The Rich World of p53 DNA Binding Targets: The Role of DNA Structure
Jazyk angličtina Země Švýcarsko Médium electronic
Typ dokumentu časopisecké články, přehledy
Grantová podpora
18-15548S
Grantová Agentura České Republiky
CZ.02.1.01/0.0/0.0/15 003/0000477
European Regional Development Fund
PubMed
31717504
PubMed Central
PMC6888028
DOI
10.3390/ijms20225605
PII: ijms20225605
Knihovny.cz E-zdroje
- Klíčová slova
- consensus sequence, cruciform, local DNA structures, p53, protein-DNA interactions,
- MeSH
- DNA chemie metabolismus MeSH
- konformace nukleové kyseliny MeSH
- konformace proteinů MeSH
- konsenzuální sekvence MeSH
- lidé MeSH
- molekulární modely MeSH
- nádorový supresorový protein p53 chemie metabolismus MeSH
- sekvence aminokyselin MeSH
- vazba proteinů MeSH
- vazebná místa MeSH
- zvířata MeSH
- Check Tag
- lidé MeSH
- zvířata MeSH
- Publikační typ
- časopisecké články MeSH
- přehledy MeSH
- Názvy látek
- DNA MeSH
- nádorový supresorový protein p53 MeSH
The tumor suppressor functions of p53 and its roles in regulating the cell cycle, apoptosis, senescence, and metabolism are accomplished mainly by its interactions with DNA. p53 works as a transcription factor for a significant number of genes. Most p53 target genes contain so-called p53 response elements in their promoters, consisting of 20 bp long canonical consensus sequences. Compared to other transcription factors, which usually bind to one concrete and clearly defined DNA target, the p53 consensus sequence is not strict, but contains two repeats of a 5'RRRCWWGYYY3' sequence; therefore it varies remarkably among target genes. Moreover, p53 binds also to DNA fragments that at least partially and often completely lack this consensus sequence. p53 also binds with high affinity to a variety of non-B DNA structures including Holliday junctions, cruciform structures, quadruplex DNA, triplex DNA, DNA loops, bulged DNA, and hemicatenane DNA. In this review, we summarize information of the interactions of p53 with various DNA targets and discuss the functional consequences of the rich world of p53 DNA binding targets for its complex regulatory functions.
Zobrazit více v PubMed
Vousden K.H., Lane D.P. p53 in health and disease. Nat. Rev. Mol. Cell Biol. 2007;8:275–283. doi: 10.1038/nrm2147. PubMed DOI
Gohler T., Reimann M., Cherny D., Walter K., Warnecke G., Kim E., Deppert W. Specific interaction of p53 with target binding sites is determined by DNA conformation and is regulated by the C-terminal domain. J. Biol. Chem. 2002;277:41192–41203. doi: 10.1074/jbc.M202344200. PubMed DOI
Meek D.W. Regulation of the p53 response and its relationship to cancer. Biochem. J. 2015;469:325–346. doi: 10.1042/BJ20150517. PubMed DOI
Kaiser H.E., Bodey B. The role of apoptosis in normal ontogenesis and solid human neoplasms. In Vivo. 2000;14:789–803. PubMed
Kylarová D., Vrchovecký J., Holinka M., Erdösová B. The occurrence of c-myc, p53 and Bcl-2 family proteins in the early phase of development of duodenal epithelium. Biomed. Pap. Med. Fac. Univ. Palacky Olomouc Czech Repub. 2004;148:229–232. doi: 10.5507/bp.2004.046. PubMed DOI
Prochazkova J., Lichnovsky V., Kylarova D., Erdosova B., Vranka P. Involvement of p53 and Bcl-2 family proteins in regulating programmed cell death and proliferation in human embryogenesis. Gen. Physiol. Biophys. 2004;23:209–229. PubMed
Porrello A., Cerone M.A., Coen S., Gurtner A., Fontemaggi G., Cimino L., Piaggio G., Sacchi A., Soddu S. P53 Regulates Myogenesis by Triggering the Differentiation Activity of pRb. J. Cell Biol. 2000;151:1295–1304. doi: 10.1083/jcb.151.6.1295. PubMed DOI PMC
Vousden K.H., Ryan K.M. p53 and metabolism. Nat. Rev. Cancer. 2009;9:691–700. doi: 10.1038/nrc2715. PubMed DOI
Chen J. The Cell-Cycle Arrest and Apoptotic Functions of p53 in Tumor Initiation and Progression. Cold Spring Harb. Perspect. Med. 2016;6:a026104. doi: 10.1101/cshperspect.a026104. PubMed DOI PMC
Kaiser A.M., Attardi L.D. Deconstructing networks of p53-mediated tumor suppression in vivo. Cell Death Differ. 2018;25:93–103. doi: 10.1038/cdd.2017.171. PubMed DOI PMC
Wang X., Simpson E.R., Brown K.A. p53: Protection against Tumor Growth beyond Effects on Cell Cycle and Apoptosis. Cancer Res. 2015;75:5001–5007. doi: 10.1158/0008-5472.CAN-15-0563. PubMed DOI
Ranjan A., Iwakuma T. Non-Canonical Cell Death Induced by p53. Int. J. Mol. Sci. 2016;17:2068. doi: 10.3390/ijms17122068. PubMed DOI PMC
Pfaff M.J., Mukhopadhyay S., Hoofnagle M., Chabasse C., Sarkar R. Tumor suppressor protein p53 negatively regulates ischemia-induced angiogenesis and arteriogenesis. J. Vasc. Surg. 2018;68:222S–233S.e1. doi: 10.1016/j.jvs.2018.02.055. PubMed DOI PMC
Chandrangsu S., Sappayatosok K. p53, p63 and p73 expression and angiogenesis in keratocystic odontogenic tumors. J. Clin. Exp. Dent. 2016;8:e505–e511. doi: 10.4317/jced.52843. PubMed DOI PMC
Williams A.B., Schumacher B. p53 in the DNA-Damage-Repair Process. Cold Spring Harb. Perspect. Med. 2016;6:a026070. doi: 10.1101/cshperspect.a026070. PubMed DOI PMC
