Cytosolic and mitochondrial Ca²⁺ signaling in procoagulant platelets

References

• Huber K, Bates ER, Valgimigli M, Wallentin L, Kristensen SD, Anderson JL, Lopez Sendon JL, Tubaro M, Granger CB, Bode C, et al. Antiplatelet and anticoagulation agents in acute coronary syndromes: what is the current status and what does the future hold? Am Heart J 2014;1685:611–621. DOI:https://doi.org/10.1016/j.ahj.2014.06.014.
   PubMed Web of Science ®Google Scholar
• Capranzano P, Capodanno D. Dual antiplatelet therapy in patients with diabetes mellitus: special considerations. Expert Rev Cardiovasc Ther 2013;113:307–317. DOI:https://doi.org/10.1586/erc.13.3.
   PubMedGoogle Scholar
• Jackson SP. Arterial thrombosis-insidious, unpredictable and deadly. Nat Med 2011;1711:1423–1436. DOI:https://doi.org/10.1038/nm.2515.
   PubMed Web of Science ®Google Scholar
• Munnix ICA, Kuijpers MJE, Auger J, Thomassen CMLGD, Panizzi P, van Zandvoort MAM, Rosing J, Bock PE, Watson SP, Heemskerk JWM, Munnix ICAA, Kuijpers MJEE, Auger J, Thomassen CMLGDLGD, Panizzi P, van Zandvoort MAMM, Rosing J, Bock PE, Watson SP, Heemskerk JWMM. Segregation of platelet aggregatory and procoagulant microdomains in thrombus formation - regulation by transient integrin activation. Arterioscler Thromb Vasc Biol 2007;2711:2484–2490. DOI:https://doi.org/10.1161/ATVBAHA.107.151100.
   PubMed Web of Science ®Google Scholar
• Heemskerk JWM, Mattheij NJA, Cosemans JMEM. Platelet-based coagulation: different populations, different functions. J Thromb Haemost 2013;111:2–16. DOI:https://doi.org/10.1111/jth.12045.
   PubMed Web of Science ®Google Scholar
• Monroe DM, Hoffman M, Roberts HR. Platelets and Thrombin Generation. Arterioscler Thromb Vasc Biol 2002;229:1381–1389. DOI:https://doi.org/10.1161/01.ATV.0000031340.68494.34.
   PubMed Web of Science ®Google Scholar
• Monroe DM, Hoffman M. What does it take to make the perfect clot? Arterioscler Thromb Vasc Biol 2006;261:41–48. DOI:https://doi.org/10.1161/01.ATV.0000193624.28251.83.
   PubMed Web of Science ®Google Scholar
• Varon D, Shai E. Platelets and their microparticles as key players in pathophysiological responses. J Thromb Haemost 2015;13:S40–S46. DOI:https://doi.org/10.1111/jth.12976.
   PubMed Web of Science ®Google Scholar
• Wei H, Davies JE, Harper MT. 2-Aminoethoxydiphenylborate (2-APB) inhibits release of phosphatidylserine-exposing extracellular vesicles from platelets. Cell Death Discov 2020;61:10. DOI:https://doi.org/10.1038/s41420-020-0244-9.
   PubMed Web of Science ®Google Scholar
• Kuijpers MJE, Munnix ICA, Cosemans JMEM, Van Vlijmen BJ, Reutelingsperger CPM, Egbrink MGAO, Heemskerk JWM. Key role of platelet procoagulant activity in tissue factor- and collagen-dependent thrombus formation in arterioles and venules in vivo - Differential sensitivity to thrombin inhibition. Microcirculation 2008;154:269–282. DOI:https://doi.org/10.1080/10739680701653517.
   PubMed Web of Science ®Google Scholar
• Dachary-Prigent J, Freyssinet J-M, Pasquet J-M, Carron J-C, 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.
