Calpain-controlled detachment of major glycoproteins from the cytoskeleton regulates adhesive properties of activated phosphatidylserine-positive platelets

Biochemical Journal

Volumn 473, Issue 4, 2016, Pages 435-448

  Artemenko, Elena O ^a,b   Yakimenko, Alena O ^a,b   Pichugin, Alexey V ^c   Ataullakhanov, Fazly I ^a,b,d,e   Panteleev, Mikhail A ^a,b,d,e,f  

^a CENTER FOR THEORETICAL PROBLEMS OF PHYSICOCHEMICAL PHARMACOLOGY   (Russian Federation)

^b Moscow   (Russian Federation)

^c INSTITUTE OF IMMUNOLOGY   (Russian Federation)

^d MOSCOW STATE UNIVERSITY   (Russian Federation)

^e MOSCOW INSTITUTE OF PHYSICS AND TECHNOLOGY   (Russian Federation)

^f PIROGOV RUSSIAN NATIONAL RESEARCH MEDICAL UNIVERSITY   (Russian Federation)

Author keywords

Adhesion; Adhesive glycoproteins; Calpain; Cytoskeleton; Platelet; Shear

Indexed keywords

ALPHA2 INTEGRIN; CALPAIN; CALPASTATIN; FILAMIN; GLYCOPROTEIN; GLYCOPROTEIN IB; MEMBRANE PROTEIN; PADGEM PROTEIN; PHOSPHATIDYLSERINE; TALIN; CYTOSKELETON PROTEIN; PROTEIN BINDING;

ARTICLE; CYTOSKELETON; FLOW CYTOMETRY; PRIORITY JOURNAL; SHEAR RATE; THROMBOCYTE; CELL ADHESION; CYTOLOGY; HUMAN; METABOLISM; PHYSIOLOGY;

BLOOD PLATELETS; CALPAIN; CELL ADHESION; CYTOSKELETAL PROTEINS; GLYCOPROTEINS; HUMANS; PHOSPHATIDYLSERINES; PROTEIN BINDING;

EID: 84958559493     PISSN: 02646021     EISSN: 14708728     Source Type: Journal    
DOI: 10.1042/BJ20150779     Document Type: Article

References (57)

