The DNA binding and accumulation of p53 from breast cancer cell lines and the link with serine 15 phosphorylation

Cancer Biology and Therapy

Volumn 13, Issue 10, 2012, Pages 848-857

  Ray, Debolina ^a   Murphy, Keith R ^a   Gal, Susannah ^a  

^a BINGHAMTON UNIVERSITY   (United States)

Author keywords

Apoptosis; Cell cycle regulation; Phosphorylation; Post translational modifications; Stabilization

Indexed keywords

DNA; PROTEIN P53; SERINE; SERINE 15; UNCLASSIFIED DRUG;

ARTICLE; BINDING AFFINITY; BREAST CANCER; CANCER CELL CULTURE; CONTROLLED STUDY; DNA BINDING; GENE MUTATION; GENE SEQUENCE; HUMAN; HUMAN CELL; PHOSPHORYLATION; PROTEIN LOCALIZATION; PROTEIN PROCESSING;

BREAST NEOPLASMS; CELL LINE, TUMOR; DNA; DNA-BINDING PROTEINS; FEMALE; HUMANS; MUTATION; PHOSPHORYLATION; PROTEIN TRANSPORT; SERINE; TUMOR SUPPRESSOR PROTEIN P53;

EID: 84864533044     PISSN: 15384047     EISSN: 15558576     Source Type: Journal    
DOI: 10.4161/cbt.20835     Document Type: Article

References (49)

