Download PDF
Semin Thromb Hemost 2022; 48(05): 552-567
DOI: 10.1055/s-0042-1749660
Review Article

Colchicine as a Modulator of Platelet Function: A Systematic Review

Caroline J. Reddel
1   ANZAC Research Institute, University of Sydney, Concord Repatriation General Hospital, Sydney, Australia
,
Gabrielle J. Pennings
1   ANZAC Research Institute, University of Sydney, Concord Repatriation General Hospital, Sydney, Australia
,
Vivien M. Chen
1   ANZAC Research Institute, University of Sydney, Concord Repatriation General Hospital, Sydney, Australia
2   Department of Haematology, Concord Repatriation General Hospital, Sydney, Australia
,
Sonali Gnanenthiran
1   ANZAC Research Institute, University of Sydney, Concord Repatriation General Hospital, Sydney, Australia
3   Department of Cardiology, Concord Repatriation General Hospital, Sydney, Australia
,
Leonard Kritharides
1   ANZAC Research Institute, University of Sydney, Concord Repatriation General Hospital, Sydney, Australia
3   Department of Cardiology, Concord Repatriation General Hospital, Sydney, Australia
› Author Affiliations
› Further Information
    Permissions and Reprints

Abstract

The microtubule inhibitor and anti-inflammatory agent colchicine is used to treat a range of conditions involving inflammasome activation in monocytes and neutrophils, and is now known to prevent coronary and cerebrovascular events. In vitro studies dating back more than 50 years showed a direct effect of colchicine on platelets, but as little contemporary attention has been paid to this area, we have critically reviewed the effects of colchicine on diverse aspects of platelet biology in vitro and in vivo. In this systematic review we searched Embase, Medline, and PubMed for articles testing platelets after incubation with colchicine and/or reporting a clinical effect of colchicine treatment on platelet function, including only papers available in English and excluding reviews and conference abstracts. We identified 98 relevant articles and grouped their findings based on the type of study and platelet function test. In vitro, colchicine inhibits traditional platelet functions, including aggregation, clotting, degranulation, and platelet-derived extracellular vesicle formation, although many of these effects were reported at apparently supraphysiological concentrations. Physiological concentrations of colchicine inhibit collagen- and calcium ionophore-induced platelet aggregation and internal signaling. There have been limited studies of in vivo effects on platelets. The colchicine-platelet interaction has the potential to contribute to colchicine-mediated reduction in cardiovascular events, but there is a pressing need for high quality clinical research in this area.

Keywords

colchicine - inflammation - platelets

Supplementary Material



Publication History

Article published online:
26 July 2022

© 2022. Thieme. All rights reserved.

Thieme Medical Publishers, Inc.
333 Seventh Avenue, 18th Floor, New York, NY 10001, USA

 

  • References

  • 1 Ridker PM, Everett BM, Thuren T. et al; CANTOS Trial Group. Antiinflammatory therapy with canakinumab for atherosclerotic disease. N Engl J Med 2017; 377 (12) 1119-1131
    CrossrefPubMedGoogle Scholar
  • 2 Papageorgiou N, Briasoulis A, Lazaros G, Imazio M, Tousoulis D. Colchicine for prevention and treatment of cardiac diseases: a meta-analysis. Cardiovasc Ther 2017; 35 (01) 10-18
    CrossrefPubMedGoogle Scholar
  • 3 Verma S, Eikelboom JW, Nidorf SM. et al. Colchicine in cardiac disease: a systematic review and meta-analysis of randomized controlled trials. BMC Cardiovasc Disord 2015; 15: 96
    CrossrefPubMedGoogle Scholar
  • 4 Katsanos AH, Palaiodimou L, Price C. et al. Colchicine for stroke prevention in patients with coronary artery disease: a systematic review and meta-analysis. Eur J Neurol 2020; 27 (06) 1035-1038
    CrossrefPubMedGoogle Scholar
  • 5 Nidorf SM, Fiolet ATL, Mosterd A. et al; LoDoCo2 Trial Investigators. Colchicine in patients with chronic coronary disease. N Engl J Med 2020; 383 (19) 1838-1847
    CrossrefPubMedGoogle Scholar
  • 6 Fiolet ATL, Opstal TSJ, Mosterd A. et al. Efficacy and safety of low-dose colchicine in patients with coronary disease: a systematic review and meta-analysis of randomized trials. Eur Heart J 2021; 42 (28) 2765-2775
    CrossrefPubMedGoogle Scholar
