Tumor exosomes: Cellular postmen of cancer diagnosis and personalized therapy

Nanomedicine

Volumn 11, Issue 4, 2016, Pages 421-437

  Sharma, Aman ^a,b   Khatun, Zamila ^a   Shiras, Anjali ^b  

^a NATIONAL CHEMICAL LABORATORY   (India)

^b NATIONAL CENTRE FOR CELL SCIENCE   (India)

Author keywords

diagnosis; exosomes; tumor biomarkers; tumor heterogeneity

Indexed keywords

BIOLOGICAL MARKER; DNA; MICRORNA;

ANTIBODY AFFINITY; CANCER DIAGNOSIS; CANCER GROWTH; CELL COMPONENT; DNA RNA HYBRIDIZATION; EXOSOME; GENE CONTROL; GENETIC HETEROGENEITY; HUMAN; MACROMOLECULE; METABOLIC STABILITY; MICROFLUIDICS; NANOSENSOR; NONHUMAN; PATIENT MONITORING; PERSONALIZED MEDICINE; PRIORITY JOURNAL; PROTEIN ANALYSIS; REVIEW; TREATMENT RESPONSE; TUMOR BIOPSY; TUMOR CELL; TUMOR MICROENVIRONMENT; CENTRIFUGATION; NEOPLASMS; PATHOLOGY;

CENTRIFUGATION; EXOSOMES; HUMANS; NEOPLASMS; PRECISION MEDICINE;

EID: 84956912746     PISSN: 17435889     EISSN: 17486963     Source Type: Journal    
DOI: 10.2217/nnm.15.210     Document Type: Review

References (98)

