MiR-135b coordinates progression of ErbB2-driven mammary carcinomas through suppression of MID1 and MTCH2

American Journal of Pathology

Volumn 182, Issue 6, 2013, Pages 2058-2070

  Arigoni, Maddalena ^a   Barutello, Giuseppina ^a   Riccardo, Federica ^a   Ercole, Elisabetta ^a   Cantarella, Daniela ^a   Orso, Francesca ^a   Conti, Laura ^a   Lanzardo, Stefania ^a   Taverna, Daniela ^a   Merighi, Irene ^a   Calogero, Raffaele A ^a   Cavallo, Federica ^a   Quaglino, Elena ^a  

^a UNIVERSITY OF TURIN   (Italy)

Author keywords

[No Author keywords available]

Indexed keywords

CELL PROTEIN; MICRORNA; MICRORNA 135A; MICRORNA 135B; MIDLINE 1; MITOCHONDRIAL CARRIER HOMOLOG 2; UNCLASSIFIED DRUG;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; BREAST CARCINOMA; CANCER CELL; CANCER GROWTH; CELL PROLIFERATION; CONTROLLED STUDY; FEMALE; GENE TARGETING; INVASIVE CARCINOMA; LUNG CANCER; METASTASIS; MOLECULAR MECHANICS; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; RAT;

ANIMALS; BREAST NEOPLASMS; CELL PROLIFERATION; DISEASE PROGRESSION; FEMALE; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION, NEOPLASTIC; GENES, ERBB-2; HUMANS; LUNG NEOPLASMS; MAMMARY NEOPLASMS, EXPERIMENTAL; MICE; MICE, INBRED BALB C; MICE, TRANSGENIC; MICRORNAS; MITOCHONDRIAL MEMBRANE TRANSPORT PROTEINS; NEOPLASM INVASIVENESS; NEOPLASM PROTEINS; NEOPLASTIC STEM CELLS; PROTEINS; RNA, NEOPLASM; TUMOR CELLS, CULTURED; UP-REGULATION;

EID: 84878236258     PISSN: 00029440     EISSN: 15252191     Source Type: Journal    
DOI: 10.1016/j.ajpath.2013.02.046     Document Type: Article

References (70)

