Soluble endoglin antagonizes Met signaling in spindle carcinoma cells

Carcinogenesis. 2015 Feb;36(2):212-22. doi: 10.1093/carcin/bgu240. Epub 2014 Dec 10.

Abstract

Increased levels of soluble endoglin (Sol-Eng) correlate with poor outcome in human cancer. We have previously shown that shedding of membrane endoglin, and concomitant release of Sol-Eng is a late event in chemical mouse skin carcinogenesis associated with the development of undifferentiated spindle cell carcinomas (SpCCs). In this report, we show that mouse skin SpCCs exhibit a high expression of hepatocyte growth factor (HGF) and an elevated ratio of its active tyrosine kinase receptor Met versus total Met levels. We have evaluated the effect of Sol-Eng in spindle carcinoma cells by transfection of a cDNA encoding most of the endoglin ectodomain or by using purified recombinant Sol-Eng. We found that Sol-Eng inhibited both mitogen-activated protein kinase (MAPK) activity and cell growth in vitro and in vivo. Sol-Eng also blocked MAPK activation by transforming growth factor-β1 (TGF-β1) and impaired both basal and HGF-induced activation of Met and downstream MAPK. Moreover, Sol-Eng strongly reduced basal and HGF-stimulated spindle cell migration and invasion. Both Sol-Eng and full-length endoglin were shown to interact with Met by coimmunoprecipitation experiments. However, full-length endoglin expressed at the plasma membrane of spindle carcinoma cells had no effect on Met signaling activity, and was unable to inhibit HGF-induced cell migration/invasion. These results point to a paradoxical suppressor role for Sol-Eng in carcinogenesis.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • 9,10-Dimethyl-1,2-benzanthracene / pharmacology
  • Animals
  • Antigens, CD / genetics
  • Antigens, CD / metabolism*
  • Carcinogenesis / metabolism*
  • Carcinogenesis / pathology
  • Cell Movement / genetics
  • Cell Proliferation / genetics
  • DNA, Complementary / genetics
  • Endoglin
  • Enzyme Activation
  • Female
  • HEK293 Cells
  • Hepatocyte Growth Factor / biosynthesis*
  • Humans
  • MAP Kinase Signaling System
  • Mice
  • Mice, Nude
  • Mitogen-Activated Protein Kinases / antagonists & inhibitors
  • Prognosis
  • Proto-Oncogene Proteins c-met / antagonists & inhibitors*
  • Receptors, Cell Surface / genetics
  • Receptors, Cell Surface / metabolism*
  • Sarcoma / metabolism*
  • Sarcoma / pathology
  • Skin Neoplasms / metabolism*
  • Skin Neoplasms / pathology
  • Tetradecanoylphorbol Acetate / pharmacology
  • Transfection
  • Transforming Growth Factor beta1 / antagonists & inhibitors
  • Tumor Cells, Cultured

Substances

  • Antigens, CD
  • DNA, Complementary
  • ENG protein, human
  • Endoglin
  • Receptors, Cell Surface
  • Transforming Growth Factor beta1
  • 9,10-Dimethyl-1,2-benzanthracene
  • Hepatocyte Growth Factor
  • Proto-Oncogene Proteins c-met
  • Mitogen-Activated Protein Kinases
  • Tetradecanoylphorbol Acetate