Melanoma cell-derived exosomes promote epithelial-mesenchymal transition in primary melanocytes through paracrine/autocrine signaling in the tumor microenvironment

Cancer Letters

Volumn 376, Issue 2, 2016, Pages 318-327

  Xiao, Deyi ^a   Barry, Samantha ^a   Kmetz, Daniel ^a   Egger, Michael ^a   Pan, Jianmin ^a   Rai, Shesh N ^a   Qu, Jifu ^a   McMasters, Kelly M ^a   Hao, Hongying ^a  

^a University of Louisville School of Medicine   (United States)

Author keywords

Epithelial to mesenchymal transition; Exosomes; Melanoma; Microenvironment; Paracrine autocrine; Tumor progression

Indexed keywords

MICRORNA; MICRORNA 191; MICRORNA LET 7A; MICRORNA LET 7I; MITOGEN ACTIVATED PROTEIN KINASE; UNCLASSIFIED DRUG; MIRN191 MICRORNA, HUMAN; MIRNLET7 MICRORNA, HUMAN;

ADULT; AGED; ARTICLE; AUTOCRINE EFFECT; CANCER PATIENT; CANCER STAGING; CLINICAL ARTICLE; CONTROLLED STUDY; EPITHELIAL MESENCHYMAL TRANSITION; EXOSOME; FEMALE; HUMAN; HUMAN CELL; MALE; MELANOCYTE; MELANOMA; MELANOMA CELL; METASTASIS; PARACRINE SIGNALING; PRIORITY JOURNAL; SIGNAL TRANSDUCTION; TUMOR MICROENVIRONMENT; CASE CONTROL STUDY; GENETIC TRANSFECTION; GENETICS; METABOLISM; MIDDLE AGED; PATHOLOGY; SECONDARY; SKIN TUMOR; TUMOR CELL LINE;

ADULT; AGED; AUTOCRINE COMMUNICATION; CASE-CONTROL STUDIES; CELL LINE, TUMOR; EPITHELIAL-MESENCHYMAL TRANSITION; EXOSOMES; FEMALE; HUMANS; MALE; MELANOCYTES; MELANOMA; MICRORNAS; MIDDLE AGED; MITOGEN-ACTIVATED PROTEIN KINASES; PARACRINE COMMUNICATION; SIGNAL TRANSDUCTION; SKIN NEOPLASMS; TRANSFECTION; TUMOR MICROENVIRONMENT;

EID: 84964322229     PISSN: 03043835     EISSN: 18727980     Source Type: Journal    
DOI: 10.1016/j.canlet.2016.03.050     Document Type: Article

References (40)

