Gata-3 negatively regulates the tumor-initiating capacity of mammary luminal progenitor cells and targets the putative tumor suppressor caspase-14

Mol Cell Biol. 2011 Nov;31(22):4609-22. doi: 10.1128/MCB.05766-11. Epub 2011 Sep 19.

Abstract

The transcription factor Gata-3 is a definitive marker of luminal breast cancers and a key regulator of mammary morphogenesis. Here we have explored a role for Gata-3 in tumor initiation and the underlying cellular mechanisms using a mouse model of "luminal-like" cancer. Loss of a single Gata-3 allele markedly accelerated tumor progression in mice carrying the mouse mammary tumor virus promoter-driven polyomavirus middle T antigen (MMTV-PyMT mice), while overexpression of Gata-3 curtailed tumorigenesis. Through the identification of two distinct luminal progenitor cells in the mammary gland, we demonstrate that Gata-3 haplo-insufficiency increases the tumor-initiating capacity of these progenitors but not the stem cell-enriched population. Overexpression of a conditional Gata-3 transgene in the PyMT model promoted cellular differentiation and led to reduced tumor-initiating capacity as well as diminished angiogenesis. Transcript profiling studies identified caspase-14 as a novel downstream target of Gata-3, in keeping with its roles in differentiation and tumorigenesis. A strong association was evident between GATA-3 and caspase-14 expression in preinvasive ductal carcinoma in situ samples, where GATA-3 also displayed prognostic significance. Overall, these studies identify GATA-3 as an important regulator of tumor initiation through its ability to promote the differentiation of committed luminal progenitor cells.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Adult
  • Aged
  • Animals
  • Antigens, Polyomavirus Transforming / genetics
  • Breast Neoplasms / genetics
  • Breast Neoplasms / metabolism*
  • Breast Neoplasms / pathology
  • Carcinoma, Intraductal, Noninfiltrating / genetics
  • Carcinoma, Intraductal, Noninfiltrating / metabolism*
  • Carcinoma, Intraductal, Noninfiltrating / pathology
  • Caspase 14 / biosynthesis
  • Caspase 14 / metabolism*
  • Cell Differentiation
  • Cell Transformation, Neoplastic / genetics
  • Female
  • GATA3 Transcription Factor / biosynthesis
  • GATA3 Transcription Factor / genetics
  • GATA3 Transcription Factor / metabolism*
  • Humans
  • Mammary Glands, Animal / cytology*
  • Mammary Glands, Animal / metabolism
  • Mammary Glands, Human / cytology*
  • Mammary Glands, Human / metabolism
  • Mammary Neoplasms, Experimental / genetics
  • Mammary Neoplasms, Experimental / metabolism*
  • Mammary Neoplasms, Experimental / pathology
  • Mammary Tumor Virus, Mouse / genetics
  • Mice
  • Middle Aged
  • Stem Cells

Substances

  • Antigens, Polyomavirus Transforming
  • GATA3 Transcription Factor
  • Gata3 protein, mouse
  • Caspase 14