Calmodulin, a regulatory partner of the estrogen receptor alpha in breast cancer cells

Molecular and Cellular Endocrinology

Volumn 291, Issue 1-2, 2008, Pages 20-26

  Gallo, Dominique ^a   Jacquot, Yves ^b   Laurent, Guy ^c   Leclercq, Guy ^a  

^a JULES BORDET INSTITUTE   (Belgium)

^b SORBONNE UNIVERSITÉ   (France)

^c UNIVERSITY OF MONS   (Belgium)

Author keywords

Breast cancer; Calmodulin; Estrogen receptor alpha

Indexed keywords

BRCA1 PROTEIN; CALCIUM ION; CALMODULIN; ESTROGEN; ESTROGEN RECEPTOR ALPHA; SYNTHETIC PEPTIDE; TAMOXIFEN;

AMINO ACID SEQUENCE; ANTINEOPLASTIC ACTIVITY; BINDING SITE; BREAST CANCER; CANCER CELL; COMPLEX FORMATION; COMPUTER ANALYSIS; CONFORMATIONAL TRANSITION; HORMONE ACTION; HUMAN; MUTATION; NONHUMAN; PATHOLOGY; PRIORITY JOURNAL; PROTEIN DOMAIN; PROTEIN FOLDING; PROTEIN FUNCTION; PROTEIN LOCALIZATION; PROTEIN METABOLISM; PROTEIN PROTEIN INTERACTION; REVIEW; TRANSACTIVATION;

EID: 48449104880     PISSN: 03037207     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.mce.2008.04.011     Document Type: Review

References (78)

