Proteolytic inactivation of tissue factor pathway inhibitor by bacterial omptins

Blood. 2009 Jan 29;113(5):1139-48. doi: 10.1182/blood-2008-05-157180. Epub 2008 Nov 6.

Abstract

The immune response to infection includes activation of the blood clotting system, leading to extravascular fibrin deposition to limit the spread of invasive microorganisms. Some bacteria have evolved mechanisms to counteract this host response. Pla, a member of the omptin family of Gram-negative bacterial proteases, promotes the invasiveness of the plague bacterium, Yersinia pestis, by activating plasminogen to plasmin to digest fibrin. We now show that the endogenous anticoagulant tissue factor pathway inhibitor (TFPI) is also highly sensitive to proteolysis by Pla and its orthologs OmpT in Escherichia coli and PgtE in Salmonella enterica serovar Typhimurium. Using gene deletions, we demonstrate that bacterial inactivation of TFPI requires omptin expression. TFPI inactivation is mediated by proteolysis since Western blot analysis showed that TFPI cleavage correlated with loss of anticoagulant function in clotting assays. Rates of TFPI inactivation were much higher than rates of plasminogen activation, indicating that TFPI is a better substrate for omptins. We hypothesize that TFPI has evolved sensitivity to proteolytic inactivation by bacterial omptins to potentiate procoagulant responses to bacterial infection. This may contribute to the hemostatic imbalance in disseminated intravascular coagulation and other coagulopathies accompanying severe sepsis.

Publication types

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

MeSH terms

  • Bacterial Proteins / genetics
  • Bacterial Proteins / metabolism*
  • Disseminated Intravascular Coagulation / metabolism
  • Disseminated Intravascular Coagulation / microbiology
  • Gene Deletion
  • Gram-Negative Bacteria / genetics
  • Gram-Negative Bacteria / metabolism*
  • Gram-Negative Bacterial Infections / genetics
  • Gram-Negative Bacterial Infections / metabolism*
  • Humans
  • Lipoproteins / genetics
  • Lipoproteins / metabolism*
  • Plasminogen Activators / genetics
  • Plasminogen Activators / metabolism
  • Sepsis / genetics
  • Sepsis / metabolism
  • Sepsis / microbiology
  • Serine Endopeptidases / genetics
  • Serine Endopeptidases / metabolism*

Substances

  • Bacterial Proteins
  • Lipoproteins
  • lipoprotein-associated coagulation inhibitor
  • Plasminogen Activators
  • Serine Endopeptidases
  • omptin outer membrane protease