The antiproliferative effects of progestins in T47D breast cancer cells are tempered by progestin induction of the ETS transcription factor Elf5

Molecular Endocrinology

Volumn 24, Issue 7, 2010, Pages 1380-1392

  Hilton, H N ^a   Kalyuga, M ^a   Cowley, M J ^a   Alles, M C ^a   Lee, H J ^a   Caldon, C E ^a   Blazek, K ^a   Kaplan, W ^a,b   Musgrove, E A ^a,b   Daly, R J ^a,b   Naylor, M J ^a,b   Graham, J D ^c   Clarke, C L ^c   Ormandy, C J ^a,b  

^a GARVAN INSTITUTE OF MEDICAL RESEARCH   (Australia)

^b UNIVERSITY OF NEW SOUTH WALES   (Australia)

^c UNIVERSITY OF SYDNEY   (Australia)

Author keywords

[No Author keywords available]

Indexed keywords

BETA ACTIN; INITIATION FACTOR 5; PROGESTERONE DERIVATIVE; PROLACTIN; SHORT HAIRPIN RNA; ELF5 PROTEIN, HUMAN; GESTAGEN; MIFEPRISTONE; TRANSCRIPTION FACTOR ETS;

ANIMAL CELL; ANIMAL EXPERIMENT; ARTICLE; BREAST CANCER; CELL CYCLE ARREST; CELL LINEAGE; CELL PROLIFERATION; CONTROLLED STUDY; GENE EXPRESSION; MOUSE; NONHUMAN; PHENOTYPE; PRIORITY JOURNAL; PROTEIN INDUCTION; REGULATORY MECHANISM; BREAST NEOPLASMS; DNA MICROARRAY; DRUG EFFECTS; FEMALE; HUMAN; METABOLISM; RNA INTERFERENCE; TUMOR CELL LINE;

BREAST NEOPLASMS; CELL LINE, TUMOR; CELL PROLIFERATION; FEMALE; HUMANS; MIFEPRISTONE; OLIGONUCLEOTIDE ARRAY SEQUENCE ANALYSIS; PROGESTINS; PROTO-ONCOGENE PROTEINS C-ETS; RNA INTERFERENCE;

EID: 77954822170     PISSN: 08888809     EISSN: None     Source Type: Journal    
DOI: 10.1210/me.2009-0516     Document Type: Article

References (54)

