Estrogen inhibits ATR signaling to cell cycle checkpoints and DNA repair

Molecular Biology of the Cell

Volumn 20, Issue 14, 2009, Pages 3374-3389

  Pedram, Ali ^b   Razandi, Mahnaz ^a,b   Evinger, Albert J ^b   Lee, Eva ^b   Levin, Ellis R ^a,b,c  

^a VA LONG BEACH HEALTHCARE SYSTEM   (United States)

^b UNIVERSITY OF CALIFORNIA   (United States)

^c UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

1,3,5 TRIS(4 HYDROXYPHENYL) 4 PROPYLPYRAZOLE; 2 MORPHOLINO 8 PHENYLCHROMONE; 4 (3 CHLOROANILINO) 6,7 DIMETHOXYQUINAZOLINE; ATR PROTEIN; CELL PROTEIN; CHECKPOINT KINASE 1; CHECKPOINT KINASE RAD3; DNA; ESTRADIOL; ESTROGEN; ESTROGEN RECEPTOR; FULVESTRANT; HYDROXYUREA; PHOSPHORUS 32; PROTEIN P53; SMALL INTERFERING RNA;

ANIMAL CELL; ARTICLE; BREAST CANCER; CELL CYCLE; CELL MEMBRANE; CELL STRAIN MCF 7; CHROMOSOME DAMAGE; CONTROLLED STUDY; DISEASE ASSOCIATION; DNA DAMAGE; DNA REPAIR; ENZYME ACTIVATION; ENZYME ASSAY; ESTROGEN ACTIVITY; FEMALE; FLUORESCENCE MICROSCOPY; GAMMA IRRADIATION; GENE MUTATION; HUMAN; HUMAN CELL; IONIZING RADIATION; ISOTOPE LABELING; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN PHOSPHORYLATION; PROTEIN PROTEIN INTERACTION; SIGNAL TRANSDUCTION; ULTRAVIOLET RADIATION;

ANIMALS; CELL CYCLE; CELL CYCLE PROTEINS; CELL LINE, TRANSFORMED; CELL LINE, TUMOR; DNA REPAIR; ENZYME ACTIVATION; EPITHELIAL CELLS; ESTRADIOL; ESTROGEN RECEPTOR ALPHA; FEMALE; HUMANS; MAMMARY GLANDS, ANIMAL; MICE; MICE, INBRED C57BL; MODELS, BIOLOGICAL; PROTEIN KINASE INHIBITORS; PROTEIN KINASES; PROTEIN-SERINE-THREONINE KINASES; PROTO-ONCOGENE PROTEINS C-AKT; SIGNAL TRANSDUCTION; SUBSTRATE SPECIFICITY;

ATAXIA TELANGIECTASIA;

EID: 67749137207     PISSN: 10591524     EISSN: None     Source Type: Journal    
DOI: 10.1091/mbc.E09-01-0085     Document Type: Article

References (55)