Nicolai S., Rossi A., Di Daniele N., Melino G., Annicchiarico-Petruzzelli M., Raschellà G. DNA repair and aging: The impact of the p53 family. Aging. 2015;7:1050–1065. doi: 10.18632/aging.100858. PubMed DOI PMC
Rufini A., Tucci P., Celardo I., Melino G. Senescence and aging: The critical roles of p53. Oncogene. 2013 doi: 10.1038/onc.2012.640. PubMed DOI
Hussain M., Tian K., Mutti L., Krstic-Demonacos M., Schwartz J.-M. The Expanded p53 Interactome as a Predictive Model for Cancer Therapy. Genom. Comput. Biol. 2015;1:e20. doi: 10.18547/gcb.2015.vol1.iss1.e20. DOI
Muller P.A.J., Vousden K.H. p53 mutations in cancer. Nat. Cell Biol. 2013;15:2–8. doi: 10.1038/ncb2641. PubMed DOI
Valenti F., Fausti F., Biagioni F., Shay T., Fontemaggi G., Domany E., Yaffe M.B., Strano S., Blandino G., Di Agostino S. Mutant p53 oncogenic functions are sustained by Plk2 kinase through an autoregulatory feedback loop. Cell Cycle. 2011;10:4330–4340. doi: 10.4161/cc.10.24.18682. PubMed DOI
Liu K., Ling S., Lin W.-C. TopBP1 mediates mutant p53 gain of function through NF-Y and p63/p73. Mol. Cell. Biol. 2011;31:4464–4481. doi: 10.1128/MCB.05574-11. PubMed DOI PMC
Stindt M.H., Muller P.A.J., Ludwig R.L., Kehrloesser S., Dötsch V., Vousden K.H. Functional interplay between MDM2, p63/p73 and mutant p53. Oncogene. 2015;34:4300–4310. doi: 10.1038/onc.2014.359. PubMed DOI PMC
Inoue K., Fry E.A., Frazier D.P. Transcription factors that interact with p53 and Mdm2. Int. J. Cancer. 2016;138:1577–1585. doi: 10.1002/ijc.29663. PubMed DOI PMC
Woods Y.L., Lane D.P. Exploiting the p53 pathway for cancer diagnosis and therapy. Hematol. J. 2003;4:233–247. doi: 10.1038/sj.thj.6200260. PubMed DOI
Cheok C.F., Lane D.P. Exploiting the p53 Pathway for Therapy. Cold Spring Harb. Perspect. Med. 2017;7:a026310. doi: 10.1101/cshperspect.a026310. PubMed DOI PMC
Levine A.J., Oren M. The first 30 years of p53: Growing ever more complex. Nat. Rev. Cancer. 2009;9:749–758. doi: 10.1038/nrc2723. PubMed DOI PMC
Lohrum M.A.E., Vousden K.H. Regulation and activation of p53 and its family members. Cell Death Differ. 1999;6:1162–1168. doi: 10.1038/sj.cdd.4400625. PubMed DOI
Zhao Y., Chen X., Du J. Cellular adaptation to hypoxia and p53 transcription regulation. J. Zhejiang Univ.-Sci. B. 2009;10:404–410. doi: 10.1631/jzus.B0820293. PubMed DOI PMC
Itoh Y., Murata A., Sakamoto S., Nanatani K., Wada T., Takahashi S., Kamagata K. Activation of p53 Facilitates the Target Search in DNA by Enhancing the Target Recognition Probability. J. Mol. Biol. 2016;428:2916–2930. doi: 10.1016/j.jmb.2016.06.001. PubMed DOI
Bochman M.L., Paeschke K., Zakian V.A. DNA secondary structures: Stability and function of G-quadruplex structures. Nat. Rev. Genet. 2012;13:770–780. doi: 10.1038/nrg3296. PubMed DOI PMC
Timsit Y. DNA Self-Assembly: From Chirality to Evolution. Int. J. Mol. Sci. 2013;14:8252–8270. doi: 10.3390/ijms14048252. PubMed DOI PMC
Frees S., Menendez C., Crum M., Bagga P.S. QGRS-Conserve: A computational method for discovering evolutionarily conserved G-quadruplex motifs. Hum. Genom. 2014;8:8. doi: 10.1186/1479-7364-8-8. PubMed DOI PMC
Palecek E. Local supercoil-stabilized DNA structures. Crit. Rev. Biochem. Mol. Biol. 1991;26:151–226. doi: 10.3109/10409239109081126. PubMed DOI
Travers A., Muskhelishvili G. DNA structure and function. FEBS J. 2015;282:2279–2295. doi: 10.1111/febs.13307. PubMed DOI
Yahyaoui W., Callejo M., Price G.B., Zannis-Hadjopoulos M. Deletion of the cruciform binding domain in CBP/14-3-3 displays reduced origin binding and initiation of DNA replication in budding yeast. BMC Mol. Biol. 2007;8:27. doi: 10.1186/1471-2199-8-27. PubMed DOI PMC
Bedrat A., Lacroix L., Mergny J.-L. Re-evaluation of G-quadruplex propensity with G4Hunter. Nucleic Acids Res. 2016;44:1746–1759. doi: 10.1093/nar/gkw006. PubMed DOI PMC
Brazdova M., Tichy V., Helma R., Bazantova P., Polaskova A., Krejci A., Petr M., Navratilova L., Ticha O., Nejedly K., et al. p53 Specifically Binds Triplex DNA In Vitro and in Cells. PLoS ONE. 2016;11:e0167439. doi: 10.1371/journal.pone.0167439. PubMed DOI PMC
Waller Z.A., Pinchbeck B.J., Buguth B.S., Meadows T.G., Richardson D.J., Gates A.J. Control of bacterial nitrate assimilation by stabilization of G-quadruplex DNA. Chem. Commun. 2016;52:13511–13514. doi: 10.1039/C6CC06057A. PubMed DOI PMC
Bartas M., Čutová M., Brázda V., Kaura P., Št’astnỳ J., Kolomazník J., Coufal J., Goswami P., Červeň J., Pečinka P. The Presence and Localization of G-Quadruplex Forming Sequences in the Domain of Bacteria. Molecules. 2019;24:1711. doi: 10.3390/molecules24091711. PubMed DOI PMC
Huppert J.L., Balasubramanian S. G-quadruplexes in promoters throughout the human genome. Nucleic Acids Res. 2006;35:406–413. doi: 10.1093/nar/gkl1057. PubMed DOI PMC
Siddiqui-Jain A., Grand C.L., Bearss D.J., Hurley L.H. Direct evidence for a G-quadruplex in a promoter region and its targeting with a small molecule to repress c-MYC transcription. Proc. Natl. Acad. Sci. USA. 2002;99:11593–11598. doi: 10.1073/pnas.182256799. PubMed DOI PMC
