Activation of the MKL1/actin signaling pathway induces hormonal escape in estrogen-responsive breast cancer cell lines

Molecular and Cellular Endocrinology

Volumn 390, Issue 1-2, 2014, Pages 34-44

  Kerdivel, Gwenneg ^a   Boudot, Antoine ^a   Habauzit, Denis ^a   Percevault, Frederic ^a   Demay, Florence ^a   Pakdel, Farzad ^a   Flouriot, Gilles ^a  

^a UNIVERSITÉ DE RENNES 1   (France)

Author keywords

Breast cancer; Cell growth; Estrogen receptor; Hormone resistance; MKL1; Tamoxifen

Indexed keywords

AMPHIREGULIN; ESTROGEN; ESTROGEN RECEPTOR ALPHA; HEPARIN BINDING EPIDERMAL GROWTH FACTOR; MEMBRANE PROTEIN; PROGESTERONE RECEPTOR; TAMOXIFEN; TRANSCRIPTION FACTOR MKL1; TRANSFORMING GROWTH FACTOR BETA; UNCLASSIFIED DRUG; ACTIN; ANTINEOPLASTIC HORMONE AGONISTS AND ANTAGONISTS; DNA BINDING PROTEIN; EPIDERMAL GROWTH FACTOR RECEPTOR 2; ERBB2 PROTEIN, HUMAN; ESTRADIOL; ESTROGEN RECEPTOR ALPHA, HUMAN; MKL1 PROTEIN, HUMAN; ONCOPROTEIN;

ANTIBIOTIC RESISTANCE; ARTICLE; BREAST CANCER; CANCER CELL; CELL DIFFERENTIATION; CELL FUNCTION; CELL PROLIFERATION; CONTROLLED STUDY; DOWN REGULATION; ENZYME ACTIVATION; ENZYME ACTIVITY; EPITHELIAL MESENCHYMAL TRANSITION; HORMONE ACTION; HUMAN; HUMAN CELL; PHENOTYPE; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN EXPRESSION; SIGNAL TRANSDUCTION; TRIPLE NEGATIVE BREAST CANCER; BREAST NEOPLASMS; DRUG RESISTANCE; FEMALE; GENETIC TRANSCRIPTION; GENETICS; MCF 7 CELL LINE; METABOLISM; NEOPLASMS, HORMONE-DEPENDENT; PHYSIOLOGY;

ACTINS; ANTINEOPLASTIC AGENTS, HORMONAL; BREAST NEOPLASMS; DNA-BINDING PROTEINS; DRUG RESISTANCE, NEOPLASM; ESTRADIOL; ESTROGEN RECEPTOR ALPHA; FEMALE; HUMANS; MCF-7 CELLS; NEOPLASMS, HORMONE-DEPENDENT; ONCOGENE PROTEINS, FUSION; RECEPTOR, ERBB-2; RECEPTORS, PROGESTERONE; SIGNAL TRANSDUCTION; TAMOXIFEN; TRANSCRIPTION, GENETIC;

EID: 84899102711     PISSN: 03037207     EISSN: 18728057     Source Type: Journal    
DOI: 10.1016/j.mce.2014.03.009     Document Type: Article

References (52)

