Runt-related transcription factor 1 (RUNX1) stimulates tumor suppressor p53 protein in response to DNA damage through complex formation and acetylation

Journal of Biological Chemistry

Volumn 288, Issue 2, 2013, Pages 1353-1364

  Wu, Dan ^a   Ozakis, Toshinori ^a   Yoshiharas, Yukari ^a   Kubos, Natsumi ^a   Nakagawara, Akira ^a  

^a CHIBA CANCER CENTER   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

ADRIAMYCIN; CELL NUCLEUS; CHROMATIN IMMUNOPRECIPITATION ASSAY; COMPLEX FORMATIONS; DNA DAMAGE RESPONSE; DNA DAMAGES; HISTONE ACETYLTRANSFERASES; MOLECULAR MECHANISM; P53 PROTEIN; TARGET GENES; TRANSACTIVATION; TRANSCRIPTIONAL ACTIVITY; TRANSCRIPTIONAL REGULATION; TUMOR SUPPRESSORS;

ACETYLATION; CELL DEATH; GENES; TRANSCRIPTION FACTORS; TUMORS;

DNA;

CYCLIN DEPENDENT KINASE INHIBITOR 1; DOXORUBICIN; HISTONE ACETYLTRANSFERASE PCAF; PROTEIN BAX; PROTEIN NOXA; PROTEIN P53; PUMA PROTEIN; TRANSCRIPTION FACTOR RUNX1;

ACETYLATION; APOPTOSIS; ARTICLE; BAX GENE; COMPLEX FORMATION; CONTROLLED STUDY; DNA DAMAGE; GENE INDUCTION; HUMAN; HUMAN CELL; NOXA GENE; P21 WAF1 GENE; PRIORITY JOURNAL; PROMOTER REGION; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN PROTEIN INTERACTION; PUMA GENE; TRANSACTIVATION; TRANSCRIPTION REGULATION;

ACETYLATION; BASE SEQUENCE; BLOTTING, WESTERN; CELL LINE, TUMOR; CHROMATIN IMMUNOPRECIPITATION; CORE BINDING FACTOR ALPHA 2 SUBUNIT; DNA DAMAGE; DNA PRIMERS; DOXORUBICIN; GENE KNOCKDOWN TECHNIQUES; HUMANS; PROMOTER REGIONS, GENETIC; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; TRANSCRIPTION, GENETIC; TUMOR SUPPRESSOR PROTEIN P53;

EID: 84872354372     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M112.402594     Document Type: Article

References (56)