1. Acconcia F., and Kumar R. Signaling regulation of genomic and nongenomic functions of estrogen receptors. Cancer Lett. 238 (2006) 1-14
2. Alarid E.T., Bakopoulos N., and Solodin N. Proteasome-mediated proteolysis of estrogen receptor: a novel component in autologous down-regulation. Mol. Endocrinol. 13 (1999) 1522-1534
3. Ariazi E.A., and Jordan V.C. Estrogen-related receptors as emerging targets in cancer and metabolic disorders. Curr. Top. Med. Chem. 6 (2006) 203-215
4. Auricchio F., Migliaccio A., Castoria G., Lastoria S., and Schiavone E. ATP-dependent enzyme activating hormone binding of estradiol receptor. Biochem. Biophys. Res. Commun. 101 (1981) 1171-1178
5. Auricchio F., Migliaccio A., and Rotondi A. Inactivation of oestrogen receptor in vitro by nuclear dephosphorylation. Biochem. J. 194 (1981) 569-574
6. Biswas D.K., Reddy P.V., Pickard M., Makkad B., Pettit N., and Pardee A.B. Calmodulin is essential for estrogen receptor interaction with its motif and activation of responsive promoter. J. Biol. Chem. 273 (1998) 33817-33824
7. Bouhoute A., and Leclercq G. Antagonistic effect of triphenylethylenic antiestrogens on the association of estrogen receptor to calmodulin. Biochem. Biophys. Res. Commun. 184 (1992) 1432-1440
8. Bouhoute A., and Leclercq G. Estradiol derivatives bearing the side-chain of tamoxifen antagonize the association between the estrogen receptor and calmodulin. Biochem. Pharmacol. 47 (1994) 748-751
9. Bouhoute A., and Leclercq G. Modulation of estradiol and DNA binding to estrogen receptor upon association with calmodulin. Biochem. Biophys. Res. Commun. 208 (1995) 748-755
10. Bouhoute A., and Leclercq G. Calmodulin decreases the estrogen binding capacity of the estrogen receptor. Biochem. Biophys. Res. Commun. 227 (1996) 651-657
11. Carlson K.E., Choi I., Gee A., Katzenellenbogen B.S., and Katzenellenbogen J.A. Altered ligand binding properties and enhanced stability of a constitutively active estrogen receptor: evidence that an open pocket conformation is required for ligand interaction. Biochemistry 36 (1997) 14897-14905
12. Castoria G., Migliaccio A., Bilancio A., Pagano M., Abbondanza C., and Auricchio F. A 67 kDa non-hormone binding estradiol receptor is present in human mammary cancers. Int. J. Cancer 65 (1996) 574-583
13. Castoria G., Migliaccio A., Green S., Di Domenico M., Chambon P., and Auricchio F. Properties of a purified estradiol-dependent calf uterus tyrosine kinase. Biochemistry 32 (1993) 1740-1750
14. Castoria G., Migliaccio A., Nola E., and Auricchio F. In vitro interaction of estradiol receptor with Ca2+-calmodulin. Mol. Endocrinol. 2 (1988) 167-174
15. Cifuentes E., Mataraza J.M., Yoshida B.A., Menon M., Sacks D.B., Barrack E.R., and Reddy G.P. Physical and functional interaction of androgen receptor with calmodulin in prostate cancer cells. Proc. Natl. Acad. Sci. U.S.A. 101 (2004) 464-469
16. Conway K., Parrish E., Edmiston S.N., Tolbert D., Tse C.K., Geradts J., Livasy C.A., Singh H., Newman B., and Millikan R.C. The estrogen receptor-alpha A908G (K303R) mutation occurs at a low frequency in invasive breast tumors: results from a population-based study. Breast Cancer Res. 7 (2005) R871-R880
17. Dayani N., McNaught R.W., and Smith R.G. ATP mediated receptor interconversion as a model of estrogen action: isolation of the factor which converts the non-estrogen binding form of the receptor to the lower affinity binding form. J. Steroid Biochem. 30 (1988) 219-224
18. de Medina P., Favre G., and Poirot M. Multiple targeting by the antitumor drug tamoxifen: a structure-activity study. Curr. Med. Chem. Anticancer Agents 4 (2004) 491-508
19. Deshaies R.J. SCF and Cullin/Ring H2-based ubiquitin ligases. Annu. Rev. Cell Dev. Biol. 15 (1999) 435-467
20. Eakin C.M., Maccoss M.J., Finney G.L., and Klevit R.E. Estrogen receptor alpha is a putative substrate for the BRCA1 ubiquitin ligase. Proc. Natl. Acad. Sci. U.S.A. 104 (2007) 5794-5799
21. El Khissiin A., and Leclercq G. Implication of proteasome in estrogen receptor degradation. FEBS Lett. 448 (1999) 160-166
