Systematic analysis of metastasis-associated genes identifies miR-17-5p as a metastatic suppressor of basal-like breast cancer

Breast Cancer Research and Treatment

Volumn 146, Issue 3, 2014, Pages 487-502

  Fan, Meiyun ^a,b   Sethuraman, Aarti ^a,b   Brown, Martin ^b   Sun, Wenlin ^c   Pfeffer, Lawrence M ^a,b  

^a Department of Pathology and Laboratory Medicine ^*  (United States)

^b Center for Cancer Research   (United States)

^c UNIVERSITY OF TENNESSEE HEALTH SCIENCE CENTER   (United States)

Author keywords

Breast cancer; Hypoxia; Metastasis; MIR17HG; TGFB

Indexed keywords

MESSENGER RNA; MICRORNA; MICRORNA 17; MICRORNA 17 5P; MICRORNA 200; MICRORNA 96; TRANSFORMING GROWTH FACTOR BETA; UNCLASSIFIED DRUG; WNT PROTEIN; MIRN17 MICRORNA, HUMAN;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; BASAL LIKE BREAST CANCER; CANCER GROWTH; CANCER PROGNOSIS; CELL INVASION; CELL MIGRATION; CONTROLLED STUDY; DISTANT METASTASIS FREE SURVIVAL; EPITHELIAL MESENCHYMAL TRANSITION; GENE EXPRESSION REGULATION; GENE FUNCTION; GENE IDENTIFICATION; GENE INTERACTION; GENE TARGETING; GENETIC ASSOCIATION; GENETIC LINKAGE; HYPOXIA; IN VITRO STUDY; IN VIVO STUDY; LUNG METASTASIS; METASTASIS; MOUSE; NONHUMAN; PRIORITY JOURNAL; RNA ANALYSIS; SIGNAL TRANSDUCTION; UPREGULATION; WNT SIGNALING PATHWAY; BASAL CELL CARCINOMA; BIOSYNTHESIS; BREAST NEOPLASMS; FEMALE; GENETICS; HUMAN; KAPLAN MEIER METHOD; LUNG TUMOR; META ANALYSIS; PATHOLOGY; SECONDARY; TUMOR SUPPRESSOR GENE;

BREAST NEOPLASMS; EPITHELIAL-MESENCHYMAL TRANSITION; FEMALE; GENE EXPRESSION REGULATION, NEOPLASTIC; GENES, TUMOR SUPPRESSOR; HUMANS; KAPLAN-MEIER ESTIMATE; LUNG NEOPLASMS; MICRORNAS; NEOPLASM METASTASIS; NEOPLASMS, BASAL CELL; RNA, MESSENGER; SIGNAL TRANSDUCTION; TRANSFORMING GROWTH FACTOR BETA;

EID: 84907598510     PISSN: 01676806     EISSN: 15737217     Source Type: Journal    
DOI: 10.1007/s10549-014-3040-5     Document Type: Article

References (56)

