Attenuation of TGF-β signaling suppresses premature senescence in a p21-dependent manner and promotes oncogenic Ras-mediated metastatic transformation in human mammary epithelial cells

Mol Biol Cell. 2012 Apr;23(8):1569-81. doi: 10.1091/mbc.E11-10-0849. Epub 2012 Feb 22.

Abstract

The molecular mechanisms that drive triple-negative, basal-like breast cancer progression are elusive. Few molecular targets have been identified for the prevention or treatment of this disease. Here we developed a series of isogenic basal-like human mammary epithelial cells (HMECs) with altered transforming growth factor-β (TGF-β) sensitivity and different malignancy, resembling a full spectrum of basal-like breast carcinogenesis, and determined the molecular mechanisms that contribute to oncogene-induced transformation of basal-like HMECs when TGF-β signaling is attenuated. We found that expression of a dominant-negative type II receptor (DNRII) of TGF-β abrogated autocrine TGF-β signaling in telomerase-immortalized HMECs and suppressed H-Ras-V12-induced senescence-like growth arrest (SLGA). Furthermore, coexpression of DNRII and H-Ras-V12 rendered HMECs highly tumorigenic and metastatic in vivo in comparison with H-Ras-V12-transformed HMECs that spontaneously escaped H-Ras-V12-induced SLGA. Microarray analysis revealed that p21 was the major player mediating Ras-induced SLGA, and attenuated or loss of p21 expression contributed to the escape from SLGA when autocrine TGF-β signaling was blocked in HMECs. Furthermore, knockdown of p21 also suppressed H-Ras-V12-induced SLGA. Our results identify that autocrine TGF-β signaling is an integral part of the cellular anti-transformation network by suppressing the expression of a host of genes, including p21-regulated genes, that mediate oncogene-induced transformation in basal-like breast cancer.

Publication types

  • Research Support, N.I.H., Extramural

MeSH terms

  • Animals
  • Breast Neoplasms / pathology*
  • Cell Line
  • Cell Transformation, Neoplastic*
  • Cellular Senescence*
  • Epithelial Cells / metabolism
  • Epithelial Cells / pathology*
  • ErbB Receptors / deficiency
  • Female
  • Humans
  • Mammary Glands, Human / metabolism
  • Mammary Glands, Human / pathology*
  • Mice
  • Mice, Nude
  • Oncogene Protein p21(ras) / genetics
  • Oncogene Protein p21(ras) / metabolism*
  • RNA Interference
  • RNA, Small Interfering
  • Receptors, Estrogen / deficiency
  • Receptors, Progesterone / deficiency
  • Signal Transduction*
  • Transforming Growth Factor beta / metabolism*
  • ras Proteins / genetics
  • ras Proteins / metabolism*

Substances

  • RNA, Small Interfering
  • Receptors, Estrogen
  • Receptors, Progesterone
  • Transforming Growth Factor beta
  • ErbB Receptors
  • Oncogene Protein p21(ras)
  • ras Proteins