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Calcium oscillation and phosphatidylinositol 3-kinase positively regulate integrin αIIbβ3-mediated outside-in signaling

  • Published:
Journal of Biomedical Science

Summary

The frequency of calcium oscillation reveals the platelet activation status, however, the biological significance of the periodic calcium responses and methods of communication with other integrin-mediated signals are not clear. RGD-containing disintegrin rhodostomin coated substrates were employed to enhance platelet spreading and calcium oscillation through direct binding and clustering of the receptor integrin αIIbβ3. The results showed that the activation of phosphatidylinositol 3-kinase (PI3-K) and internal calcium pathways were crucial for αIIbβ3 outside-in signaling. PI3-K antagonists wortmannin and LY294002 inhibited disintegrin substrates and induced platelet spreading and calcium oscillation. At the same time, pretreatment of platelets with the microsomal calcium–ATPase inhibitor thapsigargin to deplete internal calcium stores severely impaired the calcium oscillation as well as PI3-K activation and spreading on disintegrin substrates. Because inhibition of one pathway could inhibit the other, our data indicates that PI3-K and calcium oscillation are synergistically operated and form a positive-feedback regulation in integrin αIIbβ3-mediated outside-in signaling.

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References

  1. R.O. Hynes (1992) ArticleTitleIntegrins: versatility, modulation, and signaling in cell adhesion Cell 69 11–25 Occurrence Handle10.1016/0092-8674(92)90115-S Occurrence Handle1:CAS:528:DyaK38XitFWmtrg%3D Occurrence Handle1555235

    Article  CAS  PubMed  Google Scholar 

  2. R. Pytela M.D. Pierschbacher M.H. Ginsberg E.F. Plow E. Ruoslahti (1986) ArticleTitlePlatelet membrane glycoprotein IIb/IIIa: member of a family of Arg–Gly–Asp-specific adhesion receptors Science 231 1559–1562 Occurrence Handle1:CAS:528:DyaL28XksFymsLs%3D Occurrence Handle2420006

    CAS  PubMed  Google Scholar 

  3. E. Ruoslahti (1991) ArticleTitleIntegrins J. Clin. Invest. 87 1–5 Occurrence Handle1:CAS:528:DyaK3MXnslSqsg%3D%3D Occurrence Handle1985087

    CAS  PubMed  Google Scholar 

  4. H.H. Chang J.H. Kau S.J. Lo D.S. Sun (2003) ArticleTitleCell-adhesion and morphological changes are not sufficient to support anchorage-dependent cell growth via non-integrin-mediated attachment Cell Biol. Int. 27 123–133 Occurrence Handle10.1016/S1065-6995(02)00295-0 Occurrence Handle1:CAS:528:DC%2BD3sXitlWhtb8%3D Occurrence Handle12662969

    Article  CAS  PubMed  Google Scholar 

  5. H.H. Chang C.H. Lin S.J. Lo (1999) ArticleTitleRecombinant rhodostomin substrates induce transformation and active calcium oscillation in human platelets Exp. Cell Res. 250 387–400 Occurrence Handle10.1006/excr.1999.4547 Occurrence Handle1:CAS:528:DyaK1MXksFSjsb0%3D Occurrence Handle10413593

    Article  CAS  PubMed  Google Scholar 

  6. H.H. Chang S.J. Lo (1998) ArticleTitleFull-spreading platelets induced by the recombinant rhodostomin are via binding to integrins and correlated with FAK phosphorylation Toxicon 36 1087–1099 Occurrence Handle10.1016/S0041-0101(98)00088-9 Occurrence Handle1:CAS:528:DyaK1cXksFGqtrw%3D Occurrence Handle9690777

    Article  CAS  PubMed  Google Scholar 

  7. W.B. Wu H.C. Peng T.F. Huang (2003) ArticleTitleDisintegrin causes proteolysis of beta-catenin and apoptosis of endothelial cells. Involvement of cell-cell and cell-ECM interactions in regulating cell viability Exp. Cell. Res. 286 115–127 Occurrence Handle10.1016/S0014-4827(03)00105-8 Occurrence Handle1:CAS:528:DC%2BD3sXjt1OjsL8%3D Occurrence Handle12729800

