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PMID: 23508692 Published · epublish English Journal Article

Extracellular vesicles - biomarkers and effectors of the cellular interactome in cancer.

Frontiers in pharmacology ·Vol. 4 ·2013-00-00 ·Pages 21

Rak J

Abstract

In multicellular organisms both health and disease are defined by patterns of communication between the constituent cells. In addition to networks of soluble mediators, cells are also programed to exchange complex messages pre-assembled as multimolecular cargo of membraneous structures known extracellular vesicles (EV). Several biogenetic pathways produce EVs with different properties, and known as exosomes, ectosomes, and apoptotic bodies. In cancer, EVs carry molecular signatures and effectors of the disease, such as mutant oncoproteins, oncogenic transcripts, microRNA, and DNA sequences. Intercellular trafficking of such EVs (oncosomes) may contribute to horizontal cellular transformation, phenotypic reprograming, and functional re-education of recipient cells, both locally and systemically. The EV-mediated, reciprocal molecular exchange also includes tumor suppressors, phosphoproteins, proteases, growth factors, and bioactive lipids, all of which participate in the functional integration of multiple cells and their collective involvement in tumor angiogenesis, inflammation, immunity, coagulopathy, mobilization of bone marrow-derived effectors, metastasis, drug resistance, or cellular stemness. In cases where the EV role is rate limiting their production and uptake may represent and unexplored anticancer therapy target. Moreover, oncosomes circulating in biofluids of cancer patients offer an unprecedented, remote, and non-invasive access to crucial molecular information about cancer cells, including their driver mutations, classifiers, molecular subtypes, therapeutic targets, and biomarkers of drug resistance. New nanotechnologies are being developed to exploit this unique biomarker platform. Indeed, embracing the notion that human cancers are defined not only by processes occurring within cancer cells, but also between them, and amidst the altered tumor and systemic microenvironment may open new diagnostic and therapeutic opportunities.

Keywords
cancer cellular interactions exosomes extracellular vesicles oncogenes
Authors & Affiliations
1 authors, click to expand affiliations / ORCID
Rak Janusz
The Research Institute of the McGill University Health Centre, Montreal Children's Hospital, McGill University Montreal, QC, Canada.
References (135)
135 references, click to expand
  1. Coagulation activation and microparticle-associated coagulant activity in cancer patients. An exploratory prospective study.
    Thromb Haemost. 2012 Jul;108(1):160-5 PMID: 22535219
  2. Myeloid microvesicles are a marker and therapeutic target for neuroinflammation.
    Ann Neurol. 2012 Oct;72(4):610-24 PMID: 23109155
  3. Microparticle-associated tissue factor activity, venous thromboembolism and mortality in pancreatic, gastric, colorectal and brain cancer patients.
    J Thromb Haemost. 2012 Jul;10(7):1363-70 PMID: 22520016
  4. Prothrombotic state in glioblastoma multiforme: an evaluation of the procoagulant activity of circulating microparticles.
    J Neurooncol. 2011 Aug;104(1):225-31 PMID: 21104297
  5. Purification, characterization and biological significance of tumor-derived exosomes.
    Anticancer Res. 2005 Nov-Dec;25(6A):3703-7 PMID: 16302729
  6. Glioblastoma microvesicles transport RNA and proteins that promote tumour growth and provide diagnostic biomarkers.
    Nat Cell Biol. 2008 Dec;10(12):1470-6 PMID: 19011622
  7. Exosomes mediate stromal mobilization of autocrine Wnt-PCP signaling in breast cancer cell migration.
    Cell. 2012 Dec 21;151(7):1542-56 PMID: 23260141
  8. Circulating microRNAs: biomarkers or mediators of cardiovascular diseases?
    Arterioscler Thromb Vasc Biol. 2011 Nov;31(11):2383-90 PMID: 22011751
  9. Selective evolution of stromal mesenchyme with p53 loss in response to epithelial tumorigenesis.
    Cell. 2005 Dec 16;123(6):1001-11 PMID: 16360031
  10. Circulating microRNA in body fluid: a new potential biomarker for cancer diagnosis and prognosis.
    Cancer Sci. 2010 Oct;101(10):2087-92 PMID: 20624164
  11. Mosaic amplification of multiple receptor tyrosine kinase genes in glioblastoma.
    Cancer Cell. 2011 Dec 13;20(6):810-7 PMID: 22137795
  12. Intracellular signaling controlled by the endosomal-exosomal pathway.
    Commun Integr Biol. 2012 Jan 1;5(1):88-93 PMID: 22482020
  13. Rab27a supports exosome-dependent and -independent mechanisms that modify the tumor microenvironment and can promote tumor progression.
