The E3 ubiquitin ligase TRIP12 participates in cell cycle progression and chromosome stability.
Journal
Scientific reports
ISSN: 2045-2322
Titre abrégé: Sci Rep
Pays: England
ID NLM: 101563288
Informations de publication
Date de publication:
21 01 2020
21 01 2020
Historique:
received:
23
09
2019
accepted:
03
01
2020
entrez:
23
1
2020
pubmed:
23
1
2020
medline:
15
12
2020
Statut:
epublish
Résumé
Several studies have linked the E3 ubiquitin ligase TRIP12 (Thyroid hormone Receptor Interacting Protein 12) to the cell cycle. However, the regulation and the implication of this protein during the cell cycle are largely unknown. In this study, we show that TRIP12 expression is regulated during the cell cycle, which correlates with its nuclear localization. We identify an euchromatin-binding function of TRIP12 mediated by a N-terminal intrinsically disordered region. We demonstrate the functional implication of TRIP12 in the mitotic entry by controlling the duration of DNA replication that is independent from its catalytic activity. We also show the requirement of TRIP12 in the mitotic progression and chromosome stability. Altogether, our findings show that TRIP12 is as a new chromatin-associated protein with several implications in the cell cycle progression and in the maintenance of genome integrity.
Identifiants
pubmed: 31964993
doi: 10.1038/s41598-020-57762-9
pii: 10.1038/s41598-020-57762-9
pmc: PMC6972862
doi:
Substances chimiques
Carrier Proteins
0
Euchromatin
0
TRIP12 protein, human
EC 2.3.2.26
Ubiquitin-Protein Ligases
EC 2.3.2.27
Types de publication
Journal Article
Research Support, Non-U.S. Gov't
Langues
eng
Sous-ensembles de citation
IM
Pagination
789Références
Chen, D., Yoon, J.-B. & Gu, W. Reactivating the ARF-p53 axis in AML cells by targeting ULF. Cell Cycle Georget. Tex 9, 2946–2951 (2010).
Xie, Y. & Varshavsky, A. UFD4 lacking the proteasome-binding region catalyses ubiquitination but is impaired in proteolysis. Nat. Cell Biol. 4, 1003–1007 (2002).
pubmed: 12447385
doi: 10.1038/ncb889
Ju, D., Wang, X., Xu, H. & Xie, Y. The armadillo repeats of the Ufd4 ubiquitin ligase recognize ubiquitin-fusion proteins. FEBS Lett. 581, 265–270 (2007).
pubmed: 17204268
doi: 10.1016/j.febslet.2006.12.024
pmcid: 17204268
Keppler, B. R. & Archer, T. K. Ubiquitin-dependent and ubiquitin-independent control of subunit stoichiometry in the SWI/SNF complex. J. Biol. Chem. 285, 35665–35674 (2010).
pubmed: 20829358
pmcid: 2975191
doi: 10.1074/jbc.M110.173997
Park, Y., Yoon, S. K. & Yoon, J.-B. TRIP12 functions as an E3 ubiquitin ligase of APP-BP1. Biochem. Biophys. Res. Commun. 374, 294–298 (2008).
pubmed: 18627766
doi: 10.1016/j.bbrc.2008.07.019
pmcid: 18627766
Gudjonsson, T. et al. TRIP12 and UBR5 suppress spreading of chromatin ubiquitylation at damaged chromosomes. Cell 150, 697–709 (2012).
pubmed: 22884692
doi: 10.1016/j.cell.2012.06.039
Chen, D. et al. Differential effects on ARF stability by normal versus oncogenic levels of c-Myc expression. Mol. Cell 51, 46–56 (2013).
pubmed: 23747016
doi: 10.1016/j.molcel.2013.05.006
Kweon, S.-M. et al. An Adversarial DNA N6-Methyladenine-Sensor Network Preserves Polycomb Silencing. Mol. Cell https://doi.org/10.1016/j.molcel.2019.03.018 (2019).
pubmed: 30982744
pmcid: 6591016
doi: 10.1016/j.molcel.2019.03.018
Hanoun, N. et al. The E3 ubiquitin ligase thyroid hormone receptor-interacting protein 12 targets pancreas transcription factor 1a for proteasomal degradation. J. Biol. Chem. 289, 35593–35604 (2014).
