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

Volumn 126, Issue 3, 2011, Pages 621-636

  Bottino, María Cecilia ^a   Cerliani, Juan Pablo ^a   Rojas, Paola ^a   Giulianelli, Sebastián ^a   Soldati, Rocío ^a   Mondillo, Carolina ^a   Gorostiaga, María Alicia ^a   Pignataro, Omar P ^b   Calvo, Juan Carlos ^b   Gutkind, J Silvio ^c   Amornphimoltham, Panomwat ^c   Molinolo, Alfredo A ^c   Lüthy, Isabel A ^a   Lanari, Claudia ^a  

^a Facultad de Ciencias Naturales e Instituto M Lillo   (Argentina)

^b UNIVERSIDAD DE BUENOS AIRES   (Argentina)

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

Author keywords

Antiprogestins; Breast cancer treatment; Mammary carcinomas; Membrane progesterone receptors; Non genomic effects; Progesterone receptor isoforms: Membrane initiated steroid signaling; Progestins

Indexed keywords

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;

EID: 79958706576     PISSN: 01676806     EISSN: 15737217     Source Type: Journal    
DOI: 10.1007/s10549-010-0971-3     Document Type: Article

References (79)

1. Mangelsdorf DJ, Thummel C, Beato M, Herrlich P, Schutz G, Umesono K, Blumberg B, Kastner P, Mark M, Chambon P (1995) The nuclear receptor superfamily: the second decade. Cell 83:835-839
2. Torchia J, Glass C, Rosenfeld MG (1998) Co-activators and corepressors in the integration of transcriptional responses. Curr Opin Cell Biol 10:373-383 (Pubitemid 28287049)
3. Bagchi MK, Tsai SY, Weigel NL, Tsai MJ, O'Malley BW (1990) Regulation of in vitro transcription by progesterone receptor. Characterization and kinetic studies. J Biol Chem 265:5129-5134
4. Sutter-Dub MT (2002) Rapid non-genomic and genomic responses to progestogens, estrogens, and glucocorticoids in the endocrine pancreatic B cell, the adipocyte and other cell types. Steroids 67:77-93
5. Pietras RJ, Szego CM (1977) Specific binding sites for oestrogen at the outer surfaces of isolated endometrial cells. Nature 265:69-72 (Pubitemid 8004314)
6. Cato AC, Nestl A, Mink S (2002) Rapid actions of steroid receptors in cellular signaling pathways. Sci STKE 138:RE9
7. Watson CS, Gametchu B (1999) Membrane-initiated steroid actions and the proteins that mediate them. Proc Soc Exp Biol Med 220:9-19
8. Song RX, Fan P, Yue W, Chen Y, Santen RJ (2006) Role of receptor complexes in the extranuclear actions of estrogen receptor alpha in breast cancer. Endocr Relat Cancer 13(Suppl 1):S3-S13 (Pubitemid 46219244)
9. Ehring GR, Kerschbaum HH, Eder C, Neben AL, Fanger CM, Khoury RM, Negulescu PA, Cahalan MD (1998) A nongenomic mechanism for progesterone-mediated immunosuppression: inhibition of K+ channels, Ca2+ signaling, and gene expression in T lymphocytes. J Exp Med 188:1593-1602 (Pubitemid 28516104)
10. Grazzini E, Guillon G, Mouillac B, Zingg HH (1998) Inhibition of oxytocin receptor function by direct binding of progesterone. Nature 392:509-512 (Pubitemid 28169871)
11. Valera S, Ballivet M, Bertrand D (1992) Progesterone modulates a neuronal nicotinic acetylcholine receptor. Proc Natl Acad Sci USA 89:9949-9953
12. McEwen BS (1991) Non-genomic and genomic effects of steroids on neural activity. Trends Pharmacol Sci 12:141-147
13. Krebs CJ, Jarvis ED, Chan J, Lydon JP, Ogawa S, Pfaff DW (2000) A membrane-associated progesterone-binding protein, 25-Dx, is regulated by progesterone in brain regions involved in female reproductive behaviors. Proc Natl Acad Sci USA 97:12816-12821
14. Labombarda F, Gonzalez SL, Deniselle MC, Vinson GP, Schumacher M, De Nicola AF, Guennoun R (2003) Effects of injury and progesterone treatment on progesterone receptor and progesterone binding protein 25-Dx expression in the rat spinal cord. J Neurochem 87:902-913 (Pubitemid 37444566)
