165
Views
4
CrossRef citations to date
0
Altmetric
Research Article

ERα dimerization: a key factor for the weak estrogenic activity of an ERα modulator unable to compete with estradiol in binding assays

, , , , , , & show all
Pages 149-166 | Received 03 Mar 2016, Accepted 12 Jun 2016, Published online: 12 Jul 2016

References

  • Jacquot Y, Bermont L, Giorgi H, et al. Substituted benzopyranobenzothiazinones. Synthesis and estrogenic activity on MCF-7 breast carcinoma cells. Eur J Med Chem 2001;36:127–36.
  • Jacquot Y, Cleeren A, Laios I, et al. Pharmacological profile of 6,12-dihydro-3-methoxy-1-benzopyrano[3,4-b] [1,4]benzothiazin-6-one, a novel human estrogen receptor agonist. Biol Pharm Bull 2002;25:335–41.
  • Jacquot Y, Rojas C, Refouvelet B, et al. Recent advances in the development of phytoestrogens and derivatives: an update of the promising perspectives in the prevention of postmenopausal diseases. Mini Rev Med Chem 2003;3:387–400.
  • Bourgoin-Voillard S, Gallo D, Laïos I, et al. Capacity of type I and II ligands to confer to estrogen receptor alpha an appropriate conformation for the recruitment of coactivators containing a LxxLL motif – relationship with the regulation of receptor level and ERE-dependent transcription in MCF-7 cells. Biochem Pharmacol 2010;79:746–57.
  • Leclercq G, Lacroix M, Laïos I, Laurent G. Estrogen receptor alpha: impact of ligands on intracellular shuttling and turnover rate in breast cancer cells. Curr Cancer Drug Targets 2006;6:39–64.
  • El Khissiin A, Leclercq G. Implication of proteasome in estrogen receptor degradation. FEBS Lett 1997;448:160–6.
  • Marsaud V, Gougelet A, Maillard S, Renoir JM. Various phosphorylation pathways, depending on agonist and antagonist binding, differentially affect ERalpha extractability, proteasome-mediated stability, and transcriptional activity in human breast cancer cells. Mol Endocrinol 2003;17:2013–27.
  • Gust R, Keilitz R, Schmidt K. Synthesis structural evaluation, and estrogen receptor interaction of 2,3-diarylpiperazines. J Med Chem 2002;45:2325–37.
  • von Rauch M, Schlenk M, Gust R. Effects of C2-alkylation, N-alkylation, and N,N′-dialkylation on the stability and estrogen receptor interaction of (4R,5S)/(4S/5R)-4,5-bis(4-hydroxyphenyl)-2-imidazolines. J Med Chem 2004;47:915–27.
  • von Rauch M, Busch S, Gust R. Investigations on the effects of basic side chains on the hormonal profile of (4R,5S)/(4S,5R)-4,5-bis(4-hydroxyphenyl)-2-imidazolines. J Med Chem 2005;48:466–74.
  • Laïos I, Cleeren A, Leclercq G, et al. Effects of (R,S)/(S,R)-4,5-bis(2-chloro-4-hydroxyphenyl)-2-imidazolines and (R,S)/(S,R)-2,3-bis(2-chloro-4-hydroxyphenyl)piperazines on estrogen receptor alpha level and transcriptional activity in MCF-7 cells. Biochem Pharmacol 2007;74:1029–38.
  • Jacquot Y, Refouvelet B, Bermont L, et al. Synthesis and cytotoxic activity of new 2,4-diaryl-4H,5H-pyrano[3,2-c]benzopyran-5-ones on MCF-7 cells. Pharmazie 2002;57:233–7.
  • Jacquot Y, Laïos I, Cleeren A, et al. Synthesis, structure, and estrogenic activity of 4-amino-3-(2-methylbenzyl)coumarins on human breast carcinoma cells. Bioorg Med Chem 2007;15:2269–82.
  • Jacquot Y, Byrne C, Xicluna A, Leclercq G. Synthesis, structure, and estrogenic activity of 2- and 3-substituted 2,3-dihydro-4H-1-benzopyran-4-ones. Med Chem Res 2013;22:681–91.
  • Jordan VC, Schafer JM, Levenson AS, et al. Molecular classification of estrogens. Cancer Res 2001;61:6619–23.
