High-throughput assessment identifying major platelet Ca2+ entry pathways via tyrosine kinase-linked and G protein-coupled receptors

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[1] J.W. Heemskerk, Calcium and platelets, In: The Molecular Basis of Calcium Action in Biology and Medicine (Pochet, R, Donato, R, Haiech, J, Heinzmann, C and Gerke, V, eds.), Kluwer Acad. Publ., The Hague (the Netherlands). 2000, pages 45-71. [2] D. Varga-Szabo, A. Braun, B. Nieswandt, Calcium signaling in platelets, J. Thromb. Haemost. 7 (2009) 1057-1066. [3] H.H. Versteeg, J.W. Heemskerk, M. Levi, P.H. Reitsma, New fundamentals in hemostasis, Physiol. Rev. 93 (2013) 327-358. [4] E. Mammadova-Bach, M. Nagy, J.W. Heemskerk, B. Nieswandt, A. Braun, Store-operated calcium entry in thrombosis and thrombo-inflammation, Cell Calcium. 77 (2019) 39-48. [5] F.A. Solari, N.J. Mattheij, J.M. Burkhart, F. Swieringa, P.W. Collins, J.M. Cosemans, A. Sickmann, J.W. Heemskerk, R.P. Zahedi, Combined quantification of the global proteome, phosphoproteome, and proteolytic cleavage to characterize altered platelet functions in the human Scott syndrome, Mol. Cell. Proteomics. 15 (2016) 3154-3169. [6] F. Beck, J. Geiger, S. Gambaryan, F.A. Solari, M. Dell'Aica, S. Loroch, N. Mattheij, I. Mindukshev, O. Pötz, K. Jurk, J.M. Burkhart, C. Fufezan, J.W. Heemskerk, U. Walter, R.P. Zahedi, A. Sickmann, Temporal quantitative phosphoproteomics of ADP stimulation reveals novel central nodes in platelet activation and inhibition, Blood. 129 (2017) e1-e12. [7] H.Y. Cheung, C. Coman, P. Westhoff, M. Manke, A. Sickmann, O. Borst, M. Gawaz, S.P. Watson, J.W. Heemskerk, R. Ahrends, Targeted phosphoinositides analysis using high-performance ion chromatography-coupled selected reaction monitoring mass spectrometry, J. Proteome Res. 20 (2021) 3114-3123. [8] J. Wu, J.W. Heemskerk, C.C. Baaten, Platelet membrane receptor proteolysis: implications for platelet function, Front. Cardiovasc. Med. 7 (2021) 608391. [9] D.I. Fernandez, M.J. Kuijpers, J.W. Heemskerk, Platelet calcium signaling by G-protein coupled and ITAM-linked receptors regulating anoctamin-6 and procoagulant activity, Platelets. 32 (2021) 863-871. [10] P.E. Van der Meijden, J.W. Heemskerk, Platelet biology and functions: new concepts and clinical perspectives, Nat. Rev. Cardiol. 16 (2019) 166-179. [11] S.P. Watson, J.M. Auger, O.J. McCarty, A.C. Pearce, GPVI and integrin aIIbb3 signaling in platelets, J. Thromb. Haemost. 3 (2005) 1752-1762. [12] S. Offermanns, Activation of platelet function through G protein-coupled receptors, Circ. Res. 99 (2006) 1293-1304. [13] G. De Gaetano, C. Cerletti, E. Dejana, R. Latini, Pharmacology of platelet inhibition in humans: implications of the salicylate-aspirin interaction, Circulation. 72 (1985) 1185-1193. [14] S. Feske, Y. Gwack, M. Prakriya, S. Srikanth, S.H. Puppel, B. Tanasa, P.G. Hogan, R.S. Lewis, M. Daly, A.K. Rao, A mutation in Orai1 causes immune deficiency by abrogating CRAC channel function, Nature. 441 (2006) 179-185. [15] F. Lang, P. Münzer, M. Gawaz, O. Borst, Regulation of STIM1/Orai1-dependent Ca2+ signalling in platelets, Thromb. Haemost. 