Differential contribution of FXa and thrombin to vascular inflammation in a mouse model of sickle cell disease

Blood

Volumn 123, Issue 11, 2014, Pages 1747-1756

  Sparkenbaugh, Erica M ^a   Chantrathammachart, Pichika ^a,b   Mickelson, Jacqueline ^a   Van Ryn, Joanne ^c   Hebbel, Robert P ^d   Monroe, Dougald M ^a   Mackman, Nigel ^a   Key, Nigel S ^a   Pawlinski, Rafal ^a  

^a UNIVERSITY OF NORTH CAROLINA SCHOOL OF MEDICINE   (United States)

^b MAHIDOL UNIVERSITY   (Thailand)

^c BOEHRINGER INGELHEIM PHARMA GMBH AND CO KG   (Germany)

^d UNIVERSITY OF MINNESOTA MEDICAL SCHOOL   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BLOOD CLOTTING FACTOR 10A; DABIGATRAN; INTERLEUKIN 6; PLACEBO; PROTEINASE; PROTEINASE ACTIVATED RECEPTOR 1; PROTEINASE ACTIVATED RECEPTOR 2; RIVAROXABAN; THROMBIN; VASCULAR CELL ADHESION MOLECULE 1;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; ATTENUATION; BLOOD CLOTTING; BLOOD SAMPLING; BONE MARROW TRANSPLANTATION; CONTROLLED STUDY; DRUG EFFICACY; HEMOSTASIS; INFLAMMATION; LUNG; MALE; MOUSE; NEUTROPHIL CHEMOTAXIS; NONHUMAN; OPTIMAL DRUG DOSE; PRIORITY JOURNAL; PROTEIN BLOOD LEVEL; PROTEIN EXPRESSION; SICKLE CELL ANEMIA; VASCULITIS;

ANEMIA, SICKLE CELL; ANIMALS; ANTICOAGULANTS; ANTITHROMBINS; BENZIMIDAZOLES; BETA-ALANINE; BONE MARROW TRANSPLANTATION; DISEASE MODELS, ANIMAL; FACTOR XA; FEMALE; IMMUNOENZYME TECHNIQUES; INFLAMMATION; MALE; MICE; MICE, INBRED C57BL; MICE, KNOCKOUT; MORPHOLINES; RECEPTOR, PAR-1; RECEPTOR, PAR-2; THIOPHENES; THROMBIN; VASCULAR DISEASES;

EID: 84897481862     PISSN: 00064971     EISSN: 15280020     Source Type: Journal    
DOI: 10.1182/blood-2013-08-523936     Document Type: Article

References (54)

