The role of exosomes in cancer metastasis.

Exosomes are small membrane vesicles with a size ranging from 40 to 100nm. They can serve as functional mediators in cell interaction leading to cancer metastasis. Metastasis is a complex multistep process of cancer cell invasion, survival in blood vessels, attachment to and colonization of the host organ. Exosomes influence every step of this cascade and can be targeted by oncological treatment. This review highlights the role of exosomes in the various steps of the metastatic cascade and how exosome dependent pathways can be targeted as therapeutic approach or used for liquid biopsies.

[1]  Timothy D Cummins,et al.  Proteomic and functional characterisation of platelet microparticle size classes , 2009, Thrombosis and Haemostasis.

[2]  Jun Yang,et al.  A panel of five circulating microRNAs as potential biomarkers for prostate cancer , 2012, The Prostate.

[3]  S. Tsao,et al.  Proteomic analysis of exosomes from nasopharyngeal carcinoma cell identifies intercellular transfer of angiogenic proteins , 2015, International journal of cancer.

[4]  P. Shah,et al.  Modification of tumor cell exosome content by transfection with wt-p53 and microRNA-125b expressing plasmid DNA and its effect on macrophage polarization , 2016, Oncogenesis.

[5]  Laurence Zitvogel,et al.  Tumor-derived exosomes are a source of shared tumor rejection antigens for CTL cross-priming , 2001, Nature Medicine.

[6]  Olivier Lantz,et al.  Vaccination of metastatic melanoma patients with autologous dendritic cell (DC) derived-exosomes: results of thefirst phase I clinical trial , 2005, Journal of Translational Medicine.

[7]  G. Calin,et al.  Cell-to-cell miRNA transfer: from body homeostasis to therapy. , 2012, Pharmacology & therapeutics.

[8]  Clive Wilson,et al.  Exosomal miRNAs as cancer biomarkers and therapeutic targets , 2016, Journal of extracellular vesicles.

[9]  B. Chauffert,et al.  Membrane-associated Hsp72 from tumor-derived exosomes mediates STAT3-dependent immunosuppressive function of mouse and human myeloid-derived suppressor cells. , 2010, The Journal of clinical investigation.

[10]  J. Vandesompele,et al.  The impact of disparate isolation methods for extracellular vesicles on downstream RNA profiling , 2014, Journal of extracellular vesicles.

[11]  J. Cueva,et al.  M-Trap: Exosome-Based Capture of Tumor Cells as a New Technology in Peritoneal Metastasis. , 2015, Journal of the National Cancer Institute.

[12]  S. Karpatkin,et al.  Role of adhesive proteins in platelet tumor interaction in vitro and metastasis formation in vivo. , 1988, The Journal of clinical investigation.

[13]  G. Camussi,et al.  Cross Talk between Cancer and Mesenchymal Stem Cells through Extracellular Vesicles Carrying Nucleic Acids , 2016, Front. Oncol..

[14]  F. Lovat,et al.  Lung cancer exosomes as drivers of epithelial mesenchymal transition , 2016, Oncotarget.

[15]  Xin Lu,et al.  Organotropism of Breast Cancer Metastasis , 2007, Journal of Mammary Gland Biology and Neoplasia.

[16]  W. Jiang,et al.  Differentiation of tumour-promoting stromal myofibroblasts by cancer exosomes , 2014, Oncogene.

[17]  Sascha Keller,et al.  Exosomes: from biogenesis and secretion to biological function. , 2006, Immunology letters.

[18]  Jiang Li,et al.  Tumor-derived exosomes promote tumor progression and T-cell dysfunction through the regulation of enriched exosomal microRNAs in human nasopharyngeal carcinoma , 2014, Oncotarget.

[19]  D. Gabrilovich,et al.  Regulation of suppressive function of myeloid-derived suppressor cells by CD4+ T cells. , 2012, Seminars in cancer biology.

