Home LiteratureArticle Details
PMID: 23466882 Published · epublish English Journal Article

Exosomes as intercellular signaling organelles involved in health and disease: basic science and clinical applications.

International journal of molecular sciences ·Vol. 14 ·No. 3 ·2013-03-06 ·Pages 5338-66

Corrado C, Raimondo S, Chiesi A, Ciccia F, De Leo G, Alessandro R

Abstract

Cell to cell communication is essential for the coordination and proper organization of different cell types in multicellular systems. Cells exchange information through a multitude of mechanisms such as secreted growth factors and chemokines, small molecules (peptides, ions, bioactive lipids and nucleotides), cell-cell contact and the secretion of extracellular matrix components. Over the last few years, however, a considerable amount of experimental evidence has demonstrated the occurrence of a sophisticated method of cell communication based on the release of specialized membranous nano-sized vesicles termed exosomes. Exosome biogenesis involves the endosomal compartment, the multivesicular bodies (MVB), which contain internal vesicles packed with an extraordinary set of molecules including enzymes, cytokines, nucleic acids and different bioactive compounds. In response to stimuli, MVB fuse with the plasma membrane and vesicles are released in the extracellular space where they can interact with neighboring cells and directly induce a signaling pathway or affect the cellular phenotype through the transfer of new receptors or even genetic material. This review will focus on exosomes as intercellular signaling organelles involved in a number of physiological as well as pathological processes and their potential use in clinical diagnostics and therapeutics.