Rajeswari M.R. DNA triplex structures in neurodegenerative disorder, Friedreich’s ataxia. J. Biosci. 2012;37:519–532. doi: 10.1007/s12038-012-9219-1. PubMed DOI
Helma R., Bažantová P., Petr M., Adámik M., Renčiuk D., Tichý V., Pastuchová A., Soldánová Z., Pečinka P., Bowater R.P., et al. p53 Binds Preferentially to Non-B DNA Structures Formed by the Pyrimidine-Rich Strands of GAA·TTC Trinucleotide Repeats Associated with Friedreich’s Ataxia. Molecules. 2019;24:2078. doi: 10.3390/molecules24112078. PubMed DOI PMC
Cimino-Reale G., Zaffaroni N., Folini M. Emerging Role of G-quadruplex DNA as Target in Anticancer Therapy. Curr. Pharm. Des. 2016;22:6612–6624. doi: 10.2174/1381612822666160831101031. PubMed DOI
Asamitsu S., Obata S., Yu Z., Bando T., Sugiyama H. Recent Progress of Targeted G-Quadruplex-Preferred Ligands Toward Cancer Therapy. Molecules. 2019;24:429. doi: 10.3390/molecules24030429. PubMed DOI PMC
Ma B., Pan Y., Zheng J., Levine A.J., Nussinov R. Sequence analysis of p53 response-elements suggests multiple binding modes of the p53 tetramer to DNA targets. Nucleic Acids Res. 2007;35:2986–3001. doi: 10.1093/nar/gkm192. PubMed DOI PMC
Wei C.L., Wu Q., Vega V.B., Chiu K.P., Ng P., Zhang T., Shahab A., Yong H.C., Fu Y.T., Weng Z.P., et al. A global map of p53 transcription-factor binding sites in the human genome. Cell. 2006;124:207–219. doi: 10.1016/j.cell.2005.10.043. PubMed DOI
Menendez D., Inga A., Resnick M.A. The expanding universe of p53 targets. Nat. Rev. Cancer. 2009;9:724–737. doi: 10.1038/nrc2730. PubMed DOI
Menendez D., Inga A., Resnick M.A. Potentiating the p53 network. Discov. Med. 2010;10:94–100. PubMed
Wang B., Xiao Z., Ren E.C. Redefining the p53 response element. Proc. Natl. Acad. Sci. USA. 2009;106:14373–14378. doi: 10.1073/pnas.0903284106. PubMed DOI PMC
Allen M.A., Andrysik Z., Dengler V.L., Mellert H.S., Guarnieri A., Freeman J.A., Sullivan K.D., Galbraith M.D., Luo X., Kraus W.L., et al. Global analysis of p53-regulated transcription identifies its direct targets and unexpected regulatory mechanisms. Elite. 2014;3:e02200. PubMed PMC
Chang G.S., Chen X.A., Park B., Rhee H.S., Li P., Han K.H., Mishra T., Chan-Salis K.Y., Li Y., Hardison R.C., et al. A Comprehensive and High-Resolution Genome-wide Response of p53 to Stress. Cell Rep. 2014;8:513–526. doi: 10.1016/j.celrep.2014.06.030. PubMed DOI PMC
Cai B.-H., Chao C.-F., Huang H.-C., Lee H.-Y., Kannagi R., Chen J.-Y. Roles of p53 Family Structure and Function in Non-Canonical Response Element Binding and Activation. Int. J. Mol. Sci. 2019;20:3681. doi: 10.3390/ijms20153681. PubMed DOI PMC
El-Deiry W.S., Kern S.E., Pietenpol J.A., Kinzler K.W., Vogelstein B. Definition of a consensus binding site for p53. Nat. Genet. 1992;1:45. doi: 10.1038/ng0492-45. PubMed DOI
Qian H., Wang T., Naumovski L., Lopez C.D., Brachmann R.K. Groups of p53 target genes involved in specific p53 downstream effects cluster into different classes of DNA binding sites. Oncogene. 2002;21:7901–7911. doi: 10.1038/sj.onc.1205974. PubMed DOI
Veprintsev D.B., Fersht A.R. Algorithm for prediction of tumour suppressor p53 affinity for binding sites in DNA. Nucleic Acids Res. 2008;36:1589–1598. doi: 10.1093/nar/gkm1040. PubMed DOI PMC
Brazda V., Kolomaznik J., Lysek J., Haronikova L., Coufal J., Stastny J. Palindrome analyser—A new web-based server for predicting and evaluating inverted repeats in nucleotide sequences. Biochem. Biophys. Res. Commun. 2016;478:1739–1745. doi: 10.1016/j.bbrc.2016.09.015. PubMed DOI
McKinney K., Mattia M., Gottifredi V., Prives C. p53 linear diffusion along DNA requires its C terminus. Mol. Cell. 2004;16:413–424. doi: 10.1016/j.molcel.2004.09.032. PubMed DOI
Brazda V., Jagelska E.B., Fojta M., Palecek E. Searching for target sequences by p53 protein is influenced by DNA length. Biochem. Biophys. Res. Commun. 2006;341:470–477. doi: 10.1016/j.bbrc.2005.12.202. PubMed DOI
Itoh Y., Murata A., Takahashi S., Kamagata K. Intrinsically disordered domain of tumor suppressor p53 facilitates target search by ultrafast transfer between different DNA strands. Nucleic Acids Res. 2018;46:7261–7269. doi: 10.1093/nar/gky586. PubMed DOI PMC
Nguyen T.-A.T., Grimm S.A., Bushel P.R., Li J., Li Y., Bennett B.D., Lavender C.A., Ward J.M., Fargo D.C., Anderson C.W., et al. Revealing a human p53 universe. Nucleic Acids Res. 2018;46:8153–8167. doi: 10.1093/nar/gky720. PubMed DOI PMC
Kent W.J., Sugnet C.W., Furey T.S., Roskin K.M., Pringle T.H., Zahler A.M., Haussler D. The human genome browser at UCSC. Genome Res. 2002;12:996–1006. doi: 10.1101/gr.229102. PubMed DOI PMC
Raney B.J., Dreszer T.R., Barber G.P., Clawson H., Fujita P.A., Wang T., Nguyen N., Paten B., Zweig A.S., Karolchik D., et al. Track data hubs enable visualization of user-defined genome-wide annotations on the UCSC Genome Browser. Bioinformatics. 2014;30:1003–1005. doi: 10.1093/bioinformatics/btt637. PubMed DOI PMC