15. Zhu Y, Bond J, Thomas P (2003) Identification, classification, and partial characterization of genes in humans and other vertebrates homologous to a fish membrane progestin receptor. Proc Natl Acad Sci USA 100:2237-2242 (Pubitemid 36297483)
16. Zhu Y, Rice CD, Pang Y, Pace M, Thomas P (2003) Cloning, expression, and characterization of a membrane progestin receptor and evidence it is an intermediary in meiotic maturation of fish oocytes. Proc Natl Acad Sci USA 100:2231-2236 (Pubitemid 36297482)
17. Dressing GE, Thomas P (2007) Identification of membrane progestin receptors in human breast cancer cell lines and biopsies and their potential involvement in breast cancer. Steroids 72:111-116 (Pubitemid 46273489)
18. Krietsch T, Fernandes MS, Kero J, Losel R, Heyens M, Lam EW, Huhtaniemi I, Brosens JJ, Gellersen B (2006) Human homologs of the putative G protein-coupled membrane progestin receptors (mPRalpha, beta, and gamma) localize to the endoplasmic reticulum and are not activated by progesterone. Mol Endocrinol 20:3146-3164 (Pubitemid 44833562)
19. Thomas P, Pang Y, Dong J, Groenen P, Kelder J, de Vlieg J, Zhu Y, Tubbs C (2007) Steroid and G protein binding characteristics of the seatrout and human progestin membrane receptor alpha subtypes and their evolutionary origins. Endocrinology 148:705-718 (Pubitemid 46143172)
20. Molinolo AA, Lanari C, Charreau EH, Sanjuan N, Pasqualini CD (1987) Mouse mammary tumors induced by medroxyprogester-one acetate: immunohistochemistry and hormonal receptors. J Natl Cancer Inst 79:1341-1350 (Pubitemid 18036740)
21. Helguero LA, Lamb C, Molinolo AA, Lanari C (2003) Evidence for two progesterone receptor binding sites in murine mammary carcinomas. J Steroid Biochem Mol Biol 84:9-14 (Pubitemid 36329170)
22. Powell CE, Soto AM, Sonnenschein C (2001) Identification and characterization of membrane estrogen receptor from MCF7 estrogen-target cells. J Steroid Biochem Mol Biol 77:97-108 (Pubitemid 32476817)
23. Razandi M, Pedram A, Greene GL, Levin ER (1999) Cell membrane and nuclear estrogen receptors (ERs) originate from a single transcript: studies of ERalpha and ERbeta expressed in Chinese hamster ovary cells. Mol Endocrinol 13:307-319 (Pubitemid 29068005)
24. Razandi M, Oh P, Pedram A, Schnitzer J, Levin ER (2002) ERs associate with and regulate the production of caveolin: implications for signaling and cellular actions. Mol Endocrinol 16:100-115 (Pubitemid 34044501)
25. Welter BH, Hansen EL, Saner KJ, Wei Y, Price TM (2003) Membrane-bound progesterone receptor expression in human aortic endothelial cells. J Histochem Cytochem 51:1049-1055 (Pubitemid 36919982)
26. Younglai EV, Wu Y, Foster WG, Lobb DK, Price TM (2006) Binding of progesterone to cell surfaces of human granulosalutein cells. J Steroid Biochem Mol Biol 101:61-67 (Pubitemid 44301880)
27. Luconi M, Francavilla F, Porazzi I, Macerola B, Forti G, Baldi E (2004) Human spermatozoa as a model for studying membrane receptors mediating rapid nongenomic effects of progesterone and estrogens. Steroids 69:553-559 (Pubitemid 39013487)
28. Pedram A, Razandi M, Sainson RC, Kim JK, Hughes CC, Levin ER (2007) A conserved mechanism for steroid receptor translocation to the plasma membrane. J Biol Chem 282:22278-22288 (Pubitemid 47267344)
29. Lanari C, Luthy I, Lamb CA, Fabris V, Pagano E, Helguero LA, Sanjuan N, Merani S, Molinolo AA (2001) Five novel hormone-responsive cell lines derived from murine mammary ductal carcinomas: in vivo and in vitro effects of estrogens and progestins. Cancer Res 61:293-302 (Pubitemid 32095730)
