Efficacy of 2-halogen substituted D-glucose analogs in blocking glycolysis and killing "hypoxic tumor cells"

Cancer Chemother Pharmacol. 2006 Dec;58(6):725-34. doi: 10.1007/s00280-006-0207-8. Epub 2006 Mar 23.

Abstract

Purpose: Since 2-deoxy-D-glucose (2-DG) is currently in phase I clinical trials to selectively target slow-growing hypoxic tumor cells, 2-halogenated D-glucose analogs were synthesized for improved activity. Given the fact that 2-DG competes with D-glucose for binding to hexokinase, in silico modeling of molecular interactions between hexokinase I and these new analogs was used to determine whether binding energies correlate with biological effects, i.e. inhibition of glycolysis and subsequent toxicity in hypoxic tumor cells.

Methods and results: Using a QSAR-like approach along with a flexible docking strategy, it was determined that the binding affinities of the analogs to hexokinase I decrease as a function of increasing halogen size as follows: 2-fluoro-2-deoxy-D-glucose (2-FG) > 2-chloro-2-deoxy-D-glucose (2-CG) > 2-bromo-2-deoxy-D-glucose (2-BG). Furthermore, D-glucose was found to have the highest affinity followed by 2-FG and 2-DG, respectively. Similarly, flow cytometry and trypan blue exclusion assays showed that the efficacy of the halogenated analogs in preferentially inhibiting growth and killing hypoxic vs. aerobic cells increases as a function of their relative binding affinities. These results correlate with the inhibition of glycolysis as measured by lactate inhibition, i.e. ID50 1 mM for 2-FG, 6 mM for 2-CG and > 6 mM for 2-BG. Moreover, 2-FG was found to be more potent than 2-DG for both glycolytic inhibition and cytotoxicity.

Conclusions: Overall, our in vitro results suggest that 2-FG is more potent than 2-DG in killing hypoxic tumor cells, and therefore may be more clinically effective when combined with standard chemotherapeutic protocols.

Publication types

  • Research Support, N.I.H., Extramural
  • Research Support, Non-U.S. Gov't

MeSH terms

  • Cell Hypoxia
  • Cell Line, Tumor
  • Cell Proliferation / drug effects*
  • Cell Survival / drug effects
  • Deoxyglucose / analogs & derivatives
  • Deoxyglucose / chemistry
  • Deoxyglucose / pharmacology*
  • Drug Design
  • Fluorodeoxyglucose F18 / chemistry
  • Fluorodeoxyglucose F18 / pharmacology
  • Glucose-6-Phosphate / analogs & derivatives
  • Glucose-6-Phosphate / chemistry
  • Glucose-6-Phosphate / metabolism
  • Glycolysis / drug effects*
  • Halogens / chemistry*
  • Hexokinase / chemistry
  • Hexokinase / metabolism
  • Humans
  • Lactic Acid / chemistry
  • Lactic Acid / metabolism
  • Models, Molecular
  • Quantitative Structure-Activity Relationship
  • Thermodynamics

Substances

  • Halogens
  • Fluorodeoxyglucose F18
  • 2-chloro-2-deoxyglucose
  • Lactic Acid
  • 2-deoxyglucose-6-phosphate
  • 2-fluoro-2-deoxyglucose-6-phosphate
  • Glucose-6-Phosphate
  • Deoxyglucose
  • HK1 protein, human
  • Hexokinase