Delineating zinc influx mechanisms during platelet activation

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[1] J. Apgar, “Effect of zinc deficiency on parturition in the rat,” Am.J.Physiol., vol. 215, no. 1, pp. 160–163, 1968. [2] P. R. Gordon and B. L. O’Dell, “Short-term zinc deficiency and hemostasis in the rat,” Proc. Soc. Exp. Biol. Med., vol. 163, no. 2, pp. 240–244, Feb. 1980. [3] P. R. Gordon and B. L. O’Dell, “Rat platelet aggregation impaired by short-term zinc deficiency,” J.Nutr., vol. 110, no. 10, pp. 2125–2129, 1980. [4] P. R. Gordon, C. W. Woodruff, H. L. Anderson, and B. L. O’Dell, “Effect of acute zinc deprivation on plasma zinc and platelet aggregation in adult males,” Am.J.Clin.Nutr., vol. 35, no. 1, pp. 113–119, 1982. [5] M. Stefanini, “Cutaneous bleeding related to zinc deficiency in two cases of advanced cancer,” Cancer, vol. 86, no. 5, pp. 866–870, 1999, doi: 10.1002/(SICI)1097-0142(19990901)86:5<866::AID-CNCR24>3.0.CO;2-A. [6] K. A. Taylor and N. Pugh, “The contribution of zinc to platelet behaviour during haemostasis and thrombosis,” Metallomics, vol. 8, no. 2, pp. 144–155, Feb. 2016. [7] J. Lu, A. J. Stewart, P. J. Sadler, T. J. T. Pinheiro, and C. A. Blindauer, “Albumin as a zinc carrier: properties of its high-affinity zinc-binding site,” Biochem Soc Trans, vol. 36, no. Pt 6, pp. 1317–1321, Dec. 2008, doi: 10.1042/BST0361317. [8] D. C. Chilvers, J. B. Dawson, M. H. Bahreyni-Toosi, and A. Hodgkinson, “Identification and determination of copper--and zinc--protein complexes in blood plasma after chromatographic separation on DEAE-Sepharose CL-6B,” Analyst, vol. 109, no. 7, pp. 871–876, Jul. 1984, doi: 10.1039/an9840900871. [9] J. W. Foote and H. T. Delves, “Distribution of zinc amongst human serum proteins determined by affinity chromatography and atomic-absorption spectrophotometry,” Analyst, vol. 108, no. 1285, pp. 492–504, Apr. 1983, doi: 10.1039/an9830800492. [10] N. Stadler et al., “Accumulation of zinc in human atherosclerotic lesions correlates with calcium levels but does not protect against protein oxidation,” Arterioscler.Thromb.Vasc.Biol., vol. 28, no. 5, pp. 1024–1030, 2008. [11] G. Marx, G. Korner, X. Mou, and R. Gorodetsky, “Packaging zinc, fibrinogen, and factor XIII in platelet alpha-granules,” J.Cell.Physiol., vol. 156, no. 3, pp. 437–442, 1993. [12] B. Watson et al., “Zinc is a Transmembrane Agonist that Induces Platelet Activation in a Tyrosine Phosphorylation-Dependent Manner,” Metallomics, vol. 8, no. 1, pp. 91–100, 2016. [13] I. J. Forbes, P. D. Zalewski, C. Giannakis, H. S. Petkoff, and P. A. Cowled, “Interaction between protein kinase C and regulatory ligand is enhanced by a chelatable pool of cellular zinc,” Biochim.Biophys.Acta, vol. 1053, no. 2–3, pp. 113–117, 1990. [14] N. S. Ahmed, M. E. Lopes Pires, K. A. Taylor, and N. Pugh, “Agonist-Evoked Increases in Intra-Platelet Zinc Couple to Functional Responses,” Thromb. Haemost., vol. 119, no. 1, pp. 128–139, Jan. 2019. [15] P. Heyns Adu, A. Eldor, R. Yarom, and G. Marx, “Zinc-induced platelet aggregation is mediated by the fibrinogen receptor and is not accompanied by release or by thromboxane synthesis,” Blood, vol. 66, no. 1, pp. 213–219, 1985. [16] B. L. O’Dell and M. Emery, “Compromised zinc status in rats adversely affects calcium metabolism in platelets,” J.Nutr., vol. 121, no. 11, pp. 1763–1768, 1991. [17] J. Xia and B. L. O’Dell, “Zinc deficiency in rats decreases thrombin-stimulated platelet aggregation by lowering protein kinase C activity secondary to impaired calcium uptake,” J. Nutr. Biochem, no. 6, pp. 661–666, 1995. [18] S. L. Sensi et al., “Measurement of intracellular free zinc in living cortical neurons: routes of entry,” J.Neurosci., vol. 17, no. 24, pp. 9554–9564, 1997. [19] Q. Lu, H. Haragopal, K. G. Slepchenko, C. Stork, and Y. V. Li, “Intracellular zinc distribution in mitochondria, ER and the Golgi apparatus,” Int J Physiol Pathophysiol Pharmacol, vol. 8, no. 1, pp. 35–43, 2016. [20] T. Kambe, K. M. Taylor, and D. Fu, “Zinc transporters and their functional integration in mammalian cells,” J Biol Chem, vol. 296, p. 100320, 2021, doi: 10.1016/j.jbc.2021.100320. [21] B.