  • Stoessel S, Leclercq G. Competitive binding assay for estrogen receptor in monolayer culture: measure of receptor activation potency. J Steroid Biochem 1986;25:677–82.
  • Laïos I, Journé F, Nonclercq D, et al. Role of the proteasome in the regulation of estrogen receptor alpha turnover and function in MCF-7 breast carcinoma cells. J Steroid Biochem Mol Biol 2005;94:347–59.
  • Berthier A, Elie-Caille C, Lesniewska E, et al. Atomic force spectroscopy and label-free sensing for the characterization of protein–protein and protein–DNA interactions. Application to estrogen receptors. J Mol Recogn 2011;24:429–35.
  • Elie-Caille C, Rauch JY, Rouleau A, Boireau W. Preparation of flat gold terraces for protein chip development. Micro Nano Lett 2009;4:88–94.
  • Journé F, Chaboteaux C, Dumon JC, et al. Steroid-free medium discloses oestrogenic effects of the bisphosphonate clodronate on breast cancer cells. Br J Cancer 2004;91:1703–10.
  • Agouridas V, Laïos I, Cleeren A, et al. Loss of antagonistic activity of tamoxifen by replacement of one N-methyl of its side chain by fluorinated residues. Bioorg Med Chem 2006;14:7531–8.
  • Pons M, Gagne D, Nicolas JC, Mehtalli M. A new cellular model of response to estrogens: a bioluminescent test to characterize (anti) estrogen molecules. Biotechniques 1990;9:450–9.
  • Astruc ME, Chabret C, Bali P, et al. Prolonged treatment of breast cancer cells with antiestrogens increases the activating protein-1-mediated response: involvement of the estrogen receptor. Endocrinology 1995;136:824–32.
  • El Khissin A, Leclercq G. Exchange of bound estrogens and antiestrogens in MCF-7 cells: evidence for ligand-induced stable configurations of the estrogen receptor. Steroids 1998;63:565–74.
  • van Hoorn WP. Identification of a second binding site in the estrogen receptor. J Med Chem 2002;45:584–9.
  • Norman A, Mizwicki MT, Norman DPG. Steroid-hormone rapid actions, membrane receptors and a conformational ensemble model. Nat Rev Drug Discov 2004;3:27–41.
  • Mizwicki MT, Keidel D, Bula CM, et al. Identification of an alternative ligand-binding pocket in the nuclear vitamin D receptor and its functional importance in 1alpha,25(OH)2-vitamin D3 signaling. Proc Natl Acad Sci USA 2004;101:12876–81.
  • Ma Y, Tomita Y, Preet A, et al. Small-molecule “re antagonists of estrogen receptor-α” are antagonists of estrogen. Mol Endocrinol 2014;28:1971–86.
  • Wang Y, Chirgadze NY, Briggs SL, et al. A second binding site for hydroxytamoxifen within the coactivator-binding groove of estrogen receptor beta. Proc Natl Acad Sci USA 2006;103:9908–11.
  • Kojetin DJ, Burris TP, Jensen EV, Khan SA. Implications of the binding of tamoxifen to the coactivator recognition site of the estrogen receptor. Endocr Relat Cancer 2008;15:851–70.
  • Moore TW, Mayne CG, Katzenellenbogen JA. Minireview: not picking pockets: nuclear receptor alternate-site modulators (NRAMs). Mol Endocrinol 2010;24:683–95.
  • Roy U, Luck LA. Molecular modeling of estrogen receptor using molecular operating environment. Biochem Mol Biol Educ 2007;35:238–43.
  • Leclercq G, Gallo D, Cossy J, et al. Peptides targeting estrogen receptor alpha-potential applications for breast cancer treatment. Curr Pharm Design 2001;17:2632–53.
  • Bizzarri AR, Cannistraro S. The application of atomic force spectroscopy to the study of biological complexes undergoing a biorecognition process. Chem Soc Rev 2010;39:734–49.
  • Tamrazi A, Carlson KE, Daniels JR, et al. Estrogen receptor dimerization: ligand binding regulates dimer affinity and dimer dissociation rate. Mol Endocrinol 2002;16:2706–19.
