In vitro immunotoxicity assessment of culture-derived extracellular vesicles in human monocytes

References

• Alvarez-Erviti L, Seow Y, Yin H, Betts C, Lakhal S, Wood MJ. 2011. Delivery of siRNA to the mouse brain by systemic injection of targeted exosomes. Nat Biotechnol. 29:341–345.
   PubMed Web of Science ®Google Scholar
• Arimilli S, Damratoski BE, Bombick B, Borgerding MF, Prasad GL. 2012. Evaluation of cytotoxicity of different tobacco product preparations. Regul Toxicol Pharmacol. 64:350–360.
   PubMed Web of Science ®Google Scholar
• Batrakova EV, Kim MS. 2015. Using exosomes, naturally-equipped nanocarriers, for drug delivery. J Contr Rel. 219:396–405.
   PubMed Web of Science ®Google Scholar
• Berenson CS, Kruzel RL, Eberhardt E, Sethi S. 2013. Phagocytic dysfunction of human alveolar macrophages and severity of chronic obstructive pulmonary disease. J Infect Dis. 208: 2036–2045.
   PubMed Web of Science ®Google Scholar
• Chen TS, Arslan F, Yin Y, Tan SS, Lai RC, Choo AB, Padmanabhan J, Lee CN, de Kleijn DP, Lim SK. 2011. Enabling a robust scalable manufacturing process for therapeutic exosomes through oncogenic immortalization of human ESC-derived MSCs. J Transl Med. 9:47.
   PubMed Web of Science ®Google Scholar
• Colombo M, Raposo G, Thery C. 2014. Biogenesis, secretion, and intercellular interactions of exosomes and other extracellular vesicles. Annu Rev Cell Dev Biol. 30:255–289.
   PubMed Web of Science ®Google Scholar
• de Rivero Vaccari JP, Brand F, Adamczak S, Lee SW, Barcena JP, Wang MY, Bullock MR, Dietrich WD, Keane RW. 2016. Exosome-mediated inflammasome signaling after central nervous system injury. J Neurochem. 136(Suppl 1):39–48.
   PubMed Web of Science ®Google Scholar
• DeFife KM, Jenney CR, Colton E, Anderson JM. 1999. Disruption of filamentous actin inhibits human macrophage fusion. FASEB J. 13:823–832.
   PubMed Web of Science ®Google Scholar
• Diler E, Schicht M, Rabung A, Tschernig T, Meier C, Rausch F, Garreis F, Brauer L, Paulsen F. 2014a. The novel surfactant protein SP-H enhances the phagocytosis efficiency of macrophage-like cell lines U937 and MH-S. BMC Res Notes. 7:851.
   PubMedGoogle Scholar
• Diler E, Schwarz M, Nickels R, Menger MD, Beisswenger C, Meier C, Tschernig T. 2014b. Influence of external calcium and thapsigargin on the uptake of polystyrene beads by the macrophage-like cell lines U937 and MH-S. BMC Pharmacol Toxicol. 15:16.
   PubMed Web of Science ®Google Scholar
• Dolovcak S, Waldrop SL, Fitz JG, Kilic G. 2009. 5-Nitro-2-(3-phenylpropylamino)-benzoic acid (NPPB) stimulates cellular ATP release through exocytosis of ATP-enriched vesicles. J Biol Chem. 284:33894–33903.
   PubMed Web of Science ®Google Scholar
• Dovrat S, Caspi M, Zilberberg A, Lahav L, Firsow A, Gur H, Rosin-Arbesfeld R. 2014. 14-3-3 and β-catenin are secreted on extracellular vesicles to activate the oncogenic Wnt pathway. Mol Oncol. 8:894–911.
   PubMed Web of Science ®Google Scholar
• Durocher Y, Perret S, Kamen A. 2002. High-level and high-throughput recombinant protein production by transient transfection of suspension-growing human 293-EBNA1 cells. Nucl Acids Res. 30:E9.
   PubMed Web of Science ®Google Scholar
• El-Andaloussi S, Lee Y, Lakhal-Littleton S, Li J, Seow Y, Gardiner C, Alvarez-Erviti L, Sargent IL, Wood MJ. 2012. Exosome-mediated delivery of siRNA in vitro and in vivo. Nat Protoc. 7:2112–2126.
