Classical non-homologous end-joining pathway utilizes nascent RNA for error-free double-strand break repair of transcribed genes

Chakraborty, Anirban; Tapryal, Nisha; Venkova, Tatiana; Horikoshi, Nobuo; Pandita, Raj K.; Sarker, Altaf H.; Sarkar, Partha S.; Pandita, Tej K.; Hazra, Tapas K.

doi:10.1038/ncomms13049

Title: Classical non-homologous end-joining pathway utilizes nascent RNA for error-free double-strand break repair of transcribed genes

Journal Article · Wed Oct 05 00:00:00 EDT 2016 · Nature Communications

DOI:https://doi.org/10.1038/ncomms13049· OSTI ID:1623855

Chakraborty, Anirban ^[1]; Tapryal, Nisha ^[1]; Venkova, Tatiana ^[1]; Horikoshi, Nobuo ^[2]; Pandita, Raj K. ^[2]; Sarker, Altaf H. ^[3]; Sarkar, Partha S. ^[4]; Pandita, Tej K. ^[2]; Hazra, Tapas K. ^[1]

University of Texas Medical Branch, Galveston, Texas (United States). Division of Pulmonary and Critical Care Medicine, Department of Internal Medicine, Sealy Center for Molecular Medicine
The Houston Methodist Research Institute, Houston, Texas (United States). Department of Radiation Oncology, The Houston Methodist Research Institute
Lawrence Berkeley National Lab. (LBNL), Berkeley, CA (United States). Division of Life Sciences, Department of Cancer and DNA Damage Responses
University of Texas Medical Branch, Galveston, Texas (United States). Department of Neurology and Neuroscience and Cell Biology

DNA double-strand breaks (DSBs) leading to loss of nucleotides in the transcribed region can be lethal. Classical non-homologous end-joining (C-NHEJ) is the dominant pathway for DSB repair (DSBR) in adult mammalian cells. Here we report that during such DSBR, mammalian C-NHEJ proteins form a multiprotein complex with RNA polymerase II and preferentially associate with the transcribed genes after DSB induction. Depletion of C-NHEJ factors significantly abrogates DSBR in transcribed but not in non-transcribed genes. We hypothesized that nascent RNA can serve as a template for restoring the missing sequences, thus allowing error-free DSBR. We indeed found pre-mRNA in the C-NHEJ complex. Finally, when a DSB-containing plasmid with several nucleotides deleted within the E. coli lacZ gene was allowed time to repair in lacZ expressing mammalian cells, a functional lacZ plasmid could be recovered from control but not C-NHEJ factor-depleted cells, providing important mechanistic insights into C-NHEJ-mediated error-free DSBR of the transcribed genome.

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Sponsoring Organization:: USDOE

Grant/Contract Number:: AC02-05CH11231

OSTI ID:: 1623855

Journal Information:: Nature Communications, Vol. 7, Issue 1; ISSN 2041-1723

Publisher:: Nature Publishing GroupCopyright Statement

Country of Publication:: United States

Language:: English

References (54)

