Dataset Information

Robust, bistable patterning of the dorsal surface of the Drosophila embryo.

ABSTRACT: In many developing systems, the fate of a cell is determined by its position in a time-independent spatial distribution of a morphogen. However, during dorsal-ventral patterning in the Drosophila embryo, an initial low-level signal refines to a narrow, high-intensity band. This refinement suggests that cells respond to the local transient morphogen distribution that results from interactions between bone morphogenetic proteins (BMPs), their receptors, the BMP-binding proteins Sog and Tsg, the metalloprotease Tld, and a putative, positively regulated component that locally enhances surface binding of BMPs within the region of high signaling. We develop a computational model for dorsal surface patterning and show that, when positive feedback of a cell surface BMP-binding protein is incorporated, bistability in the kinetic interactions transduces the transient BMP distribution into a switch-like spatial distribution of the BMP-bound receptor. We also show that the inclusion of positive feedback leads to the observed contraction of signaling, because cells near the dorsal midline outcompete adjacent lateral cells for limited amounts of BMP. In the model, cells interpret the morphogen distribution by differentiating according to the history of their exposure rather than to a threshold concentration in a static spatial gradient of the morphogen.

SUBMITTER: Umulis DM

PROVIDER: S-EPMC1544218 | biostudies-other | 2006 Aug

REPOSITORIES: biostudies-other

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Robust, bistable patterning of the dorsal surface of the Drosophila embryo.

Umulis David M DM Serpe Mihaela M Serpe Mihaela M O'Connor Michael B MB Othmer Hans G HG

Proceedings of the National Academy of Sciences of the United States of America 20060724 31

In many developing systems, the fate of a cell is determined by its position in a time-independent spatial distribution of a morphogen. However, during dorsal-ventral patterning in the Drosophila embryo, an initial low-level signal refines to a narrow, high-intensity band. This refinement suggests that cells respond to the local transient morphogen distribution that results from interactions between bone morphogenetic proteins (BMPs), their receptors, the BMP-binding proteins Sog and Tsg, the me ...[more]

PMID: 16864795

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Project description:In early development, genes are expressed in spatial patterns which later define cellular identities and tissue locations. The mechanisms of such pattern formation have been studied extensively in early Drosophila (fruit fly) embryos. The gap gene hunchback (hb) is one of the earliest genes to be expressed in anterior-posterior (AP) body segmentation. As a transcriptional regulator for a number of downstream genes, the spatial precision of hb expression can have significant effects in the development of the body plan. To investigate the factors contributing to hb precision, we used fine spatial and temporal resolution data to develop a quantitative model for the regulation of hb expression in the mid-embryo. In particular, modelling hb pattern refinement in mid nuclear cleavage cycle 14 (NC14) reveals some of the regulatory contributions of simultaneously-expressed gap genes. Matching the model to recent data from wild-type (WT) embryos and mutants of the gap gene Krüppel (Kr) indicates that a mid-embryo Hb concentration peak important in thoracic development (at parasegment 4, PS4) is regulated in a dual manner by Kr, with low Kr concentration activating hb and high Kr concentration repressing hb. The processes of gene expression (transcription, translation, transport) are intrinsically random. We used stochastic simulations to characterize the noise generated in hb expression. We find that Kr regulation can limit the positional variability of the Hb mid-embryo border. This has been recently corroborated in experimental comparisons of WT and Kr- mutant embryos. Further, Kr regulation can decrease uncertainty in mid-embryo hb expression (i.e. contribute to a smooth Hb boundary) and decrease between-copy transcriptional variability within nuclei. Since many tissue boundaries are first established by interactions between neighbouring gene expression domains, these properties of Hb-Kr dynamics to diminish the effects of intrinsic expression noise may represent a general mechanism contributing to robustness in early development.

Dataset Information

Robust, bistable patterning of the dorsal surface of the Drosophila embryo.

Publications

Robust, bistable patterning of the dorsal surface of the Drosophila embryo.

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