Phosphorylation of progesterone receptor serine 400 mediates ligand-independent transcriptional activity in response to activation of cyclin-dependent protein kinase 2

Molecular and Cellular Biology

Volumn 24, Issue 24, 2004, Pages 10542-10557

  Pierson Mullany, Lisa K ^a   Lange, Carol A ^a,b,c  

^a UNIVERSITY OF MINNESOTA   (United States)

^b UNIVERSITY OF MINNESOTA MEDICAL SCHOOL   (United States)

^c UNIVERSITY OF MINNESOTA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ALANINE; ANTIBODY; CYCLIN DEPENDENT KINASE 2; GESTAGEN; LIGAND; MITOGENIC AGENT; MUTANT PROTEIN; PROGESTERONE RECEPTOR; PROTEIN P27; RNA; SERINE;

AMINO ACID SUBSTITUTION; ARTICLE; BREAST CANCER; BREAST CANCER CELL; CANCER CELL CULTURE; CELL CYCLE; CELL NUCLEUS; EMBRYO CELL; EMBRYONIC FIBROBLAST; ENZYME ACTIVATION; ENZYME ACTIVITY; FIBROBLAST; GENE OVEREXPRESSION; GENETIC TRANSCRIPTION; HUMAN; HUMAN CELL; KNOCKOUT GENE; PRIORITY JOURNAL; PROTEIN LOCALIZATION; PROTEIN PHOSPHORYLATION; RECEPTOR DOWN REGULATION; RNA INTERFERENCE;

ALANINE; AMINO ACID SUBSTITUTION; ANIMALS; BLOTTING, WESTERN; BREAST NEOPLASMS; CDC2-CDC28 KINASES; CELL CYCLE PROTEINS; CELL LINE, TUMOR; CELLS, CULTURED; CYCLIN E; CYCLIN-DEPENDENT KINASE 2; CYCLIN-DEPENDENT KINASE INHIBITOR P27; DOWN-REGULATION; EMBRYO; ENZYME ACTIVATION; FIBROBLASTS; GENE DELETION; HELA CELLS; HUMANS; LIGANDS; MICE; MITOGENS; PHOSPHORYLATION; PROGESTINS; PROTEIN ISOFORMS; RECEPTORS, PROGESTERONE; RNA INTERFERENCE; SERINE; TRANSCRIPTION, GENETIC; TUMOR SUPPRESSOR PROTEINS;

EID: 10044257416     PISSN: 02707306     EISSN: None     Source Type: Journal    
DOI: 10.1128/MCB.24.24.10542-10557.2004     Document Type: Article

References (100)

1. Alkarain, A., R. Jordan, and J. Slingerland. 2004. p27 deregulation in breast cancer: prognostic significance and implications for therapy. J. Mammary Gland Biol. Neoplasia 9:67-80.
2. Ansieau, S., E. Kowenz-Leutz, R. Dechend, and A. Leutz. 1997. B-Myb, a repressed trans-activating protein. J. Mol. Med. 75:815-819.
3. Bain, D. L., M. A. Franden, J. L. McManaman, G. S. Takimoto, and K. B. Horwitz. 2000. The N-terminal region of the human progesterone A-receptor. Structural analysis and the influence of the DNA binding domain. J. Biol. Chem. 275:7313-7320.
4. Bamberger, A. M., C. M. Bamberger, B. Gellersen, and H. M. Schulte. 1996. Modulation of AP-1 activity by the human progesterone receptor in endometrial adenocarcinoma cells. Proc. Natl. Acad. Sci. USA 93:6169-6174.
5. Bartkova, J., J. Lukas, H. Muller, D. Lutzhoft, M. Strauss, and J. Bartek. 1994. Cyclin D1 protein expression and function in human breast cancer. Int. J. Cancer 57:353-361.
6. Berthet, C., E. Aleem, V. Coppola, L. Tessarollo, and P. Kaldis. 2003. Cdk2 knockout mice are viable. Curr. Biol. 13:1775-1785.
