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Originally published In Press as doi:10.1074/jbc.M110090200 on November 20, 2001

J. Biol. Chem., Vol. 277, Issue 7, 5209-5218, February 15, 2002
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Differential Gene Regulation by the Two Progesterone Receptor Isoforms in Human Breast Cancer Cells*

Jennifer K. RicherDagger , Britta M. Jacobsen, Nicole G. Manning, M. Greg Abel, Douglas M. Wolf§, and Kathryn B. Horwitz

From the Department of Medicine/Endocrinology and the § Department of Obstetrics and Gynecology and Department of Pharmaceutical Science, University of Colorado School of Medicine, Denver, Colorado 80262

The PR-A and PR-B isoforms of progesterone receptors (PR) have different physiological functions, and their ratio varies widely in breast cancers. To determine whether the two PR regulate different genes, we used human breast cancer cell lines engineered to express one or the other isoform. Cells were treated with progesterone in triplicate, time-separated experiments, allowing statistical analyses of microarray gene expression data. Of 94 progesterone-regulated genes, 65 are uniquely regulated by PR-B, 4 uniquely by PR-A, and only 25 by both. Almost half the genes encode proteins that are membrane-bound or involved in membrane-initiated signaling. We also find an important set of progesterone-regulated genes involved in mammary gland development and/or implicated in breast cancer. This first, large scale study of PR gene regulation has important implications for the measurement of PR in breast cancers and for the many clinical uses of synthetic progestins. It suggests that it is important to distinguish between the two isoforms in breast cancers and that isoform-specific genes can be used to screen for ligands that selectively modulate the activity of PR-A or PR-B. Additionally, use of natural target genes, rather than "consensus" response elements, for transcription studies should improve our understanding of steroid hormone action.


* This work was supported by National Institutes of Health Grants DK48238 and CA26869, the National Foundation for Cancer Research (to K. B. H.), Department of Defense Breast Cancer Research Program Concept Award BC996535 (to J. K. R.), and an American Cancer Society IRG University of Colorado Cancer Center Seed Grant (to J. K. R.).The costs of publication of this article were defrayed in part by the payment of page charges. The article must therefore be hereby marked "advertisement" in accordance with 18 U.S.C. Section 1734 solely to indicate this fact.

Dagger To whom correspondence should be addressed: Dept. of Medicine/Endocrinology, University of Colorado School of Medicine, Box B-151, 4200 East Ninth Ave., Denver, CO 80262. Tel.: 303-315-8443; Fax: 303-315-4525; E-mail: jennifer.richer@uchsc.edu; www.khorwitzlab.org.


Copyright © 2002 by The American Society for Biochemistry and Molecular Biology, Inc.
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Cancer Epidemiol. Biomarkers Prev.Home page
A. Berchuck, J. M. Schildkraut, R. M. Wenham, B. Calingaert, S. Ali, A. Henriott, S. Halabi, G. C. Rodriguez, D. Gertig, D. M. Purdie, et al.
Progesterone Receptor Promoter +331A Polymorphism is Associated with a Reduced Risk of Endometrioid and Clear Cell Ovarian Cancers
Cancer Epidemiol. Biomarkers Prev., December 1, 2004; 13(12): 2141 - 2147.
[Abstract] [Full Text] [PDF]


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Cancer Res.Home page
T. Sumida, Y. Itahana, H. Hamakawa, and P.-Y. Desprez
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., November 1, 2004; 64(21): 7886 - 7892.
[Abstract] [Full Text] [PDF]


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Cancer Res.Home page
Q. Ji, C. Aoyama, Y.-D. Nien, P. I. Liu, P. K. Chen, L. Chang, F. Z. Stanczyk, and A. Stolz
Selective Loss of AKR1C1 and AKR1C2 in Breast Cancer and Their Potential Effect on Progesterone Signaling
Cancer Res., October 15, 2004; 64(20): 7610 - 7617.
[Abstract] [Full Text] [PDF]


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Reproductive SciencesHome page
S. Davies, D. Dai, D. M. Wolf, and K. K. Leslie
Immunomodulatory and Transcriptional Effects of Progesterone Through Progesterone A and B Receptors in Hec50co Poorly Differentiated Endometrial Cancer Cells
Reproductive Sciences, October 1, 2004; 11(7): 494 - 499.
[Abstract] [PDF]


