Novel alternatives to extracellular vesicle-based immunotherapy – exosome mimetics derived from natural killer cells

References

• Lee SJ, Kang WY, Yoon Y, et al. Nam, natural killer (NK) cells inhibit systemic metastasis of glioblastoma cells and have therapeutic effects against glioblastomas in the brain. BMC Cancer. 2015;15:1011.
   PubMed Web of Science ®Google Scholar
• Zhu L, Li XJ, Kalimuthu S, et al. Ahn, natural killer cell (NK-92MI)-based therapy for pulmonary metastasis of anaplastic thyroid cancer in a nude mouse model. Front Immunol. 2017;8:824
   PubMed Web of Science ®Google Scholar
• Zamai L, Ponti C, Mirandola P, et al. NK cells and cancer. J Immunol. 2007;178:4011–4016.
   PubMed Web of Science ®Google Scholar
• Shoae-Hassani A, Hamidieh AA, Behfar M, et al. NK cell-derived exosomes from NK cells previously exposed to neuroblastoma cells augment the antitumor activity of cytokine-activated NK cells. J Immunother. 2017;40:265–276.
   PubMed Web of Science ®Google Scholar
• Moore TC, Kumm PM, Brown DM, et al. Interferon response factor 3 is crucial to poly-I:C induced NK cell activity and control of B16 melanoma growth. Cancer Lett. 2014;346:122–128.
   PubMed Web of Science ®Google Scholar
• Zhang G, Liu R, Zhu X, et al. Retargeting NK-92 for anti-melanoma activity by a TCR-like single-domain antibody. Immunol Cell Biol. 2013;91:615–624.
   PubMed Web of Science ®Google Scholar
• Hwang MH, Li XJ, Kim JE, et al. Potential therapeutic effect of natural killer cells on doxorubicin-resistant breast cancer cells in vitro. PloS One. 2015;10:e0136209.
   PubMed Web of Science ®Google Scholar
• Kim HW, Kim JE, Hwang MH, et al. Enhancement of natural killer cell cytotoxicity by sodium/iodide symporter gene-mediated radioiodine pretreatment in breast cancer cells. PloS One. 2013;8:e70194.
   PubMed Web of Science ®Google Scholar
• Lee HW, Singh TD, Lee SW, et al. Evaluation of therapeutic effects of natural killer (NK) cell-based immunotherapy in mice using in vivo apoptosis bioimaging with a caspase-3 sensor. FASEB J. 2014;28:2932–2941.
   PubMed Web of Science ®Google Scholar
• Michel T, Poli A, Cuapio A, et al. Human CD56 bright NK cells: an update. J Immunol. 2016;196:2923–2931.
   PubMed Web of Science ®Google Scholar
• Zhu L, Kalimuthu S, Gangadaran P, et al. Exosomes derived from natural killer cells exert therapeutic effect in melanoma. Theranostics. 2017;7:2732–2745.
   PubMed Web of Science ®Google Scholar
• Kalimuthu S, Gangadaran P, Li XJ, et al. In vivo therapeutic potential of mesenchymal stem cell-derived extracellular vesicles with optical imaging reporter in tumor mice model. Sci Rep. 2016;6:30418.
   PubMed Web of Science ®Google Scholar
• Fais S. NK cell-released exosomes: natural nanobullets against tumors. Oncoimmunology. 2013;2:e22337.
   PubMed Web of Science ®Google Scholar
• Jong AY, Wu CH, Li J, et al. Large-scale isolation and cytotoxicity of extracellular vesicles derived from activated human natural killer cells. J Extracell Vesicles. 2017;6:1294368.
   PubMed Web of Science ®Google Scholar
• Sobo-Vujanovic A, Munich S, Vujanovic NL. Dendritic-cell exosomes cross-present Toll-like receptor-ligands and activate bystander dendritic cells. Cell Immunol. 2014;289:119–127.
   PubMed Web of Science ®Google Scholar
• Kim OY, Lee J, Gho YS. Extracellular vesicle mimetics: novel alternatives to extracellular vesicle-based theranostics, drug delivery, and vaccines. Semin Cell Dev Biol. 2017;67:74–82.