  • 7 Bhattacharyya B, Panda D, Gupta S, Banerjee M. Anti-mitotic activity of colchicine and the structural basis for its interaction with tubulin. Med Res Rev 2008; 28 (01) 155-183
    CrossrefPubMedGoogle Scholar
  • 8 Hastie SB. Interactions of colchicine with tubulin. Pharmacol Ther 1991; 51 (03) 377-401
    CrossrefPubMedGoogle Scholar
  • 9 Lievens D, von Hundelshausen P. Platelets in atherosclerosis. Thromb Haemost 2011; 106 (05) 827-838
    PubMedGoogle Scholar
  • 10 Baigent C, Blackwell L, Collins R. et al; Antithrombotic Trialists' (ATT) Collaboration. Aspirin in the primary and secondary prevention of vascular disease: collaborative meta-analysis of individual participant data from randomised trials. Lancet 2009; 373 (9678): 1849-1860
    CrossrefPubMedGoogle Scholar
  • 11 Reddel CJ, Pennings GJ, Curnow JL, Chen VM, Kritharides L. Procoagulant effects of low-level platelet activation and its inhibition by colchicine. Thromb Haemost 2018; 118 (04) 723-733
    PubMedGoogle Scholar
  • 12 Mody M, Lazarus AH, Semple JW, Freedman J. Preanalytical requirements for flow cytometric evaluation of platelet activation: choice of anticoagulant. Transfus Med 1999; 9 (02) 147-154
    CrossrefPubMedGoogle Scholar
  • 13 Kenney DM, Chao FC, Tullis JL, Conneely GS. Colchicine uptake and binding by human platelets. Thromb Diath Haemorrh 1975; 34 (03) 780-794
    PubMedGoogle Scholar
  • 14 Deftereos S, Giannopoulos G, Papoutsidakis N. et al. Colchicine and the heart: pushing the envelope. J Am Coll Cardiol 2013; 62 (20) 1817-1825
    CrossrefPubMedGoogle Scholar
  • 15 Chappey O, Niel E, Dervichian M, Wautier JL, Scherrmann JM, Cattan D. Colchicine concentration in leukocytes of patients with familial Mediterranean fever. Br J Clin Pharmacol 1994; 38 (01) 87-89
    CrossrefPubMedGoogle Scholar
  • 16 Ferron GM, Rochdi M, Jusko WJ, Scherrmann JM. Oral absorption characteristics and pharmacokinetics of colchicine in healthy volunteers after single and multiple doses. J Clin Pharmacol 1996; 36 (10) 874-883
    CrossrefPubMedGoogle Scholar
  • 17 Niel E, Scherrmann JM. Colchicine today. Joint Bone Spine 2006; 73 (06) 672-678
    CrossrefPubMedGoogle Scholar
  • 18 Rochdi M, Sabouraud A, Girre C, Venet R, Scherrmann JM. Pharmacokinetics and absolute bioavailability of colchicine after i.v. and oral administration in healthy human volunteers and elderly subjects. Eur J Clin Pharmacol 1994; 46 (04) 351-354
    CrossrefPubMedGoogle Scholar
  • 19 Rochdi M, Sabouraud A, Baud FJ, Bismuth C, Scherrmann JM. Toxicokinetics of colchicine in humans: analysis of tissue, plasma and urine data in ten cases. Hum Exp Toxicol 1992; 11 (06) 510-516
    CrossrefPubMedGoogle Scholar
  • 20 Sabouraud A, Chappey O, Dupin T, Scherrmann JM. Binding of colchicine and thiocolchicoside to human serum proteins and blood cells. Int J Clin Pharmacol Ther 1994; 32 (08) 429-432
    PubMedGoogle Scholar
  • 21 Kenney DM, Chao FC. Microtubule inhibitors alter the secretion of beta-glucuronidase by human blood platelets: involvement of microtubules in release reaction II. J Cell Physiol 1978; 96 (01) 43-52
    CrossrefPubMedGoogle Scholar
  • 22 Taylor EW. The mechanism of colchicine inhibition of mitosis. I. Kinetics of inhibition and the binding of H3-colchicine. J Cell Biol 1965; 25 (suppl): 145-160
    CrossrefPubMedGoogle Scholar
  • 23 Thon JN, Italiano JE. Platelets: production, morphology and ultrastructure. Handb Exp Pharmacol 2012; (Suppl. 210) 3-22
    CrossrefPubMedGoogle Scholar
  • 24 Cuenca-Zamora EJ, Ferrer-Marín F, Rivera J, Teruel-Montoya R. Tubulin in platelets: when the shape matters. Int J Mol Sci 2019; 20 (14) 20
    CrossrefPubMedGoogle Scholar
  • 25 Sadoul K. New explanations for old observations: marginal band coiling during platelet activation. J Thromb Haemost 2015; 13 (03) 333-346
    CrossrefPubMedGoogle Scholar
  • 26 Wang DL, Chang YN, Hsu HT, Usami S, Chien S. Prostaglandin E1 and dibutyryl cyclic AMP enhance platelet resistance to deformation. Thromb Res 1992; 65 (06) 757-768
    CrossrefPubMedGoogle Scholar
  • 27 White JG. Effects of colchicine and Vinca alkaloids on human platelets. I. Influence on platelet microtubules and contractile function. Am J Pathol 1968; 53 (02) 281-291
    PubMedGoogle Scholar
  • 28 Zucker-Franklin D. Microfibrils of blood platelets: their relationship to microtubules and the contractile protein. J Clin Invest 1969; 48 (01) 165-175
    CrossrefPubMedGoogle Scholar
