Melanoma affects the composition of blood cell-derived extracellular vesicles

Frontiers in Immunology

Volumn 7, Issue JUL, 2016, Pages

  Koliha, Nina ^a   Heider, Ute ^a   Ozimkowski, Tobias ^a   Wiemann, Martin ^b   Bosio, Andreas ^a   Wild, Stefan ^a  

^a MILTENYI BIOTEC GMBH   (Germany)

^b IBE RandD GGmbH   (Germany)

Author keywords

B cells; Exosome; Flow cytometry; MoDC; Nanoparticle tracking analysis; Platelets

Indexed keywords

CELL SURFACE PROTEIN;

ARTICLE; BLOOD SAMPLING; CELL DIFFERENTIATION; CELL ISOLATION; CELL MATURATION; CELL SELECTION; CELL STIMULATION; CELL SUBPOPULATION; CONTROLLED STUDY; EXOSOME; FLOW CYTOMETRY; HUMAN; HUMAN CELL; IMMUNE RESPONSE; LEUKAPHERESIS; MELANOMA; PHOTON CORRELATION SPECTROSCOPY; SCANNING ELECTRON MICROSCOPY; SIGNAL TRANSDUCTION;

EID: 84983296871     PISSN: None     EISSN: 16643224     Source Type: Journal    
DOI: 10.3389/fimmu.2016.00282     Document Type: Article

References (66)