   Google Scholar
• Jobe SM, Wilson KM, Leo L, Raimondi A, Molkentin JD, Lentz SR, Di Paola J. Critical role for the mitochondrial permeability transition pore and cyclophilin D in platelet activation and thrombosis. Blood 2008;1113:1257–1265. DOI:https://doi.org/10.1182/blood-2007-05-092684.
   PubMed Web of Science ®Google Scholar
• Harper MT, Poole AW. PKC inhibition markedly enhances Ca2+ signaling and phosphatidylserine exposure downstream of protease-activated receptor-1 but not protease-activated receptor-4 in human platelets. J Thromb Haemost 2011;98:1599–1607. DOI:https://doi.org/10.1111/j.1538-7836.2011.04393.x.
   PubMed Web of Science ®Google Scholar
• Dasgupta SK, Guchhait P, Thiagarajan P. Lactadherin binding and phosphatidylserine expression on cell surface-comparison with annexin A5. Transl Res 2006;1481:19–25. DOI:https://doi.org/10.1016/j.lab.2006.03.006.
   PubMed Web of Science ®Google Scholar
• SHI J, Pipe SW, Rasmussen JT, CW HEEGAARD, Gilbert GE. Lactadherin blocks thrombosis and hemostasis in vivo: correlation with platelet phosphatidylserine exposure. J Thromb Haemost 2008;67:1167–1174. DOI:https://doi.org/10.1111/j.1538-7836.2008.03010.x.
   PubMed Web of Science ®Google Scholar
• London FS, Marcinkiewicz M, Walsh PN. PAR-1-stimulated factor IXa binding to a small platelet subpopulation requires a pronounced and sustained increase of cytoplasmic calcium. Biochemistry 2006;4523:7289–7298. DOI:https://doi.org/10.1021/bi060294m.
   PubMed Web of Science ®Google Scholar
• 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;27919:19854–19859. DOI:https://doi.org/10.1074/jbc.M310624200.
   PubMed Web of Science ®Google Scholar
• 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;311:2545–2553. DOI:https://doi.org/10.1111/j.1538-7836.2005.01616.x.
   PubMed Web of Science ®Google Scholar
• Berny MA, Munnix ICA, Auger JM, Schols SEM, Cosemans JMEM, Panizzi P, Bock PE, Watson SP, McCarty OJT, Heemskerk JWM. Spatial distribution of factor Xa, Thrombin, and Fibrin(ogen) on Thrombi at Venous Shear Kleinschnitz C, editor. PLoS ONE 2010;54:e10415. DOI:https://doi.org/10.1371/journal.pone.0010415.
   PubMed Web of Science ®Google Scholar
• Mattheij NJA, Gilio K, van Kruchten R, Jobe SM, Wieschhaus AJ, Chishti AH, Collins P, Heemskerk JWM, Cosemans JMEM. Dual mechanism of integrin alpha(IIb)beta(3) closure in procoagulant platelets. J Biol Chem 2013;28819:13325–13336. DOI:https://doi.org/10.1074/jbc.M112.428359.
   PubMed Web of Science ®Google Scholar
• Choo H-J, Kholmukhamedov A, Zhou C, Jobe S. Inner mitochondrial membrane disruption links apoptotic and agonist-initiated phosphatidylserine externalization in platelets. Arterioscler Thromb Vasc Biol 2017;378:1503–1512. DOI:https://doi.org/10.1161/ATVBAHA.117.309473.
   PubMed Web of Science ®Google Scholar
• Baig AA, Haining EJ, Geuss E, Beck S, Swieringa F, Wanitchakool P, Schuhmann MK, Stegner D, Kunzelmann K, Kleinschnitz C, et al. TMEM16F-mediated platelet membrane phospholipid scrambling is critical for hemostasis and thrombosis but not thromboinflammation in mice—brief report. Arterioscler Thromb Vasc Biol 2016;3611:2152–2157. DOI:https://doi.org/10.1161/ATVBAHA.116.307727.
