Exosomes-structure, biogenesis and biological role in non-small-cell lung cancer

Scandinavian Journal of Immunology

Volumn 81, Issue 1, 2015, Pages 2-10

  Frydrychowicz, M ^a   Kolecka Bednarczyk, A ^a   Madejczyk, M ^a   Yasar, S ^a   Dworacki, G ^a  

^a POZNAN UNIVERSITY OF MEDICAL SCIENCES   (Poland)

Author keywords

[No Author keywords available]

Indexed keywords

ACTIN; ACTIVATED LEUKOCYTE CELL ADHESION MOLECULE; CD11B ANTIGEN; CD146 ANTIGEN; CD18 ANTIGEN; CD63 ANTIGEN; CD81 ANTIGEN; CD82 ANTIGEN; CD9 ANTIGEN; CELL PROTEIN; CHOLESTEROL; CYTOSKELETON PROTEIN; DIACYLGLYCEROL; GALECTIN 3; GLYCOPROTEIN P 15095; GUANOSINE TRIPHOSPHATASE; HEAT SHOCK PROTEIN 70; INTERCELLULAR ADHESION MOLECULE 1; LYMPHOCYTE FUNCTION ASSOCIATED ANTIGEN 1; LYMPHOCYTE FUNCTION ASSOCIATED ANTIGEN 3; MAJOR HISTOCOMPATIBILITY ANTIGEN CLASS 1; MAJOR HISTOCOMPATIBILITY ANTIGEN CLASS 2; MESSENGER RNA; MICRORNA; MOESIN; NUCLEIC ACID; PEROXIREDOXIN 2; PHOSPHOLIPID; PROTEIN 14 3 3; SYNENIN; UNCLASSIFIED DRUG; ESCRT PROTEIN; LIPID;

BIOGENESIS; CANCER GROWTH; CELL COMMUNICATION; CELL COMPONENT; CELL FUNCTION; CELL PROLIFERATION; CELL STRUCTURE; EXOSOME; FIBROBLAST; GROWTH STIMULATION; HUMAN; IMMUNE RESPONSE; IMMUNOCOMPETENT CELL; LIPID COMPOSITION; NON SMALL CELL LUNG CANCER; NONHUMAN; PHASE 1 CLINICAL TRIAL (TOPIC); PRIORITY JOURNAL; REVIEW; T LYMPHOCYTE; TUMOR MICROENVIRONMENT; TUMOR VASCULARIZATION; CHEMISTRY; GENETICS; LUNG TUMOR; METABOLISM; MULTIVESICULAR BODY; NEOVASCULARIZATION (PATHOLOGY); PATHOLOGY;

CARCINOMA, NON-SMALL-CELL LUNG; CELL COMMUNICATION; ENDOSOMAL SORTING COMPLEXES REQUIRED FOR TRANSPORT; EXOSOMES; HUMANS; LIPIDS; LUNG NEOPLASMS; MICRORNAS; MULTIVESICULAR BODIES; NEOVASCULARIZATION, PATHOLOGIC; TUMOR MICROENVIRONMENT;

EID: 84919628452     PISSN: 03009475     EISSN: 13653083     Source Type: Journal    
DOI: 10.1111/sji.12247     Document Type: Review

References (100)

