The first cleavage of the mouse zygote predicts the blastocyst axis

Abstract

One of the unanswered questions in mammalian development is how the embryonic-abembryonic axis of the blastocyst is first established. It is possible that the first cleavage division contributes to this process, because in most mouse embryos the progeny of one two-cell blastomere primarily populate the embryonic part of the blastocyst and the progeny of its sister populate the abembryonic part. However, it is not known whether the embryonic-abembryonic axis is set up by the first cleavage itself, by polarity in the oocyte that then sets the first cleavage plane with respect to the animal pole, or indeed whether it can be divorced entirely from the first cleavage and established in relation to the animal pole. Here we test the importance of the orientation of the first cleavage by imposing an elongated shape on the zygote so that the division no longer passes close to the animal pole, marked by the second polar body. Non-invasive lineage tracing shows that even when the first cleavage occurs along the short axis imposed by this experimental treatment, the progeny of the resulting two-cell blastomeres tend to populate the respective embryonic and abembryonic parts of the blastocyst. Thus, the first cleavage contributes to breaking the symmetry of the embryo, generating blastomeres with different developmental characteristics.

Cell and molecular regulation of the mouse blastocyst

“…The earlier-dividing two-cell blastomere did not give rise to any trophectoderm. However, this proposal contradicts all previously published observations regarding developmental potential and fate of cells from the two-cell embryo, because all other groups have reported contribution of both two-cell blastomeres to both ICM and TE (Gardner, 2001;Piotrowska et al, 2001;Marikawa, 2003, 2005;Chroscicka et al, 2004;Hiiragi and Solter, 2004;Plusa et al, 2005a;Motosugi et al, 2005;PiotrowskaNitsche and Zernicka-Goetz, 2005). Before these observations can be considered as changing the paradigms of early mouse development, it is essential to explore whether this lineage relationship holds true in other mouse strains and if it can be reproduced by other groups using alternate lineage tracing methods.…”

Using a histone yellow fluorescent protein fusion for tagging and tracking endothelial cells in ES cells and mice

“…Ultimately, it will be desirable to construct anatomical models for analysis of normal, mutant, and pathological vascular development. This goal can be achieved if each cell can be marked with a single, easily identifiable tag that is visible at subcellular resolution (Hadjantonakis and Papaioannou, 2004;Hadjantonakis et al, 2003;Koster and Fraser, 2001;Megason and Fraser, 2003;Plusa et al, 2005). The large size and uniform shape of the nucleus in most cell types makes it ideal for such high-resolution imaging, permitting the tracking of cell division and movement (Hadjantonakis and Papaioannou, 2004).…”

The Leading Blastomere of the 2-Cell Stage Parthenogenetic Porcine Embryo Contributes to the Abembryonic Part First

“…Moreover, the same group also claimed that the blastomere in the two-cell stage embryo that inherits the SEP divides earlier than the other blastomere and tends to contribute preferentially to the ICM [21]. Thus, the first cleavage of the mouse zygote predicts the blastocyst axis by breaking the symmetry of the embryo, thereby generating blastomeres with different developmental characteristics [23]. To determine whether sperm entry contributes to the fates of the first two blastomeres or if their fates are an intrinsic property of the oocyte itself, the distribution of the progeny of early blastomeres in parthenogenetic embryos was examined [22].…”

“…Controversy still exists as to whether the individual blastomeres from twocell-stage embryos have identical developmental fates. However, most reports have been limited to murine species [2,7,9,15,23,29]. The distribution of active mitochondria may be indicative of the energy or ion requirements of many key events during oocyte maturation, fertilization and early embryonic development [26].…”

“…The Em-Ab polarity of the embryo corresponds to the dorsal-ventral axis in the postimplantation stage embryo [2]. However, recent studies have proposed that the Em-Ab axis of the mouse blastocyst arises perpendicular to the first cleavage plane [5,7,20,23]. It has been shown that the animal-vegetal axes of mammalian embryos can be traced by the location of the polar body at the animal pole until the blastocyst stage [6].…”