Bottino, M.C.; Cerliani, J.P.; Rojas, P.; Giulianelli, S.; Soldati, R.; Mondillo, C.; Gorostiaga, M.A.; Pignataro, O.P.; Calvo, J.C.; Gutkind, J.S.; Amornphimoltham, P.; Molinolo, A.A.; Lüthy, I.A.; Lanari, C. "Classical membrane progesterone receptors in murine mammary carcinomas: Agonistic effects of progestins and RU-486 mediating rapid non-genomic effects" (2011) Breast Cancer Research and Treatment. 126(3):621-636
Estamos trabajando para incorporar este artículo al repositorio
Consulte el artículo en la página del editor
Consulte la política de Acceso Abierto del editor


In this article, we demonstrate the expression of functional progesterone binding sites at the cell membrane in murine mammary carcinomas that are stimulated by progestins and inhibited by antiprogestins. Using confocal immunofluorescence, ligand binding and cell compartment-specific western blots, we were able to identify the presence of the classical progesterone receptors. Medrox-yprogesterone acetate (MPA) and RU-486 (1 × 10-11 and 1 × 10-8 M) behaved as agonists activating extracellular signal-regulated kinases (ERKs) and progestin-regulated proteins, except for Cyclin D1 and Tissue factor which failed to increase with 1 × 10 -8 M RU-486, an experimental condition that allows PR to bind DNA. These results predicted a full agonist effect at low concentrations of RU-486. Accordingly, at concentrations lower than 1 × 10-11 M, RU-486 increased cell proliferation in vitro. This effect was abolished by incubation with the ERK kinase inhibitor PD 98059 or by OH-tamoxifen. In vivo, at a daily dose of 1.2 μg/kg body weight RU-486 increased tumor growth, whereas at 12 mg/kg induces tumor regression. Our results indicate that low concentrations of MPA and RU-486 induce similar agonistic non-genomic effects, whereas RU-486 at higher concentrations may inhibit cell proliferation by genomic-induced effects. This suggests that RU-486 should be therapeutically administered at doses high enough to guarantee its genomic inhibitory effect. © Springer Science+Business Media, LLC. 2010.


Documento: Artículo
Título:Classical membrane progesterone receptors in murine mammary carcinomas: Agonistic effects of progestins and RU-486 mediating rapid non-genomic effects
Autor:Bottino, M.C.; Cerliani, J.P.; Rojas, P.; Giulianelli, S.; Soldati, R.; Mondillo, C.; Gorostiaga, M.A.; Pignataro, O.P.; Calvo, J.C.; Gutkind, J.S.; Amornphimoltham, P.; Molinolo, A.A.; Lüthy, I.A.; Lanari, C.
Filiación:Laboratorio de Carcinogénesis Hormonal, Instituto de Biología y Medicina Experimental, Consejo Nacional de Investigaciones Científicas y Técnicas - CONICET, Vuelta de Obligado 2490, C1428ADN Buenos Aires, Argentina
Laboratorio de Hormonas y Cáncer, Instituto de Biología y Medicina Experimental, Consejo Nacional de Investigaciones Científicas y Técnicas - CONICET, Vuelta de Obligado 2490, C1428ADN Buenos Aires, Argentina
Departamento de Química Biológica, Facultad de Ciencias Exactas y Naturales, Universidad de Buenos Aires, Buenos Aires, Argentina
Oral and Pharyngeal Cancer Branch, National Institute of Dental and Craniofacial Research, National Institutes of Health, Bethesda, MD, United States
Palabras clave:Antiprogestins; Breast cancer treatment; Mammary carcinomas; Membrane progesterone receptors; Non-genomic effects; Progesterone receptor isoforms: Membrane-initiated steroid signaling; Progestins; 2 (2 amino 3 methoxyphenyl)chromone; cyclin D1; DNA; hydroxytamoxifen; medroxyprogesterone acetate; mifepristone; mitogen activated protein kinase; progesterone receptor; thromboplastin; animal experiment; animal model; animal tissue; article; binding site; breast carcinoma; cancer growth; cancer regression; cell membrane; cell proliferation; concentration response; controlled study; drug dose comparison; drug effect; enzyme activation; female; human; human cell; immunofluorescence test; in vitro study; in vivo study; ligand binding; mouse; nonhuman; nucleotide sequence; priority journal; protein DNA binding; protein expression; Western blotting; Animals; Female; Gene Expression Regulation, Neoplastic; Mammary Neoplasms, Animal; Medroxyprogesterone Acetate; Mice; Mice, Inbred BALB C; Microscopy, Confocal; Microscopy, Fluorescence; Mifepristone; Neoplasm Transplantation; Progestins; Receptors, Progesterone; Steroids
Página de inicio:621
Página de fin:636
Título revista:Breast Cancer Research and Treatment
Título revista abreviado:Breast Cancer Res. Treat.
