XACT Noncoding RNA Competes with XIST in the Control of X Chromosome Activity during Human Early Development

Cell Stem Cell. 2017 Jan 5;20(1):102-111. doi: 10.1016/j.stem.2016.10.014. Epub 2016 Dec 15.

Abstract

Sex chromosome dosage compensation is essential in most metazoans, but the developmental timing and underlying mechanisms vary significantly, even among placental mammals. Here we identify human-specific mechanisms regulating X chromosome activity in early embryonic development. Single-cell RNA sequencing and imaging revealed co-activation and accumulation of the long noncoding RNAs (lncRNAs) XACT and XIST on active X chromosomes in both early human pre-implantation embryos and naive human embryonic stem cells. In these contexts, the XIST RNA adopts an unusual, highly dispersed organization, which may explain why it does not trigger X chromosome inactivation at this stage. Functional studies in transgenic mouse cells show that XACT influences XIST accumulation in cis. Our findings therefore suggest a mechanism involving antagonistic activity of XIST and XACT in controlling X chromosome activity in early human embryos, and they highlight the contribution of rapidly evolving lncRNAs to species-specific developmental mechanisms.

Keywords: XACT; XIST; dosage compensation; human X chromosome inactivation; long noncoding RNA; naive pluripotency; preimplantation development.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Animals
  • Blastocyst / metabolism
  • Chromosomes, Human, X / genetics*
  • Databases as Topic
  • Embryonic Development / genetics*
  • Human Embryonic Stem Cells / metabolism
  • Humans
  • Mice
  • Pluripotent Stem Cells / metabolism
  • RNA, Long Noncoding / genetics*
  • RNA, Long Noncoding / metabolism
  • RNA, Untranslated / genetics*
  • RNA, Untranslated / metabolism
  • Sequence Analysis, RNA
  • Single-Cell Analysis
  • Transgenes

Substances

  • RNA, Long Noncoding
  • RNA, Untranslated
  • XIST non-coding RNA
  • long non-coding RNA XACT, human