Erythrocyte-derived microvesicles may transfer phosphatidylserine to the surface of nucleated cells and falsely 'mark' them as apoptotic

European Journal of Haematology

Volumn 83, Issue 3, 2009, Pages 220-229

  Liu, Rui ^a   Klich, Izabela ^a   Ratajczak, Janina ^a   Ratajczak, Mariusz Z ^a,b   Zuba Surma, Ewa K ^a  

^a UNIVERSITY OF LOUISVILLE   (United States)

^b POMERANIAN MEDICAL UNIVERSITY   (Poland)

Author keywords

Annexin V; Microvesicles; Phosphatidylserine; Very small embryonic like stem cells

Indexed keywords

HYPOTONIC SOLUTION; LIPOCORTIN 5; PHOSPHATIDYLSERINE;

APOPTOSIS; ARTICLE; BINDING ASSAY; BLOOD CELL; BONE MARROW; CELL PROLIFERATION; CELL SELECTION; CELL SEPARATION; CELL SURFACE; CELL VACUOLE; CELL VIABILITY; CONTROLLED STUDY; EMBRYONIC STEM CELL; ERYTHROCYTE; HEMOLYSIS; HUMAN; HUMAN CELL; MICROVESICLE; PRIORITY JOURNAL; PROTEIN BINDING; UMBILICAL CORD BLOOD;

AMMONIUM CHLORIDE; ANNEXIN A5; APOPTOSIS; BONE MARROW CELLS; CELL MEMBRANE; CELL NUCLEUS; CELL SEPARATION; ERYTHROCYTES; FLOW CYTOMETRY; HEMATOLOGY; HUMANS; LEUKOCYTES, MONONUCLEAR; MICROCIRCULATION; PHOSPHATIDYLSERINES; STEM CELLS;

EID: 68849102601     PISSN: 09024441     EISSN: 16000609     Source Type: Journal    
DOI: 10.1111/j.1600-0609.2009.01271.x     Document Type: Article

References (53)

