Diverse stresses dramatically alter genome-wide p53 binding and transactivation landscape in human cancer cells
Open accessAbstract
The effects of diverse stresses on promoter selectivity and transcription regulation by the tumor suppressor p53 are poorly understood. We have taken a comprehensive approach to characterizing the human p53 network that includes p53 levels, binding, expression and chromatin changes under diverse stresses. Human osteosarcoma U2OS cells treated with anti-cancer drugs Doxorubicin (DXR) or Nutlin-3 (Nutlin) led to strikingly different p53 gene binding patterns based on chromatin immunoprecipitation with high-throughput sequencing experiments. Although two contiguous RRRCWWGYYY decamers is the consensus binding motif, p53 can bind a single decamer and function in vivo. Although the number of sites bound by p53 was six times greater for Nutlin than DXR, expression changes induced by Nutlin were much less dramatic compared with DXR. Unexpectedly, the solvent dimethylsulphoxide (DMSO) alone induced p53 binding to many sites common to DXR; however, this binding had no effect on target gene expression. Together, these data imply a two-stage mechanism for p53 transactivation where p53 binding only constitutes the first stage. Furthermore, both p53 binding and transactivation were associated with increased active histone modification histone H3 lysine 4 trimethylation. We discovered 149 putative new p53 target genes including several that are relevant to tumor suppression, revealing potential new targets for cancer therapy and expanding our understanding of the p53 regulatory network.
The claims and statistics of this paper haven’t been checked yet.
Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.
Integrity signals
Registry
Cites
Statistics
Claims the paper makes
The claims and statistics of this paper haven’t been checked yet.
Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.
Claims other papers make about this one
Each is checked against this paper’s own text: does it say what the citing paper says it does?
p53 directly induces numerous genes involved in triggering the recruitment of immune cells and immune surveillance in human cells, which can involve the TLR gene family.
“gene expression analyses has shown that p53 directly induces numerous genes involved in triggering the recruitment of immune cells and immune surveillance in human cells [11], which can involve the TLR gene family.”
From Ligand dependent restoration of human TLR3 signaling and death in p53 mutant cells (2016) · cites this paper as [11]
The Introduction says p53 can transactivate genes involved in innate immune responses, and the Results (Novel p53 target genes; page unavailable) identify many putative direct p53 targets in human cancer cells. Our copy does not establish that numerous targets trigger immune-cell recruitment or immune surveillance, or identify the TLR gene family as part of that finding. (LLM, conf=0.83)
Experimental — accuracy not yet measuredResults from multiple studies suggest that p53 can bind and transactivate target genes through noncanonical binding sites, particularly through half-sites.
“In addition, results from multiple studies suggest that p53 can bind and transactivate target genes through noncanonical binding sites, particularly through half-sites.22, 54, 55, 56”
From Census and evaluation of p53 target genes (2017) · cites this paper as [22]
Self-check
Percentages, sums and reported differences re-computed from the paper’s own numbers.
The self-check needs the paper’s full text.
Cites
Systematic and integrative analysis of large gene lists using DAVID bioinformatics resources
Huang, D. W., Sherman, B. T., & Lempicki, R. A. (2009) · Nature Protocols · doi:10.1038/nprot.2008.211 · Cited by 35,890 · see citing works
Ultrafast and memory-efficient alignment of short DNA sequences to the human genome.
Langmead, B., Trapnell, C., Pop, M., & Salzberg, S. L. (2009) · Genome Biology · doi:10.1186/gb-2009-10-3-r25 · Cited by 21,849 · see citing works
Bolstad, B. M., Irizarry, R. A., Åstrand, M., & Speed, T. P. (2003) · Bioinformatics · doi:10.1093/bioinformatics/19.2.185 · Cited by 8,185 · see citing works
limma: Linear Models for Microarray Data
Smyth, G. K. (2005) · Statistics for Biology and Health · doi:10.1007/0-387-29362-0_23 · Cited by 5,796 · see citing works
Fitting a mixture model by expectation maximization to discover motifs in biopolymers.