CAS:2 (2 amino 3 methoxyphenyl)chromone, 167869-21-8; DNA, 9007-49-2; hydroxytamoxifen, 68047-06-3; medroxyprogesterone acetate, 71-58-9; mifepristone, 84371-65-3; mitogen activated protein kinase, 142243-02-5; thromboplastin, 9035-58-9; Medroxyprogesterone Acetate, 71-58-9; Mifepristone, 84371-65-3; Progestins; Receptors, Progesterone; Steroids


  • Mangelsdorf, D.J., Thummel, C., Beato, M., Herrlich, P., Schutz, G., Umesono, K., Blumberg, B., Chambon, P., The nuclear receptor superfamily: The second decade (1995) Cell, 83, pp. 835-839
  • Torchia, J., Glass, C., Rosenfeld, M.G., Co-activators and co-repressors in the integration of transcriptional responses (1998) Current Opinion in Cell Biology, 10 (3), pp. 373-383. , DOI 10.1016/S0955-0674(98)80014-8
  • Bagchi, M.K., Tsai, S.Y., Weigel, N.L., Tsai, M.J., O'Malley, B.W., Regulation of in vitro transcription by progesterone receptor. Characterization and kinetic studies (1990) J Biol Chem, 265, pp. 5129-5134
  • Sutter-Dub, M.T., Rapid non-genomic and genomic responses to progestogens, estrogens, and glucocorticoids in the endocrine pancreatic B cell, the adipocyte and other cell types (2002) Steroids, 67, pp. 77-93
  • Pietras, R.J., Szego, C.M., Specific binding sites for oestrogen at the outer surfaces of isolated endometrial cells (1977) Nature, 265 (5589), pp. 69-72. , DOI 10.1038/265069a0
  • Cato, A.C., Nestl, A., Mink, S., Rapid actions of steroid receptors in cellular signaling pathways (2002) Sci STKE, 138, pp. RE9
  • Watson, C.S., Gametchu, B., Membrane-initiated steroid actions and the proteins that mediate them (1999) Proc Soc Exp Biol Med, 220, pp. 9-19
  • Song, R.X.-D., Fan, P., Yue, W., Chen, Y., Santen, R.J., Role of receptor complexes in the extranuclear actions of estrogen receptor α in breast cancer (2006) Endocrine-Related Cancer, 13 (SUPPL. 1), pp. S3-S13. , DOI 10.1677/erc.1.01322
  • Ehring, G.R., Kerschbaum, H.H., Eder, C., Neben, A.L., Fanger, C.M., Khoury, R.M., Negulescu, P.A., Cahalan, M.D., A nongenomic mechanism for progesterone-mediated immunosuppression: Inhibition of K+ channels, Ca2+ signaling, and gene expression in T lymphocytes (1998) Journal of Experimental Medicine, 188 (9), pp. 1593-1602. , DOI 10.1084/jem.188.9.1593
  • Grazzini, E., Guillon, G., Mouillac, B., Zingg, H.H., Inhibition of oxytocin receptor function by direct binding of progesterone (1998) Nature, 392 (6675), pp. 509-512. , DOI 10.1038/33176
  • Valera, S., Ballivet, M., Bertrand, D., Progesterone modulates a neuronal nicotinic acetylcholine receptor (1992) Proc Natl Acad Sci USA, 89, pp. 9949-9953
  • McEwen, B.S., Non-genomic and genomic effects of steroids on neural activity (1991) Trends Pharmacol Sci, 12, pp. 141-147
  • Krebs, C.J., Jarvis, E.D., Chan, J., Lydon, J.P., Ogawa, S., Pfaff, D.W., A membrane-associated progesterone-binding protein, 25-Dx, is regulated by progesterone in brain regions involved in female reproductive behaviors (2000) Proc Natl Acad Sci USA, 97, pp. 12816-12821