22. Estebanez-Perpina E., Arnold L.A., Nguyen P., Rodrigues E.D., Mar E., Bateman R., Pallai P., Shokat K.M., Baxter J.D., Guy R.K., Webb P., and Fletterick R.J. A surface on the androgen receptor that allosterically regulates coactivator binding. Proc. Natl. Acad. Sci. U.S.A. 104 (2007) 16074-16079
23. Fanidi A., Guichard Y., Fayard J.M., Pageaux J.F., and Laugier C. Fluorimetric studies of calmodulin interactions with antiestrogens. Cancer Detect. Prev. 18 (1994) 471-478
24. Frankfurt O.S., Sugarbaker E.V., Robb J.A., and Villa L. Synergistic induction of apoptosis in breast cancer cells by tamoxifen and calmodulin inhibitors. Cancer Lett. 97 (1995) 149-154
25. Fuqua S.A., Wiltschke C., Zhang Q.X., Borg A., Castles C.G., Friedrichs W.E., Hopp T., Hilsenbeck S., Mohsin S., O'Connell P., and Allred D.C. A hypersensitive estrogen receptor-alpha mutation in premalignant breast lesions. Cancer Res. 60 (2000) 4026-4029
26. Gallo D., Haddad I., Duvillier H., Jacquemotte F., Laios I., Laurent G., Jacquot Y., Vinh J., and Leclercq G. Trophic effect in MCF-7 cells of ERalpha17p, a peptide corresponding to a platform regulatory motif of the estrogen receptor alpha-Underlying mechanisms. J. Steroid Biochem. Mol. Biol. 109 (2008) 138-149
27. Gallo, D., Haddad, I., Laurent, G., Vinh, J., Jacquemotte, F., Jarman, M., Leclercq, G., 2008b. Regulatory function of the P295-T311 motif of the Estrogen Receptor alpha-does the degradation of the receptor induce emergence of peptides implicated in estrogenic responses? Nucl. Recept. Signal., 6, e007.
28. Gallo D., Jacquemotte F., Cleeren A., Laïos I., Hadiy S., Rowlands M.G., Caille O., Nonclercq D., Laurent G., Jacquot Y., and Leclercq G. Calmodulin-independent, agonistic properties of a peptide containing the calmodulin binding site of estrogen receptor alpha. Mol. Cell Endocrinol. 268 (2007) 37-49
29. Gallo D., Jacquot Y., Cleeren A., Jacquemotte F., Laurent G., and Leclercq G. Molecular basis of agonistic activity of ERa17p, a synthetic peptide corresponding to a sequence located at the N-terminal part of the estrogen receptor a ligand binding domain. Lett. Drug Des. Discov. 4 (2007) 346-355
30. Garcia Pedrero J.M., Del Rio B., Martinez-Campa C., Muramatsu M., Lazo P.S., and Ramos S. Calmodulin is a selective modulator of estrogen receptors. Mol. Endocrinol. 16 (2002) 947-960
31. Hardcastle I.R., Rowlands M.G., Houghton J., Parr I.B., Potter G.A., Jarman M., Edwards K.J., Laughton C.A., Trent J.O., and Neidle S. Rationally designed analogues of tamoxifen with improved calmodulin antagonism. J. Med. Chem. 38 (1995) 241-248
32. Heine G.F., and Parvin J.D. BRCA1 control of steroid receptor ubiquitination. Sci. STKE (2007) e34
33. Hentschke M., Schulze C., Susens U., and Borgmeyer U. Characterization of calmodulin binding to the orphan nuclear receptor ERRgamma. Biol. Chem. 384 (2003) 473-482
34. Jacquot Y., Gallo D., and Leclercq G. Estrogen receptor alpha-identification by a modeling approach of a potential polyproline II recognizing domain within the AF-2 region of the receptor that would play a role of prime importance in its mechanism of action. J. Steroid Biochem. Mol. Biol. 104 (2007) 1-10
35. Jurado L.A., Chockalingam P.S., and Jarrett H.W. Apocalmodulin Physiol. Rev. 79 (1999) 661-682
36. Khan O.Y., Fu G., Ismail A., Srinivasan S., Cao X., Tu Y., Lu S., and Nawaz Z. Multifunction steroid receptor coactivator, E6-associated protein, is involved in development of the prostate gland. Mol. Endocrinol. 20 (2006) 544-559
37. Kong E.H., Heldring N., Gustafsson J.A., Treuter E., Hubbard R.E., and Pike A.C. Delineation of a unique protein-protein interaction site on the surface of the estrogen receptor. Proc. Natl. Acad. Sci. U.S.A. 102 (2005) 3593-3598
38. Kraus W.L., McInerney E.M., and Katzenellenbogen B.S. Ligand-dependent, transcriptionally productive association of the amino- and carboxyl-terminal regions of a steroid hormone nuclear receptor. Proc. Natl. Acad. Sci. U.S.A. 92 (1995) 12314-12318
39. Krishnaraju K., Murugesan K., Vij U., Kapur B.M., and Farooq A. Calmodulin levels in oestrogen receptor positive and negative human breast tumours. Br. J. Cancer 63 (1991) 346-347