7. Catzavelos, C., N. Bhattacharya, Y. C. Ung, J. A. Wilson, L. Roncari, C. Sandhu, P. Shaw, H. Yeger, I. Morava-Protzner, L. Kapusta, E. Franssen, K. I. Pritchard, and J. M. Slingerland. 1997. Decreased levels of the cell-cycle inhibitor p27Kip1 protein: prognostic implications in primary breast cancer. Nat. Med. 3:227-230.
8. Cesi, V., B. Tanno, R. Vitali, C. Mancini, M. L. Giuffrida, B. Calabretta, and G. Raschella. 2002. Cyclin D1-dependent regulation of B-myb activity in early stages of neuroblastoma differentiation. Cell Death Differ. 9:1232-1239.
9. Chen, Z., V. B. Indjeian, M. McManus, L. Wang, and B. D. Dynlacht. 2002. CP110, a cell cycle-dependent CDK substrate, regulates centrosome duplication in human cells. Dev. Cell 3:339-350.
10. Chlebowski, R. T., S. L. Hendrix, R. D. Langer, M. L. Stefanick, M. Gass, D. Lane, R. J. Rodabough, M. A. Gilligan, M. G. Cyr, C. A. Thomson, J. Khandekar, H. Petrovitch, and A. McTiernan. 2003. Influence of estrogen plus progestin on breast cancer and mammography in healthy postmenopausal women: the Women's Health Initiative randomized trial. JAMA 289:3243-3253.
11. Clarke, C. L., and R. L. Sutherland. 1990. Progestin regulation of cellular proliferation. Endocr. Rev. 11:266-301.
12. Coats, S., P. Whyte, M. L. Fero, S. Lacy, G. Chung, E. Randel, E. Firpo, and J. M. Roberts. 1999. A new pathway for mitogen-dependent cdk2 regulation uncovered in p27(Kip1)-deficient cells. Curr. Biol. 9:163-173.
13. Davis, S. T., B. G. Benson, H. N. Bramson, D. E. Chapman, S. H. Dickerson, K. M. Dold, D. J. Eberwein, M. Edelstein, S. V. Frye, R. T. Gampe, Jr., R. J. Griffin, P. A. Harris, A. M. Hassell, W. D. Holmes, R. N. Hunter, V. B. Knick, K. Lackey, B. Lovejoy, M. J. Luzzio, D. Murray, P. Parker, W. J. Rocque, L. Shewchuk, J. M. Veal, D. H. Walker, and L. F. Kuyper. 2001. Prevention of chemotherapy-induced alopecia in rats by CDK inhibitors. Science 291:134-137.
14. Davison, E. A., C. S. Lee, M. J. Naylor, S. R. Oakes, R. L. Sutherland, L. Hennighausen, C. J. Ormandy, and E. A. Musgrove. 2003. The cyclin-dependent kinase inhibitor p27 (Kip1) regulates both DNA synthesis and apoptosis in mammary epithelium but is not required for its functional development during pregnancy. Mol. Endocrinol. 17:2436-2447.
15. Doisneau-Sixou, S. F., C. M. Sergio, J. S. Carroll, R. Hui, E. A. Musgrove, and R. L. Sutherland. 2003. Estrogen and antiestrogen regulation of cell cycle progression in breast cancer cells. Endocr. Relat. Cancer 10:179-186.
16. Fantl, V., G. Stamp, A. Andrews, I. Rosewell, and C. Dickson. 1995. Mice lacking cyclin D1 are small and show defects in eye and mammary gland development. Genes Dev. 9:2364-2372.
17. Felzien, L. K., S. Farrell, J. C. Betts, R. Mosavin, and G. J. Nabel. 1999. Specificity of cyclin E-Cdk2, TFIIB, and E1A interactions with a common domain of the p300 coactivator. Mol. Cell. Biol. 19:4241-4246.
18. Fisk, H. A., and M. Winey. 2001. The mouse Mpslp-like kinase regulates centrosome duplication. Cell 106:95-104.
19. Font de Mora, J., and M. Brown. 2000. AIB1 is a conduit for kinase-mediated growth factor signaling to the estrogen receptor. Mol. Cell. Biol. 20:5041-5047.
20. Geng, Y., Q. Yu, E. Sicinska, M. Das, J. E. Schneider, S. Bhattacharya, W. M. Rideout, R. T. Bronson, H. Gardner, and P. Sicinski. 2003. Cyclin E ablation in the mouse. Cell 114:431-443.
