Signal transduction pathway for anterior-posterior development inDrosophila

InDrosophila, the establishment of embryonic polarity along the anterior-posterior axis of the egg is determined by the activity of maternal gene products that accumulate during oogenesis. Amongst these are the Bicoid, the Nanos, and the terminal class gene products, some of which are oncoproteins involved in signal transduction for the formation of terminal structures in the embryo. Several signal transduction pathways have been described inDrosophila, and this review explores the potential of oncogene studies using one of those pathways — the terminal class signal transduction pathway — to better understand the cellular mechanisms of proto-oncogenes that mediate cellular responses in vertebrates including humans.     

The Drosophila gap gene network is composed of two parallel toggle switches

Drosophila "gap" genes provide the first response to maternal gradients in the early fly embryo. Gap genes are expressed in a series of broad bands across the embryo during first hours of development. The gene network controlling the gap gene expression patterns includes inputs from maternal gradients and mutual repression between the gap genes themselves. In this study we propose a modular design for the gap gene network, involving two relatively independent network domains. The core of each network domain includes a toggle switch corresponding to a pair of mutually repressive gap genes, operated in space by maternal inputs. The toggle switches present in the gap network are evocative of the phage lambda switch, but they are operated positionally (in space) by the maternal gradients, so the synthesis rates for the competing components change along the embryo anterior-posterior axis. Dynamic model, constructed based on the proposed principle, with elements of fractional site occupancy, required 5-7 parameters to fit quantitative spatial expression data for gap gradients. The identified model solutions (parameter combinations) reproduced major dynamic features of the gap gradient system and explained gap expression in a variety of segmentation mutants.     

Avian mothers create different phenotypes by hormone deposition in their eggs

An increasing number of studies in a variety of taxa demonstrate the role of maternal sex steroids on offspring development. In avian species, mothers deposit substantial amounts of androgens in their eggs, and experimental evidence indicates that these maternal androgens influence the chick's early development. Despite the well-known organizing role of sex steroids on brain and behaviour, studies on avian maternal egg hormones almost exclusively focus on the chick phase. Here, we show experimentally that in Black-headed gulls maternal androgens in the egg enhance the development of the nuptial plumage and the frequency of aggressive and sexual displays almost 1 year after hatching. We conclude that maternal sex steroids may be a key factor for the determination of subtle but important individual differences within the same sex and species, which may have important consequences for Darwinian fitness and evolutionary processes.     

Maternal information and localized maternal mRNAs in eggs and early embryos of the ascidian Halocynthia roretzi

Summary

The mosaic behavior of blastomeres isolated from ascidian embryos has been taken as evidence that localized ooplasmic factors (cytoplasmic determinants) specify tissue precursor cells during embryogenesis. Experiments involving the transfer of egg cytoplasm have revealed the presence and localization of various kinds of cytoplasmic determinants in eggs of Halocynthia roretzi. Three cell fates, epidermis, muscle and endoderm, are fixed by cytoplasmic determinants. The three kinds of tissue determinants move in different directions during ooplasmic segregation. Prior to the onset of the first cleavage the three kinds of determinants reside in egg regions that correspond to the future fate map of the embryo and then they are differentially partitioned into specific blastomeres. In addition to tissue-specific determinants, there is evidence suggesting that ascidian eggs contain localized cytoplasmic factors that are responsible for controlling the cleavage pattern and morphogenetic movements. Transplantation of posterior-vegetal egg cytoplasm to an anterior-vegetal position causes a reversal of the anterior-posterior polarity of the cleavage pattern. Localized cytoplasmic factors in the posterior-vegetal region are involved in the generation of a unique cleavage pattern. When vegetal pole cytoplasm is transplanted to the animal pole or equatorial position of the egg, ectopic gastrulation occurs at the site of transplantation. This finding supports the idea that vegetal pole cytoplasm specifies the site of gastrulation. Recently, we started a cDNA project to analyze maternal mRNAs. An arrayed cDNA library of fertilized eggs of H. roretzi was constructed, and more than 2000 clones have been partially sequenced so far. To estimate the proportion of the maternal mRNAs that are localized in the egg and embryo, 150 randomly selected clones were examined by in situ hybridization. We found eight mRNAs that are localized in the eight-cell embryo, of which three were localized to the myoplasm (a specific region of the egg cytoplasm that is partitioned into muscle-lineage blastomeres) of the egg, and then to the postplasm of cleavage-stage embryos. These results indicate that the proportion of localized messages is much higher than we expected. These localized maternal messages may be involved in the regulation of various developmental processes.     

