Procoagulant Platelets and the Pathways Leading to Cell Death

Vu Minh Hua; Vivien Mun Yee Chen

doi:10.1055/s-0034-1544002

Seminars in Thrombosis and Hemostasis, Inhaltsverzeichnis

Semin Thromb Hemost 2015; 41(04): 405-412
DOI: 10.1055/s-0034-1544002

Thieme Medical Publishers 333 Seventh Avenue, New York, NY 10001, USA.

Procoagulant Platelets and the Pathways Leading to Cell Death

Vu Minh Hua

¹Lowy Cancer Research Centre, Prince of Wales Clinical School, University of New South Wales, Sydney, Australia

,

Vivien Mun Yee Chen

¹Lowy Cancer Research Centre, Prince of Wales Clinical School, University of New South Wales, Sydney, Australia

²Department of Haematology, South Eastern Area Laboratory Services, Prince of Wales Hospital, Sydney, NSW, Australia

› Institutsangaben

Abstract

Platelets are critical mediators of thrombosis and hemostasis. In response to agonist, platelets aggregate to form a thrombus via ligand binding of the glycoprotein IIb/IIIa receptor. However, activated platelets are heterogeneous in nature and a subset of platelets stimulated by strong agonists support the assembly of the coagulation complexes. It is proposed that these “procoagulant” platelets have a unique role in hemostasis and thrombosis as the link between primary and secondary hemostasis, localizing the thrombin burst required for fibrin formation to micro-domains within the platelet thrombus. Loss of procoagulant potential leads to bleeding while an increase is linked with propensity to thrombosis. While many features of the procoagulant platelet are known, the exact nature of the procoagulant platelet remains controversial. It is noted that many of the morphological and biochemical features of procoagulant platelets are also features of the cyclophilin D necrosis pathway. This review will focus on the distinct roles of platelet subpopulations, the identity of the procoagulant platelet, and the potential role of the cell death pathways in regulating platelet procoagulant response.