1. Thery C, Ostrowski M, Segura E. Membrane vesicles as conveyors of immune responses. Nat Rev (2009) 9:581-93. doi:10.1038/nri2567
2. Thery C, Zitvogel L, Amigorena S. Exosomes: composition, biogenesis and function. Nat Rev (2002) 2:569-79. doi:10.1038/nri855
3. Villarroya-Beltri C, Baixauli F, Gutierrez-Vazquez C, Sanchez-Madrid F, Mittelbrunn M. Sorting it out: regulation of exosome loading. Semin Cancer Biol (2014) 28:3-13. doi:10.1016/j.semcancer.2014.04.009
4. Escola JM, Kleijmeer MJ, Stoorvogel W, Griffith JM, Yoshie O, Geuze HJ. Selective enrichment of tetraspan proteins on the internal vesicles of multivesicular endosomes and on exosomes secreted by human B-lymphocytes. J Biol Chem (1998) 273:20121-7. doi:10.1074/jbc.273.32.20121
5. Mulcahy LA, Pink RC, Carter DR. Routes and mechanisms of extracellular vesicle uptake. J Extracell Vesicles (2014) 3. doi:10.3402/jev.v3.24641
6. Simpson RJ, Lim JW, Moritz RL, Mathivanan S. Exosomes: proteomic insights and diagnostic potential. Expert Rev Proteomics (2009) 6:267-83. doi:10.1586/epr.09.17
7. Logozzi M, De Milito A, Lugini L, Borghi M, Calabro L, Spada M, et al. High levels of exosomes expressing CD63 and caveolin-1 in plasma of melanoma patients. PLoS One (2009) 4:e5219. doi:10.1371/journal.pone.0005219
8. Valenti R, Huber V, Filipazzi P, Pilla L, Sovena G, Villa A, et al. Human tumor-released microvesicles promote the differentiation of myeloid cells with transforming growth factor-beta-mediated suppressive activity on T lymphocytes. Cancer Res (2006) 66:9290-8. doi:10.1158/0008-5472.CAN-06-1819
9. Ekstrom EJ, Bergenfelz C, von Bulow V, Serifler F, Carlemalm E, Jonsson G, et al. WNT5A induces release of exosomes containing pro-angiogenic and immunosuppressive factors from malignant melanoma cells. Mol Cancer (2014) 13:88. doi:10.1186/1476-4598-13-88
10. Clayton A, Mitchell JP, Court J, Linnane S, Mason MD, Tabi Z. Human tumor-derived exosomes down-modulate NKG2D expression. J Immunol (2008) 180:7249-58. doi:10.4049/jimmunol.180.11.7249
11. Liu C, Yu S, Zinn K, Wang J, Zhang L, Jia Y, et al. Murine mammary carcinoma exosomes promote tumor growth by suppression of NK cell function. J Immunol (2006) 176:1375-85. doi:10.4049/jimmunol.176.3.1375
12. Andreola G, Rivoltini L, Castelli C, Huber V, Perego P, Deho P, et al. Induction of lymphocyte apoptosis by tumor cell secretion of FasL-bearing microvesicles. J Exp Med (2002) 195:1303-16. doi:10.1084/jem.20011624
13. Huber V, Fais S, Iero M, Lugini L, Canese P, Squarcina P, et al. Human colorectal cancer cells induce T-cell death through release of proapoptotic microvesicles: role in immune escape. Gastroenterology (2005) 128:1796-804. doi:10.1053/j.gastro.2005.03.045
14. Klibi J, Niki T, Riedel A, Pioche-Durieu C, Souquere S, Rubinstein E, et al. Blood diffusion and Th1-suppressive effects of galectin-9-containing exosomes released by Epstein-Barr virus-infected nasopharyngeal carcinoma cells. Blood (2009) 113:1957-66. doi:10.1182/blood-2008-02-142596
15. Andre F, Schartz NE, Movassagh M, Flament C, Pautier P, Morice P, et al. Malignant effusions and immunogenic tumour-derived exosomes. Lancet (2002) 360:295-305. doi:10.1016/S0140-6736(02)09552-1
16. Wolfers J, Lozier A, Raposo G, Regnault A, Thery C, Masurier C, et al. Tumor-derived exosomes are a source of shared tumor rejection antigens for CTL cross-priming. Nat Med (2001) 7:297-303. doi:10.1038/85438
17. Caby MP, Lankar D, Vincendeau-Scherrer C, Raposo G, Bonnerot C. Exosomal-like vesicles are present in human blood plasma. Int Immunol (2005) 17:879-87. doi:10.1093/intimm/dxh267
