By increasing the affinity of heparin for fibrin, Zn(2+) promotes the formation of a ternary heparin-thrombin-fibrin complex that protects thrombin from inhibition by antithrombin

Biochemistry. 2012 Oct 9;51(40):7964-73. doi: 10.1021/bi301046b. Epub 2012 Sep 28.

Abstract

Heparin binds fibrin and, by bridging thrombin onto fibrin, promotes the formation of a ternary heparin-thrombin-fibrin complex that protects thrombin from inhibition by antithrombin. Because thrombin binds γ(A)/γ'-fibrin, a variant with an extended γ-chain, with higher affinity than the bulk γ(A)/γ(A)-fibrin, γ(A)/γ'-fibrin affords bound thrombin more protection from inhibition by antithrombin-heparin. We examined the effect of Zn(2+) on heparin-thrombin-fibrin complex formation because Zn(2+) modulates heparin-protein interactions. Zn(2+) increased the affinity of heparin for γ(A)/γ(A)- and γ(A)/γ'-fibrin by 4.3- and 3.7-fold, respectively, but had no effect on the affinity of thrombin for either form of fibrin. In contrast, in the presence of heparin, Zn(2+) increased the affinity of thrombin for γ(A)/γ(A)-fibrin 4-fold (from a K(d) value of 0.8 to 0.2 μM) and slowed the rate of thrombin dissociation from γ(A)/γ(A)-fibrin clots. These findings suggest that Zn(2+) enhances the formation of ternary heparin-thrombin-fibrin complexes with γ(A)/γ(A)-fibrin but does not influence the already high affinity interaction of thrombin with γ(A)/γ'-fibrin. Consistent with this concept, in the presence of Zn(2+), γ(A)/γ(A)-fibrin protected thrombin from inhibition by antithrombin-heparin to a similar extent as γ(A)/γ'-fibrin. Therefore, by enhancing the binding of heparin to fibrin, physiological concentrations of Zn(2+) render fibrin-bound thrombin more protected from inhibition by antithrombin. Because fibrin-bound thrombin can trigger thrombus expansion, these findings help to explain why recurrent thrombosis can occur despite heparin treatment.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Antithrombins / metabolism*
  • Blood Coagulation
  • Fibrin / chemistry
  • Fibrin / metabolism*
  • Heparin / chemistry
  • Heparin / metabolism*
  • Humans
  • Models, Molecular
  • Plasma / chemistry
  • Protein Binding
  • Protein Conformation
  • Protein Stability
  • Thrombin / antagonists & inhibitors*
  • Thrombin / chemistry
  • Thrombin / metabolism*
  • Time Factors
  • Zinc / chemistry
  • Zinc / metabolism*

Substances

  • Antithrombins
  • Fibrin
  • Heparin
  • Thrombin
  • Zinc