Fibrin, γ'-fibrinogen, and transclot pressure gradient control hemostatic clot growth during human blood flow over a collagen/tissue factor wound

Arterioscler Thromb Vasc Biol. 2015 Mar;35(3):645-54. doi: 10.1161/ATVBAHA.114.305054. Epub 2015 Jan 22.

Abstract

Objective: Biological and physical factors interact to modulate blood response in a wounded vessel, resulting in a hemostatic clot or an occlusive thrombus. Flow and pressure differential (ΔP) across the wound from the lumen to the extravascular compartment may impact hemostasis and the observed core/shell architecture. We examined physical and biological factors responsible for regulating thrombin-mediated clot growth.

Approach and results: Using factor XIIa-inhibited human whole blood perfused in a microfluidic device over collagen/tissue factor at controlled wall shear rate and ΔP, we found thrombin to be highly localized in the P-selectin(+) core of hemostatic clots. Increasing ΔP from 9 to 29 mm Hg (wall shear rate=400 s(-1)) reduced P-selectin(+) core size and total clot size because of enhanced extravasation of thrombin. Blockade of fibrin polymerization with 5 mmol/L Gly-Pro-Arg-Pro dysregulated hemostasis by enhancing both P-selectin(+) core size and clot size at 400 s(-1) (20 mm Hg). For whole-blood flow (no Gly-Pro-Arg-Pro), the thickness of the P-selectin-negative shell was reduced under arterial conditions (2000 s(-1), 20 mm Hg). Consistent with the antithrombin-1 activity of fibrin implicated with Gly-Pro-Arg-Pro, anti-γ'-fibrinogen antibody enhanced core-localized thrombin, core size, and overall clot size, especially at venous (100 s(-1)) but not arterial wall shear rates (2000 s(-1)). Pathological shear (15 000 s(-1)) and Gly-Pro-Arg-Pro synergized to exacerbate clot growth.

Conclusions: Hemostatic clotting was dependent on core-localized thrombin that (1) triggered platelet P-selectin display and (2) was highly regulated by fibrin and the transclot ΔP. Also, γ'-fibrinogen had a role in venous but not arterial conditions.

Keywords: fibrin; hemodynamics; hemostasis; thrombin.

Publication types

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

MeSH terms

  • Animals
  • Arteries / metabolism
  • Arteries / pathology
  • Arteries / physiopathology
  • Blood Flow Velocity
  • Collagen Type I / blood*
  • Disease Models, Animal
  • Fibrin / metabolism*
  • Fibrinogens, Abnormal / metabolism*
  • Hemostasis*
  • Humans
  • Lab-On-A-Chip Devices
  • Male
  • Mechanotransduction, Cellular
  • Mice
  • P-Selectin / blood
  • Polymerization
  • Pressure
  • Regional Blood Flow
  • Stress, Mechanical
  • Thrombin / metabolism*
  • Thromboplastin / metabolism*
  • Thrombosis / blood*
  • Thrombosis / pathology
  • Thrombosis / physiopathology
  • Time Factors
  • Vascular System Injuries / blood*
  • Vascular System Injuries / pathology
  • Vascular System Injuries / physiopathology
  • Veins / metabolism
  • Veins / pathology
  • Veins / physiopathology

Substances

  • Collagen Type I
  • Fibrinogens, Abnormal
  • P-Selectin
  • SELP protein, human
  • fibrinogen gamma'
  • Fibrin
  • Thromboplastin
  • Thrombin