decapentaplegic
Decapentaplegic plays a key role in the embryo during endoderm induction. During this process, Dpp stimulates transcription of the homeotic genes Ultrabithorax in the visceral mesoderm and labial in the subjacent endoderm. A cAMP response element (CRE) from anUltrabithorax enhancer mediates Dpp-responsive transcription in the embryonic midgut, and endoderm expression from a labial enhancer depends on multiple CREs. The enhancer, called Ubx B confers Wingless- and Decapentaplegic-dependent expression in the visceral mesoderm. Staining mediated by Ubx B is in two stripes of cells in the visceral mesoderm, a wide prominent one in parasegments 6-9 and a narrow weak one in parasegment 3. The Drosophila CRE-binding protein dCREB-2 binds to the Ultrabithorax
CRE. Binding is at a palindromic sequence TGGCGTCA that resembles a typical cAMP response element (CRE) (TGACGTCA). Mutation of this site results in the elimination of response to Dpp, but a maintenance of response to Wg. This residual expression is in parasegment 8 and 9 coinciding with the main source of wg expression in the middle midgut. The Ubx CRE can also mediate response to Dpp signaling in the endoderm. Other transcription factors act through the Ubx B enhancer to confer its tissue-specific response to Dpp in the visceral mesoderm. CRE needs to cooperate with an LEF-1 binding site to respond to the Dpp signal in the visceral mesoderm. Schnurri, a transcription factor implicated in Dpp signaling, fails to interact with Ubx B. Adjacent to the CRE is another palindromic sequence that antagonizes the activating effects of Dpp and Wg signaling on the Ubx B enhancer. Ubiquitous expression of a dominant-negative form of dCREB-2 suppresses CRE-mediated reporter gene expression and reduces labial expression in the endoderm. Therefore, a dCREB-2 protein may act as a nuclear target, or as a partner of a nuclear target, for Dpp signaling in the embryonic midgut (Eresh, 1997).
Dpp has a prime function during endoderm induction in Drosophila. Dpp is secreted from the outer cell layer of the embryonic midgut (the visceral mesoderm), where Dpp's main source of expression in parasegment ps7 depends directly on the homeotic gene Ultrabithorax (Ubx). In the same cell layer, Dpp stimulates expression of another extracellular signal, Wingless (Wg), in a neighboring parasegment (ps8), which in turn feeds back to ps7 to stimulate Ubx expression. Thus, Dpp is part of a "parautocrine" feedback loop of Ubx (i.e., an autocrine feedback loop based partly on paracrine action) that sustains its own expression through Dpp and Wg. Dpp also spreads to the inner layer of the embryonic midgut, the endoderm, where it synergizes with Wg to induce expression of the homeotic gene labial (lab). To achieve this, Dpp locally elevates the endodermal expression levels of Drosophila D-Fos with which it cooperates to induce lab. Differentiation of various cell types in the larval gut depends on these inductive effects of Dpp and Wg. A cAMP response element (CRE) from the Ubx midgut enhancer has been shown to be necessary and to some extent sufficient to mediate the Dpp response in the embryonic midgut (Eresh, 1997). CREs are known to be signal-responsive elements, not only for cAMP signaling as described initially but also for other signals including ones acting through Ras. This prompted an investigation of whether any other signal may play a part in the Dpp response. This led to the discovery that the Drosophila epidermal growth factor receptor (Egfr) has a critical function during endoderm induction. A secondary signal was discovered with a permissive role in this process, namely Vein, a neuregulin-like ligand that stimulates the epidermal growth factor receptor and Ras signaling. Dpp and Wg up-regulate vein expression in the midgut mesoderm in two regions overlapping the Dpp sources. This up-regulation depends on dpp and wg. Vein is thus a secondary signal of Dpp and Wg, and it stimulates homeotic gene expression in both cell layers of the midgut (Szuts, 1998).
