MiR-155-mediated loss of C/EBPβ shifts the TGF-β response from growth inhibition to epithelial-mesenchymal transition, invasion and metastasis in breast cancer

Oncogene

Volumn 32, Issue 50, 2013, Pages 5614-5624

  Johansson, J ^a   Berg, T ^a   Kurzejamska, E ^a,b   Pang, M F ^a   Tabor, V ^a   Jansson, M ^c   Roswall, P ^a   Pietras, K ^a,d   Sund, M ^c   Religa, P ^a   Fuxe, J ^a  

^a KAROLINSKA INSTITUTE   (Sweden)

^b MEDICAL UNIVERSITY OF WARSAW   (Poland)

^c UMEÅ UNIVERSITY   (Sweden)

^d LUND UNIVERSITY   (Sweden)

Author keywords

Breast cancer; CCAAT enhancer binding protein beta; epithelial mesenchymal transition; metastasis; transforming growth factor beta

Indexed keywords

CCAAT ENHANCER BINDING PROTEIN BETA; COXSACKIE VIRUS AND ADENOVIRUS RECEPTOR; MICRORNA 155; TRANSFORMING GROWTH FACTOR BETA; UVOMORULIN;

ARTICLE; BREAST CANCER; BREAST EPITHELIUM; BREAST TUMOR; CANCER GROWTH; EPITHELIAL MESENCHYMAL TRANSITION; GROWTH INHIBITION; HUMAN; HUMAN CELL; METASTASIS; PRIORITY JOURNAL; PROMOTER REGION; TUMOR INVASION;

ADENOVIRIDAE; COXSACKIEVIRUS; MOUSE MAMMARY TUMOR VIRUS; MUS;

EID: 84890572219     PISSN: 09509232     EISSN: 14765594     Source Type: Journal    
DOI: 10.1038/onc.2013.322     Document Type: Article

References (46)