1. Zhou, B. B., and Elledge, S. J. (2000) The DNA damage response. Putting checkpoints in perspective. Nature 408, 433-439
2. Pietenpol, J. A., Tokino, T., Thiagalingam, S., el-Deiry, W. S., Kinzler, K. W., and Vogelstein, B. (1994) Sequence-specific transcriptional activation is essential for growth suppression by p53. Proc. Natl. Acad. Sci. U.S.A. 91, 1998-2002 (Pubitemid 24092029)
3. Harris, C. C. (1993) p53. At the crossroads of molecular carcinogenesis and risk assessment. Science 262, 1980-1981
4. Vousden, K. H., and Lu, X. (2002) Live or let die. The cell's response to p53. Nat. Rev. Cancer 2, 594-604 (Pubitemid 37328926)
5. Vogelstein, B., and Kinzler, K. W. (1992) p53 function and dysfunction. Cell 70, 523-526
6. Velculescu, V. E., and El-Deiry, W. S. (1996) Biological and clinical importance of the p53 tumor suppressor gene. Clin. Chem. 42, 858-868
7. Vogelstein, B., Lane, D., Levine, A. J. (2000) Surfing the p53 network. Nature 408, 307-310
8. Donehower, L. A., Harvey, M., Slagle, B. L., McArthur, M. J., Montgomery, C. A., Jr., Butel, J. S., and Bradley, A. (1992) Mice deficient for p53 are developmentally normal but susceptible to spontaneous tumours. Nature 356, 215-221
9. el-Deiry, W. S., Kern, S. E., Pietenpol, J. A. (1992) Definition of a consensus binding site for p53. Nat. Genet. 1, 45-49
10. Sionov, R. V., and Haupt, Y. (1999) The cellular response to p53. The decision between life and death. Oncogene 18, 6145-6157
11. Prives, C., and Hall, P. A. (1999) The p53 pathway. J. Pathol. 187, 112-126 (Pubitemid 29009841)
12. Haupt, Y., Maya, R., Kazaz, A., and Oren, M. (1997) Mdm2 promotes the rapid degradation of p53. Nature 387, 296-299 (Pubitemid 27220766)
13. Kubbutat, M. H., Jones, S. N., and Vousden, K. H. (1997) Regulation of p53 stability by Mdm2. Nature 387, 299-303 (Pubitemid 27220767)
14. Honda, R., Tanaka, H., and Yasuda, H. (1997) Oncoprotein MDM2 is a ubiquitin ligase E3 for tumor suppressor p53. FEBS Lett. 420, 25-27 (Pubitemid 28037193)
15. Piette, J., Neel, H., and Maréchal, V. (1997) Mdm2. Keeping p53 under control. Oncogene 15, 1001-1010
16. Yuan, Z. M., Huang, Y., Ishiko, T., Nakada, S., Utsugisawa, T., Shioya, H., Utsugisawa, Y., Yokoyama, K., Weichselbaum, R., Shi, Y., and Kufe, D. (1999) Role for p300 in stabilization of p53 in the response to DNA damage. J. Biol. Chem. 274, 1883-1886
17. Oren, M. (2003) Decision making by p53. Life, death, and cancer. Cell Death Differ. 10, 431-442
18. D'Orazi, G., Cecchinelli, B., Bruno, T., Manni, I., Higashimoto, Y., Saito, S., Gostissa, M., Coen, S., Marchetti, A., Del Sal, G., Piaggio, G., Fanciulli, M., Appella, E., and Soddu, S. (2002) Homeodomain-interacting protein kinase-2 phosphorylates p53 at Ser 46 and mediates apoptosis. Nat. Cell Biol. 4, 11-19
19. Yoshida, K., Liu, H., and Miki, Y. (2006) Protein kinase Cδ regulates Ser46 phosphorylation of p53 tumor suppressor in the apoptotic response to DNA damage. J. Biol. Chem. 281, 5734-5740 (Pubitemid 43847672)
20. Oda, K., Arakawa, H., Tanaka, T., Matsuda, K., Tanikawa, C., Mori, T., Nishimori, H., Tamai, K., Tokino, T., Nakamura, Y., and Taya, Y. (2000) p53AIP1, a potential mediator of p53-dependent apoptosis, and its regulation by Ser-46-phosphorylated p53. Cell 102, 849-862
21. Shikama, N., Lee, C. W., France, S., Delavaine, L., Lyon, J., Krstic-Demonacos, M., and La Thangue, N. B. (1999) A novel cofactor for p300 that regulates the p53 response. Mol. Cell 4, 365-376 (Pubitemid 29499789)
22. Lacroix, M., Toillon, R. A., and Leclercq, G. (2006) p53 and breast cancer, an update. Endocr. Relat. Cancer 13, 293-325 (Pubitemid 43886660)
23. Kim, W. J., Rivera, M. N., Coffman, E. J., and Haber, D. A. (2012) The WTX tumor suppressor enhances p53 acetylation by CBP/p300. Mol. Cell 45, 587-597
24. Ivanov, G. S., Ivanova, T., Kurash, J., Ivanov, A., Chuikov, S., Gizatullin, F., Herrera-Medina, E. M., Rauscher, F., 3rd, Reinberg, D., and Barlev, N. A. (2007) Methylation-acetylation interplay activates p53 in response to DNA damage. Mol. Cell. Biol. 27, 6756-6769 (Pubitemid 47483627)