18. Ren Y, Yang J, Xie R, Gao L, Yang Y, Fan H, et al. Exosomal-like vesicles with immune-modulatory features are present in human plasma and can induce CD4+ T-cell apoptosis in vitro. Transfusion (2011) 51:1002-11. doi:10.1111/j.1537-2995.2010.02909.x
19. Arita S, Baba E, Shibata Y, Niiro H, Shimoda S, Isobe T, et al. B cell activation regulates exosomal HLA production. Eur J Immunol (2008) 38:1423-34. doi:10.1002/eji.200737694
20. Blanchard N, Lankar D, Faure F, Regnault A, Dumont C, Raposo G, et al. TCR activation of human T cells induces the production of exosomes bearing the TCR/CD3/zeta complex. J Immunol (2002) 168:3235-41. doi:10.4049/jimmunol.168.7.3235
21. van der Vlist EJ, Arkesteijn GJ, van de Lest CH, Stoorvogel W, Nolte-'t Hoen EN, Wauben MH. CD4(+) T cell activation promotes the differential release of distinct populations of nanosized vesicles. J Extracell Vesicles (2012) 1. doi:10.3402/jev.v1i0.18364
22. Liu Y, Gu Y, Cao X. The exosomes in tumor immunity. Oncoimmunology (2015) 4:e1027472. doi:10.1080/2162402X.2015.1027472
23. Heijnen HF, Schiel AE, Fijnheer R, Geuze HJ, Sixma JJ. Activated platelets release two types of membrane vesicles: microvesicles by surface shedding and exosomes derived from exocytosis of multivesicular bodies and alpha-granules. Blood (1999) 94:3791-9.
24. Aatonen MT, Ohman T, Nyman TA, Laitinen S, Gronholm M, Siljander PR. Isolation and characterization of platelet-derived extracellular vesicles. J Extracell Vesicles (2014) 3. doi:10.3402/jev.v3.24692
25. Admyre C, Bohle B, Johansson SM, Focke-Tejkl M, Valenta R, Scheynius A, et al. B cell-derived exosomes can present allergen peptides and activate allergen-specific T cells to proliferate and produce TH2-like cytokines. J Allergy Clin Immunol (2007) 120:1418-24. doi:10.1016/j.jaci.2007.06.040
26. Clayton A, Court J, Navabi H, Adams M, Mason MD, Hobot JA, et al. Analysis of antigen presenting cell derived exosomes, based on immuno-magnetic isolation and flow cytometry. J Immunol Methods (2001) 247:163-74. doi:10.1016/S0022-1759(00)00321-5
27. Oksvold MP, Kullmann A, Forfang L, Kierulf B, Li M, Brech A, et al. Expression of B-cell surface antigens in subpopulations of exosomes released from B-cell lymphoma cells. Clin Ther (2014) 36:847-62.e1. doi:10.1016/j.clinthera.2014.05.010
28. Raposo G, Nijman HW, Stoorvogel W, Liejendekker R, Harding CV, Melief CJ, et al. B lymphocytes secrete antigen-presenting vesicles. J Exp Med (1996) 183:1161-72. doi:10.1084/jem.183.3.1161
29. Johansson SM, Admyre C, Scheynius A, Gabrielsson S. Different types of in vitro generated human monocyte-derived dendritic cells release exosomes with distinct phenotypes. Immunology (2008) 123:491-9. doi:10.1111/j.1365-2567.2007.02714.x
30. Lamparski HG, Metha-Damani A, Yao JY, Patel S, Hsu DH, Ruegg C, et al. Production and characterization of clinical grade exosomes derived from dendritic cells. J Immunol Methods (2002) 270:211-26. doi:10.1016/S0022-1759(02)00330-7
31. Munich S, Sobo-Vujanovic A, Buchser WJ, Beer-Stolz D, Vujanovic NL. Dendritic cell exosomes directly kill tumor cells and activate natural killer cells via TNF superfamily ligands. Oncoimmunology (2012) 1:1074-83. doi:10.4161/onci.20897
32. Koliha N, Wiencek Y, Heider U, Jungst C, Kladt N, Krauthauser S I, et al. A novel multiplex bead-based platform highlights the diversity of extracellular vesicles. J Extracell Vesicles (2016) 5:29975. doi:10.3402/jev.v5.29975
33. Oikawa Y, Hansson J, Sasaki T, Rousselle P, Domogatskaya A, Rodin S, et al. Melanoma cells produce multiple laminin isoforms and strongly migrate on alpha5 laminin(s) via several integrin receptors. Exp Cell Res (2011) 317:1119-33. doi:10.1016/j.yexcr.2010.12.019
