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Mechanisms of Ubiquitin-Nucleosome Recognition and Regulation of 53BP1 Chromatin Recruitment by RNF168/169 and RAD18.

Hu Q, Botuyan MV, Cui G, Zhao D, Mer G
Mol Cell 66 473-487.e9 (2017)
Cited: 48 times
EuropePMC logo PMID: 28506460

Abstract

The protein 53BP1 plays a central regulatory role in DNA double-strand break repair. 53BP1 relocates to chromatin by recognizing RNF168-mediated mono-ubiquitylation of histone H2A Lys15 in the nucleosome core particle dimethylated at histone H4 Lys20 (NCP-ubme). 53BP1 relocation is terminated by ubiquitin ligases RNF169 and RAD18 via unknown mechanisms. Using nuclear magnetic resonance (NMR) spectroscopy and biochemistry, we show that RNF169 bridges ubiquitin and histone surfaces, stabilizing a pre-existing ubiquitin orientation in NCP-ubme to form a high-affinity complex. This conformational selection mechanism contrasts with the low-affinity binding mode of 53BP1, and it ensures 53BP1 displacement by RNF169 from NCP-ubme. We also show that RAD18 binds tightly to NCP-ubme through a ubiquitin-binding domain that contacts ubiquitin and nucleosome surfaces accessed by 53BP1. Our work uncovers diverse ubiquitin recognition mechanisms in the nucleosome, explaining how RNF168, RNF169, and RAD18 regulate 53BP1 chromatin recruitment and how specificity can be achieved in the recognition of a ubiquitin-modified substrate.

Articles - 5vey mentioned but not cited (1)

  1. Mechanisms of Ubiquitin-Nucleosome Recognition and Regulation of 53BP1 Chromatin Recruitment by RNF168/169 and RAD18. Hu Q, Botuyan MV, Cui G, Zhao D, Mer G. Mol Cell 66 473-487.e9 (2017)


Reviews citing this publication (19)

  1. How cells ensure correct repair of DNA double-strand breaks. Her J, Bunting SF. J Biol Chem 293 10502-10511 (2018)
  2. Reading chromatin signatures after DNA double-strand breaks. Wilson MD, Durocher D. Philos Trans R Soc Lond B Biol Sci 372 (2017)
  3. Ubiquitin and ubiquitin-like molecules in DNA double strand break repair. Yu J, Qin B, Lou Z. Cell Biosci 10 13 (2020)
  4. Accelerating the Field of Epigenetic Histone Modification Through Mass Spectrometry-Based Approaches. Lu C, Coradin M, Porter EG, Garcia BA. Mol Cell Proteomics 20 100006 (2021)
  5. A role of the 53BP1 protein in genome protection: structural and functional characteristics of 53BP1-dependent DNA repair. Bártová E, Legartová S, Dundr M, Suchánková J. Aging (Albany NY) 11 2488-2511 (2019)
  6. Chromatin Regulation through Ubiquitin and Ubiquitin-like Histone Modifications. Vaughan RM, Kupai A, Rothbart SB. Trends Biochem Sci 46 258-269 (2021)
  7. Beyond reversal: ubiquitin and ubiquitin-like proteases and the orchestration of the DNA double strand break repair response. Garvin AJ. Biochem Soc Trans 47 1881-1893 (2019)
  8. The Chromatin Landscape Channels DNA Double-Strand Breaks to Distinct Repair Pathways. Chen Z, Tyler JK. Front Cell Dev Biol 10 909696 (2022)
  9. Visualizing Conformational Ensembles of the Nucleosome by NMR. Musselman CA, Kutateladze TG. ACS Chem Biol 17 495-502 (2022)
  10. DNA Damage Response Regulation by Histone Ubiquitination. Sekiguchi M, Matsushita N. Int J Mol Sci 23 8187 (2022)
  11. Strategies for Generating Modified Nucleosomes: Applications within Structural Biology Studies. Musselman CA, Kutateladze TG. ACS Chem Biol 14 579-586 (2019)
  12. Ubiquitylation-Mediated Fine-Tuning of DNA Double-Strand Break Repair. Borsos BN, Majoros H, Pankotai T. Cancers (Basel) 12 (2020)
  13. Multifaceted regulation and functions of 53BP1 in NHEJ‑mediated DSB repair (Review). Lei T, Du S, Peng Z, Chen L. Int J Mol Med 50 90 (2022)
  14. 53BP1: Keeping It under Control, Even at a Distance from DNA Damage. Rass E, Willaume S, Bertrand P. Genes (Basel) 13 2390 (2022)
  15. DNA Double Strand Break Repair and Its Control by Nucleosome Remodeling. Karl LA, Peritore M, Galanti L, Pfander B. Front Genet 12 821543 (2021)
  16. Decoding histone ubiquitylation. Chen JJ, Stermer D, Tanny JC. Front Cell Dev Biol 10 968398 (2022)
  17. Insights from the protein interaction Universe of the multifunctional "Goldilocks" kinase DYRK1A. Ananthapadmanabhan V, Shows KH, Dickinson AJ, Litovchick L. Front Cell Dev Biol 11 1277537 (2023)
  18. New answers to the old RIDDLE: RNF168 and the DNA damage response pathway. Kelliher J, Ghosal G, Leung JWC. FEBS J (2021)
  19. Versatile control of the CDC48 segregase by the plant UBX-containing (PUX) proteins. Zhang J, Vancea AI, Shahul Hameed UF, Arold ST. Comput Struct Biotechnol J 19 3125-3132 (2021)

