MSC-regulated microRNAs converge on the transcription factor FOXP2 and promote breast cancer metastasis

Cell Stem Cell

Volumn 15, Issue 6, 2014, Pages 762-774

  Cuiffo, Benjamin G ^a   Campagne, Antoine ^a,b   Bell, George W ^c   Lembo, Antonio ^d   Orso, Francesca ^d   Lien, Evan C ^a   Bhasin, Manoj K ^a   Raimo, Monica ^d   Hanson, Summer E ^e   Marusyk, Andriy ^a,f   El Ashry, Dorraya ^g   Hematti, Peiman ^e   Polyak, Kornelia ^a,f   Mechta Grigoriou, Fatima ^b   Mariani, Odette ^b   Volinia, Stefano ^h   Vincent Salomon, Anne ^b   Taverna, Daniela ^d   Karnoub, Antoine E ^a,i,j  

^a HARVARD MEDICAL SCHOOL   (United States)

^b INSTITUT CURIE   (France)

^c WHITEHEAD INSTITUTE FOR BIOMEDICAL RESEARCH   (United States)

^d UNIVERSITY OF TURIN   (Italy)

^e UNIVERSITY OF WISCONSIN   (United States)

^f DANA FARBER CANCER INSTITUTE   (United States)

^g UNIVERSITY OF MIAMI   (United States)

^h UNIVERSITY OF FERRARA   (Italy)

ⁱ HARVARD STEM CELL INSTITUTE   (United States)

^j BROAD INSTITUTE OF MIT AND HARVARD   (United States)

more..

Author keywords

[No Author keywords available]

Indexed keywords

CD24 ANTIGEN; HERMES ANTIGEN; MESSENGER RNA; MICRORNA; MICRORNA 1915; MICRORNA 199A; MICRORNA 214; MICRORNA 34A; MICRORNA 762; NERVE CELL ADHESION MOLECULE; PROTEIN LYSINE 6 OXIDASE; SMOOTH MUSCLE ACTIN; TRANSCRIPTION FACTOR FOXP2; TRANSCRIPTION FACTOR GATA 6; UNCLASSIFIED DRUG; UVOMORULIN; VIMENTIN; FORKHEAD TRANSCRIPTION FACTOR; FOXP2 PROTEIN, HUMAN; MIRN199 MICRORNA, HUMAN; TUMOR MARKER;

ARTICLE; BONE MARROW DERIVED MESENCHYMAL STEM CELL; BREAST METASTASIS; CANCER GROWTH; CANCER PROGNOSIS; CANCER STEM CELL; CANCER SURVIVAL; CELL DEATH; CELL DIFFERENTIATION; CONTROLLED STUDY; DISEASE FREE SURVIVAL; DOWN REGULATION; EMBRYO; FEMALE; GENE EXPRESSION; HUMAN; HUMAN TISSUE; LANGUAGE DEVELOPMENT; MESENCHYMAL STROMA CELL; MOUSE; NONHUMAN; NUCLEOTIDE SEQUENCE; PHENOTYPE; SPEECH DEVELOPMENT; TRANSIENT EXPRESSION; UPREGULATION; BREAST NEOPLASMS; CARCINOGENESIS; GENE EXPRESSION REGULATION; GENETICS; METABOLISM; METASTASIS; MORTALITY; PATHOLOGY; PHYSIOLOGY; PROGNOSIS; SPEECH; SURVIVAL; TUMOR CELL LINE;

BREAST NEOPLASMS; CARCINOGENESIS; CELL LINE, TUMOR; FEMALE; FORKHEAD TRANSCRIPTION FACTORS; GENE EXPRESSION REGULATION, NEOPLASTIC; HUMANS; MESENCHYMAL STROMAL CELLS; MICRORNAS; NEOPLASM METASTASIS; NEOPLASTIC STEM CELLS; PROGNOSIS; SPEECH; SURVIVAL ANALYSIS; TUMOR MARKERS, BIOLOGICAL;

EID: 84919442262     PISSN: 19345909     EISSN: 18759777     Source Type: Journal    
DOI: 10.1016/j.stem.2014.10.001     Document Type: Article

References (65)

