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Hamostaseologie 2021; 41(02): 146-153
DOI: 10.1055/a-1401-2706
Review Article

Procoagulant Platelets: Mechanisms of Generation and Action

N.A. Podoplelova
1   Center for Theoretical Problems of Physicochemical Pharmacology, Russian Academy of Sciences, Moscow, Russia
2   National Medical Research Center of Pediatric Hematology, Oncology and Immunology named after Dmitry Rogachev, Moscow, Russia
,
D.Y. Nechipurenko
1   Center for Theoretical Problems of Physicochemical Pharmacology, Russian Academy of Sciences, Moscow, Russia
2   National Medical Research Center of Pediatric Hematology, Oncology and Immunology named after Dmitry Rogachev, Moscow, Russia
3   Faculty of Physics, Lomonosov Moscow State University, Moscow, Russia
,
A.A. Ignatova
1   Center for Theoretical Problems of Physicochemical Pharmacology, Russian Academy of Sciences, Moscow, Russia
2   National Medical Research Center of Pediatric Hematology, Oncology and Immunology named after Dmitry Rogachev, Moscow, Russia
,
A.N. Sveshnikova
1   Center for Theoretical Problems of Physicochemical Pharmacology, Russian Academy of Sciences, Moscow, Russia
2   National Medical Research Center of Pediatric Hematology, Oncology and Immunology named after Dmitry Rogachev, Moscow, Russia
3   Faculty of Physics, Lomonosov Moscow State University, Moscow, Russia
,
M.A. Panteleev
1   Center for Theoretical Problems of Physicochemical Pharmacology, Russian Academy of Sciences, Moscow, Russia
2   National Medical Research Center of Pediatric Hematology, Oncology and Immunology named after Dmitry Rogachev, Moscow, Russia
3   Faculty of Physics, Lomonosov Moscow State University, Moscow, Russia
› Institutsangaben Funding The authors were supported by the Russian Science Foundation grant 20-74-00133.
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Abstract

During the past decades, it has been increasingly recognized that the major function of accelerating membrane-dependent reactions of blood coagulation is predominantly implemented by a subset of activated platelets. These procoagulant platelets (also called collagen- and thrombin-activated or COAT, coated, necrotic, although there could be subtle differences between these definitions) are uniquely characterized by both procoagulant activity and, at the same time, inactivated integrins and profibrinolytic properties. The mechanisms of their generation both in vitro and in situ have been increasingly becoming clear, suggesting unique and multidirectional roles in hemostasis and thrombosis. In this mini-review, we shall highlight the existing concepts and challenges in this field.

Keywords

procoagulant platelets - thrombosis - hemostasis


Publikationsverlauf

Eingereicht: 15. Dezember 2020

Angenommen: 25. Februar 2021

Artikel online veröffentlicht:
15. April 2021

© 2021. Thieme. All rights reserved.

Georg Thieme Verlag KG
Rüdigerstraße 14, 70469 Stuttgart, Germany

 