[20]  J. Chen,et al.  Matrix metalloproteinase 13‐containing exosomes promote nasopharyngeal carcinoma metastasis , 2015, Cancer science.

[21]  Jun Yao,et al.  Microenvironment-induced PTEN loss by exosomal microRNA primes brain metastasis outgrowth , 2015, Nature.

[22]  J. Le Pecq,et al.  A phase I study of dexosome immunotherapy in patients with advanced non-small cell lung cancer , 2005, Journal of Translational Medicine.

[23]  Raghu Kalluri,et al.  The biology and function of exosomes in cancer. , 2016, The Journal of clinical investigation.

[24]  A. Yoshimura,et al.  MiR-23a regulates TGF-β-induced epithelial-mesenchymal transition by targeting E-cadherin in lung cancer cells , 2012, International journal of oncology.

[25]  M. Adam,et al.  Electron microscopic evidence for externalization of the transferrin receptor in vesicular form in sheep reticulocytes , 1985, The Journal of cell biology.

[26]  S. Emr,et al.  Ubiquitin-Dependent Sorting into the Multivesicular Body Pathway Requires the Function of a Conserved Endosomal Protein Sorting Complex, ESCRT-I , 2001, Cell.

[27]  Joshua L Hood.  Melanoma exosome induction of endothelial cell GM-CSF in pre-metastatic lymph nodes may result in different M1 and M2 macrophage mediated angiogenic processes. , 2016, Medical hypotheses.

[28]  L. Presta,et al.  Inhibitory Fc receptors modulate in vivo cytoxicity against tumor targets , 2000, Nature Medicine.

[29]  T. Whiteside.  RE: Effect of Nasopharyngeal Carcinoma-Derived Exosomes on Human Regulatory T Cells. , 2015, Journal of the National Cancer Institute.

[30]  S. Iwakawa,et al.  Effects of Decitabine on Invasion and Exosomal Expression of miR-200c and miR-141 in Oxaliplatin-Resistant Colorectal Cancer Cells. , 2015, Biological & pharmaceutical bulletin.

[31]  Donghui Li,et al.  Biomarkers of TGF-β Signaling Pathway and Prognosis of Pancreatic Cancer , 2014, PloS one.

[32]  Chao Li,et al.  CD97 promotion of gastric carcinoma lymphatic metastasis is exosome dependent , 2015, Gastric Cancer.

[33]  David R. Nadeau,et al.  Heparin and cancer revisited: Mechanistic connections involving platelets, P-selectin, carcinoma mucins, and tumor metastasis , 2001, Proceedings of the National Academy of Sciences of the United States of America.

[34]  S. Wickline,et al.  Exosomes released by melanoma cells prepare sentinel lymph nodes for tumor metastasis. , 2011, Cancer research.

[35]  M. Srougi,et al.  Evaluation of the expression of integrins and cell adhesion molecules through tissue microarray in lymph node metastases of prostate cancer , 2009, Journal of carcinogenesis.

[36]  H. Bickeböller,et al.  The Heat Shock Protein HSP70 Promotes Mouse NK Cell Activity against Tumors That Express Inducible NKG2D Ligands1 , 2007, The Journal of Immunology.

[37]  J. Dudás.  Supportive and Rejective Functions of Tumor Stroma on Tumor Cell Growth, Survival, and Invasivity: The Cancer Evolution , 2015, Front. Oncol..

[38]  Daniel B. Martin,et al.  Circulating microRNAs as stable blood-based markers for cancer detection , 2008, Proceedings of the National Academy of Sciences.

[39]  Raghu Kalluri,et al.  Exosomes in tumor microenvironment influence cancer progression and metastasis , 2013, Journal of Molecular Medicine.

[40]  M. Schön,et al.  Deadly allies: the fatal interplay between platelets and metastasizing cancer cells. , 2010, Blood.

