C/EBPβ at the core of the TGFβ cytostatic response and its evasion in metastatic breast cancer cells

Cancer Cell

Volumn 10, Issue 3, 2006, Pages 203-214

  Gomis, Roger R ^a   Alarcón, Claudio ^a   Nadal, Cristina ^a   Van Poznak, Catherine ^a   Massagué, Joan ^a  

^a MEMORIAL SLOAN KETTERING CANCER CENTER   (United States)

Author keywords

CELLCYCLE; DNA

Indexed keywords

BINDING PROTEIN; CCAAT ENHANCER BINDING PROTEIN BETA; SMAD PROTEIN; TRANSCRIPTION FACTOR FOXO; TRANSFORMING GROWTH FACTOR BETA; CYCLIN DEPENDENT KINASE INHIBITOR 2B; MYC PROTEIN;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BREAST CANCER; CELL CYCLE; CONTROLLED STUDY; COORDINATION; CYTOSTASIS; DISEASE ASSOCIATION; EPITHELIUM CELL; GENE REPRESSION; HUMAN; HUMAN CELL; METASTASIS; NONHUMAN; ONCOGENE MYC; PATHOPHYSIOLOGY; PRIORITY JOURNAL; REGULATORY MECHANISM; ANIMAL; BREAST TUMOR; CELL CULTURE; CELL PROLIFERATION; DRUG EFFECT; GENETICS; METABOLISM; MOLECULAR GENETICS; MOUSE; NUCLEOTIDE SEQUENCE; PATHOLOGY; PROMOTER REGION; TRANSACTIVATION;

ANIMALS; BASE SEQUENCE; BREAST NEOPLASMS; CCAAT-ENHANCER-BINDING PROTEIN-BETA; CELL PROLIFERATION; CYCLIN-DEPENDENT KINASE INHIBITOR P15; HUMANS; MICE; MOLECULAR SEQUENCE DATA; NEOPLASM METASTASIS; PROMOTER REGIONS (GENETICS); PROTO-ONCOGENE PROTEINS C-MYC; TRANS-ACTIVATION (GENETICS); TRANSFORMING GROWTH FACTOR BETA; TUMOR CELLS, CULTURED;

EID: 33748208668     PISSN: 15356108     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.ccr.2006.07.019     Document Type: Article

References (59)

