Exosomes: Current knowledge of their composition, biological functions, and diagnostic and therapeutic potentials

Biochimica et Biophysica Acta - General Subjects

Volumn 1820, Issue 7, 2012, Pages 940-948

  Vlassov, Alexander V ^a   Magdaleno, Susan ^a   Setterquist, Robert ^a   Conrad, Rick ^a  

^a Life Technologies   (United States)

Author keywords

Exosome; Extracellular nucleic acid; Microvesicle; Signaling

Indexed keywords

AQUAPORIN 1; AQUAPORIN 2; CD24 ANTIGEN; MICRORNA; MICRORNA 223; MICRORNA 241; MICRORNA 25; MICRORNA 515 5P; MICRORNA 521; MICRORNA 526; MICRORNA 527; NANOPARTICLE; UNCLASSIFIED DRUG; VASOPRESSIN;

ALZHEIMER DISEASE; BIOLOGICAL ACTIVITY; BLOOD ANALYSIS; BODY DISTRIBUTION; BODY FLUID; CANCER IMMUNOTHERAPY; CD24 GENE; CELL COMMUNICATION; CELL ISOLATION; CELL STRUCTURE; CELL THERAPY; CELL VACUOLE; CLINICAL EFFECTIVENESS; COLORECTAL CANCER; DENDRITIC CELL; DIABETES MELLITUS; DIAGNOSTIC VALUE; ENZYME LINKED IMMUNOSORBENT ASSAY; EXOSOME; GENE; HUMAN; KIDNEY ISCHEMIA; LUNG CANCER; LUNG NON SMALL CELL CANCER; MELANOMA; MILK LEVEL; MULTIPLE SCLEROSIS; NANOANALYSIS; NANOTECHNOLOGY; PATIENT SAFETY; PREGNANCY; PRIORITY JOURNAL; PROSTATE CANCER; REPERFUSION INJURY; REVIEW; SALIVA ANALYSIS; SIGNAL TRANSDUCTION; THERAPY; ULTRACENTRIFUGATION; URINALYSIS;

ANIMALS; BIOLOGICAL MARKERS; BIOLOGICAL TRANSPORT; CELL COMMUNICATION; EXOSOMES; HUMANS; MULTIVESICULAR BODIES; NEOPLASMS; SIGNAL TRANSDUCTION;

EID: 84860858416     PISSN: 03044165     EISSN: 18728006     Source Type: Journal    
DOI: 10.1016/j.bbagen.2012.03.017     Document Type: Review

References (79)