1. Barone I., Brusco L., Fuqua S.A.W. Estrogen receptor mutations and changes in downstream gene expression and signaling. Clin. Cancer Res. 2010, 16:2702-2708.
2. Bos P.D., Zhang X.H.-F., Nadal C., Shu W., Gomis R.R., Nguyen D.X., Minn A.J., van de Vijver M.J., Gerald W.L., Foekens J.A., Massagué J. Genes that mediate breast cancer metastasis to the brain. Nature 2009, 459:1005-1009.
3. Boudot A., Kerdivel G., Habauzit D., Eeckhoute J., Le Dily F., Flouriot G., Samson M., Pakdel F. Differential estrogen-regulation of CXCL12 chemokine receptors, CXCR4 and CXCR7, contributes to the growth effect of estrogens in breast cancer cells. PLoS ONE 2011, 6:e20898.
4. Brandt D.T., Xu J., Steinbeisser H., Grosse R. Regulation of myocardin-related transcriptional coactivators through cofactor interactions in differentiation and cancer. Cell Cycle 2009, 8:2523-2527.
5. Briand P., Nielsen K.V., Madsen M.W., Petersen O.W. Trisomy 7p and malignant transformation of human breast epithelial cells following epidermal growth factor withdrawal. Cancer Res. 1996, 56:2039-2044.
6. Busche S., Descot A., Julien S., Genth H., Posern G. Epithelial cell-cell contacts regulate SRF-mediated transcription via Rac-actin-MAL signalling. J. Cell. Sci. 2008, 121:1025-1035.
7. Busche S., Kremmer E., Posern G. E-cadherin regulates MAL-SRF-mediated transcription in epithelial cells. J. Cell. Sci. 2010, 123:2803-2809.
8. Cen B., Selvaraj A., Burgess R.C., Hitzler J.K., Ma Z., Morris S.W., Prywes R. Megakaryoblastic leukemia 1, a potent transcriptional coactivator for serum response factor (SRF), is required for serum induction of SRF target genes. Mol. Cell. Biol. 2003, 23:6597-6608.
9. Couse J.F., Korach K.S. Estrogen receptor null mice: what have we learned and where will they lead us?. Endocr. Rev. 1999, 20:358-417.
10. Dahlman-Wright K., Cavailles V., Fuqua S.A., Jordan V.C., Katzenellenbogen J.A., Korach K.S., Maggi A., Muramatsu M., Parker M.G., Gustafsson J.-A. International union of pharmacology. LXIV. Estrogen receptors. Pharmacol. Rev. 2006, 58:773-781.
11. Dardes R.C., Schafer J.M., Pearce S.T., Osipo C., Chen B., Jordan V.C. Regulation of estrogen target genes and growth by selective estrogen-receptor modulators in endometrial cancer cells. Gynecol. Oncol. 2002, 85:498-506.
12. Deroo B.J., Korach K.S. Estrogen receptors and human disease. J. Clin. Invest. 2006, 116:561-570.
13. Eeckhoute J., Keeton E.K., Lupien M., Krum S.A., Carroll J.S., Brown M. Positive cross-regulatory loop ties GATA-3 to estrogen receptor alpha expression in breast cancer. Cancer Res. 2007, 67:6477-6483.
14. Evelyn C.R., Wade S.M., Wang Q., Wu M., Iñiguez-Lluhí J.A., Merajver S.D., Neubig R.R. CCG-1423: a small-molecule inhibitor of RhoA transcriptional signaling. Mol. Cancer Ther. 2007, 6:2249-2260.
15. Habauzit D., Boudot A., Kerdivel G., Flouriot G., Pakdel F. Development and validation of a test for environmental estrogens: checking xeno-estrogen activity by CXCL12 secretion in BREAST CANCER CELL LINES (CXCL-test). Environ. Toxicol. 2010, 25:495-503.
16. Hall J.M. Stromal cell-derived factor 1, a novel target of estrogen receptor action, mediates the mitogenic effects of estradiol in ovarian and breast cancer cells. Mol. Endocrinol. 2003, 17:792-803.
17. Hinohara K., Nakajima T., Yasunami M., Houda S., Sasaoka T., Yamamoto K., Lee B.-S., Shibata H., Tanaka-Takahashi Y., Takahashi M., Arimura T., Sato A., Naruse T., Ban J., Inoko H., Yamada Y., Sawabe M., Park J.-E., Izumi T., Kimura A. Megakaryoblastic leukemia factor-1 gene in the susceptibility to coronary artery disease. Hum. Genet. 2009, 126:539-547.
18. Hu Q., Guo C., Li Y., Aronow B.J., Zhang J. LMO7 mediates cell-specific activation of the rho-myocardin-related transcription factor-serum response factor pathway and plays an important role in breast cancer cell migration. Mol. Cell. Biol. 2011, 31:3223-3240.
