Oral Bruton tyrosine kinase inhibitors selectively block atherosclerotic plaque-triggered thrombus formation in humans

Blood

Volumn 131, Issue 24, 2018, Pages 2605-2616

  Busygina, Kristina ^a   Jamasbi, Janina ^a   Seiler, Till ^b   Deckmyn, Hans ^c   Weber, Christian ^a,d,e   Brandl, Richard ^f   Lorenz, Reinhard ^a   Siess, Wolfgang ^a,d  

^a LUDWIG MAXIMILIANS UNIVERSITY   (Germany)

^b UNIVERSITY OF MUNICH   (Germany)

^c UNIVERSITY OF LEUVEN   (Belgium)

^d DZHK GERMAN CENTRE FOR CARDIOVASCULAR RESEARCH   (Germany)

^e MAASTRICHT UNIVERSITY   (Netherlands)

^f St Mary's Square Institute for Vascular Surgery and Phlebology   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

ACALABRUTINIB; ARACHIDONIC ACID; COLLAGEN; IBRUTINIB; TIRABRUTINIB; VERY LATE ACTIVATION ANTIGEN 2; VON WILLEBRAND FACTOR; ANTITHROMBOCYTIC AGENT; BENZAMIDE DERIVATIVE; GS-4059; IMIDAZOLE DERIVATIVE; PROTEIN KINASE INHIBITOR; PYRAZINE DERIVATIVE; PYRAZOLE DERIVATIVE; PYRIMIDINE DERIVATIVE;

ADULT; AGED; ARTICLE; ATHEROSCLEROTIC PLAQUE; CANCER PATIENT; CHRONIC LYMPHATIC LEUKEMIA; CONTROLLED STUDY; EX VIVO STUDY; HEMOSTASIS; HUMAN; LOADING DRUG DOSE; MALE; PRIORITY JOURNAL; THROMBOCYTE ADHESION; THROMBOCYTE AGGREGATION; TISSUE SECTION; ANTAGONISTS AND INHIBITORS; COMPLICATION; DRUG EFFECT; METABOLISM; MIDDLE AGED; ORAL DRUG ADMINISTRATION; PATHOLOGY; THROMBOSIS;

ADMINISTRATION, ORAL; ADULT; AGAMMAGLOBULINAEMIA TYROSINE KINASE; AGED; BENZAMIDES; HUMANS; IMIDAZOLES; MALE; MIDDLE AGED; PLAQUE, ATHEROSCLEROTIC; PLATELET AGGREGATION; PLATELET AGGREGATION INHIBITORS; PROTEIN KINASE INHIBITORS; PYRAZINES; PYRAZOLES; PYRIMIDINES; THROMBOSIS;

EID: 85047562162     PISSN: 00064971     EISSN: 15280020     Source Type: Journal    
DOI: 10.1182/blood-2017-09-808808     Document Type: Article

References (49)