1. Ahmad, S., Singh, N., and Glazer, R. I. (1999). Role of AKT1 in 17-beta-estradiol-and insulin-like growth factor I (IGF-1)-dependent proliferation and prevention of apoptosis in MCF-7 breast carcinoma cells. Biochem. Pharmacol. 58, 425-430.
2. Bakkenist, C. J., and Kastan, M. B. (2003). DNA damage activates ATM through intermolecular autophosphorylation and dimer dissociation. Nature 421, 499-506.
3. Bartkova, J., et al. (2005). DNA damage response as a candidate anti-cancer barrier in early human tumorigenesis. Nature 434, 864-870.
4. Boddy, M. N., Furnari, B., Mondesert, O., and Russell, P. (1998). Replication checkpoint enforced by kinases Cds1 and Chk1. Science 280, 909-912.
5. Brenner, R. M., Slayden, O. D., Rodgers, W. H., Critchley, H. O., Carroll, R., Nie, X. J., and Mah, K. (2003). Immunocytochemical assessment of mitotic activity with an antibody to phosphorylated histone H3 in the macaque and human endometrium. Hum. Reprod. 18, 1185-1193.
6. Carpten, J. D., et al. (2007). A transforming mutation in the pleckstrin homology domain of AKT1 in cancer. Nature 448, 439-444.
7. Cavalieri, E. L., et al. (1997). Molecular origin of cancer: catechol estrogen-3,4-quinones as endogenous tumor initiators. Proc. Natl. Acad. Sci. USA 94, 10937-10942.
8. Cavalieri, E., Chakravarti, D., Guttenplan, J., Hart, E., Ingle, J., Jankowiak, R., Muti, P., Rogan, E., Russo, J., Santen, R., and Sutter, T. (2006). Catechol estrogen quinones as initiators of breast and other human cancers: implications for biomarkers of susceptibility and cancer prevention. Biochim. Biophys. Acta 1766, 63-78.
9. Cordera, F., and Jordan, V. C. (2006). Steroid receptors and their role in the biology and control of breast cancer growth. Semin. Oncol. 33, 631-641.
10. Cortez, D., Guntuku, S., Qin, J., and Elledge, S. J. (2001). ATR and ATRIP: partners in checkpoint signaling. Science 294, 1713-1716.
11. Deng, C. X., and Brodie, S. G. (2001). Knockout mouse models and mammary tumorigenesis. Semin. Cancer Biol. 11, 387-394.
12. Doisneau-Sixou, S. F., Sergio, C. M., Carroll, J. S., Hui, R., Musgrove, E. A., and Sutherland, R. L. (2003). Estrogen and antiestrogen regulation of cell cycle progression in breast cancer cells. Endocr. Relat. Cancer 10, 179-186.
13. Eeckhoute, J., Carroll, J. S., Geistlinger, T. R., Torres-Arzayus, M. I., and Brown, M. (2006). A cell-type-specific transcriptional network required for estrogen regulation of cyclin D1 and cell cycle progression in breast cancer. Genes Dev. 20, 2513-2526.
14. Fernando, R. I., and Wimalasena, J. (2004). Estradiol abrogates apoptosis in breast cancer cells through inactivation of BAD: Ras-dependent nongenomic pathways requiring signaling through ERK and Akt. Mol. Biol. Cell 15, 3266-3284.
15. Filardo, E. J., Quinn, J. A., Bland, K. I., and Frackelton, A. R. (2000). Estrogen-induced activation of Erk-1 and Erk-2 requires the G protein-coupled receptor homolog, gpr30, and occurs via transactivation of the epidermal growth factor receptor through release of HB-EGF. Mol. Endocrinol. 14, 1649-1660.
16. Foster, J. S., Henley, D. C., Bukovsky, A., Seth, P., and Wimalasena, J. (2001). Multifaceted regulation of cell cycle progression by estrogen: regulation of Cdk inhibitors and Cdc25A independent of cyclin D1-Cdk4 function. Mol. Cell. Biol. 21, 794-810.
17. Gorgoulis, V. G., et al. (2005). Activation of the DNA damage checkpoint and genomic instability in human precancerous lesions. Nature 434, 907-913.
