Extracellular vesicles as shuttles of tumor biomarkers and antitumor drugs

Frontiers in Oncology

Volumn 4, Issue SEP, 2014, Pages

  Zocco, Davide ^a   Ferruzzi, Pietro ^a   Cappello, Francesco ^b   Kuo, Winston Patrick ^c   Fais, Stefano ^d  

^a Exosomics Siena Spa Siena ^*  (Italy)

^b UNIVERSITY OF PALERMO   (Italy)

^c IES Diagnostics   (United States)

^d ISTITUTO SUPERIORE DI SANITÀ   (Italy)

Author keywords

Biomarkers; Exosomes; Extracellular vesicles; Teranostics; Tumors

Indexed keywords

ANTINEOPLASTIC AGENT; BIOLOGICAL MARKER; CETUXIMAB; PROSTATE SPECIFIC ANTIGEN; PROSTATE SPECIFIC MEMBRANE ANTIGEN;

ARTICLE; CANCER GROWTH; CHEMOSENSITIZATION; DIGITAL RECTAL EXAMINATION; EXOSOME; GENE EXPRESSION; GENE MUTATION; HUMAN; MASS SPECTROMETRY; MEMBRANE VESICLE; NANOMEDICINE; PERSONALIZED MEDICINE; PROSTATE CANCER; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; SENSITIVITY AND SPECIFICITY;

EID: 84907046756     PISSN: None     EISSN: 2234943X     Source Type: Journal    
DOI: 10.3389/fonc.2014.00267     Document Type: Article

References (65)