    Article  CAS  PubMed  Google Scholar 

  8. B. Payrastre K. Missy C. Trumel S. Bodin M. Plantavid H. Chap (2000) ArticleTitleThe integrin alpha IIb/beta 3 in human platelet signal transduction Biochem. Pharmacol. 60 1069–1074 Occurrence Handle10.1016/S0006-2952(00)00417-2 Occurrence Handle1:CAS:528:DC%2BD3cXmslOjsLc%3D Occurrence Handle11007943

    Article  CAS  PubMed  Google Scholar 

  9. E.A. Clark J.S. Brugge (1995) ArticleTitleIntegrins and signal transduction pathways: the road taken Science 268 233–239 Occurrence Handle1:CAS:528:DyaK2MXltVCitLk%3D Occurrence Handle7716514

    CAS  PubMed  Google Scholar 

  10. M.A. Schwartz M.D. Schaller M.H. Ginsberg (1995) ArticleTitleIntegrins: emerging paradigms of signal transduction Annu. Rev. Cell. Dev. Biol. 11 549–599 Occurrence Handle10.1146/annurev.cb.11.110195.003001 Occurrence Handle1:CAS:528:DyaK2MXps1aqt7w%3D Occurrence Handle8689569

    Article  CAS  PubMed  Google Scholar 

  11. Y. Chang T.L. Chen G.J. Wu G. Hsiao M.Y. Shen K.H. Lin D.S. Chou C.H. Lin J.R. Sheu (2004) ArticleTitleMechanisms involved in the antiplatelet activity of ketamine in human platelets J. Biomed. Sci. 11 764–772 Occurrence Handle10.1159/000081823 Occurrence Handle1:CAS:528:DC%2BD2cXhtVOjsL7L Occurrence Handle15591773

    Article  CAS  PubMed  Google Scholar 

  12. E.A. Clark S.J. Shattil J.S. Brugge (1994) ArticleTitleRegulation of protein tyrosine kinases in platelets Trends Biochem. Sci. 19 464–469 Occurrence Handle10.1016/0968-0004(94)90131-7 Occurrence Handle1:CAS:528:DyaK2MXitlyhs7w%3D Occurrence Handle7855888

    Article  CAS  PubMed  Google Scholar 

  13. L. Lipfert B. Haimovich M.D. Schaller B.S. Cobb J.T. Parsons J.S. Brugge (1992) ArticleTitleIntegrin-dependent phosphorylation and activation of the protein tyrosine kinase pp125FAK in platelets J. Cell Biol. 119 905–912 Occurrence Handle10.1083/jcb.119.4.905 Occurrence Handle1:CAS:528:DyaK38XmtlSqsro%3D Occurrence Handle1385445

    Article  CAS  PubMed  Google Scholar 

  14. B. Haimovich L. Lipfert J.S. Brugge S.J. Shattil (1993) ArticleTitleTyrosine phosphorylation and cytoskeletal reorganization in platelets are triggered by interaction of integrin receptors with their immobilized ligands J. Biol. Chem. 268 15868–15877 Occurrence Handle1:CAS:528:DyaK3sXlsFKqsrs%3D Occurrence Handle8340412

    CAS  PubMed  Google Scholar 

  15. B. Haimovich N. Kaneshiki P. Ji (1996) ArticleTitleProtein kinase C regulates tyrosine phosphorylation of pp125FAK in platelets adherent to fibrinogen Blood 87 152–161 Occurrence Handle1:CAS:528:DyaK28Xit1Sjtw%3D%3D Occurrence Handle8547637

    CAS  PubMed  Google Scholar 

  16. J.M. Heraud C. Racaud-Sultan D. Gironcel C. Albiges-Rizo T. Giacomini S. Roques V. Martel M. Breton-Douillon B. Perret H. Chap (1998) ArticleTitleLipid products of␣phosphoinositide 3-kinase and phosphatidylinositol 4′,5′-bisphosphate are both required for ADP-dependent platelet spreading J. Biol. Chem. 273 17817–17823 Occurrence Handle10.1074/jbc.273.28.17817 Occurrence Handle1:CAS:528:DyaK1cXkvFartrc%3D Occurrence Handle9651384

