3,836
Views
7
CrossRef citations to date
0
Altmetric
Review

Disassembly of the Shieldin Complex by TRIP13

, &
Pages 1565-1575 | Received 25 Mar 2020, Accepted 08 Apr 2020, Published online: 18 May 2020

References

  • Bryant HE, Schultz N, Thomas HD, et al. Specific killing of BRCA2-deficient tumours with inhibitors of poly(ADP-ribose) polymerase. Nature. 2005;434(7035):913–917.
  • Farmer H, McCabe N, Lord CJ, et al. Targeting the DNA repair defect in BRCA mutant cells as a therapeutic strategy. Nature. 2005;434(7035):917–921.
  • Edwards SL, Brough R, Lord CJ, et al. Resistance to therapy caused by intragenic deletion in BRCA2. Nature. 2008;451(7182):1111–1115.
  • Sakai W, Swisher EM, Karlan BY, et al. Secondary mutations as a mechanism of cisplatin resistance in BRCA2-mutated cancers. Nature. 2008;451(7182):1116–1120.
  • Heyer WD, Ehmsen KT, Liu J. Regulation of homologous recombination in eukaryotes. Annu Rev Genet. 2010;44(1):113–139.
  • Bunting SF, Callén E, Wong N, et al. 53BP1 inhibits homologous recombination in Brca1-deficient cells by blocking resection of DNA breaks. Cell. 2010;141(2):243–254.
  • Bouwman P, Aly A, Escandell JM, et al. 53BP1 loss rescues BRCA1 deficiency and is associated with triple-negative and BRCA-mutated breast cancers. Nat Struct Mol Biol. 2010;17(6):688–695.
  • Zimmermann M, Lottersberger F, Buonomo SB, et al. 53BP1 regulates DSB repair using Rif1 to control 5ʹ end resection. Science. 2013;339(6120):700–704.
  • Escribano-Diaz C, Orthwein A, Fradet-Turcotte A, et al. A cell cycle-dependent regulatory circuit composed of 53BP1-RIF1 and BRCA1-CtIP controls DNA repair pathway choice. Mol Cell. 2013;49(5):872–883.
  • Chapman JR, Barral P, Vannier J-B, et al. RIF1 is essential for 53BP1-dependent nonhomologous end joining and suppression of DNA double-strand break resection. Mol Cell. 2013;49(5):858–871.
  • Callen E, Di Virgilio M, Kruhlak M, et al. 53BP1 mediates productive and mutagenic DNA repair through distinct phosphoprotein interactions. Cell. 2013;153(6):1266–1280.
  • Xu G, Chapman JR, Brandsma I, et al. REV7 counteracts DNA double-strand break resection and affects PARP inhibition. Nature. 2015;521(7553):541–544.
  • Boersma V, Moatti N, Segura-Bayona S, et al. MAD2L2 controls DNA repair at telomeres and DNA breaks by inhibiting 5ʹ end resection. Nature. 2015;521(7553):537–540.
  • Goodman MF, Woodgate R. Translesion DNA polymerases. Cold Spring Harb Perspect Biol. 2013;5(10):a010363.
  • Hara K, Hashimoto H, Murakumo Y, et al. Crystal structure of human REV7 in complex with a human REV3 fragment and structural implication of the interaction between DNA polymerase zeta and REV1. J Biol Chem. 2010;285(16):12299–12307.
  • Gupta R, Somyajit K, Narita T, et al. DNA repair network analysis reveals shieldin as a key regulator of NHEJ and PARP inhibitor sensitivity. Cell. 2018;173(4):972–988 e923.
  • Noordermeer SM, Adam S, Setiaputra D, et al. The shieldin complex mediates 53BP1-dependent DNA repair. Nature. 2018;560(7716):117–121.
  • Mirman Z, Lottersberger F, Takai H, et al. 53BP1-RIF1-shieldin counteracts DSB resection through CST- and Polalpha-dependent fill-in. Nature. 2018;560(7716):112–116.
  • Ghezraoui H, Oliveira C, Becker JR, et al. 53BP1 cooperation with the REV7-shieldin complex underpins DNA structure-specific NHEJ. Nature. 2018;560(7716):122–127.
  • Dev H, Chiang T-WW, Lescale C, et al. Shieldin complex promotes DNA end-joining and counters homologous recombination in BRCA1-null cells. Nat Cell Biol. 2018;20(8):954–965.
  • Tomida J, Takata K-I, Bhetawal S, et al. FAM 35A associates with REV 7 and modulates DNA damage responses of normal and BRCA 1-defective cells. Embo J. 2018;37(12). DOI:https://doi.org/10.15252/embj.201899543.
  • Findlay S, Heath J, Luo VM, et al. SHLD 2/ FAM 35A co-operates with REV 7 to coordinate DNA double-strand break repair pathway choice. Embo J. 2018;37(18). DOI:https://doi.org/10.15252/embj.2018100158.
