Emerging roles of exosomes during epithelial-mesenchymal transition and cancer progression

Seminars in Cell and Developmental Biology

Volumn 40, Issue , 2015, Pages 60-71

  Greening, David W ^a   Gopal, Shashi K ^a   Mathias, Rommel A ^a   Liu, Lin ^b   Sheng, Jingyi ^b   Zhu, Hong Jian ^b   Simpson, Richard J ^a  

^a LA TROBE UNIVERSITY   (Australia)

^b UNIVERSITY OF MELBOURNE   (Australia)

Author keywords

Cancer progression; EMT; Epithelial mesenchymal transition; Exosomes; Extracellular vesicles; Microparticles

Indexed keywords

DNA; MESSENGER RNA; MICRORNA;

ANGIOGENESIS; CANCER GROWTH; CELL INVASION; CELL MIGRATION; CELL TRANSFORMATION; EPITHELIAL MESENCHYMAL TRANSITION; EXOSOME; GENETIC TRANSCRIPTION; HUMAN; MEMBRANE MICROPARTICLE; METASTASIS; NONHUMAN; REVIEW; SIGNAL TRANSDUCTION; TUMOR MICROENVIRONMENT; ANIMAL; METABOLISM; NEOPLASM; PATHOLOGY;

ANIMALS; CELL TRANSFORMATION, NEOPLASTIC; EPITHELIAL-MESENCHYMAL TRANSITION; EXOSOMES; HUMANS; NEOPLASMS;

EID: 84929294542     PISSN: 10849521     EISSN: 10963634     Source Type: Journal    
DOI: 10.1016/j.semcdb.2015.02.008     Document Type: Review

References (177)

1. Kalluri R., Neilson E.G. Epithelial-mesenchymal transition and its implications for fibrosis. J Clin Invest 2003, 112:1776-1784.
2. Berx G., Raspe E., Christofori G., Thiery J.P., Sleeman J.P. Pre-EMTing metastasis? Recapitulation of morphogenetic processes in cancer. Clin Exp Metastasis 2007, 24:587-597.
3. Lamouille S., Xu J., Derynck R. Molecular mechanisms of epithelial-mesenchymal transition. Nat Rev Mol Cell Biol 2014, 15:178-196.
4. Thompson E.W., Newgreen D.F., Tarin D. Carcinoma invasion and metastasis: a role for epithelial-mesenchymal transition?. Cancer Res 2005, 65:5991-5995. discussion 5995.
5. De Craene B., Berx G. Regulatory networks defining EMT during cancer initiation and progression. Nat Rev Cancer 2013, 13:97-110.
6. Scheel C., Weinberg R.A. Cancer stem cells and epithelial-mesenchymal transition: concepts and molecular links. Semin Cancer Biol 2012, 22:396-403.
7. Thiery J.P. Epithelial-mesenchymal transitions in tumour progression. Nat Rev Cancer 2002, 2:442-454.
8. Yang J., Weinberg R.A. Epithelial-mesenchymal transition: at the crossroads of development and tumor metastasis. Dev Cell 2008, 14:818-829.
9. Gao D., Vahdat L.T., Wong S., Chang J.C., Mittal V. Microenvironmental regulation of epithelial-mesenchymal transitions in cancer. Cancer Res 2012, 72:4883-4889.
10. Barcellos-Hoff M.H., Lyden D., Wang T.C. The evolution of the cancer niche during multistage carcinogenesis. Nat Rev Cancer 2013, 13:511-518.
11. Mathias R.A., Gopal S.K., Simpson R.J. Contribution of cells undergoing epithelial-mesenchymal transition to the tumour microenvironment. J Proteomics 2013, 545-557.
12. Talbot L.J., Bhattacharya S.D., Kuo P.C. Epithelial-mesenchymal transition, the tumor microenvironment, and metastatic behavior of epithelial malignancies. Int J Biochem Mol Biol 2012, 3:117-136.
13. Quail D.F., Joyce J.A. Microenvironmental regulation of tumor progression and metastasis. Nat Med 2013, 19:1423-1437.
14. Nguyen D.X., Bos P.D., Massague J. Metastasis: from dissemination to organ-specific colonization. Nat Rev Cancer 2009, 9:274-284.
15. Gao D., Joshi N., Choi H., Ryu S., Hahn M., Catena R., et al. Myeloid progenitor cells in the premetastatic lung promote metastases by inducing mesenchymal to epithelial transition. Cancer Res 2012, 72:1384-1394.
16. Chao Y., Wu Q., Acquafondata M., Dhir R., Wells A. Partial mesenchymal to epithelial reverting transition in breast and prostate cancer metastases. Cancer Microenviron 2012, 5:19-28.
17. Jordan N.V., Johnson G.L., Abell A.N. Tracking the intermediate stages of epithelial-mesenchymal transition in epithelial stem cells and cancer. Cell Cycle 2011, 10:2865-2873.
18. Savagner P. The epithelial-mesenchymal transition (EMT) phenomenon. Ann Oncol 2010, 21(Suppl. 7):vii89-vii92.
19. van Denderen B.J., Thompson E.W. Cancer: the to and fro of tumour spread. Nature 2013, 493:487-488.
