Characterization of the p53 Cistrome – DNA Binding Cooperativity Dissects p53's Tumor Suppressor Functions
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p53 protects us from cancer by transcriptionally regulating tumor suppressive programs designed to either prevent the development or clonal expansion of malignant cells. How p53 selects target genes in the genome in a context- and tissue-specific manner remains largely obscure. There is growing evidence that the ability of p53 to bind DNA in a cooperative manner prominently influences target gene selection with activation of the apoptosis program being completely dependent on DNA binding cooperativity. Here, we used ChIP-seq to comprehensively profile the cistrome of p53 mutants with reduced or increased cooperativity. The analysis highlighted a particular relevance of cooperativity for extending the p53 cistrome to non-canonical binding sequences characterized by deletions, spacer insertions and base mismatches. Furthermore, it revealed a striking functional separation of the cistrome on the basis of cooperativity; with low cooperativity genes being significantly enriched for cell cycle and high cooperativity genes for apoptotic functions. Importantly, expression of high but not low cooperativity genes was correlated with superior survival in breast cancer patients. Interestingly, in contrast to most p53-activated genes, p53-repressed genes did not commonly contain p53 binding elements. Nevertheless, both the degree of gene activation and repression were cooperativity-dependent, suggesting that p53-mediated gene repression is largely indirect and mediated by cooperativity-dependently transactivated gene products such as CDKN1A, E2F7 and non-coding RNAs. Since both activation of apoptosis genes with non-canonical response elements and repression of pro-survival genes are crucial for p53's apoptotic activity, the cistrome analysis comprehensively explains why p53-induced apoptosis, but not cell cycle arrest, strongly depends on the intermolecular cooperation of p53 molecules as a possible safeguard mechanism protecting from accidental cell killing.
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The transactivation of target genes requires cooperative interaction between the p53 molecules at DNA response elements.
“The p53 transcription factor uses two transactivation domains to drive gene expression58 and the transactivation of target genes requires cooperative interaction between the p53 molecules at DNA REs.23, 59”
From Census and evaluation of p53 target genes (2017) · cites this paper as [23]
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Mutant p53 promotes tumor progression and metastasis by the endoplasmic reticulum UDPase ENTPD5
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p53 and RAD9, the DNA Damage Response, and Regulation of Transcription Networks
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A Mouse Homolog of a Human TP53 Germline Mutation Reveals a Lipolytic Activity of p53
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p53‐mediated regulation of bile acid disposition attenuates cholic acid‐induced cholestasis in mice
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- Authors
- Schlereth, K., Heyl, C., Krampitz, A.-M., Mernberger, M., Finkernagel, F., Scharfe, M., Jarek, M., Leich, E., Rosenwald, A., & Stiewe, T.
- Affiliations
- Philipps University of Marburg (DE)
- Helmholtz Centre for Infection Research (DE)
- University of Würzburg (DE)
- Corresponding author
- Stiewe, Thorsten
- ORCID
- Venue
- PLoS Genetics
- Publisher
- Public Library of Science (PLoS)
- Published
- 2013-08-15
- Volume
- 9
- Issue
- 8
- Pages
- e1003726
- ISSN
- 1553-7390 (ISSN-L)
- 1553-7404
- PMC
- PMC3744428
- OpenAlex
- W2117969095
- Cited by
- 87
- References
- 73
- Citations by year
- 2026: 4 · 2025: 3 · 2024: 5 · 2022: 6 · 2021: 9 · 2020: 4 · 2019: 7 · 2018: 9 · 2017: 13 · 2016: 7 · 2015: 11 · 2014: 9
- FWCI
- 4.82
- Type
- journal article
- Language
- en
- Open access
- gold
- doi.org
- Locations
- PLoS Genetics (publishedVersion, cc-by)
- Europe PMC (PubMed Central) (publishedVersion, cc-by)
- PubMed Central (publishedVersion, cc-by)
- PubMed (publishedVersion)
- HZI (Helmholtz Centre for Infection Research) (submittedVersion)
- DOAJ (DOAJ: Directory of Open Access Journals) (submittedVersion, cc-by-sa)
- Figshare (submittedVersion, cc-by)
- Online Publication Service of Würzburg University (Würzburg University) (submittedVersion, cc-by)
- Funders
- Leuka
- Deutsche Forschungsgemeinschaft
- Deutsche Krebshilfe
- Topics
- Health Sciences › Medicine › Oncology › Cancer-related Molecular Pathways
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Genomics and Chromatin Dynamics
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Chromatin Remodeling and Cancer
- Keywords
- p53, DNA binding cooperativity, apoptosis, cell cycle arrest, p21, E2F7, non-coding RNA, breast cancer survival, mutant p53, tumor suppressor function
- MeSH terms
- Base Sequence, Binding Sites, Cell Division, DNA Damage, Humans, Neoplasms, Protein Binding, Transcriptional Activation, Gene Expression Regulation, Neoplastic, Tumor Suppressor Protein p53, Apoptosis, RNA, Untranslated, E2F7 Transcription Factor, Cyclin-Dependent Kinase Inhibitor p21, Cell Cycle Checkpoints
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