Biobanking of exosomes in the era of precision medicine: Are we there yet?

International Journal of Molecular Sciences

Volumn 17, Issue 1, 2016, Pages

  Mora, Edna M ^a,b   Álvarez Cubela, Silvia ^c   Oltra, Elisa ^d  

^a UNIVERSITY OF PUERTO RICO SCHOOL OF MEDICINE   (Puerto Rico)

^b UNIVERSITY OF PUERTO RICO   (Puerto Rico)

^c UNIVERSITY OF MIAMI   (United States)

^d UNIVERSIDAD CATÓLICA DE VALENCIA SAN VICENTE MÁRTIR   (Spain)

Author keywords

Biobank; Biomarker; Exogram; Exosome; Precision medicine

Indexed keywords

CD63 ANTIGEN; CD81 ANTIGEN; CD9 ANTIGEN; MEMBRANE METALLOENDOPEPTIDASE;

BIOBANKING; ENZYME LINKED IMMUNOSORBENT ASSAY; EPITHELIAL MESENCHYMAL TRANSITION; EXOSOME; FLOW CYTOMETRY; HEALTH CARE FACILITY; MEMBRANE MICROPARTICLE; MESENCHYMAL STEM CELL; NEVUS FLAMMEUS; PARKINSON DISEASE; REVIEW; TRANSMISSION ELECTRON MICROSCOPY; ANIMAL; BIOBANK; CLASSIFICATION; HUMAN; METABOLISM; ORGANIZATION AND MANAGEMENT; PATHOLOGY; PERSONALIZED MEDICINE; PROCEDURES; STANDARDS; TRENDS;

ANIMALS; BIOLOGICAL SPECIMEN BANKS; CELL-DERIVED MICROPARTICLES; EXOSOMES; HUMANS; PRECISION MEDICINE;

EID: 84951787560     PISSN: 16616596     EISSN: 14220067     Source Type: Journal    
DOI: 10.3390/ijms17010013     Document Type: Review

References (83)

