Characterization of procoagulant extracellular vesicles and platelet membrane disintegration in DMSO-cryopreserved platelets

Journal of Extracellular Vesicles

Volumn 5, Issue 1, 2016, Pages

  Tegegn, Tseday Z ^a   De Paoli, Silvia H ^a   Orecna, Martina ^a   Elhelu, Oumsalama K ^a   Woodle, Samuel A ^a   Tarandovskiy, Ivan D ^a   Ovanesov, Mikhail V ^a   Simak, Jan ^a  

^a CENTER FOR DRUG EVALUATION AND RESEARCH   (United States)

Author keywords

atomic force microscopy; blood products; electron microscopy; extracellular vesicles; flow cytometry; microparticles; nanoparticle tracking analysis; platelet physiology; thrombin; transfusion medicine

Indexed keywords

DIMETHYL SULFOXIDE; NANOPARTICLE; PHOSPHATIDYLSERINE; SYNEXIN;

ARTICLE; ATOMIC FORCE MICROSCOPY; BLOOD CLOTTING; CELL LOSS; CELL MEMBRANE FLUIDITY; CELL SIZING (MEASUREMENT); CELLULAR DISTRIBUTION; CONTROLLED STUDY; CRYOPRESERVATION; EXOSOME; FLOW CYTOMETRY; FLUORESCENCE POLARIZATION; FREEZE THAWING; HUMAN; HUMAN CELL; PHENOTYPE; PLATELET COUNT; SCANNING ELECTRON MICROSCOPY; THROMBIN TIME; THROMBOCYTE ACTIVATION; THROMBOCYTE MEMBRANE; THROMBOCYTE PRESERVATION; THROMBOCYTE STRUCTURE; TRANSMISSION ELECTRON MICROSCOPY;

EID: 85015446593     PISSN: None     EISSN: 20013078     Source Type: Journal    
DOI: 10.3402/jev.v5.30422     Document Type: Article

References (50)