30. Dran G, Luthy IA, Molinolo AA, Charreau EH, Pasqualini CD, Lanari C (1995) Effect of medroxyprogesterone acetate (MPA) and serum factors on cell proliferation in primary cultures of an MPA-induced mammary adenocarcinoma. Breast Cancer Res Treat 35:173-186
31. Fabris VT, Benavides F, Conti C, Merani S, Lanari C (2005) Cytogenetic findings, Trp53 mutations, and hormone responsiveness in a medroxyprogesterone acetate induced murine breast cancer model. Cancer Genet Cytogenet 161:130-139 (Pubitemid 41133479)
32. Urtreger A, Ladeda V, Puricelli LI, Rivelli A, Vidal MC, Sacerdote de Lustig E, Bal de Kier Joffe E (1997) Modulation of fibronectin expression and proteolytic activity associated to the invasive and metastatic phenotype in two new murine mammary tumor cell lines. Int J Oncol 11:489-496 (Pubitemid 27364280)
33. Clemm DL, Sherman L, Boonyaratanakornkit V, Schrader WT, Weigel NL, Edwards DP (2000) Differential hormone-dependent phosphorylation of progesterone receptor A and B forms revealed by a phosphoserine site-specific monoclonal antibody. Mol Endocrinol 14:52-65 (Pubitemid 32260327)
34. Lowry OH, Rosebrough NJ, Farr AL (1951) Protein measurements with the Folin phenol reagent. J Biol Chem 193:265-275
35. Kampa M, Nifli AP, Charalampopoulos I, Alexaki VI, Theodoropoulos PA, Stathopoulos EN, Gravanis A, Castanas E (2005) Opposing effects of estradiol- and testosterone-membrane binding sites on T47D breast cancer cell apoptosis. Exp Cell Res 307:41-51 (Pubitemid 40732732)
36. Lamb CA, Helguero LA, Giulianelli S, Soldati R, Vanzulli SI, Molinolo A, Lanari C (2005) Antisense oligonucleotides targeting the progesterone receptor inhibit hormone-independent breast cancer growth in mice. Breast Cancer Res 7:R1111-R1121
37. Lamb C, Simian M, Molinolo A, Pazos P, Lanari C (1999) Regulation of cell growth of a progestin-dependent murine mammary carcinoma in vitro: progesterone receptor involvement in serum or growth factor-induced cell proliferation. J Steroid Biochem Mol Biol 70:133-142 (Pubitemid 29528423)
38. Giulianelli S, Cerliani JP, Lamb CA, Fabris VT, Bottino MC, Gorostiaga MA, Novaro V, Gongora A, Baldi A, Molinolo A, Lanari C (2008) 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 123:2518-2531
39. Vanzulli SI, Soldati R, Meiss R, Colombo L, Molinolo AA, Lanari C (2005) Estrogen or antiprogestin treatment induces complete regression of pulmonary and axillary metastases in an experimental model of breast cancer progression. Carcinogenesis 26:1055-1063 (Pubitemid 41214298)
40. Lanari C, Lamb CA, Fabris VT, Helguero LA, Soldati R, Bottino MC, Giulianelli S, Cerliani JP, Wargon V, Molinolo A (2009) The MPA mouse breast cancer model: evidence for a role of progesterone receptors in breast cancer. Endocr Relat Cancer 16:333-350
41. Helguero LA, Viegas M, Asaithamby A, Shyamala G, Lanari C, Molinolo AA (2003) Progesterone receptor expression in medroxyprogesterone acetate-induced murine mammary carcinomas and response to endocrine treatment. Breast Cancer Res Treat 79:379-390 (Pubitemid 36750945)
42. Wargon V, Helguero LA, Bolado J, Rojas P, Novaro V, Molinolo A, Lanari C (2009) Reversal of antiprogestin resistance and progesterone receptor isoform ratio in acquired resistant mammary carcinomas. Breast Cancer Res Treat 116:449-460
43. Zhang Z, Maier B, Santen RJ, Song RX (2002) Membrane association of estrogen receptor alpha mediates estrogen effect on MAPK activation. Biochem Biophys Res Commun 294:926-933 (Pubitemid 34687138)
44. Kousteni S, Bellido T, Plotkin LI, O'Brien CA, Bodenner DL, Han L, Han K, DiGregorio GB, Katzenellenbogen JA, Katzenellenbogen BS, Roberson PK, Weinstein RS, Jilka RL, Manolagas SC (2001) Nongenotropic, sex-nonspecific signaling through the estrogen or androgen receptors: dissociation from transcriptional activity. Cell 104:719-730 (Pubitemid 32241022)
