A positive role for Short gastrulation in modulating BMP signaling during dorsoventral patterning in theDrosophilaembryo

Development ◽  
2001 ◽  
Vol 128 (19) ◽  
pp. 3831-3841 ◽  
Author(s):  
Eva Decotto ◽  
Edwin L. Ferguson
Keyword(s):  
Family Members ◽  
Positional Information ◽  
Dorsal Side ◽  
Bmp Signaling ◽  
Drosophila Embryo ◽  
Functional Difference ◽  
Ligand Specificity ◽  
Dorsoventral Patterning ◽  
Positive Role ◽  
Negative Function

Positional information in the dorsoventral axis of the Drosophila embryo is encoded by a BMP activity gradient formed by synergistic signaling between the BMP family members Decapentaplegic (DPP) and Screw (SCW). short gastrulation (sog), which is functionally homologous to Xenopus Chordin, is expressed in the ventrolateral regions of the embryo and has been shown to act as a local antagonist of BMP signaling. Here we demonstrate that SOG has a second function, which is to promote BMP signaling on the dorsal side of the embryo. We show that a weak, homozygous-viable sog mutant is enhanced to lethality by reduction in the activities of the Smad family members Mad or Medea, and that the lethality is caused by defects in the molecular specification and subsequent cellular differentiation of the dorsal-most cell type, the amnioserosa. While previous data had suggested that the negative function of SOG is directed against SCW, we present data that suggests that the positive activity of SOG is directed towards DPP. We demonstrate that Chordin shares the same apparent ligand specificity as does SOG, preferentially inhibiting SCW but not DPP activity. However, in Drosophila assays Chordin does not have the same capacity to elevate BMP signaling as does SOG, identifying a functional difference in the otherwise well conserved process of dorsoventral pattern formation in arthropods and chordates.

Altered mitotic domains reveal fate map changes in Drosophila embryos mutant for zygotic dorsoventral patterning genes

Development ◽  
1992 ◽  
Vol 114 (4) ◽  
pp. 1003-1024 ◽  
Author(s):  
K. Arora ◽  
C. Nusslein-Volhard
Keyword(s):  
Positional Information ◽  
Mitotic Division ◽  
Specific Pattern ◽  
Drosophila Embryo ◽  
Dorsoventral Patterning ◽  
Fate Map ◽  
Positive Role ◽  
Dorsal Cells ◽  
Dorsal Pattern ◽  
Drosophila Embryos

The spatial and temporal pattern of mitoses during the fourteenth nuclear cycle in a Drosophila embryo reflects differences in cell identities. We have analysed the domains of mitotic division in zygotic mutants that exhibit defects in larval cuticular pattern along the dorsoventral axis. This is a powerful means of fate mapping mutant embryos, as the altered position of mitotic domains in the dorsoventral pattern mutants correlate with their late cuticular phenotypes. In the mutants twist and snail, which fail to differentiate the ventrally derived mesoderm, mitoses specific to the mesoderm are absent. The lateral mesectodermal domain shows a partial ventral shift in twist mutants but a proportion of ventral cells do not behave characteristically, suggesting that twist has a positive role in the establishment of the mesoderm. In contrast, snail is required to repress mesectodermal fates in cells of the presumptive mesoderm. In the absence of both genes, the mesodermal and the mesectodermal anlage are deleted. Mutations at five loci delete specific pattern elements in the dorsal half of the embryo and cause partial ventralization. Mutations in the genes zerknullt and shrew affect cell division only in the dorsalmost cells corresponding to the amnioserosa, while the genes tolloid, screw and decapentaplegic (dpp) affect divisions in both the prospective amnioserosa and the dorsal epidermis. We demonstrate that in each of these mutants dorsally placed mitotic domains are absent and this effect is correlated with an expansion and dorsal shift in the position of more ventral domains. The loss of activity in each of the five genes results in qualitatively similar alterations in the mitotic pattern; mutations with stronger ventralizing phenotypes affect increasingly greater subsets of the dorsal cells. Double mutant analysis indicates that these genes act in a concerted manner to specify dorsal fates. The correlation between phenotypic strength and the progressive loss of dorsal pattern elements in the ventralized mutants, suggests that one of these gene products, perhaps dpp, may provide positional information in a graded manner.

