FOXP1, an Estrogen-Inducible Transcription Factor, Modulates Cell Proliferation in Breast Cancer Cells and 5-Year Recurrence-Free Survival of Patients with Tamoxifen-Treated Breast Cancer

Hormones and Cancer

Volumn 2, Issue 5, 2011, Pages 286-297

  Shigekawa, Takashi ^a,c   Ijichi, Nobuhiro ^a   Ikeda, Kazuhiro ^a   Horie Inoue, Kuniko ^a   Shimizu, Chikako ^b   Saji, Shigehira ^a,c   Aogi, Kenjiro ^d   Tsuda, Hitoshi ^b   Osaki, Akihiko ^a   Saeki, Toshiaki ^a   Inoue, Satoshi ^a,e  

^a SAITAMA MEDICAL UNIVERSITY   (Japan)

^b NATIONAL CANCER CENTER HOSPITAL   (Japan)

^c TOKYO METROPOLITAN KOMAGOME HOSPITAL   (Japan)

^d NATIONAL HOSPITAL ORGANIZATION SHIKOKU CANCER CENTER   (Japan)

^e UNIVERSITY OF TOKYO   (Japan)

Author keywords

Breast cancer; ER ; Estrogen; FOXP1; Recurrence; Tamoxifen

Indexed keywords

EPIDERMAL GROWTH FACTOR RECEPTOR 2; ESTROGEN; ESTROGEN RECEPTOR ALPHA; FORKHEAD TRANSCRIPTION FACTOR; MESSENGER RNA; PROGESTERONE RECEPTOR; SMALL INTERFERING RNA; TAMOXIFEN; TRANSCRIPTION FACTOR FOXP1; UNCLASSIFIED DRUG;

ADULT; ARTICLE; BINDING SITE; BREAST BIOPSY; BREAST CANCER; CANCER HORMONE THERAPY; CANCER PATIENT; CANCER SURVIVAL; CANCER TISSUE; CELL PROLIFERATION; CELL STRAIN MCF 7; CONTROLLED STUDY; DISEASE SEVERITY; ESTROGEN ACTIVITY; FEMALE; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION; GENE LOCUS; GENETIC TRANSFECTION; HORMONE RECEPTOR INTERACTION; HORMONE RESPONSE; HUMAN; HUMAN CELL; HUMAN TISSUE; IMMUNOHISTOCHEMISTRY; IMMUNOREACTIVITY; PRIORITY JOURNAL; PROTEIN EXPRESSION; RECURRENCE FREE SURVIVAL; SIGNAL TRANSDUCTION; SURVIVAL TIME; TRANSCRIPTION INITIATION; TUMOR BIOPSY; UPREGULATION;

ADULT; AGED; ANTINEOPLASTIC AGENTS, HORMONAL; BREAST NEOPLASMS; CARCINOMA; CASE-CONTROL STUDIES; CELL PROLIFERATION; DISEASE-FREE SURVIVAL; ESTROGENS; FEMALE; FORKHEAD TRANSCRIPTION FACTORS; HUMANS; MIDDLE AGED; RECURRENCE; REPRESSOR PROTEINS; TAMOXIFEN; TRANSCRIPTION FACTORS; UP-REGULATION;

EID: 80054051092     PISSN: 18688497     EISSN: 18688500     Source Type: Journal    
DOI: 10.1007/s12672-011-0082-6     Document Type: Article

References (45)

