NFκB affects estrogen receptor expression and activity in breast cancer through multiple mechanisms

Molecular and Cellular Endocrinology

Volumn 418, Issue , 2015, Pages 235-239

  Frasor, Jonna ^a   El Shennawy, Lamiaa ^a   Stender, Joshua D ^b   Kastrati, Irida ^a  

^a UNIVERSITY OF ILLINOIS AT CHICAGO   (United States)

^b UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

Breast cancer; Estrogen receptor; NF B; Tamoxifen

Indexed keywords

DNA; ESTROGEN RECEPTOR; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; PROTEIN KINASE C; SYNAPTOTAGMIN I; TAMOXIFEN; TRANSCRIPTION FACTOR EZH2; TRANSCRIPTION FACTOR FKHRL1;

BINDING AFFINITY; BREAST CANCER; BREAST CANCER CELL LINE; CELL CYCLE PROGRESSION; DRUG PROTEIN BINDING; GENE REPRESSION; GENETIC TRANSCRIPTION; HUMAN; MOLECULARLY TARGETED THERAPY; PRIORITY JOURNAL; PROMOTER REGION; PROTEIN BINDING; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN LOCALIZATION; PROTEIN PHOSPHORYLATION; PROTEIN PROTEIN INTERACTION; PROTEIN TRANSPORT; REVIEW; SIGNAL TRANSDUCTION; TUMOR MICROENVIRONMENT; BREAST NEOPLASMS; DOWN REGULATION; DRUG RESISTANCE; FEMALE; GENE EXPRESSION REGULATION; GENETICS; METABOLISM;

BREAST NEOPLASMS; DOWN-REGULATION; DRUG RESISTANCE, NEOPLASM; FEMALE; GENE EXPRESSION REGULATION, NEOPLASTIC; HUMANS; NF-KAPPA B; RECEPTORS, ESTROGEN; SIGNAL TRANSDUCTION; TAMOXIFEN; TRANSCRIPTION, GENETIC;

EID: 84949554316     PISSN: 03037207     EISSN: 18728057     Source Type: Journal    
DOI: 10.1016/j.mce.2014.09.013     Document Type: Review

References (76)