1. Dumont LJ, Slichter SJ, Reade MC. Cryopreserved platelets: frozen in a logjam?. Transfusion. 2014; 54: 1907–10.
2. Valeri CR. Hemostatic effectiveness of liquid-preserved and previously frozen human platelets. N Engl J Med. 1974; 290: 353–8.
3. Valeri CR, Feingold H, Marchionni LD. A simple method for freezing human platelets using 6 per cent dimethylsulfoxide and storage at −80 degrees C. Blood. 1974; 43: 131–6.
4. Valeri CR, Ragno G, Khuri S. Freezing human platelets with 6 percent dimethyl sulfoxide with removal of the supernatant solution before freezing and storage at −80 degrees C without postthaw processing. Transfusion. 2005; 45: 1890–8.
5. Dumont LJ, Cancelas JA, Dumont DF, Siegel AH, Szczepiorkowski ZM, Rugg N, etal. A randomized controlled trial evaluating recovery and survival of 6% dimethyl sulfoxide-frozen autologous platelets in healthy volunteers. Transfusion. 2013; 53: 128–37.
6. Santos NC, Figueira-Coelho J, Martins-Silva J, Saldanha C. Multidisciplinary utilization of dimethyl sulfoxide: pharmacological, cellular, and molecular aspects. Biochem Pharmacol. 2003; 65: 1035–41.
7. Jacob SW, Herschler R. Pharmacology of DMSO. Cryobiology. 1986; 23: 14–27.
8. Fahy GM. The relevance of cryoprotectant “toxicity” to cryobiology. Cryobiology. 1986; 23: 1–13.
9. Oh JE, Karlmark Raja K, Shin JH, Pollak A, Hengstschläger M, Lubec G. Cytoskeleton changes following differentiation of N1E-115 neuroblastoma cell line. Amino Acids. 2006; 31: 289–98.
10. Jiang G, Bi K, Tang T, Wang J, Zhang Y, Zhang W, etal. Down-regulation of TRRAP-dependent hTERT and TRRAP-independent CAD activation by Myc/Max contributes to the differentiation of HL60 cells after exposure to DMSO. Int Immunopharmacol. 2006; 6: 1204–13.
11. Cox MA, Kastrup J, Hrubisko M. Historical perspectives and the future of adverse reactions associated with haemopoietic stem cells cryopreserved with dimethyl sulfoxide. Cell Tissue Bank. 2012; 13: 203–15.
12. Hornsey VS, McMillan L, Morrison A, Drummond O, Macgregor IR, Prowse CV. Freezing of buffy coat-derived, leukoreduced platelet concentrates in 6 percent dimethyl sulfoxide. Transfusion. 2008; 48: 2508–14.
13. Valeri CR, Macgregor H, Ragno G. Correlation between in vitro aggregation and thromboxane A2 production in fresh, liquid-preserved, and cryopreserved human platelets: effect of agonists, pH, and plasma and saline resuspension. Transfusion. 2005; 45: 596–603.
14. Khuri SF, Healey N, MacGregor H, Barnard MR, Szymanski IO, Birjiniuk V, etal. Comparison of the effects of transfusions of cryopreserved and liquid-preserved platelets on hemostasis and blood loss after cardiopulmonary bypass. J Thorac Cardiovasc Surg. 1999; 117: 172–83;discussion 83–4.
15. Klein E, Toch R, Farber S, Freeman G, Fiorentino R. Hemostasis in thrombocytopenic bleeding following infusion of stored, frozen platelets. Blood. 1956; 11: 693–9.
16. Slichter SJ, Jones M, Ransom J, Gettinger I, Jones MK, Christoffel T, etal. Review of in vivo studies of dimethyl sulfoxide cryopreserved platelets. Transfus Med Rev. 2014; 28: 212–25.
17. Schiffer CA, Aisner J, Wiernik PH. Clinical experience with transfusion of cryopreserved platelets. Br J Haematol. 1976; 34: 377–85.
18. Lelkens CC, Koning JG, de Kort B, Floot IB, Noorman F. Experiences with frozen blood products in the Netherlands military. Transfus Apher Sci. 2006; 34: 289–98.
19. Neuhaus SJ, Wishaw K, Lelkens C. Australian experience with frozen blood products on military operations. Med J Aust. 2010; 192: 203–5.
20. Johnson L, Coorey CP, Marks DC. The hemostatic activity of cryopreserved platelets is mediated by phosphatidylserine-expressing platelets and platelet microparticles. Transfusion. 2014; 54: 1917–26.
21. Shibeko AM, Woodle SA, Lee TK, Ovanesov MV. Unifying the mechanism of recombinant FVIIa action: dose dependence is regulated differently by tissue factor and phospholipids. Blood. 2012; 120: 891–9.
22. Woodle SA, Shibeko AM, Lee TK, Ovanesov MV. Determining the impact of instrument variation and automated software algorithms on the TGT in hemophilia and normalized plasma. Thromb Res. 2013; 132: 374–80.
23. Simak J, Holada K, Janota J, Stranák Z. Surface expression of major membrane glycoproteins on resting and TRAP-activated neonatal platelets. Pediatr Res. 1999; 46: 445–9.
24. Simak J, Gelderman MP. Cell membrane microparticles in blood and blood products: potentially pathogenic agents and diagnostic markers. Transfus Med Rev. 2006; 20: 1–26.
25. Orecna M, De Paoli SH, Janouskova O, Tegegn TZ, Filipova M, Bonevich JE. Toxicity of carboxylated carbon nanotubes in endothelial cells is attenuated by stimulation of the autophagic flux with the release of nanomaterial in autophagic vesicles. Nanomedicine. 2014; 10: 939–48.