1. Platet N, Cathiard AM, Gleizes M, Garcia M (2004) Estrogens and their receptors in breast cancer progression: a dual role in cancer proliferation and invasion. Crit Rev Oncol Hematol 51: 55-67.
2. Hall JM, McDonnell DP (2005) Coregulators in nuclear estrogen receptor action: from concept to therapeutic targeting. Mol Interv 5: 343-357.
3. Carroll JS, Brown M (2006) Estrogen receptor target gene: an evolving concept. Mol Endocrinol 20: 1707-1714.
4. Carroll JS, Liu XS, Brodsky AS, Li W, Meyer CA, Szary AJ, Eeckhoute J, Shao W, Hestermann EV, Geistelinger TR, Fox EA, Silver PA, Brown M (2005) Chromosome-wide mapping of estrogen receptor binding reveals long-range regulation requiring the forkhead protein FoxA1. Cell 122: 33-43.
5. Lupien M, Eeckhoute J, Meyer CA, Wang Q, Zhang Y, Li W, Carroll JS, Liu XS, Brown M (2008) FoxA1 translates epigenetic signatures into enhancer-driven lineage-specific transcription. Cell 132: 958-970.
6. Grange T, Roux J, Rigaud G, Pictet R (1991) Cell-type specific activity of two glucocorticoid responsive units of rat tyrosine aminotransferase gene is associated with multiple binding sites for C/EBP and a novel liver-specific nuclear factor. Nucleic Acids Res 19: 131-139.
7. Schuur ER, Loktev AV, Sharma M, Sun Z, Roth RA, Weigel RJ (2001) Ligand-dependent interaction of estrogen receptor-alpha with members of the forkhead transcription factor family. J Biol Chem 276: 33554-33560.
8. Li S, Weidenfeld J, Morrisey EE (2004) Transcriptional and DNA binding activity of the Foxp1/2/4 family is modulated by heterotypic and homotypic protein interactions. Mol Cell Biol 24: 809-822.
9. Wang B, Lin D, Li C, Tucker P (2003) Multiple domains define the expression and regulatory properties of Foxp1 forkhead transcriptional repressors. J Biol Chem 278: 24259-24268.
10. Banham AH, Beasley N, Campo E, Fernandez PL, Fidler C, Gatter K, Jones M, Mason DY, Prime JE, Trougouboff P, Wood K, Cordell JL (2001) The FOXP1 winged helix transcription factor is a novel candidate tumor suppressor gene on chromosome 3p. Cancer Res 61: 8820-8829.
11. Prown PJ, Ashe SL, Leich E, Burek C, Barrans S, Fenton JA, Jack AS, Pulford K, Rosenwald A, Banham AH (2008) Potentially oncogenic B-cell activation induced smaller isoforms of FOXP1 are highly expressed in the activated B cell-like subtype of DLBCL. Blood 111: 2816-2824.
12. Fox SB, Brown P, Han C, Ashe S, Leek RD, Harris AL, Banham AH (2004) Expression of the forkhead transcription factor FOXP1 is associated with estrogen receptor α and improved survival in primary human breast carcinomas. Clin Cancer Res 10: 3521-3527.
13. Banham AH, Boddy J, Launchbury R, Han C, Turley H, Malone PR, Harris AL, Fox SB (2007) Expression of the forkhead transcriptional factor FOXP1 is associated both with hypoxia inducible factors (HIFs) and the androgen receptor in prostate cancer but is not directly regulated by androgens or hypoxia. Prostate 67: 1091-1098.
14. Takayama K, Horie-Inoue K, Ikeda K, Urano T, Murakami K, Hayashizaki Y, Ouchi Y, Inoue S (2008) FOXP1 is an androgen-responsive transcription factor that negatively regulates androgen receptor signaling in prostate cancer cells. Biochem Biophys Res Commun 374: 388-393.
15. Ijichi N, Shigekawa T, Ikeda K, Horie-Inoue K, Fujimura T, Tsuda H, Osaki A, Saeki T, Inoue S (2011) Estrogen-related receptor γ modulates cell proliferation and estrogen signaling in breast cancer. J Steroid Biochem Mol Biol 123: 1-7.
16. Allred DC, Clark GM, Elledge R, Fuqua SA, Brown RW, Chamness GC, Osborne CK, McGuire WL (1993) Association of p53 protein expression with tumor cell proliferation rate and clinical outcome in node-negative breast cancer. J Natl Cancer Inst 85: 200-206.
