Novel synthetic lethality screening method identifies TIP60-dependent radiation sensitivity in the absence of BAF180
In recent years, research into synthetic lethality and how it can be exploited in cancer treatments has emerged as major focus in cancer research. However, the lack of a simple to use, sensitive and standardised assay to test for synthetic interactions has been slowing the efforts. Here we present a...
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| Published in: | DNA repair Vol. 46; pp. 47 - 54 |
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01.10.2016
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| Abstract | In recent years, research into synthetic lethality and how it can be exploited in cancer treatments has emerged as major focus in cancer research. However, the lack of a simple to use, sensitive and standardised assay to test for synthetic interactions has been slowing the efforts. Here we present a novel approach to synthetic lethality screening based on co-culturing two syngeneic cell lines containing individual fluorescent tags. By associating shRNAs for a target gene or control to individual fluorescence labels, we can easily follow individual cell fates upon siRNA treatment and high content imaging. We have demonstrated that the system can recapitulate the functional defects of the target gene depletion and is capable of discovering novel synthetic interactors and phenotypes. In a trial screen, we show that TIP60 exhibits synthetic lethality interaction with BAF180, and that in the absence of TIP60, there is an increase micronuclei dependent on the level of BAF180 loss, significantly above levels seen with BAF180 present. Moreover, the severity of the interactions correlates with proxy measurements of BAF180 knockdown efficacy, which may expand its usefulness to addressing synthetic interactions through titratable hypomorphic gene expression. |
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| AbstractList | In recent years, research into synthetic lethality and how it can be exploited in cancer treatments has emerged as major focus in cancer research. However, the lack of a simple to use, sensitive and standardised assay to test for synthetic interactions has been slowing the efforts. Here we present a novel approach to synthetic lethality screening based on co-culturing two syngeneic cell lines containing individual fluorescent tags. By associating shRNAs for a target gene or control to individual fluorescence labels, we can easily follow individual cell fates upon siRNA treatment and high content imaging. We have demonstrated that the system can recapitulate the functional defects of the target gene depletion and is capable of discovering novel synthetic interactors and phenotypes. In a trial screen, we show that TIP60 exhibits synthetic lethality interaction with BAF180, and that in the absence of TIP60, there is an increase micronuclei dependent on the level of BAF180 loss, significantly above levels seen with BAF180 present. Moreover, the severity of the interactions correlates with proxy measurements of BAF180 knockdown efficacy, which may expand its usefulness to addressing synthetic interactions through titratable hypomorphic gene expression. |
| Author | Downs, Jessica A. Hopkins, Suzanna R. McGregor, Grant A. Savic, Velibor Murray, Johanne M. |
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| Cites_doi | 10.1056/NEJM200104053441401 10.1038/msb.2013.54 10.1038/nchembio.2017 10.1146/annurev-pharmtox-010814-124511 10.1038/nrd3374 10.1016/j.celrep.2014.02.012 10.4161/cc.9.5.10931 10.1016/j.molcel.2014.06.028 10.1038/nrc3559 |
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| References | Vizeacoumar, Arnold, Vizeacoumar, Chandrashekhar, Buzina, Young, Kwan, Sayad, Mero, Lawo (bib0020) 2013; 9 Tebbutt, Pedersen, Johns (bib0010) 2013; 13 Brownlee, Chambers, Cloney, Bianchi, Downs (bib0030) 2014; 6 Chan, Giaccia (bib0025) 2011; 10 Sun, Jiang, Price (bib0040) 2010; 9 Druker, Talpaz, Resta, Peng, Buchdunger, Ford, Lydon, Kantarjian, Capdeville, Ohno-Jones (bib0005) 2001; 344 Kakarougkas, Ismail, Chambers, Riballo, Herbert, Kunzel, Lobrich, Jeggo, Downs (bib0035) 2014; 55 Mo, Zhuang, Liu, Yao, Qin, Su, Zang, Wang, Zhang, Dou (bib0045) 2016; 12 Fece de la Cruz, Gapp, Nijman (bib0015) 2015; 55 Mo, Zhuang, Liu, Yao, Qin, Su, Zang, Wang, Zhang, Dou (bib0050) 2016; 12 Brownlee (10.1016/j.dnarep.2016.05.030_bib0030) 2014; 6 Kakarougkas (10.1016/j.dnarep.2016.05.030_bib0035) 2014; 55 Mo (10.1016/j.dnarep.2016.05.030_bib0045) 2016; 12 Druker (10.1016/j.dnarep.2016.05.030_bib0005) 2001; 344 Tebbutt (10.1016/j.dnarep.2016.05.030_bib0010) 2013; 13 Chan (10.1016/j.dnarep.2016.05.030_bib0025) 2011; 10 Vizeacoumar (10.1016/j.dnarep.2016.05.030_bib0020) 2013; 9 Sun (10.1016/j.dnarep.2016.05.030_bib0040) 2010; 9 Fece de la Cruz (10.1016/j.dnarep.2016.05.030_bib0015) 2015; 55 Mo (10.1016/j.dnarep.2016.05.030_bib0050) 2016; 12 |
