Exosomes as immunotheranostic nanoparticles

Clinical Therapeutics

Volumn 36, Issue 6, 2014, Pages 820-829

  Natasha, G ^a,b   Gundogan, Buket ^a,b   Tan, Aaron ^a,b,d   Farhatnia, Yasmin ^a   Wu, Woffles ^c   Rajadas, Jayakumar ^d   Seifalian, Alexander M ^a,e  

^a UNIVERSITY COLLEGE LONDON   (United Kingdom)

^b ROYAL FREE AND UNIVERSITY COLLEGE MEDICAL SCHOOL   (United Kingdom)

^c Camden Medical Centre   (Singapore)

^d STANFORD UNIVERSITY SCHOOL OF MEDICINE   (United States)

^e ROYAL FREE HOSPITAL   (United Kingdom)

Author keywords

Cancer vaccine; Exosomes; Immunotherapy; Nanomedicine; Nanoparticles; Theranostics

Indexed keywords

ANNEXIN; BIOLOGICAL MARKER; CANCER VACCINE; CURCUMIN; DENDRITIC CELL VACCINE; DRUG VEHICLE; HEAT SHOCK PROTEIN 70; HEAT SHOCK PROTEIN 90; IMMUNOLOGIC AGENT; INTERCELLULAR ADHESION MOLECULE 1; LIPID; NANOPARTICLE; RAB11 PROTEIN; RNA; SIPULEUCEL T; TETRASPANIN; TUMOR MARKER; WART VIRUS VACCINE;

ASCITES CELL; BIOCOMPATIBILITY; CANCER IMMUNOTHERAPY; CLINICAL TRIAL (TOPIC); COLORECTAL CANCER; DENDRITIC CELL; DIAGNOSTIC TEST ACCURACY STUDY; DIAGNOSTIC VALUE; DRUG DELIVERY SYSTEM; DRUG DISTRIBUTION; EXOSOME; GENE TARGETING; HUMAN; IMMUNE SYSTEM; LUNG NON SMALL CELL CANCER; MEDLINE; MEMBRANE VESICLE; ORAL MUCOSITIS; PLANT; PROGNOSIS; REVIEW; TUMOR CELL; CELL COMMUNICATION; IMMUNOLOGY; SIGNAL TRANSDUCTION; THERANOSTIC NANOMEDICINE; TISSUE DISTRIBUTION;

BIOMARKERS; CANCER VACCINES; CELL COMMUNICATION; EXOSOMES; HUMANS; NANOPARTICLES; SIGNAL TRANSDUCTION; THERANOSTIC NANOMEDICINE; TISSUE DISTRIBUTION;

EID: 84902842374     PISSN: 01492918     EISSN: 1879114X     Source Type: Journal    
DOI: 10.1016/j.c11nthera.2014.04.019     Document Type: Review

References (57)

