Engineering exosomes as refined biological nanoplatforms for drug delivery

Acta Pharmacologica Sinica

Volumn 38, Issue 6, 2017, Pages 754-763

  Luan, Xin ^a   Sansanaphongpricha, Kanokwan ^a   Myers, Ila ^a   Chen, Hongwei ^a   Yuan, Hebao ^a   Sun, Duxin ^a  

^a UNIVERSITY OF MICHIGAN   (United States)

Author keywords

Drug delivery systems; Exosome; Imaging probes; Nanoparticles; Therapeutics

Indexed keywords

ANTINEOPLASTIC AGENT; CANCER VACCINE; MICRORNA; NANOCARRIER; PROTEIN ANTIBODY; SAPONIN; SMALL INTERFERING RNA; TUMOR ANTIGEN; DRUG CARRIER; NANOPARTICLE;

CANCER IMMUNOTHERAPY; CELL COMMUNICATION; CELL ENGINEERING; CLICK CHEMISTRY; CONJUGATION; DRUG DELIVERY SYSTEM; ELECTROPORATION; ENCAPSULATION; EXOSOME; FREEZE THAWING; IMAGING; IMMUNOTHERAPY; NANOTECHNOLOGY; REVIEW; TUMOR CELL; ULTRASOUND; CHEMISTRY; HUMAN; METABOLISM; NANOMEDICINE;

DRUG CARRIERS; DRUG DELIVERY SYSTEMS; EXOSOMES; HUMANS; NANOMEDICINE; NANOPARTICLES;

EID: 85020171188     PISSN: 16714083     EISSN: 17457254     Source Type: Journal    
DOI: 10.1038/aps.2017.12     Document Type: Review

References (78)