  • 29 Takeuchi K, Kuroda K, Ishigami M, Nakamura T. Actin cytoskeleton of resting bovine platelets. Exp Cell Res 1990; 186 (02) 374-380
    CrossrefPubMedGoogle Scholar
  • 30 Cimmino G, Tarallo R, Conte S. et al. Colchicine reduces platelet aggregation by modulating cytoskeleton rearrangement via inhibition of cofilin and LIM domain kinase 1. Vascul Pharmacol 2018; 111: 62-70
    CrossrefPubMedGoogle Scholar
  • 31 Sneddon JM. Effect of mitosis inhibitors on blood platelet microtubules and aggregation. J Physiol 1971; 214 (01) 145-158
    CrossrefPubMedGoogle Scholar
  • 32 Cañizares C, Vivar N, Herdoiza M. Role of the microtubular system in platelet aggregation. Braz J Med Biol Res 1994; 27 (07) 1533-1551
    PubMedGoogle Scholar
  • 33 White JG, Rao GH. Microtubule coils versus the surface membrane cytoskeleton in maintenance and restoration of platelet discoid shape. Am J Pathol 1998; 152 (02) 597-609
    PubMedGoogle Scholar
  • 34 Bouaziz A, Amor NB, Woodard GE. et al. Tyrosine phosphorylation / dephosphorylation balance is involved in thrombin-evoked microtubular reorganisation in human platelets. Thromb Haemost 2007; 98 (02) 375-384
    Article in Thieme ConnectPubMedGoogle Scholar
  • 35 Gear AR. Preaggregation reactions of platelets. Blood 1981; 58 (03) 477-490
    CrossrefPubMedGoogle Scholar
  • 36 Laufer N, Grover NB, Ben-Sasson S, Freund H. Effects of adenosine diphosphate, colchicine and temperature on size of human platelets. Thromb Haemost 1979; 41 (03) 491-497
    Article in Thieme ConnectPubMedGoogle Scholar
  • 37 Hardwick RA, Gritsman HN, Stromberg RR, Friedman LI. The biochemical mechanisms of shear-induced platelet aggregation. Trans Am Soc Artif Intern Organs 1983; 29: 448-453
    PubMedGoogle Scholar
  • 38 Mooney JJ, Chao FC, Orsulak PJ, Schildkraut JJ. An improved method for the recovery of mitochondrial monoamine oxidase from human platelets using colchicine and nitrogen decompression. Biochem Med 1981; 26 (02) 156-166
    CrossrefPubMedGoogle Scholar
  • 39 Pennings GJ, Reddel CJ, Traini M, Campbell H, Chen V, Kritharides L. Colchicine inhibits ROS generation in response to glycoprotein VI stimulation. Sci Rep 2021; 11 (01) 11965
    CrossrefPubMedGoogle Scholar
  • 40 White JG. Effects of colchicine and vinca alkaloids on human platelets. II. Changes in the dense tubular system and formation of an unusual inclusion in incubated cells. Am J Pathol 1968; 53 (03) 447-461
    PubMedGoogle Scholar
  • 41 Hovig T. Influence of various compounds and surfaces on blood platelets and platelet aggregates. A scanning electron microscopic study. Ser Haematol 1970; 3 (04) 47-67
    PubMedGoogle Scholar
  • 42 White JG. Effects of colchicine and vinca alkaloids on human platelets. 3. Influence on primary internal contraction and secondary aggregation. Am J Pathol 1969; 54 (03) 467-478
    PubMedGoogle Scholar
  • 43 Steiner M, Lüscher EF. Platelet activation studied by fluorescence polarization. Biochim Biophys Acta 1984; 803 (1-2): 48-53
    CrossrefPubMedGoogle Scholar
  • 44 Cerecedo D, Stock R, González S, Reyes E, Mondragón R. Modification of actin, myosin and tubulin distribution during cytoplasmic granule movements associated with platelet adhesion. Haematologica 2002; 87 (11) 1165-1176
    PubMedGoogle Scholar
  • 45 Booyse FM, Rafelson Jr ME. Regulation and mechanism of platelet aggregation. Ann N Y Acad Sci 1972; 201: 37-60
    CrossrefPubMedGoogle Scholar
  • 46 Shiba M, Watanabe E, Sasakawa S, Ikeda Y. Effects of taxol and colchicine on platelet membrane properties. Thromb Res 1988; 52 (04) 313-323
    CrossrefPubMedGoogle Scholar
  • 47 Jung SM, Moroi M. Platelet cytoskeletal protein distributions in two triton-insoluble fractions and how they are affected by stimulants and reagents that modify cytoskeletal protein interactions. Thromb Res 1988; 50 (06) 775-787
    CrossrefPubMedGoogle Scholar
  • 48 Pribluda V, Rotman A. Dynamics of membrane-cytoskeleton interactions in activated blood platelets. Biochemistry 1982; 21 (12) 2825-2832
    CrossrefPubMedGoogle Scholar
  • 49 Cerecedo D, Cisneros B, Mondragón R, González S, Galván IJ. Actin filaments and microtubule dual-granule transport in human adhered platelets: the role of alpha-dystrobrevins. Br J Haematol 2010; 149 (01) 124-136
    CrossrefPubMedGoogle Scholar
  • 50 Ribbi-Jaffe A, Apitz-Castro R. The effect of colchicine on human blood platelets under conditions of short-term incubation. Biochem J 1979; 178 (02) 449-454