Tebaldi T., Zaccara S., Alessandrini F., Bisio A., Ciribilli Y., Inga A. Whole-genome cartography of p53 response elements ranked on transactivation potential. BMC Genom. 2015;16:464. doi: 10.1186/s12864-015-1643-9. PubMed DOI PMC
Bao X., Wu H., Zhu X., Guo X., Hutchins A.P., Luo Z., Song H., Chen Y., Lai K., Yin M., et al. The p53-induced lincRNA-p21 derails somatic cell reprogramming by sustaining H3K9me3 and CpG methylation at pluripotency gene promoters. Cell Res. 2015;25:80–92. doi: 10.1038/cr.2014.165. PubMed DOI PMC
Pivonkova H., Brazdova M., Kasparkova J., Brabec V., Fojta M. Recognition of cisplatin-damaged DNA by p53 protein: Critical role of the p53 C-terminal domain. Biochem. Biophys. Res. Commun. 2006;339:477–484. doi: 10.1016/j.bbrc.2005.11.038. PubMed DOI
Degtyareva N., Subramanian D., Griffith J.D. Analysis of the binding of p53 to DNAs containing mismatched and bulged bases. J. Biol. Chem. 2001;276:8778–8784. doi: 10.1074/jbc.M006795200. PubMed DOI
Walter K., Warnecke G., Bowater R., Deppert W., Ella K. Tumor suppressor p53 binds with high affinity to CTG center dot CAG trinucleotide repeats and induces topological alterations in mismatched duplexes. J. Biol. Chem. 2005;280:42497–42507. doi: 10.1074/jbc.M507038200. PubMed DOI
Joerger A.C., Fersht A.R. The tumor suppressor p53: From structures to drug discovery. Cold Spring Harb. Perspect. Biol. 2010;2:a000919. doi: 10.1101/cshperspect.a000919. PubMed DOI PMC
Bourdon J.-C., Fernandes K., Murray-Zmijewski F., Liu G., Diot A., Xirodimas D.P., Saville M.K., Lane D.P. p53 isoforms can regulate p53 transcriptional activity. Genes Dev. 2005;19:2122–2137. doi: 10.1101/gad.1339905. PubMed DOI PMC
Sabapathy K., Lane D.P. Understanding p53 functions through p53 antibodies. J. Mol. Cell Biol. 2019;11:317–329. doi: 10.1093/jmcb/mjz010. PubMed DOI PMC
Cho Y., Gorina S., Jeffrey P.D., Pavletich N.P. Crystal structure of a p53 tumor suppressor-DNA complex: Understanding tumorigenic mutations. Science. 1994;265:346–355. doi: 10.1126/science.8023157. PubMed DOI
Zhao K., Chai X., Johnston K., Clements A., Marmorstein R. Crystal structure of the mouse p53 core DNA-binding domain at 2.7 A resolution. J. Biol. Chem. 2001;276:12120–12127. doi: 10.1074/jbc.M011644200. PubMed DOI
Joerger A.C., Allen M.D., Fersht A.R. Crystal structure of a superstable mutant of human p53 core domain. Insights into the mechanism of rescuing oncogenic mutations. J. Biol. Chem. 2004;279:1291–1296. doi: 10.1074/jbc.M309732200. PubMed DOI
Suad O., Rozenberg H., Brosh R., Diskin-Posner Y., Kessler N., Shimon L.J.W., Frolow F., Liran A., Rotter V., Shakked Z. Structural basis of restoring sequence-specific DNA binding and transactivation to mutant p53 by suppressor mutations. J. Mol. Biol. 2009;385:249–265. doi: 10.1016/j.jmb.2008.10.063. PubMed DOI
Malecka K.A., Ho W.C., Marmorstein R. Crystal structure of a p53 core tetramer bound to DNA. Oncogene. 2009;28:325–333. doi: 10.1038/onc.2008.400. PubMed DOI PMC
Nagaich A.K., Appella E., Harrington R.E. DNA bending is essential for the site-specific recognition of DNA response elements by the DNA binding domain of the tumor suppressor protein p53. J. Biol. Chem. 1997;272:14842–14849. doi: 10.1074/jbc.272.23.14842. PubMed DOI
Yang J., Yan R., Roy A., Xu D., Poisson J., Zhang Y. The I-TASSER Suite: Protein structure and function prediction. Nat. Methods. 2015;12:7–8. doi: 10.1038/nmeth.3213. PubMed DOI PMC
Yan Y., Zhang D., Zhou P., Li B., Huang S.-Y. HDOCK: A web server for protein-protein and protein-DNA/RNA docking based on a hybrid strategy. Nucleic Acids Res. 2017;45:W365–W373. doi: 10.1093/nar/gkx407. PubMed DOI PMC
Pettersen E.F., Goddard T.D., Huang C.C., Couch G.S., Greenblatt D.M., Meng E.C., Ferrin T.E. UCSF Chimera—A visualization system for exploratory research and analysis. J. Comput. Chem. 2004;25:1605–1612. doi: 10.1002/jcc.20084. PubMed DOI
Bakalkin G., Yakovleva T., Selivanova G., Magnusson K.P., Szekely L., Kiseleva E., Klein G., Terenius L., Wiman K.G. p53 binds single-stranded DNA ends and catalyzes DNA renaturation and strand transfer. Proc. Natl. Acad. Sci. USA. 1994;91:413–417. doi: 10.1073/pnas.91.1.413. PubMed DOI PMC
Bakalkin G., Selivanova G., Yakovleva T., Kiseleva E., Kashuba E., Magnusson K.P., Szekely L., Klein G., Terenius L., Wiman K.G. p53 binds single-stranded DNA ends through the C-terminal domain and internal DNA segments via the middle domain. Nucleic Acids Res. 1995;23:362–369. doi: 10.1093/nar/23.3.362. PubMed DOI PMC
Brázda V., Coufal J. Recognition of local DNA structures by p53 protein. Int. J. Mol. Sci. 2017;18:375. doi: 10.3390/ijms18020375. PubMed DOI PMC
Palecek E., Vlk D., Stankova V., Brazda V., Vojtesek B., Hupp T.R., Schaper A., Jovin T.M. Tumor suppressor protein p53 binds preferentially to supercoiled DNA. Oncogene. 1997;15:2201–2209. doi: 10.1038/sj.onc.1201398. PubMed DOI
Palecek E., Brazda V., Jagelska E., Pecinka P., Karlovska L., Brazdova M. Enhancement of p53 sequence-specific binding by DNA supercoiling. Oncogene. 2004;23:2119–2127. doi: 10.1038/sj.onc.1207324. PubMed DOI
