Endometrial stromal beta-catenin is required for steroid-dependent mesenchymal-epithelial cross talk and decidualization

Reprod Biol Endocrinol. 2012 Sep 7:10:75. doi: 10.1186/1477-7827-10-75.

Abstract

Background: Beta-catenin is part of a protein complex associated with adherens junctions. When allowed to accumulate to sufficient levels in its dephosphorylated form, beta-catenin serves as a transcriptional co-activator associated with a number of signaling pathways, including steroid hormone signaling pathways.

Methods: To investigate the role of beta-catenin in progesterone (P₄) signaling and female reproductive physiology, conditional ablation of Ctnnb1 from the endometrial mesenchymal (i.e. stromal and myometrial), but not epithelial, compartment was accomplished using the Amhr2-Cre mice. Experiments were conducted to assess the ability of mutant female mice to undergo pregnancy and pseudopregnancy by or through oil-induced decidualization. The ability of uteri from mutant female mice to respond to estrogen (E₂) and P₄ was also determined.

Results: Conditional deletion of Ctnnb1 from the mesenchymal compartment of the uterus resulted in infertility stemming, in part, from complete failure of the uterus to decidualize. E₂-stimulated epithelial cell mitosis and edematization were not altered in mutant uteri indicating that the mesenchyme is capable of responding to E₂. However, exposure of ovariectomized mutant female mice to a combined E₂ and P₄ hormone regimen consistent with early pregnancy revealed that mesenchymal beta-catenin is essential for indirectly opposing E₂-induced epithelial proliferation by P₄ and in some mice resulted in development of endometrial metaplasia. Lastly, beta-catenin is also required for the induced expression of genes that are known to play a fundamental role in decidualization such as Ihh, Ptch1, Gli1 and Muc1

Conclusions: Three salient points derive from these studies. First, the findings demonstrate a mechanistic linkage between the P₄ and beta-catenin signaling pathways. Second, they highlight an under appreciated role for the mesenchymal compartment in indirectly mediating P₄ signaling to the epithelium, a process that intimately involves mesenchymal beta-catenin. Third, the technical feasibility of deleting genes in the mesenchymal compartment of the uterus in an effort to understand decidualization and post-natal interactions with the overlying epithelium has been demonstrated. It is concluded that beta-catenin plays an integral role in selective P₄-directed epithelial-mesenchymal communication in both the estrous cycling and gravid uterus.

Publication types

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

MeSH terms

  • Animals
  • Cell Transdifferentiation*
  • Decidua / cytology
  • Decidua / pathology
  • Decidua / physiology*
  • Endometrium / cytology
  • Endometrium / metabolism*
  • Endometrium / pathology
  • Epithelial Cells / cytology
  • Epithelial Cells / metabolism*
  • Epithelial Cells / pathology
  • Epithelial-Mesenchymal Transition
  • Estrogens / metabolism
  • Estrous Cycle / metabolism
  • Female
  • Mice
  • Mice, Inbred ICR
  • Mice, Mutant Strains
  • Mice, Transgenic
  • Myometrium / cytology
  • Myometrium / metabolism*
  • Myometrium / pathology
  • Placentation
  • Pregnancy
  • Progesterone / metabolism
  • Pseudopregnancy / metabolism
  • Pseudopregnancy / pathology
  • Random Allocation
  • Signal Transduction
  • Stromal Cells / cytology
  • Stromal Cells / metabolism*
  • Stromal Cells / pathology
  • beta Catenin / genetics
  • beta Catenin / metabolism*

Substances

  • CTNNB1 protein, human
  • Estrogens
  • beta Catenin
  • Progesterone