Long-term estradiol exposure is a direct mitogen for insulin/EGF-primed endometrial cells and drives PTEN loss-induced hyperplasic growth

Am J Pathol. 2013 Jul;183(1):277-87. doi: 10.1016/j.ajpath.2013.03.008. Epub 2013 May 10.

Abstract

Loss of tumor-suppressor PTEN is the most common alteration in endometrial carcinoma. However, the relationship between loss of PTEN, growth factors [eg, insulin/insulin-like growth factor (IGF)-1], epidermal growth factor (EGF), and hyperestrogenism in the development of endometrial carcinoma is still controversial. By using three-dimensional (3D) cultures of PTEN(+/+) and PTEN(+/-) endometrial epithelial cells, we investigated the effects of EGF, insulin/IGF, and estradiol in endometrial cell proliferation. We have previously demonstrated that 3D cultures of endometrial cells require EGF and insulin/IGF to proliferate. Herein, we demonstrate that, in the presence of EGF and insulin/IGF, long-term estradiol treatment directly induces proliferation of 3D cultures. Moreover, we show that the mitogenic effects of estradiol require the presence of insulin/IGF and EGF, because withdrawal of such factors completely abolishes estradiol-induced proliferation. In the presence of EGF and insulin/IGF, PTEN(+/-) and PTEN(+/+) spheroids display a similar rate of proliferation. However, the addition of estradiol causes an exaggerated proliferation of PTEN(+/-) cultures, leading to formation of complex structures, such as those observed in endometrial hyperplasia or carcinoma. In summary, we demonstrate that EGF and insulin/IGF prime endometrial epithelial cells to direct the mitogenic effects of estradiol. Furthermore, PTEN deficiency results in enhanced responsiveness to this combination, leading to the development of hyperplasia of endometrial cells in culture.

Publication types

  • Evaluation Study
  • Research Support, Non-U.S. Gov't

MeSH terms

  • Animals
  • Biomarkers / metabolism
  • Blotting, Western
  • Cell Proliferation / drug effects
  • Endometrial Hyperplasia / chemically induced*
  • Endometrial Hyperplasia / metabolism
  • Endometrial Hyperplasia / pathology
  • Endometrium / drug effects*
  • Endometrium / metabolism
  • Endometrium / pathology
  • Epidermal Growth Factor / metabolism*
  • Epithelial Cells / drug effects
  • Epithelial Cells / metabolism
  • Epithelial Cells / pathology
  • Estradiol / adverse effects*
  • Estrogens / adverse effects
  • Female
  • Fluorescent Antibody Technique
  • Insulin / metabolism*
  • Insulin-Like Growth Factor I / metabolism
  • Mice
  • Mice, Inbred C57BL
  • Mice, Knockout
  • Mitogens / adverse effects*
  • PTEN Phosphohydrolase / deficiency*
  • Real-Time Polymerase Chain Reaction
  • Reverse Transcriptase Polymerase Chain Reaction
  • Spheroids, Cellular

Substances

  • Biomarkers
  • Estrogens
  • Insulin
  • Mitogens
  • insulin-like growth factor-1, mouse
  • Estradiol
  • Epidermal Growth Factor
  • Insulin-Like Growth Factor I
  • PTEN Phosphohydrolase
  • Pten protein, mouse