Authors & Affiliations
6 authors, click to expand affiliations / ORCID
Corrado Chiara
Department of Biopathology and Biomedical and Forensic Biotechnologies, Section of Biology and Genetics, Università di Palermo, Palermo 90133, Italy. riccardo.alessandro@unipa.it.
Raimondo Stefania
Chiesi Antonio
Ciccia Francesco
De Leo Giacomo
Alessandro Riccardo
References (167)
167 references, click to expand
  1. Mechanism of transfer of functional microRNAs between mouse dendritic cells via exosomes.
    Blood. 2012 Jan 19;119(3):756-66 PMID: 22031862
  2. Proteomic analysis of urine exosomes by multidimensional protein identification technology (MudPIT).
    Proteomics. 2012 Jan;12(2):329-38 PMID: 22106071
  3. Secretion of annexin A3 from ovarian cancer cells and its association with platinum resistance in ovarian cancer patients.
    J Cell Mol Med. 2012 Feb;16(2):337-48 PMID: 21435174
  4. Exosomes mediate stromal mobilization of autocrine Wnt-PCP signaling in breast cancer cell migration.
    Cell. 2012 Dec 21;151(7):1542-56 PMID: 23260141
  5. Toward tailored exosomes: the exosomal tetraspanin web contributes to target cell selection.
    Int J Biochem Cell Biol. 2012 Sep;44(9):1574-84 PMID: 22728313
  6. microRNA-155 regulates the generation of immunoglobulin class-switched plasma cells.
    Immunity. 2007 Dec;27(6):847-59 PMID: 18055230
  7. Pivotal role of paracrine effects in stem cell therapies in regenerative medicine: can we translate stem cell-secreted paracrine factors and microvesicles into better therapeutic strategies?
    Leukemia. 2012 Jun;26(6):1166-73 PMID: 22182853
  8. hsa-miR-210 Is induced by hypoxia and is an independent prognostic factor in breast cancer.
    Clin Cancer Res. 2008 Mar 1;14(5):1340-8 PMID: 18316553
  9. Astrocytes secrete exosomes enriched with proapoptotic ceramide and prostate apoptosis response 4 (PAR-4): potential mechanism of apoptosis induction in Alzheimer disease (AD).
    J Biol Chem. 2012 Jun 15;287(25):21384-95 PMID: 22532571
  10. Characterization and proteomic analysis of ovarian cancer-derived exosomes.
    J Proteomics. 2013 Mar 27;80:171-82 PMID: 23333927
  11. The majority of microRNAs detectable in serum and saliva is concentrated in exosomes.
    PLoS One. 2012;7(3):e30679 PMID: 22427800
  12. Lysosomal dysfunction increases exosome-mediated alpha-synuclein release and transmission.
    Neurobiol Dis. 2011 Jun;42(3):360-7 PMID: 21303699
  13. Exosomes derived from genetically modified DC expressing FasL are anti-inflammatory and immunosuppressive.
    Mol Ther. 2006 Feb;13(2):289-300 PMID: 16275099
  14. Exosomes: a new delivery system for tumor antigens in cancer immunotherapy.
    Int J Cancer. 2005 Apr 20;114(4):613-22 PMID: 15609328
  15. Exosome release is regulated by a calcium-dependent mechanism in K562 cells.
    J Biol Chem. 2003 May 30;278(22):20083-90 PMID: 12639953
  16. The cis-acting signals that target proteins to exosomes and microvesicles.
    Biochem Soc Trans. 2013 Feb 1;41(1):277-82 PMID: 23356297
  17. Exosomal transfer of proteins and RNAs at synapses in the nervous system.
    Biol Direct. 2007 Nov 30;2:35 PMID: 18053135
  18. Plasma exosomes can deliver exogenous short interfering RNA to monocytes and lymphocytes.
    Nucleic Acids Res. 2012 Sep 1;40(17):e130 PMID: 22618874
  19. Rab11 promotes docking and fusion of multivesicular bodies in a calcium-dependent manner.
    Traffic. 2005 Feb;6(2):131-43 PMID: 15634213
  20. Formation and release of arrestin domain-containing protein 1-mediated microvesicles (ARMMs) at plasma membrane by recruitment of TSG101 protein.
    Proc Natl Acad Sci U S A. 2012 Mar 13;109(11):4146-51 PMID: 22315426
  21. Identification, proteomic profiling, and origin of ram epididymal fluid exosome-like vesicles.
    Biol Reprod. 2005 Jun;72(6):1452-65 PMID: 15635128
