Estrogen receptor alpha mediates progestin-induced mammary tumor growth by interacting with progesterone receptors at the cyclin D1/MYC promoters

Cancer Research

Volumn 72, Issue 9, 2012, Pages 2416-2427

  Giulianelli, Sebastián ^a   Vaqué, José P ^d   Soldati, Rocío ^a   Wargon, Victoria ^a   Vanzulli, Silvia I ^b   Martins, Rubén ^c   Zeitlin, Eduardo ^c   Molinolo, Alfredo A ^d,e   Helguero, Luisa A ^a   Lamb, Caroline A ^a   Gutkind, J Silvio ^d   Lanari, Claudia ^a  

^a INST DE BIOL Y MED EXPERIMENTAL   (Argentina)

^b ACADEMIA NACIONAL DE MEDICINA   (Argentina)

^c Policlinico Bancario   (Argentina)

^d NATIONAL INSTITUTE OF DENTAL AND CRANIOFACIAL RESEARCH   (United States)

^e UNIVERSITY OF AVEIRO   (Portugal)

Author keywords

[No Author keywords available]

Indexed keywords

CYCLIN D1; ESTROGEN RECEPTOR ALPHA; FULVESTRANT; GESTAGEN; MEDROXYPROGESTERONE ACETATE; MYC PROTEIN; PROGESTERONE RECEPTOR;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BREAST CARCINOMA; CELL PROLIFERATION; CHROMATIN IMMUNOPRECIPITATION; CONTROLLED STUDY; DRUG MECHANISM; FEMALE; GENE EXPRESSION REGULATION; GENE SILENCING; HUMAN; HUMAN CELL; HUMAN TISSUE; MOUSE; NONHUMAN; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; PROMOTER REGION; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN PROTEIN INTERACTION; RECEPTOR BINDING; RNA INTERFERENCE; TUMOR CELL; TUMOR GROWTH;

ANIMALS; BREAST NEOPLASMS; CELL GROWTH PROCESSES; CELL NUCLEUS; CYCLIN D1; ESTRADIOL; ESTROGEN RECEPTOR ALPHA; FEMALE; GENE EXPRESSION REGULATION, NEOPLASTIC; GENES, MYC; GENES, REPORTER; HUMANS; MAMMARY NEOPLASMS, EXPERIMENTAL; MEDROXYPROGESTERONE ACETATE; MICE; MICE, INBRED BALB C; NEOPLASMS, HORMONE-DEPENDENT; PROMOTER REGIONS, GENETIC; RECEPTORS, PROGESTERONE;

EID: 84860540830     PISSN: 00085472     EISSN: 15387445     Source Type: Journal    
DOI: 10.1158/0008-5472.CAN-11-3290     Document Type: Article

References (49)