1. Zhang H.G., Grizzle W.E. Exosomes: a novel pathway of local and distant intercellular communication that facilitates the growth and metastasis of neoplastic lesions. Am. J. Pathol 2014, 184:28-41. 10.1016/j.ajpath.2013.09.027.
2. Greening D.W., Gopal S.K., Mathias R.A., Liu L., Sheng J., Zhu H.J., et al. Emerging roles of exosomes during epithelial-mesenchymal transition and cancer progression. Semin. Cell Dev. Biol 2015, 40:60-71. 10.1016/j.semcdb.2015.02.008.
3. Hood J.L., Pan H., Lanza G.M., Wickline S.A. Paracrine induction of endothelium by tumor microvesicles. Consortium for Translational Research in Advanced Imaging and Nanomedicine (C-TRAIN). Lab. Invest 2009, 89:1317-1328. 10.1038/labinvest.2009.94.
4. Vella L.J. The emerging role of exosomes in epithelial-mesenchymal-transition in cancer. Front. Oncol 2014, 4:361. 10.3389/fonc.2014.0036.
5. Lee J.T., Herlyn M. Microenvironmental influences in melanoma progression. J. Cell. Biochem 2007, 101:862-872. pmid:17171636.
6. Caramel J., Papadogeorgakis E., Hill L., Browne G.J., Richard G., Wierinckx A., et al. A switch in the expression of embryonic EMT-inducers drives the development of malignant melanoma. Cancer Cell 2013, 24:466-480. 10.1016/j.ccr.2013.08.018.
7. 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. 10.1016/j.ccr.2013.08.018.
8. Raposo G., Nijman H.W., Stoorvogel W., Liejendekker R., Harding C.V., Melief C.J., et al. B lymphocytes secrete antigen-presenting vesicles. J. Exp. Med 1996, 183:1161-1172. pmid:8642258.
9. Xiao D., Ohlendorf J., Chen Y., Taylor D.D., Rai S.N., Waigel S., et al. Identifying mRNA, microRNA and protein profiles of melanoma exosomes. PLoS ONE 2012, 7:e46874. 10.1371/journal.pone.0046874.
10. Smith B.N., Bhowmick N.A. Role of EMT in metastasis and therapy resistance. J. Clin. Med 2016, 5:E17. 10.3390/jcm5020017.
11. Zeisberg M., Neilson E.G. Biomarkers for epithelial-mesenchymal transitions. J. Clin. Invest 2009, 119:1429-1437. 10.1172/JCI36183.
12. Ahmad A., Maitah M.Y., Ginnebaugh K.R., Li Y., Bao B., Gadgeel S.M., et al. Inhibition of Hedgehog signaling sensitizes NSCLC cells to standard therapies through modulation of EMT-regulating miRNAs. J. Hematol. Oncol 2013, 6:77. 10.1186/1756-8722-6-77.
13. Wu A., Wu K., Li J., Mo Y., Lin Y., Wang Y., et al. Let-7a inhibits migration, invasion and epithelial-mesenchymal transition by targeting HMGA2 in nasopharyngeal carcinoma. J. Transl. Med 2015, 13:105. 10.1186/s12967-015-0462-8.
14. Liu Y., Li H., Feng J., Cui X., Huang W., Li Y., et al. Lin28 induces epithelial-to-mesenchymal transition and stemness via downregulation of let-7a in breast cancer cells. PLoS ONE 2013, 8:e83083. 10.1371/journal.pone.0083083.
15. Neuzillet C., Tijeras-Raballand A., de Mestier L., Cros J., Faivre S., Raymond E. MEK in cancer and cancer therapy. Pharmacol. Ther 2014, 141:160-171. 10.1016/j.pharmthera.2013.10.001.
16. Zhao X.P., Wang M., Song Y., Song K., Yan T.L., Wang L., et al. Membrane microvesicles as mediators for melanoma-fibroblasts communication: roles of the VCAM-1/VLA-4 axis and the ERK1/2 signal pathway. Cancer Lett 2015, 360:125-133. 10.1016/j.canlet.2015.01.032.
17. Millimaggi D., Mari M., D'Ascenzo S., Carosa E., Jannini E.A., Zucker S., et al. Tumor vesicle-associated CD147 modulates the angiogenic capability of endothelial cells. Neoplasia 2007, 9:349-357. pmid:17460779.
18. 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. 10.1158/008-5472.CAN-11-0241.
19. Taverna S., Flugy A., Saieva L., Kohn E.C., Santoro A., Meraviglia S., et al. Role of exosomes released by chronic myelogenous leukemia cells in angiogenesis. Int. J. Cancer 2012, 130:2033-2043. 10.1002/ijc.26217.
20. Liu Y., Zhu X.J., Zeng C., Wu P.H., Wang H.X., Chen Z.C., et al. Microvesicles secreted from human multiple myeloma cells promote angiogenesis. Acta Pharmacol. Sin 2014, 35:230-238. 10.1038/aps.2013.141.
21. Keshamouni V.G., Michailidis G., Grasso C.S., Anthwal S., Strahler J.R., Walker A., et al. Differential protein expression profiling by iTRAQ-2DLC-MS/MS of lung cancer cells undergoing epithelial-mesenchymal transition reveals a migratory/invasive phenotype. J. Proteome Res 2006, 5:1143-1154. pmid:16674103.