1. Al-Hajj M., Wicha M.S., Benito-Hernandez A., Morrison S.J., and Clarke M.F. Prospective identification of tumorigenic breast cancer cells. Proc. Natl. Acad. Sci. USA 100 (2003) 3983-3988
2. Baldwin B.R., Timchenko N.A., and Zahnow C.A. Epidermal growth factor receptor stimulation activates the RNA binding protein CUG-BP1 and increases expression of C/EBPβ-LIP in mammary epithelial cells. Mol. Cell. Biol. 24 (2004) 3682-3691
3. Begay V., Smink J., and Leutz A. Essential requirement of CCAAT/enhancer binding proteins in embryogenesis. Mol. Cell. Biol. 24 (2004) 9744-9751
4. Bierie B., and Moses H.L. TGF-β and cancer. Cytokine Growth Factor Rev. 17 (2006) 29-40
5. Brummelkamp T.R., Bernards R., and Agami R. Stable suppression of tumorigenicity by virus-mediated RNA interference. Cancer Cell 2 (2002) 243-247
6. Brunet A., Sweeney L.B., Sturgill J.F., Chua K.F., Greer P.L., Lin Y., Tran H., Ross S.E., Mostoslavsky R., Cohen H.Y., et al. Stress-dependent regulation of FOXO transcription factors by the SIRT1 deacetylase. Science 303 (2004) 2011-2015
7. Calonge M.J., and Massagué J. Smad4/DPC4 silencing and hyperactive Ras jointly disrupt transforming growth factor-β antiproliferative responses in colon cancer cells. J. Biol. Chem. 274 (1999) 33637-33643
8. Carcamo J., Zentella A., and Massagué J. Disruption of transforming growth factor β signaling by a mutation that prevents transphosphorylation within the receptor complex. Mol. Cell. Biol. 15 (1995) 1573-1581
9. Chen C.R., Kang Y., and Massagué J. Defective repression of c-myc in breast cancer cells: A loss at the core of the transforming growth factor β growth arrest program. Proc. Natl. Acad. Sci. USA 98 (2001) 992-999
10. Chen C.R., Kang Y., Siegel P.M., and Massagué J. E2F4/5 and p107 as Smad cofactors linking the TGFβ receptor to c-myc repression. Cell 110 (2002) 19-32
11. Choy L., and Derynck R. Transforming growth factor-β inhibits adipocyte differentiation by Smad3 interacting with CCAAT/enhancer-binding protein (C/EBP) and repressing C/EBP transactivation function. J. Biol. Chem. 278 (2003) 9609-9619
12. Derynck R., Akhurst R.J., and Balmain A. TGF-β signaling in tumor suppression and cancer progression. Nat. Genet. 29 (2001) 117-129
13. Descombes P., and Schibler U. A liver-enriched transcriptional activator protein, LAP, and a transcriptional inhibitory protein, LIP, are translated from the same mRNA. Cell 67 (1991) 569-579
14. Dumont N., and Arteaga C.L. Targeting the TGFβ signaling network in human neoplasia. Cancer Cell 3 (2003) 531-536
15. Frederick J.P., Liberati N.T., Waddell D.S., Shi Y., and Wang X.F. Transforming growth factor β-mediated transcriptional repression of c-myc is dependent on direct binding of Smad3 to a novel repressive Smad binding element. Mol. Cell. Biol. 24 (2004) 2546-2559
16. Gomis R.R., Alarcón C., He W., Wang Q., Seoane J., Lash A., and Massagué J. A FoxO-Smad synexpression group in human keratinocytes. Proc. Natl. Acad. Sci. USA 103 (2006) 12747-12752
17. Gorelik L., and Flavell R.A. Transforming growth factor-β in T-cell biology. Nat. Rev. Immunol. 2 (2002) 46-53
18. Greer E.L., and Brunet A. FOXO transcription factors at the interface between longevity and tumor suppression. Oncogene 24 (2005) 7410-7425
19. Grimm S.L., and Rosen J.M. The role of C/EBPβ in mammary gland development and breast cancer. J. Mammary Gland Biol. Neoplasia 8 (2003) 191-204
20. Hanahan D., and Weinberg R.A. The hallmarks of cancer. Cell 100 (2000) 57-70
21. Herrera R.E., Makela T.P., and Weinberg R.A. TGFβ-induced growth inhibition in primary fibroblasts requires the retinoblastoma protein. Mol. Biol. Cell 7 (1996) 1335-1342