  • References

  • 1 Heemskerk JWM, Mattheij NJA, Cosemans JMEM. Platelet-based coagulation: different populations, different functions. J Thromb Haemost 2013; 11 (01) 2-16
    CrossrefPubMedGoogle Scholar
  • 2 Ahmad SS, London FS, Walsh PN. The assembly of the factor X-activating complex on activated human platelets. J Thromb Haemost 2003; 1 (01) 48-59
    CrossrefPubMedGoogle Scholar
  • 3 Dachary-Prigent J, Freyssinet JM, Pasquet JM, Carron JC, Nurden AT. Annexin V as a probe of aminophospholipid exposure and platelet membrane vesiculation: a flow cytometry study showing a role for free sulfhydryl groups. Blood 1993; 81 (10) 2554-2565
    CrossrefPubMedGoogle Scholar
  • 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 (05) 1694-1702
    CrossrefPubMedGoogle Scholar
  • 5 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
    CrossrefPubMedGoogle Scholar
  • 6 Agbani EO, Poole AW. Procoagulant platelets: generation, function, and therapeutic targeting in thrombosis. Blood 2017; 130 (20) 2171-2179
    CrossrefPubMedGoogle Scholar
  • 7 Reddy EC, Rand ML. Procoagulant phosphatidylserine-exposing platelets in vitro and in vivo . Front Cardiovasc Med 2020; 7: 15
    CrossrefPubMedGoogle Scholar
  • 8 van der Meijden PEJ, Heemskerk JWM. Platelet biology and functions: new concepts and clinical perspectives. Nat Rev Cardiol 2019; 16 (03) 166-179
    CrossrefPubMedGoogle Scholar
  • 9 Tohidi-Esfahani I, Lee CSM, Liang HPH, Chen VMY. Procoagulant platelets: laboratory detection and clinical significance. Int J Lab Hematol 2020; 42 (Suppl. 01) 59-67
    CrossrefPubMedGoogle Scholar
  • 10 Baaten CCFMJ, Ten Cate H, van der Meijden PEJ, Heemskerk JWM. Platelet populations and priming in hematological diseases. Blood Rev 2017; 31 (06) 389-399
    CrossrefPubMedGoogle Scholar
  • 11 Dale GL. Procoagulant platelets: further details but many more questions. [Internet] Arterioscler Thromb Vasc Biol 2017; 37 (09) 1596-1597
    CrossrefPubMedGoogle Scholar
  • 12 Webber AJ, Firkin BG. Two populations of platelets. Nature 1965; 205: 1332-1332
    CrossrefPubMedGoogle Scholar
  • 13 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 (07) 2615-2625
    CrossrefPubMedGoogle Scholar
  • 14 Abaeva AA, Canault M, Kotova YN. et al. Procoagulant platelets form an α-granule protein-covered “cap” on their surface that promotes their attachment to aggregates. J Biol Chem 2013; 288 (41) 29621-29632
    CrossrefPubMedGoogle Scholar
  • 15 Agbani EO, van den Bosch MTJ, Brown E. et al. Coordinated membrane ballooning and procoagulant spreading in human platelets. Circulation 2015; 132 (15) 1414-1424
    CrossrefPubMedGoogle Scholar
  • 16 Mitchell JL, Lionikiene AS, Fraser SR, Whyte CS, Booth NA, Mutch NJ. Functional factor XIII-A is exposed on the stimulated platelet surface. Blood 2014; 124 (26) 3982-3990
    CrossrefPubMedGoogle Scholar
  • 17 Whyte CS, Swieringa F, Mastenbroek TG. et al. Plasminogen associates with phosphatidylserine-exposing platelets and contributes to thrombus lysis under flow. Blood 2015; 125 (16) 2568-2578
    CrossrefPubMedGoogle Scholar
  • 18 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
    CrossrefPubMedGoogle Scholar
  • 19 Kulkarni S, Nesbitt WS, Dopheide SM. et al. Techniques to examine platelet adhesive interactions under flow. In: Gibbins JM, Mahaut-Smith MP. eds. Platelets and Megakaryocytes. New Jersey: Humana Press; 2004: 165-186
    Google Scholar
  • 20 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
    CrossrefPubMedGoogle Scholar
  • 21 De Marco L, Mazzucato M, Masotti A, Ruggeri ZM. Localization and characterization of an alpha-thrombin-binding site on platelet glycoprotein Ib alpha. J Biol Chem 1994; 269 (09) 6478-6484
