Pericellular ca2+ recycling potentiates thrombin-evoked Ca2+ signals in human platelets

Physiological Reports

Volumn 1, Issue 5, 2013, Pages

  Sage, Stewart O ^a   Pugh, Nicholas ^a   Farndale, Richard W ^a   Harper, Alan G S ^a,b  

^a UNIVERSITY OF CAMBRIDGE   (United Kingdom)

^b KEELE UNIVERSITY   (United Kingdom)

Author keywords

Ca2+; FFP 18; Nanojunction; Open canalicular system; Pericellular; Platelets

Indexed keywords

2 [2 [4 (4 NITROBENZYLOXY)PHENYL]ETHYL]ISOTHIOUREA METHANESULFONATE; CALCIUM CHANNEL; CALCIUM CHANNEL BLOCKING AGENT; FURA 2; MRS 1845; SN 6; SODIUM CALCIUM EXCHANGE PROTEIN; THROMBIN; UNCLASSIFIED DRUG;

ARTICLE; AUTOCRINE EFFECT; BINDING AFFINITY; CALCIUM BINDING; CALCIUM CELL LEVEL; CALCIUM SIGNALING; CALCIUM TRANSPORT; CONTROLLED STUDY; CYTOSOL; DRUG MECHANISM; GLYCOCALYX; HUMAN; HUMAN CELL; NORMAL HUMAN; SECRETORY GRANULE; SODIUM CELL LEVEL; THROMBOCYTE; THROMBOCYTE RICH PLASMA;

EID: 84927579255     PISSN: None     EISSN: 2051817X     Source Type: Journal    
DOI: 10.1002/phy2.85     Document Type: Article

References (70)

