Characterization of p53 Family Homologs in Evolutionary Remote Branches of Holozoa

. 2019 Dec 18 ; 21 (1) : . [epub] 20191218

Jazyk angličtina Země Švýcarsko Médium electronic

Typ dokumentu časopisecké články

Perzistentní odkaz   https://www.medvik.cz/link/pmid31861340

Grantová podpora
project LO1208 TEWEP Ministry of Education, Youth and Sports of the Czech Republic in the "National Feasibility Program I"
18-15548S The Czech Science Foundation
CZ.1.05/2.1.00/19.0388 EU structural funding Operational Programme Research and Development for innovation
SGS/09/PrF/2019 University of Ostrava

The p53 family of transcription factors plays key roles in development, genome stability, senescence and tumor development, and p53 is the most important tumor suppressor protein in humans. Although intensively investigated for many years, its initial evolutionary history is not yet fully elucidated. Using bioinformatic and structure prediction methods on current databases containing newly-sequenced genomes and transcriptomes, we present a detailed characterization of p53 family homologs in remote members of the Holozoa group, in the unicellular clades Filasterea, Ichthyosporea and Corallochytrea. Moreover, we show that these newly characterized homologous sequences contain domains that can form structures with high similarity to the human p53 family DNA-binding domain, and some also show similarities to the oligomerization and SAM domains. The presence of these remote homologs demonstrates an ancient origin of the p53 protein family.

Zobrazit více v PubMed

Hollstein M., Sidransky D., Vogelstein B., Harris C. P53 Mutations in Human Cancers. Science. 1991;253:49–53. doi: 10.1126/science.1905840. PubMed DOI

Goh A.M., Coffill C.R., Lane D.P. The role of mutant p53 in human cancer. J. Pathol. 2011;223:116–126. doi: 10.1002/path.2784. PubMed DOI

Stiewe T., Haran T.E. How mutations shape p53 interactions with the genome to promote tumorigenesis and drug resistance. Drug Resist. Update. 2018;38:27–43. doi: 10.1016/j.drup.2018.05.001. PubMed DOI

Joerger A.C., Fersht A.R. The p53 pathway: Origins, inactivation in cancer, and emerging therapeutic approaches. Annu. Rev. Biochem. 2016;85:375–404. doi: 10.1146/annurev-biochem-060815-014710. PubMed DOI

Strano S., Rossi M., Fontemaggi G., Munarriz E., Soddu S., Sacchi A., Blandino G. From p63 to p53 across p73. FEBS Lett. 2001;490:163–170. doi: 10.1016/S0014-5793(01)02119-6. PubMed DOI

Belyi V.A., Levine A.J. One billion years of p53/p63/p73 evolution. Proc. Natl. Acad. Sci. USA. 2009;106:17609–17610. doi: 10.1073/pnas.0910634106. PubMed DOI PMC

Beckerman R., Prives C. Transcriptional Regulation by P53. Cold Spring Harb. Perspect. Biol. 2010;2:1–18. doi: 10.1101/cshperspect.a000935. PubMed DOI PMC

Brazda 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

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., 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

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;1:45–49. doi: 10.1038/ng0492-45. PubMed DOI

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

Brázda 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

Coufal J., Jagelská E.B., Liao J.C., Brázda 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

Dötsch V., Bernassola F., Coutandin D., Candi E., Melino G. p63 and p73, the Ancestors of p53. Cold Spring Harb. Perspect. Biol. 2010;2 doi: 10.1101/cshperspect.a004887. PubMed DOI PMC

Arrowsmith C.H. Structure and function in the p53 family. Cell Death Differ. 1999;6:1169–1173. doi: 10.1038/sj.cdd.4400619. PubMed DOI

Joerger A.C., Rajagopalan S., Natan E., Veprintsev D.B., Robinson C.V., Fersht A.R. Structural evolution of p53, p63, and p73: Implication for heterotetramer formation. Proc. Natl. Acad. Sci. USA. 2009;106:17705–17710. doi: 10.1073/pnas.0905867106. PubMed DOI PMC

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

Xue B., Brown C.J., Dunker A.K., Uversky V.N. Intrinsically disordered regions of p53 family are highly diversified in evolution. BBA Proteins Proteom. 2013;1834:725–738. doi: 10.1016/j.bbapap.2013.01.012. PubMed DOI PMC

Joerger A.C., Wilcken R., Andreeva A. Tracing the Evolution of the p53 Tetramerization Domain. Structure. 2014;22:1301–1310. doi: 10.1016/j.str.2014.07.010. PubMed DOI PMC