| References_xml | – volume: 9 start-page: 696 year: 2013 ident: bib0020 article-title: A negative genetic interaction map in isogenic cancer cell lines reveals cancer cell vulnerabilities publication-title: Mol. Syst. Biol. – volume: 55 start-page: 723 year: 2014 end-page: 732 ident: bib0035 article-title: Requirement for PBAF in transcriptional repression and repair at DNA breaks in actively transcribed regions of chromatin publication-title: Mol. Cell – volume: 344 start-page: 1031 year: 2001 end-page: 1037 ident: bib0005 article-title: Efficacy and safety of a specific inhibitor of the BCR-ABL tyrosine kinase in chronic myeloid leukemia publication-title: N. Engl. J. Med. – volume: 10 start-page: 351 year: 2011 end-page: 364 ident: bib0025 article-title: Harnessing synthetic lethal interactions in anticancer drug discovery publication-title: Nat. Rev. Drug Discov. – volume: 13 start-page: 663 year: 2013 end-page: 673 ident: bib0010 article-title: Targeting the ERBB family in cancer: couples therapy publication-title: Nat. Rev. Cancer – volume: 6 start-page: 973 year: 2014 end-page: 981 ident: bib0030 article-title: BAF180 promotes cohesion and prevents genome instability and aneuploidy publication-title: Cell Rep. – volume: 12 start-page: 226 year: 2016 end-page: 232 ident: bib0045 article-title: Acetylation of Aurora B by TIP60 ensures accurate chromosomal segregation publication-title: Nat. Chem. Biol. – volume: 12 start-page: 226 year: 2016 end-page: 232 ident: bib0050 article-title: Acetylation of Aurora B by TIP60 ensures accurate chromosomal segregation publication-title: Nat. Chem. Biol. – volume: 55 start-page: 513 year: 2015 end-page: 531 ident: bib0015 article-title: Synthetic lethal vulnerabilities of cancer publication-title: Annu. Rev. Pharmacol. Toxicol. – volume: 9 start-page: 930 year: 2010 end-page: 936 ident: bib0040 article-title: Tip60: connecting chromatin to DNA damage signaling publication-title: Cell Cycle (Georgetown, Tex.) – volume: 344 start-page: 1031 year: 2001 ident: 10.1016/j.dnarep.2016.05.030_bib0005 article-title: Efficacy and safety of a specific inhibitor of the BCR-ABL tyrosine kinase in chronic myeloid leukemia publication-title: N. Engl. J. Med. doi: 10.1056/NEJM200104053441401 – volume: 9 start-page: 696 year: 2013 ident: 10.1016/j.dnarep.2016.05.030_bib0020 article-title: A negative genetic interaction map in isogenic cancer cell lines reveals cancer cell vulnerabilities publication-title: Mol. Syst. Biol. doi: 10.1038/msb.2013.54 – volume: 12 start-page: 226 year: 2016 ident: 10.1016/j.dnarep.2016.05.030_bib0050 article-title: Acetylation of Aurora B by TIP60 ensures accurate chromosomal segregation publication-title: Nat. Chem. Biol. doi: 10.1038/nchembio.2017 – volume: 55 start-page: 513 year: 2015 ident: 10.1016/j.dnarep.2016.05.030_bib0015 article-title: Synthetic lethal vulnerabilities of cancer publication-title: Annu. Rev. Pharmacol. Toxicol. doi: 10.1146/annurev-pharmtox-010814-124511 – volume: 10 start-page: 351 year: 2011 ident: 10.1016/j.dnarep.2016.05.030_bib0025 article-title: Harnessing synthetic lethal interactions in anticancer drug discovery publication-title: Nat. Rev. Drug Discov. doi: 10.1038/nrd3374 – volume: 6 start-page: 973 year: 2014 ident: 10.1016/j.dnarep.2016.05.030_bib0030 article-title: BAF180 promotes cohesion and prevents genome instability and aneuploidy publication-title: Cell Rep. doi: 10.1016/j.celrep.2014.02.012 – volume: 9 start-page: 930 year: 2010 ident: 10.1016/j.dnarep.2016.05.030_bib0040 article-title: Tip60: connecting chromatin to DNA damage signaling publication-title: Cell Cycle (Georgetown, Tex.) doi: 10.4161/cc.9.5.10931 – volume: 55 start-page: 723 year: 2014 ident: 10.1016/j.dnarep.2016.05.030_bib0035 article-title: Requirement for PBAF in transcriptional repression and repair at DNA breaks in actively transcribed regions of chromatin publication-title: Mol. Cell doi: 10.1016/j.molcel.2014.06.028 – volume: 13 start-page: 663 year: 2013 ident: 10.1016/j.dnarep.2016.05.030_bib0010 article-title: Targeting the ERBB family in cancer: couples therapy publication-title: Nat. Rev. Cancer doi: 10.1038/nrc3559 – volume: 12 start-page: 226 year: 2016 ident: 10.1016/j.dnarep.2016.05.030_bib0045 article-title: Acetylation of Aurora B by TIP60 ensures accurate chromosomal segregation publication-title: Nat. Chem. Biol. doi: 10.1038/nchembio.2017 |
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| SubjectTerms | Cell Line, Tumor Cell Survival - radiation effects DNA-Binding Proteins Fluorescent Dyes - metabolism Gene Expression High-Throughput Screening Assays Histone Acetyltransferases - antagonists & inhibitors Histone Acetyltransferases - genetics Histone Acetyltransferases - metabolism Humans Lysine Acetyltransferase 5 Micronucleus Tests Molecular Imaging Nuclear Proteins - deficiency Nuclear Proteins - genetics Osteoblasts - metabolism Osteoblasts - pathology Osteoblasts - radiation effects Radiation Tolerance RNA, Small Interfering - genetics RNA, Small Interfering - metabolism Staining and Labeling - methods Synthetic Lethal Mutations Transcription Factors - deficiency Transcription Factors - genetics |
| Title | Novel synthetic lethality screening method identifies TIP60-dependent radiation sensitivity in the absence of BAF180 |
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