Bailey, T. L., & Elkan, C. (1994) · PubMed · Cited by 4,933 · see citing works
Bioinformatics and Computational Biology Solutions Using R and Bioconductor
Gentleman, R. C., Carey, V. J., Huber, W. K., Irizarry, R. A., & Dudoit, S. (2005) · Statistics in the health sciences · doi:10.1007/0-387-29362-0 · Cited by 3,470 · see citing works
COSMIC: mining complete cancer genomes in the Catalogue of Somatic Mutations in Cancer
Forbes, S. A., Bindal, N., Bamford, S., Cole, C., Kok, C. Y., Beare, D., Jia, M., Shepherd, R., Leung, K., Menzies, A., et al. (2011) · Nucleic Acids Research · doi:10.1093/nar/gkq929 · Cited by 2,278 · see citing works
De novo mutations revealed by whole-exome sequencing are strongly associated with autism
Sanders, S. J., Murtha, M. T., Gupta, A. R., Murdoch, J. D., Raubeson, M. J., Willsey, A. J., Ercan-Sencicek, A. G., DiLullo, N. M., Parikshak, N. N., Stein, J. L., et al. (2012) · Nature · doi:10.1038/nature10945 · Cited by 2,084 · see citing works
Definition of a consensus binding site for p53
El-Deiry, W. S., Kern, S. E., Pietenpol, J. A., Kinzler, K. W., & Vogelstein, B. (1992) · Nature Genetics · doi:10.1038/ng0492-45 · Cited by 1,985 · see citing works
Transcriptional control of human p53-regulated genes
Riley, T., Sontag, E., Chen, P., & Levine, A. (2008) · Nature Reviews Molecular Cell Biology · doi:10.1038/nrm2395 · Cited by 1,921 · see citing works
Evolving gene/transcript definitions significantly alter the interpretation of GeneChip data
Dai, M. (2005) · Nucleic Acids Research · doi:10.1093/nar/gni179 · Cited by 1,797 · see citing works
Combining evidence using p-values: application to sequence homology searches.
Bailey, T. L., & Gribskov, M. (1998) · Bioinformatics · doi:10.1093/bioinformatics/14.1.48 · Cited by 1,257 · see citing works
TRANSFAC: an integrated system for gene expression regulation
Wingender, E. (2000) · Nucleic Acids Research · doi:10.1093/nar/28.1.316 · Cited by 1,249 · see citing works
A Global Map of p53 Transcription-Factor Binding Sites in the Human Genome
Wei, C.-L., Wu, Q., Vega, V. B., Chiu, K. P., Ng, P., Zhang, T., Shahab, A., Yong, H. C., Fu, Y., Weng, Z., et al. (2006) · Cell · doi:10.1016/j.cell.2005.10.043 · Cited by 1,141 · see citing works
Tumor Suppression in the Absence of p53-Mediated Cell-Cycle Arrest, Apoptosis, and Senescence
Li, T., Kon, N., Jiang, L., Tan, M., Ludwig, T., Zhao, Y., Baer, R., & Gu, W. (2012) · Cell · doi:10.1016/j.cell.2012.04.026 · Cited by 912 · see citing works
A Transcriptionally Active DNA-Binding Site for Human p53 Protein Complexes
Funk, W. D., Pak, D. T. S., Karas, R. H., Wright, W. E., & Shay, J. W. (1992) · Molecular and Cellular Biology · doi:10.1128/mcb.12.6.2866 · Cited by 732 · see citing works
Asthagiri, A. R., Parry, D. M., Butman, J. A., et al. (2009) · The Lancet · doi:10.1016/s0140-6736(09)60259-2 · Cited by 666 · see citing works
Analysis of p53-regulated gene expression patterns using oligonucleotide arraysPreprint
Zhao, R., Gish, K., Murphy, M. E., Yin, Y., Notterman, D. A., Hoffman, W. H., Tom, E., Mack, D. H., & Levine, A. J. (2000) · Genes & Development · doi:10.1101/gad.14.8.981 · Cited by 631 · see citing works
