Modulating Heparanase Activity: Tuning Sulfation Pattern and Glycosidic Linkage of Oligosaccharides

J Med Chem. 2020 Apr 23;63(8):4227-4255. doi: 10.1021/acs.jmedchem.0c00156. Epub 2020 Apr 7.

Abstract

Heparanase cleaves polymeric heparan sulfate (HS) molecules into smaller oligosaccharides, allowing for release of angiogenic growth factors promoting tumor development and autoreactive immune cells to reach the insulin-producing β cells. Interaction of heparanase with HS chains is regulated by specific substrate sulfation sequences. We have synthesized 11 trisaccharides that are highly tunable in structure and sulfation pattern, allowing us to determine how heparanase recognizes HS substrate and selects a favorable cleavage site. Our study shows that (1) N-SO3- at +1 subsite and 6-O-SO3- at -2 subsite of trisaccharides are critical for heparanase recognition, (2) addition of 2-O-SO3- at the -1 subsite and of 3-O-SO3- to GlcN unit is not advantageous, and (3) the anomeric configuration (α or β) at the reducing end is crucial in controlling heparanase activity. Our study also illustrates that the α-trisaccharide having N- and 6-O-SO3- at -2 and +1 subsites inhibited heparanase and was resistant toward hydrolysis.

Publication types

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

MeSH terms

  • Animals
  • CHO Cells
  • Cricetinae
  • Cricetulus
  • Dose-Response Relationship, Drug
  • Enzyme Activation / drug effects
  • Enzyme Activation / physiology*
  • Glucuronidase / metabolism*
  • Glycosides / chemical synthesis
  • Glycosides / metabolism*
  • Heparin / pharmacology
  • Heparitin Sulfate / antagonists & inhibitors
  • Heparitin Sulfate / metabolism*
  • Humans
  • Mice
  • Molecular Docking Simulation / methods
  • Oligosaccharides / chemical synthesis
  • Oligosaccharides / metabolism*

Substances

  • Glycosides
  • Oligosaccharides
  • Heparin
  • Heparitin Sulfate
  • heparanase
  • Glucuronidase