miR-9 and miR-200 regulate PDGFRβ-mediated endothelial differentiation of tumor cells in triple-negative breast cancer

Cancer Research

Volumn 76, Issue 18, 2016, Pages 5562-5572

  D'Ippolito, Elvira ^a   Plantamura, Ilaria ^a   Bongiovanni, Lucia ^b   Casalini, Patrizia ^a   Baroni, Sara ^a   Piovan, Claudia ^a   Orlandi, Rosaria ^a   Gualeni, Ambra V ^a   Gloghini, Annunziata ^a   Rossini, Anna ^a   Cresta, Sara ^a   Tessari, Anna ^a   De Braud, Filippo ^a,c   Di Leva, Gianpiero ^d   Tripodo, Claudio ^b   Iorio, Marilena V ^a  

^a NATIONAL CANCER INSTITUTE   (Italy)

^b UNIVERSITY OF PALERMO   (Italy)

^c UNIVERSITY OF MILAN   (Italy)

^d UNIVERSITY OF SALFORD   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

MICRORNA 200; MICRORNA 9; PLATELET DERIVED GROWTH FACTOR BETA RECEPTOR; RHO GUANINE NUCLEOTIDE BINDING PROTEIN; STAR RELATED LIPID TRANSFER DOMAIN CONTAINING 13; TRANSCRIPTION FACTOR ZEB1; UNCLASSIFIED DRUG; MICRORNA; MIRN200 MICRORNA, HUMAN; MIRN92 MICRORNA, HUMAN; PDGFRB PROTEIN, HUMAN;

ANGIOGENESIS; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; BREAST CARCINOGENESIS; CANCER PROGNOSIS; CELL DIFFERENTIATION; CONTROLLED STUDY; ENZYME ACTIVATION; ENZYME INHIBITION; ENZYME REGULATION; FEMALE; HUMAN; HUMAN CELL; HUMAN TISSUE; IMMUNOFLUORESCENCE; IMMUNOHISTOCHEMISTRY; IN VITRO STUDY; IN VIVO STUDY; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN TARGETING; SIGNAL TRANSDUCTION; TRIPLE NEGATIVE BREAST CANCER; ANIMAL; BIOSYNTHESIS; ENDOTHELIUM CELL; FLUORESCENT ANTIBODY TECHNIQUE; GENE EXPRESSION REGULATION; GENE SILENCING; GENETICS; IN SITU HYBRIDIZATION; NEOVASCULARIZATION (PATHOLOGY); PATHOLOGY; POLYMERASE CHAIN REACTION; SCID MOUSE; WESTERN BLOTTING; XENOGRAFT;

ANIMALS; BLOTTING, WESTERN; CELL DIFFERENTIATION; ENDOTHELIAL CELLS; FEMALE; FLUORESCENT ANTIBODY TECHNIQUE; GENE EXPRESSION REGULATION, NEOPLASTIC; GENE KNOCKDOWN TECHNIQUES; HETEROGRAFTS; HUMANS; IMMUNOHISTOCHEMISTRY; IN SITU HYBRIDIZATION; MICE; MICE, SCID; MICRORNAS; NEOVASCULARIZATION, PATHOLOGIC; POLYMERASE CHAIN REACTION; RECEPTOR, PLATELET-DERIVED GROWTH FACTOR BETA; TRIPLE NEGATIVE BREAST NEOPLASMS;

EID: 84988913063     PISSN: 00085472     EISSN: 15387445     Source Type: Journal    
DOI: 10.1158/0008-5472.CAN-16-0140     Document Type: Article

References (42)