    Article  CAS  PubMed  Google Scholar 

  17. D.R. Phillips L. Nannizzi-Alaimo K.S. Prasad (2001) ArticleTitleBeta3 tyrosine phosphorylation in alphaIIbbeta3 (platelet membrane GP IIb-IIIa) outside-in integrin signaling Thromb. Haemost. 86 246–258 Occurrence Handle1:CAS:528:DC%2BD3MXlsVeksbs%3D Occurrence Handle11487013

    CAS  PubMed  Google Scholar 

  18. S.J. Shattil H. Kashiwagi N. Pampori (1998) ArticleTitleIntegrin signaling: the platelet paradigm Blood 91 2645–2657 Occurrence Handle1:CAS:528:DyaK1cXisVWlt74%3D Occurrence Handle9531572

    CAS  PubMed  Google Scholar 

  19. M.S. Kwon C.S. Park K. Choi J. Ahnn J.I. Kim S.H. Eom S.J. Kaufman W.K. Song (2000) ArticleTitleCalreticulin couples calcium release and calcium influx in integrin-mediated calcium signaling Mol. Biol. Cell 11 1433–1443 Occurrence Handle1:CAS:528:DC%2BD3cXlt1Wks7w%3D Occurrence Handle10749940

    CAS  PubMed  Google Scholar 

  20. A. Saci F. Rendu C. Bachelot-Loza (2000) ArticleTitlePlatelet alpha IIb-beta 3 integrin engagement induces the tyrosine phosphorylation of Cbl and its association with phosphoinositide 3-kinase and Syk Biochem. J. 351 IssueIDPt 3 669–676 Occurrence Handle1:CAS:528:DC%2BD3cXotF2qsrk%3D Occurrence Handle11042121

    CAS  PubMed  Google Scholar 

  21. C.D. Nobes A. Hall (1995) ArticleTitleRho, rac, and cdc42 GTPases regulate the assembly of multimolecular focal complexes associated with actin stress fibers, lamellipodia, and filopodia Cell 81 53–62 Occurrence Handle10.1016/0092-8674(95)90370-4 Occurrence Handle1:CAS:528:DyaK2MXkvFOisrs%3D Occurrence Handle7536630

    Article  CAS  PubMed  Google Scholar 

  22. A.J. Ridley A. Hall (1992) ArticleTitleThe small GTP-binding protein rho regulates the assembly of focal adhesions and actin stress fibers in response to growth factors Cell 70 389–399 Occurrence Handle10.1016/0092-8674(92)90163-7 Occurrence Handle1:CAS:528:DyaK38XlsVyisro%3D Occurrence Handle1643657

    Article  CAS  PubMed  Google Scholar 

  23. A.J. Ridley H.F. Paterson C.L. Johnston D. Diekmann A. Hall (1992) ArticleTitleThe small GTP-binding protein rac regulates growth factor-induced membrane ruffling Cell 70 401–410 Occurrence Handle1:CAS:528:DyaK38XlsVyisrs%3D Occurrence Handle1643658

    CAS  PubMed  Google Scholar 

  24. M. Mazzucato P. Pradella M.R. Cozzi L. Marco ParticleDe Z.M. Ruggeri (2002) ArticleTitleSequential cytoplasmic calcium signals in a 2-stage platelet activation process induced by the glycoprotein Ibalpha mechanoreceptor Blood 100 2793–2800 Occurrence Handle1:CAS:528:DC%2BD38XotVGhsbg%3D Occurrence Handle12351387

    CAS  PubMed  Google Scholar 

  25. W.S. Nesbitt S. Kulkarni S. Giuliano I. Goncalves S.M. Dopheide C.L. Yap I.S. Harper H.H. Salem S.P. Jackson (2002) ArticleTitleDistinct glycoprotein Ib/V/IX and integrin alpha IIbbeta 3-dependent calcium signals cooperatively regulate platelet adhesion under flow J. Biol. Chem. 277 2965–2972 Occurrence Handle1:CAS:528:DC%2BD38XhtVSgtLk%3D Occurrence Handle11713259

    CAS  PubMed  Google Scholar 

  26. J.W. Heemskerk P. Vis M.A. Feijge J. Hoyland W.T. Mason S.O. Sage (1993) ArticleTitleRoles of phospholipase C and Ca(2+)-ATPase in calcium responses of single, fibrinogen-bound platelets J. Biol. Chem. 268 356–363 Occurrence Handle1:CAS:528:DyaK3sXjs1Gnuw%3D%3D Occurrence Handle8416943