1. A. Jemal, R. Siegel, J. Xu, and E. Ward Cancer statistics, 2010 CA Cancer J Clin 60 2010 277 300
2. E.R. Galvao, L.M. Martins, J.O. Ibiapina, H.M. Andrade, and S.J. Monte Breast cancer proteomics: a review for clinicians J Cancer Res Clin Oncol 137 2011 915 925
3. G.P. Gupta, and J. Massague Cancer metastasis: building a framework Cell 127 2006 679 695
4. D.X. Nguyen, P.D. Bos, and J. Massague Metastasis: from dissemination to organ-specific colonization Nat Rev Cancer 9 2009 274 284
5. S. Valastyan, and R.A. Weinberg Tumor metastasis: molecular insights and evolving paradigms Cell 147 2011 275 292
6. V.S. Nair, L.S. Maeda, and J.P. Ioannidis Clinical outcome prediction by microRNAs in human cancer: a systematic review J Natl Cancer Inst 104 2012 528 540
7. S.F. Tavazoie, C. Alarcon, T. Oskarsson, D. Padua, Q. Wang, P.D. Bos, W.L. Gerald, and J. Massague Endogenous human microRNAs that suppress breast cancer metastasis Nature 451 2008 147 152
8. J. Zhang, and L. Ma MicroRNA control of epithelial-mesenchymal transition and metastasis Cancer Metastasis Rev 31 2012 653 662
9. C.L. Bockmeyer, M. Christgen, M. Muller, S. Fischer, P. Ahrens, F. Langer, H. Kreipe, and U. Lehmann MicroRNA profiles of healthy basal and luminal mammary epithelial cells are distinct and reflected in different breast cancer subtypes Breast Cancer Res Treat 130 2011 735 745
10. C. Blenkiron, L.D. Goldstein, N.P. Thorne, I. Spiteri, S.F. Chin, M.J. Dunning, N.L. Barbosa-Morais, A.E. Teschendorff, A.R. Green, I.O. Ellis, S. Tavare, C. Caldas, and E.A. Miska MicroRNA expression profiling of human breast cancer identifies new markers of tumor subtype Genome Biol 8 2007 R214
11. B.D. Adams, I.K. Guttilla, and B.A. White Involvement of microRNAs in breast cancer Semin Reprod Med 26 2008 522 536
12. E. Enerly, I. Steinfeld, K. Kleivi, S.K. Leivonen, M.R. Aure, H.G. Russnes, J.A. Ronneberg, H. Johnsen, R. Navon, E. Rodland, R. Makela, B. Naume, M. Perala, O. Kallioniemi, V.N. Kristensen, Z. Yakhini, and A.L. Borresen-Dale miRNA-mRNA integrated analysis reveals roles for miRNAs in primary breast tumors PLoS One 6 2011 e16915
13. A.J. Lowery, N. Miller, A. Devaney, R.E. McNeill, P.A. Davoren, C. Lemetre, V. Benes, S. Schmidt, J. Blake, G. Ball, and M.J. Kerin MicroRNA signatures predict oestrogen receptor, progesterone receptor and HER2/neu receptor status in breast cancer Breast Cancer Res 11 2009 R27
14. M.V. Iorio, M. Ferracin, C.G. Liu, A. Veronese, R. Spizzo, S. Sabbioni, E. Magri, M. Pedriali, M. Fabbri, M. Campiglio, S. Menard, J.P. Palazzo, A. Rosenberg, P. Musiani, S. Volinia, I. Nenci, G.A. Calin, P. Querzoli, M. Negrini, and C.M. Croce MicroRNA gene expression deregulation in human breast cancer Cancer Res 65 2005 7065 7070
15. M. Sachdeva, and Y.Y. Mo MicroRNA-145 suppresses cell invasion and metastasis by directly targeting mucin 1 Cancer Res 70 2010 378 387
16. K.J. Png, M. Yoshida, X.H. Zhang, W. Shu, H. Lee, A. Rimner, T.A. Chan, E. Comen, V.P. Andrade, S.W. Kim, T.A. King, C.A. Hudis, L. Norton, J. Hicks, J. Massague, and S.F. Tavazoie MicroRNA-335 inhibits tumor reinitiation and is silenced through genetic and epigenetic mechanisms in human breast cancer Genes Dev 25 2011 226 231
17. N. Zhu, D. Zhang, H. Xie, Z. Zhou, H. Chen, T. Hu, Y. Bai, Y. Shen, W. Yuan, Q. Jing, and Y. Qin Endothelial-specific intron-derived miR-126 is down-regulated in human breast cancer and targets both VEGFA and PIK3R2 Mol Cell Biochem 351 2011 157 164
18. L. Ma Role of miR-10b in breast cancer metastasis Breast Cancer Res 12 2010 210
19. B. Song, C. Wang, J. Liu, X. Wang, L. Lv, L. Wei, L. Xie, Y. Zheng, and X. Song MicroRNA-21 regulates breast cancer invasion partly by targeting tissue inhibitor of metalloproteinase 3 expression J Exp Clin Cancer Res 29 2010 29