The expanding universe of p53 targets
Menendez, D., Inga, A., & Resnick, M. A. (2009) · Nature Reviews Cancer · doi:10.1038/nrc2730 · Cited by 568 · see citing works
Self-citationGenome-wide identification of<i>in vivo</i>protein-DNA binding sites from ChIP-Seq data
Jothi, R., Cuddapah, S., Barski, A., Cui, K., & Zhao, K. (2008) · Nucleic Acids Research · doi:10.1093/nar/gkn488 · Cited by 539 · see citing works
Self-citationMDM2 inhibitors for cancer therapy
Vassilev, L. T. (2007) · Trends in Molecular Medicine · doi:10.1016/j.molmed.2006.11.002 · Cited by 532 · see citing works
FBXW7/hCDC4 Is a General Tumor Suppressor in Human Cancer
Akhoondi, S., Sun, D., von der Lehr, N., Apostolidou, S., Klotz, K., Malyukova, A., Cepeda, D., Fiegl, H., Dafou, D., Marth, C., et al. (2007) · Cancer Research · doi:10.1158/0008-5472.can-07-1320 · Cited by 507 · see citing works
Transcriptional regulation by p53: one protein, many possibilities
Laptenko, O., & Prives, C. L. (2006) · Cell Death and Differentiation · doi:10.1038/sj.cdd.4401916 · Cited by 500 · see citing works
Structural Basis of DNA Recognition by p53 Tetramers
Kitayner, M., Rozenberg, H., Kessler, N., Rabinovich, D., Shaulov, L., Haran, T. E., & Shakked, Z. (2006) · Molecular Cell · doi:10.1016/j.molcel.2006.05.015 · Cited by 408 · see citing works
Menon, A. G., Anderson, K. M., Riccardi, V. M., Chung, R. Y., Whaley, J. M., Yandell, D. W., Farmer, G. E., Freiman, R. N., Lee, J. K., & Li, F. P. (1990) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.87.14.5435 · Cited by 396 · see citing works
Fbxw7/Cdc4 is a p53-dependent, haploinsufficient tumour suppressor gene
Mao, J.-H., Perez-losada, J., Wu, D., DelRosario, R., Tsunematsu, R., Nakayama, K. I., Brown, K., Bryson, S., & Balmain, A. (2004) · Nature · doi:10.1038/nature03155 · Cited by 390 · see citing works
Mutations in ABCA12 Underlie the Severe Congenital Skin Disease Harlequin Ichthyosis
Kelsell, D. P., Norgett, E. E., Unsworth, H., Teh, M., Cullup, T., Mein, C. A., Dopping-Hepenstal, J. P., Dale, A. B., Tadini, G., Fleckman, P. H., et al. (2005) · The American Journal of Human Genetics · doi:10.1086/429844 · Cited by 351 · see citing works
Production and Titration of Lentiviral Vectors
Barde, I., Salmon, P., & Trono, D. (2010) · Current Protocols in Neuroscience · doi:10.1002/0471142301.ns0421s53 · Cited by 303 · see citing works
A polymorphic microsatellite that mediates induction of PIG3 by p53
Contente, A., Dittmer, A., Koch, M. C., Roth, J., & Dobbelstein, M. (2002) · Nature Genetics · doi:10.1038/ng836 · Cited by 274 · see citing works
Li, M., He, Y., Dubois, W., Wu, X., Shi, J., & Huang, J. (2012) · Molecular Cell · doi:10.1016/j.molcel.2012.01.020 · Cited by 264 · see citing works
Espinosa, J. M., Verdun, R. E., & Emerson, B. M. (2003) · Molecular Cell · doi:10.1016/s1097-2765(03)00359-9 · Cited by 256 · see citing works
Saito, S., Yamaguchi, H., Higashimoto, Y., Chao, C., Xu, Y., Fornace, A. J., Appella, E., & Anderson, C. W. (2003) · Journal of Biological Chemistry · doi:10.1074/jbc.m305135200 · Cited by 253 · see citing works
Self-citationA Transcriptionally Active DNA-Binding Site for Human p53 Protein Complexes