1. Fox, J.E.B. (1993) Regulation of platelet function by the cytoskeleton. In Mechanisms of Platelet Activation and Control (Authi, K.S., Watson, S.P. and Kakkar, VV, eds), pp. 175-185, Plenum Press, New York
2. Blockmans, D., Deckmyn, H. and Vermylen, J. (1995) Platelet activation. Blood Rev. 9, 143-156
3. Fox, J.E., Lipfert, L., Clark, E.A., Reynolds, C.C., Austin, C.D. and Brugge, J.S. (1993) On the role of the platelet membrane skeleton in mediating signal transduction. Association of GP IIb-IIIa, pp60c-src, pp62c-yes, and the p21ras GTPase-activating protein with the membrane skeleton. J. Biol. Chem. 268, 25973-25984
4. Nakamura, F., Pudas, R., Heikkinen, O., Permi, P., Kilpeläinen, I., Munday, A.D., Hartwig, J.H., Stossel, T.P. and Ylänne, J. (2006) The structure of the GPIb-filamin A complex. Blood 107, 1925-1932
5. Wehrle-Haller, B. (2012) Assembly and disassembly of cell matrix adhesions. Curr. Opin. Cell Biol. 24, 569-581
6. Savage, B., Saldívar, E. and Ruggeri, Z.M. (1996) Initiation of platelet adhesion by arrest onto fibrinogen or translocation on von Willebrand factor. Cell 84, 289-297
7. Massberg, S., Enders, G., Leiderer, R., Eisenmenger, S., Vestweber, D., Krombach, F. and Messmer, K. (1998) Platelet-endothelial cell interactions during ischemia/reperfusion: the role of P-selectin. Blood 92, 507-515
8. Miyamoto, S., Teramoto, H., Coso, O.A., Gutkind, J.S., Burbelo, P.D., Akiyama, S.K. and Yamada, K.M. (1995) Integrin function: molecular hierarchies of cytoskeletal and signaling molecules. J. Cell Biol. 131,791-805
9. Schwartz, M.A. (2010) Integrins and extracellular matrix in mechanotransduction. Cold Spring Harb. Perspect. Biol. 2, a005066
10. Williamson, D., Pikovski, I., Cranmer, S.L., Mangin, P., Mistry N., Domagala, T., Chehab, S., Lanza, F., Salem, H.H. and Jackson, S.P (2002) Interaction between platelet glycoprotein Ibalpha and filamin-1 is essential for glycoprotein Ib/IX receptor anchorage at high shear. J. Biol. Chem. 277, 2151-2159
11. Canobbio, I., Balduini, C. and Torti, M. (2004) Signalling through the platelet glycoprotein Ib-V-IX complex. Cell Signal. 16,1329-1344
12. Mangin, P., David, T., Lavaud, V., Cranmer, S.L., Pikovski, I., Jackson, S.P, Berndt, M.C., Cazenave, J.P., Gachet, C. and Lanza, F. (2004) Identification of a novel 14-3-3zeta binding site within the cytoplasmic tail of platelet glycoprotein Ibalpha. Blood 104, 420-427
13. Phillips, D.R., Jennings, L.K. and Edwards, H.H. (1980) Identification of membrane proteins mediating the interaction of human platelets. J. Cell Biol. 86, 77-86
14. Larsen, E., Celi, A., Gilbert, G.E., Furie, B.C., Erban, J.K., Bonfanti, R., Wagner, D.D. and Furie, B. (1989) PADGEM protein: a receptor that mediates the interaction of activated platelets with neutrophils and monocytes. Cell 59, 305-312
15. Geng, J.G., Bevilacqua, M.P, Moore, K.L., McIntyre, T.M., Prescott, S.M., Kim, J.M., Bliss, G.A., Zimmerman, G.A. and McEver, R.P (1990) Rapid neutrophil adhesion to activated endothelium mediated by GMP-140. Nature 343, 757-760
16. Maruthamuthu, V., Aratyn-Schaus, Y and Gardel, M.L. (2010) Conserved F-actin dynamics and force transmission at cell adhesions. Curr. Opin. Cell Biol. 22, 583-588
17. Hartwig, J.H., Barkalow, K., Azim, A. and Italiano, J. (1999) The elegant platelet: signals controlling actin assembly. Thromb. Haemost. 82, 392-398
18. Heemskerk, J.W., Vuist, W.M., Feijge, M.A., Reutelingsperger, C.P and Lindhout, T. (1997) Collagen but not fibrinogen surfaces induce bleb formation, exposure of phosphatidylserine, and procoagulant activity of adherent platelets: evidence for regulation by protein tyrosine kinase-dependent Ca#sup#2+#/sup# responses. Blood 90, 2615-2625
19. Yakimenko, A.O., Verholomova, FY, Kotova, Y.N., Ataullakhanov, F.I. and Panteleev, M.A. (2012) Identification of different proaggregatory abilities of activated platelet subpopulations. Biophys. J. 102, 2261-2269