1. Alonso, M. T., A. Sanchez, and J. Garcia-Sancho. 1989. Effects of sodium removal on calcium mobilization and dense granule secretion induced by thrombin in human platelets. Biochim. Biophys. Acta 981: 367–370.
2. Alonso, M. T., J. Alvarez, M. Montero, A. Sanchez, and J. Garcia-Sancho. 1991. Agonist-induced Ca2+ influx into human platelets is secondary to the emptying of intracellular Ca2+ stores. Biochem. J. 280: 783–789.
3. Ariyoshi, H., and E. W. Salzman. 1996. Association of localized Ca2+ gradients with redistribution of glycoprotein IIb-IIIa and F-actin in activated human blood platelets. Arterioscler. Thromb. Vasc. Biol. 16: 230–235.
4. Blatter, L. A., and E. Niggli. 1998. Confocal near-membrane detection of calcium in cardiac myocytes. Cell Calcium 23: 269–279.
5. Blaustein, M. P., and W. Lederer. 1999. Sodium/Calcium exchange: its physiological implications. Physiol. Rev. 79: 763–854.
6. Bolsover, S. R. 1986. Two components of voltage-dependent calcium influx in mouse neuroblastoma cells: measurement with Arsenazo III. J. Gen. Physiol. 88: 149–165.
7. 2+ homeostasis in unstimulated platelets. J. Biol. Chem. 259: 12571–12575.
8. Brass, L. F., and S. J. Shattil. 1982. Changes in surface-bound and exchangeable calcium during platelet activation. J. Biol. Chem. 257: 14000–14005.
9. Burkhart, J. M., M. Vaudel, S. Gambaryan, S. Radau, U. Walter, L. Martens, et al. 2012. The first comprehensive and quantitative analysis of human platelet protein composition allows the comparative analysis of structural and functional pathways. Blood 120: e73–e82.
10. Cutler, L. S., M. B. Feinstein, and C. P. Christian. 1980. Cytochemical localization of ouabain-sensitive (K+)-dependent p-nitrophenyl phosphatase (transport ATPase) in human blood platelets. J. Histochem. Cytochem. 28: 1183–1188.
11. Deisseroth, K., H. Bito, and R. W. Tsien. 1996. Signalling from synapse to nucleus: postsynaptic CREB phosphorylation during multiple forms of hippocampal synaptic plasticity. Neuron 16: 89–101.
12. Diener, H. C., D. Schneider, Y. Lampl, N. M. Bornstein, A. Kozak, and G. Rosenberg. 2008. DP-b99, a membrane-activated metal ion chelator, as neuroprotective therapy in ischemic stroke. Stroke 39: 1774–1778.
13. DiPolo, R., and L. Beauge. 1996. Sodium/Calcium Exchanger: influence of metabolic regulations on ion carrier interactions. Physiol. Rev. 86: 155–203.
14. 2+ indicator FFP18. Proc. Natl Acad. Sci. USA 93: 5368–5373.
15. Fromjovich, M. M., and J. G. Milton. 1982. Human platelet size, shape and related functions in health and disease. Physiol. Rev. 62: 185–261.
16. 2+ in the human platelet. J. Thromb. Haemost. 5: 910–917.
17. van Gorp, R. M., M. A. Feijge, W. M. Vuist, M. B. Rook, and J. W. M. Heemskerk. 2002. Irregular spiking in free calcium concentration in single, human platelets. Regulation by modulation of the inositol trisphosphate receptors. Eur. J. Biochem. 269: 1543–1552.
18. 2+ indicators with greatly improved fluorescence properties. J. Biol. Chem. 260: 3440–3450.
19. Hallam, T. J., and T. J. Rink. 1985. Agonists stimulate divalent cation channels in the plasma membrane of human platelets. FEBS Lett. 186: 175–179.
20. 2+ entry in human platelets: evidence against the de novo conformational coupling hypothesis. Cell Calcium 42: 606–617.
21. Harper, A. G. S., S. L. Brownlow, and S. O. Sage. 2009a. A role for TRPV1 in agonist-evoked activation of human platelets. J. Thromb. Haemost. 7: 330–338.
22. 2+ signal arising from store-operated calcium entry in human platelets. Cell Calcium 45: 413–420.
23. 2+ entry. J. Thromb. Haemost. 8: 1604–1613.
24. Heemskerk, J. W. M., G. M. Willems, M. B. Rook, and S. O. Sage. 2001. Ragged spiking of free calcium in ADP-stimulated human platelets: regulation of puff-like calcium signals in vitro and ex vivo. J. Physiol. 535: 625–635.
25. 2+-ATPase polypeptide in human platelets. Biochem. Biophys. Res. Commun. 153: 848–854.
26. Holmsen, H., and H. J. Weiss. 1979. Secretable storage pools in platelets. Annu. Rev. Med. 30: 119–134.
27. 2+ mobilization and aggregation in human platelets. FEBS Lett. 225: 72–76.
28. 2+ exchanger isoforms by divalent cations and isothiourea derivative. Am. J. Physiol. 275: C423–C430.
29. Jones, S., A. Solomon, D. Sanz-Rosa, C. Moore, L. Holbrook, E. J. Cartwright, et al. 2010. The plasma membrane calcium ATPase modulates calcium homeostasis, intracellular signaling events and function in platelets. J. Thromb. Haemost. 8: 2766–2774.
30. Jy, W., and D. H. Haynes. 1987. Thrombin-induced calcium movements in platelet activation. Biochim. Biophys. Acta 929: 88–102.
31. Lages, B., and H. J. Weiss. 1999. Secreted dense granule adenine nucleotides promote calcium influx and the maintenance of elevated cytosolic calcium levels in stimulated human platelets. Thromb. Haemost. 81: 286–292.
32. Lewandrowski, U., S. Wortelkamp, K. Lohrig, R. P. Zahedi, D. A. Wolters, U. Walter, et al. 2009. Platelet membrane proteomics: a novel repository for functional research. Blood 114: 10–19.
33. MacIntyre, D. E., and T. J. Rink. 1982. The role of platelet membrane potential in the initiation of aggregation. Thromb. Haemost. 47: 22–26.
34. Mahaut-Smith, M. P. 1995. Calcium-activated potassium channels in human platelets. J. Physiol. 484: 15–24.
35. Mahaut-Smith, M. P., T. J. Rink, S. C. Collins, and S. O. Sage. 1990. Voltage-gated potassium channels and the control of membrane potential in human platelets. J. Physiol. 428: 723–735.