  • Labombarda, F., Gonzalez, S.L., Deniselle, M.C.G., Vinson, G.P., Schumacher, M., De Nicola, A.F., Guennoun, R., Effects of injury and progesterone treatment on progesterone receptor and progesterone binding protein 25-Dx expression in the rat spinal cord (2003) Journal of Neurochemistry, 87 (4), pp. 902-913. , DOI 10.1046/j.1471-4159.2003.02055.x
  • Zhu, Y., Bond, J., Thomas, P., Identification, classification, and partial characterization of genes in humans and other vertebrates homologous to a fish membrane progestin receptor (2003) Proceedings of the National Academy of Sciences of the United States of America, 100 (5), pp. 2237-2242. , DOI 10.1073/pnas.0436133100
  • Zhu, Y., Rice, C.D., Pang, Y., Pace, M., Thomas, P., Cloning, expression, and characterization of a membrane progestin receptor and evidence it is an intermediary in meiotic maturation of fish oocytes (2003) Proceedings of the National Academy of Sciences of the United States of America, 100 (5), pp. 2231-2236. , DOI 10.1073/pnas.0336132100
  • Dressing, G.E., Thomas, P., Identification of membrane progestin receptors in human breast cancer cell lines and biopsies and their potential involvement in breast cancer (2007) Steroids, 72 (2), pp. 111-116. , DOI 10.1016/j.steroids.2006.10.006, PII S0039128X06002145, FASEB 2006 Summer Research Conference Mechanism of Action of Steroid Hormones: Integration of Membrane and Nucleus Initiated Effects
  • Krietsch, T., Fernandes, M.S., Kero, J., Losel, R., Heyens, M., Lam, E.W.-F., Huhtaniemi, I., Gellersen, B., Human homologs of the putative G protein-coupled membrane progestin receptors (mPRα, β, and γ) localize to the endoplasmic reticulum and are not activated by progesterone (2006) Molecular Endocrinology, 20 (12), pp. 3146-3164. ,, DOI 10.1210/me.2006-0129
  • Thomas, P., Pang, Y., Dong, J., Groenen, P., Kelder, J., De Vlieg, J., Zhu, Y., Tubbs, C., Steroid and G protein binding characteristics of the seatrout and human progestin membrane receptor α subtypes and their evolutionary origins (2007) Endocrinology, 148 (2), pp. 705-718. ,, DOI 10.1210/en.2006-0974
  • Molinolo, A.A., Lanari, C., Charreau, E.H., Sanjuan, N., Pasqualini, C.D., Mouse mammary tumors induced by medroxyprogesterone acetate: Immunohistochemistry and hormonal receptors (1987) Journal of the National Cancer Institute, 79 (6), pp. 1341-1350
  • Helguero, L.A., Lamb, C., Molinolo, A.A., Lanari, C., Evidence for two progesterone receptor binding sites in murine mammary carcinomas (2003) Journal of Steroid Biochemistry and Molecular Biology, 84 (1), pp. 9-14. , DOI 10.1016/S0960-0760(02)00267-4
  • Powell, C.E., Soto, A.M., Sonnenschein, C., Identification and characterization of membrane estrogen receptor from MCF7 estrogen-target cells (2001) Journal of Steroid Biochemistry and Molecular Biology, 77 (2-3), pp. 97-108. , DOI 10.1016/S0960-0760(01)00040-1, PII S0960076001000401
  • Razandi, M., Pedram, A., Greene, G.L., Levin, E.R., Cell membrane and nuclear estrogen receptors (ERs) originate from a single transcript: Studies of ERα and ERβ expressed in chinese hamster ovary cells (1999) Molecular Endocrinology, 13 (2), pp. 307-319. , DOI 10.1210/me.13.2.307
