Progesterone reverses the mesenchymal phenotypes of basal phenotype breast cancer cells via a membrane progesterone receptor mediated pathway

Breast Cancer Research

Volumn 12, Issue 3, 2010, Pages

  Zuo, Lian ^a   Li, Wei ^a   You, Shaojin ^a  

^a ATLANTA VA MEDICAL CENTER   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

4 (3 CHLOROANILINO) 6,7 DIMETHOXYQUINAZOLINE; CAVEOLIN 1; CELL NUCLEUS RECEPTOR; COMPLEMENTARY DNA; EPIDERMAL GROWTH FACTOR RECEPTOR; FIBRONECTIN; MIFEPRISTONE; OCCLUDIN; PHOSPHATIDYLINOSITOL 3 KINASE; PROGESTERONE; PROGESTERONE RECEPTOR; PROMEGESTONE; PROTEIN KINASE B; SMALL INTERFERING RNA; UVOMORULIN; WORTMANNIN; CADHERIN; CAV1 PROTEIN, HUMAN; EGFR PROTEIN, HUMAN; GESTAGEN; PROGESTERONE RECEPTOR A;

ARTICLE; BASAL CELL; BASAL PHENOTYPE BREAST CANCER; BIOLOGY; BREAST CANCER; CANCER CELL; CANCER CELL CULTURE; CELL MEMBRANE; CELL PROLIFERATION; CELL STRUCTURE; CONTROLLED STUDY; EPITHELIAL MESENCHYMAL TRANSITION; GENE; GENE EXPRESSION; GENE SILENCING; GENETIC TRANSFECTION; HUMAN; HUMAN CELL; IN VITRO STUDY; MESENCHYME CELL; PHENOTYPE; SIGNAL TRANSDUCTION; WESTERN BLOTTING; BASAL CELL CARCINOMA; BREAST TUMOR; CAVEOLA; CELL DEDIFFERENTIATION; CELL NUCLEUS; DRUG ANTAGONISM; ENZYME IMMUNOASSAY; EPITHELIUM CELL; FEMALE; GENE EXPRESSION REGULATION; GENETICS; MESODERM; METABOLISM; PAGET NIPPLE DISEASE; PATHOLOGY; TISSUE MICROARRAY; TUMOR CELL LINE;

1-PHOSPHATIDYLINOSITOL 3-KINASE; BLOTTING, WESTERN; BREAST NEOPLASMS; CADHERINS; CARCINOMA, DUCTAL, BREAST; CAVEOLAE; CAVEOLIN 1; CELL DEDIFFERENTIATION; CELL LINE, TUMOR; CELL MEMBRANE; CELL NUCLEUS; CELL PROLIFERATION; EPITHELIAL CELLS; FEMALE; GENE EXPRESSION REGULATION, NEOPLASTIC; HUMANS; IMMUNOENZYME TECHNIQUES; MESODERM; NEOPLASMS, BASAL CELL; PHENOTYPE; PROGESTERONE; PROGESTINS; RECEPTOR, EPIDERMAL GROWTH FACTOR; RECEPTORS, PROGESTERONE; RNA, SMALL INTERFERING; TISSUE ARRAY ANALYSIS;

EID: 78149483425     PISSN: 14655411     EISSN: 1465542X     Source Type: Journal    
DOI: 10.1186/bcr2588     Document Type: Article

References (52)