21. Gillett, C., V. Fantl, R. Smith, C. Fisher, J. Bartek, C. Dickson, D. Barnes, and G. Peters. 1994. Amplification and overexpression of cyclin D1 in breast cancer detected by immunohislochemical staining. Cancer Res. 54:1812-1817.
22. Gray, S. 2003. Breast cancer and hormone-replacement therapy: the Million Women Study. Lancet 362:1332.
23. Groshong, S. D., G. I. Owen, B. Grimison, I. E. Schauer, M. C. Todd, T. A. Langan, R. A. Sclafani, C. A. Lange, and K. B. Horwitz. 1997. Biphasic regulation of breast cancer cell growth by progesterone: role of the cyclin-dependent kinase inhibitors, p21 and p27(Kip1). Mol. Endocrinol. 11:1593-1607.
24. Guiochon-Mantel, A., P. Lescop, S. Christin-Maitre, H. Loosfelt, M. Perrot-Applanat, and E. Milgrom. 1991. Nucleocytoplasmic shuttling of the progesterone receptor. EMBO J. 10:3851-3859.
25. Hissom, J. R., and M. R. Moore. 1987. Progestin effects on growth in the human breast cancer cell line T-47D - possible therapeutic implications. Biochem. Biophys. Res. Commun. 145:706-711.
26. Horstmann, S., S. Ferrari, and K. H. Klempnauer. 2000. Regulation of B-Myb activity by cyclin D1. Oncogene 19:298-306.
27. Horwitz, K. B., M. B. Mockus, and B. A. Lessey. 1982. Variant T47D human breast cancer cells with high progesterone-receptor levels despite estrogen and antiestrogen resistance. Cell 28:633-642.
28. Hunter, T., and J. Pines. 1994. Cyclins and cancer. II: cyclin D and CDK inhibitors come of age. Cell 79:573-582.
29. Ismail, P. M., P. Amato, S. M. Soyal, F. J. DeMayo, O. M. Conneely, B. W. O'Malley, and J. P. Lydon. 2003. Progesterone involvement in breast development and tumorigenesis - as revealed by progesterone receptor "knockout" and "knockin" mouse models. Steroids 68:779-787.
30. Jackman, M., Y. Kubota, N. den Elzen, A. Hagting, and J. Pines. 2002. Cyclin A- and cyclin E-Cdk complexes shuttle between the nucleus and the cytoplasm. Mol. Biol. Cell 13:1030-1045.
31. Jans, D. A., and S. Hubner. 1996. Regulation of protein transport to the nucleus: central role of phosphorylation. Physiol. Rev. 76:651-685.
32. Jiang, W., G. Jimenez, N. J. Wells, T. J. Hope, G. M. Wahl, T. Hunter, and R. Fukunaga. 1998. PRC1: a human mitotic spindle-associated CDK substrate protein required for cytokinesis. Mol. Cell 2:877-885.
33. Johnson, T. K., R. E. Schweppe, J. Septer, and R. E. Lewis. 1999. Phosphorylation of B-Myb regulates its transactivation potential and DNA binding. J. Biol. Chem. 274:36741-36749.
34. Keyomarsi, K., N. O'Leary, G. Molnar, E. Lees, H. J. Fingert, and A. B. Pardee. 1994. Cyclin E, a potential prognostic marker for breast cancer. Cancer Res. 54:380-385.
35. Kim, T. Y., and W. G. Kaelin, Jr. 2001. Differential control of transcription by DNA-bound cyclins. Mol. Biol. Cell 12:2207-2217.
36. Knotts, T. A., R. S. Orkiszewski, R. G. Cook, D. P. Edwards, and N. L. Weigel. 2001. Identification of a phosphorylation site in the hinge region of the human progesterone receptor and additional amino-terminal phosphorylation sites. J. Biol. Chem. 276:8475-8483.
37. Krek, W., M. E. Ewen, S. Shirodkar, Z. Arany, W. G. Kaelin, Jr., and D. M. Livingston. 1994. Negative regulation of the growth-promoting transcription factor E2F-1 by a stably bound cyclin A-dependent protein kinase. Cell 78:161-172.
