42
Views
120
CrossRef citations to date
0
Altmetric
Cell Growth and Development

Progesterone Inhibits Estrogen-Induced Cyclin D1 and cdk4 Nuclear Translocation, Cyclin E- and Cyclin A-cdk2 Kinase Activation, and Cell Proliferation in Uterine Epithelial Cells in Mice

&
Pages 2251-2264 | Received 07 Jul 1998, Accepted 24 Nov 1998, Published online: 27 Mar 2023

REFERENCES

  • Altucci, L., R. Addeo, L. Cicatiello, S. Dauvois, M. G. Parker, M. Truss, M. Beato, V. Sica, F. Bresciani, and J. Weisz 1996. 17β-Estradiol induces cyclin D1 gene transcription, p36D1-p34cdk4 complex activation and p105Rb phosphorylation during mitogenic stimulation of G1-arrested human breast cancer cells. Oncogene 12:2315–2324.
  • Altucci, L., R. Addeo, L. Cicatiello, D. Germano, C. Pacilio, T. Battista, M. Cancemi, V. B. Petrizzi, F. Bresciani, and J. Weisz 1997. Estrogen induces early and timed activation of cyclin-dependent kinases 4, 5, and 6 and increases cyclin messenger ribonucleic acid expression in rat uterus. Endocrinology 138:978–984.
  • Baldin, V., J. Lukas, M. Marcote, M. Pagano, and J. Draetta 1993. Cyclin D1 is a nuclear protein required for cell cycle progression in G1. Genes Dev. 7:812–821.
  • Castles, C. G., S. A. W. Fuqua 1996. Alterations within the estrogen receptor in breast cancer, p. 81–105. In J. R. Pasqualini, B. S. Katzenellenbogen (ed.), Hormonal-dependent cancer. Marcel Dekker, Inc., New York, N.Y.
  • Cheng, M., J. A. Diehl, M. Fero, P. Olivier, E. Randel, J. M. Roberts, C. J. Sherr, M. F. Roussel 1998. Cdk inhibitors p27Kip1 and p21Cip1 are required for assembly of active cyclin D-dependent kinases in mouse fibroblasts, p. 39 Fourteenth Annual Meeting on Oncogenes. (Abstract.).
  • Cheng, S. V. Y., B. S. MacDonald, B. F. Clark, and J. Pollard 1985. Cell growth and cell proliferation may be dissociated in the mouse uterine luminal epithelium treated with female sex steroids. Exp. Cell Res. 160:459–470.
  • Cheng, S. V. Y., and J. Pollard 1986. C-rasH and ornithine decarboxylase are induced by oestradiol-17β in the mouse uterine luminal epithelium independently of the proliferative status of the cell. FEBS Lett. 196:309–314.
  • Clark, B. F. 1980. Absence of oestradiol-17 beta dehydrogenase from the progesterone-dominated mouse uterus. J. Endocrinol. 85:155–159.
  • Cohen, C. J., H. W. Bruckner, and J. Deppe 1984. Multidrug treatment of advanced and recurrent endometrial carcinoma: a gynecologic oncology group study. Obstet. Gynecol. 63:719–726.
  • Cooke, P. S., D. L. Buchanan, T. Kurita, D. B. Lubahn, G. R. Cunha 1998. Stromal-epithelial cell communication in the female reproductive tract, p. 491–506. In F. W. Bazer (ed.), Endocrinology of pregnancy. Humana Press, Totowa, N. J.
  • Cullingford, T. E., and J. Pollard 1988. RU 486 completely inhibits the action of progesterone on cell proliferation in the mouse uterus. J. Reprod. Fertil. 83:909–914.
  • Cullingford, T. E., J. W. Pollard 1994. Growth factors as mediators of sex-steroid hormone action in the uterus during the pre-implantation period, p. 13–30. In S. A. Khan, G. M. Stancel (ed.), Protooncogenes and growth factors in steroid hormone-induced growth differentiation. CRC Press, Inc., Boca Raton, Fla.
  • Cullingford, T. E., and J. W. Pollard. Unpublished observations.
  • Das, R. M., and J. Martin 1973. Progesterone inhibition of mouse uterine epithelial proliferation. J. Endocrinol. 59:205–206.
  • Diehl, J. A., and J. Sherr 1997. A dominant-negative cyclin D1 mutant prevents nuclear import of cyclin-dependent kinase 4 (CDK4) and its phosphorylation by CDK-activating kinase. Mol. Cell. Biol. 17:7362–7374.