Funk, W. D., Pak, D. T. S., Karas, R. H., et al. (1992) · Molecular and Cellular Biology · doi:10.1128/mcb.12.6.2866-2871.1992 · Cited by 239 · see citing works
Diversity in DNA recognition by p53 revealed by crystal structures with Hoogsteen base pairs
Kitayner, M., Rozenberg, H., Rohs, R., Suad, O., Rabinovich, D., Honig, B. H., & Shakked, Z. (2010) · Nature Structural & Molecular Biology · doi:10.1038/nsmb.1800 · Cited by 230 · see citing works
Characterization of genome-wide p53-binding sites upon stress response
Smeenk, L., van Heeringen, S. J., Koeppel, M., van Driel, M. A., Bartels, S. J. J., Akkers, R. C., Denissov, S., Stunnenberg, H. G., & Lohrum, M. (2008) · Nucleic Acids Research · doi:10.1093/nar/gkn232 · Cited by 211 · see citing works
Comparative Binding of p53 to its Promoter and DNA Recognition Elements
Weinberg, R. L., Veprintsev, D. B., Bycroft, M., & Fersht, A. R. (2005) · Journal of Molecular Biology · doi:10.1016/j.jmb.2005.03.014 · Cited by 206 · see citing works
Nikulenkov, F., Spinnler, C., Li, H., Tonelli, C., Shi, Y., Turunen, M. M., Kivioja, T., Ignatiev, I., Kel, A. E., Taipale, J., et al. (2012) · Cell Death and Differentiation · doi:10.1038/cdd.2012.89 · Cited by 182 · see citing works
Lefèvre, C., Bouadjar, B., Karaduman, A., Jobard, F., Saker, S., Özgüç, M., Lathrop, M. G., Prud’homme, J.-F., & Fischer, J. (2004) · Human Molecular Genetics · doi:10.1093/hmg/ddh263 · Cited by 173 · see citing works
Role of p53 Serine 46 in p53 Target Gene Regulation
Smeenk, L., van Heeringen, S. J., Koeppel, M., Gilbert, B., Janssen‐Megens, E. M., Stunnenberg, H. G., & Lohrum, M. A. E. (2011) · PLoS ONE · doi:10.1371/journal.pone.0017574 · Cited by 169 · see citing works
p53 -Altered FBXW7 Expression Determines Poor Prognosis in Gastric Cancer Cases
Yokobori, T., Mimori, K., Iwatsuki, M., Ishii, H., Onoyama, I., Fukagawa, T., Kuwano, H., Nakayama, K. I., & Mori, M. (2009) · Cancer Research · doi:10.1158/0008-5472.can-08-2846 · Cited by 158 · see citing works
The Toll-like receptor gene family is integrated into human DNA damage and p53 networks
Menendez, D., Shatz, M., Azzam, K., Garantziotis, S., Fessler, M. B., & Resnick, M. A. (2011) · PLoS Genetics · doi:10.1371/journal.pgen.1001360 · Cited by 148 · see citing works
Self-citationLee, K. H., Li, M., Michalowski, A. M., Zhang, X., Liao, H., Chen, L., Xu, Y., Wu, X., & Huang, J. L. (2009) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0909734107 · Cited by 144 · see citing works
Production and Titration of Lentiviral Vectors
Salmon, P., & Trono, D. (2006) · Current Protocols in Neuroscience · doi:10.1002/0471142301.ns0421s37 · Cited by 125 · see citing works
Hockley, S. L., Arlt, V. M., Brewer, D. S., Giddings, I., & Phillips, D. H. (2006) · BMC Genomics · doi:10.1186/1471-2164-7-260 · Cited by 124 · see citing works
Redefining the p53 response element
Wang, B., Xiao, Z., & Ren, E. C. (2009) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0903284106 · Cited by 116 · see citing works
Mechanisms of regulatory diversity within the p53 transcriptional network
Espinosa, J. M. (2008) · Oncogene · doi:10.1038/onc.2008.37 · Cited by 114 · see citing works