20. Verhallen, PF, Bevers, E.M., Comfurius, P. and Zwaal, R.F. (1988) Fluoride-dependent calcium-induced platelet procoagulant activity shows that calpain is involved in increased phospholipid transbilayer movement. Biochim. Biophys. Acta 942,150-158
21. Khorchid, A. and Ikura, M. (2002) How calpain is activated by calcium. Nat. Struct. Biol. 9,239-241
22. Topalov, N.N., Kotova, Y.N., Vasil'ev, S.A. and Panteleev, M.A. (2012) Identification of signal transduction pathways involved in the formation of platelet subpopulations upon activation. Br. J. Haematol. 157,105-115
23. Hartwig, J.H. and DeSisto, M. (1991) The cytoskeleton of the resting human blood platelet: structure of the membrane skeleton and its attachment to actin filaments. J. Cell Biol. 112, 407-425
24. Goldenthal, K.L., Hedman, K., Chen, J.W., August, J.T. and Willingham, M.C. (1985) Postfixation detergent treatment for immunofluorescence suppresses localization of some integral membrane proteins. J. Histochem. Cytochem. 33, 813-820
25. Ramjee, M.K. (2000) The use of fluorogenic substrates to monitor thrombin generation for the analysis of plasma and whole blood coagulation. Anal. Biochem. 277,11-18
26. Panteleev, M.A., Ananyeva, N.M., Greco, N.J., Ataullakhanov, F.I. and Saenko, E.L. (2005) Two subpopulations of thrombin-activated platelets differ in their binding of the components of the intrinsic factor X-activating complex. J. Thromb. Haemost. 3, 2545-2553
27. Kotova, Y.N., Ataullakhanov, F.I. and Panteleev, M.A. (2008) Formation of coated platelets is regulated by the dense granule secretion of adenosine 5'-diphosphate acting via the P2Y12 receptor. J. Thromb. Haemost. 6,1603-1605
28. Laemmli, U.K. (1970) Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature 227, 680-685
29. Dale, G.L, Friese, P., Batar, P., Hamilton, S.F, Reed, G.L., Jackson, K.W., Clemetson, K.J. and Alberio, L. (2002) Stimulated platelets use serotonin to enhance their retention of procoagulant proteins on the cell surface. Nature 415,175-179
30. Shevchenko, A., Tomas, H., Havlis, J., Olsen, J.V. and Mann, M. (2006) In-gel digestion for mass spectrometric characterization of proteins and proteomes. Nat. Protoc. 1, 2856-2860
31. Comfurius, P., Bevers, E.M. and Zwaal, R.F. (1985) The involvement of cytoskeleton in the regulation of transbilayer movement of phospholipids in human blood platelets. Biochim. Biophys. Acta 815, 143-148
32. Munnix, I.C., Kuijpers, M.J., Auger, J., Thomassen, C.M., Panizzi, P., van Zandvoort, M.A., Rosing, J., Bock, P.E., Watson, S.P. and Heemskerk, J.W. (2007) Segregation of platelet aggregatory and procoagulant microdomains in thrombus formation: regulation by transient integrin activation. Arterioscler. Thromb. Vasc. Biol. 27, 2484-2490
33. Srivastava, K. and Dash, D. (2001) Altered membrane fluidity and signal transduction in the platelets from patients of thrombotic stroke. Mol. Cell Biochem. 224, 143-149
34. Pietsch, M., Chua, K.C. and Abell, A.D. (2010) Calpains: attractive targets for the development of synthetic inhibitors. Curr. Top. Med. Chem. 10, 270-293
35. Topalov, N.N., Yakimenko, A.O., Canault, M., Artemenko, E.O., Zakharova, N.V., Abaeva, A.A., Loosveld, M., Ataullakhanov, F.I., Nurden, A.T., Alessi, M.C. et al. (2012) Two types of procoagulant platelets are formed upon physiological activation and are controlled by integrin α(IIb)β(3). Arterioscler. Thromb. Vasc. Biol. 32, 2475-2483
36. Hess, M.W. and Siljander, P. (2001) Procoagulant platelet balloons: evidence from cryopreparation and electron microscopy. Histochem. Cell Biol. 115, 439-443
37. Palabrica, T., Lobb, R., Furie, B.C., Aronovitz, M., Benjamin, C., Hsu, Y.M., Sajer, S.A. and Furie, B. (1992) Leukocyte accumulation promoting fibrin deposition is mediated in vivo by P-selectin on adherent platelets. Nature 359, 848-851
38. 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
39. Azam, M., Andrabi, S.S., Sahr, K.E., Kamath, L., Kuliopulos, A. and Chishti, A.H. (2001) Disruption of the mouse mu-calpain gene reveals an essential role in platelet function. Mol. Cell. Biol. 21, 2213-2220