20. F. Rothe, M. Ignatiadis, C. Chaboteaux, B. Haibe-Kains, N. Kheddoumi, S. Majjaj, B. Badran, H. Fayyad-Kazan, C. Desmedt, A.L. Harris, M. Piccart, and C. Sotiriou Global microRNA expression profiling identifies MiR-210 associated with tumor proliferation, invasion and poor clinical outcome in breast cancer PLoS One 6 2011 e20980
21. F.M. Buffa, C. Camps, L. Winchester, C.E. Snell, H.E. Gee, H. Sheldon, M. Taylor, A.L. Harris, and J. Ragoussis microRNA-associated progression pathways and potential therapeutic targets identified by integrated mRNA and microRNA expression profiling in breast cancer Cancer Res 71 2011 5635 5645
22. C.A. Andorfer, B.M. Necela, E.A. Thompson, and E.A. Perez MicroRNA signatures: clinical biomarkers for the diagnosis and treatment of breast cancer Trends Mol Med 17 2011 313 319
23. F. Cavallo, R. Offringa, S.H. van der Burg, G. Forni, and C.J. Melief Vaccination for treatment and prevention of cancer in animal models Adv Immunol 90 2006 175 213
24. E. Quaglino, C. Mastini, G. Forni, and F. Cavallo ErbB2 transgenic mice: a tool for investigation of the immune prevention and treatment of mammary carcinomas Curr Protoc Immunol 2008 Chap 20:Unit 20.9.1-20.9-10
25. Y. Husemann, J.B. Geigl, F. Schubert, P. Musiani, M. Meyer, E. Burghart, G. Forni, R. Eils, T. Fehm, G. Riethmuller, and C.A. Klein Systemic spread is an early step in breast cancer Cancer Cell 13 2008 58 68
26. A. Astolfi, L. Landuzzi, G. Nicoletti, C. De Giovanni, S. Croci, A. Palladini, S. Ferrini, M. Iezzi, P. Musiani, F. Cavallo, G. Forni, P. Nanni, and P.L. Lollini Gene expression analysis of immune-mediated arrest of tumorigenesis in a transgenic mouse model of HER-2/neu-positive basal-like mammary carcinoma Am J Pathol 166 2005 1205 1216
27. E. Quaglino, S. Rolla, M. Iezzi, M. Spadaro, P. Musiani, C. De Giovanni, P.L. Lollini, S. Lanzardo, G. Forni, R. Sanges, S. Crispi, P. De Luca, R. Calogero, and F. Cavallo Concordant morphologic and gene expression data show that a vaccine halts HER-2/neu preneoplastic lesions J Clin Invest 113 2004 709 717
28. K. Boggio, G. Nicoletti, E. Di Carlo, F. Cavallo, L. Landuzzi, C. Melani, M. Giovarelli, I. Rossi, P. Nanni, C. De Giovanni, P. Bouchard, S. Wolf, A. Modesti, P. Musiani, P.L. Lollini, M.P. Colombo, and G. Forni Interleukin 12-mediated prevention of spontaneous mammary adenocarcinomas in two lines of Her-2/neu transgenic mice J Exp Med 188 1998 589 596
29. P. Workman, E.O. Aboagye, F. Balkwill, A. Balmain, G. Bruder, D.J. Chaplin, J.A. Double, J. Everitt, D.A. Farningham, M.J. Glennie, L.R. Kelland, V. Robinson, I.J. Stratford, G.M. Tozer, S. Watson, S.R. Wedge, and S.A. Eccles Guidelines for the welfare and use of animals in cancer research Br J Cancer 102 2010 1555 1577
30. S. Rovero, K. Boggio, E. Di Carlo, A. Amici, E. Quaglino, P. Porcedda, P. Musiani, and G. Forni Insertion of the DNA for the 163-171 peptide of IL1beta enables a DNA vaccine encoding p185(neu) to inhibit mammary carcinogenesis in Her-2/neu transgenic BALB/c mice Gene Ther 8 2001 447 452
31. P. Nanni, C. de Giovanni, P.L. Lollini, G. Nicoletti, and G. Prodi TS/A: a new metastasizing cell line from a BALB/c spontaneous mammary adenocarcinoma Clin Exp Metastasis 1 1983 373 380
32. C. Grange, S. Lanzardo, F. Cavallo, G. Camussi, and B. Bussolati Sca-1 identifies the tumor-initiating cells in mammary tumors of BALB-neuT transgenic mice Neoplasia 10 2008 1433 1443
33. M.E. Ritchie, J. Silver, A. Oshlack, M. Holmes, D. Diyagama, A. Holloway, and G.K. Smyth A comparison of background correction methods for two-colour microarrays Bioinformatics 23 2007 2700 2707
34. R. Sanges, F. Cordero, and R.A. Calogero oneChannelGUI: a graphical interface to Bioconductor tools, designed for life scientists who are not familiar with R language Bioinformatics 23 2007 3406 3408
35. A.L. Bookout, and D.J. Mangelsdorf Quantitative real-time PCR protocol for analysis of nuclear receptor signaling pathways Nucl Recept Signal 1 2003 e012