40. Laïos I., Journe F., Laurent G., Nonclercq D., Toillon R.A., Seo H.S., and Leclercq G. Mechanisms governing the accumulation of estrogen receptor alpha in MCF-7 breast cancer cells treated with hydroxytamoxifen and related antiestrogens. J. Steroid Biochem. Mol. Biol. 87 (2003) 207-221
41. Laïos I., Journe F., Nonclercq D., Vidal D.S., Toillon R.A., Laurent G., and Leclercq G. 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. 94 (2005) 347-359
42. Leclercq G., Lacroix M., Laïos I., and Laurent G. Estrogen receptor alpha: impact of ligands on intracellular shuttling and turnover rate in breast cancer cells. Curr. Cancer Drug Targets 6 (2006) 39-64
43. Leclercq G., Legros N., and Piccart M.J. Accumulation of a non-binding form of estrogen receptor in MCF-7 cells under hydroxytamoxifen treatment. J. Steroid Biochem. Mol. Biol. 41 (1992) 545-552
44. Li L., Li Z., Howley P.M., and Sacks D.B. E6AP and calmodulin reciprocally regulate estrogen receptor stability. J. Biol. Chem. 281 (2006) 1978-1985
45. Li L., Li Z., and Sacks D.B. Calmodulin regulates the transcriptional activity of estrogen receptors Selective inhibition of calmodulin function in subcellular compartments. J. Biol. Chem. 278 (2003) 1195-1200
46. Li L., Li Z., and Sacks D.B. The transcriptional activity of estrogen receptor-alpha is dependent on Ca2+/calmodulin. J. Biol. Chem. 280 (2005) 13097-13104
47. Li Z., Joyal J.L., and Sacks D.B. Calmodulin enhances the stability of the estrogen receptor. J. Biol. Chem. 276 (2001) 17354-17360
48. Lopes M.C., Vale M.G., and Carvalho A.P. Ca2(+)-dependent binding of tamoxifen to calmodulin isolated from bovine brain. Cancer Res. 50 (1990) 2753-2758
49. Maaroufi Y., Lacroix M., Lespagnard L., Journe F., Larsimont D., and Leclercq G. Estrogen receptor of primary breast cancers: evidence for intracellular proteolysis. Breast Cancer Res. 2 (2000) 444-454
50. Maruvada P., Baumann C.T., Hager G.L., and Yen P.M. Dynamic shuttling and intranuclear mobility of nuclear hormone receptors. J. Biol. Chem. 278 (2003) 12425-12432
51. Métivier R., Penot G., Hubner M.R., Reid G., Brand H., Kos M., and Gannon F. Estrogen receptor-alpha directs ordered, cyclical, and combinatorial recruitment of cofactors on a natural target promoter. Cell 115 (2003) 751-763
52. Migliaccio A., Castoria G., de Falco A., Di Domenico M., Galdiero M., Nola E., Chambon P., and Auricchio F. In vitro phosphorylation and hormone binding activation of the synthetic wild type human estradiol receptor. J. Steroid Biochem. Mol. Biol. 38 (1991) 407-413
53. Migliaccio A., Di Domenico M., Green S., de Falco A., Kajtaniak E.L., Blasi F., Chambon P., and Auricchio F. Phosphorylation on tyrosine of in vitro synthesized human estrogen receptor activates its hormone binding. Mol. Endocrinol. 3 (1989) 1061-1069
54. Migliaccio A., Pagano M., De Goeij C.C., Di Domenico M., Castoria G., Sluyser M., and Auricchio F. Phosphorylation and estradiol binding of estrogen receptor in hormone-dependent and hormone-independent GR mouse mammary tumors. Int. J. Cancer 51 (1992) 733-739
55. Migliaccio A., Rotondi A., and Auricchio F. Calmodulin-stimulated phosphorylation of 17 beta-estradiol receptor on tyrosine. Proc. Natl. Acad. Sci. U.S.A. 81 (1984) 5921-5925
56. Nair S., and Vadlamudi R.K. Emerging significance of ER-coregulator PELP1/MNAR in cancer. Histol. Histopathol. 22 (2007) 91-96
57. Nawaz Z., Lonard D.M., Dennis A.P., Smith C.L., and O'Malley B.W. Proteasome-dependent degradation of the human estrogen receptor. Proc. Natl. Acad. Sci. U.S.A. 96 (1999) 1858-1862
58. Nawaz Z., Lonard D.M., Smith C.L., Lev-Lehman E., Tsai S.Y., Tsai M.J., and O'Malley B.W. The Angelman syndrome-associated protein, E6-AP, is a coactivator for the nuclear hormone receptor superfamily. Mol. Cell Biol. 19 (1999) 1182-1189
59. Nonclercq D., Journe F., Laios I., Chaboteaux C., Toillon R.A., Leclercq G., and Laurent G. Effect of nuclear export inhibition on estrogen receptor regulation in breast cancer cells. J. Mol. Endocrinol. 39 (2007) 105-118
60. Pedram A., Razandi M., and Levin E.R. Nature of functional estrogen receptors at the plasma membrane. Mol. Endocrinol. 20 (2006) 1996-2009
