Exosome-mediated transfer of miR-222 is sufficient to increase tumor malignancy in melanoma

Journal of Translational Medicine

Volumn 14, Issue 1, 2016, Pages

  Felicetti, Federica ^a   De Feo, Alessandra ^a   Coscia, Carolina ^a   Puglisi, Rossella ^a   Pedini, Francesca ^a   Pasquini, Luca ^a   Bellenghi, Maria ^a   Errico, Maria Cristina ^a   Pagani, Elena ^b   Carè, Alessandra ^a  

^a ISTITUTO SUPERIORE DI SANITÀ   (Italy)

^b LABORATORIO DI PATOLOGIA VASCOLARE   (Italy)

Author keywords

(da 3 a 10): Melanoma; Exosomes; MicroRNA; MiR 222; PI3K AKT

Indexed keywords

ANTAGOMIR; BUPARLISIB; CYCLIN DEPENDENT KINASE INHIBITOR 1B; MICRORNA 221; MICRORNA 222; PHOSPHATIDYLINOSITOL 3 KINASE; PROTEIN KINASE B; MICRORNA; MIRN222 MICRORNA, HUMAN; OLIGONUCLEOTIDE;

ARTICLE; CANCER CELL CULTURE; CARCINOGENESIS; CELL CYCLE; CELL INVASION; CELL VACUOLE; CHEMOTAXIS; CONFOCAL MICROSCOPY; CONTROLLED STUDY; EXOSOME; GENE OVEREXPRESSION; GENE REPRESSION; GENE SILENCING; HUMAN; HUMAN CELL; IN VITRO STUDY; INTERNALIZATION; MELANOMA; MELANOMA CELL LINE; MOUSE; NONHUMAN; REAL TIME POLYMERASE CHAIN REACTION; RNA TRANSPORT; ULTRACENTRIFUGATION; WESTERN BLOTTING; DRUG EFFECTS; GENE EXPRESSION REGULATION; GENETICS; METABOLISM; PATHOLOGY; SIGNAL TRANSDUCTION; TUMOR CELL LINE;

BLOTTING, WESTERN; CARCINOGENESIS; CELL LINE, TUMOR; EXOSOMES; GENE EXPRESSION REGULATION, NEOPLASTIC; HUMANS; MELANOMA; MICRORNAS; OLIGONUCLEOTIDES; PHOSPHATIDYLINOSITOL 3-KINASES; PROTO-ONCOGENE PROTEINS C-AKT; SIGNAL TRANSDUCTION;

EID: 84977567322     PISSN: None     EISSN: 14795876     Source Type: Journal    
DOI: 10.1186/s12967-016-0811-2     Document Type: Article

References (52)

