The role of EMT and MET in cancer dissemination

Connective Tissue Research

Volumn 56, Issue 5, 2015, Pages 403-413

  Banyard, Jacqueline ^a   Bielenberg, Diane R ^a  

^a BOSTON CHILDREN S HOSPITAL   (United States)

Author keywords

Epithelial mesenchymal transition; exosomes; hematogenous metastasis; lymphatics; lymphogenous metastasis; microRNA

Indexed keywords

MICRORNA;

CANCER STEM CELL; CARCINOMA CELL; CELL DIFFERENTIATION; CELL POLARITY; CIRCULATING TUMOR CELL; DESMOSOME; EMBRYO DEVELOPMENT; EPITHELIAL MESENCHYMAL TRANSITION; EXOSOME; GAP JUNCTION; HEMIDESMOSOME; HUMAN; LYMPH NODE METASTASIS; LYMPH VESSEL; METASTASIS; PHENOTYPE; PROMOTER REGION; REVIEW; TIGHT JUNCTION; TUMOR SUPPRESSOR GENE; TUMOR VOLUME; UPREGULATION; ANIMAL; CYTOLOGY; DISEASE COURSE; NEOPLASM; PATHOLOGY; PHYSIOLOGY;

ANIMALS; CELL DIFFERENTIATION; DISEASE PROGRESSION; EPITHELIAL-MESENCHYMAL TRANSITION; HUMANS; NEOPLASMS; NEOPLASTIC STEM CELLS; PHENOTYPE;

EID: 84943352184     PISSN: 03008207     EISSN: 16078438     Source Type: Journal    
DOI: 10.3109/03008207.2015.1060970     Document Type: Review

References (103)