    Cancer Res. 2012 Oct 1;72(19):4920-30 PMID: 22865453
  14. MicroRNAs are exported from malignant cells in customized particles.
    Nucleic Acids Res. 2012 Oct;40(18):9125-38 PMID: 22772984
  15. Molecular basis of metastasis.
    N Engl J Med. 2008 Dec 25;359(26):2814-23 PMID: 19109576
  16. RNA expression patterns in serum microvesicles from patients with glioblastoma multiforme and controls.
    BMC Cancer. 2012 Jan 17;12:22 PMID: 22251860
  17. Rab27a and Rab27b control different steps of the exosome secretion pathway.
    Nat Cell Biol. 2010 Jan;12(1):19-30; sup pp 1-13 PMID: 19966785
  18. Systemic endocrine instigation of indolent tumor growth requires osteopontin.
    Cell. 2008 Jun 13;133(6):994-1005 PMID: 18555776
  19. Exosome removal as a therapeutic adjuvant in cancer.
    J Transl Med. 2012 Jun 27;10:134 PMID: 22738135
  20. Clonal selection drives genetic divergence of metastatic medulloblastoma.
    Nature. 2012 Feb 15;482(7386):529-33 PMID: 22343890
  21. Macrophage diversity enhances tumor progression and metastasis.
    Cell. 2010 Apr 2;141(1):39-51 PMID: 20371344
  22. Hallmarks of cancer: the next generation.
    Cell. 2011 Mar 4;144(5):646-74 PMID: 21376230
  23. Endothelial expression of autocrine VEGF upon the uptake of tumor-derived microvesicles containing oncogenic EGFR.
    Proc Natl Acad Sci U S A. 2009 Mar 10;106(10):3794-9 PMID: 19234131
  24. Tumor heterogeneity is an active process maintained by a mutant EGFR-induced cytokine circuit in glioblastoma.
    Genes Dev. 2010 Aug 15;24(16):1731-45 PMID: 20713517
  25. Tumor-associated endothelial cells with cytogenetic abnormalities.
    Cancer Res. 2004 Nov 15;64(22):8249-55 PMID: 15548691
  26. Tumor response to radiotherapy regulated by endothelial cell apoptosis.
    Science. 2003 May 16;300(5622):1155-9 PMID: 12750523
  27. Cell-free nucleic acids as biomarkers in cancer patients.
    Nat Rev Cancer. 2011 Jun;11(6):426-37 PMID: 21562580
  28. CD44v6 dependence of premetastatic niche preparation by exosomes.
    Neoplasia. 2009 Oct;11(10):1093-105 PMID: 19794968
  29. Biomarkers predicting clinical outcome of epidermal growth factor receptor-targeted therapy in metastatic colorectal cancer.