[41]  Johan Skog,et al.  Glioblastoma microvesicles transport RNA and protein that promote tumor growth and provide diagnostic biomarkers , 2008, Nature Cell Biology.

[42]  Roberta Galli,et al.  MicroRNAs bind to Toll-like receptors to induce prometastatic inflammatory response , 2012, Proceedings of the National Academy of Sciences.

[43]  Laurence Zitvogel,et al.  Eradication of established murine tumors using a novel cell-free vaccine: dendritic cell derived exosomes , 1998, Nature Medicine.

[44]  M. Zöller.  Tetraspanins: push and pull in suppressing and promoting metastasis , 2009, Nature Reviews Cancer.

[45]  Laurie J. Gay,et al.  Contribution of platelets to tumour metastasis , 2011, Nature Reviews Cancer.

[46]  Fulvio Reggiori,et al.  Sorting of proteins into multivesicular bodies: ubiquitin‐dependent and ‐independent targeting , 2001, The EMBO journal.

[47]  G. G. Stokes.  "J." , 1890, The New Yale Book of Quotations.

[48]  C. Ihm,et al.  Exosome cargo reflects TGF-β1-mediated epithelial-to-mesenchymal transition (EMT) status in A549 human lung adenocarcinoma cells. , 2016, Biochemical and biophysical research communications.

[49]  A. Molinari,et al.  Microenvironmental pH Is a Key Factor for Exosome Traffic in Tumor Cells* , 2009, The Journal of Biological Chemistry.

[50]  Weiying Zhou,et al.  Breast cancer-secreted miR-122 reprograms glucose metabolism in pre-metastatic niche to promote metastasis , 2015, Nature Cell Biology.

[51]  F. Hamdy,et al.  Changes in circulating microRNA levels associated with prostate cancer , 2012, British Journal of Cancer.

[52]  Paloma Martin,et al.  Exosomes enriched in stemness/metastatic-related mRNAS promote oncogenic potential in breast cancer , 2015, Oncotarget.

[53]  Sanchita Bhatnagar,et al.  Exosome Function: From Tumor Immunology to Pathogen Biology , 2008, Traffic.

[54]  R. Montironi,et al.  The origin of prostate metastases: emerging insights , 2015, Cancer and Metastasis Reviews.

[55]  H. Horvitz,et al.  MicroRNA expression profiles classify human cancers , 2005, Nature.

[56]  Dennis C. Sgroi,et al.  Stromal Fibroblasts Present in Invasive Human Breast Carcinomas Promote Tumor Growth and Angiogenesis through Elevated SDF-1/CXCL12 Secretion , 2005, Cell.

[57]  Katrin J. Svensson,et al.  Cancer cell exosomes depend on cell-surface heparan sulfate proteoglycans for their internalization and functional activity , 2013, Proceedings of the National Academy of Sciences.

[58]  R. Kalluri,et al.  The role of stromal myofibroblast and extracellular matrix in tumor angiogenesis. , 2011, Genes & cancer.

[59]  A. Bansal,et al.  Exosomes in carcinogenesis: molecular palkis carry signals for the regulation of cancer progression and metastasis , 2016, Journal of Cell Communication and Signaling.

[60]  Miss A.O. Penney.  (b) , 1974, The New Yale Book of Quotations.

[61]  D. Spector,et al.  Long noncoding RNAs: functional surprises from the RNA world. , 2009, Genes & development.

[62]  Xiao-Fang Yu,et al.  Highly Purified Human Immunodeficiency Virus Type 1 Reveals a Virtual Absence of Vif in Virions , 1999, Journal of Virology.

[63]  B. Chauffert,et al.  Membrane-associated Hsp 72 from tumor-derived exosomes mediates STAT 3-dependent immunosuppressive function of mouse and human myeloid-derived suppressor cells , 2010 .

[64]  T. Ichim,et al.  Tumor exosomes expressing fas ligand mediate CD8+ T cell apoptosis , 2004, Annals of Surgical Oncology.