1. Liu D, Yang F, Xiong F, Gu N. The smart drug delivery system and its clinical potential. Theranostics 2016; 6: 1306-23.
2. Hinde E, Thammasiraphop K, Duong HT, Yeow J, Karagoz B, Boyer C, et al. Pair correlation microscopy reveals the role of nanoparticle shape in intracellular transport and site of drug release. Nat Nanotechnol 2017; 12: 81-9.
3. Sharma AK, Gothwal A, Kesharwani P, Alsaab H, Iyer AK, Gupta U. Dendrimer nanoarchitectures for cancer diagnosis and anticancer drug delivery. Drug Discov Today 2016; doi: 10.1016/j.drudis.2016.09.013.
4. Luan X, Guan YY, Lovell JF, Zhao M, Lu Q, Liu YR, et al. Tumor priming using metronomic chemotherapy with neovasculature-targeted, nanoparticulate paclitaxel. Biomaterials 2016; 95: 60-73.
5. Haque S, Whittaker MR, McIntosh MP, Pouton CW, Kaminskas LM. Disposition and safety of inhaled biodegradable nanomedicines: Opportunities and challenges. Nanomedicine 2016; 12: 1703-24.
6. Matsumura Y. The drug discovery by nanomedicine and its clinical experience. Jpn J Clin Oncol 2014; 44: 515-25.
7. Suk JS, Xu QG, Kim N, Hanes J, Ensign LM. PEGylation as a strategy for improving nanoparticle-based drug and gene delivery. Adv Drug Deliver Rev 2016; 99: 28-51.
8. Sun L, Wu QJ, Peng F, Liu L, Gong CY. Strategies of polymeric nanoparticles for enhanced internalization in cancer therapy. Colloid Surface B 2015; 135: 56-72.
9. Chow TH, Lin YY, Hwang JJ, Wang HE, Tseng YL, Wang SJ, et al. Improvement of biodistribution and therapeutic index via increase of polyethylene glycol on drug-carrying liposomes in an HT-29/luc xenografted mouse model. Anticancer Res 2009; 29: 2111-20.
10. Peng Q, Mu H. The potential of protein-nanomaterial interaction for advanced drug delivery. J Control Release 2016; 225: 121-32.
11. Hood JL. Post isolation modification of exosomes for nanomedicine applications. Nanomedicine (Lond) 2016; 11: 1745-56.
12. Vader P, Mol EA, Pasterkamp G, Schiffelers RM. Extracellular vesicles for drug delivery. Adv Drug Deliv Rev 2016; 106: 148-56.
13. Batrakova EV, Kim MS. Using exosomes, naturally-equipped nanocarriers, for drug delivery. J Control Release 2015; 219: 396-405.
14. Milane L, Singh A, Mattheolabakis G, Suresh M, Amiji MM. Exosome mediated communication within the tumor microenvironment. J Control Release 2015; 219: 278-94.
15. Turturici G, Tinnirello R, Sconzo G, Geraci F. Extracellular membrane vesicles as a mechanism of cell-to-cell communication: Advantages and disadvantages. Am J Physiol-Cell Ph 2014; 306: C621-C33.
16. Desrochers LM, Antonyak MA, Cerione RA. Extracellular vesicles: satellites of information transfer in cancer and stem cell biology. Dev Cell 2016; 37: 301-9.
17. Bang C, Thum T. Exosomes: new players in cell-cell communication. Int J Biochem Cell Biol 2012; 44: 2060-4.
18. Malhotra H, Sheokand N, Kumar S, Chauhan AS, Kumar M, Jakhar P, et al. Exosomes: tunable nano vehicles for macromolecular delivery of transferrin and lactoferrin to specific intracellular compartment. J Biomed Nanotechnol 2016; 12: 1101-14.
19. Rupert DL, Claudio V, Lasser C, Bally M. Methods for the physical characterization and quantification of extracellular vesicles in biological samples. Biochim Biophys Acta 2017; 1861: 3164-79.
20. Hood JL, Wickline SA. A systematic approach to exosome-based translational nanomedicine. Wiley Interdiscip Rev Nanomed Nanobiotechnol 2012; 4: 458-67.
21. Morishita M, Takahashi Y, Matsumoto A, Nishikawa M, Takakura Y. Exosome-based tumor antigens-adjuvant co-delivery utilizing genetically engineered tumor cell-derived exosomes with immunostimulatory CpG DNA. Biomaterials 2016; 111: 55-65.
22. Whiteside TL. Tumor-derived exosomes and their role in cancer progression. Adv Clin Chem 2016; 74: 103-41.
23. Romagoli GG, Zelante BB, Toniolo PA, Migliori IK, Barbuto JA. Dendritic cell-derived exosomes may be a tool for cancer immunotherapy by converting tumor cells into immunogenic targets. Front Immunol 2015; 5: 692.
24. Frydrychowicz M, Kolecka-Bednarczyk A, Madejczyk M, Yasar S, Dworacki G. Exosomes - structure, biogenesis and biological role in non-small-cell lung cancer. Scand J Immunol 2015; 81: 2-10.
25. Mahaweni NM, Kaijen-Lambers ME, Dekkers J, Aerts JG, Hegmans JP. Tumour-derived exosomes as antigen delivery carriers in dendritic cell-based immunotherapy for malignant mesothelioma. J Extracell Vesicles 2013; 2:22492.
26. 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.
27. Thomas Jefferson University. Pilot Immunotherapy trial for Recurrent Malignant Gliomas. In: ClinicalTrials.gov [Internet]. Bethesda (MD): National Library of Medicine (US). 2000-[cited 2016 Oct 20]. Available from: http://clinicaltrials.gov/show/NCT01550523 NLM Identifier: NCT01550523.