1. Akers, J.C.; Gonda, D.; Kim, R.; Carter, B.S.; Chen, C.C. Biogenesis of extracellular vesicless (EV): Exosomes, microvesicles, retrovirus-like vesicles, and apoptotic bodies. J. Neuro-Oncol. 2013, 113, 1-11. [CrossRef] [PubMed]
2. Yáñez-Mó, M.; Siljander, P.R.; Andreu, Z.; Zavec, A.B.; Borràs, F.E.; Buzas, E.I.; Buzas, K.; Casal, E.; Cappello, F.; Carvalho, J.; et al. Biological properties of EVs and their physiological functions. J. Extracell. Vesicles 2015. [CrossRef]
3. Andre, F.; Schartz, N.E.; Movassagh, M.; Flament, C.; Pautier, P.; Morice, P.; Pomel, C.; Lhomme, C.; Escudier, B.; le Chevalier, T.; et al. Malignant effusions and immunogenic tumour-derived exosomes. Lancet 2002, 360, 295-305. [CrossRef]
4. Thery, C.; Zitvogel, L.; Amigorena, S. Exosomes: Composition, biogenesis and function. Nat. Rev. Immunol. 2002, 2, 569-579. [PubMed]
5. Huebner, A.R.; Somparn, P.; Benjachat, T.; Leelahavanichkul, A.; Avihingsanon, Y.; Fenton, R.A.; Pisitkun, T. Exosomes in urine biomarker discovery. Adv. Exp. Med. Biol. 2015, 845, 43-58. [PubMed]
6. Lasser, C.; Alikhani, V.S.; Ekstrom, K.; Eldh, M.; Paredes, P.T.; Bossios, A.; Sjöstrand, M.; Gabrielsson, S.; Lötvall, J.; Valadi, H. Human saliva, plasma and breast milk exosomes contain RNA: Uptake by macrophages. J. Transl. Med. 2011. [CrossRef] [PubMed]
7. Kharaziha, P.; Ceder, S.; Li, Q.; Panaretakis, T. Tumor cell-derived exosomes: A message in a bottle. Biochim. Biophys. Acta 2012, 1826, 103-111. [CrossRef] [PubMed]
8. Mulcahy, L.A.; Pink, R.C.; Carter, D.R. Routes and mechanisms of extracellular vesicle uptake. J. Extracell. Vesicles 2014. [CrossRef] [PubMed]
9. Urbanelli, L.; Magini, A.; Buratta, S.; Brozzi, A.; Sagini, K.; Polchi A Tancini, B.; Emiliani, C. Signaling pathways in exosomes biogenesis, secretion and fate. Genes 2013, 4, 152-170. [CrossRef] [PubMed]
10. Escrevente, C.; Keller, S.; Altevogt, P.; Costa, J. Interaction and uptake of exosomes by ovarian cancer cells. BMC Cancer 2011. [CrossRef] [PubMed]
11. Villarroya-Beltri, C.; Baixauli, F.; Gutierrez-Vazquez, C.; Sánchez-Madrid, F.; Mittelbrunn, M. Sorting it out: Regulation of exosome loading. Semin. Cancer Biol. 2014, 28, 3-13. [CrossRef] [PubMed]
12. Boukouris, S.; Mathivanan, S. Exosomes in bodily fluids are a highly stableresource of disease biomarkers. Proteom. Clin. Appl. 2015, 9, 358-367. [CrossRef] [PubMed]
13. Corrado, C.; Raimondo, S.; Chiesi, A.; Ciccia, F.; de Leo, G.; Alessandro, R. Exosomes as intercellular signaling organelles involved in health and disease: Basic science and clinical applications. Int. J. Mol. Sci. 2013, 14, 5338-5366. [CrossRef] [PubMed]
14. Roma-Rodrigues, C.; Fernandes, A.R.; Baptista, P.V. Exosome in tumour microenvironment: Overview of the crosstalk between normal and cancer cells. Biomed. Res. Int. 2014. [CrossRef] [PubMed]
15. Batrakova, E.V.; Kim, M.S. Using exosomes, naturally-equipped nanocarriers, for drug delivery. J. Control. Release 2015, 219, 396-405. [CrossRef] [PubMed]
16. Johnsen, K.B.; Gudbergsson, J.M.; Skov, M.N.; Pilgaard, L.; Moos, T.; Duroux, M. A comprehensive overview of exosomes as drug delivery vehicles-Endogenous nanocarriers for targeted cancer therapy. Biochim. Biophys. Acta 2014, 1846, 75-87. [CrossRef] [PubMed]
17. Tran, T.H.; Mattheolabakis, G.; Aldawsari, H.; Amiji, M. Exosomes as nanocarriers for immunotherapy of cancer and inflammatory diseases. Clin. Immunol. 2015, 160, 46-58. [CrossRef] [PubMed]