20. Thiery J.P., Sleeman J.P. Complex networks orchestrate epithelial-mesenchymal transitions. Nat Rev Mol Cell Biol 2006, 7:131-142.
21. Martin F.T., Dwyer R.M., Kelly J., Khan S., Murphy J.M., Curran C., et al. Potential role of mesenchymal stem cells (MSCs) in the breast tumour microenvironment: stimulation of epithelial to mesenchymal transition (EMT). Breast Cancer Res Treat 2010, 124:317-326.
22. Zetter B.R. Migration of capillary endothelial cells is stimulated by tumour-derived factors. Nature 1980, 285:41-43.
23. Psaila B., Lyden D. The metastatic niche: adapting the foreign soil. Nat Rev Cancer 2009, 9:285-293.
24. Peinado H., Lavotshkin S., Lyden D. The secreted factors responsible for pre-metastatic niche formation: old sayings and new thoughts. Semin Cancer Biol 2011, 21:139-146.
25. Davis D.M., Sowinski S. Membrane nanotubes: dynamic long-distance connections between animal cells. Nat Rev Mol Cell Biol 2008, 9:431-436.
26. Yang J.D., Nakamura I., Roberts L.R. The tumor microenvironment in hepatocellular carcinoma: current status and therapeutic targets. Semin Cancer Biol 2011, 21:35-43.
27. Bissell M.J., Radisky D. Putting tumours in context. Nat Rev Cancer 2001, 1:46-54.
28. Kogure T., Yan I.K., Lin W.L., Patel T. Extracellular vesicle-mediated transfer of a novel long noncoding RNA TUC339: a mechanism of intercellular signaling in human hepatocellular cancer. Genes Cancer 2013, 4:261-272.
29. Hood J.L., Pan H., Lanza G.M., Wickline S.A. Paracrine induction of endothelium by tumor exosomes. Lab Invest 2009, 89:1317-1328.
30. Kucharzewska P., Christianson H.C., Welch J.E., Svensson K.J., Fredlund E., Ringner M., et al. Exosomes reflect the hypoxic status of glioma cells and mediate hypoxia-dependent activation of vascular cells during tumor development. Proc Natl Acad Sci U S A 2013, 110:7312-7317.
31. Ratajczak J., Wysoczynski M., Hayek F., Janowska-Wieczorek A., Ratajczak M.Z. Membrane-derived microvesicles: important and underappreciated mediators of cell-to-cell communication. Leukemia 2006, 20:1487-1495.
32. Peinado H., Aleckovic M., Lavotshkin S., Matei I., Costa-Silva B., Moreno-Bueno B., et al. Melanoma exosomes educate bone marrow progenitor cells toward a pro-metastatic phenotype through MET. Nat Med 2012, 18:883-891.
33. Luga V., Zhang L., Viloria-Petit A.M., Ogunjimi A.A., Inanlou M.R., Chiu E., et al. Exosomes mediate stromal mobilization of autocrine Wnt-PCP signaling in breast cancer cell migration. Cell 2012, 151:1542-1556.
34. Grange C., Tapparo M., Collino F., Vitillo L., Damasco C., Deregibus M.C., et al. Microvesicles released from human renal cancer stem cells stimulate angiogenesis and formation of lung premetastatic niche. Cancer Res 2011, 71:5346-5356.
35. Webber J., Steadman R., Mason M.D., Tabi Z., Clayton A. Cancer exosomes trigger fibroblast to myofibroblast differentiation. Cancer Res 2010, 70:9621-9630.
36. Hood J.L., San R.S., Wickline S.A. Exosomes released by melanoma cells prepare sentinel lymph nodes for tumor metastasis. Cancer Res 2011, 71:3792-3801.
37. Roberts C.T., Kurre P. Vesicle trafficking and RNA transfer add complexity and connectivity to cell-cell communication. Cancer Res 2013, 73:3200-3205.
38. Kahlert C., Kalluri R. Exosomes in tumor microenvironment influence cancer progression and metastasis. J Mol Med (Berl) 2013, 91:431-437.
39. Thakur B.K., Zhang H., Becker A., Matei I., Huang Y., Costa-Silva B., et al. Double-stranded DNA in exosomes: a novel biomarker in cancer detection. Cell Res 2014, 24:766-769.
40. Melo S., Sugimoto H., O'Connell J., Kato N., Villanueva A., Vidal A., et al. Cancer exosomes perform cell-independent microRNA biogenesis and promote tumorigenesis. Cancer Cell 2014, 26:707-721.
41. Mitchell J.P., Court J., Mason M.D., Tabi Z., Clayton A. Increased exosome production from tumour cell cultures using the Integra CELLine Culture System. J Immunol Methods 2008, 335:98-105.
42. Riches A., Campbell E., Borger E., Powis S. Regulation of exosome release from mammary epithelial and breast cancer cells - a new regulatory pathway. Eur J Cancer 2014, 50:1025-1034.
43. Lee Y., El Andaloussi S., Wood M.J. Exosomes and microvesicles: extracellular vesicles for genetic information transfer and gene therapy. Hum Mol Genet 2012, 21:R125-R134.
44. Ratajczak J., Miekus K., Kucia M., Zhang J., Reca R., Dvorak P., et al. Embryonic stem cell-derived microvesicles reprogram hematopoietic progenitors: evidence for horizontal transfer of mRNA and protein delivery. Leukemia 2006, 20:847-856.
