Systematic dissection of coordinated stromal remodeling identifies Sox10+ glial cells as a therapeutic target in myelofibrosis

Cell Stem Cell. 2023 Jun 1;30(6):832-850.e6. doi: 10.1016/j.stem.2023.05.002.

Abstract

Remodeling of the tissue niche is often evident in diseases, yet, the stromal alterations and their contribution to pathogenesis are poorly characterized. Bone marrow fibrosis is a maladaptive feature of primary myelofibrosis (PMF). We performed lineage tracing and found that most collagen-expressing myofibroblasts were derived from leptin-receptor-positive (LepR+) mesenchymal cells, whereas a minority were from Gli1-lineage cells. Deletion of Gli1 did not impact PMF. Unbiased single-cell RNA sequencing (scRNA-seq) confirmed that virtually all myofibroblasts originated from LepR-lineage cells, with reduced expression of hematopoietic niche factors and increased expression of fibrogenic factors. Concurrently, endothelial cells upregulated arteriolar-signature genes. Pericytes and Sox10+ glial cells expanded drastically with heightened cell-cell signaling, suggesting important functional roles in PMF. Chemical or genetic ablation of bone marrow glial cells ameliorated fibrosis and improved other pathology in PMF. Thus, PMF involves complex remodeling of the bone marrow microenvironment, and glial cells represent a promising therapeutic target.

Keywords: Gli1; LepR; glial cells; hematopoietic stem cells; lineage tracing; mesenchymal stromal cells; microenvironmental niche; myelofibrosis; single-cell RNA sequencing.

Publication types

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

MeSH terms

  • Bone Marrow / metabolism
  • Endothelial Cells / metabolism
  • Humans
  • Neuroglia / metabolism
  • Primary Myelofibrosis* / drug therapy
  • SOXE Transcription Factors / genetics
  • SOXE Transcription Factors / metabolism
  • Zinc Finger Protein GLI1 / metabolism

Substances

  • Zinc Finger Protein GLI1
  • SOX10 protein, human
  • SOXE Transcription Factors