Site of the previous meiotic division defines cleavage orientation in the mouse embryo

Płusa, Berenika; Grabarek, Joanna B.; Piotrowska, Karolina; Glover, David M.; Zernicka‐Goetz, Magdalena

doi:10.1038/ncb860

Cited by 66 publications

(48 citation statements)

References 19 publications

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“…Several studies have suggested that differential orientation of early cleavage divisions brings about differential cellular partitioning that influences the distribution of cells at the blastocyst stage (Gardner 1997(Gardner , 2001(Gardner , 2002(Gardner , 2007Piotrowska and Zernicka-Goetz 2001;Bischoff et al 2008). Thus, in the majority of embryos, the first cleavage division is along the AV axis and so distributes both A and V material to both daughter blastomeres (Gulyas 1975;Gardner 1997;Plusa et al 2002Plusa et al , 2005bGray et al 2004). Because of controversy in the early mouse embryo field, it is important to stress that such assessment can be accurate only when the marker of this axis (the second polar body) remains attached to the embryo and before any flow of membrane markers in cytokinesis (Plusa et al 2005b).…”

Section: Discussionmentioning

confidence: 99%

Role of Cdx2 and cell polarity in cell allocation and specification of trophectoderm and inner cell mass in the mouse embryo

Jędrusik

Parfitt²,

Guo³

et al. 2008

Genes Dev.

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219

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Genesis of the trophectoderm and inner cell mass (ICM) lineages occurs in two stages. It is initiated via asymmetric divisions of eight-and 16-cell blastomeres that allocate cells to inner and outer positions, each with different developmental fates. Outside cells become committed to the trophectoderm at the blastocyst stage through Cdx2 activity, but here we show that Cdx2 can also act earlier to influence cell allocation. Increasing Cdx2 levels in individual blastomeres promotes symmetric divisions, thereby allocating more cells to the trophectoderm, whereas reducing Cdx2 promotes asymmetric divisions and consequently contribution to the ICM. Furthermore, both Cdx2 mRNA and protein levels are heterogeneous at the eight-cell stage. This heterogeneity depends on cell origin and has developmental consequences. Cdx2 expression is minimal in cells with unrestricted developmental potential that contribute preferentially to the ICM and is maximal in cells with reduced potential that contribute more to the trophectoderm. Finally, we describe a mutually reinforcing relationship between cellular polarity and Cdx2: Cdx2 influences cell polarity by up-regulating aPKC, but cell polarity also influences Cdx2 through asymmetric distribution of Cdx2 mRNA in polarized blastomeres. Thus, divisions generating inside and outside cells are truly asymmetric with respect to cell fate instructions. These two interacting effects ensure the generation of a stable outer epithelium by the blastocyst stage.[Keywords: Cdx2; mouse embryo; polarization; ICM; blastocyst; trophectoderm] Supplemental material is available at http://www.genesdev.org.

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Section: Discussionmentioning

confidence: 99%

Role of Cdx2 and cell polarity in cell allocation and specification of trophectoderm and inner cell mass in the mouse embryo

Jędrusik

Parfitt²,

Guo³

et al. 2008

Genes Dev.

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219

247

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“…Because the plane of the first cleavage division correlates with both the position of the previous meiotic division -the animal pole (Plusa et al, 2002a) and the position of the fertilisation cone that marks the sperm entry Plusa et al, 2002b), the question arises of the extent of the role of the oocyte, and that of the sperm in setting up early embryo patterning. It could be argued that allocation of the progeny of 2-cell blastomeres in diploid parthenogenetic blastocysts differs from that in normal embryos because their animal pole has been perturbed by either cytochalasin treatment or electrofusion.…”

Section: Discussionmentioning

confidence: 99%

Early patterning of the mouse embryo — contributions of sperm and egg

Piotrowska

Zernicka‐Goetz

2002

Development

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The first cleavage of the fertilised mouse egg divides the zygote into two cells that have a tendency to follow distinguishable fates. One divides first and contributes its progeny predominantly to the embryonic part of the blastocyst, while the other, later dividing cell, contributes mainly to the abembryonic part. We have previously observed that both the plane of this first cleavage and the subsequent order of blastomere division tend to correlate with the position of the fertilisation cone that forms after sperm entry. But does sperm entry contribute to assigning the distinguishable fates to the first two blastomeres or is their fate an intrinsic property of the egg itself? To answer this question we examined the distribution of the progeny of early blastomeres in embryos never penetrated by sperm — parthenogenetic embryos. In contrast to fertilised eggs, we found there is no tendency for the first two parthenogenetic blastomeres to follow different fates. This outcome is independent of whether parthenogenetic eggs are haploid or diploid. Also unlike fertilised eggs, the first 2-cell blastomere to divide in parthenogenetic embryo does not necessarily contribute more cells to the blastocyst. However, even when descendants of the first dividing blastomere do predominate, they show no strong predisposition to occupy the embryonic part. Thus blastomere fate does not appear to be decided by differential cell division alone. Finally, when the cortical cytoplasm at the site of sperm entry is removed, the first cleavage plane no longer tends to divide the embryo into embryonic and abembryonic parts. Together these results indicate that in normal development fertilisation contributes to setting up embryonic patterning, alongside the role of the egg.

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“…Fixation by either method was followed by three washes in PBS and 20 minutes of permeabilization with 0.25% Triton X-100 in PBS. Immunostaining was as described previously (Plusa et al, 2002). For detection of Par3, rabbit-anti-Par3 antibody (Lin et al, 2000) was used at a dilution of 1:200 and rhodamine-conjugated secondary anti-rabbit antibody (Jackson ImmunoResearch Laboratories) at a dilution of 1:300.…”

Section: Immunolocalization Of Par3 and Apkc In Preimplantation Embryosmentioning

confidence: 99%

Downregulation of Par3 and aPKC function directs cells towards the ICM in the preimplantation mouse embryo

Płusa

Frankenberg

Chalmers

et al. 2005

Journal of Cell Science

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226

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Generation of inside cells that develop into inner cell mass (ICM) and outside cells that develop into trophectoderm is central to the development of the early mouse embryo. Critical to this decision is the development of cell polarity and the associated asymmetric (differentiative) divisions of the 8-cell-stage blastomeres. The underlying molecular mechanisms for these events are not understood. As the Par3/aPKC complex has a role in establishing cellular polarity and division orientation in other systems, we explored its potential function in the developing mouse embryo. We show that both Par3 and aPKC adopt a polarized localization from the 8-cell stage onwards and that manipulating their function re-directs cell positioning and consequently influences cell fate. Injection of dsRNA against Par3 or mRNA for a dominant negative form of aPKC into a random blastomere at the 4-cell stage directs progeny of the injected cell into the inside part of the embryo. This appears to result from both an increased frequency by which such cells undertake differentiative divisions and their decreased probability of retaining outside positions. Thus, the natural spatial allocation of blastomere progeny can be over-ridden by downregulation of Par3 or aPKC, leading to a deceased tendency for them to remain outside and so develop into trophectoderm. In addition, this experimental approach illustrates a powerful means of manipulating gene expression in a specific clonal population of cells in the preimplantation embryo.

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Site of the previous meiotic division defines cleavage orientation in the mouse embryo

Cited by 66 publications

References 19 publications

Role of Cdx2 and cell polarity in cell allocation and specification of trophectoderm and inner cell mass in the mouse embryo

Role of Cdx2 and cell polarity in cell allocation and specification of trophectoderm and inner cell mass in the mouse embryo

Early patterning of the mouse embryo — contributions of sperm and egg

Downregulation of Par3 and aPKC function directs cells towards the ICM in the preimplantation mouse embryo

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