[65]  C. Kim,et al.  MHC independent anti-tumor immune responses induced by Hsp70-enriched exosomes generate tumor regression in murine models. , 2009, Cancer letters.

[66]  M. Wojtukiewicz,et al.  Inhibition of platelet function: does it offer a chance of better cancer progression control? , 2007, Seminars in thrombosis and hemostasis.

[67]  Z. Gu,et al.  Mesenchymal stem cell-derived exosomes facilitate nasopharyngeal carcinoma progression. , 2016, American journal of cancer research.

[68]  Jung Ah Cho,et al.  Exosomes from breast cancer cells can convert adipose tissue-derived mesenchymal stem cells into myofibroblast-like cells. , 2011, International journal of oncology.

[69]  Richard O Hynes,et al.  Direct signaling between platelets and cancer cells induces an epithelial-mesenchymal-like transition and promotes metastasis. , 2011, Cancer cell.

[70]  L. Kopelovich,et al.  Detection of Exosomal miRNAs in the Plasma of Melanoma Patients , 2015, Journal of clinical medicine.

[71]  T. Whiteside.  Immune modulation of T-cell and NK (natural killer) cell activities by TEXs (tumour-derived exosomes). , 2013, Biochemical Society transactions.

[72]  Hakho Lee,et al.  Label-free detection and molecular profiling of exosomes with a nano-plasmonic sensor , 2014, Nature Biotechnology.

[73]  E. Trams,et al.  Exfoliation of membrane ecto-enzymes in the form of micro-vesicles. , 1981, Biochimica et biophysica acta.

[74]  R. Blackwell,et al.  Urothelial cells undergo epithelial-to-mesenchymal transition after exposure to muscle invasive bladder cancer exosomes , 2015, Oncogenesis.

[75]  W. Möbius,et al.  Regulation of exosome secretion by Rab35 and its GTPase-activating proteins TBC1D10A–C , 2010, The Journal of cell biology.

[76]  Emma J. Blott,et al.  Secretory lysosomes , 2002, Nature Reviews Molecular Cell Biology.

[77]  W. Stoorvogel,et al.  Prostasomes as a source of diagnostic biomarkers for prostate cancer. , 2016, The Journal of clinical investigation.

[78]  Alan Wells,et al.  Partial Mesenchymal to Epithelial Reverting Transition in Breast and Prostate Cancer Metastases , 2012, Cancer Microenvironment.

[79]  U. Welsch,et al.  Tumour exosomes inhibit binding of tumour-reactive antibodies to tumour cells and reduce ADCC , 2011, Cancer Immunology, Immunotherapy.

[80]  G. Jönsson,et al.  WNT5A induces release of exosomes containing pro-angiogenic and immunosuppressive factors from malignant melanoma cells , 2014, Molecular Cancer.

[81]  Aled Clayton,et al.  Cancer exosomes trigger fibroblast to myofibroblast differentiation. , 2010, Cancer research.

[82]  J. Li,et al.  Exosomal Transfer of Vasorin Expressed in Hepatocellular Carcinoma Cells Promotes Migration of Human Umbilical Vein Endothelial Cells , 2015, International journal of biological sciences.

[83]  Randy Schekman,et al.  Y-box protein 1 is required to sort microRNAs into exosomes in cells and in a cell-free reaction , 2016, bioRxiv.

[84]  S. Pfeffer.  Two Rabs for exosome release , 2010, Nature Cell Biology.

[85]  George A Calin,et al.  Cancer exosomes perform cell-independent microRNA biogenesis and promote tumorigenesis. , 2014, Cancer cell.

[86]  J. Slot,et al.  Proteomic and Biochemical Analyses of Human B Cell-derived Exosomes , 2003, The Journal of Biological Chemistry.