pubmed: 25355311
pmcid: 4271242
doi: 10.1074/jbc.M114.620104
Kajiro, M. et al. The E3 ubiquitin ligase activity of Trip12 is essential for mouse embryogenesis. PloS One 6, e25871 (2011).
pubmed: 22028794
pmcid: 3196520
doi: 10.1371/journal.pone.0025871
Chen, D. et al. regulation in oncogenic stress-mediated p53 responses. Nature 464, 624–627 (2010).
pubmed: 20208519
pmcid: 3737736
doi: 10.1038/nature08820
Cai, J.-B. et al. Ubiquitin-specific protease 7 accelerates p14(ARF) degradation by deubiquitinating thyroid hormone receptor-interacting protein 12 and promotes hepatocellular carcinoma progression. Hepatol. Baltim. Md. 61, 1603–1614 (2015).
doi: 10.1002/hep.27682
Wang, L. et al. TRIP12 as a mediator of human papillomavirus/p16-related radiation enhancement effects. Oncogene 36, 820–828 (2017).
pubmed: 27425591
doi: 10.1038/onc.2016.250
O’Roak, B. J. et al. Recurrent de novo mutations implicate novel genes underlying simplex autism risk. Nat. Commun. 5, 5595 (2014).
pubmed: 25418537
pmcid: 4249945
doi: 10.1038/ncomms6595
Bramswig, N. C. et al. Identification of new TRIP12 variants and detailed clinical evaluation of individuals with non-syndromic intellectual disability with or without autism. Hum. Genet. 136, 179–192 (2017).
pubmed: 27848077
doi: 10.1007/s00439-016-1743-x
Siddiqui, K., On, K. F. & Diffley, J. F. X. Regulating DNA replication in eukarya. Cold Spring Harb. Perspect. Biol. 5 (2013).
Lau, Y. F. & Arrighi, F. E. Studies of mammalian chromosome replication. II. Evidence for the existence of defined chromosome replicating units. Chromosoma 83, 721–741 (1981).
pubmed: 7028418
doi: 10.1007/BF00328530
Dunphy, W. G., Brizuela, L., Beach, D. & Newport, J. The Xenopus cdc2 protein is a component of MPF, a cytoplasmic regulator of mitosis. Cell 54, 423–431 (1988).
pubmed: 3293802
doi: 10.1016/0092-8674(88)90205-X
Parker, L. L. & Piwnica-Worms, H. Inactivation of the p34cdc2-cyclin B complex by the human WEE1 tyrosine kinase. Science 257, 1955–1957 (1992).
pubmed: 1384126
doi: 10.1126/science.1384126
McLean, J. R., Chaix, D., Ohi, M. D. & Gould, K. L. State of the APC/C: organization, function, and structure. Crit. Rev. Biochem. Mol. Biol. 46, 118–136 (2011).
pubmed: 21261459
pmcid: 4856037
doi: 10.3109/10409238.2010.541420
Musacchio, A. & Salmon, E. D. The spindle-assembly checkpoint in space and time. Nat. Rev. Mol. Cell Biol. 8, 379–393 (2007).
pubmed: 17426725
doi: 10.1038/nrm2163
Pesin, J. A. & Orr-Weaver, T. L. Regulation of APC/C activators in mitosis and meiosis. Annu. Rev. Cell Dev. Biol. 24, 475–499 (2008).
pubmed: 18598214
pmcid: 4070676
doi: 10.1146/annurev.cellbio.041408.115949
Ganem, N. J. & Pellman, D. Linking abnormal mitosis to the acquisition of DNA damage. J. Cell Biol. 199, 871–881 (2012).
pubmed: 23229895
pmcid: 3518222
doi: 10.1083/jcb.201210040
Crasta, K. et al. DNA breaks and chromosome pulverization from errors in mitosis. Nature 482, 53–58 (2012).
pubmed: 22258507
pmcid: 3271137
doi: 10.1038/nature10802
Aviner, R., Shenoy, A., Elroy-Stein, O. & Geiger, T. Uncovering Hidden Layers of Cell Cycle Regulation through Integrative Multi-omic Analysis. PLoS Genet. 11, e1005554 (2015).
pubmed: 26439921
pmcid: 4595013
doi: 10.1371/journal.pgen.1005554
van der Lee, R. et al. Classification of intrinsically disordered regions and proteins. Chem. Rev. 114, 6589–6631 (2014).
pubmed: 24773235
pmcid: 4095912
doi: 10.1021/cr400525m
Sabari, B. R. et al. Coactivator condensation at super-enhancers links phase separation and gene control. Science 361 (2018).
