Home LiteratureArticle Details
PMID: 19651615 Published · ppublish English Journal Article Research Support, N.I.H., Extramural Research Support, Non-U.S. Gov't

Control of p53 multimerization by Ubc13 is JNK-regulated.

Topisirovic I, Gutierrez GJ, Chen M, Appella E, Borden KL, Ronai ZA

Abstract

The p53 tumor suppressor protein is a key regulator of cellular proliferation and survival whose function is tightly regulated at the levels of transcription and protein stability. Here, we unveil the fine control of p53 on translationally active polysomes. We have previously reported that Ubc13, an E2 ubiquitin-conjugating enzyme, directly regulates p53 localization and transcriptional activity. We now demonstrate that the association of p53 and Ubc13 on polysomes requires ongoing translation and results in p53 ubiquitination that interferes with its tetramerization. JNK phosphorylation of p53 at Threonine 81 occurring on polysomes is required for the dissociation of Ubc13 from p53, leading to p53 multimerization and transcriptional activation. Inhibition of JNK activity or expression of a nonphosphorylatable mutant of p53 maintains an Ubc13-p53 complex that inhibits p53 multimerization. Our findings reveal a layer in the regulation of p53 multimerization that requires the concerted action of JNK and Ubc13 on polysome-bound p53.

MeSH Terms
JNK Mitogen-Activated Protein Kinases/physiology MAP Kinase Signaling System Polyribosomes/metabolism Tumor Suppressor Protein p53/chemistry,physiology Ubiquitin/metabolism Ubiquitin-Conjugating Enzymes/chemistry,physiology
Chemicals
Tumor Suppressor Protein p53 Ubiquitin UBE2N protein, human Ubiquitin-Conjugating Enzymes JNK Mitogen-Activated Protein Kinases
Authors & Affiliations
6 authors, click to expand affiliations / ORCID
Topisirovic Ivan
Institute for Research in Immunology and Cancer, Université de Montréal, Montréal, Quebec, H3T 1J4, Canada.
Gutierrez Gustavo J
Chen Meifan
Appella Ettore
Borden Katherine L B
Ronai Ze'ev A
References (18)
18 references, click to expand
  1. Germ line p53 mutations in a familial syndrome of breast cancer, sarcomas, and other neoplasms.
    Science. 1990 Nov 30;250(4985):1233-8 PMID: 1978757
  2. IARC Database of p53 gene mutations in human tumors and cell lines: updated compilation, revised formats and new visualisation tools.
    Nucleic Acids Res. 1998 Jan 1;26(1):205-13 PMID: 9399837
  3. Mitogen-activated protein (MAP) kinase pathways: regulation and physiological functions.
    Endocr Rev. 2001 Apr;22(2):153-83 PMID: 11294822
  4. JNK2 contains a specificity-determining region responsible for efficient c-Jun binding and phosphorylation.
    Genes Dev. 1994 Dec 15;8(24):2996-3007 PMID: 8001819
  5. MSL2 promotes Mdm2-independent cytoplasmic localization of p53.
    J Biol Chem. 2009 Jan 30;284(5):3250-3263 PMID: 19033443
  6. The p53 pathway: positive and negative feedback loops.
    Oncogene. 2005 Apr 18;24(17):2899-908 PMID: 15838523
  7. Parc: a cytoplasmic anchor for p53.
    Cell. 2003 Jan 10;112(1):29-40 PMID: 12526791
  8. Mdm2 regulates p53 mRNA translation through inhibitory interactions with ribosomal protein L26.
    Mol Cell. 2008 Oct 24;32(2):180-9 PMID: 18951086
  9. Jun NH2-terminal kinase phosphorylation of p53 on Thr-81 is important for p53 stabilization and transcriptional activities in response to stress.
    Mol Cell Biol. 2001 Apr;21(8):2743-54 PMID: 11283254
  10. JNK targets p53 ubiquitination and degradation in nonstressed cells.
    Genes Dev. 1998 Sep 1;12(17):2658-63 PMID: 9732264
  11. Living with p53, dying of p53.
    Cell. 2007 Aug 24;130(4):597-600 PMID: 17719538
  12. Ubiquitin chain editing revealed by polyubiquitin linkage-specific antibodies.
    Cell. 2008 Aug 22;134(4):668-78 PMID: 18724939
  13. MEKK1/JNK signaling stabilizes and activates p53.
    Proc Natl Acad Sci U S A. 1998 Sep 1;95(18):10541-6 PMID: 9724739
  14. The p53-Mdm2 module and the ubiquitin system.
    Semin Cancer Biol. 2003 Feb;13(1):49-58 PMID: 12507556
  15. Regulation of p53 translation and induction after DNA damage by ribosomal protein L26 and nucleolin.
    Cell. 2005 Oct 7;123(1):49-63 PMID: 16213212
  16. Keeping p53 in check: essential and synergistic functions of Mdm2 and Mdm4.
    Cell Death Differ. 2006 Jun;13(6):927-34 PMID: 16543935
  17. Regulation of p53 localization and activity by Ubc13.
    Mol Cell Biol. 2006 Dec;26(23):8901-13 PMID: 17000756
  18. Regulation of p53 localization and transcription by the HECT domain E3 ligase WWP1.
    Oncogene. 2007 Mar 1;26(10):1477-83 PMID: 16924229
Article Info
Journal
Proceedings of the National Academy of Sciences of the United States of America
Abbr.
Proc Natl Acad Sci U S A
ISSN
1091-6490
Published
2009-08-04
Epub
2009-00-27
Pages
12676-81
Language
English
Region
United States
NLM ID
7505876
PMCID
PMC2722327
Subset
IM
Grants
NCI NIH HHS · CA078419 · United States
NCI NIH HHS · T32 CA077109 · United States
NCI NIH HHS · R01 CA138143 · United States
PHS HHS · R01-80728 · United States
NCI NIH HHS · R01 CA078419 · United States
NCI NIH HHS · CA077109 · United States
NCI NIH HHS · CA138143 · United States
Analysis Services
Analysis Services

Contact

No. 2 Wenbo Road, Zhangqiu District, Jinan, Shandong

Qilu Normal University · Genelibs Bioinformatics Lab

750 Shunhua Rd, Jinan

2F, Bldg F, University Science Park

Tel: 0531-88819269

WeChat Official Account

Follow our WeChat subscription account for real-time updates and the latest in medical and biological research.


Business Email

E-mail: product@genelibs.com