Tamoxifen increases nuclear respiratory factor 1 transcription by activating estrogen receptor β and AP-1 recruitment to adjacent promoter binding sites

FASEB Journal

Volumn 25, Issue 4, 2011, Pages 1402-1416

  Ivanova, Margarita M ^a   Luken, Kristen H ^a   Zimmer, Amber S ^a   Lenzo, Felicia L ^a   Smith, Ryan J ^a   Arteel, Maia W ^a   Kollenberg, Tara J ^a   Mattingly, Kathleen A ^a   Klinge, Carolyn M ^a  

^a University of Louisville School of Medicine   (United States)

Author keywords

Apoptosis; Breast cancer; Estradiol ER ; PGC 1 ; RNA polymerase; TFAM

Indexed keywords

CALPAIN 1; CYTOCHROME C1; CYTOCHROME C2; ESTRADIOL; ESTROGEN RECEPTOR ALPHA; ESTROGEN RECEPTOR BETA; HISTONE ACETYLTRANSFERASE PCAF; MITOCHONDRIAL TRANSCRIPTION FACTOR A; MITOGEN ACTIVATED PROTEIN KINASE; NUCLEAR RESPIRATORY FACTOR 1; PHOSPHATIDYLINOSITOL 3 KINASE; PROTEIN C FOS; PROTEIN C JUN; PROTEIN KINASE B; RNA POLYMERASE II; SMALL INTERFERING RNA; TAMOXIFEN; TRANSCRIPTION FACTOR AP 1;

APOPTOSIS; ARTICLE; BINDING AFFINITY; BINDING SITE; CELL STRAIN MCF 7; CONTROLLED STUDY; ESTROGEN ACTIVITY; ESTROGEN RESPONSIVE ELEMENT; GENE DELETION; GENE EXPRESSION; GENE OVEREXPRESSION; GENE TARGETING; HUMAN; HUMAN CELL; INTRACELLULAR SIGNALING; PRIORITY JOURNAL; PROMOTER REGION; PROTEIN PHOSPHORYLATION; RECEPTOR BINDING; TRANSCRIPTION REGULATION; TRANSIENT TRANSFECTION;

APOPTOSIS; BINDING SITES; CELL LINE, TUMOR; ESTROGEN RECEPTOR ALPHA; ESTROGEN RECEPTOR BETA; HUMANS; NUCLEAR RESPIRATORY FACTOR 1; PROMOTER REGIONS, GENETIC; RETINOIDS; SIGNAL TRANSDUCTION; TAMOXIFEN; TRANSCRIPTION FACTOR AP-1; TRANSCRIPTION, GENETIC;

EID: 79954576048     PISSN: 08926638     EISSN: 15306860     Source Type: Journal    
DOI: 10.1096/fj.10-169029     Document Type: Article

References (73)