A group of genes required for maintenance of the amnioserosa tissue in Drosophila

Development ◽  
1996 ◽  
Vol 122 (5) ◽  
pp. 1343-1352 ◽  
Author(s):  
L.H. Frank ◽  
C. Rushlow
Keyword(s):  
Cell Death ◽  
Cell Loss ◽  
Dorsal Side ◽  
Drosophila Embryo ◽  
Epithelial Tissue ◽  
Dorsoventral Patterning ◽  
Wild Type ◽  
Germ Band ◽  
Initial Development

The amnioserosa is an extraembryonic, epithelial tissue that covers the dorsal side of the Drosophila embryo. The initial development of the amnioserosa is controlled by the dorsoventral patterning genes. Here we show that a group of genes, which we refer to as the U-shaped-group (ush-group), is required for maintenance of the amnioserosa tissue once it has differentiated. Using several molecular markers, we examined amnioserosa development in the ush-group mutants: u-shaped (ush), hindsight (hnt), serpent (srp) and tail-up (tup). Our results show that the amnioserosa in these mutants is specified correctly and begins to differentiate as in wild type. However, following germ-band extension, there is a premature loss of the amnioserosa. We demonstrate that this cell loss is a consequence of programmed cell death (apoptosis) in ush, hnt and srp, but not in tup. We discuss the role of the ush-group genes in maintaining the amnioserosa's viability. We also discuss a possible role for the amnioserosa in germ-band retraction in light of these mutants' unretracted phenotype.

The homeobox genesvoxandventare redundant repressors of dorsal fates in zebrafish

Development ◽  
2001 ◽  
Vol 128 (12) ◽  
pp. 2407-2420 ◽  
Author(s):  
Yoshiyuki Imai ◽  
Michael A. Gates ◽  
Anna E. Melby ◽  
David Kimelman ◽  
Alexander F. Schier ◽  
...  
Keyword(s):  
Early Embryo ◽  
Dorsal Side ◽  
Bmp Signaling ◽  
Loss Of Function ◽  
Dorsoventral Patterning ◽  
Patterning Defect ◽  
Morpholino Oligonucleotides ◽  
Redundant Functions ◽  
Antisense Morpholino Oligonucleotides ◽  
Antisense Morpholino

Ventralizing transcriptional repressors in the Vox/Vent family have been proposed to be important regulators of dorsoventral patterning in the early embryo. While the zebrafish genes vox (vega1) and vent (vega2) both have ventralizing activity in overexpression assays, loss-of-function studies are needed to determine whether these genes have distinct or redundant functions in dorsoventral patterning and to provide critical tests of the proposed regulatory interactions among vox, vent and other genes that act to establish the dorsoventral axis. We show that vox and vent are redundant repressors of dorsal fates in zebrafish. Mutants that lack vox function have little or no dorsoventral patterning defect, and inactivation of either vox or vent by injection of antisense morpholino oligonucleotides has little or no effect on the embryo. In contrast, embryos that lack both vox and vent function have a dorsalized phenotype. Expression of dorsal mesodermal genes, including chordin, goosecoid and bozozok, is strongly expanded in embryos that lack vox and vent function, indicating that the redundant action of vox and vent is required to restrict dorsal genes to their appropriate territories. Our genetic analysis indicates that the dorsalizing transcription factor Bozozok promotes dorsal fates indirectly, by antagonizing the expression of vox and vent. In turn, vox and vent repress chordin expression, restricting its function as an antagonist of ventral fates to the dorsal side of the embryo. Our results support a model in which BMP signaling induces the expression of ventral genes, while vox and vent act redundantly to prevent the expression of chordin, goosecoid and other dorsal genes in the lateral and ventral mesendoderm.

Proteolytic cleavage of Chordin as a switch for the dual activities of Twisted gastrulation in BMP signaling

Development ◽  
2001 ◽  
Vol 128 (22) ◽  
pp. 4439-4447 ◽  
Author(s):  
Juan Larraín ◽  
Michael Oelgeschläger ◽  
Nan I. Ketpura ◽  
Bruno Reversade ◽  
Lise Zakin ◽  
...  
Keyword(s):  
Ternary Complex ◽  
Binding Assay ◽  
Bmp Signaling ◽  
Dominant Negative ◽  
Secreted Proteins ◽  
Dorsoventral Patterning ◽  
Twisted Gastrulation ◽  
Cognate Receptor ◽  
Licl Treatment ◽  
Bmp Antagonist

Dorsoventral patterning is regulated by a system of interacting secreted proteins involving BMP, Chordin, Xolloid and Twisted gastrulation (Tsg). We have analyzed the molecular mechanism by which Tsg regulates BMP signaling. Overexpression of Tsg mRNA in Xenopus embryos has ventralizing effects similar to Xolloid, a metalloprotease that cleaves Chordin. In embryos dorsalized by LiCl treatment, microinjection of Xolloid or Tsg mRNA restores the formation of trunk-tail structures, indicating an increase in BMP signaling. Microinjection of Tsg mRNA leads to the degradation of endogenous Chordin fragments generated by Xolloid. The ventralizing activities of Tsg require an endogenous Xolloid-like activity, as they can be blocked by a dominant-negative Xolloid mutant. A BMP-receptor binding assay revealed that Tsg has two distinct and sequential activities on BMP signaling. First, Tsg makes Chordin a better BMP antagonist by forming a ternary complex that prevents binding of BMP to its cognate receptor. Second, after cleavage of Chordin by Xolloid, Tsg competes the residual anti-BMP activity of Chordin fragments and facilitates their degradation. This molecular pathway, in which Xolloid switches the activity of Tsg from a BMP antagonist to a pro-BMP signal once all endogenous full-length Chordin is degraded, may help explain how sharp borders between embryonic territories are generated.