Brázda V., Paleĉek J., Pospísilová S., Vojtêsek B., Paleĉek E. Specific modulation of p53 binding to consensus sequence within supercoiled DNA by monoclonal antibodies. Biochem. Biophys. Res. Commun. 2000;267:934–939. doi: 10.1006/bbrc.1999.2056. PubMed DOI
Palecek E., Brazdova M., Brazda V., Palecek J., Billova S., Subramaniam V., Jovin T.M. Binding of p53 and its core domain to supercoiled DNA. Eur. J. Biochem. 2001;268:573–581. doi: 10.1046/j.1432-1327.2001.01898.x. PubMed DOI
Brazdova M., Navratilova L., Tichy V., Nemcova K., Lexa M., Hrstka R., Pecinka P., Adamik M., Vojtesek B., Palecek E., et al. Preferential Binding of Hot Spot Mutant p53 Proteins to Supercoiled DNA In Vitro and in Cells. PLoS ONE. 2013;8:e59567. doi: 10.1371/journal.pone.0059567. PubMed DOI PMC
Mazur S.J., Sakaguchi K., Appella E., Wang X.W., Harris C.C., Bohr V.A. Preferential binding of tumor suppressor p53 to positively or negatively supercoiled DNA involves the C-terminal domain. J. Mol. Biol. 1999;292:241–249. doi: 10.1006/jmbi.1999.3064. PubMed DOI
Pivonkova H., Sebest P., Pecinka P., Ticha O., Nemcova K., Brazdova M., Jagelska E.B., Brazda V., Fojta M. Selective binding of tumor suppressor p53 protein to topologically constrained DNA: Modulation by intercalative drugs. Biochem. Biophys. Res. Commun. 2010;393:894–899. doi: 10.1016/j.bbrc.2010.02.120. PubMed DOI
Sandri M.I., Isaacs R.J., Ongkeko W.M., Harris A.L., Hickson I.D., Broggini M., Vikhanskaya F. p53 regulates the minimal promoter of the human topoisomerase IIalpha gene. Nucleic Acids Res. 1996;24:4464–4470. doi: 10.1093/nar/24.22.4464. PubMed DOI PMC
Jagelska E.B., Brazda V., Pecinka P., Palecek E., Fojta M. DNA topology influences p53 sequence-specific DNA binding through structural transitions within the target sites. Biochem. J. 2008;412:57–63. doi: 10.1042/BJ20071648. PubMed DOI
Carvalho C.M.B., Zhang F., Lupski J.R. Structural variation of the human genome: Mechanisms, assays, and role in male infertility. Syst. Biol. Reprod. Mech. 2011;57:3–16. doi: 10.3109/19396368.2010.527427. PubMed DOI PMC
Warburton P.E., Giordano J., Cheung F., Gelfand Y., Benson G. Inverted repeat structure of the human genome: The X-chromosome contains a preponderance of large, highly homologous inverted repeats that contain testes genes. Genome Res. 2004;14:1861–1869. doi: 10.1101/gr.2542904. PubMed DOI PMC
Feuk L., Carson A.R., Scherer S.W. Structural variation in the human genome. Nat. Rev. Genet. 2006;7:85–97. doi: 10.1038/nrg1767. PubMed DOI
Burger A.M., Dai F., Schultes C.M., Reszka A.P., Moore M.J., Double J.A., Neidle S. The G-Quadruplex-Interactive Molecule BRACO-19 Inhibits Tumor Growth, Consistent with Telomere Targeting and Interference with Telomerase Function. Cancer Res. 2005;65:1489–1496. doi: 10.1158/0008-5472.CAN-04-2910. PubMed DOI
Lee S., Ho J.Y., Liu J.J., Lee H., Park J.Y., Baik M., Ko M., Lee S.U., Choi Y.J., Hur S.Y. CKD-602, a topoisomerase I inhibitor, induces apoptosis and cell-cycle arrest and inhibits invasion in cervical cancer. Mol. Med. 2019;25:23. doi: 10.1186/s10020-019-0089-y. PubMed DOI PMC
Zheng K.-W., He Y., Liu H.-H., Li X.-M., Hao Y.-H., Tan Z. Superhelicity Constrains a Localized and R-Loop-Dependent Formation of G-Quadruplexes at the Upstream Region of Transcription. ACS Chem. Biol. 2017;12:2609–2618. doi: 10.1021/acschembio.7b00435. PubMed DOI
Lee S.M., Cavallo L., Griffith J. Human p53 binds Holliday junctions strongly and facilitates their cleavage. J. Biol. Chem. 1997;272:7532–7539. doi: 10.1074/jbc.272.11.7532. PubMed DOI
Subramanian D., Griffith J.D. p53 Monitors replication fork regression by binding to “chickenfoot” intermediates. J. Biol. Chem. 2005;280:42568–42572. doi: 10.1074/jbc.M506348200. PubMed DOI
Stansel R.M., Subramanian D., Griffith J.D. p53 binds telomeric single strand overhangs and t-loop junctions in vitro. J. Biol. Chem. 2002;277:11625–11628. doi: 10.1074/jbc.C100764200. PubMed DOI
Stros M., Muselikova-Polanska E., Pospisilova S., Strauss F. High-affinity binding of tumor-suppressor protein p53 and HMGB1 to hemicatenated DNA loops. Biochemistry. 2004;43:7215–7225. doi: 10.1021/bi049928k. PubMed DOI
Brazda V., Laister R.C., Jagelska E.B., Arrowsmith C. Cruciform structures are a common DNA feature important for regulating biological processes. BMC Mol. Biol. 2011;12:33. doi: 10.1186/1471-2199-12-33. PubMed DOI PMC
Coufal J., Jagelska E.B., Liao J.C.C., Brazda V. Preferential binding of p53 tumor suppressor to p21 promoter sites that contain inverted repeats capable of forming cruciform structure. Biochem. Biophys. Res. Commun. 2013;441:83–88. doi: 10.1016/j.bbrc.2013.10.015. PubMed DOI
Čechová J., Coufal J., Jagelská E.B., Fojta M., Brázda V. p73, like its p53 homolog, shows preference for inverted repeats forming cruciforms. PLoS ONE. 2018;13:e0195835. doi: 10.1371/journal.pone.0195835. PubMed DOI PMC
Brazda V., Cechova J., Battistin M., Coufal J., Jagelska E.B., Raimondi I., Inga A. The structure formed by inverted repeats in p53 response elements determines the transactivation activity of p53 protein. Biochem. Biophys. Res. Commun. 2017;483:516–521. doi: 10.1016/j.bbrc.2016.12.113. PubMed DOI