1. Binart N, Helloco C, Ormandy CJ, Barra J, Clément-Lacroix P, Baran N, Kelly PA 2000 Rescue of preimplantatory egg development and embryo implantation in prolactin receptor-deficient mice after progesterone administration. Endocrinology 141:2691-2697 (Pubitemid 32269091)
2. Brosens JJ, Hayashi N, White JO 1999 Progesterone receptor regulates decidual prolactin expression in differentiating human endometrial stromal cells. Endocrinology 140:4809-4820
3. Lucas BK, Ormandy CJ, Binart N, Bridges RS, Kelly PA 1998 Null mutation of the prolactin receptor gene produces a defect in maternal behavior. Endocrinology 139:4102-4107 (Pubitemid 28513694)
4. Oakes SR, Hilton HN, Ormandy CJ 2006 Key stages in mammary gland development - The alveolar switch: coordinating the proliferative cues and cell fate decisiosn that drive the formation of lobuloalveoli from ductal epithelium. Breast Cancer Research 8:207
5. Soyal S, Ismail PM, Li J, Mulac-Jericevic B, Conneely OM, Lydon JP 2002 Progesterone's role in mammary gland development and tumorigenesis as disclosed by experimental mouse genetics. Breast Cancer Res 4:191-196
6. Lydon JP, DeMayo FJ, Funk CR, Mani SK, Hughes AR, Montgomery CAJ, Shyamala G, Conneely OM, O'Malley BW 1995 Mice lacking progesterone receptor exhibit pleiotropic reproductive abnormalities. Genes Dev 9:2266-2278
7. Ormandy CJ, Camus A, Barra J, Damotte D, Lucas B, Buteau H, Edery M, Brousse N, Babinet C, Binart N, Kelly PA 1997 Null mutation of the prolactin receptor gene produces multiple reproductive defects in the mouse. Genes Dev 11:167-178
8. Neville MC, McFadden TB, Forsyth I 2002 Hormonal regulation of mammary differentiation and milk secretion. J Mammary Gland Biol Neoplasia 7:49-66
9. Boonyaratanakornkit V, McGowan E, Sherman L, Mancini MA, Cheskis BJ, Edwards DP 2007 The role of extranuclear signaling actions of progesterone receptor in mediating progesterone regulation of gene expression and the cell cycle. Mol Endocrinol 21:359-375
10. Kabotyanski EB, Rijnkels M, Freeman-Zadrowski C, Buser AC, Edwards DP, Rosen JM 2009 Lactogenic hormonal induction of long distance interactions between β-casein gene regulatory elements. J Biol Chem 284:22815-22824
11. Clevenger CV, Furth PA, Hankinson SE, Schuler LA 2003 The role of prolactin in mammary carcinoma. Endocr Rev 24:1-27
12. Lange CA 2008 Integration of progesterone receptor action with rapid signaling events in breast cancer models. J Steroid Biochem Mol Biol 108:203-212
13. Blais A, Dynlacht BD 2005 Constructing transcriptional regulatory networks. Genes Dev 19:1499-1511
14. Ormandy CJ, Hall RE, Manning DL, Robertson JF, Blamey RW, Kelly PA, Nicholson RI, Sutherland RL 1997 Coexpression and cross-regulation of the prolactin receptor and sex steroid hormone receptors in breast cancer. J Clin Endocrinol Metab 82: 3692-3699
15. Macleod K, Leprince D, Stehelin D 1992 The ets gene family. Trends Biochem Sci 17:251-256
16. Seth A, Ascione R, Fisher RJ, Mavrothalassitis GJ, Bhat NK, Papas TS 1992 The ets gene family. Cell Growth Differ 3:327-334
17. Wasylyk B, Hahn SL, Giovane A 1993 The Ets family of transcription factors. Eur J Biochem 211:7-18
18. Graves BJ, Petersen JM 1998 Specificity within the Ets family of transcription factors. Adv Cancer Res 75:1-55 (Pubitemid 28429032)
19. Harris J, Stanford PM, Sutherland K, Oakes SR, Naylor MJ, Robertson FG, Blazek KD, Kazlauskas M, Hilton HN, Wittlin S, Alexander WS, Lindeman GJ, Visvader JE, Ormandy CJ 2006 Socs2 and Elf5 mediate prolactin-induced mammary gland development. Mol Endocrinol 20: 1177-1187
20. Thomas RS, Ng AN, Zhou J, Tymms MJ, Doppler W, Kola I 2000 The Elf group of Ets-related transcription factors. ELF3 and ELF5. Adv Exp Med Biol 480:123-128
21. Zhou J, Chehab R, Tkalcevic J, Naylor MJ, Harris J, Wilson TJ, Tsao S, Tellis I, Zavarsek S, Xu D, Lapinskas EJ, Visvader J, Lindeman GJ, Thomas R, Ormandy CJ, Hertzhog PJ, Kola I, Pritchard MA 2005 Elf5 is essential for early embryogenesis and mammary gland development during prengnancy and lactation. EMBO J 24:635-644