Involvement of human polynucleotide kinase in double-strand break repair by non-homologous end joining Chappell, C. The EMBO Journal, Vol. 21, Issue 11 https://doi.org/10.1093/emboj/21.11.2827	journal	June 2002
MOF Phosphorylation by ATM Regulates 53BP1-Mediated Double-Strand Break Repair Pathway Choice Gupta, Arun; Hunt, Clayton R.; Hegde, Muralidhar L. Cell Reports, Vol. 8, Issue 1 https://doi.org/10.1016/j.celrep.2014.05.044	journal	July 2014
Homologous chromosomes make contact at the sites of double-strand breaks in genes in somatic G0/G1-phase human cells Gandhi, M.; Evdokimova, V. N.; T. Cuenco, K. Proceedings of the National Academy of Sciences, Vol. 109, Issue 24 https://doi.org/10.1073/pnas.1205759109	journal	May 2012
DNA DSB repair pathway choice: an orchestrated handover mechanism Kakarougkas, A.; Jeggo, P. A. The British Journal of Radiology, Vol. 87, Issue 1035 https://doi.org/10.1259/bjr.20130685	journal	March 2014
A human RNA polymerase II complex associated with SRB and DNA-repair proteins Maldonado, Edio; Shiekhattar, Ramin; Sheldon, Michael Nature, Vol. 381, Issue 6577 https://doi.org/10.1038/381086a0	journal	May 1996
Tidying up loose ends: the role of polynucleotide kinase/phosphatase in DNA strand break repair Weinfeld, Michael; Mani, Rajam S.; Abdou, Ismail Trends in Biochemical Sciences, Vol. 36, Issue 5 https://doi.org/10.1016/j.tibs.2011.01.006	journal	May 2011
Transcription Blockage by Bulky End Termini at Single-Strand Breaks in the DNA Template: Differential Effects of 5′ and 3′ Adducts Neil, Alexander J.; Belotserkovskii, Boris P.; Hanawalt, Philip C. Biochemistry, Vol. 51, Issue 44 https://doi.org/10.1021/bi301240y	journal	October 2012
The Role of the Mammalian DNA End-processing Enzyme Polynucleotide Kinase 3’-Phosphatase in Spinocerebellar Ataxia Type 3 Pathogenesis Chatterjee, Arpita; Saha, Saikat; Chakraborty, Anirban PLOS Genetics, Vol. 11, Issue 1 https://doi.org/10.1371/journal.pgen.1004749	journal	January 2015
RNA-driven genetic changes in bacteria and in human cells Shen, Ying; Nandi, Pavan; Taylor, Matthew B. Mutation Research/Fundamental and Molecular Mechanisms of Mutagenesis, Vol. 717, Issue 1-2 https://doi.org/10.1016/j.mrfmmm.2011.03.016	journal	December 2011
The nonhomologous end-joining pathway of DNA repair is required for genomic stability and the suppression of translocations Ferguson, D. O.; Sekiguchi, J. M.; Chang, S. Proceedings of the National Academy of Sciences, Vol. 97, Issue 12 https://doi.org/10.1073/pnas.110152897	journal	May 2000
Quantitative PCR-Based Measurement of Nuclear and Mitochondrial DNA Damage and Repair in Mammalian Cells Santos, Janine H.; Meyer, Joel N.; Mandavilli, Bhaskar S. DNA Repair Protocols https://doi.org/10.1385/1-59259-973-7:183	book	January 2006
Autonomously replicating single-copy episomes in Trypanosoma brucei show unusual stability. Patnaik, P. K.; Kulkarni, S. K.; Cross, G. A. The EMBO Journal, Vol. 12, Issue 6 https://doi.org/10.1002/j.1460-2075.1993.tb05908.x	journal	June 1993
NHEJ and its backup pathways in chromosomal translocations Lieber, Michael R. Nature Structural & Molecular Biology, Vol. 17, Issue 4 https://doi.org/10.1038/nsmb0410-393	journal	April 2010
