Latent heparanase facilitates VLA-4-mediated melanoma cell binding and emerges as a relevant target of heparin in the interference with metastatic progression

Semin Thromb Hemost. 2015 Mar;41(2):244-54. doi: 10.1055/s-0035-1544229. Epub 2015 Feb 15.

Abstract

Heparanase is an endo-β-glucuronidase that enzymatically cleaves heparan sulfates (HS) and heparan sulfate proteoglycan (HSPG) structures. Heparanase expression levels by tumors were correlated with cell invasion, angiogenic activity, and poor prognosis. Heparanase can also possess pro-tumorigenic effects independent of its enzymatic activity. Using human melanoma MV3 cells, we demonstrate that latent heparanase activates in a tightly temporary-regulated manner the binding function of the integrin very late antigen-4 (VLA-4), an important component in the metastatic spread of melanoma cells. shRNA-mediated knockdown of syndecan-4 (SDC-4) indicated that this proteoglycan is the key element to convey heparanase binding via focal adhesion complex formation, detected by vinculin staining, to an upregulated VLA-4 binding function. This inside-out signaling pathway of VLA-4 involved activated FAK and Akt, but apparently not PKCα/δ. VLA-4, however, appears representative of other integrins which together impact the heparanase/integrin activation axis in tumorigenicity. Biosensor measurements provided an insight as to how heparin can interfere with this activation process. While low-molecular-weight heparin (LMWH) cannot replace heparanase bound to SDC-4, LMWH can compete with SDC-4 binding of heparanase. Since blockade of heparanase by LMWH has functional consequences for reduced VLA-4 binding, latent heparanase appears as a novel, so far unnoticed target of heparin, underlying its antimetastatic activity.

MeSH terms

  • Cell Line, Tumor
  • Drug Delivery Systems*
  • Enzyme Activation / drug effects
  • Enzyme Activation / genetics
  • Gene Knockdown Techniques
  • HEK293 Cells
  • Heparin Lyase / genetics
  • Heparin Lyase / metabolism*
  • Heparin, Low-Molecular-Weight / pharmacology*
  • Humans
  • Integrin alpha4beta1 / genetics
  • Integrin alpha4beta1 / metabolism*
  • Melanoma / drug therapy*
  • Melanoma / genetics
  • Melanoma / metabolism*
  • Melanoma / pathology
  • Neoplasm Metastasis
  • Neoplasm Proteins / genetics
  • Neoplasm Proteins / metabolism*

Substances

  • Heparin, Low-Molecular-Weight
  • Integrin alpha4beta1
  • Neoplasm Proteins
  • Heparin Lyase