44
Views
184
CrossRef citations to date
0
Altmetric
Transcriptional Regulation

p53 Represses Cyclin D1 Transcription through Down Regulation of Bcl-3 and Inducing Increased Association of the p52 NF-κB Subunit with Histone Deacetylase 1

, , &
Pages 4713-4727 | Received 24 Feb 2003, Accepted 10 Apr 2003, Published online: 27 Mar 2023

REFERENCES

  • Agami, R., and R. Bernards. 2000. Distinct initiation and maintenance mechanisms cooperate to induce G1 cell cycle arrest in response to DNA damage. Cell 102: 55–66.
  • Albanese, C., M. D'Amico, A. T. Reutens, M. F. Fu, G. Watanabe, R. J. Lee, R. N. Kitsis, B. Henglein, M. Avantaggiati, K. Somasundaram, B. Thimmapaya, and R. G. Pestell. 1999. Activation of the cyclin D1 gene by the EPA-associated protein p300 through AP-1 inhibits cellular apoptosis. J. Biol. Chem. 274: 34186–34195.
  • Anderson, L. A., and N. D. Perkins. 2002. The large subunit of replication factor C interacts with the histone deacetylase, HDAC1. J. Biol. Chem. 277: 29550–29554.
  • Ashburner, B. P., S. D. Westerheide, and A. S. Baldwin. 2001. The p65 (RelA) subunit of NF-κB interacts with the histone deacetylase (HDAC) corepressors HDAC1 and HDAC2 to negatively regulate gene expression. Mol. Cell. Biol. 21: 7065–7077.
  • Baer, R., and T. Ludwig. 2002. The BRCA1/BARD1 heterodimer, a tumor suppressor complex with ubiquitin E3 ligase activity. Curr. Opin. Genet. Dev. 12: 86–91.
  • Baldwin, A. S. 2001. Control of oncogenesis and cancer therapy resistance by the transcription factor NF-κB. J. Clin. Investig. 107: 241–246.
  • Barkett, M., and T. D. Gilmore. 1999. Control of apoptosis by Rel/NF-κB transcription factors. Oncogene 18: 6910–6924.
  • Bours, V., G. Franzoso, V. Azarenko, S. Park, T. Kanno, K. Brown, and U. Siebenlist. 1993. The oncoprotein Bcl-3 directly transactivates through κB motifs via association with DNA-binding p50B homodimers. Cell 72: 729–739.
  • Bundy, D. L., and T. W. McKeithan. 1997. Diverse effects of BCL3 phosphorylation on its modulation of NF-κB p52 homodimer binding to DNA. J. Biol. Chem. 272: 33132–33139.
  • Chang, N. S. 2002. The non-ankyrin C terminus of IκB α physically interacts with p53 in vivo and dissociates in response to apoptotic stress, hypoxia, DNA damage, and transforming growth factor-β 1-mediated growth suppression. J. Biol. Chem. 277: 10323–10331.
  • Chao, C., S. Saito, C. W. Anderson, E. Appella, and Y. Xu. 2000. Phosphorylation of murine p53 at Ser-18 regulates the p53 responses to DNA damage. Proc. Natl. Acad. Sci. USA 97: 11936–11941.
  • Chen, X. B., J. Bargonetti, and C. Prives. 1995. p53, through p21 (WAF1/CIP1), induces cyclin D1 synthesis. Cancer Res. 55: 4257–4263.
  • Cogswell, P. C., D. C. Guttridge, W. K. Funkhouser, and A. S. Baldwin. 2000. Selective activation of NF-κB subunits in human breast cancer: potential roles for NF-κB2/p52 and for Bcl-3. Oncogene 19: 1123–1131.
  • Dechend, R., F. Hirano, K. Lehmann, V. Heissmeyer, S. Ansieau, F. G. Wulczyn, C. Scheidereit, and A. Leutz. 1999. The Bcl-3 oncoprotein acts as a bridging factor between NF-κB/Rel and nuclear co-regulators. Oncogene 18: 3316–3323.
  • Dignam, J. D., R. M. Lebovitz, and R. G. Roeder. 1983. Accurate transcription initiation by RNA polymerase II in a soluble extract from isolated mammalian nuclei. Nucleic Acids Res. 11: 1475–1489.