   PubMed Web of Science ®Google Scholar
• Escrevente C, Keller S, Altevogt P, Costa J. 2011. Interaction and uptake of exosomes by ovarian cancer cells. BMC Cancer. 11:108.
   PubMed Web of Science ®Google Scholar
• Feng D, Zhao WL, Ye YY, Bai XC, Liu RQ, Chang LF, Zhou Q, Sui SF. 2010. Cellular internalization of exosomes occurs through phagocytosis. Traffic. 11:675–687.
   PubMed Web of Science ®Google Scholar
• Ferrara F, Bertelli A, Falchi M. 2005. Evaluation of carnitine, acetylcarnitine and isovaleryl-carnitine on immune function and apoptosis. Drugs Exp Clin Res. 31:109–114.
   PubMedGoogle Scholar
• Galbiati V, Mitjans M, Corsini E. 2010. Present and future of in vitro immunotoxicology in drug development. J Immunotoxicol. 7:255–267.
   PubMed Web of Science ®Google Scholar
• Gao M, Kim YK, Zhang C, Borshch V, Zhou S, Park HS, Jakli A, Lavrentovich OD, Tamba MG, Kohlmeier A, et al. 2014. Direct observation of liquid crystals using cryo-TEM: specimen preparation and low-dose imaging. Microsc Res Tech. 77:754–772.
   PubMed Web of Science ®Google Scholar
• Gennari A, Ban M, Braun A, Casati S, Corsini E, Dastych J, Descotes J, Hartung T, Hooghe-Peters R, House R, et al. 2005. The use of in vitro systems for evaluating immunotoxicity: Report and recommendations of an ECVAM Workshop. J Immunotoxicol. 2:61–83.
   PubMedGoogle Scholar
• Greening DW, Gopal SK, Xu R, Simpson RJ, Chen W. 2015. Exosomes and their roles in immune regulation and cancer. Semin Cell Dev Biol. 40:72–81.
   PubMed Web of Science ®Google Scholar
• Guduric-Fuchs J, O'Connor A, Camp B, O'Neill CL, Medina RJ, Simpson DA. 2012. Selective extracellular vesicle-mediated export of an overlapping set of microRNAs from multiple cell types. BMC Genomics. 13:357.
   PubMed Web of Science ®Google Scholar
• Gyorgy B, Hung ME, Breakefield XO, Leonard JN. 2015. Therapeutic applications of extracellular vesicles: Clinical promise and open questions. Annu Rev Pharmacol Toxicol. 55:439–464.
   PubMed Web of Science ®Google Scholar
• Haney MJ, Klyachko NL, Zhao Y, Gupta R, Plotnikova EG, He Z, Patel T, Piroyan A, Sokolsky M, Kabanov AV, et al. 2015. Exosomes as drug delivery vehicles for Parkinson's disease therapy. J Contr Rel. 207:18–30.
   PubMed Web of Science ®Google Scholar
• Hartung T, Corsini E. 2013. Immunotoxicology: Challenges in the 21st Century and in vitro opportunities. ALTEX. 30:411–426.
   PubMedGoogle Scholar
• Hed J, Hallden G, Johansson SG, Larsson P. 1987. The use of fluorescence quenching in flow cyto-fluorometry to measure the attachment and ingestion phases in phagocytosis in peripheral blood without prior cell separation. J Immunol Meth. 101:119–125.
   PubMed Web of Science ®Google Scholar
• ICH (I.C.O.H). 2011. [Internet]. Pre-clinical Safety Evaluation of Biotechnology-Derived Pharmaceuticals. Bethesda, MD: U.S. Department of Health and Human Services, Food and Drug Administration, Center for Drug Evaluation and Research (CDER) and Center for Biologics Evaluation and Research (CBER), July 1997. Available from: http://www.ich.org/products/guidelines/safety/safety-single/article/preclinical-safety-evaluation-of-biotechnology-derived-pharmaceuticals.html.
   Google Scholar
• Izumi H, Tsuda M, Sato Y, Kosaka N, Ochiya T, Iwamoto H, Namba K, Takeda Y. 2015. Bovine milk exosomes contain microRNA and mRNA and are taken up by human macrophages. J Dairy Sci. 5:2920–2933.
