Effects of estradiol and 4-hydroxytamoxifen on the conformation, thermal stability, and DNA recognition of estrogen receptor β

Biochemistry and Cell Biology

Volumn 85, Issue 1, 2007, Pages 1-10

  Vijayanathan, Veena ^a   Greenfield, Norma J ^a   Thomas, T J ^a   Ivanova, Margarita M ^b   Tyulmenkov, Valentyn V ^b   Klinge, Carolyn M ^b   Gallo, Michael A ^a   Thomas, Thresia ^a  

^a RUTGERS ROBERT WOOD JOHNSON MEDICAL SCHOOL   (United States)

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

Author keywords

Circular dichroism spectroscopy; Conformational transitions; Estrogen receptor beta; Estrogen response element

Indexed keywords

CIRCULAR DICHROISM SPECTROSCOPY; CONFORMATIONS; DNA; SPECTRUM ANALYSIS; THERMODYNAMIC STABILITY;

DNA RECOGNITION; ESTRADIOL; ESTROGEN RECEPTOR;

PROTEINS;

4 HYDROXYTAMOXIFEN; ESTRADIOL; ESTROGEN RECEPTOR BETA; OLIGODEOXYNUCLEOTIDE; OLIGONUCLEOTIDE;

ANISOTROPY; ARTICLE; CIRCULAR DICHROISM; CONFORMATION; GEL MOBILITY SHIFT ASSAY; POLYACRYLAMIDE GEL ELECTROPHORESIS; THERMOSTABILITY; TRANSIENT TRANSFECTION; X RAY CRYSTALLOGRAPHY;

DNA-BINDING PROTEINS; ESTRADIOL; ESTROGEN RECEPTOR BETA; HUMANS; MUTATION; PROTEIN FOLDING; PROTEIN STRUCTURE, SECONDARY; RECOMBINANT PROTEINS; RESPONSE ELEMENTS; TAMOXIFEN; TEMPERATURE;

EID: 34249940243     PISSN: 08298211     EISSN: None     Source Type: Journal    
DOI: 10.1139/O06-144     Document Type: Article

References (50)

