Space Asymmetry Directs Preferential Sperm Entry in the Absence of Polarity in the Mouse Oocyte

Abstract

Knowledge about the mechanism that establishes embryonic polarity is fundamental in understanding mammalian development. In re-addressing several controversial claims, we recently proposed a model in which mouse embryonic polarity is not specified until the blastocyst stage. Before fertilization, the fully differentiated oocyte has been characterized as “polarized,” and we indeed observed that the sperm preferentially enters the polar body half. Here we show that preferential sperm entry is not due to an intrinsic polarity of the oocyte, since fertilization takes place uniformly when the zona pellucida is removed. We suggest that the term “asymmetry” denotes morphological differences, whereas “polarity” in addition implies developmental consequences. Thus, the mouse oocyte can be considered “asymmetric” but “non-polarized.” The penetration through the zona pellucida is also random, and a significant proportion of sperm binds to the oocyte membrane at a point distant from the zona penetration site. Time-lapse recordings confirmed that sperm swim around the perivitelline space before fertilization. Experimental enlargement of the perivitelline space in the non-polar body half increased the regional probability of fertilization. Based on these experiments, we propose a model in which the space asymmetry exerted by the first polar body and the zona pellucida directs sperm entry preferentially to the polar body half, with no need for oocyte polarity.

Segregation during cleavage in the mammalian embryo? A critical comparison of whole-mount/CLSM and section immunohistochemistry casts doubts on segregation of axis-relevant leptin domains in the rabbit

“…Interestingly these views come close to the earlier segregation hypothesis which was largely based on histochemistry and classical deletion experiments (Dalcq 1954;Seidel 1960;Denker 1970bDenker , 1976. Without entering into a detailed discussion of these and of the more recent studies (the conclusions of which are still being debated controversially by the different groups: Gardner 2006a, b;Gray et al 2004;Hiiragi et al 2006;Motosugi et al 2006;Tam 2004, 2009;Zernicka-Goetz 2006) we must envisage with respect to the present investigations that all these concepts imply an element of segregation at some stage of development. However, in contrast to the original version of the polarization hypothesis (which implied that segregation takes place only in the radial direction) part of the segregation is thought now (and was thought in the classical segregation theory) to create inequality of blastomeres also along the presumptive e-a axis, i.e., a second aspect of segregation, in addition to that occurring along the radial axis.…”

Actin cytoskeleton in cell polarity and asymmetric division during mouse oocyte maturation

“…The two divisions are extremely asymmetric in respect of both daughter cell size and developmental potential: whereas the large egg eventually gets fertilized and develops into an embryo, the tiny polar bodies rapidly degenerate. Such division asymmetry is essential for the mature egg to maintain a large cytoplasm, to facilitate sperm penetration, and to avoid abortive development of multiple fertilized cells within one zona pellucida [Motosugi et al, 2006;Runge et al, 2007;Otsuki et al, 2012].…”

Theoretical exploration of blastocyst morphogenesis

“…and "Do they matter?" The role of early development routines has been the subject of recent intense study (Gray et al, 2004, Motosugi et al, 2005, Plusa et al, 2005, Chazaud et al, 2006, Gardner, 2006, Hiiragi et al, 2006a, Hiiragi et al, 2006b, Motosugi et al, 2006, Plusa et al, 2006, Wakmundzka et al, 2006, Zernicka-Goetz, 2006, Dietrich and Hiiragi, 2007, Gardner, 2007, Kurotaki et al, 2007, Torres-Padilla et al, 2007, Bischoff et al, 2008. In this article we consider, theoretically, how these patterns might occur during the formation of the mouse blastocyst.…”