17. Horie-Inoue K, Bono H, Okazaki Y, Inoue S (2004) Identification and functional analysis of consensus androgen response elements in human prostate cancer cells. Biochem Biophys Res Commun 325: 1312-1317.
18. Horie-Inoue K, Takayama K, Bono HU, Ouchi Y, Okazaki Y, Inoue S (2006) Identification of novel steroid target genes through the combination of bioinformatics and functional analysis of hormone response elements. Biochem Biophys Res Commun 339: 99-106.
19. Giamarchi C, Solanas M, Chailleux C, Augereau P, Vignon F, Rochefort H, Richard-Foy H (1999) Chromatin structure of the regulatory regions of pS2 and cathepsin D genes in hormone-dependent and -independent breast cancer cell lines. Oncogene 18: 533-541.
20. Ikeda K, Ogawa S, Tsukui T, Horie-Inoue K, Ouchi Y, Kato S, Muramatsu M, Inoue S (2004) Protein phosphatase 5 is a negative regulator of estrogen receptor-mediated transcription. Mol Endocrinol 18: 1131-1143.
21. Carroll JS, Meyer CA, Song J, Li W, Geistlinger TR, Eeckhoute J, Brodsky AS, Keeton EK, Fertuck KC, Hall GF, Wang Q, Bekiranov S, Sementchenko V, Fox EA, Silver PA, Gingeras TR, Liu XS, Brown M (2006) Genome-wide analysis of estrogen receptor binding sites. Nat Genet 38: 1289-1297.
22. Lai K, Harnish DC, Evans MJ (2003) Estrogen receptor α regulates expression of the orphan receptor small heterodimer partner. J Biol Chem 278: 36418-36429.
23. Annicotte JS, Chavey C, Servant N, Teyssier J, Bardin A, Licznar A, Badia E, Pujol P, Vignon F, Maudelonde T, Lazennec G, Cavailles V, Fajas L (2005) The nuclear receptor liver receptor homolog-1 is an estrogen receptor target gene. Oncogene 24: 8167-8175.
24. Perou CM, Sørlie T, Eisen MB, van de Rijn M, Jeffrey SS, Rees CA, Pollack JR, Ross DT, Johnsen H, Akslen LA, Fluge O, Pergamenschikov A, Williams C, Zhu SX, Lønning PE, Børresen-Dale AL, Brown PO, Botstein D (2000) Molecular portraits of human breast tumours. Nature 406: 747-752.
25. Sørlie T, Perou CM, Tibshirani R, Aas T, Geisler S, Johnsen H, Hastie T, Eisen MB, van de Rijn M, Jeffrey SS, Thorsen T, Quist H, Matese JC, Brown PO, Botstein D, Eystein Lønning P, Børresen-Dale AL (2001) Gene expression patterns of breast carcinomas distinguish tumor subclasses with clinical implications. Proc Natl Acad Sci U S A 98: 10869-10874.
26. Badve S, Turbin D, Thorat MA, Morimiya A, Nielsen TO, Perou CM, Dunn S, Huntsman DG, Nakshatri H (2007) FOXA1 expression in breast cancer-correlation with luminal subtype A and survival. Clin Cancer Res 13: 4415-4421.
27. Thorat MA, Marchio C, Morimiya A, Savage K, Nakshatri H, Reis-Filho JS, Badve S (2008) Forkhead box A1 expression in breast cancer is associated with luminal subtype and good prognosis. J Clin Pathol 61: 327-332.
28. Barrans SL, Fenton JA, Banham A, Owen RG, Jack AS (2004) Strong expression of FOXP1 identifies a distinct subset of diffuse large B-cell lymphoma (DLBCL) patients with poor outcome. Blood 104: 2933-2935.
29. Banham AH, Connors JM, Brown PJ, Cordell JL, Ott G, Sreenivasan G, Farinha P, Horsman DE, Gascoyne RD (2005) Expression of the FOXP1 transcription factor is strongly associated with inferior survival in patients with diffuse large B-cell lymphoma. Clin Cancer Res 11: 1065-1072.
30. Sagaert X, De Paepe P, Libbrecht L, Vanhentenrijk V, Verhoef G, Thomas J, Wlodarska I, De Wolf-Peeters C (2006) Forkhead box protein P1 expression in mucosa-associated lymphoid tissue lymphomas predicts poor prognosis and transformation to diffuse large B-cell lymphoma. J Clin Oncol 24: 2490-2497.