   Web of Science ®Google Scholar
• Jeppesen DK, Hvam ML, Primdahl-Bengtson B, Boysen AT, Whitehead B, Dyrskjot L, Orntoft TF, Howard KA, Ostenfeld MS. 2014. Comparative analysis of discrete exosome fractions obtained by differential centrifugation. J Extracell Ves. 3:25011.
   PubMedGoogle Scholar
• Ji W, Chen X, Ma Y, Hu D, Lu R, Zhou X, Wei L. 2013. Effect of Kruppel-like factor 4 gene silencing on apoptosis and phagocytosis of murine RAW264.7 macrophages. Xi Bao Yu. 29:341–344.
   Google Scholar
• Johnstone RM, Adam M, Hammond JR, Orr L, Turbide C. 1987. Vesicle formation during reticulocyte maturation. Association of plasma membrane activities with released vesicles (exosomes). J Biol Chem. 262:9412–9420.
   PubMed Web of Science ®Google Scholar
• Lai CP, Mardini O, Ericsson M, Prabhakar S, Maguire CA, Chen JW, Tannous BA, Breakefield XO. 2014a. Dynamic biodistribution of extracellular vesicles in vivo using a multimodal imaging reporter. ACS Nano. 8:483–494.
   PubMed Web of Science ®Google Scholar
• Lai FW, Lichty BD, Bowdish DM. 2014b. Microvesicles: Ubiquitous contributors to infection and immunity. J Leukocyte Biol. 2:237–245.
   Google Scholar
• Leclerc L, Boudard D, Pourchez J, Forest V, Sabido O, Bi V, Palle S, Grosseau P, Bernache D, Cottier M. 2010. Quantification of microsized fluorescent particles phagocytosis to a better knowledge of toxicity mechanisms. Inhal Toxicol. 22:1091–1100.
   PubMed Web of Science ®Google Scholar
• Lehmann AK, Sornes S, Halstensen A. 2000. Phagocytosis: Measurement by flow cytometry. J Immunol Meth. 243:229–242.
   PubMed Web of Science ®Google Scholar
• Lessig J, Neu B, Glander HJ, Arnhold J, Reibetanz U. 2011. Phagocytotic competence of differentiated U937 cells for colloidal drug delivery systems in immune cells. Inflammation. 34:99–110.
   PubMed Web of Science ®Google Scholar
• Li, Q, Kobayashi, M, Kawada, T. 2011. Ziram induces apoptosis and necrosis in human immune cells. Arch Toxicol. 85:355–361.
   PubMed Web of Science ®Google Scholar
• Li, XB, Zhang ZR, Schluesener HJ, Xu SQ. 2006. Role of exosomes in immune regulation. J Cell Mol Med. 10:364–375.
   PubMed Web of Science ®Google Scholar
• Morelli AE, Larregina AT, Shufesky WJ, Sullivan ML, Stolz DB, Papworth GD, Zahorchak AF, Logar AJ, Wang Z, Watkins SC, et al. 2004. Endocytosis, intracellular sorting, and processing of exosomes by dendritic cells. Blood. 104:3257–3266.
   PubMed Web of Science ®Google Scholar
• Mulcahy LA, Pink RC, Carter DR. 2014. Routes and mechanisms of extracellular vesicle uptake. J Extracell Ves. 3:24641–24654.
   PubMedGoogle Scholar
• Ohno S, Takanashi M, Sudo K, Ueda S, Ishikawa A, Matsuyama N, Fujita K, Mizutani T, Ohgi T, Ochiya T, et al. 2013. Systemically injected exosomes targeted to EGFR deliver antitumor microRNA to breast cancer cells. Mol Ther. 21:185–191.
   PubMed Web of Science ®Google Scholar
• Parker H, Chitcholtan K, Hampton MB, Keenan JI. 2010. Uptake of Helicobacter pylori outer membrane vesicles by gastric epithelial cells. Infect Immun. 78:5054–5061.
   PubMed Web of Science ®Google Scholar
• Poon IK, Hulett MD, Parish CR. 2010. Molecular mechanisms of late apoptotic/necrotic cell clearance. Cell Death Differ. 17:381–397.
   PubMed Web of Science ®Google Scholar
• Prach M, Stone V, Proudfoot L. 2013. Zinc oxide nanoparticles and monocytes: Impact of size, charge and solubility on activation status. Toxicol Appl Pharmacol. 266:19–26.