22. Kang Y., Chen C.R., and Massagué J. A self-enabling TGFβ response coupled to stress signaling: Smad engages stress response factor ATF3 for Id1 repression in epithelial cells. Mol. Cell 11 (2003) 915-926
23. Kang Y., Siegel P.M., Shu W., Drobnjak M., Kakonen S.M., Cordon-Cardo C., Guise T.A., and Massagué J. A multigenic program mediating breast cancer metastasis to bone. Cancer Cell 3 (2003) 537-549
24. Kang Y., He W., Tulley S., Gupta G.P., Serganova I., Chen C.R., Manova-Todorova K., Blasberg R., Gerald W.L., and Massagué J. Breast cancer bone metastasis mediated by the Smad tumor suppressor pathway. Proc. Natl. Acad. Sci. USA 102 (2005) 13909-13914
25. Kielhorn E., Schofield K., and Rimm D.L. Use of magnetic enrichment for detection of carcinoma cells in fluid specimens. Cancer 94 (2002) 205-211
26. Kretzschmar M., Doody J., Timokhina I., and Massagué J. A mechanism of repression of TGFβ/ Smad signaling by oncogenic Ras. Genes Dev. 13 (1999) 804-816
27. Laiho M., DeCaprio J.A., Ludlow J.W., Livingston D.M., and Massagué J. Growth inhibition by TGF-β linked to suppression of retinoblastoma protein phosphorylation. Cell 62 (1990) 175-185
28. Latres E., Malumbres M., Sotillo R., Martin J., Ortega S., Martin-Caballero J., Flores J.M., Cordon-Cardo C., and Barbacid M. Limited overlapping roles of P15(INK4b) and P18(INK4c) cell cycle inhibitors in proliferation and tumorigenesis. EMBO J. 19 (2000) 3496-3506
29. Latza U., Niedobitek G., Schwarting R., Nekarda H., and Stein H. Ber-EP4: New monoclonal antibody which distinguishes epithelia from mesothelial. J. Clin. Pathol. 43 (1990) 213-219
30. Lee S.S., Kennedy S., Tolonen A.C., and Ruvkun G. DAF-16 target genes that control C. elegans life-span and metabolism. Science 300 (2003) 644-647
31. Lekstrom-Himes J., and Xanthopoulos K.G. Biological role of the CCAAT/enhancer-binding protein family of transcription factors. J. Biol. Chem. 273 (1998) 28545-28548
32. Libina N., Berman J.R., and Kenyon C. Tissue-specific activities of C. elegans DAF-16 in the regulation of lifespan. Cell 115 (2003) 489-502
33. Massagué J., Blain S.W., and Lo R.S. TGFβ signaling in growth control, cancer, and heritable disorders. Cell 103 (2000) 295-309
34. Massagué J., Seoane J., and Wotton D. Smad transcription factors. Genes Dev. 19 (2005) 2783-2810
35. McKnight S.L. McBindall-A better name for CCAAT/Enhancer binding proteins?. Cell 107 (2001) 259-261
36. Milde-Langosch K., Loning T., and Bamberger A.M. Expression of the CCAAT/enhancer-binding proteins C/EBPα, C/EBPβ and C/EBPδ in breast cancer: Correlations with clinicopathologic parameters and cell-cycle regulatory proteins. Breast Cancer Res. Treat. 79 (2003) 175-185
37. Minn A.J., Kang Y., Serganova I., Gupta G.P., Giri D.D., Doubrovin M., Ponomarev V., Gerald W.L., Blasberg R., and Massagué J. Distinct organ-specific metastatic potential of individual breast cancer cells and primary tumors. J. Clin. Invest. 115 (2005) 44-55
38. Raught B., Gingras A.C., James A., Medina D., Sonenberg N., and Rosen J.M. Expression of a translationally regulated, dominant-negative CCAAT/enhancer-binding protein β isoform and up-regulation of the eukaryotic translation initiation factor 2α are correlated with neoplastic transformation of mammary epithelial cells. Cancer Res. 56 (1996) 4382-4386
39. Roberts A.B., and Wakefield L.M. The two faces of transforming growth factor β in carcinogenesis. Proc. Natl. Acad. Sci. USA 100 (2003) 8621-8623
40. Scandura J.M., Boccuni P., Massagué J., and Nimer S.D. Transforming growth factor β-induced cell cycle arrest of human hematopoietic cells requires p57KIP2 up-regulation. Proc. Natl. Acad. Sci. USA 101 (2004) 15231-15236