1. Koga K, Matsumoto K, Akiyoshi T et at. Purification, characterization and biological significance of tumor-derived exosomes. Anticancer research, 25(6A), 3703-3707 (2005).
2. Logozzi M, De Milito A, Lugini L et at. High levels of exosomes expressing CD63 and caveolin-1 in plasma of melanoma patients. PloS one, 4(4), e5219 (2009).
3. Thakur BK, Zhang H, Becker A, Matei I, Huang Y, Costa-Silva B, Zheng Y, Hoshino A, Brazier H, Xiang J, Williams C, Rodriguez-Barrueco R, Silva JM, Zhang W, Hearn S, Elemento O, Paknejad N, Manova-Todorova K, Welte K, Bromberg J, Peinado H, Lyden D. Double-stranded DNA in exosomes: a novel biomarker in cancer detection. Cell Res. 2014 Jun;24(6):766-9.
4. Federici C, Petrucci F, Caimi S, Cesolini A, Logozzi M, Borghi M, D'llio S, Lugini L, Violante N, Azzarito T, Majorani C, Brambilla D, Fais S. Exosome release and low pH belong to a framework of resistance of human melanoma cells to cisplatin. PLoS One. 2014 Feb 6;9(2):e88193.
5. Jang SC, Kim OY, Yoon CM et al. Bioinspired exosome-mimetic nanovesicles for targeted delivery of chemotherapeutics to malignant tumors. ACS nano, 7(9), 7698-7710 (2013).
6. Zitvogel L, Regnault A, Lozier A et al. Eradication of established murine tumors using a novel cellfree vaccine: dendritic cell-derived exosomes. Nature medicine, 4(5), 594-600 (1998).
7. Mitchell PJ, Welton J, Staffurth J et al. Can urinary exosomes act as treatment response markers in prostate cancer? Journal of translational medicine, 7, 4 (2009).
8. Taylor DD, Gercel-Taylor C. MicroRNA signatures of tumor-derived exosomes as diagnostic biomarkers of ovarian cancer. Gynecologic oncology, 110(1), 13-21 (2008).
9. Dijkstra S, Birker IL, Smit FP et al. Prostate cancer biomarker profiles in urinary sediments and exosomes. The Journal of urology, 191(4), 1132-1138 (2014).
10. Peinado H, Aleckovic M, Lavotshkin S et al. Melanoma exosomes educate bone marrow progenitor cells toward a pro-metastatic phenotype through MET. Nature medicine, 18(6), 883-891 (2012).
11. Rappa F, Farina F, Zummo G et al. HSP-molecular chaperones in cancer biogenesis and tumor therapy: an overview. Anticancer research, 32(12), 5139-5150 (2012).
12. Lancaster Gl, Febbraio MA. Exosome-dependent trafficking of HSP70: a novel secretory pathway for cellular stress proteins. The Journal of biological chemistry, 280(24), 23349-23355 (2005).
13. Vega VL, Rodriguez-Silva M, Frey T et al. Hsp70 translocates into the plasma membrane after stress and is released into the extracellular environment in a membrane-associated form that activates macrophages. J Immunol, 180(6), 4299-4307 (2008).
14. 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 research, 65(12), 5238-5247 (2005).
15. Lv LH, Wan YL, Lin Y et al. Anticancer drugs cause release of exosomes with heat shock proteins from human hepatocellular carcinoma cells that elicit effective natural killer cell antitumor responses in vitro. The Journal of biological chemistry, 287(19), 15874-15885 (2012).
16. McCready J, Sims JD, Chan D, Jay DG. Secretion of extracellular hsp90alpha via exosomes increases cancer cell motility: a role for plasminogen activation. BMC cancer, 10, 294 (2010).
17. Khan S, Jutzy JM, Valenzuela MM et al. Plasma-derived exosomal survivin, a plausible biomarker for early detection of prostate cancer. PloS one, 7(10), e46737 (2012).
18. Dijkstra S, Birker IL, Smit FP et al. Prostate cancer biomarker profiles in urinary sediments and exosomes. The Journal of urology, 191(4), 1132-1138 (2014).
19. Mizutani K, Terazawa R, Kameyama K, Kato T, Horie K, Tsuchiya T, Seike K, Ehara H, Fujita Y, Kawakami K, Ito M, Deguchi T. Isolation of prostate cancer-related exosomes. Anticancer Res. 2014Jul;34(7):3419-23
20. Ogata-Kawata H, Izumiya M, Kurioka D, Honma Y, Yamada Y, Furuta K, Gunji T, Ohta H, Okamoto H, Sonoda H, Watanabe M, Nakagama H, Yokota J, Kohno T, Tsuchiya N. Circulating exosomal microRNAs as biomarkers of colon cancer. PLoS One. 2014 Ap4;9(4):e92921
21. Standardization of sample collection, isolation and analysis methods in extracellular vesicle research. Witwer KW, Buzas El, Bemis LT, Bora A, Lasser C, Lotvall J, Nolte-'t Hoen EN, Piper MG, Sivaraman S, Skog J, Thery C, Wauben MH, Hochberg F. J Extracell Vesicles. 2013 May 27;2
22. Szajnik M, Derbis M, Lach M et at. Exosomes in Plasma of Patients with Ovarian Carcinoma: Potential Biomarkers of Tumor Progression and Response to Therapy. Gynecol Obstet (Sunnyvale), Suppl 4, 3 (2013).