1. Clark AD, Jorgensen HG, Mountford J, Holyoake TL. Isolation and therapeutic potential of human haemopoietic stem cells. Cytotechnology 2003 41 : 111 31.
2. Ng YY, Baert MR, de Haas EF, Pike-Overzet K, Staal FJ. Isolation of human and mouse hematopoietic stem cells. Methods Mol Biol 2009 506 : 13 21.
3. Soleimani M, Nadri S. A protocol for isolation and culture of mesenchymal stem cells from mouse bone marrow. Nat Protoc 2009 4 : 102 6.
4. Carciero R, Valeri CR. Isolation of mononuclear leukocytes in a plastic bag system using Ficoll-Hypaque. Vox Sang 1985 49 : 373 80.
5. Gilmore MJ, Prentice HG, Blacklock HA, Janossy G, Hoffbrand AV. A technique for rapid isolation of bone marrow mononuclear cells using Ficoll-Metrizoate and the IBM 2991 blood cell processor. Br J Haematol 1982 50 : 619 26.
6. Hokland P, Nadler LM, Griffin JD, Schlossman SF, Ritz J. Purification of common acute lymphoblastic leukemia antigen positive cells from normal human bone marrow. Blood 1984 64 : 662 6.
7. Schneider GB. Cellular specificity of the cure for osteopetrosis: isolation of and treatment with pluripotent hemopoietic stem cells. Bone 1985 6 : 241 7.
8. Kucia M, Reca R, Campbell FR, Zuba-Surma E, Majka M, Ratajczak J, Ratajczak MZ. A population of very small embryonic-like (VSEL) CXCR4(+)SSEA-1(+)Oct-4+ stem cells identified in adult bone marrow. Leukemia 2006 20 : 857 69.
9. Zuba-Surma E, Kucia M, Izabela Klich I, Greco N, Laughlin M, Paul P, Ratajczak M, Ratajczak J. Optimization of isolation and further molecular and functional characterization of SSEA-4+Oct-4+CD133+CXCR4+LINneg CD45neg very small embryonic-like (VSEL) stem cells isolated from umbilical cord blood. Blood 2008 112 : 2316.
10. Zuba-Surma EK, Kucia M, Abdel-Latif A, Dawnn B, Hall B, Singh R, Lillard JW, Ratajczak MZ. Morphological characterization of very small embryonic-like stem cells (VSELs) by Imagestream system analysis. J Cell Mol Med 2008 12 : 292 303.
11. Bevers EM, Comfurius P, Dekkers DW, Harmsma M, Zwaal RF. Transmembrane phospholipid distribution in blood cells: control mechanisms and pathophysiological significance. Biol Chem 1998 379 : 973 86.
12. Bhardwaj A, Aggarwal BB. Receptor-mediated choreography of life and death. J Clin Immunol 2003 23 : 317 32.
13. Siegel RM, Lenardo MJ. Apoptosis signaling pathways. Curr Protoc Immunol 2002 Chapter 11:Unit 11.9C.
14. Vermes I, Haanen C, Richel DJ, Schaafsma MR, Kalsbeek-Batenburg E, Reutelingsperger CP. Apoptosis and secondary necrosis of lymphocytes in culture. Acta Haematol 1997 98 : 8 13.
15. Aubry JP, Blaecke A, Lecoanet-Henchoz S, Jeannin P, Herbault N, Caron G, Moine V, Bonnefoy JY. Annexin V used for measuring apoptosis in the early events of cellular cytotoxicity. Cytometry 1999 37 : 197 204.
16. Darzynkiewicz Z, Juan G, Li X, Gorczyca W, Murakami T, Traganos F. Cytometry in cell necrobiology: analysis of apoptosis and accidental cell death (necrosis). Cytometry 1997 27 : 1 20.
17. van Engeland M, Nieland LJ, Ramaekers FC, Schutte B, Reutelingsperger CP. Annexin V-affinity assay: a review on an apoptosis detection system based on phosphatidylserine exposure. Cytometry 1998 31 : 1 9.
18. Vermes I, Haanen C, Steffens-Nakken H, Reutelingsperger C. A novel assay for apoptosis. Flow cytometric detection of phosphatidylserine expression on early apoptotic cells using fluorescein labelled Annexin V. J Immunol Methods 1995 184 : 39 51.
19. Janowska-Wieczorek A, Majka M, Kijowski J, Baj-Krzyworzeka M, Reca R, Turner AR, Ratajczak J, Emerson SG, Kowalska MA, Ratajczak MZ. Platelet-derived microparticles bind to hematopoietic stemprogenitor cells and enhance their engraftment. Blood 2001 98 : 3143 9.