Petr M., Helma R., Polaskova A., Krejci A., Dvorakova Z., Kejnovska I., Navratilova L., Adamik M., Vorlickova M., Brazdova M. Wild-type p53 binds to MYC promoter G-quadruplex. Biosci. Rep. 2016;36:e00397. doi: 10.1042/BSR20160232. PubMed DOI PMC
Adamik M., Kejnovska I., Bazantova P., Petr M., Renciuk D., Vorlickova M., Brazdova M. p53 binds human telomeric G-quadruplex in vitro. Biochimie. 2016;128:83–91. doi: 10.1016/j.biochi.2016.07.004. PubMed DOI
Lee S.-H., Siaw G.E.-L., Willcox S., Griffith J.D., Hsieh T.-S. Synthesis and dissolution of hemicatenanes by type IA DNA topoisomerases. Proc. Natl. Acad. Sci. USA. 2013;110:E3587–E3594. doi: 10.1073/pnas.1304103110. PubMed DOI PMC
Bush N.G., Evans-Roberts K., Maxwell A. DNA Topoisomerases. EcoSal Plus. 2015;6 doi: 10.1128/ecosalplus.ESP-0010-2014. PubMed DOI
Lee S.-J., No Y.R., Dang D.T., Dang L.H., Yang V.W., Shim H., Yun C.C. Regulation of Hypoxia-inducible Factor 1 alpha (HIF-1 alpha) by Lysophosphatidic Acid Is Dependent on Interplay between p53 and Kruppel-like Factor 5. J. Biol. Chem. 2013;288:25244–25253. doi: 10.1074/jbc.M113.489708. PubMed DOI PMC
Stros M., Ozaki T., Bacikova A., Kageyama H., Nakagawara A. HMGB1 and HMGB2 cell-specifically down-regulate the p53- and p73- dependent sequence-specific transactivation from the human Bax gene promoter. J. Biol. Chem. 2002;277:7157–7164. doi: 10.1074/jbc.M110233200. PubMed DOI
Griffith J.D., Comeau L., Rosenfield S., Stansel R.M., Bianchi A., Moss H., de Lange T. Mammalian telomeres end in a large duplex loop. Cell. 1999;97:503–514. doi: 10.1016/S0092-8674(00)80760-6. PubMed DOI
Kar A., Willcox S., Griffith J.D. Transcription of telomeric DNA leads to high levels of homologous recombination and t-loops. Nucleic Acids Res. 2016;44:9369–9380. doi: 10.1093/nar/gkw779. PubMed DOI PMC
Stansel R.M., de Lange T., Griffith J.D. T-loop assembly in vitro involves binding of TRF2 near the 3′ telomeric overhang. EMBO J. 2001;20:5532–5540. doi: 10.1093/emboj/20.19.5532. PubMed DOI PMC
Tutton S., Azzam G.A., Stong N., Vladimirova O., Wiedmer A., Monteith J.A., Beishline K., Wang Z., Deng Z., Riethman H., et al. Subtelomeric p53 binding prevents accumulation of DNA damage at human telomeres. EMBO J. 2016;35:193–207. doi: 10.15252/embj.201490880. PubMed DOI PMC
Lieberman P.M. Retrotransposon-derived p53 binding sites enhance telomere maintenance and genome protection. Bioessays. 2016;38:943–949. doi: 10.1002/bies.201600078. PubMed DOI PMC
Frank-Kamenetskii M.D., Mirkin S.M. Triplex DNA structures. Annu. Rev. Biochem. 1995;64:65–95. doi: 10.1146/annurev.bi.64.070195.000433. PubMed DOI
Li Y., Syed J., Sugiyama H. RNA-DNA Triplex Formation by Long Noncoding RNAs. Cell Chem. Biol. 2016;23:1325–1333. doi: 10.1016/j.chembiol.2016.09.011. PubMed DOI
Thomas T.J., Faaland C.A., Gallo M.A., Thomas T. Suppression of c-myc oncogene expression by a polyamine-complexed triplex forming oligonucleotide in MCF-7 breast cancer cells. Nucleic Acids Res. 1995;23:3594–3599. doi: 10.1093/nar/23.17.3594. PubMed DOI PMC
Zhang S., Wu Y., Zhang W. G-quadruplex structures and their interaction diversity with ligands. ChemMedChem. 2014;9:899–911. doi: 10.1002/cmdc.201300566. PubMed DOI
Day H.A., Pavlou P., Waller Z.A.E. i-Motif DNA: Structure, stability and targeting with ligands. Bioorg. Med. Chem. 2014;22:4407–4418. doi: 10.1016/j.bmc.2014.05.047. PubMed DOI
Kumar N., Maiti S. A thermodynamic overview of naturally occurring intramolecular DNA quadruplexes. Nucleic Acids Res. 2008;36:5610–5622. doi: 10.1093/nar/gkn543. PubMed DOI PMC
Lane A.N., Chaires J.B., Gray R.D., Trent J.O. Stability and kinetics of G-quadruplex structures. Nucleic Acids Res. 2008;36:5482–5515. doi: 10.1093/nar/gkn517. PubMed DOI PMC
Neidle S., Parkinson G.N. Quadruplex DNA crystal structures and drug design. Biochimie. 2008;90:1184–1196. doi: 10.1016/j.biochi.2008.03.003. PubMed DOI
Neidle S. The structures of quadruplex nucleic acids and their drug complexes. Curr. Opin. Struct. Biol. 2009;19:239–250. doi: 10.1016/j.sbi.2009.04.001. PubMed DOI
Rhodes D., Lipps H.J. G-quadruplexes and their regulatory roles in biology. Nucleic Acids Res. 2015;43:8627–8637. doi: 10.1093/nar/gkv862. PubMed DOI PMC
Haronikova L., Coufal J., Kejnovska I., Jagelska E.B., Fojta M., Dvorakova P., Muller P., Vojtesek B., Brazda V. IFI16 Preferentially Binds to DNA with Quadruplex Structure and Enhances DNA Quadruplex Formation. PLoS ONE. 2016;11:e0157156. doi: 10.1371/journal.pone.0157156. PubMed DOI PMC
Kharel P., Balaratnam S., Beals N., Basu S. The role of RNA G-quadruplexes in human diseases and therapeutic strategies. Wiley Interdiscip. Rev. RNA. 2019:e1568. doi: 10.1002/wrna.1568. PubMed DOI
Gomes A.S., Trovão F., Andrade Pinheiro B., Freire F., Gomes S., Oliveira C., Domingues L., Romão M.J., Saraiva L., Carvalho A.L. The Crystal Structure of the R280K Mutant of Human p53 Explains the Loss of DNA Binding. Int. J. Mol. Sci. 2018;19:1184. doi: 10.3390/ijms19041184. PubMed DOI PMC