1. Acharyya S., Sharma S.M., Cheng A.S., Ladner K.J., He W., Kline W., et al. TNF inhibits Notch-1 in skeletal muscle cells by Ezh2 and DNA methylation mediated repression: implications in Duchenne muscular dystrophy. PLoS ONE 2010, 5:e12479.
2. Arpino G., Wiechmann L., Osborne C.K., Schiff R. Crosstalk between the estrogen receptor and the HER tyrosine kinase receptor family: molecular mechanism and clinical implications for endocrine therapy resistance. Endocr. Rev 2008, 29:217-233.
3. Baumgarten S.C., Frasor J. Inflammation: an instigator of more aggressive estrogen receptor (ER) positive breast cancers. Mol. Endocrinol 2012, 26:360-371.
4. Belguise K., Sonenshein G.E. PKCtheta promotes c-Rel-driven mammary tumorigenesis in mice and humans by repressing estrogen receptor alpha synthesis. J. Clin. Invest 2007, 117:4009-4021.
5. Biswas D.K., Shi Q., Baily S., Strickland I., Ghosh S., Pardee A.B., et al. NF-kappa B activation in human breast cancer specimens and its role in cell proliferation and apoptosis. Proc. Natl. Acad. Sci. U.S.A. 2004, 101:10137-10142.
6. Brzozowski A.M., Pike A.C., Dauter Z., Hubbard R.E., Bonn T., Engstrom O., et al. Molecular basis of agonism and antagonism in the oestrogen receptor. Nature 1997, 389:753-758.
7. Carroll J.S., Liu X.S., Brodsky A.S., Li W., Meyer C.A., Szary A.J., et al. Chromosome-wide mapping of estrogen receptor binding reveals long-range regulation requiring the forkhead protein FoxA1. Cell 2005, 122:33-43.
8. Clarke R., Liu M.C., Bouker K.B., Gu Z., Lee R.Y., Zhu Y., et al. Antiestrogen resistance in breast cancer and the role of estrogen receptor signaling. Oncogene 2003, 22:7316-7339.
9. Creighton C.J. The molecular profile of luminal B breast cancer. Biologics 2012, 6:289-297.
10. de Graffenried L.A., Chandrasekar B., Friedrichs W.E., Donzis E., Silva J., Hidalgo M., et al. NF-kappa B inhibition markedly enhances sensitivity of resistant breast cancer tumor cells to tamoxifen. Ann. Oncol 2004, 15:885-890.
11. De Bosscher K., Vanden Berghe W., Haegeman G. Cross-talk between nuclear receptors and nuclear factor kappaB. Oncogene 2006, 25:6868-6886.
12. Dutertre M., Smith C.L. Ligand-independent interactions of p160/steroid receptor coactivators and CREB-binding protein (CBP) with estrogen receptor-alpha: regulation by phosphorylation sites in the A/B region depends on other receptor domains. Mol. Endocrinol 2003, 17:1296-1314.
13. Feldman I., Feldman G.M., Mobarak C., Dunkelberg J.C., Leslie K.K. Identification of proteins within the nuclear factor-kappa B transcriptional complex including estrogen receptor-alpha. Am. J. Obstet. Gynecol 2007, 196:394.e1-394.e11. discussion 394.e11-394.e13.
14. Frasor J., Weaver A.E., Pradhan M., Mehta K. Synergistic up-regulation of prostaglandin E synthase expression in breast cancer cells by 17beta-estradiol and proinflammatory cytokines. Endocrinology 2008, 149:6272-6279.
15. Frasor J., Weaver A., Pradhan M., Dai Y., Miller L.D., Lin C.Y., et al. Positive cross-talk between estrogen receptor and NF-kappaB in breast cancer. Cancer Res 2009, 69:8918-8925.
16. Galien R., Garcia T. Estrogen receptor impairs interleukin-6 expression by preventing protein binding on the NF-kappaB site. Nucleic Acids Res 1997, 25:2424-2429.
17. Ghisletti S., Meda C., Maggi A., Vegeto E. 17beta-estradiol inhibits inflammatory gene expression by controlling NF-kappaB intracellular localization. Mol. Cell. Biol 2005, 25:2957-2968.
18. Gori I., Pellegrini C., Staedler D., Russell R., Jan C., Canny G.O. Tumor necrosis factor-alpha activates estrogen signaling pathways in endometrial epithelial cells via estrogen receptor alpha. Mol. Cell. Endocrinol 2011, 345:27-37.
19. Guo S., Sonenshein G.E. Forkhead box transcription factor FOXO3a regulates estrogen receptor alpha expression and is repressed by the Her-2/neu/phosphatidylinositol 3-kinase/Akt signaling pathway. Mol. Cell. Biol 2004, 24:8681-8690.