    CAS  PubMed  Google Scholar 

  27. J.F. Hussain M.P. Mahaut-Smith (1999) ArticleTitleReversible and irreversible intracellular Ca2+ spiking in single isolated human platelets J. Physiol. 514 IssueIDPt 3 713–718 Occurrence Handle1:CAS:528:DyaK1MXhsl2luro%3D Occurrence Handle9882743

    CAS  PubMed  Google Scholar 

  28. M.E. Gracheva J.D. Gunton (2003) ArticleTitleIntercellular communication via intracellular calcium oscillations J. Theor. Biol. 221 513–518 Occurrence Handle1:CAS:528:DC%2BD3sXjtVKitrY%3D Occurrence Handle12713937

    CAS  PubMed  Google Scholar 

  29. M.J. Berridge M.D. Bootman P. Lipp (1998) ArticleTitleCalcium – a life and death signal Nature 395 645–648

    Google Scholar 

  30. M.J. Berridge P. Lipp M.D. Bootman (2000) ArticleTitleThe versatility and universality of calcium signalling Nat. Rev. Mol. Cell. Biol. 1 11–21 Occurrence Handle1:CAS:528:DC%2BD3MXivVGjtLs%3D Occurrence Handle11413485

    CAS  PubMed  Google Scholar 

  31. T.W. Chow J.D. Hellums J.L. Moake M.H. Kroll (1992) ArticleTitleShear stress-induced von Willebrand factor binding to platelet glycoprotein Ib initiates calcium influx associated with aggregation Blood 80 113–120 Occurrence Handle1:CAS:528:DyaK38XltVyrsrg%3D Occurrence Handle1611079

    CAS  PubMed  Google Scholar 

  32. C.L. Yap K.E. Anderson S.C. Hughan S.M. Dopheide H.H. Salem S.P. Jackson (2002) ArticleTitleEssential role for phosphoinositide 3-kinase in shear-dependent signaling between platelet glycoprotein Ib/V/IX and integrin alpha(IIb) beta(3) Blood 99 151–158 Occurrence Handle1:CAS:528:DC%2BD38XivF2itQ%3D%3D Occurrence Handle11756165

    CAS  PubMed  Google Scholar 

  33. H.H. Chang S.T. Hu T.F. Huang S.H. Chen Y.H. Lee S.J. Lo (1993) ArticleTitleRhodostomin, an RGD-containing peptide expressed from a synthetic gene in Escherichia coli , facilitates the attachment of human hepatoma cells Biochem. Biophys. Res. Commun. 190 242–249 Occurrence Handle1:CAS:528:DyaK3sXitlagsr8%3D Occurrence Handle7916592

    CAS  PubMed  Google Scholar 

  34. H.H. Chang H.F. Shyu Y.M. Wang D.S. Sun R.H. Shyu S.S. Tang Y.S. Huang (2002) ArticleTitleFacilitation of cell adhesion by immobilized dengue viral nonstructural protein 1 (NS1): arginine–glycine–aspartic acid structural mimicry within the dengue viral NS1 antigen J. Infect. Dis. 186 743–751 Occurrence Handle1:CAS:528:DC%2BD38XnvVSlsLk%3D Occurrence Handle12198607

    CAS  PubMed  Google Scholar 

  35. H.H. Chang W.J. Tsai S.J. Lo (1997) ArticleTitleGlutathione S-transferase–rhodostomin fusion protein inhibits platelet aggregation and induces platelet shape change Toxicon 35 195–204 Occurrence Handle1:CAS:528:DyaK2sXhsl2nu78%3D Occurrence Handle9080576

    CAS  PubMed  Google Scholar 

  36. C. Heilmann S. Niemann B. Sinha M. Herrmann B.E. Kehrel G. Peters (2004) ArticleTitleStaphylococcus aureus fibronectin-binding protein (FnBP)-mediated adherence to platelets, and aggregation of platelets induced by FnBPA but not by FnBPB J. Infect. Dis. 190 321–329 Occurrence Handle1:CAS:528:DC%2BD2cXmsFaqtLk%3D Occurrence Handle15216468