    CrossrefPubMedGoogle Scholar
  • 51 Kenney DM, Chao FC. Ionophore-induced disassembly of blood platelet microtubules: effect of cyclic AMP and indomethacin. J Cell Physiol 1980; 103 (02) 289-298
    CrossrefPubMedGoogle Scholar
  • 52 Menche D, Israel A, Karpatkin S. Platelets and microtubules. Effect of colchicine and D2O on platelet aggregation and release induced by calcium ionophore A23187. J Clin Invest 1980; 66 (02) 284-291
    PubMedGoogle Scholar
  • 53 Steiner M. Membrane-bound tubulin in human platelets. Biochim Biophys Acta 1983; 729 (01) 17-22
    CrossrefPubMedGoogle Scholar
  • 54 Weiner JL, Buhler AV, Whatley VJ, Harris RA, Dunwiddie TV. Colchicine is a competitive antagonist at human recombinant gamma-aminobutyric acid A receptors. J Pharmacol Exp Ther 1998; 284 (01) 95-102
    PubMedGoogle Scholar
  • 55 Zhou X, Wu M, Xie Y. et al. Identification of glycine receptor α3 as a colchicine-binding protein. Front Pharmacol 2018; 9: 1238
    CrossrefPubMedGoogle Scholar
  • 56 Shah B, Allen N, Harchandani B. et al. Effect of colchicine on platelet-platelet and platelet-leukocyte interactions: a pilot study in healthy subjects. Inflammation 2016; 39 (01) 182-189
    CrossrefPubMedGoogle Scholar
  • 57 Lindgren JA, Claesson HE, Kindahl H, Hammarström S. Effects of adenosine 3′:5′-monophosphate and platelet aggregation on thromboxane biosynthesis in human platelets. FEBS Lett 1979; 98 (02) 247-250
    CrossrefPubMedGoogle Scholar
  • 58 Soppitt GD, Mitchell JR. The effect of colchicine on human platelet behaviour. J Atheroscler Res 1969; 10 (02) 247-252
    CrossrefPubMedGoogle Scholar
  • 59 Kirby EP, Mills DC, Holmsen H, Russo M. Factor VIII-induced superaggregation of human platelets. Blood 1982; 60 (06) 1359-1369
    CrossrefPubMedGoogle Scholar
  • 60 Sweeney JD, Labuzetta JW, Bernstein ZP, Bielat KL, Fitzpatrick JE. Ristocetin-induced platelet aggregate formation and adherence to the probe of an impedance aggregometer. Am J Clin Pathol 1990; 93 (04) 548-551
    CrossrefPubMedGoogle Scholar
  • 61 Coller BS. Inhibition of von Willebrand factor-dependent platelet function by increased platelet cyclic AMP and its prevention by cytoskeleton-disrupting agents. Blood 1981; 57 (05) 846-855
    CrossrefPubMedGoogle Scholar
  • 62 Cirillo P, Taglialatela V, Pellegrino G. et al. Effects of colchicine on platelet aggregation in patients on dual antiplatelet therapy with aspirin and clopidogrel. J Thromb Thrombolysis 2020; 50 (02) 468-472
    CrossrefPubMedGoogle Scholar
  • 63 Peerschke EI, Zucker MB. Relationship of ADP-induced fibrinogen binding to platelet shape change and aggregation elucidated by use of colchicine and cytochalasin B. Thromb Haemost 1980; 43 (01) 58-60
    Article in Thieme ConnectPubMedGoogle Scholar
  • 64 Harfenist EJ, Packham MA, Kinlough-Rathbone RL, Mustard JF. Inhibitors of ADP-induced platelet aggregation prevent fibrinogen binding to rabbit platelets and cause rapid deaggregation and dissociation of bound fibrinogen. J Lab Clin Med 1981; 97 (05) 680-688
    PubMedGoogle Scholar
  • 65 Jen CJ, Li HM, Wang JS, Chen HI, Usami S. Flow-induced detachment of adherent platelets from fibrinogen-coated surface. Am J Physiol 1996; 270 (1 Pt 2): H160-H166
    PubMedGoogle Scholar
  • 66 Cazenave JP, Packham MA, Guccione MA, Mustard JF. Inhibition of platelet adherence to a collagen-coated surface by agents that inhibit platelet shape change and clot retraction. J Lab Clin Med 1974; 84 (04) 483-493
    PubMedGoogle Scholar
  • 67 Cronstein BN, Molad Y, Reibman J, Balakhane E, Levin RI, Weissmann G. Colchicine alters the quantitative and qualitative display of selectins on endothelial cells and neutrophils. J Clin Invest 1995; 96 (02) 994-1002
    CrossrefPubMedGoogle Scholar
  • 68 Kakaiya RM, Kiraly TL, Cable RG. Concanavalin A induces patching/capping of the platelet membrane glycoprotein IIb/IIIa complex. Thromb Haemost 1988; 59 (02) 281-283
    Article in Thieme ConnectPubMedGoogle Scholar
  • 69 Gold M, Evensen SA, Belamarich FA, Shepro D. Platelet factor 3 activity made available from human platelets by ADP. Inhibition by colchicine. Thromb Diath Haemorrh 1973; 30 (01) 155-159
    PubMedGoogle Scholar
  • 70 Kawamoto Y, Kaibara M. Reconstituted collagen is not capable of activating factor XII but causes intrinsic coagulation by activating platelets. Blood Coagul Fibrinolysis 1992; 3: 371-379