1. Cao Z, Shang B, Zhang G, Miele L, Sarkar FH, Wang Z, et al. Tumor cell-mediated neovascularization and lymphangiogenesis contrive tumor progression and cancer metastasis. Biochim Biophys Acta 2013;1836:273-86.
2. Ricci-Vitiani L, Pallini R, Biffoni M, Todaro M, Invernici G, Cenci T, et al. Tumour vascularization via endothelial differentiation of glioblastoma stem-like cells. Nature 2010;468:824-8.
3. Soda Y, Marumoto T, Friedmann-Morvinski D, Soda M, Liu F, Michiue H, et al. Transdifferentiation of glioblastoma cells into vascular endothelial cells. Proc Natl Acad Sci U S A 2011;108:4274-80.
4. Plantamura I, Casalini P, Dugnani E, Sasso M, D'Ippolito E, Tortoreto M, et al. PDGFRβ and FGFR2 mediate endothelial cell differentiation capability of triple negative breast carcinoma cells. Mol Oncol 2014;8:968-81.
5. Dent R, Trudeau M, Pritchard KI, Hanna WM, Kahn HK, Sawka CA, et al. Triple-negative breast cancer: clinical features and patterns of recurrence. Clin Cancer Res 2007;13:4429-34.
6. Carey L, Winer E, Viale G, Cameron D, Gianni L. Triple-negative breast cancer: disease entity or title of convenience? Nat Rev Clin Oncol 2010;7:683-92.
7. Criscitiello C, Gelao L, Viale G, Esposito A, Curigliano G. Investigational platelet-derived growth factor receptor kinase inhibitors in breast cancer therapy. Expert Opin Investig Drugs 2014;23:599-610.
8. Iorio MV, Croce CM. MicroRNA dysregulation in cancer: diagnostics, monitoring and therapeutics. A comprehensive review. EMBO Mol Med 2012;4:143-59.
9. Zhang J, Chintalgattu V, Shih T, Ai D, Xia Y, Khakoo AY. MicroRNA-9 is an activation-induced regulator of PDGFR-beta expression in cardiomyocytes. J Mol Cell Cardiol 2011;51:337-46.
10. Ma L, Young J, Prabhala H, Pan E, Mestdagh P, Muth D, et al. miR-9, aMYC/MYCN-activated microRNA, regulates E-cadherin and cancer metastasis. Nat Cell Biol 2010;12:247-56.
11. Gwak JM, Kim HJ, Kim EJ, Chung YR, Yun S, Seo AN, et al. MicroRNA-9 is associated with epithelial-mesenchymal transition, breast cancer stem cell phenotype, and tumor progression in breast cancer. Breast Cancer Res Treat 2014;147:39-49.
12. Hill L, Browne G, Tulchinsky E. ZEB/miR-200 feedback loop: at the crossroads of signal transduction in cancer. Int J Cancer 2013;132:745-54.
13. Meng F, Speyer CL, Zhang B, Zhao Y, Chen W, Gorski DH, et al. PDGFRalpha and beta play critical roles in mediating Foxq1-driven breast cancer stemness and chemoresistance. Cancer Res 2015;75:584-93.
14. Kong D, Li Y, Wang Z, Banerjee S, Ahmad A, Kim HR, et al. miR-200 regulates PDGF-D-mediated epithelial-mesenchymal transition, adhesion, and invasion of prostate cancer cells. Stem Cells 2009;27:1712-21.
15. Huang X, Dugo M, Callari M, Sandri M, De CL, Valeri B, et al. Molecular portrait of breast cancer in China reveals comprehensive transcriptomic likeness to Caucasian breast cancer and low prevalence of luminal A subtype. Cancer Med 2015;4:1016-30.
16. Smyth GK.Linear models and empirical bayes methods for assessing differential expression in microarray experiments. Stat Appl Genet Mol Biol 2004;3:Article3.
17. Vlachos IS, Hatzigeorgiou AG. Online resources for miRNA analysis. Clin Biochem 2013;46:879-900.
18. Gualeni AV, Volpi CC, Carbone A, Gloghini A. A novel semi-automated in situ hybridisation protocol for microRNA detection in paraffin embedded tissue sections. J Clin Pathol 2015;68:661-4.
19. Perou CM, Sorlie T, Eisen MB, van de Rijn M, Jeffrey SS, Rees CA, et al. Molecular portraits of human breast tumours. Nature 2000;406:747-52.
20. Tang F, Zhang R, He Y, Zou M, Guo L, Xi T. MicroRNA-125b induces metastasis by targeting STARD13 in MCF-7 and MDA-MB-231 breast cancer cells. PLoS ONE 2012;7:e35435.
21. Burk U, Schubert J, Wellner U, Schmalhofer O, Vincan E, Spaderna S, et al. A reciprocal repression between ZEB1 and members of the miR-200 family promotes EMT and invasion in cancer cells. EMBO Rep 2008;9:582-9.
22. Thomson S, Petti F, Sujka-Kwok I, Mercado P, Bean J, Monaghan M, et al. A systems view of epithelial-mesenchymal transition signaling states. Clin Exp Metastasis 2011;28:137-55.