1. Boyer B, Tucker GC, Valles AM, Gavrilovic J, Thiery JP. Reversible transition towards a fibroblastic phenotype in a rat carcinoma cell line. Int J Cancer Suppl 1989, 4:69-75. 10.1002/ijc.2910440719, 2509387.
2. Thiery JP. Epithelial-mesenchymal transitions in tumour progression. Nat Rev Cancer 2002, 2:442-454. 10.1038/nrc822, 12189386.
3. Lee JM, Dedhar S, Kalluri R, Thompson EW. The epithelial-mesenchymal transition: new insights in signaling, development, and disease. J Cell Biol 2006, 172:973-981. 10.1083/jcb.200601018, 2063755, 16567498.
4. Cano A, Perez-Moreno MA, Rodrigo I, Locascio A, Blanco MJ, del Barrio MG, Portillo F, Nieto MA. The transcription factor snail controls epithelial-mesenchymal transitions by repressing E-cadherin expression. Nat Cell Biol 2000, 2:76-83. 10.1038/35000025, 10655586.
5. Batlle E, Sancho E, Franci C, Dominguez D, Monfar M, Baulida J, Garcia De Herreros A. The transcription factor snail is a repressor of E-cadherin gene expression in epithelial tumour cells. Nat Cell Biol 2000, 2:84-89. 10.1038/35000034, 10655587.
6. Thomas P. Characteristics of membrane progestin receptor alpha (mPRalpha) and progesterone membrane receptor component 1 (PGMRC1) and their roles in mediating rapid progestin actions. Front Neuroendocrinol 2008, 29:292-312. 10.1016/j.yfrne.2008.01.001, 2600886, 18343488.
7. Dressing GE, Thomas P. Identification of membrane progestin receptors in human breast cancer cell lines and biopsies and their potential involvement in breast cancer. Steroids 2007, 72:111-116. 10.1016/j.steroids.2006.10.006, 17157338.
8. Falkenstein E, Tillmann HC, Christ M, Feuring M, Wehling M. Multiple actions of steroid hormones--a focus on rapid, nongenomic effects. Pharmacol Rev 2000, 52:513-556.
9. Losel R, Wehling M. Nongenomic actions of steroid hormones. Nat Rev Mol Cell Biol 2003, 4:46-56. 10.1038/nrm1009, 12511868.
10. Losel R, Breiter S, Seyfert M, Wehling M, Falkenstein E. Classic and non-classic progesterone receptors are both expressed in human spermatozoa. Horm Metab Res 2005, 37:10-14. 10.1055/s-2005-861023, 15702432.
11. Sleiter N, Pang Y, Park C, Horton TH, Dong J, Thomas P, Levine JE. Progesterone receptor A (PRA) and PRB-independent effects of progesterone on gonadotropin-releasing hormone release. Endocrinology 2009, 150:3833-3844. 10.1210/en.2008-0774, 19423765.
12. Zhu Y, Rice CD, 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. Proc Natl Acad Sci USA 2003, 100:2231-2236. 10.1073/pnas.0336132100, 151323, 12574519.
13. Karteris E, Zervou S, Pang Y, Dong J, Hillhouse EW, Randeva HS, Thomas P. Progesterone signaling in human myometrium through two novel membrane G protein-coupled receptors: potential role in functional progesterone withdrawal at term. Mol Endocrinol 2006, 20:1519-1534. 10.1210/me.2005-0243, 16484338.
14. Ashley RL, Clay CM, Farmerie TA, Niswender GD, Nett TM. Cloning and characterization of an ovine intracellular seven transmembrane receptor for progesterone that mediates calcium mobilization. Endocrinology 2006, 147:4151-4159. 10.1210/en.2006-0002, 16794007.
15. Neve RM, Chin K, Fridlyand J, Yeh J, Baehner FL, Fevr T, Clark L, Bayani N, Coppe JP, Tong F, Speed T, Spellman PT, DeVries S, Lapuk A, Wang NJ, Kuo WL, Stilwell JL, Pinkel D, Albertson DG, Waldman FM, McCormick F, Dickson RB, Johnson MD, Lippman M, Ethier S, Gazdar A, Gray JW. A collection of breast cancer cell lines for the study of functionally distinct cancer subtypes. Cancer Cell 2006, 10:515-527. 10.1016/j.ccr.2006.10.008, 2730521, 17157791.
16. Jo M, Lester RD, Montel V, Eastman B, Takimoto S, Gonias SL. Reversibility of epithelial-mesenchymal transition (EMT) induced in breast cancer cells by activation of urokinase receptor-dependent cell signaling. J Biol Chem 2009, 284:22825-22833. 10.1074/jbc.M109.023960, 19546228.
17. Fernandez P, Burghardt R, Smith R, Nodland K, Safe S. High passage T47 D human breast cancer cells: altered endocrine and 2,3,7,8-tetrachlorodibenzo-p-dioxin responsiveness. Eur J Pharmacol 1994, 270:53-65.
