Dynamic expression of Drosophila segmental cell surface-encoding genes and their pair-rule regulators.

Drosophila segmentation is regulated by a complex network of transcription factors that include products of the pair-rule genes (PRGs). PRGs are expressed in early embryos in the primorida of alternate segmental units, establishing the repeated, segmental body plan of the fly. Despite detailed analysis of the regulatory logic among segmentation genes, the relationship between these genes and the morphological formation of segments is still poorly understood, since regulation of transcription factor expression is not sufficient to explain how segments actually form and are maintained. Cell surface proteins containing Leucine rich repeats (LRR) play a variety of roles in development, and those expressed in segmental patterns likely impact segment morphogenesis. Here we explore the relationships between the PRG network and segmentally expressed LRR-encoding (sLRR) genes. We examined expression of Toll2, Toll6, Toll7, Toll8 and tartan (trn) in wild type or PRG mutant embryos. Expression of each sLRR-encoding gene is dynamic, but each has a unique register along the anterior-posterior axis. The registers for different sLRRs are off-set from one another resulting in a continually changing set of overlapping expression patterns among the sLRR-encoding genes themselves and between the sLRR-encoding genes and the PRGs. Accordingly, each sLRR-encoding gene is regulated by a unique combination of PRGs. These findings suggest that one role of the PRG network is to promote segmentation by establishing a cell surface code: each row of cells in the two-segment-wide primordia expresses a unique combination of sLRRs, thereby translating regulatory information from the PRGs to direct segment morphogenesis.

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

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.