38. Krek, W., and E. A. Nigg. 1991. Mutations of p34cdc2 phosphorylation sites induce premature mitotic events in HeLa cells: evidence for a double block to p34cdc2 kinase activation in vertebrates. EMBO J. 10:3331-3341.
39. Labriola, L., M. Salatino, C. J. Proietti, A. Pecci, O. A. Coso, A. R. Kornblihtt, E. H. Charreau, and P. V. Elizalde. 2003. Heregulin induces transcriptional activation of the progesterone receptor by a mechanism that requires functional ErbB-2 and mitogen-activated protein kinase activation in breast cancer cells. Mol. Cell. Biol. 23:1095-1111.
40. Lane, S., P. Farlie, and R. Watson. 1997. B-Myb function can be markedly enhanced by cyclin A-dependent kinase and protein truncation. Oncogene 14:2445-2453.
41. Lange, C. A. 2004. Making sense of cross-talk between steroid hormone receptors and intracellular signaling pathways: who will have the last word? Mol. Endocrinol. 18:269-278.
42. Lange, C. A., J. K. Richer, T. Shen, and K. B. Horwitz. 1998. Convergence of progesterone and epidermal growth factor signaling in breast cancer. Potentiation of mitogen-activated protein kinase pathways. J. Biol. Chem. 273:31308-31316.
43. Lange, C. A., T. Shen, and K. B. Horwitz. 2000. Phosphorylation of human progesterone receptors at serine-294 by mitogen-activated protein kinase signals their degradation by the 26S proteasome. Proc. Natl. Acad. Sci. USA 97:1032-1037.
44. Ma, T., B. A. Van Tine, Y. Wei, M. D. Garrett, D. Nelson, P. D. Adams, J. Wang, J. Qin, L. T. Chow, and J. W. Harper. 2000. Cell cycle-regulated phosphorylation of p220(NPAT) by cyclin E/Cdk2 in Cajal bodies promotes histone gene transcription. Genes Dev. 14:2298-2313.
45. Kip1 inhibition of GRB2-SOS formation can regulate Ras activation. Mol. Cell. Biol. 23:3735-3752.
46. Moore, M. R. 2004. A rationale for inhibiting progesterone-related pathways to combat breast cancer. Curr. Cancer Drug Targets 4:183-189.
47. Moore, M. R., J. L. Conover, and K. M. Franks. 2000. Progestin effects on long-term growth, death, and Bcl-xL in breast cancer cells. Biochem. Biophys. Res. Commun. 277:650-654.
48. Muller-Tidow, C., W. Wang, G. E. Idos, S. Diederichs, R. Yang, C. Readhead, W. E. Berdel, H. Serve, M. Saville, R. Watson, and H. P. Koeffler. 2001. Cyclin Al directly interacts with B-myb and cyclin A1/cdk2 phosphorylate B-myb at functionally important serine and threonine residues: tissue-specific regulation of B-myb function. Blood 97:2091-2097.
49. Muraoka, R. S., A. E. Lenferink, J. Simpson, D. M. Brantley, L. R. Roebuck, F. M. Yakes, and C. L. Arteaga. 2001. Cyclin-dependent kinase inhibitor p27(Kip1) is required for mouse mammary gland morphogenesis and function. J. Cell Biol. 153:917-932.
50. Murphy, C. S., J. J. Pink, and V. C. Jordan. 1990. Characterization of a receptor-negative, hormone-nonresponsive clone derived from a T47D human breast cancer cell line kept under estrogen-free conditions. Cancer Res. 50:7285-7292.
51. Murphy, L., T. Cherlet, A. Lewis, Y. Banu, and P. Watson. 2003. New insights into estrogen receptor function in human breast cancer. Ann. Med. 35:614-631.
52. 1 to complete the cell cycle. Proc. Natl. Acad. Sci. USA 91:8022-8026.
53. Musgrove, E. A., C. S. Lee, and R. L. Sutherland. 1991. Progestins both stimulate and inhibit breast cancer cell cycle progression while increasing expression of transforming growth factor alpha, epidermal growth factor receptor, c-fos, and c-myc genes. Mol. Cell. Biol. 11:5032-5043.