45. Corrigan L., Redhai S., Leiblich A., Fan S.J., Perera S.M., Patel R., et al. BMP-regulated exosomes from Drosophila male reproductive glands reprogram female behavior. J Cell Biol 2014, 206:671-688.
46. Camussi G., Deregibus M.C., Bruno S., Grange C., Fonsato V., Tetta C. Exosome/microvesicle-mediated epigenetic reprogramming of cells. Am J Cancer Res 2011, 1:98-110.
47. Saleem S.N., Abdel-Mageed A.B. Tumor-derived exosomes in oncogenic reprogramming and cancer progression. Cell Mol Life Sci 2014, 72:1-10.
48. Ohno S., Takanashi M., Sudo K., Ueda S., Ishikawa A., Matsuyama N., et al. Systemically injected exosomes targeted to EGFR deliver antitumor microRNA to breast cancer cells. Mol Ther 2013, 21:185-191.
49. Breakefield X.O., Frederickson R.M., Simpson R.J. Gesicles: microvesicle "cookies" for transient information transfer between cells. Mol Ther 2011, 19:1574-1576.
50. Mathivanan S., Ji H., Simpson R.J. Exosomes: extracellular organelles important in intercellular communication. J Proteomics 2010, 73:1907-1920.
51. Villarroya-Beltri C., Baixauli F., Gutierrez-Vazquez C., Sanchez-Madrid F., Mittelbrunn M. Sorting it out: regulation of exosome loading. Semin Cancer Biol 2014, 28:3-13.
52. Cocucci E., Racchetti G., Meldolesi J. Shedding microvesicles: artefacts no more. Trends Cell Biol 2009, 19:43-51.
53. Piccin A., Murphy W.G., Smith O.P. Circulating microparticles: pathophysiology and clinical implications. Blood Rev 2007, 21:157-171.
54. Bianco F., Perrotta C., Novellino L., Francolini M., Riganti L., Menna E., et al. Acid sphingomyelinase activity triggers microparticle release from glial cells. EMBO J 2009, 28:1043-1054.
55. Di Vizio D., Kim J., Hager M.H., Morello M., Yang W., Lafargue C.J., et al. Oncosome formation in prostate cancer: association with a region of frequent chromosomal deletion in metastatic disease. Cancer Res 2009, 69:5601-5609.
56. Thery C., Ostrowski M., Segura E. Membrane vesicles as conveyors of immune responses. Nat Rev Immunol 2009, 9:581-593.
57. Ostrowski M., Carmo N.B., Krumeich S., Fanget I., Raposo G., Savina A., et al. Rab27a and Rab27b control different steps of the exosome secretion pathway. Nat Cell Biol 2010, 12(Suppl. 19-30):11-13.
58. Yu X., Harris S.L., Levine A.J. The regulation of exosome secretion: a novel function of the p53 protein. Cancer Res 2006, 66:4795-4801.
59. Trajkovic K., Hsu C., Chiantia S., Rajendran L., Wenzel D., Wieland F., et al. Ceramide triggers budding of exosome vesicles into multivesicular endosomes. Science 2008, 319:1244-1247.
60. Baietti M.F., Zhang Z., Mortier E., Melchior A., Degeest G., Geeraerts A., et al. Syndecan-syntenin-ALIX regulates the biogenesis of exosomes. Nat Cell Biol 2012, 14:677-685.
61. Lespagnol A., Duflaut D., Beekman C., Blanc L., Fiucci G., Marine J.C., et al. Exosome secretion, including the DNA damage-induced p53-dependent secretory pathway, is severely compromised in TSAP6/Steap3-null mice. Cell Death Differ 2008, 15:1723-1733.
62. Colombo M., Moita C., van Niel G., Kowal J., Vigneron J., Benaroch P., et al. Analysis of ESCRT functions in exosome biogenesis, composition and secretion highlights the heterogeneity of extracellular vesicles. J Cell Sci 2013, 126:5553-5565.
63. Buschow S.I., Nolte-'t Hoen E.N., van Niel G., Pols M.S., ten Broeke T., Lauwen M., et al. MHC II in dendritic cells is targeted to lysosomes or T cell-induced exosomes via distinct multivesicular body pathways. Traffic 2009, 10:1528-1542.
64. Tauro B.J., Greening D.W., Mathias R.A., Mathivanan S., Ji H., Simpson R.J. Two distinct populations of exosomes are released from LIM1863 colon carcinoma cell-derived organoids. Mol Cell Proteomics 2013, 12:587-598.
65. Morelli A.E., Larregina A.T., Shufesky W.J., Sullivan M.L., Stolz D.B., Papworth G.D., et al. Endocytosis, intracellular sorting, and processing of exosomes by dendritic cells. Blood 2004, 104:3257-3266.
66. Valadi H., Ekstrom K., Bossios A., Sjostrand M., Lee J.J., Lotvall J.O. Exosome-mediated transfer of mRNAs and microRNAs is a novel mechanism of genetic exchange between cells. Nat Cell Biol 2007, 9:654-659.
67. Feng D., Zhao W.L., Ye Y.Y., Bai X.C., Liu R.Q., Chang L.F., et al. Cellular internalization of exosomes occurs through phagocytosis. Traffic 2010, 11:675-687.
