Compaction of the preimplantation embryo is the earliest morphogenetic process essential for mammalian development, yet it remains unclear how round cells elongate to form a compacted embryo. Here, using live mouse embryo imaging, we demonstrate that cells extend long E-cadherin-dependent filopodia on to neighbouring cells, which control the cell shape changes necessary for compaction. We found that filopodia extension is tightly coordinated with cell elongation, whereas retraction occurs before cells become round again before dividing. Laser-based ablations revealed that filopodia are required to maintain elongated cell shapes. Moreover, molecular disruption of the filopodia components E-cadherin, α- and β-catenin, F-actin and myosin-X prevents cells from elongating and compacting the embryo. Finally, we show that early filopodia formation triggered by overexpressing myosin-X is sufficient to induce premature compaction. Our findings establish a role for filopodia during preimplantation embryonic development and provide an in vivo context to investigate the biological functions of filopodia in mammals.
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We thank A. Yap, E. Jesudason, A. Fouras and J. Polo for comments on the manuscript; T. Bell for advice on laser ablations; S. Firth and I. Harper for help with imaging experiments; and R. Cheney, A. Yap and B. Henderson for sharing DNA constructs. N.P. is supported by ARC DP120104594 and DE120100794, NHMRC APP1052171 and Monash University Strategic and Interdisciplinary grants, and J.C.F-G. by Wenner-Gren Foundations and Swedish Society for Medical Research Postdoctoral Fellowships.
Integrated supplementary information
Time-lapse imaging of a representative embryo during compaction shows two cells extending filopodia, which then fully retract before cell division. The embryo was microinjected with memb-mCherry into one cell at the 2-cell stage. Orthogonal scale bar, 5 μm.
Time-lapse imaging of a representative embryo during compaction shows a cell (left) with E-cad-GFP-expressing filopodia extended onto its E-cad-GFP-labelled neighbouring cell (right). The long finger-like processes clearly retract and return to the membrane apical border region where filopodia initially attached (left). Orthogonal scale bar, 5 μm.
Time-lapse imaging of a representative embryo during compaction shows two cells retracting their memb-mCherry-labelled filopodia just prior to division. H2B-Cerulean-labelled nuclei show chromatin condensation and chromosome separation at the time when filopodia start to retract. Orthogonal scale bar, 5 μm.