36. R.C. Gentleman, V.J. Carey, D.M. Bates, B. Bolstad, M. Dettling, S. Dudoit, B. Ellis, L. Gautier, Y. Ge, J. Gentry, K. Hornik, T. Hothorn, W. Huber, S. Iacus, R. Irizarry, F. Leisch, C. Li, M. Maechler, A.J. Rossini, G. Sawitzki, C. Smith, G. Smyth, L. Tierney, J.Y. Yang, and J. Zhang Bioconductor: open software development for computational biology and bioinformatics Genome Biol 5 2004 R80
37. R. Breitling, P. Armengaud, A. Amtmann, and P. Herzyk Rank products: a simple, yet powerful, new method to detect differentially regulated genes in replicated microarray experiments FEBS Lett 573 2004 83 92
38. A. Sasson, and T.P. Michael Filtering error from SOLiD Output Bioinformatics 26 2010 849 850
39. S.M. Rumble, P. Lacroute, A.V. Dalca, M. Fiume, A. Sidow, and M. Brudno SHRiMP: accurate mapping of short color-space reads PLoS Comput Biol 5 2009 e1000386
40. M.D. Robinson, and G.K. Smyth Small-sample estimation of negative binomial dispersion, with applications to SAGE data Biostatistics 9 2008 321 332
41. C.M. Perou, T. Sorlie, M.B. Eisen, M. van de Rijn, S.S. Jeffrey, C.A. Rees, J.R. Pollack, D.T. Ross, H. Johnsen, L.A. Akslen, O. Fluge, A. Pergamenschikov, C. Williams, S.X. Zhu, P.E. Lonning, A.L. Borresen-Dale, P.O. Brown, and D. Botstein Molecular portraits of human breast tumours Nature 406 2000 747 752
42. D. Betel, A. Koppal, P. Agius, C. Sander, and C. Leslie Comprehensive modeling of microRNA targets predicts functional non-conserved and non-canonical sites Genome Biol 11 2010 R90
43. F. Gilli, R.L. Lindberg, P. Valentino, F. Marnetto, S. Malucchi, A. Sala, M. Capobianco, A. di Sapio, F. Sperli, L. Kappos, R.A. Calogero, and A. Bertolotto Learning from nature: pregnancy changes the expression of inflammation-related genes in patients with multiple sclerosis PLoS One 5 2010 e8962
44. G.K. Smyth Linear models and empirical bayes methods for assessing differential expression in microarray experiments Stat Appl Genet Mol Biol 3 2004 Article3
45. R.A. Calogero, E. Quaglino, S. Saviozzi, G. Forni, and F. Cavallo Oncoantigens as anti-tumor vaccination targets: the chance of a lucky strike? Cancer Immunol Immunother 57 2008 1685 1694
46. R.W. Cho, X. Wang, M. Diehn, K. Shedden, G.Y. Chen, G. Sherlock, A. Gurney, J. Lewicki, and M.F. Clarke Isolation and molecular characterization of cancer stem cells in MMTV-Wnt-1 murine breast tumors Stem Cells 26 2008 364 371
47. C.R. Jeter, B. Liu, X. Liu, X. Chen, C. Liu, T. Calhoun-Davis, J. Repass, H. Zaehres, J.J. Shen, and D.G. Tang NANOG promotes cancer stem cell characteristics and prostate cancer resistance to androgen deprivation Oncogene 30 2011 3833 3845
48. J.M. Hao, J.Z. Chen, H.M. Sui, X.Q. Si-Ma, G.Q. Li, C. Liu, J.L. Li, Y.Q. Ding, and J.M. Li A five-gene signature as a potential predictor of metastasis and survival in colorectal cancer J Pathol 220 2010 475 489
49. K. Yu, K. Ganesan, L.K. Tan, M. Laban, J. Wu, X.D. Zhao, H. Li, C.H. Leung, Y. Zhu, C.L. Wei, S.C. Hooi, L. Miller, and P. Tan A precisely regulated gene expression cassette potently modulates metastasis and survival in multiple solid cancers PLoS Genet 4 2008 e1000129
50. U. Klein, and R. Dalla-Favera New insights into the pathogenesis of chronic lymphocytic leukemia Semin Cancer Biol 20 2010 377 383
51. D.R. Hurst, M.D. Edmonds, and D.R. Welch Metastamir: the field of metastasis-regulatory microRNA is spreading Cancer Res 69 2009 7495 7498
52. K. Polyak, and R.A. Weinberg Transitions between epithelial and mesenchymal states: acquisition of malignant and stem cell traits Nat Rev Cancer 9 2009 265 273
53. C. Urbich, A. Kuehbacher, and S. Dimmeler Role of microRNAs in vascular diseases, inflammation, and angiogenesis Cardiovasc Res 79 2008 581 588
54. A. Astolfi, S. Rolla, P. Nanni, E. Quaglino, C. De Giovanni, M. Iezzi, P. Musiani, G. Forni, P.L. Lollini, F. Cavallo, and R.A. Calogero Immune prevention of mammary carcinogenesis in HER-2/neu transgenic mice: a microarray scenario Cancer Immunol Immunother 54 2005 599 610