   PubMed Web of Science ®Google Scholar
• Bevers EM, Comfurius P, Zwaal RFA. Platelet procoagulant activity: physiological significance and mechanisms of exposure. Blood Rev 1991;53:146–154. DOI:https://doi.org/10.1016/0268-960X(91)90031-7.
   PubMed Web of Science ®Google Scholar
• Fox JEB, Austin CD, Reynolds CC, Steffen PK. Evidence that agonist-induced activation of calpain causes the shedding of procoagulant-containing microvesicles from the membrane of aggregating platelets. J Biol Chem 1991;26620:13289–13295. DOI:https://doi.org/10.1016/S0021-9258(18)98837-X.
   PubMed Web of Science ®Google Scholar
• Wei H, Harper MT. ABT-737 triggers caspase-dependent inhibition of platelet procoagulant extracellular vesicle release during apoptosis and secondary necrosis in vitro. Thromb Haemost 2019;19:1665–1674.
   Google Scholar
• Morel O, Jesel L, Freyssinet JM, Toti F. Cellular mechanisms underlying the formation of circulating microparticles. Arterioscler Thromb Vasc Biol 2011;311:15–26. DOI:https://doi.org/10.1161/ATVBAHA.109.200956.
   PubMed Web of Science ®Google Scholar
• Watson SP, Auger JM, McCarty OJT, Pearce AC. GPVI and integrin αIIbβ3 signaling in platelets. J Thromb Haemost 2005;38:1752–1762. DOI:https://doi.org/10.1111/j.1538-7836.2005.01429.x.
   PubMed Web of Science ®Google Scholar
• Braun A, Varga-Szabo D, Kleinschnitz C, Pleines I, Bender M, Austinat M, Boesl M, Stoll G, Nieswandt B. Orai1 (CRACM1) is the platelet SOC channel and essential for pathological thrombus formation. Blood 2009;1139:2056–2063. DOI:https://doi.org/10.1182/blood-2008-07-171611.
   PubMed Web of Science ®Google Scholar
• Gilio K, van Kruchten R, Braun A, Berna-Erro A, Feijge MAH, Stegner D, van der Meijden PEJ, Kuijpers MJE, Varga-Szabo D, Heemskerk JWM, et al. Roles of platelet STIM1 and orai1 in glycoprotein VI- and Thrombin-dependent procoagulant activity and thrombus formation. J Biol Chem 2010;28531:23629–23638. DOI:https://doi.org/10.1074/jbc.M110.108696.
   PubMed Web of Science ®Google Scholar
• Gamage TH, Gunnes G, Lee RH, Louch WE, Holmgren A, Bruton JD, Lengle E, Kolstad TRS, Revold T, Amundsen SS, et al. STIM1 R304W causes muscle degeneration and impaired platelet activation in mice. Cell Calcium 2018;76:87–100. DOI:https://doi.org/10.1016/j.ceca.2018.10.001.
   PubMed Web of Science ®Google Scholar
• Varga-Szabo D, Braun A, Kleinschnitz C, Bender M, Pleines I, Pham M, Renné T, Stoll G, Nieswandt B. The calcium sensor STIM1 is an essential mediator of arterial thrombosis and ischemic brain infarction. J Exp Med 2008;2057:1583–1591. DOI:https://doi.org/10.1084/jem.20080302.
   PubMed Web of Science ®Google Scholar
• Chen W, Thielmann I, Gupta S, Subramanian H, Stegner D, van Kruchten R, Dietrich A, Gambaryan S, Heemskerk JWM, Hermanns HM, et al. Orai1-induced store-operated Ca 2+ entry enhances phospholipase activity and modulates canonical transient receptor potential channel 6 function in murine platelets. J Thromb Haemost 2014;124:528–539. DOI:https://doi.org/10.1111/jth.12525.
