Accumulation of the Drosophila Torso-like protein at the blastoderm plasma membrane suggests that it translocates from the eggshell

Abstract

The eggshell serves as a depository for proteins that play an important role in early embryonic development. In particular, the Drosophila eggshell is responsible for transferring asymmetries from the egg chamber to specify the regions at both ends of the embryo through the uneven activation of the Torso (Tor) receptor in its membrane. This process relies on the restricted expression of the gene torso-like (tsl) in subpopulations of follicle cells during oogenesis and its protein accumulation at both poles of the eggshell, but it is not known how this signal is transmitted to the embryo. Here, we show that Tsl accumulates at the embryonic plasma membrane, even in the absence of the Tor receptor. However, during oogenesis, we detected Tsl accumulation only at the eggshell. These results suggest that there is a two-step mechanism to transfer the asymmetric positional cues from the egg chamber into the early embryo: initial anchoring of Tsl at the eggshell as it is secreted, followed by its later translocation to the egg plasma membrane, where it enables Tor receptor activation. Translocation of anchored determinants from the eggshell might then regulate the spatial and temporal control of early embryonic developmental processes.

Repurposing a pore: highly conserved perforin-like proteins with alternative mechanisms

“…Tsl is translocated from the eggshell to the egg plasma membrane, where it enables the regional activation of the Torso tyrosine kinase receptor (Tor) [44]. Ectopic expression of Tsl activates the Tor receptor, leading to developmental abnormality.…”

Evolution of the Torso activation cassette, a pathway required for terminal patterning and moulting

“…Torso-like is expressed in specialized follicle cells adjacent to the termini of the mature oocyte (Savant-Bhonsale and Montell, 1993). Torso-like protein is placed in the vitelline membrane (Mineo et al, 2015), and may be involved in processing (Casali and Casanova, First published online 24 January 2019.…”

Reconstitution of Torso signaling in cultured cells suggests a role for both Trunk and Torso-like in receptor activation

“…Tsl has been detected in the plasma membrane at the two ends of the early embryo (Martin et al, 1994;Mineo et al, 2015) and Tsl bears a MACPF motif (Ponting, 1999), which is found in proteins known to become inserted into lipid bilayers (Lukoyanova et al, 2016). One possibility is that Tsl may modulate the local membrane environment in which Torso resides, perhaps by organizing lipid microdomains and thereby driving the formation of complexes competent to signal.…”

“…Tsl becomes localized to the anterior and posterior regions of the vitelline membrane (VM) (Stevens et al, 2003): the inner layer of the eggshell that surrounds the developing embryo. In addition, Tsl has been detected in the membrane of the embryo at the anterior and posterior poles (Martin et al, 1994;Mineo et al, 2015). When tsl is ectopically expressed throughout the follicle cell layer, the resulting embryos exhibit phenotypes similar to those produced by the constitutively active torso gain-of-function alleles (Klingler et al, 1988;Savant-Bhonsale and Montell, 1993;Martin et al, 1994), suggesting that in wild-type embryos, Tsl determines where Torso is activated.…”