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Mol. Cell. Biol.Home page
L. Cicatiello, R. Addeo, A. Sasso, L. Altucci, V. B. Petrizzi, R. Borgo, M. Cancemi, S. Caporali, S. Caristi, C. Scafoglio, 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., August 15, 2004; 24(16): 7260 - 7274.
[Abstract] [Full Text] [PDF]


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J. Biol. Chem.Home page
C. Qi, P. Kashireddy, Y. T. Zhu, S. M. Rao, and Y.-J. Zhu
Null Mutation of Peroxisome Proliferator-activated Receptor-interacting Protein in Mammary Glands Causes Defective Mammopoiesis
J. Biol. Chem., August 6, 2004; 279(32): 33696 - 33701.
[Abstract] [Full Text] [PDF]


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DevelopmentHome page
R. Bagheri-Yarmand, A. H. Talukder, R.-A. Wang, R. K. Vadlamudi, and R. Kumar
Metastasis-associated protein 1 deregulation causes inappropriate mammary gland development and tumorigenesis
Development, July 15, 2004; 131(14): 3469 - 3479.
[Abstract] [Full Text] [PDF]


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J. Biol. Chem.Home page
R. C. M. Simmen, R. R. Eason, J. R. McQuown, A. L. Linz, T.-J. Kang, L. Chatman Jr., S. R. Till, Y. Fujii-Kuriyama, F. A. Simmen, and S. P. Oh
Subfertility, Uterine Hypoplasia, and Partial Progesterone Resistance in Mice Lacking the Kruppel-like Factor 9/Basic Transcription Element-binding Protein-1 (Bteb1) Gene
J. Biol. Chem., July 9, 2004; 279(28): 29286 - 29294.
[Abstract] [Full Text] [PDF]


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EndocrinologyHome page
F. Stossi, D. H. Barnett, J. Frasor, B. Komm, C. R. Lyttle, and B. S. Katzenellenbogen
Transcriptional Profiling of Estrogen-Regulated Gene Expression via Estrogen Receptor (ER) {alpha} or ER{beta} in Human Osteosarcoma Cells: Distinct and Common Target Genes for These Receptors
Endocrinology, July 1, 2004; 145(7): 3473 - 3486.
[Abstract] [Full Text] [PDF]


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ScienceHome page
J. L. Turgeon, D. P. McDonnell, K. A. Martin, and P. M. Wise
Hormone Therapy: Physiological Complexity Belies Therapeutic Simplicity
Science, May 28, 2004; 304(5675): 1269 - 1273.
[Abstract] [Full Text] [PDF]


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EndocrinologyHome page
O. Gonzalez-Flores, C. Guerra-Araiza, M. Cerbon, I. Camacho-Arroyo, and A. M. Etgen
The 26S Proteasome Participates in the Sequential Inhibition of Estrous Behavior Induced by Progesterone in Rats
Endocrinology, May 1, 2004; 145(5): 2328 - 2336.
[Abstract] [Full Text] [PDF]


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Clin. Cancer Res.Home page
T. A. Hopp, H. L. Weiss, S. G. Hilsenbeck, Y. Cui, D. C. Allred, K. B. Horwitz, and S. A. W. Fuqua
Breast Cancer Patients with Progesterone Receptor PR-A-Rich Tumors Have Poorer Disease-Free Survival Rates
Clin. Cancer Res., April 15, 2004; 10(8): 2751 - 2760.
[Abstract] [Full Text] [PDF]


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Cancer Res.Home page
J. Wu, J. Richer, K. B. Horwitz, and S. M. Hyder
Progestin-Dependent Induction of Vascular Endothelial Growth Factor in Human Breast Cancer Cells: Preferential Regulation by Progesterone Receptor B
Cancer Res., March 15, 2004; 64(6): 2238 - 2244.
[Abstract] [Full Text] [PDF]


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J. Clin. Endocrinol. Metab.Home page
R. L. Arnett-Mansfield, A. deFazio, P. A. Mote, and C. L. Clarke
Subnuclear Distribution of Progesterone Receptors A and B in Normal and Malignant Endometrium
J. Clin. Endocrinol. Metab., March 1, 2004; 89(3): 1429 - 1442.
[Abstract] [Full Text] [PDF]


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Mol. Biol. CellHome page
M. Kian Tee, I. Rogatsky, C. Tzagarakis-Foster, A. Cvoro, J. An, R. J. Christy, K. R. Yamamoto, and D. C. Leitman
Estradiol and Selective Estrogen Receptor Modulators Differentially Regulate Target Genes with Estrogen Receptors {alpha} and {beta}
Mol. Biol. Cell, March 1, 2004; 15(3): 1262 - 1272.
[Abstract] [Full Text] [PDF]