The TIP60 Complex Regulates Bivalent Chromatin Recognition by 53BP1 through Direct H4K20me Binding and H2AK15 Acetylation Jacquet, Karine; Fradet-Turcotte, Amélie; Avvakumov, Nikita Molecular Cell, Vol. 62, Issue 3 https://doi.org/10.1016/j.molcel.2016.03.031	journal	May 2016
Posttranscriptional regulation of gene expression—adding another layer of complexity to the DNA damage response Boucas, Jorge; Riabinska, Arina; Jokic, Mladen Frontiers in Genetics, Vol. 3 https://doi.org/10.3389/fgene.2012.00159	journal	January 2012
The Mechanism of Double-Strand DNA Break Repair by the Nonhomologous DNA End-Joining Pathway Lieber, Michael R. Annual Review of Biochemistry, Vol. 79, Issue 1 https://doi.org/10.1146/annurev.biochem.052308.093131	journal	June 2010
AP Endonuclease-Independent DNA Base Excision Repair in Human Cells Wiederhold, Lee; Leppard, John B.; Kedar, Padmini Molecular Cell, Vol. 15, Issue 2 https://doi.org/10.1016/j.molcel.2004.06.003	journal	July 2004
Transcript RNA supports precise repair of its own DNA gene Keskin, Havva; Meers, Chance; Storici, Francesca RNA Biology, Vol. 13, Issue 2 https://doi.org/10.1080/15476286.2015.1116676	journal	December 2015
Accurate transcription initiation by RNA polymerase II in a soluble extract from isolated mammalian nuclei Dignam, J. D.; Lebovitz, R. M.; Roeder, R. G. Nucleic Acids Research, Vol. 11, Issue 5 https://doi.org/10.1093/nar/11.5.1475	journal	March 1983
RNA-templated DNA repair Storici, Francesca; Bebenek, Katarzyna; Kunkel, Thomas A. Nature, Vol. 447, Issue 7142 https://doi.org/10.1038/nature05720	journal	April 2007
Mechanism of Eukaryotic Homologous Recombination San Filippo, Joseph; Sung, Patrick; Klein, Hannah Annual Review of Biochemistry, Vol. 77, Issue 1 https://doi.org/10.1146/annurev.biochem.77.061306.125255	journal	June 2008
DICER, DROSHA and DNA damage response RNAs are necessary for the secondary recruitment of DNA damage response factors Francia, Sofia; Cabrini, Matteo; Matti, Valentina Journal of Cell Science, Vol. 129, Issue 7 https://doi.org/10.1242/jcs.182188	journal	February 2016
Neil2 -null Mice Accumulate Oxidized DNA Bases in the Transcriptionally Active Sequences of the Genome and Are Susceptible to Innate Inflammation Chakraborty, Anirban; Wakamiya, Maki; Venkova-Canova, Tatiana Journal of Biological Chemistry, Vol. 290, Issue 41 https://doi.org/10.1074/jbc.m115.658146	journal	August 2015
Alternative end-joining is suppressed by the canonical NHEJ component Xrcc4–ligase IV during chromosomal translocation formation Simsek, Deniz; Jasin, Maria Nature Structural & Molecular Biology, Vol. 17, Issue 4 https://doi.org/10.1038/nsmb.1773	journal	March 2010
DNA damage during the G0/G1 phase triggers RNA-templated, Cockayne syndrome B-dependent homologous recombination Wei, Leizhen; Nakajima, Satoshi; Böhm, Stefanie Proceedings of the National Academy of Sciences, Vol. 112, Issue 27 https://doi.org/10.1073/pnas.1507105112	journal	June 2015
Deficiency in Repair of the Mitochondrial Genome Sensitizes Proliferating Myoblasts to Oxidative Damage Szczesny, Bartosz; Olah, Gabor; Walker, Dillon K. PLoS ONE, Vol. 8, Issue 9 https://doi.org/10.1371/journal.pone.0075201	journal	September 2013
Regulation of ultraviolet light-induced gene expression by gene size McKay, B. C.; Stubbert, L. J.; Fowler, C. C. Proceedings of the National Academy of Sciences, Vol. 101, Issue 17 https://doi.org/10.1073/pnas.0308181101	journal	April 2004