54. Nandi, S., R. C. Guzman, and J. Yang. 1995. Hormones and mammary carcinogenesis in mice, rats, and humans: a unifying hypothesis. Proc. Natl. Acad. Sci. USA 92:3650-3657.
55. 2 phase of the cell cycle. Progr. Abstr. Endocr. Soc. 85th Annu. Meet. Endocr. Soc. Endo 2003, abstr. OR5-2, p. 65. The Endocrine Society, Chevy Chase, Md.
56. Nardulli, A. M., and B. S. Katzenellenbogen. 1988. Progesterone receptor regulation in T47D human breast cancer cells: analysis by density labeling of progesterone receptor synthesis and degradation and their modulation by progestin. Endocrinology 122:1532-1540.
57. Norbury, C., M. MacFarlane, H. Fearnhead, and G. M. Cohen. 1994. Cdc2 activation is not required for thymocyte apoptosis. Biochem. Biophys. Res. Commun. 202:1400-1406.
58. Okuda, M., H. F. Horn, P. Tarapore, Y. Tokuyama, A. G. Smulian, P. K. Chan, E. S. Knudsen, I. A. Hofmann, J. D. Snyder, K. E. Bove, and K. Fukasawa. 2000. Nucleophosmin/B23 is a target of CDK2/cyclin E in centrosome duplication. Cell 103:127-140.
59. Ortega, S., I. Prieto, J. Odajima, A. Martin, P. Dubus, R. Sotillo, J. L. Barbero, M. Malumbres, and M. Barbacid. 2003. Cyclin-dependent kinase 2 is essential for meiosis but not for mitotic cell division in mice. Nat. Genet. 35:25-31.
60. Parisi, T., A. R. Beck, N. Rougier, T. McNeil, L. Lucian, Z. Werb, and B. Amati. 2003. Cyclins E1 and E2 are required for endoreplication in placental trophoblast giant cells. EMBO J. 22:4794-4803.
61. Perkins, N. D., L. K. Felzien, J. C. Betts, K. Leung, D. H. Beach, and G. J. Nabel. 1997. Regulation of NF-κB by cyclin-dependent kinases associated with the p300 coactivator. Science 275:523-527.
62. Petersen, B. O., J. Lukas, C. S. Sorensen, J. Bartek, and K. Helin. 1999. Phosphorylation of mammalian CDC6 by cyclin A/CDK2 regulates its subcellular localization. EMBO J. 18:396-410.
63. Porter, P. L., K. E. Malone, P. J. Heagerty, G. M. Alexander, L. A. Gatti, E. J. Firpo, J. R. Daling, and J. M. Roberts. 1997. Expression of cell-cycle regulators p27Kip1 and cyclin E, alone and in combination, correlate with survival in young breast cancer patients. Nat. Med. 3:222-225.
64. Pratt, W. B., and D. O. Toft. 2003. Regulation of signaling protein function and trafficking by the hsp90/hsp70-based chaperone machinery. Exp. Biol. Med. 228:111-133.
65. Qiu, M., and C. A. Lange. 2003. MAP kinases couple multiple functions of human progesterone receptors: degradation, transcriptional synergy, and nuclear association. J. Steroid Biochem. Mol. Biol. 85:147-157.
66. Qiu, M., A. Olsen, E. Faivre, K. B. Horwitz, and C. A. Lange. 2003. Mitogen activated protein kinase regulates nuclear association of human progesterone receptors. Mol. Endocrinol. 17:628-642.
67. Reid, G., M. R. Hubner, R. Metivier, H. Brand, S. Denger, D. Manu, J. Beaudouin, J. Ellenberg, and F. Gannon. 2003. Cyclic, proteasome-mediated turnover of unliganded and liganded ERα on responsive promoters is an integral feature of estrogen signaling. Mol. Cell 11:695-707.
68. Robinson, C., Y. Light, R. Groves, D. Mann, R. Marias, and R. Watson. 1996. Cell-cycle regulation of B-Myb protein expression: specific phosphorylation during the S phase of the cell cycle. Oncogene 12:1855-1864.