    CrossrefPubMedGoogle Scholar
  • 71 Kuntamukkula MS, Moake JL, McIntire LV, Cimo PL. Effects of colchicine and vinblastine on platelet contractility and release. Thromb Res 1982; 26 (05) 329-339
    CrossrefPubMedGoogle Scholar
  • 72 Jen CJ, McIntire LV. The structural properties and contractile force of a clot. Cell Motil 1982; 2 (05) 445-455
    CrossrefPubMedGoogle Scholar
  • 73 Jen CJ, McIntire LV. Platelet microtubules in clot structure formation and contractile force generation: investigation of a controversy. Thromb Haemost 1986; 56 (01) 23-27
    Article in Thieme ConnectPubMedGoogle Scholar
  • 74 Shepro D, Belamarich FA, Chao FC. Retardation of clot retraction after incubation of platelets with colchicine and heavy water. Nature 1969; 221 (5180): 563-565
    CrossrefPubMedGoogle Scholar
  • 75 Chao FC, Shepro D, Tullis JL, Belamarich FA, Curby WA. Similarities between platelet contraction and cellular motility during mitosis: role of platelet microtubules in clot retraction. J Cell Sci 1976; 20 (03) 569-588
    CrossrefPubMedGoogle Scholar
  • 76 Kubisz P, Cronberg S. Inhibitory effect of colchicine and vinblastine on reptilase clot retraction. Thromb Res 1976; 9 (02) 109-114
    CrossrefPubMedGoogle Scholar
  • 77 Moake JL, Cimo PL, Widmer K, Peterson DM, Gum JR. Effects of prostaglandins, derivatives of cyclic 3′:5′-AMP, theophylline, cholinergic agents and colchicine on clot retraction in dilute platelet-rich plasma and gel-separated platelet test systems. Thromb Haemost 1977; 38 (02) 420-428
    Article in Thieme ConnectPubMedGoogle Scholar
  • 78 Hua VM, Abeynaike L, Glaros E. et al. Necrotic platelets provide a procoagulant surface during thrombosis. Blood 2015; 126 (26) 2852-2862
    CrossrefPubMedGoogle Scholar
  • 79 Cole NB, Lippincott-Schwartz J. Organization of organelles and membrane traffic by microtubules. Curr Opin Cell Biol 1995; 7 (01) 55-64
    CrossrefPubMedGoogle Scholar
  • 80 Kockx M, Guo DL, Huby T. et al. Secretion of apolipoprotein E from macrophages occurs via a protein kinase A and calcium-dependent pathway along the microtubule network. Circ Res 2007; 101 (06) 607-616
    CrossrefPubMedGoogle Scholar
  • 81 Dai Y, Li J. Evidence for thrombin-induced human platelet secretion regulated by the cytoskeleton. Shi yan sheng wu xue bao 1995; 28: 236-240
    PubMedGoogle Scholar
  • 82 Bennett WF, Belville JS, Lynch G. A study of protein phosphorylation in shape change and Ca++-dependent serotonin release by blood platelets. Cell 1979; 18 (04) 1015-1023
    CrossrefPubMedGoogle Scholar
  • 83 Henson PM, Oades ZG. Activation of platelets by platelet-activating factor (PAF) derived from IgE-sensitized basophils. II. The role of serine proteases, cyclic nucleotides, and contractile elements in PAF-induced secretion. J Exp Med 1976; 143 (04) 953-968
    CrossrefPubMedGoogle Scholar
  • 84 Verhoeven AJ, Mommersteeg ME, Akkerman JW. Comparative studies on the energetics of platelet responses induced by different agonists. Biochem J 1986; 236 (03) 879-887
    CrossrefPubMedGoogle Scholar
  • 85 Zucker MB. Proteolytic inhibitors, contact and other variables in the release reaction of human platelets. Thromb Diath Haemorrh 1972; 28 (03) 393-407
    PubMedGoogle Scholar
  • 86 Jung SM, Yamazaki H, Tetsuka T, Moroi M. Effect of nocodazole, a new microtubule inhibitor, on platelet aggregation and release. Thromb Res 1981; 23 (4-5): 401-410
    CrossrefPubMedGoogle Scholar
  • 87 Friedman F, Detwiler TC. Stimulus-secretion coupling in platelets. Effects of drugs on secretion on adenosine 5′-triphosphate. Biochemistry 1975; 14 (06) 1315-1320
    CrossrefPubMedGoogle Scholar
  • 88 Redondo PC, Harper AG, Sage SO, Rosado JA. Dual role of tubulin-cytoskeleton in store-operated calcium entry in human platelets. Cell Signal 2007; 19 (10) 2147-2154
    CrossrefPubMedGoogle Scholar
  • 89 Bourguignon LY, Iida N, Jin H. The involvement of the cytoskeleton in regulating IP3 receptor-mediated internal Ca2+ release in human blood platelets. Cell Biol Int 1993; 17 (08) 751-758
    CrossrefPubMedGoogle Scholar
  • 90 van der Stoep M, Korporaal SJ, Van Eck M. High-density lipoprotein as a modulator of platelet and coagulation responses. Cardiovasc Res 2014; 103 (03) 362-371
    CrossrefPubMedGoogle Scholar