1. Jordan, V. C. (2009) A century of deciphering the control mechanisms of sex steroid action in breast and prostate cancer: the origins of targeted therapy and chemoprevention. Cancer Res. 69, 1243-1254
2. Burstein, H. J., Prestrud, A. A., Seidenfeld, J., Anderson, H., Buchholz, T. A., Davidson, N. E., Gelmon, K E., Giordano, S. H., Hudis, C. A., Malin, J., Mamounas, E. P., Rowden, D., Solky, A. J., Sowers, M. R., Stearns, V., Winer, E. P., Somerfield, M. R., and Griggs, J. J. (2010) American Society of Clinical Oncology clinical practice guideline: update on adjuvant endocrine therapy for women with hormone receptor-positive breast cancer. J. Clin. Oncol. 28, 3784-3796
3. Sotoca Covaleda, A. M., van den Berg, H., Vervoort, J., van der Saag, P., Strom, A., Gustafsson, J.-A., Rietjens, I., and Murk, A. J. (2008) Influence of cellular ERαERβ ratio on the ERα-agonist induced proliferation of human T47D breast cancer cells. Toxicol. Sci. 105, 303-311
4. Welboren, W.-J., Sweep, F. C. G. J., Span, P. N., and Stunnenberg, H. G. (2009) Genomic actions of estrogen receptor α: what are the targets and how are they regulated? Endocr. Relat. Cancer 16, 1073-1089
5. Berry, M., Metzger, D., and Chambon, P. (1990) Role of the two activating domains of the oestrogen receptor in the cell-type and promoter-context dependent agonistic activity of the anti-oestrogen 4-hydroxytamoxifen. EMBO J. 9, 2811-2818
6. Lewis, J. S., and Jordan, V. C. (2005) Selective estrogen receptor modulators (SERMs): mechanisms of anticarcinogenesis and drug resistance. Mutat. Res. 591, 247-263 (Pubitemid 41654853)
7. Shang, Y., and Brown, M. (2002) Molecular determinants for the tissue specificity of SERMs. Science 295, 2465-2468 (Pubitemid 34270263)
8. Delaunay, F., Pettersson, K., Tujague, M., and Gustafsson, J. A (2000) Functional differences between the amino-terminal domains of estrogen receptors alpha and beta. Mol. Pharmacol. 58, 584-590
9. Paech, K., Webb, P., Kuiper, G. G., Nilsson, S., Gustafsson, J., Kushner, P. J., and Scanlan, T. S. (1997) Differential ligand activation of estrogen receptors ERalpha and ERbeta at AP1 sites. Science 277, 1508-1510 (Pubitemid 27449239)
10. Kushner, P. J., Agard, D. A., Greene, G. L., Scanlan, T. S., Shiau, A. K., Uht, R. M., and Webb, P. (2000) Estrogen receptor pathways to AP-1. J. Steroid Biochem. Mol. Biol. 74, 311-317 (Pubitemid 32126243)
11. Charn, T. H., Liu, E. T.-B., Chang, E. C., Lee, Y. K., Katzenellenbogen, J. A., and Katzenellenbogen, B. S. (2010) Genomewide dynamics of chromatin binding of estrogen receptors α and β: mutual restriction and competitive site selection. Mol. Endocrinol. 24, 47-59
12. Chang, E. C., Frasor, J., Komm, B., and Katzenellenbogen, B. S. (2006) Impact of estrogen receptor β on gene networks regulated by estrogen receptor α in breast cancer cells. Endocrinology 147, 4831-4842 (Pubitemid 44402189)
13. Liu, Y., Gao, H., Marstrand, T. T., Ström, A., Valen, E., Sandelin, A., Gustafsson, J.-Å., and Dahlman-Wright, K (2008) The genome landscape of ERa-and ERβ-binding DNA regions. Proc. Natl. Acad. Sci. 105, 2604-2609 (Pubitemid 351520560)
14. Vivar, O. I., Zhao, X., Saunier, E. F., Griffin, C., Mayba, O. S., Tagliaferri, M., Cohen, I., Speed, T. P., and Leitman, D. C. (2010) Estrogen receptor β binds to and regulates three distinct classes of target genes. J. Biol. Chem. 285, 22059-22066
15. Paruthiyil, S., Parmar, H., Kerekatte, V., Cunha, G. R., Firestone, G. L., and Leitman, D. C. (2004) Estrogen receptor beta inhibits human breast cancer cell proliferation and tumor formation by causing a G (2) cell cycle arrest. Cancer Res. 64, 423-428 (Pubitemid 38114127)
