Coevolution; DNA binding; DNA replication; Domestication; Expression enhancer; MITE; Transposon; Protein Isoforms; Histone-Lysine N-Methyltransferase; SETMAR protein, human; Colon/metabolism; Enhancer Elements, Genetic; Humans; Protein Isoforms/genetics; DNA Repair; Histone-Lysine N-Methyltransferase/genetics; Regulatory Sequences, Nucleic Acid; Colon; Genetics
Abstract :
[en] Setmar is a gene specific to simian genomes. The function(s) of its isoforms are poorly understood and their existence in healthy tissues remains to be validated. Here we profiled SETMAR expression and its genome-wide binding landscape in colon tissue. We found isoforms V3 and V6 in healthy and tumour colon tissues as well as incell lines. In two colorectal cell lines SETMAR binds to several thousand Hsmar1 and MADE1 terminal ends, transposons mostly located in non-genic regions of active chromatin including in enhancers. It also binds to a 12-bp motifs similar to an inner motif in Hsmar1 and MADE1 terminal ends. This motif is interspersed throughout the genome and is enriched in GC-rich regions as well as in CpG islands that contain constitutive replication origins. It is also found in enhancers other than those associated with Hsmar1 and MADE1. The role of SETMAR in the expression of genes, DNA replication and in DNA repair are discussed.
Disciplines :
Biochemistry, biophysics & molecular biology
Author, co-author :
Antoine-Lorquin, Aymeric; IRISA, 263 avenue du Général Leclerc, 35042 Rennes, France
Arensburger, Peter; Biological Sciences Department, California State Polytechnic University, Pomona, CA 91768, - United States
Arnaoty, Ahmed; EA GICC, 7501, CHRU de Tours, 37044 TOURS, Cedex 09, France
Asgari, Sassan; School of Biological Sciences, The University of Queensland, Brisbane, QLD 4072, Australia
Batailler, Martine; PRC, UMR INRA 0085, CNRS 7247, Centre INRA Val de Loire, 37380 Nouzilly, France
Beauclair, Linda; PRC, UMR INRA 0085, CNRS 7247, Centre INRA Val de Loire, 37380 Nouzilly, France
Belleannée, Catherine; IRISA, 263 avenue du Général Leclerc, 35042 Rennes, France
Buisine, Nicolas; UMR CNRS 7221, Muséum National d'Histoire Naturelle, 75005 Paris, France
Coustham, Vincent; BOA, INRAE, Université de Tours, 37380 Nouzilly, France
Guyetant, Serge; Tumorothèque du CHRU de Tours, 37044 Tours, Cedex, France
Helou, Laura ; Université de Liège - ULiège > Département des sciences cliniques ; PRC, UMR INRA 0085, CNRS 7247, Centre INRA Val de Loire, 37380 Nouzilly, France
Lecomte, Thierry; EA GICC, 7501, CHRU de Tours, 37044 TOURS, Cedex 09, France
Pitard, Bruno; Université de Nantes, CNRS ERL6001, Inserm 1232, CRCINA, F-44000 Nantes, France
Stévant, Isabelle; Institut de Génomique Fonctionnelle de Lyon, Univ Lyon, CNRS UMR 5242, Ecole Normale Supérieure de Lyon, Université Claude Bernard Lyon, 1, 46 allée d'Italie, 69364 Lyon, France
Bigot, Yves; PRC, UMR INRA 0085, CNRS 7247, Centre INRA Val de Loire, 37380 Nouzilly, France. Electronic address: yves.bigot@inrae.fr
National Cancer Association SNFGE - French National Society of Gastroenterology [FR] Cancéropôle du Grand Ouest [FR]
Funding text :
This work was funded by the C.N.R.S., the I.N.R.A., and the GDR CNRS 2157. It also received funds from a research program grant from the Cancéropôle Grand-Ouest, the Ligue Nationale Contre le Cancer and grants from Amgen and the French National Society of Gastroenterology. Laura Helou holds a PhD fellowship from the Région Centre Val de Loire. The funders have had no role in the design of the study and collection, analysis, and interpretation of data and in writing the manuscript.
