Potassium leakage primes stored erythrocytes for phosphatidylserine exposure and shedding of pro-coagulant vesicles

British Journal of Haematology

Volumn 160, Issue 3, 2013, Pages 377-386

  Burger, Patrick ^a   Kostova, Elena ^a   Bloem, Esther ^a   Hilarius Stokman, Petra ^a   Meijer, Alexander B ^a   van den Berg, Timo K ^a   Verhoeven, Arthur J ^a   de Korte, Dirk ^a   Van Bruggen, Robin ^a  

^a UNIVERSITY OF AMSTERDAM   (Netherlands)

Author keywords

Blood transfusion; Coagulalion; Erythrocytes; Red cell membrane

Indexed keywords

BLOOD CLOTTING FACTOR 10A; BLOOD CLOTTING FACTOR 8; ENZYME; FLIPPASE; PHOSPHATIDYLSERINE; POTASSIUM; UNCLASSIFIED DRUG;

ARTICLE; BLOOD CLOTTING; CELL CULTURE; CELL DAMAGE; CELL MEMBRANE; CELL POTASSIUM LEAKAGE; CELLULAR DISTRIBUTION; CELLULAR PARAMETERS; COMPLEX FORMATION; CONTROLLED STUDY; ENZYME ACTIVITY; ENZYME DEGRADATION; ERYTHROCYTE; HEMOLYSIS; HUMAN; HUMAN CELL; INCUBATION TEMPERATURE; INCUBATION TIME; MEMBRANE VESICLE; POTASSIUM CELL LEVEL; PRIORITY JOURNAL; PROTEIN PROTEIN INTERACTION;

BLOOD COAGULATION; BLOOD COAGULATION FACTORS; BLOOD PRESERVATION; ERYTHROCYTES; HEMOLYSIS; HUMANS; PHOSPHATIDYLSERINES; POTASSIUM; TRANSPORT VESICLES;

EID: 84872596546     PISSN: 00071048     EISSN: 13652141     Source Type: Journal    
DOI: 10.1111/bjh.12133     Document Type: Article

References (37)