16. Hodges-Gallagher, L., Valentine, C. D., El Bader, S., and Kushner, P. J. (2008) Estrogen receptor beta increases the efficacy of antiestrogens by effects on apoptosis and cell cycling in breast cancer cells. Breast Cancer Res. Treat. 109, 241-250 (Pubitemid 351644839)
17. Levy, N., Paruthiyil, S., Zhao, X., Vivar, O. I., Saunier, E. F., Griffin, C., Tagliaferri, M., Cohen, I., Speed, T. P., and Leitman, D. C. (2010) Unliganded estrogen receptor-β regulation of genes is inhibited by tamoxifen. Mol. Cell. Endocrinol. 315, 201-207
18. Sripathy, S. P., Chaplin, L. J., Gaikwad, N. W., Rogan, E. G., and Montano, M. M. (2008) hPMC2 is required for recruiting an ERβ coactivator complex to mediate transcriptional upregulation of NQO1 and protection against oxidative DNA damage by tamoxifen. Oncogene 27, 6376-6384
19. Mattingly, K. A., Ivanova, M. M., Riggs, K. A., Wickramasinghe, N. S., Barch, M. J., and Klinge, C. M. (2008) Estradiol stimulates transcription of nuclear respiratory factor-1 and increases mitochondrial biogenesis. Mol. Endocrinol. 22, 609-622 (Pubitemid 351397789)
20. Scarpulla, R. C. (2008) Nuclear control of respiratory chain expression by nuclear respiratory factors and PGC-1-related coactivator. Ann. N. Y. Acad. Sci. 1147, 321-334
21. Nehra, R., Riggins, R. B., Shajahan, A. N., Zwart, A., Crawford, A. C., and Clarke, R. (2010) BCL2 and CASP8 regulation by NF-kB differentially affect mitochondrial function and cell fate in antiestrogen-sensitive and-resistant breast cancer cells. FASEB J. 24, 2040-2055
22. Kisanga, E. R., Gjerde, J., Guerrieri-Gonzaga, A., Pigatto, F., Pesci-Feltri, A., Robertson, C., Serrano, D., Pelosi, G., Decensi, A, and Lien, E. A. (2004) Tamoxifen and metabolite concentrations in serum and breast cancer tissue during three dose regimens in a randomized preoperative trial. Clin. Cancer Res. 10, 2336-2343 (Pubitemid 38445691)
23. Virbasius, C. A., Virbasius, J. V., and Scarpulla, R. C. (1993) NRF-1, an activator involved in nuclear-mitochondrial interactions, utilizes a new DNA-binding domain conserved in a family of developmental regulators. Genes Dev. 7, 2431-2445 (Pubitemid 24003245)
24. Kulakosky, P. C., McCarty, M. A., Jernigan, S. C., Risinger, K. E., and Klinge, C. M. (2002) Response element sequence modulates estrogen receptor alpha and beta affinity and activity. J. Mol. Endocrinol. 29, 137-152 (Pubitemid 34965752)
25. Bourdeau, V., Deschenes, J., Metivier, R., Nagai, Y., Nguyen, D., Bretschneider, N., Gannon, F., White, J. H., and Mader, S. (2004) Genome-wide identification of high-affinity estrogen response elements in human and mouse. Mol. Endocrinol. 18, 1411-1427 (Pubitemid 38692179)
26. Zhao, C., Matthews, J., Tujague, M., Wan, J., Strom, A., Toresson, G., Lam, E. W. F., Cheng, G., Gustafsson, J.-A., and Dahlman-Wright, K. (2007) Estrogen receptor β2 negatively regulates the transactivation of estrogen receptor α in human breast cancer cells. Cancer Res. 67, 3955-3962 (Pubitemid 46762185)
27. Klinge, C. M., Peale, F. V., Jr., Hilf, R., Bambara, R. A., and Zain, S. (1992) Cooperative estrogen receptor interaction with consensus or variant estrogen responsive elements in vitro. Cancer Res. 52, 1073-1081
28. DuSell, C. D., Nelson, E. R., Wittmann, B. M., Fretz, J. A., Kazmin, D., Thomas, R. S., Pike, J. W., and McDonnell, D. P. (2010) Regulation of aryl hydrocarbon receptor function by selective estrogen receptor modulators. Mol. Endocrinol. 24, 33-46
29. Paige, L. A., Christensen, D. J., Gron, H., Norris, J. D., Gottlin, E. B., Padilla, K. M., Chang, C.-Y., Ballas, L. M., Hamilton, P. T., McDonnell, D. P., and Fowlkes, D. M. (1999) Estrogen receptor (ER) modulators each induce distinct conformational changes in ER alpha and ER beta. Proc. Natl. Acad. Sci. U. S. A. 96, 3999-4004 (Pubitemid 29169025)