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  1. 53BP1 Enforces Distinct Pre- and Post-resection Blocks on Homologous Recombination. Callen E, Zong D, Wu W, Wong N, Stanlie A, Ishikawa M, Pavani R, Dumitrache LC, Byrum AK, Mendez-Dorantes C, Martinez P, Canela A, Maman Y, Day A, Kruhlak MJ, Blasco MA, Stark JM, Mosammaparast N, McKinnon PJ, Nussenzweig A. Mol Cell 77 26-38.e7 (2020)
  2. Stimulation of CRISPR-mediated homology-directed repair by an engineered RAD18 variant. Nambiar TS, Billon P, Diedenhofen G, Hayward SB, Taglialatela A, Cai K, Huang JW, Leuzzi G, Cuella-Martin R, Palacios A, Gupta A, Egli D, Ciccia A. Nat Commun 10 3395 (2019)
  3. Acetylation of 53BP1 dictates the DNA double strand break repair pathway. Guo X, Bai Y, Zhao M, Zhou M, Shen Q, Yun CH, Zhang H, Zhu WG, Wang J. Nucleic Acids Res 46 689-703 (2018)
  4. A comprehensive proteomics-based interaction screen that links DYRK1A to RNF169 and to the DNA damage response. Roewenstrunk J, Di Vona C, Chen J, Borras E, Dong C, Arató K, Sabidó E, Huen MSY, de la Luna S. Sci Rep 9 6014 (2019)
  5. DYRK1A regulates the recruitment of 53BP1 to the sites of DNA damage in part through interaction with RNF169. Menon VR, Ananthapadmanabhan V, Swanson S, Saini S, Sesay F, Yakovlev V, Florens L, DeCaprio JA, Washburn MP, Dozmorov M, Litovchick L. Cell Cycle 18 531-551 (2019)
  6. Human papillomavirus E7 oncoprotein targets RNF168 to hijack the host DNA damage response. Sitz J, Blanchet SA, Gameiro SF, Biquand E, Morgan TM, Galloy M, Dessapt J, Lavoie EG, Blondeau A, Smith BC, Mymryk JS, Moody CA, Fradet-Turcotte A. Proc Natl Acad Sci U S A 116 19552-19562 (2019)
  7. Mechanism of 53BP1 activity regulation by RNA-binding TIRR and a designer protein. Botuyan MV, Cui G, Drané P, Oliveira C, Detappe A, Brault ME, Parnandi N, Chaubey S, Thompson JR, Bragantini B, Zhao D, Chapman JR, Chowdhury D, Mer G. Nat Struct Mol Biol 25 591-600 (2018)
  8. RNF168-Mediated Ubiquitin Signaling Inhibits the Viability of BRCA1-Null Cancers. Krais JJ, Wang Y, Bernhardy AJ, Clausen E, Miller JA, Cai KQ, Scott CL, Johnson N. Cancer Res 80 2848-2860 (2020)
  9. RNF169 limits 53BP1 deposition at DSBs to stimulate single-strand annealing repair. An L, Dong C, Li J, Chen J, Yuan J, Huang J, Chan KM, Yu CH, Huen MSY. Proc Natl Acad Sci U S A 115 E8286-E8295 (2018)
  10. Comprehensive nucleosome interactome screen establishes fundamental principles of nucleosome binding. Skrajna A, Goldfarb D, Kedziora KM, Cousins EM, Grant GD, Spangler CJ, Barbour EH, Yan X, Hathaway NA, Brown NG, Cook JG, Major MB, McGinty RK. Nucleic Acids Res 48 9415-9432 (2020)
  11. Structural basis of specific H2A K13/K15 ubiquitination by RNF168. Horn V, Uckelmann M, Zhang H, Eerland J, Aarsman I, le Paige UB, Davidovich C, Sixma TK, van Ingen H. Nat Commun 10 1751 (2019)
  12. A bi-terminal protein ligation strategy to probe chromatin structure during DNA damage. Kilic S, Boichenko I, Lechner CC, Fierz B. Chem Sci 9 3704-3709 (2018)
