Exosomes as Tools to Suppress Primary Brain Tumor

Cellular and Molecular Neurobiology

Volumn 36, Issue 3, 2016, Pages 343-352

  Katakowski, Mark ^a   Chopp, Michael ^a,b  

^a HENRY FORD HOSPITAL   (United States)

^b OAKLAND UNIVERSITY   (United States)

Author keywords

Brain tumor; Exosome therapy; Exosomes; Glioblastoma; Glioma; miRNA

Indexed keywords

DRUG VEHICLE; NUCLEOTIDE; ANTINEOPLASTIC AGENT; DRUG CARRIER;

BRAIN TUMOR; CANCER IMMUNOTHERAPY; CANCER INHIBITION; DRUG DELIVERY SYSTEM; EXOSOME; HUMAN; IMMUNOMODULATION; NONHUMAN; PRIMARY TUMOR; PRIORITY JOURNAL; REVIEW; ANIMAL; BRAIN NEOPLASMS; CHEMISTRY; DRUG EFFECTS; IMMUNOTHERAPY; METABOLISM;

ANIMALS; ANTINEOPLASTIC AGENTS; BRAIN NEOPLASMS; DRUG CARRIERS; DRUG DELIVERY SYSTEMS; EXOSOMES; HUMANS; IMMUNOTHERAPY;

EID: 84961214830     PISSN: 02724340     EISSN: 15736830     Source Type: Journal    
DOI: 10.1007/s10571-015-0280-9     Document Type: Review

References (119)