Piégu, B., Bire, S., Arensburger, P., Bigot, Y., A survey of transposable element classification systems - a call for a fundamental update to meet the challenge of their diversity and complexity. Mol. Phylogenet. Evol. 86 (2015), 90–109, 10.1016/j.ympev.2015.03.009.
Cordaux, R., Udit, S., Batzer, M.A., Feschotte, C., Birth of a chimeric primate gene by capture of the transposase gene from a mobile element. Proc. Natl. Acad. Sci. U. S. A. 103 (2006), 8101–8106, 10.1073/pnas.0601161103.
Finstermeier, K., Zinner, D., Brameier, M., et al. A mitogenomic phylogeny of living primates. PLoS One, 8, 2013, e69504, 10.1371/journal.pone.0069504.
Carlson, S.M., Moore, K.E., Sankaran, S.M., et al. A proteomic strategy identifies lysine methylation of splicing factor snRNP70 by the SETMAR enzyme. J. Biol. Chem. 290 (2015), 12040–12047, 10.1074/jbc.M115.641530.
Fnu, S., Williamson, E.A., De Haro, L.P., et al. Methylation of histone H3 lysine 36 enhances DNA repair by nonhomologous end-joining. Proc. Natl. Acad. Sci. U. S. A. 108 (2011), 540–545, 10.1073/pnas.1013571108.
Weinberg, D.N., Papillon-Cavanagh, S., Chen, H., et al. The histone mark H3K36me2 recruits DNMT3A and shapes the intergenic DNA methylation landscape. Nature. 573 (2019), 281–286, 10.1038/s41586-019-1534-3.
Liu, D., Bischerour, J., Siddique, A., et al. The human SETMAR protein preserves most of the activities of the ancestral Hsmar1 transposase. Mol. Cell. Biol. 27 (2007), 1125–1132, 10.1128/MCB.01899-06.
Miskey, C., Papp, B., Mátés, L., et al. The ancient mariner sails again: transposition of the human Hsmar1 element by a reconstructed transposase and activities of the SETMAR protein on transposon ends. Mol. Cell. Biol. 27 (2007), 4589–4600, 10.1128/MCB.02027-06.
Beck, B.D., Park, S.J., Lee, Y.J., et al. Human Pso4 is a metnase (SETMAR)-binding partner that regulates metnase function in DNA repair. J. Biol. Chem. 283 (2008), 9023–9030, 10.1074/jbc.M800150200.
Beck, B.D., Lee, S.S., Hromas, R., et al. Regulation of Metnase's TIR binding activity by its binding partner, Pso4. Arch. Biochem. Biophys. 498 (2010), 89–94, 10.1016/j.abb.2010.04.011.
Williamson, E.A., Rasila, K.K., Corwin, L.K., et al. The SET and transposase domain protein Metnase enhances chromosome decatenation: regulation by automethylation. Nucleic Acids Res. 36 (2008), 5822–5831, 10.1093/nar/gkn560.
Hromas, R., Wray, J., Lee, S.H., et al. The human set and transposase domain protein Metnase interacts with DNA ligase IV and enhances the efficiency and accuracy of non-homologous end-joining. DNA Repair 7 (2008), 1927–1937, 10.1016/j.dnarep.2008.08.002.
Shaheen, M., Williamson, E., Nickoloff, J., et al. Metnase/SETMAR: a domesticated primate transposase that enhances DNA repair, replication, and decatenation. Genetica 138 (2010), 559–566, 10.1007/s10709-010-9452-1.
Beck, B.D., Lee, S.S., Williamson, E., et al. Biochemical characterization of metnase's endonuclease activity and its role in NHEJ repair. Biochemistry. 50 (2011), 4360–4370, 10.1021/bi200333k.