45. Qiu M, Olsen A, Faivre E, Horwitz KB, Lange CA (2003) Mitogen activated protein kinase regulates nuclear association of human progesterone receptors. Mol Endocrinol 17:628-642 (Pubitemid 36403575)
46. Balana ME, Lupu R, Labriola L, Charreau EH, Elizalde PV (1999) Interactions between progestins and heregulin (HRG) signaling pathways: HRG acts as mediator of progestins proliferative effects in mouse mammary adenocarcinomas. Oncogene 18:6370-6379
47. Carbajal L, Deng J, Dressing GE, Hagan CR, Lange CA, Hammes SR (2009) Meeting review: extra-nuclear steroid receptors-integration with multiple signaling pathways. Steroids 74:551-554
48. Quiles I, Millan-Arino L, Subtil-Rodriguez A, Minana B, Spinedi N, Ballare C, Beato M, Jordan A (2009) Mutational analysis of progesterone receptor functional domains in stable cell lines delineates sets of genes regulated by different mechanisms. Mol Endocrinol 23:809-826
49. Marino M, Ascenzi P, Acconcia F (2006) S-Palmitoylation modulates estrogen receptor alpha localization and functions. Steroids 71:298-303
50. Salatino M, Beguelin W, Peters MG, Carnevale R, Proietti CJ, Galigniana MD, Vedoy CG, Schillaci R, Charreau EH, Sogayar MC, Elizalde PV (2006) Progestin-induced caveolin-1 expression mediates breast cancer cell proliferation. Oncogene 25:7723-7739 (Pubitemid 44967967)
51. Karteris E, Zervou S, Pang Y, Dong J, Hillhouse EW, Randeva HS, Thomas P (2006) Progesterone signaling in human myometrium through two novel membrane G protein-coupled receptors: potential role in functional progesterone withdrawal at term. Mol Endocrinol 20:1519-1534 (Pubitemid 43967561)
52. Bullock LP, Barthe PL, Mowszowicz I, Orth DN, Bardin CW (1975) The effect of progestins on submaxillary gland epidermal growth factor: demonstration of androgenic, synandrogenic and antiandrogenic actions. Endocrinology 97:189-195
53. Kontula K, Paavonen T, Luukkainen T, Andersson LC (1983) Binding of progestins to the glucocorticoid receptor. Correlation to their glucocorticoid-like effects on in vitro functions of human mononuclear leukocytes. Biochem Pharmacol 32:1511-1518 (Pubitemid 13096010)
54. Montecchia MF, Lamb C, Molinolo AA, Luthy IA, Pazos P, Charreau E, Vanzulli S, Lanari C (1999) Progesterone receptor involvement in independent tumor growth in MPA-induced murine mammary adenocarcinomas. J Steroid Biochem Mol Biol 68:11-21 (Pubitemid 29130381)
55. Horwitz KB, Tung L, Takimoto GS (1996) Novel mechanisms of antiprogestin action. Acta Oncol 35:129-140 (Pubitemid 26155137)
56. Horwitz KB (1992) The molecular biology of RU486. Is there a role for antiprogestins in the treatment of breast cancer? Endocr Rev 13:146-163
57. Labriola L, Salatino M, Proietti CJ, Pecci A, Coso OA, Kornblihtt AR, Charreau EH, Elizalde PV (2003) 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. Mol Cell Biol 23:1095-1111 (Pubitemid 36133525)
58. Carnevale RP, Proietti CJ, Salatino M, Urtreger A, Peluffo G, Edwards DP, Boonyaratanakornkit V, Charreau EH, Bal de Kier JE, Schillaci R, Elizalde PV (2007) 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. Mol Endocrinol 21:1335-1358 (Pubitemid 46984741)
59. Skildum A, Faivre E, Lange CA (2005) Progesterone receptors induce cell cycle progression via activation of mitogen-activated protein kinases. Mol Endocrinol 19:327-339 (Pubitemid 40223458)
60. Arruvito L, Giulianelli S, Flores AC, Paladino N, Barboza M, Lanari C, Fainboim L (2008) NK cells expressing a progesterone receptor are susceptible to progesterone-induced apoptosis. J Immunol 180:5746-5753