1. Johnstone RM, Adam M, Hammond JR, Orr L, Turbide C. Vesicle formation during reticulocyte maturation. Association of plasma membrane activities with released vesicles (exosomes). J. Biol. Chem. 262(19), 9412-9420 (1987).
2. Urbanelli L, Magini A, Buratta S et al. Signaling pathways in exosomes biogenesis, secretion and fate. Genes 4(2), 152-170 (2013).
3. Raposo G, Stoorvogel W. Extracellular vesicles: exosomes, microvesicles, and friends. J. Cell Biol. 200(4), 373-383 (2013).
4. Li XB, Zhang ZR, Schluesener HJ, Xu SQ. Role of exosomes in immune regulation. J. Cell. Mol. Med. 10(2), 364-375 (2006).
5. Colombo M, Moita C, Van Niel G et al. Analysis of ESCRT functions in exosome biogenesis, composition and secretion highlights the heterogeneity of extracellular vesicles. J. Cell Sci. 126(Pt 24), 5553-5565 (2013).
6. Colombo M, Raposo G, Thery C. Biogenesis, secretion, and intercellular interactions of exosomes and other extracellular vesicles. Annu. Rev. Cell. Dev. Biol. 30, 255-289 (2014).
7. 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. 81(1), 2-10 (2015).
8. Robbins PD, Morelli AE. Regulation of immune responses by extracellular vesicles. Nat. Rev. Immunol. 14(3), 195-208 (2014).
9. Ostrowski M, Carmo NB, Krumeich S et al. Rab27a and Rab27b control different steps of the exosome secretion pathway. Nat. Cell Biol. 12(1), 19-30; sup pp 11-13 (2010).
10. Parolini I, Federici C, Raggi C et al. Microenvironmental pH is a key factor for exosome traffic in tumor cells. J. Biol. Chem. 284(49), 34211-34222 (2009).
11. Zhang HG, Grizzle WE. Exosomes: A novel pathway of local and distant intercellular communication that facilitates the growth and metastasis of neoplastic lesions. Am. J. Pathol. 184(1), 28-41 (2014).
12. Testa JS, Apcher GS, Comber JD, Eisenlohr LC. Exosomedriven antigen transfer for MHC class II presentation facilitated by the receptor binding activity of influenza hemagglutinin. J. Immunol. 185(11), 6608-6616 (2010).
13. Kourembanas S. Exosomes: vehicles of intercellular signaling, biomarkers, and vectors of cell therapy. Annu. Rev. Physiol. 77, 13-27 (2015).
14. Guo L, Guo N. Exosomes: Potent regulators of tumor malignancy and potential bio-tools in clinical application. Crit. Rev. Oncol. Hematol. 95(3), 346-358 (2015).
15. Vlassov AV, Magdaleno S, Setterquist R, Conrad R. Exosomes: current knowledge of their composition, biological functions, and diagnostic and therapeutic potentials. Biochim. Biophys. Acta 1820(7), 940-948 (2012).
16. Azmi AS, Bao B, Sarkar FH. Exosomes in cancer development, metastasis, and drug resistance: A comprehensive review. Cancer Metastasis Rev. 32(3-4), 623-642 (2013).
17. Cossetti C, Lugini L, Astrologo L, Saggio I, Fais S, Spadafora C. Soma-to-germline transmission of RNA in mice xenografted with human tumor cells: Possible transport by exosomes. PLoS ONE 9(7), e101629 (2014).
18. Kahlert C, Melo SA, Protopopov A et al. Identification of double-stranded genomic DNA spanning all chromosomes with mutated KRAS and p53 DNA in the serum exosomes of patients with pancreatic cancer. J. Biol. Chem. 289(7), 3869-3875 (2014).
19. Demory Beckler M, Higginbotham JN, Franklin JL et al. Proteomic analysis of exosomes from mutant KRAS colon cancer cells identifies intercellular transfer of mutant KRAS. Mol. Cell. Proteomics 12(2), 343-355 (2013).
20. Al-Nedawi K, Meehan B, Micallef J et al. Intercellular transfer of the oncogenic receptor EGFRvIII by microvesicles derived from tumor cells. Nat. Cell Biol. 10(5), 619-624 (2008).
21. Ciravolo V, Huber V, Ghedini GC et al. Potential role of HER2-overexpressing exosomes in countering trastuzumabbased therapy. J. Cell. Physiol. 227(2), 658-667 (2012).
22. Li X, Xin S, He Z et al. microRNA-21 (miR-21) posttranscriptionally downregulates tumor suppressor PDCD4 and promotes cell transformation, proliferation, and metastasis in renal cell carcinoma. Cell. Physiol. Biochem. 33(6), 1631-1642 (2014).
23. Cappellesso R, Tinazzi A, Giurici T et al. Programmed cell death 4 and microRNA 21 inverse expression is maintained in cells and exosomes from ovarian serous carcinoma effusions. Cancer Cytopathol. 122(9), 685-693 (2014).