Because loss-of-function mutants of the Drosophila Egfr are very abnormal and do not develop properly beyond the early embryonic stages, a temperature-sensitive allele of Egfr, flb1F26, was used to ask whether this receptor has any function in the embryonic midgut. flb1F26 embryos were stained with anti-Labial antibody after shifting the embryos from the permissive to the restrictive temperature at 6-8 hr of development (i.e., before midgut formation, but allowing normal germ-band retraction). The midguts of the homozygous flb1F26 embryos are severely abnormal, with none of the constrictions forming properly, and they show virtually no Lab staining in the midgut epithelium. These phenotypes indicate a critical function for Egfr in the embryonic midgut. Many endodermal cells were missing or seemingly unhealthy, especially in the middle midgut where lab is induced and in the anterior midgut near the gastric caeca. These two midgut regions correspond to the domains of Dpp expression. Similar effects of Egfr loss of function on cell health have been observed in earlier studies of the embryonic epidermis. Although this putative function of Egfr in cell survival may contribute to the observed loss of lab induction, it is believed that it does not account for all aspects of the gut phenotypes attributable to Egfr loss of function (Szuts, 1998).
The activity of the minimal Ubx midgut enhancer (Ubx B) was examined after mesodermal expression of dominant negative Egfr (DN-DER). Ubx B normally mediates strong lacZ staining in a region spanning the middle midgut constriction (ps6-ps9) and also some staining in the gastric caeca (ps3); the strongest staining in ps7/ps8 spans the main Dpp and Wg sources in the middle midgut, whereas the ps3 staining coincides with the anterior source of Dpp. Mesodermal expression of DN-DER almost completely eliminates staining in ps3 and strongly reduces staining in the ps6/ps7 region. These results lend strong support to the notion that Egfr functions in the visceral mesoderm; they indicate that Egfr positively regulates Ubx expression (Szuts, 1998).
Two ligands are known that activate Egfr in the somatic cells of Drosophila: Spitz, which apparently needs to be processed to an active form by the membrane-spanning protein Rhomboid, and Vein. spitz and rhomboid loss-of-function mutants were examined by staining embryos with Lab antibody, but these mutants appear to have only a minor effect on Lab expression: typically, Lab staining is found to be missing in just a few cells in the lab domain, and the midgut constrictions are normal in these mutants. However, vein mutant embryos show a drastic effect on Lab expression. The most extreme mutant conditions caused nearly complete loss of Lab staining in the midgut; none of the midgut constrictions form, nor do the gastric caeca elongate. Milder mutant conditions have only sporadic effects in the midgut, since only some cells in the lab domain lack Lab expression; the constrictions and the gastric caeca form normally under these conditions. These results implicate Vein as a critical ligand of Egfr in the embryonic midgut (Szuts, 1998).
EGFR expression is thought to be fairly ubiquitous in the embryo. However, vein transcripts are found in a highly restricted pattern, primarily in the embryonic mesoderm. In the midgut too, vein expression is spatially regulated, as follows: vein transcripts in the midgut are restricted to the visceral mesoderm. Initially, during stage 13, low levels of vein expression are seen at intervals throughout the midgut mesoderm. However, soon after the formation of the midgut epithelium, vein transcripts start to accumulate locally, and two main domains of prominent vein expression develop, one in the anterior and one in the middle midgut. Anteriorly, vein expression spans approximately ps2-ps4 and is strongest around the ps3/ps4 junction, that is, posterior to the gastric caeca. In the middle midgut, there is a fairly wide band of low vein expression spanning approximately ps6-ps10, with strongly up-regulated expression levels throughout ps7 (and trailing into anterior ps8). Posterior ps7 becomes the most prominent site of vein expression in the midgut. Finally, a narrow band with low levels of vein transcripts is seen at the posterior end of the midgut. The two main expression domains of vein overlap the two domains of Dpp expression in the visceral mesoderm (in ps3 and ps7), but each of them is considerably wider than the corresponding dpp domain. vein expression in the visceral mesoderm is severely diminished in dpps4 mutants. The prominent band of vein expression in ps7 is no longer seen, and expression in ps4 is reduced too. Instead, the strongest expression of vein in these mutants is seen at a novel location, at the ps5/ps6 junction around the incipient first midgut constriction (this ps5/ps6 expression is higher than in the wild type, and can be used to identify young dpp mutant embryos). It is concluded that dpp is required for the localized up-regulation of vein expression in the midgut (Szuts, 1998).
vein expression is also strongly diminished in wg mutants. vein expression can still be seen at moderate levels in the ps4 region, but vein expression is barely visible elsewhere in the midgut of these mutants. In particular, there are only traces of vein expression in the ps7/ps8 region, and expression at both midgut ends is almost undetectable. Clearly, wg plays an essential role as well in up-regulating vein expression. dpp and wg are sufficient to position the two domains of vein up-regulation. High mesodermal Wg causes very strong vein expression in ps2-ps7, significantly stronger than that caused in this region by mesodermal Dpp expression alone. This indicates that wg cooperates with dpp in positioning vein up-regulation. It is shown that neither Dpp for Egfr signaling is particularly effective in the absence of the other. Thus these two pathways are functionally interdependent and that they synergize with each other, revealing functional intertwining (Szuts, 1998).
