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