1. Reiners KS, Dassler J, Coch CH, Pogge von Strandmann E. Role of exosomes released by dendritic cells and/or by tumor targets: regulation of NK cell plasticity. Front Immunol 2014;5:91.
2. Hannafon BN, Ding W-Q. Intracellular communication by exosome-derived microRNAs in cancer. Int J Mol Sci 2013;14:14240-69.
3. 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 1987;262:9412-20.
4. Bobrie A, Colombo M, Raposo G, Théry C. Exosome secretion: molecular mechanisms and roles in immune responses. Traffic 2011;12:1659-68.
5. Cocucci E, Racchetti G, Meldolesi J. Shedding microvesicles: artefacts no more. Trends Cell Biol 2009;19:43-51.
6. Harding C, Heuser J, Stahl P. Receptor-mediated endocytosis of transferrin and recycling of the transferrin receptor in rat reticulocytes. J Cell Biol 1983;97:329-39.
7. Mignot G, Roux S, Thery C, Ségura E, Zitvogel L. Prospects for exosomes in immunotherapy of cancer. J Cell Mol Med 2006;10:376-88.
8. Johnstone RM, Bianchini A, Teng K. Reticulocyte maturation and exosome release: transferrin receptor containing exosomes shows multiple plasma membrane functions. Blood 1989;74:1844-51.
9. Fader CM, Savina A, Sanchez D, Colombo MI. Exosome secretion and red cell maturation: exploring molecular components involved in the docking and fusion of multivesicular bodies in K562 cells. Blood Cells Mol Dis 2005;35:153-7.
10. Raposo G, Nijman HW, Stoorvogel W et al. B lymphocytes secrete antigen-presenting vesicles. J Exp Med 1996;183:1161-72.
11. Clayton A, Turkes A, Navabi H, Mason MD, Tabi Z. Induction of heat shock proteins in B-cell exosomes. J Cell Sci 2005;118 (Pt 16):3631-8.
12. Chaput N, Flament C, Viaud S et al. Dendritic cell derived-exosomes: bilogy and clinical implementations. J Leukoc Biol 2006;80:471-8.
13. Blanchard N, Lankar D, Faure F et al. TCR activation of human T cells induces the production of exosomes bearing the TCR/CD3/complex. J Immunol 2002;168:3235-41.
14. Zitvogel L, Regnault A, Lozier A et al. Eradication of established murine tumors using a novel cell-free vaccine: dendritic cell-derived exosomes. Nat Med 1998;4:594-600.
15. Laulagnier K, Motta C, Hamdi S et al. Mast cell and dendritic cell-derived exosomes display a specific lipid composition and anunusual membrane organization. Biochem J 2004;380 (Pt 1):161-71.
16. Heijnen HF, Schiel AE, Fijnheer R, Geuze HJ, Sixma JJ. Activated platelets release two types of membrane vesicles: microvesicles by surface shedding and exosomes derived from exocytosis of multivesicular bodies and alpha-granules. Blood 1999;94:3791-9.
17. Skokos D, Botros HG, Demeure C et al. Mast cell-derived exosomes induce phenotypic and functional maturation of dendritic cells and elicit specific immune responses in vivo. J Immunol 2003;170:3037-45.
18. Nguyen DG, Booth A, Gould SJ, Hildreth JE. Evidence that HIV budding in primary macrophages occurs through the exosome release pathway. Nat Med 1998;4:594-600.
19. Schorey JS, Bhatnagar S. Exosome function: from tumor immunology to pathogen biology. Traffic 2008;9:871-81.
20. van Niel G, Heyman M. The epithelial cell cytoskeleton and intracellular trafficking. II. Intestinal epithelial cell exosomes: perspectives on their structure and function. Am J Physiol Gastrointest Liver Physiol 2002;283:G251-5.
21. van Niel G, Mallegol J, Bevilacqua C et al. Intestinal epithelial exosomes carry MHC class II/peptides able to inform the immune system in mice. Gut 2003;52:1690-7.
22. Taylor DD, Gercel-Taylor C. Tumor-derived exosomes and their role in cancer-associated T-cell signaling defects. Br J Cancer 2005;92:305-11.
23. Wolfers J, Lozier A, Raposo G et al. Tumor-derived exosomes are a source of shared tumor rejection antigens for CTL cross-priming. Nat Med 2001;7:297-303.
24. Riteau B, Faure F, Menier C et al. Exosomes bearing HLA-G are released by melanoma cells. Hum Immunol 2003;64:1064-72.
25. Andre F, Schartz NE, Chaput N et al. Tumor-derived exosomes: a new source of tumor rejection antigens. Vaccine 2002;20 (Suppl. 4):A28-31.