68. Tian T., Zhu Y.L., Zhou Y.Y., Liang G.F., Wang Y.Y., Hu F.H., et al. Exosome uptake through clathrin-mediated endocytosis and macropinocytosis and mediating miR-21 delivery. J Biol Chem 2014, 289:22258-22267.
69. Fitzner D., Schnaars M., van Rossum D., Krishnamoorthy G., Dibaj P., Bakhti M., et al. Selective transfer of exosomes from oligodendrocytes to microglia by macropinocytosis. J Cell Sci 2011, 124:447-458.
70. Christianson H.C., Svensson K.J., van Kuppevelt T.H., Li J.P., Belting M. Cancer cell exosomes depend on cell-surface heparan sulfate proteoglycans for their internalization and functional activity. Proc Natl Acad Sci U S A 2013, 110:17380-17385.
71. Parolini I., Federici C., Raggi C., Lugini L., Palleschi S., De Milito A., et al. Microenvironmental pH is a key factor for exosome traffic in tumor cells. J Biol Chem 2009, 284:34211-34222.
72. Hong B.S., Cho J.H., Kim H., Choi E.J., Rho S., Kim J., et al. Colorectal cancer cell-derived microvesicles are enriched in cell cycle-related mRNAs that promote proliferation of endothelial cells. BMC Genomics 2009, 10:556.
73. Sheldon H., Heikamp E., Turley H., Dragovic R., Thomas P., Oon C.E., et al. New mechanism for Notch signaling to endothelium at a distance by Delta-like 4 incorporation into exosomes. Blood 2010, 116:2385-2394.
74. Guescini M., Guidolin D., Vallorani L., Casadei L., Gioacchini A.M., Tibollo P., et al. C2C12 myoblasts release micro-vesicles containing mtDNA and proteins involved in signal transduction. Exp Cell Res 2010, 316:1977-1984.
75. Balaj L., Lessard R., Dai L., Cho Y.J., Pomeroy S.L., Breakefield X.O., et al. Tumour microvesicles contain retrotransposon elements and amplified oncogene sequences. Nat Commun 2011, 2:180.
76. Ekstrom K., Valadi H., Sjostrand M., Malmhall C., Bossios A., Eldh M., et al. Characterization of mRNA and microRNA in human mast cell-derived exosomes and their transfer to other mast cells and blood CD34 progenitor cells. J Extracell Vesicles 2012, 1.
77. Skog J., Wurdinger T., van Rijn S., Meijer D.H., Gainche L., Sena-Esteves M., et al. Glioblastoma microvesicles transport RNA and proteins that promote tumour growth and provide diagnostic biomarkers. Nat Cell Biol 2008, 10:1470-1476.
78. Valencia-Sanchez M.A., Liu J., Hannon G.J., Parker R. Control of translation and mRNA degradation by miRNAs and siRNAs. Genes Dev 2006, 20:515-524.
79. Martello G., Rosato A., Ferrari F., Manfrin A., Cordenonsi M., Dupont S., et al. A microRNA targeting dicer for metastasis control. Cell 2010, 141:1195-1207.
80. Inui M., Martello G., Piccolo S. MicroRNA control of signal transduction. Nat Rev Mol Cell Biol 2010, 11:252-263.
81. Cheng L., Sharples R.A., Scicluna B.J., Hill A.F. Exosomes provide a protective and enriched source of miRNA for biomarker profiling compared to intracellular and cell-free blood. J Extracell Vesicles 2014, 3.
82. Fabbri M., Paone A., Calore F., Galli R., Gaudio E., Santhanam R., et al. MicroRNAs bind to Toll-like receptors to induce prometastatic inflammatory response. Proc Natl Acad Sci U S A 2012, 109:E2110-E2116.
83. Ohshima K., Inoue K., Fujiwara A., Hatakeyama K., Kanto K., Watanabe Y., et al. Let-7 microRNA family is selectively secreted into the extracellular environment via exosomes in a metastatic gastric cancer cell line. PLoS ONE 2010, 5:e13247.
84. Yang M., Chen J., Su F., Yu B., Su F., Lin L., et al. Microvesicles secreted by macrophages shuttle invasion-potentiating microRNAs into breast cancer cells. Mol Cancer 2011, 10:117.
85. Bronisz A., Wang Y., Nowicki M.O., Peruzzi P., Ansari K.I., Ogawa D., et al. Extracellular vesicles modulate the glioblastoma microenvironment via a tumor suppression signaling network directed by miR-1. Cancer Res 2014, 74:738-750.
86. Thompson E.W., Williams E.D. EMT and MET in carcinoma - clinical observations, regulatory pathways and new models. Clin Exp Metastasis 2008, 25:591-592.
87. Thiery J.P., Chopin D. Epithelial cell plasticity in development and tumor progression. Cancer Metastasis Rev 1999, 18:31-42.
88. Tam W.L., Weinberg R.A. The epigenetics of epithelial-mesenchymal plasticity in cancer. Nat Med 2013, 19:1438-1449.
89. De Wever O., Pauwels P., De Craene B., Sabbah M., Emami S., Redeuilh G., et al. Molecular and pathological signatures of epithelial-mesenchymal transitions at the cancer invasion front. Histochem Cell Biol 2008, 130:481-494.