-H. Bin, J. Seo, and S. T. Kim, “Function, Structure, and Transport Aspects of ZIP and ZnT Zinc Transporters in Immune Cells,” Journal of Immunology Research, vol. 2018, pp. 1–9, Oct. 2018. [22] R. J. Cousins, J. P. Liuzzi, and L. A. Lichten, “Mammalian zinc transport, trafficking, and signals,” J Biol Chem, vol. 281, no. 34, pp. 24085–24089, Aug. 2006, doi: 10.1074/jbc.R600011200. [23] M. K. Monteilh-Zoller, M. C. Hermosura, M. J. S. Nadler, A. M. Scharenberg, R. Penner, and A. Fleig, “TRPM7 Provides an Ion Channel Mechanism for Cellular Entry of Trace Metal Ions,” J Gen Physiol, vol. 121, no. 1, pp. 49–60, Jan. 2003, doi: 10.1085/jgp.20028740. [24] M. Chevallet et al., “Functional consequences of the over-expression of TRPC6 channels in HEK cells: impact on the homeostasis of zinc,” Metallomics, vol. 6, no. 7, pp. 1269–1276, Jul. 2014, doi: 10.1039/c4mt00028e. [25] W. Maret, “The redox biology of redox-inert zinc ions,” Free Radic Biol Med, vol. 134, pp. 311–326, Apr. 2019, doi: 10.1016/j.freeradbiomed.2019.01.006. [26] M. E. Lopes-Pires, N. S. Ahmed, D. Vara, J. M. Gibbins, G. Pula, and N. Pugh, “Zinc regulates reactive oxygen species generation in platelets,” Platelets, pp. 1–10, Apr. 2020. [27] F. C. Gombedza, S. Shin, Y. L. Kanaras, and B. C. Bandyopadhyay, “Abrogation of store-operated Ca2+ entry protects against crystal-induced ER stress in human proximal tubular cells,” Cell Death Discov, vol. 5, p. 124, 2019, doi: 10.1038/s41420-019-0203-5. [28] G. P. Tolstykh, J. C. Cantu, M. Tarango, and B. L. Ibey, “Receptor- and store-operated mechanisms of calcium entry during the nanosecond electric pulse-induced cellular response,” Biochim Biophys Acta Biomembr, vol. 1861, no. 3, pp. 685–696, Mar. 2019, doi: 10.1016/j.bbamem.2018.12.007. [29] M. Prakriya and R. S. Lewis, “Store-Operated Calcium Channels,” Physiol Rev, vol. 95, no. 4, pp. 1383–1436, Oct. 2015, doi: 10.1152/physrev.00020.2014. [30] M. T. Harper and A. W. Poole, “Store-operated calcium entry and non-capacitative calcium entry have distinct roles in thrombin-induced calcium signalling in human platelets,” Cell Calcium, vol. 50, no. 4, pp. 351–358, Oct. 2011, doi: 10.1016/j.ceca.2011.06.005. [31] D. Varga-Szabo, A. Braun, and B. Nieswandt, “STIM and Orai in platelet function,” Cell Calcium, vol. 50, no. 3, pp. 270–278, 2011, doi: 10.1016/j.ceca.2011.04.002. [32] D. Varga-Szabo et al., “Store-operated Ca(2+) entry in platelets occurs independently of transient receptor potential (TRP) C1,” Pflugers Arch, vol. 457, no. 2, pp. 377–387, Nov. 2008, doi: 10.1007/s00424-008-0531-4. [33] K. Gilio et al., “Roles of platelet STIM1 and Orai1 in glycoprotein VI- and thrombin-dependent procoagulant activity and thrombus formation,” J Biol Chem, vol. 285, no. 31, pp. 23629–23638, Jul. 2010, doi: 10.1074/jbc.M110.108696. [34] D. Varga-Szabo, A. Braun, and B. Nieswandt, “Calcium signaling in platelets,” J.Thromb.Haemost., vol. 7, no. 7, pp. 1057–1066, 2009. [35] N. Pugh, D. Bihan, D. J. Perry, and R. W. Farndale, “Dynamic analysis of platelet deposition to resolve platelet adhesion receptor activity in