The torpedo (DER) receptor tyrosine kinase is required at multiple times during Drosophila embryogenesis

Abstract

The torpedo (DER) gene of Drosophila, which encodes a receptor tyrosine kinase of the EGF receptor subfamily, is essential for oogenesis, embryogenesis and imaginal disc development. To gain insight into the nature of the signals transduced by the torpedo product, we have characterized the gene's loss-of-function phenotype in the embryo. Through the induction of germline clones, we provide a genetic demonstration that maternal torpedo product does not contribute to zygotic development. Thus, the embryonic lethal phenotypes examined accurately reflect the consequences of eliminating all gene activity from the zygote. Temperature-shift experiments with the conditional allele topIF26 show that torpedo is required at two distinct times during embryonic development: the gene is first needed for germband retraction and for the production of anterior, posterior and ventral cuticle, then later for the secretion of ventral denticles. Since denticle formation can be severely disrupted in topIF26 animals without affecting cuticle production, the early and late requirements for torpedo appear to be functionally unrelated. torpedo, therefore, is required at multiple times in the development of the ventral epidermis, and may transduce qualitatively different signals. Since the early requirement for torpedo correlates with the first visible defect in embryonic development, increased cell death in the amnioserosa, cephalic ectoderm and ventral epidermis, the abnormalities in cuticle production and germband shortening seen in the mutant may be secondary consequences of a primary defect in cell viability. Given that the onset of cell death in torpedo embryos is not preceded by any obvious defects in mitogenesis, the establishment of cell identities or the maintenance of gene expression, it is possible that torpedo transduces a signal necessary for cell survival per se during early embryogenesis. During late embryogenesis, torpedo may mediate the reception of a second signal which regulates ventral epidermal cell differentiation.

Epidermal growth factor receptor signaling protects epithelia from morphogenetic instability and tissue damage in Drosophila

“…Massive cell death was observed in EGFR mutants ( Price et al, 1989 ; Schejter and Shilo, 1989 ). Although EGFR is ubiquitously expressed ( Revaitis et al, 2020 ), the onset of extensive cell death in EGFR mutants is limited to the epidermis of the head and ventral thorax, suggesting that additional factors contribute to the specificity of the prosurvival function of EGFR ( Clifford and Schüpbach, 1992 ). In addition, EGFR supports the survival of potentially apoptotic cells in mutants of segmentation genes ( Crossman et al, 2018 ) and promotes the repair of the epithelial opening after apoptotic cell extrusion ( Valon et al, 2021 ).…”

Epidermal growth factor receptor signaling protects epithelia from morphogenetic instability and tissue damage in Drosophila

“…Massive cell death was observed in EGFR mutants (Price et al, 1989; Schejter and Shilo, 1989). Although EGFR is ubiquitously expressed (Revaitis et al, 2020), the onset of extensive cell death in EGFR mutants is limited to the epidermis of the head and ventral thorax, suggesting that additional factors contribute to the specificity of the prosurvival function of EGFR (Clifford and Schupbach, 1992). In addition, EGFR supports the survival of potentially apoptotic cells in mutants of segmentation genes (Crossman et al, 2018) and promotes the closure of the epithelial opening after apoptotic cell extrusion (Moreno et al, 2019; Valon et al, 2021).…”