28. Rana S, Yue SJ, Stadel D, Zoller M. Toward tailored exosomes: The exosomal tetraspanin web contributes to target cell selection. Int J Biochem Cell B 2012; 44: 1574-84.
29. Zomer A, Maynard C, Verweij FJ, Kamermans A, Schafer R, Beerling E, et al. In vivo imaging reveals extracellular vesicle-mediated phenocopying of metastatic behavior. Cell 2015; 161: 1046-57.
30. Harris DA, Patel SH, Gucek M, Hendrix A, Westbroek W, Taraska JW. Exosomes released from breast cancer carcinomas stimulate cell movement. PLoS One 2015; 10: e0117495.
31. Melo SA, Sugimoto H, O'Connell JT, Kato N, Villanueva A, Vidal A, et al. Cancer exosomes perform cell-independent microRNA biogenesis and promote tumorigenesis. Cancer Cell 2014; 26: 707-21.
32. Frey AB. Myeloid suppressor cells regulate the adaptive immune response to cancer. J Clin Invest 2006; 16: 2587-90.
33. Talor DD, Gercel-Taylor C. Exosomes/microvesicles: mediators of cancer-associated immunosuppressive microenvironmen-ts. Semin Immunopathol 2011; 33: 441-54.
34. Tomihari M, Chung JS, Akiyoshi H, Cruz PD Jr, Ariizumi K. DC-HIL/glycoprotein Nmb promotes growth of melanoma in mice by inhibiting the activation of tumor-reactive T cells. Cancer Res 2010; 70: 5778-87.
35. 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: 1010-20.
36. Ju SW, Mu JY, Dokland T, Zhuang XY, Wang QL, Jiang H, et al. Grape Exosome-like nanoparticles induce intestinal stem cells and protect mice from dss-induced colitis. Mol Ther 2013; 21: 1345-57.
37. Munagala R, Aqil F, Jeyabalan J, Gupta RC. Bovine milk-derived exosomes for drug delivery. Cancer Lett 2016; 371: 48-61.
38. James Graham Brown Cancer Center; University of Louisville. Study Investigating the Ability of Plant Exosomes to Deliver Curcumin to Normal and Colon Cancer Tissue. In: ClinicalTrials.gov [Internet]. Bethesda (MD): National Library of Medicine (US). 2000-[cited 2016 Oct 20]. Available from: http://clinicaltrials.gov/show/NCT01294072 NLM Identifier: NCT01294072.
39. Wang QL, Ren Y, Mu JY, Egilmez NK, Zhuang XY, Deng ZB, et al. Grapefruit-derived nanovectors use an activated leukocyte trafficking pathway to deliver therapeutic agents to inflammatory tumor sites. Cancer Res 2015; 75: 2520-9.
40. Escudier B, Dorval T, Chaput N, Andre F, Caby MP, Novault S, et al. Vaccination of metastatic melanoma patients with autologous dendritic cell (DC) derived-exosomes: results of thefirst phase I clinical trial. J Transl Med 2005; 3: 10.
41. Viaud S, Terme M, Flament C, Taieb J, Andre F, Novault S, et al. Dendritic cell-derived exosomes promote natural killer cell activation and proliferation: A role for NKG2D ligands and IL-15R alpha. PLoS One 2009; 4: e4942.
42. Simhadri VR, Reiners KS, Hansen HP, Topolar D, Simhadri VL, Nohroudi K, et al. Dendritic cells release hla-b-associated transcript-3 positive exosomes to regulate natural killer function. PLoS One 2008; 3: e3377.
43. Shenoda BB, Ajit SK. Modulation of immune responses by exosomes derived from antigen-presenting cells. Clin Med Insights Pathol 2016; 9: 1-8.
44. Haney MJ, Klyachko NL, Zhaoa YL, Gupta R, Plotnikova EG, He ZJ, et al. Exosomes as drug delivery vehicles for Parkinson's disease therapy. J Control Release 2015; 207: 18-30.
45. Gustave Roussy, Cancer Campus, Grand Paris. Trial of a Vaccination With Tumor Antigen-loaded Dendritic Cell-derived Exosomes (CSET 1437). In: ClinicalTrials.gov [Internet]. Bethesda (MD): National Library of Medicine (US). 2000-[cited 2016 Oct 20]. Available from: http://clinicaltrials.gov/show/NCT01159288 NLM Identifier: NCT01159288.
46. Thery C, Duban L, Segura E, Veron P, Lantz O, Amigorena S. Indirect activation of naive CD4(+) T cells by dendritic cell-derived exosomes. Nat Immunol 2002; 3: 1156-62.
47. Sun D, Zhuang XY, Xiang X, Liu Y, Zhang S, Liu C, et al. A novel nanoparticle drug delivery system: the anti-inflammatory activity of curcumin is enhanced when encapsulated in exosomes. Mol Ther 2010; 18: 1606-14.
48. Pascucci L, Cocce V, Bonomi A, Ami D, Ceccarelli P, Ciusani E, et al. Paclitaxel is incorporated by mesenchymal stromal cells and released in exosomes that inhibit in vitro tumor growth: A new approach for drug delivery. J Control Release 2014; 192: 262-70.
49. Kim MS, Haney MJ, Zhao Y, Mahajan V, Deygen I, Klyachko NL, et al. Development of exosome-encapsulated paclitaxel to overcome MDR in cancer cells. Nanomed-Nanotechnol 2016; 12: 655-64.
50. Fuhrmann G, Serio A, Mazo M, Nair R, Stevens MM. Active loading into extracellular vesicles significantly improves the cellular uptake and photodynamic effect of porphyrins. J Control Release 2015; 205: 35-44.
51. Sato YT, Umezaki K, Sawada S, Mukai S, Sasaki Y, Harada N, et al. Engineering hybrid exosomes by membrane fusion with liposomes. Sci Rep 2016; 6: 21933.