[87]  Ling Li,et al.  Exosomes Derived from Hypoxic Oral Squamous Cell Carcinoma Cells Deliver miR-21 to Normoxic Cells to Elicit a Prometastatic Phenotype. , 2016, Cancer research.

[88]  D. Steinhilber,et al.  Novel insights into the regulation of cyclooxygenase-2 expression by platelet-cancer cell cross-talk , 2015, Biochemical Society transactions.

[89]  S Paget,et al.  THE DISTRIBUTION OF SECONDARY GROWTHS IN CANCER OF THE BREAST. , 1889 .

[90]  Jeffrey W Pollard,et al.  Gene Expression Analysis of Macrophages That Facilitate Tumor Invasion Supports a Role for Wnt-Signaling in Mediating Their Activity in Primary Mammary Tumors , 2009, The Journal of Immunology.

[91]  Jung-Ah Cho,et al.  Exosomes: A new delivery system for tumor antigens in cancer immunotherapy , 2005, International journal of cancer.

[92]  Myung Soo Kim,et al.  Development of exosome-encapsulated paclitaxel to overcome MDR in cancer cells. , 2016, Nanomedicine : nanotechnology, biology, and medicine.

[93]  Aled Clayton,et al.  Isolation and Characterization of Exosomes from Cell Culture Supernatants and Biological Fluids , 2006, Current protocols in cell biology.

[94]  Graça Raposo,et al.  Exosomes--vesicular carriers for intercellular communication. , 2009, Current opinion in cell biology.

[95]  Lijun Wu,et al.  Exosomes in cancer: small particle, big player , 2015, Journal of Hematology & Oncology.

[96]  Gary K. Schwartz,et al.  Tumour exosome integrins determine organotropic metastasis , 2015, Nature.

[97]  J. Chin,et al.  Tumor exosomes expressing Fas ligand mediate CD8+ T-cell apoptosis , 2005 .

[98]  M. Zöller,et al.  The tetraspanins CD151 and Tspan8 are essential exosome components for the crosstalk between cancer initiating cells and their surrounding , 2014, Oncotarget.

[99]  Michael A. Hollingsworth,et al.  Pancreatic cancer exosomes initiate pre-metastatic niche formation in the liver , 2015, Nature Cell Biology.

[100]  G. Berchem,et al.  Hypoxic tumor-derived microvesicles negatively regulate NK cell function by a mechanism involving TGF-β and miR23a transfer , 2015, Oncoimmunology.

[101]  L. Vella.  The Emerging Role of Exosomes in Epithelial–Mesenchymal-Transition in Cancer , 2014, Front. Oncol..

[102]  T. Boulikas.  Clinical overview on Lipoplatin™: a successful liposomal formulation of cisplatin , 2009, Expert opinion on investigational drugs.

[103]  Gerhard Christofori,et al.  Epithelial-mesenchymal transition (EMT) and metastasis: yes, no, maybe? , 2016, Current opinion in cell biology.

[104]  S. Kondo,et al.  Exosomal HIF1α supports invasive potential of nasopharyngeal carcinoma-associated LMP1-positive exosomes , 2014, Oncogene.

[105]  A. Régnault,et al.  TCR Activation of Human T Cells Induces the Production of Exosomes Bearing the TCR/CD3/ζ Complex1 , 2002, The Journal of Immunology.

[106]  Hamid Cheshmi.  Glioblastoma microvesicles transport RNA and proteins that promote tumour growth and provide diagnostic biomarkers , 2011 .

[107]  J. Koenderink.  Q… , 2014, Les noms officiels des communes de Wallonie, de Bruxelles-Capitale et de la communaute germanophone.

[108]  Z. Duan,et al.  The roles and implications of exosomes in sarcoma , 2016, Cancer and Metastasis Reviews.

[109]  B. Echtenacher,et al.  Lysis of tumor cells by natural killer cells in mice is impeded by platelets. , 1999, Cancer research.