The mutant analysis suggests strongly that Vein is the main, if not the only, ligand that stimulates Egfr in the embryonic midgut. This contrasts with other tissues, mainly of ectodermal origin, in which Spitz is the main Egfr ligand. Interestingly, Vein also has a major role during an inductive process between muscle and epidermis: Vein is secreted from muscle cells and triggers differentiation of the receiving epidermal cells into tendon cells. These functions of Vein during inductive processes between different cell layers suggest that the molecular properties of Vein are particularly suited to such processes that require the signal to cross basal membranes. Similarly, the extensive mesodermal expression of Vein may mean that this signal protein is particularly well-adapted to its production in this cell layer. Note that Vein is similar to mammalian neuregulins that appear to function in developmental contexts that involve communication between different cell layers (Szutz, 1998 and references).
The transcriptional response elements for the Dpp signal in midgut enhancers from homeotic target genes are bipartite, comprising CRE sites as well as binding sites for the Dpp signal-transducing protein Mad. Of these sites, the CRE seems to function primarily in the response to Ras, the secondary signal of Dpp. It is also shown that the Dpp response element in the labial enhancer comprises CREs and Mad binding sites. The results with the labial enhancer confirm the conclusions derived from the Ubx enhancer, namely that the response element to Dpp signaling is bipartite and contains Mad binding sites as well as CREs. The latter are critical in both cell layers for the signal response, whereas the former seem less criticial in the endoderm than in the visceral mesoderm. Perhaps this reflects the fact that lab is the ultimate target gene of the endoderm induction and that its enhancer clearly integrates a number of distinct positional inputs, some of which may be partially redundant (Szuts, 1998).
Why should there be this secondary signal whose role is entirely permissive, namely to assist the primary signal in implementing its tasks? Two kinds of answers are proposed. The first one is based on the observation that lack of Vein/Egfr signaling in the midgut appears to make cells sick and perhaps causes them to die. Therefore, Vein/Egfr signaling may serve as a "survival signal." Intriguingly, cell survival in embryos lacking vein or Egfr function appear to be affected preferentially near the two Dpp sources (where vein expression is up-regulated). Perhaps high levels of Dpp signaling can cause cell death; if so, vein signaling may be up-regulated to counteract a putative local deleterious effect of Dpp. A precedent for such a scenario may be found in the developing chick limb bud where the cell death-inducing properties of BMP (a TGF-beta-like signal) seem to be antagonized locally by a signal triggering the Ras pathway. However, although antagonistic effects between Egfr- and TGF-beta-type signaling have been observed, the evidence provided here suggests strongly that Vein/Egfr and Dpp both act positively in the embryonic midgut of Drosophila. Furthermore, they synergize with each other in the transcriptional stimulation of target genes. This observed synergy parallels cooperation between Ras and TGF-beta signaling during epithelial tumor progression. It is therefore thought unlikely that Vein functions in the midgut entirely as a survival signal near Dpp sources (Szuts, 1998).
The second kind of answer builds on the observations that indicate functional interdependence and synergy between the two signaling pathways in stimulating transcription of target genes. This could be beneficial for developmental systems in two ways: (1) if cells need to be costimulated by cooperating primary and secondary signals, this would serve to sharpen their signal response. This putative sharpening effect may be a contributory factor in sharp responses to signaling thresholds such as those observed in the Xenopus embryo.(2) The need for costimulation would safeguard against fortuitous and random stimulation of cells by any one signal, thus improving the reliability of their signal response. And although a requirement for the secondary signal is observed throughout the functional realm of the primary signal, it is envisaged that the role of the secondary signal is particularly critical in remote cells where the distribution of the primary signal becomes shallow, imprecise, and unreliable. Therefore, the secondary signal may provide primarily "remote stimulation." Whatever the case, it seems very likely that the use of a functionally coupled primary-secondary signal system results in a refinement and stabilization of positional information and in a degree of precision of this information that could not be conferred by one signal alone. Functional intertwining of a secondary and a primary signal may represent a mechanistic solution of how morphogens such as Dpp and activins work. Perhaps, signaling pathways do not function on their own in eliciting multiple different cellular responses, as envisaged by the purest version of the morphogen concept (Szuts, 1998).
