Engineering kunitz domain 1 (KD1) of human tissue factor pathway inhibitor-2 to selectively inhibit fibrinolysis: properties of KD1-L17R variant

J Biol Chem. 2011 Feb 11;286(6):4329-40. doi: 10.1074/jbc.M110.191163. Epub 2010 Nov 29.

Abstract

Tissue factor pathway inhibitor-2 (TFPI-2) inhibits factor XIa, plasma kallikrein, and factor VIIa/tissue factor; accordingly, it has been proposed for use as an anticoagulant. Full-length TFPI-2 or its isolated first Kunitz domain (KD1) also inhibits plasmin; therefore, it has been proposed for use as an antifibrinolytic agent. However, the anticoagulant properties of TFPI-2 or KD1 would diminish its antifibrinolytic function. In this study, structure-based investigations and analysis of the serine protease profiles revealed that coagulation enzymes prefer a hydrophobic residue at the P2' position in their substrates/inhibitors, whereas plasmin prefers a positively charged arginine residue at the corresponding position in its substrates/inhibitors. Based upon this observation, we changed the P2' residue Leu-17 in KD1 to Arg (KD1-L17R) and compared its inhibitory properties with wild-type KD1 (KD1-WT). Both WT and KD1-L17R were expressed in Escherichia coli, folded, and purified to homogeneity. N-terminal sequences and mass spectra confirmed proper expression of KD1-WT and KD1-L17R. Compared with KD1-WT, the KD1-L17R did not inhibit factor XIa, plasma kallikrein, or factor VIIa/tissue factor. Furthermore, KD1-L17R inhibited plasmin with ∼6-fold increased affinity and effectively prevented plasma clot fibrinolysis induced by tissue plasminogen activator. Similarly, in a mouse liver laceration bleeding model, KD1-L17R was ∼8-fold more effective than KD1-WT in preventing blood loss. Importantly, in this bleeding model, KD1-L17R was equally or more effective than aprotinin or tranexamic acid, which have been used as antifibrinolytic agents to prevent blood loss during major surgery/trauma. Furthermore, as compared with aprotinin, renal toxicity was not observed with KD1-L17R.

Publication types

  • Comparative Study
  • Research Support, N.I.H., Extramural

MeSH terms

  • Amino Acid Substitution*
  • Animals
  • Antifibrinolytic Agents* / chemistry
  • Antifibrinolytic Agents* / pharmacology
  • Aprotinin / chemistry
  • Aprotinin / pharmacology
  • Blood Coagulation Factors / chemistry
  • Disease Models, Animal
  • Escherichia coli
  • Fibrinolysis / drug effects*
  • Glycoproteins* / chemistry
  • Glycoproteins* / genetics
  • Glycoproteins* / pharmacology
  • Hemorrhage / drug therapy*
  • Humans
  • Mice
  • Mutation, Missense
  • Protein Folding*
  • Protein Structure, Tertiary
  • Recombinant Proteins / chemistry
  • Recombinant Proteins / genetics
  • Recombinant Proteins / pharmacology
  • Structure-Activity Relationship
  • Tranexamic Acid / chemistry
  • Tranexamic Acid / pharmacology

Substances

  • Antifibrinolytic Agents
  • Blood Coagulation Factors
  • Glycoproteins
  • Recombinant Proteins
  • tissue-factor-pathway inhibitor 2
  • Tranexamic Acid
  • Aprotinin