This Title All WIREs
How to cite this WIREs title:
WIREs Dev Biol
Impact Factor: 3.883

Signals and mechanics shaping compartment boundaries in Drosophila

Full article on Wiley Online Library:   HTML PDF

Can't access this content? Tell your librarian.

During animal development groups of cells with similar fates and functions often stay together and separate from cells with different fates. An example for this cellular behavior is the formation of compartments, groups of cells with similar fates that are separated by sharp boundaries from neighboring groups of cells. Compartments play important roles during patterning by serving as units of growth and gene expression. Boundaries between compartments are associated with organizers that secrete signaling molecules instructing growth and differentiation throughout the tissue. The straight shape of the boundary between compartments is important for maintaining the position and shape of the organizer and thus for precise patterning. The straight shape of compartment boundaries, however, is challenged by cell divisions and cell intercalations that take place in many developing tissues. Early work established a role for selector genes and signaling pathways in setting up and keeping boundaries straight. Recent work in Drosophila has now begun to further unravel the physical and cellular mechanisms that maintain compartment boundaries. Key to the separation of compartments is a local increase of actomyosin‐dependent mechanical tension at cell junctions along the boundary. Increased mechanical tension acts as a barrier to cell mixing during cell division and influences cell rearrangements during cell intercalations along the compartment boundary in a way that the straight shape of the boundary is maintained. An important question for the future is how the signaling pathways that maintain the straight shape of compartment boundaries control mechanical tension along these boundaries. WIREs Dev Biol 2015, 4:407–417. doi: 10.1002/wdev.178 This article is categorized under: Establishment of Spatial and Temporal Patterns > Cell Sorting and Boundary Formation
Lineage and nonlineage boundaries. Tissues with two domains differing in their gene expression (white and green) are schematized. At lineage boundaries, cells that mis‐segregate (outlined in red) need to physically rearrange to reestablish the straight boundary (a). At nonlineage boundaries, cells that mis‐segregate (outlined in red) readjust their gene expression to the new environment in order to reestablish a straight boundary (b). Boundaries are highlighted in blue.
[ Normal View | Magnified View ]
Cellular mechanisms shaping compartment boundaries. In the embryonic epidermis, an actomyosin cable acts as a barrier to cell mixing between neighboring compartments (a). During cell division, cells round up and transiently deform the compartment boundary. As cells exit mitosis, the boundary straightens again, apparently by the contractile activity of the actomyosin cable. Cell rearrangements involving T1 transitions lead to cell mixing (neighbor exchange) within compartments (b). During a T1 transition, a cell junction between two neighboring cells (left, red) shrinks into a fourfold vertex (middle). A new junction (right, red) is formed separating the original pair of cells. T1 transitions along the AP boundary are biased (c). During junctional shrinkage, the junction preferentially shrinks by the movement of the vertex located away from the compartment boundary. As a consequence, the new junction is formed in line with the existing junctions along the AP boundary and the straight shape of the AP boundary is maintained.
[ Normal View | Magnified View ]
Physical mechanisms shaping compartment boundaries. Reducing cell proliferation rate near a compartment boundary (grey shaded region) can keep a compartment boundary straight and prevent cell mixing (a). Tissue anisotropies (large arrows) can keep a compartment boundary straight, but cannot prevent cell mixing (b). Orientation of cell division dependent on cell shape has little influence on compartment boundary shape (c). In conjunction with a local increase in mechanical tension, however, it can further straighten the shape of compartment boundaries. A local increase in mechanical tension (red arrows) at cell junctions along a compartment boundary can keep the boundary straight and prevent cell mixing (d). Compartment boundaries are highlighted in blue.
[ Normal View | Magnified View ]
Signals shaping compartment boundaries in wing imaginal disks. A twin spot analysis to test whether mutant cell clones disturb a compartment boundary is shown. Inter‐chromosomal recombination between a wild‐type and a mutation‐carrying (or control) chromosome arm followed by cell proliferation results in two clones: a mutant (or control) clone (red) and a twin spot clone (grey). The twin spot clone, which inherits two copies of the wild‐type chromosome arm, identifies the compartment in which the recombination took place. Control clones remain in the compartment of origin, whereas mutant clones, which inherit two copies of the mutant chromosome arm (here smo), may rearrange toward the neighboring compartment (green). Rearrangement of a mutant clone into the neighboring compartment indicates that the wild‐type function of the gene is to segregate cells along the compartment boundary. The compartment boundary is depicted in blue (a and b). The homeodomain‐containing proteins Engrailed and Invected induce the expression of the short‐range signaling molecule Hedgehog in all cells of the posterior compartment in the wing imaginal disk. Hedgehog protein moves to the anterior compartment, where it activates a transduction pathway involving Smoothened (Smo) leading to the activation of the transcription factor Cubitus interruptus (Ci). Activated Ci induces the expression of the long‐range signaling molecule Dpp in a strip of anterior cells along the AP boundary (c). The LIM‐homeodomain protein Apterous induces the expression of the Notch‐ligand Serrate in dorsal cells and restricts expression of the Notch‐ligand Delta to ventral cells. Serrate and Delta activate Notch symmetrically in a few cells rows along both sides of the DV boundary. Apterous also induces the expression of the glycosyltransferase Fringe that enhances the sensitivity of dorsal cells to Delta and reduces their sensitivity to Serrate, thus contributing to the local activation of Notch along the DV boundary. Notch represses the bantam micro‐RNA, which in turn represses the actin regulator Enabled (Ena), thus resulting in a local increase of Enabled protein along the DV boundary (d).
[ Normal View | Magnified View ]
Compartments in Drosophila. The embryonic epidermis is subdivided into multiple anterior (A, red) and posterior (P, green) compartments (a). The larval wing imaginal disk is subdivided into anterior and posterior, and dorsal (D) and ventral (V) compartments (b). Neighboring anterior and posterior histoblast nests are separated by a compartment boundary during pupal development (c). In the adult fly, the wing is subdivided into anterior and posterior compartments. The abdominal epidermis, derived from histoblast nests, is subdivided into multiple anterior and posterior compartments (d). Original versions of panels (b) and (d) were first published in Ref .
[ Normal View | Magnified View ]
Identification of compartment boundaries. A cell is stably marked (red) during early development so that all its descendants carry the mark. Cell proliferation leads to a clone of marked cells. The clone border is irregular where it is interfacing cells of the same compartment. Clone borders are straight along compartment boundaries. This straight shape of the clonal border identifies the compartment boundary (blue) (a). A clone of cells (red) abutting the AP boundary in a Drosophila wing imaginal disk. The posterior compartment is visualized by the activity of the engrailed‐lacZ line (green) (b).
[ Normal View | Magnified View ]

Browse by Topic

Establishment of Spatial and Temporal Patterns > Cell Sorting and Boundary Formation