90. Hay E.D. An overview of epithelio-mesenchymal transformation. Acta Anat 1995, 154:8-20.
91. Hugo H., Ackland M.L., Blick T., Lawrence M.G., Clements J.A., Williams E.D., et al. Epithelial-mesenchymal and mesenchymal-epithelial transitions in carcinoma progression. J Cell Physiol 2007, 213:374-383.
92. Kalluri R., Weinberg R.A. The basics of epithelial-mesenchymal transition. J Clin Invest 2009, 119:1420-1428.
93. Nieto M.A. The ins and outs of the epithelial to mesenchymal transition in health and disease. Annu Rev Cell Dev Biol 2011, 27:347-376.
94. Radisky D.C. Epithelial-mesenchymal transition. J Cell Sci 2005, 118:4325-4326.
95. Guarino M. Epithelial-mesenchymal transition and tumour invasion. Int J Biochem Cell Biol 2007, 39:2153-2160.
96. Peinado H., Olmeda D., Cano A. Snail, Zeb and bHLH factors in tumour progression: an alliance against the epithelial phenotype?. Nat Rev Cancer 2007, 7:415-428.
97. Bresnick E.H., Lee H.Y., Fujiwara T., Johnson K.D., Keles S. GATA switches as developmental drivers. J Biol Chem 2010, 285:31087-31093.
98. Campbell K., Whissell G., Franch-Marro X., Batlle E., Casanova J. Specific GATA factors act as conserved inducers of an endodermal-EMT. Dev Cell 2011, 21:1051-1061.
99. Kondoh H., Kamachi Y. SOX-partner code for cell specification: regulatory target selection and underlying molecular mechanisms. Int J Biochem Cell Biol 2010, 42:391-399.
100. Sakai D., Suzuki T., Osumi N., Wakamatsu Y. Cooperative action of Sox9, Snail2 and PKA signaling in early neural crest development. Development 2006, 133:1323-1333.
101. Guo W., Keckesova Z., Donaher J.L., Shibue T., Tischler V., Reinhardt F., et al. Slug and Sox9 cooperatively determine the mammary stem cell state. Cell 2012, 148:1015-1028.
102. Moreno-Bueno G., Portillo F., Cano A. Transcriptional regulation of cell polarity in EMT and cancer. Oncogene 2008, 27:6958-6969.
103. Long J., Zuo D., Park M. Pc2-mediated sumoylation of Smad-interacting protein 1 attenuates transcriptional repression of E-cadherin. J Biol Chem 2005, 280:35477-35489.
104. Hu P., Yang J., Hou Y., Zhang H., Zeng Z., Zhao L., et al. LncRNA expression signatures of twist-induced epithelial-to-mesenchymal transition in MCF10A cells. Cell Signal 2014, 26:83-93.
105. Schliekelman M.J., Gibbons D.L., Faca V.M., Creighton C.J., Rizvi Z.H., Zhang Q., et al. Targets of the tumor suppressor miR-200 in regulation of the epithelial-mesenchymal transition in cancer. Cancer Res 2011, 71:7670-7682.
106. Yuan J.H., Yang F., Wang F., Ma J.Z., Guo Y.J., Tao Q.F., et al. A long noncoding RNA activated by TGF-beta promotes the invasion-metastasis cascade in hepatocellular carcinoma. Cancer Cell 2014, 25:666-681.
107. Mercer T.R., Dinger M.E., Mattick J.S. Long non-coding RNAs: insights into functions. Nat Rev Genet 2009, 10:155-159.
108. Park S.M., Gaur A.B., Lengyel E., Peter M.E. The miR-200 family determines the epithelial phenotype of cancer cells by targeting the E-cadherin repressors ZEB1 and ZEB2. Genes Dev 2008, 22:894-907.
109. Gregory P.A., Bracken C.P., Smith E., Bert A.G., Wright J.A., Roslan S., et al. An autocrine TGF-beta/ZEB/miR-200 signaling network regulates establishment and maintenance of epithelial-mesenchymal transition. Mol Biol Cell 2011, 22:1686-1698.
110. Beltran M., Puig I., Pena C., Garcia J.M., Alvarez A.B., Pena R., et al. A natural antisense transcript regulates Zeb2/Sip1 gene expression during snail1-induced epithelial-mesenchymal transition. Genes Dev 2008, 22:756-769.
111. van Zijl F., Krupitza G., Mikulits W. Initial steps of metastasis: cell invasion and endothelial transmigration. Mutat Res 2011, 728:23-34.
112. Yu Y., Xiao C.H., Tan L.D., Wang Q.S., Li X.Q., Feng Y.M. Cancer-associated fibroblasts induce epithelial-mesenchymal transition of breast cancer cells through paracrine TGF-beta signalling. Br J Cancer 2014, 110:724-732.
113. Dangi-Garimella S., Krantz S.B., Shields M.A., Grippo P.J., Munshi H.G. Epithelial-mesenchymal transition and pancreatic cancer progression. Pancreatic cancer and tumor microenvironment, Trivandrum, India 2012, G. PJ, M. HG (Eds.).
114. Tuxhorn J.A., Ayala G.E., Smith M.J., Smith V.C., Dang T.D., Rowley D.R. Reactive stroma in human prostate cancer: induction of myofibroblast phenotype and extracellular matrix remodeling. Clin Cancer Res 2002, 8:2912-2923.