  22. Cells release prions in association with exosomes.
    Proc Natl Acad Sci U S A. 2004 Jun 29;101(26):9683-8 PMID: 15210972
  23. TfR2 localizes in lipid raft domains and is released in exosomes to activate signal transduction along the MAPK pathway.
    J Cell Sci. 2006 Nov 1;119(Pt 21):4486-98 PMID: 17046995
  24. Exosomes as potent cell-free peptide-based vaccine. I. Dendritic cell-derived exosomes transfer functional MHC class I/peptide complexes to dendritic cells.
    J Immunol. 2004 Feb 15;172(4):2126-36 PMID: 14764678
  25. Increased expression of annexin A3 is a mechanism of platinum resistance in ovarian cancer.
    Cancer Res. 2010 Feb 15;70(4):1616-24 PMID: 20103635
  26. CD8+ dendritic cells use LFA-1 to capture MHC-peptide complexes from exosomes in vivo.
    J Immunol. 2007 Aug 1;179(3):1489-96 PMID: 17641014
  27. Microvesicles: messengers and mediators of tumor progression.
    Cell Cycle. 2009 Jul 1;8(13):2014-8 PMID: 19535896
  28. Exosome-associated tau is secreted in tauopathy models and is selectively phosphorylated in cerebrospinal fluid in early Alzheimer disease.
    J Biol Chem. 2012 Feb 3;287(6):3842-9 PMID: 22057275
  29. Protein targeting to exosomes/microvesicles by plasma membrane anchors.
    J Biol Chem. 2011 Apr 22;286(16):14383-95 PMID: 21300796
  30. Exosome secreted by MSC reduces myocardial ischemia/reperfusion injury.
    Stem Cell Res. 2010 May;4(3):214-22 PMID: 20138817
  31. bicoid RNA localization requires specific binding of an endosomal sorting complex.
    Nature. 2007 Feb 1;445(7127):554-8 PMID: 17268469
  32. Tolerance induction by exosomes from immature dendritic cells and rapamycin in a mouse cardiac allograft model.
    PLoS One. 2012;7(8):e44045 PMID: 22952868
  33. From the antigen-presenting cell to the antigen-presenting vesicle: the exosomes.
    Curr Opin Mol Ther. 2002 Aug;4(4):372-81 PMID: 12222875
  34. ExoCarta: A compendium of exosomal proteins and RNA.
    Proteomics. 2009 Nov;9(21):4997-5000 PMID: 19810033
  35. Liposome-bound APO2L/TRAIL is an effective treatment in a rabbit model of rheumatoid arthritis.
    Arthritis Rheum. 2010 Aug;62(8):2272-82 PMID: 20506326
  36. Immunosuppressive exosomes from TGF-β1 gene-modified dendritic cells attenuate Th17-mediated inflammatory autoimmune disease by inducing regulatory T cells.
    Cell Res. 2012 Mar;22(3):607-10 PMID: 22157651
  37. Activated T cells recruit exosomes secreted by dendritic cells via LFA-1.
    Blood. 2009 Feb 26;113(9):1977-81 PMID: 19064723
  38. Anti-CCP antibodies: the past, the present and the future.
    Nat Rev Rheumatol. 2011 Jun 07;7(7):391-8 PMID: 21647203
  39. Tolerosome-induced oral tolerance is MHC dependent.
    Immunology. 2005 Dec;116(4):464-76 PMID: 16313360
  40. T84-intestinal epithelial exosomes bear MHC class II/peptide complexes potentiating antigen presentation by dendritic cells.
    Gastroenterology. 2007 May;132(5):1866-76 PMID: 17484880
  41. Proteomic analysis of microvesicles in human saliva by gel electrophoresis with liquid chromatography-mass spectrometry.
    Anal Chim Acta. 2012 Apr 20;723:61-7 PMID: 22444574
  42. Exfoliation of membrane ecto-enzymes in the form of micro-vesicles.
    Biochim Biophys Acta. 1981 Jul 6;645(1):63-70 PMID: 6266476
  43. Human tumor-derived exosomes down-modulate NKG2D expression.
    J Immunol. 2008 Jun 1;180(11):7249-58 PMID: 18490724
  44. Role of exosomes released by chronic myelogenous leukemia cells in angiogenesis.
    Int J Cancer. 2012 May 1;130(9):2033-43 PMID: 21630268
  45. Cutting edge: unique T cells that recognize citrullinated peptides are a feature of protein immunization.
    J Immunol. 2006 Aug 1;177(3):1421-5 PMID: 16849447
  46. Get on the exosome bus with ALIX.
    Nat Cell Biol. 2012 Jun 29;14(7):654-5 PMID: 22743708