    CrossrefPubMedGoogle Scholar
  • 22 Kempton CL, Hoffman M, Roberts HR, Monroe DM. Platelet heterogeneity: variation in coagulation complexes on platelet subpopulations. Arterioscler Thromb Vasc Biol 2005; 25 (04) 861-866
    CrossrefPubMedGoogle Scholar
  • 23 Panteleev MA, Ananyeva NM, Greco NJ, Ataullakhanov FI, Saenko EL. Two subpopulations of thrombin-activated platelets differ in their binding of the components of the intrinsic factor X-activating complex. J Thromb Haemost 2005; 3 (11) 2545-2553
    CrossrefPubMedGoogle Scholar
  • 24 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
    CrossrefPubMedGoogle Scholar
  • 25 Dasgupta SK, Abdel-Monem H, Niravath P. et al. Lactadherin and clearance of platelet-derived microvesicles. [Internet] Blood 2009; 113 (06) 1332-1339
    CrossrefPubMedGoogle Scholar
  • 26 Sveshnikova AN, Balatskiy AV, Demianova AS. et al. Systems biology insights into the meaning of the platelet's dual-receptor thrombin signaling. J Thromb Haemost 2016; 14 (10) 2045-2057
    CrossrefPubMedGoogle Scholar
  • 27 Kotova YN, Ataullakhanov FI, Panteleev MA. Formation of coated platelets is regulated by the dense granule secretion of adenosine 5'diphosphate acting via the P2Y12 receptor. J Thromb Haemost 2008; 6 (09) 1603-1605
    CrossrefPubMedGoogle Scholar
  • 28 Kotova YN, Podoplelova NA, Obydennyy SI. et al. Binding of coagulation factor XIII zymogen to activated platelet subpopulations: roles of integrin αIIbβ3 and fibrinogen. Thromb Haemost 2019; 119 (06) 906-915
    Artikel in Thieme ConnectPubMedGoogle Scholar
  • 29 Shakhidzhanov SS, Shaturny VI, Panteleev MA, Sveshnikova AN. Modulation and pre-amplification of PAR1 signaling by ADP acting via the P2Y12 receptor during platelet subpopulation formation. Biochim Biophys Acta 2015; 1850 (12) 2518-2529
    CrossrefPubMedGoogle Scholar
  • 30 Leon C, Ravanat C, Freund M, Cazenave JP, Gachet C. Differential involvement of the P2Y1 and P2Y12 receptors in platelet procoagulant activity. Arterioscler Thromb Vasc Biol 2003; 23 (10) 1941-1947
    CrossrefPubMedGoogle Scholar
  • 31 van der Meijden PE, Feijge MA, Giesen PL, Huijberts M, van Raak LP, Heemskerk JW. Platelet P2Y12 receptors enhance signalling towards procoagulant activity and thrombin generation: a study with healthy subjects and patients at thrombotic risk. Thromb Haemost 2005; 93 (06) 1128-1136
    Artikel in Thieme ConnectPubMedGoogle Scholar
  • 32 Polgár J, Clemetson JM, Kehrel BE. et al. Platelet activation and signal transduction by convulxin, a C-type lectin from Crotalus durissus terrificus (tropical rattlesnake) venom via the p62/GPVI collagen receptor. J Biol Chem 1997; 272 (21) 13576-13583
    CrossrefPubMedGoogle Scholar
  • 33 Ignatova AA, Ponomarenko EA, Polokhov DM. et al. Flow cytometry for pediatric platelets. Platelets 2019; 30 (04) 428-437
    CrossrefPubMedGoogle Scholar
  • 34 Mammadova-Bach E, Ollivier V, Loyau S. et al. Platelet glycoprotein VI binds to polymerized fibrin and promotes thrombin generation. Blood 2015; 126 (05) 683-691
    CrossrefPubMedGoogle Scholar
  • 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 (02) 467-471
    CrossrefPubMedGoogle Scholar
  • 36 Schoenwaelder SM, Yuan Y, Josefsson EC. et al. Two distinct pathways regulate platelet phosphatidylserine exposure and procoagulant function. Blood 2009; 114 (03) 663-666
    CrossrefPubMedGoogle Scholar
  • 37 Sveshnikova AN, Ataullakhanov FI, Panteleev MA. Compartmentalized calcium signaling triggers subpopulation formation upon platelet activation through PAR1. Mol Biosyst 2015; 11 (04) 1052-1060
    CrossrefPubMedGoogle Scholar
  • 38 Obydennyi SI, Artemenko EO, Sveshnikova AN. et al. Mechanisms of increased mitochondria-dependent necrosis in Wiskott-Aldrich syndrome platelets. Haematologica 2020; 105 (04) 1095-1106