115. Egeblad M., Werb Z. New functions for the matrix metalloproteinases in cancer progression. Nat Rev Cancer 2002, 2:161-174.
116. Zhou B.B., Fridman J.S., Liu X., Friedman S.M., Newton R.C., Scherle P.A. ADAM proteases, ErbB pathways and cancer. Expert Opin Investig Drugs 2005, 14:591-606.
117. Streuli C.H., Bailey N., Bissell M.J. Control of mammary epithelial differentiation: basement membrane induces tissue-specific gene expression in the absence of cell-cell interaction and morphological polarity. J Cell Biol 1991, 115:1383-1395.
118. Weaver V.M., Petersen O.W., Wang F., Larabell C.A., Briand P., Damsky C., et al. Reversion of the malignant phenotype of human breast cells in three-dimensional culture and in vivo by integrin blocking antibodies. J Cell Biol 1997, 137:231-245.
119. Muthuswamy S.K., Li D., Lelievre S., Bissell M.J., Brugge J.S. ErbB2, but not ErbB1, reinitiates proliferation and induces luminal repopulation in epithelial acini. Nat cell Biol 2001, 3:785-792.
120. Correia A.L., Mori H., Chen E.I., Schmitt F.C., Bissell M.J. The hemopexin domain of MMP3 is responsible for mammary epithelial invasion and morphogenesis through extracellular interaction with HSP90beta. Genes Dev 2013, 27:805-817.
121. Shintani Y., Wheelock M.J., Johnson K.R. Phosphoinositide-3 kinase-Rac1-c-Jun NH2-terminal kinase signaling mediates collagen I-induced cell scattering and up-regulation of N-cadherin expression in mouse mammary epithelial cells. Mol Biol Cell 2006, 17:2963-2975.
122. Sohara N., Znoyko I., Levy M.T., Trojanowska M., Reuben A. Reversal of activation of human myofibroblast-like cells by culture on a basement membrane-like substrate. J Hepatol 2002, 37:214-221.
123. Thannickal V.J., Lee D.Y., White E.S., Cui Z., Larios J.M., Chacon R., et al. Myofibroblast differentiation by transforming growth factor-beta1 is dependent on cell adhesion and integrin signaling via focal adhesion kinase. J Biol Chem 2003, 278:12384-12389.
124. Jo M., Lester R.D., Montel V., Eastman B., Takimoto S., Gonias S.L. Reversibility of epithelial-mesenchymal transition (EMT) induced in breast cancer cells by activation of urokinase receptor-dependent cell signaling. J Biol Chem 2009, 284:22825-22833.
125. Schedin P., Keely P.J. Mammary gland ECM remodeling, stiffness, and mechanosignaling in normal development and tumor progression. Cold Spring Harb Perspect Biol 2011, 3:a003228.
126. Lochter A., Galosy S., Muschler J., Freedman N., Werb Z., Bissell M.J. Matrix metalloproteinase stromelysin-1 triggers a cascade of molecular alterations that leads to stable epithelial-to-mesenchymal conversion and a premalignant phenotype in mammary epithelial cells. J Cell Biol 1997, 139:1861-1872.
127. Gibbons D.L., Lin W., Creighton C.J., Rizvi Z.H., Gregory P.A., Goodall G.J., et al. Contextual extracellular cues promote tumor cell EMT and metastasis by regulating miR-200 family expression. Genes Dev 2009, 23:2140-2151.
128. Mathias R.A., Chen Y.S., Wang B., Ji H., Kapp E.A., Moritz R.L., et al. Extracellular remodelling during oncogenic Ras-induced epithelial-mesenchymal transition facilitates MDCK cell migration. J Proteome Res 2010, 9:1007-1019.
129. Mathias R.A., Wang B., Ji H., Kapp E.A., Moritz R.L., Zhu H.J., et al. Secretome-based proteomic profiling of Ras-transformed MDCK cells reveals extracellular modulators of epithelial-mesenchymal transition. J Proteome Res 2009, 8:2827-2837.
130. Tauro B.J., Mathias R.A., Greening D.W., Gopal S.K., Ji H., Kapp E.A., et al. Oncogenic H-ras reprograms Madin-Darby canine kidney (MDCK) cell-derived exosomal proteins following epithelial-mesenchymal transition. Mol Cell Proteomics 2013, 12:2148-2159.
131. Garnier D., Magnus N., Meehan B., Kislinger T., Rak J. Qualitative changes in the proteome of extracellular vesicles accompanying cancer cell transition to mesenchymal state. Exp Cell Res 2013, 319:2747-2757.
132. Tickner J.A., Urquhart A.J., Stephenson S.A., Richard D.J., O'Byrne K.J. Functions and therapeutic roles of exosomes in cancer. Front Oncol 2014, 4:127.
133. Garnier D., Magnus N., Lee T.H., Bentley V., Meehan B., Milsom C., et al. Cancer cells induced to express mesenchymal phenotype release exosome-like extracellular vesicles carrying tissue factor. J Biol Chem 2012, 287:43565-43572.
134. Ji H., Greening D.W., Barnes T.W., Lim J.W., Tauro B.J., Rai A., et al. Proteome profiling of exosomes derived from human primary and metastatic colorectal cancer cells reveal differential expression of key metastatic factors and signal transduction components. Proteomics 2013, 13:1672-1686.