18. Shaw, D.M.; Elger, B.S.; Colledge, F. What is a biobank? Differing definitions among biobank stakeholders. Clin. Genet. 2014, 85, 223-227. [CrossRef] [PubMed]
19. Artene, S.A.; Ciurea, M.E.; Purcaru, S.O.; Tache, D.E.; Tataranu, L.G.; Lupu, M.; Dricu, A. Biobanking in a constantly developing medical world. Sci. World J. 2013. [CrossRef]
20. Van der Pol, E.; Böing, A.N.; Harrison, P.; Sturk, A.; Nieuwland, R. Classification, functions, and clinical relevance of extracellular vesicles. Pharmacol. Rev. 2012, 64, 676-705. [CrossRef] [PubMed]
21. Tauro, B.J.; Greening, D.W.; Mathias, R.A.; Mathivanan, S.; Ji, H.; Simpson, R.J. Two distinct populations of exosomes are released from LIM1863 colon carcinoma cell-derived organoids. Mol. Cell. Proteom. 2013. [CrossRef] [PubMed]
22. Kim, D.K.; Kang, B.; Kim, O.Y.; Choi, D.S.; Lee, J.; Kim, S.R.; Go, G.; Yoon, Y.J.; Kim, J.H.; Jang, S.C.; et al. EVpedia: An integrated database of high-throughput data for systemic analyses of extracellular vesicles. J. Extracell. Vesicles 2013. [CrossRef]
23. Thery, C.; Amigorena, S.; Raposo, G.; Clayton, A. Isolation and characterization of exosomes from cell culture supernatants and biological fluids. Curr. Protoc. Cell Biol. 2006. [CrossRef]
24. Osteikoetxea, X.; Balogh, A.; Szabó-Taylor, K.; Németh, A.; Szabó, T.G.; Pálóczi, K.; Sódar, B.; Kittel, Á.; György, B.; Pállinger, É.; et al. Improved characterization of EV preparations based on protein to lipid ratio and lipid properties. PLoS ONE 2015. [CrossRef] [PubMed]
25. Kalra, H.; Simpson, R.J.; Ji, H.; Aikawa, E.; Altevogt, P.; Askenase, P.; Bond, V.C.; Borràs, F.E.; Breakefield, X.; Budnik, V.; et al. Vesiclepedia: A compendium for extracellular vesicles with continuous community annotation. PLoS Biol. 2012. [CrossRef] [PubMed]
26. Simpson, R.J.; Kalra, H.; Mathivanan, S. ExoCarta as a resource for exosomal research. J. Extracell. Vesicles 2012. [CrossRef] [PubMed]
27. Oltra, E. Relevance of splicing on tumor-released exosome landscape: Implications in cancer therapeutics. Front. Endocrinol. 2014. [CrossRef] [PubMed]
28. Azmi, A.S.; Bao, B.; Sarkar, F.H. Exosomes in cancer development, metastases and drug resistance: A comprehensive review. Cancer Metastases Rev. 2013, 32, 1-33.
29. Zhao, L.; Liu, W.; Xiao, J.; Cao, B. The role of exosomes and "exosomal shuttle microRNA" in tumorigenesis and drug resistance. Cancer Lett. 2015, 356, 339-346. [CrossRef] [PubMed]
30. Alečković, M.; Kang, Y. Regulation of cancer metastasis by cell-free miRNAs. Biochim. Biophys. Acta 2015, 1855, 24-42. [CrossRef] [PubMed]
31. Videira,M.; Reis, R.L.; Brito, M.A. Deconstructing breast cancer cell biology and the mechanism of multidrug resistance. Biochim. Biophys. Acta 2014, 1846, 312-325. [CrossRef] [PubMed]
32. Vella, L.J. The emerging role of exosomes in epithelial-mesenchymal-transition in cancer. Front. Oncol. 2014, 4, 1-4. [CrossRef] [PubMed]
33. Kahlert, C.; Kalluri, R. Exosomes in tumor microenvironment influence cancer progression and metastasis. J. Mol. Med. 2013, 91, 431-437. [CrossRef] [PubMed]
34. Thuma, F.; Zöller, M. Outsmart tumor exosomes to steal the cancer initiating cell its niche. Semin. Cancer Biol. 2014, 28, 39-50. [CrossRef] [PubMed]
35. Gehrmann, U.; Näslund, T.I.; Hiltbrunner, S.; Larssen, P.; Gabrielsson, S. Harnessing the exosome-induced immune response for cancer immunotherapy. Semin. Cancer Biol. 2014, 28, 58-67. [CrossRef] [PubMed]
