A novel 3D heterotypic spheroid model for studying extracellular vesicle-mediated tumour and immune cell communication

Biochemical and Biophysical Research Communications

Volumn 495, Issue 2, 2018, Pages 1930-1935

  Sadovska, Lilite ^a   Zandberga, Elīna ^a   Sagini, Krizia ^b   Jēkabsons, Kaspars ^c   Riekstiņa, Una ^c   Kalniņa, Zane ^a   Llorente, Alicia ^b   Linē, Aija ^a  

^a LATVIAN BIOMEDICAL RESEARCH AND STUDY CENTRE   (Latvia)

^b OSLO UNIVERSITY HOSPITAL   (Norway)

^c UNIVERSITY OF LATVIA   (Latvia)

Author keywords

3D heterotypic spheroids; Extracellular vesicles; Immune cells; Macropinocytosis; Prostate cancer; Uptake

Indexed keywords

CD63 ANTIGEN; GREEN FLUORESCENT PROTEIN;

ARTICLE; B LYMPHOCYTE; BIOLOGICAL MODEL; CD3+ T LYMPHOCYTE; CELL COMMUNICATION; CELL SURFACE; CELL TRANSFER; CONTROLLED STUDY; EXOSOME; FLOW CYTOMETRY; FLUORESCENCE IMAGING; HUMAN; HUMAN CELL; IMMUNOCOMPETENT CELL; MALE; PC-3 [HUMAN PROSTATE CARCINOMA] CELL LINE; PERIPHERAL BLOOD MONONUCLEAR CELL; PINOCYTOSIS; PRIORITY JOURNAL; TUMOR CELL CULTURE; TUMOR MICROENVIRONMENT;

EID: 85039431587     PISSN: 0006291X     EISSN: 10902104     Source Type: Journal    
DOI: 10.1016/j.bbrc.2017.12.072     Document Type: Article

References (32)