    CrossrefPubMedGoogle Scholar
  • 39 Obydennyy SI, Sveshnikova AN, Ataullakhanov FI, Panteleev MA. Dynamics of calcium spiking, mitochondrial collapse and phosphatidylserine exposure in platelet subpopulations during activation. J Thromb Haemost 2016; 14 (09) 1867-1881
    CrossrefPubMedGoogle Scholar
  • 40 Artemenko EO, Yakimenko AO, Pichugin AV, Ataullakhanov FI, Panteleev MA. Calpain-controlled detachment of major glycoproteins from the cytoskeleton regulates adhesive properties of activated phosphatidylserine-positive platelets. Biochem J 2016; 473 (04) 435-448
    CrossrefPubMedGoogle Scholar
  • 41 Reddy EC, Wang H, Christensen H. et al. Analysis of procoagulant phosphatidylserine-exposing platelets by imaging flow cytometry. Res Pract Thromb Haemost 2018; 2 (04) 736-750
    CrossrefPubMedGoogle Scholar
  • 42 Alberio L, Ravanat C, Hechler B, Mangin PH, Lanza F, Gachet C. Delayed-onset of procoagulant signalling revealed by kinetic analysis of COAT platelet formation. Thromb Haemost 2017; 117 (06) 1101-1114
    Artikel in Thieme ConnectPubMedGoogle Scholar
  • 43 Aliotta A, Bertaggia Calderara D, Zermatten MG. et al. Sodium-calcium exchanger reverse mode sustains dichotomous ion fluxes required for procoagulant COAT platelet formation. Thromb Haemost 2021; 121 (03) 309-321
    Artikel in Thieme ConnectPubMedGoogle Scholar
  • 44 Abbasian N, Millington-Burgess SL, Chabra S, Malcor JD, Harper MT. Supramaximal calcium signaling triggers procoagulant platelet formation. Blood Adv 2020; 4 (01) 154-164
    CrossrefPubMedGoogle Scholar
  • 45 Harper MT, Londoño JE, Quick K. et al. Transient receptor potential channels function as a coincidence signal detector mediating phosphatidylserine exposure. [Internet] Sci Signal 2013; 6 (281) ra50
    CrossrefPubMedGoogle Scholar
  • 46 Rukoyatkina N, Begonja AJ, Geiger J, Eigenthaler M, Walter U, Gambaryan S. Phosphatidylserine surface expression and integrin alpha IIb beta 3 activity on thrombin/convulxin stimulated platelets/particles of different sizes. Br J Haematol 2009; 144 (04) 591-602
    CrossrefPubMedGoogle Scholar
  • 47 Handtke S, Wesche J, Palankar R, Greinacher A, Thiele T. Function of large and small platelets differs, depending on extracellular calcium availability and type of inductor. Thromb Haemost 2020; 120 (07) 1075-1086
    Artikel in Thieme ConnectPubMedGoogle Scholar
  • 48 Falati S, Gross P, Merrill-Skoloff G, Furie BC, Furie B. Real-time in vivo imaging of platelets, tissue factor and fibrin during arterial thrombus formation in the mouse. Nat Med 2002; 8 (10) 1175-1181
    CrossrefPubMedGoogle Scholar
  • 49 Stalker TJ, Traxler EA, Wu J. et al. Hierarchical organization in the hemostatic response and its relationship to the platelet-signaling network. Blood 2013; 121 (10) 1875-1885
    CrossrefPubMedGoogle Scholar
  • 50 Welsh JD, Poventud-Fuentes I, Sampietro S, Diamond SL, Stalker TJ, Brass LF. Hierarchical organization of the hemostatic response to penetrating injuries in the mouse macrovasculature. J Thromb Haemost 2017; 15 (03) 526-537
    CrossrefPubMedGoogle Scholar
  • 51 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
    CrossrefPubMedGoogle Scholar
  • 52 Hayashi T, Mogami H, Murakami Y. et al. Real-time analysis of platelet aggregation and procoagulant activity during thrombus formation in vivo. Pflugers Arch 2008; 456 (06) 1239-1251
    CrossrefPubMedGoogle Scholar
  • 53 Hua VM, Abeynaike L, Glaros E. et al. Necrotic platelets provide a procoagulant surface during thrombosis. Blood 2015; 126 (26) 2852-2862
    CrossrefPubMedGoogle Scholar