  47. Human tumor nanoparticles induce apoptosis of pancreatic cancer cells.
    FASEB J. 2008 Sep;22(9):3358-69 PMID: 18511551
  48. Syndecan-syntenin-ALIX regulates the biogenesis of exosomes.
    Nat Cell Biol. 2012 Jun 03;14(7):677-85 PMID: 22660413
  49. Eradication of established murine tumors using a novel cell-free vaccine: dendritic cell-derived exosomes.
    Nat Med. 1998 May;4(5):594-600 PMID: 9585234
  50. Hypoxic tumor cell modulates its microenvironment to enhance angiogenic and metastatic potential by secretion of proteins and exosomes.
    Mol Cell Proteomics. 2010 Jun;9(6):1085-99 PMID: 20124223
  51. Isolation of bovine milk-derived microvesicles carrying mRNAs and microRNAs.
    Biochem Biophys Res Commun. 2010 May 28;396(2):528-33 PMID: 20434431
  52. "Tolerosomes" are produced by intestinal epithelial cells.
    Eur J Immunol. 2001 Oct;31(10):2892-900 PMID: 11592064
  53. Vesicle formation during reticulocyte maturation. Association of plasma membrane activities with released vesicles (exosomes).
    J Biol Chem. 1987 Jul 5;262(19):9412-20 PMID: 3597417
  54. Bovine milk exosome proteome.
    J Proteomics. 2012 Feb 16;75(5):1486-92 PMID: 22129587
  55. Exosomal-like vesicles are present in human blood plasma.
    Int Immunol. 2005 Jul;17(7):879-87 PMID: 15908444
  56. MHC class II+ exosomes in plasma suppress inflammation in an antigen-specific and Fas ligand/Fas-dependent manner.
    J Immunol. 2007 Aug 15;179(4):2235-41 PMID: 17675484
  57. Microenvironmental pH is a key factor for exosome traffic in tumor cells.
    J Biol Chem. 2009 Dec 4;284(49):34211-22 PMID: 19801663
  58. The multifaceted exosome: biogenesis, role in normal and aberrant cellular function, and frontiers for pharmacological and biomarker opportunities.
    Biochem Pharmacol. 2012 Jun 1;83(11):1484-94 PMID: 22230477
  59. Induction of tolerance by exosomes and short-term immunosuppression in a fully MHC-mismatched rat cardiac allograft model.
    Am J Transplant. 2006 Jul;6(7):1541-50 PMID: 16827854
  60. Hypoxia--a key regulatory factor in tumour growth.
    Nat Rev Cancer. 2002 Jan;2(1):38-47 PMID: 11902584
  61. Delivery of siRNA to the mouse brain by systemic injection of targeted exosomes.
    Nat Biotechnol. 2011 Apr;29(4):341-5 PMID: 21423189
  62. Serum-derived exosomes from antigen-fed mice prevent allergic sensitization in a model of allergic asthma.
    Immunology. 2008 Sep;125(1):21-7 PMID: 18355242
  63. The role of tetraspanin CD63 in antigen presentation via MHC class II.
    Eur J Immunol. 2011 Sep;41(9):2556-61 PMID: 21660937
  64. T cell-induced secretion of MHC class II-peptide complexes on B cell exosomes.
    EMBO J. 2007 Oct 3;26(19):4263-72 PMID: 17805347
  65. Urinary exosomes: a reservoir for biomarker discovery and potential mediators of intrarenal signalling.
    Proteomics. 2013 May;13(10-11):1572-80 PMID: 23129434
  66. Vesiclepedia: a compendium for extracellular vesicles with continuous community annotation.
    PLoS Biol. 2012;10(12):e1001450 PMID: 23271954
  67. Immature dendritic cell-derived exosomes: a promise subcellular vaccine for autoimmunity.
    Inflammation. 2013 Feb;36(1):232-40 PMID: 22956173
  68. Induction of exosome release in primary B cells stimulated via CD40 and the IL-4 receptor.
    J Immunol. 2008 Jun 15;180(12):8146-52 PMID: 18523279
  69. Exosomes from Plasmodium yoelii-infected reticulocytes protect mice from lethal infections.
    PLoS One. 2011;6(10):e26588 PMID: 22046311
  70. Gastric cancer exosomes promote tumour cell proliferation through PI3K/Akt and MAPK/ERK activation.
    Dig Liver Dis. 2009 Dec;41(12):875-80 PMID: 19473897
  71. Tumor-exosomes and leukocyte activation: an ambivalent crosstalk.
    Cell Commun Signal. 2012 Nov 28;10(1):37 PMID: 23190502
  72. Mast cell synapses and exosomes: membrane contacts for information exchange.