1. Society AC (2013-2014) Breast cancer facts & figures
2. Parker JS, Mullins M, Cheang MC, Leung S, Voduc D, Vickery T, Davies S, Fauron C, He X, Hu Z, Quackenbush JF, Stijleman IJ, Palazzo J, Marron JS, Nobel AB, Mardis E, Nielsen TO, Ellis MJ, Perou CM, Bernard PS (2009) Supervised risk predictor of breast cancer based on intrinsic subtypes. J Clin Oncol 27:1160-1167. doi:10.1200/JCO.2008.18.1370
3. Prat A, Parker JS, Karginova O, Fan C, Livasy C, Herschkowitz JI, He X, Perou CM (2010) Phenotypic and molecular characterization of the claudin-low intrinsic subtype of breast cancer. Breast Cancer Res 12:R68. doi:10.1186/bcr2635
4. Santagata S, Thakkar A, Ergonul A, Wang B, Woo T, Hu R, Harrell JC, McNamara G, Schwede M, Culhane AC, Kindelberger D, Rodig S, Richardson A, Schnitt SJ, Tamimi RM, Ince TA (2014) Taxonomy of breast cancer based on normal cell phenotype predicts outcome. J Clin Investig 124:859-870. doi:10.1172/JCI70941
5. Wang ZA, Mitrofanova A, Bergren SK, Abate-Shen C, Cardiff RD, Califano A, Shen MM (2013) Lineage analysis of basal epithelial cells reveals their unexpected plasticity and supports a cell-of-origin model for prostate cancer heterogeneity. Nat Cell Biol 15:274-283. doi:10.1038/ncb2697
6. Ince TA, Richardson AL, Bell GW, Saitoh M, Godar S, Karnoub AE, Iglehart JD, Weinberg RA (2007) Transformation of different human breast epithelial cell types leads to distinct tumor phenotypes. Cancer Cell 12:160-170. doi:10.1016/j.ccr.2007.06.013 (Pubitemid 47199120)
7. Smid M, Wang Y, Zhang Y, Sieuwerts AM, Yu J, Klijn JG, Foekens JA, Martens JW (2008) Subtypes of breast cancer show preferential site of relapse. Cancer Res 68:3108-3114. doi:10.1158/0008-5472.CAN-07-5644
8. Cancer Genome Atlas N (2012) Comprehensive molecular portraits of human breast tumours. Nature 490:61-70. doi:10.1038/nature11412
9. Ellis MJ, Perou CM (2013) The genomic landscape of breast cancer as a therapeutic roadmap. Cancer Discov 3:27-34. doi:10.1158/2159-8290.CD-12-0462
10. Metzger-Filho O, Sun Z, Viale G, Price KN, Crivellari D, Snyder RD, Gelber RD, Castiglione-Gertsch M, Coates AS, Goldhirsch A, Cardoso F (2013) Patterns of Recurrence and outcome according to breast cancer subtypes in lymph node-negative disease: results from international breast cancer study group trials VIII and IX. J Clin Oncol 31:3083-3090. doi:10.1200/JCO.2012.46.1574
11. Shah SP, Roth A, Goya R, Oloumi A, Ha G, Zhao Y, Turashvili G, Ding J, Tse K, Haffari G, Bashashati A, Prentice LM, Khattra J, Burleigh A, Yap D, Bernard V, McPherson A, Shumansky K, Crisan A, Giuliany R, Heravi-Moussavi A, Rosner J, Lai D, Birol I, Varhol R, Tam A, Dhalla N, Zeng T, Ma K, Chan SK, Griffith M, Moradian A, Cheng SW, Morin GB, Watson P, Gelmon K, Chia S, Chin SF, Curtis C, Rueda OM, Pharoah PD, Damaraju S, Mackey J, Hoon K, Harkins T, Tadigotla V, Sigaroudinia M, Gascard P, Tlsty T, Costello JF, Meyer IM, Eaves CJ, Wasserman WW, Jones S, Huntsman D, Hirst M, Caldas C, Marra MA, Aparicio S (2012) The clonal and mutational evolution spectrum of primary triple-negative breast cancers. Nature 486:395-399. doi:10.1038/nature10933
12. Van't Veer LJ, Dai H, van de Vijver MJ, He YD, Hart AA, Mao M, Peterse HL, van der Kooy K, Marton MJ, Witteveen AT, Schreiber GJ, Kerkhoven RM, Roberts C, Linsley PS, Bernards R, Friend SH (2002) Gene expression profiling predicts clinical outcome of breast cancer. Nature 415:530-536. doi:10.1038/415530a (Pubitemid 34130608)