   PubMed Web of Science ®Google Scholar
• Ramery E, O'Brien PJ. 2014. Evaluation of cytotoxicity of organic dust components on THP1 monocytes-derived macrophages using high content analysis. Environ Toxicol. 29:310–319.
   PubMed Web of Science ®Google Scholar
• Raposo G, Stoorvogel W. 2013. Extracellular vesicles: Exosomes, microvesicles, and friends. J Cell Biol. 200:373–383.
   PubMed Web of Science ®Google Scholar
• Robbins PD, Morelli AE. 2014. Regulation of immune responses by extracellular vesicles. Nat Rev Immunol. 14:195–208.
   PubMed Web of Science ®Google Scholar
• Romagnoli GG, Zelante BB, Toniolo PA, Migliori IK, Barbuto JA. 2014. Dendritic cell-derived exosomes may be a tool for cancer immunotherapy by converting tumor cells into immunogenic targets. Front Immunol. 5:692.
   PubMed Web of Science ®Google Scholar
• Roy MK, Takenaka M, Kobori M, Nakahara K, Isobe S, Tsushida T. 2006. Apoptosis, necrosis. and cell proliferation inhibition by cyclosporine A in U937 cells (a human mono-cytic cell line). Pharmacol Res. 53:293–302.
   PubMed Web of Science ®Google Scholar
• Ruiss R, Jochum S, Mocikat R, Hammerschmidt W, Zeidler R. 2011. EBV-gp350 confers B-cell tropism to tailored exosomes and is a neo-antigen in normal and malignant B-cells - a new option for treatment of B-CLL. PLoS One. 6:e25294.
   Web of Science ®Google Scholar
• Saenz-Cuesta M, Osorio-Querejeta I, Otaegui D. 2014. Extracellular vesicles in multiple sclerosis: What are they telling us? Front Cell Neurosci. 8:100.
   PubMedGoogle Scholar
• Thery C, Amigorena S, Raposo G, Clayton A. 2006. Isolation and characterization of exosomes from cell culture supernatants and biological fluids. Curr Protocol Cell Biol. Chapter 3:Unit 3.22. DOI: 10.1002/0471143030.cb0322s30.
   PubMedGoogle Scholar
• Tian T, Zhu YL, Zhou YY, Liang GF, Wang YY, Hu FH, Xiao ZD. 2014. Exosome uptake through clathrin-mediated endocytosis and macropinocytosis and mediating miR-21 delivery. J Biol Chem. 289:22258–22267.
   PubMed Web of Science ®Google Scholar
• Tickner JA, Urquhart AJ, Stephenson SA, Richard DJ, O'Byrne KJ. 2014. Functions and therapeutic roles of exosomes in cancer. Front Oncol. 4:127.
   PubMedGoogle Scholar
• Valiunas V, Wang HZ, Li L, Gordon C, Valiuniene L, Cohen IS, Brink PR. 2015. A comparison of two cellular delivery mechanisms for small interfering RNA. Physiol Rep. 3:e12286.
   Google Scholar
• van Deun J, Mestdagh P, Sormunen R, Cocquyt V, Vermaelen K, Vandesompele J, Bracke M, de Wever O, Hendrix A. 2014. The impact of disparate isolation methods for extracellular vesicles on downstream RNA profiling. J Extracell Ves. 3:24858–24871.
   PubMedGoogle Scholar
• Yang J, Zhang L, Yu C, Yang X, Wang H. 2014. Monocyte and macrophage differentiation: Circulation inflammatory monocyte as biomarker for inflammatory diseases. Biomarker Res. 2:1.
   PubMedGoogle Scholar
• Yeo RW, Lai RC, Zhang B, Tan SS, Yin Y, Teh BJ, Lim SK. 2013. Mesenchymal stem cell: An efficient mass producer of exosomes for drug delivery. Adv Drug Deliv Rev. 65:336–341.
   PubMed Web of Science ®Google Scholar
• Zhang B, Yin Y, Lai RC, Lim SK. 2014. Immunotherapeutic potential of extracellular vesicles. Front Immunol. 5:518.
   PubMed Web of Science ®Google Scholar
• Zhou M, Chen J, Zhou L, Chen W, Ding G, Cao L. 2014. Pancreatic cancer-derived exosomes regulate expression of TLR4 in dendritic cells via miR-203. Cell Immunol. 292:65–69.
   PubMed Web of Science ®Google Scholar