TAGLN mediated stiffness-regulated ovarian cancer progression via RhoA/ROCK pathway

J Exp Clin Cancer Res. 2021 Sep 19;40(1):292. doi: 10.1186/s13046-021-02091-6.

Abstract

Background: Ovarian cancer (OC) progression is an unmet medical challenge. Since omental metastases were palpated harder than their primary counterparts during cytoreductive surgery of patients with epithelial ovarian cancer (EOC), we were inspired to investigate OC progression from the perspective of biomechanics.

Methods: Atomic Force Microscope (AFM) was used to measure the Young's modulus of tissues. The collagen-coated polyacrylamide hydrogel (PA gel) system was prepared to mimic the soft and stiff substrates in vitro. The effect of TAGLN was evaluated both in vitro and in vivo using transwell assay, immunofluorescence, western blot analysis and immunohistochemistry.

Results: We quantitatively confirmed that omental metastases were stiffer and more abundant in desmoplasia compared with paired primary tumors, and further demonstrated that matrix stiffness could notably regulate OC progression. Remarkably, TAGLN, encoding an actin cross-linking/gelling protein, was identified as a potent mechanosensitive gene that could form a regulation loop with Src activation reacting to environmental stiffness, thus mediating stiffness-regulated OC progression through regulating RhoA/ROCK pathway.

Conclusions: These data demonstrate that targeting extra-cellular matrix (ECM) stiffness could probably hamper OC progression, and of note, targeting TAGLN might provide promising clinical therapeutic value for OC therapy.

Keywords: Ovarian cancer; Progression; RhoA/ROCK; TAGLN; Tissue mechanics.

MeSH terms

  • Animals
  • Cell Line, Tumor
  • Disease Models, Animal
  • Disease Progression
  • Extracellular Matrix / metabolism
  • Female
  • Fluorescent Antibody Technique
  • Gene Expression
  • Gene Expression Profiling
  • Humans
  • Mice
  • Microfilament Proteins / genetics
  • Microfilament Proteins / metabolism*
  • Models, Biological
  • Muscle Proteins / genetics
  • Muscle Proteins / metabolism*
  • Neoplasm Metastasis
  • Ovarian Neoplasms / etiology
  • Ovarian Neoplasms / metabolism*
  • Ovarian Neoplasms / mortality
  • Ovarian Neoplasms / pathology*
  • Prognosis
  • Signal Transduction*
  • Tumor Microenvironment
  • rho-Associated Kinases / metabolism*
  • rhoA GTP-Binding Protein / metabolism*
  • src-Family Kinases / genetics
  • src-Family Kinases / metabolism

Substances

  • Microfilament Proteins
  • Muscle Proteins
  • transgelin
  • RHOA protein, human
  • src-Family Kinases
  • rho-Associated Kinases
  • rhoA GTP-Binding Protein