22. Christiansen J.J., Rajasekaran A.K. Reassessing epithelial to mesenchymal transition as a prerequisite for carcinoma invasion and metastasis. Cancer Res 2006, 66:8319-8326. pmid:16951136.
23. Peinado H., Aleckovic M., Lavotshkin S., Matei I., Costa-Silva B., Moreno-Bueno G., et al. Melanoma exosomes educate bone marrow progenitor cells toward a pro-metastatic phenotype through MET. Nat. Med 2012, 18:883-891. 10.1038/nm.2753.
24. 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. 10.1073/pnas.1310501111.
25. Webber J., Steadman R., Mason M.D., Tabi Z., Clayton A. Cancer exosomes trigger fibroblast to myofibroblast differentiation. Cancer Res 2010, 70:9621-9630. 10.1158/0008-5472.CAN-10-1722.
26. Cho J.A., Park H., Lim E.H., Lee K.W. Exosomes from breast cancer cells can convert adipose tissue-derived mesenchymal stem cells into myofibroblast-like cells. Int. J. Oncol 2012, 40:130-138. 10.3892/ijo.2011.1193.
27. Abd Elmageed Z.Y., Yang Y., Thomas R., Ranjan M., Mondal D., Moroz K., et al. Neoplastic reprogramming of patient-derived adipose stem cells by prostate cancer cell-associated exosomes. Stem Cells 2014, 32:983-997. 10.1002/stem.1619.
28. Gregory P.A., Bert A.G., Paterson E.L., Barry S.C., Tsykin A., Farshid G., et al. The miR-200 family and miR-205 regulate epithelial to mesenchymal transition by targeting ZEB1 and SIP1. Nat. Cell Biol 2008, 10:593-601. 10.1038/ncb1722.
29. Koutsaki M., Spandidos D.A., Zaravinos A. Epithelial-mesenchymal transition-associated miRNAs in ovarian carcinoma, with highlight on the miR-200 family: prognostic value and prospective role in ovarian cancer therapeutics. Cancer Lett 2014, 351:173-181. 10.1016/j.canlet.2014.05.022.
30. Feng X., Wang Z., Fillmore R., Xi Y. MiR-200, a new star miRNA in human cancer. Cancer Lett 2014, 344:166-173. 10.1016/j.canlet.2013.11.004.
31. Peter M.E. Let-7 and miR-200 microRNAs: guardians against pluripotency and cancer progression. Cell Cycle 2009, 8:843-852. pmid:19221491.
32. Alam M., Ahmad R., Rajabi H., Kufe D. MUC1-C induces the LIN28B→LET-7→HMGA2 axis to regulate self-renewal in NSCLC. Mol. Cancer Res 2015, 13:449-460. 10.1158/1541-7786.MCR-14-0363.
33. Yang N., Kaur S., Volinia S., Greshock J., Lassus H., Hasegawa K., et al. MicroRNA microarray identifies let-7i as a novel biomarker and therapeutic target in human epithelial ovarian cancer. Cancer Res 2008, 68:10307-10314. 10.1158/0008-5472.CAN-08-1954.
34. Meier F., Schittek B., Busch S., Garbe C., Smalley K., Satyamoorthy K., et al. The RAS/RAF/MEK/ERK and PI3K/AKT signaling pathways present molecular targets for the effective treatment of advanced melanoma. Front. Biosci 2005, 10:2986-3001. pmid:15970553.
35. Weiss M.B., Abel E.V., Mayberry M.M., Basile K.J., Berger A.C., Aplin A.E. TWIST1 is an ERK1/2 effector that promotes invasion and regulates MMP-1 expression in human melanoma cells. Cancer Res 2012, 72:6382-6392. 10.1158/0008-5472.CAN-12-1033.
36. Roberts P.J., Der C.J. Targeting the Raf-MEK-ERK mitogen-activated protein kinase cascade for the treatment of cancer. Oncogene 2007, 26:3291-3310. pmid:17496923.
37. Lin K., Baritaki S., Militelo L., Malaponte G., Bevelacqua Y., Bonavida B. The Role of B-RAF mutations in melanoma and the induction of EMT via dysregulation of the NF-k B/snail/RKIP/PTEN circuit. Genes Cancer 2010, 1:409-420. pmid:20827424.
38. Xu W., Ji J., Xu Y., Liu Y., Shi L., Liu Y., et al. MicroRNA-191, by promoting the EMT and increasing CSC-like properties, is involved in neoplastic and metastatic properties of transformed human bronchial epithelial cells. Mol. Carcinog 2015, 54:E148-E161. 10.1002/mc.22221.
39. Zheng H., Li W., Wang Y., Xie T., Cai Y., Wang Z., et al. miR-23a inhibits E-cadherin expression and is regulated by AP-1 and NFAT4 complex during Fas-induced EMT in gastrointestinal cancer. Carcinogenesis 2014, 35:173-183. 10.1093/carcin/bgt274.
40. Cao M., Seike M., Soeno C., Mizutani H., Kitamura K., Minegishi Y., et al. MiR-23a regulates TGF-β-induced epithelial-mesenchymal transition by targeting E-cadherin in lung cancer cells. Int. J. Oncol 2012, 41:869-875. 10.3892/ijo.2012.1535.