Abstract
During Drosophila embryogenesis the process of dorsal closure (DC) results in continuity of the embryonic epidermis, and DC is well recognized as a model system for the analysis of epithelial morphogenesis as well as wound healing. During DC the flanking lateral epidermal sheets stretch, align, and fuse along the dorsal midline, thereby sealing a hole in the epidermis occupied by an extra-embryonic tissue known as the amnioserosa (AS). Successful DC requires the regulation of cell shape change via actomyosin contractility in both the epidermis and the AS, and this involves bidirectional communication between these two tissues. We previously demonstrated that transcriptional regulation of myosin from the zipper (zip) locus in both the epidermis and the AS involves the expression of Ack family tyrosine kinases in the AS in conjunction with Dpp secreted from the epidermis. A major function of Ack in other species, however, involves the negative regulation of Egfr. We have, therefore, asked what role Egfr might play in the regulation of DC. Our studies demonstrate that Egfr is required to negatively regulate epidermal expression of dpp during DC. Interestingly, we also find that Egfr signaling in the AS is required to repress zip expression in both the AS and the epidermis, and this may be generally restrictive to the progression of morphogenesis in these tissues. Consistent with this theme of restricting morphogenesis, it has previously been shown that programmed cell death of the AS is essential for proper DC, and we show that Egfr signaling also functions to inhibit or delay AS programmed cell death. Finally, we present evidence that Ack regulates zip expression by promoting the endocytosis of Egfr in the AS. We propose that the general role of Egfr signaling during DC is that of a braking mechanism on the overall progression of DC.
Highlights
Dorsal closure (DC) is a developmental event occurring in the Drosophila embryo between stages 11 and 16, commencing immediately after germband retraction
The various roles identified for Egfr signaling during DC are consistent with negative regulation of morphogenesis, and we propose that Egfr acts as a brake to adjust the rate of closure in response to endocytic regulation
Egfr Negatively Regulates zip Expression in the Epidermis and AS During DC An important target of Dpp regulation during DC is zip, and we evaluated zip expression in Egfr mutant embryos and embryos with tissue-specific attenuation of Egfr signaling. zip shows two major events of transcriptional upregulation that are relevant to the morphogenetic events during DC: first, a burst of expression occurs in the AS during germband retraction and terminates around the beginning of DC; and, second, upregulation occurs in the dorsal-most epidermal (DME) cells beginning during the germband retraction stage and persists throughout DC [12,24,26](Fig. 4A)
Summary
Dorsal closure (DC) is a developmental event occurring in the Drosophila embryo between stages 11 and 16, commencing immediately after germband retraction (reviewed in [1]). Upon the completion of germband retraction, a large dorsal opening is evident in the epidermis. The amnioserosa (AS), an extraembryonic tissue composed of a single layer of large flat epithelial cells, spans the opening. The dorsal-most epidermal (DME) cells from one side of the embryo meet their counterpart DME cells at the dorsal midline. The epidermal sealing process occurs in a zipperlike manner, progressing simultaneously from both the anterior and posterior ends of the dorsal opening and finishing at the center of the dorsal midline. Upon the completion of DC, the entire AS degenerates by programmed cell death [2]
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