Integrin-dependent interaction of lipid rafts with the actin cytoskeleton in activated human platelets

Journal of Cell Science

Volumn 118, Issue 4, 2005, Pages 759-769

  Bodin, Stéphane ^a   Soulet, Carine ^a   Tronchère, Hélène ^a   Sié, Pierre ^b   Gachet, Christian ^a   Plantavid, Monique ^a   Payrastre, Bernard ^a  

^a INSERM   (France)

^b CHU PURPAN   (France)

Author keywords

Actin; Cytoskeleton; Integrins; Lipid rafts; Phosphoinositides; Platelets

Indexed keywords

ACTIN; ALPHA2 INTEGRIN; BETA3 INTEGRIN; FIBRINOGEN RECEPTOR ANTAGONIST; INTEGRIN; THROMBIN;

ACTIN FILAMENT; ARTICLE; BLOOD CLOT RETRACTION; CELL MEMBRANE; CELL ULTRASTRUCTURE; CONTROLLED STUDY; CORRELATION FUNCTION; CYTOSKELETON; GLANZMANN DISEASE; HUMAN; HUMAN CELL; LIPID RAFT; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN BINDING; PROTEIN FUNCTION; PROTEIN LIPID INTERACTION; THROMBOCYTE ACTIVATION; THROMBOCYTE AGGREGATION; THROMBOCYTE FUNCTION; UPREGULATION;

BLOOD PLATELETS; CLOT RETRACTION; HUMANS; MEMBRANE MICRODOMAINS; MICROFILAMENT PROTEINS; MICROFILAMENTS; PHOSPHATIDYLINOSITOL 4,5-DIPHOSPHATE; PLATELET ACTIVATION; PLATELET GLYCOPROTEIN GPIIB-IIIA COMPLEX;

EID: 14944344230     PISSN: 00219533     EISSN: None     Source Type: Journal    
DOI: 10.1242/jcs.01648     Document Type: Article

References (57)