  • Diehl, J. A., F. Zindy, and J. Sherr 1997. Inhibition of cyclin D1 phosphorylation on threonine-286 prevents its rapid degradation via the ubiquitin-proteasone pathway. Genes Dev. 11:957–972.
  • Fagg, B., L. Martin, L. A. Rogers, B. F. Clark, and J. Quarmby 1979. A simple method for preparing pure samples of uterine epithelial cells. J. Reprod. Fertil. 57:335–345.
  • Fang, F., G. Orend, N. Watanabe, T. Hunter, and J. Ruoslahti 1996. Dependence of cyclin E-CDK2 kinase activity on cell anchorage. Science 271:499–502.
  • Fantl, V., G. Stamp, A. Andrews, I. Rosewell, and J. Dickson 1995. Mice lacking cyclin D1 are small and show defects in eye and mammary gland development. Genes Dev. 9:2364–2372.
  • Fero, M. L., M. Rivkin, M. Tasch, P. Porter, C. E. Carow, E. Firpo, K. Polyak, L.-H. Tsai, V. Broudy, R. M. Perlmutter, K. Kaushansky, and J. Roberts 1996. A syndrome of multiorgan hyperplasia with features of gigantism, tumorigenesis, and female sterility in p27Kip1-deficient mice. Cell 85:733–744.
  • Finn, C. A., and J. Martin 1970. The role of the oestrogen secreted before oestrus in the preparation of the uterus for implantation in the mouse. J. Endocrinol. 47:431–438.
  • Finn, C. A., D. G. Porter 1975. Handbooks in reproductive biology, vol. 1. The uterus. Elek Science, London, United Kingdom.
  • Galand, P., and J. de Maertelaer 1992. Models of oestrogen action: a cell kineticist’s view. Epithelial Cell Biol. 1:177–188.
  • Groshong, S. D., G. I. Owen, B. Grimison, I. E. Schauer, M. C. Todd, T. A. Langan, R. A. Sclafani, C. A. Lange, and J. Horwitz 1997. Biphasic regulation of breast cancer cell growth by progesterone: role of the cyclin-dependent kinase inhibitors, p21 and p27Kip1. Mol. Endocrinol. 11:1593–1607.
  • Haslam, S. Z. 1989. The ontogeny of mouse mammary gland responsiveness to ovarian steroid hormones. Endocrinology 125:2766–2772.
  • Henderson, B. E., R. K. Ross, and J. Pike 1993. Hormonal chemoprevention of cancer in women. Science 259:633–638.
  • Hunter, T., and J. Pines 1994. Cyclins and cancer II: cyclin D and CDK inhibitors come of age. Cell 79:573–582.
  • Hyde-Dunn, J., G. E. Jones 1997. Visualization of cell replication using antibody to proliferating cell nuclear antigen, p. 341–349. In J. W. Pollard, J. M. Walker (ed.), Basic cell culture protocols. Humana Press, Totowa, N.J.
  • Iavarone, A., and J. Massagué 1997. Repression of the CDK activator Cdc25A and cell-cycle arrest by cytokine TGF-β in cells lacking the CDK inhibitor p15. Nature 387:417–422.
  • Key, T. J. A., and J. Pike 1997. The role of oestrogen and progestagens in the epidemiology and prevention of breast cancer. Eur. J. Cancer Clin. Oncol. 24:29–43.
  • Kiyokawa, H., R. D. Kineman, K. O. Manova-Todorova, V. C. Soares, E. S. Hoffman, M. Ono, D. Khanam, A. C. Hayday, L. A. Frohman, and J. Koff 1996. Enhanced growth of mice lacking the cyclin-dependent kinase inhibitor function of p27Kip1. Cell 85:721–732.
  • Koyama, H., E. W. Raines, J. M. Bornfeldt, J. M. Roberts, and J. Ross 1996. Fibrillar collagen inhibits arterial smooth muscle proliferation through regulation of Cdk2 inhibitors. Cell 87:1069–1078.
  • LaBaer, J., M. D. Garrett, L. F. Stevenson, J. M. Slingerland, C. Sandhu, H. S. Chou, A. Fattaey, and J. Harlow 1997. New functional activities for the p21 family of CDK inhibitors. Genes Dev. 11:847–862.
  • Lee, W.-S., J. A. Harder, M. Yoshizumi, M.-E. Lee, and J. Haber 1997. Progesterone inhibits arterial smooth muscle cell proliferation. Nat. Med. 3:1005–1008.