    Front Immunol. 2012 Mar 15;3:46 PMID: 22566928
  73. A strategy of antigen incorporation into exosomes: comparing cross-presentation levels of antigens delivered by engineered exosomes and by lentiviral virus-like particles.
    Vaccine. 2012 Nov 26;30(50):7229-37 PMID: 23099330
  74. Effective treatment of inflammatory disease models with exosomes derived from dendritic cells genetically modified to express IL-4.
    J Immunol. 2007 Aug 15;179(4):2242-9 PMID: 17675485
  75. Human prostasomes express CD48 and interfere with NK cell function.
    Immunobiology. 2011 Jan-Feb;216(1-2):41-6 PMID: 20382443
  76. Atheroprotective communication between endothelial cells and smooth muscle cells through miRNAs.
    Nat Cell Biol. 2012 Feb 12;14(3):249-56 PMID: 22327366
  77. Exosomes derived from human bone marrow mesenchymal stem cells promote tumor growth in vivo.
    Cancer Lett. 2012 Feb 1;315(1):28-37 PMID: 22055459
  78. Tumour exosomes inhibit binding of tumour-reactive antibodies to tumour cells and reduce ADCC.
    Cancer Immunol Immunother. 2011 May;60(5):639-48 PMID: 21293856
  79. MicroRNAs bind to Toll-like receptors to induce prometastatic inflammatory response.
    Proc Natl Acad Sci U S A. 2012 Jul 31;109(31):E2110-6 PMID: 22753494
  80. Mesenchymal stem cells within tumour stroma promote breast cancer metastasis.
    Nature. 2007 Oct 4;449(7162):557-63 PMID: 17914389
  81. Exosomes: the ideal nanovectors for biodelivery.
    Biol Chem. 2013 Jan;394(1):1-15 PMID: 23241589
  82. Mesenchymal stem cells derived from bone marrow favor tumor cell growth in vivo.
    Exp Mol Pathol. 2006 Jun;80(3):267-74 PMID: 16214129
  83. Proteomic analysis of exosomes from mutant KRAS colon cancer cells identifies intercellular transfer of mutant KRAS.
    Mol Cell Proteomics. 2013 Feb;12(2):343-55 PMID: 23161513
  84. Receptor-mediated endocytosis of transferrin and recycling of the transferrin receptor in rat reticulocytes.
    J Cell Biol. 1983 Aug;97(2):329-39 PMID: 6309857
  85. MicroRNAs modulate hematopoietic lineage differentiation.
    Science. 2004 Jan 2;303(5654):83-6 PMID: 14657504
  86. Pregnancy-associated exosomes and their modulation of T cell signaling.
    J Immunol. 2006 Feb 1;176(3):1534-42 PMID: 16424182
  87. Exosomes are released by cultured cortical neurones.
    Mol Cell Neurosci. 2006 Apr;31(4):642-8 PMID: 16446100
  88. Exosomes: current knowledge of their composition, biological functions, and diagnostic and therapeutic potentials.
    Biochim Biophys Acta. 2012 Jul;1820(7):940-8 PMID: 22503788
  89. γ-Synuclein: seeding of α-synuclein aggregation and transmission between cells.
    Biochemistry. 2012 Jun 12;51(23):4743-54 PMID: 22620680
  90. Immune surveillance properties of human NK cell-derived exosomes.
    J Immunol. 2012 Sep 15;189(6):2833-42 PMID: 22904309
  91. Electron microscopic evidence for externalization of the transferrin receptor in vesicular form in sheep reticulocytes.
    J Cell Biol. 1985 Sep;101(3):942-8 PMID: 2993317
  92. Increased microRNA-1 and microRNA-133a levels in serum of patients with cardiovascular disease indicate myocardial damage.
    Circ Cardiovasc Genet. 2011 Aug 1;4(4):446-54 PMID: 21642241
  93. Direct B cell stimulation by dendritic cells in a mouse model of lupus.
    Arthritis Rheum. 2008 Jun;58(6):1741-50 PMID: 18512810
  94. Exosomes with immune modulatory features are present in human breast milk.
    J Immunol. 2007 Aug 1;179(3):1969-78 PMID: 17641064
  95. Comparative and targeted proteomic analyses of urinary microparticles from bladder cancer and hernia patients.
    J Proteome Res. 2012 Dec 7;11(12):5611-29 PMID: 23082778
  96. Exosomes communicate protective messages during oxidative stress; possible role of exosomal shuttle RNA.
    PLoS One. 2010 Dec 17;5(12):e15353 PMID: 21179422