  • 54 Kamocka MM, Mu J, Liu X. et al. Two-photon intravital imaging of thrombus development. J Biomed Opt 2010; 15 (01) 016020
    CrossrefPubMedGoogle Scholar
  • 55 Yuan Y, Alwis I, Wu MCL. et al. Neutrophil macroaggregates promote widespread pulmonary thrombosis after gut ischemia. Sci Transl Med 2017; 9 (409) eaam5861
    CrossrefPubMedGoogle Scholar
  • 56 Jørgensen L, Borchgrevink CF. The platelet plug in normal persons. Acta Pathol Microbiol Scand 1963; 57: 427-437
    CrossrefPubMedGoogle Scholar
  • 57 Hovig T, Rowsell HC, Dodds WJ, Jorgensen L, Mustard JF. Experimental hemostasis in normal dogs and dogs with congenital disorders of blood coagulation. Blood 1967; 30 (05) 636-668
    CrossrefPubMedGoogle Scholar
  • 58 Tomaiuolo M, Matzko CN, Poventud-Fuentes I, Weisel JW, Brass LF, Stalker TJ. Interrelationships between structure and function during the hemostatic response to injury. Proc Natl Acad Sci U S A 2019; 116 (06) 2243-2252
    CrossrefPubMedGoogle Scholar
  • 59 Nechipurenko DY, Receveur N, Yakimenko AO. et al. Clot contraction drives the translocation of procoagulant platelets to thrombus surface. Arterioscler Thromb Vasc Biol 2019; 39 (01) 37-47
    CrossrefPubMedGoogle Scholar
  • 60 Zwaal RFA, Comfurius P, Bevers EM. Scott syndrome, a bleeding disorder caused by defective scrambling of membrane phospholipids. Biochim Biophys Acta 2004; 1636 (2-3): 119-128
    CrossrefPubMedGoogle Scholar
  • 61 Rosing J, Bevers EM, Comfurius P. et al. Impaired factor X and prothrombin activation associated with decreased phospholipid exposure in platelets from a patient with a bleeding disorder. Blood 1985; 65 (06) 1557-1561
    CrossrefPubMedGoogle Scholar
  • 62 Daskalakis M, Colucci G, Keller P. et al. Decreased generation of procoagulant platelets detected by flow cytometric analysis in patients with bleeding diathesis. Cytometry B Clin Cytom 2014; 86 (06) 397-409
    CrossrefPubMedGoogle Scholar
  • 63 Misceo D, Holmgren A, Louch WE. et al. A dominant STIM1 mutation causes Stormorken syndrome. Hum Mutat 2014; 35 (05) 556-564
    CrossrefPubMedGoogle Scholar
  • 64 Böhm J, Laporte J. Gain-of-function mutations in STIM1 and ORAI1 causing tubular aggregate myopathy and Stormorken syndrome. Cell Calcium 2018; 76: 1-9
    CrossrefPubMedGoogle Scholar
  • 65 Winkler J, Kroiss S, Rand ML. et al. Platelet apoptosis in paediatric immune thrombocytopenia is ameliorated by intravenous immunoglobulin. Br J Haematol 2012; 156 (04) 508-515
    CrossrefPubMedGoogle Scholar
  • 66 Ignatova AA, Demina IA, Ptushkin VV. et al. Evolution of platelet function in adult patients with chronic immune thrombocytopenia on romiplostim treatment. Br J Haematol 2019; 187 (02) e38-e42
    CrossrefPubMedGoogle Scholar
  • 67 Martyanov AA, Morozova DS, Sorokina MA. et al. Heterogeneity of integrin αIIbβ3 function in pediatric immune thrombocytopenia revealed by continuous flow cytometry analysis. Int J Mol Sci MDPI AG 2020; 21: 3035
    CrossrefPubMedGoogle Scholar
  • 68 Zhao L, Bi Y, Kou J, Shi J, Piao D. Phosphatidylserine exposing-platelets and microparticles promote procoagulant activity in colon cancer patients. J Exp Clin Cancer Res 2016; 35: 54
    CrossrefPubMedGoogle Scholar
  • 69 Yang C, Ma R, Jiang T. et al. Contributions of phosphatidylserine-positive platelets and leukocytes and microparticles to hypercoagulable state in gastric cancer patients. Tumour Biol 2016; 37 (06) 7881-7891
    CrossrefPubMedGoogle Scholar
  • 70 Prodan CI, Dale GL. Coated-platelets in ischemic stroke - potential insight into the etiology of stroke subtypes. Int J Stroke 2008; 3 (04) 249-250
    CrossrefPubMedGoogle Scholar
  • 71 Prodan CI, Vincent AS, Dale GL. Coated-platelet levels are elevated in patients with transient ischemic attack. Transl Res 2011; 158 (01) 71-75