25. Samuels-Lev, Y., O'Connor, D. J., Bergamaschi, D., Trigiante, G., Hsieh, J. K., Zhong, S., Campargue, I., Naumovski, L., Crook, T., and Lu, X. (2001) ASPP proteins specifically stimulate the apoptotic function of p53. Mol. Cell 8, 781-794 (Pubitemid 33030212)
26. Yang, H. Y., Wen, Y. Y., Chen, C. H., Lozano, G., and Lee, M. H. (2003) 14-3-3 sigma positively regulates p53 and suppresses tumor growth. Mol. Cell. Biol. 23, 7096-7107 (Pubitemid 37210993)
27. Ito, Y. (2008) RUNX genes in development and cancer. Regulation of viral gene expression and the discovery of RUNX family genes. Adv. Cancer Res. 99, 33-76
28. Miyoshi, H., Shimizu, K., Kozu, T., Maseki, N., Kaneko, Y., and Ohki, M. (1991) t(8;21) breakpoints on chromosome 21 in acute myeloid leukemia are clustered within a limited region of a single gene, AML1. Proc. Natl. Acad. Sci. U.S.A. 88, 10431-10434 (Pubitemid 21915849)
29. Golub, T. R., Barker, G. F., Bohlander, S. K., Hiebert, S. W., Ward, D. C., Bray-Ward, P., Morgan, E., Raimondi, S. C., Rowley, J. D., and Gilliland, D. G. (1995) Fusion of the TEL gene on 12p13 to the AML1 gene on 21q22 in acute lymphoblastic leukemia. Proc. Natl. Acad. Sci. U.S.A. 92, 4917-4921
30. Silva, F. P., Morolli, B., Storlazzi, C. T., Anelli, L., Wessels, H., Bezrookove, V., Kluin-Nelemans, H. C., and Giphart-Gassler, M. (2003) Identification of RUNX1/AML1 as a classical tumor suppressor gene. Oncogene 22, 538-547 (Pubitemid 36188611)
31. Roumier, C., Fenaux, P., Lafage, M., Imbert, M., Eclache, V., and Preudhomme, C. (2003) New mechanisms of AML1 gene alteration in hematological malignancies. Leukemia 17, 9-16 (Pubitemid 36175882)
32. Okuda, T., van Deursen, J., Hiebert, S. W., Grosveld, G., and Downing, J. R. (1996) AML1, the target of multiple chromosomal translocations in human leukemia, is essential for normal fetal liver hematopoiesis. Cell 84, 321-330 (Pubitemid 26042836)
33. Wang, Q., Stacy, T., Binder, M., Marin-Padilla, M., Sharpe, A. H., and Speck, N. A. (1996) Disruption of the Cbfa2 gene causes necrosis and hemorrhaging in the central nervous system and blocks definitive hematopoiesis. Proc. Natl. Acad. Sci. U.S.A. 93, 3444-3449 (Pubitemid 26125639)
34. Takahashi, A., Satake, M., Yamaguchi-Iwai, Y., Bae, S. C., Lu, J., Maruyama, M., Zhang, Y. W., Oka, H., Arai, N., Arai, K., et al. (1995) Positive and negative regulation of granulocyte-macrophage colony-stimulating factor promoter activity by AML1-related transcription factor, PEBP2. Blood 86, 607-616
35. Taniuchi, I., Osato, M., Egawa, T., Sunshine, M. J., Bae, S. C., Komori, T., Ito, Y., and Littman, D. R. (2002) Differential requirements for Runx proteins in CD4 repression and epigenetic silencing during T lymphocyte development. Cell 111, 621-633 (Pubitemid 35441245)
36. Lutterbach, B., Westendorf, J. J., Linggi, B., Isaac, S., Seto, E., and Hiebert, S. W. (2000) A mechanism of repression by acute myeloid leukemia-1, the target of multiple chromosomal translocations in acute leukemia. J. Biol. Chem. 275, 651-656 (Pubitemid 30039030)
37. Guo, H., and Friedman, A. D. (2011) Phosphorylation of RUNX1 by cyclin-dependent kinase reduces direct interaction with HDAC1 and HDAC3. J. Biol. Chem. 286, 208-215
38. Yamaguchi, Y., Kurokawa, M., Imai, Y., Izutsu, K., Asai, T., Ichikawa, M., Yamamoto, G., Nitta, E., Yamagata, T., Sasaki, K., Mitani, K., Ogawa, S., Chiba, S., and Hirai, H. (2004) AML1 is functionally regulated through p300-mediated acetylation on specific lysine residues. J. Biol. Chem. 279, 15630-15638 (Pubitemid 38618964)
39. Zhao, X., Jankovic, V., Gural, A., Huang, G., Pardanani, A., Menendez, S., Zhang, J., Dunne, R., Xiao, A., Erdjument-Bromage, H., Allis, C. D., Tempst, P., and Nimer, S. D. (2008) Methylation of RUNX1 by PRMT1 abrogates SIN3A binding and potentiates its transcriptional activity. Genes Dev. 22, 640-653 (Pubitemid 351342436)
40. Linggi, B., Müller-Tidow, C., van de Locht, L., Hu, M., Nip, J., Serve, H., Berdel, W. E., van der Reijden, B., Quelle, D. E., Rowley, J. D., Cleveland, J., Jansen, J. H., Pandolfi, P. P., and Hiebert, S. W. (2002) The t(8;21) fusion protein, AML1 ETO, specifically represses the transcription of the p14(ARF) tumor suppressor in acute myeloid leukemia. Nat. Med. 8, 743-750