1. Allan, D., Thomas, P. & Limbrick, A.R. (1980) The isolation and characterization of 60 nm vesicles ('nanovesicles') produced during ionophore A23187-induced budding of human erythrocytes. The Biochemical journal, 188, 881-887.
2. Amabile, N., Rautou, P.E., Tedgui, A. & Boulanger, C.M. (2010) Microparticles: key protagonists in cardiovascular disorders. Seminars in thrombosis and hemostasis, 36, 907-916.
3. Bloem, E., Meems, H., van den Biggelaar, M., van der Zwaan, C., Mertens, K. & Meijer, A.B. (2012) A mass spectrometry-assisted study reveals that lysine residues 1967 and 1968 have an opposite contribution to the stability of activated factor VIII. The Journal of biological chemistry, 287, 5775-5783.
4. Burger, P., Korsten, H., de Korte, D., Rombout, E., Van, B.R. & Verhoeven, A.J. (2010) An improved red blood cell additive solution maintains 2, 3-diphosphoglycerate and adenosine triphosphate levels by an enhancing effect on phosphofructokinase activity during cold storage. Transfusion, 50, 2386-2392.
5. Daleke, D.L. (2003) Regulation of transbilayer plasma membrane phospholipid asymmetry. Journal of lipid research, 44, 233-242.
6. Deregibus, M.C., Cantaluppi, V., Calogero, R., Lo, I.M., Tetta, C., Biancone, L., Bruno, S., Bussolati, B. & Camussi, G. (2007) Endothelial progenitor cell derived microvesicles activate an angiogenic program in endothelial cells by a horizontal transfer of mRNA. Blood, 110, 2440-2448.
7. Donadee, C., Raat, N.J., Kanias, T., Tejero, J., Lee, J.S., Kelley, E.E., Zhao, X., Liu, C., Reynolds, H., Azarov, I., Frizzell, S., Meyer, E.M., Donnenberg, A.D., Qu, L., Triulzi, D., Kim-Shapiro, D.B. & Gladwin, M.T. (2011) Nitric oxide scavenging by red blood cell microparticles and cell-free hemoglobin as a mechanism for the red cell storage lesion. Circulation, 124, 465-476.
8. Dumont, L.J. & AuBuchon, J.P. (2008) Evaluation of proposed FDA criteria for the evaluation of radiolabeled red cell recovery trials. Transfusion, 48, 1053-1060.
9. Elliott, J.I., Sardini, A., Cooper, J.C., Alexander, D.R., Davanture, S., Chimini, G. & Higgins, C.F. (2006) Phosphatidylserine exposure in B lymphocytes: a role for lipid packing. Blood, 108, 1611-1617.
10. Fadok, V.A., Voelker, D.R., Campbell, P.A., Cohen, J.J., Bratton, D.L. & Henson, P.M. (1992) Exposure of phosphatidylserine on the surface of apoptotic lymphocytes triggers specific recognition and removal by macrophages. Journal of immunology, 148, 2207-2216.
11. Fens, M.H., Mastrobattista, E., de Graaff, A.M., Flesch, F.M., Ultee, A., Rasmussen, J.T., Molema, G., Storm, G. & Schiffelers, R.M. (2008) Angiogenic endothelium shows lactadherin-dependent phagocytosis of aged erythrocytes and apoptotic cells. Blood, 111, 4542-4550.
12. Gladwin, M.T. & Kim-Shapiro, D.B. (2009) Storage lesion in banked blood due to hemolysis-dependent disruption of nitric oxide homeostasis. Current opinion in hematology, 16, 515-523.
13. Hanayama, R., Tanaka, M., Miyasaka, K., Aozasa, K., Koike, M., Uchiyama, Y. & Nagata, S. (2004) Autoimmune disease and impaired uptake of apoptotic cells in MFG-E8-deficient mice. Science, 304, 1147-1150.
14. Henson, P.M., Bratton, D.L. & Fadok, V.A. (2001) Apoptotic cell removal. Current biology : CB, 11, R795-R805.
15. Hod, E.A., Zhang, N., Sokol, S.A., Wojczyk, B.S., Francis, R.O., Ansaldi, D., Francis, K.P., Della-Latta, P., Whittier, S., Sheth, S., Hendrickson, J.E., Zimring, J.C., Brittenham, G.M. & Spitalnik, S.L. (2010) Transfusion of red blood cells after prolonged storage produces harmful effects that are mediated by iron and inflammation. Blood, 115, 4284-4292.
16. Hu, H., Xenocostas, A., Chin-Yee, N., Lu, X., Chin-Yee, I. & Feng, Q. (2012) Transfusion of fresh but not old stored blood reduces infarct size and improves cardiac function after acute myocardial infarction in anemic rats. Critical Care Medicine, 40, 1-7.
17. Jy, W., Ricci, M., Shariatmadar, S., Gomez-Marin, O., Horstman, L.H. & Ahn, Y.S. (2011) Microparticles in stored red blood cells as potential mediators of transfusion complications. Transfusion, 51, 886-893.
18. Kahlenberg, A., Walker, C. & Rohrlick, R. (1974) Evidence for an asymmetric distribution of phospholipids in the human erythrocyte membrane. Canadian journal of biochemistry, 52, 803-806.