24. Putz U, Howitt J, Doan A et al. The tumor suppressor PTEN is exported in exosomes and has phosphatase activity in recipient cells. Sci. Signal. 5(243), ra70(2012).
25. Aspe JR, Diaz Osterman CJ, Jutzy JM, Deshields S, Whang S, Wall NR. Enhancement of gemcitabine sensitivity in pancreatic adenocarcinoma by novel exosome-mediated delivery of the Survivin-T34A mutant. J. Extracell. Vesicles 3, doi:10. 3402/jev. v3. 23244 (2014).
26. Pap E, Pallinger E, Falus A. The role of membrane vesicles in tumorigenesis. Crit. Rev. Oncol. Hematol. 79(3), 213-223 (2011).
27. Khan S, Aspe JR, Asumen MG et al. Extracellular, cellpermeable survivin inhibits apoptosis while promoting proliferative and metastatic potential. Br. J. Cancer 100(7), 1073-1086 (2009).
28. Federici C, Petrucci F, Caimi S et al. Exosome release and low pH belong to a framework of resistance of human melanoma cells to cisplatin. PLoS ONE 9(2), e88193 (2014).
29. Gangoda L, Boukouris S, Liem M, Kalra H, Mathivanan S. Extracellular vesicles including exosomes are mediators of signal transduction: Are they protective or pathogenic? Proteomics 15(2-3), 260-271 (2015).
30. Lim PK, Bliss SA, Patel SA et al. Gap junction-mediated import of microRNA from bone marrow stromal cells can elicit cell cycle quiescence in breast cancer cells. Cancer Res. 71(5), 1550-1560 (2011).
31. Lee TH, D'asti E, Magnus N, Al-Nedawi K, Meehan B, Rak J. Microvesicles as mediators of intercellular communication in cancer-the emerging science of cellular 'debris'. Semin. Immunopathol. 33(5), 455-467 (2011).
32. Nazarenko I, Rana S, Baumann A et al. Cell surface tetraspanin Tspan8 contributes to molecular pathways of exosome-induced endothelial cell activation. Cancer Res. 70(4), 1668-1678 (2010).
33. Sharghi-Namini S, Tan E, Ong LL, Ge R, Asada HH. Dll4-containing exosomes induce capillary sprout retraction in a 3D microenvironment. Sci. Rep. 4 4031 (2014).
34. Park JE, Tan HS, Datta A et al. Hypoxic tumor cell modulates its microenvironment to enhance angiogenic and metastatic potential by secretion of proteins and exosomes. Mol. Cell. Proteomics 9(6), 1085-1099 (2010).
35. Franzen CA, Blackwell RH, Todorovic V et al. Urothelial cells undergo epithelial-to-mesenchymal transition after exposure to muscle invasive bladder cancer exosomes. Oncogenesis 4, e163 (2015).
36. Greening DW, Gopal SK, Mathias RA et al. Emerging roles of exosomes during epithelial-mesenchymal transition and cancer progression. Semin. Cell Dev. Biol. 40, 60-71 (2015).
37. D'asti E, Garnier D, Lee TH, Montermini L, Meehan B, Rak J. Oncogenic extracellular vesicles in brain tumor progression. Front. Physiol. 3, 294 (2012).
38. Fong MY, Zhou W, Liu L et al. Breast-cancer-secreted miR-122 reprograms glucose metabolism in premetastatic niche to promote metastasis. Nat. Cell Biol. 17(2), 183-194 (2015).
39. Milane L, Singh A, Mattheolabakis G, Suresh M, Amiji MM. Exosome mediated communication within the tumor microenvironment. J. Control. Release 21, 278-294 (2015).
40. Taylor DD, Gercel-Taylor C. Exosomes/microvesicles: mediators of cancer-associated immunosuppressive microenvironments. Semin. Immunopathol. 33(5), 441-454 (2011).
41. Kahlert C, Kalluri R. Exosomes in tumor microenvironment influence cancer progression and metastasis. J. Mol. Med. (Berl.) 91(4), 431-437 (2013).
42. Ichim TE, Zhong Z, Kaushal S et al. Exosomes as a tumor immune escape mechanism: Possible therapeutic implications. J. Transl. Med. 6, 37 (2008).
43. Bhatia A, Kumar Y. Cellular and molecular mechanisms in cancer immune escape: A comprehensive review. Expert Rev. Clin. Immunol. 10(1), 41-62 (2014).
44. Marleau AM, Chen CS, Joyce JA, Tullis RH. Exosome removal as a therapeutic adjuvant in cancer. J. Transl. Med. 10, 134 (2012).
45. Monleon I, Martinez-Lorenzo MJ, Monteagudo L et al. Differential secretion of Fas ligand-or APO2 ligand/TNFrelated apoptosis-inducing ligand-carrying microvesicles during activation-induced death of human T cells. J. Immunol. 167(12), 6736-6744 (2001).
46. Andreola G, Rivoltini L, Castelli C et al. Induction of lymphocyte apoptosis by tumor cell secretion of FasL-bearing microvesicles. J. Exp. Med. 195(10), 1303-1316 (2002).
47. 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 128(7), 1796-1804 (2005).