    J Natl Cancer Inst. 2009 Oct 7;101(19):1308-24 PMID: 19738166
  30. Will targeted therapy hold its promise? An evidence-based review.
    Curr Opin Oncol. 2008 Jan;20(1):104-11 PMID: 18043264
  31. The regulation of exosome secretion: a novel function of the p53 protein.
    Cancer Res. 2006 May 1;66(9):4795-801 PMID: 16651434
  32. Effect of tumour cells killed by x-rays upon the growth of admixed viable cells.
    Nature. 1956 Dec 22;178(4547):1391-2 PMID: 13387716
  33. The tumor suppressor PTEN is exported in exosomes and has phosphatase activity in recipient cells.
    Sci Signal. 2012 Sep 25;5(243):ra70 PMID: 23012657
  34. ARF6-regulated shedding of tumor cell-derived plasma membrane microvesicles.
    Curr Biol. 2009 Dec 1;19(22):1875-85 PMID: 19896381
  35. Ceramide triggers budding of exosome vesicles into multivesicular endosomes.
    Science. 2008 Feb 29;319(5867):1244-7 PMID: 18309083
  36. Protein typing of circulating microvesicles allows real-time monitoring of glioblastoma therapy.
    Nat Med. 2012 Dec;18(12):1835-40 PMID: 23142818
  37. Exosomes biological significance: A concise review.
    Blood Cells Mol Dis. 2006 Mar-Apr;36(2):315-21 PMID: 16487731
  38. Circulating microparticles: pathophysiology and clinical implications.
    Blood Rev. 2007 May;21(3):157-71 PMID: 17118501
  39. Intratumor heterogeneity and branched evolution revealed by multiregion sequencing.
    N Engl J Med. 2012 Mar 8;366(10):883-892 PMID: 22397650
  40. The pathogenesis of cancer metastasis: the 'seed and soil' hypothesis revisited.
    Nat Rev Cancer. 2003 Jun;3(6):453-8 PMID: 12778135
  41. Specificity of Drosophila cytonemes for distinct signaling pathways.
    Science. 2011 Apr 15;332(6027):354-8 PMID: 21493861
  42. Exosome release of β-catenin: a novel mechanism that antagonizes Wnt signaling.
    J Cell Biol. 2010 Sep 20;190(6):1079-91 PMID: 20837771
  43. Resistance to cytotoxic and anti-angiogenic anticancer agents: similarities and differences.
    Drug Resist Updat. 2003 Jun;6(3):111-27 PMID: 12860459
  44. Predominant expression of mutant EGFR (EGFRvIII) is rare in primary glioblastomas.
    Brain Pathol. 2004 Apr;14(2):131-6 PMID: 15193025
  45. Delivery of siRNA to the mouse brain by systemic injection of targeted exosomes.
    Nat Biotechnol. 2011 Apr;29(4):341-5 PMID: 21423189
  46. Stromal gene expression predicts clinical outcome in breast cancer.
    Nat Med. 2008 May;14(5):518-27 PMID: 18438415
  47. Cancer genes and the pathways they control.
    Nat Med. 2004 Aug;10(8):789-99 PMID: 15286780
  48. Human breast cancer cells selected for resistance to trastuzumab in vivo overexpress epidermal growth factor receptor and ErbB ligands and remain dependent on the ErbB receptor network.
    Clin Cancer Res. 2007 Aug 15;13(16):4909-19 PMID: 17699871
  49. Tissue factor-bearing microparticles and thrombus formation.
    Arterioscler Thromb Vasc Biol. 2011 Apr;31(4):728-33 PMID: 21252066
  50. Systemic induction of the angiogenesis switch by the tetraspanin D6.1A/CO-029.
    Cancer Res. 2006 Jul 15;66(14):7083-94 PMID: 16849554
  51. Tumor cell societies.
    J Natl Cancer Inst. 1989 May 3;81(9):648-9 PMID: 2709420
  52. Arrest and metastasis of blood-borne tumor cells are modified by fusion of plasma membrane vesicles from highly metastatic cells.
    Proc Natl Acad Sci U S A. 1980 Jan;77(1):399-403 PMID: 6928631
  53. Cancer cell-derived microvesicles induce transformation by transferring tissue transglutaminase and fibronectin to recipient cells.
    Proc Natl Acad Sci U S A. 2011 Mar 22;108(12):4852-7 PMID: 21368175
  54. Exosomes/microvesicles as a mechanism of cell-to-cell communication.
    Kidney Int. 2010 Nov;78(9):838-48 PMID: 20703216
  55. Microvesicles derived from activated platelets induce metastasis and angiogenesis in lung cancer.
    Int J Cancer. 2005 Feb 20;113(5):752-60 PMID: 15499615
  56. Vesiclepedia: a compendium for extracellular vesicles with continuous community annotation.
    PLoS Biol. 2012;10(12):e1001450 PMID: 23271954
  57. Inability of Rous sarcoma virus to cause sarcomas in the avian embryo.
    Nature. 1984 Jun 7-13;309(5968):552-6 PMID: 6203040
  58. Modes of resistance to anti-angiogenic therapy.
    Nat Rev Cancer. 2008 Aug;8(8):592-603 PMID: 18650835
  59. Horizontal transfer of oncogenes by uptake of apoptotic bodies.
    Proc Natl Acad Sci U S A. 2001 May 22;98(11):6407-11 PMID: 11353826
  60. The distribution of secondary growths in cancer of the breast. 1889.
    Cancer Metastasis Rev. 1989 Aug;8(2):98-101 PMID: 2673568
  61. Exosomes as intercellular signalosomes and pharmacological effectors.
    Biochem Pharmacol. 2011 May 15;81(10):1171-82 PMID: 21371441
  62. Stem cell concepts renew cancer research.
    Blood. 2008 Dec 15;112(13):4793-807 PMID: 19064739
  63. Microparticle-associated nucleic acids mediate trait dominance in cancer.
    FASEB J. 2012 Jan;26(1):420-9 PMID: 21965597
  64. Feedback regulation of EGFR signalling: decision making by early and delayed loops.
    Nat Rev Mol Cell Biol. 2011 Feb;12(2):104-17 PMID: 21252999
  65. Release of extracellular membrane particles carrying the stem cell marker prominin-1 (CD133) from neural progenitors and other epithelial cells.