1. Steinberg MH. Management of sickle cell disease. N Engl J Med. 1999;340(13):1021-1030. (Pubitemid 29157635)
2. Frenette PS. Sickle cell vaso-occlusion: multistep and multicellular paradigm. Curr Opin Hematol. 2002;9(2):101-106. (Pubitemid 34171484)
3. Hebbel RP. Reconstructing sickle cell disease: a data-based analysis of the "hyperhemolysis paradigm" for pulmonary hypertension from the perspective of evidence-based medicine. Am J Hematol. 2011;86(2):123-154.
4. Salvaggio JE, Arnold CA, Banov CH. Long-term anti-coagulation in sickle-cell disease. A clinical study. N Engl J Med. 1963;269:182-186.
5. Wolters HJ, ten Cate H, Thomas LL, et al. Low-intensity oral anticoagulation in sickle-cell disease reverses the prethrombotic state: promises for treatment? Br J Haematol. 1995;90(3):715-717.
6. Chaplin H Jr, Monroe MC, Malecek AC, Morgan LK, Michael J, Murphy WA. Preliminary trial of minidose heparin prophylaxis for painful sickle cell crises. East Afr Med J. 1989;66(9):574-584.
7. Ataga KI, Key NS. Hypercoagulability in sickle cell disease: new approaches to an old problem. Hematology (Am Soc Hematol Educ Program). 2007;91-96.
8. Qari MH, Aljaouni SK, Alardawi MS, et al. Reduction of painful vaso-occlusive crisis of sickle cell anaemia by tinzaparin in a double-blind randomized trial. Thromb Haemost. 2007;98(2):392-396. (Pubitemid 47250243)
9. Solovey A, Kollander R, Shet A, et al. Endothelial cell expression of tissue factor in sickle mice is augmented by hypoxia/reoxygenation and inhibited by lovastatin. Blood. 2004;104(3):840-846. (Pubitemid 38970583)
10. Solovey A, Gui L, Key NS, Hebbel RP. Tissue factor expression by endothelial cells in sickle cell anemia. J Clin Invest. 1998;101(9):1899-1904. (Pubitemid 28226109)
11. Chantrathammachart P, Mackman N, Sparkenbaugh E, et al. Tissue factor promotes activation of coagulation and inflammation in a mouse model of sickle cell disease. Blood. 2012;120(3):636-646.
12. Gavins FN, Russell J, Senchenkova EL, et al. Mechanisms of enhanced thrombus formation in cerebral microvessels of mice expressing hemoglobin-S. Blood. 2011;117(15):4125-4133.
13. Coughlin SR. Thrombin signalling and protease-activated receptors. Nature. 2000;407(6801):258-264.
14. Riewald M, Kravchenko VV, Petrovan RJ, et al. Gene induction by coagulation factor Xa is mediated by activation of protease-activated receptor 1. Blood. 2001;97(10):3109-3116.
15. Camerer E, Huang W, Coughlin SR. Tissue factor- and factor X-dependent activation of protease-activated receptor 2 by factor VIIa. Proc Natl Acad Sci USA. 2000;97(10):5255-5260. (Pubitemid 30313705)
16. Rao LV, Pendurthi UR. Tissue factor-factor VIIa signaling. Arterioscler Thromb Vasc Biol. 2005;25(1):47-56. (Pubitemid 40054253)
17. Leger AJ, Covic L, Kuliopulos A. Protease-activated receptors in cardiovascular diseases. Circulation. 2006;114(10):1070-1077. (Pubitemid 44358884)
18. Mackman N, Tilley RE, Key NS. Role of the extrinsic pathway of blood coagulation in hemostasis and thrombosis. Arterioscler Thromb Vasc Biol. 2007;27(8):1687-1693. (Pubitemid 47207163)
19. Rothmeier AS, Ruf W. Protease-activated receptor 2 signaling in inflammation. Semin Immunopathol. 2012;34(1):133-149.
20. Pászty C, Brion CM, Manci E, et al. Transgenic knockout mice with exclusively human sickle hemoglobin and sickle cell disease. Science. 1997;278(5339):876-878. (Pubitemid 27467927)
21. Darrow AL, Fung-Leung WP, Ye RD, et al. Biological consequences of thrombin receptor deficiency in mice. Thromb Haemost. 1996;76(6):860-866. (Pubitemid 27013619)
22. Damiano BP, Cheung WM, Santulli RJ, et al. Cardiovascular responses mediated by protease-activated receptor-2 (PAR-2) and thrombin receptor (PAR-1) are distinguished in mice deficient in PAR-2 or PAR-1. J Pharmacol Exp Ther. 1999;288(2):671-678. (Pubitemid 29119680)
23. Stangier J, Rathgen K, Stähle H, Gansser D, Roth W. The pharmacokinetics, pharmacodynamics and tolerability of dabigatran etexilate, a new oral direct thrombin inhibitor, in healthy male subjects. Br J Clin Pharmacol. 2007;64(3):292-303. (Pubitemid 47283865)
24. Whinna HC, Monroe DM. A novel murine hemostasis model: studies on recombinant factor VIIa and NN1731. J Thromb Haemost. 2009;7:PP-MO-379.
25. Iannone R, Luznik L, Engstrom LW, et al. Effects of mixed hematopoietic chimerism in a mouse model of bone marrow transplantation for sickle cell anemia. Blood. 2001;97(12):3960-3965.
26. van Ryn J, Goss A, Hauel N, et al. The discovery of dabigatran etexilate. Front Pharmacol. 2013;4:12.
27. Connolly SJ, Ezekowitz MD, Yusuf S, et al RE-LY Steering Committee and Investigators. Dabigatran versus warfarin in patients with atrial fibrillation. N Engl J Med. 2009;361(12):1139-1151.