  • Lubahn, D. B., J. S. Moyer, T. S. Golding, J. F. Couse, K. S. Korach, and J. Smithies 1993. Alteration of reproductive function but not prenatal sexual development after insertional disruption of the mouse estrogen receptor gene. Proc. Natl. Acad. Sci. USA 90:11162–11166.
  • Lydon, J. P., F. J. DeMayo, C. Funk, S. K. Mani, A. R. Hughes, C. A. Montgomery, G. Shyamala, O. M. Conneely, and J. O’Malley 1995. Mice lacking progesterone receptor exhibit pleiotropic reproductive abnormalities. Genes Dev. 9:2266–2278.
  • Martin, L., R. M. Das, and J. Finn 1973. The inhibition by progesterone of uterine epithelial proliferation in the mouse. J. Endocrinol. 57:549–554.
  • Martin, L., and J. Finn 1970. Interactions of oestradiol and progestins in the mouse uterus. J. Endocrinol. 48:109–115.
  • Martin, L., C. A. Finn 1971. Oestrogen-gestagen interactions on mitosis in target tissues, p. 172–188. In P. O. Hubinont et al. (ed.), Basic actions of sex steroids on target organs. S. Karger, Basel, Switzerland.
  • Martin, L., C. A. Finn, and J. Trinder 1973. DNA synthesis in the endometrium of progesterone-treated mice. J. Endocrinol. 56:303–307.
  • Martin, L., C. A. Finn, and J. Trinder 1973. Hypertrophy and hyperplasia in the mouse uterus after oestrogen treatment: an autoradiographic study. J. Endocrinol. 56:133–144.
  • Martin, L., J. W. Pollard, and J. Fagg 1976. Oestriol, oestradiol-17β and the proliferation and death of uterine cells. J. Endocrinol. 69:103–115.
  • Massagué, J., and J. Polyak 1995. Mammalian antiproliferative signals and their targets. Curr. Opin. Genet. Dev. 5:91–96.
  • Matsushime, H., M. F. Roussel, R. A. Ashmun, and J. Sherr 1991. Colony-stimulating factor 1 regulates novel cyclins during the G1 phase of the cell cycle. Cell 65:701–713.
  • Mittnacht, S., J. A. Lees, D. Desai, E. Harlow, D. O. Morgan, and J. Weinberg 1994. Distinct sub-populations of the retinoblastoma protein show a distinct pattern of phosphorylation. EMBO J. 13:118–127.
  • Mittnacht, S., and J. Weinberg 1991. G1/S phosphorylation of the retinoblastoma protein is associated with an altered affinity for the nuclear compartment. Cell 65:381–393.
  • Morgan, C., J. W. Pollard, and J. Stanley 1987. Isolation and characterization of a cloned growth factor dependent macrophage cell line, BAC-1.2F5. J. Cell. Physiol. 130:420–427.
  • Morgan, D. O. 1995. Principles of CDK regulation. Nature 374:131–134.
  • Musgrove, E. A., C. S. L. Lee, M. F. Buckley, and J. Sutherland 1994. Cyclin D1 induction in breast cancer cells shortens G1 and is sufficient for cells arrested in G1 to complete the cell cycle. Proc. Natl. Acad. Sci. USA 91:8022–8026.
  • Musgrove, E. A., A. Swarbrick, C. S. L. Lee, A. L. Cornish, and J. Sutherland 1998. Mechanisms of cyclin-dependent kinase inactivation by progestins. Mol. Cell. Biol. 18:1812–1825.
  • Nakayama, K.-I., N. Ishida, M. Shirane, A. Inomata, T. Inoue, N. Shishido, I. Horii, and J. Loh 1996. Mice lacking p27Kip1 display increased body size, multiple organ hyperplasia, retinal dysplasia, and pituitary tumors. Cell 85:707–720.
  • Nephew, K. P., G. A. Peters, and J. Khan 1995. Cellular localization of estradiol-induced c-fos messenger ribonucleic acid in the rat uterus: c-fos expression and uterine cell proliferation do not correlate strictly. Endocrinology 136:3007–3015.
  • Neuman, E., M. H. Ladha, N. Lin, T. M. Upton, S. J. Miller, J. DiRenzo, R. G. Pestell, P. W. Hinds, S. F. Dowdy, M. Brown, and J. Ewen 1997. Cyclin D1 stimulation of estrogen receptor transcriptional activity independent of cdk4. Mol. Cell. Biol. 17:5338–5347.