   PubMed Web of Science ®Google Scholar
• Harper MT, Londono JEC, Quick K, Londono JC, Flockerzi V, Philipp SE, Birnbaumer L, Freichel M, Poole AW. Transient receptor potential channels function as a coincidence signal detector mediating phosphatidylserine exposure. Sci Signal 2013;6281:281. DOI:https://doi.org/10.1126/scisignal.2003701.
   Web of Science ®Google Scholar
• Abbasian N, Millington-Burgess SL, Chabra S, Malcor JD, Harper MT. Supramaximal calcium signaling triggers procoagulant platelet formation. Blood Adv 2020;41:154–164. DOI:https://doi.org/10.1182/bloodadvances.2019000182.
   PubMed Web of Science ®Google Scholar
• Harper MT, Poole AW. Store-operated calcium entry and non-capacitative calcium entry have distinct roles in thrombin-induced calcium signalling in human platelets. Cell Calcium 2011;504:351–358. DOI:https://doi.org/10.1016/j.ceca.2011.06.005.
   PubMed Web of Science ®Google Scholar
• Fung CYE, Jones S, Ntrakwah A, Naseem KM, Farndale RW, Mahaut-Smith MP, Platelet C. 2+ responses coupled to glycoprotein VI and Toll-like receptors persist in the presence of endothelial-derived inhibitors: roles for secondary activation of P2X1 receptors and release from intracellular Ca 2+ stores. Blood 2012;11915:3613–3621. DOI:https://doi.org/10.1182/blood-2011-10-386052.
   PubMed Web of Science ®Google Scholar
• Aliotta A, Bertaggia Calderara D, Zermatten MG, Alberio L. Sodium–calcium exchanger reverse mode sustains dichotomous ion fluxes required for procoagulant COAT platelet formation. Thromb Haemost 2020.
   Web of Science ®Google Scholar
• Heemskerk JWM, Willems GM, Rook MB, Sage SO. Ragged spiking of free calcium in ADP-stimulated human platelets: regulation of puff-like calcium signals in vitro and ex vivo. J Physiol 2001;5353:625–635. DOI:https://doi.org/10.1111/j.1469-7793.2001.00625.x.
   PubMed Web of Science ®Google Scholar
• Purvis JE, Chatterjee MS, Brass LF, Diamond SL. Amolecular signaling model of platelet phosphoinositide and calcium regulation during homeostasis and P2Y1 activation. Blood 2008;11210:4069–4079. DOI:https://doi.org/10.1182/blood-2008-05-157883.
   PubMed Web of Science ®Google Scholar
• Obydennyy S, Sveshnikova AN, Ataullakhanov FI, Panteleev MA. Dynamics of calcium spiking, mitochondrial collapse and phosphatidylserine exposure in single platelets during activation. J Thromb Haemost 2015;13:649.
   Web of Science ®Google Scholar
• Bye AP, Gibbins JM, Mahaut-Smith MP. Ca2+ waves coordinate purinergic receptor-evoked integrin activation and polarization. Sci Signal 2020;13:615. DOI:https://doi.org/10.1126/scisignal.aav7354.
   Web of Science ®Google Scholar
• Glancy B, Balaban RS. Role of mitochondrial Ca 2+ in the regulation of cellular energetics. Biochemistry 2012;5114:2959–2973. DOI:https://doi.org/10.1021/bi2018909.
   PubMed Web of Science ®Google Scholar
• Shoshan-Barmatz V, De S. Mitochondrial VDAC, the Na+/Ca2+ exchanger, and the Ca2+ uniporter in Ca2+ dynamics and signaling. Advances in experimental medicine and biology Vol. 981. Springer New York LLC; 2017. 323–347.
   Google Scholar
• Belosludtsev KN, Dubinin MV, Belosludtseva NV, Mironova GD. Mitochondrial Ca2+ transport: mechanisms, molecular structures, and role in cells. Biochemistry (Moscow) 2019;846:593–607. DOI:https://doi.org/10.1134/S0006297919060026.
