Striped Expression of Leucine-Rich Repeat Proteins Coordinates Cell Intercalation and Compartment Boundary Formation in the Early Drosophila Embryo

Abstract

Planar polarity is a commonly observed phenomenon in which proteins display a consistent asymmetry in their subcellular localization or activity across the plane of a tissue. During animal development, planar polarity is a fundamental mechanism for coordinating the behaviors of groups of cells to achieve anisotropic tissue remodeling, growth, and organization. Therefore, a primary focus of developmental biology research has been to understand the molecular mechanisms underlying planar polarity in a variety of systems to identify conserved principles of tissue organization. In the early Drosophila embryo, the germband neuroectoderm epithelium rapidly doubles in length along the anterior-posterior axis through a process known as convergent extension (CE); it also becomes subdivided into tandem tissue compartments through the formation of compartment boundaries (CBs). Both processes are dependent on the planar polarity of proteins involved in cellular tension and adhesion. The enrichment of actomyosin-based tension and adherens junction-based adhesion at specific cell-cell contacts is required for coordinated cell intercalation, which drives CE, and the creation of highly stable cell-cell contacts at CBs. Recent studies have revealed a system for rapid cellular polarization triggered by the expression of leucine-rich-repeat (LRR) cell-surface proteins in striped patterns. In particular, the non-uniform expression of Toll-2, Toll-6, Toll-8, and Tartan generates local cellular asymmetries that allow cells to distinguish between cell-cell contacts oriented parallel or perpendicular to the anterior-posterior axis. In this review, we discuss (1) the biomechanical underpinnings of CE and CB formation, (2) how the initial symmetry-breaking events of anterior-posterior patterning culminate in planar polarity, and (3) recent advances in understanding the molecular mechanisms downstream of LRR receptors that lead to planar polarized tension and junctional adhesion.

The first embryo, the origin of cancer and animal phylogeny. IV. The neoplastic basis for the formation of the innate immune system

“…With the expansion of TLRs in mollusks, sccTLRs (TLRs with a single cysteine cluster in their ectodomain) emerged. The developmental (convergence extension, planar polarity, and invagination) and immunity functions of Toll (Kuebler and Pare, 2023) were first identified in studies with Drosophila (Gerttula et al, 1988). These embryological functions were also demonstrated in more basal Arthropoda (Benton et al, 2016), indicating that they are highly evolutionarily conserved biological functions, being present in basal groups of animals.…”