26. Andre F, Schartz NE, Movassagh M et al. Malignant effusions and immunogenic tumor-derived exosomes. Lancet 2002;360:295-305.
27. van Niel G, Raposo G, Candalh C et al. Intestinal epithelial cells secrete exosome-like vesicles. Gastroenterology 2001;121:337-49.
28. Ge R, Tan E, Sharghi-Namini S, Asada HH. Exosomes in cancer microenvironment and beyond: have we overlooked these extracellular messengers? Cancer Microenviron 2012;5:323-32.
29. Faure J, Lachenal G, Court M et al. Exosomes are released by cultured cortical neurones. Mol Cell Neurosci 2006;31:642-8.
30. Hu G, Drescher KM, Chen X-M. Exosomal miRNAs: biological properties and therapeutic potential. Front Genet 2012;3:56.
31. Thery C, Zitvogel L, Amigorena S. Exosomes: composition, biogenesis and function. Nat Rev Immunol 2002;2:569-79.
32. Lotvall J, Valadi H. Cell to cell signalling via exosomes through esRNA. Cell Adh Migr 2007;1:156-8.
33. Hanson PI, Cashikar A. Multivesicular body morphogenesis. Annu Rev Cell Dev Biol 2012;28:337-62.
34. Schmidt O, Teis D. The ESCRT machinery. Curr Biol 2012;22:116-20.
35. Katzmann DJ, Babst M, Emr SD. Ubiquitin-dependent sorting into the multivesicular body pathway requires the function of a conserved endosomal protein sorting complex, ESCRT-I. Cell 2001;106:145-55.
36. Wollert T, Wunder C, Lippincott-Schwartz J, Hurley JH. Membrane scission by the ESCRT-III complex. Nature 2009;458:172-7.
37. Kosaka N, Iguchi H, Yoshioka Y, Takeshita F, Matsuki Y, Ochiya T. Secretory mechanisms and intercellular transfer of microRNAs in living cells. J Biol Chem 2010;285:17442-52.
38. Kogure T, Lin WL, Yan IK, Braconi C, Patel T. Intercellular nanovesicle-mediated microRNA transfer: a mechanism of environmental modulation of hepatocellular cancer cell growth. Hepatology 2011;54:1237-48.
39. Mittelbrunn M, Gutiérrez-Vázquez C, Villarroya-Beltri C et al. Unidirectional transfer of microRNA-loaded exosomes from T cells to antigen-presenting cells. Nat Commun 2011;2:282.
40. Trajkovic K, Hsu C, Chiantia S et al. Ceramide triggers budding of exosome vesicles into multivesicular endosomes. Science 2008;319:1244-7.
41. van Blitterswijk WJ, van der Luit AH, Veldman RJ, Verheij M, Borst J. Ceramide: second messenger or modulator of membrane structure and dynamics? Biochem J 2003;369 (Pt 2):199-211.
42. Subra C, Laulagnier K, Perret B, Record M. Exosome lipidomics unravels lipid sorting at the level of multivesicular bodies. Biochimie 2007;89:205-12.
43. van Niel G, Charrin S, Simoes S et al. The tetraspanin CD63 regulates ESCRT-independent and -dependent endosomal sorting during melanogenesis. Dev Cell 2011;21:708-21.
44. Savina A, Furlan M, Vidal M, Colombo MI. Exosome release is regulated by a calcium-dependent mechanism in K562 cells. J Biol Chem 2003;278:20083-90.
45. Iero M, Valenti R, Huber V et al. Tumour-released exosomes and their implications in cancer immunity. Cell Death Differ 2008;15:80-8.
46. Mathivanan S, Fahner CJ, Reid GE, Simpson RJ. ExoCarta 2012: database of exosomal proteins, RNA and lipids. Nucleic Acids Res 2012;40 (Database issue):D1241-4.
47. Mathivanan S, Simpson RJ. ExoCarta: a compendium of exosomal proteins and RNA. Proteomics 2009;9:4997-5000.
48. Mears R, Craven RA, Hanrahan S et al. Proteomic analysis of melanoma-derived exosomes by two-dimensional polyacrylamide gel electrophoresis and mass spectrometry. Proteomics 2004;4:4019-31.
49. Futter CE, White IJ. Annexins and endocytosis. Traffic 2007;8:951-8.
50. Thery C, Boussac M, Veron P et al. Proteomic analysis of dendritic cell-derived exosomes: a secreted subcellular compartment distinct from apoptotic vesicles. J Immunol 2001;166:7309-18.
51. Veron P, Segura E, Sugano G, Amigorena S, Thery C. Accumulation of MFG-E8/lactadherin on exosomes from immature dendritic cells. Blood Cells Mol Dis 2005;35:81-8.
