Mechanisms of microparticle generation: On the trail of the mitochondrion!

Seminars in Thrombosis and Hemostasis

Volumn 36, Issue 8, 2010, Pages 833-844

  Morel, Olivier ^a,b   Toti, Florence ^a,b   Jesel, Laurence ^b   Freyssinet, Jean Marie ^a,b  

^a BICÊTRE HOSPITAL   (France)

^b UNIVERSITÉ DE STRASBOURG   (France)

Author keywords

apoptosis; Phosphatidylserine; platelet; Scott's syndrome; thrombosis

Indexed keywords

AZATHIOPRINE; CALCIUM; COLLAGEN; CYCLOSPORIN; CYCLOSPORIN A; MEMBRANE PHOSPHOLIPID; MYCOPHENOLIC ACID 2 MORPHOLINOETHYL ESTER; PHOSPHATASE; PHOSPHATIDYLSERINE; PHOSPHOTRANSFERASE; TACROLIMUS; THROMBIN; VALINOMYCIN;

CALCIUM CELL LEVEL; CELL STIMULATION; CYTOSKELETON; ENDOTHELIAL MICROPARTICLE; EXOCYTOSIS; GENETIC DISORDER; GENETIC TRAIT; HOMEOSTASIS; HUMAN; ION TRANSPORT; MITOCHONDRION; PLASMA; PRIORITY JOURNAL; REVIEW; RISK FACTOR; SCOTT SYNDROME; THROMBOSIS;

ANIMALS; BLOOD COAGULATION DISORDERS; CELL-DERIVED MICROPARTICLES; HOMEOSTASIS; HUMANS; MITOCHONDRIA; PHOSPHATIDYLSERINES;

EID: 78149287957     PISSN: 00946176     EISSN: 10989064     Source Type: Journal    
DOI: 10.1055/s-0030-1267037     Document Type: Review

References (101)

