Cathepsin L-induced galectin-1 may act as a proangiogenic factor in the metastasis of high-grade serous carcinoma

J Transl Med. 2019 Jul 3;17(1):216. doi: 10.1186/s12967-019-1963-7.

Abstract

Background: New treatment options for metastasised high-grade serous carcinoma (HGSC) are urgently needed. HGSC frequently metastasises to the omentum, inducing angiogenesis in the local omental microvasculature to facilitate tumour growth. We previously showed that HGSC-secreted cathepsin L (CathL) induces pro-angiogenic changes in disease relevant human omental microvascular endothelial cells (HOMECs), suggesting a role in tumour angiogenesis. Here we investigate whether CathL acts by inducing local production of the carbohydrate-binding protein galectin-1 (Gal1), which has been reported to be involved in tumourigenesis in other tumours.

Methods: HOMECs were used for all experiments. Gal1 mRNA and protein levels were measured by RT-PCR and ELISA respectively. Gal1-induced cell proliferation was assessed using WST-1 assay, migration using a transwell assay and in vivo Gal1 expression by immunohistochemistry.

Results: CathL transcriptionally regulated HOMEC production and secretion of Gal1 via activation of NFκB (significantly inhibited by sulfasalazine). Gal1 significantly enhanced HOMEC migration (p < 0.001) and proliferation (p < 0.001), suggesting an autocrine action. The latter was significantly reduced by the MEK/ERK1/2 inhibitors U0126 and PD98059 suggesting downstream activation of this pathway. Immunohistochemical analysis of omenta from HGSC patients with or without metastatic disease demonstrated a positive correlation between Gal1 expression and number of microvessels (r = 0.8702, p < 0.001), and area of vessels (r = 0.7283, p < 0.001), supporting a proangiogenic role for Gal1 in omental metastases.

Conclusion: HOMEC Gal1 transcription and release in response to CathL secreted from metastasising HGSC acts in an autocrine manner on the local microvasculature to induce pro-angiogenic changes, highlighting a potential new therapeutic target.

Keywords: Angiogenesis; Galectin-1; High-grade serous carcinoma; Metastasis; Signalling pathways.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Adult
  • Cathepsin L / metabolism*
  • Cell Movement
  • Cell Proliferation / genetics
  • Endothelial Cells / pathology
  • Extracellular Signal-Regulated MAP Kinases / metabolism
  • Female
  • Galectin 1 / genetics*
  • Galectin 1 / metabolism
  • Gene Expression Regulation, Neoplastic
  • Humans
  • Microvessels / pathology
  • Middle Aged
  • NF-kappa B / metabolism
  • Neoplasm Grading
  • Neoplasm Metastasis
  • Neoplasms, Cystic, Mucinous, and Serous / genetics*
  • Neoplasms, Cystic, Mucinous, and Serous / pathology*
  • Neovascularization, Pathologic / genetics*
  • Omentum / blood supply
  • Omentum / pathology
  • Peritoneal Neoplasms / blood supply*
  • Peritoneal Neoplasms / genetics
  • Peritoneal Neoplasms / pathology*
  • Proto-Oncogene Proteins c-akt / metabolism
  • RNA, Messenger / genetics
  • RNA, Messenger / metabolism
  • Up-Regulation / genetics

Substances

  • Galectin 1
  • NF-kappa B
  • RNA, Messenger
  • Proto-Oncogene Proteins c-akt
  • Extracellular Signal-Regulated MAP Kinases
  • Cathepsin L