Abstract
A hypercoagulable state, chronic inflammation, and increased risk of venous thrombosis and stroke are prominent features in patients with sickle cell disease (SCD). Coagulation factor XII (FXII) triggers activation of the contact system that is known to be involved in both thrombosis and inflammation, but not in physiological hemostasis. Therefore, we investigated whether FXII contributes to the prothrombotic and inflammatory complications associated with SCD. We found that when compared with healthy controls, patients with SCD exhibit increased circulating biomarkers of FXII activation that are associated with increased activation of the contact pathway. We also found that FXII, but not tissue factor, contributes to enhanced thrombin generation and systemic inflammation observed in sickle cell mice challenged with tumor necrosis factor α. In addition, FXII inhibition significantly reduced experimental venous thrombosis, congestion, and microvascular stasis in a mouse model of SCD. Moreover, inhibition of FXII attenuated brain damage and reduced neutrophil adhesion to the brain vasculature of sickle cell mice after ischemia/reperfusion induced by transient middle cerebral artery occlusion. Finally, we found higher FXII, urokinase plasminogen activator receptor, and αMβ2 integrin expression in neutrophils of patients with SCD compared with healthy controls. Our data indicate that targeting FXII effectively reduces experimental thromboinflammation and vascular complications in a mouse model of SCD, suggesting that FXII inhibition may provide a safe approach for interference with inflammation, thrombotic complications, and vaso-occlusion in patients with SCD.
Original language | English (US) |
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Pages (from-to) | 1871-1883 |
Number of pages | 13 |
Journal | Blood |
Volume | 141 |
Issue number | 15 |
DOIs | |
State | Published - Apr 13 2023 |
Bibliographical note
Funding Information:This work was funded in part by the National Institutes of Health (NIH), National Heart, Lung, and Blood Institute (NHLBI) grants R01s HL142604 (R.P.), HL157441 (R.P., N.S.K.) and U01 HL117659 (R.P., N.S.K.). E.M.S. is supported by NIH, NHLBI grant R01 HL 155193 . M.K. was supported by NIH, NHLBI grant R00HL144817 and University of Alabama at Birmingham AMC21 grant MULTIPI6724. G.M.V. and J.D.B. were supported by research funding from NIH, NHLBI grant 5R01 HL114567 . T.R. acknowledges the Deutsche Forschungsgemeinschaft (DFG, German Research Foundation) grants P6 - KFO306, 80750187 - SFB841 and 470698011 -SFB877. D.G. was supported by NIH, NHLBI grant R35 HL140025 . F.E.G. was supported by the Royal Society Wolfson Foundation (RSWF∖R3∖183001). A.G. and M.W. were supported by NIH, NHLBI grant R44 HL126235 . This work was supported by NIH, NHLBI grant R01 HL137695 (E.X.S.), Merit Review Awards BX003851 (E.X.S.), and the Oscar D. Ratnoff Endowed Professorship (E.X.S.).
Funding Information:
The authors thank Daniel Kirchhofer and Genentech, Inc for the anti-TF antibody 1H1. This work was funded in part by the National Institutes of Health (NIH), National Heart, Lung, and Blood Institute (NHLBI) grants R01s HL142604 (R.P.), HL157441 (R.P. N.S.K.) and U01 HL117659 (R.P. N.S.K.). E.M.S. is supported by NIH, NHLBI grant R01 HL 155193. M.K. was supported by NIH, NHLBI grant R00HL144817 and University of Alabama at Birmingham AMC21 grant MULTIPI6724. G.M.V. and J.D.B. were supported by research funding from NIH, NHLBI grant 5R01 HL114567. T.R. acknowledges the Deutsche Forschungsgemeinschaft (DFG, German Research Foundation) grants P6 - KFO306, 80750187 - SFB841 and 470698011 -SFB877. D.G. was supported by NIH, NHLBI grant R35 HL140025. F.E.G. was supported by the Royal Society Wolfson Foundation (RSWF∖R3∖183001). A.G. and M.W. were supported by NIH, NHLBI grant R44 HL126235. This work was supported by NIH, NHLBI grant R01 HL137695 (E.X.S.), Merit Review Awards BX003851 (E.X.S.), and the Oscar D. Ratnoff Endowed Professorship (E.X.S.). The contents are solely the responsibility of the authors and do not necessarily represent the official views of the National Institutes of Health, the US Department of Veterans Affairs, or the US Government. Contribution: E.M.S. designed the research, performed experiments, analyzed data, and wrote the manuscript; M.W.H. M.M. C.A. A.I. F.T. N.R. S.V. D.B. K.L.B. M.P. C.C. M.K. and B.C. performed experiments and analyzed data; M.W. T.R. and A.G. provided valuable reagents; D.G. performed experiments and provided valuable reagents; N.S.K. and G.M.V. provided critical guidance on experimental procedures and revised the manuscript; F.E.G. J.D.B. and E.X.S. performed experiments, analyzed data, and critically reviewed the manuscript; and R.P. designed the research, analyzed data, and wrote the manuscript.
Publisher Copyright:
© 2023
PubMed: MeSH publication types
- Journal Article
- Research Support, N.I.H., Extramural