20. Gutierrez M.C., Detre S., Johnston S., Mohsin S.K., Shou J., Allred D.C., et al. Molecular changes in tamoxifen-resistant breast cancer: relationship between estrogen receptor, HER-2, and p38 mitogen-activated protein kinase. J. Clin. Oncol 2005, 23:2469-2476.
21. Harvey J.M., Clark G.M., Osborne C.K., Allred D.C. Estrogen receptor status by immunohistochemistry is superior to the ligand-binding assay for predicting response to adjuvant endocrine therapy in breast cancer. J. Clin. Oncol 1999, 17:1474-1481.
22. Hoehn J.L., Plotka E.D., Dickson K.B. Comparison of estrogen receptor levels in primary and regional metastatic carcinoma of the breast. Ann. Surg 1979, 190:69-71.
23. Hurtado A., Holmes K.A., Ross-Innes C.S., Schmidt D., Carroll J.S. FOXA1 is a key determinant of estrogen receptor function and endocrine response. Nat. Genet 2011, 43:27-33.
24. Iorio M.V., Ferracin M., Liu C.G., Veronese A., Spizzo R., Sabbioni S., et al. MicroRNA gene expression deregulation in human breast cancer. Cancer Res 2005, 65:7065-7070.
25. Jones R.L., Rojo F., A'Hern R., Villena N., Salter J., Corominas J.M., et al. Nuclear NF-kappaB/p65 expression and response to neoadjuvant chemotherapy in breast cancer. J. Clin. Pathol 2011, 64:130-135.
26. Karin M., Cao Y., Greten F.R., Li Z.W. NF-kappaB in cancer: from innocent bystander to major culprit. Nat. Rev. Cancer 2002, 2:301-310.
27. Kastrati I., Canestrari E., Frasor J. PHLDA1 expression is controlled by an estrogen receptor-NFkappaB-miR-181 regulatory loop and is essential for formation of ER+ mammospheres. Oncogene 2014, 10.1038/onc.2014.180.
28. Kim H.J., Hawke N., Baldwin A.S. NF-kappaB and IKK as therapeutic targets in cancer. Cell Death Differ 2006, 13:738-747.
29. King A.E., Collins F., Klonisch T., Sallenave J.M., Critchley H.O., Saunders P.T. An additive interaction between the NFkappaB and estrogen receptor signalling pathways in human endometrial epithelial cells. Hum. Reprod 2010, 25:510-518.
30. Kubo M., Kanaya N., Petrossian K., Ye J., Warden C., Liu Z., et al. Inhibition of the proliferation of acquired aromatase inhibitor-resistant breast cancer cells by histone deacetylase inhibitor LBH589 (panobinostat). Breast Cancer Res. Treat 2013, 137:93-107.
31. Le Romancer M., Poulard C., Cohen P., Sentis S., Renoir J.M., Corbo L. Cracking the estrogen receptor's posttranslational code in breast tumors. Endocr. Rev 2011, 32:597-622.
32. Lee A.V., Cui X., Oesterreich S. Cross-talk among estrogen receptor, epidermal growth factor, and insulin-like growth factor signaling in breast cancer. Clin. Cancer Res 2001, 7:4429s-4435s. discussion 4411s-4412s.
33. Levin E.R., Pietras R.J. Estrogen receptors outside the nucleus in breast cancer. Breast Cancer Res. Treat 2008, 108:351-361.
34. Li S., Shen D., Shao J., Crowder R., Liu W., Prat A., et al. Endocrine-therapy-resistant ESR1 variants revealed by genomic characterization of breast-cancer-derived xenografts. Cell Rep 2013, 4:1116-1130.
35. Likhite V.S., Stossi F., Kim K., Katzenellenbogen B.S., Katzenellenbogen J.A. Kinase-specific phosphorylation of the estrogen receptor changes receptor interactions with ligand, deoxyribonucleic acid, and coregulators associated with alterations in estrogen and tamoxifen activity. Mol. Endocrinol 2006, 20:3120-3132.
36. Liu H., Lee E.S., Gajdos C., Pearce S.T., Chen B., Osipo C., et al. Apoptotic action of 17beta-estradiol in raloxifene-resistant MCF-7 cells in vitro and in vivo. J. Natl Cancer Inst 2003, 95:1586-1597.
37. Luo M., Koh M., Feng J., Wu Q., Melamed P. Cross talk in hormonally regulated gene transcription through induction of estrogen receptor ubiquitylation. Mol. Cell. Biol 2005, 25:7386-7398.
38. Lupien M., Eeckhoute J., Meyer C.A., Wang Q., Zhang Y., Li W., et al. FoxA1 translates epigenetic signatures into enhancer-driven lineage-specific transcription. Cell 2008, 132:958-970.
39. Merenbakh-Lamin K., Ben-Baruch N., Yeheskel A., Dvir A., Soussan-Gutman L., Jeselsohn R., et al. D538G mutation in estrogen receptor-alpha: a novel mechanism for acquired endocrine resistance in breast cancer. Cancer Res 2013, 73:6856-6864.