  • Gao S, Feng S, Ning S, et al. An OB-fold complex controls the repair pathways for DNA double-strand breaks. Nat Commun. 2018;9(1):3925.
  • Clairmont CS, Sarangi P, Ponnienselvan K, et al. TRIP13 regulates DNA repair pathway choice through REV7 conformational change. Nat Cell Biol. 2020;22(1):87–96.
  • Fradet-Turcotte A, Canny MD, Escribano-Díaz C, et al. 53BP1 is a reader of the DNA-damage-induced H2A Lys 15 ubiquitin mark. Nature. 2013;499(7456):50–54.
  • Sanders SL, Portoso M, Mata J, et al. Methylation of histone H4 lysine 20 controls recruitment of Crb2 to sites of DNA damage. Cell. 2004;119(5):603–614.
  • Botuyan MV, Lee J, Ward IM, et al. Structural basis for the methylation state-specific recognition of histone H4-K20 by 53BP1 and Crb2 in DNA repair. Cell. 2006;127(7):1361–1373.
  • Mattiroli F, Vissers JA, van Dijk W, et al. RNF168 ubiquitinates K13-15 on H2A/H2AX to drive DNA damage signaling. Cell. 2012;150(6):1182–1195.
  • Kolas NK, Chapman JR, Nakada S, et al. Orchestration of the DNA-damage response by the RNF8 ubiquitin ligase. Science. 2007;318(5856):1637–1640.
  • Huen MS, Grant R, Manke I, et al. RNF8 transduces the DNA-damage signal via histone ubiquitylation and checkpoint protein assembly. Cell. 2007;131(5):901–914. .
  • Mailand N, Bekker-Jensen S, Faustrup H, et al. RNF8 ubiquitylates histones at DNA double-strand breaks and promotes assembly of repair proteins. Cell. 2007;131(5):887–900.
  • Doil C, Mailand N, Bekker-Jensen S, et al. RNF168 binds and amplifies ubiquitin conjugates on damaged chromosomes to allow accumulation of repair proteins. Cell. 2009;136(3):435–446.
  • Stewart GS, Panier S, Townsend K, et al. The RIDDLE syndrome protein mediates a ubiquitin-dependent signaling cascade at sites of DNA damage. Cell. 2009;136(3):420–434.
  • Pesavento JJ, Yang H, Kelleher NL, et al. Certain and progressive methylation of histone H4 at lysine 20 during the cell cycle. Mol Cell Biol. 2008;28(1):468–486.
  • Drane P, Brault M-E, Cui G, et al. TIRR regulates 53BP1 by masking its histone methyl-lysine binding function. Nature. 2017;543(7644):211–216.
  • Zhang A, Peng B, Huang P, et al. The p53-binding protein 1-Tudor-interacting repair regulator complex participates in the DNA damage response. J Biol Chem. 2017;292(16):6461–6467.
  • Pellegrino S, Michelena J, Teloni F, et al. Replication-coupled dilution of H4K20me2 guides 53BP1 to pre-replicative chromatin. Cell Rep. 2017;19(9):1819–1831.
  • Simonetta M, de Krijger I, Serrat J, et al. H4K20me2 distinguishes pre-replicative from post-replicative chromatin to appropriately direct DNA repair pathway choice by 53BP1-RIF1-MAD2L2. Cell Cycle. 2018;17(1):124–136.
  • Nelson G, Buhmann M, von Zglinicki T. DNA damage foci in mitosis are devoid of 53BP1. Cell Cycle. 2009;8(20):3379–3383.
  • van Vugt MA, Gardino AK, Linding R, et al. A mitotic phosphorylation feedback network connects Cdk1, Plk1, 53BP1, and Chk2 to inactivate the G(2)/M DNA damage checkpoint. PLoS Biol. 2010;8(1):e1000287.
  • Orthwein A, Fradet-Turcotte A, Noordermeer SM, et al. Mitosis inhibits DNA double-strand break repair to guard against telomere fusions. Science. 2014;344(6180):189–193.
  • Peterson SE, Li Y, Chait BT, et al. Cdk1 uncouples CtIP-dependent resection and Rad51 filament formation during M-phase double-strand break repair. J Cell Biol. 2011;194(5):705–720.
  • Aravind L, Koonin EV. The HORMA domain: a common structural denominator in mitotic checkpoints, chromosome synapsis and DNA repair. Trends Biochem Sci. 1998;23(8):284–286.
  • Suzuki SW, Yamamoto H, Oikawa Y, et al. Atg13 HORMA domain recruits Atg9 vesicles during autophagosome formation. Proc Natl Acad Sci U S A. 2015;112(11):3350–3355.