  • 91 Martin-Nizard F, Richard B, Torpier G. et al. Analysis of phospholipid transfer during HDL binding to platelets using a fluorescent analog of phosphatidylcholine. Thromb Res 1987; 46 (06) 811-825
    CrossrefPubMedGoogle Scholar
  • 92 Pedreño J, Vila M, Masana L. Mechanisms for regulating platelet high density lipoprotein type3 binding sites: evidence that binding sites are downregulated by a protein kinase C-dependent mechanism. Thromb Res 1999; 94 (01) 33-44
    CrossrefPubMedGoogle Scholar
  • 93 Pedreño J, de Castellarnau C, Cullaré C. et al. Platelet LDL receptor recognizes with the same apparent affinity both oxidized and native LDL. Evidence that the receptor-ligand complexes are not internalized. Arterioscler Thromb 1994; 14 (03) 401-408
    CrossrefPubMedGoogle Scholar
  • 94 Wolkers WF, Looper SA, Fontanilla RA, Tsvetkova NM, Tablin F, Crowe JH. Temperature dependence of fluid phase endocytosis coincides with membrane properties of pig platelets. Biochim Biophys Acta 2003; 1612 (02) 154-163
    CrossrefPubMedGoogle Scholar
  • 95 Nishio H, Segawa T, Takagi H. Effect of cold treatment and some drugs on the 5-hydroxytryptamine uptake by rabbit blood platelets and their ultrastructure. Jpn J Pharmacol 1979; 29 (01) 77-86
    CrossrefPubMedGoogle Scholar
  • 96 Setiadi H, Herington AC. Specific non-saturable binding of insulin by human platelets. Mol Cell Endocrinol 1985; 43 (01) 23-30
    CrossrefPubMedGoogle Scholar
  • 97 Nishio H, Segawa T, Takagi H. Effects of concanavalin A on 5-hydroxytryptamine uptake by rabbit blood platelets and on their ultrastructure. Br J Pharmacol 1979; 65 (04) 557-563
    CrossrefPubMedGoogle Scholar
  • 98 Secret CJ, Hadfield JR, Beer CT. Studies on the binding of ( 3 H)vinblastine by rat blood platelets in vitro. Effects of colchicine and vincristine. Biochem Pharmacol 1972; 21 (11) 1609-1624
    CrossrefPubMedGoogle Scholar
  • 99 Wittels E, Israel A, Karpatkin S. Evidence for colchicine-dependent protease activity in human platelets. Thromb Res 1981; 24 (03) 215-221
    CrossrefPubMedGoogle Scholar
  • 100 Zhang B, Huang R, Yang D. et al. Combination of colchicine and ticagrelor inhibits carrageenan-induced thrombi in mice. Oxid Med Cell Longev 2022; 2022: 3087198
    PubMedGoogle Scholar
  • 101 Oggero S, Austin-Williams S, Norling LV. The contrasting role of extracellular vesicles in vascular inflammation and tissue repair. Front Pharmacol 2019; 10: 1479
    CrossrefPubMedGoogle Scholar
  • 102 Théry C, Witwer KW, Aikawa E. et al. Minimal information for studies of extracellular vesicles 2018 (MISEV2018): a position statement of the International Society for Extracellular Vesicles and update of the MISEV2014 guidelines. J Extracell Vesicles 2018; 7 (01) 1535750
    CrossrefPubMedGoogle Scholar
  • 103 van Niel G, D'Angelo G, Raposo G. Shedding light on the cell biology of extracellular vesicles. Nat Rev Mol Cell Biol 2018; 19 (04) 213-228
    CrossrefPubMedGoogle Scholar
  • 104 Freikman I, Ringel I, Fibach E. Shedding of phosphatidylserine from developing erythroid cells involves microtubule depolymerization and affects membrane lipid composition. J Membr Biol 2012; 245 (12) 779-787
    CrossrefPubMedGoogle Scholar
  • 105 Meshki J, Douglas SD, Hu M, Leeman SE, Tuluc F. Substance P induces rapid and transient membrane blebbing in U373MG cells in a p21-activated kinase-dependent manner. PLoS One 2011; 6 (09) e25332
    CrossrefPubMedGoogle Scholar
  • 106 Kobayashi T, Yamada J, Setaka M, Kwan T. Effects of chlorpromazine and other calmodulin antagonists on phosphatidylcholine-induced vesiculation of platelet plasma membranes. Biochim Biophys Acta 1986; 855 (01) 58-62
    CrossrefPubMedGoogle Scholar
  • 107 Skarlatos SI, Amende LM, Chao FF, Blanchette-Mackie EJ, Gamble W, Kruth HS. Biochemical characterization of isolated cholesterol-phospholipid particles continuously released from rat and human platelets after activation. Lab Invest 1988; 59 (03) 344-352
    PubMedGoogle Scholar
  • 108 Simonsen JB. What are we looking at? Extracellular vesicles, lipoproteins, or both?. Circ Res 2017; 121 (08) 920-922
    CrossrefPubMedGoogle Scholar
  • 109 Molad Y. Update on colchicine and its mechanism of action. Curr Rheumatol Rep 2002; 4 (03) 252-256
    CrossrefPubMedGoogle Scholar
  • 110 Martínez GJ, Celermajer DS, Patel S. The NLRP3 inflammasome and the emerging role of colchicine to inhibit atherosclerosis-associated inflammation. Atherosclerosis 2018; 269: 262-271
