The Heparan Sulfate Proteoglycan Syndecan-1 Triggers Breast Cancer Cell-Induced Coagulability by Induced Expression of Tissue Factor

Cells. 2023 Mar 16;12(6):910. doi: 10.3390/cells12060910.

Abstract

Syndecan-1 (Sdc-1) upregulation is associated with poor prognosis in breast cancer. Sdc-1 knockdown results in reduced angiogenesis and the dysregulation of tissue factor (TF) pathway constituents. Here, we evaluate the regulatory mechanisms and functional consequences of the Sdc-1/TF-axis using Sdc-1 knockdown and overexpression approaches in MCF-7 and MDA-MB-231 breast cancer cells. Gene expression was analyzed by means of qPCR. Thrombin generation and cell migration were detected. Cell-cycle progression and apoptosis were investigated using flow cytometry. In MDA-MB-231 cells, IL6, IL8, VEGF, and IGFR-dependent signaling affected TF pathway expression depending on Sdc-1. Notably, Sdc-1 depletion and TF pathway inhibitor (TFPI) synergistically affected PTEN, MAPK, and STAT3 signaling. At the functional level, the antiproliferative and pro-apoptotic effects of TFPI depended on Sdc-1, whereas Sdc-1's modulation of cell motility was not affected by TFPI. Sdc-1 overexpression in MCF-7 and MDA-MB-231 cells led to increased TF expression, inducing a procoagulative phenotype, as indicated by the activation of human platelets and increased thrombin formation. A novel understanding of the functional interplay between Sdc-1 and the TF pathway may be compatible with the classical co-receptor role of Sdc-1 in cytokine signaling. This opens up the possibility of a new functional understanding, with Sdc-1 fostering coagulation and platelet communication as the key to the hematogenous metastatic spread of breast cancer cells.

Keywords: apoptosis; breast cancer; cell cycle; cell motility; heparan sulfate; platelets; signal transduction; syndecan-1; thrombin; tissue factor.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Breast Neoplasms* / metabolism
  • Breast Neoplasms* / pathology
  • Female
  • Humans
  • Signal Transduction
  • Syndecan-1* / metabolism
  • Thrombin / metabolism
  • Thrombin / pharmacology
  • Thromboplastin* / genetics
  • Thromboplastin* / metabolism

Substances

  • Syndecan-1
  • Thrombin
  • Thromboplastin

Grants and funding

This study was funded by DFG Research Grants—GR4743/5-1 (to B.G.) and GO 1392/8-1 (to M.G.), European Union: Marie Skłodowska-Curie Actions (MSCA) project #101086322 HEPINIB (To M.G. and G.B.), and the German Academic Exchange Service (DAAD) German–Egyptian Research Long-Term Scholarship program (GERLS) Grant 91664677 (to N.H.).