40. Montagut C., Tusquets I., Ferrer B., Corominas J.M., Bellosillo B., Campas C., et al. Activation of nuclear factor-kappa B is linked to resistance to neoadjuvant chemotherapy in breast cancer patients. Endocr. Relat. Cancer 2006, 13:607-616.
41. Mulrane L., McGee S.F., Gallagher W.M., O'Connor D.P. miRNA dysregulation in breast cancer. Cancer Res 2013, 73:6554-6562.
42. Murphy L.C., Seekallu S.V., Watson P.H. Clinical significance of estrogen receptor phosphorylation. Endocr. Relat. Cancer 2011, 18:R1-R14.
43. Nakshatri H., Bhat-Nakshatri P., Martin D.A., Goulet R.J., Sledge G.W. Constitutive activation of NF-kappaB during progression of breast cancer to hormone-independent growth. Mol. Cell. Biol 1997, 17:3629-3639.
44. Oida K., Matsuda A., Jung K., Xia Y., Jang H., Amagai Y., et al. Nuclear factor-kB plays a critical role in both intrinsic and acquired resistance against endocrine therapy in human breast cancer cells. Sci. Rep 2014, 4:4057.
45. Park K.J., Krishnan V., O'Malley B.W., Yamamoto Y., Gaynor R.B. Formation of an IKKalpha-dependent transcription complex is required for estrogen receptor-mediated gene activation. Mol. Cell 2005, 18:71-82.
46. Perou C.M., Sorlie T., Eisen M.B., van de Rijn M., Jeffrey S.S., Rees C.A., et al. Molecular portraits of human breast tumours. Nature 2000, 406:747-752.
47. Porter W., Saville B., Hoivik D., Safe S. Functional synergy between the transcription factor Sp1 and the estrogen receptor. Mol. Endocrinol 1569-1580, 11:1997.
48. Pradhan M., Bembinster L.A., Baumgarten S.C., Frasor J. Proinflammatory cytokines enhance estrogen-dependent expression of the multidrug transporter gene ABCG2 through estrogen receptor and NF{kappa}B cooperativity at adjacent response elements. J. Biol. Chem 2010, 285:31100-31106.
49. Pradhan M., Baumgarten S.C., Bembinster L.A., Frasor J. CBP mediates NF-kappaB-dependent histone acetylation and estrogen receptor recruitment to an estrogen response element in the BIRC3 promoter. Mol. Cell. Biol 2012, 32:569-575.
50. Reijm E.A., Jansen M.P., Ruigrok-Ritstier K., van Staveren I.L., Look M.P., van Gelder M.E., et al. Decreased expression of EZH2 is associated with upregulation of ER and favorable outcome to tamoxifen in advanced breast cancer. Breast Cancer Res. Treat 2011, 125:387-394.
51. Riggins R.B., Zwart A., Nehra R., Clarke R. The nuclear factor kappa B inhibitor parthenolide restores ICI 182,780 (Faslodex; fulvestrant)-induced apoptosis in antiestrogen-resistant breast cancer cells. Mol. Cancer Ther 2005, 4:33-41.
52. Robinson D.R., Wu Y.M., Vats P., Su F., Lonigro R.J., Cao X., et al. Activating ESR1 mutations in hormone-resistant metastatic breast cancer. Nat. Genet 2013, 45:1446-1451.
53. Santen R.J., Fan P., Zhang Z., Bao Y., Song R.X., Yue W. Estrogen signals via an extra-nuclear pathway involving IGF-1R and EGFR in tamoxifen-sensitive and -resistant breast cancer cells. Steroids 2009, 74:586-594.
54. Sas L., Lardon F., Vermeulen P.B., Hauspy J., Van Dam P., Pauwels P., et al. The interaction between ER and NFkappaB in resistance to endocrine therapy. Breast Cancer Res 2012, 14:212.
55. Schiff R., Massarweh S., Shou J., Osborne C.K. Breast cancer endocrine resistance: how growth factor signaling and estrogen receptor coregulators modulate response. Clin. Cancer Res 2003, 9:447S-454S.
56. Schmitz M.L., Mattioli I., Buss H., Kracht M. NF-kappaB: a multifaceted transcription factor regulated at several levels. Chembiochem 2004, 5:1348-1358.
57. Schuettengruber B., Chourrout D., Vervoort M., Leblanc B., Cavalli G. Genome regulation by polycomb and trithorax proteins. Cell 2007, 128:735-745.
58. Shah Y.M., Rowan B.G. The Src kinase pathway promotes tamoxifen agonist action in Ishikawa endometrial cells through phosphorylation-dependent stabilization of estrogen receptor (alpha) promoter interaction and elevated steroid receptor coactivator 1 activity. Mol. Endocrinol 2005, 19:732-748.