  • Planas-Silva, M., and J. Weinberg 1997. Estrogen-dependent cyclin E-cdk2 activation through p21 redistribution. Mol. Cell. Biol. 17:4059–4069.
  • Pollard, J. W., J. Pacy, S. V. Y. Cheng, and J. Jordan 1987. Estrogens and cell death in the mouse uterine luminal epithelium. Cell Tissue Res. 249:533–540.
  • Prall, O. W. J., B. Sarcevic, E. A. Musgrove, C. K. W. Watts, and J. Sutherland 1997. Estrogen-induced activation of Cdk4 and Cdk2 during G1-S phase progression is accompanied by increased cyclin D1 expression and decreased cyclin-dependent kinase inhibition association. J. Biol. Chem. 272:10882–10894.
  • Quarmby, V. E., and J. Korach 1984. The influence of 17β-estradiol on patterns of cell division in the uterus. Endocrinology 114:694–702.
  • Quarmby, V. E., and J. Martin 1982. Effects of progesterone on uptake and metabolism of 17β-estradiol by mouse uterine luminal epithelium. Mol. Cell. Endocrinol. 27:317–330.
  • Quarmby, V. E., and J. Martin 1982. Qualitative effects of progesterone on estrogen binding in mouse uterine luminal epithelium. Mol. Cell. Endocrinol. 27:331–342.
  • Ravitz, M. J., and J. Wenner 1997. Cyclin-dependent kinase regulation during G1 phase and cell cycle regulation by TGF-β. Adv. Cancer Res. 71:165–207.
  • Sherr, C. J. 1994. G1 phase progression: cycling on cue. Cell 79:551–555.
  • Sherr, C. J. 1996. Cancer cell cycles. Science 274:1672–1677.
  • Sherr, C. J., and J. Roberts 1995. Inhibitors of mammalian G1 cyclin-dependent kinases. Genes Dev. 9:1149–1163.
  • Sicinski, L. P., J. L. Donaher, S. B. Parker, T. Li, A. Fazeli, H. Gardner, S. Z. Haslam, R. T. Bronson, S. J. Elledge, and J. Weinberg 1995. Cyclin D1 provides a link between development and oncogenesis in the retina and breast. Cell 82:621–630.
  • Stacey, K., B. Beasley, P. A. Wilce, and J. Martin 1991. Effects of female sex hormones on lipid metabolism in the uterine epithelium of the mouse. Int. J. Biochem. 23:371–376.
  • Stepanova, L., X. Leng, S. B. Parker, and J. Harper 1996. Mammalian p50Cdc37 is a protein kinase-targeting subunit of Hsp90 that binds and stabilizes Cdk4. Genes Dev. 10:1491–1502.
  • Terada, N., R. Yamamoto, T. Takada, T. Miyake, N. Terakawa, H. Wakimoto, H. Taniguchi, W. Li, Y. Kitamura, and J. Matsumoto 1989. Inhibitory effect of progesterone on cell death of mouse uterine epithelium. J. Steroid Biochem. 33:1091–1096.
  • Tong, W., H. Kiyokawa, T. J. Soos, M. S. Park, V. C. Soares, K. Manova, J. W. Pollard, and J. Koff 1998. The absence of p27Kip1, an inhibitor of G1 cyclin-dependent kinases, uncouples differentiation and growth arrest during the granulosa→luteal transition. Cell Growth Differ. 9:787–794.
  • Zwijsen, R. M. L., E. Wientjens, R. Klompmaker, J. van der Sman, R. Bernards, and J. Michalides 1997. CDK-independent activation of estrogen receptor by cyclin D1. Cell 88:405–415.

Reprints and Corporate Permissions

Please note: Selecting permissions does not provide access to the full text of the article, please see our help page How do I view content?

To request a reprint or corporate permissions for this article, please click on the relevant link below:

Academic Permissions

Please note: Selecting permissions does not provide access to the full text of the article, please see our help page How do I view content?

Obtain permissions instantly via Rightslink by clicking on the button below:

If you are unable to obtain permissions via Rightslink, please complete and submit this Permissions form. For more information, please visit our Permissions help page.