   PubMed Web of Science ®Google Scholar
• Nemani N, Shanmughapriya S, Madesh M. Molecular regulation of MCU: implications in physiology and disease. Cell Calcium 2018;74:86–93. DOI:https://doi.org/10.1016/j.ceca.2018.06.006.
   PubMed Web of Science ®Google Scholar
• Patron M, Checchetto V, Raffaello A, Teardo E, VecellioReane D, Mantoan M, Granatiero V, Szabò I, DeStefani D, Rizzuto R. MICU1 and MICU2 finely tune the mitochondrial Ca2+ uniporter by exerting opposite effects on MCU activity. Mol Cell 2014;535:726–737. DOI:https://doi.org/10.1016/j.molcel.2014.01.013.
   PubMed Web of Science ®Google Scholar
• Mammucari C, Gherardi G, Rizzuto R. Structure, activity regulation, and role of the mitochondrial calcium uniporter in health and disease. Front Oncol 2017;7. DOI:https://doi.org/10.3389/fonc.2017.00139.
   Google Scholar
• Kholmukhamedov A, Janecke R, Choo H-J, Jobe SM. The mitochondrial calcium uniporter regulates procoagulant platelet formation. J Thromb Haemost 2018;1611:2315–2321. DOI:https://doi.org/10.1111/jth.14284.
   PubMed Web of Science ®Google Scholar
• Brenner C, Moulin M. Physiological Roles of the Permeability Transition Pore. Circ Res 2012;1119:1237–1247. DOI:https://doi.org/10.1161/CIRCRESAHA.112.265942.
   PubMed Web of Science ®Google Scholar
• Bernardi P, von Stockum S. The permeability transition pore as a Ca2+ release channel: new answers to an old question. Cell Calcium 2012;521:22–27. DOI:https://doi.org/10.1016/j.ceca.2012.03.004.
   PubMed Web of Science ®Google Scholar
• Sveshnikova AN, Ataullakhanov FI, Panteleev MA. Compartmentalized calcium signaling triggers subpopulation formation upon platelet activation through PAR1. Mol Biosyst 2015;114:1052–1060. DOI:https://doi.org/10.1039/C4MB00667D.
   PubMedGoogle Scholar
• 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;2911:1883–1889. DOI:https://doi.org/10.1161/ATVBAHA.109.190926.
   PubMed Web of Science ®Google Scholar
• 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;3212:2946–2955. 2946-+. DOI:https://doi.org/10.1161/ATVBAHA.112.300433.
   PubMed Web of Science ®Google Scholar
• Weinberg JM, Davis JA, Venkatachalam MA. Cytosolic-free calcium increases to greater than 100 micromolar in ATP-depleted proximal tubules. J Clin Invest 1997;1003:713–722. DOI:https://doi.org/10.1172/JCI119584.
   PubMed Web of Science ®Google Scholar
• Dong Z, Saikumar P, Griess GA, Weinberg JM, Venkatachalam MA. Intracellular Ca2+ thresholds that determine survival or death of energy-deprived cells. Am J Pathol 1998;1521:231–240.
   PubMed Web of Science ®Google Scholar
• Hyrc K, Handran SD, Rothman SM, Goldberg MP. Ionized intracellular calcium concentration predicts excitotoxic neuronal death: observations with low-affinity fluorescent calcium indicators. The Journal of Neuroscience 1997;1717:6669–6677. DOI:https://doi.org/10.1523/JNEUROSCI.17-17-06669.1997.
   PubMed Web of Science ®Google Scholar
• Hua VM, Abeynaike L, Glaros E, Campbell H, Pasalic L, Hogg PJ, Chen VMY, Vu Minh H, Abeynaike L, Glaros E, et al. Necrotic platelets provide a procoagulant surface during thrombosis. Blood 2015;12626:2852–2862. DOI:https://doi.org/10.1182/blood-2015-08-663005.