Pines, J. & Hunter, T. Isolation of a human cyclin cDNA: evidence for cyclin mRNA and protein regulation in the cell cycle and for interaction with p34cdc2. Cell 58, 833–846 (1989).
pubmed: 2570636
doi: 10.1016/0092-8674(89)90936-7
Enders, G. H. Gauchos and ochos: a Wee1-Cdk tango regulating mitotic entry. Cell Div. 5, 12 (2010).
pubmed: 20465818
pmcid: 2886006
doi: 10.1186/1747-1028-5-12
Lindqvist, A., van Zon, W., Karlsson Rosenthal, C. & Wolthuis, R. M. F. Cyclin B1-Cdk1 activation continues after centrosome separation to control mitotic progression. PLoS Biol. 5, e123 (2007).
pubmed: 17472438
pmcid: 1858714
doi: 10.1371/journal.pbio.0050123
Coverley, D., Laman, H. & Laskey, R. A. Distinct roles for cyclins E and A during DNA replication complex assembly and activation. Nat. Cell Biol. 4, 523–528 (2002).
pubmed: 12080347
doi: 10.1038/ncb813
Li, C., Andrake, M., Dunbrack, R. & Enders, G. H. A bifunctional regulatory element in human somatic Wee1 mediates cyclin A/Cdk2 binding and Crm1-dependent nuclear export. Mol. Cell. Biol. 30, 116–130 (2010).
pubmed: 19858290
doi: 10.1128/MCB.01876-08
pmcid: 19858290
den Elzen, N. & Pines, J. Cyclin A is destroyed in prometaphase and can delay chromosome alignment and anaphase. J. Cell Biol. 153, 121–136 (2001).
doi: 10.1083/jcb.153.1.121
De Boer, L. et al. Cyclin A/cdk2 coordinates centrosomal and nuclear mitotic events. Oncogene 27, 4261–4268 (2008).
pubmed: 18372919
doi: 10.1038/onc.2008.74
pmcid: 18372919
Whitfield, M. L. et al. Identification of Genes Periodically Expressed in the Human Cell Cycle and Their Expression in Tumors. Mol. Biol. Cell 13, 1977–2000 (2002).
pubmed: 12058064
pmcid: 117619
doi: 10.1091/mbc.02-02-0030
Dobson, T., Chen, J. & Krushel, L. A. Dysregulating IRES-Dependent Translation Contributes to Overexpression of Oncogenic Aurora A Kinase. Mol. Cancer Res. 11, 887–900 (2013).
pubmed: 23661421
pmcid: 4109694
doi: 10.1158/1541-7786.MCR-12-0707
Chen, W., Smeekens, J. M. & Wu, R. Systematic study of the dynamics and half-lives of newly synthesized proteins in human cells. Chem. Sci. 7, 1393–1400 (2016).
pubmed: 29910897
doi: 10.1039/C5SC03826J
pmcid: 29910897
Ma, H. et al. M phase phosphorylation of the epigenetic regulator UHRF1 regulates its physical association with the deubiquitylase USP7 and stability. Proc. Natl. Acad. Sci. USA 109, 4828–4833 (2012).
pubmed: 22411829
doi: 10.1073/pnas.1116349109
Petrone, A., Adamo, M. E., Cheng, C. & Kettenbach, A. N. Identification of Candidate Cyclin-dependent kinase 1 (Cdk1) Substrates in Mitosis by Quantitative Phosphoproteomics. Mol. Cell. Proteomics MCP 15, 2448–2461 (2016).
pubmed: 27134283
doi: 10.1074/mcp.M116.059394
pmcid: 27134283
Dyson, H. J. & Wright, P. E. Intrinsically unstructured proteins and their functions. Nat. Rev. Mol. Cell Biol. 6, 197–208 (2005).