40. Dachary-Prigent, J., Freyssinet, J.M., Pasquet, J.M., Carron, J.C. and Nurden, A.T. (1993) Annexin V as a probe of aminophospholipid exposure and platelet membrane vesiculation: a flow cytometry study showing a role for free sulfhydryl groups. Blood 81, 2554-2565
41. Pasquet, J.M., Dachary-Prigent, J. and Nurden, A.T. (1996) Calcium influx is a determining factor of calpain activation and microparticle formation in platelets. Eur. J. Biochem. 239, 647-654
42. Shcherbina, A. and Remold-O'Donnell, E. (1999) Role of caspase in a subset of human platelet activation responses. Blood 93, 4222-4231
43. Siljander, P., Farndale, R.W., Feijge, M.A., Comfurius, P., Kos, S., Bevers, E.M. and Heemskerk, J.W. (2001) Platelet adhesion enhances the glycoprotein VI-dependent procoagulant response: involvement of p38 MAP kinase and calpain. Arterioscler. Thromb. Vasc. Biol. 21, 618-627
44. Wang, K.K. (2000) Calpain and caspase: can you tell the difference? Trends Neurosci. 23, 20-26
45. Jackson, S.P. and Schoenwaelder, S.M. (2010) Procoagulant platelets: are they necrotic? Blood 116, 2011-2018
46. van Kruchten, R., Mattheij, N.J., Saunders, C., Feijge, M.A., Swieringa, F., Wolfs, J.L., Collins, P.W., Heemskerk, J.W. and Bevers, E.M. (2013) Both TMEM16F-dependent and TMEM16F-independent pathways contribute to phosphatidylserine exposure in platelet apoptosis and platelet activation. Blood 121, 1850-1857
47. Dale, G.L., Remenyi, G. and Friese, P. (2005) Quantitation of microparticles released from coated-platelets. J. Thromb. Haemost. 3, 2081-2088
48. Yano, Y., Shiba, E., Kambayashi, J., Sakon, M., Kawasaki, T., Fujitani, K., Kang, J. and Mori, T. (1993) The effects of calpeptin (a calpain specific inhibitor) on agonist induced microparticle formation from the platelet plasma membrane. Thromb. Res. 71, 385-396
49. Agbani, E.O., van den Bosch, M.T., Brown, E., Williams, C.M., Mattheij, N.J., Cosemans, J.M., Collins, P.W., Heemskerk, J.W., Hers, I. and Poole, A.W. (2015) Coordinated membrane ballooning and procoagulant spreading in human platelets. Circulation 132, 1414-1424
50. Gaffet, P., Bettache, N. and Bienvenüe, A. (1995) Phosphatidylserine exposure on the platelet plasma membrane during A23187-induced activation is independent of cytoskeleton reorganization. Eur. J. Cell Biol. 67, 336-345
51. Liu, F., Gamez, G., Myers, D.R., Clemmons, W., Lam, W.A. and Jobe, S.M. (2013) Mitochondrially mediated integrin αIIbβ3 protein inactivation limits thrombus growth. J. Biol. Chem. 288, 30672-30681
52. Mattheij, N.J., Gilio, K., van Kruchten, R., Jobe, S.M., Wieschhaus, A.J., Chishti, A.H., Collins, P., Heemskerk, J.W. and Cosemans, J.M. (2013) Dual mechanism of integrin αIIbβ3 closure in procoagulant platelets. J. Biol. Chem. 288, 13325-13336
53. Cranmer, S.L., Ashworth, K.J., Yao, Y., Berndt, M.C., Ruggeri, Z.M., Andrews, R.K. and Jackson, S.P. (2011) High shear-dependent loss of membrane integrity and defective platelet adhesion following disruption of the GPIbα-filamin interaction. Blood 117, 2718-2727
54. Perrault, C., Mangin, P., Santer, M., Baas, M.J., Moog, S., Cranmer, S.L., Pikovski, I., Williamson, D., Jackson, S.P., Cazenave, J.P. et al. (2003) Role of the intracellular domains of GPIb in controlling the adhesive properties of the platelet GPIb/V/IX complex. Blood 101, 3477-3484
55. Pasquet, J.M., Dachary-Prigent, J. and Nurden, A.T. (1998) Microvesicle release is associated with extensive protein tyrosine dephosphorylation in platelets stimulated by A23187 or a mixture of thrombin and collagen. Biochem. J. 333, 591-599
56. Kulkarni, S. and Jackson, S.P. (2004) Platelet factor XIII and calpain negatively regulate integrin alphaIIbbeta3 adhesive function and thrombus growth. J. Biol. Chem. 279, 30697-30706
57. Abaeva, A.A., Canault, M., Kotova, Y.N., Obydennyy, S.I., Yakimenko, A.O., Podoplelova, N.A., Kolyadko, V.N., Chambost, H., Mazurov, A.V., Ataullakhanov, F.I. et al. (2013) Procoagulant platelets form an α-granule protein-covered 'cap' on their surface that promotes their attachment to aggregates. J. Biol. Chem. 288, 29621-29632