19. Huet G., Mérot Y., Le Dily F., Kern L., Ferrière F., Saligaut C., Boujrad N., Pakdel F., Métivier R., Flouriot G. Loss of E-cadherin-mediated cell contacts reduces estrogen receptor alpha (ER alpha) transcriptional efficiency by affecting the respective contribution exerted by AF1 and AF2 transactivation functions. Biochem. Biophys. Res. Commun. 2008, 365:304-309.
20. Huet G., Mérot Y., Percevault F., Tiffoche C., Arnal J.-F., Boujrad N., Pakdel F., Métivier R., Flouriot G. Repression of the estrogen receptor-alpha transcriptional activity by the Rho/megakaryoblastic leukemia 1 signaling pathway. J. Biol. Chem. 2009, 284:33729-33739.
21. Jordan V.C. Antiestrogens and selective estrogen receptor modulators as multifunctional medicines. 2. Clinical considerations and new agents. J. Med. Chem. 2003, 46:1081-1111.
22. Kerdivel G., Boudot A., Pakdel F. Estrogen represses CXCR7 gene expression by inhibiting the recruitment of NFκB transcription factor at the CXCR7 promoter in breast cancer cells. Biochem. Biophys. Res. Commun. 2013.
23. Kikuchi K., Li X., Zheng Y., Takano Y. Invasion of breast cancer cells into collagen matrix requires TGF-α and Cdc42 signaling. FEBS Lett. 2011, 585:286-290.
24. Kim C., Tang G., Pogue-Geile K.L., Costantino J.P., Baehner F.L., Baker J., Cronin M.T., Watson D., Shak S., Bohn O.L., Fumagalli D., Taniyama Y., Lee A., Reilly M.L., Vogel V.G., McCaskill-Stevens W., Ford L.G., Geyer C.E., Wickerham D.L., Wolmark N., Paik S. Estrogen receptor (ESR1) mRNA expression and benefit from tamoxifen in the treatment and prevention of estrogen receptor-positive breast cancer. J. Clin. Oncol. 2011, 29:4160-4167.
25. Luker K.E., Luker G.D. Functions of CXCL12 and CXCR4 in breast cancer. Cancer Lett. 2006, 238:30-41.
26. Massarweh S., Schiff R. Resistance to endocrine therapy in breast cancer: exploiting estrogen receptor/growth factor signaling crosstalk. Endocr. Related Cancer 2006, 13(Suppl. 1):S15-S24.
27. Medjkane S., Perez-Sanchez C., Gaggioli C., Sahai E., Treisman R. Myocardin-related transcription factors and SRF are required for cytoskeletal dynamics and experimental metastasis. Nat. Cell Biol. 2009, 11:257-268.
28. Mérot Y., Métivier R., Penot G., Manu D., Saligaut C., Gannon F., Pakdel F., Kah O., Flouriot G. The relative contribution exerted by AF-1 and AF-2 transactivation functions in estrogen receptor alpha transcriptional activity depends upon the differentiation stage of the cell. J. Biol. Chem. 2004, 279:26184-26191.
29. Micalizzi D.S., Farabaugh S.M., Ford H.L. Epithelial-mesenchymal transition in cancer: parallels between normal development and tumor progression. J. Mammary Gland Biol. Neoplasia 2010, 15:117-134.
30. Milyavsky M., Shats I., Cholostoy A., Brosh R., Buganim Y., Weisz L., Kogan I., Cohen M., Shatz M., Madar S., Kalo E., Goldfinger N., Yuan J., Ron S., MacKenzie K., Eden A., Rotter V. Inactivation of myocardin and p16 during malignant transformation contributes to a differentiation defect. Cancer Cell 2007, 11:133-146.
31. Mirisola V., Zuccarino A., Bachmeier B.E., Sormani M.P., Falter J., Nerlich A., Pfeffer U. CXCL12/SDF1 expression by breast cancers is an independent prognostic marker of disease-free and overall survival. Eur. J. Cancer 2009, 45:2579-2587.
32. Miyamoto S., Yagi H., Yotsumoto F., Kawarabayashi T., Mekada E. Heparin-binding epidermal growth factor-like growth factor as a novel targeting molecule for cancer therapy. Cancer Sci. 2006, 97:341-347.
33. Morita T., Mayanagi T., Sobue K. Dual roles of myocardin-related transcription factors in epithelial mesenchymal transition via slug induction and actin remodeling. J. Cell Biol. 2007, 179:1027-1042.
34. Muehlich S., Wang R., Lee S.-M., Lewis T.C., Dai C., Prywes R. Serum-induced phosphorylation of the serum response factor coactivator MKL1 by the extracellular signal-regulated kinase 1/2 pathway inhibits its nuclear localization. Mol. Cell. Biol. 2008, 28:6302-6313.
35. Muehlich S., Hampl V., Khalid S., Singer S., Frank N., Breuhahn K., et al. The transcriptional coactivators megakaryoblastic leukemia 1/2 mediate the effects of loss of the tumor suppressor deleted in liver cancer 1. Oncogene 2011, e-pub ahead of print 5 December 2011; http://dx.doi.org/10.1038/onc.2011.560.
