resemble a repressed antennal primordium within the leg Duncan, It has been known for almost thirty years that Antp is required in the leg to repress antennal identity.
However, an understanding of how this repression occurs has been lacking. The current results indicate that Antp functions within the proximal ring to directly repress antennal genes that would otherwise be activated by combined expression of Dll, Hth, and Exd. This appears to be the only function of Antp in the leg, at least during the third instar larval stage. The results are entirely consistent with the idea that second leg is the 'ground state' ventral appendage the limb type that develops in the absence of identity specification and that the role of Antp in the leg is to preserve this ground state by repressing the activation of 'head-determining' genes Duncan, Segment-specific regulation of the Drosophila AP-2 gene during leg and antennal development Segmentation involves subdivision of a developing body part into multiple repetitive units during embryogenesis.
In Drosophila and other insects, embryonic segmentation is regulated by genes expressed in the same domain of every segment. Less is known about the molecular basis for segmentation of individual body parts occurring at later developmental stages.
The Drosophila transcription factor AP-2 gene, dAP-2 , is required for outgrowth of leg and antennal segments and is expressed in every segment boundary within the larval imaginal discs. To investigate the molecular mechanisms generating the segmentally repetitive pattern of dAP-2 expression, transgenic reporter analyses was performed and multiple cis-regulatory elements were isolated that can individually or cooperatively recapitulate endogenous dAP-2 expression in different segments of the appendages. An enhancer specific for the proximal femur region, which corresponds to the distal-most expression domain of homothorax hth , was analyzed in the leg imaginal discs.
Hth is known to be responsible for the nuclear localization and, hence, function of the Hox cofactor, Extradenticle Exd. These loss- and gain-of-function studies further support direct regulation of dAP-2 by Hox proteins and suggest that Hox proteins function redundantly in dAP-2 regulation. This study reveals that discrete segment-specific enhancers underlie the seemingly simple repetitive expression of dAP-2 and provides evidence for direct regulation of leg segmentation by regional combinations of the proximodistal patterning genes Ahn, The segmentally repeated expression of dAP-2 in the developing leg and antennal discs may suggest that its expression in each segment is regulated in a similar manner by upstream segmentation genes.
Alternatively, each domain ring of dAP-2 expression could result from the combinatorial activities of multiple transcription factors, which themselves are not expressed in a repeated pattern, but instead occupy distinct and broader domains along the PD axis of the appendages. Current data provide strong evidence that the latter strategy is utilized to establish dAP-2 expression in all but the tarsal segments.
It seems that the tarsus has adopted a strategy different from that of other leg segments to regulate dAP-2 expression Ahn, In an effort to understand molecular mechanisms controlling dAP-2 expression during leg development, the regulatory potential of dAP-2 genomic fragments was tested using transgenic reporter analyses.
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Multiple enhancers were successfully isolated which can independently direct reporter expression in specific leg segments and together recapitulate, almost completely, the endogenous expression pattern. It is intriguing that the relative positions of these enhancers on the chromosome are well correlated with the position of their activity along the PD axis of the leg. Importantly, the presence of segment-specific enhancers suggests that dAP-2 expression is differentially regulated in each leg segment. It is likely that each domain of dAP-2 expression in the true joints is regulated by a combination of upstream regulators involved in PD patterning using segment-specific enhancers similar to the distinct enhancers used to regulate expression of the pair-rule gene, even-skipped , in every other parasegment during embryonic segmentation.
Interestingly, dAP-2 expression in the coxa is differentially regulated along the DV axis and depends on two region-specific enhancers.