  • Dumaz, N., and D. W. Meek. 1999. Serine15 phosphorylation stimulates p53 transactivation but does not directly influence interaction with HDM2. EMBO J. 18: 7002–7010.
  • Franzoso, G., V. Bours, S. Park, M. Tomita-Yamaguchi, K. Kelly, and U. Siebenlist. 1992. The candidate oncoprotein Bcl-3 is an antagonist of P50/NF-κB-mediated inhibition. Nature 359: 339–342.
  • Fujita, T., G. P. Nolan, H. C. Liou, M. L. Scott, and D. Baltimore. 1993. The candidate protooncogene Bcl-3 encodes a transcriptional coactivator that activates through NF-κB p50 homodimers. Genes Dev. 7: 1354–1363.
  • Gu, L. B., H. W. Findley, and M. X. Zhou. 2002. MDM2 induces NF-κB/p65 expression transcriptionally through Sp1-binding sites: a novel, p53-independent role of MDM2 in doxorubicin resistance in acute lymphoblastic leukemia. Blood 99: 3367–3375.
  • Guardavaccaro, D., G. Corrente, F. Covone, L. Micheli, I. D'Agnano, G. Starace, M. Caruso, and F. Tirone. 2000. Arrest of G1-S progression by the p53-inducible gene PC3 is Rb dependent and relies on the inhibition of cyclin D1 transcription. Mol. Cell. Biol. 20: 1797–1815.
  • Guttridge, D. C., C. Albanese, J. Y. Reuther, R. G. Pestell, and A. S. Baldwin. 1999. NF-κB controls cell growth and differentiation through transcriptional regulation of cyclin D1. Mol. Cell. Biol. 19: 5785–5799.
  • Hanahan, D., and R. A. Weinberg. 2000. The hallmarks of cancer. Cell 100: 57–70.
  • Harbour, J. W., and D. C. Dean. 2000. The Rb/E2F pathway: expanding roles and emerging paradigms. Genes Dev. 14: 2393–2409.
  • Hellin, A. C., P. Calmant, J. Gielen, V. Bours, and M. P. Merville. 1998. Nuclear factor-κB-dependent regulation of p53 gene expression induced by daunomycin genotoxic drug. Oncogene 16: 1187–1195.
  • Hupp, T. R., D. P. Lane, and K. L. Ball. 2000. Strategies for manipulating the p53 pathway in the treatment of human cancer. Biochem. J. 352: 1–17.
  • Irminger-Finger, I., and W. C. Leung. 2002. BRCA1-dependent and independent functions of BARD1. Int. J. Biochem. Cell Biol. 34: 582–587.
  • Irminger-Finger, I., W. C. Leung, J. Li, M. Dubois-Dauphin, J. Harb, A. Feki, C. E. Jefford, J. V. Soriano, M. Jaconi, R. Montesano, and K. H. Krause. 2001. Identification of BARD1 as mediator between proapoptotic stress and p53-dependent apoptosis. Mol. Cell 8: 1255–1266.
  • Joyce, D., B. Bouzahzah, M. F. Fu, C. Albanese, M. D'Amico, J. Steer, J. U. Klein, R. J. Lee, J. E. Segall, J. K. Westwick, C. J. Der, and R. G. Pestell. 1999. Integration of Rac-dependent regulation of cyclin D1 transcription through a nuclear factor-κB-dependent pathway. J. Biol. Chem. 274: 25245–25249.
  • Kawai, H., Y. Yamada, M. Tatsuka, O. Niwa, K. Yamamoto, and F. Suzuki. 1999. Down-regulation of nuclear factor κB is required for p53-dependent apoptosis in X-ray-irradiated mouse lymphoma cells and thymocytes. Cancer Res. 59: 6038–6041.
  • Kirch, H. C., S. Flaswinkel, H. Rumpf, D. Brockmann, and H. Esche. 1999. Expression of human p53 requires synergistic activation of transcription from the p53 promoter by AP-1, NF-κB and Myc/Max. Oncogene 18: 2728–2738.
  • Lambert, P. F., F. Kashanchi, M. F. Radonovich, R. Shiekhattar, and J. N. Brady. 1998. Phosphorylation of p53 serine 15 increases interaction with CBP. J. Biol. Chem. 273: 33048–33053.