   PubMed Web of Science ®Google Scholar
• Yang H, Kim A, David T, Palmer D, Jin T, Tien J, Huang F, Cheng T, Coughlin SR, Jan YN, et al. TMEM16F forms a Ca2+-activated cation channel required for lipid scrambling in platelets during blood coagulation. Cell 2012;1511:111–122. DOI:https://doi.org/10.1016/j.cell.2012.07.036.
   PubMed Web of Science ®Google Scholar
• Basse F, Stout JG, Sims PJ, Wiedmer T. Isolation of an erythrocyte membrane protein that mediates Ca2+-dependent transbilayer movement of phospholipid. J Biol Chem 1996;27129:17205–17210. DOI:https://doi.org/10.1074/jbc.271.29.17205.
   PubMed Web of Science ®Google Scholar
• Kojima H, Newtonnash D, Weiss HJ, Zhao J, Sims PJ, Wiedmer T. PRODUCTION AND CHARACTERIZATION OF TRANSFORMED B-LYMPHOCYTES EXPRESSING THE MEMBRANE DEFECT OF SCOTT SYNDROME. J Clin Invest 1994;946:2237–2244. DOI:https://doi.org/10.1172/JCI117586.
   PubMed Web of Science ®Google Scholar
• Verhoven B, Schlegel RA, Williamson P. RAPID LOSS AND RESTORATION OF LIPID ASYMMETRY BY DIFFERENT PATHWAYS IN RESEALED ERYTHROCYTE-GHOSTS. Biochim Biophys Acta 1992;11041:15–23. DOI:https://doi.org/10.1016/0005-2736(92)90126-7.
   PubMedGoogle Scholar
• Malvezzi M, Chalat M, Janjusevic R, Picollo A, Terashima H, Menon AK, Accardi A. Ca2+-dependent phospholipid scrambling by a reconstituted TMEM16 ion channel. Nat Commun 2013;4. DOI:https://doi.org/10.1038/ncomms3367.
   Google Scholar
• Moldoveanu T, Hosfield CM, Lim D, Elce JS, Jia Z, Davies PL. A Ca2+ switch aligns the active site of calpain. Cell 2002;1085:649–660. DOI:https://doi.org/10.1016/S0092-8674(02)00659-1.
   PubMed Web of Science ®Google Scholar
• Ye W, Han TW, Nassar LM, Zubia M, Jan YN, Jan LY. Phosphatidylinositol-(4, 5)-bisphosphate regulates calcium gating of small-conductance cation channel TMEM16F. Proc Natl Acad Sci U S A 2018;1157:E1667–E1674. DOI:https://doi.org/10.1073/pnas.1718728115.
   PubMed Web of Science ®Google Scholar
• Obydennyi SI, Artemenko EO, Sveshnikova AN, Ignatova AA, Varlamova TV, Gambaryan S, Lomakina GY, Ugarova NN, Kireev II, Ataullakhanov FI, et al. Mechanisms of increased mitochondria-dependent necrosis in Wiskott-Aldrich syndrome platelets. Haematologica 2020;1054:1095–1106. DOI:https://doi.org/10.3324/haematol.2018.214460.
   PubMed Web of Science ®Google Scholar
• Boudreau LH, Duchez AC, Cloutier N, Soulet D, Martin N, Bollinger J, Paré A, Rousseau M, Naika GS, Lévesque T, et al. Platelets release mitochondria serving as substrate for bactericidal group IIA-secreted phospholipase a to promote inflammation. Blood 2014;12414:2173–2183. DOI:https://doi.org/10.1182/blood-2014-05-573543.
   PubMed Web of Science ®Google Scholar
• Vanden Berghe T, Linkermann A, Jouan-Lanhouet S, Walczak H, Vandenabeele P. Regulated necrosis: the expanding network of non-apoptotic cell death pathways. Nat Rev Mol Cell Biol 2014;152:134–146.