48. Manterola L, Guruceaga E, Gallego Perez-Larraya J et al. A small noncoding RNA signature found in exosomes of GBM patient serum as a diagnostic tool. Neuro Oncol. 16(4), 520-527 (2014).
49. Skog J, Wurdinger T, Van Rijn S et al. Glioblastoma microvesicles transport RNA and proteins that promote tumor growth and provide diagnostic biomarkers. Nat. Cell Biol. 10(12), 1470-1476 (2008).
50. Zhang J, Li S, Li L et al. Exosome and exosomal microRNA: trafficking, sorting, and function. Genomics Proteomics Bioinformatics 13(1), 17-24 (2015).
51. Silva J, Garcia V, Zaballos A et al. Vesicle-related microRNAs in plasma of nonsmall cell lung cancer patients and correlation with survival. Eur. Respir. J. 37(3), 617-623 (2011).
52. Cheng G. Circulating miRNAs: roles in cancer diagnosis, prognosis and therapy. Adv. Drug Deliv. Rev. 81, 75-93 (2015).
53. Rabinowits G, Gercel-Taylor C, Day JM, Taylor DD, Kloecker GH. Exosomal microRNA: A diagnostic marker for lung cancer. Clin. Lung Cancer 10(1), 42-46 (2009).
54. 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).
55. Mitchell PJ, Welton J, Staffurth J et al. Can urinary exosomes act as treatment response markers in prostate cancer? J. Transl. Med. 7, 4 (2009).
56. Bryant RJ, Pawlowski T, Catto JW et al. Changes in circulating microRNA levels associated with prostate cancer. Br. J. Cancer 106(4), 768-774 (2012).
57. Ravelli A, Reuben JM, Lanza F et al. Breast cancer circulating biomarkers: Advantages, drawbacks, and new insights. Tumor Biol. doi:10. 1007/s13277-015-3944-7 (2015).
58. Choi DS, Park JO, Jang SC et al. Proteomic analysis of microvesicles derived from human colorectal cancer ascites. Proteomics 11(13), 2745-2751 (2011).
59. Matsumura T, Sugimachi K, Iinuma H et al. Exosomal microRNA in serum is a novel biomarker of recurrence in human colorectal cancer. Br. J. Cancer 113(2), 275-281 (2015).
60. Wang M, Zhao C, Shi H et al. Deregulated microRNAs in gastric cancer tissue-derived mesenchymal stem cells: novel biomarkers and a mechanism for gastric cancer. Br. J. Cancer 110(5), 1199-1210 (2014).
61. Eldh M, Olofsson Bagge R, Lasser C et al. MicroRNA in exosomes isolated directly from the liver circulation in patients with metastatic uveal melanoma. BMC Cancer 14, 962 (2014).
62. Keller S, Konig AK, Marme F et al. Systemic presence and tumor-growth promoting effect of ovarian carcinoma released exosomes. Cancer Lett. 278(1), 73-81 (2009).
63. Li J, Sherman-Baust CA, Tsai-Turton M, Bristow RE, Roden RB, Morin PJ. Claudin-containing exosomes in the peripheral circulation of women with ovarian cancer. BMC Cancer 9, 244 (2009).
64. Taylor DD, Gercel-Taylor C. microRNA signatures of tumorderived exosomes as diagnostic biomarkers of ovarian cancer. Gynecol. Oncol. 110(1), 13-21 (2008).
65. Szajnik M, Derbis M, Lach M et al. Exosomes in plasma of patients with ovarian carcinoma: Potential biomarkers of tumor progression and response to therapy. Gynecol. Obstetr. 4(Suppl.), 3 (2013).
66. Hanahan D, Weinberg RA. Hallmarks of cancer: the next generation. Cell 144(5), 646-674 (2011).
67. Van Deun J, Mestdagh P, Sormunen R et al. The impact of disparate isolation methods for extracellular vesicles on downstream RNA profiling. J. Extracell. Vesicles 3, doi:10. 3402/jev. v3. 24858 (2014).
68. Lobb RJ, Becker M, Wen SW et al. Optimized exosome isolation protocol for cell culture supernatant and human plasma. J. Extracell. Vesicles 4, 27031 (2015).
69. Lozano-Ramos I, Bancu I, Oliveira-Tercero A et al. Sizeexclusion chromatography-based enrichment of extracellular vesicles from urine samples. J. Extracell. Vesicles 4, 27369 (2015).
70. Hong CS, Muller L, Boyiadzis M, Whiteside TL. Isolation and characterization of CD34+ blast-derived exosomes in acute myeloid leukemia. PLoS ONE 9(8), e103310 (2014).
71. Pospichalova V, Svoboda J, Dave Z et al. Simplified protocol for flow cytometry analysis of fluorescently labeled exosomes and microvesicles using dedicated flow cytometer. J. Extracell. Vesicles 4, 25530 (2015).
72. Shin H, Han C, Labuz JM et al. High-yield isolation of extracellular vesicles using aqueous two-phase system. Sci. Rep. 5, 13103 (2015).