  • Razandi, M., Oh, P., Pedram, A., Schnitzer, J., Levin, E.R., ERs associate with and regulate the production of caveolin: Implications for signaling and cellular actions (2002) Molecular Endocrinology, 16 (1), pp. 100-115. , DOI 10.1210/me.16.1.100
  • Welter, B.H., Hansen, E.L., Saner, K.J., Wei, Y., Price, T.M., Membrane-bound progesterone receptor expression in human aortic endothelial cells (2003) Journal of Histochemistry and Cytochemistry, 51 (8), pp. 1049-1055
  • Younglai, E.V., Wu, Y., Foster, W.G., Lobb, D.K., Price, T.M., Binding of progesterone to cell surfaces of human granulosa-lutein cells (2006) Journal of Steroid Biochemistry and Molecular Biology, 101 (1), pp. 61-67. , DOI 10.1016/j.jsbmb.2006.06.018, PII S0960076006001622
  • Luconi, M., Francavilla, F., Porazzi, I., Macerola, B., Forti, G., Baldi, E., Human spermatozoa as a model for studying membrane receptors mediating rapid nongenomic effects of progesterone and estrogens (2004) Steroids, 69 (8-9), pp. 553-559. , DOI 10.1016/j.steroids.2004.05.013, PII S0039128X04000789
  • Pedram, A., Razandi, M., Sainson, R.C.A., Kim, J.K., Hughes, C.C., Levin, E.R., A conserved mechanism for steroid receptor translocation to the plasma membrane (2007) Journal of Biological Chemistry, 282 (31), pp. 22278-22288. ,, DOI 10.1074/jbc.M611877200
  • Lanari, C., Luthy, I., Lamb, C.A., Fabris, V., Pagano, E., Helguero, L.A., Sanjuan, N., Molinolo, A.A., Five novel hormone-responsive cell lines derived from murine mammary ductal carcinomas: In vivo and in vitro effects of estrogens and progestins (2001) Cancer Research, 61 (1), pp. 293-302
  • Dran, G., Luthy, I.A., Molinolo, A.A., Charreau, E.H., Pasqualini, C.D., Lanari, C., Effect of medroxyprogesterone acetate (MPA) and serum factors on cell proliferation in primary cultures of an MPA-induced mammary adenocarcinoma (1995) Breast Cancer Res Treat, 35, pp. 173-186
  • Fabris, V.T., Benavides, F., Conti, C., Merani, S., Lanari, C., Cytogenetic findings, Trp53 mutations, and hormone responsiveness in a medroxyprogesterone acetate induced murine breast cancer model (2005) Cancer Genetics and Cytogenetics, 161 (2), pp. 130-139. , DOI 10.1016/j.cancergencyto.2005.02.008, PII S0165460805000968
  • Urtreger, A.J., Ladeda, V.E., Puricelli, L.I., Rivelli, A., Del Carmen Vidal, M., De Lustig, E.S., De Bal Kier Joffe, E.D., Modulation of fibronectin expression and proteolytic activity associated with the invasive and metastatic phenotype in two new murine mammary tumor cell lines (1997) International Journal of Oncology, 11 (3), pp. 489-496
  • Clemm, D.L., Sherman, L., Boonyaratanakornkit, V., Schrader, W.T., Weigel, N.L., Edwards, D.P., Differential hormone-dependent phosphorylation of progesterone receptor A and B forms revealed by a phosphoserine site-specific monoclonal antibody (2000) Molecular Endocrinology, 14 (1), pp. 52-65. , DOI 10.1210/me.14.1.52
  • Lowry, O.H., Rosebrough, N.J., Farr, A.L., Protein measurements with the folin phenol reagent (1951) J Biol Chem, 193, pp. 265-275