135. Jeppesen D.K., Nawrocki A., Jensen S.G., Thorsen K., Whitehead B., Howard K.A., et al. Quantitative proteomics of fractionated membrane and lumen exosome proteins from isogenic metastatic and nonmetastatic bladder cancer cells reveal differential expression of EMT factors. Proteomics 2014, 14:699-712.
136. Demory Beckler M., Higginbotham J.N., Franklin J.L., Ham A.J., Halvey P.J., Imasuen I.E., et al. Proteomic analysis of exosomes from mutant KRAS colon cancer cells identifies intercellular transfer of mutant KRAS. Mol Cell Proteomics 2013, 12:343-355.
137. Al-Nedawi K., Meehan B., Micallef J., Lhotak V., May L., Guha A., et al. Intercellular transfer of the oncogenic receptor EGFRvIII by microvesicles derived from tumour cells. Nat Cell Biol 2008, 10:619-624.
138. Hao S., Ye Z., Li F., Meng Q., Qureshi M., Yang J., et al. Epigenetic transfer of metastatic activity by uptake of highly metastatic B16 melanoma cell-released exosomes. Exp Oncol 2006, 28:126-131.
139. Antonyak M.A., Li B., Boroughs L.K., Johnson J.L., Druso J.E., Bryant K.L., et al. Cancer cell-derived microvesicles induce transformation by transferring tissue transglutaminase and fibronectin to recipient cells. Proc Natl Acad Sci U S A 2011, 108:4852-4857.
140. Zhu X., You Y., Li Q., Zeng C., Fu F., Guo A., et al. BCR-ABL1-positive microvesicles transform normal hematopoietic transplants through genomic instability: implications for donor cell leukemia. Leukemia 2014, 28:1666-1675.
141. Luga V., Wrana J.L. Tumor-stroma interaction: revealing fibroblast-secreted exosomes as potent regulators of Wnt-planar cell polarity signaling in cancer metastasis. Cancer Res 2013, 73:6843-6847.
142. Chairoungdua A., Smith D.L., Pochard P., Hull M., Caplan M.J. Exosome release of beta-catenin: a novel mechanism that antagonizes Wnt signaling. J Cell Biol 2010, 190:1079-1091.
143. Gross J.C., Chaudhary V., Bartscherer K., Boutros M. Active Wnt proteins are secreted on exosomes. Nat Cell Biol 2012, 14:1036-1045.
144. Zhai L., Chaturvedi D., Cumberledge S. Drosophila Wnt-1 undergoes a hydrophobic modification and is targeted to lipid rafts, a process that requires porcupine. J Biol Chem 2004, 279:33220-33227.
145. Borges F.T., Melo S.A., Ozdemir B.C., Kato N., Revuelta I., Miller C.A., et al. TGF-beta1-containing exosomes from injured epithelial cells activate fibroblasts to initiate tissue regenerative responses and fibrosis. J Am Soc Nephrol 2013, 24:385-392.
146. Webber J.P., Spary L.K., Sanders A.J., Chowdhury R., Jiang W.G., Steadman R., et al. Differentiation of tumour-promoting stromal myofibroblasts by cancer exosomes. Oncogene 2014.
147. Lehmann K., Janda E., Pierreux C.E., Rytomaa M., Schulze A., McMahon M., et al. Raf induces TGFbeta production while blocking its apoptotic but not invasive responses: a mechanism leading to increased malignancy in epithelial cells. Genes Dev 2000, 14:2610-2622.
148. Janda E., Lehmann K., Killisch I. Ras and TGF[beta] cooperatively regulate epithelial cell plasticity and metastasis: dissection of Ras signaling pathways. J Cell Biol 2002, 156:299-313.
149. Putz U., Howitt J., Doan A., Goh C.P., Low L.H., Silke J., et al. The tumor suppressor PTEN is exported in exosomes and has phosphatase activity in recipient cells. Sci Signal 2012, 5:ra70.
150. Hanahan D., Weinberg R.A. Hallmarks of cancer: the next generation. Cell 2011, 144:646-674.
151. Atay S., Banskota S., Crow J., Sethi G., Rink L., Godwin A.K. Oncogenic KIT-containing exosomes increase gastrointestinal stromal tumor cell invasion. Proc Natl Acad Sci U S A 2014, 111:711-716.
152. Hendrix A., Westbroek W., Bracke M., De Wever O. An ex(o)citing machinery for invasive tumor growth. Cancer Res 2010, 70:9533-9537.
153. Higginbotham J.N., Demory Beckler M., Gephart J.D., Franklin J.L., Bogatcheva G., Kremers G.J., et al. Amphiregulin exosomes increase cancer cell invasion. Curr Biol CB 2011, 21:779-786.
154. Muller M., Beck I.M., Gadesmann J., Karschuk N., Paschen A., Proksch E., et al. MMP19 is upregulated during melanoma progression and increases invasion of melanoma cells. Modern Pathol 2010, 23:511-521.
155. Rocks N., Paulissen G., El Hour M., Quesada F., Crahay C., Gueders M., et al. Emerging roles of ADAM and ADAMTS metalloproteinases in cancer. Biochimie 2008, 90:369-379.