1. Jemal A, Siegel R, Ward E, Hao Y, Xu J, Thun MJ. Cancer statistics, 2009. CA Cancer J Clin. 2009;59(4):225-49.
2. Tsao H, Chin L, Garraway LA, Fisher DE. Melanoma: from mutations to medicine. Genes Dev. 2012;26(11):1131-55. doi: 10.1101/gad.191999.112.
3. Lujambio A, Lowe SW. The microcosmos of cancer. Nature. 2012;482(7385):347-55.
4. Bartels CL, Tsongalis GJ. MicroRNAs: novel biomarkers for human cancer. Clin Chem. 2009;55(4):623-31. doi: 10.1373/clinchem.2008.
5. Cortez MA, Bueso-Ramos C, Ferdin J, Lopez-Berestein G, Sood AK, Calin GA. MicroRNAs in body fluids-the mix of hormones and biomarkers. Nat Rev Clin Oncol. 2011;8:467-77.
6. Felicetti F, Errico MC, Bottero L, Segnalini P, Stoppacciaro A, Biffoni M, et al. The promyelocytic leukemia zinc finger-microRNA-221/-222 pathway controls melanoma progression through multiple oncogenic mechanisms. Cancer Res. 2008;68(8):2745-54.
7. Errico MC, Felicetti F, Bottero L, Mattia G, Boe A, Felli N, et al. The abrogation of the HOXB7/PBX2 complex induces apoptosis in melanoma through the miR-221&222-c-FOS pathway. Int J Cancer. 2013;133(4):879-92.
8. Zhao L, Liu W, Xiao J, Cao B. The role of exosomes and "exosomal shuttle microRNA" in tumorigenesis and drug resistance. Cancer Lett. 2015;356(2 Pt B):339-46.
9. Melo SA, Sugimoto H, O'Connell JT, Kato N, Villanueva A, Vidal A, et al. Cancer exosomes perform cell-independent microRNA biogenesis and promote tumorigenesis. Cancer Cell. 2014;26(5):707-21.
10. Saleem SN, Abdel-Mageed AB. Tumor-derived exosomes in oncogenic reprogramming and cancer progression. Cell Mol Life Sci. 2015;72(1):1-10.
11. Squadrito ML, Baer C, Burdet F, Maderna C, Gilfillan GD, Lyle R, et al. Endogenous RNAs modulate microRNA sorting to exosomes and transfer to acceptor cells. Cell Rep. 2014;8(5):1432-46.
12. Felli N, Fontana L, Pelosi E, Botta R, Bonci D, Facchiano F, et al. MicroRNAs 221 and 222 inhibit normal erythropoiesis and erythroleukemic cell growth via kit receptor down-modulation. Proc Natl Acad Sci USA. 2005;102(50):18081-6.
13. Yazawa EM, Geddes-Sweeney JE, Cedeno-Laurent F, Walley KC, Barthel SR, Opperman MJ, et al. Melanoma Cell Galectin-1 Ligands Functionally Correlate with Malignant Potential. J Invest Dermatol. 2015;135(7):1849-62. doi: 10.1038/jid.2015.95.
14. Garofalo M, Quintavalle C, Romano G, Croce CM, Condorelli G. miR221/222 in cancer: their role in tumor progression and response to therapy. Curr Mol Med. 2012;12(1):27-33.
15. Zhang C, Zhang J, Zhang A, Wang Y, Han L, You Y, et al. PUMA is a novel target of miR-221/222 in human epithelial cancers. Int J Oncol. 2010;37(6):1621-6.
16. Fu Z, Qian F, Yang X, Jiang H, Chen Y, Liu S. Circulating miR-222 in plasma and its potential diagnostic and prognostic value in gastric cancer. Med Oncol. 2014;31(9):164. doi: 10.1007/s12032-014-0164-8.
17. Felicetti F, Parolini I, Bottero L, Fecchi K, Errico MC, Raggi C, et al. Caveolin-1 tumor promoting role in human melanoma. Int J Cancer. 2009;125(7):1514-22.
18. Logozzi M, De Milito A, Lugini L, Borghi M, Calabro L, Spada M, et al. High levels of exosomes expressing CD63 and caveolin-1 in plasma of melanoma patients. PLoS One. 2009;4(4):e5219.
19. 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(6):883-91.
20. Palmieri G, Ombra M, Colombino M, Casula M, Sini M, Manca A, et al. Multiple molecular pathways in melanomagenesis: characterization of therapeutic targets. Front Oncol. 2015;5:183. doi: 10.3389/fonc.2015.00183.
21. Cardinali B, Castellani L, Fasanaro P, Basso A, Alemà S, Martelli F, et al. Microrna-221 and microrna-222 modulate differentiation and maturation of skeletal muscle cells. PLoS One. 2009;4(10):e7607. doi: 10.1371/journal.pone.0007607.
22. Terasawa K, Ichimura A, Sato F, Shimizu K, Tsujimoto G. Sustained activation of ERK1/2 by NGF induces microRNA-221 and 222 in PC12 cells. FEBS J. 2009;276(12):3269-76. doi: 10.1111/j.1742-4658.2009.07041.x.
23. Zhang J, Han L, Ge Y, Zhou X, Zhang A, Zhang C, et al. miR-221/222 promote malignant progression of glioma through activation of the Akt pathway. Int J Oncol. 2010;36(4):913-20.
24. Li W, Guo F, Wang P, Hong S, Zhang C. miR-221/222 confers radioresistance in glioblastoma cells through activating Akt independent of PTEN status. Curr Mol Med. 2014;14(1):185-95.
25. Teixeira AL, Ferreira M, Silva J, Gomes M, Dias F, Santos JI, et al. Higher circulating expression levels of miR-221 associated with poor overall survival in renal cell carcinoma patients. Tumour Biol. 2014;35(5):4057-66. doi: 10.1007/s13277-013-1531-3.
26. Calderaro J, Rebouissou S, de Koning L, Masmoudi A, Herault A, Dubois T, et al. PI3K/AKT pathway activation in bladder carcinogenesis. Int J Cancer. 2014;134(8):1776-84.