1. 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
2. Andre F et al (2002) Tumor-derived exosomes: a new source of tumor rejection antigens. Vaccine 20(Suppl 4):A28–A31
3. Anthony DF, Shiels PG (2013) Exploiting paracrine mechanisms of tissue regeneration to repair damaged organs. Transpl Res 2:10. doi:10.1186/2047-1440-2-10
4. Ardon H et al (2012) Integration of autologous dendritic cell-based immunotherapy in the standard of care treatment for patients with newly diagnosed glioblastoma: results of the HGG-2006 phase I/II trial. Cancer Immunol Immunother 61:2033–2044
5. Arroyo JD et al (2011) Argonaute2 complexes carry a population of circulating microRNAs independent of vesicles in human plasma. Proc Natl Acad Sci USA 108:5003–5008
6. Arslantas A et al (2007) Genomic alterations in low-grade, anaplastic astrocytomas and glioblastomas. Pathol Oncol Res 13:39–46
7. Azmi AS, Bao B, Sarkar FH (2013) Exosomes in cancer development, metastasis, and drug resistance: a comprehensive review. Cancer Metastasis Rev 32:623–642
8. Balaj L, Lessard R, Dai L, Cho YJ, Pomeroy SL, Breakefield XO, Skog J (2011) Tumour microvesicles contain retrotransposon elements and amplified oncogene sequences. Nat Commun 2:180
9. Bao S et al (2006) Glioma stem cells promote radioresistance by preferential activation of the DNA damage response. Nature 444:756–760
10. Barbano R et al (2014) A miRNA signature for defining aggressive phenotype and prognosis in gliomas. PLoS One 9:e108950
11. Barua NU, Gill SS, Love S (2014) Convection-enhanced drug delivery to the brain: therapeutic potential and neuropathological considerations. Brain Pathol 24(2):117–127
12. Baxevanis CN, Papamichail M, Perez SA (2015) Prostate cancer vaccines: the long road to clinical application. Cancer Immunol Immunother 64:401–408
13. Bronisz A et al (2014) Extracellular vesicles modulate the glioblastoma microenvironment via a tumor suppression signaling network directed by miR-1. Cancer Res 74:738–750
14. Bu N et al (2015a) Exosome from chaperone-rich cell lysates-loaded dendritic cells produced by CELLine 1000 culture system exhibits potent immune activity. Biochem Biophys Res Commun 456:513–518
15. Bu N et al (2015b) Exosomes from dendritic cells loaded with chaperone-rich cell lysates elicit a potent T cell immune response against intracranial glioma in mice. J Mol Neurosci 56:631–643
16. Challagundla KB et al (2015) Exosome-mediated transfer of microRNAs within the tumor microenvironment and neuroblastoma resistance to chemotherapy. J Natl Cancer Inst. doi:10.1093/jnci/djv135
17. Chaput N, Taieb J, Schartz NE, Andre F, Angevin E, Zitvogel L (2004) Exosome-based immunotherapy Cancer Immunol Immunother 53:234–239
18. Chen KG et al (2006) Melanosomal sequestration of cytotoxic drugs contributes to the intractability of malignant melanomas. Proc Natl Acad Sci USA 103:9903–9907
19. Chen TS et al (2011) Enabling a robust scalable manufacturing process for therapeutic exosomes through oncogenic immortalization of human ESC-derived MSCs. J Transl Med 9:47
20. Cho DY et al (2013) Targeting cancer stem cells for treatment of glioblastoma multiforme. Cell Transplant 22:731–739
21. Christianson HC, Svensson KJ, van Kuppevelt TH, Li JP, Belting M (2013) Cancer cell exosomes depend on cell-surface heparan sulfate proteoglycans for their internalization and functional activity. Proc Natl Acad Sci USA 110:17380–17385
22. Cocucci E, Meldolesi J (2015) Ectosomes and exosomes: shedding the confusion between extracellular vesicles. Trends Cell Biol 25:364–372
23. Delcayre A, Shu H, Le Pecq JB (2005) Dendritic cell-derived exosomes in cancer immunotherapy: exploiting nature’s antigen delivery pathway. Expert Rev Anticancer Ther 5:537–547
24. Denzer K, Kleijmeer MJ, Heijnen HF, Stoorvogel W, Geuze HJ (2000) Exosome: from internal vesicle of the multivesicular body to intercellular signaling device. J Cell Sci 113(19):3365–3374