20. Rozmyslowicz T, Majka M, Kijowski J, Murphy SL, Conover DO, Poncz M, Ratajczak J, Gaulton GN, Ratajczak MZ. Platelet- and megakaryocyte-derived microparticles transfer CXCR4 receptor to CXCR4-null cells and make them susceptible to infection by X4-HIV. AIDS 2003 17 : 33 42.
21. Hugel B, Martinez MC, Kunzelmann C, Freyssinet JM. Membrane microparticles: two sides of the coin. Physiology (Bethesda) 2005 20 : 22 7.
22. Zwaal RF, Schroit AJ. Pathophysiologic implications of membrane phospholipid asymmetry in blood cells. Blood 1997 89 : 1121 32.
23. Baj-Krzyworzeka M, Majka M, Pratico D, Ratajczak J, Vilaire G, Kijowski J, Reca R, Janowska-Wieczorek A, Ratajczak MZ. Platelet-derived microparticles stimulate proliferation, survival, adhesion, and chemotaxis of hematopoietic cells. Exp Hematol 2002 30 : 450 9.
24. Beaudoin AR, Grondin G. Shedding of vesicular material from the cell surface of eukaryotic cells: different cellular phenomena. Biochim Biophys Acta 1991 1071 : 203 19.
25. Greenwalt TJ. The how and why of exocytic vesicles. Transfusion 2006 46 : 143 52.
26. Ratajczak J, Wysoczynski M, Hayek F, Janowska-Wieczorek A, Ratajczak MZ. Membrane-derived microvesicles: important and underappreciated mediators of cell-to-cell communication. Leukemia 2006 20 : 1487 95.
27. Amabile N, Heiss C, Real WM, Minasi P, McGlothlin D, Rame EJ, Grossman W, De Marco T, Yeghiazarians Y. Circulating endothelial microparticle levels predict hemodynamic severity of pulmonary hypertension. Am J Respir Crit Care Med 2008 177 : 1268 75.
28. Lynch SF, Ludlam CA. Plasma microparticles and vascular disorders. Br J Haematol 2007 137 : 36 48.
29. Schwartzenberg S, Deutsch V, Maysel-Auslender S, Kissil S, Keren G, George J. Circulating apoptotic progenitor cells: a novel biomarker in patients with acute coronary syndromes. Arterioscler Thromb Vasc Biol 2007 27 : e27 31.
30. Ginestra A, La Placa MD, Saladino F, Cassara D, Nagase H, Vittorelli ML. The amount and proteolytic content of vesicles shed by human cancer cell lines correlates with their in vitro invasiveness. Anticancer Res 1998 18 : 3433 7.
31. Janowska-Wieczorek A, Wysoczynski M, Kijowski J, Marquez-Curtis L, Machalinski B, Ratajczak J, Ratajczak MZ. Microvesicles derived from activated platelets induce metastasis and angiogenesis in lung cancer. Int J Cancer 2005 113 : 752 60.
32. Kim HK, Song KS, Park YS, Kang YH, Lee YJ, Lee KR, Kim HK, Ryu KW, Bae JM, Kim S. Elevated levels of circulating platelet microparticles, VEGF, IL-6 and RANTES in patients with gastric cancer: possible role of a metastasis predictor. Eur J Cancer 2003 39 : 184 91.
33. Nagaeva O, Bondestam K, Olofsson J, Damber MG, Mincheva-Nilsson L. An optimized technique for separation of human decidual leukocytes for cellular and molecular analyses. Am J Reprod Immunol 2002 47 : 203 12.
34. Seeger FH, Tonn T, Krzossok N, Zeiher AM, Dimmeler S. Cell isolation procedures matter: a comparison of different isolation protocols of bone marrow mononuclear cells used for cell therapy in patients with acute myocardial infarction. Eur Heart J 2007 28 : 766 72.
35. Bagamery K, Kvell K, Landau R, Graham J. Flow cytometric analysis of CD41-labeled platelets isolated by the rapid, one-step OptiPrep method from human blood. Cytometry A 2005 65 : 84 7.
36. Boyum A, Brincker Fjerdingstad H, Martinsen I, Lea T, Lovhaug D. Separation of human lymphocytes from citrated blood by density gradient (NycoPrep) centrifugation: monocyte depletion depending upon activation of membrane potassium channels. Scand J Immunol 2002 56 : 76 84.
37. Pertoft H. Fractionation of cells and subcellular particles with Percoll. J Biochem Biophys Methods 2000 44 : 1 30.