1. van Zanten GH, de Graaf S, Slootweg PJ, et al. Increased platelet deposition on atherosclerotic coronary arteries. J Clin Invest. 1994; 93(2):615-632.
2. Penz S, Reininger AJ, Brandl R, et al. Human atheromatous plaques stimulate thrombus formation by activating platelet glycoprotein VI. FASEB J. 2005;19(8):898-909.
3. Katsuda S, Kaji T. Atherosclerosis and extracellular matrix. J Atheroscler Thromb. 2003; 10(5):267-274.
4. Reininger AJ, Bernlochner I, Penz SM, et al. A 2-step mechanism of arterial thrombus formation induced by human atherosclerotic plaques. J Am Coll Cardiol. 2010;55(11): 1147-1158.
5. Schulz C, Penz S, Hoffmann C, et al. Platelet GPVI binds to collagenous structures in the core region of human atheromatous plaque and is critical for atheroprogression in vivo. Basic Res Cardiol. 2008;103(4):356-367.
6. Goto S, Tamura N, Handa S, Arai M, Kodama K, Takayama H. Involvement of glycoprotein VI in platelet thrombus formation on both collagen and von Willebrand factor surfaces under flow conditions. Circulation. 2002; 106(2):266-272.
7. Nieswandt B, Watson SP. Platelet-collagen interaction: Is GPVI the central receptor?. Blood. 2003;102(2):449-461.
8. Herr AB, Farndale RW. Structural insights into the interactions between platelet receptors and fibrillar collagen. J Biol Chem. 2009; 284(30):19781-19785.
9. Deckmyn H, De Meyer SF, Broos K, Vanhoorelbeke K. Inhibitors of the interactions between collagen and its receptors on platelets. Handb Exp Pharmacol. 2012;(210): 311-337.
10. Jamasbi J, Ayabe K, Goto S, Nieswandt B, Peter K, Siess W. Platelet receptors as therapeutic targets: Past, present and future. Thromb Haemost. 2017;117(7):1249-1257.
11. Kuijpers MJ, Gilio K, Reitsma S, et al. Complementary roles of platelets and coagulation in thrombus formation on plaques acutely ruptured by targeted ultrasound treatment: A novel intravital model. J Thromb Haemost. 2009;7(1):152-161.
12. Hechler B, Gachet C. Comparison of two murine models of thrombosis induced by atherosclerotic plaque injury. Thromb Haemost. 2011;105(suppl 1):S3-S12.
13. Jamasbi J, Megens RT, Bianchini M, et al. Differential inhibition of human atherosclerotic plaque-induced platelet activation by dimeric GPVI-Fc and anti-GPVI antibodies: Functional and imaging studies. J Am Coll Cardiol. 2015;65(22):2404-2415.
14. Penz SM, Reininger AJ, Toth O, Deckmyn H, Brandl R, Siess W. Glycoprotein Ibalpha inhibition and ADP receptor antagonists, but not aspirin, reduce platelet thrombus formation in flowing blood exposed to atherosclerotic plaques. Thromb Haemost. 2007;97(3): 435-443.
15. Kuijpers MJ, Schulte V, Bergmeier W, et al. Complementary roles of glycoprotein VI and alpha2beta1 integrin in collagen-induced thrombus formation in flowing whole blood ex vivo. FASEB J. 2003;17(6):685-687.
16. Liu J, Fitzgerald ME, Berndt MC, Jackson CW, Gartner TK. Bruton tyrosine kinase is essential for botrocetin/VWF-induced signaling and GPIb-dependent thrombus formation in vivo. Blood. 2006;108(8):2596-2603.
17. Oda A, Ikeda Y, Ochs HD, et al. Rapid tyrosine phosphorylation and activation of Bruton's tyrosine/Tec kinases in platelets induced by collagen binding or CD32 cross-linking. Blood. 2000;95(5):1663-1670.
18. Quek LS, Bolen J, Watson SP. A role for Bruton's tyrosine kinase (Btk) in platelet activation by collagen. Curr Biol. 1998;8(20): 1137-1140.
19. Watson SP, Auger JM, McCarty OJ, Pearce AC. GPVI and integrin alphaIIb beta3 signaling in platelets. J Thromb Haemost. 2005;3(8): 1752-1762.
20. Siess W. Molecular mechanisms of platelet activation. Physiol Rev. 1989;69(1):58-178.
21. Honigberg LA, Smith AM, Sirisawad M, et al. The Bruton tyrosine kinase inhibitor PCI-32765 blocks B-cell activation and is efficacious in models of autoimmune disease and B-cell malignancy. Proc Natl Acad Sci USA. 2010;107(29):13075-13080.
22. Byrd JC, Harrington B, O'Brien S, et al. Acalabrutinib (ACP-196) in relapsed chronic lymphocytic leukemia. N Engl J Med. 2016; 374(4):323-332.
23. Walter HS, Rule SA, Dyer MJ, et al. A phase 1 clinical trial of the selective BTK inhibitor ONO/GS-4059 in relapsed and refractory mature B-cell malignancies. Blood. 2016; 127(4):411-419.
24. Wu J, Liu C, Tsui ST, Liu D. Second-generation inhibitors of Bruton tyrosine kinase. J Hematol Oncol. 2016;9(1):80.
25. Auger JM, Kuijpers MJ, Senis YA, Watson SP, Heemskerk JW. Adhesion of human and mouse platelets to collagen under shear: A unifying model. FASEB J. 2005;19(7):825-827.