25. Dillman RO et al (2004) Intracavitary placement of autologous lymphokine-activated killer (LAK) cells after resection of recurrent glioblastoma. J Immunother 27:398–404
26. El-Andaloussi S et al (2012) Exosome-mediated delivery of siRNA in vitro and in vivo. Nat Protoc 7:2112–2126
27. Escudier B et al (2005) Vaccination of metastatic melanoma patients with autologous dendritic cell (DC) derived-exosomes: results of thefirst phase I clinical trial. J Transl Med 3:10
28. Fabbri M, Croce CM, Calin GA (2008) MicroRNAs Cancer J 14:1–6
29. Feng D et al (2010) Cellular internalization of exosomes occurs through phagocytosis. Traffic 11:675–687
30. Gabriely G et al (2011) Human glioma growth is controlled by microRNA-10b. Cancer Res 71:3563–3572
31. Gallo A, Tandon M, Alevizos I, Illei GG (2012) The majority of microRNAs detectable in serum and saliva is concentrated in exosomes. PLoS ONE 7:e30679
32. Geletneky K et al (2012) Phase I/IIa study of intratumoral/intracerebral or intravenous/intracerebral administration of Parvovirus H-1 (ParvOryx) in patients with progressive primary or recurrent glioblastoma multiforme: ParvOryx01 protocol. BMC Cancer 12:99
33. Gheldof D, Mullier F, Chatelain B, Dogne JM, Chatelain C (2013) Inhibition of tissue factor pathway inhibitor increases the sensitivity of thrombin generation assay to procoagulant microvesicles. Blood Coagul Fibrinolysis 24:567–572. doi:10.1097/MBC.0b013e328360a56e
34. Graner MW, Alzate O, Dechkovskaia AM, Keene JD, Sampson JH, Mitchell DA, Bigner DD (2009) Proteomic and immunologic analyses of brain tumor exosomes. Faseb J 23:1541–1557
35. 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 Genom 13:357
36. Hagiwara K, Ochiya T, Kosaka N (2014) A paradigm shift for extracellular vesicles as small RNA carriers: from cellular waste elimination to therapeutic applications. Drug Deliv Transl Res 4:31–37
37. Heddleston JM et al (2011) Glioma stem cell maintenance: the role of the microenvironment. Curr Pharm Des 17:2386–2401
38. Hu G, Drescher KM, Chen XM (2012) Exosomal miRNAs: Biological Properties and Therapeutic Potential. Front Genet 3:56
39. Iorio MV, Croce CM (2012a) MicroRNA dysregulation in cancer: diagnostics, monitoring and therapeutics. A comprehensive review. EMBO Mol Med 4:143–159
40. Iorio MV, Croce CM (2012b) microRNA involvement in human cancer. Carcinogenesis 33:1126–1133
41. Johnsen KB, Gudbergsson JM, Skov MN, Pilgaard L, Moos T, Duroux M (2014) A comprehensive overview of exosomes as drug delivery vehicles—endogenous nanocarriers for targeted cancer therapy. Biochim Biophys Acta 1846:75–87
42. Kahlert C, Kalluri R (2011) Exosomes in tumor microenvironment influence cancer progression and metastasis. J Mol Med (Berl) 91:431–437
43. Kang TW et al (2014) Growth arrest and forced differentiation of human primary glioblastoma multiforme by a novel small molecule. Sci Rep 4:5546
44. Katakowski M, Buller B, Wang X, Rogers T, Chopp M (2010a) Functional microRNA is transferred between glioma cells. Cancer Res 70:8259–8263
45. Katakowski M, Zheng X, Jiang F, Rogers T, Szalad A, Chopp M (2010b) MiR-146b-5p suppresses EGFR expression and reduces in vitro migration and invasion of glioma. Cancer Invest 28:1024–1030
46. Katakowski M et al (2012) Exosomes from marrow stromal cells expressing miR-146b inhibit glioma growth. Cancer Lett 335:201–204
47. Keller S, Ridinger J, Rupp AK, Janssen JW, Altevogt P (2011) Body fluid derived exosomes as a novel template for clinical diagnostics. J Transl Med 9:86
48. Kooijmans SA, Vader P, van Dommelen SM, van Solinge WW, Schiffelers RM (2012) Exosome mimetics: a novel class of drug delivery systems. Int J Nanomed 7:1525–1541. doi:10.2147/IJN.S29661
49. Kooijmans SA et al (2013) Electroporation-induced siRNA precipitation obscures the efficiency of siRNA loading into extracellular vesicles. J Control Release 172:229–238
