Techniques to improve detection and analysis of extracellular vesicles using flow cytometry

Cytometry Part A

Volumn 87, Issue 11, 2015, Pages 1052-1063

  Inglis, Heather C ^a   Danesh, Ali ^a,b   Shah, Avani ^a   Lacroix, Jacques ^c   Spinella, Philip C ^d   Norris, Philip J ^a,b  

^a BLOOD SYSTEMS RESEARCH INSTITUTE   (United States)

^b UNIVERSITY OF CALIFORNIA   (United States)

^c UNIVERSITÉ DE MONTRÉAL   (Canada)

^d WASHINGTON UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

Antibody aggregates; Extracellular vesicles; Filtration; Flow cytometry; Microparticles

Indexed keywords

ANTIBODY; LEUKOCYTE ANTIGEN;

EXOSOME; FILTRATION; FLOW CYTOMETRY; HUMAN; IMMUNOLOGY; PROCEDURES; STAINING;

ANTIBODIES; ANTIGENS, CD; EXTRACELLULAR VESICLES; FILTRATION; FLOW CYTOMETRY; HUMANS; STAINING AND LABELING;

EID: 84945468957     PISSN: 15524922     EISSN: 15524930     Source Type: Journal    
DOI: 10.1002/cyto.a.22649     Document Type: Article

References (72)