23. Kahlert C, Melo SA, Protopopov A, Tang J, Seth S, Koch M, Zhang J, Weitz J, Chin L, Futreal A, Kalluri R. Identification of double-stranded genomic DNA spanning all chromosomes with mutated KRAS and p53 DNA in the serum exosomes of patients with pancreatic cancer./Biol Chem. 2014 Feb 14;289(7):3869-75.
24. Yamashita T, Kamada H, Kanasaki S et at. Epidermal growth factor receptor localized to exosome membranes as a possible biomarker for lung cancer diagnosis. Die Pharmazie, 68(12), 969-973 (2013).
25. Duijvesz D, Burnum-Johnson KE, Gritsenko MA et at. Proteomic profiling of exosomes leads to the identification of novel biomarkers for prostate cancer. PloS one, 8(12), e82589 (2013).
26. Andre F, Escudier B, Angevin E, Tursz T, Zitvogel L. Exosomes for cancer immunotherapy. Annals of oncology: official journal of the European Society for Medical Oncology/ESMO, 15 Suppl 4, ivl41-144 (2004).
27. Hood JL et al. Exosomes released by melanoma cells prepare sentinel lymph nodes for tumor metastasis. Cancer Res 2011: 71 (11): 3792-801.
28. Lero M et al. Tumour-released exosomes and their implications in cancer immunity. Cell Death Differ 2008:15(1): 80-8.
29. Skog J, Wurdinger T, van Rijn S et al. Glioblastoma microvesicles transport RN A and proteins that promote tumour growth and provide diagnostic biomarkers. Nature cell biology, 10(12), 1470-1476 (2008).
30. Andreola G, Rivoltini L, Castelli C et al. Induction of lymphocyte apoptosis by tumor cell secretion of FasL-bearing microvesicles. The Journal of experimental medicine, 195(10), 1303-1316 (2002).
31. Huber V, Fais S, lero M et al. Human colorectal cancer cells induce T-cell death through release of proapoptotic microvesicles: role in immune escape. Gastroenterology, 128(7), 1796-1804 (2005).
32. Parolini I, Federici C, Raggi C et al. Microenvironmental pH is a key factor for exosome traffic in tumor cells. The Journal of biological chemistry, 284(49), 34211-34222 (2009).
33. De Milito A, Fais S. Tumor acidity, chemoresistance and proton pump inhibitors. Future Oncol, 1(6), 779-786 (2005).
34. Ferrari S, Perut F, Fagioli F et al. Proton pump inhibitor chemosensitization in human osteosarcoma: from the bench to the patients' bed. Journal of translational medicine, 11, 268 (2013).
35. Luciani F, Spada M, De Milito A et al. Effect of proton pump inhibitor pretreatment on resistance of solid tumors to cytotoxic drugs. Journal of the National Cancer Institute, 96(22), 1702-1713 (2004).
36. 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. Nature biotechnology, 29(4), 341-345 (2011).
37. Zeelenberg IS, Ostrowski M, Krumeich S et al. Targeting tumor antigens to secreted membrane vesicles in vivo induces efficient antitumor immune responses. Cancer research, 68(4), 1228-1235 (2008).
38. El-Andaloussi S, Lee Y, Lakhal-Littleton S, Li J, Seow Y, Gardiner C, Alvarez-Erviti L, Sargent IL, Wood MJ. Exosome-mediated delivery of siRNA in vitro and in vivo. Nat Protoc. 2012 Dec;7(12):2112-26.
39. Akao Y, Mo A, Itoh T et al. Microvesicle-mediated RNA molecule delivery system using monocytes/macrophages. Molecular therapy: the journal of the American Society of Gene Therapy, 19(2), 395-399 (2011).
40. Putz U, Howitt J, Doan A et al. The tumor suppressor PTEN is exported in exosomes and has phosphatase activity in recipient cells. Science signaling, 5(243), ra70 (2012).
41. Hergenreider E, Heydt S, Treguer K et al. Atheroprotective communication between endothelial cells and smooth muscle cells through miRNAs. Nature cell biology, 14(3), 249-256 (2012).
42. Kosaka N, Iguchi H, Yoshioka Y, Hagiwara K, Takeshita F, Ochiya T. Competitive interactions of cancer cells and normal cells via secretory microRNAs. The Journal of biological chemistry, 287(2), 1397-1405 (2012).
43. Mizrak A, Bolukbasi MF, Ozdener GB et al. Genetically engineered microvesicles carrying suicide mRNA/protein inhibit schwannoma tumor growth. Molecular therapy: the journal of the American Society of Gene Therapy, 21(1), 101-108 (2013).
44. Ohno S, Takanashi M, Sudo K et al. Systemically injected exosomes targeted to EGFR deliver antitumor microRNA to breast cancer cells. Molecular therapy: the journal of the American Society of Gene Therapy, 21(1), 185-191 (2013).