1. Talmadge JE, Fidler IJ. AACR centennial series: the biology of cancer metastasis: historical perspective. Cancer Res 2010; 70 (14): 5649-69.
2. Hanahan D, Weinberg RA. Hallmarks of cancer: the next generation. Cell 2011; 144 (5): 646-74.
3. Migliozzi MT, Mucka P, Bielenberg DR. Lymphangiogenesis and metastasis-a closer look at the neuropilin/semaphorin3 axis. Microvasc Res 2014; 96C: 68-76.
4. Baluk P, Fuxe J, Hashizume H, Romano T, Lashnits E, Butz S, Vestweber D, Corada M, Molendini C, Dejana E, McDonald DM. Functionally specialized junctions between endothelial cells of lymphatic vessels. J Exp Med 2007; 204 (10): 2349-62.
5. Wong SY, Hynes RO. Lymphatic or hematogenous dissemination: how does a metastatic tumor cell decide? Cell Cycle 2006; 5 (8): 812-17.
6. Das S, Sarrou E, Podgrabinska S, Cassella M, Mungamuri SK, Feirt N, Gordon R, Nagi CS, Wang Y, Entenberg D, Condeelis J, Skobe M. Tumor cell entry into the lymph node is controlled by CCL1 chemokine expressed by lymph node lymphatic sinuses. J Exp Med 2013; 210 (8): 1509-28.
7. Nagy JA, Chang SH, Shih SC, Dvorak AM, Dvorak HF. Heterogeneity of the tumor vasculature. Semin Thromb Hemost 2010; 36 (3): 321-31.
8. Weidner N. Tumor angiogenesis: review of current applications in tumor prognostication. Semin Diagn Pathol 1993; 10 (4): 302-13.
9. Nico B, Benagiano V, Mangieri D, Maruotti N, Vacca A, Ribatti D. Evaluation of microvascular density in tumors: pro and contra. Histol Histopathol 2008; 23 (5): 601-7.
10. Zwaans BM, Bielenberg DR. Potential therapeutic strategies for lymphatic metastasis. Microvasc Res 2007; 74 (2-3): 145-58.
11. Dadras SS, Lange-Asschenfeldt B, Velasco P, Nguyen L, Vora A, Muzikansky A, Jahnke K, Hauschild A, Hirakawa S, Mihm MC, Detmar M. Tumor lymphangiogenesis predicts melanoma metastasis to sentinel lymph nodes. Mod Pathol 2005; 18 (9): 1232-42.
12. Lamouille S, Xu J, Derynck R. Molecular mechanisms of epithelial-mesenchymal transition. Nat Rev Mol Cell Biol 2014; 15 (3): 178-96.
13. Kalluri R, Weinberg RA. The basics of epithelial-mesenchymal transition. J Clin Invest 2009; 119 (6): 1420-8.
14. Zeisberg M, Duffield JS. Resolved: EMT produces fibroblasts in the kidney. J Am Soc Nephrol 2010; 21 (8): 1247-53.
15. De Craene B, Berx G. Regulatory networks defining EMT during cancer initiation and progression. Nat Rev Cancer 2013; 13 (2): 97-110.
16. Samatov TR, Tonevitsky AG, Schumacher U. Epithelial-mesenchymal transition: focus on metastatic cascade, alternative splicing, non-coding RNAs and modulating compounds. Mol Cancer 2013; 12 (1): 107.
17. Wu CY, Tsai YP, Wu MZ, Teng SC, Wu KJ. Epigenetic reprogramming and post-transcriptional regulation during the epithelial-mesenchymal transition. Trends Genet 2012; 28 (9): 454-63.
18. Warzecha CC, Carstens RP. Complex changes in alternative pre-mRNA splicing play a central role in the epithelial-to-mesenchymal transition (EMT). Semin Cancer Biol 2012; 22 (5-6): 417-27.
19. Zheng H, Kang Y. Multilayer control of the EMT master regulators. Oncogene 2014; 33 (14): 1755-63.
20. Tsai JH, Yang J. Epithelial-mesenchymal plasticity in carcinoma metastasis. Genes Dev 2013; 27 (20): 2192-206.
21. Papageorgis P. TGFbeta signaling in tumor initiation, epithelial-to-mesenchymal transition, and metastasis. J Oncol 2015; 2015: 587193.
22. Jiang J, Tang YL, Liang XH. EMT: a new vision of hypoxia promoting cancer progression. Cancer Biol Ther 2011; 11 (8): 714-23.
