Mammary molecular portraits reveal lineage-specific features and progenitor cell vulnerabilities

J Cell Biol. 2018 Aug 6;217(8):2951-2974. doi: 10.1083/jcb.201804042. Epub 2018 Jun 19.

Abstract

The mammary epithelium depends on specific lineages and their stem and progenitor function to accommodate hormone-triggered physiological demands in the adult female. Perturbations of these lineages underpin breast cancer risk, yet our understanding of normal mammary cell composition is incomplete. Here, we build a multimodal resource for the adult gland through comprehensive profiling of primary cell epigenomes, transcriptomes, and proteomes. We define systems-level relationships between chromatin-DNA-RNA-protein states, identify lineage-specific DNA methylation of transcription factor binding sites, and pinpoint proteins underlying progesterone responsiveness. Comparative proteomics of estrogen and progesterone receptor-positive and -negative cell populations, extensive target validation, and drug testing lead to discovery of stem and progenitor cell vulnerabilities. Top epigenetic drugs exert cytostatic effects; prevent adult mammary cell expansion, clonogenicity, and mammopoiesis; and deplete stem cell frequency. Select drugs also abrogate human breast progenitor cell activity in normal and high-risk patient samples. This integrative computational and functional study provides fundamental insight into mammary lineage and stem cell biology.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Animals
  • Breast Neoplasms / genetics
  • Breast Neoplasms / metabolism*
  • Breast Neoplasms / pathology*
  • Cell Line, Tumor
  • Cell Lineage
  • DNA Methylation
  • DNA, Neoplasm / metabolism
  • Epigenesis, Genetic / drug effects
  • Epigenomics
  • Humans
  • Mice
  • Mice, Transgenic
  • Neoplastic Stem Cells / drug effects
  • Neoplastic Stem Cells / metabolism
  • Neoplastic Stem Cells / pathology
  • Progesterone / pharmacology
  • Proteome
  • RNA, Neoplasm / metabolism
  • Risk Factors
  • Transcriptome
  • Tumor Suppressor Protein p53 / genetics
  • Tumor Suppressor Protein p53 / metabolism
  • Up-Regulation

Substances

  • DNA, Neoplasm
  • Proteome
  • RNA, Neoplasm
  • Trp53 protein, mouse
  • Tumor Suppressor Protein p53
  • Progesterone