110 (2013) 925-930. [16] J.W. Heemskerk, P. Vis, M.A. Feijge, J. Hoyland, W.T. Mason, S.O. Sage, Roles of phospholipase C and Ca2+-ATPase in calcium responses of single, fibrinogen-bound platelets, J. Biol. Chem. 268 (1993) 356-363. [17] M. Prakriya, S. Feske, Y. Gwack, S. Srikanth, A. Rao, P.G. Hogan, Orai1 is an essential pore subunit of the CRAC channel, Nature. 443 (2006) 230-233. [18] R.M. Luik, B. Wang, M. Prakriya, M. Wu, R.S. Lewis, Oligomerization of STIM1 couples ER calcium depletion to CRAC channel activation, Nature. 454 (2008) 538-542. [19] D. Varga-Szabo, A. Braun, B. Nieswandt, STIM1 and Orai1 in platelet function, Cell Calcium. 50 (2011) 70-278. [20] J. Volz, C. Kusch, S. Beck, M. Popp, T. Vögtle, M. Meub, I. Scheller, H.S. Heil, J. Preu, M.K. Schuhmann, K. Hemmen, T. Premsler, A. Sickmann, K.G. Heinze, D. Stegner, G. Stoll, A. Braun, M. Sauer, B. Nieswandt, BIN2 orchestrates platelet calcium signaling in thrombosis and thrombo-inflammation, J. Clin. Invest. 130 (2020) 6064-6079. [21] W. Bergmeier, M. Oh-hora, C.A. McCarl, R.C. Roden, P.F. Bray, S. Feske, R93W mutation in Orai1 causes impaired calcium calcium influx in platelets, Blood. 109 (2009) 6875-6878. [22] A. Braun, D. Varga-Szabo, C. Kleinschnitz, I. Pleines, M. Bernder, M. Austinat, M. Bösi, G. Stoll, B. Nieswandt, Orai1 (CRACM1) is the platelet SOC channel and essential for pathological thrombus formation, Blood. 113 (2009) 2056-2063. [23] K. Gilio, R. van Kruchten, A. Braun, A. Berna-Erro, M.A. Feijge, D. Stegner, P.E. van der Meijden, M.J. Kuijpers, D. Varga-Szabo, J.W. Heemskerk, B. Nieswandt, Roles of platelet STIM1 and Orai1 in glycoprotein VI- and thrombin-dependent procoagulant activity and thrombus formation, J. Biol. Chem. 285 (2010) 23629-29638. [24] M. Nagy, T.G. Mastenbroek, N.J. Mattheij, S. de Witt, K.J. Clemetson, J. Kirschner, A. Schulz, A. Braun, J.M. Cosemans, B. Zieger, J.W. Heemskerk, Variable impairment of platelet functions in patients with severe, genetically linked immune deficiencies, Haematologica. 103 (2018) 540-549. [25] M.T. Harper, A.W. Poole, Store-operated calcium entry and non-capacitative calcium entry have distinct roles in thrombin-induced calcium signaling in human platelets, Cell Calcium. 50 (2011) 351-358. [26] M.P. Mahaut-Smith, S.J. Ennion, M.G. Rolf, R.J. Evans, ADP is not an agonist at P2X1 receptors: evidence for separate receptors stimulated by ATP and ADP on human platelets., Br. J. Pharmacol. 131 (2000) 108-114. [27] M.P. Mahaut-Smith, K.A. Taylor, R.J. Evans, Calcium signalling through ligand-gated ion channels such as P2X1 receptors in the platelet and other non-excitable cells, Adv. Exp. Med. Biol. 898 (2016) 305-329. [28] M.T. Harper, J.E. Camacho-Londono, K. Quick, J. Camacho-Londono, V. Flockerzi, S.E. Phillipp, L. Birnbaumer, M. Freichei, A.W. Poole, Transient receptor potential channels function as a coincidence signal mediating phosphatidylserine exposure, Sci. Signal. 6 (2013) ra50. [29] G. Ramanathan, S. Gupta, I. Thielmann, I. Pleines, D. Varga-Szabo, F. May, C. Mannhalter, A. Dietrich, B. Nieswandt, A. Braun, Defective diacylglycerol-induced Ca2+ entry but normal agonist-induced activation responses in TRPC6-deficient mouse platelets, J. Thromb. Haemost. 