Keywords

procoagulant - platelet - necrosis - apoptosis

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Referenzen

References
1 Jackson SP. The growing complexity of platelet aggregation. Blood 2007; 109 (12) 5087-5095
2 Nieswandt B, Pleines I, Bender M. Platelet adhesion and activation mechanisms in arterial thrombosis and ischaemic stroke. J Thromb Haemost 2011; 9 (Suppl. 01) 92-104
3 Monroe DM, Hoffman M. What does it take to make the perfect clot?. Arterioscler Thromb Vasc Biol 2006; 26 (1) 41-48
4 Alberio L, Safa O, Clemetson KJ, Esmon CT, Dale GL. Surface expression and functional characterization of alpha-granule factor V in human platelets: effects of ionophore A23187, thrombin, collagen, and convulxin. Blood 2000; 95 (5) 1694-1702
5 Kempton CL, Hoffman M, Roberts HR, Monroe DM. Platelet heterogeneity: variation in coagulation complexes on platelet subpopulations. Arterioscler Thromb Vasc Biol 2005; 25 (4) 861-866
6 Ariëns RA, Lai TS, Weisel JW, Greenberg CS, Grant PJ. Role of factor XIII in fibrin clot formation and effects of genetic polymorphisms. Blood 2002; 100 (3) 743-754
7 Hoffman M, Monroe III DM. A cell-based model of hemostasis. Thromb Haemost 2001; 85 (6) 958-965
8 Yang H, Kim A, David T , et al. TMEM16F forms a Ca2+-activated cation channel required for lipid scrambling in platelets during blood coagulation. Cell 2012; 151 (1) 111-122
9 Suzuki J, Umeda M, Sims PJ, Nagata S. Calcium-dependent phospholipid scrambling by TMEM16F. Nature 2010; 468 (7325) 834-838
10 Toti F, Satta N, Fressinaud E, Meyer D, Freyssinet JM. Scott syndrome, characterized by impaired transmembrane migration of procoagulant phosphatidylserine and hemorrhagic complications, is an inherited disorder. Blood 1996; 87 (4) 1409-1415
11 van Kruchten R, Mattheij NJA, Saunders C , et al. Both TMEM16F-dependent and TMEM16F-independent pathways contribute to phosphatidylserine exposure in platelet apoptosis and platelet activation. Blood 2013; 121 (10) 1850-1857
12 Jackson SP. Arterial thrombosis—insidious, unpredictable and deadly. Nat Med 2011; 17 (11) 1423-1436
13 Kirkpatrick AC, Stoner JA, Dale GL, Prodan CI. Elevated coated-platelets in symptomatic large-artery stenosis patients are associated with early stroke recurrence. Platelets 2014; 25 (2) 93-96
14 Collaboration AT. Antithrombotic Trialists' Collaboration. Collaborative meta-analysis of randomised trials of antiplatelet therapy for prevention of death, myocardial infarction, and stroke in high risk patients. BMJ 2002; 324 (7329) 71-86
15 Dale GL, Friese P, Batar P , et al. Stimulated platelets use serotonin to enhance their retention of procoagulant proteins on the cell surface. Nature 2002; 415 (6868) 175-179
16 Yakimenko AO, Verholomova FY, Kotova YN, Ataullakhanov FI, Panteleev MA. Identification of different proaggregatory abilities of activated platelet subpopulations. Biophys J 2012; 102 (10) 2261-2269
17 Topalov NN, Yakimenko AO, Canault M , et al. Two types of procoagulant platelets are formed upon physiological activation and are controlled by integrin α(IIb)β(3). Arterioscler Thromb Vasc Biol 2012; 32 (10) 2475-2483
18 Bevers EM, Comfurius P, van Rijn JLML, Hemker HC, Zwaal RF. Generation of prothrombin-converting activity and the exposure of phosphatidylserine at the outer surface of platelets. Eur J Biochem 1982; 122 (2) 429-436
19 Jobe SM, Wilson KM, Leo L , et al. Critical role for the mitochondrial permeability transition pore and cyclophilin D in platelet activation and thrombosis. Blood 2008; 111 (3) 1257-1265
20 Fager AM, Wood JP, Bouchard BA, Feng P, Tracy PB. Properties of procoagulant platelets: defining and characterizing the subpopulation binding a functional prothrombinase. Arterioscler Thromb Vasc Biol 2010; 30 (12) 2400-2407
21 Munnix ICA, Kuijpers MJE, Auger J , et al. Segregation of platelet aggregatory and procoagulant microdomains in thrombus formation: regulation by transient integrin activation. Arterioscler Thromb Vasc Biol 2007; 27 (11) 2484-2490
22 Heemskerk JW, Vuist WM, Feijge MA, Reutelingsperger CP, Lindhout T. Collagen but not fibrinogen surfaces induce bleb formation, exposure of phosphatidylserine, and procoagulant activity of adherent platelets: evidence for regulation by protein tyrosine kinase-dependent Ca2+ responses. Blood 1997; 90 (7) 2615-2625
23 Kulkarni S, Jackson SP. Platelet factor XIII and calpain negatively regulate integrin alphaIIbbeta3 adhesive function and thrombus growth. J Biol Chem 2004; 279 (29) 30697-30706
24 Mattheij NJA, Gilio K, van Kruchten R , et al. Dual mechanism of integrin αIIbβ3 closure in procoagulant platelets. J Biol Chem 2013; 288 (19) 13325-13336
25 Nesbitt WS, Westein E, Tovar-Lopez FJ , et al. A shear gradient-dependent platelet aggregation mechanism drives thrombus formation. Nat Med 2009; 15 (6) 665-673
26 Munnix IC, Cosemans JM, Auger JM, Heemskerk JW. Platelet response heterogeneity in thrombus formation. Thromb Haemost 2009; 102 (6) 1149-1156
27 von Brühl ML, Stark K, Steinhart A , et al. Monocytes, neutrophils, and platelets cooperate to initiate and propagate venous thrombosis in mice in vivo. J Exp Med 2012; 209 (4) 819-835
28 Voronov RS, Stalker TJ, Brass LF, Diamond SL. Simulation of intrathrombus fluid and solute transport using in vivo clot structures with single platelet resolution. Ann Biomed Eng 2013; 41 (6) 1297-1307