Yang A., Kaghad M., Caput D., McKeon F. On the shoulders of giants: p63, p73 and the rise of p53. Trends Genet. 2002;18:90–95. doi: 10.1016/S0168-9525(02)02595-7. PubMed DOI

Dos Santos H.G., Nunez-Castilla J., Siltberg-Liberles J. Functional diversification after gene duplication: Paralog specific regions of structural disorder and phosphorylation in p53, p63, and p73. PLoS ONE. 2016;11:e0151961. doi: 10.1371/journal.pone.0151961. PubMed DOI PMC

Laptenko O., Shiff I., Freed-Pastor W., Zupnick A., Mattia M., Freulich E., Shamir I., Kadouri N., Kahan T., Manfredi J. The p53 C terminus controls site-specific DNA binding and promotes structural changes within the central DNA binding domain. Mol. Cell. 2015;57:1034–1046. doi: 10.1016/j.molcel.2015.02.015. PubMed DOI PMC

Gu W., Roeder R.G. Activation of p53 sequence-specific DNA binding by acetylation of the p53 C-terminal domain. Cell. 1997;90:595–606. doi: 10.1016/S0092-8674(00)80521-8. PubMed DOI

Pospísilová S., Brázda V., Kucharíková K., Luciani M.G., Hupp T.R., Skládal P., Palecek E., Vojtesek B. Activation of the DNA-binding ability of latent p53 protein by protein kinase C is abolished by protein kinase CK2. Biochem. J. 2004;378:939–947. doi: 10.1042/bj20030662. PubMed DOI PMC

Ou Y.-H., Chung P.-H., Sun T.-P., Shieh S.-Y. p53 C-terminal phosphorylation by CHK1 and CHK2 participates in the regulation of DNA-damage-induced C-terminal acetylation. Mol. Biol. Cell. 2005;16:1684–1695. doi: 10.1091/mbc.e04-08-0689. PubMed DOI PMC

Muller P., Chan J.M., Simoncik O., Fojta M., Lane D.P., Hupp T., Vojtesek B. Evidence for allosteric effects on p53 oligomerization induced by phosphorylation. Protein Sci. 2018;27:523–530. doi: 10.1002/pro.3344. PubMed DOI PMC

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

Weinberg R.L., Freund S.M.V., Veprintsev D.B., Bycroft M., Fersht A.R. Regulation of DNA binding of p53 by its C-terminal domain. J. Mol. Biol. 2004;342:801–811. doi: 10.1016/j.jmb.2004.07.042. PubMed DOI

Lu W.-J., Amatruda J.F., Abrams J.M. p53 ancestry: Gazing through an evolutionary lens. Nat. Rev. Cancer. 2009;9:758–762. doi: 10.1038/nrc2732. PubMed DOI

Belyi V.A., Ak P., Markert E., Wang H., Hu W., Puzio-Kuter A., Levine A.J. The origins and evolution of the p53 family of genes. Cold Spring Harb. Perspect. Biol. 2010;2:a001198. doi: 10.1101/cshperspect.a001198. PubMed DOI PMC

Nedelcu A.M., Tan C. Early diversification and complex evolutionary history of the p53 tumor suppressor gene family. Dev. Genes Evol. 2007;217:801–806. doi: 10.1007/s00427-007-0185-9. PubMed DOI

King N., Westbrook M.J., Young S.L., Kuo A., Abedin M., Chapman J., Fairclough S., Hellsten U., Isogai Y., Letunic I., et al. The genome of the choanoflagellate Monosiga brevicollis and the origin of metazoans. Nature. 2008;451:783–788. doi: 10.1038/nature06617. PubMed DOI PMC

Sebé-Pedrós A., de Mendoza A., Lang B.F., Degnan B.M., Ruiz-Trillo I. Unexpected repertoire of metazoan transcription factors in the unicellular holozoan Capsaspora owczarzaki. Mol. Biol. Evol. 2011;28:1241–1254. doi: 10.1093/molbev/msq309. PubMed DOI PMC

de Mendoza A., Sebé-Pedrós A., Šestak M.S., Matejčić M., Torruella G., Domazet-Lošo T., Ruiz-Trillo I. Transcription factor evolution in eukaryotes and the assembly of the regulatory toolkit in multicellular lineages. Proc. Natl. Acad. Sci. USA. 2013;110:E4858–E4866. doi: 10.1073/pnas.1311818110. PubMed DOI PMC