    CrossrefPubMedGoogle Scholar
  • 72 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 (02) 287-292
    CrossrefPubMedGoogle Scholar
  • 73 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 (02) 93-96
    CrossrefPubMedGoogle Scholar
  • 74 Kirkpatrick AC, Tafur AJ, Vincent AS, Dale GL, Prodan CI. Coated-platelets improve prediction of stroke and transient ischemic attack in asymptomatic internal carotid artery stenosis. Stroke 2014; 45 (10) 2995-3001
    CrossrefPubMedGoogle Scholar
  • 75 Kirkpatrick AC, Vincent AS, Dale GL, Prodan CI. Coated-platelets predict stroke at 30 days following TIA. Neurology 2017; 89 (02) 125-128
    CrossrefPubMedGoogle Scholar
  • 76 Ray B, Pandav VM, Mathews EA. et al. Coated-platelet trends predict short-term clinical outcome after subarachnoid hemorrhage. Transl Stroke Res 2018; 9 (05) 459-470
    CrossrefPubMedGoogle Scholar
  • 77 Prodan CI, Vincent AS, Padmanabhan R, Dale GL. Coated-platelet levels are low in patients with spontaneous intracerebral hemorrhage. Stroke 2009; 40 (07) 2578-2580
    CrossrefPubMedGoogle Scholar
  • 78 Prodan CI, Vincent AS, Dale GL. Coated platelet levels correlate with bleed volume in patients with spontaneous intracerebral hemorrhage. Stroke 2010; 41 (06) 1301-1303
    CrossrefPubMedGoogle Scholar
  • 79 Prodan CI, Stoner JA, Dale GL. Lower coated-platelet levels are associated with increased mortality after spontaneous intracerebral hemorrhage. Stroke 2015; 46 (07) 1819-1825
    CrossrefPubMedGoogle Scholar
  • 80 Saxena K, Pethe K, Dale GL. Coated-platelet levels may explain some variability in clinical phenotypes observed with severe hemophilia. J Thromb Haemost 2010; 8 (05) 1140-1142
    CrossrefPubMedGoogle Scholar
  • 81 Deb S, Boknäs N, Sjöström C, Tharmakulanathan A, Lotfi K, Ramström S. Varying effects of tyrosine kinase inhibitors on platelet function—a need for individualized CML treatment to minimize the risk for hemostatic and thrombotic complications?. Cancer Med 2020; 9 (01) 313-323
    CrossrefPubMedGoogle Scholar
  • 82 Mezei G, Debreceni IB, Kerenyi A. et al. Dasatinib inhibits coated-platelet generation in patients with chronic myeloid leukemia. Platelets 2019; 30 (07) 836-843
    CrossrefPubMedGoogle Scholar
  • 83 Kostos L, Burbury K, Srivastava G, Prince HM. Gastrointestinal bleeding in a chronic myeloid leukaemia patient precipitated by dasatinib-induced platelet dysfunction: Case report. Platelets 2015; 26 (08) 809-811
    CrossrefPubMedGoogle Scholar
  • 84 Quintás-Cardama A, Kantarjian H, Ravandi F. et al. Bleeding diathesis in patients with chronic myelogenous leukemia receiving dasatinib therapy. Cancer 2009; 115 (11) 2482-2490
    CrossrefPubMedGoogle Scholar
  • 85 Dmitrieva EA, Nikitin EA, Ignatova AA. et al. Platelet function and bleeding in chronic lymphocytic leukemia and mantle cell lymphoma patients on ibrutinib. J Thromb Haemost 2020; 18 (10) 2672-2684
    CrossrefPubMedGoogle Scholar
  • 86 Colucci G, Stutz M, Rochat S. et al. The effect of desmopressin on platelet function: a selective enhancement of procoagulant COAT platelets in patients with primary platelet function defects. Blood 2014; 123 (12) 1905-1916
    CrossrefPubMedGoogle Scholar
  • 87 Kjalke M, Kjellev S, Rojkjaer R. Preferential localization of recombinant factor VIIa to platelets activated with a combination of thrombin and a glycoprotein VI receptor agonist. J Thromb Haemost 2007; 5 (04) 774-780
    CrossrefPubMedGoogle Scholar
  • 88 Podoplelova NA, Sveshnikova AN, Kotova YN. et al. Coagulation factors bound to procoagulant platelets concentrate in cap structures to promote clotting. Blood 2016; 128 (13) 1745-1755
    CrossrefPubMedGoogle Scholar