1. Barkhem, T., Carlsson, B., Nilsson, Y., Enmark, E., Gustafsson, J., and Nilsson, S. 1998. Differential response of estrogen receptor alpha and estrogen receptor beta to partial estrogen agonists/antagonists. Mol. Pharmacol. 54: 105-112.
2. Berstein, L.M., Wang, J.P., Zheng, H., Yue, W., Conaway, M., and Santen, R.J. 2004. Long-term exposure to tamoxifen induces hypersensitivity to estradiol. Clin. Cancer Res. 10: 1530-1534. doi:10.1158/1078-0432.CCR- 0433-03.
3. Bohm, G., Muhr, R., and Jaenicke, R. 1992. Quantitative analysis of protein far UV circular dichroism spectra by neural networks. Protein Eng. 5: 191-195.
4. Bouter, A., Le Tilly, V., and Sire, O. 2005. Interplay of flexibility and stability in the control of estrogen receptor activity. Biochemistry, 44: 790-798. doi:10.1021/bi0483716.
5. Brahms, S., and Brahms, J. 1980. Determination of protein secondary structure in solution by vacuum ultraviolet circular dichroism. J. Mol. Biol. 138: 149-178. doi:10.1016/0022-2836(80)90282-X.
6. Brzozowski, A.M., Pike, A.C., Dauter, Z., Hubbard, R.E., Bonn, T., Engstrom, O., et al. 1997. Molecular basis of agonism and antagonism in the estrogen receptor. Nature (London), 389: 753-758. doi:10.1038/39645.
7. Cowley, S.M., Hoare, S., Mosselman, S., and Parker, M.G. 1997. Estrogen receptors alpha and beta form heterodimers on DNA. J. Biol. Chem. 272: 19858-19862. doi:10.1074/jbc.272.32.19858.
8. Driscoll, M.D., Sathya, G., Muyan, M., Klinge, C.M., Hilf, R., and Bambara, R.A. 1998. Sequence requirements for estrogen receptor binding to estrogen response elements. J. Biol. Chem. 273: 29321-29330. doi:10.1074/jbc.273.45.29321.
9. Esslimani-Sahla, M., Simony-Lafontaine, J., Kramar, A., Lavaill, R., Mollevi, C., Warner, M., Gustafsson, J.A., and Rochefort, H. 2004. Estrogen receptor beta (ER beta) level but not its ER beta ex variant helps to predict tamoxifen resistance in breast cancer. Clin. Cancer Res. 10: 5769-5776. doi:10.1158/1078-0432.CCR-04-0389.
10. Gewirth, D.T., and Sigler, P.B. 1995. The basis for half-site specificity explored through a non-cognate steroid receptor-DNA complex. Nat. Struct. Biol. 2: 386-394. doi:10.1038/nsb0595-386.
11. Greenfield, N., Vijayanathan, V., Thomas, T.J., Gallo, M.A., and Thomas, T. 2001. Increase in the stability and helical content of estrogen receptor alpha in the presence of the estrogen response element: analysis by circular dichroism spectroscopy. Biochemistry, 40: 6646-6652. doi:10.1021/ bi0028461.
12. Hall, J.M., McDonnell, D.P., and Korach, K.S. 2002. Allosteric regulation of estrogen receptor structure, function, and coactivator recruitment by different estrogen response elements. Mol. Endocrinol. 16: 469-486. doi:10.1210/me.16.3.469.
13. Hall, J.M., and Korach, K.S. 2002. Analysis of the molecular mechanisms of human estrogen receptors alpha and beta reveals differential specificity in target promoter regulation by xenoestrogens. J. Biol. Chem. 277: 44455-44461. doi:10.1074/jbc.M200849200.
14. Jordan, V.C. 2004. Selective estrogen receptor modulation: concept and consequences in cancer. Cancer Cell, 5: 207-213. doi:10.1016/S1535- 6108(04)00059-5.
15. Kabata, H., Kurosawa, O., Arai, I., Washizu, M., Margarson, S.A., Glass, R.E., and Shimamoto, N. 1993. Visualization of single molecules of RNA polymerase sliding along DNA. Science (Washington, D.C.), 262: 1561-1563.
16. Kalodimos, C.G., Biris, N., Bonvin, A.M., Levandoski, M.M., Guennuegues, M., Boelens, R., and Kaptein, R. 2004. Structure and flexibility adaptation in nonspecific and specific protein-DNA complexes. Science (Washington, D.C.), 305: 386-389. doi:10.1126/science.1097064.
17. Katzenellenbogen, B.S., and Frasor, J. 2004. Therapeutic targeting in the estrogen receptor hormonal pathway. Semin. Oncol. 31: 28-38. doi:10.1053/j.seminoncol.2004.01.004.