55. F. Cavallo, R.A. Calogero, and G. Forni Are oncoantigens suitable targets for anti-tumour therapy? Nat Rev Cancer 7 2007 707 713
56. R.A. Calogero, E. Quaglino, S. Saviozzi, G. Forni, and F. Cavallo Oncoantigens as anti-tumor vaccination targets: the chance of a lucky strike? Cancer Immunol Immunother 57 2008 1685 1694
57. L.N. Li, H.D. Zhang, R. Zhi, and S.J. Yuan Down-regulation of some miRNAs by degrading their precursors contributes to anti-cancer effect of mistletoe lectin-I Br J Pharmacol 162 2011 349 364
58. A. Navarro, T. Diaz, A. Martinez, A. Gaya, A. Pons, B. Gel, C. Codony, G. Ferrer, C. Martinez, E. Montserrat, and M. Monzo Regulation of JAK2 by miR-135a: prognostic impact in classic Hodgkin lymphoma Blood 114 2009 2945 2951
59. Y.X. Wang, X.Y. Zhang, B.F. Zhang, C.Q. Yang, X.M. Chen, and H.J. Gao Initial study of microRNA expression profiles of colonic cancer without lymph node metastasis J Dig Dis 11 2010 50 54
60. M.M. Vickers, J. Bar, I. Gorn-Hondermann, N. Yarom, M. Daneshmand, J.E. Hanson, C.L. Addison, T.R. Asmis, D.J. Jonker, J. Maroun, I.A. Lorimer, G.D. Goss, and J. Dimitroulakos Stage-dependent differential expression of microRNAs in colorectal cancer: potential role as markers of metastatic disease Clin Exp Metastasis 29 2012 123 132
61. X.M. Xu, J.C. Qian, Z.L. Deng, Z. Cai, T. Tang, P. Wang, K.H. Zhang, and J.P. Cai Expression of miR-21, miR-31, miR-96 and miR-135b is correlated with the clinical parameters of colorectal cancer Oncol Lett 4 2012 339 345
62. R.R. Lulla, F.F. Costa, J.M. Bischof, P.M. Chou, M. de F Bonaldo, E.F. Vanin, and M.B. Soares Identification of differentially expressed microRNAs in osteosarcoma Sarcoma 2011 2011 732690
63. F.F. Costa, J.M. Bischof, E.F. Vanin, R.R. Lulla, M. Wang, S.T. Sredni, V. Rajaram, F. Bonaldo Mde, D. Wang, S. Goldman, T. Tomita, and M.B. Soares Identification of microRNAs as potential prognostic markers in ependymoma PLoS One 6 2011 e25114
64. S. Liu, W. Guo, J. Shi, N. Li, X. Yu, J. Xue, X. Fu, K. Chu, C. Lu, J. Zhao, D. Xie, M. Wu, and S. Cheng MicroRNA-135a contributes to the development of portal vein tumor thrombus by promoting metastasis in hepatocellular carcinoma J Hepatol 56 2012 389 396
65. S. Rovero, A. Amici, E. Di Carlo, R. Bei, P. Nanni, E. Quaglino, P. Porcedda, K. Boggio, A. Smorlesi, P.L. Lollini, L. Landuzzi, M.P. Colombo, M. Giovarelli, P. Musiani, and G. Forni DNA vaccination against rat her-2/Neu p185 more effectively inhibits carcinogenesis than transplantable carcinomas in transgenic BALB/c mice J Immunol 165 2000 5133 5142
66. M. Lindow, and J. Gorodkin Principles and limitations of computational microRNA gene and target finding DNA Cell Biol 26 2007 339 351
67. P. Alexiou, M. Maragkakis, G.L. Papadopoulos, M. Reczko, and A.G. Hatzigeorgiou Lost in translation: an assessment and perspective for computational microRNA target identification Bioinformatics 25 2009 3049 3055
68. B. Aranda-Orgilles, J. Aigner, M. Kunath, R. Lurz, R. Schneider, and S. Schweiger Active transport of the ubiquitin ligase MID1 along the microtubules is regulated by protein phosphatase 2A PLoS One 3 2008 e3507
69. R. Leibowitz-Amit, G. Tsarfaty, Y. Abargil, G.M. Yerushalmi, J. Horev, and I. Tsarfaty Mimp, a mitochondrial carrier homologue, inhibits Met-HGF/SF-induced scattering and tumorigenicity by altering Met-HGF/SF signaling pathways Cancer Res 66 2006 8687 8697
70. Y. Zaltsman, L. Shachnai, N. Yivgi-Ohana, M. Schwarz, M. Maryanovich, R.H. Houtkooper, F.M. Vaz, F. De Leonardis, G. Fiermonte, F. Palmieri, B. Gillissen, P.T. Daniel, E. Jimenez, S. Walsh, C.M. Koehler, S.S. Roy, L. Walter, G. Hajnoczky, and A. Gross MTCH2/MIMP is a major facilitator of tBID recruitment to mitochondria Nat Cell Biol 12 2010 553 562