10 (2012) 419-429. [30] W. Chen, I. Thielmann, S. Gupta, H. Subramanian, D. Stegner, R. van Kruchten, A. Dietrich, S. Gambaryan, J.W. Heemskerk, H.M. Hermanns, B. Nieswandt, A. Braun, Orai1-induced store-operated Ca2+ entry enhances phospholipase activity and modulates canonical transient receptor potential channel 6 function in murine platelets, J. Thromb. Haemost. 12 (2014) 528-539. [31] C. Bae, F. Sachs, P.A. Gottlieb, The mechanosensitive ion channel Piezo1 is inhibited by the peptide GsMTx4, Biochemistry. 50 (2011) 6295-6300. [32] A. Aliotta, D. Bertaggia Calderara, M.G. Zermatten, L. Alberio, Sodium-calcium exchanger reverse mode sustains dichotomous ion fluxes required for procoagulant COAT platelet formation, Thromb. Haemost. 121 (2021) 309-321. [33] D.I. Fernandez, I. Provenzale, J. van Groningen, B.M.E. Tullemans, A. Veninga, J.L. Dunster, S. Honarnejad, H. van den Hurk, M.J. Kuijpers, J.W. Heemskerk, Ultra-high throughput Ca2+ response patterns in platelets to distinguish between ITAM-linked and G- protein coupled receptor activation, iScience. 25 (2022) 103718. [34] K. Gilio, I.C. Munnix, P. Mangin, J.M. Cosemans, M.A. Feijge, P.E. van der Meijden, S. Olieslagers, M.B. Chrzanowska-Wodnicka, R. Lillian, S. Schoenwaelder, S. Koyasu, S.O. Sage, S.P. Jackson, J.W. Heemskerk, Non-redundant roles of phosphoinositide 3-kinase isoforms alpha and beta in glycoprotein VI-induced platelet signaling and thrombus formation, J. Biol. Chem. 284 (2009) 33750-33762. [35] M.A. Feijge, E.C. van Pampus, C. Lacabaratz-Porret, K. Hamulyak, S. Lévy-Toledano, J. Enouf, J.W. Heemskerk, Inter-individual varability in Ca2+ signalling in platelets from healthy volunteers, relation with expression of endomembrane Ca2+-ATPases, Br. J. Haematol. 102 (1998) 850-859. [36] P. Sargeant, W.D. Clarkson, S.O. Sage, J.W. Heemskerk, Calcium influx in Fura-2-loaded human platelets is evoked by thapsigargin and 2,5-di-(t-butyl)-1,4-benzohydroquinone and reduced by inhibitors of cytochrome P-450, Cell Calcium. 13 (1992) 553-564. [37] J.W. Heemskerk, M.A. Feijge, S.O. Sage, U. Walter, Indirect regulation of Ca2+ entry by cAMP-dependent and cGMP-dependent protein kinases and phospholipase C in rat platelets, Eur. J. Biochem. 223 (1994) 543-551. [38] I.M. Keularts, R.M. van Gorp, M.A. Feijge, M.W. Vuist, J.W. Heemskerk, a2A-Adrenergic receptor stimulation potentiates calcium release in platelets by modulating cAMP levels, J. Biol. Chem. 275 (2000) 1763-1772. [39] A. Veninga, C.C. Baaten, B.M. Tullemans, I. De Simone, M.J. Kuijpers, J.W. Heemskerk, P.E. van der Meijden, Effects of platelet agonists and priming on the formation of platelet populations, Thromb. Haemost. 122 (2022) 726-738. [40] N.J. Jooss, I. De Simone, I. Provenzale, D.I. Fernandez, S.L. Brouns, R.W. Farndale, Y.M. Henskens, M.J. Kuijpers, H. ten Cate, P.E. van der Meijden, R. Cavill, J.W. Heemskerk, Role of platelet glycoprotein VI and tyrosine kinase Syk in thrombus formation on collagen-like surfaces, Int. J. Mol. Sci. 20 (2019) e2788. [41] G. Grynkiewicz, M. Poenie, R.Y. Tsien, A new generation of Ca2+ indicators with greatly improved fluorescence properties, J. Biol. Chem. 260 (1985) 3440-3450. [42] J.P. Van Geffen, S.L. Brouns, J. Batista, H. McKinney, C. Kempster, M. Nagy, S. Sivapalaratnam, C.C. Baaten, N. Bourry, M. Frontini, K. Jurk, M. Krause, D. Pillitteri, F. Swieringa, R. Verdoold, R. Cavill, M.J. Kuijpers, W.H. Ouwehand, K. Downes, J.W. Heemskerk, High-throughput elucidation of thrombus formation reveals sources of platelet function variability, Haematologica. 