1. Ferlay J, Shin HR, Bray F, Forman D, Mathers C, Parkin DM. Estimates of worldwide burden of cancer in 2008:GLOBOCAN2008. Int J Cancer 2010;127:2893-917.
2. Santen R, Cavalieri E, Rogan E, Russo J, Guttenplan J, Ingle J, et al. Estrogen mediation of breast tumor formation involves estrogen receptor-dependent, as well as independent, genotoxic effects. Ann N Y Acad Sci 2009;1155:132-40.
3. Aupperlee M, Kariagina A, Osuch J, Haslam SZ. Progestins and breast cancer. Breast Dis 2005;24:37-57.
4. Lange CA, Sartorius CA, Abdel-Hafiz H, Spillman MA, Horwitz KB, Jacobsen BM. Progesterone receptor action: translating studies in breast cancer models to clinical insights. Adv Exp Med Biol 2008;630:94-111.
5. Lange CA. Challenges to defining a role for progesterone in breast cancer. Steroids 2008;73:914-21.
6. Cho H, Aronica SM, Katzenellenbogen BS. Regulation of progesterone receptor gene expression in MCF-7 breast cancer cells: a comparison of the effects of cyclic adenosine 3′,5′-monophosphate, estradiol, insulin-like growth factor-I, and serum factors. Endocrinology 1994;134:658-64.
7. Migliaccio A, Piccolo D, Castoria G, Di Domenico M, Bilancio A, Lombardi M, et al. Activation of the Src/p21ras/Erk pathway by progesterone receptor via cross-talk with estrogen receptor. EMBO J 1998;17:2008-18. (Pubitemid 28154530)
8. Ballare C, Uhrig M, Bechtold T, Sancho E, Di Domenico M, Migliaccio A, et al. Two domains of the progesterone receptor interact with the estrogen receptor and are required for progesterone activation of the c-Src/Erk pathway in mammalian cells. Mol Cell Biol 2003;23:1994-2008. (Pubitemid 36278811)
9. Boonyaratanakornkit V, Scott MP, Ribon V, Sherman L, Anderson SM, Maller JL, et al. Progesterone receptor contains a proline-rich motif that directly interacts with SH3 domains and activates c-Src family tyrosine kinases. Mol Cell 2001;8:269-80. (Pubitemid 32831545)
10. Lanari C, Lamb CA, Fabris VT, Helguero LA, Soldati R, Bottino MC, et al. The MPA mouse breast cancer model: evidence for a role of progesterone receptors in breast cancer. Endocr Relat Cancer 2009;16:333-50.
11. Hissom JR, Moore MR. Progestin effects on growth in the human breast cancer cell line T-47D-possible therapeutic implications. Biochem Biophys Res Commun 1987;145:706-11. (Pubitemid 17093511)
12. Lange CA, Richer JK, Horwitz KB. Hypothesis: Progesterone primes breast cancer cells for cross-talk with proliferative or antiproliferative signals. Mol Endocrinol 1999;13:829-36. (Pubitemid 30645301)
13. Institute of Laboratory Animal ResourcesCoLSNRC. Guide for the care and use of laboratory animals. Washington, D.C.: National Academy Press; 1996.
14. Osborne CK, Coronado-Heinsohn EB, Hilsenbeck SG, McCue BL, Wakeling AE, McClelland RA, et al. Comparison of the effects of a pure steroidal antiestrogen with those of tamoxifen in a model of human breast cancer. J Natl Cancer Inst 1995;87:746-50.
15. Giulianelli S, Cerliani JP, Lamb CA, Fabris VT, Bottino MC, Gorostiaga MA, et al. Carcinoma-associated fibroblasts activate progesterone receptors and induce hormone independent mammary tumor growth: A role for the FGF-2/FGFR-2 axis. Int J Cancer 2008;123:2518-31.
16. Lamb CA, Helguero LA, Fabris V, Lucas C, Molinolo AA, Lanari C. Differential effects of raloxifene, tamoxifen and fulvestrant on a murine mammary carcinoma. Breast Cancer Res Treat 2003;79:25-35. (Pubitemid 36561040)
17. Soldati R, Wargon V, Cerliani JP, Giulianelli S, Vanzulli SI, Gorostiaga MA, et al. Inhibition of mammary tumor growth by estrogens: is there a specific role for estrogen receptors alpha and beta? Breast Cancer Res Treat 2010;123:709-24.