Kim, H.S., Chen, Q., Kim, S.K., et al. The DDN catalytic motif is required for Metnase functions in non-homologous end joining (NHEJ) repair and replication restart. J. Biol. Chem. 289 (2014), 10930–10938, 10.1074/jbc.M113.533216.
Kim, H.S., Kim, S.K., Hromas, R., et al. The SET domain is essential for Metnase functions in replication restart and the 5′ end of SS-overhang cleavage. PLoS One, 10, 2015, e0139418, 10.1371/journal.pone.0139418.
Lee, S.H., Oshige, M., Durant, S.T., et al. The SET domain protein Metnase mediates foreign DNA integration and links integration to nonhomologous end-joining repair. Proc. Natl. Acad. Sci. U. S. A. 102 (2005), 18075–18080, 10.1073/pnas.0503676102.
Williamson, E.A., Farrington, J., Martinez, L., et al. Expression levels of the human DNA repair protein metnase influence lentiviral genomic integration. Biochimie. 90 (2008), 1422–1426, 10.1016/j.biochi.2008.05.010.
Williamson, E.A., Damiani, L., Leitao, A., et al. Targeting the transposase domain of the DNA repair component Metnase to enhance chemotherapy. Cancer Res. 72 (2012), 6200–6208, 10.1158/0008-5472.CAN-12-0313.
Apostolou, P., Toloudi, M., Kourtidou, E., et al. Potential role for the Metnase transposase fusion gene in colon cancer through the regulation of key genes. PLoS One, 9, 2014, e109741, 10.1371/journal.pone.0109741.
Tellier, M., Chalmers, R., Human SETMAR is a DNA sequence-specific histone-methylase with a broad effect on the transcriptome. Nucleic Acids Res. 47 (2019), 122–133, 10.1093/nar/gky937.
Tellier, M., Chalmers, R., The roles of the human SETMAR (Metnase) protein in illegitimate DNA recombination and non-homologous end joining repair. DNA Repair (Amst) 80 (2019), 26–35, 10.1016/j.dnarep.2019.06.006.
Wray, J., Williamson, E.A., Chester, S., et al. The transposase domain protein Metnase/SETMAR suppresses chromosomal translocations. Cancer Genet. Cytogenet. 200 (2010), 184–190, 10.1016/j.cancergencyto.2010.04.011.
Wray, J., Williamson, E.A., Royce, M., et al. Metnase mediates resistance to topoisomerase II inhibitors in breast cancer cells. PLoS One, 4, 2009, e5323, 10.1371/journal.pone.0005323.
Jeyaratnam, D.C., Baduin, B.S., Hansen, M.C., et al. Delineation of known and new transcript variants of the SETMAR (Metnase) gene and the expression profile in hematologic neoplasms. Exp. Hematol. 42 (2014), 448–456, 10.1016/j.exphem.2014.02.005.
Arnaoty, A., Gouilleux-Gruart, V., Casteret, S., et al. Reliability of the nanopheres-DNA immunization technology to produce polyclonal antibodies directed against human neogenic proteins. Mol. Gen. Genomics. 288 (2013), 347–363, 10.1007/s00438-013-0754-8.
Dussaussois-Montagne, A., Jaillet, J., Babin, L., et al. SETMAR isoforms in glioblastoma: a matter of protein stability. Oncotarget 8 (2017), 9835–9848, 10.18632/oncotarget.14218.
Belleannée, C., Sallou, O., Nicolas, J., Logol: expressive pattern matching in sequences. application to ribosomal frameshift modeling. Comin, M., Kall, L., Marchiori, E., Ngom, A., Rajapakse, J., (eds.) PRIB2014 - Pattern Recognition in Bioinformatics, 9th IAPR International Conference, 8626, 2014, Springer International Publishing, Stockholm, 34–47, 10.1007/978-3-319-09192-1.