    CrossrefPubMedGoogle Scholar
  • 111 Akodad M, Fauconnier J, Sicard P. et al. Interest of colchicine in the treatment of acute myocardial infarct responsible for heart failure in a mouse model. Int J Cardiol 2017; 240: 347-353
    CrossrefPubMedGoogle Scholar
  • 112 Mewton N, Roubille F, Bresson D. et al. Effect of colchicine on myocardial injury in acute myocardial infarction. Circulation 2021; 144 (11) 859-869
    CrossrefPubMedGoogle Scholar
  • 113 Opstal TSJ, Hoogeveen RM, Fiolet ATL. et al. Colchicine attenuates inflammation beyond the inflammasome in chronic coronary artery disease: a LoDoCo2 proteomic substudy. Circulation 2020; 142 (20) 1996-1998
    CrossrefPubMedGoogle Scholar
  • 114 Tucker B, Kurup R, Barraclough J. et al. Colchicine as a novel therapy for suppressing chemokine production in patients with an acute coronary syndrome: a pilot study. Clin Ther 2019; 41 (10) 2172-2181
    CrossrefPubMedGoogle Scholar
  • 115 Rayes J, Watson SP, Nieswandt B. Functional significance of the platelet immune receptors GPVI and CLEC-2. J Clin Invest 2019; 129 (01) 12-23
    CrossrefPubMedGoogle Scholar
  • 116 Andrews RK, Arthur JF, Gardiner EE. Targeting GPVI as a novel antithrombotic strategy. J Blood Med 2014; 5: 59-68
    PubMedGoogle Scholar
  • 117 Lindemann S, Tolley ND, Dixon DA. et al. Activated platelets mediate inflammatory signaling by regulated interleukin 1beta synthesis. J Cell Biol 2001; 154 (03) 485-490
    CrossrefPubMedGoogle Scholar
  • 118 Brown GT, McIntyre TM. Lipopolysaccharide signaling without a nucleus: kinase cascades stimulate platelet shedding of proinflammatory IL-1β-rich microparticles. J Immunol 2011; 186 (09) 5489-5496
    CrossrefPubMedGoogle Scholar
  • 119 Hottz ED, Lopes JF, Freitas C. et al. Platelets mediate increased endothelium permeability in dengue through NLRP3-inflammasome activation. Blood 2013; 122 (20) 3405-3414
    CrossrefPubMedGoogle Scholar
  • 120 Murthy P, Durco F, Miller-Ocuin JL. et al. The NLRP3 inflammasome and bruton's tyrosine kinase in platelets co-regulate platelet activation, aggregation, and in vitro thrombus formation. Biochem Biophys Res Commun 2017; 483 (01) 230-236
    CrossrefPubMedGoogle Scholar
  • 121 Pennings GJ, Reddel CJ, Traini M. et al. Rapid release of interleukin-1β from human platelets is independent of NLRP3 and caspase. Thromb Haemost 2021
    PubMedGoogle Scholar
  • 122 Rolfes V, Ribeiro LS, Hawwari I. et al. Platelets fuel the inflammasome activation of innate immune cells. Cell Rep 2020; 31 (06) 107615
    CrossrefPubMedGoogle Scholar
  • 123 Sheikh S, Rahman M, Gale Z. et al. Differing mechanisms of leukocyte recruitment and sensitivity to conditioning by shear stress for endothelial cells treated with tumour necrosis factor-alpha or interleukin-1beta. Br J Pharmacol 2005; 145 (08) 1052-1061
    CrossrefPubMedGoogle Scholar
  • 124 Lisman T. Platelet-neutrophil interactions as drivers of inflammatory and thrombotic disease. Cell Tissue Res 2018; 371 (03) 567-576
    CrossrefPubMedGoogle Scholar
  • 125 Zucoloto AZ, Jenne CN. Platelet-neutrophil interplay: insights into neutrophil extracellular trap (NET)-driven coagulation in infection. Front Cardiovasc Med 2019; 6: 85
    CrossrefPubMedGoogle Scholar
  • 126 Vaidya K, Tucker B, Kurup R. et al. Colchicine inhibits neutrophil extracellular trap formation in patients with acute coronary syndrome after percutaneous coronary intervention. J Am Heart Assoc 2021; 10 (01) e018993
    CrossrefPubMedGoogle Scholar
  • 127 Raju NC, Yi Q, Nidorf M, Fagel ND, Hiralal R, Eikelboom JW. Effect of colchicine compared with placebo on high sensitivity C-reactive protein in patients with acute coronary syndrome or acute stroke: a pilot randomized controlled trial. J Thromb Thrombolysis 2012; 33 (01) 88-94
    CrossrefPubMedGoogle Scholar
  • 128 Onat AM, Ozçakar L, Oztürk MA. et al. Plasma and platelet serotonin levels in familial Mediterranean fever. Clin Exp Rheumatol 2007; 25 (04, Suppl 45) S16-S20
    PubMedGoogle Scholar
  • 129 Ataş H, Cemil BC, Canpolat F, Gönül M. The effect of colchicine on mean platelet volume in Behcet's disease. Ann Clin Lab Sci 2015; 45 (05) 545-549
    PubMedGoogle Scholar
  • 130 Coban E, Adanir H. Platelet activation in patients with familial Mediterranean fever. Platelets 2008; 19 (06) 405-408
    CrossrefPubMedGoogle Scholar
