Membrane metallo-endopeptidase mediates cellular senescence induced by oncogenic PIK3CAH1047R accompanied with pro-tumorigenic secretome

Int J Cancer. 2019 Aug 1;145(3):817-829. doi: 10.1002/ijc.32153. Epub 2019 Feb 7.

Abstract

The hotspot mutation H1047R in the oncogenic PIK3CA gene is frequently detected in breast cancer and enhances the enzymatic activity of PI3K to activate AKT/mTOR signaling cascade. Aberrant elevated PI3K activation has been reported to promote the tumorigenesis of breast cancer, but the mechanisms underlying are still needed to be elucidated. Here, we found that continuously activating PIK3CAH1047R conferred human mammary epithelial MCF-10A cells to cellular senescence upon serum-starvation. Similarly, breast cancer T47D and HCC1954 cells harboring H1047R mutation were senescent when cells were deprived of serum. PI3K/AKT/mTOR axis but not p53 or RB might be required for the induction of senescence. Notably, membrane metallo-endopeptidase (MME) was identified as a downstream effector of PI3K to mediate the induction of senescence, which might be associated with its glycosylation. Senescent cells elicited a distinct secretome dependent on PI3K and MME. Specifically, IL-6 promoted the proliferation of normal cells and CCL2 induced the M2-like polarization of macrophages, which might create an immunosuppressive microenvironment during the initiation and/or development of breast cancer. This study shed new light on the tumorigenesis induced by hyper-activated PI3K and might provide new clues for the prevention and therapy of breast cancer.

Keywords: PI3Kα; breast cancer; macrophage; membrane metallo-endopeptidase; senescence.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Animals
  • Breast Neoplasms / enzymology*
  • Breast Neoplasms / genetics*
  • Breast Neoplasms / pathology
  • Cell Line, Tumor
  • Cell Proliferation
  • Cellular Senescence / physiology
  • Chemokine CCL2 / metabolism
  • Class I Phosphatidylinositol 3-Kinases / antagonists & inhibitors
  • Class I Phosphatidylinositol 3-Kinases / genetics*
  • Class I Phosphatidylinositol 3-Kinases / metabolism*
  • Epithelial Cells / cytology
  • Epithelial Cells / enzymology
  • Glycosylation
  • Humans
  • Interleukin-6 / metabolism
  • Mammary Glands, Human / cytology
  • Mammary Glands, Human / enzymology
  • Metalloendopeptidases / metabolism*
  • Mice
  • Mice, Inbred BALB C
  • Proto-Oncogene Proteins c-akt / antagonists & inhibitors
  • Proto-Oncogene Proteins c-akt / metabolism
  • TOR Serine-Threonine Kinases / antagonists & inhibitors
  • TOR Serine-Threonine Kinases / metabolism
  • Tumor Suppressor Protein p53 / metabolism

Substances

  • CCL2 protein, human
  • Chemokine CCL2
  • IL6 protein, human
  • Interleukin-6
  • TP53 protein, human
  • Tumor Suppressor Protein p53
  • MTOR protein, human
  • Class I Phosphatidylinositol 3-Kinases
  • PIK3CA protein, human
  • Proto-Oncogene Proteins c-akt
  • TOR Serine-Threonine Kinases
  • Metalloendopeptidases