27. Lee JC, Zhao JT, Gundara J, Serpell J, Bach LA, Sidhu S. Papillary thyroid cancer-derived exosomes contain miRNA-146b and miRNA-222. J Surg Res. 2015;196(1):39-48. doi: 10.1016/j.jss.2015.02.027.
28. Chen WX, Liu XM, Lv MM, Chen L, Zhao JH, Zhong SL, et al. Exosomes from drug-resistant breast cancer cells transmit chemoresistance by a horizontal transfer of microRNAs. PLoS One. 2014;9(4):e95240. doi: 10.1371/journal.pone.0095240.
29. Hannafon BN, Ding WQ. Intercellular communication by exosome-derived microRNAs in cancer. Int J Mol Sci. 2013;14(7):14240-69.
30. Valadi H, Ekstrom K, Bossios A, Sjostrand M, Lee JJ, Lotvall JO. Exosome-mediated transfer of mRNAs and microRNAs is a novel mechanism of genetic exchange between cells. Nat Cell Biol. 2007;9(6):654-9.
31. Halaban R. Growth factors and melanomas. Semin Oncol. 1996;23(6):673-81.
32. Mahabeleshwar GH, Byzova TV. Angiogenesis in melanoma. Semin Oncol. 2007;34(6):555-65.
33. Bubka M, Link-Lenczowski P, Janik M, Pochec E, Litynska A. Overexpression of Nacetylglucosaminyltransferases III and V in human melanoma cells. Implications for MCAM Nglycosylation. Biochimie. 2014;103:37-49.
34. Mendelsohn R, Cheung P, Berger L, Partridge E, Lau K, Datti A, et al. Complex N-glycan and metabolic control in tumor cells. Cancer Res. 2007;67(20):9771-80.
35. Li DQ, Pakala SB, Nair SS, Eswaran J, Kumar R. Metastasis-associated protein 1/nucleosome remodeling and histone deacetylase complex in cancer. Cancer Res. 2012;72(2):387-94.
36. Inui M, Martello G, Piccolo S. MicroRNA control of signal transduction. Nat Rev Mol Cell Biol. 2010;11(4):252-63.
37. Lotvall J, Hill AF, Hochberg F, Buzas EI, Di Vizio D, Gardiner C, et al. Minimal experimental requirements for definition of extracellular vesicles and their functions: a position statement from the International Society for Extracellular Vesicles. J Extracell Vesicles. 2014;3:26913.
38. Villarroya-Beltri C, Gutierrez-Vazquez C, Sanchez-Cabo F, Perez-Hernandez D, Vazquez J, Martin-Cofreces N, et al. Sumoylated hnRNPA2B1 controls the sorting of miRNAs into exosomes through binding to specific motifs. Nat Commun. 2013;4:2980.
39. 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(10):e13247.
40. Singh R, Pochampally R, Watabe K, Lu Z, Mo YY. Exosome-mediated transfer of miR-10b promotes cell invasion in breast cancer. Mol Cancer. 2014;13:256.
41. Eissa S, Matboli M, Shehata HH, Essawy NO. MicroRNA-10b and minichromosome maintenance complex component 5 gene as prognostic biomarkers in breast cancer. Tumour Biol. 2015;36(6):4487-94. doi: 10.1007/s13277-015-3090-2.
42. Chang CH, Fan TC, Yu JC, Liao GS, Lin YC, Shih AC, et al. The prognostic significance of RUNX2 and miR-10a/10b and their inter-relationship in breast cancer. J Transl Med. 2014;12:257.
43. Felli N, Errico MC, Pedini F, Petrini M, Puglisi R, Bellenghi M, et al. AP2α controls the dynamic balance between miR-126&126* and miR-221&222 during melanoma progression. Oncogene. 2015. doi: 10.1038/onc.2015.357.
44. Ostrowski M, Carmo NB, 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(1):19-30. sup pp 1-13.
45. Boelens MC, Wu TJ, Nabet BY, Xu B, Qiu Y, Yoon T, et al. Exosome transfer from stromal to breast cancer cells regulates therapy resistance pathways. Cell. 2014;159(3):499-513. doi: 10.1016/j.cell.2014.09.051.
46. Raposo G, Stoorvogel W. Extracellular vesicles: exosomes, microvesicles, and friends. J Cell Biol. 2013;200(4):373-83. doi: 10.1083/jcb.201211138.
47. Seubert B, Cui H, Simonavicius N, Honert K, Schafer S, Reuning U, et al. Tetraspanin CD63 acts as a pro-metastatic factor via beta-catenin stabilization. Int J Cancer. 2015;136(10):2304-15.
48. Diaz J, Mendoza P, Ortiz R, Diaz N, Leyton L, Stupack D, et al. Rab5 is required in metastatic cancer cells for Caveolin-1-enhanced Rac1 activation, migration and invasion. J Cell Sci. 2014;127(Pt 11):2401-6.
49. Toricelli M, Melo FH, Peres GB, Silva DC, Jasiulionis MG. Timp1 interacts with beta-1 integrin and CD63 along melanoma genesis and confers anoikis resistance by activating PI3-K signaling pathway independently of Akt phosphorylation. Mol Cancer. 2013;12:22.
50. Cui H, Seubert B, Stahl E, Dietz H, Reuning U, Moreno-Leon L, et al. Tissue inhibitor of metalloproteinases-1 induces a pro-tumourigenic increase of miR-210 in lung adenocarcinoma cells and their exosomes. Oncogene. 2015;34(28):3640-50. doi: 10.1038/onc.2014.300.
51. Tang MR, Wang YX, Guo S, Han SY, Li HH, Jin SF. Prognostic significance of in situ and plasma levels of transforming growth factor β1, -2 and -3 in cutaneous melanoma. Mol Med Rep. 2015;11(6):4508-12. doi: 10.3892/mmr.2015.3250.
52. Wesche J, Malecki J, Wiedlocha A, Skjerpen CS, Claus P, Olsnes S. FGF-1 and FGF-2 require the cytosolic chaperone Hsp90 for translocation into the cytosol and the cell nucleus. J Biol Chem. 2006;281(16):11405-12.