  • Kampa, M., Nifli, A.-P., Charalampopoulos, I., Alexaki, V.-I., Theodoropoulos, P.A., Stathopoulos, E.N., Gravanis, A., Castanas, E., Opposing effects of estradiol- and testosterone-membrane binding sites on T47D breast cancer cell apoptosis (2005) Experimental Cell Research, 307 (1), pp. 41-51. , DOI 10.1016/j.yexcr.2005.02.027, PII S0014482705000935
  • Lamb, C.A., Helguero, L.A., Giulianelli, S., Soldati, R., Vanzulli, S.I., Molinolo, A., Lanari, C., Antisense oligonucleotides targeting the progesterone receptor inhibit hormone-independent breast cancer growth in mice (2005) Breast Cancer Res, 7, pp. R1111-R1121
  • Lamb, C., Simian, M., Molinolo, A., Pazos, P., Lanari, C., Regulation of cell growth of a progestin-dependent murine mammary carcinoma in vitro: Progesterone receptor involvement in serum or growth factor-induced cell proliferation (1999) Journal of Steroid Biochemistry and Molecular Biology, 70 (4-6), pp. 133-142. , DOI 10.1016/S0960-0760(99)00108-9, PII S0960076099001089
  • Giulianelli, S., Cerliani, J.P., Lamb, C.A., Fabris, V.T., Bottino, M.C., Gorostiaga, M.A., Novaro, V., Lanari, C., Carcinoma-associated fibroblasts activate progesterone receptors and induce hormone independent mammary tumor growth: A role for the FGF-2/FGFR-2 axis (2008) Int J Cancer, 123, pp. 2518-2531
  • Vanzulli, S.I., Soldati, R., Meiss, R., Colombo, L., Molinolo, A.A., Lanari, C., Estrogen or antiprogestin treatment induces complete regression of pulmonary and axillary metastases in an experimental model of breast cancer progression (2005) Carcinogenesis, 26 (6), pp. 1055-1063. , DOI 10.1093/carcin/bgi060
  • Lanari, C., Lamb, C.A., Fabris, V.T., Helguero, L.A., Soldati, R., Bottino, M.C., Giulianelli, S., Molinolo, A., The MPA mouse breast cancer model: Evidence for a role of progesterone receptors in breast cancer (2009) Endocr Relat Cancer, 16, pp. 333-350
  • Helguero, L.A., Viegas, M., Asaithamby, A., Shyamala, G., Lanari, C., Molinolo, A.A., Progesterone receptor expression in medroxyprogesterone acetate-induced murine mammary carcinomas and response to endocrine treatment (2003) Breast Cancer Research and Treatment, 79 (3), pp. 379-390. , DOI 10.1023/A:1024029826248
  • Wargon, V., Helguero, L.A., Bolado, J., Rojas, P., Novaro, V., Molinolo, A., Lanari, C., Reversal of antiprogestin resistance and progesterone receptor isoform ratio in acquired resistant mammary carcinomas (2009) Breast Cancer Res Treat, 116, pp. 449-460
  • Zhang, Z., Maier, B., Santen, R.J., Song, R.X.-D., Membrane association of estrogen receptor a mediates estrogen effect on MAPK activation (2002) Biochemical and Biophysical Research Communications, 294 (5), pp. 926-933. , DOI 10.1016/S0006-291X(02)00348-0, PII S0006291X02003480
  • Kousteni, S., Bellido, T., Plotkin, L.I., O'Brien, C.A., Bodenner, D.L., Han, L., Han, K., Manolagas, S.C., Nongenotropic, sex-nonspecific signaling through the estrogen or androgen receptors: Dissociation from transcriptional activity (2001) Cell, 104 (5), pp. 719-730
  • Qiu, M., Olsen, A., Faivre, E., Horwitz, K.B., Lange, C.A., Mitogen-activated protein kinase regulates nuclear association of human progesterone receptors (2003) Molecular Endocrinology, 17 (4), pp. 628-642. , DOI 10.1210/me.2002-0378
