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. 1995 May;115(1):101–106. doi: 10.1111/j.1476-5381.1995.tb16326.x

Regulation of cytosolic calcium by collagen in single human platelets.

A W Poole 1, S P Watson 1
PMCID: PMC1908739  PMID: 7647963

Abstract

1. There is controversy in the literature as to whether collagen is able to induce directly a rise in cytosolic calcium concentration ([Ca2+]i) in human platelets. We have addressed this question by observing the cytosolic calcium response of single fura-2-loaded human platelets settling onto a collagen-coated surface using dynamic fluorescence ratio imaging. 2. Following a short lag phase after adherence to collagen fibres, platelets underwent a rapid rise in cytosolic calcium from basal values of 80 +/- 13 nM (n = 24) to a peak of 475 +/- 42 nM (n = 24) which was sustained for the remaining period of the experiment. 3. The tyrphostin protein tyrosine kinase inhibitor, ST271, reduced substantially the proportion of platelets which exhibited a rise in [Ca2+]i on adherence to collagen and transformed the response in remaining cells to one of oscillations. 4. In contrast, and as a control for collagen, laminin-coated surfaces induced adherence of human platelets without elevating intracellular [Ca2+]; the cells however remained responsive to ADP. 5. We conclude that collagen directly induces a rise in cytosolic calcium in single human platelets through a tyrosine kinase-mediated pathway.

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Selected References

These references are in PubMed. This may not be the complete list of references from this article.

