The Influence of Quadruplex Structure in Proximity to P53 Target Sequences on the Transactivation Potential of P53 Alpha Isoforms

. 2019 Dec 24 ; 21 (1) : . [epub] 20191224

Jazyk angličtina Země Švýcarsko Médium electronic

Typ dokumentu časopisecké články

Perzistentní odkaz   https://www.medvik.cz/link/pmid31878115

Grantová podpora
18-15548S Grantová Agentura České Republiky
CZ.02.1.01/0.0/0.0/15 003/0000477 European Regional Development Fund

p53 is one of the most studied tumor suppressor proteins that plays an important role in basic biological processes including cell cycle, DNA damage response, apoptosis, and senescence. The human TP53 gene contains alternative promoters that produce N-terminally truncated proteins and can produce several isoforms due to alternative splicing. p53 function is realized by binding to a specific DNA response element (RE), resulting in the transactivation of target genes. Here, we evaluated the influence of quadruplex DNA structure on the transactivation potential of full-length and N-terminal truncated p53α isoforms in a panel of S. cerevisiae luciferase reporter strains. Our results show that a G-quadruplex prone sequence is not sufficient for transcription activation by p53α isoforms, but the presence of this feature in proximity to a p53 RE leads to a significant reduction of transcriptional activity and changes the dynamics between co-expressed p53α isoforms.

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Lane D.P. Cancer. p53, guardian of the genome. Nature. 1992;358:15–16. doi: 10.1038/358015a0. PubMed DOI

Oren M. Decision making by p53: Life, death and cancer. Cell Death Differ. 2003;10:431–442. doi: 10.1038/sj.cdd.4401183. PubMed DOI

Suzuki K., Dashzeveg N., Lu Z.G., Taira N., Miki Y., Yoshida K. Programmed cell death 6, a novel p53-responsive gene, targets to the nucleus in the apoptotic response to DNA damage. Cancer Sci. 2012;103:1788–1794. doi: 10.1111/j.1349-7006.2012.02362.x. 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

Levine A.J. p53, the Cellular Gatekeeper for Growth and Division. Cell. 1997;88:323–331. doi: 10.1016/S0092-8674(00)81871-1. PubMed DOI

Khoury M.P., Bourdon J.-C. p53 Isoforms: An Intracellular Microprocessor? Genes Cancer. 2011;2:453–465. doi: 10.1177/1947601911408893. 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

Meek D.W., Anderson C.W. Posttranslational Modification of p53: Cooperative Integrators of Function. Cold Spring Harb. Perspect. Biol. 2009;1:a000950. doi: 10.1101/cshperspect.a000950. 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

Ghosh A., Stewart D., Matlashewski G. Regulation of Human p53 Activity and Cell Localization by Alternative Splicing. Mol. Cell Biol. 2004;24:7987–7997. doi: 10.1128/MCB.24.18.7987-7997.2004. PubMed DOI PMC

Marcel V., Tran P.L.T., Sagne C., Martel-Planche G., Vaslin L., Teulade-Fichou M.-P., Hall J., Mergny J.-L., Hainaut P., Van Dyck E. G-quadruplex structures in TP53 intron 3: Role in alternative splicing and in production of p53 mRNA isoforms. Carcinogenesis. 2011;32:271–278. doi: 10.1093/carcin/bgq253. PubMed DOI

Pavletich N.P., Chambers K.A., Pabo C.O. The DNA-binding domain of p53 contains the four conserved regions and the major mutation hot spots. Genes Dev. 1993;7:2556–2564. doi: 10.1101/gad.7.12b.2556. PubMed DOI

Nutthasirikul N., Limpaiboon T., Leelayuwat C., Patrakitkomjorn S., Jearanaikoon P. Ratio disruption of the Δ133p53 and TAp53 isoform equilibrium correlates with poor clinical outcome in intrahepatic cholangiocarcinoma. Int. J. Oncol. 2013;42:1181–1188. doi: 10.3892/ijo.2013.1818. PubMed DOI

Chambers S.K., Martinez J.D. The significance of p53 isoform expression in serous ovarian cancer. Future Oncol. 2012;8:683–686. doi: 10.2217/fon.12.60. 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

Weinberg R.L., Veprintsev D.B., Bycroft M., Fersht A.R. Comparative Binding of p53 to its Promoter and DNA Recognition Elements. J. Mol. Biol. 2005;348:589–596. doi: 10.1016/j.jmb.2005.03.014. PubMed DOI

Vyas P., Beno I., Xi Z., Stein Y., Golovenko D., Kessler N., Rotter V., Shakked Z., Haran T.E. Diverse p53/DNA binding modes expand the repertoire of p53 response elements. Proc. Natl. Acad. Sci. USA. 2017;114:10624–10629. doi: 10.1073/pnas.1618005114. 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

Brázda V., Fojta M. The Rich World of p53 DNA Binding Targets: The Role of DNA Structure. Int. J. Mol. Sci. 2019;20:5605. doi: 10.3390/ijms20225605. PubMed DOI PMC

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

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

Göhler 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

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

Coufal J., Jagelská 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

Brazda V., Čechová J., Battistin M., Coufal J., Jagelská 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

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

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

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

Spradling A., Ganetsky B., Hieter P., Johnston M., Olson M., Orr-Weaver T., Rossant J., Sanchez A., Waterston R. New roles for model genetic organisms in understanding and treating human disease: Report from the 2006 Genetics Society of America meeting. Genetics. 2006;172:2025–2032. PubMed PMC