23. Lopez-Novoa JM, Nieto MA. Inflammation and EMT: an alliance towards organ fibrosis and cancer progression. EMBO Mol Med 2009; 1 (6-7): 303-14.
24. Khan MA, Chen HC, Zhang D, Fu J. Twist: a molecular target in cancer therapeutics. Tumour Biol 2013; 34 (5): 2497-506.
25. Philip B, Ito K, Moreno-Sanchez R, Ralph SJ. HIF expression and the role of hypoxic microenvironments within primary tumours as protective sites driving cancer stem cell renewal and metastatic progression. Carcinogenesis 2013; 34 (8): 1699-707.
26. Su J, Yin X, Zhou X, Wei W, Wang Z. The functions of F-box proteins in regulating the epithelial to mesenchymal transition. Curr Pharm Des 2015; 21 (10): 1311-17.
27. Greening DW, Gopal SK, Mathias RA, Liu L, Sheng J, Zhu HJ, Simpson RJ. Emerging roles of exosomes during epithelial-mesenchymal transition and cancer progression. Semin Cell Dev Biol 2015; 40: 60-71.
28. Lee JM, Dedhar S, Kalluri R, Thompson EW. The epithelial-mesenchymal transition: new insights in signaling, development, and disease. J Cell Biol 2006; 172 (7): 973-81.
29. Nistico P, Bissell MJ, Radisky DC. Epithelial-mesenchymal transition: general principles and pathological relevance with special emphasis on the role of matrix metalloproteinases. Cold Spring Harb Perspect Biol 2012; 4 (2): a011908.
30. Tiwari N, Gheldof A, Tatari M, Christofori G. EMT as the ultimate survival mechanism of cancer cells. Semin Cancer Biol 2012; 22 (3): 194-207.
31. Singh A, Settleman J. EMT, cancer stem cells and drug resistance: an emerging axis of evil in the war on cancer. Oncogene 2010; 29 (34): 4741-51.
32. Chouaib S, Janji B, Tittarelli A, Eggermont A, Thiery JP. Tumor plasticity interferes with anti-tumor immunity. Crit Rev Immunol 2014; 34 (2): 91-102.
33. Friedl P, Wolf K. Tumour-cell invasion and migration: diversity and escape mechanisms. Nat Rev Cancer 2003; 3 (5): 362-74.
34. Pankova K, Rosel D, Novotny M, Brabek J. The molecular mechanisms of transition between mesenchymal and amoeboid invasiveness in tumor cells. Cell Mol Life Sci 2010; 67 (1): 63-71.
35. Kim KJ, Hong SW, Lee YS, Kim BW, Lee SC, Chang HS, Park CS. Tumor margin histology predicts tumor aggressiveness in papillary thyroid carcinoma: a study of 514 consecutive patients. J Korean Med Sci 2011; 26 (3): 346-51.
36. Lee JA, Bae JW, Woo SU, Kim H, Kim CH. D2-40, Podoplanin, and CD31 as a prognostic predictor in invasive ductal carcinomas of the breast. J Breast Cancer 2011; 14 (2): 104-11.
37. Hasebe T, Tamura N, Iwasaki M, Okada N, Akashi-Tanaka S, Hojo T, Shimizu C, Adachi M, Fujiwara Y, Shibata T, Sasajima Y, Tsuda H, Kinoshita T. Grading system for lymph vessel tumor emboli: significant outcome predictor for patients with invasive ductal carcinoma of the breast who received neoadjuvant therapy. Modern Pathol 2010; 23 (4): 581-92.
38. Banyard J, Chung I, Migliozzi M, Phan DT, Wilson AM, Zetter BR, Bielenberg DR. Identification of genes regulating migration and invasion using a new model of metastatic prostate cancer. BMC Cancer 2014; 14: 387.
39. Giampieri S, Manning C, Hooper S, Jones L, Hill CS, Sahai E. Localized and reversible TGFbeta signalling switches breast cancer cells from cohesive to single cell motility. Nat Cell Biol 2009; 11 (11): 1287-96.
40. Yang J, Mani SA, Donaher JL, Ramaswamy S, Itzykson RA, Come C, Savagner P, Gitelman I, Richardson A, Weinberg RA. Twist, a master regulator of morphogenesis, plays an essential role in tumor metastasis. Cell 2004; 117 (7): 927-39.