30. Choi, Y. S., Lee, K. U., and Pak, Y K. (2004) Regulation of mitochondrial transcription factor A expression by high glucose. Ann. N. Y. Acad. Sci. 1011, 69-77 (Pubitemid 38608393)
31. Wijayaratne, A. L., and McDonnell, D. P. (2001) The human estrogen receptor-alpha is a ubiquitinated protein whose stability is affected differentially by agonists, antagonists, and selective estrogen receptor modulators. J. Biol. Chem. 276, 35684-35692
32. Peekhaus, N., Chang, T., Hayes, E., Wilkinson, H., Mitra, S., Schaeffer, J., and Rohrer, S. (2004) Distinct effects of the antiestrogen Faslodex on the stability of estrogen receptorsalpha and-beta in the breast cancer cell line MCF-7. J. Mol. Endocrinol. 32, 987-995 (Pubitemid 38877699)
33. Felty, Q., Xiong, W. C., Sun, D., Sarkar, S., Singh, K. P., Parkash, J., and Roy, D. (2005) Estrogen-induced mitochondrial reactive oxygen species as signal-transducing messengers. Biochemistry 44, 6900-6909 (Pubitemid 40632408)
34. Duong, V., Licznar, A., Margueron, R., Boulle, N., Busson, M., Lacroix, M., Katzenellenbogen, B. S., Cavailles, V., and Lazennec, G. (2006) ERalpha and ERbeta expression and transcriptional activity are differentially regulated by HDAC inhibitors. Oncogene 25, 1799-1806
35. Liu, X.-F., and Bagchi, M. K. (2004) Recruitment of distinct chromatin-modifying complexes by tamoxifen-complexed estrogen receptor at natural target gene promoters in vivo. J. Biol. Chem. 279, 15050-15058 (Pubitemid 38618898)
36. Gillesby, B. E., Stanostefano, M., Porter, W., Safe, S., Wu, Z. F., and Zacharewski, T. R. (1997) Identification of a motif within the 5' regulatory region of pS2 which is responsible for AP-1 binding and TCDD-mediated suppression. Biochemistry 36, 6080-6089 (Pubitemid 27257874)
37. Metivier, R., Penot, G., Hubner, M. R., Reid, G., Brand, H., Kos, M., and Gannon, F. (2003) Estrogen receptor-alpha directs ordered, cyclical, and combinatorial recruitment of cofactors on a natural target promoter. Cell 115, 751-763 (Pubitemid 38030303)
38. Kininis, M., Chen, B. S., Diehl, A. G., Isaacs, G. D., Zhang, T., Siepel, A. C., Clark, A. G., and Kraus, W. L. (2007) Genomic analyses of transcription factor binding, histone acetylation, and gene expression reveal mechanistically distinct classes of estrogen-regulated promoters. Mol. Cell. Biol. 27, 5090-5104 (Pubitemid 47068284)
39. Mohamood, A. S., Gyles, P., Balan, K. V., Hollis, V. W., Eckberg, W. R., Asseffa, A., Han, Z., Wyche, J. H., and Anderson, W. A (1997) Estrogen receptor, growth factor receptor and protooncogene protein activities and possible signal transduction crosstalk in estrogen dependent and independent breast cancer cell lines. J. Submicrosc. Cytol. Pathol. 29, 1-17 (Pubitemid 127462168)
40. Klinge, C. M. (1999) Estrogen receptor binding to estrogen response elements slows ligand dissociation and synergistically activates reporter gene expression. Mol. Cell. Endocrinol. 150, 99-111 (Pubitemid 29292855)
41. Huang, C., Ma, W. Y., Dawson, M. I., Rincon, M., Flavell, R. A., and Dong, Z. (1997) Blocking activator protein-1 activity, but not activating retinoic acid response element, is required for the antitumor promotion effect of retinoic acid. Proc. Natl. Acad. Sci. U. S. A. 94, 5826-5830 (Pubitemid 27241856)
42. Li, J. J., Westergaard, C., Ghosh, P., and Colburn, N. H. (1997) Inhibitors of both nuclear factor-kappaB and activator protein-1 activation block the neoplastic transformation response. Cancer Res. 57, 3569-3576 (Pubitemid 27355509)