1. Momen-Heravi F, Balaj L, Alian S, Mantel P-Y, Halleck AE, Trachtenberg AJ, Soria CE, Oquin S, Bonebreak CM, Saracoglu E, et al. Current methods for the isolation of extracellular vesicles. Biol Chem 2013;394:1253-1262.
2. Raposo G, Stoorvogel W. Extracellular vesicles: Exosomes, microvesicles, and friends. J Cell Biol 2013;200:373-383.
3. Nolte-'t Hoen ENM, van der Vlist EJ, Aalberts M, Mertens HCH, Bosch BJ, Bartelink W, Mastrobattista E, van Gaal EVB, Stoorvogel W, Arkesteijn GJA, et al. Quantitative and qualitative flow cytometric analysis of nanosized cell-derived membrane vesicles. Nanomed Nanotechnol Biol Med 2012;8:712-720.
4. Barteneva NS, Fasler-Kan E, Bernimoulin M, Stern JN, Ponomarev ED, Duckett L, Vorobjev IA. Circulating microparticles: Square the circle. BMC Cell Biol 2013;14:23.
5. Van der Pol E, Böing AN, Harrison P, Sturk A, Nieuwl R. Classification, functions, and clinical relevance of extracellular vesicles. Pharmacol Rev 2012;64:676-705.
6. Cocucci E, Racchetti G, Meldolesi J. Shedding microvesicles: Artefacts no more. Trends Cell Biol 2009;19:43-51.
7. Furmanski P. Revealing the mechanism of tissue damage due to tobacco use: Finally, a smoking gun? Am J Pathol 2013;182:1489-1493.
8. Vasina EM, Cauwenberghs S, Feijge MAH, Heemskerk JWM, Weber C, Koenen RR. Microparticles from apoptotic platelets promote resident macrophage differentiation. Cell Death Dis 2011; 2:e210.
9. Dignat-George F, Boulanger CM. The many faces of endothelial microparticles. Arterioscler Thromb Vasc Biol 2011;31:27-33.
10. Mathivanan S, Ji H, Simpson RJ. Exosomes: Extracellular organelles important in intercellular communication. J Proteomics 2010;73:1907-1920.
11. Strasser EF, Happ S, Weiss DR, Pfeiffer A, Zimmermann R, Eckstein R. Microparticle detection in platelet products by three different methods. Transfusion (Paris) 2013;53:156-166.
12. Sugawara A, Nollet KE, Yajima K, Saito S, Ohto H. Preventing platelet-derived microparticle formation and possible side effects-with prestorage leukofiltration of whole blood. Arch Pathol Lab Med 2010;134:771-775.
13. Théry C, Ostrowski M, Segura E. Membrane vesicles as conveyors of immune responses. Nat Rev Immunol 2009;9:581-593.
14. Spinella PC, Sparrow RL, Hess JR, Norris PJ. Properties of stored red blood cells: Understanding immune and vascular reactivity. Transfusion (Paris) 2011;51:894-900.
15. Andreola G, Rivoltini L, Castelli C, Huber V, Perego P, Deho P, Squarcina P, Accornero P, Lozupone F, Lugini L, et al. Induction of lymphocyte apoptosis by tumor cell secretion of FasL-bearing microvesicles. J Exp Med 2002;195:1303-1316.
16. Huber V, Fais S, Iero M, Lugini L, Canese P, Squarcina P, Zaccheddu A, Colone M, Arancia G, Gentile M, et al. Human colorectal cancer cells induce T-cell death through release of proapoptotic microvesicles: Role in immune escape. Gastroenterology 2005;128:1796-1804.
17. Kim JW, Wieckowski E, Taylor DD, Reichert TE, Watkins S, Whiteside TL. Fas ligand-positive membranous vesicles isolated from sera of patients with oral cancer induce apoptosis of activated T Lymphocytes. Clin Cancer Res 2005;11:1010-1020.
18. Taylor DD, Gerçel-Taylor Ç, Lyons KS, Stanson J, Whiteside TL. T-cell apoptosis and suppression of T-cell receptor/CD3-ζ by fas Ligand-containing membrane vesicles shed from ovarian tumors. Clin Cancer Res 2003;9:5113-5119.
19. Valenti R, Huber V, Iero M, Filipazzi P, Parmiani G, Rivoltini L. Tumor-released microvesicles as vehicles of immunosuppression. Cancer Res 2007;67:2912-2915.
20. Dolo V, D'Ascenzo S, Violini S, Pompucci L, Festuccia C, Ginestra A, Vittorelli ML, Canevari S, Pavan A. Matrix-degrading proteinases are shed in membrane vesicles by ovarian cancer cells in vivo and in vitro. Clin Exp Metastasis 1999;17:131-140.
21. Ginestra A, La Placa MD, Saladino F, Cassarà 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;18:3433-3437.
22. Rak J. Microparticles in cancer. Semin Thromb Hemost 2010;36:888-906.
23. Hood JL, San RS, Wickline SA. Exosomes released by melanoma cells prepare sentinel lymph nodes for tumor metastasis. Cancer Res 2011;71:3792-3801.
24. Ranghino A, Cantaluppi V, Grange C, Vitillo L, Fop F, Biancone L, Deregibus MC, Tetta C, Segoloni GP, Camussi G. Endothelial progenitor cell-derived microvesicles improve neovascularization in a murine model of hindlimb ischemia. Int J Immunopathol Pharmacol 2012;25:75-85.
25. Gatti S, Bruno S, Deregibus MC, Sordi A, Cantaluppi V, Tetta C, Camussi G. Microvesicles derived from human adult mesenchymal stem cells protect against ischaemia-reperfusion-induced acute and chronic kidney injury. Nephrol Dial Transplant 2011;26:1474-1483.
26. Miguet L, Béchade G, Fornecker L, Zink E, Felden C, Gervais C, Herbrecht R, van Dorsselaer A, Mauvieux L, Sanglier-Cianferani S. Proteomic analysis of malignant B-cell derived microparticles reveals CD148 as a potentially useful antigenic biomarker for mantle cell lymphoma diagnosis. J. Proteome Res 2009;8:3346-3354.