scholarly journals Successive specification of Drosophila neuroblasts NB 6-4 and NB 7-3 depends on interaction of the segment polarity genes wingless, gooseberry and naked cuticle

Development ◽  
2001 ◽  
Vol 128 (17) ◽  
pp. 3253-3261 ◽  
Author(s):  
Nirupama Deshpande ◽  
Rainer Dittrich ◽  
Gerhard M. Technau ◽  
Joachim Urban
Keyword(s):  
Cell Fate ◽  
Cell Lineage ◽  
Positional Information ◽  
Dorsoventral Patterning ◽  
Expression Domain ◽  
Direct Role ◽  
Segment Polarity Genes ◽  
Segment Polarity ◽  
Unique Identity

The Drosophila central nervous system derives from neural precursor cells, the neuroblasts (NBs), which are born from the neuroectoderm by the process of delamination. Each NB has a unique identity, which is revealed by the production of a characteristic cell lineage and a specific set of molecular markers it expresses. These NBs delaminate at different but reproducible time points during neurogenesis (S1-S5) and it has been shown for early delaminating NBs (S1/S2) that their identities depend on positional information conferred by segment polarity genes and dorsoventral patterning genes. We have studied mechanisms leading to the fate specification of a set of late delaminating neuroblasts, NB 6-4 and NB 7-3, both of which arise from the engrailed (en) expression domain, with NB 6-4 delaminating first. In contrast to former reports, we did not find any evidence for a direct role of hedgehog in the process of NB 7-3 specification. Instead, we present evidence to show that the interplay of the segmentation genes naked cuticle (nkd) and gooseberry (gsb), both of which are targets of wingless (wg) activity, leads to differential commitment to NB 6-4 and NB 7-3 cell fate. In the absence of either nkd or gsb, one NB fate is replaced by the other. However, the temporal sequence of delamination is maintained, suggesting that formation and specification of these two NBs are under independent control.

Genes that control dorsoventral polarity affect gene expression along the anteroposterior axis of the Drosophila embryo

Development ◽  
1987 ◽  
Vol 99 (3) ◽  
pp. 327-332 ◽  
Author(s):  
S.B. Carroll ◽  
G.M. Winslow ◽  
V.J. Twombly ◽  
M.P. Scott
Keyword(s):  
Gene Expression ◽  
Cell Fate ◽  
Maternal Effect ◽  
Positional Information ◽  
Drosophila Embryo ◽  
Dorsoventral Polarity ◽  
Anteroposterior Axis ◽  
Positional Marker ◽  
Control Pattern ◽  
The Relationship

At least 13 genes control the establishment of dorsoventral polarity in the Drosophila embryo and more than 30 genes control the anteroposterior pattern of body segments. Each group of genes is thought to control pattern formation along one body axis, independently of the other group. We have used the expression of the fushi tarazu (ftz) segmentation gene as a positional marker to investigate the relationship between the dorsoventral and anteroposterior axes. The ftz gene is normally expressed in seven transverse stripes. Changes in the striped pattern in embryos mutant for other genes (or progeny of females homozygous for maternal-effect mutations) can reveal alterations of cell fate resulting from such mutations. We show that in the absence of any of ten maternal-effect dorsoventral polarity gene functions, the characteristic stripes of ftz protein are altered. Normally there is a difference between ftz stripe spacing on the dorsal and ventral sides of the embryo; in dorsalized mutant embryos the ftz stripes appear to be altered so that dorsal-type spacing occurs on all sides of the embryo. These results indicate that cells respond to dorsoventral positional information in establishing early patterns of gene expression along the anteroposterior axis and that there may be more significant interactions between the different axes of positional information than previously determined.

scholarly journals Regulation of the BMP Signaling-Responsive Transcriptional Network in the Drosophila Embryo

PLoS Genetics ◽  
2016 ◽  
Vol 12 (7) ◽  
pp. e1006164 ◽  
Author(s):  
Lisa Deignan ◽  
Marco T. Pinheiro ◽  
Catherine Sutcliffe ◽  
Abbie Saunders ◽  
Scott G. Wilcockson ◽  
...  
Keyword(s):  
Transcriptional Network ◽  
Bmp Signaling ◽  
Drosophila Embryo

scholarly journals A translational block to HSPG synthesis permits BMP signaling in the early Drosophila embryo

Development ◽  
2008 ◽  
Vol 135 (6) ◽  
pp. 1039-1047 ◽  
Author(s):  
D. J. Bornemann ◽  
S. Park ◽  
S. Phin ◽  
R. Warrior
Keyword(s):  
Bmp Signaling ◽  
Drosophila Embryo ◽  
Early Drosophila Embryo ◽  
Translational Block
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