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Proc. Natl. Acad. Sci. USAHome page
D. Auboeuf, D. H. Dowhan, Y. K. Kang, K. Larkin, J. W. Lee, S. M. Berget, and B. W. O'Malley
Differential recruitment of nuclear receptor coactivators may determine alternative RNA splice site choice in target genes
PNAS, February 24, 2004; 101(8): 2270 - 2274.
[Abstract] [Full Text] [PDF]


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Am J EpidemiolHome page
F. Modugno
Ovarian Cancer and Polymorphisms in the Androgen and Progesterone Receptor Genes: A HuGE Review
Am. J. Epidemiol., February 15, 2004; 159(4): 319 - 335.
[Abstract] [Full Text] [PDF]


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Toxicol PatholHome page
Progesterone, Estrogens, and their Receptors in Breast Cancers KATHRYN B. HORWITZ, Departments of Medicine, Pathology and the Molecular Biology Program, University of Colorado School of Medicine, Denver, Colorado
Toxicol Pathol, January 1, 2004; 32(1): 142 - 143.
[PDF]


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EndocrinologyHome page
V. C. L. Lin, C. T. Woon, S. E. Aw, and C. Guo
Distinct Molecular Pathways Mediate Progesterone-Induced Growth Inhibition And Focal Adhesion
Endocrinology, December 1, 2003; 144(12): 5650 - 5657.
[Abstract] [Full Text] [PDF]


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J. Biol. Chem.Home page
X. Li and B. W. O'Malley
Unfolding the Action of Progesterone Receptors
J. Biol. Chem., October 10, 2003; 278(41): 39261 - 39264.
[Full Text] [PDF]


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Clin. Cancer Res.Home page
E. E. Hanekamp, S. C. J. P. Gielen, E. Smid-Koopman, L. C. M. Kuhne, P. E. de Ruiter, S. Chadha-Ajwani, A. O. Brinkmann, J. A. Grootegoed, C. W. Burger, F. J. Huikeshoven, et al.
Consequences of Loss of Progesterone Receptor Expression in Development of Invasive Endometrial Cancer
Clin. Cancer Res., September 15, 2003; 9(11): 4190 - 4199.
[Abstract] [Full Text] [PDF]


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Cancer Res.Home page
I. De Vivo, S. E. Hankinson, G. A. Colditz, and D. J. Hunter
A Functional Polymorphism in the Progesterone Receptor Gene Is Associated with an Increase in Breast Cancer Risk
Cancer Res., September 1, 2003; 63(17): 5236 - 5238.
[Abstract] [Full Text] [PDF]


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Proc. Natl. Acad. Sci. USAHome page
B. Mulac-Jericevic, J. P. Lydon, F. J. DeMayo, and O. M. Conneely
Defective mammary gland morphogenesis in mice lacking the progesterone receptor B isoform
PNAS, August 19, 2003; 100(17): 9744 - 9749.
[Abstract] [Full Text] [PDF]


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J. Biol. Chem.Home page
J. R. Wood, V. L. Nelson, C. Ho, E. Jansen, C. Y. Wang, M. Urbanek, J. M. McAllister, S. Mosselman, and J. F. Strauss III
The Molecular Phenotype of Polycystic Ovary Syndrome (PCOS) Theca Cells and New Candidate PCOS Genes Defined by Microarray Analysis
J. Biol. Chem., July 11, 2003; 278(29): 26380 - 26390.
[Abstract] [Full Text] [PDF]


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J. Biol. Chem.Home page
X.-L. Zhang, D. Zhang, F. J. Michel, J. L. Blum, F. A. Simmen, and R. C. M. Simmen
Selective Interactions of Kruppel-like Factor 9/Basic Transcription Element-binding Protein with Progesterone Receptor Isoforms A and B Determine Transcriptional Activity of Progesterone-responsive Genes in Endometrial Epithelial Cells
J. Biol. Chem., June 6, 2003; 278(24): 21474 - 21482.
[Abstract] [Full Text] [PDF]


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EndocrinologyHome page
T. R. Hubler, W. B. Denny, D. L. Valentine, J. Cheung-Flynn, D. F. Smith, and J. G. Scammell
The FK506-Binding Immunophilin FKBP51 Is Transcriptionally Regulated by Progestin and Attenuates Progestin Responsiveness
Endocrinology, June 1, 2003; 144(6): 2380 - 2387.
[Abstract] [Full Text] [PDF]


