Abstract
BackgroundIn Dictyostelium discoideum, vesicular transport of the adenylyl cyclase A (ACA) to the posterior of polarized cells is essential to relay exogenous 3′,5′-cyclic adenosine monophosphate (cAMP) signals during chemotaxis and for the collective migration of cells in head-to-tail arrangements called streams.ResultsUsing fluorescence in situ hybridization (FISH), we discovered that the ACA mRNA is asymmetrically distributed at the posterior of polarized cells. Using both standard estimators and Monte Carlo simulation methods, we found that the ACA mRNA enrichment depends on the position of the cell within a stream, with the posterior localization of ACA mRNA being strongest for cells at the end of a stream. By monitoring the recovery of ACA-YFP after cycloheximide (CHX) treatment, we observed that ACA mRNA and newly synthesized ACA-YFP first emerge as fluorescent punctae that later accumulate to the posterior of cells. We also found that the ACA mRNA localization requires 3′ ACA cis-acting elements.ConclusionsTogether, our findings suggest that the asymmetric distribution of ACA mRNA allows the local translation and accumulation of ACA protein at the posterior of cells. These data represent a novel functional role for localized translation in the relay of chemotactic signal during chemotaxis.
Highlights
In Dictyostelium discoideum, vesicular transport of the adenylyl cyclase A (ACA) to the posterior of polarized cells is essential to relay exogenous 3′,5′-cyclic adenosine monophosphate signals during chemotaxis and for the collective migration of cells in head-to-tail arrangements called streams
We found that the fluorescence in situ hybridization (FISH) signals appeared in randomly distributed punctae likely representing multiple individual transcripts, within the cytoplasm of non-polarized vegetative aca− cells expressing ACA-YFP (ACA-YFP/aca−) as well as car1/3−/− cells expressing cAR1-YFP (Additional file 1: Figure S1A-B)
Whereas F-actin localized to the leading edge of WT cells, we observed that ACA mRNA was enriched at the posterior of cells (Fig. 1a)
Summary
In Dictyostelium discoideum, vesicular transport of the adenylyl cyclase A (ACA) to the posterior of polarized cells is essential to relay exogenous 3′,5′-cyclic adenosine monophosphate (cAMP) signals during chemotaxis and for the collective migration of cells in head-to-tail arrangements called streams. As cells respond to cAMP gradients and migrate directionally, they align in a head-to-tail fashion and form streams - a process that increases recruitment range during chemotaxis [10]. We found that this streaming behavior depends on the presence of ACA, but most remarkably, on its enrichment at the posterior of polarized cells [11, 12]. We proposed that the asymmetric distribution of vesicular ACA provides a compartment from which cAMP is locally released from the posterior of cells to spatially attract neighboring cells
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