    CAS  PubMed  Google Scholar 

  37. G. Hsiao M.Y. Shen D.S. Chou C.H. Lin T.F. Chen J.R. Sheu (2004) ArticleTitleInvolvement of the antiplatelet activity of magnesium sulfate in suppression of protein kinase C and the Na+/H+ exchanger J. Biomed. Sci. 11 19–26 Occurrence Handle1:CAS:528:DC%2BD2cXkt12gsw%3D%3D Occurrence Handle14730206

    CAS  PubMed  Google Scholar 

  38. G. Hsiao M.Y. Shen C.L. Fang D.S. Chou C.H. Lin T.F. Chen J.R. Sheu (2003) ArticleTitleMorphine-potentiated platelet aggregation in in vitro and platelet plug formation in in␣vitro experiments J. Biomed. Sci. 10 292–301 Occurrence Handle1:CAS:528:DC%2BD3sXksFyju7o%3D Occurrence Handle12711856

    CAS  PubMed  Google Scholar 

  39. A.Y. Chang J.Y. Chan S.H. Chan (2003) ArticleTitleDifferential distribution of nitric oxide synthase isoforms in the rostral ventrolateral medulla of the rat J. Biomed. Sci. 10 285–291 Occurrence Handle1:CAS:528:DC%2BD3sXksFyju70%3D Occurrence Handle12711855

    CAS  PubMed  Google Scholar 

  40. S.S. Fan M.S. Chen J.F. Lin W.T. Chao V.C. Yang (2003) ArticleTitleUse of gain-of-function study to delineate the roles of crumbs in Drosophila eye development J. Biomed. Sci. 10 766–773 Occurrence Handle14631116

    PubMed  Google Scholar 

  41. N.K. Mak T.W. Kok R.N. Wong S.W. Lam Y.K. Lau W.N. Leung N.H. Cheung D.P. Huang L.L. Yeung C.K. Chang (2003) ArticleTitlePhotodynamic activities of sulfonamide derivatives of porphycene on nasopharyngeal carcinoma cells J. Biomed. Sci. 10 418–429 Occurrence Handle1:CAS:528:DC%2BD3sXkvVegs7o%3D Occurrence Handle12824701

    CAS  PubMed  Google Scholar 

  42. M. Gorka M.M. Godlewski B. Gajkowska U. Wojewodzka T. Motyl (2004) ArticleTitleKinetics of Smac/DIABLO release from mitochondria during apoptosis of MCF-7 breast cancer cells Cell. Biol. Int. 28 741–754 Occurrence Handle1:CAS:528:DC%2BD2cXhtVWit7nK Occurrence Handle15563396

    CAS  PubMed  Google Scholar 

  43. K.G. Lee T. Miller I. Anastassov W.D. Cohen (2004) ArticleTitleShape transformation and cytoskeletal reorganization in activated non-mammalian thrombocytes Cell Biol. Int. 28 299–310 Occurrence Handle1:CAS:528:DC%2BD2cXjsVWlu7c%3D Occurrence Handle15109987

    CAS  PubMed  Google Scholar 

  44. L.M. Mascari J.M. Ross (2003) ArticleTitleQuantification of staphylococcal-collagen binding interactions in whole blood by use of a confocal microscopy shear-adhesion assay J. Infect. Dis. 188 98–107 Occurrence Handle12825177

    PubMed  Google Scholar 

  45. A. Oertel A. Holzinger U. Lutz-Meindl (2003) ArticleTitleInvolvement of myosin in intracellular motility and cytomorphogenesis in Micrasterias Cell Biol. Int. 27 977–986 Occurrence Handle1:CAS:528:DC%2BD3sXptF2rtrY%3D Occurrence Handle14642529

    CAS  PubMed  Google Scholar 

  46. K.E. Yates-Siilata T.E. Dahms R.O. Webster R.M. Heuertz (2004) ArticleTitleC-reactive protein increases F-actin assembly and cortical distribution with resultant loss of lamellipod formation in human neutrophils Cell Biol. Int. 28 33–39 Occurrence Handle1:CAS:528:DC%2BD2cXps1Oksw%3D%3D Occurrence Handle14759766