    J Cell Sci. 2005 Jul 1;118(Pt 13):2849-58 PMID: 15976444
  66. Proteomic and immunologic analyses of brain tumor exosomes.
    FASEB J. 2009 May;23(5):1541-57 PMID: 19109410
  67. VEGFR1-positive haematopoietic bone marrow progenitors initiate the pre-metastatic niche.
    Nature. 2005 Dec 8;438(7069):820-7 PMID: 16341007
  68. Host genetics influence tumour metastasis.
    Nat Rev Cancer. 2006 Feb;6(2):141-6 PMID: 16491073
  69. Microvesicles/exosomes as potential novel biomarkers of metabolic diseases.
    Diabetes Metab Syndr Obes. 2012;5:247-82 PMID: 22924003
  70. Defining MAP3 kinases required for MDA-MB-231 cell tumor growth and metastasis.
    Oncogene. 2012 Aug 23;31(34):3889-900 PMID: 22139075
  71. LNA-mediated anti-miR-155 silencing in low-grade B-cell lymphomas.
    Blood. 2012 Aug 23;120(8):1678-86 PMID: 22797699
  72. 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
  73. Is cancer stem cell a cell, or a multicellular unit capable of inducing angiogenesis?
    Med Hypotheses. 2006;66(3):601-4 PMID: 16229960
  74. Differential gene expression analysis reveals generation of an autocrine loop by a mutant epidermal growth factor receptor in glioma cells.
    Cancer Res. 2006 Jan 15;66(2):867-74 PMID: 16424019
  75. Exosomes for cancer immunotherapy.
    Ann Oncol. 2004;15 Suppl 4:iv141-4 PMID: 15477298
  76. Oncogenic events regulate tissue factor expression in colorectal cancer cells: implications for tumor progression and angiogenesis.
    Blood. 2005 Feb 15;105(4):1734-41 PMID: 15494427
  77. Characterization of the epidermal growth factor receptor in human glioma cell lines and xenografts.
    Cancer Res. 1990 Dec 15;50(24):8017-22 PMID: 2253244
  78. Tumour-derived exosomes and their role in cancer-associated T-cell signalling defects.
    Br J Cancer. 2005 Jan 31;92(2):305-11 PMID: 15655551
  79. Epigenetic transfer of metastatic activity by uptake of highly metastatic B16 melanoma cell-released exosomes.
    Exp Oncol. 2006 Jun;28(2):126-31 PMID: 16837903
  80. MicroRNA signatures of tumor-derived exosomes as diagnostic biomarkers of ovarian cancer.
    Gynecol Oncol. 2008 Jul;110(1):13-21 PMID: 18589210
  81. 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
  82. Functional delivery of viral miRNAs via exosomes.
    Proc Natl Acad Sci U S A. 2010 Apr 6;107(14):6328-33 PMID: 20304794
  83. Extracellular vesicles--vehicles that spread cancer genes.
    Bioessays. 2012 Jun;34(6):489-97 PMID: 22442051
  84. Oncosome formation in prostate cancer: association with a region of frequent chromosomal deletion in metastatic disease.
    Cancer Res. 2009 Jul 1;69(13):5601-9 PMID: 19549916
  85. Genetic heterogeneity and cancer drug resistance.
    Lancet Oncol. 2012 Apr;13(4):e178-85 PMID: 22469128
  86. Treatment of brain inflammatory diseases by delivering exosome encapsulated anti-inflammatory drugs from the nasal region to the brain.