36. Merritt, J. E., W. P. Armstrong, C. D. Benham, T. J. Hallam, R. Jacob, A. Jaxa-Chamiec, et al. 1990. SK&F 96365, a novel inhibitor of receptor-mediated calcium entry. Biochem. J. 271: 515–522.
37. Mihalyi, E. 2004. A review of some unusual effects of calcium binding to fibrinogen. Biophys. Chem. 112: 131–140.
38. Mogami, H., J. Gardner, O. V. Gerasimenko, P. Camello, O. H. Petersen, and A. V. Tepikin. 1999. Calcium binding capacity of the cytoplasm and endoplasmic reticulum of mouse pancreatic acinar cells. J. Physiol. 518: 463–467.
39. 2+ cycling in vascular smooth muscle. Cell Calcium 24: 275–283.
40. Neco, P., B. Rose, N. Hyunh, R. Zhang, J. H. B. Bridge, K. D. Philipson, et al. 2010. Sodium-calcium exchange is essential for effective triggering calcium release in mouse heart. Biophys. J. 99: 755–764.
41. Nesbitt, W. S., S. Giuliano, S. Kulkarni, S. M. Dopheide, I. S. Harper, and S. P. Jackson. 2003. Intercellular calcium communication regulates platelet aggregation and thrombus growth. J. Cell Biol. 160: 1151–1161.
42. 2+ signalling events. Cell Calcium 4–5: 379–387.
43. van Nispen tot Pannerden, H., F. de Haas, W. Geerts, G. Posthuma, S. van Dijk, and H. F. G. Heijnen. 2010. The platelet interior revisited: electron tomography reveals tubular a-granule subtypes. Blood 116: 1147–1156.
44. Orchard, C. H., M. Pasek, and F. Brette. 2009. The role of mammalian cardiac t-tubules in excitation–contraction coupling: experimental and computational approaches. Exp. Physiol. 94: 509–519.
45. Petersen, O. H., and A. Verkhratsky. 2007. Endoplasmic reticulum calcium tunnels integrate signalling in polarized cells. Cell Calcium 42: 373–378.
46. Pethig, R., M. Kuhn, R. Payne, E. Adler, T. H. Chen, and L. F. Jaffe. 1989. On the dissociation constants of BAPTA-type calcium buffers. Cell Calcium 10: 491–498.
47. Pipili, E. 1985. Platelet membrane potential: simultaneous measurement of DiSC3 (5) fluorescence and optical density. Thromb. Haemost. 54: 645–649.
48. Prakriya, M., and R. S. Lewis. 2003. CRAC channels: activation, permeation and the search for a molecular identity. Cell Calcium 33: 311–321.
49. Purvis, J. E., M. S. Chatterjee, L. F. Brass, and S. L. Diamond. 2008. A molecular signalling model of platelet phosphoinositide and calcium regulation during homeostasis and P2Y1 activation. Blood 112: 4069–4079.
50. 2+ exchange in plasma membrane vesicles. Thromb. Haemost. 57: 337–340.
51. Rink, T. J., and S. O. Sage. 1990. Calcium signalling in human platelets. Annu. Rev. Physiol. 52: 429–447.
52. Rittenhouse, S. E., and J. P. Sasson. 1985. Mass changes in myoinositol trisphosphate in human platelets stimulated by thrombin. J. Biol. Chem. 260: 8657–8660.
53. Roberts, D. E., A. McNicol, and R. Bose. 2004. Mechanism of collagen activation in human platelets. J. Biol. Chem. 279: 19421–19430.
54. 2+ exchangers. Br. J. Pharmacol. 165: 922–936.
55. Rosado, J. A., E. M. Meijer, K. Hamulyak, I. Novakova, J. W. Heemskerk, and S. O. Sage. 2001. Fibrinogen binding to the integrin alpha (IIb) beta (3) modulates store-mediated calcium entry in human platelets. Blood 97: 2648–2656.
56. Ruiz, F. A., C. R. Lea, E. Oldfield, and R. Docampo. 2004. Human platelet dense granules contain polyphosphate and are similar to acidocalcisomes of bacteria and unicellular eukaryotes. J. Biol. Chem. 297: 44250–44257.
57. Sage, S. O., and T. J. Rink. 1987. The kinetics of changes in intracellular calcium concentration in fura-2-loaded human platelets. J. Biol. Chem. 262: 16364–16369.
58. 2+ concentration in agonist-stimulated, intact human platelets using Fluo-5N. J. Thromb. Haemost. 9: 540–551.
59. 2+] and pH in human platelets. Cytoplasmic alkalinisation is not a prerequisite for calcium mobilization. Biochim. Biophys. Acta 938: 497–500.
60. Sato, T., L. Herman, J. A. Chandler, A. Stracher, and T. C. Detwiler. 1975. Localisation of a thrombin-sensitive calcium pool in platelets. J. Histiochem. Cytochem. 23: 103–106.
61. Schaeffer, J., and M. P. Blaustein. 1989. Platelet-free calcium concentrations measured with fura-2 are influenced by the transmembrane sodium gradient. Cell Calcium 10: 101–113.
62. 2+ buffers. Cold Spring Harb. Perspect. Biol. 2: a004051.
63. 2+. Nature 325: 456–458.
64. Somasunduram, B., M. J. Mason, and M. P. Mahaut-Smith. 1997. Thrombin dependent calcium signalling in single human erythroleukaemia cells. J. Physiol. 501: 485–495.
65. Stamouli, V., C. Vakirtzi-Lemonias, and W. Siffert. 1993. Thrombin and NaF, but not epinephrine, raise cytosolic free Na+ in human platelets. Biochim. Biophys. Acta 1176: 215–221.
66. Steiner, M. 1986. Role of glycosaminoglycans in calcium metabolism of human platelets. Biochim. Biophys. Acta 886: 406–410.
67. Stern, M. D. 1992. Buffering of calcium in the vicinity of a channel pore. Cell Calcium 13: 183–192.
68. Tang, Q., M.-W. Jin, J.-Z. Xiang, M.-Q. Dong, H.-Y. Sun, C.-P. Lau, et al. 2007. The membrane permeable calcium chelator BAPTA-AM directly blocks human ether ether a-go-go-related gene potassium channels stably expressed in HEK 293 cells. Biochem. Pharmacol. 74: 1596–1607.
69. 2+-activated K+ currents in cultured bovine chromaffin cells. NeuroReport 9: 3403–3407.
70. White, J. G. 1972. Interaction of membrane systems in blood platelets. Am. J. Pathol. 66: 295–312.