Regulation of intercellular biomolecule transfer-driven tumor angiogenesis and responses to anticancer therapies

J Clin Invest. 2021 May 17;131(10):e144225. doi: 10.1172/JCI144225.

Abstract

Intercellular biomolecule transfer (ICBT) between malignant and benign cells is a major driver of tumor growth, resistance to anticancer therapies, and therapy-triggered metastatic disease. Here we characterized cholesterol 25-hydroxylase (CH25H) as a key genetic suppressor of ICBT between malignant and endothelial cells (ECs) and of ICBT-driven angiopoietin-2-dependent activation of ECs, stimulation of intratumoral angiogenesis, and tumor growth. Human CH25H was downregulated in the ECs from patients with colorectal cancer and the low levels of stromal CH25H were associated with a poor disease outcome. Knockout of endothelial CH25H stimulated angiogenesis and tumor growth in mice. Pharmacologic inhibition of ICBT by reserpine compensated for CH25H loss, elicited angiostatic effects (alone or combined with sunitinib), augmented the therapeutic effect of radio-/chemotherapy, and prevented metastatic disease induced by these regimens. We propose inhibiting ICBT to improve the overall efficacy of anticancer therapies and limit their prometastatic side effects.

Keywords: Colorectal cancer; Endothelial cells; Oncology; Vascular Biology.

Publication types

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

MeSH terms

  • Animals
  • Endothelial Cells / enzymology
  • Gene Knockdown Techniques
  • HCT116 Cells
  • Humans
  • Mice
  • Mice, Knockout
  • Neoplasm Metastasis
  • Neoplasm Proteins* / antagonists & inhibitors
  • Neoplasm Proteins* / genetics
  • Neoplasm Proteins* / metabolism
  • Neoplasms, Experimental / drug therapy*
  • Neoplasms, Experimental / enzymology
  • Neoplasms, Experimental / genetics
  • Neovascularization, Pathologic / drug therapy*
  • Neovascularization, Pathologic / enzymology
  • Neovascularization, Pathologic / genetics
  • Reserpine / pharmacology*
  • Steroid Hydroxylases* / antagonists & inhibitors
  • Steroid Hydroxylases* / genetics
  • Steroid Hydroxylases* / metabolism
  • Sunitinib / pharmacology*

Substances

  • Neoplasm Proteins
  • Reserpine
  • Steroid Hydroxylases
  • cholesterol 25-hydroxylase
  • Sunitinib