1. Hanahan D, Weinberg RA. The hallmarks of cancer. Cell 2000; 100: 57-70.
2. Bierie B, Moses HL. Tumour microenvironment: TGFbeta: The molecular Jekyll and Hyde of cancer. Nat Rev Cancer 2006; 6: 506-520.
3. Heldin CH, Landstrom M, Moustakas A. Mechanism of TGF-beta signaling to growth arrest, apoptosis, and epithelial-mesenchymal transition. Curr Opin Cell Biol 2009; 21: 166-176.
4. Massague J. TGFbeta in cancer. Cell 2008; 134: 215-230.
5. Kalluri R, Weinberg RA. The basics of epithelial-mesenchymal transition. J Clin Invest 2009; 119: 1420-1428.
6. Thiery JP, Acloque H, Huang RY, Nieto MA. Epithelial-mesenchymal transitions in development and disease. Cell 2009; 139: 871-890.
7. Blick T, Widodo E, Hugo H, Waltham M, Lenburg ME, Neve RM et al. Epithelial mesenchymal transition traits in human breast cancer cell lines. Clin Exp Metastasis 2008; 25: 629-642.
8. Jeong H, Ryu YJ, An J, Lee Y, Kim A. Epithelial-mesenchymal transition in breast cancer correlates with high histological grade and triple-negative phenotype. Histopathology 2012; 60: E87-E95.
9. Mani SA, Guo W, Liao MJ, Eaton EN, Ayyanan A, Zhou AY et al. The epithelialmesenchymal transition generates cells with properties of stem cells. Cell 2008; 133: 704-715.
10. Fuxe J, Vincent T, De Herreros AG. Transcriptional crosstalk between TGFbeta and stem cell pathways in tumor cell invasion: role of EMT promoting Smad complexes. Cell Cycle 2010; 9: 2363-2374.
11. Vincent T, Neve EP, Johnson JR, Kukalev A, Rojo F, Albanell J et al. A SNAIL1- SMAD3/4 transcriptional repressor complex promotes TGF-beta mediated epithelial-mesenchymal transition. Nat Cell Biol 2009; 11: 943-950.
12. Xu J, Lamouille S, Derynck R. TGF-beta-induced epithelial to mesenchymal transition. Cell Res 2009; 19: 156-172.
13. Gomis RR, Alarcon C, He W, Wang Q, Seoane J, Lash A et al. A FoxO-Smad synexpression group in human keratinocytes. Proc Natl Acad Sci USA 2006; 103: 12747-12752.
14. Seoane J, Le HV, Shen L, Anderson SA, Massague J. Integration of Smad and forkhead pathways in the control of neuroepithelial and glioblastoma cell proliferation. Cell 2004; 117: 211-223.
15. Chen CR, Kang Y, Siegel PM, Massague J. E2F4/5 and p107 as Smad cofactors linking the TGFbeta receptor to c-myc repression. Cell 2002; 110: 19-32.
16. Frederick JP, Liberati NT, Waddell DS, Shi Y, Wang XF. Transforming growth factor beta-mediated transcriptional repression of c-myc is dependent on direct binding of Smad3 to a novel repressive Smad binding element. Mol Cell Biol 2004; 24: 2546-2559.
17. Kang Y, Chen CR, Massague J. A self-enabling TGFbeta response coupled to stress signaling: Smad engages stress response factor ATF3 for Id1 repression in epithelial cells. Mol Cell 2003; 11: 915-926.
18. Gomis RR, Alarcon C, Nadal C, Van Poznak C, Massague J. C/EBPbeta at the core of the TGFbeta cytostatic response and its evasion in metastatic breast cancer cells. Cancer Cell 2006; 10: 203-214.
19. Arnal-Estape A, Tarragona M, Morales M, Guiu M, Nadal C, Massague J et al. HER2 silences tumor suppression in breast cancer cells by switching expression of C/EBPss isoforms. Cancer Res 2010; 70: 9927-9936.
20. Robinson GW, Johnson PF, Hennighausen L, Sterneck E. The C/EBPbeta transcription factor regulates epithelial cell proliferation and differentiation in the mammary gland. Genes Dev 1998; 12: 1907-1916.
21. Seagroves TN, Krnacik S, Raught B, Gay J, Burgess-Beusse B, Darlington GJ et al. C/EBPbeta, but not C/EBPalpha, is essential for ductal morphogenesis, lobuloalveolar proliferation, and functional differentiation in the mouse mammary gland. Genes Dev 1998; 12: 1917-1928.
22. Zahnow CA. CCAAT/enhancer-binding protein beta: its role in breast cancer and associations with receptor tyrosine kinases. Expert Rev Mol Med 2009; 11: e12.
23. Sebastian T, Malik R, Thomas S, Sage J, Johnson PF. C/EBPbeta cooperates with RB:E2F to implement Ras(V12)-induced cellular senescence. EMBO J 2005; 24: 3301-3312.
24. Zahnow CA, Cardiff RD, Laucirica R, Medina D, Rosen JM. A role for CCAAT/ enhancer binding protein beta-liver-enriched inhibitory protein in mammary epithelial cell proliferation. Cancer Res 2001; 61: 261-269.
25. Bundy LM, Sealy L. CCAAT/enhancer binding protein beta (C/EBPbeta)-2 transforms normal mammary epithelial cells and induces epithelial to mesenchymal transition in culture. Oncogene 2003; 22: 869-883.