1. R.J. Simpson, S.S. Jensen, and J.W. Lim Proteomic profiling of exosomes: current perspectives Proteomics 8 2008 4083 4099
2. E. Cocucci, G. Racchetti, and J. Meldolesi Shedding microvesicles: artefacts no more Trends Cell Biol. 19 2009 43 51
3. C. Lässer, M. Eldh, and J. Lötvall Isolation and characterization of RNA-containing exosomes J. Vis. Exp. 59 2012 3037 3047
4. G. Van Niel, I. Porto-Carreiro, S. Simoes, and G. Raposo Exosomes: a common pathway for a specialized function J. Biochem. (Tokyo) 140 2006 13 21
5. A. Lakkaraju, and E. Rodriguez-Boulan Itinerant exosomes: emerging roles in cell and tissue polarity Trends Cell Biol. 18 2008 199 209
6. E.G. Trams, C.J. Lauter, N. Salem Jr., and U. Heine Exfoliation of membrane ecto-enzymes in the form of micro-vesicles Biochim. Biophys. Acta 645 1981 63 70
7. C. Harding, J. Heuser, and P. Stahl Receptor-mediated endocytosis of transferrin and recycling of the transferrin receptor in rat reticulocytes J. Cell Biol. 97 1983 329 339
8. B.T. Pan, K. Teng, C. Wu, M. Adam, and R.M. Johnstone Electron microscopic evidence for externalization of the transferring receptor in vesicular form in sheep reticulocytes J. Cell Biol. 101 1985 942 948
9. R.M. Johnstone, M. Adam, J.R. Hammond, L. Orr, and C. Turbide Vesicle formation during reticulocyte maturation. Association of plasma membrane activities with released vesicles (exosomes) J. Biol. Chem. 262 1987 9412 9420
10. H. Valadi, K. Ekstrom, A. Bossios, M. Sjostrand, J.J. Lee, and J.O. Lotvall Exosome-mediated transfer of mRNAs and microRNAs is a novel mechanism of genetic exchange between cells Nat. Cell Biol. 9 2007 654 659
11. G. Raposo, H.W. Nijman, W. Stoorvogel, R. Liejendekker, C.V. Harding, C.J. Melief, and H.J. Geuze B lymphocytes secrete antigen-presenting vesicles J. Exp. Med. 183 1996 1161 1172
12. K. Trajkovic, C. Hsu, S. Chiantia, L. Rajendran, D. Wenzel, F. Wieland, P. Schwille, B. Brugger, and M. Simons Ceramide triggers budding of exosome vesicles into multivesicular endosomes Science 319 2008 1244 1247
13. P. Nieuwenhuysen, and J. Clauwaert Physical properties of Artemia salina ribosomes Biochemistry 17 1978 4260 4425
14. J. Conde-Vancells, E. Rodriguez-Suarez, N. Embade, D. Gil, R. Matthiesen, M. Valle, F. Elortza, S.C. Lu, J.M. Mato, and J.M. Falcon-Perez Characterization and comprehensive proteome profiling of exosomes secreted by hepatocytes J. Proteome Res. 7 2008 5157 5166
15. C. Subra, D. Grand, K. Laulagnier, A. Stella, G. Lambeau, M. Paillasse, P. De Medina, B. Monsarrat, B. Perret, S. Silvente-Poirot, M. Poirot, and M. Record Exosomes account for vesicle-mediated transcellular transport of activatable phospholipases and prostaglandins J. Lipid Res. 51 2010 2105 2120
16. S. Mathivanan, and R.J. Simpson ExoCarta: a compendium of exosomal proteins and RNA Proteomics 9 2009 4997 5000
17. K. Carayon, K. Chaoui, E. Ronzier, I. Lazar, J. Bertrand-Michel, V. Roques, S. Balor, F. Terce, A. Lopez, L. Salome, and E. Joly Proteolipidic composition of exosomes changes during reticulocyte maturation J. Biol. Chem. 286 2011 34426 34439
18. C. Subra, K. Laulagnier, B. Perret, and M. Record Exosome lipidomics unravels lipid sorting at the level of multivesicular bodies Biochimie 89 2007 205 212
19. R. Wubbolts, R.S. Leckie, P.T. Veenhuizen, G. Schwarzmann, W. Mobius, J. Hoernschemeyer, J.W. Slot, H.J. Geuze, and W. Stoorvogel Proteomic and biochemical analyses of human B cell-derived exosomes. Potential implications for their function and multivesicular body formation J. Biol. Chem. 278 2003 10963 10972
20. K. Laulagnier, C. Motta, S. Hamdi, S. Roy, F. Fauvelle, J.F. Pageaux, T. Kobayashi, J.P. Salles, B. Perret, C. Bonnerot, and M. Record Mast cell- and dendritic cell-derived exosomes display a specific lipid composition and an unusual membrane organization Biochem. J. 380 2004 161 171
21. B.S. Batista, W.S. Eng, K.T. Pilobello, K.D. Hendricks-Muñoz, and L.K. Mahal Identification of a conserved glycan signature for microvesicles J. Proteome Res. 10 2011 4624 4633