69. Said, T. K., R. C. Moraes, U. Singh, F. S. Kittrell, and D. Medina. 2001. Cyclin-dependent kinase (cdk) inhibitors/cdk4/cdk2 complexes in early stages of mouse mammary preneoplasia. Cell Growth Differ. 12:285-295.
70. Sala, A., M. Kundu, I. Casella, A. Engelhard, B. Calabretta, L. Grasso, M. G. Paggi, A. Giordano, R. J. Watson, K. Khalili, and C. Peschle. 1997. Activation of human B-MYB by cyclins. Proc. Natl. Acad. Sci. USA 94:532-536.
71. Salghetti, S. E., A. A. Caudy, J. G. Chenoweth, and W. P. Tansey. 2001. Regulation of transcriptional activation domain function by ubiquitin. Science 293:1651-1653.
72. Salghetti, S. E., S. Y. Kim, and W. P. Tansey. 1999. Destruction of Myc by ubiquitin-mediated proteolysis: cancer-associated and transforming mutations stabilize Myc. EMBO J. 18:717-726.
73. Salghetti, S. E., M. Muratani, H. Wijnen, B. Futcher, and W. P. Tansey. 2000. Functional overlap of sequences that activate transcription and signal ubiquitin-mediated proteolysis. Proc. Natl. Acad. Sci. USA 97:3118-3123.
74. Santen, R. J., R. X. Song, R. McPherson, R. Kumar, L. Adam, M. H. Jeng, and W. Yue. 2002. The role of mitogen-activated protein (MAP) kinase in breast cancer. J. Steroid Biochem. Mol. Biol. 80:239-256.
75. Santilli, G., M. N. Cervellera, T. K. Johnson, R. E. Lewis, S. Iacobelli, and A. Sala. 2001. PARP co-activates B-MYB through enhanced phosphorylation at cyclin/cdk2 sites. Oncogene 20:8167-8174.
76. Sartorius, C. A., S. D. Groshong, L. A. Miller, R. L. Powell, L. Tung, G. S. Takimoto, and K. B. Horwitz. 1994. New T47D breast cancer cell lines for the independent study of progesterone B- and A-receptors: only antiprogestin- occupied B-receptors are switched to transcriptional agonists by cAMP. Cancer Res. 54:3868-3877.
77. Scott, K. A., and R. A. Walker. 1997. Lack of cyclin E immunoreactivity in non-malignant breast and association with proliferation in breast cancer. Br. J. Cancer 76:1288-1292.
78. Shen, T., K. B. Horwitz, and C. A. Lange. 2001. 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. 21:6122-6131.
79. Sheridan, P. L., R. M. Evans, and K. B. Horwitz. 1989. Phosphotryptic peptide analysis of human progesterone receptor. New phosphorylated sites formed in nuclei after hormone treatment. J. Biol. Chem. 264:6520-6528.
80. Sicinski, P., J. L. Donaher, S. B. Parker, T. Li, A. Fazeli, H. Gardner, S. Z. Haslam, R. T. Bronson, S. J. Elledge, and R. A. Weinberg. 1995. Cyclin D1 provides a link between development and oncogenesis in the retina and breast. Cell 82:621-630.
81. Sicinski, P., and R. A. Weinberg. 1997. A specific role for cyclin D1 in mammary gland development. J. Mammary Gland Biol. Neoplasia 2:335-342.
82. Sutherland, R. L., and E. A. Musgrove. 2002. Cyclin D1 and mammary carcinoma: new insights from transgenic mouse models. Breast Cancer Res. 4:14-17.
83. Sutherland, R. L., O. W. J. Prall, C. K. W. Watts, and E. A. Musgrove. 1998. Estrogen and progestin regulation of cell cycle progression. J. Mammary Gland Biol. Neoplasia 3:63-72.
84. Sweeney, K. J., B. Sarcevic, R. L. Sutherland, and E. A. Musgrove. 1997. Cyclin D2 activates Cdk2 in preference to Cdk4 in human breast epithelial cells. Oncogene 14:1329-1340.