[110]  Carmen Visus,et al.  Tumor-Derived Microvesicles Promote Regulatory T Cell Expansion and Induce Apoptosis in Tumor-Reactive Activated CD8+ T Lymphocytes1 , 2009, The Journal of Immunology.

[111]  G. Hartmann,et al.  Therapeutic efficacy of bifunctional siRNA combining TGF-β1 silencing with RIG-I activation in pancreatic cancer. , 2013, Cancer research.

[112]  Tohru Mochizuki,et al.  Let-7 MicroRNA Family Is Selectively Secreted into the Extracellular Environment via Exosomes in a Metastatic Gastric Cancer Cell Line , 2010, PloS one.

[113]  Daehee Hwang,et al.  Colorectal cancer cell-derived microvesicles are enriched in cell cycle-related mRNAs that promote proliferation of endothelial cells , 2009, BMC Genomics.

[114]  L. Zitvogel,et al.  Malignant effusions and immunogenic tumour-derived exosomes , 2002, The Lancet.

[115]  Laurence Zitvogel,et al.  Exosomes: composition, biogenesis and function , 2002, Nature Reviews Immunology.

[116]  L. Yin,et al.  Exosome-shuttling microRNA-21 promotes cell migration and invasion-targeting PDCD4 in esophageal cancer. , 2016, International journal of oncology.

[117]  Robert M Hoffman,et al.  Imaging exosome transfer from breast cancer cells to stroma at metastatic sites in orthotopic nude-mouse models. , 2013, Advanced drug delivery reviews.

[118]  I. Fidler,et al.  Selection of successive tumour lines for metastasis. , 1973, Nature: New biology.

[119]  Johannes Schöneberg,et al.  Reverse-topology membrane scission by the ESCRT proteins , 2016, Nature Reviews Molecular Cell Biology.

[120]  R. Luo,et al.  Immunosuppression of breast cancer cells mediated by transforming growth factor-β in exosomes from cancer cells. , 2016, Oncology letters.

[121]  Weiying Zhou,et al.  Cancer-secreted miR-105 destroys vascular endothelial barriers to promote metastasis. , 2014, Cancer cell.

[122]  C. Croce,et al.  MicroRNA signatures in human cancers , 2006, Nature Reviews Cancer.

[123]  T. Whiteside,et al.  Tumor-Derived Microvesicles Induce, Expand and Up-Regulate Biological Activities of Human Regulatory T Cells (Treg) , 2010, PloS one.

[124]  S. Barni,et al.  Clinical activity and cardiac tolerability of non-pegylated liposomal doxorubicin in breast cancer: a synthetic review. , 2011, Tumori.

[125]  I. Macdonald,et al.  Metastasis: Dissemination and growth of cancer cells in metastatic sites , 2002, Nature Reviews Cancer.

[126]  M. Oppermann,et al.  Exosomal evasion of humoral immunotherapy in aggressive B-cell lymphoma modulated by ATP-binding cassette transporter A3 , 2011, Proceedings of the National Academy of Sciences.

[127]  Y. Matsuki,et al.  Secretory Mechanisms and Intercellular Transfer of MicroRNAs in Living Cells*♦ , 2010, The Journal of Biological Chemistry.

[128]  Bethan Psaila,et al.  The metastatic niche: adapting the foreign soil , 2009, Nature Reviews Cancer.

[129]  R. Schiffelers,et al.  Exosome mimetics: a novel class of drug delivery systems , 2012, International journal of nanomedicine.

[130]  C. Croce,et al.  MicroRNA gene expression deregulation in human breast cancer. , 2005, Cancer research.

[131]  J. Wrana,et al.  Exosomes Mediate Stromal Mobilization of Autocrine Wnt-PCP Signaling in Breast Cancer Cell Migration , 2012, Cell.

[132]  M. Bronner,et al.  Arousal of Cancer-Associated Stroma: Overexpression of Palladin Activates Fibroblasts to Promote Tumor Invasion , 2012, PloS one.