1. Freyssinet J M., Toti F, Hugel B et al. Apoptosis in vascular disease. Thromb Haemost 1999 82 (2) 727-735
2. Fadok V A., Bratton D L., Rose D M., Pearson A, Ezekewitz R A., Henson P M. A receptor for phosphatidylserine-specific clearance of apoptotic cells. Nature 2000 405 (6782) 85-90
3. Morel O, Morel N, Freyssinet J M., Toti F. Platelet microparticles and vascular cells interactions: a checkpoint between the haemostatic and thrombotic responses. Platelets 2008 19 (1) 9-23
4. VanWijk M J., VanBavel E, Sturk A, Nieuwland R. Microparticles in cardiovascular diseases. Cardiovasc Res 2003 59 (2) 277-287
5. Morel O, Toti F, Hugel B et al. Procoagulant microparticles: disrupting the vascular homeostasis equation? Arterioscler Thromb Vasc Biol 2006 26 (12) 2594-2604
6. Bach R, Rifkin D B. Expression of tissue factor procoagulant activity: regulation by cytosolic calcium. Proc Natl Acad Sci U S A 1990 87 (18) 6995-6999
7. Mackman N, Tilley R E., Key N S. Role of the extrinsic pathway of blood coagulation in hemostasis and thrombosis. Arterioscler Thromb Vasc Biol 2007 27 (8) 1687-1693
8. M?ller I, Klocke A, Alex M et al. Intravascular tissue factor initiates coagulation via circulating microvesicles and platelets. FASEB J 2003 17 (3) 476-478
9. Théry C, Ostrowski M, Segura E. Membrane vesicles as conveyors of immune responses. Nat Rev Immunol 2009 9 (8) 581-593
10. Hugel B, Mart?nez M C., Kunzelmann C, Freyssinet J M. Membrane microparticles: two sides of the coin. Physiology (Bethesda) 2005 20 22-27
11. Seigneuret M, Zachowski A, Hermann A, Devaux P F. Asymmetric lipid fluidity in human erythrocyte membrane: new spin-label evidence. Biochemistry 1984 23 (19) 4271-4275
12. Smeets E F., Comfurius P, Bevers E M., Zwaal R F. Calcium-induced transbilayer scrambling of fluorescent phospholipid analogs in platelets and erythrocytes. Biochim Biophys Acta 1994 1195 (2) 281-286
13. Williamson P, Bevers E M., Smeets E F., Comfurius P, Schlegel R A., Zwaal R F. Continuous analysis of the mechanism of activated transbilayer lipid movement in platelets. Biochemistry 1995 34 (33) 10448-10455
14. Comfurius P, Williamson P, Smeets E F., Schlegel R A., Bevers E M., Zwaal R F. Reconstitution of phospholipid scramblase activity from human blood platelets. Biochemistry 1996 35 (24) 7631-7634
15. Weiss H J., Vicic W J., Lages B A., Rogers J. Isolated deficiency of platelet procoagulant activity. Am J Med 1979 67 (2) 206-213
16. Toti F, Satta N, Fressinaud E, Meyer D, Freyssinet J M. Scott syndrome, characterized by impaired transmembrane migration of procoagulant phosphatidylserine and hemorrhagic complications, is an inherited disorder. Blood 1996 87 (4) 1409-1415
17. Miletich J P., Kane W H., Hofmann S L., Stanford N, Majerus P W. Deficiency of factor Xa-factor Va binding sites on the platelets of a patient with a bleeding disorder. Blood 1979 54 (5) 1015-1022
18. Rosing J, Bevers E M., Comfurius P et al. Impaired factor X and prothrombin activation associated with decreased phospholipid exposure in platelets from a patient with a bleeding disorder. Blood 1985 65 (6) 1557-1561
19. Sims P J., Wiedmer T, Esmon C T., Weiss H J., Shattil S J. Assembly of the platelet prothrombinase complex is linked to vesiculation of the platelet plasma membrane. Studies in Scott syndrome: an isolated defect in platelet procoagulant activity. J Biol Chem 1989 264 (29) 17049-17057
20. Bevers E M., Wiedmer T, Comfurius P et al. Defective Ca(2+)-induced microvesiculation and deficient expression of procoagulant activity in erythrocytes from a patient with a bleeding disorder: a study of the red blood cells of Scott syndrome. Blood 1992 79 (2) 380-388
21. Kojima H, Newton-Nash D, Weiss H J., Zhao J, Sims P J., Wiedmer T. Production and characterization of transformed B-lymphocytes expressing the membrane defect of Scott syndrome. J Clin Invest 1994 94 (6) 2237-2244
22. Munnix I C., Harmsma M, Giddings J C. et al. Store-mediated calcium entry in the regulation of phosphatidylserine exposure in blood cells from Scott patients. Thromb Haemost 2003 89 (4) 687-695