  • Jao CC, Ragusa MJ, Stanley RE, et al. A HORMA domain in Atg13 mediates PI 3-kinase recruitment in autophagy. Proc Natl Acad Sci U S A. 2013;110(14):5486–5491.
  • Michel M, Schwarten M, Decker C, et al. The mammalian autophagy initiator complex contains 2 HORMA domain proteins. Autophagy. 2015;11(12):2300–2308.
  • Ye Q, Lau RK, Mathews IT, et al. HORMA domain proteins and a Trip13-like ATPase regulate bacterial cGAS-like enzymes to mediate bacteriophage immunity. Mol Cell. 2020;77(4):709–722 e707.
  • Luo X, Tang Z, Xia G, et al. The Mad2 spindle checkpoint protein has two distinct natively folded states. Nat Struct Mol Biol. 2004;11(4):338–345.
  • West AMV, Komives EA, Corbett KD. Conformational dynamics of the Hop1 HORMA domain reveal a common mechanism with the spindle checkpoint protein Mad2. Nucleic Acids Res. 2018;46(1):279–292.
  • Chen RH, Shevchenko A, Mann M, et al. Spindle checkpoint protein XMAD1 recruits Xmad2 to unattached kinetochores. J Cell Biol. 1998;143(2):283–295.
  • Luo X, Tang Z, Rizo J, et al. The Mad2 spindle checkpoint protein undergoes similar major conformational changes upon binding to either MAD1 or Cdc20. Mol Cell. 2002;9(1):59–71.
  • Sironi L, Mapelli M, Knapp S, et al. Crystal structure of the tetrameric MAD1-Mad2 core complex: implications of a ‘safety belt’ binding mechanism for the spindle checkpoint. Embo J. 2002;21(10):2496–2506.
  • De Antoni A, Pearson CG, Cimini D, et al. The MAD1/Mad2 complex as a template for Mad2 activation in the spindle assembly checkpoint. Curr Biol. 2005;15(3):214–225.
  • Mapelli M, Massimiliano L, Santaguida S, et al. The Mad2 conformational dimer: structure and implications for the spindle assembly checkpoint. Cell. 2007;131(4):730–743.
  • Qi S, Kim DJ, Stjepanovic G, et al. Structure of the Human Atg13-Atg101 HORMA Heterodimer: an Interaction Hub within the ULK1 Complex. Structure. 2015;23(10):1848–1857.
  • Hwang LH, Lau LF, Smith DL, et al. Budding yeast Cdc20: a target of the spindle checkpoint. Science. 1998;279(5353):1041–1044.
  • Luo X, Wagner G, Luo X, et al. Structure of the Mad2 spindle assembly checkpoint protein and its interaction with Cdc20. Nat Struct Biol. 2000;7(3):224–229.
  • Hollingsworth NM, Byers B. HOP1: a yeast meiotic pairing gene. Genetics. 1989;121(3):445–462.
  • Hollingsworth NM, Goetsch L, Byers B. The HOP1 gene encodes a meiosis-specific component of yeast chromosomes. Cell. 1990;61(1):73–84.
  • Kim Y, Rosenberg S, Kugel C, et al. The chromosome axis controls meiotic events through a hierarchical assembly of HORMA domain proteins. Dev Cell. 2014;31(4):487–502.
  • Tomida J, Takata K-I, Lange SS, et al. REV7 is essential for DNA damage tolerance via two REV3L binding sites in mammalian DNA polymerase ζ. Nucleic Acids Res. 2015;43(2):1000–1011.
  • Hara K, Taharazako S, Ikeda M, et al. Dynamic feature of mitotic arrest deficient 2-like protein 2 (MAD2L2) and structural basis for its interaction with chromosome alignment-maintaining phosphoprotein (CAMP). J Biol Chem. 2017;292(43):17658–17667.
  • Rizzo AA, Vassel F-M, Chatterjee N, et al. Rev7 dimerization is important for assembly and function of the Rev1/Polζ translesion synthesis complex. Proc Natl Acad Sci U S A. 2018;115(35):E8191–E8200.
  • Wojtasz L, Daniel K, Roig I, et al. Mouse HORMAD1 and HORMAD2, two conserved meiotic chromosomal proteins, are depleted from synapsed chromosome axes with the help of TRIP13 AAA-ATPase. PLoS Genet. 2009;5(10):e1000702.
  • Ye Q, Rosenberg SC, Moeller A, et al. TRIP13 is a protein-remodeling AAA+ ATPase that catalyzes MAD2 conformation switching. Elife. 2015;4. DOI:https://doi.org/10.7554/eLife.07367.
  • Ma HT, Poon RYC. TRIP13 regulates both the activation and inactivation of the spindle-assembly checkpoint. Cell Rep. 2016;14(5):1086–1099.