36. Fabbri, M.; Paone, A.; Calore, F.; Galli, R.; Gaudio, E.; Santhanam, R.; Lovat, F.; Fadda, P.; Mao, C.; Nuovo, G.J.; et al. MicroRNAs bind to Toll-like receptors to induce prometastatic inflammatory response. Proc. Natl. Acad. Sci. USA 2012, 109, E2110-E2116. [CrossRef] [PubMed]
37. Fabbri, M.; Paone, A.; Calore, F.; Galli, R.; Croce, C.M. A new role for microRNAs, as ligands of Toll-like receptors. RNA Biol. 2013, 10, 169-174. [CrossRef] [PubMed]
38. Properzi, F.; Logozzi, M.; Fais, S. Exosomes: The future of biomarkers in medicine. Biomark. Med. 2013, 7, 769-778. [CrossRef] [PubMed]
39. Mishra, P.J. Non-coding RNAs as clinical biomarkers for cancer diagnosis and prognosis. Expert Rev. Mol. Diagn. 2014, 14, 917-919. [CrossRef] [PubMed]
40. Sato-Kuwabar, Y.; Melo, S.A.; Soares, F.; Calin, G.A. The fusion of two worlds: Non-coding RNAs and EVs-diagnostic and therapeutic implications (Review). Int. J. Oncol. 2015, 46, 17-27.
41. Melo, S.A.; Luecke, L.B.; Kahlert, C.; Fernandez, A.F.; Gammon, S.T.; Kaye, J.; LeBleu, V.S.; Mittendorf, E.A.; Weitz, J.; Rahbari, N.; et al. Glypican-1 identifies cancer exosomes and detects early pancreatic cancer. Nature 2015, 523, 177-182. [CrossRef] [PubMed]
42. Braicu, C.; Tomuleasa, C.; Monroig, P.; Cucuianu, A.; Berindan-Neagoe, I.; Calin, G.A. Exosomes as divine messengers: Are they the hermes of modern molecular oncology? Cell Death Differ. 2015, 22, 34-45. [CrossRef] [PubMed]
43. Kumar, D.; Gupta, D.; Shankar, S.; Srivastava, R.K. Biomolecular characterization of exosomes released from cancer stem cells: Possible implications for biomarker and treatment of cancer. Oncotarget 2015, 6, 3280-3291. [CrossRef] [PubMed]
44. Katsuda, T.; Kosaka, N.; Ochiya, T. The roles of extracellular vesicles in cancer biology: Toward the development of novel cancer biomarkers. Proteomics 2014, 14, 412-425. [CrossRef] [PubMed]
45. Natasha, G.; Gundogan, B.; Tan, A.; Farhatnia, Y.; Wu, W.; Rajadas, J.; Seifalian, A.M. Exosomes as immunotheranostic nanoparticles. Clin. Ther. 2014, 36, 820-829. [CrossRef] [PubMed]
46. Sun, Y.; Liu, J. Potential of cancer cell-derived Exosomes in clinical application: A review of recent research advances. Clin. Ther. 2014, 36, 863-872. [CrossRef] [PubMed]
47. El Andaloussi, S.; Lakhal, S.; Mäger, I.; Wood, M.J. Exosomes for targeted siRNA delivery across biological barriers. Adv. Drug Deliv. Rev. 2013, 65, 391-397. [CrossRef] [PubMed]
48. Marcus, M.E.; Leonard, J.N. FedExosomes: Engineering therapeutic biological nanoparticles that truly deliver. Pharmaceuticals 2013, 6, 659-680. [CrossRef] [PubMed]
49. O'Loughlin, A.J.;Woffindale, C.A.;Wood, M.J.A. Exosomes and the emerging field of exosome-based gene therapy. Curr. Gene Ther. 2012, 12, 262-274. [CrossRef] [PubMed]
50. Yeo, R.W.Y.; Lai, R.C.; Zhang, B.; Tan, S.S.; Yin, Y.; Teh, B.J.; Lim, S.K. Mesenchymal stem cell: An efficient mass producer of exosomes for drug delivery. Adv. Drug Deliv. Rev. 2013, 65, 336-341. [CrossRef] [PubMed]
51. Lai, R.C.; Yeo, R.W.Y.; Tan, K.H.; Lim, S.K. Exosomes for drug delivery-A novel application for the mesenchymal stem cell. Biotechnol. Adv. 2013, 31, 543-551. [CrossRef] [PubMed]
52. Katsuda, T.; Kosaka, N.; Takeshita, F.; Ochiya, T. The therapeutic potential of mesenchymal stem cell-derived extracellular vesicles. Proteomics 2013, 13, 1637-1653. [CrossRef] [PubMed]