104 (2019) 1256-1267. [43] J.G. White, Platelet structure, In: Platelets, 2nd edition (Michelson A, ed.) Academic Press, Amsterdam. 2007, pages 45-73. [44] J.W. Heemskerk, G.M. Willems, M.B. Rook, S.O. Sage, Ragged spiking of free calcium in ADP-stimulated human platelets: regulation of puff-like calcium signals in vitro and ex vivo, J. Physiol. 535 (2001) 625-635. [45] P. Sargeant, S.O. Sage, Calcium signalling in platelets and other nonexcitable cells, Pharmacol. Ther. 64 (1994) 395-443. [46] A. Malayev, D.J. Nelson, Extracellular pH modulates the Ca2+ current activated by depletion of intracellular Ca2+ stores in human macrophages, J. Membr. Biol. 146 (1995) 101-111. [47] A. Beck, A. Fleig, R. Penner, C. Peinelt, Regulation of endogenous and heterologous Ca²⁺ release-activated Ca²⁺ currents by pH, Cell Calcium. 56 (2014) 235-243. [48] M.D. Bootman, T.J. Collins, L. Mackenzie, H.L. Roderick, M.J. Berridge, C.M. Peppiatt, 2-aminoethoxydiphenyl borate (2-APB) is a reliable blocker of store-operated Ca2+ entry but an inconsistent inhibitor of InsP3-induced Ca2+ release, FASEB J. 16 (2002) 1145-1150. [49] R. Van Kruchten, A. Braun, M.A. Feijge, M.J. Kuijpers, R. Rivera-Galdos, P. Kraft, G. Stoll, G. Kleinschnitz, E.M. Bevers, B. Nieswandt, J.W. Heemskerk, Antithrombotic potential of blockers of store-operated calcium channels in platelets, Arterioscler. Thromb. Vasc. Biol. 32 (2012) 1717-1723. [50] A. Kondratskyi, M. Yassine, C. Slomianny, K. Kondratska, D. Gordienko, E. Dewailly, V. Lehen'kyi, R. Skryma, N. Prevarskaya, Identification of ML-9 as a lysosomotropic agent targeting autophagy and cell death, Cell Death Dis. 5 (2014) e1193. [51] L. Waldherr, A. Tiffner, D. Mishra, M. Sallinger, R. Schober, I. Frischauf, T. Schmidt, V. Handl, P. Sagmeister, M. Köckinger, I. Derler, M. Üçal, D. Bonhenry, S. Patz, R. Schindl, Blockage of store-operated Ca2+ influx by Synta66 is mediated by direct inhibition of the Ca2+ selective Orai1 pore, Cancers (Basel). 12 (2020) 2876. [52] B.L. Lin, D. Matera, J.F. Doerner, N. Zheng, D. Del Camino, S. Mishra, H. Bian, et al., In vivo selective inhibition of TRPC6 by antagonist BI 749327 ameliorates fibrosis and dysfunction in cardiac and renal disease, Proc. Natl. Acad. Sci. USA. 116 (2019) 10156-10161. [53] Y. Tan, W. Lu, X. Yi, H. Cai, Y. Yuan, S. Zhang, Improvement of platelet preservation by inhibition of TRPC6, Transfus Med. in press (2023). [54] Z. Ilkan, J.R. Wright, A.H. Goodall, J.M. Gibbins, C.I. Jones, M.P. Mahaut-Smith, Evidence for shear-mediated Ca2+ entry through mechanosensitive cation channels in human platelets and a megakaryocytic cell line, J. Biol. Chem. 292 (2017) 9204-9217. [55] M.T. Harper, M.J. Mason, S.O. Sage, A.G. Harper, Phorbol ester-evoked Ca2+ signaling in human platelets is via autocrine activation of P2X1 receptors, not a novel non-capacitative Ca2+ entry, J. Thromb. Haemost. 