1. Lane DP. p53, guardian of the genome. Nature 1992; 358:15-6; PMID:1614522; http://dx.doi.org/10.1038/358015a0.
2. Riley T, Sontag E, Chen P, Levine A. Transcriptional control of human p53-regulated genes. Nat Rev Mol Cell Biol 2008; 9:402-12; PMID:18431400; http://dx.doi.org/10.1038/nrm2395.
3. INK4a loss. Genes Dev 2008; 22:1337-44; PMID:18483220; http://dx.doi.org/10.1101/gad. 1662908.
4. Bode AM, Dong Z. Post-translational modification of p53 in tumorigenesis. Nat Rev Cancer 2004; 4:793-805; PMID:15510160; http://dx.doi.org/10.1038/ nrc1455.
5. Komarova EA, Zelnick CR, Chin D, Zeremski M, Gleiberman AS, Bacus SS, et al. Intracellular localization of p53 tumor suppressor protein in γ-irradiated cells is cell cycle regulated and determined by the nucleus. Cancer Res 1997; 57:5217-20; PMID:9393737.
6. Appella E, Anderson CW. Post-translational modifications and activation of p53 by genotoxic stresses. Eur J Biochem 2001; 268:2764-72; PMID:11358490; http://dx.doi.org/10.1046/j.1432-327.2001.02225.x.
7. Arbely E, Natan E, Brandt T, Allen MD, Veprintsev DB, Robinson CV, et al. Acetylation of lysine 120 of p53 endows DNA-binding specificity at effective physiological salt concentration. Proc Nat Acad Sci USA 2011; 108:8251-6.
8. Luo J, Li M, Tang Y, Laszkowska M, Roeder RG, Gu W. Acetylation of p53 augments its site-specific DNA binding both in vitro and in vivo. Proc Natl Acad Sci USA 2004; 101:2259-64; PMID:14982997; http://dx.doi.org/10.1073/pnas. 0308762101.
9. Collavin L, Lunardi A, Del Sal G. p53-family proteins and their regulators: hubs and spokes in tumor suppression. Cell Death Differ 2010; 17:901-11; PMID:20379196; http://dx.doi.org/10.1038/cdd.2010.35.
10. Malkin D, Li FP, Strong LC, Fraumeni JF Jr, Nelson CE, Kim DH, et al. Germ line p53 mutations in a familial syndrome of breast cancer, sarcomas and other neoplasms. Science 1990; 250:1233-8; PMID:1978757; http://dx.doi.org/10. 1126/science.1978757.
11. Done SJ, Eskandarian S, Bull S, Redston M, Andrulis IL. p53 missense mutations in microdissected high-grade ductal carcinoma in situ of the breast. J Natl Cancer Inst 2001; 93:700-4; PMID:11333292; http://dx.doi.org/10.1093/jnci/ 93.9.700.
12. Xu J, Reumers J, Couceiro JR, De Smet F, Gallardo R, Rudyak S, et al. Gain of function of mutant p53 by coaggregation with multiple tumor suppressors. Nat Chem Biol 2011; 7:285-95; PMID:21445056; http://dx.doi.org/10.1038/ nchembio.546.
13. Chandrachud U, Gal S. Three assays show differences in binding of wild-type and mutant p53 to unique gene sequences. Technol Cancer Res Treat 2009; 8:445-53; PMID:19925028.
14. Ray D, Balmer MT, Gal S. The functionality of p53 in thyroid cancer. Fahey TJ, [Ed.]. Updates in the Understanding and Management of Thyroid Cancer. Intech Publishers, Rijeka, Croatia 2012; 33-52.
15. Park DJ, Nakamura H, Chumakov AM, Said JW, Miller CW, Chen DL, et al. Transactivational and DNA binding abilities of endogenous p53 in p53 mutant cell lines. Oncogene 1994; 9:1899-906; PMID:8208536.
16. Vousden KH, Lu X. Live or let die: the cell's response to p53. Nat Rev Cancer 2002; 2:594-604; PMID:12154352; http://dx.doi.org/10.1038/nrc864.
17. Sugikawa E, Yazaki N, Tsunoda S, Nakanishi N, Ohashi M. Inhibition of mutant p53 phosphorylation at serine 15 or serine 315 partially restores the function of wild-type p53. Biochem Biophys Res Commun 1999; 261:256-63; PMID:10425175; http://dx.doi.org/10.1006/bbrc.1999.1019.
18. Okaichi K, Nose K, Kotake T, Izumi N, Kudo T. Phosphorylation of p53 modifies sensitivity to ionizing radiation. Anticancer Res 2011; 31:2255-8; PMID:21737649.