50. Lai RC, Yeo RW, Tan KH, Lim SK (2013) Exosomes for drug delivery—a novel application for the mesenchymal stem cell. Biotechnol Adv 31:543–551
51. Lee Y, El Andaloussi S, Wood MJ (2012) Exosomes and microvesicles: extracellular vesicles for genetic information transfer and gene therapy. Hum Mol Genet 21:R125–R134
52. Li J, Sherman-Baust CA, Tsai-Turton M, Bristow RE, Roden RB, Morin PJ (2009) Claudin-containing exosomes in the peripheral circulation of women with ovarian cancer. BMC Cancer 9:244
53. Markert JM et al (2009) Phase Ib trial of mutant herpes simplex virus G207 inoculated pre-and post-tumor resection for recurrent GBM. Mol Ther 17:199–207
54. Marsh M, van Meer G (2008) Cell biology. No ESCRTs for exosomes. Science 319:1191–1192
55. Mathivanan S, Ji H, Simpson RJ (2010) Exosomes: extracellular organelles important in intercellular communication. J Proteomics 73:1907–1920
56. Meckes DG Jr et al (2013) Modulation of B-cell exosome proteins by gamma herpesvirus infection. Proc Natl Acad Sci USA. doi:10.1073/pnas.1303906110
57. Miller IV, Grunewald TG (2015) Tumour-derived exosomes: tiny envelopes for big stories. Biol Cell. doi:10.1111/boc.201400095
58. Mittelbrunn M, Sanchez-Madrid F (2012) Intercellular communication: diverse structures for exchange of genetic information. Nat Rev Mol Cell Biol 13:328–335
59. Mittelbrunn M et al (2012) Unidirectional transfer of microRNA-loaded exosomes from T cells to antigen-presenting cells. Nat Commun 2:282
60. Momen-Heravi F, Bala S, Bukong T, Szabo G (2014) Exosome-mediated delivery of functionally active miRNA-155 inhibitor to macrophages. Nanomedicine 10(7):1517–1527
61. Morse MA et al (2005) A phase I study of dexosome immunotherapy in patients with advanced non-small cell lung cancer. J Transl Med 3:9
62. Munoz JL, Bliss SA, Greco SJ, Ramkissoon SH, Ligon KL, Rameshwar P (2013) Delivery of functional anti-miR-9 by mesenchymal stem cell-derived exosomes to glioblastoma multiforme cells conferred chemosensitivity. Mol Ther Nucleic Acids 2:e126
63. Nazarenko I, Rupp AK, Altevogt P (2013) Exosomes as a potential tool for a specific delivery of functional molecules. Methods Mol Biol 1049:495–511
64. Nicoloso MS, Calin GA (2008) MicroRNA involvement in brain tumors: from bench to bedside. Brain Pathol 18:122–129
65. Nolte-’t Hoen EN, Buermans HP, Waasdorp M, Stoorvogel W, Wauben MH, t Hoen PA (2012) Deep sequencing of RNA from immune cell-derived vesicles uncovers the selective incorporation of small non-coding RNA biotypes with potential regulatory functions. Nucleic Acids Res 40:9272–9285
66. Ohno S et al (2013) Systemically injected exosomes targeted to EGFR deliver antitumor microRNA to breast cancer cells. Mol Ther 21:185–191
67. Okada H et al (2011) Induction of CD8+ T-cell responses against novel glioma-associated antigen peptides and clinical activity by vaccinations with {alpha}-type 1 polarized dendritic cells and polyinosinic-polycytidylic acid stabilized by lysine and carboxymethylcellulose in patients with recurrent malignant glioma. J Clin Oncol 29:330–336
68. Ono M et al (2014) Exosomes from bone marrow mesenchymal stem cells contain a microRNA that promotes dormancy in metastatic breast cancer cells. Sci Signal 7:ra63
69. Oshiro S et al (2006) Evaluation of intratumoral administration of tumor necrosis factor-alpha in patients with malignant glioma. Anticancer Res 26:4027–4032
70. Papagiannakopoulos T, Shapiro A, Kosik KS (2008) MicroRNA-21 targets a network of key tumor-suppressive pathways in glioblastoma cells. Cancer Res 68:8164–8172
71. Penfornis P, Vallabhaneni KC, Whitt J, Pochampally R (2015) Extracellular vesicles as carriers of microRNA, proteins and lipids in tumor microenvironment. Int J Cancer. doi:10.1002/ijc.29417
72. Pershouse MA, Stubblefield E, Hadi A, Killary AM, Yung WK, Steck PA (1993) Analysis of the functional role of chromosome 10 loss in human glioblastomas. Cancer Res 53:5043–5050