41. Wotton, S. F., Blyth, K., Kilbey, A., Jenkins, A., Terry, A., Bernardin-Fried, F., Friedman, A. D., Baxter, E. W., Neil, J. C., and Cameron, E. R. (2004) RUNX1 transformation of primary embryonic fibroblasts is revealed in the absence of p53. Oncogene 23, 5476-5486 (Pubitemid 39044058)
42. Li, X. L., Arai, Y., Harada, H., Shima, Y., Yoshida, H., Rokudai, S., Aikawa, Y., Kimura, A., and Kitabayashi, I. (2007) Mutations of the HIPK2 gene in acute myeloid leukemia and myelodysplastic syndrome impair AML1- and p53-mediated transcription. Oncogene 26, 7231-7239 (Pubitemid 350085316)
43. Hanamoto, T., Ozaki, T., Furuya, K., Hosoda, M., Hayashi, S., Nakanishi, M., Yamamoto, H., Kikuchi, H., Todo, S., and Nakagawara, A. (2005) Identification of protein kinase A catalytic subunit beta as a novel binding partner of p73 and regulation of p73 function. J. Biol. Chem. 280, 16665-16675 (Pubitemid 41389124)
44. Li, Y., Ozaki, T., Kikuchi, H., Yamamoto, H., Ohira, M., and Nakagawara, A. (2008) A novel HECT-type E3 ubiquitin protein ligase NEDL1 enhances the p53-mediated apoptotic cell death in its catalytic activity-independent manner. Oncogene 27, 3700-3709 (Pubitemid 351912965)
45. Yoshihara, Y., Wu, D., Kubo, N., Sang, M., Nakagawara, A., and Ozaki, T. (2012) Inhibitory role of E2F-1 in the regulation of tumor suppressor p53 during DNA damage response. Biochem. Biophys. Res. Commun. 421, 57-63
46. Kitabayashi, I., Yokoyama, A., Shimizu, K., and Ohki, M. (1998) Interaction and functional cooperation of the leukemia-associated factors AML1 and p300 in myeloid cell differentiation. EMBO J. 17, 2994-3004 (Pubitemid 28254372)
47. Sakaguchi, K., Herrera, J. E., Saito, S., Miki, T., Bustin, M., Vassilev, A., Anderson, C. W., and Appella, E. (1998) DNA damage activates p53 through a phosphorylation-acetylation cascade. Genes Dev. 12, 2831-2841 (Pubitemid 28440142)
48. Tang, Y., Zhao, W., Chen, Y., Zhao, Y., and Gu, W. (2008) Acetylation is indispensable for p53 activation. Cell 133, 612-626 (Pubitemid 351636297)
49. Michishita, E., Park, J. Y., Burneskis, J. M., Barrett, J. C., and Horikawa, I. (2005) Evolutionarily conserved and nonconserved cellular localizations and functions of human SIRT proteins. Mol. Biol. Cell 16, 4623-4635 (Pubitemid 41416446)
50. Wen, Z., Pyeon, D., Wang, Y., Lambert, P., Xu, W., and Ahlquist, P. (2012) Orphan nuclear receptor PNR/NR2E3 stimulates p53 functions by enhancing p53 acetylation. Mol. Cell. Biol. 32, 26-35
51. Kawai, H., Nie, L., Wiederschain, D., and Yuan, Z. M. (2001) Dual role of p300 in the regulation of p53 stability. J. Biol. Chem. 276, 45928-45932
52. Zhao, Y., Lu, S., Wu, L., Chai, G., Wang, H., Chen, Y., Sun, J., Yu, Y., Zhou, W., Zheng, Q., Wu, M., Otterson, G. A., and Zhu, W. G. (2006) Acetylation of p53 at lysine 373/382 by the histone deacetylase inhibitor depsipeptide induces expression of p21(Waf1/Cip1). Mol. Cell. Biol. 26, 2782-2790
53. Wildey, G. M., Patil, S., and Howe, P. H. (2003) Smad3 potentiates transforming growth factor β (TGFβ)-induced apoptosis and expression of the BH3-only protein Bim in WEHI 231 B lymphocytes. J. Biol. Chem. 278, 18069-18077 (Pubitemid 36799419)
54. Wildey, G. M., and Howe, P. H. (2009) Runx1 is a co-activator with FOXO3 to mediate transforming growth factor β (TGFβ)-induced Bim transcription in hepatic cells. J. Biol. Chem. 284, 20227-20239
55. Yano, T., Ito, K., Fukamachi, H., Chi, X. Z., Wee, H. J., Inoue, K., Ida, H., Bouillet, P., Strasser, A., Bae, S. C., and Ito, Y. (2006) The RUNX3 tumor suppressor up-regulates Bim in gastric epithelial cells undergoing transforming growth factor β-induced apoptosis. Mol. Cell. Biol. 26, 4474-4488 (Pubitemid 43877568)
56. Yamada, C., Ozaki, T., Ando, K., Suenaga, Y., Inoue, K., Ito, Y., Okoshi, R., Kageyama, H., Kimura, H., Miyazaki, M., and Nakagawara, A. (2010) RUNX3 modulates DNA damage-mediated phosphorylation of tumor suppressor p53 at Ser-15 and acts as a co-activator for p53. J. Biol. Chem. 285, 16693-16703