31. Goatly A, Bacon CM, Nakamura S, Ye H, Kim I, Brown PJ, Ruskoné-Fourmestraux A, Cervera P, Streubel B, Banham AH, Du MQ (2008) FOXP1 abnormalities in lymphoma: translocation breakpoint mapping reveals insights into deregulated transcriptional control. Mod Pathol 21: 902-911.
32. Hoeller S, Schneider A, Haralambieva E, Dirnhofer S, Tzankov A (2010) FOXP1 protein overexpression is associated with inferior outcome in nodal diffuse large B-cell lymphomas with non-germinal centre phenotype, independent of gains and structural aberrations at 3p14. 1. Histopathology 57: 73-80.
33. Kastner P, Krust A, Turcotte B, Stropp U, Tora L, Gronemeyer H, Chambon P (1990) Two distinct estrogen-regulated promoters generate transcripts encoding the two functionally different human progesterone receptor forms A and B. EMBO J 9: 1603-1614.
34. Rayoo M, Yan M, Takano EA, Bates GJ, Brown PJ, Banham AH, Fox SB (2009) Expression of the forkhead box transcription factor FOXP1 is associated with oestrogen receptor alpha, oestrogen receptor beta and improved survival in familial breast cancers. J Clin Pathol 62: 896-902.
35. Wolf I, Bose S, Williamson EA, Miller CW, Karlan BY, Koeffler HP (2007) FOXA1: growth inhibitor and a favorable prognostic factor in human breast cancer. Int J Cancer 120: 1013-1022.
36. Habashy HO, Powe DG, Rakha EA, Ball G, Paish C, Gee J, Nicholson RI, Ellis IO (2008) Forkhead-box A1 (FOXA1) expression in breast cancer and its prognostic significance. Eur J Cancer 44: 1541-1551.
37. Skliris GP, Carder PJ, Lansdown MR, Speirs V (2001) Immunohistochemical detection of ERβ in breast cancer: towards more detailed receptor profiling? Br J Cancer 84: 1095-1098.
38. Bates GJ, Fox SB, Han C, Launchbury R, Leek RD, Harris AL, Banham AH (2008) Expression of the forkhead transcription factor FOXP1 is associated with that of estrogen receptorβ in primary invasive breast carcinomas. Breast Cancer Res Treat 111: 453-459.
39. Sotoca AM, van den Berg H, Vervoort J, van der Saag P, Ström A, Gustafsson JA, Rietjens I, Murk AJ (2008) Influence of cellular ERα/ERβ ratio on the ERα-agonist induced proliferation of human T47D breast cancer cells. Toxicol Sci 105: 303-311.
40. Métivier R, Penot G, Hübner MR, Reid G, Brand H, Kos M, Gannon F (2003) Estrogen receptor-α directs ordered, cyclical, and combinatorial recruitment of cofactors on a natural target promoter. Cell 115: 751-763.
41. Mattingly KA, Ivanova MM, Riggs KA, Wickramasinghe NS, Barch MJ, Klinge CM (2008) Estradiol stimulates transcription of nuclear respiratory factor-1 and increases mitochondrial biogenesis. Mol Endocrinol 22: 609-622.
42. Wang B, Weidenfeld J, Lu MM, Maika S, Kuziel WA, Morrisey EE, Tucker PW (2004) Foxp1 regulates cardiac outflow tract, endocardial cushion morphogenesis and myocyte proliferation and maturation. Development 131: 4477-4487.
43. Craig VJ, Cogliatti SB, Imig J, Renner C, Neuenschwander S, Rehrauer H, Schlapbach R, Dirnhofer S, Tzankov A, Müller A (2011) Myc-mediated repression of microRNA-34a promotes high grade transformation of B-cell lymphoma by dysregulation of FoxP1. Blood 117(23): 6227-6236.
44. Zhang Y, Li S, Yuan L, Tian Y, Weidenfeld J, Yang J, Liu F, Chokas AL, Morrisey EE (2010) Foxp1 coordinates cardiomyocyte proliferation through both cell-autonomous and nonautonomous mechanisms. Genes Dev 24: 1746-1757.
45. Chamorro MN, Schwartz DR, Vonica A, Brivanlou AH, Cho KR, Varmus HE (2005) FGF-20 and DKK1 are transcriptional targets of β-catenin and FGF-20 is implicated in cancer and development. EMBO J 24: 73-84.