1. Yanez-Mo, M., Siljander, P.R., Andreu, Z., et al. Biological properties of extracellular vesicles and their physiological functions. J. Extracell. Vesicles, 4, 2015, 27066.
2. Sadovska, L., Santos, C.B., Kalniņa, Z., Line, A., Biodistribution, uptake and effects caused by cancer-derived extracellular vesicles. J. Circulating Biomarkers, 2015, 1.
3. Whiteside, T.L., Tumor-derived exosomes and their role in cancer progression. Adv. Clin. Chem. 74 (2016), 103–141.
4. Taylor, D.D., Gercel-Taylor, C., Tumour-derived exosomes and their role in cancer-associated T-cell signalling defects. Br. J. Canc. 92 (2005), 305–311.
5. Yang, L., Wu, X., Wang, D., Luo, C., Chen, L., Renal carcinoma cell-derived exosomes induce human immortalized line of Jurkat T lymphocyte apoptosis in vitro. Urol. Int. 91 (2013), 363–369.
6. Lundholm, M., Schroder, M., Nagaeva, O., et al. Prostate tumor-derived exosomes down-regulate NKG2D expression on natural killer cells and CD8+ T cells: mechanism of immune evasion. PLos One, 9, 2014, e108925.
7. Muller, L., Mitsuhashi, M., Simms, P., Gooding, W.E., Whiteside, T.L., Tumor-derived exosomes regulate expression of immune function-related genes in human T cell subsets. Sci. Rep., 6, 2016, 20254.
8. Szajnik, M., Czystowska, M., Szczepanski, M.J., Mandapathil, M., Whiteside, T.L., Tumor-derived microvesicles induce, expand and up-regulate biological activities of human regulatory T cells (Treg). PLos One, 5, 2010, e11469.
9. Yamada, N., Kuranaga, Y., Kumazaki, M., et al. Colorectal cancer cell-derived extracellular vesicles induce phenotypic alteration of T cells into tumor-growth supporting cells with transforming growth factor-β1-mediated suppression. Oncotarget 7 (2016), 27033–27043.
10. Clayton, A., Mitchell, J.P., Court, J., Mason, M.D., Tabi, Z., Human tumor-derived exosomes selectively impair lymphocyte responses to interleukin-2. Cancer. Res. 67 (2007), 7458–7466.
11. Muller, L., Simms, P., Hong, C.S., et al. Human tumor-derived exosomes (TEX) regulate Treg functions via cell surface signaling rather than uptake mechanisms. OncoImmunology, 6, 2017, e1261243.
12. Marton, A., Vizler, C., Kusz, E., et al. Melanoma cell-derived exosomes alter macrophage and dendritic cell functions in vitro. Immunol. Lett. 148 (2012), 34–38.
13. de Vrij, J., Maas, S.L., Kwappenberg, K.M., et al. Glioblastoma-derived extracellular vesicles modify the phenotype of monocytic cells. Int J Cancer 137 (2015), 1630–1642.
14. Gutzeit, C., Nagy, N., Gentile, M., et al. Exosomes derived from Burkitt's lymphoma cell lines induce proliferation, differentiation, and class-switch recombination in B cells. J. Immunol. 192 (2014), 5852–5862.
15. Hessvik, N.P., Overbye, A., Brech, A., et al. PIKfyve inhibition increases exosome release and induces secretory autophagy. Cell. Mol. Life Sci. 73 (2016), 4717–4737.
16. Roberts-Dalton, H.D., Cocks, A., Falcon-Perez, J.M., et al. Fluorescence labelling of extracellular vesicles using a novel thiol-based strategy for quantitative analysis of cellular delivery and intracellular traffic. Nanoscale 9 (2017), 13693–13706.
17. Barres, C., Blanc, L., Bette-Bobillo, P., et al. Galectin-5 is bound onto the surface of rat reticulocyte exosomes and modulates vesicle uptake by macrophages. Blood 115 (2010), 696–705.
18. Sagar, G., Sah, R.P., Javeed, N., et al. Pathogenesis of pancreatic cancer exosome-induced lipolysis in adipose tissue. Gut 65 (2016), 1165–1174.
19. Hellwinkel, J.E., Redzic, J.S., Harland, T.A., et al. Glioma-derived extracellular vesicles selectively suppress immune responses. Neuro Oncol. 18 (2016), 497–506.
20. Caponnetto, F., Manini, I., Skrap, M., et al. Size-dependent cellular uptake of exosomes. Nanomedicine 13 (2017), 1011–1020.
21. Pols, M.S., Klumperman, J., Trafficking and function of the tetraspanin CD63. Exp. Cell Res. 315 (2009), 1584–1592.
22. Kowal, J., Arras, G., Colombo, M., et al. Proteomic comparison defines novel markers to characterize heterogeneous populations of extracellular vesicle subtypes. Proc. Nat. Acad. Sci. USA 113 (2016), E968–E977.
23. Herter, S., Morra, L., Schlenker, R., et al. A novel three-dimensional heterotypic spheroid model for the assessment of the activity of cancer immunotherapy agents. Canc. Immunol. Immunother.: CII 66 (2017), 129–140.
24. Kim, H., Phung, Y., Ho, M., Changes in global gene expression associated with 3D structure of tumors: an ex vivo matrix-free mesothelioma spheroid model. PLos One, 7, 2012, e39556.
25. Hirschhaeuser, F., Menne, H., Dittfeld, C., et al. Multicellular tumor spheroids: an underestimated tool is catching up again. J. Biotechnol. 148 (2010), 3–15.
26. Panayiotou, H., Orsi, N.M., Thygesen, H.H., et al. The prognostic significance of tumour-stroma ratio in endometrial carcinoma. BMC Cancer., 15, 2015, 955.
27. Wu, J., Liang, C., Chen, M., Su, W., Association between tumor-stroma ratio and prognosis in solid tumor patients: a systematic review and meta-analysis. Oncotarget 7 (2016), 68954–68965.
28. Koivusalo, M., Welch, C., Hayashi, H., et al. Amiloride inhibits macropinocytosis by lowering submembranous pH and preventing Rac1 and Cdc42 signaling. J. Cell Biol. 188 (2010), 547–563.
29. Fitzner, D., Schnaars, M., van Rossum, D., et al. Selective transfer of exosomes from oligodendrocytes to microglia by macropinocytosis. J. Cell Sci. 124 (2011), 447–458.
30. Costa Verdera, H., Gitz-Francois, J.J., Schiffelers, R.M., Vader, P., Cellular uptake of extracellular vesicles is mediated by clathrin-independent endocytosis and macropinocytosis. J. Contr. Release 266 (2017), 100–108.
31. Mulcahy, L.A., Pink, R.C., Carter, D.R., Routes and mechanisms of extracellular vesicle uptake. J. Extracell. Vesicles, 3, 2014.
32. Nakase, I., Kobayashi, N.B., Takatani-Nakase, T., Yoshida, T., Active macropinocytosis induction by stimulation of epidermal growth factor receptor and oncogenic Ras expression potentiates cellular uptake efficacy of exosomes. Sci. Rep., 5, 2015, 10300.