18. Klein-Hitpass, L., Ryffel, G.U., Heitlinger, E., and Cato, A.C. 1988. A 13 bp palindrome is a functional estrogen responsive element and interacts specifically with estrogen receptor. Nucleic Acids Res. 16: 647-663.
19. Klinge, C.M. 2001. Estrogen receptor interaction with estrogen response elements. Nucleic Acids Res. 29: 2905-2919. doi:10.1093/nar/29.14.2905.
20. Klinge, C.M., Jernigan, S.C., Mattingly, K.A., Risinger, K.E., and Zhang, J. 2004. Estrogen response element-dependent regulation of transcriptional activation of estrogen receptors alpha and beta by coactivators and corepressors. J. Mol. Endocrinol. 33: 387-410. doi:10.1677/jme.1.01541.
21. Kong, E.H., Heldring, N., Gustafsson, J.A., Treuter, E., Hubbard, R.E., and Pike, A.C. 2005. Delineation of a unique protein-protein interaction site on the surface of the estrogen receptor. Proc. Natl. Acad. Sci. U.S.A. 102: 3593-3598. doi:10.1073/ pnas.0407189102.
22. Kuiper, G.G., Enmark, E., Pelto-Huikko, M., Nilsson, S., and Gustafsson, J.A. 1996. Cloning of a novel receptor expressed in rat prostate and ovary. Proc. Natl. Acad. Sci. U.S.A. 93: 5925-5930. doi:10.1073/pnas.93.12.5925.
23. Kuiper, G.G., Carlsson, B., Grandien, K., Enmark, E., Haggblad, J., Nilsson, S., and Gustafsson, J.A. 1997. Comparison of the ligand binding specificity and transcript tissue distribution of estrogen receptors alpha and beta. Endocrinology, 138: 863-870. doi:10.1210/en.138.3.863.
24. Liu, M.M., Albanese, C., Anderson, C.M., Hilty, K., Webb, P., Uht, R.M., et al. 2002. Opposing action of estrogen receptors alpha and beta on cyclin D1 gene expression. J. Biol. Chem. 277: 24353-24360. doi:10.1074/jbc. M201829200.
25. Manas, E.S., Xu, Z.B., Unwalla, R.J., and Somers, W.S. 2004. Understanding the selectivity of genistein for human estrogen receptor-beta using X-ray crystallography and computational methods. Structure, 12: 2197-2207. doi:10.1016/j.str.2004.09.015.
26. Matthews, J., and Gustafsson, J.A. 2003. Estrogen signaling: a subtle balance between ER alpha and ER beta. Mol. Interv. 3: 281-292. doi:10.1124/mi.3.5.281.
27. Margeat, E., Bourdoncle, A., Margueron, R., Poujol, N., Cavailles, V., and Royer, C. 2003. Ligands differentially modulate the protein interactions of the human estrogen receptors alpha and beta. J. Mol. Biol. 326: 77-92. doi:10.1016/S0022-2836(02)01355-4.
28. McDonnell, D.P. 2005. The molecular pharmacology of estrogen receptor modulators: implications for the treatment of breast cancer. Clin. Cancer Res. 11: 871s-877s.
29. McInerney, E.M., Weis, K.E., Sun, J., Mosselman, S., and Katzenellenbogen, B.S. 1998. Transcription activation by the human estrogen receptor subtype beta (ER beta) studied with ER beta and ER alpha receptor chimeras. Endocrinology, 139: 4513-4522. doi:10.1210/en.139.11.4513.
30. Melvin, V.S., Harrell, C., Adelman, J.S., Kraus, W.L., Churchill, M., and Edwards, D.P. 2004. The role of the C-terminal extension (CTE) of the estrogen receptor alpha and beta DNA binding domain in DNA binding and interaction with HMGB. J. Biol. Chem. 279: 14763-14771. doi:10.1074/jbc.M313335200.
31. Melamed, M., Arnold, S.F., Notides, A.C., and Sasson, S. 1996. Kinetic analysis of the interaction of human estrogen receptor with an estrogen response element. J. Steroid Biochem. Mol. Biol. 57: 153-159. doi:10.1016/0960-0760(95)00264-2.
32. Metivier, R., Stark, A., Flouriot, G., Hubner, M.R., Brand, H., Penot, G., et al. 2002. A dynamic structural model for estrogen receptor-alpha activation by ligands, emphasizing the role of interactions between distant A and E domains. Mol. Cell, 10: 1019-1032. doi:10.1016/S1097-2765(02)00746- 3.
33. Michalides, R., Griekspoor, A., Balkenende, A., Verwoerd, D., Janssen, L., Jalink, K., et al. 2004. Tamoxifen resistance by a conformational arrest of the estrogen receptor alpha after PKA activation in breast cancer. Cancer Cell, 5: 597-605. doi:10.1016/j.ccr.2004.05.016.