23. Parry D H., Giddings J C., Bloom A L. Familial haemostatic defect associated with reduced prothrombin consumption. Br J Haematol 1980 44 (2) 323-334
24. Brooks M B., Catalfamo J L., Brown H A., Ivanova P, Lovaglio J. A hereditary bleeding disorder of dogs caused by a lack of platelet procoagulant activity. Blood 2002 99 (7) 2434-2441
25. Zhou Q, Zhao J, Stout J G., Luhm R A., Wiedmer T, Sims P J. Molecular cloning of human plasma membrane phospholipid scramblase. A protein mediating transbilayer movement of plasma membrane phospholipids. J Biol Chem 1997 272 (29) 18240-18244
26. Zhou Q, Zhao J, Wiedmer T, Sims P J. Normal hemostasis but defective hematopoietic response to growth factors in mice deficient in phospholipid scramblase 1. Blood 2002 99 (11) 4030-4038
27. Janel N, Leroy C, Laude I et al. Assessment of the expression of candidate human plasma membrane phospholipid scramblase in Scott syndrome cells. Thromb Haemost 1999 81 (2) 322-323
28. Zhou Q, Sims P J., Wiedmer T. Expression of proteins controlling transbilayer movement of plasma membrane phospholipids in the B lymphocytes from a patient with Scott syndrome. Blood 1998 92 (5) 1707-1712
29. Bateman A, Finn R D., Sims P J., Wiedmer T, Biegert A, S?ding J. Phospholipid scramblases and Tubby-like proteins belong to a new superfamily of membrane tethered transcription factors. Bioinformatics 2009 25 (2) 159-162
30. Nofer J R., Herminghaus G, Brodde M et al. Impaired platelet activation in familial high density lipoprotein deficiency (Tangier disease). J Biol Chem 2004 279 (32) 34032-34037
31. Hamon Y, Broccardo C, Chambenoit O et al. ABC1 promotes engulfment of apoptotic cells and transbilayer redistribution of phosphatidylserine. Nat Cell Biol 2000 2 (7) 399-406
32. Schmitz G, Schambeck C M. Molecular defects in the ABCA1 pathway affect platelet function. Pathophysiol Haemost Thromb 2006 35 (12) 166-174
33. Elliott J I., Sardini A, Cooper J C. et al. Phosphatidylserine exposure in B lymphocytes: a role for lipid packing. Blood 2006 108 (5) 1611-1617
34. Albrecht C, McVey J H., Elliott J I. et al. A novel missense mutation in ABCA1 results in altered protein trafficking and reduced phosphatidylserine translocation in a patient with Scott syndrome. Blood 2005 106 (2) 542-549
35. Brooks M B., Catalfamo J L., Etter K, Brisbin A, Bustamante C D. Exclusion of ABCA-1 as a candidate gene for canine Scott syndrome. J Thromb Haemost 2008 6 (9) 1608-1610
36. Toti F, Schindler V, Riou J F. et al. Another link between phospholipid transmembrane migration and ABC transporter gene family, inferred from a rare inherited disorder of phosphatidylserine externalization. Biochem Biophys Res Commun 1997 241 (2) 548-552
37. van Helvoort A, Smith A J., Sprong H et al. MDR1 P-glycoprotein is a lipid translocase of broad specificity, while MDR3 P-glycoprotein specifically translocates phosphatidylcholine. Cell 1996 87 (3) 507-517
38. Brooks M, Etter K, Catalfamo J, Brisbin A, Bustamante C, Mezey J. A genome-wide linkage scan in German shepherd dogs localizes canine platelet procoagulant deficiency (Scott syndrome) to canine chromosome 27. Gene 2010 450 (12) 70-75
39. Wolfs J L., Comfurius P, Rasmussen J T. et al. Activated scramblase and inhibited aminophospholipid translocase cause phosphatidylserine exposure in a distinct platelet fraction. Cell Mol Life Sci 2005 62 (13) 1514-1525
40. Dale G L. Coated-platelets: an emerging component of the procoagulant response. J Thromb Haemost 2005 3 (10) 2185-2192
41. Morel O, Toti F, Hugel B, Freyssinet J M. Cellular microparticles: a disseminated storage pool of bioactive vascular effectors. Curr Opin Hematol 2004 11 (3) 156-164
42. Simak J, Gelderman M P. Cell membrane microparticles in blood and blood products: potentially pathogenic agents and diagnostic markers. Transfus Med Rev 2006 20 (1) 1-26
43. Horstman L L., Jy W, Jimenez J J., Bidot C, Ahn Y S. New horizons in the analysis of circulating cell-derived microparticles. Keio J Med 2004 53 (4) 210-230