    Mol Ther. 2011 Oct;19(10):1769-79 PMID: 21915101
  87. Role of platelet P-selectin and microparticle PSGL-1 in thrombus formation.
    Trends Mol Med. 2004 Apr;10(4):171-8 PMID: 15059608
  88. New mechanism for Notch signaling to endothelium at a distance by Delta-like 4 incorporation into exosomes.
    Blood. 2010 Sep 30;116(13):2385-94 PMID: 20558614
  89. The clonal evolution of tumor cell populations.
    Science. 1976 Oct 1;194(4260):23-8 PMID: 959840
  90. Shedding of membrane vesicles by tumor and endothelial cells.
    Ital J Anat Embryol. 2005;110(2 Suppl 1):127-33 PMID: 16101030
  91. Exosome-mediated delivery of siRNA in vitro and in vivo.
    Nat Protoc. 2012 Dec;7(12):2112-26 PMID: 23154783
  92. Cellular microparticles: new players in the field of vascular disease?
    Eur J Clin Invest. 2004 Jun;34(6):392-401 PMID: 15200490
  93. Acid sphingomyelinase activity triggers microparticle release from glial cells.
    EMBO J. 2009 Apr 22;28(8):1043-54 PMID: 19300439
  94. Malignant gliomas in adults.
    N Engl J Med. 2008 Jul 31;359(5):492-507 PMID: 18669428
  95. Tumor-derived tissue factor activates coagulation and enhances thrombosis in a mouse xenograft model of human pancreatic cancer.
    Blood. 2012 Jun 7;119(23):5543-52 PMID: 22547577
  96. Tumour microvesicles contain retrotransposon elements and amplified oncogene sequences.
    Nat Commun. 2011 Feb 01;2:180 PMID: 21285958
  97. Effect of the secretory small GTPase Rab27B on breast cancer growth, invasion, and metastasis.
    J Natl Cancer Inst. 2010 Jun 16;102(12):866-80 PMID: 20484105
  98. Large-scale proteomics and phosphoproteomics of urinary exosomes.
    J Am Soc Nephrol. 2009 Feb;20(2):363-79 PMID: 19056867
  99. Membrane vesicles as conveyors of immune responses.
    Nat Rev Immunol. 2009 Aug;9(8):581-93 PMID: 19498381
  100. RhoA triggers a specific signaling pathway that generates transforming microvesicles in cancer cells.
    Oncogene. 2012 Nov 8;31(45):4740-9 PMID: 22266864
  101. Potential role of HER2-overexpressing exosomes in countering trastuzumab-based therapy.
    J Cell Physiol. 2012 Feb;227(2):658-67 PMID: 21465472
  102. Intercellular transfer of the oncogenic receptor EGFRvIII by microvesicles derived from tumour cells.
    Nat Cell Biol. 2008 May;10(5):619-24 PMID: 18425114
  103. From genes to drugs: targeted strategies for melanoma.
    Nat Rev Cancer. 2012 Apr 05;12(5):349-61 PMID: 22475929
  104. Rap2, but not Rap1 GTPase is expressed in human red blood cells and is involved in vesiculation.
    Biochim Biophys Acta. 2006 Mar;1763(3):330-5 PMID: 16540189
  105. Normal genetically mosaic mice produced from malignant teratocarcinoma cells.
    Proc Natl Acad Sci U S A. 1975 Sep;72(9):3585-9 PMID: 1059147
  106. Glioblastoma stem-like cell lines with either maintenance or loss of high-level EGFR amplification, generated via modulation of ligand concentration.
    Clin Cancer Res. 2012 Apr 1;18(7):1901-13 PMID: 22316604
  107. Inhibition of microparticle release triggers endothelial cell apoptosis and detachment.
    Thromb Haemost. 2007 Nov;98(5):1096-107 PMID: 18000616
  108. The roles of tumor-derived exosomes in cancer pathogenesis.
    Clin Dev Immunol. 2011;2011:842849 PMID: 22190973
  109. Melanoma exosomes educate bone marrow progenitor cells toward a pro-metastatic phenotype through MET.
    Nat Med. 2012 Jun;18(6):883-91 PMID: 22635005
  110. Imatinib as a paradigm of targeted therapies.
    Adv Cancer Res. 2004;91:1-30 PMID: 15327887
  111. Genetically engineered mouse models of brain cancer and the promise of preclinical testing.
    Brain Pathol. 2009 Jan;19(1):132-43 PMID: 19076778
  112. Cellular interactions in metastasis.
    Cancer Metastasis Rev. 1990 Jul;9(1):21-34 PMID: 2208566
  113. Molecular subclasses of high-grade glioma predict prognosis, delineate a pattern of disease progression, and resemble stages in neurogenesis.