Molecular Cloning of the Human Gene, PNKP , Encoding a Polynucleotide Kinase 3′-Phosphatase and Evidence for Its Role in Repair of DNA Strand Breaks Caused by Oxidative Damage Jilani, Arshad; Ramotar, Dindial; Slack, Carolyn Journal of Biological Chemistry, Vol. 274, Issue 34 https://doi.org/10.1074/jbc.274.34.24176	journal	August 1999
How does RNase H recognize a DNA.RNA hybrid? Nakamura, H.; Oda, Y.; Iwai, S. Proceedings of the National Academy of Sciences, Vol. 88, Issue 24 https://doi.org/10.1073/pnas.88.24.11535	journal	December 1991
Menage á trois: Double strand break repair, V(D)J recombination and DNA-PK: Menage á trois Jeggo, Penny A.; Taccioli, Guillermo E.; Jackson, Stephen P. BioEssays, Vol. 17, Issue 11 https://doi.org/10.1002/bies.950171108	journal	November 1995
The Case for Junk DNA Palazzo, Alexander F.; Gregory, T. Ryan PLoS Genetics, Vol. 10, Issue 5 https://doi.org/10.1371/journal.pgen.1004351	journal	May 2014
Dynamic nuclear reorganization during genome remodeling of Tetrahymena Chalker, Douglas L. Biochimica et Biophysica Acta (BBA) - Molecular Cell Research, Vol. 1783, Issue 11 https://doi.org/10.1016/j.bbamcr.2008.07.012	journal	November 2008
Repair of DNA double-strand breaks by templated nucleotide sequence insertions derived from distant regions of the genome Onozawa, M.; Zhang, Z.; Kim, Y. J. Proceedings of the National Academy of Sciences, Vol. 111, Issue 21 https://doi.org/10.1073/pnas.1321889111	journal	May 2014
Small RNA and transcriptional upregulation: Small RNA and transcriptional upregulation Portnoy, Victoria; Huang, Vera; Place, Robert F. Wiley Interdisciplinary Reviews: RNA, Vol. 2, Issue 5 https://doi.org/10.1002/wrna.90	journal	May 2011
Transcriptionally active chromatin recruits homologous recombination at DNA double-strand breaks Aymard, François; Bugler, Beatrix; Schmidt, Christine K. Nature Structural & Molecular Biology, Vol. 21, Issue 4 https://doi.org/10.1038/nsmb.2796	journal	March 2014
Site-specific DICER and DROSHA RNA products control the DNA-damage response Francia, Sofia; Michelini, Flavia; Saxena, Alka Nature, Vol. 488, Issue 7410 https://doi.org/10.1038/nature11179	journal	May 2012
RNA polymerase: The most specific damage recognition protein in cellular responses to DNA damage? Lindsey-Boltz, L. A.; Sancar, A. Proceedings of the National Academy of Sciences, Vol. 104, Issue 33 https://doi.org/10.1073/pnas.0706316104	journal	August 2007
Transcript-RNA-templated DNA recombination and repair Keskin, Havva; Shen, Ying; Huang, Fei Nature, Vol. 515, Issue 7527 https://doi.org/10.1038/nature13682	journal	September 2014
Regulation of Homologous Recombination in Eukaryotes Heyer, Wolf-Dietrich; Ehmsen, Kirk T.; Liu, Jie Annual Review of Genetics, Vol. 44, Issue 1 https://doi.org/10.1146/annurev-genet-051710-150955	journal	December 2010
Requirement for the Kinase Activity of Human DNA-Dependent Protein Kinase Catalytic Subunit in DNA Strand Break Rejoining Kurimasa, Akihiro; Kumano, Satoshi; Boubnov, Nikolai V. Molecular and Cellular Biology, Vol. 19, Issue 5 https://doi.org/10.1128/mcb.19.5.3877	journal	May 1999
Ku and DNA-dependent Protein Kinase Dynamic Conformations and Assembly Regulate DNA Binding and the Initial Non-homologous End Joining Complex Hammel, Michal; Yu, Yaping; Mahaney, Brandi L. Journal of Biological Chemistry, Vol. 285, Issue 2 https://doi.org/10.1074/jbc.M109.065615	journal	November 2009
