Progesterone receptor action: defining a role in breast cancer

References

• Tsai SY, Carlstedt-Duke J, Weigel NL et al. Molecular interactions of steroid hormone receptor with its enhancer element: evidence for receptor dimer formation. Cell55(2), 361–369 (1988).
   PubMed Web of Science ®Google Scholar
• Richer JK, Lange CA, Manning NG et al. Convergence of progesterone with growth factor and cytokine signaling in breast cancer. Progesterone receptors regulate signal transducers and activators of transcription expression and activity. J. Biol. Chem.273(47), 31317–31326 (1998).
   PubMed Web of Science ®Google Scholar
• Owen GI, Richer JK, Tung L, Takimoto G, Horwitz KB. Progesterone regulates transcription of the p21(WAF1) cyclin-dependent kinase inhibitor gene through Sp1 and CBP/p300. J. Biol. Chem.273(17), 10696–10701 (1998).
   PubMed Web of Science ®Google Scholar
• Proietti C, Salatino M, Rosemblit C et al. Progestins induce transcriptional activation of signal transducer and activator of transcription 3 (Stat3) via a Jak- and Src-dependent mechanism in breast cancer cells. Mol. Cell Biol.25(12), 4826–4840 (2005).
   PubMed Web of Science ®Google Scholar
• Tseng L, Tang M, Wang Z, Mazella J. Progesterone receptor (hPR) upregulates the fibronectin promoter activity in human decidual fibroblasts. DNA Cell Biol.22(10), 633–640 (2003).
   PubMedGoogle Scholar
• Jacobsen BM, Richer JK, Sartorius CA, Horwitz KB. Expression profiling of human breast cancers and gene regulation by progesterone receptors. J. Mammary Gland Biol. Neoplasia8(3), 257–268 (2003).
   PubMedGoogle Scholar
• Richer JK, Jacobsen BM, Manning NG et al. Differential gene regulation by the two progesterone receptor isoforms in human breast cancer cells. J. Biol. Chem.277(7), 5209–5218 (2002).
   PubMed Web of Science ®Google Scholar
• Lange CA, Sartorius CA, Abdel-Hafiz H et al. Progesterone receptor action: translating studies in breast cancer models to clinical insights. Adv. Exp. Med. Biol.630, 94–111 (2008).
   PubMedGoogle Scholar
• Condon JC, Hardy DB, Kovaric K, Mendelson CR. Up-regulation of the progesterone receptor (PR)-C isoform in laboring myometrium by activation of nuclear factor-κB may contribute to the onset of labor through inhibition of PR function. Mol. Endocrinol.20(4), 764–775 (2006).
   PubMedGoogle Scholar
• Migliaccio A, Piccolo D, Castoria G et al. Activation of the Src/p21ras/Erk pathway by progesterone receptor via cross-talk with estrogen receptor. EMBO J.17(7), 2008–2018 (1998).
   PubMed Web of Science ®Google Scholar
• Boonyaratanakornkit V, Scott MP, Ribon V et al. Progesterone receptor contains a proline-rich motif that directly interacts with SH3 domains and activates c-Src family tyrosine kinases. Mol. Cell8(2), 269–280 (2001).
   PubMed Web of Science ®Google Scholar
• Saitoh M, Ohmichi M, Takahashi K et al. Medroxyprogesterone acetate induces cell proliferation through up-regulation of cyclin D1 expression via phosphatidylinositol 3-kinase/Akt/nuclear factor-κB cascade in human breast cancer cells. Endocrinology146(11), 4917–4925 (2005).
   PubMed Web of Science ®Google Scholar
• Ballare C, Uhrig M, Bechtold T et al. Two domains of the progesterone receptor interact with the estrogen receptor and are required for progesterone activation of the c-Src/Erk pathway in mammalian cells. Mol. Cell Biol.23(6), 1994–2008 (2003).
   PubMed Web of Science ®Google Scholar
• 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.27(2), 466–480 (2007).
   PubMed Web of Science ®Google Scholar
• Faivre EJ, Daniel AR, Hillard CJ, Lange CA. Progesterone receptor rapid signaling mediates serine 345 phosphorylation and tethering to specificity protein 1 transcription factors. Mol. Endocrinol.22(4), 823–837 (2008).