41. Ansieau S, Bastid J, Doreau A, Morel AP, Bouchet BP, Thomas C, Fauvet F, Puisieux I, Doglioni C, Piccinin S, Maestro R, Voeltzel T, Selmi A, Valsesia-Wittmann S, Caron de Fromentel C, Puisieux A. Induction of EMT by twist proteins as a collateral effect of tumor-promoting inactivation of premature senescence. Cancer Cell 2008; 14 (1): 79-89.
42. Ozawa M, Kobayashi W. Reversibility of the Snail-induced epithelial-mesenchymal transition revealed by the Cre-loxP system. Biochem Biophys Res Commun 2015; 458 (3): 608-13.
43. Chui MH. Insights into cancer metastasis from a clinicopathologic perspective: epithelial-mesenchymal transition is not a necessary step. Int J Cancer 2013; 132 (7): 1487-95.
44. Thiery JP. Epithelial-mesenchymal transitions in tumour progression. Nat Rev Cancer 2002; 2 (6): 442-54.
45. Scheel C, Weinberg RA. Cancer stem cells and epithelial-mesenchymal transition: concepts and molecular links. Semin Cancer Biol 2012; 22 (5-6): 396-403.
46. Gorges TM, Tinhofer I, Drosch M, Rose L, Zollner TM, Krahn T, von Ahsen O. Circulating tumour cells escape from EpCAM-based detection due to epithelial-to-mesenchymal transition. BMC Cancer 2012; 12: 178.
47. Wu S, Liu S, Liu Z, Huang J, Pu X, Li J, Yang D, Deng H, Yang N, Xu J. Classification of circulating tumor cells by epithelial-mesenchymal transition markers. PLoS One 2015; 10 (4): e0123976.
48. Armstrong AJ, Marengo MS, Oltean S, Kemeny G, Bitting RL, Turnbull JD, Herold CI, Marcom PK, George DJ, Garcia-Blanco MA. Circulating tumor cells from patients with advanced prostate and breast cancer display both epithelial and mesenchymal markers. Mol Cancer Res 2011; 9 (8): 997-1007.
49. Chaffer CL, Brennan JP, Slavin JL, Blick T, Thompson EW, Williams ED. Mesenchymal-to-epithelial transition facilitates bladder cancer metastasis: role of fibroblast growth factor receptor-2. Cancer Res 2006; 66 (23): 11271-8.
50. Banyard J, Chung I, Wilson AM, Vetter G, Le Bechec A, Bielenberg DR, Zetter BR. Regulation of epithelial plasticity by miR-424 and miR-200 in a new prostate cancer metastasis model. Sci Rep 2013; 3: 3151.
51. Ocana OH, Corcoles R, Fabra A, Moreno-Bueno G, Acloque H, Vega S, Barrallo-Gimeno A, Cano A, Nieto MA. Metastatic colonization requires the repression of the epithelial-mesenchymal transition inducer Prrx1. Cancer Cell 2012; 22 (6): 709-24.
52. Korpal M, Ell BJ, Buffa FM, Ibrahim T, Blanco MA, Celia-Terrassa T, Mercatali L, Khan Z, Goodarzi H, Hua Y, Wei Y, Hu G, Garcia BA, Ragoussis J, Amadori D, Harris AL, Kang Y. Direct targeting of Sec23a by miR-200s influences cancer cell secretome and promotes metastatic colonization. Nature Med 2011; 17 (9): 1101-8.
53. Tsai JH, Donaher JL, Murphy DA, Chau S, Yang J. Spatiotemporal regulation of epithelial-mesenchymal transition is essential for squamous cell carcinoma metastasis. Cancer Cell 2012; 22 (6): 725-36.
54. Liu Q, Wang G, Chen Y, Li G, Yang D, Kang J. A miR-590/Acvr2a/Rad51b axis regulates DNA damage repair during mESC proliferation. Stem Cell Rep 2014; 3 (6): 1103-17.
55. Lecharpentier A, Vielh P, Perez-Moreno P, Planchard D, Soria JC, Farace F. Detection of circulating tumour cells with a hybrid (epithelial/mesenchymal) phenotype in patients with metastatic non-small cell lung cancer. Brit J Cancer 2011; 105 (9): 1338-41.
56. Xie G, Ji A, Yuan Q, Jin Z, Yuan Y, Ren C, Guo Z, Yao Q, Yang K, Lin X, Chen L. Tumour-initiating capacity is independent of epithelial-mesenchymal transition status in breast cancer cell lines. Brit J Cancer 2014; 110 (10): 2514-23.