   PubMed Web of Science ®Google Scholar
• Bretz NP, Ridinger J, Rupp AK, et al. Body fluid exosomes promote secretion of inflammatory cytokines in monocytic cells via Toll-like receptor signaling. J Biol Chem. 2013;288:36691–36702.
   PubMed Web of Science ®Google Scholar
• Watson DC, Bayik D, Srivatsan A, et al. Efficient production and enhanced tumor delivery of engineered extracellular vesicles. Biomaterials. 2016;105:195–205.
   PubMed Web of Science ®Google Scholar
• Munoz JL, Bliss SA, Greco SJ, et al. Delivery of functional anti-miR-9 by mesenchymal stem cell-derived exosomes to glioblastoma multiforme cells conferred chemosensitivity. Mol Ther Nucleic Acids. 2013;2:e126.
   PubMedGoogle Scholar
• Katakowski M, Buller B, Zheng X, et al. Exosomes from marrow stromal cells expressing miR-146b inhibit glioma growth. Cancer Lett. 2013;335:201–204.
   PubMed Web of Science ®Google Scholar
• Wen SW, Sceneay J, Lima LG, et al. The biodistribution and immune suppressive effects of breast cancer-derived exosomes. Cancer Res. 2016;76:6816–6827.
   PubMed Web of Science ®Google Scholar
• Yu DD, Wu Y, Shen HY, et al. Exosomes in development, metastasis and drug resistance of breast cancer. Cancer Sci. 2015;106:959–964.
   PubMed Web of Science ®Google Scholar
• Lugini L, Cecchetti S, Huber V, et al. Immune surveillance properties of human NK cell-derived exosomes. J Immunol. 2012;189:2833–2842.
   PubMed Web of Science ®Google Scholar
• Oh K, Kim SR, Kim DK, et al. In vivo differentiation of therapeutic insulin-producing cells from bone marrow cells via extracellular vesicle-mimetic nanovesicles. ACS Nano. 2015;9:11718–11727.
   PubMed Web of Science ®Google Scholar
• Jang SC, Gho YS. Could bioengineered exosome-mimetic nanovesicles be an efficient strategy for the delivery of chemotherapeutics? Nanomedicine (Lond). 2014;9:177–180.
   PubMed Web of Science ®Google Scholar
• Jang SC, Kim OY, Yoon CM, et al. Bioinspired exosome-mimetic nanovesicles for targeted delivery of chemotherapeutics to malignant tumors. ACS Nano. 2013;7:7698–7710.
   PubMed Web of Science ®Google Scholar
• Cheung AM, Brown AS, Hastie LA, et al. Three-dimensional ultrasound biomicroscopy for xenograft growth analysis. Ultrasound Med Biol. 2005;31:865–870.
   PubMed Web of Science ®Google Scholar
• Wirtzfeld LA, Wu G, Bygrave M, et al. A new three-dimensional ultrasound microimaging technology for preclinical studies using a transgenic prostate cancer mouse model. Cancer Res. 2005;65:6337–6345.
   PubMed Web of Science ®Google Scholar
• Vivier E, Tomasello E, Baratin M, et al. Functions of natural killer cells. Nat Immunol. 2008;9:503–510.
   PubMed Web of Science ®Google Scholar
• Dubois S, Conlon KC, Muller JR, et al. IL15 infusion of cancer patients expands the subpopulation of cytotoxic CD56bright NK cells and increases NK-cell cytokine release capabilities. Cancer Immunol Res. 2017;5:929–938.
   PubMed Web of Science ®Google Scholar
• Augstein P, Heinke P, Schober C, et al. Impact of cytokine- and FasL-induced apoptosis in the beta-cell line NIT-1. Horm Metab Res. 2009;41:207–212.
   PubMed Web of Science ®Google Scholar
• Roux PP, Blenis J. ERK and p38 MAPK-activated protein kinases: a family of protein kinases with diverse biological functions. Microbiol Mol Biol Rev. 2004;68:320–344.