whole blood at arterial shear rate,” Platelets, vol. 26, no. 3, pp. 216–219, 2015. [36] J. Gaburjakova and M. Gaburjakova, “The Cardiac Ryanodine Receptor Provides a Suitable Pathway for the Rapid Transport of Zinc (Zn2+),” Cells, vol. 11, no. 5, p. 868, Mar. 2022, doi: 10.3390/cells11050868. [37] J. Woodier, R. D. Rainbow, A. J. Stewart, and S. J. Pitt, “Intracellular Zinc Modulates Cardiac Ryanodine Receptor-mediated Calcium Release,” J. Biol. Chem., vol. 290, no. 28, pp. 17599–17610, Jul. 2015, doi: 10.1074/jbc.M115.661280. [38] A. G. S. Harper, S. L. Brownlow, and S. O. Sage, “A role for TRPV1 in agonist-evoked activation of human platelets,” J Thromb Haemost, vol. 7, no. 2, pp. 330–338, Feb. 2009, doi: 10.1111/j.1538-7836.2008.03231.x. [39] S. L. Brownlow and S. O. Sage, “Transient receptor potential protein subunit assembly and membrane distribution in human platelets,” Thromb Haemost, vol. 94, no. 4, pp. 839–845, Oct. 2005, doi: 10.1160/TH05-06-0391. [40] J. Zheng, “Molecular mechanism of TRP channels,” Compr Physiol, vol. 3, no. 1, pp. 221–242, Jan. 2013, doi: 10.1002/cphy.c120001. [41] R. A. Colvin, “Zinc inhibits Ca2+ transport by rat brain NA+/Ca2+ exchanger,” Neuroreport, vol. 9, no. 13, pp. 3091–3096, Sep. 1998, doi: 10.1097/00001756-199809140-00032. [42] R. Kraft, “The Na+/Ca2+ exchange inhibitor KB-R7943 potently blocks TRPC channels,” Biochemical and Biophysical Research Communications, vol. 361, no. 1, pp. 230–236, Sep. 2007, doi: 10.1016/j.bbrc.2007.07.019. [43] L. Albarrán, J. J. Lopez, N. Dionisio, T. Smani, G. M. Salido, and J. A. Rosado, “Transient receptor potential ankyrin-1 (TRPA1) modulates store-operated Ca(2+) entry by regulation of STIM1-Orai1 association,” Biochim Biophys Acta, vol. 1833, no. 12, pp. 3025–3034, Dec. 2013, doi: 10.1016/j.bbamcr.2013.08.014. [44] K. Kazandzhieva, E. Mammadova-Bach, A. Dietrich, T. Gudermann, and A. Braun, “TRP channel function in platelets and megakaryocytes: basic mechanisms and pathophysiological impact,” Pharmacol Ther, vol. 237, p. 108164, Sep. 2022, doi: 10.1016/j.pharmthera.2022.108164. [45] M. Estacion et al., “Activation of human TRPC6 channels by receptor stimulation,” J Biol Chem, vol. 279, no. 21, pp. 22047–22056, May 2004, doi: 10.1074/jbc.M402320200. [46] S. M. Bousquet, M. Monet, and G. Boulay, “Protein kinase C-dependent phosphorylation of transient receptor potential canonical 6 (TRPC6) on serine 448 causes channel inhibition,” J Biol Chem, vol. 285, no. 52, pp. 40534–40543, Dec. 2010, doi: 10.1074/jbc.M110.160051. [47] J. T. Warren, Q. Guo, and W.-J. Tang, “A 1.3-A structure of zinc-bound N-terminal domain of calmodulin elucidates potential early ion-binding step,” J Mol Biol, vol. 374, no. 2, pp. 517–527, Nov. 2007, doi: 10.1016/j.jmb.2007.09.048. [48] J. S. Mills and J. D. Johnson, “Metal ions as allosteric regulators of calmodulin,” J. Biol. Chem., vol. 260, no. 28, pp. 15100–15105, Dec. 1985. [49] S. Ziliotto et al., “Activated zinc transporter ZIP7 as an indicator of anti-hormone resistance in breast cancer,” Metallomics, vol. 11, no. 9, pp. 1579–1592, Sep. 2019, doi: 10.1039/c9mt00136k. [50] K. M. Taylor, S. Hiscox, R. I. Nicholson, C. Hogstrand, and P. Kille, “Protein kinase CK2 triggers cytosolic zinc signaling pathways by phosphorylation of zinc channel ZIP7,” Sci.Signal., vol. 5, no. 210, p. ra11, 2012, doi: 10.1126/scisignal.2002585. [51] N. Calloway, M. Vig, J.