73. Piwecka M et al (2015) Comprehensive analysis of microRNA expression profile in malignant glioma tissues. Mol Oncol 9:1324–1340
74. Pritchard AL et al (2015) Exome sequencing to predict neoantigens in melanoma. Cancer Immunol Res. doi:10.1158/2326-6066
75. Qin J, Xu Q (2014) Functions and application of exosomes. Acta Pol Pharm 71:537–543
76. Ramachandran S, Palanisamy V (2012) Horizontal transfer of RNAs: exosomes as mediators of intercellular communication. Wiley Interdiscip Rev RNA 3:286–293
77. Rana S, Yue S, Stadel D, Zoller M (2012) Toward tailored exosomes: the exosomal tetraspanin web contributes to target cell selection. Int J Biochem Cell Biol 44:1574–1584
78. Raposo G, Stoorvogel W (2013) Extracellular vesicles: exosomes, microvesicles, and friends. J Cell Biol 200:373–383
79. Raposo G, Nijman HW, Stoorvogel W, Liejendekker R, Harding CV, Melief CJ, Geuze HJ (1996) B lymphocytes secrete antigen-presenting vesicles. J Exp Med 183:1161–1172
80. Rasheed BK, Fuller GN, Friedman AH, Bigner DD, Bigner SH (1992) Loss of heterozygosity for 10q loci in human gliomas. Genes Chromosomes Cancer 5:75–82
81. Romagnoli GG, Zelante BB, Toniolo PA, Migliori IK, Barbuto JA (2015) Dendritic cell-derived exosomes may be a tool for cancer immunotherapy by converting tumor cells into immunogenic targets. Front Immunol 5:692
82. Safaei R, Larson BJ, Cheng TC, Gibson MA, Otani S, Naerdemann W, Howell SB (2005) Abnormal lysosomal trafficking and enhanced exosomal export of cisplatin in drug-resistant human ovarian carcinoma cells. Mol Cancer Ther 4:1595–1604
83. Saito R et al (2006) Tissue affinity of the infusate affects the distribution volume during convection-enhanced delivery into rodent brains: implications for local drug delivery. J Neurosci Methods 154:225–232
84. Salmaggi A et al (2006) Glioblastoma-derived tumorospheres identify a population of tumor stem-like cells with angiogenic potential and enhanced multidrug resistance phenotype. Glia 54:850–860
85. Sampson JH et al (2009) An epidermal growth factor receptor variant III-targeted vaccine is safe and immunogenic in patients with glioblastoma multiforme. Mol Cancer Ther 8:2773–2779
86. Santiago-Dieppa DR, Steinberg J, Gonda D, Cheung VJ, Carter BS, Chen CC (2014) Extracellular vesicles as a platform for ‘liquid biopsy’ in glioblastoma patients. Expert Rev Mol Diagn 14:819–825
87. Shao H et al (2012) Protein typing of circulating microvesicles allows real-time monitoring of glioblastoma therapy. Nat Med 18:1835–1840
88. Shedden K, Xie XT, Chandaroy P, Chang YT, Rosania GR (2003) Expulsion of small molecules in vesicles shed by cancer cells: association with gene expression and chemosensitivity profiles. Cancer Res 63:4331–4337
89. Shelke GV, Lasser C, Gho YS, Lotvall J (2014) Importance of exosome depletion protocols to eliminate functional and RNA-containing extracellular vesicles from fetal bovine serum. J Extracell Vesicles. doi:10.3402/jev.v3.24783
90. Shimbo K, Miyaki S, Ishitobi H, Kato Y, Kubo T, Shimose S, Ochi M (2014) Exosome-formed synthetic microRNA-143 is transferred to osteosarcoma cells and inhibits their migration. Biochem Biophys Res Commun 445:381–387
91. Silber J, James CD, Hodgson JG (2009) microRNAs in gliomas: small regulators of a big problem. Neuromolecular Med 11:208–222
92. Singh M, Overwijk WW (2015) Intratumoral immunotherapy for melanoma Cancer. Immunol Immunother 64:911–921
93. Skog J et al (2008) Glioblastoma microvesicles transport RNA and proteins that promote tumour growth and provide diagnostic biomarkers. Nat Cell Biol 10:1470–1476
94. Smyth T, Kullberg M, Malik N, Smith-Jones P, Graner MW, Anchordoquy TJ (2015) Biodistribution and delivery efficiency of unmodified tumor-derived exosomes. J Control Release 199:145–155
95. Sun Y, Liu J (2014) Potential of cancer cell-derived exosomes in clinical application: a review of recent research advances. Clin Ther 36(6):863–872