    CAS  PubMed  Google Scholar 

  47. D.S. Sun H.H. Chang (2003) ArticleTitleDifferential regulation of JNK in caspase-3-mediated apoptosis of MPP(+)-treated primary cortical neurons Cell Biol. Int. 27 769–777 Occurrence Handle1:CAS:528:DC%2BD3sXntVGmtb8%3D Occurrence Handle12972283

    CAS  PubMed  Google Scholar 

  48. Y.L. Tseng H.C. Peng T.F. Huang (2004) ArticleTitleRhodostomin, a disintegrin, inhibits adhesion of neutrophils to fibrinogen and attenuates superoxide production J. Biomed. Sci. 11 683–691 Occurrence Handle1:CAS:528:DC%2BD2cXmslCgsLk%3D Occurrence Handle15316144

    CAS  PubMed  Google Scholar 

  49. Y.S. Kao J.C. Fong (2004) ArticleTitleThapsigargin and EGTA inhibit endothelin-1-induced glucose transport J. Biomed. Sci. 11 206–213 Occurrence Handle1:CAS:528:DC%2BD2cXht1Cnu7w%3D Occurrence Handle14966371

    CAS  PubMed  Google Scholar 

  50. R.C. Carroll R.G. Butler P.A. Morris J.M. Gerrard (1982) ArticleTitleSeparable assembly of platelet pseudopodal and contractile cytoskeletons Cell 30 385–393 Occurrence Handle1:CAS:528:DyaL38Xls1Sgsbg%3D Occurrence Handle6890413

    CAS  PubMed  Google Scholar 

  51. D. Dash M. Aepfelbacher W. Siess (1995) ArticleTitleIntegrin alpha IIb beta 3-mediated translocation of CDC42Hs to the cytoskeleton in stimulated human platelets J. Biol. Chem. 270 17321–17326 Occurrence Handle1:CAS:528:DyaK2MXntVOrt7w%3D Occurrence Handle7542236

    CAS  PubMed  Google Scholar 

  52. A.N. Carter R. Huang A. Sorisky C.P. Downes S.E. Rittenhouse (1994) ArticleTitlePhosphatidylinositol 3,4,5-trisphosphate is formed from phosphatidylinositol 4,5-bisphosphate in thrombin-stimulated platelets Biochem. J. 301 IssueIDPt 2 415–420 Occurrence Handle1:CAS:528:DyaK2cXksl2hsbY%3D Occurrence Handle8042983

    CAS  PubMed  Google Scholar 

  53. S. Boitano E.R. Dirksen M.J. Sanderson (1992) ArticleTitleIntercellular propagation of calcium waves mediated by inositol trisphosphate Science 258 292–295 Occurrence Handle1:CAS:528:DyaK38XmsV2itr0%3D Occurrence Handle1411526

    CAS  PubMed  Google Scholar 

  54. G.W. Hennig C.B. Smith D.M. O’Shea T.K. Smith (2002) ArticleTitlePatterns of intracellular and intercellular Ca2+ waves in the␣longitudinal muscle layer of the murine large intestine in vitro J. Physiol. 543 233–253 Occurrence Handle1:CAS:528:DC%2BD38XmvFOnurc%3D Occurrence Handle12181295

    CAS  PubMed  Google Scholar 

  55. R. Levi M. Samoilova A.I. Selverston (2003) ArticleTitleCalcium signaling components of oscillating invertebrate neurons in vitro Neuroscience 118 283–296 Occurrence Handle1:CAS:528:DC%2BD3sXisFSgsb8%3D Occurrence Handle12676158

    CAS  PubMed  Google Scholar 

  56. T.E. Danciu R.M. Adam K. Naruse M.R. Freeman P.V. Hauschka (2003) ArticleTitleCalcium regulates the PI3K-Akt pathway in stretched osteoblasts FEBS Lett. 536 193–197 Occurrence Handle1:CAS:528:DC%2BD3sXhtVGgsLk%3D Occurrence Handle12586362

    CAS  PubMed  Google Scholar 

  57. J.C. Yarrow T. Lechler R. Li T.J. Mitchison (2003) ArticleTitleRapid de-localization of actin leading edge components with BDM treatment BMC Cell Biol. 4 5 Occurrence Handle12783627