18. Cerliani JP, Guillardoy T, Giulianelli S, Vaque JP, Gutkind JS, Vanzulli SI, et al. Interaction between FGFR-2, STAT5, and progesterone receptors in breast cancer. Cancer Res 2011;71:3720-31.
19. French AP, Mills S, Swarup R, Bennett MJ, Pridmore TP. Colocalization of fluorescent markers in confocal microscope images of plant cells. Nat Protoc 2008;3:619-28. (Pubitemid 351516758)
20. Helguero LA, Viegas M, Asaithamby A, Shyamala G, Lanari C, Molinolo AA. Progesterone receptor expression in medroxyprogesterone acetate-induced murinemammary carcinomas and response to endocrine treatment. Breast Cancer Res Treat 2003;79:379-90. (Pubitemid 36750945)
21. Bottino MC, Cerliani JP, Rojas P, Giulianelli S, Soldati R, Mondillo C, et al. Classical membrane progesterone receptors in murine mammary carcinomas: agonistic effects of progestins and RU-486 mediating rapid non-genomic effects. Breast Cancer Res Treat 2011;126:621-36.
22. Gardmo C, Kotokorpi P, Helander H, Mode A. Transfection of adult primary rat hepatocytes in culture. Biochem Pharmacol 2005;69:1805-13. (Pubitemid 40780080)
23. Cerliani JP, Giulianelli S, Sahores A, Wargon V, Gongora A, Baldi A, et al. Mifepristone inhibits MPA-and FGF2-induced mammary tumor growth but not FGF2-induced mammary hyperplasia. Medicina (B Aires) 2010;70:529-32.
24. Weigel NL, Moore NL. Steroid receptor phosphorylation: a key modulator of multiple receptor functions. Mol Endocrinol 2007;21:2311-9. (Pubitemid 47529347)
25. Urtreger A, Lapeda V, Puricelli L, Rivelli A, Vidal MC, Lustig E, et al. Modulation of fibronectin expression and proteolytic activity associated with the invasive and metastatic phenotype in two new murine mammary tumor cell lines. Int J Oncol 1997;3:489-96. (Pubitemid 27364280)
26. Beguelin W, Diaz Flaque MC, Proietti CJ, Cayrol F, Rivas MA, Tkach M, et al. Progesterone receptor induces ErbB-2 nuclear translocation to promote breast cancer growth via a novel transcriptional effect: ErbB-2 function as a coactivator of Stat3. Mol Cell Biol 2010;30:5456-72.
27. Boonyaratanakornkit V, McGowan E, Sherman L, Mancini MA, Cheskis BJ, Edwards DP. The role of extranuclear signaling actions of progesterone receptor in mediating progesterone regulation of gene expression and the cell cycle. Mol Endocrinol 2007;21:359-75. (Pubitemid 46184890)
28. Musgrove EA, Hamilton JA, Lee CS, Sweeney KJ, Watts CK, Sutherland RL. Growth factor, steroid, and steroid antagonist regulation of cyclin gene expression associated with changes in T-47D human breast cancer cell cycle progression. Mol Cell Biol 1993;13:3577-87. (Pubitemid 23157295)
29. Saitoh M, Ohmichi M, Takahashi K, Kawagoe J, Ohta T, Doshida M, et al. Medroxyprogesterone acetate induces cell proliferation through up-regulation of cyclin D1 expression via phosphatidylinositol 3-kinase/Akt/nuclear factor-kappaB cascade in human breast cancer cells. Endocrinology 2005;146:4917-25. (Pubitemid 41446630)
30. Skildum A, Faivre E, Lange CA. Progesterone receptors induce cell cycle progression via activation of mitogen-activated protein kinases. Mol Endocrinol 2005;19:327-39. (Pubitemid 40223458)
31. Moore MR, Zhou JL, Blankenship KA, Strobl JS, Edwards DP, Gentry RN. A sequence in the 50 flanking region confers progestin responsiveness on the human c-myc gene. J Steroid Biochem Mol Biol 1997;62:243-52. (Pubitemid 27504755)
32. Musgrove EA, Lee CS, Sutherland RL. Progestins both stimulate and inhibit breast cancer cell cycle progression while increasing expression of transforming growth factor alpha, epidermal growth factor receptor, c-fos, and c-myc genes. Mol Cell Biol 1991;11:5032-43. (Pubitemid 21895264)