22. M. Mittelbrunn, C. Gutiérrez-Vázquez, C. Villarroya-Beltri, S. González, F. Sánchez-Cabo, M.A. González, A. Bernad, and F. Sánchez-Madrid Unidirectional transfer of microRNA-loaded exosomes from T cells to antigen-presenting cells Nat. Commun. 2 2011 282
23. J. Skog, T. Wurdinger, S. Van Rijn, D.H. Meijer, L. Gainche, M. Sena-Esteves, W.T. Curry Jr., B.S. Carter, A.M. Krichevsky, and X.O. Breakefield Glioblastoma microvesicles transport RNA and proteins that promote tumour growth and provide diagnostic biomarkers Nat. Cell Biol. 10 2008 1470 1476
24. A. Zomer, T. Vendrig, E.S. Hopmans, M. van Eijndhoven, J.M. Middeldorp, and D.M. Pegtel Exosomes: fit to deliver small RNA Commun. Integr. Biol. 3 2010 447 450
25. G. Rabinowits, C. Gerçel-Taylor, J.M. Day, D.D. Taylor, and G.H. Kloecker Exosomal microRNA: a diagnostic marker for lung cancer Clin. Lung Cancer 10 2009 42 46
26. D.D. Taylor, and C. Gercel-Taylor MicroRNA signatures of tumor-derived exosomes as diagnostic biomarkers of ovarian cancer Gynecol. Oncol. 110 2008 13 21
27. C. Thery, S. Amigorena, G. Raposo, and A. Clayton Isolation and characterization of exosomes from cell culture supernatants and biological fluids Curr. Protoc. Cell Biol. 3 2006 22 30
28. A. Cheruvanky, H. Zhou, T. Pisitkun, J.B. Kopp, M.A. Knepper, P.S.T. Yuen, and R.A. Star Rapid isolation of urinary exosomal biomarkers using a nanomembrane ultrafiltration concentrator Am. J. Physiol. Renal Physiol. 292 2007 1657 1661
29. www.BiooScientific.com.
30. R.C. Lai, F. Arslan, M.M. Lee, N.S.K. Sze, A. Choo, T.S. Chen, M. Salto-Tellez, L. Timmers, C.N. Lee, R.M. El Oakley, G. Pasterkamp, D.P.V. de Kleijn, and S.K. Lim Exosome secreted by MSC reduces myocardial ischemia/reperfusion injury Stem Cell Research 4 2010 214 222
31. K. Wang, S. Zhang, J. Weber, D. Baxter, and D.J. Galas Export of microRNAs and microRNA-protective protein by mammalian cells Nucleic Acids Res. 38 2010 7248 7259
32. K.R. Yamamoto, B.M. Alberts, R. Benzinger, L. Lawhorne, and G. Treiber Rapid bacteriophage sedimentation in the presence of polyethylene glycol and its application to large-scale virus purification Virology 40 1970 734 744
33. A. Adams Concentration of Epstein-Barr virus from cell culture fluids with polyethylene glycol J. Gen. Virol. 20 1973 391 394
34. G.D. Lewis, and T.G. Metcalf Polyethylene glycol precipitation for recovery of pathogenic viruses, including Hepatitis A virus and human Rotavirus, from oyster, water, and sediment samples Appl. Environ. Microbiol. 4 1988 1983 1988
35. www.SystemBio.com.
36. C. Chen, J. Skog, C.H. Hsu, R.T. Lessard, L. Balaj, T. Wurdinger, B.S. Carter, X.O. Breakefield, M. Toner, and D. Irimia Microfluidic isolation and transcriptome analysis of serum microvesicles Lab Chip 10 2010 505 511
37. www.HansaBioMed.eu.
38. www.AethlonMedical.com.
39. A. Lakkaraju, and E. Rodriguez-Boulan Itinerant exosomes: emerging roles in cell and tissue polarity Trends Cell Biol. 18 2008 199 209
40. J.S. Schorey, and S. Bhatnagar Exosome function: from tumor immunology to pathogen biology Traffic 9 2008 871 881
41. R.M. Johnstone, A. Mathew, A.B. Mason, and K. Teng Exosome formation during maturation of mammalian and avian reticulocytes: evidence that exosome release is a major route for externalization of obsolete membrane proteins J. Cell. Physiol. 147 1991 27 36
42. R.M. Johnstone Exosomes biological significance: a concise review Blood Cells Mol. Dis. 36 2006 315 321
43. C. Thery, M. Ostrowski, and E. Segura Membrane vesicles as conveyors of immune responses Nat. Rev. Immunol. 9 2009 581 593
44. C. Thery, L. Zitvogel, and S. Amigorena Exosomes: composition, biogenesis and function Nat. Rev. Immunol. 2 2002 569 579
45. A. Janowska-Wieczorek, M. Wysoczynski, J. Kijowski, L. Marquez-Curtis, B. Machalinski, J. Ratajczak, and M.Z. Ratajczak Microvesicles derived from activated platelets induce metastasis and angiogenesis in lung cancer Int. J. Cancer 113 2005 752 760