Bailey, T., Krajewski, P., Ladunga, I., et al. Practical guidelines for the comprehensive analysis of ChIP-seq data. PLoS Comput. Biol., 9, 2013, e1003326, 10.1371/journal.pcbi.1003326.
Langmead, B., Salzberg, S.L., Fast gapped-read alignment with bowtie 2. Nat. Methods 9 (2012), 357–359, 10.1038/nmeth.1923.
Zhang, Y., Lin, Y.H., Johnson, T.D., et al. PePr: a peak-calling prioritization pipeline to identify consistent or differential peaks from replicated ChIP-Seq data. Bioinformatics. 30 (2014), 2568–2575, 10.1093/bioinformatics/btu372.
Feng, J., Liu, T., Qin, B., et al. Identifying ChIP-seq enrichment using MACS. Nat. Protoc. 7 (2012), 1728–1740, 10.1038/nprot.2012.101.
Bailey, T.L., Johnson, J., Grant, C.E., et al. The MEME suite. Nucleic Acids Res. 43 (2015), W39–W49, 10.1093/nar/gkv416.
Thomas-Chollier, M., Herrmann, C., Defrance, M., et al. RSAT peak-motifs: motif analysis in full-size ChIP-seq datasets. Nucleic Acids Res., 40, 2011, e31, 10.1093/nar/gkr1104.
Thomas-Chollier, M., Darbo, E., Herrmann, C., et al. A complete workflow for the analysis of full-size ChIP-seq (and similar) data sets using peak-motifs. Nat. Protoc. 7 (2012), 1551–1568, 10.1038/nprot.2012.088.
Grant, C.E., Bailey, T.L., Noble, W.S., FIMO: scanning for occurrences of a given motif. Bioinformatics. 27 (2011), 1017–1018, 10.1093/bioinformatics/btr064.
Bindea, G., Mlecnik, B., Hackl, H., et al. ClueGO: a Cytoscape plug-in to decipher functionally grouped gene ontology and pathway annotation networks. Bioinformatics. 25 (2009), 1091–1093, 10.1093/bioinformatics/btp101.
Akerman, I., Kasaai, B., Bazarova, A., et al. A predictable conserved DNA base composition signature defines human core DNA replication origins. Nat. Commun., 11, 2020, 4826, 10.1038/s41467-020-18527-0.
Katoh, K., Standley, D.M., MAFFT multiple sequence alignment software version 7: improvements in performance and usability. Mol. Biol. Evol. 30 (2013), 772–780, 10.1093/molbev/mst010.
Suyama, M., Torrents, D., Bork, P., PAL2NAL: robust conversion of protein sequence alignments into the corresponding codon alignments. Nucleic Acids Res. 34 (2006), W609–W612, 10.1093/nar/gkl315.
Stamatakis, A., RAxML version 8: a tool for phylogenetic analysis and post-analysis of large phylogenies. Bioinformatics. 30 (2014), 1312–1313, 10.1093/bioinformatics/btu033.
Yang, Z., PAML 4: phylogenetic analysis by maximum likelihood. Mol. Biol. Evol. 24 (2007), 1586–1591, 10.1093/molbev/msm088.
Uhlén, M., Fagerberg, L., Hallström, B.M., et al. Proteomics. Tissue-based map of the human proteome. Science, 347, 2015, 1260419, 10.1126/science.1260419.
Song, X.C., Fu, G., Yang, X., et al. Protein expression profiling of breast cancer cells by dissociable antibody microarray (DAMA) staining. Mol. Cell. Proteomics 7 (2008), 163–169, 10.1074/mcp.M700115-MCP200.
Pan, C., Kumar, C., Bohl, S., et al. Comparative proteomic phenotyping of cell lines and primary cells to assess preservation of cell type-specific functions. Mol. Cell. Proteomics 8 (2009), 443–540, 10.1074/mcp.M800258-MCP200.