   PubMedGoogle Scholar
• Béguelin W, Diaz Flaque MC, Proietti CJ et al. Progesterone receptor induces ErbB-2 nuclear translocation to promote breast cancer growth via a novel transcriptional effect: ErbB-2 function as a coactivator of Stat3. Mol. Cell Biol.30(23), 5456–5472 (2010).
   PubMed Web of Science ®Google Scholar
• Razandi M, Pedram A, Levin ER. Heat shock protein 27 is required for sex steroid receptor trafficking to and functioning at the plasma membrane. Mol. Cell Biol.30(13), 3249–3261 (2010).
   PubMed Web of Science ®Google Scholar
• Narayanan R, Adigun AA, Edwards DP, Weigel NL. Cyclin-dependent kinase activity is required for progesterone receptor function: novel role for cyclin A/Cdk2 as a progesterone receptor coactivator. Mol. Cell Biol.25(1), 264–277 (2005).
   PubMed Web of Science ®Google Scholar
• Daniel AR, Faivre EJ, Lange CA. Phosphorylation-dependent antagonism of sumoylation derepresses progesterone receptor action in breast cancer cells. Mol. Endocrinol.21(12), 2890–2906 (2007).
   PubMed Web of Science ®Google Scholar
• Daniel AR, Gaviglio AL, Czaplicki LM et al. The progesterone receptor hinge region regulates the kinetics of transcriptional responses through acetylation, phosphorylation, and nuclear retention. Mol. Endocrinol.24(11), 2126–2138 (2010).
   PubMed Web of Science ®Google Scholar
• Lange CA, Shen T, Horwitz KB. Phosphorylation of human progesterone receptors at serine-294 by mitogen-activated protein kinase signals their degradation by the 26S proteasome. Proc. Natl Acad. Sci. USA97(3), 1032–1037 (2000).
   PubMed Web of Science ®Google Scholar
• Weigel NL, Bai W, Zhang Y et al. Phosphorylation and progesterone receptor function. J. Steroid Biochem. Mol. Biol.53(1–6), 509–514 (1995).
   PubMed Web of Science ®Google Scholar
• Abdel-Hafiz H, Takimoto GS, Tung L, Horwitz KB. The inhibitory function in human progesterone receptor N termini binds SUMO-1 protein to regulate autoinhibition and transrepression. J. Biol. Chem.277(37), 33950–33956 (2002).
   PubMed Web of Science ®Google Scholar
• Ward RD, Weigel NL. Steroid receptor phosphorylation: assigning function to site-specific phosphorylation. Biofactors35(6), 528–536 (2009).
   PubMedGoogle Scholar
• Zhang Y, Beck CA, Poletti A et al. Phosphorylation of human progesterone receptor by cyclin-dependent kinase 2 on three sites that are authentic basal phosphorylation sites in vivo. Mol. Endocrinol.11(6), 823–832 (1997).
   PubMedGoogle Scholar
• Pierson-Mullany LK, Lange CA. Phosphorylation of progesterone receptor serine 400 mediates ligand-independent transcriptional activity in response to activation of cyclin-dependent protein kinase 2. Mol. Cell. Biol.24(24) 10542–10557 (2004).
   PubMed Web of Science ®Google Scholar
• Knotts TA, Orkiszewski RS, Cook RG, Edwards DP, Weigel NL. Identification of a phosphorylation site in the hinge region of the human progesterone receptor and additional amino-terminal phosphorylation sites. J. Biol. Chem.276(11), 8475–8483 (2001).
   PubMed Web of Science ®Google Scholar
• Daniel AR, Lange CA. Protein kinases mediate ligand-independent derepression of sumoylated progesterone receptors in breast cancer cells. Proc. Natl Acad. Sci. USA106(34), 14287–14292 (2009).
   PubMedGoogle Scholar
• Cui Y, Zhang M, Pestell R et al. Phosphorylation of estrogen receptor α blocks its acetylation and regulates estrogen sensitivity. Cancer Res.64(24), 9199–9208 (2004).