  • Chandsawangbhuwana C, Baker ME. 3D models of human ERα and ERβ complexed with coumestrol. Steroids 2014;80:37–43.
  • Kushner PJ, Agard DA, Greene GL, et al. Estrogen receptor pathways to AP-1. J Steroid Biochem Mol Biol 2000;74:311–17.
  • Maselli A, Pierdominici M, Vitale C, Ortone E. Membrane lipid rafts and estrogenic signalling: a functional role in the modulation of cell homeostasis. Apoptosis 2015;20:671–8.
  • Nag S, Mokha SS. Activation of a Gq-coupled membrane estrogen receptor rapidly attenuates α2-adrenoceptor-induced nociception via an ERKI/II-dependent, non-genomic mechanism in the female rat. Neuroscience 2014;267:122–34.
  • Ali S, Coombes C. Endocrine-responsive breast cancer and strategies for combating resistance. Nat Rev Cancer 2002;2:101–15.
  • Visram H, Greer PA. 17beta-estradiol and tamoxifen stimulate rapid and transient ERK activation in MCF-7 cells via distinct signaling mechanisms. Cancer Biol Ther 2006;5:1677–82.
  • Kang K, Lee SB, Jung SH, et al. Tectoridin, a poor ligand of estrogen receptor alpha, exerts its estrogenic effects via an ERK-dependent pathway. Mol. Cells 2009;27:351–7.
  • Leiber D, Burlina F, Byrne C, et al. The sequence Pro295-Thr311 of the hinge region of oestrogen receptor α is involved in ERK1/2 activation via GPR30 in leiomyoma cells. Biochem J 2015;472:97–109.
  • Pedram A, Razandi M, Sainson RCA, et al. A conserved mechanism for steroid receptor translocation to the plasma membrane. J Biol Chem 2007;282:22278–88.
  • La Rosa P, Pesiri V, Leclercq G, et al. Palmitoylation regulates 17β-estradiol-induced estrogen receptor-α degradation and transcriptional activity. Mol Endocrinol 2012;26:762–74.
  • Acconcia F, Ascenzi P, Bocedi A, et al. Palmitoylation-dependent estrogen receptor alpha membrane localization: regulation by 17beta-estradiol. Mol Biol Cell 2005;16:231–7.
  • Agell N, Bachs O, Rocamora N, Villalonga P. Modulation of the Ras/Raf/MEK/ERK pathway by Ca(2+), and calmodulin. Cell Signal 2002;14:649–54.
  • Giretti MS, Fu XD, De Rosa G, et al. Extra-nuclear signalling of estrogen receptor to breast cancer cytoskeletal remodelling, migration and invasion. PLoS One 2008;3:e2238.
  • Razandi M, Pedram A, Merchenthaler I, et al. Plasma membrane estrogen receptors exist and functions as dimers. Mol Endocrinol 2004;18:2854–65.
  • Razandi M, Pedram A, Levin ER. Heat shock protein 27 is required for sex steroid receptor trafficking to and functioning at the plasma membrane. Mol Cell Biol 2010;30:3249–61.
  • Kuiper GGJ, Lemmen JG, Carlsson B, et al. Interaction of estrogenic chemicals and phytoestrogens with estrogen receptor β. Endocrinology 1998;139:4252–63.
  • Delfosse V, Grimaldi M, Pons JL, et al. Structural and mechanistic insights into bisphenols action provide guidelines for risk assessment and discovery of bisphenol A substitutes. Proc Natl Acad Sci USA 2012;109:14930–5.
  • Li L, Wang Q, Zhang Y, et al. The molecular mechanism of bisphenol A (BPA) as an endocrine disruptor by interacting with nuclear receptors: insights from molecular dynamics (MD) stimulations. PLoS One 2015;10:e0120330.
  • Tanenbaum DM, Wang Y, Williams SP, Sigler PB. Crystallographic comparison of the estrogen and progesterone receptor's ligand binding domains. Proc Natl Acad Sci USA 1998;95:5998–6003.
  • Ekena K, Weis KE, Katzenellenbogen JA, Katzenellenbogen BS. Identification of amino acids in the hormone binding domain of the human estrogen receptor important in estrogen binding. J Biol Cell 1996;271:20053–9.