44. Bucki R, Giraud F, Sulpice J C. Phosphatidylinositol 4,5-bisphosphate domain inducers promote phospholipid transverse redistribution in biological membranes. Biochemistry 2000 39 (19) 5838-5844
45. Bucki R, Janmey P A., Vegners R, Giraud F, Sulpice J C. Involvement of phosphatidylinositol 4,5-bisphosphate in phosphatidylserine exposure in platelets: use of a permeant phosphoinositide-binding peptide. Biochemistry 2001 40 (51) 15752-15761
46. Cauwenberghs S, Feijge M A., Harper A G., Sage S O., Curvers J, Heemskerk J W. Shedding of procoagulant microparticles from unstimulated platelets by integrin-mediated destabilization of actin cytoskeleton. FEBS Lett 2006 580 (22) 5313-5320
47. Wolfs J L., Wielders S J., Comfurius P et al. Reversible inhibition of the platelet procoagulant response through manipulation of the Gardos channel. Blood 2006 108 (7) 2223-2228
48. Shcherbina A, Remold-O'Donnell E. Role of caspase in a subset of human platelet activation responses. Blood 1999 93 (12) 4222-4231
49. Dachary-Prigent J, Freyssinet J M., Pasquet J M., Carron J C., Nurden A T. Annexin V as a probe of aminophospholipid exposure and platelet membrane vesiculation: a flow cytometry study showing a role for free sulfhydryl groups. Blood 1993 81 (10) 2554-2565
50. Yano Y, Kambayashi J, Shiba E et al. The role of protein phosphorylation and cytoskeletal reorganization in microparticle formation from the platelet plasma membrane. Biochem J 1994 299 (Pt 1) 303-308
51. Sebbagh M, Renvoizé C, Hamelin J, Riché N, Bertoglio J, Bréard J. Caspase-3-mediated cleavage of ROCK I induces MLC phosphorylation and apoptotic membrane blebbing. Nat Cell Biol 2001 3 (4) 346-352
52. Sapet C, Simoncini S, Loriod B et al. Thrombin-induced endothelial microparticle generation: identification of a novel pathway involving ROCK-II activation by caspase-2. Blood 2006 108 (6) 1868-1876
53. Simoncini S, Njock M S., Robert S et al. TRAIL/Apo2L mediates the release of procoagulant endothelial microparticles induced by thrombin in vitro: a potential mechanism linking inflammation and coagulation. Circ Res 2009 104 (8) 943-951
54. Dachary-Prigent J, Pasquet J M., Freyssinet J M., Nurden A T. Calcium involvement in aminophospholipid exposure and microparticle formation during platelet activation: a study using Ca2+-ATPase inhibitors. Biochemistry 1995 34 (36) 11625-11634
55. Parekh A B., Putney J W. Jr. Store-operated calcium channels. Physiol Rev 2005 85 (2) 757-810
56. Mart?nez M C., Martin S, Toti F et al. Significance of capacitative Ca2+entry in the regulation of phosphatidylserine expression at the surface of stimulated cells. Biochemistry 1999 38 (31) 10092-10098
57. Elliott J I., Mumford A D., Albrecht C et al. Characterisation of lymphocyte responses to Ca2+ in Scott syndrome. Thromb Haemost 2004 91 (2) 412-415
58. Kunzelmann-Marche C, Freyssinet J M., Mart?nez M C. Loss of plasma membrane phospholipid asymmetry requires raft integrity. Role of transient receptor potential channels and ERK pathway. J Biol Chem 2002 277 (22) 19876-19881
59. Arachiche A, Badirou I, Dachary-Prigent J, Garcin I, Geldwerth-Feniger D, Kerbiriou-Nabias D. ERK activation by Ca2+ ionophores depends on Ca2+ entry in lymphocytes but not in platelets, and does not conduct membrane scrambling. Cell Mol Life Sci 2008 65 (23) 3861-3871
60. Arachiche A, Kerbiriou-Nabias D, Garcin I, Letellier T, Dachary-Prigent J. Rapid procoagulant phosphatidylserine exposure relies on high cytosolic calcium rather than on mitochondrial depolarization. Arterioscler Thromb Vasc Biol 2009 29 (11) 1883-1889
61. Kunzelmann-Marche C, Freyssinet J M., Mart?nez M C. Regulation of phosphatidylserine transbilayer redistribution by store-operated Ca2+ entry: role of actin cytoskeleton. J Biol Chem 2001 276 (7) 5134-5139
62. Dervaux T, Porro C, Kunzelmann C, Freyssinet J M., Mart?nez M C. Cyclic GMP modulates store-operated calcium entry inducing phosphatidylserine translocation at the surface of megakaryocytic cells. Biochimie 2006 88 (9) 1175-1182