96. Sun D et al (2010) A novel nanoparticle drug delivery system: the anti-inflammatory activity of curcumin is enhanced when encapsulated in exosomes. Mol Ther 18:1606–1614
97. Tan CY, Lai RC, Wong W, Dan YY, Lim SK, Ho HK (2014) Mesenchymal stem cell-derived exosomes promote hepatic regeneration in drug-induced liver injury models. Stem Cell Res Ther 5:76
98. Tavoosidana G et al (2011) Multiple recognition assay reveals prostasomes as promising plasma biomarkers for prostate cancer. Proc Natl Acad Sci USA 108:8809–8814
99. Thery C (2011) Exosomes: secreted vesicles and intercellular communications F1000. Biol Rep 3:15
100. Tian Y et al (2014) A doxorubicin delivery platform using engineered natural membrane vesicle exosomes for targeted tumor therapy. Biomaterials 35:2383–2390
101. Tickner JA, Urquhart AJ, Stephenson SA, Richard DJ, O’Byrne KJ (2014) Functions and therapeutic roles of exosomes in cancer Front. Oncol 4:127
102. Turner JD, Williamson R, Almefty KK, Nakaji P, Porter R, Tse V, Kalani MY (2010) The many roles of microRNAs in brain tumor biology. Neurosurg Focus 28:E3
103. Utsugi-Kobukai S, Fujimaki H, Hotta C, Nakazawa M, Minami M (2003) MHC class I-mediated exogenous antigen presentation by exosomes secreted from immature and mature bone marrow derived dendritic cells. Immunol Lett 89:125–131
104. Valadi H, Ekstrom K, Bossios A, Sjostrand M, Lee JJ, Lotvall JO (2007) Exosome-mediated transfer of mRNAs and microRNAs is a novel mechanism of genetic exchange between cells. Nat Cell Biol 9:654–659
105. Vickers KC, Palmisano BT, Shoucri BM, Shamburek RD, Remaley AT (2011) MicroRNAs are transported in plasma and delivered to recipient cells by high-density lipoproteins. Nat Cell Biol 13:423–433
106. Vik-Mo EO et al (2013) Therapeutic vaccination against autologous cancer stem cells with mRNA-transfected dendritic cells in patients with glioblastoma. Cancer Immunol Immunother 62:1499–1509
107. Villarroya-Beltri C et al (2013) Sumoylated hnRNPA2B1 controls the sorting of miRNAs into exosomes through binding to specific motifs. Nat Commun 4:2980
108. Wahlgren J, De LKT, Brisslert M, Vaziri Sani F, Telemo E, Sunnerhagen P, Valadi H (2012) Plasma exosomes can deliver exogenous short interfering RNA to monocytes and lymphocytes. Nucleic Acids Res 40:e130
109. Wheeler CJ et al (2008) Vaccination elicits correlated immune and clinical responses in glioblastoma multiforme patients. Cancer Res 68:5955–5964
110. Wolfers J et al (2001) Tumor-derived exosomes are a source of shared tumor rejection antigens for CTL cross-priming. Nat Med 7:297–303
111. Xin H et al (2012) Exosome mediated transfer of miR-133b from multipotent mesenchymal stromal cells to neural cells contributes to neurite outgrowth. Stem Cells 30(7):1556–1564
112. Xin H, Li Y, Chopp M (2014) Exosomes/miRNAs as mediating cell-based therapy of stroke Front Cell Neurosci 8:377
113. Yang C, Robbins PD (2011) The roles of tumor-derived exosomes in cancer pathogenesis. Clin Dev Immunol 2011:842849
114. Yang T et al (2015) Exosome delivered anticancer drugs across the blood-brain barrier for brain cancer therapy in Danio rerio. Pharm Res 32:2003–2014
115. 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
116. Zhang Y, Dutta A, Abounader R (2012) The role of microRNAs in glioma initiation and progression. Front Biosci 17:700–712
117. Zhang Y, Chopp M, Meng Y, Katakowski M, Xin H, Mahmood A, Xiong Y (2015) Effect of exosomes derived from multipluripotent mesenchymal stromal cells on functional recovery and neurovascular plasticity in rats after traumatic brain injury. J Neurosurg 122:856–867
118. Zhou J et al (2013) Highly penetrative, drug-loaded nanocarriers improve treatment of glioblastoma. Proc Natl Acad Sci USA 110:11751–11756
119. Zitvogel L et al (1998) Eradication of established murine tumors using a novel cell-free vaccine: dendritic cell-derived exosomes. Nat Med 4:594–600