pubmed: 15738986
doi: 10.1038/nrm1589
Peng, Z. & Kurgan, L. High-throughput prediction of RNA, DNA and protein binding regions mediated by intrinsic disorder. Nucleic Acids Res. 43, e121 (2015).
pubmed: 26109352
pmcid: 4605291
doi: 10.1093/nar/gkv585
Wang, C., Uversky, V. N. & Kurgan, L. Disordered nucleiome: Abundance of intrinsic disorder in the DNA- and RNA-binding proteins in 1121 species from Eukaryota, Bacteria and Archaea. Proteomics 16, 1486–1498 (2016).
pubmed: 27037624
doi: 10.1002/pmic.201500177
Maréchal, A. 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, 235–246 (2014).
pubmed: 24332808
doi: 10.1016/j.molcel.2013.11.002
Braden, W. A., McClendon, A. K. & Knudsen, E. S. Cyclin-dependent kinase 4/6 activity is a critical determinant of pre-replication complex assembly. Oncogene 27, 7083–7093 (2008).
pubmed: 18776921
doi: 10.1038/onc.2008.319
Demeret, C., Vassetzky, Y. & Méchali, M. Chromatin remodelling and DNA replication: from nucleosomes to loop domains. Oncogene 20, 3086–3093 (2001).
pubmed: 11420724
doi: 10.1038/sj.onc.1204333
Cao, Q. et al. The central role of EED in the orchestration of polycomb group complexes. Nat. Commun. 5, 3127 (2014).
pubmed: 24457600
pmcid: 4073494
doi: 10.1038/ncomms4127
Oliviero, G. et al. Dynamic Protein Interactions of the Polycomb Repressive Complex 2 during Differentiation of Pluripotent Cells. Mol. Cell. Proteomics MCP 15, 3450–3460 (2016).
pubmed: 27634302
doi: 10.1074/mcp.M116.062240
Abe, S. et al. The initial phase of chromosome condensation requires Cdk1-mediated phosphorylation of the CAP-D3 subunit of condensin II. Genes Dev. 25, 863–874 (2011).
pubmed: 21498573
pmcid: 3078710
doi: 10.1101/gad.2016411
Wu, R. S., Kohn, K. W. & Bonner, W. M. Metabolism of ubiquitinated histones. J. Biol. Chem. 256, 5916–5920 (1981).
pubmed: 6263895
Arora, M. et al. Promoters active in interphase are bookmarked during mitosis by ubiquitination. Nucleic Acids Res. 40, 10187–10202 (2012).
pubmed: 22941662
pmcid: 3488253
doi: 10.1093/nar/gks820
Giunta, S., Belotserkovskaya, R. & Jackson, S. P. DNA damage signaling in response to double-strand breaks during mitosis. J. Cell Biol. 190, 197–207 (2010).
pubmed: 20660628
pmcid: 2930281
doi: 10.1083/jcb.200911156
Nakajima, D. et al. Preparation of a set of expression-ready clones of mammalian long cDNAs encoding large proteins by the ORF trap cloning method. DNA Res. Int. J. Rapid Publ. Rep. Genes Genomes 12, 257–267 (2005).
Torrisani, J. et al. let-7 MicroRNA transfer in pancreatic cancer-derived cells inhibits in vitro cell proliferation but fails to alter tumor progression. Hum Gene Ther 20, 831–44 (2009).
pubmed: 19323605
doi: 10.1089/hum.2008.134
Dosztányi, Z., Csizmók, V., Tompa, P. & Simon, I. The pairwise energy content estimated from amino acid composition discriminates between folded and intrinsically unstructured proteins. J. Mol. Biol. 347, 827–839 (2005).
pubmed: 15769473
doi: 10.1016/j.jmb.2005.01.071
Linding, R., Russell, R. B., Neduva, V. & Gibson, T. J. GlobPlot: Exploring protein sequences for globularity and disorder. Nucleic Acids Res. 31, 3701–3708 (2003).
pubmed: 12824398
pmcid: 169197
doi: 10.1093/nar/gkg519
Linding, R. et al. Protein disorder prediction: implications for structural proteomics. Struct. Lond. Engl. 1993 11, 1453–1459 (2003).