41. Sebastian T., Malik R., Thomas S., Sage J., and Johnson P.F. C/EBPβ cooperates with RB:E2F to implement Ras(V12)-induced cellular senescence. EMBO J. 24 (2005) 3301-3312
42. Seoane J., Le H.V., and Massagué J. Myc suppression of the p21(Cip1) Cdk inhibitor influences the outcome of the p53 response to DNA damage. Nature 419 (2002) 729-734
43. Seoane J., Le H.V., Shen L., Anderson S.A., and Massagué J. Integration of Smad and forkhead pathways in the control of neuroepithelial and glioblastoma cell proliferation. Cell 117 (2004) 211-223
44. Seoane J., Pouponnot C., Staller P., Schader M., Eilers M., and Massagué J. TGFβ influences Myc, Miz-1 and Smad to control the CDK inhibitor p15INK4b. Nat. Cell Biol. 3 (2001) 400-408
45. Shang Y., Hu X., DiRenzo J., Lazar M.A., and Brown M. Cofactor dynamics and sufficiency in estrogen receptor-regulated transcription. Cell 103 (2000) 843-852
46. Siegel P.M., and Massagué J. Cytostatic and apoptotic actions of TGF-β in homeostasis and cancer. Nat. Rev. Cancer 3 (2003) 807-821
47. Siegel P.M., Shu W., Cardiff R.D., Muller W.J., and Massagué J. Transforming growth factor β signaling impairs Neu-induced mammary tumorigenesis while promoting pulmonary metastasis. Proc. Natl. Acad. Sci. USA 100 (2003) 8430-8435
48. Staller P., Peukert K., Kiermaier A., Seoane J., Lukas J., Karsunky H., Moroy T., Bartek J., Massagué J., Hanel F., and Eilers M. Repression of p15INK4b expression by Myc through association with Miz-1. Nat. Cell Biol. 3 (2001) 392-399
49. Thomas D.A., and Massagué J. TGF-β directly targets cytotoxic T cell functions during tumor evasion of immune surveillance. Cancer Cell 8 (2005) 369-380
50. Timchenko N.A., Welm A.L., Lu X., and Timchenko L.T. CUG repeat binding protein (CUGBP1) interacts with the 5′ region of C/EBPβ mRNA and regulates translation of C/EBPβ isoforms. Nucleic Acids Res. 27 (1999) 4517-4525
51. Timchenko N.A., Cai Z.J., Welm A.L., Reddy S., Ashizawa T., and Timchenko L.T. RNA CUG repeats sequester CUGBP1 and alter protein levels and activity of CUGBP1. J. Biol. Chem. 276 (2001) 7820-7826
52. Timchenko N.A., Wang G.L., and Timchenko L.T. RNA CUG-binding protein 1 increases translation of 20-kDa isoform of CCAAT/enhancer-binding protein β by interacting with the α and β subunits of eukaryotic initiation translation factor 2. J. Biol. Chem. 280 (2005) 20549-20557
53. Tremain R., Marko M., Kinnimulki V., Ueno H., Bottinger E., and Glick A. Defects in TGF-β signaling overcome senescence of mouse keratinocytes expressing v-Ha-ras. Oncogene 19 (2000) 1698-1709
54. Vijayachandra K., Lee J., and Glick A.B. Smad3 regulates senescence and malignant conversion in a mouse multistage skin carcinogenesis model. Cancer Res. 63 (2003) 3447-3452
55. Wojtowicz-Praga S. Reversal of tumor-induced immunosuppression by TGF-β inhibitors. Invest. New Drugs 21 (2003) 21-32
56. Yin J.J., Selander K., Chirgwin J.M., Dallas M., Grubbs B.G., Wieser R., Massagué J., Mundy G.R., and Guise T.A. TGF-β signaling blockade inhibits PTHrP secretion by breast cancer cells and bone metastases development. J. Clin. Invest. 103 (1999) 197-206
57. Zahnow C.A. CCAAT/enhancer binding proteins in normal mammary development and breast cancer. Breast Cancer Res. 4 (2002) 113-121
58. Zahnow C.A., Younes P., Laucirica R., and Rosen J.M. Overexpression of C/EBPβ-LIP, a naturally occurring, dominant-negative transcription factor, in human breast cancer. J. Natl. Cancer Inst. 89 (1997) 1887-1891
59. Zahnow C.A., Cardiff R.D., Laucirica R., Medina D., and Rosen J.M. A role for CCAAT/enhancer binding protein β-liver-enriched inhibitory protein in mammary epithelial cell proliferation. Cancer Res. 61 (2001) 261-269