  • 131 Seçkin HY, Bütün I, Baş Y, Takcı Z, Kalkan G. Effects of colchicine treatment on mean platelet volume and the inflammatory markers in recurrent aphthous stomatitis. J Dermatolog Treat 2016; 27 (04) 389-391
    CrossrefPubMedGoogle Scholar
  • 132 Gasecka A, Nieuwland R, Budnik M. et al. Ticagrelor attenuates the increase of extracellular vesicle concentrations in plasma after acute myocardial infarction compared to clopidogrel. J Thromb Haemost 2020; 18 (03) 609-623
    CrossrefPubMedGoogle Scholar
  • 133 Silvis MJM, Fiolet ATL, Opstal TSJ. et al. Colchicine reduces extracellular vesicle NLRP3 inflammasome protein levels in chronic coronary disease: a LoDoCo2 biomarker substudy. Atherosclerosis 2021; 334: 93-100
    CrossrefPubMedGoogle Scholar
  • 134 White JG, Burris SM, Tukey D, Smith II C, Clawson CC. Micropipette aspiration of human platelets: influence of microtubules and actin filaments on deformability. Blood 1984; 64 (01) 210-214
    PubMedGoogle Scholar
  • 135 Ariad S, Dvilansky A, Nathan I. Effect of activators and inhibitors on human blood platelets: study by freeze-fracturing technique and electron microscopy. Int J Tissue React 1984; 6 (04) 311-315
    PubMedGoogle Scholar
  • 136 Lewis JC, White MS, Prater T, Taylor RG, Davis KS. Ultrastructural analysis of platelets in nonhuman primates. III. Stereo microscopy of microtubules during platelet adhesion and the release reaction. Exp Mol Pathol 1982; 37 (03) 370-381
    PubMedGoogle Scholar
  • 137 Kattlove HE. Primary platelet aggregation. Energy metabolism and the effect of inhibitors. Biochim Biophys Acta 1974; 372 (01) 135-140
    CrossrefPubMedGoogle Scholar
  • 138 Join F, Tremblay F. Platelet reactions and immune processes. II. The inhibition of platelet aggregation by complement inhibitors. Thromb Diath Haemorrh 1969; 22 (03) 466-481
    PubMedGoogle Scholar
  • 139 Ben Amor N, Bouaziz A, Romera-Castillo C. et al. Characterization of the intracellular mechanisms involved in the antiaggregant properties of cinnamtannin B-1 from bay wood in human platelets. J Med Chem 2007; 50 (16) 3937-3944
    CrossrefPubMedGoogle Scholar
  • 140 Herman GE, Seegers WH, Henry RL. Autoprothrombin ii-a, thrombin, and epinephrine: interrelated effects on platelet aggregation. Bibl Haematol 1977; 44: 21-27
    PubMedGoogle Scholar
  • 141 Rodriguez-Linares B, Cano E. In-vitro platelet responses to arachidonic acid in the rat. J Pharm Pharmacol 1995; 47 (12A): 1015-1020
    CrossrefPubMedGoogle Scholar
  • 142 Levy-Toledano S, Maclouf J, Bryon P, Savariau E, Hardisty RM, Caen JP. Human platelet activation in the absence of aggregation: a calcium-dependent phenomenon independent of thromboxane formation. Blood 1982; 59 (05) 1078-1085
    CrossrefPubMedGoogle Scholar
  • 143 Rendu F, Lebret M. Interaction of wheat germ agglutinin with human platelets: a model for studying platelet response. Thromb Res 1984; 36 (05) 447-456
    CrossrefPubMedGoogle Scholar
  • 144 Shah VO, Zamora PO, Mills SL, Mann PL, Comp PC. In vitro studies with the platelet-reactive antibody 50H.19 and its fragments. Thromb Res 1990; 58 (05) 493-504
    CrossrefPubMedGoogle Scholar
  • 145 Jen CJ, Chen HI, Lai KC, Usami S. Changes in cytosolic calcium concentrations and cell morphology in single platelets adhered to fibrinogen-coated surface under flow. Blood 1996; 87 (09) 3775-3782
    CrossrefPubMedGoogle Scholar
  • 146 Bennett WF, Glenn KC. Hypersensitivity of platelets to thrombin: formation of stable thrombin-receptor complexes and the role of shape change. Cell 1980; 22 (2 Pt 2): 621-627
    CrossrefPubMedGoogle Scholar
  • 147 Martin JF, Greaves M. Vincristine inhibits the synthesis of malondialdehyde by human platelets in vitro. Cancer 1982; 49 (04) 665-668
    CrossrefPubMedGoogle Scholar
  • 148 Conway R, Murphy CL, Madigan A. et al. Increased platelet reactivity as measured by plasma glycoprotein VI in gout. Platelets 2018; 29 (08) 821-826
    CrossrefPubMedGoogle Scholar
  • 149 Abanonu GB, Daskin A, Akdogan MF, Uyar S, Demirtunc R. Mean platelet volume and β-thromboglobulin levels in familial Mediterranean fever: effect of colchicine use?. Eur J Intern Med 2012; 23 (07) 661-664
    CrossrefPubMedGoogle Scholar
  • 150 Arıca S, Ozer C, Arıca V, Karakuş A, Celik T, Güneşaçar R. Evaluation of the mean platelet volume in children with familial Mediterranean fever. Rheumatol Int 2012; 32 (11) 3559-3563
    CrossrefPubMedGoogle Scholar