13. Landemaine T, Jackson A, Bellahcene A, Rucci N, Sin S, Abad BM, Sierra A, Boudinet A, Guinebretiere JM, Ricevuto E, Nogues C, Briffod M, Bieche I, Cherel P, Garcia T, Castronovo V, Teti A, Lidereau R, Driouch K (2008) A six-gene signature predicting breast cancer lung metastasis. Cancer Res 68:6092-6099. doi:10.1158/0008-5472.CAN-08-0436
14. Minn AJ, Gupta GP, Siegel PM, Bos PD, Shu W, Giri DD, Viale A, Olshen AB, Gerald WL, Massague J (2005) Genes that mediate breast cancer metastasis to lung. Nature 436:518-524. doi:10.1038/nature03799 (Pubitemid 41112921)
15. Bos PD, Zhang XH, Nadal C, Shu W, Gomis RR, Nguyen DX, Minn AJ, van de Vijver MJ, Gerald WL, Foekens JA, Massague J (2009) Genes that mediate breast cancer metastasis to the brain. Nature 459:1005-1009. doi:10.1038/nature08021
16. Culhane AC, Quackenbush J (2009) Confounding effects in "A six-gene signature predicting breast cancer lung metastasis". Cancer Res 69:7480-7485. doi:10.1158/0008-5472.CAN-08-3350
17. Kennecke H, Yerushalmi R, Woods R, Cheang MC, Voduc D, Speers CH, Nielsen TO, Gelmon K (2010) Metastatic behavior of breast cancer subtypes. J Clin Oncol 28:3271-3277. doi:10.1200/JCO.2009.25.9820
18. Wang Y, Klijn JG, Zhang Y, Sieuwerts AM, Look MP, Yang F, Talantov D, Timmermans M, Meijer-van Gelder ME, Yu J, Jatkoe T, Berns EM, Atkins D, Foekens JA (2005) Gene-expression profiles to predict distant metastasis of lymph-node-negative primary breast cancer. Lancet 365:671-679. doi:10.1016/S0140-6736(05)17947-1 (Pubitemid 40260888)
19. Lehmann BD, Bauer JA, Chen X, Sanders ME, Chakravarthy AB, Shyr Y, Pietenpol JA (2011) Identification of human triple-negative breast cancer subtypes and preclinical models for selection of targeted therapies. J Clin Investig 121:2750-2767. doi:10.1172/JCI45014
20. Lim E, Vaillant F, Wu D, Forrest NC, Pal B, Hart AH, Asselin-Labat ML, Gyorki DE, Ward T, Partanen A, Feleppa F, Huschtscha LI, Thorne HJ, kConFab, Fox SB, Yan M, French JD, Brown MA, Smyth GK, Visvader JE, Lindeman GJ (2009) Aberrant luminal progenitors as the candidate target population for basal tumor development in BRCA1 mutation carriers. Nat Med 15:907-913. doi:10.1038/nm.2000
21. Taube JH, Herschkowitz JI, Komurov K, Zhou AY, Gupta S, Yang J, Hartwell K, Onder TT, Gupta PB, Evans KW, Hollier BG, Ram PT, Lander ES, Rosen JM, Weinberg RA, Mani SA (2010) Core epithelial-to-mesenchymal transition interactome gene-expression signature is associated with claudin-low and metaplastic breast cancer subtypes. Proc Natl Acad Sci USA 107:15449-15454. doi:10.1073/pnas.1004900107
22. Ringner M, Fredlund E, Hakkinen J, Borg A, Staaf J (2011) GOBO: gene expression-based outcome for breast cancer online. PLoS ONE 6:e17911. doi:10.1371/journal.pone.0017911
23. Gyorffy B, Lanczky A, Eklund AC, Denkert C, Budczies J, Li Q, Szallasi Z (2010) An online survival analysis tool to rapidly assess the effect of 22,277 genes on breast cancer prognosis using microarray data of 1,809 patients. Breast Cancer Res Treat 123:725-731. doi:10.1007/s10549-009-0674-9
24. Rusinova I, Forster S, Yu S, Kannan A, Masse M, Cumming H, Chapman R, Hertzog PJ (2013) Interferome v2.0: an updated database of annotated interferon-regulated genes. Nucleic Acids Res 41:D1040-D1046. doi:10.1093/nar/gks1215
25. Majmundar AJ, Wong WJ, Simon MC (2010) Hypoxia-inducible factors and the response to hypoxic stress. Mol Cell 40:294-309. doi:10.1016/j.molcel.2010.09. 022
26. Massague J (2012) TGFbeta signalling in context. Nat Rev Mol Cell Biol 13:616-630. doi:10.1038/nrm3434
