Inhibition of Sphingosine Phosphate Receptor 1 Signaling Enhances the Efficacy of VEGF Receptor Inhibition

Mol Cancer Ther. 2019 Apr;18(4):856-867. doi: 10.1158/1535-7163.MCT-18-0548. Epub 2019 Feb 20.

Abstract

Inhibition of VEGFR signaling is an effective treatment for renal cell carcinoma, but resistance continues to be a major problem. Recently, the sphingosine phosphate (S1P) signaling pathway has been implicated in tumor growth, angiogenesis, and resistance to antiangiogenic therapy. S1P is a bioactive lipid that serves an essential role in developmental and pathologic angiogenesis via activation of the S1P receptor 1 (S1P1). S1P1 signaling counteracts VEGF signaling and is required for vascular stabilization. We used in vivo and in vitro angiogenesis models including a postnatal retinal angiogenesis model and a renal cell carcinoma murine tumor model to test whether simultaneous inhibition of S1P1 and VEGF leads to improved angiogenic inhibition. Here, we show that inhibition of S1P signaling reduces the endothelial cell barrier and leads to excessive angiogenic sprouting. Simultaneous inhibition of S1P and VEGF signaling further disrupts the tumor vascular beds, decreases tumor volume, and increases tumor cell death compared with monotherapies. These studies suggest that inhibition of angiogenesis at two stages of the multistep process may maximize the effects of antiangiogenic therapy. Together, these data suggest that combination of S1P1 and VEGFR-targeted therapy may be a useful therapeutic strategy for the treatment of renal cell carcinoma and other tumor types.

Publication types

  • Research Support, N.I.H., Extramural

MeSH terms

  • Angiogenesis Inhibitors / pharmacology
  • Animals
  • Antibodies, Monoclonal / pharmacology
  • Carcinoma, Renal Cell / blood supply
  • Carcinoma, Renal Cell / drug therapy*
  • Carcinoma, Renal Cell / metabolism*
  • Carcinoma, Renal Cell / pathology
  • Cell Line, Tumor
  • Drug Therapy, Combination
  • Endothelial Cells / drug effects
  • Endothelial Cells / metabolism
  • Female
  • Humans
  • Kidney Neoplasms / blood supply
  • Kidney Neoplasms / drug therapy*
  • Kidney Neoplasms / metabolism*
  • Kidney Neoplasms / pathology
  • Lysophospholipids / antagonists & inhibitors
  • Male
  • Mice
  • Mice, Inbred C57BL
  • Mice, Nude
  • Neovascularization, Pathologic / drug therapy
  • Sphingosine / analogs & derivatives
  • Sphingosine / antagonists & inhibitors
  • Sphingosine-1-Phosphate Receptors / antagonists & inhibitors*
  • Sunitinib / pharmacology
  • Treatment Outcome
  • Tumor Burden / drug effects
  • Vascular Endothelial Growth Factor A / pharmacology
  • Vascular Endothelial Growth Factor Receptor-2 / antagonists & inhibitors*
  • Xenograft Model Antitumor Assays

Substances

  • Angiogenesis Inhibitors
  • Antibodies, Monoclonal
  • DC101 monoclonal antibody
  • Lysophospholipids
  • S1pr1 protein, mouse
  • Sphingosine-1-Phosphate Receptors
  • Vascular Endothelial Growth Factor A
  • vascular endothelial growth factor A, mouse
  • sphingosine 1-phosphate
  • Kdr protein, mouse
  • Vascular Endothelial Growth Factor Receptor-2
  • Sphingosine
  • Sunitinib