1. Azim, A. C., Barkalow, K., Chou, J. and Hartwig, J. H. (2000). Activation of the small GTPases, rac and cdc42, after ligation of the platelet PAR-1 receptor. Blood 95, 959-964.
2. Baglia, F. A., Shrimpton, C. N., Lopez, J. A. and Walsh, P. N. (2003). The glycoprotein Ib-IX-V complex mediates localization of factor XI to lipid rafts on the platelet membrane. J. Biol. Chem. 278, 21744-21750.
3. Barret, C., Roy, C., Montcourrier, P., Mangeat, P. and Niggli, V. (2000). Mutagenesis of the phosphatidylinositol 4,5-bisphosphate (PIP(2)) binding site in the NH(2)-terminal domain of ezrin correlates with its altered cellular distribution. J. Cell Biol. 151, 1067-1080.
4. Berditchevski, F. (2001). Complexes of tetraspanins with integrins: more than meets the eye. J. Cell Sci. 114, 4143-4151.
5. Bligh, E. G. and Dyer, W. J. (1959). A rapid method of total lipid extraction and purification. Can. J. Biochem. Phys. 37, 911-917.
6. Bodin, S., Giuriato, S., Ragab, J., Humbel, B. M., Viala, C., Vieu, C., Chap, H. and Payrastre, B. (2001). Production of phosphatidylinositol 3,4,5-trisphosphate and phosphatidic acid in platelet rafts: evidence for a critical role of cholesterol-enriched domains in human platelet activation. Biochemistry 40, 15290-15299.
7. Bodin, S., Tronchere, H. and Payrastre, B. (2003a). Lipid rafts are critical membrane domains in blood platelet activation processes. Biochim. Biophys. Acta 1610, 247-257.
8. Bodin, S., Viala, C., Ragab, A. and Payrastre, B. (2003b). A critical role of lipid rafts in the organization of a key FcgammaRIIa-mediated signaling pathway in human platelets. Thromb. Haemost. 89, 318-330.
9. Brdickova, N., Brdicka, T., Andera, L., Spicka, J., Angelisova, P., Milgram, S. L. and Horejsi, V. (2001). Interaction between two adapter proteins, PAG and EBP50: a possible link between membrane rafts and actin cytoskeleton. FEBS Lett. 507, 133-136.
10. Brown, D. A. and London, E. (2000). Structure and function of sphingolipid-and cholesterol-rich membrane rafts. J. Biol. Chem. 275, 17221-17224.
11. Brown, D. A. and Rose, J. K. (1992). Sorting of GPI-anchored proteins to glycolipid-enriched membrane subdomains during transport to the apical cell surface. Cell 68, 533-544.
12. Chatah, N. E. and Abrams, C. S. (2001). G-protein-coupled receptor activation induces the membrane translocation and activation of phosphatidylinositol-4-phosphate 5-kinase I alpha by a Rac- and Rho-dependent pathway. J. Biol. Chem. 276, 34059-34065.
13. del Pozo, M. A., Alderson, N. B., Kiosses, W. B., Chiang, H. H., Anderson, R. G. and Schwartz, M. A. (2004). Integrins regulate Rac targeting by internalization of membrane domains. Science 303, 839-842.
14. Dorahy, D. J., Berndt, M. C., Shafren, D. R. and Burns, G. F. (1996). CD36 is spatially associated with glycoprotein IIb-IIIa (alpha IIb beta 3) on the surface of resting platelets. Biochem. Biophys. Res. Commun. 218, 575-581.
15. Drevot, P., Langlet, C., Guo, X. J., Bernard, A. M., Colard, O., Chauvin, J. P., Lasserre, R. and He, H. T. (2002). TCR signal initiation machinery is pre-assembled and activated in a subset of membrane rafts. EMBO J. 21, 1899-1908.
16. Elzagallaai, A., Rose, S. D. and Trifaro, J. M. (2000). Platelet secretion induced by phorbol esters stimulation is mediated through phosphorylation of MARCKS: a MARCKS-derived peptide blocks MARCKS phosphorylation and serotonin release without affecting pleckstrin phosphorylation. Blood 95, 894-902.
17. Engqvist-Goldstein, A. E. and Drubin, D. G. (2003). Actin assembly and endocytosis: from yeast to mammals. Annu. Rev. Cell Dev. Biol. 19, 287-332.
18. Fais, S. and Malorni, W. (2003). Leukocyte uropod formation and membrane/cytoskeleton linkage in immune interactions. J. Leukoc. Biol. 73, 556-563.
19. Foger, N., Marhaba, R. and Zoller, M. (2001). Involvement of CD44 in cytoskeleton rearrangement and raft reorganization in T cells. J. Cell Sci. 114, 1169-1178.
20. Fox, J. E. (1993). The platelet cytoskeleton. Thromb. Haemost. 70, 884-893.