1. M.H. Barcellos-Hoff, D. Lyden, and T.C. Wang The evolution of the cancer niche during multistage carcinogenesis Nat. Rev. Cancer 13 2013 511 518
2. D.P. Bartel MicroRNAs: target recognition and regulatory functions Cell 136 2009 215 233
3. V.L. Battula, Y. Shi, K.W. Evans, R.Y. Wang, E.L. Spaeth, R.O. Jacamo, R. Guerra, A.A. Sahin, F.C. Marini, and G. Hortobagyi Ganglioside GD2 identifies breast cancer stem cells and promotes tumorigenesis J. Clin. Invest. 122 2012 2066 2078
4. C.L. Bockmeyer, M. Christgen, M. Müller, S. Fischer, P. Ahrens, F. Länger, 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
5. B. Brenner, M.B. Hoshen, O. Purim, M.B. David, K. Ashkenazi, G. Marshak, Y. Kundel, R. Brenner, S. Morgenstern, and M. Halpern MicroRNAs as a potential prognostic factor in gastric cancer World J. Gastroenterol. 17 2011 3976 3985
6. Cancer Genome Atlas Network Comprehensive molecular portraits of human breast tumours Nature 490 2012 61 70
7. P. Chaturvedi, D.M. Gilkes, C.C. Wong, Kshitiz, W. Luo, H. Zhang, H. Wei, N. Takano, L. Schito, A. Levchenko, and G.L. Semenza Hypoxia-inducible factor-dependent breast cancer-mesenchymal stem cell bidirectional signaling promotes metastasis J. Clin. Invest. 123 2013 189 205
8. D.T. Chen, A. Nasir, A. Culhane, C. Venkataramu, W. Fulp, R. Rubio, T. Wang, D. Agrawal, S.M. McCarthy, and M. Gruidl Proliferative genes dominate malignancy-risk gene signature in histologically-normal breast tissue Breast Cancer Res. Treat. 119 2010 335 346
9. D. Cimino, C. De Pitta, F. Orso, M. Zampini, S. Casara, E. Penna, E. Quaglino, M. Forni, C. Damasco, and E. Pinatel miR148b is a major coordinator of breast cancer progression in a relapse-associated microRNA signature by targeting ITGA5, ROCK1, PIK3CA, NRAS, and CSF1 FASEB J 27 2013 1223 1235
10. B.G. Cuiffo, and A.E. Karnoub Mesenchymal stem cells in tumor development: emerging roles and concepts Cell Adhes. Migr. 6 2012 220 230
11. S. Dedeurwaerder, C. Desmedt, E. Calonne, S.K. Singhal, B. Haibe-Kains, M. Defrance, S. Michiels, M. Volkmar, R. Deplus, and J. Luciani DNA methylation profiling reveals a predominant immune component in breast cancers EMBO Mol Med 3 2011 726 741
12. J. Dorado, E. Lonardo, I. Miranda-Lorenzo, and C. Heeschen Pancreatic cancer stem cells: new insights and perspectives J. Gastroenterol. 46 2011 966 973
13. K. Drews-Elger, J.A. Brinkman, P. Miller, S.H. Shah, J.C. Harrell, T.G. da Silva, Z. Ao, A. Schlater, D.J. Azzam, and K. Diehl Primary breast tumor-derived cellular models: characterization of tumorigenic, metastatic, and cancer-associated fibroblasts in dissociated tumor (DT) cultures Breast Cancer Res. Treat. 144 2014 503 517
14. C.P. El-Haibi, G.W. Bell, J. Zhang, A.Y. Collmann, D. Wood, C.M. Scherber, E. Csizmadia, O. Mariani, C. Zhu, and A. Campagne Critical role for lysyl oxidase in mesenchymal stem cell-driven breast cancer malignancy Proc. Natl. Acad. Sci. USA 109 2012 17460 17465
15. T.A. Farazi, H.M. Horlings, J.J. Ten Hoeve, A. Mihailovic, H. Halfwerk, P. Morozov, M. Brown, M. Hafner, F. Reyal, and M. van Kouwenhove MicroRNA sequence and expression analysis in breast tumors by deep sequencing Cancer Res. 71 2011 4443 4453
16. A. Feber, L. Xi, A. Pennathur, W.E. Gooding, S. Bandla, M. Wu, J.D. Luketich, T.E. Godfrey, and V.R. Litle MicroRNA prognostic signature for nodal metastases and survival in esophageal adenocarcinoma Ann. Thorac. Surg. 91 2011 1523 1530
17. S.E. Fisher, and C. Scharff FOXP2 as a molecular window into speech and language Trends Genet. 25 2009 166 177
