An essential role of CBL and CBL-B ubiquitin ligases in mammary stem cell maintenance

Development. 2017 Mar 15;144(6):1072-1086. doi: 10.1242/dev.138164. Epub 2017 Jan 18.

Abstract

The ubiquitin ligases CBL and CBL-B are negative regulators of tyrosine kinase signaling with established roles in the immune system. However, their physiological roles in epithelial tissues are unknown. Here, we used MMTV-Cre-mediated Cbl gene deletion on a Cbl-b null background, as well as a tamoxifen-inducible mammary stem cell (MaSC)-specific Cbl and Cbl-b double knockout (Cbl/Cbl-b DKO) using Lgr5-EGFP-IRES-CreERT2, to demonstrate a mammary epithelial cell-autonomous requirement of CBL and CBL-B in the maintenance of MaSCs. Using a newly engineered tamoxifen-inducible Cbl and Cbl-b deletion model with a dual fluorescent reporter (Cblflox/flox; Cbl-bflox/flox; Rosa26-CreERT; mT/mG), we show that Cbl/Cbl-b DKO in mammary organoids leads to hyperactivation of AKT-mTOR signaling with depletion of MaSCs. Chemical inhibition of AKT or mTOR rescued MaSCs from Cbl/Cbl-b DKO-induced depletion. Our studies reveal a novel, cell-autonomous requirement of CBL and CBL-B in epithelial stem cell maintenance during organ development and remodeling through modulation of mTOR signaling.

Keywords: Basal cells; CBLB; Casitas B-lineage lymphoma; Lgr5; Luminal cells; Mammary gland development; Mammary stem cells; Mouse; mTOR signaling.

MeSH terms

  • Adaptor Proteins, Signal Transducing / metabolism*
  • Animals
  • Cell Self Renewal / drug effects
  • Cell Separation
  • Epithelial Cells / cytology
  • Epithelial Cells / metabolism
  • Female
  • Gene Deletion
  • Integrases / metabolism
  • Mammary Glands, Animal / cytology*
  • Mammary Glands, Animal / growth & development
  • Mammary Tumor Virus, Mouse / metabolism
  • Mice
  • Mice, Knockout
  • Organoids / cytology
  • Proto-Oncogene Proteins c-akt / metabolism
  • Proto-Oncogene Proteins c-cbl / metabolism*
  • Receptors, G-Protein-Coupled / metabolism
  • Signal Transduction
  • Stem Cells / cytology*
  • Stem Cells / metabolism
  • TOR Serine-Threonine Kinases / metabolism
  • Tamoxifen / pharmacology

Substances

  • Adaptor Proteins, Signal Transducing
  • Cblb protein, mouse
  • Lgr5 protein, mouse
  • Receptors, G-Protein-Coupled
  • Tamoxifen
  • Proto-Oncogene Proteins c-cbl
  • Proto-Oncogene Proteins c-akt
  • TOR Serine-Threonine Kinases
  • Cre recombinase
  • Integrases