Synchronous and symmetric migration of Drosophila caudal visceral mesoderm cells requires dual input by two FGF ligands

Abstract

SUMMARYCaudal visceral mesoderm (CVM) cells migrate synchronously towards the anterior of the Drosophila embryo as two distinct groups located on each side of the body, in order to specify longitudinal muscles that ensheath the gut. Little is known about the molecular cues that guide cells along this path, the longest migration of embryogenesis, except that they closely associate with trunk visceral mesoderm (TVM). The expression of the fibroblast growth factor receptor (FGFR) heartless and its ligands, pyramus (pyr) and thisbe (ths), within CVM and TVM cells, respectively, suggested FGF signaling may influence CVM cell guidance. In FGF mutants, CVM cells die before reaching the anterior region of the TVM. However, an earlier phenotype observed was that the two cell clusters lose direction and converge at the midline. Live in vivo imaging and tracking analyses identified that the movements of CVM cells were slower and no longer synchronous. Moreover, CVM cells were found to cross over from one group to the other, disrupting bilateral symmetry, whereas such mixing was never observed in wild-type embryos. Ectopic expression of either Pyr or Ths was sufficient to redirect CVM cell movement, but only when the endogenous source of these ligands was absent. Collectively, our results show that FGF signaling regulates directional movement of CVM cells and that native presentation of both FGF ligands together is most effective at attracting cells. This study also has general implications, as it suggests that the activity supported by two FGF ligands in concert differs from their activities in isolation.

Leading and trailing cells cooperate in collective migration of the zebrafish posterior lateral line primordium

“…As noted earlier, cells in the leading zone are a source of FGF ligands (Aman and Piotrowski, 2008). FGFs serve as migratory cues in a variety of other contexts (Kadam et al, 2012;Vitorino and Meyer, 2008), making them strong candidates for providing a chemoattractive cue for trailing cells. Previous work has already shown that cryptic lamellipodia in trailing cells of the intact PLLp are normally polarized toward the leading edge, and that this polarization is lost upon inhibition of FGF signaling by treatment with the Fgfr1 inhibitor SU5402 (Lecaudey et al, 2008;Sun et al, 1999).…”

FGF signaling supports Drosophila fertility by regulating development of ovarian muscle tissues

“…UAS lines utilized for genetic analysis were: UAS .htl. RNAi40627 [Vienna Drosophila Research Center (VDRC); reported to have one off target]; (Dietzl et al, 2007; Kadam et al, 2012)], UAS .htl. RNAi6692 (VDRC; reported to have no off targets), UAS.…”

Chemokine and Fgf signalling act as opposing guidance cues in formation of the lateral line primordium

“…Because in other tissues Fgfs act as chemoattractive signals (Sutherland et al, 1996;Sato et al, 2011;Kadam et al, 2012), we considered the possibility that Fgfs also have a more direct role in lateral line cell migration. We analysed the expression of Fgf signalling components and found that after the fusion between the SPCs and primordium, fgf3 and fgf10 are expressed in the leading zone, and fgfr1 in the trailing zone, as previously reported ( , 2008).…”