   PubMedGoogle Scholar
• Graham JD, Mote PA, Salagame U et al. DNA replication licensing and progenitor numbers are increased by progesterone in normal human breast. Endocrinology150(7), 3318–3326 (2009).
   PubMed Web of Science ®Google Scholar
• Graham JD, Clarke CL. Physiological action of progesterone in target tissues. Endocr. Rev.18(4), 502–519 (1997).
   PubMed Web of Science ®Google Scholar
• Joshi PA, Jackson HW, Beristain AG et al. Progesterone induces adult mammary stem cell expansion. Nature465(7299), 803–807 (2010).
   PubMed Web of Science ®Google Scholar
• Conneely OM, Mulac-Jericevic B, Lydon JP, De Mayo FJ. Reproductive functions of the progesterone receptor isoforms: lessons from knock-out mice. Mol. Cell Endocrinol.1(1–2), 97–103 (2001).
   Google Scholar
• Fata JE, Kong YY, Li J et al. The osteoclast differentiation factor osteoprotegerin-ligand is essential for mammary gland development. Cell103(1), 41–50 (2000).
   PubMed Web of Science ®Google Scholar
• Sicinski P, Donaher JL, Parker SB et al. Cyclin D1 provides a link between development and oncogenesis in the retina and breast. Cell82(4), 621–630 (1995).
   PubMed Web of Science ®Google Scholar
• Gonzalez-Suarez E, Jacob AP, Jones J et al. RANK ligand mediates progestin-induced mammary epithelial proliferation and carcinogenesis. Nature468(7320), 103–107 (2010).
   PubMed Web of Science ®Google Scholar
• Kariagina A, Aupperlee MD, Haslam SZ. Progesterone receptor isoform functions in normal breast development and breast cancer. Crit. Rev. Eukaryot. Gene Expr.18(1), 11–33 (2008).
   PubMed Web of Science ®Google Scholar
• Brisken C, O’Malley B. Hormone action in the mammary gland. Cold Spring Harb. Perspect. Biol.2(12), a003178 (2010).
   PubMedGoogle Scholar
• Clarke RB, Howell A, Potten CS, Anderson E. Dissociation between steroid receptor expression and cell proliferation in the human breast. Cancer Res.57(22), 4987–4991 (1997).
   PubMed Web of Science ®Google Scholar
• Russo J, Ao X, Grill C, Russo IH. Pattern of distribution of cells positive for estrogen receptor α and progesterone receptor in relation to proliferating cells in the mammary gland. Breast Cancer Res. Treat.53(3), 217–227 (1999).
   PubMed Web of Science ®Google Scholar
• Seagroves TN, Lydon JP, Hovey RC, Vonderhaar BK, Rosen JM. C/EBPβ (CCAAT/enhancer binding protein) controls cell fate determination during mammary gland development. Mol. Endocrinol.14(3), 359–368 (2000).
   PubMed Web of Science ®Google Scholar
• Brisken C, Park S, Vass T et al. A paracrine role for the epithelial progesterone receptor in mammary gland development. Proc. Natl Acad. Sci. USA95(9), 5076–5081 (1998).
   PubMed Web of Science ®Google Scholar
• Beleut M, Rajaram RD, Caikovski M et al. Two distinct mechanisms underlie progesterone-induced proliferation in the mammary gland. Proc. Natl Acad. Sci. USA107(7), 2989–2994 (2010).
   PubMed Web of Science ®Google Scholar
• Brisken C, Heineman A, Chavarria T et al. Essential function of Wnt-4 in mammary gland development downstream of progesterone signaling. Genes Dev.14(6), 650–654 (2000).
   PubMed Web of Science ®Google Scholar
• Kariagina A, Aupperlee MD, Haslam SZ. Progesterone receptor isoforms and proliferation in the rat mammary gland during development. Endocrinology148(6), 2723–2736 (2007).
   PubMed Web of Science ®Google Scholar
• Arpino G, Weiss H, Lee AV et al. Estrogen receptor-positive, progesterone receptor-negative breast cancer: association with growth factor receptor expression and tamoxifen resistance. J. Natl Cancer Inst.97(17), 1254–1261 (2005).