18. Greene, G., Closs, L. E., Fleming, H., DeSoimbre, E. R., and Jensen, E. (1977). Antibodies to estrogen receptor: immunochemical similarity of estrophillin from various mammalian species. Proc. Natl. Acad. Sci. USA 74, 3681-3685.
19. Harrington, W. R., Sheng, S., Barnett, D. H., Petz, L. N., Katzenellenbogen, J. A., and Katzenellenbogen, B. S. (2003). Activities of estrogen receptor alpha-and beta-selective ligands at diverse estrogen responsive gene sites mediating transactivation or transrepression. Mol. Cell Endocrinol. 206, 13-22.
20. Howell, A. (2006). Pure oestrogen antagonists for the treatment of advanced breast cancer. Endocr. Relat. Cancer 13, 689-706.
21. Horvath, G., Leser, G., Karlsson, L., and Delle, U. (1996). Estradiol regulates tumor growth by influencing p53 and bcl-2 expression in human endometrial adenocarcinomas grown in nude mice. In Vivo 10, 411-416.
22. Hutchins, J. R., and Clarke, P. R. (2004). Many fingers on the mitotic trigger: post-translational regulation of the Cdc25C phosphatase. Cell Cycle 3, 41-45.
23. Kastan, M. B., and Bartek, J. (2004). Cell-cycle checkpoints and cancer. Nature 432, 316-323.
24. Keeton, E. R., and Brown, M. (2005). Cell cycle progression stimulated by tamoxifen-bound estrogen receptor-alpha and promoter-specific effects in breast cancer cells deficient in N-CoR and SMRT. Mol. Endocrinol. 19, 1543-1554.
25. King, F. W., Skeen, J., Hay, N., and Shtivelman, E. (2004). Inhibition of Chk1 by activated PKB/Akt. Cell Cycle 3, 634-637.
26. Kuiper, G.G.J.M., Enmark, E., Pelto-Huiko, M., Nilsson, S., and Gustafsson, J.-A. (1996). Cloning of a novel receptor expressed in rat prostate and ovary. Proc. Natl. Acad. Sci. USA 93, 5925-5930.
27. Kumagai, A., Kim, S. M., and Dunphy, W. G. (2004). Claspin and the activated form of ATR-ATRIP collaborate in the activation of Chk1. J. Biol. Chem. 279, 49599-49608.
28. Kumagai, A., Lee, J., Yoo, H. Y., and Dunphy, W. G. (2006). TopBP1 activates the ATR-ATRIP complex. Cell 124, 943-955.
29. Levin, E. R. (2005). Integration of the extra-nuclear and nuclear actions of estrogen. Mol. Endocrinol. 19, 1951-1959.
30. Levin, E. R., and Pietras, R. J. (2007). Estrogen receptors outside the nucleus in breast cancer. Breast Cancer Res. Treat. 108, 351-361.
31. Li, J. J., Papa, D., Davis, M. F., Weroha, S. J., Aldaz, C. M., El-Bayoumy, K., Ballenger, J., Tawfik, O., and Li, S. A. (2002). Ploidy differences between hormone- and chemical carcinogen-induced rat mammary neoplasms: comparison to invasive human ductal breast cancer. Mol. Carcinog. 33, 56-65.
32. Li, J. J., Weroha, S. J., Lingle, W. L., Papa, D., Salisbury, J. L., and Li, S. A. (2004). Estrogen mediates Aurora-A overexpression, centrosome amplification, chromosomal instability, and breast cancer in female ACI rats. Proc. Natl. Acad. Sci. USA 101, 18123-18128.
33. Linggi, B., and Carpenter, G. (2006). ErbB receptors: new insights on mechanisms and biology. Trends Cell Biol. 16, 649-656.
34. Lippman, M. E., and Dickson, R. B. (1989). Mechanisms of growth control in normal and malignant breast epithelium. Recent Prog. Horm. Res. 45, 383-435.
35. Liu, S., Bekker-Jensen, S., Mailand, N., Lukas, C., Bartek, J., and Lukas, J. (2006a). Claspin operates downstream of TopBP1 to direct ATR signaling towards Chk1 activation. Mol. Cell. Biol. 26, 6056-6064.
36. Liu, K., Paik, J. C., Wang, B., Lin, F. T., and Lin, W. C. (2006b). Regulation of TopBP1 oligomerization by Akt/PKB for cell survival. EMBO J. 25, 4795-4807.