In addition to the joint requirement of DFos and DJun during dorsal closure, DFos functions independently of DJun during
embryogenesis. Early dpp expression on the dorsal side of embryos induces expression of several genes, including race, which encodes a protein with homology to angiotensin-converting enzyme in the amnioserosa. The race cis-acting sequences required for dpp-mediated expression contain AP-1 binding sites. Consistent with DFos-mediated direct activation of race through these AP-1 sites, race expression in the amnioserosa is abolished in DFos mutants. In contrast, race expression is normal in DJun or basket mutant embryos. This early DJun-independent function of DFos may be mediated by a DFos homodimer. During wound healing in vertebrates (a process that exhibits parallels with dorsal closure), TGF-beta induces c-fos expression and AP-1 activity. The reciprocal regulatory relation between DFos and dpp in Drosophila appears to be conserved in mammalian cells. In mammalian myeloid cells, induction of c-jun and c-fos by serum or oncogenic v-src results in expression of TGF-beta1 by direction activation of TGF-beta1 transcription by AP1. TGF-beta induces AP-1 activity in keratinocytes during wound healing. These findings demonstrate common and distinct roles for DFos and DJun during embryogenesis and suggest a conserved link between AP-1 (activating protein-1) and TGF-beta (transforming growth factor-beta) signaling during epithelial cell shape changes (Riesgo-Escovar, 1997).
Fos-related antigen expression is induced by Dpp signaling and is unchanged in labial mutants. In dpp mutants, the band of elevated Fra expression in the second gut lobe is no longer visable. Conversely, when Dpp is expressed ubiquitously, strong Fra staining is observed throughout the endoderm. Fra is expressed in the absence of wingless and does not require schnurri (as does labial expression). Ectopic Wg does not induce Fra expression ectopically in the endoderm (Riese, 1997)
The identification of mutations in Tgfbeta-60A as dominant enhancers
of tkv 6 in the imaginal discs raises the
possibility that Tgfbeta-60A is required for optimal signaling by the dpp
pathway. To determine if there is a general requirement for
Tgfbeta-60A in dpp signaling, the effects of Tgfbeta-60A
mutations were examined on dpp signaling in the visceral mesoderm where
both dpp and Tgfbeta-60A are expressed.
dpp is expressed in two discrete domains in the visceral
mesoderm. The anterior domain of dpp coincides with the gastric caecae primordia, which are
immediately anterior to the expression domain of Sex combs
reduced (Scr) in parasegment (ps) 4. The failure to initiate dpp
expression in ps3 in dpp shv mutants results in anterior
expansion of Scr expression and arrested outgrowth of the
gastric caecae, indicating a role for dpp in repressing Scr in ps3. tkv 6
homozygotes are homozygous viable, so it is not surprising
that all the midgut gene expression patterns examined are
essentially normal. Scr expression in tkv 6 and Tgfbeta-60A
mutants is normal. However, in tkv 6 and Tgfbeta-60A
double mutants, the Scr expression extends anteriorly into ps3 as it does in dpp shv mutants, suggesting that Tgfbeta-60A activity
is required in ps3 for optimal dpp signaling (Chen, 1998).
The midgut consists of two germ layers: the visceral mesoderm and the endoderm. Cells of the portion of the middle midgut that are derived from the endoderm differentiate into four distinct cell types: copper, interstitial, large flat, and iron cells. These endodermal cell types are specified by Dpp and Wg, which are expressed in
the adhering visceral mesoderm of the parasegments (PS) 7 and 8, respectively. Copper cells exhibit a
unique morphology with banana shapes and exhibit UV light-induced fluorescence after copper
feeding. These characteristics are specified by a homeotic gene, labial (lab), which is activated by the Dpp signal in the midgut. Two different thresholds of Wg define copper and large flat cells. However, it has been unclear how Lab confers the transcriptional regulation to specify copper cells. In the middle midgut,
the defective proventriculus gene is expressed in all precursors of the four distinct cell types; subsequent to this broad expression, dve is repressed only in
copper cells. This repression is mediated by two Dpp target genes, lab and dve itself, and is also essential for the functional specification of copper cells. Thus, dve is involved in different
developmental aspects of the midgut under the control of different extracellular signals (Nakagoshi, 1998).