   PubMed Web of Science ®Google Scholar
• Gaestel M. MAPK-activated protein kinases (MKs): novel insights and challenges. Front Cell Dev Biol. 2016;3:88.
   PubMed Web of Science ®Google Scholar
• Cargnello M, Roux PP. Activation and function of the MAPKs and their substrates, the MAPK-activated protein kinases. Microbiol Mol Biol Rev. 2011;75:50–83.
   PubMed Web of Science ®Google Scholar
• Klingemann H, Boissel L, Toneguzzo F. Natural killer cells for immunotherapy - advantages of the NK-92 cell line over blood NK cells. Front Immunol. 2016;7:91.
   PubMed Web of Science ®Google Scholar
• Guillerey C, Huntington ND, Smyth MJ. Targeting natural killer cells in cancer immunotherapy. Nat Immunol. 2016;17:1025–1036.
   PubMed Web of Science ®Google Scholar
• Kremer V, Ligtenberg M, Zendehdel R, et al. Genetic engineering of human NK cells to express CXCR2 improves migration to renal cell carcinoma. J Immunotherapy Cancer. 2017;5:73.
   PubMed Web of Science ®Google Scholar
• Roth JC, Curiel DT, Pereboeva L. Cell vehicle targeting strategies. Gene Ther. 2008;15:716–729.
   PubMed Web of Science ®Google Scholar
• Lam PY, Nissen MD, Mattarollo SR. Invariant natural killer T cells in immune regulation of blood cancers: harnessing their potential in immunotherapies. Front Immunol. 2017;8:1355.
   PubMed Web of Science ®Google Scholar
• Lunavat TR, Jang SC, Nilsson L, et al. RNAi delivery by exosome-mimetic nanovesicles – implications for targeting c-Myc in cancer. Biomaterials. 2016;102:231–238.
   PubMed Web of Science ®Google Scholar
• Yuan D, Zhao Y, Banks WA, et al. Macrophage exosomes as natural nanocarriers for protein delivery to inflamed brain. Biomaterials. 2017;142:1–12.
   PubMed Web of Science ®Google Scholar
• Escudier B, Dorval T, Chaput N, et al. Vaccination of metastatic melanoma patients with autologous dendritic cell (DC) derived-exosomes: results of the first phase I clinical trial. J Transl Med. 2005;3:10.
   PubMed Web of Science ®Google Scholar
• Kim OY, Choi SJ, Jang SC, et al. Bacterial protoplast-derived nanovesicles as vaccine delivery system against bacterial infection. Nano Lett. 2015;15:266–274.
   PubMed Web of Science ®Google Scholar
• Gangadaran P, Rajendran RL, Lee HW, et al. Extracellular vesicles from mesenchymal stem cells activates VEGF receptors and accelerates recovery of hindlimb ischemia. J Control Release. 2017;264:112–126.
   PubMed Web of Science ®Google Scholar
• Imai T, Takahashi Y, Nishikawa M, et al. Macrophage-dependent clearance of systemically administered B16BL6-derived exosomes from the blood circulation in mice. J Extracell Vesicles. 2015;4:26238.
   PubMed Web of Science ®Google Scholar
• Lobb RJ, Becker M, Wen SW, et al. Optimized exosome isolation protocol for cell culture supernatant and human plasma. J Extracell Vesicles. 2015;4:27031.
   PubMed Web of Science ®Google Scholar
• Vashisht M, Rani P, Onteru SK, et al. Curcumin encapsulated in milk exosomes resists human digestion and possesses enhanced intestinal permeability in vitro. Appl Biochem Biotechnol. 2017;183:993–1007.
   PubMed Web of Science ®Google Scholar
• Pitt JM, Andre F, Amigorena S, et al. Dendritic cell-derived exosomes for cancer therapy. J Clin Invest. 2016;126:1224–1232.
   PubMed Web of Science ®Google Scholar
• Gilligan KE, Dwyer RM. Engineering exosomes for cancer therapy. Int J Mol Sci. 2017;18:1122.