43. Fisch, T. M., Prywes, R., and Roeder, R. G. (1989) An AP1-binding site in the c-fos gene can mediate induction by epidermal growth factor and 12-O-tetradecanoyl phorbol-13-acetate. Mol. Cell. Biol. 9, 1327-1331 (Pubitemid 19071701)
44. Uht, R., Webb, P., Nguyen, P., Price Jr., R., Valentine, C, Favre, H., and Kushner, P. (2004) A conserved lysine in the estrogen receptor DNA binding domain regulates ligand activation profiles at AP-1 sites, possibly by controlling interactions with a modulating repressor. Nucl. Recept. 2, 2
45. Perumal, S. S., Shanthi, P., and Sachdanandam, P. (2005) Therapeutic effect of tamoxifen and energy-modulating vitamins on carbohydrate-metabolizing enzymes in breast cancer. Cancer Chemother. Pharmacol. 56, 105-114 (Pubitemid 41201763)
46. Kelly, D. P., and Scarpulla, R. C. (2004) Transcriptional regulatory circuits controlling mitochondrial biogenesis and function. Genes Dev. 18, 357-368 (Pubitemid 38316342)
47. Piantadosi, C. A., and Suliman, H. B. (2006) Mitochondrial transcription factor A induction by redox activation of nuclear respiratory factor 1. J. Biol. Chem. 281, 324-333 (Pubitemid 43671192)
48. Liu, Z., Yu, X., and Shaikh, Z. A. (2008) Rapid activation of ERK1/2 and AKT in human breast cancer cells by cadmium. Toxicol. Appl. Pharmacol. 228, 286-294
49. Monroe, D. G., Berger, R. R., and Sanders, M. M. (2002) Tissue-protective effects of estrogen involve regulation of caspase gene expression. Mol. Endocrinol. 16, 1322-1331 (Pubitemid 34621079)
50. Bowie, M. L., Dietze, E. C., Delrow, J., Bean, G. R., Troch, M. M., Marjoram, R. J., and Seewaldt, V. L. (2004) Interferonregulatory factor-1 is critical for tamoxifen-mediated apoptosis in human mammary epithelial cells. Oncogene 23, 8743-8755 (Pubitemid 39593289)
51. Vladusic, E. A., Hornby, A. E., Guerra-Vladusic, F. K., Lakins, J., and Lupu, R. (2000) Expression and regulation of estrogen receptor beta in human breast tumors and cell lines. Oncol. Rep. 7, 157-167
52. Frasor, J., Chang, E. C., Komm, B., Lin, C.-Y., Vega, V. B., Liu, E. T., Miller, L. D., Smeds, J., Bergh, J., and Katzenellenbogen, B. S. (2006) Gene expression preferentially regulated by tamoxifen in breast cancer cells and correlations with clinical outcome. Cancer Res. 66, 7334-7340 (Pubitemid 44197716)
53. Safe, S., and Kim, K. (2008) Non-classical genomic estrogen receptor (ER)/specificity protein and ER/activating protein-1 signaling pathways. J. Mol. Endocrinol. 41, 263-275
54. Cheung, E., Acevedo, M. L., Cole, P. A., and Kraus, W. L. (2005) Altered pharmacology and distinct coactivator usage for estrogen receptor-dependent transcription through activating protein-1. Proc. Natl. Acad. Sci. U. S. A. 102, 559-564 (Pubitemid 40282704)
55. Ring, A., and Dowsett, M. (2004) Mechanisms of tamoxifen resistance. Endocr. Relat. Cancer 11, 643-658 (Pubitemid 40065543)
56. Bourdoncle, A., Labesse, G., Margueron, R., Castet, A., Cavailles, V., and Royer, C. A. (2005) The nuclear receptor coactivator PGC-1α exhibits modes of interaction with the estrogen receptor distinct from those of SRC-1. J. Mol. Biol. 347, 921-934 (Pubitemid 40387444)
57. Zhao, C., Dahlman-Wright, K., and Gustafsson, J.-Å. (2010) Estrogen signaling via estrogen receptor β. J. Biol. Chem. 285, 39575-39579
58. Wu, Z., Puigserver, P., Andersson, U., Zhang, C., Adelmant, G., Mootha, V., Troy, A., Cinti, S., Lowell, B., Scarpulla, R. C., and Spiegelman, B. M. (1999) Mechanisms controlling mitochondrial biogenesis and respiration through the thermogenic coactivator PGC-1. Cell 98, 115-124 (Pubitemid 29331201)