   Web of Science ®Google Scholar
• Kolbrink B, Riebeling T, Kunzendorf U, Krautwald S. Plasma membrane pores drive inflammatory cell death. Front Cell Dev Biol 2020;8. DOI:https://doi.org/10.3389/fcell.2020.00817.
   Google Scholar
• Liu X, Zhang Z, Ruan J, Pan Y, Magupalli VG, Wu H, Lieberman J. Inflammasome-activated gasdermin D causes pyroptosis by forming membrane pores. Nature 2016;5357610:153–158. DOI:https://doi.org/10.1038/nature18629.
   PubMed Web of Science ®Google Scholar
• Sborgi L, Rühl S, Mulvihill E, Pipercevic J, Heilig R, Stahlberg H, Farady CJ, Müller DJ, Broz P, Hiller S. GSDMD membrane pore formation constitutes the mechanism of pyroptotic cell death. Embo J 2016;3516:1766–1778. DOI:https://doi.org/10.15252/embj.201694696.
   PubMed Web of Science ®Google Scholar
• Rogers C, Fernandes-Alnemri T, Mayes L, Alnemri D, Cingolani G, Alnemri ES. Cleavage of DFNA5 by caspase-3 during apoptosis mediates progression to secondary necrotic/pyroptotic cell death. Nat Commun 2017;8. DOI:https://doi.org/10.1038/ncomms14128.
   Google Scholar
• Bergmeier W, Masatsugu OH, McCarl CA, Roden RC, Bray PF, Feske S. R93W mutation in Orai1 causes impaired calcium influx in platelets. Blood 2009;1133:675–678. DOI:https://doi.org/10.1182/blood-2008-08-174516.
   PubMed Web of Science ®Google Scholar
• Lacruz RS, Feske S. Diseases caused by mutations in ORAI1 and STIM1. Ann N Y Acad Sci 2015;13561:45–79. DOI:https://doi.org/10.1111/nyas.12938.
   PubMed Web of Science ®Google Scholar
• Murphy E, Pan X, Nguyen T, Liu J, Holmström KM, Finkel T. Unresolved questions from the analysis of mice lacking MCU expression. Biochem Biophys Res Commun 2014;4494:384–385. DOI:https://doi.org/10.1016/j.bbrc.2014.04.144.
   PubMed Web of Science ®Google Scholar
• Millington-Burgess SL, Harper MT. Gene of the issue: ANO6 and Scott Syndrome. Platelets 2019;317:964–967. DOI:https://doi.org/10.1080/09537104.2019.1693039.
   PubMed Web of Science ®Google Scholar
• Dekkers DWC, Comfurius P, Vuist WMJ, Billheimer JT, Dicker I, Weiss HJ, Zwaal RFA, Bevers EM. Impaired Ca2+-induced tyrosine phosphorylation and defective lipid scrambling in erythrocytes from a patient with Scott syndrome: A study using an inhibitor for scramblase that mimics the defect in Scott syndrome. Blood 1998;916:2133–2138. DOI:https://doi.org/10.1182/blood.V91.6.2133.
   PubMed Web of Science ®Google Scholar
• Millington-Burgess SL, Bonna AM, Rahman T, Harper MT. Ethaninidothioic acid (R5421) is not a selective inhibitor of platelet phospholipid scramblase activity. Br J Pharmacol 2020;17717:4007–4020. DOI:https://doi.org/10.1111/bph.15152.
   PubMed Web of Science ®Google Scholar
• Suzuki T, Suzuki J, Nagata S. Functional Swapping between Transmembrane Proteins TMEM16A and TMEM16F. J Biol Chem 2014;28911:7438–7447. DOI:https://doi.org/10.1074/jbc.M113.542324.
   PubMed Web of Science ®Google Scholar
• Watanabe R, Sakuragi T, Noji H, Nagata S. Single-molecule analysis of phospholipid scrambling by TMEM16F. Proc Natl Acad Sci U S A 2018;11512:3066–3071.