52. Wahlgren J, Karlson TD, Brisslert M, Sani FV, Telemo E, Sunnerhagen P, et al. Plasma exosomes can deliver exogenous short interfering RNA to monocytes and lymphocytes. Nucleic Acids Res 2012; 40: e130.
53. Johnsen KB, Gudbergsson JM, Skov MN, Christiansen G, Gurevich L, Moos T, et al. Evaluation of electroporation-induced adverse effects on adipose-derived stem cell exosomes. Cytotechnology 2016; 68: 2125-38.
54. Podolak I, Galanty A, Sobolewska D. Saponins as cytotoxic agents: A review. Phytochem Rev 2010; 9: 425-74.
55. Wang M, Altinoglu S, Takeda YS, Xu QB. Integrating protein engineering and bioorthogonal click conjugation for extracellular vesicle modulation and intracellular delivery. PLoS One 2015; 10: e0141860.
56. Smyth T, Petrova K, Payton NM, Persaud I, Redzic JS, Gruner MW, et al. Surface functionalization of exosomes using click chemistry. Bioconjugate Chem 2014; 25: 1777-84.
57. Higginbotham JN, Zhang Q, Jeppesen DK, Scott AM, Manning HC, Ochieng J, et al. Identification and characterization of EGF receptor in individual exosomes by fluorescence-activated vesicle sorting. J Extracell Vesicles 2016; 5: 29254.
58. Munagala R, Aqil F, Jeyabalan J, Gupta RC. Bovine milk-derived exosomes for drug delivery. Cancer Lett 2016; 371: 48-61.
59. Kim MS, Haney MJ, Zhao Y, Mahajan V, Deygen I, Klyachko NL, et al. Development of exosome-encapsulated paclitaxel to overcome mdr in cancer cells. Nanomedicine 2016; 12: 655-64.
60. Yano J, Hirabayashi K, Nakagawa S, Yamaguchi T, Nogawa M, Kashimori I, et al. Antitumor activity of small interfering RNA/cationic liposome complex in mouse models of cancer. Clin Cancer Res 2004; 10: 7721-6.
61. Sioud M, Sorensen DR. Cationic liposome-mediated delivery of siRNAs in adult mice. Biochem Biophys Res Commun 2003; 312: 1220-5.
62. Patil ML, Zhang M, Taratula O, Garbuzenko OB, He H, Minko T. Internally cationic polyamidoamine PAMAM-OH dendrimers for siRNA delivery: effect of the degree of quaternization and cancer targeting. Biomacromolecules 2009; 10: 258-66.
63. Thomas M, Lu JJ, Ge Q, Zhang C, Chen J, Klibanov AM. Full deacylation of polyethylenimine dramatically boosts its gene delivery efficiency and specificity to mouse lung. Proc Natl Acad Sci U S A 2005; 102: 5679-84.
64. Kesharwani P, Gajbhiye V, Jain NK. A review of nanocarriers for the delivery of small interfering RNA. Biomaterials 2012; 33: 713-50.
65. Alvarez-Erviti L, Seow Y, Yin H, Betts C, Lakhal S, Wood MJ. Delivery of siRNA to the mouse brain by systemic injection of targeted exosomes. Nat Biotechnol 2011; 29: 341-5.
66. Ohno S, Takanashi M, Sudo K, Ueda S, Ishikawa A, Matsuyama N, et al. Systemically injected exosomes targeted to EGFR deliver antitumor microRNA to breast cancer cells. Mol Ther 2013; 21: 185-91.
67. Lai CP, Mardini O, Ericsson M, Prabhakar S, Maguire CA, Chen JW, et al. Dynamic biodistribution of extracellular vesicles in vivo using a multimodal imaging reporter. ACS Nano 2014; 8: 483-94.
68. Oosthuyzen W, Sime NE, Ivy JR, Turtle EJ, Street JM, Pound J, et al. Quantification of human urinary exosomes by nanoparticle tracking analysis. J Physiol 2013; 591: 5833-42.
69. Wang J, Guo R, Yang Y, Jacobs B, Chen S, Iwuchukwu I, et al. The novel methods for analysis of exosomes released from endothelial cells and endothelial progenitor cells. Stem Cells Int 2016; 2016: 2639728.
70. Wang CF, Makila EM, Kaasalainen MH, Liu D, Sarparanta MP, Airaksinen AJ, et al. Copper-free azide-alkyne cycloaddition of targeting peptides to porous silicon nanoparticles for intracellular drug uptake. Biomaterials 2014; 35: 1257-66.
71. Amstrong JP, Holme MN, Stevens MM. Re-engineering extracellular vesicles as smart nanoscale therapeutics. ACS Nano 2017; doi: 10.1021/acsnano.6b07607.
72. Nakase I, Futaki S. Combined treatment with a pH-sensitive fusogenic peptide and cationic lipids achieves enhanced cytosolic delivery of exosomes. Sci Rep 2015; 5: 10112.
73. Qi H, Liu C, Long L, Ren Y, Zhang S, Chang X, et al. Blood exosomes endowed with magnetic and targeting properties for cancer therapy. ACS Nano 2016; 10: 3323-33.
74. Shao Y, Shen Y, Chen T, Xu F, Chen X, Zheng S. The functions and clinical application of tumor-derived exosomes. Oncotarget 2016; 7: 60736-51.
75. Whiteside TL. Tumor-derived exosomes and their role in cancer progression. Adv Clin Chem 2016; 74: 103-41.
76. Whiteside TL. Exosomes and tumor-mediated immune suppression. J Clin Invest 2016; 126: 1216-23.
77. van der Meel R, Fens MH, Vader P, van Solinge WW, Eniola-Adefeso O, Schiffelers RM. Extracellular vesicles as drug delivery systems: lessons from the liposome field. J Control Release 2014; 195: 72-85.
78. 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.