38. Montuoro A, De Rosa L, Del Monte C, Blandino F, Pandolfi A, Lanti T, De Laurenzi A. A technique for isolation of bone marrow cells using hydroxyethyl starch (HES) sedimentation agent. Haematologica 1991 76 (Suppl. 1 7 9.
39. Solves P, Mirabet V, Planelles D, Blasco I, Perales A, Carbonell-Uberos F, Soler MA, Roig R. Red blood cell depletion with a semiautomated system or hydroxyethyl starch sedimentation for routine cord blood banking: a comparative study. Transfusion 2005 45 : 867 73.
40. Ridings J, Weedon H, Ioannou C, Flego L, Macardle PJ, Zola H. Purification of cord blood lymphocytes. J Immunol Methods 1996 195 : 43 8.
41. Timeus F, Crescenzio N, Doria A, Foglia L, Linari A, Giaccone M, Pastore G, di Montezemolo LC, Ramenghi U, Saracco P. Flow cytometric evaluation of circulating CD34+ cell counts and apoptotic rate in children with acquired aplastic anemia and myelodysplasia. Exp Hematol 2005 33 : 597 604.
42. Ferrero D, Tarella C, Cherasco C, Bondesan P, Omede P, Ravaglia R, Caracciolo D, Castellino C, Pileri A. A single step density gradient separation for large scale enrichment of mobilized peripheral blood progenitor cells collected for autotransplantation. Bone Marrow Transplant 1998 21 : 409 13.
43. Rambaldi A, Borleri G, Dotti G, Bellavita P, Amaru R, Biondi A, Barbui T. Innovative two-step negative selection of granulocyte colony-stimulating factor-mobilized circulating progenitor cells: adequacy for autologous and allogeneic transplantation. Blood 1998 91 : 2189 96.
44. Rogers I, Sutherland DR, Holt D, Macpate F, Lains A, Hollowell S, Cruickshank B, Casper RF. Human UC-blood banking: impact of blood volume, cell separation and cryopreservation on leukocyte and CD34(+) cell recovery. Cytotherapy 2001 3 : 269 76.
45. Zuba-Surma EK, Kucia M, Wu W, Klich I, Lillard JW Jr., Ratajczak J, Ratajczak MZ. Very small embryonic-like stem cells are present in adult murine organs: ImageStream-based morphological analysis and distribution studies. Cytometry A 2008 73A : 1116 27.
46. Bacigalupo A, Piaggio G, Podesta M, et al. Collection of peripheral blood hematopoietic progenitors (PBHP) from patients with severe aplastic anemia (SAA) after prolonged administration of granulocyte colony-stimulating factor. Blood 1993 82 : 1410 4.
47. Fuchigami K, Mori H, Matsuo T, Iwanaga M, Nagai K, Kuriyama K, Tomonaga M. Absolute number of circulating CD34+ cells is abnormally low in refractory anemias and extremely high in RAEB and RAEB-t; novel pathologic features of myelodysplastic syndromes identified by highly sensitive flow cytometry. Leuk Res 2000 24 : 163 74.
48. Benesch M, Platzbecker U, Ward J, Deeg HJ, Leisenring W. Expression of FLIP(Long) and FLIP(Short) in bone marrow mononuclear and CD34+ cells in patients with myelodysplastic syndrome: correlation with apoptosis. Leukemia 2003 17 : 2460 6.
49. Brada SJ, van de Loosdrecht AA, Koudstaal J, de Wolf JT, Vellenga E. Limited numbers of apoptotic cells in fresh paraffin embedded bone marrow samples of patients with myelodysplastic syndrome. Leuk Res 2004 28 : 921 5.
50. Merchant SH, Gonchoroff NJ, Hutchison RE. Apoptotic index by Annexin V flow cytometry: adjunct to morphologic and cytogenetic diagnosis of myelodysplastic syndromes. Cytometry 2001 46 : 28 32.
51. Pecci A, Travaglino E, Klersy C, Invernizzi R. Apoptosis in relation to CD34 antigen expression in normal and myelodysplastic bone marrow. Acta Haematol 2003 109 : 29 34.
52. Marguet D, Luciani MF, Moynault A, Williamson P, Chimini G. Engulfment of apoptotic cells involves the redistribution of membrane phosphatidylserine on phagocyte and prey. Nat Cell Biol 1999 1 : 454 6.
53. Bedner E, Li X, Gorczyca W, Melamed MR, Darzynkiewicz Z. Analysis of apoptosis by laser scanning cytometry. Cytometry 1999 35 : 181 95.