19. Wolff A, Technau A, Ihling C, Technau-Ihling K, Erber R, Bosch FX, et al. Evidence that wild-type p53 in neuroblastoma cells is in a conformation refractory to integration into the transcriptional complex. Oncogene 2001; 20:1307-17; PMID:11313875; http://dx.doi.org/10.1038/sj.onc.1204251.
20. Ostermeyer AG, Runko E, Winkfield B, Ahn B, Moll UM. Cytoplasmically sequestered wild-type p53 protein in neuroblastoma is relocated to the nucleus by a C-terminal peptide. Proc Natl Acad Sci USA 1996; 93:15190-4; PMID:8986786; http://dx.doi.org/10.1073/pnas.93.26.15190.
21. Zhang H, Somasundaram K, Peng Y, Tian H, Zhang H, Bi D, et al. BRCA1 physically associates with p53 and stimulates its transcriptional activity. Oncogene 1998; 16:1713-21; PMID:9582019; http://dx.doi.org/10.1038/sj.onc. 1201932.
22. Umbricht CB, Evron E, Gabrielson E, Ferguson A, Marks J, Sukumar S. Hypermethylation of 14-3-3 sigma (stratifin) is an early event in breast cancer. Oncogene 2001; 20:3348-53; PMID:11423985; http://dx.doi.org/10.1038/sj.onc. 1204438.
23. Jagelská E, Brázda V, Pospisilová S, Vojtešek B, Palecek E. New ELISA technique for analysis of p53 protein/DNA binding properties. J Immunol Methods 2002; 267:227-35; PMID:12165443; http://dx.doi.org/10.1016/S0022-1759(02)00182-5.
24. Lavin MF, Gueven N. The complexity of p53 stabilization and activation. Cell Death Differ 2006; 13:941-50; PMID:16601750; http://dx.doi.org/10.1038/sj. cdd.4401925.
25. Ito T, Kaneko K, Makino R, Ito H, Konishi K, Kurahashi T, et al. Prognostic value of p53 mutations in patients with locally advanced esophageal carcinoma treated with definitive chemoradiotherapy. J Gastroenterol 2001; 36:303-11; PMID:11388392; http://dx.doi.org/10.1007/s005350170095.
26. Zerbini LF, Wang Y, Correa RG, Cho JY, Libermann TA. Blockage of NFkappaB induces serine 15 phosphorylation of mutant p53 by JNK kinase in prostate cancer cells. Cell Cycle 2005; 4:1247-53; PMID:16082226; http://dx.doi.org/10. 4161/cc.4.9.1966.
27. Huovinen M, Loikkanen J, Myllynen P, Vähäkangas KH. Characterization of human breast cancer cell lines for the studies on p53 in chemical carcinogenesis. Toxicol In Vitro 2011; 25:1007-17; PMID:21457773; http://dx.doi.org/10.1016/j.tiv.2011.03.018.
28. Moll UM, Petrenko O. The MDM2-p53 interaction. Mol Cancer Res 2003; 1:1001-8; PMID:14707283.
29. Fuchs SY, Adler V, Buschmann T, Yin Z, Wu X, Jones SN, et al. JNK targets p53 ubiquitination and degradation in nonstressed cells. Genes Dev 1998; 12:2658-63; PMID:9732264; http://dx.doi.org/10.1101/gad.12.17.2658.
30. Matsuoka M, Igisu H. Cadmium induces phosphorylation of p53 at serine 15 in MCF-7 cells. Biochem Biophys Res Commun 2001; 282:1120-5; PMID:11302731; http://dx.doi.org/10.1006/bbrc.2001.4700.
31. Lambert PF, Kashanchi F, Radonovich MF, Shiekhattar R, Brady JN. Phosphorylation of p53 serine 15 increases interaction with CBP. J Biol Chem 1998; 273:33048-53; PMID:9830059; http://dx.doi.org/10.1074/jbc.273.49.33048.
32. Ashcroft M, Taya Y, Vousden KH. Stress signals utilize multiple pathways to stabilize p53. Mol Cell Biol 2000; 20:3224-33; PMID:10757806; http://dx.doi.org/10.1128/MCB.20.9.3224-33.2000.
33. Gottifredi V, Shieh SY, Taya Y, Prives C. p53 accumulates but is functionally impaired when DNA synthesis is blocked. Proc Natl Acad Sci USA 2001; 98:1036-41; PMID:11158590; http://dx.doi.org/10.1073/pnas.021282898.
34. Göhler T, Jäger S, Warnecke G, Yasuda H, Kim E, Deppert W. Mutant p53 proteins bind DNA in a DNA structure-selective mode. Nucleic Acids Res 2005; 33:1087-100; PMID:15722483; http://dx.doi.org/10.1093/nar/gki252.
35. Weinberg RL, Freund SM, Veprintsev DB, Bycroft M, Fersht AR. Regulation of DNA binding of p53 by its C-terminal domain. J Mol Biol 2004; 342:801-11; PMID:15342238; http://dx.doi.org/10.1016/j.jmb.2004.07.042.