61. Park JI, Strock CJ, Ball DW, Nelkin BD (2003) The Ras/Raf/MEK/ extracellular signal-regulated kinase pathway induces autocrine-paracrine growth inhibition via the leukemia inhibitory factor/JAK/STAT pathway. Mol Cell Biol 23:543-554 (Pubitemid 36050548)
62. Marshall CJ (1995) Specificity of receptor tyrosine kinase signaling: transient versus sustained extracellular signal-regulated kinase activation. Cell 80:179-185
63. Murphy LO, Blenis J (2006) MAPK signal specificity: the right place at the right time. Trends Biochem Sci 31:268-275 (Pubitemid 43674354)
64. Leonhardt SA, Boonyaratanakornkit V, Edwards DP (2003) Progesterone receptor transcription and non-transcription signaling mechanisms. Steroids 68:761-770 (Pubitemid 37532398)
65. Rowan BG, O'Malley BW (2000) Progesterone receptor coactivators. Steroids 65:545-549
66. Dressing GE, Hagan CR, Knutson TP, Daniel AR, Lange CA (2009) Progesterone receptors act as sensors for mitogenic protein kinases in breast cancer models. Endocr Relat Cancer 16:351-361
67. Kato S, Pinto M, Carvajal A, Espinoza N, Monso C, Sadarangani A, Villalon M, Brosens JJ, White JO, Richer JK, Horwitz KB, Owen GI (2005) Progesterone increases tissue factor gene expression, procoagulant activity, and invasion in the breast cancer cell line ZR-75-1. J Clin Endocrinol Metab 90:1181-1188 (Pubitemid 40279252)
68. Owen GI, Richer JK, Tung L, Takimoto G, Horwitz KB (1998) Progesterone regulates transcription of the p21(WAF1) cyclindependent kinase inhibitor gene through Sp1 and CBP/p300. J Biol Chem 273:10696-10701 (Pubitemid 28227684)
69. Cicatiello L, Addeo R, Sasso A, Altucci L, Petrizzi VB, Borgo R, Cancemi M, Caporali S, Caristi S, Scafoglio C, Teti D, Bresciani F, Perillo B, Weisz A (2004) 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 24:7260-7274 (Pubitemid 39014451)
70. Lydon JP, DeMayo FJ, Funk CR, Mani SK, Hughes AR, Montgomery CA Jr, Shyamala G, Conneely OM, O'Malley BW (1995) Mice lacking progesterone receptor exhibit pleiotropic reproductive abnormalities. Genes Dev 9:2266-2278
71. Sicinski P, Donaher JL, Parker SB, Li T, Fazeli A, Gardner H, Haslam SZ, Bronson RT, Elledge SJ, Weinberg RA (1995) Cyclin D1 provides a link between development and oncogenesis in the retina and breast. Cell 82:621-630
72. Boonyaratanakornkit V, Bi Y, Rudd M, Edwards DP (2008) The role and mechanism of progesterone receptor activation of extra-nuclear signaling pathways in regulating gene transcription and cell cycle progression. Steroids 73:922-928
73. Faivre EJ, Daniel AR, Hillard CJ, Lange CA (2008) Progesterone receptor rapid signaling mediates serine 345 phosphorylation and tethering to specificity protein 1 transcription factors. Mol Endocrinol 22:823-837 (Pubitemid 351482820)
74. Hoffman B, Liebermann DA (2008) Apoptotic signaling by c-MYC. Oncogene 27:6462-6472
75. Dressing GE, Lange CA (2009) Integrated actions of progesterone receptor and cell cycle machinery regulate breast cancer cell proliferation. Steroids 74:573-576
76. Faivre EJ, Lange CA (2007) 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. Mol Cell Biol 27:466-480 (Pubitemid 46080117)
77. Klijn JG, Setyono-Han B, Foekens JA (2000) Progesterone antagonists and progesterone receptor modulators in the treatment of breast cancer. Steroids 65:825-830
78. Gaddy VT, Barrett JT, Delk JN, Kallab AM, Porter AG, Schoenlein PV (2004) Mifepristone induces growth arrest, caspase activation, and apoptosis of estrogen receptor-expressing, antiestrogen-resistant breast cancer cells. Clin Cancer Res 10:5215-5225 (Pubitemid 39099796)
79. Moore MR (2004) A rationale for inhibiting progesterone-related pathways to combat breast cancer. Curr Cancer Drug Targets 4:183-189 (Pubitemid 38332555)