    PubMed  Google Scholar 

  58. M. Kuwahara M. Sugimoto S. Tsuji S. Miyata A. Yoshioka (1999) ArticleTitleCytosolic calcium changes in a process of platelet adhesion and cohesion on a von Willebrand factor-coated surface under flow conditions Blood 94 1149–1155 Occurrence Handle1:CAS:528:DyaK1MXlt1Olurw%3D Occurrence Handle10438701

    CAS  PubMed  Google Scholar 

  59. K. Kuwahara T. Kawai S. Mitsuyoshi Y. Matsuo H. Kikuchi S. Imajoh-Ohmi E. Hashimoto S. Inui M.D. Cooper N. Sakaguchi (1996) ArticleTitleCross-linking of B cell antigen receptor-related structure of pre-B cell lines induces tyrosine phosphorylation of p85 and p110 subunits and activation of phosphatidylinositol 3-kinase Int. Immunol. 8 1273–1285 Occurrence Handle1:CAS:528:DyaK28XltlKjtb0%3D Occurrence Handle8918697

    CAS  PubMed  Google Scholar 

  60. I. Goncalves S.C. Hughan S.M. Schoenwaelder C.L. Yap Y. Yuan S.P. Jackson (2003) ArticleTitleIntegrin alpha IIb beta 3-dependent calcium signals regulate platelet–fibrinogen interactions under flow. Involvement of phospholipase C gamma 2 J. Biol. Chem. 278 34812–34822 Occurrence Handle1:CAS:528:DC%2BD3sXntVWqsLg%3D Occurrence Handle12832405

    CAS  PubMed  Google Scholar 

  61. J.W. Heemskerk J. Hoyland W.T. Mason S.O. Sage (1992) ArticleTitleSpiking in cytosolic calcium concentration in single fibrinogen-bound fura-2-loaded human platelets Biochem. J. 283 IssueIDPt 2 379–383 Occurrence Handle1:CAS:528:DyaK38XitFWkt7s%3D Occurrence Handle1575681

    CAS  PubMed  Google Scholar 

  62. J.M. Pasquet L. Quek C. Stevens R. Bobe M. Huber V. Duronio G. Krystal S.P. Watson (2000) ArticleTitlePhosphatidylinositol 3,4,5-trisphosphate regulates Ca(2+) entry via btk in platelets and megakaryocytes without increasing phospholipase C activity EMBO J. 19 2793–2802 Occurrence Handle1:CAS:528:DC%2BD3cXmtFCru7g%3D Occurrence Handle10856225

    CAS  PubMed  Google Scholar 

  63. Y.S. Bae L.G. Cantley C.S. Chen S.R. Kim K.S. Kwon S.G. Rhee (1998) ArticleTitleActivation of phospholipase C-gamma by phosphatidylinositol 3,4,5-trisphosphate J. Biol. Chem. 273 4465–4469 Occurrence Handle1:CAS:528:DyaK1cXhtlSrtbg%3D Occurrence Handle9468499

    CAS  PubMed  Google Scholar 

  64. M. Falasca S.K. Logan V.P. Lehto G. Baccante M.A. Lemmon J. Schlessinger (1998) ArticleTitleActivation of phospholipase C gamma by PI 3-kinase-induced PH domain-mediated membrane targeting EMBO J. 17 414–422 Occurrence Handle1:CAS:528:DyaK1cXosFGksA%3D%3D Occurrence Handle9430633

    CAS  PubMed  Google Scholar 

  65. K.L. Hippen A.M. Buhl D. D’Ambrosio K. Nakamura C. Persin J.C. Cambier (1997) ArticleTitleFc gammaRIIB1 inhibition of BCR-mediated phosphoinositide hydrolysis and Ca2+ mobilization is integrated by CD19 dephosphorylation Immunity 7 49–58 Occurrence Handle1:CAS:528:DyaK2sXltFWht78%3D Occurrence Handle9252119

    CAS  PubMed  Google Scholar 

  66. M.D. Bootman M.J. Berridge (1995) ArticleTitleThe elemental principles of calcium signaling Cell 83 675–678 Occurrence Handle1:CAS:528:DyaK2MXpvVeht7s%3D Occurrence Handle8521483