57. Celia-Terrassa T, Meca-Cortes O, Mateo F, de Paz AM, Rubio N, Arnal-Estape A, Ell BJ, Bermudo R, Diaz A, Guerra-Rebollo M, Lozano JJ, Estaras C, Ulloa C, Alvarez-Simon D, Mila J, Vilella R, Paciucci R, Martinez-Balbas M, de Herreros AG, Gomis RR, Kang Y, Blanco J, Fernandez PL, Thomson TM. Epithelial-mesenchymal transition can suppress major attributes of human epithelial tumor-initiating cells. J Clin Invest 2012; 122 (5): 1849-68.
58. Barriere G, Fici P, Gallerani G, Fabbri F, Zoli W, Rigaud M. Circulating tumor cells and epithelial, mesenchymal and stemness markers: characterization of cell subpopulations. Ann Transl Med 2014; 2 (11): 109.
59. Ombrato L, Malanchi I. The EMT universe: space between cancer cell dissemination and metastasis initiation. Crit Rev Oncogenesis 2014; 19 (5): 349-61.
60. Mitra A, Mishra L, Li S. EMT, CTCs and CSCs in tumor relapse and drug-resistance. Oncotarget 2015; 6 (13): 10697-711.
61. Tsuji T, Ibaragi S, Shima K, Hu MG, Katsurano M, Sasaki A, Hu GF. Epithelial-mesenchymal transition induced by growth suppressor p12CDK2-AP1 promotes tumor cell local invasion but suppresses distant colony growth. Cancer Res 2008; 68 (24): 10377-86.
62. Hoshida T, Isaka N, Hagendoorn J, di Tomaso E, Chen YL, Pytowski B, Fukumura D, Padera TP, Jain RK. Imaging steps of lymphatic metastasis reveals that vascular endothelial growth factor-C increases metastasis by increasing delivery of cancer cells to lymph nodes: therapeutic implications. Cancer Res 2006; 66 (16): 8065-75.
63. Zhang J, Ma L. MicroRNA control of epithelial-mesenchymal transition and metastasis. Cancer Metastasis Rev 2012; 31 (3-4): 653-62.
64. Lamouille S, Subramanyam D, Blelloch R, Derynck R. Regulation of epithelial-mesenchymal and mesenchymal-epithelial transitions by microRNAs. Curr Opin Cell Biol 2013; 25 (2): 200-7.
65. Zaravinos A. The regulatory role of MicroRNAs in EMT and cancer. J Oncol 2015; 2015: 865816.
66. Gregory PA, Bert AG, Paterson EL, Barry SC, Tsykin A, Farshid G, Vadas MA, Khew-Goodall Y, Goodall GJ. The miR-200 family and miR-205 regulate epithelial to mesenchymal transition by targeting ZEB1 and SIP1. Nat Cell Biol 2008; 10 (5): 593-601.
67. Park SM, Gaur AB, Lengyel E, Peter ME. The miR-200 family determines the epithelial phenotype of cancer cells by targeting the E-cadherin repressors ZEB1 and ZEB2. Genes Develop 2008; 22 (7): 894-907.
68. Burk U, Schubert J, Wellner U, Schmalhofer O, Vincan E, Spaderna S, Brabletz T. A reciprocal repression between ZEB1 and members of the miR-200 family promotes EMT and invasion in cancer cells. EMBO Rep 2008; 9 (6): 582-9.
69. Bracken CP, Gregory PA, Kolesnikoff N, Bert AG, Wang J, Shannon MF, Goodall GJ. A double-negative feedback loop between ZEB1-SIP1 and the microRNA-200 family regulates epithelial-mesenchymal transition. Cancer Res 2008; 68 (19): 7846-54.
70. Gregory PA, Bracken CP, Smith E, Bert AG, Wright JA, Roslan S, Morris M, Wyatt L, Farshid G, Lim YY, Lindeman GJ, Shannon MF, Drew PA, Khew-Goodall Y, Goodall GJ. An autocrine TGF-beta/ZEB/miR-200 signaling network regulates establishment and maintenance of epithelial-mesenchymal transition. Mol Biol Cell 2011; 22 (10): 1686-98.
71. Kumarswamy R, Mudduluru G, Ceppi P, Muppala S, Kozlowski M, Niklinski J, Papotti M, Allgayer H. MicroRNA-30a inhibits epithelial-to-mesenchymal transition by targeting Snai1 and is downregulated in non-small cell lung cancer. Int J Cancer 2012; 130 (9): 2044-53.