  13. An LTR retrotransposon-derived lncRNA interacts with RNF169 to promote homologous recombination. Deng B, Xu W, Wang Z, Liu C, Lin P, Li B, Huang Q, Yang J, Zhou H, Qu L. EMBO Rep 20 e47650 (2019)
  14. Letter Chemically synthesized histone H2A Lys13 di-ubiquitination promotes binding of 53BP1 to nucleosomes. Li JB, Qi YK, He QQ, Ai HS, Liu SL, Wang JX, Zheng JS, Liu L, Tian C. Cell Res 28 257-260 (2018)
  15. Structural basis of nucleosome dynamics modulation by histone variants H2A.B and H2A.Z.2.2. Zhou M, Dai L, Li C, Shi L, Huang Y, Guo Z, Wu F, Zhu P, Zhou Z. EMBO J 40 e105907 (2021)
  16. Ubiquitin Phosphorylation at Thr12 Modulates the DNA Damage Response. Walser F, Mulder MPC, Bragantini B, Burger S, Gubser T, Gatti M, Botuyan MV, Villa A, Altmeyer M, Neri D, Ovaa H, Mer G, Penengo L. Mol Cell 80 423-436.e9 (2020)
  17. Mechanisms of BRCA1-BARD1 nucleosome recognition and ubiquitylation. Hu Q, Botuyan MV, Zhao D, Cui G, Mer E, Mer G. Nature 596 438-443 (2021)
  18. Structural Basis for the Interaction of Mutasome Assembly Factor REV1 with Ubiquitin. Cui G, Botuyan MV, Mer G. J Mol Biol 430 2042-2050 (2018)
  19. Ectopic RNF168 expression promotes break-induced replication-like DNA synthesis at stalled replication forks. Krais JJ, Johnson N. Nucleic Acids Res 48 4298-4308 (2020)
  20. Design of genetically encoded sensors to detect nucleosome ubiquitination in live cells. Dos Santos Passos C, Choi YS, Snow CD, Yao T, Cohen RE. J Cell Biol 220 (2021)
  21. Histone H2A variants alpha1-extension helix directs RNF168-mediated ubiquitination. Kelliher JL, West KL, Gong Q, Leung JWC. Nat Commun 11 2462 (2020)
  22. Enhancement of CRISPR-Cas9 induced precise gene editing by targeting histone H2A-K15 ubiquitination. Bashir S, Dang T, Rossius J, Wolf J, Kühn R. BMC Biotechnol 20 57 (2020)
  23. Two NEMO-like Ubiquitin-Binding Domains in CEP55 Differently Regulate Cytokinesis. Said Halidi KN, Fontan E, Boucharlat A, Davignon L, Charpentier M, Boullé M, Weil R, Israël A, Laplantine E, Agou F. iScience 20 292-309 (2019)
  24. Ubiquitylation in DNA double-strand break repair. Tang M, Li S, Chen J. DNA Repair (Amst) 103 103129 (2021)
  25. Defective repair of topoisomerase I induced chromosomal damage in Huntington's disease. Palminha NM, Dos Santos Souza C, Griffin J, Liao C, Ferraiuolo L, El-Khamisy SF. Cell Mol Life Sci 79 160 (2022)
  26. Laser Microirradiation and Real-time Recruitment Assays Using an Engineered Biosensor. Passos CDS, Cohen RE, Yao T. Bio Protoc 12 e4337 (2022)
  27. TRABID overexpression enables synthetic lethality to PARP inhibitor via prolonging 53BP1 retention at double-strand breaks. Ma J, Zhou Y, Pan P, Yu H, Wang Z, Li LL, Wang B, Yan Y, Pan Y, Ye Q, Liu T, Feng X, Xu S, Wang K, Wang X, Jian Y, Ma B, Fan Y, Gao Y, Huang H, Li L. Nat Commun 14 1810 (2023)
  28. UBA80 and UBA52 fine-tune RNF168-dependent histone ubiquitination and DNA repair. Lee SO, Kelliher JL, Song W, Tengler K, Sarkar A, Dray E, Leung JWC. J Biol Chem 299 105043 (2023)


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