Oren M., Rotter V. Mutant p53 Gain-of-Function in Cancer. Cold Spring Harb. Perspect. Biol. 2010;2:a001107. doi: 10.1101/cshperspect.a001107. PubMed DOI PMC
Vaughan C., Pearsall I., Yeudall A., Deb S.P., Deb S. p53: Its mutations and their impact on transcription. Subcell. Biochem. 2014;85:71–90. PubMed
Brazda V., Muller P., Brozkova K., Vojtesek B. Restoring wild-type conformation and DNA-binding activity of mutant p53 is insufficient for restoration of transcriptional activity. Biochem. Biophys. Res. Commun. 2006;351:499–506. doi: 10.1016/j.bbrc.2006.10.065. PubMed DOI
Viadiu H., Fronza G., Inga A. Structural studies on mechanisms to activate mutant p53. Subcell. Biochem. 2014;85:119–132. PubMed
Quante T., Otto B., Brazdova M., Kejnovska I., Deppert W., Tolstonog G.V. Mutant p53 is a transcriptional co-factor that binds to G-rich regulatory regions of active genes and generates transcriptional plasticity. Cell Cycle. 2012;11:3290–3303. doi: 10.4161/cc.21646. PubMed DOI PMC
Brazdova M., Quante T., Toegel L., Walter K., Loscher C., Tichy V., Cincarova L., Deppert W., Tolstonog G.V. Modulation of gene expression in U251 glioblastoma cells by binding of mutant p53 R273H to intronic and intergenic sequences. Nucleic Acids Res. 2009;37:1486–1500. doi: 10.1093/nar/gkn1085. PubMed DOI PMC
Sampath J., Sun D.X., Kidd V.J., Grenet J., Gandhi A., Shapiro L.H., Wang Q.J., Zambetti G.P., Schuetz J.D. Mutant p53 cooperates with ETS and selectively up-regulates human MDR1 not MRP1. J. Biol. Chem. 2001;276:39359–39367. doi: 10.1074/jbc.M103429200. PubMed DOI
Chicas A., Molina P., Bargonetti J. Mutant p53 forms a complex with Sp1 on HIV-LTR DNA. Biochem. Biophys. Res. Commun. 2000;279:383–390. doi: 10.1006/bbrc.2000.3965. PubMed DOI
Brazda V., Haronikova L., Liao J.C.C., Fojta M. DNA and RNA Quadruplex-Binding Proteins. Int. J. Mol. Sci. 2014;15:17493–17517. doi: 10.3390/ijms151017493. PubMed DOI PMC
Ramos E.M., Gillis T., Mysore J.S., Lee J.M., Alonso I., Gusella J.F., Smoller J.W., Sklar P., MacDonald M.E., Perlis R.H. Prevalence of Huntington’s disease gene CAG trinucleotide repeat alleles in patients with bipolar disorder. Bipolar Disord. 2015;17:403–408. doi: 10.1111/bdi.12289. PubMed DOI PMC
Den Dunnen W.F.A. Handbook of Clinical Neurology. Volume 145. Elsevier B.V.; Oxford, UK: 2017. Trinucleotide repeat disorders; pp. 383–391. PubMed
Pearson C.E., Sinden R.R. Trinucleotide repeat DNA structures: Dynamic mutations from dynamic DNA. Curr. Opin. Struct. Biol. 1998;8:321–330. doi: 10.1016/S0959-440X(98)80065-1. PubMed DOI
Beaver J.M., Lai Y., Rolle S.J., Liu Y. Proliferating cell nuclear antigen prevents trinucleotide repeat expansions by promoting repeat deletion and hairpin removal. DNA Repair. 2016;48:17–29. doi: 10.1016/j.dnarep.2016.10.006. PubMed DOI PMC
Pearson C.E., Zorbas H., Price G.B., ZannisHadjopoulos M. Inverted repeats, stem-loops, and cruciforms: Significance for initiation of DNA replication. J. Cell. Biochem. 1996;63:1–22. doi: 10.1002/(SICI)1097-4644(199610)63:1<1::AID-JCB1>3.0.CO;2-3. PubMed DOI
Brázda V., Coufal J., Liao J.C.C., Arrowsmith C.H. Preferential binding of IFI16 protein to cruciform structure and superhelical DNA. Biochem. Biophys. Res. Commun. 2012;422:716–720. doi: 10.1016/j.bbrc.2012.05.065. PubMed DOI
van Holde K., Zlatanova J. Unusual DNA structures, chromatin and transcription. Bioessays. 1994;16:59–68. doi: 10.1002/bies.950160110. PubMed DOI
Kim E., Rohaly G., Heinrichs S., Gimnopoulos D., Meissner H., Deppert W. Influence of promoter DNA topology on sequence-specific DNA binding and transactivation by tumor suppressor p53. Oncogene. 1999;18:7310–7318. doi: 10.1038/sj.onc.1203139. PubMed DOI
Saramaki A., Banwell C.M., Campbell M.J., Carlberg C. Regulation of the human p21(waf1/cip1) gene promoter via multiple binding sites for p53 and the vitamin D-3 receptor. Nucleic Acids Res. 2006;34:543–554. doi: 10.1093/nar/gkj460. PubMed DOI PMC
Jett S.D., Cherny D.I., Subramaniam V., Jovin T.M. Scanning force microscopy of the complexes of p53 core domain with supercoiled DNA. J. Mol. Biol. 2000;299:585–592. doi: 10.1006/jmbi.2000.3759. PubMed DOI
Cherny D.I., Striker G., Subramaniam V., Jett S.D., Palecek E., Jovin T.M. DNA bending due to specific p53 and p53 core domain-DNA interactions visualized by electron microscopy. J. Mol. Biol. 1999;294:1015–1026. doi: 10.1006/jmbi.1999.3299. PubMed DOI
Moore L.D., Le T., Fan G. DNA methylation and its basic function. Neuropsychopharmacology. 2013;38:23–38. doi: 10.1038/npp.2012.112. PubMed DOI PMC
Stillman B. Histone Modifications: Insights into Their Influence on Gene Expression. Cell. 2018;175:6–9. doi: 10.1016/j.cell.2018.08.032. PubMed DOI
Holoch D., Moazed D. RNA-mediated epigenetic regulation of gene expression. Nat. Rev. Genet. 2015;16:71–84. doi: 10.1038/nrg3863. PubMed DOI PMC
Chen Z., Li S., Subramaniam S., Shyy J.Y.-J., Chien S. Epigenetic Regulation: A New Frontier for Biomedical Engineers. Annu. Rev. Biomed. Eng. 2017;19:195–219. doi: 10.1146/annurev-bioeng-071516-044720. PubMed DOI