36. Murphy L.C., Seekallu S.V., Watson P.H. Clinical significance of estrogen receptor phosphorylation. Endocr. Related Cancer 2011, 18:R1-R14.
37. Musgrove E.A., Sutherland R.L. Biological determinants of endocrine resistance in breast cancer. Nat. Rev. Cancer 2009, 9:631-643.
38. Newby J.C., Johnston S.R., Smith I.E., Dowsett M. Expression of epidermal growth factor receptor and c-erbB2 during the development of tamoxifen resistance in human breast cancer. Clin. Cancer Res. 1997, 3:1643-1651.
39. Normanno N., Qi C., Gullick W., Persico G., Yarden Y., Wen D., Plowman G., Kenney N., Johnson G., Kim N., Brandt R., Martinezlacaci I., Dickson R., Salomon D. Expression of amphiregulin, cripto-1, and heregulin-alpha in human breast-cancer cells. Int. J. Oncol. 1993, 2:903-911.
40. Platet N., Cathiard A.M., Gleizes M., Garcia M. Estrogens and their receptors in breast cancer progression: a dual role in cancer proliferation and invasion. Crit. Rev. Oncol. Hematol. 2004, 51:55-67.
41. Posern G., Sotiropoulos A., Treisman R. Mutant actins demonstrate a role for unpolymerized actin in control of transcription by serum response factor. Mol. Biol. Cell 2002, 13:4167-4178.
42. Purrington K.S., Slager S., Eccles D., Yannoukakos D., Fasching P.A., Miron P., Carpenter J., et al. Genome-wide association study identifies 25 known breast cancer susceptibility loci as risk factors for triple-negative breast cancer. Carcinogenesis 2013, (Epub ahead of print).
43. Rastelli F., Biancanelli S., Falzetta A., Martignetti A., Casi C., Bascioni R., Giustini L., Crispino S. Triple-negative breast cancer: current state of the art. Tumori 2010, 96:875-888.
44. Rau K.-M., Kang H.-Y., Cha T.-L., Miller S.A., Hung M.-C. The mechanisms and managements of hormone-therapy resistance in breast and prostate cancers. Endocr. Related Cancer 2005, 12:511-532.
45. Rhodes L.V., Short S.P., Neel N.F., Salvo V.A., Zhu Y., Elliott S., Wei Y., Yu D., Sun M., Muir S.E., Fonseca J.P., Bratton M.R., Segar C., Tilghman S.L., Sobolik-Delmaire T., Horton L.W., Zaja-Milatovic S., Collins-Burow B.M., Wadsworth S., Beckman B.S., Wood C.E., Fuqua S.A., Nephew K.P., Dent P., Worthylake R.A., Curiel T.J., Hung M.-C., Richmond A., Burow M.E. Cytokine receptor CXCR4 mediates estrogen-independent tumorigenesis, metastasis, and resistance to endocrine therapy in human breast cancer. Cancer Res. 2010, 71:603-613.
46. Rochefort H., Platet N., Hayashido Y., Derocq D., Lucas A., Cunat S., Garcia M. Estrogen receptor mediated inhibition of cancer cell invasion and motility: an overview. J. Steroid Biochem. Mol. Biol. 1998, 65:163-168.
47. Scharenberg M.A., Chiquet-Ehrismann R., Asparuhova M.B. Megakaryoblastic leukemia protein-1 (MKL1): Increasing evidence for an involvement in cancer progression and metastasis. Int. J. Biochem. Cell Biol. 2010, 42:1911-1914.
48. Vartiainen M.K., Guettler S., Larijani B., Treisman R. Nuclear actin regulates dynamic subcellular localization and activity of the SRF cofactor MAL. Science 2007, 316:1749-1752.
49. Wickerham D.L., Costantino J.P., Vogel V.G., Cronin W.M., Cecchini R.S., Ford L.G., Wolmark N. The use of tamoxifen and raloxifene for the prevention of breast cancer. Recent Res. Cancer Res. 2009, 181:113-119.
50. Willmarth N.E., Ethier S.P. Autocrine and juxtacrine effects of amphiregulin on the proliferative, invasive, and migratory properties of normal and neoplastic human mammary epithelial cells. J. Biol. Chem. 2006, 281:37728-37737.
51. Zhang Z., Funk C., Roy D., Glasser S., Mulholland J. Heparin-binding epidermal growth factor-like growth factor is differentially regulated by progesterone and estradiol in rat uterine epithelial and stromal cells. Endocrinology 1994, 134:1089-1094.
52. Zhao C., Dahlman-Wright K., Gustafsson J.-A. Estrogen receptor beta: an overview and update. Nucl. Recept. Signal. 2008, 6:e003.