59. Tcherepanova, I., Puigserver, P., Norris, J. D., Spiegelman, B. M., and McDonnell, D. P. (2000) Modulation of estrogen receptor-alpha transcriptional activity by the coactivator PGC-1. J. Biol. Chem. 275, 16302-16308 (Pubitemid 30366945)
60. Flageng, M. H., Haugan Moi, L. L., Dixon, J. M., Geisler, J., Lien, E. A., Miller, W. R., Lonning, P. E., and Mellgren, G. (2009) Nuclear receptor co-activators and HER-2/neu are upregulated in breast cancer patients during neo-adjuvant treatment with aromatase inhibitors. Br. J. Cancer 101, 1253-1260
61. O'Lone, R., Knorr, K., Jaffe, I. Z., Schaffer, M. E., Martini, P. G. V., Karas, R. H., Bienkowska, J., Mendelsohn, M. E., and Hansen, U. (2007) Estrogen receptors α and β mediate distinct pathways of vascular gene expression, including genes involved in mitochondrial electron transport and generation of reactive oxygen species. Mol. Endocrinol. 21, 1281-1296 (Pubitemid 46991958)
62. Jayachandran, M., Preston, C. C., Hunter, L. W., Jahangir, A., Owen, W. G., Korach, K. S., and Miller, V. M. (2010) Loss of estrogen receptor beta decreases mitochondrial energetic potential and increases thrombogenicity of platelets in aged female mice. Age (Dordr.) 32, 109-121
63. Klinge, C. M. (2001) Estrogen receptor interaction with estrogen response elements. Nucleic Acids Res. 29, 2905-2919 (Pubitemid 32685217)
64. Baron, S., Escande, A., Alberola, G., Bystricky, K., Balaguer, P., and Richard-Foy, H. (2007) Estrogen receptor α and the activating protein-1 complex cooperate during insulin-like growth factor-i-induced transcriptional activation of the pS2/TFF1 Gene. J. Biol. Chem. 282, 11732-11741 (Pubitemid 47100665)
65. Picard, N., Charbonneau, C., Sanchez, M., Licznar, A., Busson, M., Lazennec, G., and Tremblay, A. (2008) Phosphorylation of activation function-1 regulates proteasome-dependent nuclear mobility and E6-associated protein ubiquitin ligase recruitment to the estrogen receptor β. Mol. Endocrinol. 22, 317-330 (Pubitemid 351192911)
66. Shah, Y. M., and Rowan, B. G. (2005) The Src kinase pathway promotes tamoxifen agonist action in ishikawa endometrial cells through phosphorylation-dependent stabilization of estrogen receptor α promoter interaction and elevated steroid receptor coactivator 1 activity. Mol. Endocrinol. 19, 732-748 (Pubitemid 40349444)
67. Yoo, Y. A., Kim, Y H., Kim, J. S., and Seo, J. H. (2008) The functional implications of Akt activity and TGF-β signaling in tamoxifen-resistant breast cancer. Biochim. Biophys. Acta Mol. Cell Res. 1783, 438-447
68. Bruni, F., Polosa, P. L., Gadaleta, M. N., Cantatore, P., and Roberti, M. (2010) Nuclear respiratory factor 2 induces the expression of many but not all human proteins acting in mitochondrial DNA transcription and replication. J. Biol. Chem. 285, 3939-3948
69. Asangani, I. A., Rasheed, S. A. K., Leupold, J. H., Post, S., and Allgayer, H. (2008) NRF-1, and AP-1 regulate the promoter of the human calpain small subunit 1 (CAPNS1) gene. Gene 410, 197-206
70. Tan, Y., Wu, C., De Veyra, T., and Greer, P. A. (2006) Ubiquitous calpains promote both apoptosis and survival signals in response to different cell death stimuli. J. Biol. Chem. 281, 17689-17698 (Pubitemid 44035567)
71. Buck, M. B., Pfizenmaier, K., and Knabbe, C. (2004) Antiestrogens induce growth inhibition by sequential activation of p38 mitogen-activated protein kinase and transforming growth factor-β pathways in human breast cancer cells. Mol. Endocrinol. 18, 1643-1657 (Pubitemid 38859573)
72. Mandlekar, S., and Kong, A. N. (2001) Mechanisms of tamoxifen-induced apoptosis. Apoptosis 6, 469-477 (Pubitemid 33078758)
73. O'Malley, B. W. (2009) The "fourth dimension" of gene transcription. Mol. Endocrinol. 23, 587-589