Estrogen receptor α L543A,L544A mutation changes antagonists to agonists, correlating with the ligand binding domain dimerization associated with DNA binding activity

Journal of Biological Chemistry

Volumn 288, Issue 29, 2013, Pages 21105-21116

  Arao, Yukitomo ^a   Hamilton, Katherine J ^a   Coons, Laurel A ^a,b   Korach, Kenneth S ^a  

^a NATIONAL INSTITUTE OF ENVIRONMENTAL HEALTH SCIENCES   (United States)

^b DUKE UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

AGONIST ACTIVITY; DNA BINDING ACTIVITY; ESTROGEN RECEPTOR; HOMODIMERIZATION; LIGAND BINDING DOMAIN; SELECTIVE ESTROGEN RECEPTOR MODULATORS;

BIOCHEMISTRY; BIOLOGY;

DIMERIZATION;

ESTROGEN RECEPTOR ALPHA; SELECTIVE ESTROGEN RECEPTOR MODULATOR;

ARTICLE; BINDING AFFINITY; BIOTINYLATION; CONTROLLED STUDY; CORRELATION ANALYSIS; DIMERIZATION; DNA BINDING; GENE AMPLIFICATION; GENE MUTATION; HUMAN; HUMAN CELL; LIGAND BINDING; MOLECULAR DYNAMICS; PLASMID; POLYMERASE CHAIN REACTION; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN DEGRADATION; PROTEIN DOMAIN; SITE DIRECTED MUTAGENESIS; TRANSCRIPTION INITIATION;

ANTAGONIST REVERSAL; DIMERIZATION; ESTROGEN; ESTROGEN RECEPTOR; FULVESTRANT; MUTANT; PROTEIN DOMAINS; SERMS; TAMOXIFEN; TRANSCRIPTION;

AMINO ACID SUBSTITUTION; ANIMALS; DNA; ESTRADIOL; ESTROGEN ANTAGONISTS; ESTROGEN RECEPTOR ALPHA; ESTROGENS; HELA CELLS; HEP G2 CELLS; HUMANS; LIGANDS; MICE; MUTANT PROTEINS; MUTATION; NUCLEAR RECEPTOR COACTIVATOR 1; PROTEIN BINDING; PROTEIN MULTIMERIZATION; PROTEIN STRUCTURE, SECONDARY; PROTEIN STRUCTURE, TERTIARY; PROTEOLYSIS; RESPONSE ELEMENTS; SELECTIVE ESTROGEN RECEPTOR MODULATORS; TRANSCRIPTION, GENETIC;

EID: 84880537183     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M113.463455     Document Type: Article

References (28)