53. Katsuda, T.; Tsuchiya, R.; Kosaka, N.; Yoshioka, Y.; Takagaki, K.; Oki, K.; Takeshita, F.; Sakai, Y.; Kuroda, M.; Ochiya, T. Human adipose tissue-derived mesenchymal stem cells secrete functional neprilysin-bound exosomes. Sci. Rep. 2013, 3, 1-10. [CrossRef] [PubMed]
54. Kosaka, N.; Takeshita, F.; Yoshioka, Y.; Hagiwara, K.; Katsuda, T.; Ono, M.; Ochiya, T. Exosomal tumor-suppressive microRNAs as novel cancer therapy "exocure" is another choice for cancer treatment. Adv. Drug Deliv. Rev. 2013, 65, 376-382. [CrossRef] [PubMed]
55. ClinicalTrials.gov. Available online: http://www.clinicaltrials.gov (accessed on 26 November 2015).
56. Marleau, A.M.; Chen, C.S.; Joyce, J.A.; Tullis, R.H. Exosome removal as a therapeutic adjuvant in cancer. J. Transl. Med. 2012, 10, 1-12. [CrossRef] [PubMed]
57. Vader, P.; Breakefield, X.O.; Wood, M.J.A. Extracellular vesicles: Emerging targets for cancer therapy. Trends Mol. Med. 2014, 20, 385-393. [CrossRef] [PubMed]
58. Lässer, C.; Eldh, M.; Lötvall, J. Isolation and characterization of RNA-containing exosomes. J. Vis. Exp. 2012. [CrossRef] [PubMed]
59. Cvjetkovic, A.; Lötvall, J.; Lässer, C. The influence of rotor type and centrifugation time on the yield and purity of extracellular vesicles. J. Extracell. Vesicles 2014. [CrossRef] [PubMed]
60. Lobb, R.J.; Becker, M.; Wen, S.W.; Wong, C.S.F.; Wiegmans, A.P.; Leimgruber, A.; Möller, A. Optimized exosome isolation protocol for cell culture supernatant and human plasma. J. Extracell. Vesicles 2015, 4, 1-11.
61. Yamashita, T.; Takahashi, Y.; Nishikawa, M.; Takakura, Y. Effect of Exosome isolation methods on physicochemical properties of exosomes and clearance of exosomes from the blood circulation. Eur. J. Pharm. Biopharm. 2016. [CrossRef] [PubMed]
62. Brownlee, Z.; Lynn, K.D.; Thorpe, P.E.; Schroit, A.J. A novel "salting-out" procedure for the isolation of tumor-derived exosomes. J. Immunol. Methods 2014, 407, 120-126. [CrossRef] [PubMed]
63. Caradec, J.; Kharmate, G.; Hosseini-Beheshti, E.; Adomat, H.; Gleave, M.; Guns, E. Reproducibility and efficiency of serum-derived exosome extraction methods. Clin. Biochem. 2014, 47, 1286-1292. [CrossRef] [PubMed]
64. Muller, L.; Hong, C.S.; Stolz, D.B.;Watkins, S.C.; Whiteside, T.L. Isolation of biologically-active exosomes from human plasma. J. Immunol. Methods 2014, 411, 55-65. [CrossRef] [PubMed]
65. Mathivanan, S.; Lim, J.W.; Tauro, B.J.; Ji, H.; Moritz, R.L.; Simpson, R.J. Proteomics analysis of A33 immunoaffinity-purified exosomes released from the human colon tumor cell line LIM1215 reveals a tissue-specific protein signature. Mol. Cell. Proteom. 2010. [CrossRef] [PubMed]
66. Shin, H.; Han, C.; Labuz, J.M.; Kim, J.; Cho, S.; Gho, Y.S.; Takayama, S.; Park, J. High-yield isolation of extracellular vesicles using aqueous two-phase system. Sci. Rep. 2015. [CrossRef]
67. Atai, N.A.; Balaj, L.; van Veen, H.; Breakefield, X.O.; Jarzyna, P.A.; van Noorden, C.J.; Skog, J.; Maguire, C.A. Heparin blocks transfer of extracellular vesicles between donor and recipient cells. J. Neuro-Oncol. 2013. [CrossRef] [PubMed]
68. Sánchez Fito, M.T.; Oltra, E. Optimized treatment of heparinized blood fractions to make them suitable for analysis. Biopreserv. Biobank. 2015, 13, 287-295. [CrossRef] [PubMed]
69. Graner, M.W.; Alzate, O.; Dechkovskaia, A.M.; Keene, J.D.; Sampson, J.H.; Mitchell, D.A.; Bigner, D.D. Proteomic and immunologic analyses of brain tumor exosomes. FASEB J. 2009. [CrossRef]
