For a cell or group of cells to move, they must relinquish their bonds with the basement membrane. Medioni and Noselli have studied how this is accomplished in Drosophila melanogaster using polar cells that move from the anterior to the posterior of the egg chamber during oogenesis. They found that these cells have an intriguing way of remodelling the cellular anchor — it involves shuttling basement membrane components from their basal to apical surface, from where they are released.
Accompanied by six border cells, the two anterior polar cells move as a 'border cell cluster' towards the oocyte. Medioni and Noselli studied what happens before this, when the polar cells are still part of the monolayer epithelium that surrounds the central germline cells. They showed that a fusion of green fluorescent protein (GFP) and the type IV collagen α2 chain, as well as other basement membrane components, accumulated not only in the basement membrane of the monolayer epithelial cells, but also in a discrete cap over the apical surface of the anterior polar cells. Blocking the differentiation of anterior polar cells prevented the formation of this apical cap, whereas generating ectopic anterior polar cells gave rise to ectopic polar caps.
Three-dimensional imaging showed that the polar cells were capped asymmetrically. When the polar cells began to undergo rounding and detach from the basement membrane that lined the whole egg chamber, the apical cap was still there, but it was lost when the border cell cluster started to migrate. Interestingly, whereas the border cells had to reorganize their cellular junctions and detach or degrade their basement membrane during migration, reverting to their original cellular organization only when they reached the oocyte, the polar cells remained fully polarized, with an intact basal basement membrane, during delamination and migration.
The authors then showed that neither the basement membrane proteins that were present in the apical cap, nor those of the normal basement membrane, were made cell autonomously. So the apical cap must have originated from outside the polar cells. Blocking intracellular trafficking by inhibiting D. melanogaster Drab5 and Shibire in the border cells showed that these proteins are required for border cell migration. However, only dominant-negative Drab5 inhibited the formation of apical caps — a dominant-negative form of Shibire failed to inhibit this process. So Drab5-dependent transcytosis seems to regulate apical capping.
How might apical shedding of the basement membrane be coordinated with the migration of the border cell cluster? Could the border cells regulate the status of the apical basement membrane in the polar cells? Polar cells activate the JAK (Janus kinase)–STAT (signal transducer and activator of transcription) pathway in neighbouring cells by secreting Unpaired, which induces the neighbouring cells to become outer border cells. Inhibiting the function of Domeless (Dome), the Unpaired receptor, blocked border cell formation and, consequently, polar cell migration. And, noticeably, the apical cap wasn't shed from polar cells.
Outer border cells are therefore needed to remove the apical cap before the border cell cluster can migrate (see figure). This might be a quality-control mechanism to ensure that only mature clusters can begin to migrate.
References
ORIGINAL RESEARCH PAPER
Medioni, C. & Noselli, S. Dynamics of the basement membrane in invasive epithelial clusters in Drosophila. Development 132, 3069–3077 (2005)
FURTHER READING
Montell, D. J. Border-cell migration: the race is on. Nature Rev. Mol. Cell Biol. 4, 13–24 (2003)
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Katrin, B. Anchors away!. Nat Rev Mol Cell Biol 6, 595 (2005). https://doi.org/10.1038/nrm1719
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DOI: https://doi.org/10.1038/nrm1719