18. Koli KM, Ramsey TT, Ko Y, Dugger TC, Brattain MG, Arteaga CL. Blockade of transforming growth factor-beta signaling does not abrogate antiestrogen-induced growth inhibition of human breast carcinoma cells. J Biol Chem 1997, 272:8296-8302. 10.1074/jbc.272.13.8296, 9079651.
19. Zuo L, Li L, Wang Q, Fleming TP, You S. Mammaglobin as a potential molecular target for breast cancer drug delivery. Cancer Cell Int 2009, 9:8. 10.1186/1475-2867-9-8, 2662795, 19309500.
20. 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 alpha subtypes and their evolutionary origins. Endocrinology 2007, 148:705-718. 10.1210/en.2006-0974, 17082257.
21. Brainard AM, Miller AJ, Martens JR, England SK. Maxi-K channels localize to caveolae in human myometrium: a role for an actin-channel-caveolin complex in the regulation of myometrial smooth muscle K+ current. Am J Physiol Cell Physiol 2005, 289:C49-57. 10.1152/ajpcell.00399.2004, 15703204.
22. You S, Zuo L, Varma V. Broad tissue expression of membrane progesterone receptor alpha in normal mice. J Mol Histol 2010,
23. Purmonen S, Manninen T, Pennanen P, Ylikomi T. Progestins regulate genes that can elicit both proliferative and antiproliferative effects in breast cancer cells. Oncol Rep 2008, 19:1627-1634.
24. Horwitz KB, Dye WW, Harrell JC, Kabos P, Sartorius CA. Rare steroid receptor-negative basal-like tumorigenic cells in luminal subtype human breast cancer xenografts. Proc Natl Acad Sci USA 2008, 105:5774-5779. 10.1073/pnas.0706216105, 2311360, 18391223.
25. Li J, Yen C, Liaw D, Podsypanina K, Bose S, Wang SI, Puc J, Miliaresis C, Rodgers L, McCombie R, Bigner SH, Giovanella BC, Ittmann M, Tycko B, Hibshoosh H, Wigler MH, Parsons R. PTEN, a putative protein tyrosine phosphatase gene mutated in human brain, breast, and prostate cancer. Science 1997, 275:1943-1947. 10.1126/science.275.5308.1943, 9072974.
26. Zhang B, Peng F, Wu D, Ingram AJ, Gao B, Krepinsky JC. Caveolin-1 phosphorylation is required for stretch-induced EGFR and Akt activation in mesangial cells. Cell Signal 2007, 19:1690-1700. 10.1016/j.cellsig.2007.03.005, 17446044.
27. Galbiati F, Volonte D, Brown AM, Weinstein DE, Ben-Ze'ev A, Pestell RG, Lisanti MP. Caveolin-1 expression inhibits Wnt/beta-catenin/Lef-1 signaling by recruiting beta-catenin to caveolae membrane domains. J Biol Chem 2000, 275:23368-23377. 10.1074/jbc.M002020200, 10816572.
28. Razani B, Zhang XL, Bitzer M, von Gersdorff G, Bottinger EP, Lisanti MP. Caveolin-1 regulates transforming growth factor (TGF)-beta/SMAD signaling through an interaction with the TGF-beta type I receptor. J Biol Chem 2001, 276:6727-6738. 10.1074/jbc.M008340200, 11102446.
29. Felley-Bosco E, Bender FC, Courjault-Gautier F, Bron C, Quest AF. Caveolin-1 down-regulates inducible nitric oxide synthase via the proteasome pathway in human colon carcinoma cells. Proc Natl Acad Sci U S A 2000, 97:14334-14339. 10.1073/pnas.250406797, 11114180, 18919.
30. Lange CA, Richer JK, Horwitz KB. Hypothesis: Progesterone primes breast cancer cells for cross-talk with proliferative or antiproliferative signals. Mol Endocrinol 1999, 13:829-836. 10.1210/me.13.6.829, 10379882.
31. Sumida T, Itahana Y, Hamakawa H, Desprez PY. Reduction of human metastatic breast cancer cell aggressiveness on introduction of either form a or B of the progesterone receptor and then treatment with progestins. Cancer Res 2004, 64:7886-7892. 10.1158/0008-5472.CAN-04-1155, 15520195.
32. Pelekanou V, Kampa M, Kafousi M, Dambaki K, Darivianaki K, Vrekoussis T, Sanidas E, Tsiftsis DD, Stathopoulos EN, Castanas E. Erythropoietin and its receptor in breast cancer: correlation with steroid receptors and outcome. Cancer Epidemiol Biomarkers Prev 2007, 16:2016-2023. 10.1158/1055-9965.EPI-06-1023, 17932349.
33. Kuroda N, Ohara M, Inoue K, Mizuno K, Fujishima N, Hamaguchi N, Lee GH. The majority of triple-negative breast cancer may correspond to basal-like carcinoma, but triple-negative breast cancer is not identical to basal-like carcinoma. Med Mol Morphol 2009, 42:128-131. 10.1007/s00795-008-0428-5, 19536621.
34. Rakha EA, Ellis IO. Triple-negative/basal-like breast cancer: review. Pathology 2009, 41:40-47. 10.1080/00313020802563510, 19089739.