22. Oakes SR, Naylor MJ, Asselin-Labat M-L, Blazek KD, Gardiner-Garden M, Hilton HN, Kazlauskas M, Pritchard MA, Chodosh LA, Pfeffer PL, Lindeman GJ, Visvader JE, Ormandy CJ 2008 The Ets transcription factor Elf5 specifies mammary alveolar cell fate. Genes Dev 22:581-586
23. Choi YS, Chakrabarti R, Escamilla-Hernandez R, Sinha S 2009 Elf5 conditional knockout mice reveal its role as a master regulator in mammary alveolar development: failure of Stat5 activation and functional differentiation in the absence of Elf5. Dev Biol 329:227-241
24. Brisken C, Kaur S, Chavarria TE, Binart N, Sutherland RL, Weinberg RA, Kelly PA, Ormandy CJ 1999 Prolactin controls mammary gland development via direct and indirect mechanisms. Dev Biol 210:96-106
25. Lim E, Vaillant F, Wu D, Forrest NC, Pal B, Hart AH, Asselin-Labat ML, Gyorki DE, Ward T, Partanen A, Feleppa F, Huschtscha LI, Thorne HJ, Fox SB, Yan M, French JD, Brown MA, Smyth GK, Visvader JE, Lindeman GJ 2009 Aberrant luminal progenitors as the candidate target population for basal tumor development in BRCA1 mutation carriers. Nat Med 15:907-913
26. Fernandez-Valdivia R, Mukherjee A, Creighton CJ, Buser AC, DeMayo FJ, Edwards DP, Lydon JP 2008 Transcriptional response of the murine mammary gland to acute progesterone exposure. Endocrinology 149:6236-6250
27. Caldon CE, Lee CS, Sutherland RL, Musgrove EA 2008 Wilms' tumor protein 1: an early target of progestin regulation in T-47D breast cancer cells that modulates proliferation and differentiation. Oncogene 27:126-138
28. Chambon M, Rochefort H, Vial HJ, Chalbos D 1989 Progestins and androgens stimulate lipid accumulation in T47D breast cancer cells via their own receptors. J Steroid Biochem 33:915-922
29. Kester HA, van der Leede BM, van der Saag PT, van der Burg B 1997 Novel progesterone target genes identified by an improved differential display technique suggest that progestin-induced growth inhibition of breast cancer cells coincides with enhancement of differentiation. J Biol Chem 272:16637-16643
30. Musgrove EA, Lee CS, Sutherland RL 1991 Progestins both stimulate and inhibit breast cancer cell cycle progression while increasing expression of transforming growth factor α, epidermal growth factor receptor, c-fos and c-myc genes. Mol Cell Biol 11:5032-5043
31. Sutherland RL, Hall RE, Pang GY, Musgrove EA, Clarke CL 1988 Effect of medroxyprogesterone acetate on proliferation and cell cycle kinetics of human mammary carcinoma cells. Cancer Res 48:5084-5091
32. Gray D, Hoeflich K, Peng L, Gu Z, Gogineni A, Murray L, Eby M, Kljavin N, Seshagiri S, Cole M, Davis D 2007 pHUSH: a single vector system for conditional gene expression. BMC Biotechnol 7:61
33. Ashburner M, Ball CA, Blake JA, Botstein D, Butler H, Cherry JM, Davis AP, Dolinski K, Dwight SS, Eppig JT, Harris MA, Hill DP, Issel-Tarver L, Kasarskis A, Lewis S, Matese JC, Richardson JE, Ringwald M, Rubin GM, Sherlock G 2000 Gene ontology: tool for the unification of biology. The Gene Ontology Consortium. Nat Genet 25:25-29
34. Kanehisa M, Goto S, Hattori M, Aoki-Kinoshita KF, Itoh M, Kawashima S, Katayama T, Araki M, Hirakawa M 2006 From genomics to chemical genomics: new developments in KEGG. Nucleic Acids Res 34:D354-357
35. Subramanian A, Tamayo P, Mootha VK, Mukherjee S, Ebert BL, Gillette MA, Paulovich A, Pomeroy SL, Golub TR, Lander ES, Mesirov JP 2005 Gene set enrichment analysis: a knowledge-based approach for interpreting genome-wide expression profiles. Proc Natl Acad Sci USA 102:15545-15550
36. Mootha VK, Lindgren CM, Eriksson KF, Subramanian A, Sihag S, Lehar J, Puigserver P, Carlsson E, Ridderstråle M, Laurila E, Houstis N, Daly MJ, Patterson N, Mesirov JP, Golub TR, Tamayo P, Spiegelman B, Lander ES, Hirschhorn JN, Altshuler D, Groop LC 2003 PGC-1α-responsive genes involved in oxidative phosphorylation are coordinately downregulated in human diabetes. Nat Genet 34:267-273
