Combined Single-Cell Profiling of lncRNAs and Functional Screening Reveals that H19 Is Pivotal for Embryonic Hematopoietic Stem Cell Development

Cell Stem Cell. 2019 Feb 7;24(2):285-298.e5. doi: 10.1016/j.stem.2018.11.023. Epub 2019 Jan 10.

Abstract

The generation of hematopoietic stem cells (HSCs) from embryonic endothelial precursors and pre-HSCs is precisely regulated by signaling pathways and transcription factors. Nevertheless, regulatory roles of non-coding RNAs remain unknown. Taking advantage of our ability to capture rare pre-HSCs and HSCs in vivo, we generated a single-cell landscape of long non-coding RNAs (lncRNAs) during HSC development. Combining bioinformatics and functional screening, we identified 6 lncRNAs influencing hematopoiesis in vitro. We further revealed that H19 lncRNA is pivotal for in vivo HSC emergence in aorta-gonads-mesonephros region. Early H19 lncRNA deficiency blocked endothelial-to-hematopoietic transition, which was independent of the H19-derived miR, miR-675. Moreover, H19-deficient pre-HSCs displayed promoter hypermethylation and concomitant downregulation of several master hematopoietic transcription factors, including Runx1 and Spi1. H19 deficiency increased the activity of S-adenosylhomocysteine hydrolase, a regulator of DNA methylation, which partially contributed to the observed hematopoietic defect. Our findings provide a resource for further analysis of lncRNAs in embryonic HSC development.

Keywords: DNA methylation; H19; Runx1; S-adenosylhomocysteine hydrolase; aorta-gonads-mesonephros region; endothelial-to-hematopoietic transition; hematopoietic stem cells; long non-coding RNAs; pre-hematopoietic stem cells; single-cell RNA sequencing.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Animals
  • DNA Methylation / genetics
  • Embryo, Mammalian / cytology*
  • Gene Expression Regulation
  • Genome, Human
  • Hematopoiesis / genetics
  • Hematopoietic Stem Cells / cytology*
  • Hematopoietic Stem Cells / metabolism*
  • Humans
  • Mice, Inbred C57BL
  • Open Reading Frames / genetics
  • Promoter Regions, Genetic / genetics
  • RNA, Long Noncoding / genetics
  • RNA, Long Noncoding / metabolism*
  • RNA, Messenger / genetics
  • RNA, Messenger / metabolism
  • Single-Cell Analysis*
  • Transcription Factors / metabolism

Substances

  • H19 long non-coding RNA
  • RNA, Long Noncoding
  • RNA, Messenger
  • Transcription Factors