  • Liou, H. C., G. P. Nolan, S. Ghosh, T. Fujita, and D. Baltimore. 1992. The NF-κB p50 precursor, p105, contains an internal I κB-like inhibitor that preferentially inhibits p50. EMBO J. 11: 3003–3009.
  • Matsumura, I., T. Kitamura, H. Wakao, H. Tanaka, K. Hashimoto, C. Albanese, J. Downward, R. G. Pestell, and Y. Kanakura. 1999. Transcriptional regulation of the cyclin D1 promoter by STAT5: its involvement in cytokine-dependent growth of hematopoietic cells. EMBO J. 18: 1367–1377.
  • McKeithan, T. W., G. S. Takimoto, H. Ohno, V. S. Bjorling, R. Morgan, B. K. Hecht, I. Dube, A. A. Sandberg, and J. D. Rowley. 1997. BCL3 rearrangements and t(14;19) in chronic lymphocytic leukemia and other B-cell malignancies: a molecular and cytogenetic study. Genes Chromosomes Cancer 20: 64–72.
  • Michaux, L., C. Mecucci, M. Stul, I. Wlodarska, J. M. Hernandez, P. Meeus, J. L. Michaux, J. M. Scheiff, H. Noel, A. Louwagie, A. Criel, M. Boogaerts, A. Van Orshoven, J. J. Cassiman, and H. Van Den Berghe. 1996. BCL3 rearrangement and t(14;19)(q32;q13) in lymphoproliferative disorders. Genes Chromosomes Cancer 15: 38–47.
  • Na, S. Y., H. S. Choi, J. W. Kim, D. S. Na, and J. W. Lee. 1998. Bcl3, an IκB protein, as a novel transcription coactivator of the retinoid X receptor. J. Biol. Chem. 273: 30933–30938.
  • Na, S. Y., J. E. Choi, H. J. Kim, B. H. Jhun, Y. C. Lee, and J. W. Lee. 1999. Bcl3, an IκB protein, stimulates activating protein-1 transactivation and cellular proliferation. J. Biol. Chem. 274: 28491–28496.
  • 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 M. E. Ewen. 1997. Cyclin D1 stimulation of estrogen receptor transcriptional activity independent of cdk4. Mol. Cell. Biol. 17: 5338–5347.
  • Nolan, G. P., T. Fujita, K. Bhatia, C. Huppi, H. C. Liou, M. L. Scott, and D. Baltimore. 1993. The Bcl-3 protooncogene encodes a nuclear IκB-like molecule that preferentially interacts with NF-κB p50 and p52 in a phosphorylation-dependent manner. Mol. Cell. Biol. 13: 3557–3566.
  • Ong, S. T., M. L. Hackbarth, L. C. Degenstein, D. A. Baunoch, J. Anastasi, and T. W. McKeithan. 1998. Lymphadenopathy, splenomegaly, and altered immunoglobulin production in BCL3 transgenic mice. Oncogene 16: 2333–2343.
  • Pahl, H. L. 1999. Activators and target genes of Rel/NF-κB transcription factors. Oncogene 18: 6853–6866.
  • Pei, X. H., Y. Nakanishi, K. Takayama, F. Bai, and N. Hara. 1999. Benzo[a]pyrene activates the human p53 gene through induction of nuclear factor κB activity. J. Biol. Chem. 274: 35240–35246.
  • Perkins, N. D. 2002. Not just a CDK inhibitor: regulation of transcription by p21WAF1/CIP1/SDI1. Cell Cycle 1: 39–41.
  • Perkins, N. D. 2000. The Rel/NF-κB family: friend and foe. Trends Biochem. Sci. 25: 434–440.
  • Perkins, N. D., R. M. Schmid, C. S. Duckett, K. Leung, N. R. Rice, and G. J. Nabel. 1992. Distinct combinations of NF-κB subunits determine the specificity of transcriptional activation. Proc. Natl. Acad. Sci. USA 89: 1529–1533.
  • Ravi, R., B. Mookerjee, Y. van Hensbergen, G. C. Bedi, A. Giordano, W. S. El-Deiry, E. J. Fuchs, and A. Bedi. 1998. p53-mediated repression of nuclear factor-κB RelA via the transcriptional integrator p300. Cancer Res. 58: 4531–4536.