    CAS  PubMed  Google Scholar 

  67. M.D. Bootman T.J. Collins C.M. Peppiatt L.S. Prothero L. MacKenzie P. De Smet M. Travers S.C. Tovey J.T. Seo M.J. Berridge F. Ciccolini P. Lipp (2001) ArticleTitleCalcium signalling – an overview Semin. Cell. Dev. Biol. 12 3–10 Occurrence Handle1:CAS:528:DC%2BD3MXlsFWmtA%3D%3D Occurrence Handle11162741

    CAS  PubMed  Google Scholar 

  68. G. Hajnoczky L.D. Robb-Gaspers M.B. Seitz A.P. Thomas (1995) ArticleTitleDecoding of cytosolic calcium oscillations in the mitochondria Cell 82 415–424 Occurrence Handle1:STN:280:ByqA28%2FpvVE%3D Occurrence Handle7634331

    CAS  PubMed  Google Scholar 

  69. S. Kulkarni S.M. Dopheide C.L. Yap C. Ravanat M. Freund P. Mangin K.A. Heel A. Street I.S. Harper F. Lanza S.P. Jackson (2000) ArticleTitleA revised model of platelet aggregation J. Clin. Invest. 105 783–791 Occurrence Handle1:CAS:528:DC%2BD3cXhvFehsbo%3D Occurrence Handle10727447

    CAS  PubMed  Google Scholar 

  70. V. Fuster L. Badimon J.J. Badimon J.H. Chesebro (1992) ArticleTitleThe pathogenesis of coronary artery disease and the acute coronary syndromes (1) New Engl. J. Med. 326 242–250 Occurrence Handle1:STN:280:By2D1MzgtlA%3D Occurrence Handle1727977

    CAS  PubMed  Google Scholar 

  71. V. Fuster L. Badimon J.J. Badimon J.H. Chesebro (1992) ArticleTitleThe pathogenesis of coronary artery disease and the acute coronary syndromes (2) New Engl. J. Med. 326 310–318 Occurrence Handle1:STN:280:By2C3c%2FhsVE%3D Occurrence Handle1728735

    CAS  PubMed  Google Scholar 

  72. K. Vanschoonbeek M.A. Feijge J.F. Keuren H. Coenraad Hemker J.J. Lodder K. Hamulyak E.C. Pampus Particlevan J.W. Heemskerk (2002) ArticleTitleThrombin-induced hyperactivity of platelets of young stroke patients: involvement of thrombin receptors in the subject-dependent variability in Ca2+ signal generation Thromb. Haemost. 88 931–937 Occurrence Handle1:CAS:528:DC%2BD3sXisVWgsw%3D%3D Occurrence Handle12529741

    CAS  PubMed  Google Scholar 

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Authors and Affiliations

  1. Institute of Molecular and Cellular Biology, Taiwan

    Der-Shan Sun, Mei-Shiuan Yu, Ching-Yi Huang & Hsin-Hou Chang

  2. Institute of Human Genetics, Taiwan

    Der-Shan Sun, Yao-Fong Chen & Hsin-Hou Chang

  3. Department of Microbiology & Immunology, Taiwan

    Mei-Shiuan Yu

  4. Institute of Anthropology, Tzu-Chi University, Hualien, Taiwan

    Yao-Fong Chen

  5. Department of Life Science, Chang Gung University, Tao-Yuan, Taiwan

    Szecheng J. Lo

  6. Institute of Microbiology and Immunology, National Yang-Ming University, Taipei, Taiwan, ROC

    Szecheng J. Lo & Chi-Hung Lin

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  1. Der-Shan Sun
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  2. Szecheng J. Lo
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  3. Chi-Hung Lin
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  4. Mei-Shiuan Yu
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  6. Yao-Fong Chen
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  7. Hsin-Hou Chang
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Correspondence to Hsin-Hou Chang.

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Sun, DS., Lo, S.J., Lin, CH. et al. Calcium oscillation and phosphatidylinositol 3-kinase positively regulate integrin αIIbβ3-mediated outside-in signaling. J Biomed Sci 12, 321–333 (2005). https://doi.org/10.1007/s11373-005-0979-6

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  • DOI: https://doi.org/10.1007/s11373-005-0979-6

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