Algorithm for prediction of tumour suppressor p53 affinity for binding sites in DNA
Veprintsev, D. B., & Fersht, A. R. (2008) · Nucleic Acids Research · doi:10.1093/nar/gkm1040 · Cited by 109 · see citing works
Noncanonical DNA Motifs as Transactivation Targets by Wild Type and Mutant p53
Jordan, J. J., Menendez, D., Inga, A., Nourredine, M., Bell, D., & Resnick, M. A. (2008) · PLoS Genetics · doi:10.1371/journal.pgen.1000104 · Cited by 103 · see citing works
Self-citationStaib, F., Robles, A. I., Varticovski, L., Wang, X. W., Zeebèrg, B. R., Sirotin, M., Zhurkin, V. B., Hofseth, L. J., Hussain, S. P., Weinstein, J. N., et al. (2005) · Cancer Research · doi:10.1158/0008-5472.can-05-1714 · Cited by 103 · see citing works
Fbw7 and p53 Cooperatively Suppress Advanced and Chromosomally Unstable Intestinal Cancer
Grim, J. E., Knoblaugh, S. E., Guthrie, K. A., Hagar, A., Swanger, J., Hespelt, J., Delrow, J. J., Small, T., Grady, W. M., Nakayama, K. I., et al. (2012) · Molecular and Cellular Biology · doi:10.1128/mcb.00305-12 · Cited by 97 · see citing works
Joachim, T., Ram, Z., Rappaport, Z. H., et al. (2001) · International Journal of Cancer · doi:10.1002/ijc.1467 · Cited by 91 · see citing works
The p53 response element and transcriptional repression
Wang, B., Xiao, Z., Ko, H. L., & Ren, E.-C. (2010) · Cell Cycle · doi:10.4161/cc.9.5.10825 · Cited by 90 · see citing works
Distinct p53 genomic binding patterns in normal and cancer-derived human cells
Botcheva, K., McCorkle, S., McCombie, W. R., Dunn, J. J., & Anderson, C. W. (2011) · Cell Cycle · doi:10.4161/cc.10.24.18383 · Cited by 83 · see citing works
Self-citationA SNP in the flt-1 promoter integrates the VEGF system into the p53 transcriptional network
Menéndez, D., Krysiak, O., Inga, A., Krysiak, B., Resnick, M. A., & Schönfelder, G. (2006) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0508103103 · Cited by 82 · see citing works
Self-citationFunctional Analysis of p53 Binding under Differential Stresses
Krieg, A. J., Hammond, E. M., & Giaccia, A. J. (2006) · Molecular and Cellular Biology · doi:10.1128/mcb.00322-06 · Cited by 66 · see citing works
CLEAN: CLustering Enrichment ANalysis
Freudenberg, J., Joshi, V. K., Hu, Z., & Medvedovic, M. (2009) · BMC Bioinformatics · doi:10.1186/1471-2105-10-234 · Cited by 64 · see citing works
Self-citationFu, D.-Y., Wang, Z.-M., Wang, B.-L., Chen, L., Yang, W.-T., Shen, Z., Huang, W. C., & Shao, Z. (2009) · Human Pathology · doi:10.1016/j.humpath.2009.06.007 · Cited by 59 · see citing works
p53 induces distinct epigenetic states at its direct target promoters
Vrba, L., Junk, D. J., Novák, P., & Futscher, B. W. (2008) · BMC Genomics · doi:10.1186/1471-2164-9-486 · Cited by 58 · see citing works
Shaked, H., Shiff, I., Kott-Gutkowski, M., Siegfried, Z., Haupt, Y., & Simon, I. (2008) · Cancer Research · doi:10.1158/0008-5472.can-08-0865 · Cited by 57 · see citing works
An integrated map of p53-binding sites and histone modification in the human ENCODE regions
Kaneshiro, K., Tsutsumi, S., Tsuji, S., Shirahige, K., & Aburatani, H. (2006) · Genomics · doi:10.1016/j.ygeno.2006.09.001 · Cited by 52 · see citing works