  • Rayet, B., and C. Gelinas. 1999. Aberrant rel/nfkb genes and activity in human cancer. Oncogene 18: 6938–6947.
  • Rebollo, A., L. Dumoutier, J.-C. Renauld, A. Zaballos, V. Ayllón, and C. Martínez-A. 2000. Bcl-3 expression promotes cell survival following interleukin-4 deprivation and is controlled by AP1 and AP1-like transcription factors. Mol. Cell. Biol. 20: 3407–3416.
  • Ryan, K. M., M. K. Ernst, N. R. Rice, and K. H. Vousden. 2000. Role of NF-κB in p53-mediated programmed cell death. Nature 404: 892–897.
  • Scheinman, R. I., A. A. Beg, and A. S. Baldwin, Jr. 1993. NF-κB p100 (Lyt-10) is a component of H2TF1 and can function as an IκB-like molecule. Mol. Cell. Biol. 13: 6089–6101.
  • Shao, J., T. Fujiwara, Y. Kadowaki, T. Fukazawa, T. Waku, T. Itoshima, T. Yamatsuji, M. Nishizaki, J. A. Roth, and N. Tanaka. 2000. Overexpression of the wild-type p53 gene inhibits NF-κB activity and synergizes with aspirin to induce apoptosis in human colon cancer cells. Oncogene 19: 726–736.
  • Taylor, W. R., and G. R. Stark. 2001. Regulation of the G2/M transition by p53. Oncogene 20: 1803–1815.
  • Tergaonkar, V., M. Pando, O. Vafa, G. Wahl, and I. Verma. 2002. p53 stabilization is decreased upon NFκB activation: a role for NFκB in acquisition of resistance to chemotherapy. Cancer Cell 1: 493–503.
  • Tetsu, O., and F. McCormick. 1999. β-Catenin regulates expression of cyclin D1 in colon carcinoma cells. Nature 398: 422–426.
  • Vousden, K. H. 2002. Activation of the p53 tumor suppressor protein. Biochim. Biophys. Acta Rev. Cancer 1602: 47–59.
  • Vousden, K. H. 2002. Switching from life to death: the Miz-ing link between Myc and p53. Cancer Cell 2: 351–352.
  • Wadgaonkar, R., K. M. Phelps, Z. Haque, A. J. Williams, E. S. Silverman, and T. Collins. 1999. CREB-binding protein is a nuclear integrator of nuclear factor-κB and p53 signaling. J. Biol. Chem. 274: 1879–1882.
  • Watanabe, G., C. Albanese, R. J. Lee, A. Reutens, G. Vairo, B. Henglein, and R. G. Pestell. 1998. Inhibition of cyclin D1 kinase activity is associated with E2F-mediated inhibition of cyclin D1 promoter activity through E2F and Sp1. Mol. Cell. Biol. 18: 3212–3222.
  • Webster, G. A., and N. D. Perkins. 1999. Transcriptional cross talk between NF-κB and p53. Mol. Cell. Biol. 19: 3485–3495.
  • Weinstat-Saslow, D., M. J. Merino, R. E. Manrow, J. A. Lawrence, R. F. Bluth, K. D. Wittenbel, J. F. Simpson, D. L. Page, and P. S. Steeg. 1995. Overexpression of cyclin D mRNA distinguishes invasive and in situ breast carcinomas from non-malignant lesions. Nat. Med. 1: 1257–1260.
  • Westerheide, S. D., M. W. Mayo, V. Anest, J. L. Hanson, and A. S. Baldwin, Jr. 2001. The putative oncoprotein Bcl-3 induces cyclin D1 to stimulate G1 transition. Mol. Cell. Biol. 21: 8428–8436.
  • Zhao, R. B., K. Gish, M. Murphy, Y. X. Yin, D. Notterman, W. H. Hoffman, E. Tom, D. H. Mack, and A. J. Levine. 2000. Analysis of p53-regulated gene expression patterns using oligonucleotide arrays. Genes Dev. 14: 981–993.
  • Zhong, H. H., M. J. May, E. Jimi, and S. Ghosh. 2002. The phosphorylation status of nuclear NF-κB determines its association with CBP/p300 or HDAC-1. Mol. Cell 9: 625–636.
  • Zwijsen, R. M. L., 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.

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.