   PubMed Web of Science ®Google Scholar
• Moore MR, Conover JL, Franks KM. Progestin effects on long-term growth, death, and Bcl-xL in breast cancer cells. Biochem. Biophys. Res. Commun.277(3), 650–654 (2000).
   PubMed Web of Science ®Google Scholar
• Lydon JP, Ge G, Kittrell FS, Medina D, O’Malley BW. Murine mammary gland carcinogenesis is critically dependent on progesterone receptor function. Cancer Res.59(17), 4276–4284 (1999).
   PubMed Web of Science ®Google Scholar
• Poole AJ, Li Y, Kim Y et al. Prevention of Brca1-mediated mammary tumorigenesis in mice by a progesterone antagonist. Science314(5804), 1467–1470 (2006).
   PubMed Web of Science ®Google Scholar
• Lanari C, Lamb CA, Fabris VT et al. The MPA mouse breast cancer model: evidence for a role of progesterone receptors in breast cancer. Endocr. Relat. Cancer16(2), 333–350 (2009).
   PubMed Web of Science ®Google Scholar
• Wiehle RD, Lantvit DD, Yamada T, Christov K. CDB-4124, a progesterone receptor modulator, inhibits mammary carcinogenesis by supressing cell proliferation and inducing apoptosis. Cancer Prev. Res. (Phila.)4(3), 414–424 (2011).
   PubMedGoogle Scholar
• Perrault D, Eisenhauer EA, Pritchard KI et al. Phase II study of the progesterone antagonist mifepristone in patients with untreated metastatic breast carcinoma: a National Cancer Institute of Canada Clinical Trials Group study. J. Clin. Oncol.14(10), 2709–2712 (1996).
   PubMed Web of Science ®Google Scholar
• Robertson JF, Willsher PC, Winterbottom L, Blamey RW, Thorpe S. Onapristone, a progesterone receptor antagonist, as first-line therapy in primary breast cancer. Eur. J. Cancer35(2), 214–218 (1999).
   PubMed Web of Science ®Google Scholar
• Chlebowski RT, Anderson GL, Gass M et al. Estrogen plus progestin and breast cancer incidence and mortality in postmenopausal women. JAMA304(15), 1684–1692 (2010).
   PubMed Web of Science ®Google Scholar
• Beral V. Breast cancer and hormone-replacement therapy in the Million Women Study. Lancet362(9382), 419–427 (2003).
   PubMed Web of Science ®Google Scholar
• Hagan CR, Regan TM, Dressing GE, Lange CA. Ck2-dependent phosphorylation of progesterone receptors (PR) on Ser81 regulates PR-B-isoform-specific target gene regulation in breast cancer cells. Mol. Cell Biol. DOI: 10.1128/MCB.01246-10 (2011) (Epub ahead of print).
   PubMedGoogle Scholar
• Bernstein L. Epidemiology of endocrine-related risk factors for breast cancer. J. Mammary Gland Biol. Neoplasia7(1), 3–15 (2002).
   PubMed Web of Science ®Google Scholar
• Brisken C, Duss S. Stem cells and the stem cell niche in the breast: an integrated hormonal and developmental perspective. Stem Cell Rev.3(2), 147–156 (2007).
   PubMed Web of Science ®Google Scholar
• Harmes DC, DiRenzo J. Cellular quiescence in mammary stem cells and breast tumor stem cells: got testable hypotheses? J. Mammary Gland Biol. Neoplasia14(1), 19–27 (2009).
   PubMed Web of Science ®Google Scholar
• Shackleton M, Vaillant F, Simpson KJ et al. Generation of a functional mammary gland from a single stem cell. Nature439(7072), 84–88 (2006).
   PubMed Web of Science ®Google Scholar
• Smith GH. Label-retaining epithelial cells in mouse mammary gland divide asymmetrically and retain their template DNA strands. Development132(4), 681–687 (2005).
   PubMed Web of Science ®Google Scholar
• Booth BW, Boulanger CA, Smith GH. Selective segregation of DNA strands persists in long-label-retaining mammary cells during pregnancy. Breast Cancer Res.10(5), R90 (2008).