52. Hegmans JP, Bard MP, Hemmes A et al. Proteomic analysis of exosomes secreted by human mesothelioma cells. Am J Pathol 2004;164:1807-15.
53. Record M. Exosomal lipids in cell-cell communication. In: Zhang H-G, ed. Emerging Concepts of Tumor Exosome-Mediated Cell-Cell Communication. New York, NY: Springer, 2013;8:47-68.
54. Subra C, Grand D, Laulagnier K et al. Exosomes account for vesicle-mediated transcellular transport of activatable phospholipases and prostaglandins. J Lipid Res 2010;51:2105-20.
55. Martinas VR, Dias MS, Hainaut P. Tumor-cell-derived microvesicles as carriers of molecular information in cancer. Curr Opin Oncol 2013;25:66-75.
56. Rana S, Malinowska K, Zöller M. Exosomal tumor microRNA modulates premetastatic organ cells. Neoplasia 2013;15:281-95.
57. Mathivanan S, Ji H, Simpson RJ. Exosomes: extracellular organelles important in intercellular communication. J Proteomics 2010;73:1907-20.
58. Lykke-Andersen S, Brodersen DE, Jensen TH. Origins and activities of the eukaryotic exosome. J Cell Sci 2009;122 (Pt 10):1487-94.
59. Zöller M. Pancreatic cancer diagnosis by free and exosomal miRNA. World J Gastrointest Pathophysiol 2013;4:74-90.
60. Nazarenko I, Rana S, Baumann A et al. Cell surface tetraspanin Tspan8 contributes to molecular pathways of exosome-induced endothelial cell activation. Cancer Res 2010;70:1668-78.
61. Skog J, Würdinger T, van Rijn S et al. Glioblastoma microvesicles transport RNA and proteins that promote tumour growth and provide diagnostic biomarkers. Nat Cell Biol 2008;10:1470-6.
62. Turchinovich A, Samatov TR, Tonevitsky AG, Burwinkel B. Circulating miRNAs: cell-cell communication function? Front Genet 2013;4:119.
63. Ajit SK. Circulating microRNAs as biomarkers, therapeutic targets, and signaling molecules. Sensors (Basel) 2012;12:3359-69.
64. 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;14:5338-66.
65. Bartel DP. MicroRNAs: genomics, biogenesis, mechanism, and function. Cell 2004;116:281-97.
66. Sahu R, Kaushik S, Clement CC et al. Microautophagy of cytosolic proteins by late endosomes. Dev Cell 2011;20:131-9.
67. Henderson MC, Azorsa DO. High-throughput RNAi screening for the identification of novel targets. Methods Mol Biol 2013;986:89-95.
68. Wittmann J, Jäck HM. Serum microRNAs as powerful cancer biomarkers. Biochim Biophys Acta 2010;1806:200-7.
69. Admyre C, Johansson SM, Qazi KR et al. Exosomes with immune modulatory features are present in human breast milk. J Immunol 2007;179:1969-78.
70. Masyuk AI, Masyuk TV, Larusso NF. Exosomes in the pathogenesis, diagnostics and therapeutics of liver diseases. J Hepatol 2013;59:621-5.
71. Vella LJ, Sharples RA, Nisbet RM, Cappai R, Hill AF. The role of exosomes in the processing of proteins associated with neurodegenerative diseases. Eur Biophys J 2008;37:323-32.
72. Kahlert C, Kalluri R. Exosomes in tumor microenvironment influence cancer progression and metstasis. J Mol Med (Berl) 2013;91:431-7.
73. Chalmin F, Ladoire S, Mignot G et al. Membrane-associated Hsp72 from tumor-derived exosomes mediates STAT3-dependent immunosuppressive function of mouse and human myeloid-derived suppressor cells. J Clin Invest 2010;120:457-71.
74. Nagaraj S, Gabrilovich DI. Regulation of suppressive function of myeloid-derived suppressor cells by CD4+ T cells. Semin Cancer Biol 2012;22:282-8.
75. Taylor DD, Gerçel-Taylor C, Lyons KS, Stanson J, Whiteside TL. T-cell apoptosis and suppression of T-cell receptor/CD3-zeta by Fas ligand-containing membrane vesicles shed from ovarian tumors. Clin Cancer Res 2003;9:5113-9.
76. Martínez-Lorenzo MJ, Anel A, Alava MA et al. The human melanoma cell line MelJuSo secretes bioactive FasL and APO2L/TRAIL on the surface of microvesicles. Possible contribution to tumor counterattack. Exp Cell Res 2004;295:315-29.
77. Wieckowski EU, Visus C, Szajnik M, Szczepanski MJ, Storkus WJ, Whiteside TL. Tumor-derived microvesicles promote regulatory T cell expansion and induce apoptosis in tumor-reactive activated CD8+ T lymphocytes. J Immunol 2009;183:3720-30.