37. Huang da W, Sherman BT, Lempicki RA 2009 Systematic and integrative analysis of large gene lists using DAVID bioinformatics resources. Nat Protoc 4:44-57
38. Rankin S 2005 Sororin, the cell cycle and sister chromatid cohesion. Cell Cycle 4:1039-1042
39. Bharadwaj R, Qi W, Yu H 2004 Identification of two novel components of the human NDC80 kinetochore complex. J Biol Chem 279:13076-13085
40. Rubino D, Driggers P, Arbit D, Kemp L, Miller B, Coso O, Pagliai K, Gray K, Gutkind S, Segars J 1998 Characterization of Brx, a novel Dbl family member that modulates estrogen receptor action. Oncogene 16:2513-2526
41. Lim RW, Halpain S 2000 Regulated association of microtubule-associated protein 2 (MAP2) with Src and Grb2: evidence for MAP2 as a scaffolding protein. J Biol Chem 275:20578-20587
42. Lange CA, Richer JK, Horwitz KB 1999 Hypothesis: Progesterone primes breast cancer cells for cross-talk with proliferative or antiproliferative signals. Mol Endocrinol 13:829-836
43. Lange CA, Richer JK, Shen T, Horwitz KB 1998 Convergence of progesterone and epidermal growth factor signaling in breast cancer. J Biol Chem 273:31308-31316
44. Richer JK, Lange CA, Manning NG, Owen G, Powell R, Horwitz KB 1998 Convergence of progesterone with growth factor and cytokine signaling in breast cancer. J Biol Chem 273:31317-31326
45. Shyamala G, Yang X, Silberstein G, Barcellos-Hoff MH, Dale E 1998 Transgenic mice carrying an imbalance in the native ratio of A to B forms of progesterone receptor exhibit developmental abnormalities in mammary glands. Proc Natl Acad Sci USA 95:696-701
46. Graham JD, Yager ML, Hill HD, Byth K, O'Neill GM, Clarke CL 2005 Altered progesterone receptor isoform expression remodels progestin responsiveness of breast cancer cells. Mol Endocrinol 19:2713-2735 (Pubitemid 41577245)
47. Santos SJ, Aupperlee MD, Xie J, Durairaj S, Miksicek R, Conrad SE, Leipprandt JR, Tan YS, Schwartz RC, Haslam SZ 2009 Progesterone receptor A-regulated gene expression in mammary organoid cultures. J Steroid Biochem Mol Biol 115:161-172
48. Migliaccio A, Piccolo D, Castoria G, Di Domenico M, Bilancio A, Lombardi M, Gong W, Beato M, Auricchio F 1998 Activation of the Src/p21ras/Erk pathway by progesterone receptor via cross-talk with estrogen receptor. EMBO J 17:2008-2018
49. Musgrove EA, Hunter LJ, Lee CS, Swarbrick A, Hui R, Sutherland RL 2001 Cyclin D1 overexpression induces progestin resistance in T-47D breast cancer cells despite p27-Kip1 association with cyclin E-Cdk2. J Biol Chem 276:47675-47693
50. Smyth GK 2005 Limma: linear models for microarray data. In: Gentleman R, Carey V, Dudoity S, Irizarry R, Huber W, eds. Bioinformatics and computational biology solutions using R and bioconductor. Chap 23. New York: Springer-Verlag
51. Benjamini Y, Yekutieli D 2001 The control of the false discovery rate in multiple testing under dependency. Ann Statist 29:1165-1188
52. Pollard KS, Dudoit S, van der Laan MJ 2005 Multiple testing procedures: the multtest package and application to genomics. In Gentleman R, Carey VY, Huber W, Irizarry RA, Dudoit S, eds. Statistics for biology and health: bioinformatics and computational biology solutions using R and bioconductor. Chap 15. New York: Springer
53. Alles MC, Gardiner-Garden M, Nott DJ, Wang Y, Foekens JA, Sutherland RL, Musgrove EA, Ormandy CJ 2009 Meta-analysis and gene set enrichment relative to er status reveal elevated activity of MYC and E2F in the "basal" breast cancer subgroup. PLoS One 4:e4710
54. Irizarry RA, Warren D, Spencer F, Kim IF, Biswal S, Frank BC, Gabrielson E, Garcia JG, Geoghegan J, Germino G, Griffin C, Hilmer SC, Hoffman E, Jedlicka AE, Kawasaki E, Martínez-Murillo F, Morsberger L, Lee H, Petersen D, Quackenbush J, Scott A, Wilson M, Yang Y, Ye SQ, Yu W 2005 Multiple-laboratory comparison of microarray platforms. Nat Methods 2:345-350