34. Pluschke G, Vanek M, Evans A, Dittmar T, Schmid P, Itin P, et al. Molecular cloning of a human melanoma-associated chondroitin sulfate proteoglycan. Proc Natl Acad Sci U S A (1996) 93:9710-5. doi:10.1073/pnas.93.18.9710
35. Satyamoorthy K, Muyrers J, Meier F, Patel D, Herlyn M. Mel-CAM-specific genetic suppressor elements inhibit melanoma growth and invasion through loss of gap junctional communication. Oncogene (2001) 20:4676-84. doi:10.1038/sj.onc.1204616
36. Leong HS, Podor TJ, Manocha B, Lewis JD. Validation of flow cytometric detection of platelet microparticles and liposomes by atomic force microscopy. J Thromb Haemost (2011) 9:2466-76. doi:10.1111/j.1538-7836.2011.04528.x
37. Liu X, Sempere LF, Galimberti F, Freemantle SJ, Black C, Dragnev KH, et al. Uncovering growth-suppressive MicroRNAs in lung cancer. Clin Cancer Res (2009) 15:1177-83. doi:10.1158/1078-0432.CCR-08-1355
38. Saeed AI, Sharov V, White J, Li J, Liang W, Bhagabati N, et al. TM4: a free, open-source system for microarray data management and analysis. Biotechniques (2003) 34:374-8.
39. Robbins PD, Morelli AE. Regulation of immune responses by extracellular vesicles. Nat Rev (2014) 14:195-208. doi:10.1038/nri3622
40. Yanez-Mo M, Siljander PR, Andreu Z, Zavec AB, Borras FE, Buzas EI, et al. Biological properties of extracellular vesicles and their physiological functions. J Extracell Vesicles (2015) 4:27066. doi:10.3402/jev.v4.27066
41. Jorgensen M, Baek R, Pedersen S, Sondergaard EK, Kristensen SR, Varming K. Extracellular Vesicle (EV) Array: microarray capturing of exosomes and other extracellular vesicles for multiplexed phenotyping. J Extracell Vesicles (2013) 2. doi:10.3402/jev.v2i0.20920
42. Berditchevski F, Zutter MM, Hemler ME. Characterization of novel complexes on the cell surface between integrins and proteins with 4 transmembrane domains (TM4 proteins). Mol Biol Cell (1996) 7:193-207. doi:10.1091/mbc.7.2.193
43. Gutierrez-Lopez MD, Ovalle S, Yanez-Mo M, Sanchez-Sanchez N, Rubinstein E, Olmo N, et al. A functionally relevant conformational epitope on the CD9 tetraspanin depends on the association with activated beta1 integrin. J Biol Chem (2003) 278:208-18. doi:10.1074/jbc.M207805200
44. Rubinstein E, Le Naour F, Lagaudriere-Gesbert C, Billard M, Conjeaud H, Boucheix C. CD9, CD63, CD81, and CD82 are components of a surface tetraspan network connected to HLA-DR and VLA integrins. Eur J Immunol (1996) 26:2657-65. doi:10.1002/eji.1830261117
45. Clayton A, Turkes A, Dewitt S, Steadman R, Mason MD, Hallett MB. Adhesion and signaling by B cell-derived exosomes: the role of integrins. FASEB J (2004) 18:977-9. doi:10.1096/fj.03-1094fje
46. Hakulinen J, Sankkila L, Sugiyama N, Lehti K, Keski-Oja J. Secretion of active membrane type 1 matrix metalloproteinase (MMP-14) into extracellular space in microvesicular exosomes. J Cell Biochem (2008) 105:1211-8. doi:10.1002/jcb.21923
47. Rieu S, Geminard C, Rabesandratana H, Sainte-Marie J, Vidal M. Exosomes released during reticulocyte maturation bind to fibronectin via integrin alpha4beta1. Eur J Biochem (2000) 267:583-90. doi:10.1046/j.1432-1327.2000.01036.x
48. Wubbolts R, Leckie RS, Veenhuizen PT, Schwarzmann G, Mobius W, Hoernschemeyer J, et al. Proteomic and biochemical analyses of human B cell-derived exosomes. Potential implications for their function and multivesicular body formation. J Biol Chem (2003) 278:10963-72. doi:10.1074/jbc.M207550200