Ghazalpour, A., Bennett, B., Petyuk, V.A., et al. Comparative analysis of proteome and transcriptome variation in mouse. PLoS Genet., 7, 2011, e1001393, 10.1371/journal.pgen.1001393.
Vogel, C., Marcotte, E.M., Insights into the regulation of protein abundance from proteomic and transcriptomic analyses. Nat. Rev. Genet. 13 (2012), 227–232, 10.1038/nrg3185.
Payne, S.H., The utility of protein and mRNA correlation. Trends Biochem. Sci. 40 (2015), 1–3, 10.1016/j.tibs.2014.10.010.
Liu, Y., Beyer, A., Aebersold, R., On the dependency of cellular protein levels on mRNA abundance. Cell. 165 (2016), 535–550, 10.1016/j.cell.2016.03.014.
Kind, J., Pagie, L., de Vries, S.S., et al. Genome-wide maps of nuclear lamina interactions in single human cells. Cell. 163 (2015), 134–147, 10.1016/j.cell.2015.08.040.
Dixon, J.R., Selvaraj, S., Yue, F., et al. Topological domains in mammalian genomes identified by analysis of chromatin interactions. Nature. 485 (2012), 376–380, 10.1038/nature11082.
McCole, R.B., Erceg, J., Saylor, W., et al. Ultraconserved elements occupy specific arenas of three-dimensional mammalian genome organization. Cell Rep. 24 (2018), 479–488, 10.1016/j.celrep.2018.06.031.
Hong, S., Kim, D., Computational characterization of chromatin domain boundary-associated genomic element. Nucleic Acids Res. 45 (2017), 10403–10414, 10.1093/nar/gkx738.
Picard, F., Cadoret, J.C., Audit, B., et al. The spatiotemporal program of DNA replication is associated with specific combinations of chromatin marks in human cells. PLoS Genet., 10, 2014, e1004282, 10.1371/journal.pgen.1004282.
Langley, A.R., Gräf, S., Smith, J.C., et al. Genome-wide identification and characterisation of human DNA replication origins by initiation site sequencing (ini-seq). Nucleic Acids Res. 44 (2016), 10230–10247, 10.1093/nar/gkw760.
Petryk, N., Kahli, M., d'Aubenton-Carafa, Y., et al. Replication landscape of the human genome. Nat. Commun., 7, 2016, 10208, 10.1038/ncomms10208.
Kuruppumullage Don, P., Ananda, G., Chiaromonte, F., et al. Segmenting the human genome based on states of neutral genetic divergence. Proc. Natl. Acad. Sci. U. S. A. 110 (2013), 14699–14704, 10.1073/pnas.1221792110.
Gao, T., Qian, J., EnhancerAtlas 2.0: an updated resource with enhancer annotation in 586 tissue/cell types across nine species. Nucleic. Acids. Res. 48 (2020), D58–D64, 10.1093/nar/gkz980.
The FANTOM 5 Consortium and the RIKEN PMI and CLST (DGT), A promoter-level mammalian expression atlas. Nature 507 (2014), 462–470, 10.1038/nature13182.
Miotto, B., How genomic approaches help the understanding of the initiation of DNA replication. Med. Sci. (Paris) 33 (2017), 143–150.
Hyrien, O., Peaks cloaked in the mist: the landscape of mammalian replication origins. J. Cell Biol. 208 (2015), 147–160, 10.1083/jcb.201407004.
Vaklavas, C., Blume, S.W., Grizzle, W.E., Translational dysregulation in cancer: molecular insights and potential clinical applications in biomarker development. Front. Oncol., 7, 2017, 158, 10.3389/fonc.2017.00158.
Ingolia, N.T., Ribosome footprint profiling of translation throughout the genome. Cell 165:2016 (2016), 22–33, 10.1016/j.cell.2016.02.066.
Na, C.H., Barbhuiya, M.A., Kim, M.S., et al. Discovery of noncanonical translation initiation sites through mass spectrometric analysis of protein N termini. Genome Res. 28 (2018), 25–36, 10.1101/gr.226050.117.