37. Marquez, D. C., and Pietras, R. J. (2001). Membrane-associated binding sites for estrogen contribute to growth regulation of human breast cancer cells. Oncogene 20, 5420-5430.
38. Meek, D. W. (2002). p53 Induction: phosphorylation sites cooperate in regulating interaction. Cancer Biol. Ther. 1, 284-290.
39. Naugler, W. E., Sakurai, T., Kim, S., Maeda, S., Kim, K., Elsharkawy, A. M., and Karin, M. (2007). Gender disparity in liver cancer due to sex differences in MyD88-dependent IL-6 production. Science 317, 121-124.
40. Pedram, A., Razandi, M., and Levin, E. R. (2006a). Nature of functional estrogen receptors at the plasma membrane. Mol. Endocrinol. 20, 1996-2009.
41. Pedram, A., Razandi, M., Wallace, D. C., and Levin, E. R. (2006b). Functional estrogen receptors in the mitochondria of breast cancer cells. Mol. Biol. Cell 17, 2125-2137.
42. Pedram, A., Razandi, M., Sainson, R.C.A., Kim, J. K., Hughes, C. C., and Levin, E. R. (2007). A conserved mechanism for steroid receptor translocation to the plasma membrane. J. Biol. Chem. 282, 2278-2288.
43. Pellman, D. (2007). Aneuploidy and cancer. Nature 446, 38-39.
44. Platet, N., Cathiard, A. M., Gleizes, M., and Garcia, M. (2004). Estrogens and their receptors in breast cancer progression: a dual role in cancer proliferation and invasion. Crit. Rev. Oncol. Hematol. 51, 55-67.
45. Puc, J., et al. (2005). Lack of PTEN sequesters CHK1 and initiates genetic instability. Cancer Cell 7, 193-204.
46. Qin, C., Nguyen, T., Stewart, J., Samudio, I., Burghardt, R., and Safe, S. (2002). Estrogen up-regulation of p53 gene expression in MCF-7 breast cancer cells is mediated by calmodulin kinase IV-dependent activation of a nuclear factor kappaB/CCAAT-binding transcription factor-1 complex. Mol Endocrinol. 16, 1793-1809.
47. Razandi, M., Alton, G., Pedram, A., Ghonshani, S., Webb, D., and Levin, E. R. (2003a). Identification of a structural determinant for the membrane localization of ERα. Mol. Cell. Biol. 23, 1633-1646.
48. Razandi, M., Pedram, A., Parks, S., and Levin, E. R. (2003b). Proximal events in ER signaling from the plasma membrane. J. Biol. Chem. 278, 2701-2712.
49. Redemann, N., Holzmann, B., von Ruden, T., Wagner, E. F., Schlessinger, J., and Ullrich, A. (1992). Anti-oncogenic activity of signalling-defective epidermal growth factor receptor mutants. Mol. Cell. Biol. 12, 491-498.
50. Rodrik, V., Zheng, Y., Harrow, F., Chen, Y., and Foster, D. A. (2005). Survival signals generated by estrogen and phospholipase D in MCF-7 breast cancer cells are dependent on Myc. Mol. Cell. Biol. 25, 7917-7925.
51. Sancar, A., Lindsey-Boltz, L. A., Unsal-Kacmaz, K., and Linn, S. (2004). Molecular mechanisms of mammalian DNA repair and the DNA damage checkpoints. Annu. Rev. Biochem. 273, 39-85.
52. Sanchez, Y., Wong, C., Thoma, R. S., Richman, R., Wu, Z., Piwnica-Worms, H., and Elledge, S. J. (1997). Conservation of the Chk1 checkpoint pathway in mammals: linkage of DNA damage to Cdk regulation through Cdc25. Science 277, 1497-1501.
53. Stanford, J. S., and Ruderman, J. V. (2005). Changes in regulatory phosphorylation of Cdc25C Ser287 and Wee1 Ser549 during normal cell cycle progression and checkpoint arrests. Mol. Biol. Cell 16, 5749-5760.
54. Xu, B., and Kastan, M. B. (2004). Analyzing cell cycle checkpoints after ionizing radiation. Methods Mol. Biol. 281, 283-292.
55. Yoo, H. Y., Jeong, S. Y., and Dunphy, W. G. (2006). Site-specific phosphorylation of a checkpoint mediator protein controls its responses to different DNA structures. Genes Dev. 20, 772-783.