85. Takimoto, G. S., D. M. Tasset, A. C. Eppert, and K. B. Horwitz. 1992. Hormone-induced progesterone receptor phosphorylation consists of sequential DNA-independent and DNA-dependent stages: analysis with zinc finger mutants and the progesterone antagonist ZK98299. Proc. Natl. Acad. Sci. USA 89:3050-3054.
86. Tan, M., J. Yao, and D. Yu. 1997. Overexpression of the c-erbB-2 gene enhanced intrinsic metastasis potential in human breast cancer cells without increasing their transformation abilities. Cancer Res. 57:1199-1205.
87. Tan, P., B. Cady, M. Wanner, P. Worland, B. Cukor, C. Magi-Galluzzi Galluzzl, P. Lavin, G. Draetta, M. Pagano, and M. Loda. 1997. The cell cycle inhibitor p27 is an independent prognostic marker in small (Tla,b) invasive breast carcinomas. Cancer Res. 57:1259-1263.
88. Tokuyama, Y., H. F. Horn, K. Kawamura, P. Tarapore, and K. Fukasawa. 2001. Specific phosphorylation of nucleophosmin on Thr(199) by cyclin-dependent kinase 2-cyclin E and its role in centrosome duplication. J. Biol. Chem. 276:21529-21537.
89. Topper, Y. J., and C. S. Freeman. 1980. Multiple hormone interactions in the developmental biology of the mammary gland. Physiol. Rev. 60:1049-1106.
90. Trowbridge, J. M., I. Rogatsky, and M. J. Garabedian. 1997. Regulation of estrogen receptor transcriptional enhancement by the cyclin A/Cdk2 complex. Proc. Natl. Acad. Sci. USA 94:10132-10137.
91. Vlach, J., S. Hennecke, and B. Amati. 1997. Phosphorylation-dependent degradation of the cyclin-dependent kinase inhibitor p27. EMBO J. 16:5334-5344.
92. Wang, Z., and M. J. Garabedian. 2003. Modulation of glucocorticoid receptor transcriptional activation, phosphorylation, and growth inhibition by p27Kip1. J. Biol. Chem. 278:50897-50901.
93. Weigel, N. L. 1996. Steroid hormone receptors and their regulation by phosphorylation. Biochem. J. 319:657-667.
94. Xu, M., K. A. Sheppard, C. Y. Peng, A. S. Yee, and H. Piwnica-Worms. 1994. Cyclin A/CDK2 binds directly to E2F-1 and inhibits the DNA-binding activity of E2F-1/DP-1 by phosphorylation. Mol. Cell. Biol. 14:8420-8431.
95. Zhang, Y., C. A. Beck, A. Poletti, J. P. Clement, P. Prendergast, T. T. Yip, T. W. Hutchens, D. P. Edwards, and N. L. Weigel. 1997. Phosphorylation of human progesterone receptor by cyclin-dependent kinase 2 on three sites that are authentic basal phosphorylation sites in vivo. Mol. Endocrinol. 11:823-832.
96. Zhang, Y., C. A. Beck, A. Poletti, D. P. Edwards, and N. L. Weigel. 1995. Identification of a group of Ser-Pro motif hormone-inducible phosphorylation sites in the human progesterone receptor. Mol. Endocrinol. 9:1029-1040.
97. Zhang, Y., C. A. Beck, A. Poletti, D. P. Edwards, and N. L. Weigel. 1994. Identification of phosphorylation sites unique to the B form of human progesterone receptor. In vitro phosphorylation by casein kinase II. J. Biol. Chem. 269:31034-31040.
98. Zhao, J., B. K. Kennedy, B. D. Lawrence, D. A. Barbie, A. G. Matera, J. A. Fletcher, and E. Harlow. 2000. NPAT links cyclin E-Cdk2 to the regulation of replication-dependent histone gene transcription. Genes Dev. 14:2283-2297.
99. Ziebold, U., O. Bartsch, R. Marais, S. Ferrari, and K. H. Klempnauer. 1997. Phosphorylation and activation of B-Myb by cyclin A-Cdk2. Curr. Biol. 7:253-260.
100. Zwijsen, R. M., E. Wientjens, R. Klompmaker, J. van der Sman, R. Bernards, and R. J. Michalides. 1997. CDK-independent activation of estrogen receptor by cyclin D1. Cell 88:405-415.