Sphingolipid Modulation Activates Proteostasis Programs to Govern Human Hematopoietic Stem Cell Self-Renewal

Cell Stem Cell. 2019 Nov 7;25(5):639-653.e7. doi: 10.1016/j.stem.2019.09.008. Epub 2019 Oct 17.

Abstract

Cellular stress responses serve as crucial decision points balancing persistence or culling of hematopoietic stem cells (HSCs) for lifelong blood production. Although strong stressors cull HSCs, the linkage between stress programs and self-renewal properties that underlie human HSC maintenance remains unknown, particularly at quiescence exit when HSCs must also dynamically shift metabolic state. Here, we demonstrate distinct wiring of the sphingolipidome across the human hematopoietic hierarchy and find that genetic or pharmacologic modulation of the sphingolipid enzyme DEGS1 regulates lineage differentiation. Inhibition of DEGS1 in hematopoietic stem and progenitor cells during the transition from quiescence to cellular activation with N-(4-hydroxyphenyl) retinamide activates coordinated stress pathways that coalesce on endoplasmic reticulum stress and autophagy programs to maintain immunophenotypic and functional HSCs. Thus, our work identifies a linkage between sphingolipid metabolism, proteostatic quality control systems, and HSC self-renewal and provides therapeutic targets for improving HSC-based cellular therapeutics.

Keywords: DEGS1; StemRegenin-1; UM171; autophagy; fenretinide; hematopoietic stem cell; lipidomics; sphingolipid metabolism; umbilical cord blood; unfolded protein response.

Publication types

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

MeSH terms

  • Animals
  • Autophagy / drug effects
  • Autophagy / genetics
  • Cell Differentiation / drug effects
  • Cell Differentiation / genetics
  • Cell Self Renewal / drug effects
  • Cell Self Renewal / genetics*
  • Cell Survival / drug effects
  • Cell Survival / genetics
  • Endoplasmic Reticulum Stress / drug effects
  • Endoplasmic Reticulum Stress / genetics
  • Fatty Acid Desaturases / antagonists & inhibitors*
  • Fatty Acid Desaturases / genetics
  • Fatty Acid Desaturases / metabolism
  • Female
  • Fenretinide / pharmacology*
  • Gene Expression Regulation / genetics
  • Gene Knockdown Techniques
  • Hematopoietic Stem Cells / enzymology
  • Hematopoietic Stem Cells / metabolism*
  • Humans
  • Male
  • Mass Spectrometry
  • Mice
  • Mice, Inbred NOD
  • Proteostasis / drug effects
  • Proteostasis / genetics*
  • RNA, Small Interfering
  • RNA-Seq
  • Single-Cell Analysis
  • Sphingolipids / chemistry
  • Sphingolipids / metabolism*
  • Transplantation, Heterologous

Substances

  • RNA, Small Interfering
  • Sphingolipids
  • Fenretinide
  • Fatty Acid Desaturases
  • DEGS1 protein, human