72. Siemens H, Jackstadt R, Hunten S, Kaller M, Menssen A, Gotz U, Hermeking H. miR-34 and SNAIL form a double-negative feedback loop to regulate epithelial-mesenchymal transitions. Cell Cycle 2011; 10 (24): 4256-71.
73. Moes M, Le Bechec A, Crespo I, Laurini C, Halavatyi A, Vetter G, Del Sol A, Friederich E. A novel network integrating a miRNA-203/SNAI1 feedback loop which regulates epithelial to mesenchymal transition. PLoS One 2012; 7 (4): e35440.
74. Zhu X, Shen H, Yin X, Long L, Xie C, Liu Y, Hui L, Lin X, Fang Y, Cao Y, Xu Y, Li M, Xu W, Li Y. miR-186 regulation of Twist1 and ovarian cancer sensitivity to cisplatin. Oncogene 2015; in press.
75. Ma L, Young J, Prabhala H, Pan E, Mestdagh P, Muth D, Teruya-Feldstein J, Reinhardt F, Onder TT, Valastyan S, Westermann F, Speleman F, Vandesompele J, Weinberg RA. miR-9, a MYC/MYCN-activated microRNA, regulates E-cadherin and cancer metastasis. Nat Cell Biol 2010; 12 (3): 247-56.
76. Drasin DJ, Guarnieri AL, Neelakantan D, Kim J, Cabrera JH, Wang CA, Zaberezhnyy V, Gasparini P, Cascione L, Huebner K, Tan AC, Ford HL. TWIST1-induced miR-424 reversibly drives mesenchymal programming while inhibiting tumor initiation. Cancer Res 2015; 75 (9): 1908-21.
77. Yan Y, Wang Q, Yan XL, Zhang Y, Li W, Tang F, Li X, Yang P. miR-10a controls glioma migration and invasion through regulating epithelial-mesenchymal transition via EphA8. FEBS Lett 2015; 589 (6): 756-65.
78. Stinson S, Lackner MR, Adai AT, Yu N, Kim HJ, O'Brien C, Spoerke J, Jhunjhunwala S, Boyd Z, Januario T, Newman RJ, Yue P, Bourgon R, Modrusan Z, Stern HM, Warming S, de Sauvage FJ, Amler L, Yeh RF, Dornan D. TRPS1 targeting by miR-221/222 promotes the epithelial-to-mesenchymal transition in breast cancer. Sci Signal 2011; 4 (177): ra41.
79. Gebeshuber CA, Zatloukal K, Martinez J. miR-29a suppresses tristetraprolin, which is a regulator of epithelial polarity and metastasis. EMBO Rep 2009; 10 (4): 400-5.
80. Martello G, Rosato A, Ferrari F, Manfrin A, Cordenonsi M, Dupont S, Enzo E, Guzzardo V, Rondina M, Spruce T, Parenti AR, Daidone MG, Bicciato S, Piccolo S. A MicroRNA targeting dicer for metastasis control. Cell 2010; 141 (7): 1195-207.
81. Han M, Liu M, Wang Y, Chen X, Xu J, Sun Y, Zhao L, Qu H, Fan Y, Wu C. Antagonism of miR-21 reverses epithelial-mesenchymal transition and cancer stem cell phenotype through AKT/ERK1/2 inactivation by targeting PTEN. PLoS One 2012; 7 (6): e39520.
82. Ma L, Reinhardt F, Pan E, Soutschek J, Bhat B, Marcusson EG, Teruya-Feldstein J, Bell GW, Weinberg RA. Therapeutic silencing of miR-10b inhibits metastasis in a mouse mammary tumor model. Nature Biotechnol 2010; 28 (4): 341-7.
83. Ma L, Teruya-Feldstein J, Weinberg RA. Tumour invasion and metastasis initiated by microRNA-10b in breast cancer. Nature 2007; 449 (7163): 682-8.
84. Valastyan S, Benaich N, Chang A, Reinhardt F, Weinberg RA. Concomitant suppression of three target genes can explain the impact of a microRNA on metastasis. Genes Develop 2009; 23 (22): 2592-7.
85. Wang Y, Shang Y. Epigenetic control of epithelial-to-mesenchymal transition and cancer metastasis. Exp Cell Res 2013; 319 (2): 160-9.
86. Nickel A, Stadler SC. Role of epigenetic mechanisms in epithelial-to-mesenchymal transition of breast cancer cells. Transl Res 2015; 165 (1): 126-42.