19. Kerbiriou-Nabias, D., Arachiche, A. & Dachary-Prigent, J. (2011) Phosphatidylserine exposure and calcium-activated potassium efflux in platelets. British journal of haematology, 155, 268-270.
20. Kobayashi, N., Karisola, P., Pena-Cruz, V., Dorfman, D.M., Jinushi, M., Umetsu, S.E., Butte, M.J., Nagumo, H., Chernova, I., Zhu, B., Sharpe, A.H., Ito, S., Dranoff, G., Kaplan, G.G., Casasnovas, J.M., Umetsu, D.T., DeKruyff, R.H. & Freeman, G.J. (2007) TIM-1 and TIM-4 glycoproteins bind phosphatidylserine and mediate uptake of apoptotic cells. Immunity, 27, 927-940.
21. de Korte, D., Kleine, M., Korsten, H.G. & Verhoeven, A.J. (2008) Prolonged maintenance of 2, 3-diphosphoglycerate acid and adenosine triphosphate in red blood cells during storage. Transfusion, 48, 1081-1089.
22. Kozuma, Y., Sawahata, Y., Takei, Y., Chiba, S. & Ninomiya, H. (2011) Procoagulant properties of microparticles released from red blood cells in paroxysmal nocturnal haemoglobinuria. British journal of haematology, 152, 631-639.
23. Lang, P.A., Kaiser, S., Myssina, S., Wieder, T., Lang, F. & Huber, S.M. (2003) Role of Ca2+-activated K+ channels in human erythrocyte apoptosis. American journal of physiology. Cell physiology, 285, C1553-C1560.
24. Leal-Noval, S.R., Munoz-Gomez, M., Arellano-Orden, V., Marin-Caballos, A., Amaya-Villar, R., Marin, A., Puppo-Moreno, A., Ferrandiz-Millon, C., Flores-Cordero, J.M. & Murillo-Cabezas, F. (2008) Impact of age of transfused blood on cerebral oxygenation in male patients with severe traumatic brain injury. Critical Care Medicine, 36, 1290-1296.
25. Lee, S.J., Park, S.Y., Jung, M.Y., Bae, S.M. & Kim, I.S. (2011) Mechanism for phosphatidylserine-dependent erythrophagocytosis in mouse liver. Blood, 117, 5215-5223.
26. Luten, M., Roerdinkholder-Stoelwinder, B., Schaap, N.P., de Grip, W.J., Bos, H.J. & Bosman, G.J. (2008) Survival of red blood cells after transfusion: a comparison between red cells concentrates of different storage periods. Transfusion, 48, 1478-1485.
27. Nandrot, E.F., Anand, M., Almeida, D., Atabai, K., Sheppard, D. & Finnemann, S.C. (2007) Essential role for MFG-E8 as ligand for alphavbeta5 integrin in diurnal retinal phagocytosis. Proceedings of the National Academy of Sciences of the United States of America, 104, 12005-12010.
28. Owens, A.P. III. & Mackman, N. (2011) Microparticles in hemostasis and thrombosis. Circulation research, 108, 1284-1297.
29. Rhee, J.S., Black, M., Schubert, U., Fischer, S., Morgenstern, E., Hammes, H.P. & Preissner, K.T. (2004) The functional role of blood platelet components in angiogenesis. Thrombosis and haemostasis, 92, 394-402.
30. Rubin, O., Crettaz, D., Tissot, J.D. & Lion, N. (2010) Microparticles in stored red blood cells: submicron clotting bombs? Blood transfusion, 8(Suppl 3), s31-s38.
31. Sadallah, S., Eken, C. & Schifferli, J.A. (2008) Erythrocyte-derived ectosomes have immunosuppressive properties. Journal of leukocyte biology, 84, 1316-1325.
32. Sparrow, R.L., Healey, G., Patton, K.A. & Veale, M.F. (2006) Red blood cell age determines the impact of storage and leukocyte burden on cell adhesion molecules, glycophorin A and the release of annexin V. Transfusion and apheresis science, 34, 15-23.
33. Tinmouth, A., Fergusson, D., Yee, I.C. & Hebert, P.C. (2006) Clinical consequences of red cell storage in the critically ill. Transfusion, 46, 2014-2027.
34. Verhoeven, A.J., Hilarius, P.M., Dekkers, D.W., Lagerberg, J.W. & de Korte, D. (2006) Prolonged storage of red blood cells affects aminophospholipid translocase activity. Vox Sanguinis, 91, 244-251.
35. Vlaar, A.P., Hofstra, J.J., Levi, M., Kulik, W., Nieuwland, R., Tool, A.T., Schultz, M.J., De, K.D. & Juffermans, N.P. (2010) Supernatant of aged erythrocytes causes lung inflammation and coagulopathy in a "two-hit" in vivo syngeneic transfusion model. Anesthesiology, 113, 92-103.
36. Wolfs, J.L., Comfurius, P., Bekers, O., Zwaal, R.F., Balasubramanian, K., Schroit, A.J., Lindhout, T. & Bevers, E.M. (2009) Direct inhibition of phospholipid scrambling activity in erythrocytes by potassium ions. Cellular and molecular life sciences : CMLS, 66, 314-323.
37. Wu, Y., Tibrewal, N. & Birge, R.B. (2006) Phosphatidylserine recognition by phagocytes: a view to a kill. Trends in Cell Biology, 16, 189-197.