  97. Exosomes derived from immature bone marrow dendritic cells induce tolerogenicity of intestinal transplantation in rats.
    J Surg Res. 2011 Dec;171(2):826-32 PMID: 20828738
  98. Advances in membranous vesicle and exosome proteomics improving biological understanding and biomarker discovery.
    Proteomics. 2011 Feb;11(4):709-20 PMID: 21241021
  99. Enabling a robust scalable manufacturing process for therapeutic exosomes through oncogenic immortalization of human ESC-derived MSCs.
    J Transl Med. 2011 Apr 25;9:47 PMID: 21513579
  100. A novel nanoparticle drug delivery system: the anti-inflammatory activity of curcumin is enhanced when encapsulated in exosomes.
    Mol Ther. 2010 Sep;18(9):1606-14 PMID: 20571541
  101. MicroRNA signatures of tumor-derived exosomes as diagnostic biomarkers of ovarian cancer.
    Gynecol Oncol. 2008 Jul;110(1):13-21 PMID: 18589210
  102. Exosome-mediated transfer of mRNAs and microRNAs is a novel mechanism of genetic exchange between cells.
    Nat Cell Biol. 2007 Jun;9(6):654-9 PMID: 17486113
  103. MicroRNA regulation of DNA repair gene expression in hypoxic stress.
    Cancer Res. 2009 Feb 1;69(3):1221-9 PMID: 19141645
  104. Mesenchymal stem cells as all-round supporters in a normal and neoplastic microenvironment.
    Cell Commun Signal. 2012 Sep 03;10(1):26 PMID: 22943670
  105. The regulation of the endosomal compartment by p53 the tumor suppressor gene.
    FEBS J. 2009 Apr;276(8):2201-12 PMID: 19302216
  106. Exosomes released by K562 chronic myeloid leukemia cells promote angiogenesis in a Src-dependent fashion.
    Angiogenesis. 2012 Mar;15(1):33-45 PMID: 22203239
  107. Platelet-derived exosomes from septic shock patients induce myocardial dysfunction.
    Crit Care. 2007;11(6):R120 PMID: 17996049
  108. Alzheimer's disease results from the cerebral accumulation and cytotoxicity of amyloid beta-protein.
    J Alzheimers Dis. 2001 Feb;3(1):75-80 PMID: 12214075
  109. Organizing the cell cortex: the role of ERM proteins.
    Nat Rev Mol Cell Biol. 2010 Apr;11(4):276-87 PMID: 20308985
  110. Role of exosomes/microvesicles in the nervous system and use in emerging therapies.
    Front Physiol. 2012 Jun 27;3:228 PMID: 22754538
  111. Proteomic analysis of microglia-derived exosomes: metabolic role of the aminopeptidase CD13 in neuropeptide catabolism.
    J Immunol. 2005 Aug 15;175(4):2237-43 PMID: 16081791
  112. A membrane form of TNF-alpha presented by exosomes delays T cell activation-induced cell death.
    J Immunol. 2006 Jun 15;176(12):7385-93 PMID: 16751383
  113. Exosome-mediated delivery of siRNA in vitro and in vivo.
    Nat Protoc. 2012 Dec;7(12):2112-26 PMID: 23154783
  114. Role of hypoxia in the hallmarks of human cancer.
    J Cell Biochem. 2009 Aug 15;107(6):1053-62 PMID: 19479945
  115. Degradation of AP2 during reticulocyte maturation enhances binding of hsc70 and Alix to a common site on TFR for sorting into exosomes.
    Traffic. 2004 Mar;5(3):181-93 PMID: 15086793
  116. Mesenchymal stem cells enhance growth and metastasis of colon cancer.
    Int J Cancer. 2010 Nov 15;127(10):2323-33 PMID: 20473928
  117. miR-181a is an intrinsic modulator of T cell sensitivity and selection.
    Cell. 2007 Apr 6;129(1):147-61 PMID: 17382377
  118. Abnormal lysosomal trafficking and enhanced exosomal export of cisplatin in drug-resistant human ovarian carcinoma cells.
    Mol Cancer Ther. 2005 Oct;4(10):1595-604 PMID: 16227410
  119. Role of Exosome in infectious disease.
    Inflamm Allergy Drug Targets. 2012 Dec 04;: PMID: 23228092
  120. Exosomes as a short-range mechanism to spread alloantigen between dendritic cells during T cell allorecognition.
    J Immunol. 2008 Mar 1;180(5):3081-90 PMID: 18292531
  121. First trimester trophoblast cells secrete Fas ligand which induces immune cell apoptosis.