Sebé-Pedrós A., Peña M.I., Capella-Gutiérrez S., Antó M., Gabaldón T., Ruiz-Trillo I., Sabidó E. High-throughput proteomics reveals the unicellular roots of animal phosphosignaling and cell differentiation. Dev. Cell. 2016;39:186–197. doi: 10.1016/j.devcel.2016.09.019. PubMed DOI

Altschul S.F., Gish W., Miller W., Myers E.W., Lipman D.J. Basic local alignment search tool. J. Mol. Biol. 1990;215:403–410. doi: 10.1016/S0022-2836(05)80360-2. PubMed DOI

Grau-Bove X., Torruella G., Donachie S., Suga H., Leonard G., Richards T.A., Ruiz-Trillo I. Dynamics of genomic innovation in the unicellular ancestry of animals. eLife. 2017;6:e26036. doi: 10.7554/eLife.26036. PubMed DOI PMC

de Mendoza A., Suga H., Permanyer J., Irimia M., Ruiz-Trillo I. Complex transcriptional regulation and independent evolution of fungal-like traits in a relative of animals. eLife. 2015;4:e08904. doi: 10.7554/eLife.08904. PubMed DOI PMC

Potter S.C., Luciani A., Eddy S.R., Park Y., Lopez R., Finn R.D. HMMER web server: 2018 update. Nucleic Acids Res. 2018;46:W200–W204. doi: 10.1093/nar/gky448. PubMed DOI PMC

Chang F.-L., Lai M.-D. Various forms of mutant p53 confer sensitivity to cisplatin and doxorubicin in bladder cancer cells. J. Urol. 2001;166:304–310. doi: 10.1016/S0022-5347(05)66150-2. PubMed DOI

Olivier M., Hollstein M., Hainaut P. TP53 Mutations in Human Cancers: Origins, Consequences, and Clinical Use. Cold Spring Harb. Perspect. Biol. 2010;2:a001008. doi: 10.1101/cshperspect.a001008. PubMed DOI PMC

Eldar A., Rozenberg H., Diskin-Posner Y., Rohs R., Shakked Z. Structural studies of p53 inactivation by DNA-contact mutations and its rescue by suppressor mutations via alternative protein–DNA interactions. Nucleic Acids Res. 2013;41:8748–8759. doi: 10.1093/nar/gkt630. PubMed DOI PMC

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

Dittmer D., Pati S., Zambetti G., Chu S., Teresky A.K., Moore M., Finlay C., Levine A.J. Gain of function mutations in p53. Nat. Genet. 1993;4:42–46. doi: 10.1038/ng0593-42. PubMed DOI

Xu D., Zhang Y. Ab initio protein structure assembly using continuous structure fragments and optimized knowledge-based force field. Proteins Struct. Funct. Bioinform. 2012;80:1715–1735. doi: 10.1002/prot.24065. PubMed DOI PMC

Xu D., Zhang Y. Toward optimal fragment generations for ab initio protein structure assembly. Proteins Struct. Funct. Bioinform. 2013;81:229–239. doi: 10.1002/prot.24179. PubMed DOI PMC

Waterhouse A., Bertoni M., Bienert S., Studer G., Tauriello G., Gumienny R., Heer F.T., de Beer T.A.P., Rempfer C., Bordoli L., et al. SWISS-MODEL: Homology modelling of protein structures and complexes. Nucleic Acids Res. 2018;46:W296–W303. doi: 10.1093/nar/gky427. 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

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:e0116177. doi: 10.1371/journal.pone.0116177. PubMed DOI PMC

Jordan A., Reichard P. Ribonucleotide Reductases. Annu. Rev. Biochem. 1998;67:71–98. doi: 10.1146/annurev.biochem.67.1.71. PubMed DOI

Åberg E., Saccoccia F., Grabherr M., Ore W.Y.J., Jemth P., Hultqvist G. Evolution of the p53-MDM2 pathway. BMC Evol. Biol. 2017;17:177. doi: 10.1186/s12862-017-1023-y. PubMed DOI PMC

Mendoza L., Orozco E., Rodriguez M.A., Garcia-Rivera G., Sanchez T., Garcia E., Gariglio P. Ehp53, an Entamoeba histolytica protein, ancestor of the mammalian tumour suppressor p53. Microbiology. 2003;149:885–893. doi: 10.1099/mic.0.25892-0. PubMed DOI

Biscotti M.A., Barucca M., Carducci F., Forconi M., Canapa A. The p53 gene family in vertebrates: Evolutionary considerations. J. Exp. Zool. Part B. 2019;332:171–178. doi: 10.1002/jez.b.22856. PubMed DOI

