Abstract
In multicellular organisms, oocytes and sperm undergo fusion during fertilization and the resulting zygote gives rise to a new individual. The ability of zygotes to produce a fully formed individual from a single cell when placed in a supportive environment is known as totipotency. Given that totipotent cells are the source of all multicellular organisms, a better understanding of totipotency may have a wide-ranging impact on biology. The precise delineation of totipotent cells in mammals has remained elusive, however, although zygotes and single blastomeres of embryos at the two-cell stage have been thought to be the only totipotent cells in mice. We now show that a single blastomere of two- or four-cell mouse embryos can give rise to a fertile adult when placed in a uterus, even though blastomere isolation disturbs the transcriptome of derived embryos. Single blastomeres isolated from embryos at the eight-cell or morula stages and cultured in vitro manifested pronounced defects in the formation of epiblast and primitive endoderm by the inner cell mass and in the development of blastocysts, respectively. Our results thus indicate that totipotency of mouse zygotes extends to single blastomeres of embryos at the four-cell stage.
Highlights
In multicellular organisms, oocytes and sperm undergo fusion during fertilization and the resulting zygote gives rise to a new individual
We refer to embryos developed from single blastomeres at the two-cell, four-cell, eight-cell, or morula stage or those developed from zygotes with or without the zona pellucida (ZP) as 2CB, 4CB, 8CB, MB, 1CZ, and 1C embryos, respectively
We have here shown that totipotency of mouse zygotes extends to blastomeres at the four-cell stage, the proportion of totipotent blastomeres is relatively small at the four-cell stage, and that pre- and peri-implantation developmental potential are essentially lost in blastomeres of embryos at the morula and eight-cell stages, respectively
Summary
Oocytes and sperm undergo fusion during fertilization and the resulting zygote gives rise to a new individual. Our results indicate that totipotency of mouse zygotes extends to single blastomeres of embryos at the four-cell stage. Preimplantation mammalian embryos at the stage prior to segregation of the first two cell lineages— the embryonic cell lineage (the inner cell mass, or ICM) and the extraembryonic cell lineage (the trophectoderm, or TE)—contain two distinct types of cell: totipotent cells and plenipotent cells, the latter of which are able to generate all derivative cells of both the ICM and TE but are unable to produce a fully formed individual from a single cell[1]. The molecular basis and key determinants of pluripotency, including transcriptional and epigenetic networks, have been extensively characterized in E SCs4–6 Knowledge obtained from these studies led to the development of methods for the generation of another type of pluripotent cell, the induced pluripotent stem cell (iPSC). The precise delineation of totipotent cells in mammals has remained unclear, with evidence suggesting that totipotent cells exist up to the two-cell stage (mouse12, rat[13], and h orse14), four-cell stage ( cattle[15] and m onkey16), or eight-cell stage ( rabbit17, sheep[18], and pig19) of preimplantation embryos
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