    Mol Hum Reprod. 2004 Jan;10(1):55-63 PMID: 14665707
  122. Nanotubes, exosomes, and nucleic acid-binding peptides provide novel mechanisms of intercellular communication in eukaryotic cells: implications in health and disease.
    J Cell Biol. 2008 Dec 29;183(7):1187-91 PMID: 19103810
  123. Packaging of prions into exosomes is associated with a novel pathway of PrP processing.
    J Pathol. 2007 Apr;211(5):582-590 PMID: 17334982
  124. Immune-related microRNAs are abundant in breast milk exosomes.
    Int J Biol Sci. 2012;8(1):118-23 PMID: 22211110
  125. Large-scale proteomics and phosphoproteomics of urinary exosomes.
    J Am Soc Nephrol. 2009 Feb;20(2):363-79 PMID: 19056867
  126. Proteomic analysis of human parotid gland exosomes by multidimensional protein identification technology (MudPIT).
    J Proteome Res. 2009 Mar;8(3):1304-14 PMID: 19199708
  127. Exosomal microRNA: a diagnostic marker for lung cancer.
    Clin Lung Cancer. 2009 Jan;10(1):42-6 PMID: 19289371
  128. Isolation and identification of potential urinary microparticle biomarkers of bladder cancer.
    J Proteome Res. 2008 May;7(5):2088-96 PMID: 18373357
  129. Exosomes/microvesicles: mediators of cancer-associated immunosuppressive microenvironments.
    Semin Immunopathol. 2011 Sep;33(5):441-54 PMID: 21688197
  130. Transmission of prions.
    Proc Natl Acad Sci U S A. 2002 Dec 10;99 Suppl 4:16378-83 PMID: 12181490
  131. Proteomics analysis of A33 immunoaffinity-purified exosomes released from the human colon tumor cell line LIM1215 reveals a tissue-specific protein signature.
    Mol Cell Proteomics. 2010 Feb;9(2):197-208 PMID: 19837982
  132. Exosomal transmission of functional aquaporin 2 in kidney cortical collecting duct cells.
    J Physiol. 2011 Dec 15;589(Pt 24):6119-27 PMID: 22025668
  133. Melanoma exosomes educate bone marrow progenitor cells toward a pro-metastatic phenotype through MET.
    Nat Med. 2012 Jun;18(6):883-91 PMID: 22635005
  134. Exosomes--vesicular carriers for intercellular communication.
    Curr Opin Cell Biol. 2009 Aug;21(4):575-81 PMID: 19442504
  135. Association of citrullinated proteins with synovial exosomes.
    Arthritis Rheum. 2006 Dec;54(12):3809-14 PMID: 17133577
  136. Human saliva, plasma and breast milk exosomes contain RNA: uptake by macrophages.
    J Transl Med. 2011 Jan 14;9:9 PMID: 21235781
  137. Export of microRNAs and microRNA-protective protein by mammalian cells.
    Nucleic Acids Res. 2010 Nov;38(20):7248-59 PMID: 20615901
  138. Exosomes from bronchoalveolar fluid of tolerized mice prevent allergic reaction.
    J Immunol. 2008 Jul 15;181(2):1519-25 PMID: 18606707
  139. Salivary gland epithelial cell exosomes: A source of autoantigenic ribonucleoproteins.
    Arthritis Rheum. 2005 May;52(5):1517-21 PMID: 15880835
  140. Cellular internalization of exosomes occurs through phagocytosis.
    Traffic. 2010 May;11(5):675-87 PMID: 20136776
  141. Carboxyamidotriazole-orotate inhibits the growth of imatinib-resistant chronic myeloid leukaemia cells and modulates exosomes-stimulated angiogenesis.
    PLoS One. 2012;7(8):e42310 PMID: 22879938
  142. Release of exosomes from differentiated neurons and its regulation by synaptic glutamatergic activity.
    Mol Cell Neurosci. 2011 Feb;46(2):409-18 PMID: 21111824
  143. B lymphocytes secrete antigen-presenting vesicles.
    J Exp Med. 1996 Mar 1;183(3):1161-72 PMID: 8642258
  144. Regulation of heat shock protein 70 release in astrocytes: role of signaling kinases.
    Dev Neurobiol. 2007 Nov;67(13):1815-29 PMID: 17701989
  145. Cytoplasmic microvesicular form of Fas ligand in human early placenta: switching the tissue immune privilege hypothesis from cellular to vesicular level.
    Mol Hum Reprod. 2005 Jan;11(1):35-41 PMID: 15579659