73. Dudani JS, Gossett DR, Tse HT, Lamm RJ, Kulkarni RP, Carlo DD. Rapid inertial solution exchange for enrichment and flow cytometric detection of microvesicles. Biomicrofluidics 9(1), 014112 (2015).
74. Kanwar SS, Dunlay CJ, Simeone DM, Nagrath S. Microfluidic device (ExoChip) for on-chip isolation, quantification and characterization of circulating exosomes. Lab Chip 14(11), 1891-1900 (2014).
75. Santana SM, Antonyak MA, Cerione RA, Kirby BJ. Microfluidic isolation of cancer-cell-derived microvesicles from hetergeneous extracellular shed vesicle populations. Biomed. Microdevices 16(6), 869-877 (2014).
76. Chen C, Skog J, Hsu CH et al. Microfluidic isolation and transcriptome analysis of serum microvesicles. Lab Chip 10(4), 505-511 (2010).
77. Im H, Shao H, Park YI et al. Label-free detection and molecular profiling of exosomes with a nano-plasmonic sensor. Nat. Biotechnol. 32(5), 490-495 (2014).
78. Rho J, Chung J, Im H et al. Magnetic nanosensor for detection and profiling of erythrocyte-derived microvesicles. ACS Nano 7(12), 11227-11233 (2013).
79. Cvjetkovic A, Lotvall J, Lasser C. The influence of rotor type and centrifugation time on the yield and purity of extracellular vesicles. J. Extracell. Vesicles 3, doi:10. 3402/jev. v3. 23111 (2014).
80. Li J, Liu K, Liu Y et al. Exosomes mediate the cell-to-cell transmission of IFN-alpha-induced antiviral activity. Nat. Immunol. 14(8), 793-803 (2013).
81. Zhang Z, Wang C, Li T, Liu Z, Li L. Comparison of ultracentrifugation and density gradient separation methods for isolating Tca8113 human tongue cancer cell line-derived exosomes. Oncol. Lett. 8(4), 1701-1706 (2014).
82. Logozzi M, De Milito A, Lugini L et al. High levels of exosomes expressing CD63 and caveolin-1 in plasma of melanoma patients. PLoS ONE 4(4), e5219 (2009).
83. Ban JJ, Lee M, Im W, Kim M. Low pH increases the yield of exosome isolation. Biochem. Biophys. Res. Commun. 461(1), 76-79 (2015).
84. Ko J, Carpenter E, Issadore D. Detection and isolation of circulating exosomes and microvesicles for cancer monitoring and diagnostics using micro-/nano-based devices. Analyst doi:10. 1039/c5an01610j (2015) (Epub ahead of print).
85. Im H, Shao H, Weissleder R, Castro CM, Lee H. Nano-plasmonic exosome diagnostics. Expert Rev. Mol. Diagn. 15(6), 725-733 (2015).
86. Yoshioka Y, Kosaka N, Konishi Y et al. Ultra-sensitive liquid biopsy of circulating extracellular vesicles using ExoScreen. Nat. Commun. 5, 3591 (2014).
87. Exosome Diagnostics. Personalized Precision Healthcare. www. exosomedx. com
88. Caris Life Sciences: Precision Medicine for Cancer Care. www. carislifesciences. eu
89. ExoCan Healthcare Technology Pvt. Ltd. www. exocanhealthcare. com
90. De Mello RA, Madureira P, Carvalho LS, Araujo A, O'brien M, Popat. S EGFR and KRAS mutations, and ALK fusions: current developments and personalized therapies for patients with advanced non-small-cell lung cancer. Pharmacogenomics 14(14), 1765-1777 (2013).
91. Brinton LT, Sloane HS, Kester M, Kelly KA. Formation and role of exosomes in cancer. Cell. Mol. Life Sci. 72(4), 659-671 (2015).
92. An T, Qin S, Xu Y et al. Exosomes serve as tumor markers for personalized diagnostics owing to their important role in cancer metastasis. J. Extracell. Vesicles 4, 27522 (2015).
93. Shao H, Chung J, Lee K et al. Chip-based analysis of exosomal mRNA mediating drug resistance in glioblastoma. Nat. Commun. 6, 6999 (2015).
94. Hong CS, Muller L, Whiteside TL, Boyiadzis M. Plasma exosomes as markers of therapeutic response in patients with acute myeloid leukemia. Front. Immunol. 5, 160 (2014).
95. Boukouris S, Mathivanan S. Exosomes in bodily fluids are a highly stable resource of disease biomarkers. Proteomics Clin. Appl. 9(3-4), 358-367 (2015).
96. Thakur BK, Zhang H, Becker A et al. Double-stranded DNA in exosomes: A novel biomarker in cancer detection. Cell Res. 24(6), 766-769 (2014).
97. Villagrasa A, Alvarez PJ, Osuna A, Garrido JM, Aranega A, Rodriguez-Serrano F. Exosomes Derived from Breast Cancer Cells, Small Trojan Horses? J. Mammary Gland Biol. Neoplasia 19(3-4), 303-313 (2014).
98. Hannafon BN, Carpenter KJ, Berry WL, Janknecht R, Dooley WC, Ding WQ. Exosome-mediated microRNA signaling from breast cancer cells is altered by the antiangiogenesis agent docosahexaenoic acid (DHA). Mol. Cancer 14, 133 (2015).