  1. Anderson G. P., Anderson C. L. Signal transduction by the platelet Fc receptor. Blood. 1990 Sep 15;76(6):1165–1172. [PubMed] [Google Scholar]
  2. Berridge M. J. Calcium oscillations. J Biol Chem. 1990 Jun 15;265(17):9583–9586. [PubMed] [Google Scholar]
  3. Berridge M. J., Galione A. Cytosolic calcium oscillators. FASEB J. 1988 Dec;2(15):3074–3082. doi: 10.1096/fasebj.2.15.2847949. [DOI] [PubMed] [Google Scholar]
  4. Blake R. A., Schieven G. L., Watson S. P. Collagen stimulates tyrosine phosphorylation of phospholipase C-gamma 2 but not phospholipase C-gamma 1 in human platelets. FEBS Lett. 1994 Oct 17;353(2):212–216. doi: 10.1016/0014-5793(94)01037-4. [DOI] [PubMed] [Google Scholar]
  5. Blake R. A., Walker T. R., Watson S. P. Activation of human platelets by peroxovanadate is associated with tyrosine phosphorylation of phospholipase C gamma and formation of inositol phosphates. Biochem J. 1993 Mar 1;290(Pt 2):471–475. doi: 10.1042/bj2900471. [DOI] [PMC free article] [PubMed] [Google Scholar]
  6. Chiang T. M., Kang A. H. Isolation and purification of collagen alpha 1(I) receptor from human platelet membrane. J Biol Chem. 1982 Jul 10;257(13):7581–7586. [PubMed] [Google Scholar]
  7. Chiang T. M., Seyer J. M., Kang A. H. Collagen-platelet interaction: separate receptor sites for types I and III collagen. Thromb Res. 1993 Sep 15;71(6):443–456. doi: 10.1016/0049-3848(93)90118-8. [DOI] [PubMed] [Google Scholar]
  8. Coller B. S., Beer J. H., Scudder L. E., Steinberg M. H. Collagen-platelet interactions: evidence for a direct interaction of collagen with platelet GPIa/IIa and an indirect interaction with platelet GPIIb/IIIa mediated by adhesive proteins. Blood. 1989 Jul;74(1):182–192. [PubMed] [Google Scholar]
  9. Daniel J. L., Dangelmaier C., Smith J. B. Evidence for a role for tyrosine phosphorylation of phospholipase C gamma 2 in collagen-induced platelet cytosolic calcium mobilization. Biochem J. 1994 Sep 1;302(Pt 2):617–622. doi: 10.1042/bj3020617. [DOI] [PMC free article] [PubMed] [Google Scholar]
  10. Haimovich B., Lipfert L., Brugge J. S., Shattil S. J. Tyrosine phosphorylation and cytoskeletal reorganization in platelets are triggered by interaction of integrin receptors with their immobilized ligands. J Biol Chem. 1993 Jul 25;268(21):15868–15877. [PubMed] [Google Scholar]
  11. Harootunian A. T., Kao J. P., Paranjape S., Tsien R. Y. Generation of calcium oscillations in fibroblasts by positive feedback between calcium and IP3. Science. 1991 Jan 4;251(4989):75–78. doi: 10.1126/science.1986413. [DOI] [PubMed] [Google Scholar]
  12. Heemskerk J. W., Hoyland J., Mason W. T., Sage S. O. Spiking in cytosolic calcium concentration in single fibrinogen-bound fura-2-loaded human platelets. Biochem J. 1992 Apr 15;283(Pt 2):379–383. doi: 10.1042/bj2830379. [DOI] [PMC free article] [PubMed] [Google Scholar]
  13. Heemskerk J. W., Vis P., Feijge M. A., Hoyland J., Mason W. T., Sage S. O. Roles of phospholipase C and Ca(2+)-ATPase in calcium responses of single, fibrinogen-bound platelets. J Biol Chem. 1993 Jan 5;268(1):356–363. [PubMed] [Google Scholar]
  14. King M., McDermott P., Schreiber A. D. Characterization of the Fc gamma receptor on human platelets. Cell Immunol. 1990 Jul;128(2):462–479. doi: 10.1016/0008-8749(90)90041-o. [DOI] [PubMed] [Google Scholar]
  15. Kruse H. J., Negrescu E. V., Weber P. C., Siess W. Thrombin-induced Ca2+ influx and protein tyrosine phosphorylation in endothelial cells is inhibited by herbimycin A. Biochem Biophys Res Commun. 1994 Aug 15;202(3):1651–1656. doi: 10.1006/bbrc.1994.2123. [DOI] [PubMed] [Google Scholar]
  16. Lee K. M., Toscas K., Villereal M. L. Inhibition of bradykinin- and thapsigargin-induced Ca2+ entry by tyrosine kinase inhibitors. J Biol Chem. 1993 May 15;268(14):9945–9948. [PubMed] [Google Scholar]
  17. Nieuwenhuis H. K., Akkerman J. W., Houdijk W. P., Sixma J. J. Human blood platelets showing no response to collagen fail to express surface glycoprotein Ia. Nature. 1985 Dec 5;318(6045):470–472. doi: 10.1038/318470a0. [DOI] [PubMed] [Google Scholar]