  146. The role of microRNA-1 and microRNA-133 in skeletal muscle proliferation and differentiation.
    Nat Genet. 2006 Feb;38(2):228-33 PMID: 16380711
  147. GP120-specific exosome-targeted T cell-based vaccine capable of stimulating DC- and CD4(+) T-independent CTL responses.
    Vaccine. 2011 Apr 27;29(19):3538-47 PMID: 21406265
  148. Hypoxic enhancement of exosome release by breast cancer cells.
    BMC Cancer. 2012 Sep 24;12:421 PMID: 22998595
  149. Adhesion and signaling by B cell-derived exosomes: the role of integrins.
    FASEB J. 2004 Jun;18(9):977-9 PMID: 15059973
  150. Exosome-like vesicles with dipeptidyl peptidase IV in human saliva.
    Biol Pharm Bull. 2008 Jun;31(6):1059-62 PMID: 18520029
  151. Signal transduction targets in invasion.
    Clin Exp Metastasis. 2002;19(3):265-73 PMID: 12067207
  152. Therapeutic potential of mesenchymal stem cell-derived microvesicles.
    Nephrol Dial Transplant. 2012 Aug;27(8):3037-42 PMID: 22851627
  153. Leukemia cell to endothelial cell communication via exosomal miRNAs.
    Oncogene. 2013 May 30;32(22):2747-55 PMID: 22797057
  154. The transcellular spread of cytosolic amyloids, prions, and prionoids.
    Neuron. 2009 Dec 24;64(6):783-90 PMID: 20064386
  155. Bronchoalveolar lavage fluid exosomes contribute to cytokine and leukotriene production in allergic asthma.
    Allergy. 2012 Jul;67(7):911-9 PMID: 22620679
  156. Exosomes: extracellular organelles important in intercellular communication.
    J Proteomics. 2010 Sep 10;73(10):1907-20 PMID: 20601276
  157. The metastatic niche: adapting the foreign soil.
    Nat Rev Cancer. 2009 Apr;9(4):285-93 PMID: 19308068
  158. Molecular characterization of dendritic cell-derived exosomes. Selective accumulation of the heat shock protein hsc73.
    J Cell Biol. 1999 Nov 1;147(3):599-610 PMID: 10545503
  159. Human placenta expresses and secretes NKG2D ligands via exosomes that down-modulate the cognate receptor expression: evidence for immunosuppressive function.
    J Immunol. 2009 Jul 1;183(1):340-51 PMID: 19542445
  160. RNA trafficking by acute myelogenous leukemia exosomes.
    Cancer Res. 2013 Jan 15;73(2):918-29 PMID: 23149911
  161. Exosomes with major histocompatibility complex class II and co-stimulatory molecules are present in human BAL fluid.
    Eur Respir J. 2003 Oct;22(4):578-83 PMID: 14582906
  162. Systemically injected exosomes targeted to EGFR deliver antitumor microRNA to breast cancer cells.
    Mol Ther. 2013 Jan;21(1):185-91 PMID: 23032975
  163. Unidirectional transfer of microRNA-loaded exosomes from T cells to antigen-presenting cells.
    Nat Commun. 2011;2:282 PMID: 21505438
  164. Characterization of extracellular circulating microRNA.
    Nucleic Acids Res. 2011 Sep 1;39(16):7223-33 PMID: 21609964
  165. Alzheimer's disease beta-amyloid peptides are released in association with exosomes.
    Proc Natl Acad Sci U S A. 2006 Jul 25;103(30):11172-7 PMID: 16837572
  166. Identification and proteomic profiling of exosomes in human urine.
    Proc Natl Acad Sci U S A. 2004 Sep 7;101(36):13368-73 PMID: 15326289
  167. Horizontal transfer of microRNAs: molecular mechanisms and clinical applications.
    Protein Cell. 2012 Jan;3(1):28-37 PMID: 22314808
Article Info
Journal
International journal of molecular sciences
Abbr.
Int J Mol Sci
ISSN
1422-0067
Published
2013-03-06
Epub
2013-00-06
Pages
5338-66
Language
English
Region
Switzerland
NLM ID
101092791
PMCID
PMC3634447
Analysis Services
Analysis Services

Contact

No. 2 Wenbo Road, Zhangqiu District, Jinan, Shandong

Qilu Normal University · Genelibs Bioinformatics Lab

750 Shunhua Rd, Jinan

2F, Bldg F, University Science Park

Tel: 0531-88819269

WeChat Official Account

Follow our WeChat subscription account for real-time updates and the latest in medical and biological research.


Business Email

E-mail: product@genelibs.com