61. Piccart M.J., Trivedi S., Maaroufi Y., Debbaudt A., Veenstra S., and Leclercq G. Evolution towards hormone independence of the MXT mouse mammary tumor is associated with a gradual change in its estrogen receptor molecular polymorphism. Cancer Biochem. Biophys. 16 (1998) 169-182
62. Read L.D., Greene G.L., and Katzenellenbogen B.S. Regulation of estrogen receptor messenger ribonucleic acid and protein levels in human breast cancer cell lines by sex steroid hormones, their antagonists, and growth factors. Mol. Endocrinol. 3 (1989) 295-304
63. Reid G., Hubner M.R., Metivier R., Brand H., Denger S., Manu D., Beaudouin J., Ellenberg J., and Gannon F. Cyclic, proteasome-mediated turnover of unliganded and liganded ERalpha on responsive promoters is an integral feature of estrogen signaling. Mol. Cell 11 (2003) 695-707
64. Rowlands M.G., Grimshaw R., Jarman M., Bouhoute A., and Leclercq G. Antagonism of estrogen receptor and calmodulin association by antiestrogens is not dependent on an interaction with calmodulin. Biochem. Pharmacol. 53 (1997) 241-244
65. Seielstad D.A., Carlson K.E., Kushner P.J., Greene G.L., and Katzenellenbogen J.A. Analysis of the structural core of the human estrogen receptor ligand binding domain by selective proteolysis/mass spectrometric analysis. Biochemistry 34 (1995) 12605-12615
66. Singer A.L., Sherwin R.P., Dunn A.S., and Appleman M.M. Cyclic nucleotide phosphodiesterases in neoplastic and nonneoplastic human mammary tissues. Cancer Res. 36 (1976) 60-66
67. Song R.X. Membrane-initiated steroid signaling action of estrogen and breast cancer. Semin. Reprod. Med. 25 (2007) 187-197
68. Stenoien D.L., Mancini M.G., Patel K., Allegretto E.A., Smith C.L., and Mancini M.A. Subnuclear trafficking of estrogen receptor-alpha and steroid receptor coactivator-1. Mol. Endocrinol. 14 (2000) 518-534
69. Strobl J.S., and Peterson V.A. Tamoxifen-resistant human breast cancer cell growth: inhibition by thioridazine, pimozide and the calmodulin antagonist W-13. J. Pharmacol. Exp. Ther. 263 (1992) 186-193
70. Sweitzer T.D., and Hanover J.A. Calmodulin activates nuclear protein import: a link between signal transduction and nuclear transport. Proc. Natl. Acad. Sci. U.S.A. 93 (1996) 14574-14579
71. Wang C., Fu M., Angeletti R.H., Siconolfi-Baez L., Reutens A.T., Albanese C., Lisanti M.P., Katzenellenbogen B.S., Kato S., Hopp T., Fuqua S.A., Lopez G.N., Kushner P.J., and Pestell R.G. Direct acetylation of the estrogen receptor alpha hinge region by p300 regulates transactivation and hormone sensitivity. J. Biol. Chem. 276 (2001) 18375-18383
72. Wang R.A., Mazumdar A., Vadlamudi R.K., and Kumar R. P21-activated kinase-1 phosphorylates and transactivates estrogen receptor-alpha and promotes hyperplasia in mammary epithelium. EMBO J. 21 (2002) 5437-5447
73. Wärnmark A., Treuter E., Gustafsson J.A., Hubbard R.E., Brzozowski A.M., and Pike A.C. Interaction of transcriptional intermediary factor 2 nuclear receptor box peptides with the coactivator binding site of estrogen receptor alpha. J. Biol. Chem. 277 (2002) 21862-21868
74. Wijayaratne A.L., and McDonnell D.P. 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 (2001) 35684-35692
75. Yang Z., Barnes C.J., and Kumar R. Human epidermal growth factor receptor 2 status modulates subcellular localization of and interaction with estrogen receptor alpha in breast cancer cells. Clin. Cancer Res. 10 (2004) 3621-3628
76. Yudt M.R., Vorojeikina D., Zhong L., Skafar D.F., Sasson S., Gasiewicz T.A., and Notides A.C. Function of estrogen receptor tyrosine 537 in hormone binding, DNA binding, and transactivation. Biochemistry 38 (1999) 14146-14156
77. Zhou D., Ye J.J., Li Y., Lui K., and Chen S. The molecular basis of the interaction between the proline-rich SH3-binding motif of PNRC and estrogen receptor alpha. Nucleic Acids Res. 34 (2006) 5974-5986
78. Zwart W., Griekspoor A., Berno V., Lakeman K., Jalink K., Mancini M., Neefjes J., and Michalides R. PKA-induced resistance to tamoxifen is associated with an altered orientation of ERalpha towards co-activator SRC-1. EMBO J. 26 (2007) 3534-3544