34. Nettles, K.W., Sun, J., Radek, J.T., Sheng, S., Rodriguez, A.L., Katzenellenbogen, J.A., Katzenellenbogen, B.S., and Greene, G.L. 2004. Allosteric control of ligand selectivity between estrogen receptors alpha and beta: implications for other nuclear receptors. Mol. Cell, 13: 317-327. doi:10.1016/S1097-2765(04)00054-1.
35. 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 (Washington, D.C.), 277: 1508-1510. doi:10.1126/science.277.5331.1508.
36. Pavlik, E.J., and Coulson, P.B. 1976. Hydroxylapatite "batch" assay for estrogen receptors: increased sensitivity over present receptor assays. J. Steroid Biochem. 7: 357-368. doi:10.1016/0022-4731(76)90095-9.
37. Ramsey, T.L., and Klinge, C.M. 2001. Estrogen response element binding induces alterations in estrogen receptor-alpha conformation as revealed by susceptibility to partial proteolysis. J. Mol. Endocrinol. 27: 275-292. doi:10.1677/jme.0.0270275.
38. Ramsey, T.L., Risinger, K.E., Jernigan, S.C., Mattingly, K.A., and Klinge, C.M. 2004. Estrogen receptor beta isoforms exhibit differences in ligand-activated transcriptional activity in an estrogen response element sequence-dependent manner. Endocrinology, 145: 149-160.
39. Savitsky, A., and Golay, M.J.E. 1964. Smoothing and differentiation of data by simplified least squares procedures. Anal. Chem. 36: 1627-1639.
40. Schultz, J.R., Loven, M.A., Melvin, V.M., Edwards, D.P., and Nardulli, A.M. 2002. Differential modulation of DNA conformation by estrogen receptors alpha and beta. J. Biol. Chem. 277: 8702-8707. doi:10.1074/jbc. M108491200.
41. Shah, N., Thomas, T.J., Lewis, J.S., Klinge, C.M., Shirahata, A., Gelinas, C., and Thomas, T. 2001. Regulation of estrogenic and nuclear factor kappa B functions by polyamines and their role in polyamine analog-induced apoptosis of breast cancer cells. Oncogene, 20: 1715-1729. doi:10.1038/sj.onc.1204247.
42. Shang, Y., and Brown, M. 2002. Molecular determinants for the tissue specificity of SERMs. Science (Washington, D.C.), 295: 2465-2468. doi:10.1126/science.1068537.
43. Siggers, T.W., Silkov, A., and Honig, B. 2004. Structural alignment of protein-DNA interfaces: insights into the determinants of binding specificity. J. Mol. Biol. 345: 1027-1045.
44. Smith, C.L., and O'Malley, B.W. 2004. Coregulator function: a key to understanding tissue specificity of selective receptor modulators. Endocr. Rev. 25: 45-71. doi:10.1210/er.2003-0023.
45. Strom, A., Hartman, J., Foster, J.S., Kietz, S., Wimalasena, J., and Gustafsson, J.A. 2004. Estrogen receptor beta inhibits 17beta-estradiol- stimulated proliferation of the breast cancer cell line T47D. Proc. Natl. Acad. Sci. U.S.A. 101: 1566-1571. doi:10.1073/pnas.0308319100.
46. Thomas, T., Gallo, M.A., and Thomas, T.J. 2004. Estrogen receptors as targets for drug development for breast cancer, osteoporosis and cardiovascular diseases. Curr. Cancer Drug Targets, 4: 483-499. doi:10.2174/ 1568009043332880.
47. Tyulmenkov, V.V., and Klinge, C.M. 2001a. Estrogen receptors alpha and beta exhibit different estradiol and estrogen response element binding in the presence of nonspecific DNA. Arch. Biochem. Biophys. 390: 253-264. doi:10.1006/abbi.2001.2382.
48. Tyulmenkov, V.V., and Klinge, C.M. 2001b. A mathematical approach to predict the affinity of estrogen receptors alpha and beta binding to DNA. Mol. Cell. Endocrinol. 182: 109-119. doi:10.1016/S0303-7207(01)00508-1.
49. Wood, J.R., Likhite, V.S., Loven, M.A., and Nardulli, A.M. 2001. Allosteric modulation of estrogen receptor conformation by different estrogen response elements. Mol. Endocrinol. 15: 1114-1126. doi:10.1210/me.15.7. 1114.
50. Yi, P., Driscoll, M.D., Huang, J., Bhagat, S., Hilf, R., Bambara, R.A., and Muyan, M. 2002. The effects of estrogen-responsive element- and ligand-induced structural changes on the recruitment of cofactors and transcriptional responses by ER alpha and ER beta. Mol. Endocrinol. 16: 674-693. doi:10.1210/me.16.4.674.