  • Balana, M.E., Lupu, R., Labriola, L., Charreau, E.H., Elizalde, P.V., Interactions between progestins and heregulin (HRG) signaling pathways: HRG acts as mediator of progestins proliferative effects in mouse mammary adenocarcinomas (1999) Oncogene, 18, pp. 6370-6379
  • Carbajal, L., Deng, J., Dressing, G.E., Hagan, C.R., Lange, C.A., Hammes, S.R., Meeting review: Extra-nuclear steroid receptors-integration with multiple signaling pathways (2009) Steroids, 74, pp. 551-554
  • Quiles, I., Millan-Arino, L., Subtil-Rodriguez, A., Minana, B., Spinedi, N., Ballare, C., Beato, M., Jordan, A., Mutational analysis of progesterone receptor functional domains in stable cell lines delineates sets of genes regulated by different mechanisms (2009) Mol Endocrinol, 23, pp. 809-826
  • Marino, M., Ascenzi, P., Acconcia, F., S-palmitoylation modulates estrogen receptor alpha localization and functions (2006) Steroids, 71, pp. 298-303
  • Salatino, M., Beguelin, W., Peters, M.G., Carnevale, R., Proietti, C.J., Galigniana, M.D., Vedoy, C.G., Elizalde, P.V., Progestin-induced caveolin-1 expression mediates breast cancer cell proliferation (2006) Oncogene, 25 (59), pp. 7723-7739. , DOI 10.1038/sj.onc.1209757, PII 1209757
  • Karteris, E., Zervou, S., Pang, Y., Dong, J., Hillhouse, E.W., Randeva, H.S., Thomas, P., Progesterone signaling in human myometrium through two novel membrane G protein-coupled receptors: Potential role in functional progesterone withdrawal at term (2006) Molecular Endocrinology, 20 (7), pp. 1519-1534. ,, DOI 10.1210/me.2005-0243
  • Bullock, L.P., Barthe, P.L., Mowszowicz, I., Orth, D.N., Bardin, C.W., The effect of progestins on submaxillary gland epidermal growth factor: Demonstration of androgenic, synandrogenic and antiandrogenic actions (1975) Endocrinology, 97, pp. 189-195
  • Kontula, K., Paavonen, T., Luukkainen, T., Andersson, L.C., Binding of progestins to the glucocorticoid receptor. Correlation to their glucocorticoid-like effects on in vitro functions of human mononuclear leukocytes (1983) Biochemical Pharmacology, 32 (9), pp. 1511-1518. , DOI 10.1016/0006-2952(83)90474-4
  • Montecchia, M.F., Lamb, C., Molinolo, A.A., Luthy, I.A., Pazos, P., Charreau, E., Vanzulli, S., Lanari, C., Progesterone receptor involvement in independent tumor growth in MPA- induced murine mammary adenocarcinomas (1999) Journal of Steroid Biochemistry and Molecular Biology, 68 (1-2), pp. 11-21. , DOI 10.1016/S0960-0760(98)00166-6, PII S0960076098001666
  • Horwitz, K.B., Tung, L., Takimoto, G.S., Novel mechanisms of antiprogestin action (1996) Acta Oncologica, 35 (2), pp. 129-140
  • Horwitz, K.B., The molecular biology of RU486 (1992) Is there a Role for Antiprogestins in the Treatment of Breast Cancer? Endocr Rev, 13, pp. 146-163
  • Labriola, L., Salatino, M., Proietti, C.J., Pecei, A., Coso, O.A., Kornblihtt, A.R., Charreau, E.H., Elizalde, P.V., Heregulin induces transcriptional activation of the progesterone receptor by a mechanism that requires functional ErbB-2 and mitogen-activated protein kinase activation in breast cancer cells (2003) Molecular and Cellular Biology, 23 (3), pp. 1095-1111. , DOI 10.1128/MCB.23.3.1095-1111.2003
