A cargo model of yolk syncytial nuclear migration during zebrafish epiboly

Abstract

In teleost fish, the multinucleate yolk syncytial layer functions as an extra-embryonic signaling center to pattern mesendoderm, coordinate morphogenesis and supply nutrients to the embryo. External yolk syncytial nuclei (e-YSN) undergo microtubule-dependent movements that distribute the nuclei over the large yolk mass. How e-YSN migration proceeds, and the role of the yolk microtubules, is not understood, but it is proposed that e-YSN are pulled vegetally as the microtubule network shortens from the vegetal pole. Live imaging revealed that nuclei migrate along microtubules, consistent with a cargo model in which e-YSN are moved down the microtubules by direct association with motor proteins. We found that blocking the plus-end directed microtubule motor kinesin significantly attenuated yolk nuclear movement. Blocking the outer nuclear membrane LINC complex protein Syne2a also slowed e-YSN movement. We propose that e-YSN movement is mediated by the LINC complex, which functions as the adaptor between yolk nuclei and motor proteins. Our work provides new insights into the role of microtubules in morphogenesis of an extraembryonic tissue and further contributes to the understanding of nuclear migration mechanisms during development.

Syne2b/Nesprin-2 Is Required for Actin Organization and Epithelial Integrity During Epiboly Movement in Zebrafish

“…Thus, disruption of microtubule networks in the yolk cell of MZsyne2b mutants may also contribute to impaired YSN movements during epiboly. This observation is consistent with a previous report showing that overexpression of the dominant negative Syne2a KASH slows migration speeds of YSN (Fei et al, 2019). Thus, our results further illustrate an important role of the LINC complex in coordinating nuclear movements.…”

The recycling endosome protein Rab25 coordinates collective cell movements in the zebrafish surface epithelium

“…Between dome and 50% epiboly, when the EVL is most proliferative, Venus-Rab25a and eGFP-Rab25b appeared to localize near centrosomes during mitosis and then moved towards the opposing poles of dividing cells (Figure 1B, arrowheads; Video 1). Injection of mcherry-rab25b mRNA into transgenic animals expressing Tubulin-GFP (Fei et al, 2019) confirmed that mCherry-Rab25b localized near centrosomes and dissipated following cell division (Figure 1C; arrows). During cytokinetic abscission, co-expression of eGFP-Rab25b with the midbody marker mCherry-Mklp1 demonstrated that eGFP-Rab25b dynamically localized within intercellular bridges adjacent to the midbody (Figure 1D), the sites of bridge scission.…”

The recycling endosome protein Rab25 coordinates collective cell movements in the zebrafish surface epithelium

“…Venus-Rab25a and eGFP-Rab25b appeared to localize near centrosomes during mitosis and then moved towards the opposing poles of dividing cells (Figure 1B; arrowheads; Video S1). Injection of mcherry-rab25b mRNA into transgenic animals expressing Tubulin-GFP (Fei et al, 2019) confirmed that mCherry-Rab25b localized near centrosomes and dissipated following cell division ( Figure 1C; arrows). Recycling endosomes (REs) become positioned near centrosomes during mitosis, suggesting that Rab25 associates with REs in the EVL, as in other systems (Casanova et al, 1999;Hehnly and Doxsey, 2014).…”