23. Gravgaard KH, Lyng MB, Laenkholm AV, Sokilde R, Nielsen BS, Litman T, et al. The miRNA-200 family and miRNA-9 exhibit differential expression in primary versus corresponding metastatic tissue in breast cancer. Breast Cancer Res Treat 2012;134:207-17.
24. Hsu PY, Deatherage DE, Rodriguez BA, Liyanarachchi S, Weng YI, Zuo T, et al. Xenoestrogen-induced epigenetic repression of microRNA-9-3 in breast epithelial cells. Cancer Res 2009;69:5936-45.
25. Jechlinger M, Sommer A, Moriggl R, Seither P, Kraut N, Capodiecci P, et al. Autocrine PDGFR signaling promotes mammary cancer metastasis. J Clin Invest 2006;116:1561-70.
26. Kuzmanov A, Hopfer U, Marti P, Meyer-Schaller N, Yilmaz M, Christofori G. LIM-homeobox gene 2 promotes tumor growth and metastasis by inducing autocrine and paracrine PDGF-B signaling. Mol Oncol 2014;8:401-16.
27. Jurmeister S, Baumann M, Balwierz A, Keklikoglou I, Ward A, Uhlmann S, et al. MicroRNA-200c represses migration and invasion of breast cancer cells by targeting actin-regulatory proteins FHOD1 and PPM1F. Mol Cell Biol 2012;32:633-51.
28. Lim YY, Wright JA, Attema JL, Gregory PA, Bert AG, Smith E, et al. Epigenetic modulation of the miR-200 family is associated with transition to a breast cancer stem-cell-like state. J Cell Sci 2013;126:2256-66.
29. Kopp F, Oak PS, Wagner E, Roidl A. miR-200c sensitizes breast cancer cells to doxorubicin treatment by decreasing TrkB and Bmi1 expression. PLoS ONE 2012;7:e50469.
30. Lin J, Liu C, Gao F, Mitchel RE, Zhao L, Yang Y, et al. miR-200c enhances radiosensitivity of human breast cancer cells. J Cell Biochem 2013;114:606-15.
31. Bai WD, Ye XM, Zhang MY, Zhu HY, Xi WJ, Huang X, et al. MiR-200c suppresses TGF-beta signaling and counteracts trastuzumab resistance and metastasis by targeting ZNF217 and ZEB1 in breast cancer. Int J Cancer 2014;135:1356-68.
32. Madhavan D, Zucknick M, Wallwiener M, Cuk K, Modugno C, Scharpff M, et al. Circulating miRNAs as surrogate markers for circulating tumor cells and prognostic markers in metastatic breast cancer. Clin Cancer Res 2012;18:5972-82.
33. Wang J, Zhao H, Tang D, Wu J, Yao G, Zhang Q. Overexpressions of microRNA-9 and microRNA-200c in human breast cancers are associated with lymph node metastasis. Cancer Biother Radiopharm 2013;28:283-8.
34. Le MT, Hamar P, Guo C, Basar E, Perdigao-Henriques R, Balaj L, et al. miR-200-containing extracellular vesicles promote breast cancer cell metastasis. J Clin Invest 2014;124:5109-28.
35. Knezevic J, Pfefferle AD, Petrovic I, Greene SB, Perou CM, Rosen JM. Expression of miR-200c in claudin-low breast cancer alters stem cell functionality, enhances chemosensitivity and reduces metastatic potential. Oncogene 2015;34:5997-6006.
36. Castilla MA, Diaz-Martin J, Sarrio D, Romero-Perez L, Lopez-Garcia MA, Vieites B, et al. MicroRNA-200 family modulation in distinct breast cancer phenotypes. PLoS ONE 2012;7:e47709.
37. Riaz M, van Jaarsveld MT, Hollestelle A, Prager-van der Smissen WJ, Heine AA, Boersma AW, et al. miRNA expression profiling of 51 human breast cancer cell lines reveals subtype and driver mutation-specific miRNAs. Breast Cancer Res 2013;15:R33.
38. Ahmad A, Wang Z, Kong D, Ali R, Ali S, Banerjee S, et al. Platelet-derived growth factor-D contributes to aggressiveness of breast cancer cells by upregulating Notch and NF-kappaB signaling pathways. Breast Cancer Res Treat 2011;126:15-25.
39. Chen HF, Huang CH, Liu CJ, Hung JJ, Hsu CC, Teng SC, et al. Twist1 induces endothelial differentiation of tumour cells through the Jagged1-KLF4 axis. Nat Commun 2014;5:4697.
40. Vasudev NS, Reynolds AR. Anti-angiogenic therapy for cancer: current progress, unresolved questions and future directions. Angiogenesis 2014;17:471-94.
41. Pecot CV, Rupaimoole R, Yang D, Akbani R, Ivan C, Lu C, et al. Tumour angiogenesis regulation by the miR-200 family. Nat Commun 2013;4:2427.
42. Zhuang G, Wu X, Jiang Z, Kasman I, Yao J, Guan Y, et al. Tumour-secreted miR-9 promotes endothelial cell migration and angiogenesis by activating the JAK-STAT pathway. EMBO J 2012;31:3513-23.