26. Semberova J, De Paoli Lacerda SH, Simakova O, Holada K, Gelderman MP, Simak J. Carbon nanotubes activate blood platelets by inducing extracellular Ca2+ influx sensitive to calcium entry inhibitors. Nano Lett. 2009; 9: 3312–7.
27. Lacerda SH, Semberova J, Holada K, Simakova O, Hudson SD, Simak J. Carbon nanotubes activate store-operated calcium entry in human blood platelets. ACS Nano. 2011; 5: 5808–13.
28. Dobrovolskaia MA, Patri AK, Simak J, Hall JB, Semberova J, De Paoli Lacerda SH, etal. Nanoparticle size and surface charge determine effects of PAMAM dendrimers on human platelets in vitro. Mol Pharm. 2012; 9: 382–93.
29. De Paoli SH, Diduch LL, Tegegn TZ, Orecna M, Strader MB, Karnaukhova E, etal. The effect of protein corona composition on the interaction of carbon nanotubes with human blood platelets. Biomaterials. 2014; 35: 6182–94.
30. Shinitzky M, Barenholz Y. Fluidity parameters of lipid regions determined by fluorescence polarization. Biochim Biophys Acta. 1978; 515: 367–94.
31. Rooney TA, Hager R, Stubbs CD, Thomas AP. Halothane regulates G-protein-dependent phospholipase C activity in turkey erythrocyte membranes. J Biol Chem. 1993; 268: 15550–6.
32. Popov VM, Vladareanu AM, Bumbea H, Kovacs E, Moisescu MG, Onisai M, etal. Assessment of changes in membrane properties of platelets from patients with chronic myeloid leukaemia in different stages of the disease. Blood Coagul Fibrinolysis. 2014; 25: 142–50.
33. Watala C, Golanski J, Boncler MA, Pietrucha T, Gwozdzinski K. Membrane lipid fluidity of blood platelets: a common denominator that underlies the opposing actions of various agents that affect platelet activation in whole blood. Platelets. 1998; 9: 315–27.
34. Spector JI, Flor WJ, Valeri CR. Ultrastructural alterations and phagocytic function of cryopreserved platelets. Transfusion. 1979; 19: 307–12.
35. Spector JI, Skrabut EM, Valeri CR. Oxygen consumption, platelet aggregation and release reactions in platelets freeze-preserved with dimethylsulfoxide. Transfusion. 1977; 17: 99–109.
36. Odink J, Brank A., Platelet preservation V. Survival, serotonin uptake velocity, and response to hypotonic stress of fresh and cryopreserved human platelets. Transfusion. 1977; 17: 203–9.
37. Holtz GC, Davis RB. Inhibition of human platelet aggregation by dimethylsulfoxide, dimethylacetamide, and sodium glycerophosphate. Proc Soc Exp Biol Med. 1972; 141: 244–8.
38. Kim BK, Baldini MG. Biochemistry, function, and hemostatic effectiveness of frozen human platelets. Proc Soc Exp Biol Med. 1974; 145: 830–5.
39. Owens M, Cimino C, Donnelly J. Cryopreserved platelets have decreased adhesive capacity. Transfusion. 1991; 31: 160–3.
40. Crowley JP, Rene A, Valeri CR. Changes in platelet shape and structure after freeze preservation. Blood. 1974; 44: 599–603.
41. Baythoon H, Tuddenham EG, Hutton RA. Morphological and functional disturbances of platelets induced by cryopreservation. J Clin Pathol. 1982; 35: 870–4.
42. Murphy S, Sayar SN, Abdou NL, Gardner FH. Platelet preservation by freezing. Use of dimethylsulfoxide as cryoprotective agent. Transfusion. 1974; 14: 139–44.
43. Valeri CR. Cryopreservation of human platelets and bone marrow and peripheral blood totipotential mononuclear stem cells. Ann N Y Acad Sci. 1985; 459: 353–66.
44. van der Pol E, Coumans F, Varga Z, Krumrey M, Nieuwland R. Innovation in detection of microparticles and exosomes. J Thromb Haemost. 2013; 11(Suppl 1):36–45.
45. Dragovic RA, Collett GP, Hole P, Ferguson DJ, Redman CW, Sargent IL, etal. Isolation of syncytiotrophoblast microvesicles and exosomes and their characterisation by multicolour flow cytometry and fluorescence Nanoparticle Tracking Analysis. Methods. 2015; 87: 64–74.
46. Dragovic RA, Southcombe JH, Tannetta DS, Redman CW, Sargent IL. Multicolor flow cytometry and nanoparticle tracking analysis of extracellular vesicles in the plasma of normal pregnant and pre-eclamptic women. Biol Reprod. 2013; 89: 151.
47. Gardiner C, Ferreira YJ, Dragovic RA, Redman CW, Sargent IL. Extracellular vesicle sizing and enumeration by nanoparticle tracking analysis. J Extracell Vesicles. 2013; 2: 19671. doi: http://dx.doi.org/10.3402/jev.v2i0.19671.
48. Raynel S, Padula MP, Marks DC, Johnson L. Cryopreservation alters the membrane and cytoskeletal protein profile of platelet microparticles. Transfusion. 2015; 55: 2422–32.
49. Filella M, Zhang J, Newman ME, Buffle J. Analytical applications of photon correlation spectroscopy for size distribution measurements of natural colloidal suspensions: capabilities and limitations. Colloids Surfaces A. 1997; 120: 27–46.
50. Gardiner C, Harrison P, Belting M, Böing A, Campello E, Carter BS, etal. Extracellular vesicles, tissue factor, cancer and thrombosis–discussion themes of the ISEV 2014 Educational Day. J Extracell Vesicles. 2015; 4: 26901. doi: http://dx.doi.org/10.3402/jev.v4.26901.