Hexokinase 2-driven glycolysis in pericytes activates their contractility leading to tumor blood vessel abnormalities

Nat Commun. 2021 Oct 14;12(1):6011. doi: 10.1038/s41467-021-26259-y.

Abstract

Defective pericyte-endothelial cell interaction in tumors leads to a chaotic, poorly organized and dysfunctional vasculature. However, the underlying mechanism behind this is poorly studied. Herein, we develop a method that combines magnetic beads and flow cytometry cell sorting to isolate pericytes from tumors and normal adjacent tissues from patients with non-small cell lung cancer (NSCLC) and hepatocellular carcinoma (HCC). Pericytes from tumors show defective blood vessel supporting functions when comparing to those obtained from normal tissues. Mechanistically, combined proteomics and metabolic flux analysis reveals elevated hexokinase 2(HK2)-driven glycolysis in tumor pericytes, which up-regulates their ROCK2-MLC2 mediated contractility leading to impaired blood vessel supporting function. Clinically, high percentage of HK2 positive pericytes in blood vessels correlates with poor patient overall survival in NSCLC and HCC. Administration of a HK2 inhibitor induces pericyte-MLC2 driven tumor vasculature remodeling leading to enhanced drug delivery and efficacy against tumor growth. Overall, these data suggest that glycolysis in tumor pericytes regulates their blood vessel supporting role.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • A549 Cells
  • Animals
  • Blood Vessels / abnormalities*
  • Blood Vessels / metabolism
  • Blood Vessels / pathology
  • Cardiac Myosins / genetics
  • Cardiac Myosins / metabolism
  • Cell Line, Tumor
  • Cell Proliferation / drug effects
  • Endothelial Cells / metabolism
  • Gene Expression Regulation, Neoplastic
  • Glycolysis*
  • Hexokinase / genetics
  • Hexokinase / metabolism*
  • Humans
  • Mice
  • Mice, Inbred C57BL
  • Myosin Light Chains / genetics
  • Myosin Light Chains / metabolism
  • Neoplasms / metabolism
  • Neoplasms, Vascular Tissue / drug therapy
  • Neoplasms, Vascular Tissue / genetics
  • Neoplasms, Vascular Tissue / metabolism*
  • Neoplasms, Vascular Tissue / pathology
  • Pericytes / metabolism*
  • Tumor Microenvironment / physiology
  • Up-Regulation
  • rho-Associated Kinases

Substances

  • Myosin Light Chains
  • myosin light chain 2
  • HK2 protein, human
  • Hexokinase
  • ROCK2 protein, human
  • rho-Associated Kinases
  • Cardiac Myosins