   PubMed Web of Science ®Google Scholar
• Le T, Le SC, Zhang Y, Liang P, Yang H. Evidence that polyphenols do not inhibit the phospholipid scramblase TMEM16F. J Biol Chem 2020;29535:12537–12544. DOI:https://doi.org/10.1074/jbc.AC120.014872.
   PubMed Web of Science ®Google Scholar
• Faggio C, Sureda A, Morabito S, Sanches-Silva A, Mocan A, Nabavi SF, Nabavi SM. Flavonoids and platelet aggregation: A brief review. Eur J Pharmacol 2017;807:91–101. DOI:https://doi.org/10.1016/j.ejphar.2017.04.009.
   PubMed Web of Science ®Google Scholar
• Khan H, Jawad M, Kamal MA, Baldi A, Xiao J, Nabavi SM, Daglia M. Evidence and prospective of plant derived flavonoids as antiplatelet agents: strong candidates to be drugs of future. Food Chem Toxicol 2018;119:355–367. DOI:https://doi.org/10.1016/j.fct.2018.02.014.
   PubMed Web of Science ®Google Scholar
• Sanchez M, Romero M, Gomez-Guzman M, Tamargo J, Perez-Vizcaino F, Duarte J. Cardiovascular effects of flavonoids. Curr Med Chem 2018;26: 6991-7034.
   Web of Science ®Google Scholar
• Ed Nignpense B, Chinkwo KA, Blanchard CL, Santhakumar AB. Polyphenols: modulators of platelet function and platelet microparticle generation? Int J Mol Sci 2020;21:1.
   Web of Science ®Google Scholar
• Wright B, Spencer JPE, Lovegrove JA, Gibbins JM. Insights into dietary flavonoids as molecular templates for the design of anti-platelet drugs. Cardiovasc Res 2013;971:13–22. DOI:https://doi.org/10.1093/cvr/cvs304.
   PubMed Web of Science ®Google Scholar
• Lopez JJ, El Haouari M, Jardin I, Alonso N, Regodon S, Diez-Bello R, Redondo PC, Rosado JA. Flavonoids and Platelet-Derived Thrombotic Disorders. Curr Med Chem 2020;2639:7035–7047. DOI:https://doi.org/10.2174/0929867325666180417170218.
   Web of Science ®Google Scholar
• Chernysh IN, Nagaswami C, Kosolapova S, Peshkova AD, Cuker A, Cines DB, Cambor CL, Litvinov RI, Weisel JW. The distinctive structure and composition of arterial and venous thrombi and pulmonary emboli. Sci Rep 2020;101:1. DOI:https://doi.org/10.1038/s41598-020-59526-x.
   PubMed Web of Science ®Google Scholar
• Wei H, Malcor J, Harper M. Lipid rafts are essential for release of phosphatidylserine-exposing extracellular vesicles from platelets. Sci Rep 2018;81:9987. DOI:https://doi.org/10.1038/s41598-018-28363-4.
   PubMedGoogle Scholar
• Owens A, Mackman N. Microparticles in Hemostasis and Thrombosis. Circ Res 2011;108:1284–1297. DOI:https://doi.org/10.1161/CIRCRESAHA.110.233056.
   PubMed Web of Science ®Google Scholar
• Jackson SP, Schoenwaelder SM. Procoagulant platelets: are they necrotic? Blood 2010;11612:2011–2018. DOI:https://doi.org/10.1182/blood-2010-01-261669.
   PubMed Web of Science ®Google Scholar
• Ghasemzadeh M, Kaplan ZS, Alwis I, Schoenwaelder SM, Ashworth KJ, Westein E, Hosseini E, Salem HH, Slattery R, McColl SR, et al. The CXCR1/2 ligand NAP-2 promotes directed intravascular leukocyte migration through platelet thrombi. Blood 2013;12122:4555–4566. DOI:https://doi.org/10.1182/blood-2012-09-459636.
   PubMed Web of Science ®Google Scholar