Lion M., Raimondi I., Donati S., Jousson O., Ciribilli Y., Inga A. Evolution of p53 Transactivation Specificity through the Lens of a Yeast-Based Functional Assay. PLoS ONE. 2015;10 doi: 10.1371/journal.pone.0116177. PubMed DOI PMC

Guaragnella N., Palermo V., Galli A., Moro L., Mazzoni C., Giannattasio S. The expanding role of yeast in cancer research and diagnosis: Insights into the function of the oncosuppressors p53 and BRCA1/2. FEMS Yeast Res. 2014;14:2–16. doi: 10.1111/1567-1364.12094. PubMed DOI

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

Brázda V., Kolomazník J., Lýsek J., Bartas M., Fojta M., Šťastný J., Mergny J.-L. G4Hunter web application: A web server for G-quadruplex prediction. Bioinformatics. 2019;35:3493–3495. doi: 10.1093/bioinformatics/btz087. 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

Yang D., Hurley L.H. Structure of the biologically relevant G-quadruplex in the c-MYC promoter. Nucleosides Nucleotides Nucleic Acids. 2006;25:951–968. doi: 10.1080/15257770600809913. PubMed DOI

Ambrus A., Chen D., Dai J., Bialis T., Jones R.A., Yang D. Human telomeric sequence forms a hybrid-type intramolecular G-quadruplex structure with mixed parallel/antiparallel strands in potassium solution. Nucleic Acids Res. 2006;34:2723–2735. doi: 10.1093/nar/gkl348. PubMed DOI PMC

Del Villar-Guerra R., Trent J.O., Chaires J.B. G-Quadruplex Secondary Structure Obtained from Circular Dichroism Spectroscopy. Angew. Chem. Int. Ed. Engl. 2018;57:7171–7175. doi: 10.1002/anie.201709184. 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

Jordan J.J., Menendez D., Inga A., Nourredine M., Bell D., Resnick M.A. Noncanonical DNA Motifs as Transactivation Targets by Wild Type and Mutant p53. PLoS Genet. 2008;4:e1000104. doi: 10.1371/annotation/f7fc9c28-14ae-480d-a69e-ee9cc4fba9a7. PubMed DOI PMC

Brázda V., Laister R.C., Jagelská 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

Huppert J.L., Balasubramanian S. G-quadruplexes in promoters throughout the human genome. Nucleic Acids Res. 2007;35:406–413. doi: 10.1093/nar/gkl1057. PubMed DOI PMC

Tokan V., Puterova J., Lexa M., Kejnovsky E. Quadruplex DNA in long terminal repeats in maize LTR retrotransposons inhibits the expression of a reporter gene in yeast. BMC Genom. 2018;19:184. doi: 10.1186/s12864-018-4563-7. PubMed DOI PMC

Candeias M.M., Hagiwara M., Matsuda M. Cancer-specific mutations in p53 induce the translation of Δ160p53 promoting tumorigenesis. EMBO Rep. 2016;17:1542–1551. doi: 10.15252/embr.201541956. PubMed DOI PMC

User guide: Gateway Technology with Clonase II-A universal technology to clone DNA sequences for functional analysis and expression in multiple systems. [(accessed on 10 January 2019)]; Available online: http://tools.thermofisher.com/content/sfs/manuals/gateway_clonaseii_man.pdf.

Storici F., Resnick M.A. The delitto perfetto approach to in vivo site-directed mutagenesis and chromosome rearrangements with synthetic oligonucleotides in yeast. Methods Enzym. 2006;409:329–345. PubMed

Sharma V., Monti P., Fronza G., Inga A. Human transcription factors in yeast: The fruitful examples of P53 and NF-κB. FEMS Yeast Res. 2016;16 doi: 10.1093/femsyr/fow083. PubMed DOI

Andreotti V., Ciribilli Y., Monti P., Bisio A., Lion M., Jordan J., Fronza G., Menichini P., Resnick M.A., Inga A. p53 Transactivation and the Impact of Mutations, Cofactors and Small Molecules Using a Simplified Yeast-Based Screening System. PLoS ONE. 2011;6:e20643. doi: 10.1371/journal.pone.0020643. PubMed DOI PMC

Vojtesek B., Dolezalova H., Lauerova L., Svitakova M., Havlis P., Kovarik J., Midgley C.A., Lane D.P. Conformational changes in p53 analysed using new antibodies to the core DNA binding domain of the protein. Oncogene. 1995;10:389–393. 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

Pospísilová S., Brázda V., Amrichová J., Kamermeierová R., Palecek E., Vojtesek B. Precise characterisation of monoclonal antibodies to the C-terminal region of p53 protein using the PEPSCAN ELISA technique and a new non-radioactive gel shift assay. J. Immunol. Methods. 2000;237:51–64. doi: 10.1016/S0022-1759(99)00246-X. PubMed DOI

Sayers E.W., Agarwala R., Bolton E.E., Brister J.R., Canese K., Clark K., Connor R., Fiorini N., Funk K., Hefferon T., et al. Database resources of the National Center for Biotechnology Information. Nucleic Acids Res. 2019;47:D23–D28. doi: 10.1093/nar/gky1069. PubMed DOI PMC

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