-P. Kinet, D. Holowka, and B. Baird, “Molecular clustering of STIM1 with Orai1/CRACM1 at the plasma membrane depends dynamically on depletion of Ca2+ stores and on electrostatic interactions,” Mol Biol Cell, vol. 20, no. 1, pp. 389–399, Jan. 2009, doi: 10.1091/mbc.e07-11-1132. [52] A. M. Sadaghiani et al., “Identification of Orai1 channel inhibitors by using minimal functional domains to screen small molecule microarrays,” Chem Biol, vol. 21, no. 10, pp. 1278–1292, Oct. 2014, doi: 10.1016/j.chembiol.2014.08.016. [53] S. Hojyo and T. Fukada, “Zinc transporters and signaling in physiology and pathogenesis,” Archives of Biochemistry and Biophysics, vol. 611, pp. 43–50, Dec. 2016. [54] K. S. Authi, “TRP channels in platelet function,” Handb Exp Pharmacol, no. 179, pp. 425–443, 2007, doi: 10.1007/978-3-540-34891-7_25. [55] N. Dionisio, P. C. Redondo, I. Jardin, and J. A. Rosado, “Transient receptor potential channels in human platelets: expression and functional role,” Curr Mol Med, vol. 12, no. 10, pp. 1319–1328, Dec. 2012, doi: 10.2174/156652412803833616. [56] G. Ramanathan et al., “Defective diacylglycerol-induced Ca2+ entry but normal agonist-induced activation responses in TRPC6-deficient mouse platelets,” J Thromb Haemost, vol. 10, no. 3, pp. 419–429, Mar. 2012, doi: 10.1111/j.1538-7836.2011.04596.x. [57] A. Fajmut, M. Brumen, and S. Schuster, “Theoretical model of the interactions between Ca2+, calmodulin and myosin light chain kinase,” FEBS Lett, vol. 579, no. 20, pp. 4361–4366, Aug. 2005, doi: 10.1016/j.febslet.2005.06.076. [58] K. E. Kamm and J. T. Stull, “Dedicated myosin light chain kinases with diverse cellular functions,” J Biol Chem, vol. 276, no. 7, pp. 4527–4530, Feb. 2001, doi: 10.1074/jbc.R000028200. [59] M. C. Carpenter and A. E. Palmer, “Native and engineered sensors for Ca2+ and Zn2+: lessons from calmodulin and MTF1,” Essays Biochem, vol. 61, no. 2, pp. 237–243, May 2017, doi: 10.1042/EBC20160069. [60] I. J. Forbes, P. D. Zalewski, and C. Giannakis, “Role for zinc in a cellular response mediated by protein kinase C in human B lymphocytes,” Exp. Cell Res., vol. 195, no. 1, pp. 224–229, Jul. 1991. [61] N. Ansari, H. Hadi-Alijanvand, M. Sabbaghian, M. Kiaei, and F. Khodagholi, “Interaction of 2-APB, dantrolene, and TDMT with IP3R and RyR modulates ER stress-induced programmed cell death I and II in neuron-like PC12 cells: an experimental and computational investigation,” J Biomol Struct Dyn, vol. 32, no. 8, pp. 1211–1230, 2014, doi: 10.1080/07391102.2013.812520. [62] R. F. P. Bertolo, W. J. Bettger, and S. A. Atkinson, “Calcium competes with zinc for a channel mechanism on the brush border membrane of piglet intestine,” J Nutr Biochem, vol. 12, no. 2, pp. 66–72, Feb. 2001, doi: 10.1016/s0955-2863(00)00125-x. [63] J. M. Burkhart et al., “The first comprehensive and quantitative analysis of human platelet protein composition allows the comparative analysis of structural and functional pathways,” Blood, vol. 120, no. 15, pp. e73-82, 2012, doi: 10.1182/blood-2012-04-416594. [64] C. Hogstrand, P. Kille, R. I. Nicholson, and K. M. Taylor, “Zinc transporters and cancer: a potential role for ZIP7 as a hub for tyrosine kinase activation,” Trends Mol.Med., vol. 15, no. 3, pp. 101–111, 2009. [65] K. M. Taylor, P. Vichova, N. Jordan, S. Hiscox, R. Hendley, and R. I. Nicholson, “ZIP7-mediated intracellular zinc transport contributes to aberrant growth factor signaling in antihormone-resistant breast cancer Cells,” Endocrinology, vol. 149, no. 10, pp. 4912–4920, 2008, doi: 10.1210/en.2008-0351. [66] S. Yamasaki et al., “Zinc is a novel intracellular second messenger,” J. Cell Biol., vol. 177, no. 4, pp. 637–645, May 2007. [67] C. J. Stork and Y. V. Li, “Zinc release from thapsigargin/IP3-sensitive stores in cultured cortical neurons,” J Mol Signal, vol. 5, p. 5, May 2010, doi: 10.1186/1750-2187-5-5.