27. Pencheva N, Tavazoie SF (2013) Control of metastatic progression by microRNA regulatory networks. Nat Cell Biol 15:546-554. doi:10.1038/ncb2769
28. Fan M, Krutilina R, Sun J, Sethuraman A, Yang CH, Wu ZH, Yue J, Pfeffer LM (2013) Comprehensive analysis of microRNA (miRNA) targets in breast cancer cells. J Biol Chem 288:27480-27493. doi:10.1074/jbc.M113.491803
29. Farazi TA, Horlings HM, Ten Hoeve JJ, Mihailovic A, Halfwerk H, Morozov P, Brown M, Hafner M, Reyal F, van Kouwenhove M, Kreike B, Sie D, Hovestadt V, Wessels LF, van de Vijver MJ, Tuschl T (2011) MicroRNA sequence and expression analysis in breast tumors by deep sequencing. Cancer Res 71:4443-4453. doi:10.1158/0008-5472.CAN-11-0608
30. Park SM, Gaur AB, Lengyel E, Peter ME (2008) The miR-200 family determines the epithelial phenotype of cancer cells by targeting the E-cadherin repressors ZEB1 and ZEB2. Genes Dev 22:894-907. doi:10.1101/gad.1640608 (Pubitemid 351482843)
31. Li XL, Hara T, Choi Y, Subramanian M, Francis P, Bilke S, Walker RL, Pineda M, Zhu Y, Yang Y, Luo J, Wakefield LM, Brabletz T, Park BH, Sharma S, Chowdhury D, Meltzer PS, Lal A (2014) A p21-ZEB1 complex inhibits epithelial-mesenchymal transition through the microRNA 183-96-182 cluster. Mol Cell Biol 34:533-550. doi:10.1128/MCB.01043-13
32. Dews M, Fox JL, Hultine S, Sundaram P, Wang W, Liu YY, Furth E, Enders GH, El-Deiry W, Schelter JM, Cleary MA, Thomas-Tikhonenko A (2010) The myc-miR-17-92 axis blunts TGF{beta} signaling and production of multiple TGF{beta}-dependent antiangiogenic factors. Cancer Res 70:8233-8246. doi:10.1158/0008-5472.CAN-10-2412
33. Vanharanta S, Massague J (2013) Hypoxia signaling-license to metastasize. Cancer Discov 3:1103-1104. doi:10.1158/2159-8290.CD-13-0481
34. Liberzon A, Subramanian A, Pinchback R, Thorvaldsdottir H, Tamayo P, Mesirov JP (2011) Molecular signatures database (MsigDB) 3.0. Bioinformatics 27:1739-1740. doi:10.1093/bioinformatis/btr260
35. Nieto MA (2013) Epithelial plasticity: a common theme in embryonic and cancer cells. Science 342:1234850. doi:10.1126/science.1234850
36. Lu X, Kang Y (2010) Hypoxia and hypoxia-inducible factors: master regulators of metastasis. Clin Cancer Res 16:5928-5935. doi:10.1158/1078-0432. CCR-10-1360
37. Luga V, Wrana JL (2013) Tumor-stroma interaction: revealing fibroblast-secreted exosomes as potent regulators of Wnt-planar cell polarity signaling in cancer metastasis. Cancer Res 73:6843-6847. doi:10.1158/0008-5472. CAN-13-1791
38. Macheda ML, Sun WW, Kugathasan K, Hogan BM, Bower NI, Halford MM, Zhang YF, Jacques BE, Lieschke GJ, Dabdoub A, Stacker SA (2012) The Wnt receptor Ryk plays a role in mammalian planar cell polarity signaling. J Biol Chem 287:29312-29323. doi:10.1074/jbc.M112.362681
39. Wang Y (2009) Wnt/Planar cell polarity signaling: a new paradigm for cancer therapy. Mol Cancer Ther 8:2103-2109. doi:10.1158/1535-7163.MCT-09-0282
40. Green J, Nusse R, van Amerongen R (2014) The role of ryk and ror receptor tyrosine kinases in wnt signal transduction. Cold Spring Harbor perspectives in biology, vol 6. doi:10.1101/cshperspect.a009175
41. Zhang P, Cai Y, Soofi A, Dressler GR (2012) Activation of Wnt11 by transforming growth factor-beta drives mesenchymal gene expression through non-canonical Wnt protein signaling in renal epithelial cells. J Biol Chem 287:21290-21302. doi:10.1074/jbc.M112.357202