28. Turpie AG, Lassen MR, Eriksson BI, et al. Rivaroxaban for the prevention of venous thromboembolism after hip or knee arthroplasty. Pooled analysis of four studies. Thromb Haemost. 2011;105(3):444-453.
29. Kreutz R. Pharmacodynamic and pharmacokinetic basics of rivaroxaban. Fundam Clin Pharmacol. 2012;26(1):27-32.
30. van Ryn J, Stangier J, Haertter S, et al. Dabigatran etexilate - a novel, reversible, oral direct thrombin inhibitor: interpretation of coagulation assays and reversal of anticoagulant activity. Thromb Haemost. 2010;103(6):1116-1127.
31. Kubitza D, Becka M, Voith B, Zuehlsdorf M, Wensing G. Safety, pharmacodynamics, and pharmacokinetics of single doses of BAY 59-7939, an oral, direct factor Xa inhibitor. Clin Pharmacol Ther. 2005;78(4):412-421. (Pubitemid 41393676)
32. Petzelbauer P, Zacharowski PA, Miyazaki Y, et al. The fibrin-derived peptide Bbeta15-42 protects the myocardium against ischemia-reperfusion injury. Nat Med. 2005;11(3):298-304. (Pubitemid 40460558)
33. Ahamed J, Belting M, Ruf W. Regulation of tissue factor-induced signaling by endogenous and recombinant tissue factor pathway inhibitor 1. Blood. 2005;105(6):2384-2391. (Pubitemid 40387035)
34. Vincent L, Vang D, Nguyen J, et al. Mast cell activation contributes to sickle cell pathobiology and pain in mice. Blood. 2013;122(11):1853-1862.
35. Qari MH, Dier U, Mousa SA. Biomarkers of inflammation, growth factor, and coagulation activation in patients with sickle cell disease. Clin Appl Thromb Hemost. 2012;18(2):195-200.
36. Riewald M, Petrovan RJ, Donner A, Mueller BM, Ruf W. Activation of endothelial cell protease activated receptor 1 by the protein C pathway. Science. 2002;296(5574):1880-1882. (Pubitemid 34596276)
37. Riewald M, Ruf W. Protease-activated receptor-1 signaling by activated protein C in cytokine-perturbed endothelial cells is distinct from thrombin signaling. J Biol Chem. 2005;280(20):19808-19814. (Pubitemid 41379506)
38. Esmon CT. Protein C anticoagulant system - anti-inflammatory effects. Semin Immunopathol. 2012;34(1):127-132.
39. Bouwens EA, Stavenuiter F, Mosnier LO. Mechanisms of anticoagulant and cytoprotective actions of the protein C pathway. J Thromb Haemost. 2013;11(suppl 1):242-253.
40. Hebbel RP, Osarogiagbon R, Kaul D. The endothelial biology of sickle cell disease: inflammation and a chronic vasculopathy. Microcirculation. 2004;11(2):129-151. (Pubitemid 39619075)
41. Mehari A, Gladwin MT, Tian X, Machado RF, Kato GJ. Mortality in adults with sickle cell disease and pulmonary hypertension. JAMA. 2012;307(12):1254- 1256.
42. Mehari A, Alam S, Tian X, et al. Hemodynamic predictors of mortality in adults with sickle cell disease. Am J Respir Crit Care Med. 2013;187(8):840-847.
43. Bunn HF, Nathan DG, Dover GJ, et al. Pulmonary hypertension and nitric oxide depletion in sickle cell disease. Blood. 2010;116(5):687-692.
44. Adedeji MO, Cespedes J, Allen K, Subramony C, Hughson MD. Pulmonary thrombotic arteriopathy in patients with sickle cell disease. Arch Pathol Lab Med. 2001;125(11):1436-1441. (Pubitemid 33070181)
45. Francis RB. Large-vessel occlusion in sickle cell disease: pathogenesis, clinical consequences, and therapeutic implications. Med Hypotheses. 1991;35(2):88-95.
46. Ataga KI, Moore CG, Hillery CA, et al. Coagulation activation and inflammation in sickle cell disease-associated pulmonary hypertension. Haematologica. 2008;93(1):20-26. (Pubitemid 351156147)
47. Crosswhite P, Sun Z. Nitric oxide, oxidative stress and inflammation in pulmonary arterial hypertension. J Hypertens. 2010;28(2):201-212.
48. Delbeck M, Nickel KF, Perzborn E, et al. A role for coagulation factor Xa in experimental pulmonary arterial hypertension. Cardiovasc Res. 2011;92(1):159-168.
49. Kwapiszewska G, Markart P, Dahal BK, et al. PAR-2 inhibition reverses experimental pulmonary hypertension. Circ Res. 2012;110(9):1179-1191.
50. Savale L, Tu L, Rideau D, et al. Impact of interleukin-6 on hypoxia-induced pulmonary hypertension and lung inflammation in mice. Respir Res. 2009;10:6.
51. Furuya Y, Satoh T, Kuwana M. Interleukin-6 as a potential therapeutic target for pulmonary arterial hypertension. Int J Rheumatol. 2010;2010:720305.
52. Bogdanov VY, Balasubramanian V, Hathcock J, Vele O, Lieb M, Nemerson Y. Alternatively spliced human tissue factor: a circulating, soluble, thrombogenic protein. Nat Med. 2003;9(4):458-462. (Pubitemid 36460081)
53. Srinivasan R, Ozhegov E, van den Berg YW, et al. Splice variants of tissue factor promote monocyte-endothelial interactions by triggering the expression of cell adhesion molecules via integrin-mediated signaling. J Thromb Haemost. 2011;9(10):2087-2096.
54. Setty BN, Key NS, Rao AK, et al. Tissue factor-positive monocytes in children with sickle cell disease: correlation with biomarkers of haemolysis. Br J Haematol. 2012;157(3):370-380.