   Google Scholar
• Booth BW, Smith GH. Estrogen receptor-α and progesterone receptor are expressed in label-retaining mammary epithelial cells that divide asymmetrically and retain their template DNA strands. Breast Cancer Res.8(4), R49 (2006).
   PubMed Web of Science ®Google Scholar
• Asselin-Labat ML, Shackleton M, Stingl J et al. Steroid hormone receptor status of mouse mammary stem cells. J. Natl Cancer Inst.98(14), 1011–1014 (2006).
   PubMedGoogle Scholar
• Clarke RB. Isolation and characterization of human mammary stem cells. Cell Prolif.38(6), 375–386 (2005).
   PubMedGoogle Scholar
• Dontu G, Al-Hajj M, Abdallah WM, Clarke MF, Wicha MS. Stem cells in normal breast development and breast cancer. Cell Prolif.36(Suppl. 1) 59–72 (2003).
   PubMed Web of Science ®Google Scholar
• Schramek D, Leibbrandt A, Sigl V et al. Osteoclast differentiation factor RANKL controls development of progestin-driven mammary cancer. Nature468(7320), 98–102 (2010).
   PubMed Web of Science ®Google Scholar
• Tanos T, Brisken C. High hopes for RANKL: will the mouse model live up to its promise? Breast Cancer Res.13(1), 302 (2011).
   PubMedGoogle Scholar
• Ayyanan A, Civenni G, Ciarloni L et al. Increased Wnt signaling triggers oncogenic conversion of human breast epithelial cells by a Notch-dependent mechanism. Proc. Natl Acad. Sci. USA103(10), 3799–3804 (2006).
   PubMed Web of Science ®Google Scholar
• Dontu G, Jackson KW, McNicholas E et al. Role of Notch signaling in cell-fate determination of human mammary stem/progenitor cells. Breast Cancer Res.6(6), R605–R615 (2004).
   PubMed Web of Science ®Google Scholar
• 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. USA105(15), 5774–5779 (2008).
   PubMed Web of Science ®Google Scholar
• Horwitz KB, Sartorius CA. Progestins in hormone replacement therapies reactivate cancer stem cells in women with preexisting breast cancers: a hypothesis. J. Clin. Endocrinol. Metab.93(9), 3295–3298 (2008).
   PubMed Web of Science ®Google Scholar
• Groshong SD, Owen GI, Grimison B et al. Biphasic regulation of breast cancer cell growth by progesterone: role of the cyclin-dependent kinase inhibitors, p21 and p27(Kip1). Mol. Endocrinol.11(11), 1593–1607 (1997).
   PubMed Web of Science ®Google Scholar
• Allred DC, Medina D. The relevance of mouse models to understanding the development and progression of human breast cancer. J. Mammary Gland Biol. Neoplasia13(3), 279–288 (2008).
   PubMed Web of Science ®Google Scholar
• Lange CA, Yee D. Progesterone and breast cancer. Womens Health4(2), 151–162 (2008).
   Google Scholar
• Benakanakere I, Besch-Williford C, Ellersieck MR, Hyder SM. Regression of progestin-accelerated 7, 12-dimethylbenz[a]anthracene-induced mammary tumors in Sprague–Dawley rats by p53 reactivation and induction of massive apoptosis: a pilot study. Endocr. Relat. Cancer16(1), 85–98 (2009).
   PubMedGoogle Scholar
• Cerliani JP, Giulianelli S, Sahores A et al. Mifepristone inhibits MPA-and FGF2-induced mammary tumor growth but not FGF2-induced mammary hyperplasia. Medicina (B. Aires)70(6), 529–532 (2010).
   PubMedGoogle Scholar
• Graham JD, Yeates C, Balleine RL et al. Characterization of progesterone receptor A and B expression in human breast cancer. Cancer Res.55(21), 5063–5068 (1995).
   PubMed Web of Science ®Google Scholar
• Anderson E. The role of oestrogen and progesterone receptors in human mammary development and tumorigenesis. Breast Cancer Res.4(5), 197–201 (2002).
