Basement membrane perforations guide anterior–posterior axis formation

Dong-Yuan Chen, Nikolas H. Claussen, Shiny Titus, Wenqi Hu, Bailey A. T. Weatherbee, Rachel S. Mandelbaum, Richard T. Scott, Emre Seli, Sebastian J. Streichan and Magdalena Zernicka-Goetz ()
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Dong-Yuan Chen: California Institute of Technology
Nikolas H. Claussen: University of California Santa Barbara
Shiny Titus: Irving Cancer Medical Center
Wenqi Hu: California Institute of Technology
Bailey A. T. Weatherbee: Cincinnati Children’s Hospital Medical Center
Rachel S. Mandelbaum: University of Southern California
Richard T. Scott: Foundation for Embryonic Competence
Emre Seli: 333 Cedar St
Sebastian J. Streichan: University of California Santa Barbara
Magdalena Zernicka-Goetz: California Institute of Technology

Nature Communications, 2025, vol. 16, issue 1, 1-19

Abstract: Abstract Establishment of the anterior-posterior (AP) axis is a critical symmetry-breaking event in mammalian development. In mice, this process involves the directed migration of the distal visceral endoderm (DVE). Here, we use targeted perturbations to demonstrate that asymmetric perforations in the basement membrane guide DVE migration. During implantation, matrix metalloproteinases in extra-embryonic tissues create uneven basement membrane perforations, establishing directional cues for cohesive DVE migration. Using light-sheet microscopy and tissue cartography, we show that migrating DVE deforms surrounding tissues. Physical modeling and live imaging of DVE protrusions indicate that basement membrane perforations orchestrate active force generation within the DVE. Extending these findings to human embryos and stem cell-derived models, we identify basement membranes with enriched perforations near the anterior hypoblast in embryos, suggesting a conserved mechanism for AP axis specification. These findings reveal an unrecognized role of basement membrane remodeling and mechanical heterogeneity in guiding directional tissue migration during mammalian development.

Date: 2025
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DOI: 10.1038/s41467-025-61441-6

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