brachyenteron


DEVELOPMENTAL BIOLOGY

Embryonic

During cell cycle 14, transcription of Trg commences throughout the posterior terminal region of the embryo. During cellularization, expression is down-regulated in the posterior tip, resulting in expression in a ring of cells that encompass the primordium of the hindgut and anal pads. Expression continues after invagination of the posterior midgut (Kispert, 1994 and Murakami, 1995).

Effects of Mutation or Deletion

After germ-band retraction in Trg deficient embryos, the major part of the hindgut is missing (Kispert, 1994 and Murakami, 1995).

Loss of Zn finger homeodomain 1 activity disrupts the development of two distinct mesodermal populations: the caudal visceral mesoderm (along which germ cells migrate) and the gonadal mesoderm (the final destination of the germ cells). The caudal visceral mesoderm facilitates the migration of germ cells from the endoderm to the mesoderm. Zfh-1 is also expressed in the gonadal mesoderm throughout the development of this tissue. Ectopic expression of Zfh-1 is sufficient to induce additional gonadal mesodermal cells and to alter the temporal course of gene expression within these cells. Germ cell migration was also analyzed in brachyenteron mutant embryos. Like zfh-1, byn is required for the migration of the caudal visceral mesoderm, but unlike zfh-1, it is not required for gonadal mesoderm development. Since byn and zfh-1 both disrupt caudal visceral mesoderm migration and show similar defects in germ cell migration, it is proposed that in wild-type embryos, the caudal visceral mesoderm facilitates the transition of many germ cells from the endoderm to the lateral mesoderm. abdominal-A is also required for gonadal mesoderm specification. Zfh-1 expression was analyzed in abdA mutants. Zfh-1 is expressed normally in mesodermal clusters at stage 10, however, its levels are not enhanced in PS10-12 during stage ll. The loss of high Zfh-1 expression correlates with the failure of SGP specification in abdA mutants. Although abdA is required for SGP specification, the initial stages of germ cell migration are unaffected in abdA mutant embryos (Broihier, 1998).

There are a number of mesodermal tissues that do not properly develop in embryos lacking the CVM, as in byn, fkh or tll embryos. For instance, the TVM develops aberrantly in byn mutants during late stages of embryogenesis. Although the inner layer of circular muscles differentiates in the absence of the CVM as in wild type, the morphogenesis of this layer does not proceed properly. The nuclei of the TVM are normally arranged as one broad band on each side of the midgut during germband retraction and subsequently split into two bands when the midgut primordia meet at stage 13. During this movement, the nuclei pass the rows of CVM cells, which are located at the dorsal and the ventral edge of the midgut primordium, respectively. In a byn mutant, however, the movement of the TVM nuclei is irregular, so that their organization into bands is lost and they become distributed over the entire gut circumference. Since byn is never expressed in the TVM, it is concluded that the proper arrangement and integrity of the circular muscle fibers requires the presence of the CVM. The irregular dorsoventral extension of the fibers results in an incomplete closure of the layer and the circular muscle layer of the midgut in byn embryos shows sporadic ruptures. These defects might be the reason why the three constrictions that normally subdivide the midgut tube into four gastric chambers are not formed in byn mutants. It seems rather unlikely that the longitudinal muscle fibers physically participate in the formation of the constrictions, since the fibers are oriented perpendicularly to the constriction planes (Kusch, 1999).

Strikingly, other mesodermal tissues that are affected in mutants lacking the CVM are not in obvious contact with the CVM during development. For instance, in byn mutants, the two rows of cardiac cells do not unite to form the heart vessel. In addition, pericardial cells are missing and the most dorsal internal muscle (dorsal acute 1: DA1) is absent or might be fused with DA2 in many segments. The progenitors of DA1 and of a subset of pericardial cells develop from a common cluster of dorsal mesodermal cells that can be followed from stage 10 on by their even-skipped (eve) expression. Three cells per hemisegment begin to express eve in each of 11 dorsal clusters in the mesoderm. By stage 12, the number of mesodermal eve cells increases by one in each cluster. This additional eve cell appears in succession from posterior to anterior clusters. Furthermore, it has been noted that the cells of the CVM pass the mesodermal eve clusters at a distance of about one cell diameter as they migrate anteriorly along the TVM. Shortly after the time when the leading edge of the CVM had passed, the fourth eve cell is added to the cluster. This addition occurs toward the CVM and by recruitment from neighboring cells rather than by cell division. Most importantly, the temporal and spatial correlation between the appearance of the fourth eve cell and the migration of the CVM is not a mere coincidence. In byn, tll or zfh-1 mutants in which the CVM fails to migrate anteriorly or is absent, the number of eve cells does not increase during germband retraction. It is proposed that this is the primary defect in the dorsal mesoderm that causes the defects in heart and dorsal muscle development of byn or tll mutants, and that normally an inductive signal emerging from the migrating CVM triggers the addition of the fourth eve cells. This view is supported by the observation that the specific rescue of CVM development in byn mutant embryos restores the dorsal mesodermal structures to a considerable extent. byn is neither expressed in the mesodermal eve cells nor in other dorsal mesodermal derivatives of the experimental embryos, but nevertheless the number and position of pericardial cells is essentially normal, the two rows of cardiac cells join and DA1 muscles are detectable in many segments (Kusch, 1999).

It was of interest to know whether byn is required solely for the early specification and migration of the CVM, or whether it is more directly involved in the signalling to the dorsal mesoderm. byn was therefore expressed outside the CVM, throughout the mesoderm, and the number of mesodermal eve cells was monitored. In such experimental embryos, a drastic increase of eve cells is seen at the dorsal edge of the mesoderm in the proximity to the original eve clusters during stage 11. Initially, these additional cells only appear close to the CVM, i.e. in the posterior half of the experimental embryos. Later, they also fill the gaps between the anterior eve clusters, to which the CVM fails to migrate upon ubiquitous mesodermal byn expression, and then form a band of cells along the entire dorsal mesoderm. Only the dorsal mesoderm appears to be competent to (directly or indirectly) respond to byn. This notion is supported by the finding that, in htl embryos that specifically lack derivatives of the dorsal mesoderm, ubiquitous mesodermal expression of byn does not lead to ectopic eve expression. Thus byn is not directly involved in transcriptionally activating eve in the dorsal mesoderm, since byn is normally never expressed in the eve clusters. Instead, it is proposed that byn regulates the expression of the ligand in the signalling process. byn can only exert this function on mesodermal cells, since a strictly ectodermal misexpression of byn has no effect on mesodermal eve expression. In fact, only cells in the neighborhood of the eve cells begin to express eve upon ubiquitous mesodermal byn expression, indicating that the competence to perceive the byn-mediated signal is dictated by contact with other eve cells (Kusch, 1999).


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Brachyenteron/T-related gene: Biological Overview | Evolutionary Homologs | Regulation | Developmental Biology | Effects of Mutation

date revised: 12 December 2016

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