26. Muraoka RS, Dumont N, Ritter CA, Dugger TC, Brantley DM, Chen J et al. Blockade of TGF-beta inhibits mammary tumor cell viability, migration, and metastases. J Clin Invest 2002; 109: 1551-1559.
27. Brown KA, Aakre ME, Gorska AE, Price JO, Eltom SE, Pietenpol JA et al. Induction by transforming growth factor-beta1 of epithelial to mesenchymal transition is a rare event in vitro. Breast Cancer Res 2004; 6: R215-R231.
28. Oft M, Peli J, Rudaz C, Schwarz H, Beug H, Reichmann E. TGF-beta1 and Ha-Ras collaborate in modulating the phenotypic plasticity and invasiveness of epithelial tumor cells. Genes Dev 1996; 10: 2462-2477.
29. He M, Xu Z, Ding T, Kuang DM, Zheng L. MicroRNA-155 regulates inflammatory cytokine production in tumor-associated macrophages via targeting C/EBPbeta. Cell Mol Immunol 2009; 6: 343-352.
30. Costinean S, Sandhu SK, Pedersen IM, Tili E, Trotta R, Perrotti D et al. Src homology 2 domain-containing inositol-5-phosphatase and CCAAT enhancer-binding protein beta are targeted by miR-155 in B cells of Emicro-MiR-155 transgenic mice. Blood 2009; 114: 1374-1382.
31. Kong W, Yang H, He L, Zhao JJ, Coppola D, Dalton WS et al. MicroRNA-155 is regulated by the transforming growth factor beta/Smad pathway and contributes to epithelial cell plasticity by targeting RhoA. Mol Cell Biol 2008; 28: 6773-6784.
32. Gal A, Sjoblom T, Fedorova L, Imreh S, Beug H, Moustakas A. Sustained TGF beta exposure suppresses Smad and non-Smad signalling in mammary epithelial cells, leading to EMT and inhibition of growth arrest and apoptosis. Oncogene 2008; 27: 1218-1230.
33. McEarchern JA, Kobie JJ, Mack V, Wu RS, Meade-Tollin L, Arteaga CL et al. Invasion and metastasis of a mammary tumor involves TGF-beta signaling. Int J Cancer 2001; 91: 76-82.
34. Uhlen M, Bjorling E, Agaton C, Szigyarto CA, Amini B, Andersen E et al. A human protein atlas for normal and cancer tissues based on antibody proteomics. Mol Cell Proteomics 2005; 4: 1920-1932.
35. Peinado H, Olmeda D, Snail Cano A. Zeb and bHLH factors in tumour progression: an alliance against the epithelial phenotype? Nat Rev Cancer 2007; 7: 415-428.
36. Mattiske S, Suetani RJ, Neilsen PM, Callen DF. The oncogenic role of miR-155 in breast cancer. Cancer Epidemiol Biomarkers Prev 2012; 21: 1236-1243.
37. Wang HR, Zhang Y, Ozdamar B, Ogunjimi AA, Alexandrova E, Thomsen GH et al. Regulation of cell polarity and protrusion formation by targeting RhoA for degradation. Science 2003; 302: 1775-1779.
38. Terry S, Nie M, Matter K, Balda MS. Rho signaling and tight junction functions. Physiology (Bethesda) 2010; 25: 16-26.
39. Gotoh T, Chowdhury S, Takiguchi M, Mori M. The glucocorticoid-responsive gene cascade. Activation of the rat arginase gene through induction of C/EBPbeta. J Biol Chem 1997; 272: 3694-3698.
40. Rhim AD, Mirek ET, Aiello NM, Maitra A, Bailey JM, McAllister F et al. EMT and dissemination precede pancreatic tumor formation. Cell 2012; 148: 349-361.
41. Zhang L, Lei W, Wang X, Tang Y, Song J. Glucocorticoid induces mesenchymal-toepithelial transition and inhibits TGF-beta1-induced epithelial-to-mesenchymal transition and cell migration. FEBS Lett 2010; 584: 4646-4654.
42. Zuo L, Li W, You S. Progesterone reverses the mesenchymal phenotypes of basal phenotype breast cancer cells via a membrane progesterone receptor mediated pathway. Breast Cancer Res 2012; 12: R34.
43. Tseng YH, Kokkotou E, Schulz TJ, Huang TL, Winnay JN, Taniguchi CM et al. New role of bone morphogenetic protein 7 in brown adipogenesis and energy expenditure. Nature 2008; 454: 1000-1004.
44. Zeisberg M, Hanai J, Sugimoto H, Mammoto T, Charytan D, Strutz F et al. BMP-7 counteracts TGF-beta1-induced epithelial-to-mesenchymal transition and reverses chronic renal injury. Nat Med 2003; 9: 964-968.
45. Buijs JT, Henriquez NV, van Overveld PG, van der Horst G, Que I, Schwaninger R et al. Bone morphogenetic protein 7 in the development and treatment of bone metastases from breast cancer. Cancer Res 2007; 67: 8742-8751.
46. Janda E, Lehmann K, Killisch I, Jechlinger M, Herzig M, Downward J et al. Ras and TGF[beta] cooperatively regulate epithelial cell plasticity and metastasis: dissection of Ras signaling pathways. J Cell Biol 2002; 156: 299-313.