MicroRNA-127-3p controls murine hematopoietic stem cell maintenance by limiting differentiation

Haematologica. 2019 Sep;104(9):1744-1755. doi: 10.3324/haematol.2018.198499. Epub 2019 Feb 21.

Abstract

The balance between self-renewal and differentiation is crucial to ensure the homeostasis of the hematopoietic system, and is a hallmark of hematopoietic stem cells. However, the underlying molecular pathways, including the role of micro-RNA, are not completely understood. To assess the contribution of micro-RNA, we performed micro-RNA profiling of hematopoietic stem cells and their immediate downstream progeny multi-potent progenitors from wild-type control and Pbx1-conditional knockout mice, whose stem cells display a profound self-renewal defect. Unsupervised hierarchical cluster analysis separated stem cells from multi-potent progenitors, suggesting that micro-RNA might regulate the first transition step in the adult hematopoietic development. Notably, Pbx1-deficient and wild-type cells clustered separately, linking micro-RNAs to self-renewal impairment. Differential expression analysis of micro-RNA in the physiological stem cell-to-multi-potent progenitor transition and in Pbx1-deficient stem cells compared to control stem cells revealed miR-127-3p as the most differentially expressed. Furthermore, miR-127-3p was strongly stem cell-specific, being quickly down-regulated upon differentiation and not re-expressed further downstream in the bone marrow hematopoietic hierarchy. Inhibition of miR-127-3p function in Lineage-negative cells, achieved through a lentiviral-sponge vector, led to severe stem cell depletion, as assessed with serial transplantation assays. miR-127-3p-sponged stem cells displayed accelerated differentiation, which was uncoupled from proliferation, accounting for the observed stem cell reduction. miR-127-3p overexpression in Lineage-negative cells did not alter stem cell pool size, but gave rise to lymphopenia, likely due to lack of miR-127-3p physiological downregulation beyond the stem cell stage. Thus, tight regulation of miR-127-3p is crucial to preserve the self-renewing stem cell pool and homeostasis of the hematopoietic system.

Publication types

  • Research Support, N.I.H., Extramural
  • Research Support, Non-U.S. Gov't

MeSH terms

  • Animals
  • Cell Differentiation*
  • Cell Lineage / genetics
  • Cluster Analysis
  • Crosses, Genetic
  • Gene Expression Profiling
  • Hematopoiesis
  • Hematopoietic Stem Cells / cytology*
  • Homeostasis
  • Humans
  • K562 Cells
  • Lentivirus / genetics
  • Mice
  • Mice, Knockout
  • MicroRNAs / physiology*
  • Oxidative Stress
  • Pre-B-Cell Leukemia Transcription Factor 1 / metabolism

Substances

  • MicroRNAs
  • Mirn127 microRNA, mouse
  • Pbx1 protein, mouse
  • Pre-B-Cell Leukemia Transcription Factor 1