18. C. Ginestier, M.H. Hur, E. Charafe-Jauffret, F. Monville, J. Dutcher, M. Brown, J. Jacquemier, P. Viens, C.G. Kleer, and S. Liu ALDH1 is a marker of normal and malignant human mammary stem cells and a predictor of poor clinical outcome Cell Stem Cell 1 2007 555 567
19. R.H. Goldstein, M.R. Reagan, K. Anderson, D.L. Kaplan, and M. Rosenblatt Human bone marrow-derived MSCs can home to orthotopic breast cancer tumors and promote bone metastasis Cancer Res. 70 2010 10044 10050
20. S.E. Hanson, J. Kim, and P. Hematti Comparative analysis of adipose-derived mesenchymal stem cells isolated from abdominal and breast tissue Aesthet. Surg. J. 33 2013 888 898
21. Y. Hu, and G.K. Smyth ELDA: extreme limiting dilution analysis for comparing depleted and enriched populations in stem cell and other assays J. Immunol. Methods 347 2009 70 78
22. M. Hu, J. Yao, D.K. Carroll, S. Weremowicz, H. Chen, D. Carrasco, A. Richardson, S. Violette, T. Nikolskaya, and Y. Nikolsky Regulation of in situ to invasive breast carcinoma transition Cancer Cell 13 2008 394 406
23. M.V. Iorio, R. Visone, G. Di Leva, V. Donati, F. Petrocca, P. Casalini, C. Taccioli, S. Volinia, C.G. Liu, and H. Alder MicroRNA signatures in human ovarian cancer Cancer Res. 67 2007 8699 8707
24. Y. Jung, J.K. Kim, Y. Shiozawa, J. Wang, A. Mishra, J. Joseph, J.E. Berry, S. McGee, E. Lee, and H. Sun Recruitment of mesenchymal stem cells into prostate tumours promotes metastasis Nat Commun 4 2013 1795
25. A.E. Karnoub, A.B. Dash, A.P. Vo, A. Sullivan, M.W. Brooks, G.W. Bell, A.L. Richardson, K. Polyak, R. Tubo, and R.A. Weinberg Mesenchymal stem cells within tumour stroma promote breast cancer metastasis Nature 449 2007 557 563
26. G. Konopka, J.M. Bomar, K. Winden, G. Coppola, Z.O. Jonsson, F. Gao, S. Peng, T.M. Preuss, J.A. Wohlschlegel, and D.H. Geschwind Human-specific transcriptional regulation of CNS development genes by FOXP2 Nature 462 2009 213 217
27. S. Li, J. Weidenfeld, and E.E. Morrisey Transcriptional and DNA binding activity of the Foxp1/2/4 family is modulated by heterotypic and homotypic protein interactions Mol. Cell. Biol. 24 2004 809 822
28. M. Liu, M.C. Casimiro, C. Wang, L.A. Shirley, X. Jiao, S. Katiyar, X. Ju, Z. Li, Z. Yu, and J. Zhou p21CIP1 attenuates Ras- and c-Myc-dependent breast tumor epithelial mesenchymal transition and cancer stem cell-like gene expression in vivo Proc. Natl. Acad. Sci. USA 106 2009 19035 19039
29. S. Liu, C. Ginestier, S.J. Ou, S.G. Clouthier, S.H. Patel, F. Monville, H. Korkaya, A. Heath, J. Dutcher, and C.G. Kleer Breast cancer stem cells are regulated by mesenchymal stem cells through cytokine networks Cancer Res. 71 2011 614 624
30. L. Ma, J. Teruya-Feldstein, and R.A. Weinberg Tumour invasion and metastasis initiated by microRNA-10b in breast cancer Nature 449 2007 682 688
31. I. Malanchi, A. Santamaria-Martínez, E. Susanto, H. Peng, H.A. Lehr, J.F. Delaloye, and J. Huelsken Interactions between cancer stem cells and their niche govern metastatic colonization Nature 481 2012 85 89
32. C. Mascaux, J.F. Laes, G. Anthoine, A. Haller, V. Ninane, A. Burny, and J.P. Sculier Evolution of microRNA expression during human bronchial squamous carcinogenesis Eur. Respir. J. 33 2009 352 359
33. K. McLean, Y. Gong, Y. Choi, N. Deng, K. Yang, S. Bai, L. Cabrera, E. Keller, L. McCauley, K.R. Cho, and R.J. Buckanovich Human ovarian carcinoma-associated mesenchymal stem cells regulate cancer stem cells and tumorigenesis via altered BMP production J. Clin. Invest. 121 2011 3206 3219
