Initiation of a conserved trophectoderm program in human, cow and mouse embryos

Nature. 2020 Nov;587(7834):443-447. doi: 10.1038/s41586-020-2759-x. Epub 2020 Sep 23.

Abstract

Current understandings of cell specification in early mammalian pre-implantation development are based mainly on mouse studies. The first lineage differentiation event occurs at the morula stage, with outer cells initiating a trophectoderm (TE) placental progenitor program. The inner cell mass arises from inner cells during subsequent developmental stages and comprises precursor cells of the embryo proper and yolk sac1. Recent gene-expression analyses suggest that the mechanisms that regulate early lineage specification in the mouse may differ in other mammals, including human2-5 and cow6. Here we show the evolutionary conservation of a molecular cascade that initiates TE segregation in human, cow and mouse embryos. At the morula stage, outer cells acquire an apical-basal cell polarity, with expression of atypical protein kinase C (aPKC) at the contact-free domain, nuclear expression of Hippo signalling pathway effectors and restricted expression of TE-associated factors such as GATA3, which suggests initiation of a TE program. Furthermore, we demonstrate that inhibition of aPKC by small-molecule pharmacological modulation or Trim-Away protein depletion impairs TE initiation at the morula stage. Our comparative embryology analysis provides insights into early lineage specification and suggests that a similar mechanism initiates a TE program in human, cow and mouse embryos.

Publication types

  • Comparative Study
  • Research Support, Non-U.S. Gov't

MeSH terms

  • Adaptor Proteins, Signal Transducing / metabolism
  • Animals
  • Biological Evolution*
  • Blastocyst Inner Cell Mass / cytology
  • Blastocyst Inner Cell Mass / metabolism
  • Cattle
  • Cell Lineage
  • Cell Polarity
  • Ectoderm / cytology
  • Ectoderm / metabolism*
  • Embryo, Mammalian / cytology*
  • Embryo, Mammalian / enzymology
  • Embryo, Mammalian / metabolism*
  • Female
  • GATA3 Transcription Factor / metabolism
  • Gene Expression Regulation, Developmental*
  • Hippo Signaling Pathway
  • Humans
  • Mice
  • Morula / cytology
  • Morula / enzymology
  • Morula / metabolism
  • Placenta / cytology
  • Placenta / metabolism
  • Pregnancy
  • Protein Kinase C / metabolism
  • Protein Serine-Threonine Kinases / metabolism
  • SOXB1 Transcription Factors / metabolism
  • Signal Transduction
  • Transcription Factors / metabolism
  • Transcription, Genetic*
  • Trophoblasts / cytology
  • Trophoblasts / metabolism*
  • YAP-Signaling Proteins
  • Yolk Sac / cytology
  • Yolk Sac / metabolism

Substances

  • Adaptor Proteins, Signal Transducing
  • GATA3 Transcription Factor
  • SOXB1 Transcription Factors
  • Transcription Factors
  • YAP-Signaling Proteins
  • YAP1 protein, human
  • Protein Serine-Threonine Kinases
  • Protein Kinase C