46. H.F. Heijnen, A.E. Schiel, R. Fijnheer, H.J. Geuze, and J.J. Sixma Activated platelets release two types of membrane vesicles: microvesicles by surface shedding and exosomes derived from exocytosis of multivesicular bodies and alpha-granules Blood 94 1999 3791 3799
47. P.W. Kriebel, V.A. Barr, E.C. Rericha, G. Zhang, and C.A. Parent Collective cell migration requires vesicular trafficking for chemoattractant delivery at the trailing edge J. Cell Biol. 183 2008 949 961
48. N. Kosaka, H. Izumi, K. Sekine, and T. Ochiya microRNA as a new immune-regulatory agent in breast milk Silence 3 2010 1 7
49. D.M. Pegtel, M.D. van de Garde, and J.M. Middeldorp Viral miRNAs exploiting the endosomal-exosomal pathway for intercellular cross-talk and immune evasion Biochim. Biophys. Acta 1809 2011 715 721
50. M. Belting, and A. Wittrup Nanotubes, exosomes, and nucleic acid-binding peptides provide novel mechanisms of intercellular communication in eukaryotic cells: implications in health and disease J. Cell Biol. 183 2008 1187 1191
51. K. Al-Nedawi, B. Meehan, J. Micallef, V. Lhotak, L. May, A. Guha, and J. Rak Intercellular transfer of the oncogenic receptor EGFRvIII by microvesicles derived from tumour cells Nat. Cell Biol. 10 2008 619 624
52. P. Leblanc, S. Alais, I. Porto-Carreiro, S. Lehmann, J. Grassi, G. Raposo, and J.L. Darlix Retrovirus infection strongly enhances scrapie infectivity release in cell culture EMBO J. 25 2006 2674 2685
53. D.M. Pegtel, K. Cosmopoulos, D.A. Thorley-Lawson, M.A. van Eijndhoven, E.S. Hopmans, J.L. Lindenberg, T.D. de Gruijl, T. Wurdinger, and J.M. Middeldorp Functional delivery of viral miRNAs via exosomes Proc. Natl. Acad. Sci. U. S. A. 107 2010 6328 6333
54. E. Chertova, O. Chertov, L.V. Coren, J.D. Roser, C.M. Trubey, J.W. Bess Jr., R.C. Sowder II, E. Barsov, B.L. Hood, R.J. Fisher, K. Nagashima, T.P. Conrads, T.D. Veenstra, J.D. Lifson, and D.E. Ott Proteomic and biochemical analysis of purified human immunodeficiency virus type 1 produced from infected monocyte-derived macrophages J. Virol. 80 2006 9039 9052
55. N. Izquierdo-Useros, M. Naranjo-Gomez, J. Archer, S.C. Hatch, I. Erkizia, J. Blanco, F.E. Borras, M.C. Puertas, J.H. Connor, M.T. Fernandez-Figueras, L. Moore, B. Clotet, S. Gummuluru, and J. Martinez-Picado Capture and transfer of HIV-1 particles by mature dendritic cells converges with the exosome-dissemination pathway Blood 113 2009 2732 2741
56. J. Ratajczak, M. Wysoczynski, F. Hayek, A. Janowska-Wieczorek, and M.Z. Ratajczak Membrane-derived microvesicles: important and underappreciated mediators of cell-to-cell communication Leukemia 20 2006 1487 1495
57. J. Mallegol, G. Van Niel, C. Lebreton, Y. Lepelletier, C. Candalh, C. Dugave, J.K. Heath, G. Raposo, N. Cerf-Bensussan, and M. Heyman T84-intestinal epithelial exosomes bear MHC Class II/peptide complexes potentiating antigen presentation by dendritic cells Gastroenterology 132 2007 1866 1876
58. C. Thery, A. Regnault, J. Garin, J. Wolfers, L. Zitvogel, P. Ricciardi-Castagnoli, G. Raposo, and S. Amigorena Molecular characterization of dendritic cell-derived exosomes. Selective accumulation of the heat shock protein hsc73 J. Cell Biol. 147 1999 599 610
59. X. Chen, Y. Ba, L. Ma, X. Cai, Y. Yin, K. Wang, J. Guo, Y. Zhang, J. Chen, X. Guo, Q. Li, X. Li, W. Wang, Y. Zhang, J. Wang, X. Jiang, Y. Xiang, C. Xu, P. Zheng, J. Zhang, R. Li, H. Zhang, X. Shang, T. Gong, G. Ning, J. Wang, K. Zen, J. Zhang, and C.-Y. Zhang Characterization of microRNAs in serum: a novel class of biomarkers for diagnosis of cancer and other diseases Cell Res. 5 2008 1 10
60. P.S. Mitchell, R.K. Parkin, E.M. Kroh, B.R. Fritz, S.K. Wyman, E.L. Pogosova-Agadjanyan, A. Peterson, J. Noteboom, K.C. O'Briant, A. Allen, D.W. Lin, N. Urban, C.W. Drescher, B.S. Knudsen, D.L. Stirewalt, R. Gentleman, R.L. Vessella, P.S. Nelson, D.B. Martin, and M. Tewari Circulating microRNAs as stable blood-based markers for cancer detection PNAS 105 2008 10513 10518