29 Furihata K, Clemetson KJ, Deguchi H, Kunicki TJ. Variation in human platelet glycoprotein VI content modulates glycoprotein VI-specific prothrombinase activity. Arterioscler Thromb Vasc Biol 2001; 21 (11) 1857-1863
30 Pasquet JM, Toti F, Nurden AT, Dachary-Prigent J. Procoagulant activity and active calpain in platelet-derived microparticles. Thromb Res 1996; 82 (6) 509-522
31 Smeets EF, Heemskerk JW, Comfurius P, Bevers EM, Zwaal RF. Thapsigargin amplifies the platelet procoagulant response caused by thrombin. Thromb Haemost 1993; 70 (6) 1024-1029
32 Thiagarajan P, Tait JF. Collagen-induced exposure of anionic phospholipid in platelets and platelet-derived microparticles. J Biol Chem 1991; 266 (36) 24302-24307
33 London FS, Marcinkiewicz M, Walsh PN. A subpopulation of platelets responds to thrombin- or SFLLRN-stimulation with binding sites for factor IXa. J Biol Chem 2004; 279 (19) 19854-19859
34 Butenas S, van't Veer C, Mann KG. “Normal” thrombin generation. Blood 1999; 94 (7) 2169-2178
35 Remenyi G, Szasz R, Friese P, Dale GL. Role of mitochondrial permeability transition pore in coated-platelet formation. Arterioscler Thromb Vasc Biol 2005; 25 (2) 467-471
36 Leytin V, Allen DJ, Mutlu A, Gyulkhandanyan AV, Mykhaylov S, Freedman J. Mitochondrial control of platelet apoptosis: effect of cyclosporin A, an inhibitor of the mitochondrial permeability transition pore. Lab Invest 2009; 89 (4) 374-384
37 Batar P, Dale GL. Simultaneous engagement of thrombin and Fc γ RIIA receptors results in platelets expressing high levels of procoagulant proteins. J Lab Clin Med 2001; 138 (6) 393-402
38 Heemskerk JW, Bevers EM, Lindhout T. Platelet activation and blood coagulation. Thromb Haemost 2002; 88 (2) 186-193
39 Feng P, Tracy PB. Not all platelets are equivalent procoagulants. Blood 1998; 92: 1441a
40 Kuijpers MJE, Schulte V, Oury C , et al. Facilitating roles of murine platelet glycoprotein Ib and alphaIIbbeta3 in phosphatidylserine exposure during vWF-collagen-induced thrombus formation. J Physiol 2004; 558 (Pt 2) 403-415
41 Prodan CI, Stoner JA, Cowan LD, Dale GL. Higher coated-platelet levels are associated with stroke recurrence following nonlacunar brain infarction. J Cereb Blood Flow Metab 2013; 33 (2) 287-292
42 Brown SB, Clarke MC, Magowan L, Sanderson H, Savill J. Constitutive death of platelets leading to scavenger receptor-mediated phagocytosis. A caspase-independent cell clearance program. J Biol Chem 2000; 275 (8) 5987-5996
43 Kile BT. The role of apoptosis in megakaryocytes and platelets. Br J Haematol 2014; 165 (2) 217-226
44 White MJ, Schoenwaelder SM, Josefsson EC , et al. Caspase-9 mediates the apoptotic death of megakaryocytes and platelets, but is dispensable for their generation and function. Blood 2012; 119 (18) 4283-4290
45 Mason KD, Carpinelli MR, Fletcher JI , et al. Programmed anuclear cell death delimits platelet life span. Cell 2007; 128 (6) 1173-1186
46 Schoenwaelder SM, Jackson SP. Bcl-xL-inhibitory BH3 mimetics (ABT-737 or ABT-263) and the modulation of cytosolic calcium flux and platelet function. Blood 2012; 119 (5) 1320-1321 , author reply 1321–1322
47 Josefsson EC, White MJ, Dowling MR, Kile BT. Platelet life span and apoptosis. Methods Mol Biol 2012; 788: 59-71
48 Leytin V, Allen DJ, Mykhaylov S, Lyubimov E, Freedman J. Thrombin-triggered platelet apoptosis. J Thromb Haemost 2006; 4 (12) 2656-2663
49 Li S, Wang Z, Liao Y , et al. The glycoprotein Ibalpha-von Willebrand factor interaction induces platelet apoptosis. J Thromb Haemost 2010; 8 (2) 341-350
50 Arachiche A, Kerbiriou-Nabias D, Garcin I, Letellier T, Dachary-Prigent J. Rapid procoagulant phosphatidylserine exposure relies on high cytosolic calcium rather than on mitochondrial depolarization. Arterioscler Thromb Vasc Biol 2009; 29 (11) 1883-1889
51 Schoenwaelder SM, Yuan Y, Josefsson EC , et al. Two distinct pathways regulate platelet phosphatidylserine exposure and procoagulant function. Blood 2009; 114 (3) 663-666
52 Schoenwaelder SM, Jarman KE, Gardiner EE , et al. Bcl-xL-inhibitory BH3 mimetics can induce a transient thrombocytopathy that undermines the hemostatic function of platelets. Blood 2011; 118 (6) 1663-1674
53 Festjens N, Vanden Berghe T, Vandenabeele P. Necrosis, a well-orchestrated form of cell demise: signalling cascades, important mediators and concomitant immune response. Biochim Biophys Acta 2006; 1757 (9-10) 1371-1387
54 Zong WX, Thompson CB. Necrotic death as a cell fate. Genes Dev 2006; 20 (1) 1-15
55 Nakagawa T, Shimizu S, Watanabe T , et al. Cyclophilin D-dependent mitochondrial permeability transition regulates some necrotic but not apoptotic cell death. Nature 2005; 434 (7033) 652-658
56 Choo H-J, Saafir TB, Mkumba L, Wagner MB, Jobe SM. Mitochondrial calcium and reactive oxygen species regulate agonist-initiated platelet phosphatidylserine exposure. Arterioscler Thromb Vasc Biol 2012; 32 (12) 2946-2955
57 Reményi G, Szász R, Debreceni IB , et al. Comparison of coated-platelet levels in patients with essential thrombocythemia with and without hydroxyurea treatment. Platelets 2013; 24 (6) 486-492
58 Prodan CI, Vincent AS, Dale GL. Coated-platelet levels are elevated in patients with transient ischemic attack. Transl Res 2011; 158 (1) 71-75