Menéndez, D., Inga, A., & Resnick, M. A. (2010) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0909129107 · Cited by 48 · see citing works
Self-citationMethyl‐CpG binding column‐based identification of nine genes hypermethylated in colorectal cancer
Kober, P., Bujko, M., Olędzki, J., Tysarowski, A., & SIEDLECKI, J. A. (2011) · Molecular Carcinogenesis · doi:10.1002/mc.20763 · Cited by 47 · see citing works
Noureddine, M., Menéndez, D., Campbell, M. R., Bandele, O. J., Horvath, M. M., Wang, X., Pittman, G. S., Chorley, B. N., Resnick, M. A., & Bell, D. A. (2009) · PLoS Genetics · doi:10.1371/journal.pgen.1000462 · Cited by 45 · see citing works
Self-citationWalker, M. M., Ellis, S. M., Auza, M. J., et al. (2007) · Modern Pathology · doi:10.1038/modpathol.3800988 · Cited by 27 · see citing works
Purrington, K. S., Wang, X., Fredericksen, Z., et al. (2011) · Breast Cancer Research and Treatment · doi:10.1007/s10549-011-1587-y · Cited by 26 · see citing works
A role for the p53 pathway in the pathology of meningiomas with NF2 loss
Chang, Z., Guo, C., Ahronowitz, I. Z., Stemmer-Rachamimov, A. O., MacCollin, M., & Nunes, F. P. (2008) · Journal of Neuro-Oncology · doi:10.1007/s11060-008-9721-3 · Cited by 25 · see citing works
Synergy of Nf2 and p53 mutations in development of malignant tumours of neural crest origin
Robanus-Maandag, E. C., Giovannini, M., van der Valk, M., Niwa‐Kawakita, M., Abramowski, V., Antonescu, C., Thomas, G. D., & Berns, A. J. M. (2004) · Oncogene · doi:10.1038/sj.onc.1207858 · Cited by 24 · see citing works
Yan, J., Menéndez, D., Yang, X.-P., Resnick, M. A., & Jetten, A. M. (2009) · Journal of Biological Chemistry · doi:10.1074/jbc.m109.013102 · Cited by 16 · see citing works
Self-citationMillau, J., Bastien, N., Bouchard, É. F., & Drouin, R. (2009) · Cancer Research · doi:10.1158/0008-5472.can-09-2036 · Cited by 16 · see citing works
A half-site of the p53-binding site on the keratin 14 promoter is specifically activated by p63
Cai, B., Chao, C.-F., Lu, M.-H., Lin, H.-C., & Chen, J.-Y. (2012) · The Journal of Biochemistry · doi:10.1093/jb/mvs053 · Cited by 16 · see citing works
Zhu, H., Smith, C. C., Ansah, C., & Gooderham, N. J. (2005) · Cancer Cell International · doi:10.1186/1475-2867-5-28 · Cited by 15 · see citing works
Flagged first, then by citations
Cited by
Sorted by citations
Census and evaluation of p53 target genes
Fischer, M. (2017) · Oncogene · doi:10.1038/onc.2016.502 · Cited by 971 · see citing works
iRegulon: From a Gene List to a Gene Regulatory Network Using Large Motif and Track Collections
Janky, R., Verfaillie, A., Imrichová, H., Van de Sande, B., Standaert, L., Christiaens, V., Hulselmans, G., Herten, K., Naval Sanchez, M., Potier, D., et al. (2014) · PLoS Computational Biology · doi:10.1371/journal.pcbi.1003731 · Cited by 900 · see citing works
“When extending the analysis and including target genes recently reported in literature [58,59,68], it becomes clear that most overlap coincides within this metatargetome (34/44) (Table S6).”
BackgroundFischer, M., Grossmann, P., Padi, M., & DeCaprio, J. A. (2016) · Nucleic Acids Research · doi:10.1093/nar/gkw523 · Cited by 330 · see citing works
The transcription factor p53: Not a repressor, solely an activator.