Bao F., LoVerso P.R., Fisk J.N., Zhurkin V.B., Cui F. p53 binding sites in normal and cancer cells are characterized by distinct chromatin context. Cell Cycle. 2017;16:2073–2085. doi: 10.1080/15384101.2017.1361064. PubMed DOI PMC
Nabilsi N.H., Ryder D.J., Peraza-Penton A.C., Poudyal R., Loose D.S., Kladde M.P. Local depletion of DNA methylation identifies a repressive p53 regulatory region in the NEK2 promoter. J. Biol. Chem. 2013;288:35940–35951. doi: 10.1074/jbc.M113.523837. PubMed DOI PMC
Sammons M.A., Zhu J., Drake A.M., Berger S.L. TP53 engagement with the genome occurs in distinct local chromatin environments via pioneer factor activity. Genome Res. 2015;25:179–188. doi: 10.1101/gr.181883.114. PubMed DOI PMC
Yu X., Buck M.J. Defining TP53 pioneering capabilities with competitive nucleosome binding assays. Genome Res. 2019;29:107–115. doi: 10.1101/gr.234104.117. PubMed DOI PMC
Taube J.H., Allton K., Duncan S.A., Shen L., Barton M.C. Foxa1 functions as a pioneer transcription factor at transposable elements to activate Afp during differentiation of embryonic stem cells. J. Biol. Chem. 2010;285:16135–16144. doi: 10.1074/jbc.M109.088096. PubMed DOI PMC
Zhabinskaya D., Benham C.J. Competitive superhelical transitions involving cruciform extrusion. Nucleic Acids Res. 2013;41:9610–9621. doi: 10.1093/nar/gkt733. PubMed DOI PMC
Drolet M. Growth inhibition mediated by excess negative supercoiling: The interplay between transcription elongation, R-loop formation and DNA topology. Mol. Microbiol. 2006;59:723–730. doi: 10.1111/j.1365-2958.2005.05006.x. PubMed DOI
Krasilnikov A.S., Podtelezhnikov A., Vologodskii A., Mirkin S.M. Large-scale effects of transcriptional DNA supercoiling in vivo. J. Mol. Biol. 1999;292:1149–1160. doi: 10.1006/jmbi.1999.3117. PubMed DOI
Schiavone D., Guilbaud G., Murat P., Papadopoulou C., Sarkies P., Prioleau M.-N., Balasubramanian S., Sale J.E. Determinants of G quadruplex-induced epigenetic instability in REV1-deficient cells. EMBO J. 2014;33:2507–2520. doi: 10.15252/embj.201488398. PubMed DOI PMC
Guilbaud G., Murat P., Recolin B., Campbell B.C., Maiter A., Sale J.E., Balasubramanian S. Local epigenetic reprogramming induced by G-quadruplex ligands. Nat. Chem. 2017;9:1110–1117. doi: 10.1038/nchem.2828. PubMed DOI PMC
Allers T., Leach D.R. DNA palindromes adopt a methylation-resistant conformation that is consistent with DNA cruciform or hairpin formation in vivo. J. Mol. Biol. 1995;252:70–85. doi: 10.1006/jmbi.1994.0476. PubMed DOI
Jara-Espejo M., Peres Line S.R. DNA G-quadruplex stability, position and chromatin accessibility are associated with CpG island methylation. FEBS J. 2019 doi: 10.1111/febs.15065. PubMed DOI
Schlereth K., Heyl C., Krampitz A.-M., Mernberger M., Finkernagel F., Scharfe M., Jarek M., Leich E., Rosenwald A., Stiewe T. Characterization of the p53 cistrome—DNA binding cooperativity dissects p53′s tumor suppressor functions. PLoS Genet. 2013;9:e1003726. doi: 10.1371/journal.pgen.1003726. PubMed DOI PMC
Stiewe T., Haran T.E. How mutations shape p53 interactions with the genome to promote tumorigenesis and drug resistance. Drug Resist. Updat. 2018;38:27–43. doi: 10.1016/j.drup.2018.05.001. PubMed DOI
Ohtsuka J., Oshima H., Ezawa I., Abe R., Oshima M., Ohki R. Functional loss of p53 cooperates with the in vivo microenvironment to promote malignant progression of gastric cancers. Sci. Rep. 2018;8:2291. doi: 10.1038/s41598-018-20572-1. PubMed DOI PMC
Nakayama M., Sakai E., Echizen K., Yamada Y., Oshima H., Han T.-S., Ohki R., Fujii S., Ochiai A., Robine S., et al. Intestinal cancer progression by mutant p53 through the acquisition of invasiveness associated with complex glandular formation. Oncogene. 2017;36:5885–5896. doi: 10.1038/onc.2017.194. PubMed DOI PMC
Iyer S.V., Parrales A., Begani P., Narkar A., Adhikari A.S., Martinez L.A., Iwakuma T. Allele-specific silencing of mutant p53 attenuates dominant-negative and gain-of-function activities. Oncotarget. 2016;7:5401–5415. doi: 10.18632/oncotarget.6634. PubMed DOI PMC
Parrales A., Ranjan A., Iyer S.V., Padhye S., Weir S.J., Roy A., Iwakuma T. DNAJA1 controls the fate of misfolded mutant p53 through the mevalonate pathway. Nat. Cell Biol. 2016;18:1233–1243. doi: 10.1038/ncb3427. PubMed DOI PMC
Joruiz S.M., Bourdon J.-C. p53 Isoforms: Key Regulators of the Cell Fate Decision. Cold Spring Harb. Perspect. Med. 2016;6:a026039. doi: 10.1101/cshperspect.a026039. PubMed DOI PMC
Bischof K., Knappskog S., Hjelle S.M., Stefansson I., Woie K., Salvesen H.B., Gjertsen B.T., Bjorge L. Influence of p53 Isoform Expression on Survival in High-Grade Serous Ovarian Cancers. Sci. Rep. 2019;9:5244. doi: 10.1038/s41598-019-41706-z. PubMed DOI PMC
Interaction of Proteins with Inverted Repeats and Cruciform Structures in Nucleic Acids
The Changes in the p53 Protein across the Animal Kingdom Point to Its Involvement in Longevity
Characterization of p53 Family Homologs in Evolutionary Remote Branches of Holozoa