    Cancer Cell. 2006 Mar;9(3):157-73 PMID: 16530701
  114. LMP1 association with CD63 in endosomes and secretion via exosomes limits constitutive NF-κB activation.
    EMBO J. 2011 Jun 1;30(11):2115-29 PMID: 21527913
  115. Exosomes released by melanoma cells prepare sentinel lymph nodes for tumor metastasis.
    Cancer Res. 2011 Jun 1;71(11):3792-801 PMID: 21478294
  116. New phosphatidylserine receptors: clearance of apoptotic cells and more.
    Dev Cell. 2007 Dec;13(6):759-60 PMID: 18061557
  117. Neural precursor cells induce cell death of high-grade astrocytomas through stimulation of TRPV1.
    Nat Med. 2012 Aug;18(8):1232-8 PMID: 22820645
  118. Interaction between Ras(V12) and scribbled clones induces tumour growth and invasion.
    Nature. 2010 Jan 28;463(7280):545-8 PMID: 20072127
  119. Human tumor virus utilizes exosomes for intercellular communication.
    Proc Natl Acad Sci U S A. 2010 Nov 23;107(47):20370-5 PMID: 21059916
  120. Horizontal gene transfer: you are what you eat.
    Biochem Biophys Res Commun. 2010 May 21;396(1):147-51 PMID: 20494129
  121. Somatic EGFR mutations and efficacy of tyrosine kinase inhibitors in NSCLC.
    Nat Rev Clin Oncol. 2009 Jun;6(6):352-66 PMID: 19483740
  122. Membrane microparticles mediate transfer of P-glycoprotein to drug sensitive cancer cells.
    Leukemia. 2009 Sep;23(9):1643-9 PMID: 19369960
  123. Molecular determinants of the response of glioblastomas to EGFR kinase inhibitors.
    N Engl J Med. 2005 Nov 10;353(19):2012-24 PMID: 16282176
  124. Endothelial progenitor cell derived microvesicles activate an angiogenic program in endothelial cells by a horizontal transfer of mRNA.
    Blood. 2007 Oct 1;110(7):2440-8 PMID: 17536014
  125. Exosome isolation for proteomic analyses and RNA profiling.
    Methods Mol Biol. 2011;728:235-46 PMID: 21468952
  126. Rab27b regulates number and secretion of platelet dense granules.
    Proc Natl Acad Sci U S A. 2007 Apr 3;104(14):5872-7 PMID: 17384153
  127. Active Wnt proteins are secreted on exosomes.
    Nat Cell Biol. 2012 Oct;14(10):1036-45 PMID: 22983114
  128. Cancer cells induced to express mesenchymal phenotype release exosome-like extracellular vesicles carrying tissue factor.
    J Biol Chem. 2012 Dec 21;287(52):43565-72 PMID: 23118232
  129. Circulating microvesicles in B-cell chronic lymphocytic leukemia can stimulate marrow stromal cells: implications for disease progression.
    Blood. 2010 Mar 4;115(9):1755-64 PMID: 20018914
  130. The genomic landscapes of human breast and colorectal cancers.
    Science. 2007 Nov 16;318(5853):1108-13 PMID: 17932254
  131. Membrane-derived microvesicles: important and underappreciated mediators of cell-to-cell communication.
    Leukemia. 2006 Sep;20(9):1487-95 PMID: 16791265
  132. Systemically injected exosomes targeted to EGFR deliver antitumor microRNA to breast cancer cells.
    Mol Ther. 2013 Jan;21(1):185-91 PMID: 23032975
  133. The genomic and transcriptomic architecture of 2,000 breast tumours reveals novel subgroups.
    Nature. 2012 Apr 18;486(7403):346-52 PMID: 22522925
  134. Clonal evolution in cancer.
    Nature. 2012 Jan 18;481(7381):306-13 PMID: 22258609
  135. Exosome secretion, including the DNA damage-induced p53-dependent secretory pathway, is severely compromised in TSAP6/Steap3-null mice.
    Cell Death Differ. 2008 Nov;15(11):1723-33 PMID: 18617898
Article Info
Journal
Frontiers in pharmacology
Abbr.
Front Pharmacol
ISSN
1663-9812
Published
2013-00-00
Epub
2013-00-06
Pages
21
Language
English
Region
Switzerland
NLM ID
101548923
PMCID
PMC3589665
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