Human Mre11/Human Rad50/Nbs1 and DNA Ligase IIIα/XRCC1 Protein Complexes Act Together in an Alternative Nonhomologous End Joining Pathway Della-Maria, Julie; Zhou, Yi; Tsai, Miaw-Sheue Journal of Biological Chemistry, Vol. 286, Issue 39 https://doi.org/10.1074/jbc.M111.274159	journal	August 2011
53BP1, BRCA1, and the Choice between Recombination and End Joining at DNA Double-Strand Breaks Daley, J. M.; Sung, P. Molecular and Cellular Biology, Vol. 34, Issue 8 https://doi.org/10.1128/MCB.01639-13	journal	January 2014
Probing the phenomics of noncoding RNA Mattick, John S. eLife, Vol. 2 https://doi.org/10.7554/eLife.01968	journal	December 2013
RNA-Mediated Programming of Developmental Genome Rearrangements in Paramecium tetraurelia Garnier, Olivier; Serrano, Vincent; Duharcourt, Sandra Molecular and Cellular Biology, Vol. 24, Issue 17 https://doi.org/10.1128/MCB.24.17.7370-7379.2004	journal	September 2004
Preferential Repair of Oxidized Base Damage in the Transcribed Genes of Mammalian Cells Banerjee, Dibyendu; Mandal, Santi M.; Das, Aditi Journal of Biological Chemistry, Vol. 286, Issue 8 https://doi.org/10.1074/jbc.M110.198796	journal	December 2010
Hyperthermia Activates a Subset of Ataxia-Telangiectasia Mutated Effectors Independent of DNA Strand Breaks and Heat Shock Protein 70 Status Hunt, Clayton R.; Pandita, Raj K.; Laszlo, Andrei Cancer Research, Vol. 67, Issue 7 https://doi.org/10.1158/0008-5472.CAN-06-4328	journal	April 2007
Reversible cross-linking combined with immunoprecipitation to study RNA–protein interactions in vivo Niranjanakumari, S. Methods, Vol. 26, Issue 2 https://doi.org/10.1016/S1046-2023(02)00021-X	journal	February 2002
Role of Human DNA Glycosylase Nei-like 2 (NEIL2) and Single Strand Break Repair Protein Polynucleotide Kinase 3′-Phosphatase in Maintenance of Mitochondrial Genome Mandal, Santi M.; Hegde, Muralidhar L.; Chatterjee, Arpita Journal of Biological Chemistry, Vol. 287, Issue 4 https://doi.org/10.1074/jbc.M111.272179	journal	November 2011
Quantitative PCR-Based Measurement of Nuclear and Mitochondrial DNA Damage and Repair in Mammalian Cells Furda, Amy; Santos, Janine H.; Meyer, Joel N. Molecular Toxicology Protocols https://doi.org/10.1007/978-1-62703-739-6_31	book	January 2014
Roles of the BRD4 short isoform in phase separation and active gene transcription Han, Xinye; Yu, Di; Gu, Ruirui Nature Structural & Molecular Biology, Vol. 27, Issue 4 https://doi.org/10.1038/s41594-020-0394-8	journal	March 2020
MOF Phosphorylation by ATM Regulates 53BP1-Mediated Double-Strand Break Repair Pathway Choice Gupta, Arun; Hunt, Clayton R.; Hegde, Muralidhar L. Cell Reports, Vol. 8, Issue 1 https://doi.org/10.1016/j.celrep.2014.06.034	journal	July 2014
Ataxin-3, DNA Damage Repair, and SCA3 Cerebellar Degeneration: On the Path to Parsimony? Ward, Jacqueline M.; La Spada, Albert R. PLOS Genetics, Vol. 11, Issue 1 https://doi.org/10.1371/journal.pgen.1004937	journal	January 2015
Multiple knockout mouse models reveal lincRNAs are required for life and brain development Sauvageau, Martin; Goff, Loyal A.; Lodato, Simona eLife, Vol. 2 https://doi.org/10.7554/elife.01749	journal	December 2013

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