Perivascular cell-derived extracellular vesicles stimulate colorectal cancer revascularization after withdrawal of antiangiogenic drugs

J Extracell Vesicles. 2021 May;10(7):e12096. doi: 10.1002/jev2.12096. Epub 2021 May 21.

Abstract

Antiangiogenic tyrosine kinase inhibitors (AA-TKIs) have become a promising therapeutic strategy for colorectal cancer (CRC). In clinical practice, a significant proportion of cancer patients temporarily discontinue AA-TKI treatment due to recurrent toxicities, economic burden or acquired resistance. However, AA-TKI therapy withdrawal-induced tumour revascularization frequently occurs, hampering the clinical application of AA-TKIs. Here, this study demonstrates that tumour perivascular cells mediate tumour revascularization after withdrawal of AA-TKI therapy. Pharmacological inhibition and genetic ablation of perivascular cells largely attenuate the rebound effect of CRC vascularization in the AA-TKI cessation experimental settings. Mechanistically, tumour perivascular cell-derived extracellular vehicles (TPC-EVs) contain Gas6 that instigates the recruitment of endothelial progenitor cells (EPCs) for tumour revascularization via activating the Axl pathway. Gas6 silence and an Axl inhibitor markedly inhibit tumour revascularization by impairing EPC recruitment. Consequently, combination therapy of regorafenib with the Axl inhibitor improves overall survival in mice metastatic CRC model by inhibiting tumour growth. Together, these data shed new mechanistic insights into perivascular cells in off-AA-TKI-induced tumour revascularization and indicate that blocking the Axl signalling may provide an attractive anticancer approach for sustaining long-lasting angiostatic effects to improve the therapeutic outcomes of antiangiogenic drugs in CRC.

Keywords: antiangiogenic therapy; endothelial progenitor cell; extracellular vesicle; perivascular cell; tyrosine kinase inhibitor.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Angiogenesis Inhibitors / pharmacology
  • Animals
  • Carcinoma, Non-Small-Cell Lung / drug therapy
  • Cell Line, Tumor
  • China
  • Colorectal Neoplasms / drug therapy*
  • Colorectal Neoplasms / metabolism
  • Drug Resistance, Neoplasm / drug effects
  • ErbB Receptors / antagonists & inhibitors
  • Extracellular Vesicles / metabolism
  • Extracellular Vesicles / physiology*
  • Female
  • Humans
  • Lung Neoplasms / drug therapy
  • Male
  • Mice
  • Mice, Inbred BALB C
  • Mice, Nude
  • Mutation / drug effects
  • Neovascularization, Pathologic / drug therapy
  • Neovascularization, Pathologic / metabolism*
  • Neovascularization, Pathologic / prevention & control
  • Perivascular Epithelioid Cell Neoplasms / drug therapy
  • Perivascular Epithelioid Cell Neoplasms / metabolism
  • Perivascular Epithelioid Cell Neoplasms / physiopathology
  • Protein Kinase Inhibitors / pharmacology
  • Proto-Oncogene Proteins / antagonists & inhibitors
  • Receptor Protein-Tyrosine Kinases / antagonists & inhibitors
  • Signal Transduction / drug effects
  • Substance Withdrawal Syndrome / physiopathology
  • Xenograft Model Antitumor Assays

Substances

  • Angiogenesis Inhibitors
  • Protein Kinase Inhibitors
  • Proto-Oncogene Proteins
  • ErbB Receptors
  • Receptor Protein-Tyrosine Kinases