  • Ekena K, Katzenellenbogen JA, Katzenellenbogen BS. Determinants of ligand specificity of estrogen receptor-alpha: estrogen versus androgen discrimination. J Biol Chem 1998;273:693–9.
  • Shiau AK, Barstad D, Loria PM, et al. The structural basis of estrogen receptor/coactivator recognition and the antagonism of this interaction by tamoxifen. Cell 1998;95:927–37.
  • Fang H, Tong W, Shi LM, et al. Structure-activity relationships for a large diverse set of natural, synthetic, and environmental estrogens. Chem Res Toxicol 2001;14:280–94.
  • Bentrem D, Fox JE, Pearce ST, et al. Distinct molecular conformations of the estrogen receptor alpha complex exploited by environmental estrogens. Cancer Res 2003;63:7490–6.
  • Delfosse V, Grimaldi M, Cavaillès V, et al. Structural and functional profiling of environmental ligands for estrogen receptors. Environ Health Perspect 2014;122:1306–13.
  • Fadiel A, Song J, Tivon D, et al. Phenytoin is an estrogen receptor α-selective modulator that interacts with helix 12. Reprod Sci 2015;22:146–55.
  • Fanning SW, Mayne CG, Dharmarajan V, et al. Estrogen receptor alpha somatic mutations Y537S and D538G confer breast cancer endocrine resistance by stabilizing the activating function-2 binding conformation. Elife 2016;5:e12792.
  • D'Ursi P, Salvi E, Fossa P, et al. Modelling the interaction of steroid receptors with endocrine disrupting chemicals. BMC Bioinformat 2005;6:S10.
  • Powers CN, Setzer WN. A molecular docking study of phytochemical estrogen mimics from dietary herbal supplements. In Silico Pharmacol 2015;3:4.
  • Niinivehmas SP, Manivannan E, Rauhamäki S, et al. Identification of estrogen receptor α ligands with virtual screening techniques. J Mol Graph Model 2016;64:30–9.
  • Webb P, Lopez GN, Uht RM, Kushner PJ. Tamoxifen activation of the estrogen receptor/AP-1 pathway: potential origin for the cell-specific estrogen-like effects of antiestrogens. Mol Endocrinol 1995;9:443–56.
  • Weatherman RV, Clegg NJ, Scanlan TS. Differential SERM activation of the estrogen receptors (ERalpha and ERbeta) at AP-1 sites. Chem Biol 2001;8:427–36.
  • Jordan VC. Linking estrogen-induced apoptosis with decreases in mortality following long-term adjuvant tamoxifen therapy. J Natl Cancer Inst 2014;106:dju296.
  • Lykkesfeldt A, Madsen MW, Briand P. Altered expression of estrogen-regulated genes in a tamoxifen-resistant and ICI 164,384 and ICI 182,780 sensitive human breast cancer cell line, MCF-7/TAMR-1. Cancer Res 1994;54:1578–95.
  • Madsen MW, Reiter BE, Lykkesfeldt AE. Differential expression of estrogen receptor mRNA splice variants in the tamoxifen resistant human breast cancer cell line, MCF7/TAMR-1 compared to the parental MCF-7 cell line. Mol Cell Endocrinol 1995;109:197–207.
  • Rondar G, Kuo J, Hamid N, Micevych P. Estradiol-induced estrogen receptor-alpha trafficking. J Neurosci 2009;29:15323–30.

Reprints and Corporate Permissions

Please note: Selecting permissions does not provide access to the full text of the article, please see our help page How do I view content?

To request a reprint or corporate permissions for this article, please click on the relevant link below:

Academic Permissions

Please note: Selecting permissions does not provide access to the full text of the article, please see our help page How do I view content?

Obtain permissions instantly via Rightslink by clicking on the button below:

If you are unable to obtain permissions via Rightslink, please complete and submit this Permissions form. For more information, please visit our Permissions help page.