Heparin's anti-inflammatory effects require glucosamine 6-O-sulfation and are mediated by blockade of L- and P-selectins

J Clin Invest. 2002 Jul;110(1):127-36. doi: 10.1172/JCI14996.

Abstract

Heparin has been used clinically as an anticoagulant and antithrombotic agent for over 60 years. Here we show that the potent anti-inflammatory property of heparin results primarily from blockade of P-selectin and L-selectin. Unfractionated heparin and chemically modified analogs were tested as inhibitors of selectin binding to immobilized sialyl Lewis(X) and of cell adhesion to immobilized selectins or thrombin-activated endothelial cells. Compared with unfractionated heparin, the modified heparinoids had inhibitory activity in this general order: over-O-sulfated heparin > heparin > 2-O,3-O-desulfated > or = N-desulfated/N-acetylated heparin > or = carboxyl-reduced heparin > or= N-,2-O,3-O-desulfated heparin >> 6-O-desulfated heparin. The heparinoids also showed similar differences in their ability to inhibit thioglycollate-induced peritonitis and oxazolone-induced delayed-type hypersensitivity. Mice deficient in P- or L-selectins showed impaired inflammation, which could be further reduced by heparin. However, heparin had no additional effect in mice deficient in both P- and L-selectins. We conclude that (a) heparin's anti-inflammatory effects are mainly mediated by blocking P- and L-selectin-initiated cell adhesion; (b) the sulfate groups at C6 on the glucosamine residues play a critical role in selectin inhibition; and (c) some non-anticoagulant forms of heparin retain anti-inflammatory activity. Such analogs may prove useful as therapeutically effective inhibitors of inflammation.

Publication types

  • Research Support, U.S. Gov't, P.H.S.

MeSH terms

  • Animals
  • Anti-Inflammatory Agents, Non-Steroidal / pharmacology*
  • Cell Adhesion / drug effects
  • Cell Adhesion / physiology
  • Dermatitis, Allergic Contact / drug therapy
  • Disease Models, Animal
  • Glucosamine / chemistry*
  • Heparin / analogs & derivatives
  • Heparin / chemistry*
  • Heparin / pharmacology*
  • Humans
  • Inflammation / drug therapy
  • L-Selectin / genetics
  • L-Selectin / physiology*
  • Mice
  • Mice, Inbred C57BL
  • Mice, Knockout
  • Molecular Structure
  • Oligosaccharides / metabolism
  • P-Selectin / genetics
  • P-Selectin / physiology*
  • Peritonitis / drug therapy
  • Sialyl Lewis X Antigen
  • Sulfates / chemistry
  • U937 Cells

Substances

  • Anti-Inflammatory Agents, Non-Steroidal
  • Oligosaccharides
  • P-Selectin
  • Sialyl Lewis X Antigen
  • Sulfates
  • L-Selectin
  • Heparin
  • Glucosamine