1. Hall, J. M., Couse, J. F., and Korach, K. S. (2001) The multifaceted mechanisms of estradiol and estrogen receptor signaling. J. Biol. Chem. 276, 36869-36872
2. Heldring, N., Pike, A., Andersson, S., Matthews, J., Cheng, G., Hartman, J., Tujague, M., Strom, A., Treuter, E., Warner, M., and Gustafsson, J. A. (2007) Estrogen receptors. How do they signal and what are their targets. Physiol. Rev. 87, 905-931
3. Mangelsdorf, D. J., Thummel, C., Beato, M., Herrlich, P., Schutz, G., Ume-sono, K., Blumberg, B., Kastner, P., Mark, M., Chambon, P., and Evans, R. M. (1995) The nuclear receptor superfamily. The second decade. Cell 83, 835-839
4. Germain, P., Staels, B., Dacquet, C., Spedding, M., and Laudet, V. (2006) Overview of nomenclature of nuclear receptors. Pharmacol. Rev. 58, 685-704
5. Brzozowski, A. M., Pike, A. C., Dauter, Z., Hubbard, R. E., Bonn, T., Engstrom, O., Ohman, L., Greene, G. L., Gustafsson, J. A., and Carlquist, M. (1997) Molecular basis of agonism and antagonism in the oestrogen receptor. Nature 389, 753-758
6. Fawell, S. E., Lees, J. A., White, R., and Parker, M. G. (1990) Characterization and colocalization of steroid binding and dimerization activities in the mouse estrogen receptor. Cell 60, 953-962
7. Schwabe, J. W., Chapman, L., Finch, J. T., and Rhodes, D. (1993) The crystal structure of the estrogen receptor DNA-binding domain bound to DNA. How receptors discriminate between their response elements. Cell 75, 567-578
8. Tanenbaum, D. M., Wang, Y., Williams, S. P., and Sigler, P. B. (1998) Crystallographic comparison of the estrogen and progesterone receptor's ligand binding domains. Proc. Natl. Acad. Sci. U.S.A. 95, 5998-6003
9. Arao, Y., Hamilton, K. J., Ray, M. K., Scott, G., Mishina, Y., and Korach, K. S. (2011) Estrogen receptor a AF-2 mutation results in antagonist reversal and reveals tissue selective function of estrogen receptor modulators. Proc. Natl. Acad. Sci. U.S.A. 108,14986-14991
10. Arao, Y., Hamilton, K. J., Goulding, E. H., Janardhan, K. S., Eddy, E. M., and Korach, K. S. (2012) Transactivating function (AF) 2-mediated AF-1 activity of estrogen receptor a is crucial to maintain male reproductive tract function. Proc. Natl. Acad. Sci. U.S.A. 109, 21140-21145
11. Hewitt, S. C., Kissling, G. E., Fieselman, K. E., Jayes, F. L., Gerrish, K. E., and Korach, K. S. (2010) Biological and biochemical consequences of global deletion of exon 3 from the ERa gene. FASEB J. 24, 4660-4667
12. Berry, M., Metzger, D., and Chambon, P. (1990) Role ofthe 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
13. Chang, C. Y., Norris, J. D., Gron, H., Paige, L. A., Hamilton, P. T., Kenan, D. J., Fowlkes, D., and McDonnell, D. P. (1999) Dissection of the LXXLL nuclear receptor-coactivator interaction motif using combinatorial pep-tide libraries. Discovery of peptide antagonists of estrogen receptors a and β. Mol. Cell Biol. 19, 8226-8239
14. Dauvois, S., Danielian, P. S., White, R., and Parker, M. G. (1992) Anties-trogen ICI 164,384 reduces cellular estrogen receptor content by increasing its turnover. Proc. Natl. Acad. Sci. U.S.A. 89, 4037-4041
15. Gibson, M. K., Nemmers, L. A., Beckman, W. C. Jr., Davis, V. L., Curtis, S. W., Korach, K. S. (1991) The mechanism of ICI 164,384 antiestrogenic-ity involves rapid loss of estrogen receptor in uterine tissue. Endocrinology 129, 2000-2010
16. Howell, A. (2006) Pure oestrogen antagonists for the treatment of advanced breast cancer. Endocr.-Relat. Cancer 13, 689 -706
17. Tamrazi, A., Carlson, K. E., Daniels, J. R., Hurth, K. M., and Katzenellenbogen, J. A. (2002) Estrogen receptor dimerization. Ligand binding regulates dimer affinity and dimer dissociation rate. Mol. Endocrinol. 16, 2706 -2719
18. Lees, J. A., Fawell, S. E., White, R., and Parker, M. G. (1990) A 22-amino-acid peptide restores DNA-binding activity to dimerization-defective mutants of the estrogen receptor. Mol. Cell Biol. 10, 5529-5531
19. Hilmi, K., Hussein, N., Mendoza-Sanchez, R., El-Ezzy, M., Ismail, H., Du-rette, C., Bail, M., Rozendaal, M. J., Bouvier, M., Thibault, P., Gleason, J. L., and Mader, S. (2012) Role of SUMOylation in full antiestrogenicity. Mol. Cell Biol 32, 3823-3837
20. Mahfoudi, A., Roulet, E., Dauvois, S., Parker, M. G., and Wahli, W. (1995) Specific mutations in the estrogen receptor change the properties of an-tiestrogens to full agonists. Proc. Natl. Acad. Sci. U.S.A. 92, 4206-4210
21. Montano, M. M., Ekena, K., Krueger, K. D., Keller, A. L., and Katzenellenbogen, B. S. (1996) Human estrogen receptor ligand activity inversion mutants. Receptors that interpret antiestrogens as estrogens and estrogens as antiestrogens and discriminate among different antiestrogens. Mol. Endocrinol. 10, 230-242
22. Lupien, M., Jeyakumar, M., Hebert, E., Hilmi, K., Cotnoir-White, D., Loch, C., Auger, A., Dayan, G., Pinard, G. A., Wurtz, J. M., Moras, D., Katzenellenbogen, J. A., and Mader, S. (2007) Raloxifene and ICI182,780 increase estrogen receptor association with a nuclear compartment via overlapping sets of hydrophobic amino acids in activation function 2 helix 12. Mol. Endocrinol. 21, 797-816
23. Schwartz, J. A., and Brooks, S. C. (1997) Neutral mutations to three acidic AF2 residues in the mouse estrogen receptor confer agonist activity to A-ring isomers of estradiol. J. Steroid Biochem. Mol. Biol. 62, 173-184
24. Nichols, M., Cheng, P., Liu, Y., Kanterewicz, B., Hershberger, P. A., and McCarty, K. S. (2010) Breast cancer-derived M543V mutation in helix 12 of estrogen receptor a inverts response to estrogen and SERMs. Breast Cancer Res. Treat. 120, 761-768
25. Shiau, A. K., Barstad, D., Loria, P. M., Cheng, L., Kushner, P. J., Agard, D. A., and Greene, G. L. (1998) The structural basis of estrogen receptor/ coactivator recognition and the antagonism of this interaction by tamox-ifen. Cell 95, 927-937
26. Wu, Y. L., Yang, X., Ren, Z., McDonnell, D. P., Norris, J. D., Willson, T. M., and Greene, G. L. (2005) Structural basis for an unexpected mode of SERM-mediated ER antagonism. Mol. Cell 18, 413-424
27. Pike, A. C., Brzozowski, A. M., Walton, J., Hubbard, R. E., Thorsell, A. G., Li, Y. L., Gustafsson, J. A., and Carlquist, M. (2001) Structural insights into the mode of action of a pure antiestrogen. Structure 9,145-153
28. Métivier, R., Stark, A., Flouriot, G., Hübner, M. R., Brand, H., Penot, G., Manu, D., Denger, S., Reid, G., Kos, M., Russell, R. B., Kah, O., Pakdel, F., and Gannon, F. (2002) A dynamic structural model for estrogen receptor-a activation by ligands, emphasizing the role of interactions between distant A and E domains. Mol. Cell 10,1019 -1032