70. Epple, L.M.; Griffiths, S.G.; Dechkovskaia, A.M.; Dusto, N.L.; White, J.; Ouellette, R.J.; Anchordoquy, T.J.; Bemis, L.T.; Graner, M.W. Medulloblastoma exosome proteomics yield functional roles for extracellular vesicles. PLoS ONE 2012. [CrossRef] [PubMed]
71. Kang, D.; Oh, S.; Ahn, S.M.; Lee, B.H.; Moon, M.H. Proteomic analysis of exosomes from human neural stem cells by flow field-flow fractionation and nanoflow liquid chromatography tandem mass spectrometry. J. Proteome Res. 2008. [CrossRef] [PubMed]
72. Taylor, D.D.; Shah, S. Methods of isolating extracellular vesicles impact down-stream analyses of their cargoes. Methods 2015, 87, 3-10. [CrossRef] [PubMed]
73. Peterson, M.F.; Otoc, N.; Sethi, J.K.; Gupta, A.; Antes, T.J. Integrated systems for exosome investigation. Methods 2015, 87, 31-45. [CrossRef] [PubMed]
74. György, B.; Módos, K.; Pállinger, É.; Pálóczi, K.; Pásztói, M.; Misják, P.; Deli, M.A.; Sipos, A.; Szalai, A.; Voszka, I.; et al. Detection and isolation of cell-derived microparticles are compromised by protein complexes due to shared biophysical parameters. Blood 2011, 117, e39-e48. [CrossRef] [PubMed]
75. Kalra, H.; Adda, C.G.; Liem, M.; Ang, C.S.; Mechler, A.; Simpson, R.J.; Hulett, M.D.; Mathivanan, S. Comparative proteomics evaluation of plasma exosome isolation techniques and assessment of the stability of exosomes in normal human blood plasma. Proteomics 2013, 13, 3354-3364. [CrossRef] [PubMed]
76. Fertig, E.T.; Gherghiceanu, M.; Popescu, L.M. Extracellular vesicles release by cardiac telocytes: Electron microscopy and electron tomography. J. Cell. Mol. Med. 2014, 18, 1938-1943. [CrossRef] [PubMed]
77. Mehdiani, A.; Maier, A.; Pinto, A.; Barth, M.; Akhyari, P.; Lichtenberg, A. An innovative method for exosome quantification and size measurement. J. Vis. Exp. 2015. [CrossRef] [PubMed]
78. Savina, A.; Vidal, M.; Colombo, M.I. The exosome pathway in K562 cells is regulated by Rab11. J. Cell Sci. 2002, 115, 2505-2515. [PubMed]
79. Gupta, S.; Knowlton, A.A. HSP60 trafficking in adult cardiac myocytes: Role of the exosomal pathway. Am. J. Physiol. Heart Circ. Physiol. 2007, 292, H3052-H3056. [CrossRef] [PubMed]
80. Llorente, A.; Skotland, T.; Sylvanne, T.; Kauhanen, D.; Rog, T.; Orłowski, A.; Vattulainen, I.; Ekroos, K.; Sandvig, K. Molecular lipidomics of exosomes released by PC-3 prostate cancer cells. Biochim. Biophys. Acta 2013, 1831, 1302-1309. [CrossRef] [PubMed]
81. Record, M.; Carayon, K.; Poirot, M.; Silvente-Poirot, S. Exosomes as new vesicular lipid transporters involved in cell-cell communication and various pathophysiologies. Biochim. Biophys. Acta 2014, 1841, 108-120. [CrossRef] [PubMed]
82. Lacroix, R.; Judicone, C.; Mooberry, M.; Boucekine, M.; Key, N.S.; Dignat-George, F. Standardization of pre-analytical variables in plasma microparticle determination: Results of the International Society on Thrombosis and Haemostasis SSC Collaborative workshop. J. Thromb. Haemost. 2013, 11, 1190-1193. [CrossRef] [PubMed]
83. Betsou, F.; Lehmann, S.; Ashton, G.; Barnes, M.; Benson, E.E.; Coppola, D.; DeSouza, Y.; Eliason, J.; Glazer, B.; Guadagni, F.; et al. International Society for Biological and Environmental Repositories (ISBER) Working Group on Biospecimen Science. Standard preanalytical coding for biospecimens: Defining the sample PREanalytical code. Cancer Epidemiol. Biomark. Prev. 2010, 19, 1004-1011. [CrossRef] [PubMed]