   PubMed Web of Science ®Google Scholar
• Gangadaran P, Ahn BC. Molecular imaging: a useful tool for the development of natural killer cell-based immunotherapies. Front Immunol. 2017;8:1090.
   PubMed Web of Science ®Google Scholar
• Trapani JA, Smyth MJ. Functional significance of the perforin/granzyme cell death pathway. Nat Rev Immunol. 2002;2:735–747.
   PubMed Web of Science ®Google Scholar
• Smyth T, Kullberg M, Malik N, et al. Biodistribution and delivery efficiency of unmodified tumor-derived exosomes. J Control Release. 2015;199:145–155.
   PubMed Web of Science ®Google Scholar
• Munagala R, Aqil F, Jeyabalan J, et al. Bovine milk-derived exosomes for drug delivery. Cancer Lett. 2016;371:48–61.
   PubMed Web of Science ®Google Scholar
• Gangadaran P, Hong CM, Ahn BC. Current perspectives on in vivo noninvasive tracking of extracellular vesicles with molecular imaging. BioMed Res Int. 2017;2017:1.
   Web of Science ®Google Scholar
• Xin H, Li Y, Buller B, et al. Exosome-mediated transfer of miR-133b from multipotent mesenchymal stromal cells to neural cells contributes to neurite outgrowth. Stem Cells. 2012;30:1556–1564.
   PubMed Web of Science ®Google Scholar
• McDonald MK, Tian Y, Qureshi RA, et al. Functional significance of macrophage-derived exosomes in inflammation and pain. Pain. 2014;155:1527–1539.
   PubMed Web of Science ®Google Scholar
• Haney MJ, Klyachko NL, Zhao Y, et al. Exosomes as drug delivery vehicles for Parkinson’s disease therapy. J Control Release. 2015;207:18–30.
   PubMed Web of Science ®Google Scholar
• Yang T, Martin P, Fogarty B, et al. Exosome delivered anticancer drugs across the blood-brain barrier for brain cancer therapy in Danio rerio. Pharm Res. 2015;32:2003–2014.
   PubMed Web of Science ®Google Scholar
• Tan S, Wu T, Zhang D, et al. Cell or cell membrane-based drug delivery systems. Theranostics. 2015;5:863–881.
   PubMed Web of Science ®Google Scholar
• Chen X, Han J, Chu J, et al. A combinational therapy of EGFR-CAR NK cells and oncolytic herpes simplex virus 1 for breast cancer brain metastases. Oncotarget. 2016;7:27764–27777.
   PubMedGoogle Scholar
• Zhang C, Oberoi P, Oelsner S, et al. Chimeric antigen receptor-engineered NK-92 cells: an off-the-shelf cellular therapeutic for targeted elimination of cancer cells and induction of protective antitumor immunity. Front Immunol. 2017;8:533.
   PubMed Web of Science ®Google Scholar
• Alvarez-Erviti L, Seow Y, Yin H, et al. Delivery of siRNA to the mouse brain by systemic injection of targeted exosomes. Nat Biotechnol. 2011;29:341–345.
   PubMed Web of Science ®Google Scholar
• Lakhal S, Wood MJ. Exosome nanotechnology: an emerging paradigm shift in drug delivery: exploitation of exosome nanovesicles for systemic in vivo delivery of RNAi heralds new horizons for drug delivery across biological barriers. Bioessays. 2011;33:737–741.
   PubMed Web of Science ®Google Scholar
• Kim SM, Kim HS. Engineering of extracellular vesicles as drug delivery vehicles. Stem Cell Investig. 2017;4:74.
   PubMedGoogle Scholar
• Muller N, Michen S, Tietze S, et al. Engineering NK cells modified with an EGFRvIII-specific chimeric antigen receptor to overexpress CXCR4 improves immunotherapy of CXCL12/SDF-1alpha-secreting glioblastoma. J Immunother. 2015;38:197–210.
   PubMed Web of Science ®Google Scholar