36. Weinberg RL, Veprintsev DB, Fersht AR. Cooperative binding of tetrameric p53 to DNA. J Mol Biol 2004; 341:1145-59; PMID:15321712; http://dx.doi.org/10. 1016/j.jmb.2004.06.071.
37. Liu W, Konduri SD, Bansal S, Nayak BK, Rajasekaran SA, Karuppayil SM, et al. Estrogen receptor-α binds p53 tumor suppressor protein directly and represses its function. J Biol Chem 2006; 281:9837-40; PMID:16469747; http://dx.doi.org/10.1074/jbc.C600001200.
38. Liu W, Ip MM, Podgorsak MB, Das GM. Disruption of estrogen receptor alpha-p53 interaction in breast tumors: a novel mechanism underlying the anti-tumor effect of radiation therapy. Breast Cancer Res Treat 2009; 115:43-50; PMID:18481172; http://dx.doi.org/10.1007/s10549-008-0044-z.
39. Sayeed A, Konduri SD, Liu W, Bansal S, Li F, Das GM. Estrogen receptor α inhibits p53-mediated transcriptional repression: implications for the regulation of apoptosis. Cancer Res 2007; 67:7746-55; PMID:17699779; http://dx.doi.org/10.1158/0008-5472.CAN-06-3724.
40. Mihara M, Erster S, Zaika A, Petrenko O, Chittenden T, Pancoska P, et al. p53 has a direct apoptogenic role at the mitochondria. Mol Cell 2003; 11:577-90; PMID:12667443; http://dx.doi.org/10.1016/S1097-2765(03)00050-9.
41. Huntington ND, Labi V, Cumano A, Vieira P, Strasser A, Villunger A, et al. Loss of the pro-apoptotic BH3-only Bcl-2 family member Bim sustains B lymphopoiesis in the absence of IL-7. Int Immunol 2009; 21:715-25; PMID:19454543; http://dx.doi.org/10.1093/intimm/dxp043.
42. Formby B, Wiley TS. Bcl-2, survivin and variant CD44 v7-v10 are downregulated and p53 is upregulated in breast cancer cells by progesterone: inhibition of cell growth and induction of apoptosis. Mol Cell Biochem 1999; 202:53-61; PMID:10705995; http://dx.doi.org/10.1023/A:1007081021483.
43. Le Gac G, Estève P-O, Ferec C, Pradhan S. DNA damage-induced downregulation of human Cdc25C and Cdc2 is mediated by cooperation between p53 and maintenance DNA (cytosine-5) methyltransferase 1. J Biol Chem 2006; 281:24161-70; PMID:16807237; http://dx.doi.org/10.1074/jbc.M603724200.
44. Zauberman A, Lupo A, Oren M. Identification of p53 target genes through immune selection of genomic DNA: the cyclin G gene contains two distinct p53 binding sites. Oncogene 1995; 10:2361-6; PMID:7784084.
45. Smith ML, Kontny HU, Bortnick R, Fornace AJ Jr. The p53-regulated cyclin G gene promotes cell growth: p53 downstream effectors cyclin G and Gadd45 exert different effects on cisplatin chemosensitivity. Exp Cell Res 1997; 230:61-8; PMID:9013707; http://dx.doi.org/10.1006/excr.1996.3402.
46. Mercer WE, Shields MT, Lin D, Appella E, Ullrich S. J Growth suppression induced by wild-type p53 protein is accompanied by selective downregulation of proliferating-cell nuclear antigen expression. Proceesings of the National Academy of Sciences (USA) 1996; 88:1958-62; http://dx.doi.org/10.1073/pnas.88.5. 1958.
47. Morris GF, Bischoff JR, Mathews MB. Transcriptional activation of the human proliferating-cell nuclear antigen promoter by p53. Proc Natl Acad Sci USA 1996; 93:895-9; PMID:8570655; http://dx.doi.org/10.1073/pnas.93.2.895.
48. Bodner SM, Minna JD, Jensen SM, D'Amico D, Carbone D, Mitsudomi T, et al. Expression of mutant p53 proteins in lung cancer correlates with the class of p53 gene mutation. Oncogene 1992; 7:743-9; PMID:1565469.
49. Allred DC, Clark GM, Elledge R, Fuqua SAW, Brown RW, Chamness GC, et al. Association of p53 protein expression with tumor cell proliferation rate and clinical outcome in node-negative breast cancer. J Natl Cancer Inst 1993; 85:200-6; PMID:8423624; http://dx.doi.org/10.1093/jnci/85.3.200.