34. L.D. Miller, J. Smeds, J. George, V.B. Vega, L. Vergara, A. Ploner, Y. Pawitan, P. Hall, S. Klaar, E.T. Liu, and J. Bergh An expression signature for p53 status in human breast cancer predicts mutation status, transcriptional effects, and patient survival Proc. Natl. Acad. Sci. USA 102 2005 13550 13555
35. N. Miyoshi, H. Ishii, H. Nagano, N. Haraguchi, D.L. Dewi, Y. Kano, S. Nishikawa, M. Tanemura, K. Mimori, and F. Tanaka Reprogramming of mouse and human cells to pluripotency using mature microRNAs Cell Stem Cell 8 2011 633 638
36. S.S. Myatt, and E.W. Lam The emerging roles of forkhead box (Fox) proteins in cancer Nat. Rev. Cancer 7 2007 847 859
37. R. Nair, D.L. Roden, W.S. Teo, A. McFarland, S. Junankar, S. Ye, A. Nguyen, J. Yang, I. Nikolic, and M. Hui c-Myc and Her2 cooperate to drive a stem-like phenotype with poor prognosis in breast cancer Oncogene 33 2014 3992 4002
38. O.K. Okamoto, S.M. Oba-Shinjo, L. Lopes, and S.K. Nagahashi Marie Expression of HOXC9 and E2F2 are up-regulated in CD133(+) cells isolated from human astrocytomas and associate with transformation of human astrocytes Biochim. Biophys. Acta 1769 2007 437 442
39. Y. Pawitan, J. Bjöhle, L. Amler, A.L. Borg, S. Egyhazi, P. Hall, X. Han, L. Holmberg, F. Huang, and S. Klaar Gene expression profiling spares early breast cancer patients from adjuvant therapy: derived and validated in two population-based cohorts Breast Cancer Res. 7 2005 R953 R964
40. N. Pencheva, H. Tran, C. Buss, D. Huh, M. Drobnjak, K. Busam, and S.F. Tavazoie Convergent multi-miRNA targeting of ApoE drives LRP1/LRP8-dependent melanoma metastasis and angiogenesis Cell 151 2012 1068 1082
41. 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
42. L. Prantl, F. Muehlberg, N.M. Navone, Y.H. Song, J. Vykoukal, C.J. Logothetis, and E.U. Alt Adipose tissue-derived stem cells promote prostate tumor growth Prostate 70 2010 1709 1715
43. D.J. Prockop, D.J. Kota, N. Bazhanov, and R.L. Reger Evolving paradigms for repair of tissues by adult stem/progenitor cells (MSCs) J. Cell. Mol. Med. 14 2010 2190 2199
44. D.F. Quail, and J.A. Joyce Microenvironmental regulation of tumor progression and metastasis Nat. Med. 19 2013 1423 1437
45. R. Sabatier, P. Finetti, N. Cervera, E. Lambaudie, B. Esterni, E. Mamessier, A. Tallet, C. Chabannon, J.M. Extra, and J. Jacquemier A gene expression signature identifies two prognostic subgroups of basal breast cancer Breast Cancer Res. Treat. 126 2011 407 420
46. K. Sakurai, C. Furukawa, T. Haraguchi, K. Inada, K. Shiogama, T. Tagawa, S. Fujita, Y. Ueno, A. Ogata, and M. Ito MicroRNAs miR-199a-5p and -3p target the Brm subunit of SWI/SNF to generate a double-negative feedback loop in a variety of human cancers Cancer Res. 71 2011 1680 1689
47. L. Scapoli, A. Palmieri, L. Lo Muzio, F. Pezzetti, C. Rubini, A. Girardi, F. Farinella, M. Mazzotta, and F. Carinci MicroRNA expression profiling of oral carcinoma identifies new markers of tumor progression Int. J. Immunopathol. Pharmacol. 23 2010 1229 1234
48. H. Schwarzenbach, K. Milde-Langosch, B. Steinbach, V. Müller, and K. Pantel Diagnostic potential of PTEN-targeting miR-214 in the blood of breast cancer patients Breast Cancer Res. Treat. 134 2012 933 941
49. K. Shinagawa, Y. Kitadai, M. Tanaka, T. Sumida, M. Kodama, Y. Higashi, S. Tanaka, W. Yasui, and K. Chayama Mesenchymal stem cells enhance growth and metastasis of colon cancer Int. J. Cancer 127 2010 2323 2333