Fischer, M., Steiner, L., & Engeland, K. (2014) · Cell Cycle · doi:10.4161/15384101.2014.949083 · Cited by 153 · see citing works
TRIM67 Activates p53 to Suppress Colorectal Cancer Initiation and Progression
Wang, S., Zhang, Y., Huang, J., Wong, C. C., Zhai, J., Li, C., Wei, G., Zhao, L., Wang, G., Wei, H., et al. (2019) · Cancer Research · doi:10.1158/0008-5472.can-18-3614 · Cited by 104 · see citing works
Integrative genomic analysis reveals widespread enhancer regulation by p53 in response to DNA damage
Younger, S. T., Kenzelmann-Broz, D., Jung, H., Attardi, L. D., & Rinn, J. L. (2015) · Nucleic Acids Research · doi:10.1093/nar/gkv284 · Cited by 99 · see citing works
Multiplex enhancer-reporter assays uncover unsophisticated TP53 enhancer logic
Verfaillie, A., Svetlichnyy, D., Imrichova, H., Davie, K., Fiers, M., Kalender Atak, Z., Hulselmans, G., Christiaens, V., & Aerts, S. (2016) · Genome Research · doi:10.1101/gr.204149.116 · Cited by 82 · see citing works
Whole-genome cartography of p53 response elements ranked on transactivation potential
Tebaldi, T., Zaccara, S., Alessandrini, F., Bisio, A., Ciribilli, Y., & Inga, A. (2015) · BMC Genomics · doi:10.1186/s12864-015-1643-9 · Cited by 72 · see citing works
Ligand dependent restoration of human TLR3 signaling and death in p53 mutant cells
Menendez, D., Lowe, J. M., Snipe, J., & Resnick, M. A. (2016) · Oncotarget · doi:10.18632/oncotarget.11210 · Cited by 31 · see citing works
Self-citationMenendez, D., Anand, J. R., Murphy, C. C., Bell, W. J., Fu, J., Slepushkina, N., Buehler, E., Martin, S. E., Lal-Nag, M., Nitiss, J. L., et al. (2022) · Oncotarget · doi:10.18632/oncotarget.28195 · Cited by 22 · see citing works
Self-citation
- Authors
- Menendez, D., Nguyen, T.-A., Freudenberg, J. M., Mathew, V. J., Anderson, C. W., Jothi, R., & Resnick, M. A.
- Affiliations
- National Institutes of Health (US)
- Corresponding author
- Jothi, Raja
- Venue
- Nucleic Acids Research
- Publisher
- Oxford University Press (OUP)
- Published
- 2013-06-17
- Volume
- 41
- Issue
- 15
- Pages
- 7286-7301
- ISSN
- 0305-1048 (ISSN-L)
- 1362-4962
- PMC
- PMC3753631
- OpenAlex
- W2118254139
- Cited by
- 154
- References
- 71
- Citations by year
- 2026: 5 · 2025: 7 · 2024: 11 · 2023: 16 · 2022: 8 · 2021: 7 · 2020: 9 · 2019: 6 · 2018: 4 · 2017: 26 · 2016: 14 · 2015: 17 · 2014: 24
- FWCI
- 9.82
- Type
- journal article
- Language
- en
- Open access
- gold
- doi.org
- Licence
- public-domain
- Locations
- Nucleic Acids Research (publishedVersion, public-domain)
- Europe PMC (PubMed Central) (publishedVersion, public-domain)
- PubMed Central (publishedVersion, public-domain)
- PubMed (publishedVersion)
- Funders
- Johns Hopkins University
- National Institutes of Health
- U.S. Public Health Service (1ZIAES102625-04)
- National Institute of Environmental Health Sciences (Z01ES065079, ZIAES102625)
- 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, p53 binding sites, p53 transactivation, transcriptional regulation, stress response, doxorubicin, nutlin, dimethyl sulfoxide, p53 target genes, histone H3 lysine 4 trimethylation, chromatin, osteosarcoma, tumor suppression
- MeSH terms
- Antineoplastic Agents, Binding Sites, Dimethyl Sulfoxide, DNA, Neoplasm, Doxorubicin, Histones, Humans, Imidazoles, Methylation, Piperazines, Promoter Regions, Genetic, Protein Binding, Osteosarcoma, Transcriptional Activation, Gene Expression Regulation, Neoplastic, Genes, p53, Tumor Suppressor Protein p53, Consensus Sequence, HCT116 Cells, Gene Regulatory Networks, Nucleotide Motifs
About these checks
Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.
Statistics and arithmetic are recomputed, not judged.
Confidence bands are shown only for fields calibrated on our annotated test set. None is calibrated yet, so no band is shown.
What counts as a claim ›How we measure confidence ›How we check this ›
Are you an author, or do you see a problem with this page? Request a review