1. Thery C, Zitvogel L, Amigorena S. Exosomes: composition, biogenesis and function. Nat Rev Immunol. 2002;2:569-579. (Pubitemid 37328732)
2. 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;29:341-345.
3. Taylor DD, Gercel-Taylor C. MicroRNA signatures of tumor-derived exosomes as diagnostic biomarkers of ovarian cancer. Gynecol Oncol. 2008;110:13-21. (Pubitemid 351853251)
4. Jokerst JV, Gambhir SS. Molecular imaging with thera-nostic nanoparticles. Acc Chem Res. 2011;44:1050-1060.
5. Raposo G, Nijman HW, Stoorvogel W, et al. B lymphocytes secrete antigen-presenting vesicles. J Exp Med. 1996;183:1161-1172.
6. Thery C, Boussac M, Veron P, et al. Proteomic analysis of dendritic cell-derived exosomes: a secreted subcellular compartment distinct from apoptotic vesicles. J Immunol. 2001;166:7309-7318. (Pubitemid 32525606)
7. Schorey JS, Bhatnagar S. Exosome function: from tumor immunology to pathogen biology. Traffic. 2008;9: 871-881. (Pubitemid 351639493)
8. Mears R, Craven RA, Hanrahan S, et al. Proteomic analysis of melanoma-derived exosomes by two-dimensional polyacrylamide gel electrophoresis and mass spectrometry. Proteomics. 2004;4:4019-4031. (Pubitemid 39657475)
9. Savina A, Fader CM, Damiani MT, Colombo MI. Rab11 promotes docking and fusion of multivesicular bodies in a calcium-dependent manner. Traffic. 2005;6:131-143.
10. Futter CE, White IJ. Annexins and endocytosis. Traffic. 2007;8:951-958. (Pubitemid 47074030)
11. . Bu N, Wu H, Sun B, et al. Exosome-loaded dendritic cells elicit tumor-specific CD8 cytotoxic T cells in patients with glioma. J Neurooncol. 2011;104:659-667.
12. Gastpar R, Gehrmann M, Bausero MA, et al. Heat shock protein 70 surface-positive tumor exosomes stimulate migratory and cytolytic activity of natural killer cells. Cancer Res. 2005;65:5238-5247. (Pubitemid 40827334)
13. 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 exo-somes secreted by human B-lymphocytes. J Bio Chem. 1998;273:20121-20127. (Pubitemid 28377568)
14. Laulagnier K, Motta C, Hamdi S, et al. Mast cell- and dendritic cell-derived exosomes display a specific lipid composition and an unusual membrane organization. Biochem J. 2004;380:161-171. (Pubitemid 38725741)
15. Johnstone RM, Adam M, Pan BT. The fate of the trans-ferrin receptor during maturation of sheep reticulocytes in vitro. Can J Biochem Cell Biol. 1984;62:1246-1254. (Pubitemid 15193145)
16. Zhang HG, Liu C, Su K, et al. A membrane form of TNF-α presented by exosomes delays T cell activation-induced cell death. J Immunol. 2006;176:7385-7393. (Pubitemid 43849040)
17. Valadi H, Ekstrom K, Bossios A, et al. Exosome-mediated transfer of mRNAs and microRNAs is a novel mechanism of genetic exchange between cells. Nat Cell Biol. 2007;9: 654-659. (Pubitemid 47214727)
18. Thery C, Ostrowski M, Segura E. Membrane vesicles as conveyors of immune responses. Nat Rev Immunol. 2009; 9:581-593.
19. Zitvogel L, Regnault A, Lozier A, et al. Eradication of established murine tumors using a novel cell-free vaccine: dendritic cell-derived exosomes. Nat Med. 1998;4:594-600. (Pubitemid 28237359)
20. Chen W, Wang J, Shao C, et al. Efficient induction of antitumor T cell immunity by exosomes derived from heat-shocked lymphoma cells. Eur J Immunol. 2006;36:1598-1607. (Pubitemid 43942147)
21. Bhatnagar S, Schorey JS. Exosomes released from infected macrophages contain Mycobacterium avium glycopepti-dolipids and are proinflammatory. J Biol Chem. 2007;282: 25779-25789. (Pubitemid 47372821)
22. Hao S, Bai O, Li F, Yuan J, Laferte S, Xiang J. Mature dendritic cells pulsed with exosomes stimulate efficient cytotoxic T-lymphocyte responses and antitumour immunity. Immunology. 2007;120:90-102. (Pubitemid 44950474)
23. Huber V, Fais S, Iero M, et al. Human colorectal cancer cells induce T-cell death through release of proapoptotic microvesicles: role in immune escape. Gastroenterology. 2005;128:1796-1804. (Pubitemid 40824690)
24. Andreola G, Rivoltini L, Castelli C, et al. Induction of lymphocyte apoptosis by tumor cell secretion of FasL-bearing microvesicles. J Exp Med. 2002;195:1303-1316. (Pubitemid 34564332)
25. Monleon I, Martinez-Lorenzo MJ, Monteagudo L, et al. Differential secretion of Fas ligand- or APO2 ligand/TNF-related apoptosis-inducing ligand-carrying microvesicles during activation-induced death of human T cells. J Immunol. 2001;167:6736-6744. (Pubitemid 33144163)
26. Pegtel DM, Cosmopoulos K, Thorley-Lawson DA, et al. Functional delivery of viral miRNAs via exosomes. Proc Natl Acad Sci U S A. 2010;107:6328-6333.
27. Meckes DG, Jr, Shair KH, Marquitz AR, et al. Human tumor virus utilizes exosomes for intercellular communication. Proc Natl Acad Sci U S A. 2010;107:20370- 20375.
28. Skog J, Wurdinger T, van Rijn S, et al. Glioblastoma microvesicles transport RNA and proteins that promote tumour growth and provide diagnostic biomarkers. Nat Cell Biol. 2008;10:1470-1476.