21. Gamulescu, M. A., Seifert, K., Tingart, M., Falet, H. and Hoffmeister, K. M. (2003). Platelet moesin interacts with PECAM-1 (CD31). Platelets 14, 211-217.
22. Gratacap, M. P., Payrastre, B., Viala, C., Mauco, G., Plantavid, M. and Chap, H. (1998). Phosphatidylinositol 3,4,5-trisphosphate-dependent stimulation of phospholipase C-gamma2 is an early key event in FcgammaRIIA-mediated activation of human platelets. J. Biol. Chem. 273, 24314-24321.
23. Harder, T. and Simons, K. (1999). Clusters of glycolipid and glycosylphosphatidylinositol-anchored proteins in lymphoid cells: accumulation of actin regulated by local tyrosine phosphorylation. Eur. J. Immunol. 29, 556-562.
24. Hartwig, J. H., Barkalow, K., Azim, A. and Italiano, J. (1999). The elegant platelet: signals controlling actin assembly. Thromb. Haemost. 82, 392-398.
25. Heijnen, H. F., van Lier, M., Waaijenborg, S., Ohno-Iwashita, Y., Waheed, A. A., Inomata, M., Gorter, G., Mobius, W., Akkerman, J. W. and Slot, J. W. (2003). Concentration of rafts in platelet filopodia correlates with recruitment of c-Src and CD63 to these domains. J Thromb. Haemost. 1, 1161-1173.
26. Higgs, H. N. and Pollard, T. D. (2001). Regulation of actin filament network formation through ARP2/3 complex: activation by a diverse array of proteins. Annu. Rev. Biochem. 70, 649-676.
27. Hinchliffe, K. A., Irvine, R. F. and Divecha, N. (1996). Aggregation-dependent, integrin-mediated increases in cytoskeletally associated PtdInsP2 (4,5) levels in human platelets are controlled by translocation of PtdIns 4-P 5-kinase C to the cytoskeleton. EMBO J. 15, 6516-6524.
28. Kovacsovics, T. J., Bachelot, C., Toker, A., Vlahos, C. J., Duckworth, B., Cantley, L. C. and Hartwig, J. H. (1995). Phosphoinositide 3-kinase inhibition spares actin assembly in activating platelets but reverses platelet aggregation. J. Biol. Chem. 270 11358-11366.
29. Laux, T., Fukami, K., Thelen, M., Golub, T., Frey, D. and Caroni, P. (2000). GAP43, MARCKS, and CAP23 modulate PI(4,5)P(2) at plasmalemmal rafts, and regulate cell cortex actin dynamics through a common mechanism. J. Cell Biol. 149, 1455-1472.
30. Litjens, P. E., Kroner, C. I., Akkerman, J. W. and van Willigen, G. (2003). Cytoplasmic regions of the beta3 subunit of integrin alphaIIbbeta3 involved in platelet adhesion on fibrinogen under flow conditions. J. Thromb. Haemost. 1, 2014-2021.
31. Livne, A., Packham, M. A., Guccione, M. A. and Mustard, J. F. (1988). Aggregation-related association of lipid with the cytoskeleton of rabbit and human platelets prelabeled with [3H]palmitic acid. Similar effects of adenosine diphosphate- and thrombin-induced aggregation. J. Clin. Invest. 81, 288-299.
32. Mangeat, P., Roy, C. and Martin, M. (1999). ERM proteins in cell adhesion and membrane dynamics. Trends Cell Biol. 9, 187-192.
33. Meh, D. A., Siebenlist, K. R., Bergtrom, G. and Mosesson, M. W. (1995). Sequence of release of fibrinopeptide A from fibrinogen molecules by thrombin or Atroxin. J. Lab. Clin. Med. 125, 384-391.
34. Moran, M. and Miceli, M. C. (1998). Engagement of GPI-linked CD48 contributes to TCR signals and cytoskeletal reorganization: a role for lipid rafts in T cell activation. Immunity 9, 787-796.
35. Munro, S. (2003). Lipid rafts: elusive or illusive? Cell 115, 377-388.
36. Nair, S., Ghosh, K., Kulkarni, B., Shetty, S. and Mohanty, D. (2002). Glanzmann's thrombasthenia: updated. Platelets 13 387-393.
37. Payrastre, B., van Bergen en Henegouwen, P. M., Breton, M., den Hartigh, J. C., Plantavid, M., Verkleij, A. J. and Boonstra, J. (1991). Phosphoinositide kinase, diacylglycerol kinase, and phospholipase C activities associated to the cytoskeleton: effect of epidermal growth factor. J. Cell Biol. 115, 121-128.
38. Pike, L. J. and Casey, L. (1996). Localization and turnover of phosphatidylinositol 4,5-bisphosphate in caveolin-enriched membrane domains. J. Biol. Chem. 271, 26453-26456.
39. Pizzo, P., Giurisato, E., Tassi, M., Benedetti, A., Pozzan, T. and Viola, A. (2002). Lipid rafts and T cell receptor signaling: a critical re-evaluation. Eur. J. Immunol. 32, 3082-3091.