  18. Nishio H., Ikegami Y., Segawa T. Fluorescence digital image analysis of serotonin-induced calcium oscillations in single blood platelets. Cell Calcium. 1991 Feb-Mar;12(2-3):177–184. doi: 10.1016/0143-4160(91)90019-b. [DOI] [PubMed] [Google Scholar]
  19. Poenie M. Alteration of intracellular Fura-2 fluorescence by viscosity: a simple correction. Cell Calcium. 1990 Feb-Mar;11(2-3):85–91. doi: 10.1016/0143-4160(90)90062-y. [DOI] [PubMed] [Google Scholar]
  20. Pollock W. K., Rink T. J., Irvine R. F. Liberation of [3H]arachidonic acid and changes in cytosolic free calcium in fura-2-loaded human platelets stimulated by ionomycin and collagen. Biochem J. 1986 May 1;235(3):869–877. doi: 10.1042/bj2350869. [DOI] [PMC free article] [PubMed] [Google Scholar]
  21. Rhee S. G., Choi K. D. Regulation of inositol phospholipid-specific phospholipase C isozymes. J Biol Chem. 1992 Jun 25;267(18):12393–12396. [PubMed] [Google Scholar]
  22. Rink T. J., Sanchez A., Hallam T. J. Diacylglycerol and phorbol ester stimulate secretion without raising cytoplasmic free calcium in human platelets. Nature. 1983 Sep 22;305(5932):317–319. doi: 10.1038/305317a0. [DOI] [PubMed] [Google Scholar]
  23. Santoro S. A. Identification of a 160,000 dalton platelet membrane protein that mediates the initial divalent cation-dependent adhesion of platelets to collagen. Cell. 1986 Sep 12;46(6):913–920. doi: 10.1016/0092-8674(86)90073-5. [DOI] [PubMed] [Google Scholar]
  24. Sargeant P., Farndale R. W., Sage S. O. ADP- and thapsigargin-evoked Ca2+ entry and protein-tyrosine phosphorylation are inhibited by the tyrosine kinase inhibitors genistein and methyl-2,5-dihydroxycinnamate in fura-2-loaded human platelets. J Biol Chem. 1993 Aug 25;268(24):18151–18156. [PubMed] [Google Scholar]
  25. Sargeant P., Farndale R. W., Sage S. O. The tyrosine kinase inhibitors methyl 2,5-dihydroxycinnamate and genistein reduce thrombin-evoked tyrosine phosphorylation and Ca2+ entry in human platelets. FEBS Lett. 1993 Jan 11;315(3):242–246. doi: 10.1016/0014-5793(93)81172-v. [DOI] [PubMed] [Google Scholar]
  26. Shattil S. J., Brugge J. S. Protein tyrosine phosphorylation and the adhesive functions of platelets. Curr Opin Cell Biol. 1991 Oct;3(5):869–879. doi: 10.1016/0955-0674(91)90062-4. [DOI] [PubMed] [Google Scholar]
  27. Smith J. B., Dangelmaier C. Determination of platelet adhesion to collagen and the associated formation of phosphatidic acid and calcium mobilization. Anal Biochem. 1990 May 15;187(1):173–178. doi: 10.1016/0003-2697(90)90437-e. [DOI] [PubMed] [Google Scholar]
  28. Smith J. B., Selak M. A., Dangelmaier C., Daniel J. L. Cytosolic calcium as a second messenger for collagen-induced platelet responses. Biochem J. 1992 Dec 15;288(Pt 3):925–929. doi: 10.1042/bj2880925. [DOI] [PMC free article] [PubMed] [Google Scholar]
  29. Sonnenberg A., Modderman P. W., Hogervorst F. Laminin receptor on platelets is the integrin VLA-6. Nature. 1988 Dec 1;336(6198):487–489. doi: 10.1038/336487a0. [DOI] [PubMed] [Google Scholar]
  30. Sugiyama T., Okuma M., Ushikubi F., Sensaki S., Kanaji K., Uchino H. A novel platelet aggregating factor found in a patient with defective collagen-induced platelet aggregation and autoimmune thrombocytopenia. Blood. 1987 Jun;69(6):1712–1720. [PubMed] [Google Scholar]
  31. Tandon N. N., Kralisz U., Jamieson G. A. Identification of glycoprotein IV (CD36) as a primary receptor for platelet-collagen adhesion. J Biol Chem. 1989 May 5;264(13):7576–7583. [PubMed] [Google Scholar]
  32. Vostal J. G., Jackson W. L., Shulman N. R. Cytosolic and stored calcium antagonistically control tyrosine phosphorylation of specific platelet proteins. J Biol Chem. 1991 Sep 5;266(25):16911–16916. [PubMed] [Google Scholar]
  33. Watson S. P., Reep B., McConnell R. T., Lapetina E. G. Collagen stimulates [3H]inositol trisphosphate formation in indomethacin-treated human platelets. Biochem J. 1985 Mar 15;226(3):831–837. doi: 10.1042/bj2260831. [DOI] [PMC free article] [PubMed] [Google Scholar]

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