Gogol-Döring, A., Ammar, I., Gupta, S., et al. Genome-wide profiling reveals remarkable parallels between insertion site selection properties of the MLV retrovirus and the piggyBac transposon in primary human CD4(+) T cells. Mol. Ther. 24 (2016), 592–606, 10.1038/mt.2016.11.
Rhee, H.S., Pugh, B.F., ChIP-exo method for identifying genomic location of DNA-binding proteins with near-single-nucleotide accuracy. Curr. Protoc. Mol. Biol., 21, 2012, 10.1002/0471142727.mb2124s100 Unit 21.24.
Hillion, S., Rochas, C., Youinou, P., et al. Signaling pathways regulating RAG expression in B lymphocytes. Autoimmun. Rev. 8 (2019), 599–604, 10.1016/j.autrev.2009.02.004.
Spicuglia, S., Pekowska, A., Zacarias-Cabeza, J., et al. Epigenetic control of Tcrb gene rearrangement. Semin. Immunol. 22 (2010), 330–336, 10.1016/j.smim.2010.07.002.
Majumder, K., Bassing, C.H., Oltz, E.M., Regulation of Tcrb gene assembly by genetic, epigenetic, and topological mechanisms. Adv. Immunol. 128 (2015), 273–306, 10.1016/bs.ai.2015.07.001.
Zhang, Y., Cheng, T.C., Huang, G., et al. Transposon molecular domestication and the evolution of the RAG recombinase. Nature 569 (2019), 79–84.
Navarro, J.M., Touzart, A., Pradel, L.C., et al. Site- and allele-specific polycomb dysregulation in T-cell leukaemia. Nat. Commun., 6, 2015, 6094, 10.1038/s41586-019-1093-7.
Papaemmanuil, E., Rapado, I., Li, Y., et al. RAG-mediated recombination is the predominant driver of oncogenic rearrangement in ETV6-RUNX1 acute lymphoblastic leukemia. Nat. Genet. 46 (2014), 116–125, 10.1038/ng.2874.
Halper-Stromberg, E., Steranka, J., Giraldo-Castillo, N., et al. Fine mapping of V(D)J recombinase mediated rearrangements in human lymphoid malignancies. BMC Genomics, 14, 2013, 565, 10.1186/1471-2164-14-565.
Liu, P., Xiang, Y., Fujinaga, K., et al. Release of positive transcription elongation factor b (P-TEFb) from 7SK small nuclear ribonucleoprotein (snRNP) activates hexamethylene bisacetamide-inducible protein (HEXIM1) transcription. J. Biol. Chem. 289 (2014), 9918–9925, 10.1074/jbc.M113.539015.
Stadelmayer, B., Micas, G., Gamot, A., et al. Integrator complex regulates NELF-mediated RNA polymerase II pause/release and processivity at coding genes. Nat. Commun., 5, 2014, 5531, 10.1038/ncomms6531.
Welboren, W.J., Sweep, F.C., Span, P.N., et al. Genomic actions of estrogen receptor alpha: what are the targets and how are they regulated?. Endocr. Relat. Cancer 16 (2009), 1073–1089, 10.1677/ERC-09-0086.
Francesca Finotello, F., Camillo, B.D., Measuring differential gene expression with RNA-seq: challenges and strategies for data analysis. Brief Funct. Genomics. 14 (2015), 130–142, 10.1093/bfgp/elu035.
Anders, S., Huber, W., Differential expression analysis for sequence count data. Genome Biol., 11, 2010, R106, 10.1186/gb-2010-11-10-r106.
Nie, Z., Hu, G., Wei, G., et al. c-Myc is a universal amplifier of expressed genes in lymphocytes and embryonic stem cells. Cell 151 (2012), 68–79, 10.1016/j.cell.2012.08.033.