Aravind L., Anantharaman V., Iyer L.M. Evolutionary connections between bacterial and eukaryotic signaling systems: A genomic perspective. Curr. Opin. Microbiol. 2003;6:490–497. doi: 10.1016/j.mib.2003.09.003. PubMed DOI

Okonechnikov K., Golosova O., Fursov M., Team U. Unipro UGENE: A unified bioinformatics toolkit. Bioinformatics. 2012;28:1166–1167. doi: 10.1093/bioinformatics/bts091. PubMed DOI

Kozlowski L.P. IPC—Isoelectric Point Calculator. Biol. Direct. 2016;11:55. doi: 10.1186/s13062-016-0159-9. PubMed DOI PMC

Marchler-Bauer A., Derbyshire M.K., Gonzales N.R., Lu S., Chitsaz F., Geer L.Y., Geer R.C., He J., Gwadz M., Hurwitz D.I., et al. CDD: NCBI’s conserved domain database. Nucleic Acids Res. 2015;43:D222–D226. doi: 10.1093/nar/gku1221. PubMed DOI PMC

Kosugi S., Hasebe M., Tomita M., Yanagawa H. Systematic identification of cell cycle-dependent yeast nucleocytoplasmic shuttling proteins by prediction of composite motifs. Proc. Natl. Acad. Sci. USA. 2009;106:10171–10176. doi: 10.1073/pnas.0900604106. PubMed DOI PMC

Hedges S.B., Marin J., Suleski M., Paymer M., Kumar S. Tree of life reveals clock-like speciation and diversification. Mol. Biol. Evol. 2015;32:835–845. doi: 10.1093/molbev/msv037. PubMed DOI PMC

Kumar S., Stecher G., Suleski M., Hedges S.B. TimeTree: A resource for timelines, timetrees, and divergence times. Mol. Biol. Evol. 2017;34:1812–1819. doi: 10.1093/molbev/msx116. PubMed DOI

Letunic I., Bork P. 20 years of the SMART protein domain annotation resource. Nucleic Acids Res. 2018;46:D493–D496. doi: 10.1093/nar/gkx922. PubMed DOI PMC

Edgar R.C. MUSCLE: Multiple sequence alignment with high accuracy and high throughput. Nucleic Acids Res. 2004;32:1792–1797. doi: 10.1093/nar/gkh340. PubMed DOI PMC

de Anta J.M., Jassem E., Rosell R., Martínez-Roca M., Jassem J., Martínez-López E., Monzó M., Sánchez-Hernández J.J., Moreno I., Sánchez-Céspedes M. TP53 mutational pattern in Spanish and Polish non-small cell lung cancer patients: Null mutations are associated with poor prognosis. Oncogene. 1997;15:2951. doi: 10.1038/sj.onc.1201475. PubMed DOI

Huelsenbeck J.P., Ronquist F. MRBAYES: Bayesian inference of phylogenetic trees. Bioinformatics. 2001;17:754–755. doi: 10.1093/bioinformatics/17.8.754. PubMed DOI

Enthart A., Klein C., Dehner A., Coles M., Gemmecker G., Kessler H., Hagn F. Solution structure and binding specificity of the p63 DNA binding domain. Sci. Rep. 2016;6:26707. doi: 10.1038/srep26707. PubMed DOI PMC

Meng E.C., Pettersen E.F., Couch G.S., Huang C.C., Ferrin T.E. Tools for integrated sequence-structure analysis with UCSF Chimera. BMC Bioinform. 2006;7:339 PubMed PMC

Hu B., Jin J., Guo A.-Y., Zhang H., Luo J., Gao G. GSDS 2.0: An upgraded gene feature visualization server. Bioinformatics. 2015;31:1296–1297. doi: 10.1093/bioinformatics/btu817. PubMed DOI PMC

Dereeper A., Guignon V., Blanc G., Audic S., Buffet S., Chevenet F., Dufayard J.-F., Guindon S., Lefort V., Lescot M. Phylogeny. fr: Robust phylogenetic analysis for the non-specialist. Nucleic Acids Res. 2008;36:W465–W469. doi: 10.1093/nar/gkn180. PubMed DOI PMC

Notredame C., Higgins D.G., Heringa J. T-Coffee: A novel method for fast and accurate multiple sequence alignment. J. Mol. Biol. 2000;302:205–217. doi: 10.1006/jmbi.2000.4042. PubMed DOI

Najít záznam

Citační ukazatele

Nahrávání dat ...

    Možnosti archivace