The expression domains and regulation of labial and dve in the middle midgut were compared. It was found that there are two endodermal expression domains: one is located immediately adjacent to the visceral mesoderm, and the other in a more interior inner endoderm layer. Dpp has been shown to be sufficient to induce dve expression in the midgut without Wg. These results indicate that dve expression in the middle midgut does not depend on Wg
but on Dpp. This is in contrast to dve expression during proventriculus development. lab is expressed under the control of Dpp as is dve, however, lab is regulated
negatively by the Wg signal to generate a sharp posterior border. The expression of lab is observed in the endoderm just beneath the dpp-expressing visceral mesoderm of PS 7, but not in the inner endodermal cells. In contrast, dve is expressed more broadly throughout
the inner endodermal layers, including presumptive interstitial cell precursors. Another
difference in lab and dve expression is that dve expression is subsequently repressed in lab-expressing cells that become copper cells. The possibility that Lab might be involved in
the repression of dve in copper cells was examined. In lab mutants, dve expression is not repressed in presumptive copper cells. This pattern of gene expression is
similar to that of neighboring interstitial cells, which express dve continuously without lab expression in the wild type. Evidence is presented that it is unlikely that the lab mutation causes the transformation of copper cells into interstitial cells. Taken together, the repression of dve requires the activities of both Lab and Dve itself (Nakagoshi, 1998).
defective proventriculus is composed of two homeodomains and is expressed in the
Drosophila endoderm. dve expression can first be detected at the rostral tip of the anterior midgut primordium. This expression persists until late stages of embryogenesis and becomes confined to the outer endodermal wall of the developing proventriculus. In stage 12 embryos, dve is expressed in the migrating posterior midgut primordium and soon thereafter in an endodermal domain at the junction of the midgut and hindgut. In stage 13 embryos, when the anterior and the posterior midgut primordia have fused, dve expression is most prominent in the anterior, central and posterior portion of the midgut. Weak expression is detectable in the region from where the gastric caecae will bud out. In stage 14 embryos, the central expression domain broadens and finally covers the second and third midgut lobes in stage 16. Additional expression domains of dve include the tip cells of the Malpighian tubules, mesectodermal cells, nerve cells of the central and peripheral nervous system and a group of cells that lie below the pharynx
(Fuß, 1998).
hedgehog, wingless and decapentaplegic define through their restricted expression a signaling center at the boundary of the forgut ectoderm and the midgut endoderm where proventriculus morphogenesis occurs. This boundary become established at the posterior margin of the keyhole structure, formed from cells that migrate out of a mesoderm free zone of the foregut epithelium. The keyhole tissue folds back on itself to generate a structure called the cardiac valve, which is subsequently pushed as an extension of the eosophagus into an endodermal sac-like midgut chamber which forms the outer wall of the proventriculus. wg is initially transcribed in an expression domain that includes the ectodermal region from which the keyhole will form and extends slightly beyond it into the proventriculus. The striped dve expression domain extends from the ectoderm/endoderm boundary toward the posterior and overlaps at its anterior margin with the wg expression domain. With the onset of keyhole formation, the wg expression domain becomes split into two domains: one lies at the anterior border of the keyhole in the ectodermal forgut cells and the other in endodermal cells posterior to the keyhole. Both expression domains of wg persist in the developing proventriculus until very late stages of embryogenesis. dve expression continues to overlap the domain of wg until the end of embryogenesis. dve is required for the maintenance of the posterior wg domain. wingless is required for dve activation in both the anterior and posterior dve expression domains (Fuß, 1998).