40. Ragab, A., Bodin, S., Viala, C., Chap, H., Payrastre, B. and Ragab-Thomas, J. (2003). The tyrosine phosphatase 1B regulates linker for activation of T-cell phosphorylation and platelet aggregation upon FcgammaRIIa cross-linking. J. Biol. Chem. 278, 40923-40932.
41. Raucher, D., Stauffer, T., Chen, W., Shen, K., Guo, S., York, J. D., Sheetz, M. P. and Meyer, T. (2000). Phosphatidylinositol 4,5-bisphosphate functions as a second messenger that regulates cytoskeleton-plasma membrane adhesion. Cell 100, 221-228.
42. Rozelle, A. L., Machesky, L. M., Yamamoto, M., Driessens, M. H., Insall, R. H., Roth, M. G., Luby-Phelps, K., Marriott, G., Hall, A. and Yin, H. L. (2000). Phosphatidylinositol 4,5-bisphosphate induces actin-based movement of raft-enriched vesicles through WASP-Arp2/3. Curr. Biol. 10, 311-320.
43. Savi, P., Zamboni, G., Rescanieres, O. and Herbert, J. M. (2001). Studies on the binding of 3H-SR121566, an inhibitor of Gp IIb-IIIa activation. Thromb. Haemost. 85, 702-709.
44. Schick, P. K., Tuszynski, G. P. and Vander Voort, P. W. (1983). Human platelet cytoskeletons: specific content of glycolipids and phospholipids. Blood 61, 163-166.
45. Schoenwaelder, S. M., Yuan, Y., Cooray, P., Salem, H. H. and Jackson, S. P. (1997). Calpain cleavage of focal adhesion proteins regulates the cytoskeletal attachment of integrin alphaIIbbeta3 (platelet glycoprotein IIb/IIIa) and the cellular retraction of fibrin clots. J. Biol. Chem. 272, 1694-1702.
46. Sechi, A. S. and Wehland, J. (2000). The actin cytoskeleton and plasma membrane connection: PtdIns(4,5)P(2) influences cytoskeletal protein activity at the plasma membrane. J. Cell Sci. 113, 3685-3695.
47. Seveau, S., Eddy, R. J., Maxfield, F. R. and Pierini, L. M. (2001). Cytoskeleton-dependent membrane domain segregation during neutrophil polarization. Mol. Biol. Cell 12, 3550-3562.
48. Sharma, P., Varma, R., Sarasij, R. C., Ira, Gousset, K., Krishnamoorthy, G., Rao, M. and Mayor, S. (2004). Nanoscale organization of multiple GPI-anchored proteins in living cell membranes. Cell 116, 577-589.
49. Shcherbina, A., Kenney, D. M., Bretscher, A. and Remold, O. D. E. (1999). Dynamic association of moesin with the membrane skeleton of thrombin-activated platelets. Blood 93, 2128-2129.
50. Shrimpton, C. N., Borthakur, G., Larrucea, S., Cruz, M. A., Dong, J. F. and Lopez, J. A. (2002). Localization of the adhesion receptor glycoprotein Ib-IX-V complex to lipid rafts is required for platelet adhesion and activation. J. Exp. Med. 196, 1057-1066.
51. Simons, K. and Toomre, D. (2000). Lipid rafts and signal transduction. Nat. Rev. 1, 31-39.
52. Tolias, K. F., Hartwig, J. H., Ishihara, H., Shibasaki, Y., Cantley, L. C. and Carpenter, C. L. (2000). Type Ialpha phosphatidylinositol-4-phosphate 5-kinase mediates Rac-dependent actin assembly. Curr. Biol. 10, 153-156.
53. Trumel, C., Payrastre, B., Plantavid, M., Hechler, B., Viala, C., Presek, P., Martinson, E. A., Cazenave, J. P., Chap, H. and Gachet, C. (1999). A key role of adenosine diphosphate in the irreversible platelet aggregation induced by the PAR1-activating peptide through the late activation of phosphoinositide 3-kinase. Blood 94, 4156-4165.
54. Tuszynski, G. P., Mauco, G. P., Koshy, A., Schick, P. K. and Walsh, P. N. (1984). The platelet cytoskeleton contains elements of the prothrombinase complex. J. Biol. Chem. 259, 6947-6951.
55. Villalba, M., Bi, K., Rodriguez, F., Tanaka, Y., Schoenberger, S. and Altman, A. (2001). Vav1/Rac-dependent actin cytoskeleton reorganization is required for lipid raft clustering in T cells. J. Cell Biol. 155, 331-338.
56. Wonerow, P., Obergfell, A., Wilde, J. I., Bobe, R., Asazuma, N., Brdicka, T., Leo, A., Schraven, B., Horejsi, V., Shattil, S. J. et al. (2002). Differential role of glycolipid-enriched membrane domains in glycoprotein VI- and integrin-mediated phospholipase Cgamma2 regulation in platelets. Biochem. J. 364, 755-765.
57. Zucker, M. B. and Masiello, N. C. (1983). The Triton X-100-insoluble residue of aggregated platelets contains increased lipid phosphorus as well as 125I-labeled glycoproteins. Blood 61, 676-683.