26. Brandl R, Richter T, Haug K, Wilhelm MG, Maurer PC, Nathrath W. Topographic analysis of proliferative activity in carotid endarterectomy specimens by immunocytochemical detection of the cell cycle-related antigen Ki-67. Circulation. 1997;96(10):3360-3368.
27. Tóth O, Calatzis A, Penz S, Losonczy H, Siess W. Multiple electrode aggregometry: A new device to measure platelet aggregation in whole blood. Thromb Haemost. 2006;96(6): 781-788.
28. Bampalis VG, Brantl SA, Siess W. Why and how to eliminate spontaneous platelet aggregation in blood measured by multiple electrode aggregometry. J Thromb Haemost. 2012;10(8):1710-1714.
29. Jamasbi J, Megens RT, Bianchini M, et al. Crosslinking GPVI-Fc by anti-Fc antibodies potentiates its inhibition of atherosclerotic plaque- and collagen-induced platelet activation. JACC Basic Transl Sci. 2016;1(131):142-13.
30. Kratzer MA, Negrescu EV, Hirai A, Yeo YK, Franke P, Siess W. The Thrombostat system. A useful method to test antiplatelet drugs and diets. Semin Thromb Hemost. 1995; 21(suppl 2):25-31.
31. Kundu SK, Heilmann EJ, Sio R, Garcia C, Davidson RM, Ostgaard RA. Description of an in vitro platelet function analyzer-PFA-100. Semin Thromb Hemost. 1995;21(suppl 2): 106-112.
32. Levade M, David E, Garcia C, et al. Ibrutinib treatment affects collagen and von Willebrand factor-dependent platelet functions. Blood. 2014;124(26):3991-3995.
33. Kazianka L, Drucker C, Skrabs C, et al. Ristocetin-induced platelet aggregation for monitoring of bleeding tendency in CLL treated with ibrutinib. Leukemia. 2017;31(5): 1117-1122.
34. Reny JL, De Moerloose P, Dauzat M, Fontana P. Use of the PFA-100 closure time to predict cardiovascular events in aspirin-treated cardiovascular patients: A systematic review and meta-analysis. J Thromb Haemost. 2008;6(3): 444-450.
35. Penz SM, Bernlochner I, Tóth O, Lorenz R, Calatzis A, Siess W. Selective and rapid monitoring of dual platelet inhibition by aspirin and P2Y12 antagonists by using multiple electrode aggregometry. Thromb J. 2010; 8(1):9.
36. Wang ML, Blum KA, Martin P, et al. Long-term follow-up of MCL patients treated with singleagent ibrutinib: Updated safety and efficacy results. Blood. 2015;126(6):739-745.
37. Byrd JC, Furman RR, Coutre SE, et al. Threeyear follow-up of treatment-naïve and previously treated patients with CLL and SLL receiving single-agent ibrutinib. Blood. 2015;125(16):2497-2506.
38. Walter HS, Jayne S, Rule SA, et al. Long-term follow-up of patients with CLL treated with the selective Bruton's tyrosine kinase inhibitor ONO/GS-4059. Blood. 2017;129(20): 2808-2810.
39. Kamel S, Horton L, Ysebaert L, et al. Ibrutinib inhibits collagen-mediated but not ADPmediated platelet aggregation. Leukemia. 2015;29(4):783-787.
40. Cheruvu PK, Finn AV, Gardner C, et al. Frequency and distribution of thin-cap fibroatheroma and ruptured plaques in human coronary arteries: A pathologic study. J Am Coll Cardiol. 2007;50(10):940-949.
41. Bye AP, Unsworth AJ, Vaiyapuri S, Stainer AR, Fry MJ, Gibbins JM. Ibrutinib inhibits platelet integrin aIIbb3 outside-in signaling and thrombus stability but not adhesion to collagen. Arterioscler Thromb Vasc Biol. 2015; 35(11):2326-2335.
42. Laffargue M, Ragab-Thomas JM, Ragab A, et al. Phosphoinositide 3-kinase and integrin signalling are involved in activation of Bruton tyrosine kinase in thrombinstimulated platelets. FEBS Lett. 1999;443(1):66-70.
43. Kraft WK, Gilmartin JH, Chappell DL, et al. Effect of vorapaxar alone and in combination with aspirin on bleeding time and platelet aggregation in healthy adult subjects. Clin Transl Sci. 2016;9(4):221-227.
44. Atkinson BT, Ellmeier W, Watson SP. Tec regulates platelet activation by GPVI in the absence of Btk. Blood. 2003;102(10): 3592-3599.
45. Barf T, Covey T, Izumi R, et al. Acalabrutinib (ACP-196): A covalent Bruton tyrosine kinase inhibitor with a differentiated selectivity and in vivo potency profile. J Pharmacol Exp Ther. 2017;363(2):240-252.
46. Rigg RA, Aslan JE, Healy LD, et al. Oral administration of Bruton's tyrosine kinase inhibitors impairs GPVI-mediated platelet function. Am J Physiol Cell Physiol. 2016; 310(5):C373-C380.
47. Futatani T, Watanabe C, Baba Y, Tsukada S, Ochs HD. Bruton's tyrosine kinase is present in normal platelets and its absence identifies patients with X-linked agammaglobulinaemia and carrier females. Br J Haematol. 2001; 114(1):141-149.
48. Stewart DM, Lian L, Nelson DL. The clinical spectrum of Bruton's agammaglobulinemia. Curr Allergy Asthma Rep. 2001;1(6): 558-565.
49. Lorenz RL, Boehlig B, Uedelhoven WM, Weber PC. Superior antiplatelet action of alternate day pulsed dosing versus split dose administration of aspirin. Am J Cardiol. 1989; 64(18):1185-1188.