Ovarian cancer-derived lysophosphatidic acid stimulates secretion of VEGF and stromal cell-derived factor-1 alpha from human mesenchymal stem cells

Exp Mol Med. 2010 Apr 30;42(4):280-93. doi: 10.3858/emm.2010.42.4.027.

Abstract

Lysophosphatidic acid (LPA) stimulates growth and invasion of ovarian cancer cells and tumor angiogenesis. Cancer-derived LPA induces differentiation of human adipose tissue-derived mesenchymal stem cells (hASCs) to alpha-smooth muscle actin (alpha-SMA)-positive cancer-associated fibroblasts. Presently, we explored whether cancer-derived LPA regulates secretion of pro-angiogenic factors from hASCs. Conditioned medium (CM) from the OVCAR-3 and SKOV3 ovarian cancer cell lines stimulated secretion angiogenic factors such as stromal-derived factor-1 alpha (SDF-1 alpha) and VEGF from hASCs. Pretreatment with the LPA receptor inhibitor Ki16425 or short hairpin RNA lentiviral silencing of the LPA((1)) receptor abrogated the cancer CM-stimulated expression of alpha-SMA, SDF-1, and VEGF from hASCs. LPA induced expression of myocardin and myocardin-related transcription factor-A, transcription factors involved in smooth muscle differentiation, in hASCs. siRNA-mediated depletion of endogenous myocardin and MRTF-A abrogated the expression of alpha-SMA, but not SDF-1 and VEGF. LPA activated RhoA in hASCs and pretreatment with the Rho kinase inhibitor Y27632 completely abrogated the LPA-induced expression of alpha-SMA, SDF-1, and VEGF in hASCs. Moreover, LPA-induced alpha-SMA expression was abrogated by treatment with the ERK inhibitor U0126 or the phosphoinositide-3-kinase inhibitor LY294002, but not the PLC inhibitor U73122. LPA-induced VEGF secretion was inhibited by LY294002, whereas LPA-induced SDF-1 secretion was markedly attenuated by U0126, U73122, and LY294002. These results suggest that cancer-secreted LPA induces differentiation of hASCs to cancer-associated fibroblasts through multiple signaling pathways involving Rho kinase, ERK, PLC, and phosphoinositide-3-kinase.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Actins / metabolism
  • Adipose Tissue / cytology
  • Cell Line, Tumor
  • Chemokine CXCL12 / metabolism*
  • Culture Media, Conditioned
  • Endothelial Cells / drug effects
  • Endothelial Cells / metabolism
  • Female
  • Humans
  • Lysophospholipids / pharmacology*
  • Mesenchymal Stem Cells / drug effects*
  • Mesenchymal Stem Cells / metabolism*
  • Microphthalmia-Associated Transcription Factor / metabolism
  • Neovascularization, Physiologic / drug effects
  • Ovarian Neoplasms / enzymology
  • Ovarian Neoplasms / metabolism*
  • Ovarian Neoplasms / pathology
  • Paracrine Communication / drug effects
  • Receptors, Lysophosphatidic Acid / metabolism
  • Signal Transduction / drug effects
  • Vascular Endothelial Growth Factors / metabolism*
  • rho-Associated Kinases / metabolism
  • rhoA GTP-Binding Protein / metabolism

Substances

  • Actins
  • Chemokine CXCL12
  • Culture Media, Conditioned
  • Lysophospholipids
  • MITF protein, human
  • Microphthalmia-Associated Transcription Factor
  • Receptors, Lysophosphatidic Acid
  • Vascular Endothelial Growth Factors
  • rho-Associated Kinases
  • rhoA GTP-Binding Protein
  • lysophosphatidic acid