Unipolar distributions of junctional Myosin II identify cell stripe boundaries that drive cell intercalation throughout Drosophila axis extension

摘要

Early in development, a growing embryo elongates to form its main body (head–tail) axis. This elongation is driven by a process called cell intercalation – when cells insert between each other. The mechanism that controls this coordinated cell movement is well understood on a small scale. However, it is not known how hundreds of cells rapidly intercalate across a whole tissue without deforming a tissue or inappropriately mixing. During fruit fly development, an embryo divides into repeated segments of tissue while elongating. While this happens, cells redistribute an essential structure called the actomyosin cytoskeleton so that it is found more commonly along certain sides of the cell. This structure, which can be thought of as the cell’s “muscle”, is a contractile web made of proteins called actin and myosin. It is closely associated with the cell’s membrane and causes cells to contract and push past each other. The enrichment of the actomyosin cytoskeleton on certain sides of a cell is determined by signaling systems, which are controlled by the segmentation genes in the fruit fly and by the so-called planar cell polarity pathway in vertebrates. Tetley, Blanchard et al. have now investigated cell intercalation across a whole tissue by filming live fruit fly embryos in which both actomyosin and cell membranes were made visible with fluorescent markers. Computational tools were then used to quantify how much actomyosin is enriched in the sides of thousands of cells in the embryo at particular points in time while the embryos elongated. This revealed reproducible patterns of actomyosin enrichment. As embryos elongated, the actomyosin cytoskeleton redistributed itself inside the cells whereas at the start two opposite sides of each cell were enriched in actomyosin (a bipolar distribution), at later times the enrichment occurred on just one side (a unipolar distribution). Incorporating these patterns into a model of tissue-wide cell intercalation showed that cells along the head–tail axis acquire a specific identity depending on their position. Interactions between the cells then allow the cells to compare their identities with each other and modify their pattern of actomyosin enrichment accordingly. Where the identities of neighbouring cells are different, the cells enrich actomyosin along their shared sides, creating boundaries between stripes of cells that share the same identity. These findings show that actomyosin-rich boundaries drive the elongation of the head–tail axis while limiting cell intermixing. Future work will investigate how the patterns of actomyosin enrichment are altered in fly mutants in which the identities of the cells along the head–tail axis are disrupted.