Targeting acid sphingomyelinase with anti-angiogenic chemotherapy

Cell Signal. 2017 Jan:29:52-61. doi: 10.1016/j.cellsig.2016.09.010. Epub 2016 Oct 1.

Abstract

Despite great promise, combining anti-angiogenic and conventional anti-cancer drugs has produced limited therapeutic benefit in clinical trials, presumably because mechanisms of anti-angiogenic tissue response remain only partially understood. Here we define a new paradigm, in which anti-angiogenic drugs can be used to chemosensitize tumors by targeting the endothelial acid sphingomyelinase (ASMase) signal transduction pathway. We demonstrate that paclitaxel and etoposide, but not cisplatin, confer ASMase-mediated endothelial injury within minutes. This rapid reaction is required for human HCT-116 colon cancer xenograft complete response and growth delay. Whereas VEGF inhibits ASMase, anti-VEGFR2 antibodies de-repress ASMase, enhancing endothelial apoptosis and drug-induced tumor response in asmase+/+, but not in asmase-/-, hosts. Such chemosensitization occurs only if the anti-angiogenic drug is delivered 1-2h before chemotherapy, but at no other time prior to or post chemotherapy. Our studies suggest that precisely-timed administration of anti-angiogenic drugs in combination with ASMase-targeting anti-cancer drugs is likely to optimize anti-tumor effects of systemic chemotherapy. This strategy warrants evaluation in future clinical trials.

Keywords: Acid sphingomyelinase; Anti-angiogenic drugs; Ceramide-rich macrodomains; Chemotherapy; Endothelial cells.

Publication types

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

MeSH terms

  • Angiogenesis Inhibitors / pharmacology*
  • Animals
  • Antineoplastic Agents / pharmacology*
  • Apoptosis / drug effects
  • Cattle
  • Ceramides / metabolism
  • Drug Delivery Systems
  • Endothelium / metabolism
  • Enzyme Activation / drug effects
  • HCT116 Cells
  • Humans
  • Male
  • Mice, Inbred C57BL
  • Molecular Targeted Therapy*
  • Paclitaxel / pharmacology
  • Sphingomyelin Phosphodiesterase / antagonists & inhibitors*
  • Sphingomyelin Phosphodiesterase / metabolism

Substances

  • Angiogenesis Inhibitors
  • Antineoplastic Agents
  • Ceramides
  • Sphingomyelin Phosphodiesterase
  • Paclitaxel