The anterior-posterior axis emerges respecting the morphology of the mouse embryo that changes and aligns with the uterus before gastrulation

BACKGROUND: When the anterior-posterior axis of the mouse embryo becomes explicit at gastrulation, it is almost perpendicular to the long uterine axis. This led to the belief that the uterus could play a key role in positioning this future body axis. RESULTS: Here, we demonstrate that when the anterior-posterior axis first emerges it does not respect the axes of the uterus but, rather, the morphology of the embryo. Unexpectedly, the emerging anterior-posterior axis is initially aligned not with the long, but the short axis of the embryo. Then whether the embryo develops in vitro or in utero, the anterior-posterior axis becomes aligned with the long axis of embryo just prior to gastrulation. Of three mechanisms that could account for this apparent shift in anterior-posterior axis orientation-cell migration, spatial change of gene expression, or change in embryo shape-lineage tracing studies favor a shape change accompanied by restriction of the expression domain of anterior markers. This property of the embryo must be modulated by interactions with the uterus as ultimately the anterior-posterior and long axes of the embryo align with the left-right uterine axis. CONCLUSIONS: The emerging anterior-posterior axis relates to embryo morphology rather than that of the uterus. The apparent shift in its orientation to align with the long embryonic axis and with the uterus is associated with a change in embryo shape and a refinement of anterior gene expression pattern. This suggests an interdependence between anterior-posterior gene expression, the shape of the embryo, and the uterus.     

Cytoplasmic domains in eggs

One way of organizing the body plan of a developing embryo is to establish domains in the egg with distinct compositions in defined spatial relationships to one another: when the egg divides up, these domains segregate preferentially to certain regions of the embryo and influence their development. In this review we discuss the nature, formation and reorganization of distinguishable domains in various eggs.     

Role of Scrib and Dlg in anterior-posterior patterning of the follicular epithelium during Drosophila oogenesis

Background  

Proper patterning of the follicle cell epithelium over the egg chamber is essential for the Drosophila egg development. Differentiation of the epithelium into several distinct cell types along the anterior-posterior axis requires coordinated activities of multiple signaling pathways. Previously, we reported that lethal(2)giant larvae (lgl), a Drosophila tumor suppressor gene, is required in the follicle cells for the posterior follicle cell (PFC) fate induction at mid-oogenesis. Here we explore the role of another two tumor suppressor genes, scribble (scrib) and discs large (dlg), in the epithelial patterning.     

Conservation of Hox/ParaHox-related genes in the early development of a cnidarian.

To clarify the relationship between axial patterning in cnidarians and bilaterians, we have investigated the embryonic development of the hydrozoan Podocoryne carnea. The expression of Hox-like homeobox genes was analyzed by RT-PCR and in situ hybridization. Cnox1-Pc, an anterior Hox gene, is a maternal message. It is present throughout larval development, first weakly in all blastomeres and later restricted mostly to the anterior pole of the planula. Gsx, an anterior ParaHox gene, is first seen in the anterior endoderm but also extends into posterior regions. Cnox4-Pc, an orphan Hox-like gene, is expressed in the egg as a ring-shaped cloud around the germinal vesicle. After fertilization, the message remains in most animal blastomeres. When the embryo elongates in late blastula, staining is restricted to a few cells at the posterior pole where gastrulation will start. However, once gastrulation starts, the Cnox4-Pc signal disappears and is absent in later stages of larval development. Phylogenetic analysis shows that not all cnidarian Hox-like genes have recognizable orthologues in bilaterian groups. However, the expression analysis of Cnox1-Pc and Gsx correlates to some extent with the expression pattern of cognate genes of bilaterians, confirming the conservation of genes involved in organizing animal body plans and their putative common ancestral origin.     