  • San-Segundo PA, Roeder GS. Pch2 links chromatin silencing to meiotic checkpoint control. Cell. 1999;97(3):313–324.
  • Ho HC, Burgess SM, McKim KS. Pch2 acts through Xrs2 and Tel1/ATM to modulate interhomolog bias and checkpoint function during meiosis. PLoS Genet. 2011;7(11):e1002351.
  • Li XC, Schimenti JC. Mouse pachytene checkpoint 2 (trip13) is required for completing meiotic recombination but not synapsis. PLoS Genet. 2007;3(8):e130.
  • Chen C, Jomaa A, Ortega J, et al. Pch2 is a hexameric ring ATPase that remodels the chromosome axis protein Hop1. Proc Natl Acad Sci U S A. 2014;111(1):E44–53.
  • Ye Q, Kim DH, Dereli I, et al. The AAA + ATP ase TRIP 13 remodels HORMA domains through N-terminal engagement and unfolding. Embo J. 2017;36(16):2419–2434.
  • Eytan E, Wang K, Miniowitz-Shemtov S, et al. Disassembly of mitotic checkpoint complexes by the joint action of the AAA-ATPase TRIP13 and p31(comet). Proc Natl Acad Sci U S A. 2014;111(33):12019–12024.
  • Yang M, Li B, Tomchick DR, et al. p31comet blocks Mad2 activation through structural mimicry. Cell. 2007;131(4):744–755.
  • Ji J, Tang D, Shen Y, et al. P31 comet, a member of the synaptonemal complex, participates in meiotic DSB formation in rice. Proc Natl Acad Sci U S A. 2016;113(38):10577–10582.
  • van Hooff JJ, Tromer E, van Wijk LM, et al. Evolutionary dynamics of the kinetochore network in eukaryotes as revealed by comparative genomics. EMBO Rep. 2017;18(9):1559–1571.
  • Kaisari S, Shomer P, Ziv T, et al. Role of Polo-like kinase 1 in the regulation of the action of p31(comet) in the disassembly of mitotic checkpoint complexes. Proc Natl Acad Sci U S A. 2019;116(24):11725–11730. .
  • Nelson CR, Hwang T, Chen PH, et al. TRIP13PCH-2 promotes Mad2 localization to unattached kinetochores in the spindle checkpoint response. J Cell Biol. 2015;211(3):503–516.
  • Joshi N, Barot A, Jamison C, et al. Pch2 links chromosome axis remodeling at future crossover sites and crossover distribution during yeast meiosis. PLoS Genet. 2009;5(7):e1000557.
  • Wang K, Sturt-Gillespie B, Hittle JC, et al. Thyroid hormone receptor interacting protein 13 (TRIP13) AAA-ATPase is a novel mitotic checkpoint-silencing protein. J Biol Chem. 2014;289(34):23928–23937.
  • Kurita K, Maeda M, Mansour MA, et al. TRIP13 is expressed in colorectal cancer and promotes cancer cell invasion. Oncol Lett. 2016;12(6):5240–5246.
  • Li W, Zhang G, Li X, et al. Thyroid hormone receptor interactor 13 (TRIP13) overexpression associated with tumor progression and poor prognosis in lung adenocarcinoma. Biochem Biophys Res Commun. 2018;499(3):416–424.
  • Banerjee R, Russo N, Liu M, et al. TRIP13 promotes error-prone nonhomologous end joining and induces chemoresistance in head and neck cancer. Nat Commun. 2014;5(1):4527.
  • Mellacheruvu D, Wright Z, Couzens AL, et al. The CRAPome: a contaminant repository for affinity purification-mass spectrometry data. Nat Methods. 2013;10(8):730–736.
  • Yost S, de Wolf B, Hanks S, et al. Biallelic TRIP13 mutations predispose to Wilms tumor and chromosome missegregation. Nat Genet. 2017;49(1):1148–1151.
  • Marks DH, Thomas R, Chin Y, et al. Mad2 overexpression uncovers a critical role for TRIP13 in mitotic exit. Cell Rep. 2017;19(9):1832–1845.
  • Chao WC, Kulkarni K, Zhang Z, et al. Structure of the mitotic checkpoint complex. Nature. 2012;484(7393):208–213.
  • Kikuchi S, Hara K, Shimizu T, et al. Structural basis of recruitment of DNA polymerase ζ by interaction between REV1 and REV7 proteins. J Biol Chem. 2012;287(40):33847–33852.
  • Dai Y, Zhang F, Wang L, et al. Structural basis for shieldin complex subunit 3-mediated recruitment of the checkpoint protein REV7 during DNA double-strand break repair. J Biol Chem. 2020;295(1):250–262.
  • Alfieri C, Chang L, Barford D. Mechanism for remodelling of the cell cycle checkpoint protein MAD2 by the ATPase TRIP13. Nature. 2018;559(7713):274–278.