33. Katiyar P, Ma Y, Riegel A, Fan S, Rosen EM. Mechanism of BRCA1-mediated inhibition of progesterone receptor transcriptional activity. Mol Endocrinol 2009;23:1135-46.
34. Quiles I, Millan-Arino L, Subtil-Rodriguez A, Minana B, Spinedi N, Ballare C, et al. Mutational analysis of progesterone receptor functional domains in stable cell lines delineates sets of genes regulated by different mechanisms. Mol Endocrinol 2009;23:809-26.
35. Nishino T, Ishibashi K, Hirtreiter C, Nishino Y. Potentiation of the antitumor effect of tamoxifen by combination with the antiprogestin onapristone. J Steroid Biochem Mol Biol 2009;116:187-90.
36. Wargon V, Helguero LA, Bolado J, Rojas P, Novaro V, Molinolo A, et al. Reversal of antiprogestin resistance and progesterone receptor isoform ratio in acquired resistant mammary carcinomas. Breast Cancer Res Treat 2009;116:449-60.
37. Lin VC, Ng EH, Aw SE, Tan MG, Ng EH, Chan VS, et al. Progestins inhibit the growth of MDA-MB-231 cells transfected with progesterone receptor complementary DNA. Clin Cancer Res 1999;5:395-403. (Pubitemid 29085193)
38. Vazquez SM, Mladovan A, Garbovesky C, Baldi A, Luthy IA. Three novel hormone-responsive cell lines derivedfromprimaryhuman breast carcinomas: functional characterization. J Cell Physiol 2004;199:460-9. (Pubitemid 38580442)
39. Dressing GE, Hagan CR, Knutson TP, Daniel AR, Lange CA. Progesterone receptors act as sensors formitogenic protein kinases in breast cancer models. Endocr Relat Cancer 2009;16:351-61.
40. Jacobsen BM, Horwitz KB. Progesterone receptors, their isoforms and progesterone regulated transcription. Mol Cell Endocrinol 2011 Sep 17. [Epub ahead of print].
41. Wang C, Mayer JA, Mazumdar A, Fertuck K, Kim H, Brown M, et al. Estrogen induces c-myc gene expression via an upstream enhancer activated by the estrogen receptor and the AP-1 transcription factor. Mol Endocrinol 2011;25:1527-38.
42. Vicent GP, Nacht AS, Zaurin R, Ballare C, Clausell J, Beato M. Minireview: role of kinases and chromatin remodeling in progesterone signaling to chromatin. Mol Endocrinol 2010;24:2088-98.
43. Lange CA. Making sense of cross-talk between steroid hormone receptors and intracellular signaling pathways: who will have the last word? Mol Endocrinol 2004;18:269-78. (Pubitemid 38183927)
44. Cicatiello L, Addeo R, Sasso A, Altucci L, Petrizzi VB, Borgo R, et al. Estrogens and progesterone promote persistent CCND1 gene activation during G1 by inducing transcriptional derepression via c-Jun/c-Fos/estrogen receptor (progesterone receptor) complex assembly to a distal regulatory element and recruitment of cyclin D1 to its own gene promoter. Mol Cell Biol 2004;24:7260-74. (Pubitemid 39014451)
45. Fernandez-Valdivia R, Mukherjee A, Creighton CJ, Buser AC, DeMayo FJ, Edwards DP, et al. Transcriptional response of the murine mammary gland to acute progesterone exposure. Endocrinology 2008;149:6236-50.
46. Buser AC, Obr AE, Kabotyanski EB, Grimm SL, Rosen JM, Edwards DP. Progesterone receptor directly inhibits {beta}-casein gene transcription in mammary epithelial cells through promoting promoter and enhancer repressive chromatin modifications. Mol Endocrinol 2011;25:955-68.
47. O'Malley BW, Kumar R. Nuclear receptor coregulators in cancer biology. Cancer Res 2009;69:8217-22.
48. Lange CA, Yee D. Progesterone and breast cancer. Womens Health (Lond Engl) 2008;4:151-62. (Pubitemid 351513635)
49. Gonzalez V, Hurley LH. The c-MYC NHE III(1): function and regulation. Annu Rev Pharmacol Toxicol 2010;50:111-29.