Regenerative potential of prostate luminal cells revealed by single-cell analysis

Science. 2020 May 1;368(6490):497-505. doi: 10.1126/science.aay0267.

Abstract

Androgen deprivation is the cornerstone of prostate cancer treatment. It results in involution of the normal gland to ~90% of its original size because of the loss of luminal cells. The prostate regenerates when androgen is restored, a process postulated to involve stem cells. Using single-cell RNA sequencing, we identified a rare luminal population in the mouse prostate that expresses stemlike genes (Sca1 + and Psca +) and a large population of differentiated cells (Nkx3.1 +, Pbsn +). In organoids and in mice, both populations contribute equally to prostate regeneration, partly through androgen-driven expression of growth factors (Nrg2, Rspo3) by mesenchymal cells acting in a paracrine fashion on luminal cells. Analysis of human prostate tissue revealed similar differentiated and stemlike luminal subpopulations that likewise acquire enhanced regenerative potential after androgen ablation. We propose that prostate regeneration is driven by nearly all persisting luminal cells, not just by rare stem cells.

Publication types

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

MeSH terms

  • Androgen Antagonists / therapeutic use
  • Androgen-Binding Protein / genetics
  • Androgens / metabolism*
  • Animals
  • Antigens, Neoplasm / genetics
  • Ataxin-1 / genetics
  • Cell Differentiation / genetics
  • GPI-Linked Proteins / genetics
  • Gene Expression
  • Homeodomain Proteins / genetics
  • Humans
  • Male
  • Mesenchymal Stem Cells / physiology
  • Mice
  • Neoplasm Proteins / genetics
  • Nerve Growth Factors / genetics
  • Organ Size
  • Organoids / metabolism
  • Organoids / physiology
  • Prostate / metabolism
  • Prostate / physiology*
  • Prostate / surgery*
  • Prostatic Neoplasms / drug therapy
  • Prostatic Neoplasms / metabolism
  • Prostatic Neoplasms / surgery*
  • Regeneration* / genetics
  • Sequence Analysis, RNA
  • Single-Cell Analysis
  • Thrombospondins / genetics
  • Transcription Factors / genetics

Substances

  • Androgen Antagonists
  • Androgen-Binding Protein
  • Androgens
  • Antigens, Neoplasm
  • Ataxin-1
  • Atxn1 protein, mouse
  • GPI-Linked Proteins
  • Homeodomain Proteins
  • Neoplasm Proteins
  • Nerve Growth Factors
  • Nkx3-1 protein, mouse
  • Nrg2 protein, mouse
  • Psca protein, mouse
  • R-spondin3 protein, mouse
  • Thrombospondins
  • Transcription Factors
  • probasin