59. Shang Y., Hu X., DiRenzo J., Lazar M.A., Brown M. Cofactor dynamics and sufficiency in estrogen receptor-regulated transcription. Cell 2000, 103:843-852.
60. Sorlie T., Perou C.M., Tibshirani R., Aas T., Geisler S., Johnsen H., et al. Gene expression patterns of breast carcinomas distinguish tumor subclasses with clinical implications. Proc. Natl. Acad. Sci. U.S.A. 2001, 98:10869-10874.
61. Sorlie T., Tibshirani R., Parker J., Hastie T., Marron J.S., Nobel A., et al. Repeated observation of breast tumor subtypes in independent gene expression data sets. Proc. Natl. Acad. Sci. U.S.A. 2003, 100:8418-8423.
62. Sotiriou C., Neo S.Y., McShane L.M., Korn E.L., Long P.M., Jazaeri A., et al. Breast cancer classification and prognosis based on gene expression profiles from a population-based study. Proc. Natl. Acad. Sci. U.S.A. 2003, 100:10393-10398.
63. Stender J.D., Stossi F., Funk C.C., Charn T.H., Barnett D.H., Katzenellenbogen B.S. The estrogen-regulated transcription factor PITX1 coordinates gene-specific regulation by estrogen receptor-alpha in breast cancer cells. Mol. Endocrinol 2011, 25:1699-1709.
64. Tobias J.S. Recent advances in endocrine therapy for postmenopausal women with early breast cancer: implications for treatment and prevention. Ann. Oncol 2004, 15:1738-1747.
65. Toy W., Shen Y., Won H., Green B., Sakr R.A., Will M., et al. ESR1 ligand-binding domain mutations in hormone-resistant breast cancer. Nat. Genet 2013, 45:1439-1445.
66. Tu Z., Prajapati S., Park K.J., Kelly N.J., Yamamoto Y., Gaynor R.B. IKK alpha regulates estrogen-induced cell cycle progression by modulating E2F1 expression. J. Biol. Chem 2006, 281:6699-6706.
67. Umayahara Y., Kawamori R., Watada H., Imano E., Iwama N., Morishima T., et al. Estrogen regulation of the insulin-like growth factor I gene transcription involves an AP-1 enhancer. J. Biol. Chem 1994, 269:16433-16442.
68. Van Laere S.J., Van der Auwera I., Van den Eynden G.G., Elst H.J., Weyler J., Harris A.L., et al. Nuclear factor-kappaB signature of inflammatory breast cancer by cDNA microarray validated by quantitative real-time reverse transcription-PCR, immunohistochemistry, and nuclear factor-kappaB DNA-binding. Clin. Cancer Res 2006, 12:3249-3256.
69. Vogel V.G., Costantino J.P., Wickerham D.L., Cronin W.M., Cecchini R.S., Atkins J.N., et al. Effects of tamoxifen vs raloxifene on the risk of developing invasive breast cancer and other disease outcomes: the NSABP Study of Tamoxifen and Raloxifene (STAR) P-2 trial. JAMA 2006, 295:2727-2741.
70. Wang X., Belguise K., Kersual N., Kirsch K.H., Mineva N.D., Galtier F., et al. Oestrogen signalling inhibits invasive phenotype by repressing RelB and its target BCL2. Nat. Cell Biol 2007, 9:470-478.
71. Wang X., Belguise K., O'Neill C.F., Sanchez-Morgan N., Romagnoli M., Eddy S.F., et al. RelB NF-kappaB represses estrogen receptor alpha expression via induction of the zinc finger protein Blimp1. Mol. Cell. Biol 2009, 29:3832-3844.
72. Weitsman G.E., Li L., Skliris G.P., Davie J.R., Ung K., Niu Y., et al. Estrogen receptor-alpha phosphorylated at Ser118 is present at the promoters of estrogen-regulated genes and is not altered due to HER-2 overexpression. Cancer Res 2006, 66:10162-10170.
73. Yu M., Bardia A., Aceto N., Bersani F., Madden M.W., Donaldson M.C., et al. Cancer therapy. Ex vivo culture of circulating breast tumor cells for individualized testing of drug susceptibility. Science 2014, 345:216-220.
74. Zheng W.Q., Lu J., Zheng J.M., Hu F.X., Ni C.R. Variation of ER status between primary and metastatic breast cancer and relationship to p53 expression*. Steroids 2001, 66:905-910.
75. Zhou Y., Eppenberger-Castori S., Marx C., Yau C., Scott G.K., Eppenberger U., et al. Activation of nuclear factor-kappaB (NFkappaB) identifies a high-risk subset of hormone-dependent breast cancers. Int. J. Biochem. Cell Biol 2005, 37:1130-1144.
76. Zhu P., Baek S.H., Bourk E.M., Ohgi K.A., Garcia-Bassets I., Sanjo H., et al. Macrophage/cancer cell interactions mediate hormone resistance by a nuclear receptor derepression pathway. Cell 2006, 124:615-629.