156. Hakulinen J., Sankkila L., Sugiyama N., Lehti K., Keski-Oja J. Secretion of active membrane type 1 matrix metalloproteinase (MMP-14) into extracellular space in microvesicular exosomes. J Cell Biochem 2008, 105:1211-1218.
157. McCready J., Sims J.D., Chan D., Jay D.G. Secretion of extracellular hsp90alpha via exosomes increases cancer cell motility: a role for plasminogen activation. BMC Cancer 2010, 10:294.
158. Juhasz K., Lipp A.M., Nimmervoll B., Sonnleitner A., Hesse J., Haselgruebler T., et al. The complex function of hsp70 in metastatic cancer. Cancers 2013, 6:42-66.
159. Weis S.M., Cheresh D.A. Tumor angiogenesis: molecular pathways and therapeutic targets. Nat Med 2011, 17:1359-1370.
160. Ekstrom E.J., Bergenfelz C., von Bulow V., Serifler F., Carlemalm E., Jonsson G., et al. WNT5A induces release of exosomes containing pro-angiogenic and immunosuppressive factors from malignant melanoma cells. Mol Cancer 2014, 13:88.
161. Park J.E., Tan H.S., Datta A., Lai R.C., Zhang H., Meng W., et al. Hypoxic tumor cell modulates its microenvironment to enhance angiogenic and metastatic potential by secretion of proteins and exosomes. Mol Cell Proteomics 2010, 9:1085-1099.
162. Xiao H., Cheng S., Tong R., Lv Z., Ding C., Du C., et al. BAG3 regulates epithelial-mesenchymal transition and angiogenesis in human hepatocellular carcinoma. Lab Invest 2014, 94:252-261.
163. van Balkom B.W., de Jong O.G., Smits M., Brummelman J., den Ouden K., de Bree P.M., et al. Endothelial cells require miR-214 to secrete exosomes that suppress senescence and induce angiogenesis in human and mouse endothelial cells. Blood 2013, 121:3997-4006. S3991-S3915.
164. Mineo M., Garfield S.H., Taverna S., Flugy A., Da Leo G., Alessandro R., et al. Exosomes released by K562 chronic myeloid leukemia cells promote angiogenesis in a Src-dependent fashion. Angiogenesis 2012, 15:33-45.
165. Sharghi-Namini S., Tan E., Ong L.L., Ge R., Asada H.H. Dll4-containing exosomes induce capillary sprout retraction in a 3D microenvironment. Sci Rep 2014, 4:4031.
166. Lee H.D., Kim Y.H., Kim D.S. Exosomes derived from human macrophages suppress endothelial cell migration by controlling integrin trafficking. Eur J Immunol 2014, 44:1156-1169.
167. Wang T., Gilkes D.M., Takano N., Xiang L., Luo W., Bishop C.J., et al. Hypoxia-inducible factors and RAB22A mediate formation of microvesicles that stimulate breast cancer invasion and metastasis. Proc Natl Acad Sci U S A 2014.
168. Taraboletti G., D'Ascenzo S., Borsotti P., Giavazzi R., Pavan A., Dolo V. Shedding of the matrix metalloproteinases MMP-2, MMP-9, and MT1-MMP as membrane vesicle-associated components by endothelial cells. Am J Pathol 2002, 160:673-680.
169. Wang X., Huang W., Liu G., Cai W., Millard R.W., Wang Y., et al. Cardiomyocytes mediate anti-angiogenesis in type 2 diabetic rats through the exosomal transfer of miR-320 into endothelial cells. J Mol Cell Cardiol 2014, 74:139-150.
170. Bergers G., Benjamin L.E. Tumorigenesis and the angiogenic switch. Nat Rev Cancer 2003, 3:401-410.
171. Sceneay J., Smyth M.J., Moller A. The pre-metastatic niche: finding common ground. Cancer Metastasis Rev 2013, 32:449-464.
172. Zhou W., Fong M.Y., Min Y., Somlo G., Liu L., Palomares M.R., et al. Cancer-secreted miR-105 destroys vascular endothelial barriers to promote metastasis. Cancer Cell 2014, 25:501-515.
173. Rana S., Malinowska K., Zoller M. Exosomal tumor microRNA modulates premetastatic organ cells. Neoplasia 2013, 15:281-295.
174. Valencia K., Luis-Ravelo D., Bovy N., Anton I., Martinez-Canarias S., Zandueta C., et al. miRNA cargo within exosome-like vesicle transfer influences metastatic bone colonization. Mol Oncol 2014, 8:689-703.
175. Feng S., Cong S., Zhang X., Bao X., Wang W., Li H., et al. MicroRNA-192 targeting retinoblastoma 1 inhibits cell proliferation and induces cell apoptosis in lung cancer cells. Nucleic Acids Res 2011, 39:6669-6678.
176. Jung T., Castellana D., Klingbeil P., Cuesta Hernandez I., Vitacolonna M., Orlicky D.J., et al. CD44v6 dependence of premetastatic niche preparation by exosomes. Neoplasia 2009, 11:1093-1105.
177. Ono M., Kosaka N., Tominaga N., Yoshioka Y., Takeshita F., Takahashi R.U., et al. Exosomes from bone marrow mesenchymal stem cells contain a microRNA that promotes dormancy in metastatic breast cancer cells. Sci Signal 2014, 7:ra63.