42. Fox JL, Dews M, Minn AJ, Thomas-Tikhonenko A (2013) Targeting of TGFbeta signature and its essential component CTGF by miR-18 correlates with improved survival in glioblastoma. RNA 19:177-190. doi:10.1261/rna.036467.112
43. Yu Z, Willmarth NE, Zhou J, Katiyar S, Wang M, Liu Y, McCue PA, Quong AA, Lisanti MP, Pestell RG (2010) microRNA 17/20 inhibits cellular invasion and tumor metastasis in breast cancer by heterotypic signaling. Proc Natl Acad Sci USA 107:8231-8236. doi:10.1073/pnas.1002080107
44. Mu P, Han YC, Betel D, Yao E, Squatrito M, Ogrodowski P, de Stanchina E, D'Andrea A, Sander C, Ventura A (2009) Genetic dissection of the miR-17-92 cluster of microRNAs in Myc-induced B-cell lymphomas. Genes Dev 23:2806-2811. doi:10.1101/gad.1872909
45. Becker LE, Lu Z, Chen W, Xiong W, Kong M, Li Y (2012) A systematic screen reveals MicroRNA clusters that significantly regulate four major signaling pathways. PLoS ONE 7:e48474. doi:10.1371/journal.pone.0048474
46. Jin HY, Oda H, Lai M, Skalsky RL, Bethel K, Shepherd J, Kang SG, Liu WH, Sabouri-Ghomi M, Cullen BR, Rajewsky K, Xiao C (2013) MicroRNA-17-92 plays a causative role in lymphomagenesis by coordinating multiple oncogenic pathways. EMBO J 32:2377-2391. doi:10.1038/emboj.2013.178
47. Nie Z, Hu G, Wei G, Cui K, Yamane A, Resch W, Wang R, Green DR, Tessarollo L, Casellas R, Zhao K, Levens D (2012) c-Myc is a universal amplifier of expressed genes in lymphocytes and embryonic stem cells. Cell 151:68-79. doi:10.1016/j.cell.2012.08.033
48. Alfano D, Votta G, Schulze A, Downward J, Caputi M, Stoppelli MP, Iaccarino I (2010) Modulation of cellular migration and survival by c-Myc through the downregulation of urokinase (uPA) and uPA receptor. Mol Cell Biol 30:1838-1851. doi:10.1128/MCB.01442-09
49. Liu H, Radisky DC, Yang D, Xu R, Radisky ES, Bissell MJ, Bishop JM (2012) MYC suppresses cancer metastasis by direct transcriptional silencing of alphav and beta3 integrin subunits. Nat Cell Biol 14:567-574. doi:10.1038/ncb2491
50. Desmedt C, Haibe-Kains B, Wirapati P, Buyse M, Larsimont D, Bontempi G, Delorenzi M, Piccart M, Sotiriou C (2008) Biological processes associated with breast cancer clinical outcome depend on the molecular subtypes. Clin Cancer Res 14:5158-5165. doi:10.1158/1078-0432.CCR-07-4756
51. Teschendorff AE, Miremadi A, Pinder SE, Ellis IO, Caldas C (2007) An immune response gene expression module identifies a good prognosis subtype in estrogen receptor negative breast cancer. Genome Biol 8:R157. doi:10.1186/gb-2007-8-8-r157
52. Bidwell BN, Slaney CY, Withana NP, Forster S, Cao Y, Loi S, Andrews D, Mikeska T, Mangan NE, Samarajiwa SA, de Weerd NA, Gould J, Argani P, Moller A, Smyth MJ, Anderson RL, Hertzog PJ, Parker BS (2012) Silencing of Irf7 pathways in breast cancer cells promotes bone metastasis through immune escape. Nat Med 18:1224-1231. doi:10.1038/nm.2830
53. Schneider CA, Rasband WS, Eliceiri KW (2012) NIH Image to ImageJ: 25 years of image analysis. Nat Methods 9:671-675
54. Spandidos A, Wang X, Wang H, Seed B (2010) PrimerBank: a resource of human and mouse PCR primer pairs for gene expression detection and quantification. Nucleic Acids Res 38:D792-D799. doi:10.1093/nar/gkp1005
55. Reczko M, Maragkakis M, Alexiou P, Grosse I, Hatzigeorgiou AG (2012) Functional microRNA targets in protein coding sequences. Bioinformatics 28:771-776. doi:10.1093/bioinformatics/bts043
56. Wang X, El Naqa IM (2008) Prediction of both conserved and nonconserved microRNA targets in animals. Bioinformatics 24:325-332. doi:10.1093/ bioinformatics/btm595 (Pubitemid 351189007)