  • Carnevale, R.P., Proietti, C.J., Salatino, M., Urtreger, A., Peluffo, G., Edwards, D.P., Boonyaratanakornkit, V., Elizalde, P.V., Progestin effects on breast cancer cell proliferation, proteases activation, and in vivo development of metastatic phenotype all depend on progesterone receptor capacity to activate cytoplasmic signaling pathways (2007) Molecular Endocrinology, 21 (6), pp. 1335-1358. ,, DOI 10.1210/me.2006-0304
  • Skildum, A., Faivre, E., Lange, C.A., Progesterone receptors induce cell cycle progression via activation of mitogen-activated protein kinases (2005) Molecular Endocrinology, 19 (2), pp. 327-339. , DOI 10.1210/me.2004-0306
  • Arruvito, L., Giulianelli, S., Flores, A.C., Paladino, N., Barboza, M., Lanari, C., Fainboim, L., NK cells expressing a progesterone receptor are susceptible to progesterone-induced apoptosis (2008) J Immunol, 180, pp. 5746-5753
  • Park, J.-I., Strock, C.J., Ball, D.W., Nelkin, B.D., The Ras/Raf/MEK/extracellular signal-regulated kinase pathway induces autocrine-paracrine growth inhibition via the leukemia inhibitory factor/JAK/STAT pathway (2003) Molecular and Cellular Biology, 23 (2), pp. 543-554. , DOI 10.1128/MCB.23.2.543-554.2003
  • Marshall, C.J., Specificity of receptor tyrosine kinase signaling: Transient versus sustained extracellular signal-regulated kinase activation (1995) Cell, 80, pp. 179-185
  • Murphy, L.O., Blenis, J., MAPK signal specificity: The right place at the right time (2006) Trends in Biochemical Sciences, 31 (5), pp. 268-275. , DOI 10.1016/j.jsg.2005.10.009, PII S0968000406000867
  • Leonhardt, S.A., Boonyaratanakornkit, V., Edwards, D.P., Progesterone receptor transcription and non-transcription signaling mechanisms (2003) Steroids, 68 (10-13), pp. 761-770. , DOI 10.1016/S0039-128X(03)00129-6
  • Rowan, B.G., O'Malley, B.W., Progesterone receptor coactivators (2000) Steroids, 65, pp. 545-549
  • Dressing, G.E., Hagan, C.R., Knutson, T.P., Daniel, A.R., Lange, C.A., Progesterone receptors act as sensors for mitogenic protein kinases in breast cancer models (2009) Endocr Relat Cancer, 16, pp. 351-361
  • Kato, S., Pinto, M., Carvajal, A., Espinoza, N., Monso, C., Sadarangani, A., Villalon, M., Owen, G.I., Progesterone increases tissue factor gene expression, procoagulant activity, and invasion in the breast cancer cell line ZR-75-1 (2005) Journal of Clinical Endocrinology and Metabolism, 90 (2), pp. 1181-1188. , DOI 10.1210/jc.2004-0857
  • Owen, G.I., Richer, J.K., Tung, L., Takimoto, G., Horwitz, K.B., Progesterone regulates transcription of the p21(WAF1) cyclin-dependent kinase inhibitor gene through Sp1 and CBP/p300 (1998) Journal of Biological Chemistry, 273 (17), pp. 10696-10701. , DOI 10.1074/jbc.273.17.10696
  • Cicatiello, L., Addeo, R., Sasso, A., Altucci, L., Petrizzi, V.B., Borgo, R., Cancemi, M., Weisz, A., 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 (2004) Molecular and Cellular Biology, 24 (16), pp. 7260-7274. , DOI 10.1128/MCB.24.16.7260-7274.2004