78. Abusamra AJ, Zhong Z, Zheng X et al. Tumor exosomes expressing Fas ligand mediate CD8+ T-cell apoptosis. Blood Cells Mol Dis 2005;35:169-73.
79. Szajnik M, Czystowska M, Szczepanski MJ, Mandapathil M, Whiteside TL. Tumor-derived microvesicles induce, expand and up-regulate biological activities of human regulatory T cells (Treg). PLoS One 2010;5:e11469.
80. Lindau D, Gielen P, Kroesen M, Wesseling P, Adema GJ. The immunosuppressive tumor network: MDSCs, Tregs and NKT cells. Immunology 2013;138:105-15.
81. Grange C, Tapparo M, Collino F et al. Microvesicles released from human renal cancer stem cells stimulate angiogenesis and formation of lung premetastatic niche. Cancer Res 2011;71:5346-56.
82. Peinado H, Alečković M, Lavotshkin S et al. Melanoma exosomes educate bone marrow progenitor cells toward a pro-metastatic phenotype through MET. Nat Med 2012;18:883-91.
83. Chen T, Guo J, Yang M, Zhu X, Cao X. Chemokine-containing exosomes are released from heat-stressed tumor cells via lipid raft-dependent pathway and act as efficient tumor vaccine. J Immunol 2011;186:2219-28.
84. Xiao X, Yu S, Li S et al. Exosomes: decreased sensitivity of lung cancer A549 cells to cisplatin. PLoS One 2014;9:e89534.
85. Li W, Hu Y, Jiang T et al. Rab27A regulates exosome secretion from lung adenocarcinoma cells A549: involvement of EPI64. APMIS 2014;1080-7.
86. Fabbri M, Paone A, Calore F et al. MicroRNAs bind to Toll-like receptors to induce prometastatic inflammatory response. Proc Natl Acad Sci USA 2012;109:E2110-6.
87. Escudier B, Dorval T, Chaput N et al. Vaccination of metastatic melanoma patients with autologous dendritic cell (DC) derived-exosomes: results of the first phase I clinical trial. J Transl Med 2005;3:10.
88. Morse MA, Garst J, Osada T et al. A phase I study of dexosome immunotherapy in patients with advanced non-small cell lung cancer. J Transl Med 2005;3:9.
89. Li Y, Zhang Y, Qiu F, Qiu Z. Proteomic identification of exosomal LRG1: a potential urinary biomarker for detecting NSCLC. Electrophoresis 2011;32:1976-83.
90. Yamashita T, Kamada H, Kanasaki S et al. Epidermal growth factor receptor localized to exosome membranes as a possible biomarker for lung cancer diagnosis. Pharmazie 2013;68:969-73.
91. Valadi H, Ekström K, Bossios A, Sjöstrand M, Lee JJ, Lötvall JO. Exosome-mediated transfer of mRNAs and microRNAs is a novel mechanism of genetic exchange between cells. Nat Cell Biol 2007;9:654-9.
92. Rabinowits G, Gerçel-Taylor C, Day JM, Taylor DD, Kloecker GH. Exosomal microRNA: a diagnostic marker for lung cancer. Clin Lung Cancer 2009;10:42-6.
93. Yanaihara N, Caplen N, Bowman E et al. Unique microRNA molecular profiles in lung cancer diagnosis and prognosis. Cancer Cell 2006;9:189-98.
94. Seike M, Goto A, Okano T et al. MiR-21 is an EGFR regulated anti-apoptotic factor in lung cancer in never-smokers. Proc Natl Acad Sci USA 2009;106:12085-90.
95. Cho WC, Chow AS, Au JS. Restoration of tumour suppressor hsa-miR-145 inhibits cancer cell growth in lung adenocarcinoma patients with epidermal growth factor receptor mutation. Eur J Cancer 2009;45:2197-206.
96. Saito M, Schetter AJ, Mollerup S et al. The association of microRNA expression with prognosis and progression in early-stage, non-small cell lung adenocarcinoma: a retrospective analysis of three cohorts. Clin Cancer Res 2011;17:1875-82.
97. Rodríguez M, Silva J, López-Alfonso A et al. Different exosome cargo from plasma/bronchoalveolar lavage in non-small-cell lung cancer. Genes Chromosom Cancer 2014;731-24:1-12.
98. Sun Y, Bai Y, Zhang F, Wang Y, Guo Y, Guo L. miR-126 inhibits non-small cell lung cancer cells proliferation by targeting EGFL7. Biochem Biophys Res Commun 2010;391:483-9.
99. Ren G, Kang Y. A one-two punch of miR-126/126* against metastasis. Nat Cell Biol 2013;15:231-3.
100. Lipchina I, Studer L, Betel D. The expanding role of miR-302-367 in pluripotency and reprogramming. Cell Cycle 2012;11:1517-23.