49. de Gassart A, Geminard C, Fevrier B, Raposo G, Vidal M. Lipid raft-associated protein sorting in exosomes. Blood (2003) 102:4336-44. doi:10.1182/blood-2003-03-0871
50. Jorgensen MM, Baek R, Varming K. Potentials and capabilities of the Extracellular Vesicle (EV) Array. J Extracell Vesicles (2015) 4:26048. doi:10.3402/jev.v4.26048
51. Muntasell A, Berger AC, Roche PA. T cell-induced secretion of MHC class II-peptide complexes on B cell exosomes. EMBO J (2007) 26:4263-72. doi:10.1038/sj.emboj.7601842
52. Anolik J, Looney RJ, Bottaro A, Sanz I, Young F. Down-regulation of CD20 on B cells upon CD40 activation. Eur J Immunol (2003) 33:2398-409. doi:10.1002/eji.200323515
53. Rickert RC. Regulation of B lymphocyte activation by complement C3 and the B cell coreceptor complex. Curr Opin Immunol (2005) 17:237-43. doi:10.1016/j.coi.2005.03.001
54. Arva E, Andersson B. Kinetics of cytokine release and expression of lymphocyte cell-surface activation markers after in vitro stimulation of human peripheral blood mononuclear cells with Streptococcus pneumoniae. Scand J Immunol (1999) 49:237-43. doi:10.1046/j.1365-3083.1999.00481.x
55. Liu K, Nussenzweig MC. Origin and development of dendritic cells. Immunol Rev (2010) 234:45-54. doi:10.1111/j.0105-2896.2009.00879.x
56. Soruri A, Zwirner J. Dendritic cells: limited potential in immunotherapy. Int J Biochem Cell Biol (2005) 37:241-5. doi:10.1016/j.biocel.2004.07.003
57. Janowska-Wieczorek A, Wysoczynski M, Kijowski J, Marquez-Curtis L, Machalinski B, Ratajczak J, et al. Microvesicles derived from activated platelets induce metastasis and angiogenesis in lung cancer. Int J Cancer (2005) 113:752-60. doi:10.1002/ijc.20657
58. Janowska-Wieczorek A, Marquez-Curtis LA, Wysoczynski M, Ratajczak MZ. Enhancing effect of platelet-derived microvesicles on the invasive potential of breast cancer cells. Transfusion (2006) 46:1199-209. doi:10.1111/j.1537-2995.2006.00871.x
59. Lugini L, Cecchetti S, Huber V, Luciani F, Macchia G, Spadaro F, et al. Immune surveillance properties of human NK cell-derived exosomes. J Immunol (2012) 189:2833-42. doi:10.4049/jimmunol.1101988
60. Mittelbrunn M, Gutierrez-Vazquez C, Villarroya-Beltri C, Gonzalez S, Sanchez-Cabo F, Gonzalez MA, et al. Unidirectional transfer of microRNA-loaded exosomes from T cells to antigen-presenting cells. Nat Commun (2011) 2:282. doi:10.1038/ncomms1285
61. Yuana Y, Boing AN, Grootemaat AE, van der Pol E, Hau CM, Cizmar P, et al. Handling and storage of human body fluids for analysis of extracellular vesicles. J Extracell Vesicles (2015) 4:29260. doi:10.3402/jev.v4.29260
62. Mullier F, Bailly N, Chatelain C, Chatelain B, Dogne JM. Pre-analytical issues in the measurement of circulating microparticles: current recommendations and pending questions. J Thromb Haemost (2013) 11:693-6. doi:10.1111/jth.12171
63. Witwer KW, Buzas EI, Bemis LT, Bora A, Lasser C, Lotvall J, et al. Standardization of sample collection, isolation and analysis methods in extracellular vesicle research. J Extracell Vesicles (2013) 2. doi:10.3402/jev.v2i0.20360
64. Rak J. Extracellular vesicles-biomarkers and effectors of the cellular interactome in cancer. Front Pharmacol (2013) 4:21. doi:10.3389/fphar.2013.00021
65. Rosdahl I, Rorsman H. An estimate of the melanocyte mass in humans. J Invest Dermatol (1983) 81:278-81. doi:10.1111/1523-1747.ep12518318
66. Laresche C, Pelletier F, Garnache-Ottou F, Lihoreau T, Biichle S, Mourey G, et al. Increased levels of circulating microparticles are associated with increased procoagulant activity in patients with cutaneous malignant melanoma. J Invest Dermatol (2014) 134:176-82. doi:10.1038/jid.2013.288