35. Tubbs C, Thomas P. Progestin signaling through an olfactory G protein and membrane progestin receptor-alpha in Atlantic croaker sperm: potential role in induction of sperm hypermotility. Endocrinology 2009, 150:473-484. 10.1210/en.2008-0512, 18801904.
36. Depowski PL, Rosenthal SI, Ross JS. Loss of expression of the PTEN gene protein product is associated with poor outcome in breast cancer. Mod Pathol 2001, 14:672-676. 10.1038/modpathol.3880371, 11454999.
37. Pandolfi PP. Breast cancer--loss of PTEN predicts resistance to treatment. N Engl J Med 2004, 351:2337-2338. 10.1056/NEJMcibr043143, 15564551.
38. DeGraffenried LA, Fulcher L, Friedrichs WE, Grunwald V, Ray RB, Hidalgo M. Reduced PTEN expression in breast cancer cells confers susceptibility to inhibitors of the PI3 kinase/Akt pathway. Ann Oncol 2004, 15:1510-1516. 10.1093/annonc/mdh388, 15367412.
39. Pfeiler G, Horn F, Lattrich C, Klappenberger S, Ortmann O, Treeck O. Apoptotic effects of signal transduction inhibitors on human tumor cells with different PTEN expression. Oncol Rep 2007, 18:1305-1309.
40. Okamoto T, Schlegel A, Scherer PE, Lisanti MP. Caveolins, a family of scaffolding proteins for organizing "preassembled signaling complexes" at the plasma membrane. J Biol Chem 1998, 273:5419-5422. 10.1074/jbc.273.10.5419, 9488658.
41. Elsheikh SE, Green AR, Rakha EA, Samaka RM, Ammar AA, Powe D, Reis-Filho JS, Ellis IO. Caveolin 1 and Caveolin 2 are associated with breast cancer basal-like and triple-negative immunophenotype. Br J Cancer 2008, 99:327-334. 10.1038/sj.bjc.6604463, 2480981, 18612310.
42. Pinilla SM, Honrado E, Hardisson D, Benitez J, Palacios J. Caveolin-1 expression is associated with a basal-like phenotype in sporadic and hereditary breast cancer. Breast Cancer Res Treat 2006, 99:85-90. 10.1007/s10549-006-9184-1, 16541313.
43. Lu Z, Ghosh S, Wang Z, Hunter T. Downregulation of caveolin-1 function by EGF leads to the loss of E-cadherin, increased transcriptional activity of beta-catenin, and enhanced tumor cell invasion. Cancer Cell 2003, 4:499-515. 10.1016/S1535-6108(03)00304-0, 14706341.
44. Schlessinger J. Cell signaling by receptor tyrosine kinases. Cell 2000, 103:211-225. 10.1016/S0092-8674(00)00114-8, 11057895.
45. Bjorge JD, Chan TO, Antczak M, Kung HJ, Fujita DJ. Activated type I phosphatidylinositol kinase is associated with the epidermal growth factor (EGF) receptor following EGF stimulation. Proc Natl Acad Sci USA 1990, 87:3816-3820. 10.1073/pnas.87.10.3816, 53994, 2160078.
46. Rodrigues GA, Falasca M, Zhang Z, Ong SH, Schlessinger J. A novel positive feedback loop mediated by the docking protein Gab1 and phosphatidylinositol 3-kinase in epidermal growth factor receptor signaling. Mol Cell Biol 2000, 20:1448-1459. 10.1128/MCB.20.4.1448-1459.2000, 85307, 10648629.
47. Gu H, Maeda H, Moon JJ, Lord JD, Yoakim M, Nelson BH, Neel BG. New role for Shc in activation of the phosphatidylinositol 3-kinase/Akt pathway. Mol Cell Biol 2000, 20:7109-7120. 10.1128/MCB.20.19.7109-7120.2000, 86258, 10982827.
48. Wang HQ, Altomare DA, Skele KL, Poulikakos PI, Kuhajda FP, Di Cristofano A, Testa JR. Positive feedback regulation between AKT activation and fatty acid synthase expression in ovarian carcinoma cells. Oncogene 2005, 24:3574-3582. 10.1038/sj.onc.1208463, 15806173.
49. Wang H, Quah SY, Dong JM, Manser E, Tang JP, Zeng Q. PRL-3 down-regulates PTEN expression and signals through PI3K to promote epithelial-mesenchymal transition. Cancer Res 2007, 67:2922-2926. 10.1158/0008-5472.CAN-06-3598, 17409395.
50. Micalizzi DS, Ford HL. Epithelial-mesenchymal transition in development and cancer. Future Oncol 2009, 5:1129-1143. 10.2217/fon.09.94, 19852726.
51. Faivre EJ, Lange CA. 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 2007, 27:466-480. 10.1128/MCB.01539-06, 1800800, 17074804.
52. Lester RD, Jo M, Montel V, Takimoto S, Gonias SL. uPAR induces epithelial-mesenchymal transition in hypoxic breast cancer cells. J Cell Biol 2007, 178:425-436. 10.1083/jcb.200701092, 2064849, 17664334.