61. S. Gilad, E. Meiri, Y. Yogev, S. Benjamin, D. Lebanony, N. Yerushalmi, H. Benjamin, M. Kushnir, H. Cholakh, N. Melamed, Z. Bentwich, M. Hod, Y. Goren, and A. Chajut Serum microRNAs are promising novel biomarkers PLoS One 3 2008 e3148
62. J. Nilsson, J. Skog, A. Nordstrand, V. Baranov, L. Mincheva-Nilsson, X.O. Breakefield, and A. Widmark Prostate cancer-derived urine exosomes: a novel approach to biomarkers for prostate cancer Br. J. Cancer 100 2009 1603 1607
63. K. Takata, T. Matsuzaki, Y. Tajika, A. Ablimit, and T. Hasegawa Localization and trafficking of aquaporin 2 in the kidney Histochem. Cell Biol. 130 2008 197 209
64. V. Palanisamy, S. Sharma, A. Deshpande, H. Zhou, J. Gimzewski, and D.T. Wong Nanostructural and transcriptomic analyses of human saliva derived exosomes PLoS One 5 2010 e8577
65. N. Spielmann, and D.T. Wong Saliva: diagnostics and therapeutics perspectives Oral Dis. 17 2011 345 354
66. S. Keller, C. Rupp, A. Stoeck, S. Runz, M. Fogel, S. Lugert, H.D. Hager, M.S. Abdel-Bakky, P. Gutwein, and P. Altevogt CD24 is a marker of exosomes secreted into urine and amniotic fluid Kidney Int. 72 2007 1095 1102
67. www.CarisLifeSciences.com.
68. www.ExosomeDx.com.
69. B. Escudier, T. Dorval, N. Chaput, F. Andre, M.P. Caby, S. Novault, C. Flament, C. Leboulaire, C. Borg, S. Amigorena, C. Boccaccio, C. Bonnerot, O. Dhellin, M. Movassagh, S. Piperno, C. Robert, V. Serra, N. Valente, J.B. Le Pecq, A. Spatz, O. Lantz, T. Tursz, E. Angevin, and L. Zitvogel Vaccination of metastatic melanoma patients with autologous dendritic cell (DC) derived-exosomes: results of the first phase I clinical trial J. Transl. Med. 3 2005 10
70. M.A. Morse, J. Garst, T. Osada, S. Khan, A. Hobeika, T.M. Clay, N. Valente, R. Shreeniwas, M.A. Sutton, A. Delcayre, D.H. Hsu, J.B. Le Pecq, and H.K. Lyerly A phase I study of dexosome immunotherapy in patients with advanced non-small cell lung cancer J. Transl. Med. 3 2005 9
71. S. Dai, D. Wei, Z. Wu, X. Zhou, X. Wei, H. Huang, and G. Li Phase I clinical trial of autologous ascites-derived exosomes combined with GM-CSF for colorectal cancer Mol. Ther. 16 2008 782 790
72. S. Viaud, C. Thery, S. Ploix, T. Tursz, V. Lapierre, O. Lantz, L. Zitvogel, and N. Chaput Dendritic cell-derived exosomes for cancer immunotherapy: what's next? Cancer Res. 70 2010 1281 1285
73. L. Luketic, J. Delanghe, P.T. Sobol, P. Yang, E. Frotten, K.L. Mossman, J. Gauldie, J. Bramson, and Y. Wan Antigen presentation by exosomes released from peptide-pulsed dendritic cells is not suppressed by the presence of active CTL J. Immunol. 179 2007 5024 5032
74. H.G. Zhang, and W.E. Grizzle Exosomes and cancer: a newly described pathway of immune suppression Clin. Cancer Res. 17 2011 959 964
75. L. Blanc, C. Barres, P. Bette-Bobillo, and M. Vidal Reticulocyte-secreted exosomes bind natural IgM antibodies: involvement of a ROS activatable endosomal phospholipase iPLA2 Blood 110 2007 3407 3416
76. R. Safaei, B.J. Larson, T.C. Cheng, M.A. Gibson, S. Otani, W. Naerdemann, and S.B. Howell Abnormal lysosomal trafficking and enhanced exosomal export of cisplatin in drug-resistant human ovarian carcinoma cells Mol. Cancer Ther. 4 2005 1595 1604
77. K. Shedden, X.T. Xie, P. Chandaroy, Y.T. Chang, and G.R. Rosania Expulsion of small molecules in vesicles shed by cancer cells: association with gene expression and chemosensitivity profiles Cancer Res. 63 2003 4331 4337
78. L. Alvarez-Erviti, Y. Seow, H.F. Yin, C. Betts, S. Lakhal, and M.J. Wood Delivery of siRNA to the mouse brain by systemic injection of targeted exosomes Nat. Biotechnol. 29 2011 341 345
79. D. Sun, X. Zhuang, X. Xiang, Y. Liu, S. Zhang, C. Liu, S. Barnes, W. Grizzle, D. Miller, and H.G. Zhang A novel nanoparticle drug delivery system: the anti-inflammatory activity of curcumin is enhanced when encapsulated in exosomes Mol. Ther. 18 2010 1606 1614