   PubMed Web of Science ®Google Scholar
• Clarke CA, Glaser SL, Uratsu CS et al. Recent declines in hormone therapy utilization and breast cancer incidence: clinical and population-based evidence. J. Clin. Oncol.24(33), e49–e50 (2006).
   PubMed Web of Science ®Google Scholar
• Hofseth LJ, Raafat AM, Osuch JR et al. Hormone replacement therapy with estrogen or estrogen plus medroxyprogesterone acetate is associated with increased epithelial proliferation in the normal postmenopausal breast. J. Clin. Endocrinol. Metab.84(12), 4559–4565 (1999).
   PubMed Web of Science ®Google Scholar
• Lee S, Kolonel L, Wilkens L et al. Postmenopausal hormone therapy and breast cancer risk: the Multiethnic Cohort. Int. J. Cancer118(5), 1285–1291 (2006).
   PubMed Web of Science ®Google Scholar
• Ross RK, Paganini-Hill A, Wan PC, Pike MC. Effect of hormone replacement therapy on breast cancer risk: estrogen versus estrogen plus progestin. J. Natl Cancer Inst.92(4), 328–332 (2000).
   PubMed Web of Science ®Google Scholar
• Rossouw JE, Anderson GL, Prentice RL et al. Risks and benefits of estrogen plus progestin in healthy postmenopausal women: principal results from the Women’s Health Initiative randomized controlled trial. JAMA288(3), 321–333 (2002).
   PubMed Web of Science ®Google Scholar
• Shen T, Horwitz KB, Lange CA. Transcriptional hyperactivity of human progesterone receptors is coupled to their ligand-dependent down-regulation by mitogen-activated protein kinase-dependent phosphorylation of serine 294. Mol. Cell Biol.21(18), 6122–6131 (2001).
   PubMed Web of Science ®Google Scholar
• Hennighausen L, Robinson GW. Signaling pathways in mammary gland development. Dev. Cell1(4), 467–475 (2001).
   PubMed Web of Science ®Google Scholar
• Fan P, Yue W, Wang JP et al. Mechanisms of resistance to structurally diverse antiestrogens differ under premenopausal and postmenopausal conditions: evidence from in vitro breast cancer cell models. Endocrinology150(5), 2036–2045 (2009).
   PubMedGoogle Scholar
• Massarweh S, Osborne CK, Creighton CJ et al. Tamoxifen resistance in breast tumors is driven by growth factor receptor signaling with repression of classic estrogen receptor genomic function. Cancer Res.68(3), 826–833 (2008).
   PubMed Web of Science ®Google Scholar
• Ring A, Dowsett M. Mechanisms of tamoxifen resistance. Endocr. Relat. Cancer11(4), 643–658 (2004).
   PubMed Web of Science ®Google Scholar
• Mote PA, Bartow S, Tran N, Clarke CL. Loss of co-ordinate expression of progesterone receptors A and B is an early event in breast carcinogenesis. Breast Cancer Res. Treat.72(2), 163–172 (2002).
   PubMed Web of Science ®Google Scholar
• Cui X, Schiff R, Arpino G, Osborne CK, Lee AV. Biology of progesterone receptor loss in breast cancer and its implications for endocrine therapy. J. Clin. Oncol.23(30), 7721–7735 (2005).
   PubMed Web of Science ®Google Scholar
• Cui X, Zhang P, Deng W et al. 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.17(4), 575–588 (2003).
   PubMed Web of Science ®Google Scholar
• Chu I, Arnaout A, Loiseau S et al. Src promotes estrogen-dependent estrogen receptor α proteolysis in human breast cancer. J. Clin. Invest.117(8), 2205–2215 (2007).
   PubMedGoogle Scholar
• Daniel AR, Knutson TP, Lange CA. Signaling inputs to progesterone receptor gene regulation and promoter selectivity. Mol. Cell Endocrinol.308(1–2), 47–52 (2009).
   PubMed Web of Science ®Google Scholar
• Levin ER. Bidirectional signaling between the estrogen receptor and the epidermal growth factor receptor. Mol. Endocrinol.17(3), 309–317 (2003).
   PubMedGoogle Scholar