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Role for sperm in spatial patterning of the early mouse embryo

Abstract

Despite an apparent lack of determinants that specify cell fate, spatial patterning of the mouse embryo is evident early in development. The axis of the post-implantation egg cylinder can be traced back to organization of the pre-implantation blastocyst1. This in turn reflects the organization of the cleavage-stage embryo and the animal–vegetal axis of the zygote2,3. These findings suggest that the cleavage pattern of normal development may be involved in specifying the future embryonic axis; however, how and when this pattern becomes established is unclear. In many animal eggs, the sperm entry position provides a cue for embryonic patterning4,5,6, but until now no such role has been found in mammals. Here we show that the sperm entry position predicts the plane of initial cleavage of the mouse egg and can define embryonic and abembryonic halves of the future blastocyst. In addition, the cell inheriting the sperm entry position acquires a division advantage and tends to cleave ahead of its sister. As cell identity reflects the timing of the early cleavages, these events together shape the blastocyst whose organization will become translated into axial patterning after implantation. We present a model for axial development that accommodates these findings with the regulative nature of mouse embryos.

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Figure 1: Landmarks in the development of the pre-implantation embryo.
Figure 2: The SEP predicts the Em–Ab axis of the blastocyst.
Figure 3: The SEP predicts the first cleavage plane.
Figure 4: Relationship between the SEP at the two-cell stage and its fate at the blastocyst stage.
Figure 5: Two markers of the egg surface colocalize from the SEP in the zygote to the blastocyst.
Figure 6: A model to show the developmental consequences of the first cleavage division defined by the SEP.

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Acknowledgements

We are grateful to D. Glover for invaluable suggestions and support; R. Pedersen and C. Graham for helpful discussions; and J. Gurdon for his critical comments. This work was supported by a Lister Institute of Preventive Medicine Fellowship, a Wellcome Trust Project Grant and a Royal Society Equipment Grant to M.Z.-G.

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Correspondence to Magdalena Zernicka-Goetz.

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Piotrowska, K., Zernicka-Goetz, M. Role for sperm in spatial patterning of the early mouse embryo. Nature 409, 517–521 (2001). https://doi.org/10.1038/35054069

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