Lin, C.Y., Lovén, J., Rahl, P.B., et al. Transcriptional amplification in tumor cells with elevated c-Myc. Cell 151 (2012), 56–67, 10.1016/j.cell.2012.08.026.
Staveley, B.E., Heslip, T.R., Hodgetts, R.B., et al. Protected P-element termini suggest a role for inverted-repeat-binding protein in transposase-induced gap repair in Drosophila melanogaster. Genetics 139 (1995), 1321–1329 7768441.
Jin, Y., Chen, Y., Zhao, S., et al. DNA-PK facilitates piggyBac transposition by promoting paired-end complex formation. Proc. Natl. Acad. Sci. U. S. A. 114 (2017), 7408–7413, 10.1073/pnas.1612980114.
Izsvák, Z., Stüwe, E.E., Fiedler, D., et al. Healing the wounds inflicted by sleeping beauty transposition by double-strand break repair in mammalian somatic cells. Mol. Cell 13 (2004), 279–290, 10.1016/s1097-2765(03)00524-0.
Raval, P., Kriatchko, A.N., Kumar, S., et al. Evidence for Ku70/Ku80 association with full-length RAG1. Nucleic Acids Res. 36 (2008), 2060–2072, 10.1093/nar/gkn049.
Marmignon, A., Bischerour, J., Silve, A., et al. Ku-mediated coupling of DNA cleavage and repair during programmed genome rearrangements in the ciliate Paramecium tetraurelia. PLoS Genet., 10, 2014, e1004552, 10.1371/journal.pgen.1004552.
Kolacsek, O., Pergel, E., Varga, N., et al. Ct shift: a novel and accurate real-time PCR quantification model for direct comparison of different nucleic acid sequences and its application for transposon quantifications. Gene. 598 (2017), 43–49, 10.1016/j.gene.2016.10.035.
Kolacsek, O., Orbán, T.I., Transcription activity of transposon sequence limits sleeping beauty transposition. Gene. 676 (2018), 184–188, 10.1016/j.gene.2018.07.045.
Kasten-Pisula, U., Tastan, H., Dikomey, E., Huge differences in cellular radiosensitivity due to only very small variations in double-strand break repair capacity. Int. J. Radiat. Biol. 81 (2005), 409–419, 10.1080/09553000500140498.
Kaur, E., Nair, J., Ghorai, A., et al. Inhibition of SETMAR-H3K36me2-NHEJ repair axis in residual disease cells prevent glioblastoma recurrence. Neuro. Oncol., 2020, 10.1093/neuonc/noaa128 in press.
Maréchal, A., Li, J.M., Ji, X.Y., et al. PRP19 transforms into a sensor of RPA-ssDNA after DNA damage and drives ATR activation via a ubiquitin-mediated circuitry. Mol. Cell 53 (2014), 235–246, 10.1016/j.molcel.2013.11.002.
Mahajan, K., hPso4/hPrp19: a critical component of DNA repair and DNA damage checkpoint complexes. Oncogene. 35 (2016), 2279–2286, 10.1038/onc.2015.321.
Augé-Gouillou, C., Hamelin, M.H., Demattei, M.V., et al. The ITR binding domain of the mariner Mos-1 transposase. Mol. Gen. Genomics. 265 (2001), 58–65, 10.1007/s004380000386.
Zhang, L., Dawson, A., Finnegan, D.J., DNA-binding activity and subunit interaction of the mariner transposase. Nucleic Acids Res. 29 (2001), 3566–3575, 10.1093/nar/29.17.3566.
Augé-Gouillou, C., Brillet, B., Germon, S., et al. Mariner Mos1 transposase dimerizes prior to ITR binding. J. Mol. Biol. 351 (2005), 117–130, 10.1016/j.jmb.2005.05.019.
Demattei, M.V., Hedhili, S., Sinzelle, L., et al. Nuclear importation of mariner transposases among eukaryotes: motif requirements and homo-protein interactions. PLoS One, 6, 2011, e23693, 10.1371/journal.pone.0023693.