[133]  J. McKiernan,et al.  Dysregulation of circulating microRNAs and prediction of aggressive prostate cancer , 2012, The Prostate.

[134]  Jeffrey W. Pollard,et al.  Macrophage Diversity Enhances Tumor Progression and Metastasis , 2010, Cell.

[135]  J. Lötvall,et al.  Exosome-mediated transfer of mRNAs and microRNAs is a novel mechanism of genetic exchange between cells , 2007, Nature Cell Biology.

[136]  H. Riechelmann,et al.  Tumor-associated fibroblast-conditioned medium induces CDDP resistance in HNSCC cells , 2015, Oncotarget.

[137]  Gema Moreno-Bueno,et al.  Melanoma exosomes educate bone marrow progenitor cells toward a pro-metastatic phenotype through MET , 2012, Nature Medicine.

[138]  Wei Liu,et al.  High expression of small GTPase Rab3D promotes cancer progression and metastasis , 2015, Oncotarget.

[139]  M. Kortylewski,et al.  Macrophage immunomodulation by breast cancer-derived exosomes requires Toll-like receptor 2-mediated activation of NF-κB , 2014, Scientific Reports.

[140]  Jianqing Xu,et al.  Exosomes for Immunoregulation and Therapeutic Intervention in Cancer , 2016, Journal of Cancer.

[141]  Yunyan Shi,et al.  Gastric Cancer Exosomes Trigger Differentiation of Umbilical Cord Derived Mesenchymal Stem Cells to Carcinoma-Associated Fibroblasts through TGF-β/Smad Pathway , 2012, PloS one.

[142]  M. Zöller,et al.  CD44v6 dependence of premetastatic niche preparation by exosomes. , 2009, Neoplasia.

[143]  J. Wrana,et al.  Free somatostatin receptor fraction predicts the antiproliferative effect of octreotide in a neuroendocrine tumor model: implications for dose optimization. , 2013, Cancer research.

[144]  S. Lim,et al.  Hypoxic Tumor Cell Modulates Its Microenvironment to Enhance Angiogenic and Metastatic Potential by Secretion of Proteins and Exosomes* , 2010, Molecular & Cellular Proteomics.

[145]  Yibin Kang.  Dissecting Tumor-Stromal Interactions in Breast Cancer Bone Metastasis , 2016, Endocrinology and metabolism.

[146]  N. Kosaka.  Decoding the Secret of Cancer by Means of Extracellular Vesicles , 2016, Journal of clinical medicine.

[147]  C. Théry,et al.  Proteomic comparison defines novel markers to characterize heterogeneous populations of extracellular vesicle subtypes , 2016, Proceedings of the National Academy of Sciences.

[148]  P. Ricciardi-Castagnoli,et al.  Proteomic Analysis of Dendritic Cell-Derived Exosomes: A Secreted Subcellular Compartment Distinct from Apoptotic Vesicles1 , 2001, The Journal of Immunology.

[149]  A. Wells,et al.  E-cadherin as an indicator of mesenchymal to epithelial reverting transitions during the metastatic seeding of disseminated carcinomas , 2008, Clinical & Experimental Metastasis.

[150]  Christian Pilarsky,et al.  Glypican-1 identifies cancer exosomes and detects early pancreatic cancer , 2015, Nature.

[151]  Michael E. Egger,et al.  Melanoma cell-derived exosomes promote epithelial-mesenchymal transition in primary melanocytes through paracrine/autocrine signaling in the tumor microenvironment. , 2016, Cancer letters.

[152]  F. Aqil,et al.  Exosomal miRNAs as biomarkers of recurrent lung cancer , 2016, Tumor Biology.

[153]  M. Zöller,et al.  CD44v6-competent tumor exosomes promote motility, invasion and cancer-initiating cell marker expression in pancreatic and colorectal cancer cells , 2016, Oncotarget.