When the anterior and posterior midgut primordia fuse, dve is expressed in the central part of the endoderm region that underlies parasegments 7 and 8 of the visceral mesoderm in which dpp and wg are expressed. Once the second midgut constriction starts to build at the border of parasegments 7 and 8, dve expression expands towards both sides into the endoderm region underlying the parasegments 6-9. After the formation of the second constriction, dve expression persists in the second and third midgut lobes. In wg mutants, dve is still expressed in the central region of the embryo but the expression only weakly expands towards the posterior, as compared to wild type embryos. In dpp mutants there is a lack of dve expression in the anterior region of the dve domain parasegment 7 of the visceral mesoderm where dpp is expressed in wild type embryos. At later stages, dve expression is found only in the third midgut lobe instead of the second and third lobes, both of which display dve expression in wild type embryos. No expression of dve is found in schnurri mutants, which encode a transcription factor mediating the Dpp signal. Dpp can activate dve in the complete absence of wg expression and it is not the combination of both which is critical for dve expression. Ubiquitous expression of Wg in the visceral mesoderm leads to a repression of dve in the central region of the embryos. These results provide evidence that the Dpp signaling pathway eminating from the visceral mesoderm plays a pivital roe in activating central dve expression. The mutant analysis suggests that Wg is required to maintain dve in the posterior part of the central dve domain (Fuß, 1998).
Dorsoventral (DV) patterning in the trunk region of Drosophila embryo is established through intricate molecular interactions that regulate Dpp/Scw signaling during the early blastoderm stages. The hindgut of Drosophila, which derives from posterior region of the cellular blastoderm, also shows dorsoventral patterning, being subdivided into distinct dorsal and ventral domains. engrailed (en) is expressed in the dorsal domain, which determines dorsal fate of the hindgut. This study shows that a repressor Brk restricts en expression to the dorsal domain of the hindgut. Expression domain of brk during early blastodermal stages is defined through antagonistic interaction with dpp, and expression domains of dpp and brk in the early blastoderm include prospective hindgut domain. After stage 9, dpp expression in the dorsal domain of the hindgut primordium disappears, but, the brk expression in the ventral domain continues. It was found that Dorsocross (Doc), which is a target gene of Dpp, is responsible for restricting brk expression to the ventral domain of the hindgut. On the other hand, activation of en is under the control of brachyenteron (byn) that is regulated independently of dpp, brk, and Doc. The cooperative interaction of common DV positional cues with byn during hindgut development represents another aspect of mechanisms of DV patterning in the Drosophila embryo (Hamaguchi, 2012).
A model is presented of the genetic pathway leading to the DV subdivision of the Drosophila hindgut. The dorsal fate of the hindgut is finally determined by a selector gene en that is expressed in the dorsal domain of the hindgut. The present study revealed that DV patterning of the hindgut is based on antagonistic interaction of Dpp and Brk in the early cellular blastoderm. Dpp expression disappears in the hindgut primordium after stage 9, but, Dpp target gene Doc takes over the repressive effect on Brk, and restricts Brk expression to the ventral domain. In other words, primary role of Dpp in the hindgut development is to activate Doc genes in the dorsal domain for repression of Brk. Eventually, Brk represses the selector gene en in the ventral domain, restricting it to the dorsal domain. This is the outline of gene regulatory pathway of DV patterning of the hindgut. It should be noted that Doc represses brk in the dorsal domain, while Brk does not regulate Doc expression in the hindgut in normal development, since brk mutation does not affect Doc expression in the hindgut. Dpp and Doc do not determine the dorsal fate directly, but, act indirectly by repressing brk in the dorsal domain. In fact, brk; DocA (null) double-mutant embryos, as well as brk; dpp double mutant embryos, expressed en in both dorsal and ventral domains of the hindgut. This regulatory interrelation between brk and Dpp/Doc is partially reminiscent of that in the wing discs, in which primary role of Dpp is repression of brk, and the latter is responsible for defining antero-posterior pattern of gene expression in the wing discs. Repression of brk by Dpp signals has been reported to depend on the zinc finger protein Schnurri (Shn) in some tissues. However, brk expression in the hindgut did not expand dorsally in the shn mutant embryo, and also, en expression was observed in the hindgut in shn mutant embryo. Thus, shn may not be essential for regulation of brk in the hindgut (Hamaguchi, 2012).
However, activation of en in the hindgut, is under the control of byn, the process of which is independent of DV patterning. The expression domain of byn is included in the region where intricate interaction of dpp, brk, and Doc proceeds. The dpp, brk, and Doc genes are all under the control of the dorsal system, while byn is activated under the control of the terminal system that provides AP positional cues in terminal regions of the early blastoderm. In other words, AP positional cues activate en, while DV positional cues repress en. Thus, cooperative interaction of the two independent gene regulatory systems establishes the expression pattern of en in the hindgut (Hamaguchi, 2012).
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