29. Cho JA, Park H, Lim EH, Lee KW. Exosomes from breast cancer cells can convert adipose tissue-derived mesenchymal stem cells into myofibroblast-like cells. Int J Oncol. 2012;40:130-138 .
30. Yang M, Chen J, Su F, et al. Micro-vesicles secreted by macrophages shuttle invasion-potentiating microRNAs into breast cancer cells. Mol Cancer. 2011; 10 :117 .
31. Kogure T, Lin WL, Yan IK, Braconi C, Patel T. Intercellular nanovesicle-mediated microRNA transfer: a mechanism of environmental modulation of hepatocellular cancer cell growth. Hepatology. 2011;54:1237-1248.
32. Aung T, Chapuy B, Vogel D, et al. Exosomal evasion of humoral immu-notherapy in aggressive B-cell lym-phoma modulated by ATP-binding cassette transporter A3. Proc Natl Acad Sci U S A. 2011;108:15336-15341 .
33. Vella LJ, Sharples RA, Lawson VA, et al. Packaging of prions into exo-somes is associated with a novel pathway of PrP processing. J Pathol. 2007;211(5):582-590. (Pubitemid 46502435)
34. Fevrier B, Vilette D, Archer F, et al. Cells release prions in association with exosomes. Proc Natl Acad Sci U S A. 2004;101:9683-9688. (Pubitemid 38869296)
35. Porto-Carreiro I, Fevrier B, Paquet S, et al. Prions and exosomes: from PrPc trafficking to PrPsc propagation. Blood Cells Mol Dis. 2005;35:143-148. (Pubitemid 41267041)
36. Tasaki M, Ueda M, Ochiai S, et al. Transmission of circulating cell-free AA amyloid oligomers in exosomes vectors via a prion-like mechanism. Biochem Biophys Res Commun. 2010; 400:559-562.
37. Takahashi RH, Milner TA, Li F, et al. Intraneuronal Alzheimer β42 accumulates in multivesicular bodies and is associated with synaptic pathology. Am J Pathol. 2002;161: 1869-1879. (Pubitemid 35265544)
38. Lublin AL, Gandy S. Amyloid-ß oligomers: possible roles as key neu-rotoxins in Alzheimer's disease. Mt Sinai J Med. 2010;77:43-49.
39. Aronin N, Kim M, Laforet G, DiFi-glia M. Are there multiple pathways in the pathogenesis of Huntington's disease? Philos Trans R Soc Lond B Biol Sci. 1999;354:995-1003.
40. Sapp E, Schwarz C, Chase K, et al. Huntingtin localization in brains of normal and Huntington's disease patients. Ann Neurol. 1997;42:604-612 . (Pubitemid 27439023)
41. Pan BT, Teng K, Wu C, et al. Electron microscopic evidence for exter-nalization of the transferrin receptor in vesicular form in sheep reticulo-cytes. J Cell Biol. 1985;101:942-948. (Pubitemid 16256847)
42. Tan A, Rajadas J, Seifalian AM. Exosomes as nano-theranostic delivery platforms for gene therapy. Adv Drug Deliv Rev. 2013;65:357-367.
43. Quesenberry PJ, Aliotta JM. Cellular phenotype switching and microvesicles. Adv Drug Deliv Rev. 2010;62:1141-1148.
44. Reiners KS, Dassler J, Coch C, Pogge von Strandmann E. Role of exo-somes released by dendritic cells and/or by tumor targets: regulation of NK cell plasticity. Front Immunol. 2014;5:91.
45. Chaput N, Flament C, Viaud S, et al. Dendritic cell derived-exosomes: biology and clinical implementations. J Leukoc Biol. 2006;80:471-478. (Pubitemid 44835779)
46. Andre F, Schartz NE, Movassagh M, et al. Malignant effusions and immu-nogenic tumour-derived exosomes. Lancet. 2002;360:295-305. (Pubitemid 34874721)
47. World Health Organization. World Cancer Report 2014. Geneva, Switzerland: World Health Organization; 2014.
48. Tan A, De La Pena H, Seifalian AM. The application of exosomes as a nanoscale cancer vaccine. Int J Nanomed. 2010;5:889-900.
49. Koos D, Josephs SF, Alexandrescu DT, et al. Tumor vaccines in 2010: need for integration. Cell Immunol. 2010;263:138-147.
50. Weber J, Sondak VK, Scotland R, et al. Granulocyte-macrophage-colony- stimulating factor added to a multi-peptide vaccine for resected stage II melanoma. Cancer. 2003;97:186-200. (Pubitemid 36033878)
51. Hodge JW, Chakraborty M, Kudo-Saito C, et al. Multiple costimula-tory modalities enhance CTL avidity. J Immunol. 2005;174:5994-6004. (Pubitemid 40663786)
52. Thery C. Exosomes: secreted vesicles and intercellular communications. F1000 Biology Rep. 2011;3:15.
53. Liu T, Mendes DE, Berkman CE. Functional prostate-specific membrane antigen is enriched in exo-somes from prostate cancer cells. Int J Oncol. 2014;44:918-922.
54. Khan S, Ferguson Bennit H, Turay D, et al. Early diagnostic value of Sur-vivin and its alternative splice variants in breast cancer. BMC Cancer. 2014;14:176.
55. Suetsugu A, Honma K, Saji S, et al. Imaging exosome transfer from breast cancer cells to stroma at metastatic sites in orthotopic nude-mouse models. Adv Drug Deliv Rev. 2013;65:383-390.
56. Simpson RJ, Jensen SS, Lim JW. Proteomic profiling of exosomes: current perspectives. Proteomics. 2008; 8:4083-4099.
57. van Dommelen SM, Vader P, Lakhal S, et al. Microvesicles and exosomes: opportunities for cell-derived membrane vesicles in drug delivery. J Control Release. 2012;161:635-644.