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Mechanical stress can cause epithelial cells to lose their normal polarity, a phenomenon observed in cancers. This study shows that disrupting mechanical balance can lead to "apical-out" eversion, suggesting a new mechanism for cancer development.

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Area of Science:

  • Cell Biology
  • Biophysics
  • Cancer Biology

Background:

  • Epithelial cells normally polarize with apical proteins facing lumens and basal proteins facing the extracellular matrix.
  • Aberrant cell polarity, including apical-out polarity, is a hallmark of human cancers.
  • Altered protein trafficking and tissue-level unfolding are potential causes of aberrant polarity.

Purpose of the Study:

  • To investigate whether mechanical perturbations can induce apical-out polarity (eversion) in epithelial acini.
  • To explore the role of RhoA-mediated actomyosin tension in this process.
  • To determine if mechanical homeostasis loss contributes to cancer-associated polarity changes.

Main Methods:

  • Induction of acinar eversion via RhoA activation (direct or indirect) in normal and tumor epithelial cells.
  • Utilizing various methods to activate RhoA, including blocking β1-integrins, disrupting the LINC complex, Ras activation, and Rac1 inhibition.
  • Employing laser ablation to induce eversion in untreated acini.
  • Analyzing cell surface curvature and phosphorylated myosin levels.
  • Developing a vertex-based mathematical model to simulate cell-cell tension and surface energy.

Main Results:

  • Acinar eversion was robustly induced by RhoA activation through multiple pathways.
  • Laser ablation of acini also triggered eversion, highlighting mechanical disruption's role.
  • Analysis revealed higher apical curvature and lower apical phosphorylated myosin compared to basal surfaces.
  • Mathematical modeling indicated a fivefold greater basal cell surface tension than apical surface tension.
  • The difference in surface energy between apical and basal surfaces was identified as the driving force for eversion.

Conclusions:

  • Perturbing mechanical homeostasis, particularly through RhoA activation, can cause apical-out eversion in epithelial acini.
  • This mechanical mechanism offers an alternative pathway for altered cell polarity in cancer.
  • Loss of mechanical homeostasis may be a significant factor in the development of apical-out polarity states in human cancers.