8 (2010) 1604-1613. [56] F.M. Bennett, J.I. Mobbs, S. Ventura, D.M. Thal, The P2X1 receptor as a therapeutic target, Purinergic Sign. 18 (2022) 421-433. [57] N. Jost, N. Nagy, C. Corici, Z. Kohajda, A. Horváth, K. Acsai, P. Biliczki, J. Levijoki, P. Pollesello, T. Koskelainen, L. Otsomaa, A. Tóth, J.G. Papp, A. Varró, L. Virág, ORM-10103, a novel specific inhibitor of the Na+/Ca2+ exchanger, decreases early and delayed afterdepolarizations in the canine heart, Br. J. Pharmacol. 170 (2013) 768-778. [58] A. Kholmukhamedov, R. Janecke, H.J. Choo, S.M. Jobe, The mitochondrial calcium uniporter regulates procoagulant platelet formation, J. Thromb. Haemost. 16 (2018) 2315-2321. [59] M.H. Flamm, T.V. Colace, M.S. Chatterjee, H. Jing, S. Zhou, D. Jaeger, L.F. Brass, T. Sinno, S.L. Diamond, Multiscale prediction of patient-specific platelet function under flow, Blood. 120 (2012) 190-198. [60] L. Joutsi-Korhonen, P.A. Smethurst, A. Rankin, E. Gray, M. IJsseldijk, C.M. Onley, N.A. Watkins, L.M. Williamson, A.H. Goodall, P.G. de Groot, R.W. Farndale, W.H. Ouwehand, The low-frequency allele of the platelet collagen signaling receptor glycoprotein VI is associated with reduced functional responses and expression, Blood. 101 (2003) 4372-4379. [61] C.C. Baaten, H. ten Cate, P.E. van der Meijden, J.W. Heemskerk, Platelet populations and priming in hematological diseases, Blood Rev. 31 (2017) 389-399. [62] M.S. Chatterjee, J.E. Purvis, L.F. Brass, S.L. Diamond, Pairwise agonist scanning predicts cellular signaling responses to combinatorial stimuli, Nat. Biotechnol. 28 (2010) 727-732. [63] A.T. Dolan, S.L. Diamond, Systems modeling of Ca2+ homeostasis and mobilization in platelets mediated by IP3 and store-operated Ca2+ entry, Biophys. J. 106 (2014) 2049-60. [64] J.I. Goto, A.Z. Suzuki, S. Ozaki, N. Matsumoto, T. Nakamura, E. Ebisui, A. Fleig, R. Penner, K. Mikoshiba, Two novel 2-aminoethyl diphenylborinate (2-APB) analogues differentially activate and inhibit store-operated Ca2+ entry via STIM proteins, Cell Calcium. 47 (2010) 1-10. [65] J. Huang, F. Swieringa, F.A. Solari, I. Provenzale, L. Grassi, I. De Simone, C.C. Baaten, R. Cavill, A. Sickmann, M. Frontini, J.W. Heemskerk, Assessment of a complete and classified platelet proteome from genome-wide transcripts of human platelets and megakaryocytes covering platelet functions, Sci. Rep. 11 (2021) 12358. [66] B.B. Dawood, J. Wilde, S.P. Watson, Reference curves for aggregation and ATP secretion to aid diagnose of platelet-based bleeding disorders: effect of inhibition of ADP and thromboxane A2 pathways, Platelets. 18 (2007) 329-345. [67] OMIM, OMIM online catalog of human genes and genetic disorders, http://omim.org. (2023). [68] J.M. Burkhart, M. Vaudel, S. Gambaryan, S. Radau, U. Walter, L. Martens, G. J., A. Sickmann, R.P. Zahedi, The first comprehensive and quantitative analysis of human platelet protein composition allows the comparative analysis of structural and functional pathways, Blood. 120 (2012) e73-e82. [69] M. Zeiler, M. Moser, M. Mann, Copy number analysis of the murine platelet proteome spanning the complete abundance range, Mol. Cell. Proteomics. 13 (2014) 3435-3445.