45. Rechavi O, Erlich Y, Amram H et al. Cell contact-dependent acquisition of cellular and viral nonautonomously encoded small RNAs. Genes & development, 23(16), 1971-1979 (2009).
46. Sun D, Zhuang X, Xiang X et al. A novel nanoparticle drug delivery system: the anti-inflammatory activity of curcumin is enhanced when encapsulated in exosomes. Molecular therapy: the journal of the American Society of Gene Therapy, 18(9), 1606-1614 (2010).
47. Zhuang X, Xiang X, Grizzle W et al. Treatment of brain inflammatory diseases by delivering exosome encapsulated anti-inflammatory drugs from the nasal region to the brain. Molecular therapy: the journal of the American Society of Gene Therapy, 19(10), 1769-1779 (2011).
48. Shen B, Wu N, Yang JM, Gould SJ. Protein targeting to exosomes/microvesicles by plasma membrane anchors. The Journal of biological chemistry, 286(16), 14383-14395 (2011).
49. Lugini L, Cecchetti S, Huber V et al. Immune surveillance properties of human NK cell-derived exosomes. J Immunol, 189(6), 2833-2842 (2012).
50. Pitt JM, Charrier M, Viaud S, Andre F, Besse B, Chaput N, Zitvogel L. Dendritic Cell-Derived Exosomes as Immunotherapies in the Fight against Cancer. J Immunol. 2014 Aug l;193(3):1006-1011.
51. Lamparski HG, Metha-Damani A, Yao JY et al. Production and characterization of clinical grade exosomes derived from dendritic cells. Journal of immunological methods, 270(2), 211-226 (2002).
52. Escudier B, Dorval T, Chaput N et al. Vaccination of metastatic melanoma patients with autologous dendritic cell (DC) derived-exosomes: results of thefirst phase I clinical trial. Journal of translational medicine, 3(1), 10 (2005).
53. Morse MA, Garst J, Osada T et al. A phase I study of dexosome immunotherapy in patients with advanced non-small cell lung cancer. Journal of translational medicine, 3(1), 9 (2005).
54. Viaud S, Terme M, Flament C, Taieb J, Andre F, Novault S, Escudier B, Robert C, Caillat-Zucman S, Tursz T, Zitvogel L, Chaput N. Dendritic cell-derived exosomes promote natural killer cell activation and proliferation: a role for NKG2D ligands and IL-15Ralpha. PLoS One. 2009;4(3)
55. Viaud S, Ploix S, Lapierre V, Thery C, Commere PH, Tramalloni D, Gorrichon K, Virault-Rocroy P, Tursz T, Lantz O, Zitvogel L, Chaput N. Updated technology to produce highly immunogenic dendritic cell-derived exosomes of clinical grade: a critical role of interferon-y. J Immunother. 2011Jan;34(1):65-75. doi: 10.1097/CJI.0b013e3181fe535b
56. Dai S, Wei D, Wu Z et al. Phase I clinical trial of autologous ascites-derived exosomes combined with GM-CSF for colorectal cancer. Molecular therapy: the journal of the American Society of Gene Therapy, 16(4), 782-790 (2008).
57. Bettegowda C, Sausen M, Leary RJ et al. Detection of circulating tumor DNA in early- and latestage human malignancies. Science translational medicine, 6(224), 224ra224 (2014).
58. Yap TA, Lorente D, Omlin A, Olmos D, de Bono JS. Circulating tumor cells: a multifunctional biomarker. Clinical cancer research: an official journal of the American Association for Cancer Research, 20(10), 2553-2568 (2014).
59. Cazzoli R, Buttitta F, Di Nicola M, Malatesta S, Marchetti A, Rom WN, Pass HI. microRNAs derived from circulating exosomes as noninvasive biomarkers for screening and diagnosing lung cancer. J Thorac Oncol. 2013 Sep;8(9):1156-62.
60. Manterola L, Guruceaga E, Gallego Perez-Larraya J et at. A small noncoding RNA signature found in exosomes of GBM patient serum as a diagnostic tool. Neuro-oncology, 16(4), 520-527 (2014).
61. Rupp AK, Rupp C, Keller S et at. Loss of EpCAM expression in breast cancer derived serum exosomes: role of proteolytic cleavage. Gynecologic oncology, 122(2), 437-446 (2011).
62. Tanaka Y, Kamohara H, Kinoshita K et af. Clinical impact of serum exosomal microRNA-21 as a clinical biomarker in human esophageal squamous cell carcinoma. Cancer, 119(6), 1159-1167 (2013).
63. Que R, Ding G, Chen J, Cao L. Analysis of serum exosomal microRNAs and clinicopathologic features of patients with pancreatic adenocarcinoma. World J Surg Oncol. 2013 Sep 4;11:219.
64. Gourzones C, Gelin A, Bombik. Extra-cellular release and blood diffusion of BART viral micro-RNAs produced by EBV-infected nasopharyngeal carcinoma cells. Virol J 2010;7:271
65. Aushev VN, Zborovskaya IB, Laktionov KK. Comparisons of microRNA patterns in plasma before and after tumor removal reveal new biomarkers of lung squamous cell carcinoma. PLoS One 2013;8(10):e78649