50. W. Shu, H. Yang, L. Zhang, M.M. Lu, and E.E. Morrisey Characterization of a new subfamily of winged-helix/forkhead (Fox) genes that are expressed in the lung and act as transcriptional repressors J. Biol. Chem. 276 2001 27488 27497
51. W. Shu, M.M. Lu, Y. Zhang, P.W. Tucker, D. Zhou, and E.E. Morrisey Foxp2 and Foxp1 cooperatively regulate lung and esophagus development Development 134 2007 1991 2000
52. E. Spiteri, G. Konopka, G. Coppola, J. Bomar, M. Oldham, J. Ou, S.C. Vernes, S.E. Fisher, B. Ren, and D.H. Geschwind Identification of the transcriptional targets of FOXP2, a gene linked to speech and language, in developing human brain Am. J. Hum. Genet. 81 2007 1144 1157
53. K. Suzuki, R. Sun, M. Origuchi, M. Kanehira, T. Takahata, J. Itoh, A. Umezawa, H. Kijima, S. Fukuda, and Y. Saijo Mesenchymal stromal cells promote tumor growth through the enhancement of neovascularization Mol. Med. 17 2011 579 587
54. S.F. Tavazoie, C. Alarcón, T. Oskarsson, D. Padua, Q. Wang, P.D. Bos, W.L. Gerald, and J. Massagué Endogenous human microRNAs that suppress breast cancer metastasis Nature 451 2008 147 152
55. A. Toullec, D. Gerald, G. Despouy, B. Bourachot, M. Cardon, S. Lefort, M. Richardson, G. Rigaill, M.C. Parrini, and C. Lucchesi Oxidative stress promotes myofibroblast differentiation and tumour spreading EMBO Mol Med 2 2010 211 230
56. D. Tsui, J.P. Vessey, H. Tomita, D.R. Kaplan, and F.D. Miller FoxP2 regulates neurogenesis during embryonic cortical development J. Neurosci. 33 2013 244 258
57. M.J. van de Vijver, Y.D. He, L.J. van't Veer, H. Dai, A.A. Hart, D.W. Voskuil, G.J. Schreiber, J.L. Peterse, and C. Roberts A gene-expression signature as a predictor of survival in breast cancer N. Engl. J. Med. 347 2002 1999 2009
58. S.C. Vernes, P.L. Oliver, E. Spiteri, H.E. Lockstone, R. Puliyadi, J.M. Taylor, J. Ho, C. Mombereau, A. Brewer, and E. Lowy Foxp2 regulates gene networks implicated in neurite outgrowth in the developing brain PLoS Genet. 7 2011 e1002145
59. S. Volinia, M. Galasso, M.E. Sana, T.F. Wise, J. Palatini, K. Huebner, and C.M. Croce Breast cancer signatures for invasiveness and prognosis defined by deep sequencing of microRNA Proc. Natl. Acad. Sci. USA 109 2012 3024 3029
60. D. Wan, S. He, B. Xie, G. Xu, W. Gu, C. Shen, Y. Hu, X. Wang, Q. Zhi, and L. Wang Aberrant expression of miR-199a-3p and its clinical significance in colorectal cancers Med. Oncol. 30 2013 378
61. X.L. Yan, C.J. Fu, L. Chen, J.H. Qin, Q. Zeng, H.F. Yuan, X. Nan, H.X. Chen, J.N. Zhou, and Y.L. Lin Mesenchymal stem cells from primary breast cancer tissue promote cancer proliferation and enhance mammosphere formation partially via EGF/EGFR/Akt pathway Breast Cancer Res. Treat. 132 2012 153 164
62. H. Yang, W. Kong, L. He, J.J. Zhao, J.D. O'Donnell, J. Wang, R.M. Wenham, D. Coppola, P.A. Kruk, S.V. Nicosia, and J.Q. Cheng MicroRNA expression profiling in human ovarian cancer: miR-214 induces cell survival and cisplatin resistance by targeting PTEN Cancer Res. 68 2008 425 433
63. Y. Zhang, A.M. Goss, E.D. Cohen, R. Kadzik, J.J. Lepore, K. Muthukumaraswamy, J. Yang, F.J. DeMayo, J.A. Whitsett, M.S. Parmacek, and E.E. Morrisey A Gata6-Wnt pathway required for epithelial stem cell development and airway regeneration Nat. Genet. 40 2008 862 870
64. X.J. Zhang, H. Ye, C.W. Zeng, B. He, H. Zhang, and Y.Q. Chen Dysregulation of miR-15a and miR-214 in human pancreatic cancer J Hematol Oncol 3 2010 46
65. J. Zhou, S.B. Ng, and W.J. Chng LIN28/LIN28B: an emerging oncogenic driver in cancer stem cells Int. J. Biochem. Cell Biol. 45 2013 973 978