63. Kunzelmann C, Freyssinet J M., Mart?nez M C. Rho A participates in the regulation of phosphatidylserine-dependent procoagulant activity at the surface of megakaryocytic cells. J Thromb Haemost 2004 2 (4) 644-650
64. Bergmeier W, Oh-Hora M, McCarl C A., Roden R C., Bray P F., Feske S. R93W mutation in Orai1 causes impaired calcium influx in platelets. Blood 2009 113 (3) 675-678
65. Galitzine M, Capiod T, Le Deist F, Meyer D, Freyssinet J M., Kerbiriou-Nabias D. Ca2+ ionophores trigger membrane remodeling without a need for store-operated Ca2+ entry. Biochem Biophys Res Commun 2005 327 (1) 335-341
66. Michel V, Bakovic M. Lipid rafts in health and disease. Biol Cell 2007 99 (3) 129-140
67. Le Goff W, Peng D Q., Settle M, Brubaker G, Morton R E., Smith J D. Cyclosporin A traps ABCA1 at the plasma membrane and inhibits ABCA1-mediated lipid efflux to apolipoprotein A-I. Arterioscler Thromb Vasc Biol 2004 24 (11) 2155-2161
68. Lorenzi I, von Eckardstein A, Cavelier C, Radosavljevic S, Rohrer L. Apolipoprotein A-I but not high-density lipoproteins are internalised by RAW macrophages: roles of ATP-binding cassette transporter A1 and scavenger receptor BI. J Mol Med 2008 86 (2) 171-183
69. Karwatsky J, Ma L, Dong F, Zha X. Cholesterol efflux to apoA-I in ABCA1-expressing cells is regulated by Ca2+ -dependent calcineurin signaling. J Lipid Res 2010 51 (5) 1144-1156
70. Pasquet J M., Dachary-Prigent J, Nurden A T. Microvesicle release is associated with extensive protein tyrosine dephosphorylation in platelets stimulated by A23187 or a mixture of thrombin and collagen. Biochem J 1998 333 (Pt 3) 591-599
71. Heemskerk J W., Vuist W M., Feijge M A., Reutelingsperger C P., Lindhout T. 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 Ca2+ responses. Blood 1997 90 (7) 2615-2625
72. Siljander P, Farndale R W., Feijge M A. et al. Platelet adhesion enhances the glycoprotein VI-dependent procoagulant response: Involvement of p38 MAP kinase and calpain. Arterioscler Thromb Vasc Biol 2001 21 (4) 618-627
73. Imam-Sghiouar N, Laude-Lemaire I, Labas V et al. Subproteomics analysis of phosphorylated proteins: application to the study of B-lymphoblasts from a patient with Scott syndrome. Proteomics 2002 2 (7) 828-838
74. Elliott J I., Higgins C F. IKCa1 activity is required for cell shrinkage, phosphatidylserine translocation and death in T lymphocyte apoptosis. EMBO Rep 2003 4 (2) 189-194
75. Bucki R, Pastore J J., Giraud F, Janmey P A., Sulpice J C. Involvement of the Na+ /H+ exchanger in membrane phosphatidylserine exposure during human platelet activation. Biochim Biophys Acta 2006 1761 (2) 195-204
76. Raphael R M., Waugh R E., Svetina S, Zeks B. Fractional occurrence of defects in membranes and mechanically driven interleaflet phospholipid transport. Phys Rev E Stat Nonlin Soft Matter Phys 2001 64 (5 Pt 1) 051913
77. Lang K S., Lang P A., Bauer C et al. Mechanisms of suicidal erythrocyte death. Cell Physiol Biochem 2005 15 (5) 195-202
78. Contreras F X., Villar A V., Alonso A, Kolesnick R N., Go?i F M. Sphingomyelinase activity causes transbilayer lipid translocation in model and cell membranes. J Biol Chem 2003 278 (39) 37169-37174
79. Devaux P F., L?pez-Montero I, Bryde S. Proteins involved in lipid translocation in eukaryotic cells. Chem Phys Lipids 2006 141 (12) 119-132
80. Bernardi P, Scorrano L, Colonna R, Petronilli V, Di Lisa F. Mitochondria and cell death. Mechanistic aspects and methodological issues. Eur J Biochem 1999 264 (3) 687-701
81. Leytin V, Allen D J., Mutlu A, Gyulkhandanyan A V., Mykhaylov S, Freedman J. Mitochondrial control of platelet apoptosis: effect of cyclosporin A, an inhibitor of the mitochondrial permeability transition pore. Lab Invest 2009 89 (4) 374-384
82. Fadok V A., Voelker D R., Campbell P A., Cohen J J., Bratton D L., Henson P M. Exposure of phosphatidylserine on the surface of apoptotic lymphocytes triggers specific recognition and removal by macrophages. J Immunol 1992 148 (7) 2207-2216