A gradient of JAK pathway activity patterns the anterior-posterior axis of the follicular epithelium

The Drosophila egg develops through closely coordinated activities of associated germline and somatic cells. An essential aspect of egg development is the differentiation of the somatic follicle cells into several distinct subpopulations with specific functions. Here we demonstrate that the graded activity of the Janus kinase (JAK) pathway, stimulated by the Unpaired ligand, patterns the anterior-posterior axis of the follicular epithelium. Different levels of JAK activity instruct adoption of distinct anterior cell fates. Further, the coordinated activities of the JAK/STAT and epidermal growth factor receptor (EGFR) pathways are required to specify the posterior terminal cell fate. We propose that Upd secreted from the polar cells may act as a morphogen to stimulate A/P-derived follicular fates through JAK pathway activation.     

Patterning of an ascidian embryo along the anterior-posterior axis through spatial regulation of competence and induction ability by maternally localized PEM

In ascidian embryos, anterior-posterior (A-P) patterning of the vegetal cells is regulated by posteriorizing activities of a localized egg region known as posterior-vegetal cortex/cytoplasm (PVC). PEM is an essential component of the PVC and is involved in the posterior-specific cell cleavage pattern. Here we report a novel function of PEM independently of its function in cleavage regulation; it controls cell fate by excluding competence to respond to the FGF signal for notochord induction from posterior-vegetal cells. PEM was found to regulate the nuclear accumulation of β-catenin, an upstream activator of the competence factor. PEM also influences A-P patterning in the animal hemisphere. It was found to regulate FGF signal expression and restrict the occurrence of brain induction only in the anterior region. Our results suggest a model in which PEM patterns the embryo along the A-P axis through regulation of the spatial distribution of competence and induction ability.     

Fitness consequences of variable maternal provisioning in quacking frogs (Crinia georgiana)

Variable maternal provisioning may evolve when there is variation in the quality of offspring environments. The frog Crinia georgiana has high variability in egg size both within and between clutches, independent of female phenotype. It breeds in ponds with high spatial and temporal variation in habitat quality. Egg size strongly affected offspring fitness in good and poor quality offspring environments, whether the egg size difference was from between or within clutches. Since there is a trade-off in egg size and number, these fitness consequences translate to strong effects on maternal fitness. In the variable and unpredictable offspring environment of C. georgiana, the maintenance of variable maternal provisioning both within and between clutches is likely to be an evolved response to the offspring environment.     

Modeling segmental patterning in Drosophila: Maternal and gap genes

We propose a new mathematical model describing the establishment of maternal and gap proteins segmental patterning along the antero-posterior axis of the Drosophila early embryo. This model is based on experimental data and, without recurring to pre-defined activation thresholds, predicts qualitatively and quantitatively the expression patterns of the maternal and gap proteins, as well as the expression patterns of proteins resulting from mRNA ectopic expression and from some loss-of-function mutations. We conclude that the gap genes segmental patterning and consequent spatial organization of the embryo is determined by three main factors: (1) the initial positioning of the maternal bicoid and torso mRNA inside the egg, and subsequent diffusion of the corresponding proteins; (2) the structure of the genetic regulatory network; (3) the role of conservation laws in the establishment of steady and non-uniform spatial distributions of non-diffusing proteins.     

A common translational control mechanism functions in axial patterning and neuroendocrine signaling in Drosophila

Translational repression of maternal nanos (nos) mRNA by a cis-acting Translational Control Element (TCE) in the nos 3'UTR is critical for anterior-posterior patterning of the Drosophila embryo. We show, through ectopic expression experiments, that the nos TCE is capable of repressing gene expression at later stages of development in neuronal cells that regulate the molting cycle. Our results predict additional targets of TCE-mediated repression within the nervous system. They also suggest that mechanisms that regulate maternal mRNAs, like TCE-mediated repression, may function more widely during development to spatially or temporally control gene expression.