  • Lydon, J.P., DeMayo, F.J., Funk, C.R., Mani, S.K., Hughes, A.R., Montgomery Jr., C.A., Shyamala, G., O'Malley, B.W., Mice lacking progesterone receptor exhibit pleiotropic reproductive abnormalities (1995) Genes Dev, 9, pp. 2266-2278
  • Sicinski, P., Donaher, J.L., Parker, S.B., Li, T., Fazeli, A., Gardner, H., Haslam, S.Z., Weinberg, R.A., Cyclin D1 provides a link between development and oncogenesis in the retina and breast (1995) Cell, 82, pp. 621-630
  • Boonyaratanakornkit, V., Bi, Y., Rudd, M., Edwards, D.P., The role and mechanism of progesterone receptor activation of extra-nuclear signaling pathways in regulating gene transcription and cell cycle progression (2008) Steroids, 73, pp. 922-928
  • Faivre, E.J., Daniel, A.R., Hillard, C.J., Lange, C.A., Progesterone receptor rapid signaling mediates serine 345 phosphorylation and tethering to specificity protein 1 transcription factors (2008) Molecular Endocrinology, 22 (4), pp. 823-837. ,, DOI 10.1210/me.2007-0437
  • Hoffman, B., Liebermann, D.A., Apoptotic signaling by c-MYC (2008) Oncogene, 27, pp. 6462-6472
  • Dressing, G.E., Lange, C.A., Integrated actions of progesterone receptor and cell cycle machinery regulate breast cancer cell proliferation (2009) Steroids, 74, pp. 573-576
  • Faivre, E.J., Lange, C.A., Progesterone receptors upregulate Wnt-1 to induce epidermal growth factor receptor transactivation and c-Src-dependent sustained activation of Erk1/2 mitogen-activated protein kinase in breast cancer cells (2007) Molecular and Cellular Biology, 27 (2), pp. 466-480. , DOI 10.1128/MCB.01539-06
  • Klijn, J.G., Setyono-Han, B., Foekens, J.A., Progesterone antagonists and progesterone receptor modulators in the treatment of breast cancer (2000) Steroids, 65, pp. 825-830
  • Gaddy, V.T., Barrett, J.T., Delk, J.N., Kallab, A.M., Porter, A.G., Schoenlein, P.V., Mifepristone induces growth arrest, caspase activation, and apoptosis of estrogen receptor-expressing, antiestrogen-resistant breast cancer cells (2004) Clinical Cancer Research, 10 (15), pp. 5215-5225. , DOI 10.1158/1078-0432.CCR-03-0637
  • Moore, M.R., A rationale for inhibiting progesterone-related pathways to combat breast cancer (2004) Current Cancer Drug Targets, 4 (2), pp. 183-189. , DOI 10.2174/1568009043481515


---------- APA ----------
Bottino, M.C., Cerliani, J.P., Rojas, P., Giulianelli, S., Soldati, R., Mondillo, C., Gorostiaga, M.A.,..., Lanari, C. (2011) . Classical membrane progesterone receptors in murine mammary carcinomas: Agonistic effects of progestins and RU-486 mediating rapid non-genomic effects. Breast Cancer Research and Treatment, 126(3), 621-636.
---------- CHICAGO ----------
Bottino, M.C., Cerliani, J.P., 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 Research and Treatment 126, no. 3 (2011) : 621-636.
---------- MLA ----------
Bottino, M.C., Cerliani, J.P., 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 Research and Treatment, vol. 126, no. 3, 2011, pp. 621-636.
---------- VANCOUVER ----------
Bottino, M.C., Cerliani, J.P., 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(3):621-636.