27. Fleitas T, Martínez-Sales V, Vila V, Reganon E, Mesado D, Martín M, Gómez-Codina J, Montalar J, Reynés G. Circulating endothelial cells and microparticles as prognostic markers in advanced non-small cell lung cancer. PLoS One 2012;7:e47365.
28. Baran J, Baj-Krzyworzeka M, Weglarczyk K, Szatanek R, Zembala M, Barbasz J, Czupryna A, Szczepanik A, Zembala M. Circulating tumour-derived microvesicles in plasma of gastric cancer patients. Cancer Immunol Immunother CII 2010;59:841-850.
29. Angelillo-Scherrer A. Leukocyte-derived microparticles in vascular homeostasis. Circ Res 2012;110:356-369.
30. Grange C, Tapparo M, Collino F, Vitillo L, Damasco C, Deregibus MC, Tetta C, Bussolati B, Camussi G. Microvesicles released from human renal cancer stem cells stimulate angiogenesis and formation of lung premetastatic niche. Cancer Res 2011;71:5346-5356.
31. Momen-Heravi F, Balaj L, Alian S, Tigges J, Toxavidis V, Ericsson M, Distel RJ, Ivanov AR, Skog J, Kuo WP. Alternative methods for characterization of extracellular vesicles. Front Physiol 2012;3:354. [CrossRef][10.3389/fphys.2012.00354]
32. Graves LE, Ariztia EV, Navari JR, Matzel HJ, Stack MS, Fishman DA. Proinvasive properties of ovarian cancer ascites-derived membrane vesicles. Cancer Res 2004;64:7045-7049.
33. Van Doormaal FF, Kleinjan A, Di Nisio M, Büller HR, Nieuwl R. Cell-derived microvesicles and cancer. Neth J Med 2009;67:266-273.
34. Sinning J-M, Losch J, Walenta K, Böhm M, Nickenig G, Werner N. Circulating CD31+/annexin V+ microparticles correlate with cardiovascular outcomes. Eur Heart J 2011;32:2034-2041.
35. Bruno S, Grange C, Collino F, Deregibus MC, Cantaluppi V, Biancone L, Tetta C, Camussi G. Microvesicles derived from mesenchymal stem cells enhance survival in a lethal model of acute kidney injury. PloS One 2012;7:e33115.
36. Bruno S, Collino F, Deregibus MC, Grange C, Tetta C, Camussi G. Microvesicles derived from human bone marrow mesenchymal stem cells inhibit tumor growth. Stem Cells Dev 2013;22:758-771.
37. Sun D, Zhuang X, Xiang X, Liu Y, Zhang S, Liu C, Barnes S, Grizzle W, Miller D, Zhang H-G. A novel nanoparticle drug delivery system: The anti-inflammatory activity of curcumin is enhanced when encapsulated in exosomes. Mol Ther 2010;18:1606-1614.
38. El Andaloussi S, Mäger I, Breakefield XO, Wood MJA. Extracellular vesicles: Biology and emerging therapeutic opportunities. Nat Rev Drug Discov 2013;12:347-357.
39. Tilley RE, Holscher T, Belani R, Nieva J, Mackman N. Tissue factor activity is increased in a combined platelet and microparticle sample from cancer Patients. Thromb Res 2008;122:604-609.
40. Rood IM, Deegens JKJ, Merchant ML, Tamboer WPM, Wilkey DW, Wetzels JFM, Klein JB. Comparison of three methods for isolation of urinary microvesicles to identify biomarkers of nephrotic syndrome. Kidney Int 2010;78:810-816.
41. Peramo A, Diaz JA. Physical characterization of mouse deep vein thrombosis derived microparticles by differential filtration with nanopore filters. Membranes 2012;2:1-15.
42. Van der Pol E, Hoekstra AG, Sturk A, Otto C, van Leeuwen TG, Nieuwl R. Optical and non-optical methods for detection and characterization of microparticles and exosomes. J Thromb Haemost 2010;8:2596-2607.
43. Yuana Y, Bertina RM, Osanto S. Pre-analytical and analytical issues in the analysis of blood microparticles. Thromb Haemost 2011;105:396-408.
44. György B, Szabó TG, Pásztói M, Pál Z, Misják P, Aradi B, László V, Pállinger É, Pap E, Kittel Á, et al. Membrane vesicles, current state-of-the-art: Emerging role of extracellular vesicles. Cell Mol Life Sci 2011;68:2667-2688.
45. Lawrie AS, Albanyan A, Cardigan RA, Mackie IJ, Harrison P. Microparticle sizing by dynamic light scattering in fresh-frozen plasma. Vox Sang 2009;96:206-212.
46. Miguet L, Sanglier S, Schaeffer C, Potier N, Mauvieux L, Van Dorsselaer A. Microparticles: A new tool for plasma membrane sub-cellular proteomic. Subcell Biochem 2007;43:21-34.
47. Smalley DM, Root KE, Cho H, Ross MM. Ley K. Proteomic discovery of 21 proteins expressed in human plasma-derived but not platelet-derived microparticles. Thromb Haemost 2007;97:67-80.
48. Lacroix R, Robert S, Poncelet P, Dignat-George F. Overcoming limitations of microparticle measurement by flow cytometry. Semin Thromb Hemost 2010;36:807-818.
49. Mobarrez F, Antovic J, Egberg N, Hansson M, Jörneskog G, Hultenby K, Wallén H. A multicolor flow cytometric assay for measurement of platelet-derived microparticles. Thromb Res 2010;125:e110-e116.
50. Van der Pol E, van Gemert MJC, Sturk A, Nieuwl R, van Leeuwen TG. Single vs. swarm detection of microparticles and exosomes by flow cytometry. J Thromb Haemost 2012;10:919-930.
51. Hexley P, Rismiller KP, Robinson CT, Babcock GF. Protocol standardization reveals MV correlation to healthy donor BMI. Exosomes Microvesicles 2014;2:2.