87. Cocucci E, Meldolesi J. Ectosomes and exosomes: shedding the confusion between extracellular vesicles. Trends Cell Biol 2015; 25 (6): 364-72.
88. Le MT, Hamar P, Guo C, Basar E, Perdigao-Henriques R, Balaj L, Lieberman J. miR-200-containing extracellular vesicles promote breast cancer cell metastasis. J Clin Invest 2014; 124 (12): 5109-28.
89. Vella LJ. The emerging role of exosomes in epithelial-mesenchymal-transition in cancer. Front Oncol 2014; 4: 361.
90. Boukouris S, Mathivanan S. Exosomes in bodily fluids are a highly stable resource of disease biomarkers. Proteomics Clin Appl 2015; 9 (3-4): 358-67.
91. Paget S. The distribution of secondary growths in cancer of the breast. Lancet 1889; 133 (3421): 571-3.
92. Fidler IJ, Poste G. The "seed and soil" hypothesis revisited. Lancet Oncol 2008; 9 (8): 808.
93. Psaila B, Lyden D. The metastatic niche: adapting the foreign soil. Nat Rev Cancer 2009; 9 (4): 285-93.
94. Rinderknecht M, Detmar M. Tumor lymphangiogenesis and melanoma metastasis. J Cell Physiol 2008; 216 (2): 347-54.
95. Marimpietri D, Petretto A, Raffaghello L, Pezzolo A, Gagliani C, Tacchetti C, Mauri P, Melioli G, Pistoia V. Proteome profiling of neuroblastoma-derived exosomes reveal the expression of proteins potentially involved in tumor progression. PLoS One 2013; 8 (9): e75054.
96. Grange C, Tapparo M, Collino F, Vitillo L, Damasco C, Deregibus MC, Tetta C, Bussolati B, Camussi G. Microvesicles released from human renal cancer stem cells stimulate angiogenesis and formation of lung premetastatic niche. Cancer Res 2011; 71 (15): 5346-56.
97. Webber JP, Spary LK, Sanders AJ, Chowdhury R, Jiang WG, Steadman R, Wymant J, Jones AT, Kynaston H, Mason MD, Tabi Z, Clayton A. Differentiation of tumour-promoting stromal myofibroblasts by cancer exosomes. Oncogene 2015; 34 (3): 290-302.
98. Yoshizaki T, Kondo S, Wakisaka N, Murono S, Endo K, Sugimoto H, Nakanishi S, Tsuji A, Ito M. Pathogenic role of Epstein-Barr virus latent membrane protein-1 in the development of nasopharyngeal carcinoma. Cancer Lett 2013; 337 (1): 1-7.
99. Aga M, Bentz GL, Raffa S, Torrisi MR, Kondo S, Wakisaka N, Yoshizaki T, Pagano JS, Shackelford J. Exosomal HIF1alpha supports invasive potential of nasopharyngeal carcinoma-associated LMP1-positive exosomes. Oncogene 2014; 33 (37): 4613-22.
100. Ramteke A, Ting H, Agarwal C, Mateen S, Somasagara R, Hussain A, Graner M, Frederick B, Agarwal R, Deep G. Exosomes secreted under hypoxia enhance invasiveness and stemness of prostate cancer cells by targeting adherens junction molecules. Mol Carcinog 2015; 54 (7): 554 - 65.
101. Peinado H, Aleckovic M, Lavotshkin S, Matei I, Costa-Silva B, Moreno-Bueno G, Hergueta-Redondo M, Williams C, Garcia-Santos G, Ghajar C, Nitadori-Hoshino A, Hoffman C, Badal K, Garcia BA, Callahan MK, Yuan J, Martins VR, Skog J, Kaplan RN, Brady MS, Wolchok JD, Chapman PB, Kang Y, Bromberg J, Lyden D. Melanoma exosomes educate bone marrow progenitor cells toward a pro-metastatic phenotype through MET. Nature Med 2012; 18 (6): 883-91.
102. Zhou W, Fong MY, Min Y, Somlo G, Liu L, Palomares MR, Yu Y, Chow A, O'Connor ST, Chin AR, Yen Y, Wang Y, Marcusson EG, Chu P, Wu J, Wu X, Li AX, Li Z, Gao H, Ren X, Boldin MP, Lin PC, Wang SE. Cancer-secreted miR-105 destroys vascular endothelial barriers to promote metastasis. Cancer Cell 2014; 25 (4): 501-15.
103. Zeisberg M, Neilson EG. Biomarkers for epithelial-mesenchymal transitions. J Clin Invest 2009; 119 (6): 1429-37.