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Mol. Endocrinol.Home page
X. Cui, P. Zhang, W. Deng, S. Oesterreich, Y. Lu, G. B. Mills, and A. V. Lee
Insulin-Like Growth Factor-I Inhibits Progesterone Receptor Expression in Breast Cancer Cells via the Phosphatidylinositol 3-Kinase/Akt/Mammalian Target of Rapamycin Pathway: Progesterone Receptor as a Potential Indicator of Growth Factor Activity in Breast Cancer
Mol. Endocrinol., April 1, 2003; 17(4): 575 - 588.
[Abstract] [Full Text] [PDF]


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DevelopmentHome page
L. Cherbas, X. Hu, I. Zhimulev, E. Belyaeva, and P. Cherbas
EcR isoforms in Drosophila: testing tissue-specific requirements by targeted blockade and rescue
Development, March 2, 2003; 130(2): 271 - 284.
[Abstract] [Full Text] [PDF]


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Biol. Reprod.Home page
R. Shao, E. Markstrom, P. A. Friberg, M. Johansson, and H. Billig
Expression of Progesterone Receptor (PR) A and B Isoforms in Mouse Granulosa Cells: Stage-Dependent PR-Mediated Regulation of Apoptosis and Cell Proliferation
Biol Reprod, March 1, 2003; 68(3): 914 - 921.
[Abstract] [Full Text] [PDF]


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Recent Prog Horm ResHome page
Y. Wan and S. K. Nordeen
Overlapping but Distinct Profiles of Gene Expression Elicited by Glucocorticoids and Progestins
Recent Prog. Horm. Res., January 1, 2003; 58(1): 199 - 226.
[Abstract] [Full Text] [PDF]


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Exp. Biol. Med.Home page
S. A. Leonhardt and D. P. Edwards
Mechanism of Action of Progesterone Antagonists
Experimental Biology and Medicine, December 1, 2002; 227(11): 969 - 980.
[Abstract] [Full Text]


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Am. J. Physiol. Endocrinol. Metab.Home page
X. Fang, S. Wong, and B. F. Mitchell
Messenger RNA for progesterone receptor isoforms in the late-gestation rat uterus
Am J Physiol Endocrinol Metab, December 1, 2002; 283(6): E1167 - E1172.
[Abstract] [Full Text] [PDF]


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Proc. Natl. Acad. Sci. USAHome page
I. De Vivo, G. S. Huggins, S. E. Hankinson, P. J. Lescault, M. Boezen, G. A. Colditz, and D. J. Hunter
A functional polymorphism in the promoter of the progesterone receptor gene associated with endometrial cancer risk
PNAS, September 17, 2002; 99(19): 12263 - 12268.
[Abstract] [Full Text] [PDF]


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J. Biol. Chem.Home page
H. Abdel-Hafiz, G. S. Takimoto, L. Tung, and K. B. Horwitz
The Inhibitory Function in Human Progesterone Receptor N Termini Binds SUMO-1 Protein to Regulate Autoinhibition and Transrepression
J. Biol. Chem., September 6, 2002; 277(37): 33950 - 33956.
[Abstract] [Full Text] [PDF]


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EndocrinologyHome page
G. Sathya, M. S. Jansen, S. C. Nagel, C. E. Cook, and D. P. MCDonnell
Identification and Characterization of Novel Estrogen Receptor-{beta}-Sparing Antiprogestins
Endocrinology, August 1, 2002; 143(8): 3071 - 3082.
[Abstract] [Full Text] [PDF]


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J. Biol. Chem.Home page
B. M. Jacobsen, J. K. Richer, S. A. Schittone, and K. B. Horwitz
New Human Breast Cancer Cells to Study Progesterone Receptor Isoform Ratio Effects and Ligand-independent Gene Regulation
J. Biol. Chem., July 26, 2002; 277(31): 27793 - 27800.
[Abstract] [Full Text] [PDF]


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EndocrinologyHome page
D. Soulet and S. Rivest
Perspective: How to Make Microarray, Serial Analysis of Gene Expression, and Proteomic Relevant to Day-to-Day Endocrine Problems and Physiological Systems
Endocrinology, June 1, 2002; 143(6): 1995 - 2001.
[Abstract] [Full Text] [PDF]




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