83. Majno G, Joris I. Apoptosis, oncosis, and necrosis. An overview of cell death. Am J Pathol 1995 146 (1) 3-15
84. Aupeix K, Hugel B, Martin T et al. The significance of shed membrane particles during programmed cell death in vitro, and in vivo, in HIV-1 infection. J Clin Invest 1997 99 (7) 1546-1554
85. Mart?nez M C., Freyssinet J M. Deciphering the plasma membrane hallmarks of apoptotic cells: phosphatidylserine transverse redistribution and calcium entry. BMC Cell Biol 2001 2 20
86. Kozian D, Proulle V, Nitsche A et al. Identification of genes involved in Ca2+ ionophore A23187-mediated apoptosis and demonstration of a high susceptibility for transcriptional repression of cell cycle genes in B lymphoblasts from a patient with Scott syndrome. BMC Genomics 2005 6 146
87. MacKenzie A, Wilson H L., Kiss-Toth E, Dower S K., North R A., Surprenant A. Rapid secretion of interleukin-1beta by microvesicle shedding. Immunity 2001 15 (5) 825-835
88. Cohen Z, Gonzales R F., Davis-Gorman G F., Copeland J G., McDonagh P F. Thrombin activity and platelet microparticle formation are increased in type 2 diabetic platelets: a potential correlation with caspase activation. Thromb Res 2002 107 (5) 217-221
89. Dale G L., Friese P. Bax activators potentiate coated-platelet formation. J Thromb Haemost 2006 4 (12) 2664-2669
90. Lopez J J., Salido G M., Pariente J A., Rosado J A. Thrombin induces activation and translocation of Bid, Bax and Bak to the mitochondria in human platelets. J Thromb Haemost 2008 6 (10) 1780-1788
91. Halestrap A P., Davidson A M. Inhibition of Ca2(+)-induced large-amplitude swelling of liver and heart mitochondria by cyclosporin is probably caused by the inhibitor binding to mitochondrial-matrix peptidyl-prolyl cis-trans isomerase and preventing it interacting with the adenine nucleotide translocase. Biochem J 1990 268 (1) 153-160
92. Dale G L., Remenyi G, Friese P. Quantitation of microparticles released from coated-platelets. J Thromb Haemost 2005 3 (9) 2081-2088
93. Augereau O, Rossignol R, DeGiorgi F, Mazat J P., Letellier T, Dachary-Prigent J. Apoptotic-like mitochondrial events associated to phosphatidylserine exposure in blood platelets induced by local anaesthetics. Thromb Haemost 2004 92 (1) 104-113
94. Baines C P., Kaiser R A., Purcell N H. et al. Loss of cyclophilin D reveals a critical role for mitochondrial permeability transition in cell death. Nature 2005 434 (7033) 658-662
95. Schoenwaelder S M., Yuan Y, Josefsson E C. et al. Two distinct pathways regulate platelet phosphatidylserine exposure and procoagulant function. Blood 2009 114 (3) 663-666
96. Dachary-Prigent J, Pasquet J M., Fressinaud E, Toti F, Freyssinet J M., Nurden A T. Aminophospholipid exposure, microvesiculation and abnormal protein tyrosine phosphorylation in the platelets of a patient with Scott syndrome: a study using physiologic agonists and local anaesthetics. Br J Haematol 1997 99 (4) 959-967
97. Rand M L., Wang H, Bang K W., Poon K S., Packham M A., Freedman J. Procoagulant surface exposure and apoptosis in rabbit platelets: association with shortened survival and steady-state senescence. J Thromb Haemost 2004 2 (4) 651-659
98. Cardoso C M., Rumjanek V M., De Meis L. Uncoupling of Ca2+ transport ATPase in muscle and blood platelets by diacylglycerol analogues and cyclosporin A antagonism. Biochem J 1997 327 (Pt 3) 795-801
99. Arber S, Krause K H., Caroni P. s-cyclophilin is retained intracellularly via a unique COOH-terminal sequence and colocalizes with the calcium storage protein calreticulin. J Cell Biol 1992 116 (1) 113-125
100. Al-Massarani G, Vacher-Coponat H, Paul P et al. Kidney transplantation decreases the level and procoagulant activity of circulating microparticles. Am J Transplant 2009 9 (3) 550-557
101. Morel O, Toti F, Morel N, Freyssinet J M. Microparticles in endothelial cell and vascular homeostasis: are they really noxious? Haematologica 2009 94 (3) 313-317