52. Shet AS, Aras O, Gupta K, Hass MJ, Rausch DJ, Saba N, Koopmeiners L, Key NS, Hebbel RP. Sickle blood contains tissue factor-positive microparticles derived from endothelial cells and monocytes. Blood 2003;102:2678-2683.
53. Connor DE, Exner T, Ma DDF, Joseph JE. The majority of circulating platelet-derived microparticles fail to bind annexin V, lack phospholipid-dependent procoagulant activity and demonstrate greater expression of glycoprotein ib. Thromb Haemost 2010;103:1044-1052.
54. Montoro-García S, Shantsila E, Orenes-Piñero E, Lozano ML, Lip GYH. An innovative flow cytometric approach for small-size platelet microparticles: Influence of calcium. Thromb Haemost 2012;108:373-383.
55. György B, Módos K, Pállinger É, Pálóczi K, Pásztói M, Misják P, Deli MA, Sipos Á, Szalai A, Voszka I, et al. Detection and isolation of cell-derived microparticles are compromised by protein complexes resulting from shared biophysical parameters. Blood 2011;117:e39-e48.
56. György B, Szabó TG, Turiák L, Wright M, Herczeg P, Lédeczi Z, Kittel Á, Polgár A, Tóth K, Dérfalvi B, et al. Improved flow cytometric assessment reveals distinct microvesicle (cell-derived microparticle) signatures in joint diseases. PLoS One 2012;7:e49726.
57. György B, Pasztoi M, Buzas EI. Response: Systematic use of triton lysis as a control for microvesicle labeling. Blood 2012;119:2175-2176.
58. Trummer A, De Rop C, Tiede A, Ganser A, Eisert R. Isotype controls in phenotyping and quantification of microparticles: A major source of error and how to evade it. Thromb Res 2008;122:691-700.
59. Dey-Hazra E, Hertel B, Kirsch T, Woywodt A, Lovric S, Haller H, Haubitz M, Erdbruegger U. Detection of circulating microparticles by flow cytometry: Influence of centrifugation, filtration of buffer, and freezing. Vasc Health Risk Manag 2010;6:1125-1133.
60. Jayachandran M, Miller VM, Heit JA, Owen WG. Methodology for isolation, identification and characterization of microvesicles in peripheral blood. J Immunol Methods 2012;375:207-214.
61. Witwer KW, Buzas EI, Bemis LT, Bora A, Lasser C, Lotvall J, Nolte-'t Hoen EN, Piper MG, Sivaraman S, Skog J, et al. Standardization of sample collection, isolation and analysis methods in extracellular vesicle research. J Extracell Vesicles 2013;2. Available at:. http://www.ncbi.nlm.nih.gov/pmc/articles/PMC3760646/. Accessed March 11, 2014.
62. Shah MD, Bergeron AL, Dong J-F, López JA. Flow cytometric measurement of microparticles: Pitfalls and protocol modifications. Platelets 2008;19:365-372.
63. Ayers L, Kohler M, Harrison P, Sargent I, Dragovic R, Schaap M, Nieuwl R, Brooks SA, Ferry B. Measurement of circulating cell-derived microparticles by flow cytometry: Sources of variability within the assay. Thromb Res 2011;127:370-377.
64. Lacroix R, Judicone C, Mooberry M, Boucekine M, Key NS, Dignat-George F, The ISTH SSC Workshop. Standardization of pre-analytical variables in plasma microparticle determination: Results of the International Society on Thrombosis and Haemostasis SSC Collaborative workshop. J Thromb Haemost 2013;11:1190-1193.
65. Lacroix J, Hébert P, Fergusson D, Tinmouth A, Blajchman MA, Callum J, Cook D, Marshall JC, McIntyre L, Turgeon AF, ABLE Study group. The age of blood evaluation (ABLE) randomized controlled trial: Study design. Transfus Med Rev 2011;25:197-205.
66. Shet AS. Characterizing blood microparticles: Technical aspects and challenges. Vasc Health Risk Manag 2008;4:769-774.
67. Orozco AF, Lewis DE. Flow cytometric analysis of circulating microparticles in plasma. Cytometry A 2010;77A:502-514.
68. Danesh A, Inglis HC, Jackman RP, Wu S, Deng X, Muench MO, Heitman JW, Norris PJ. Exosomes from red blood cell units bind to monocytes and induce proinflammatory cytokines, boosting T-cell responses in vitro. Blood 2014;123:687-696.
69. Aass HCD, Øvstebø R, Trøseid A-MS, Kierulf P, Berg JP, Henriksson CE. Fluorescent particles in the antibody solution result in false TF- and CD14-positive microparticles in flow cytometric analysis. Cytometry A 2011;79A:990-999.
70. Van der Vlist EJ, Nolte-'t Hoen ENM, Stoorvogel W, Arkesteijn GJA, Wauben MHM. Fluorescent labeling of nano-sized vesicles released by cells and subsequent quantitative and qualitative analysis by high-resolution flow cytometry. Nat Protoc 2012;7:1311-1326.
71. Amabile N, Renard JM, Caussin C, Boulanger CM. Circulating immune complexes do not affect microparticle flow cytometry analysis in acute coronary syndrome. Blood 2012;119:2174-2175. Available at: http://bloodjournal.hematologylibrary.org/content/119/9/2174.full.
72. Gelderman MP, Simak J. Flow cytometric analysis of cell membrane microparticles. In: Thompson JD, Ueffing M, Schaeffer-Reiss C, editors. Funct. Proteomics, Vol. 484. Totowa, NJ: Humana Press; 2008. pp 79-93. Available at: http://www.springerprotocols.com/Abstract/doi/10.1007/978-1-59745-398-1_6. Accessed August 22, 2013.