The HLTF-PARP1 Interaction in the Progression and Stability of Damaged Replication Forks Caused by Methyl Methanesulfonate

Overview

Journal Oncogenesis

Date 2020 Dec 7

PMID 33281189

Citations 9

Authors

Jia-Lin Shiu

Cheng-Kuei Wu

Song-Bin Chang

Yan-Jhih Sun

Yen-Ju Chen

Chien-Chen Lai

Wen-Tai Chiu

Wen-Tsan Chang

Kyungjae Myung

Wen-Pin Su

Hungjiun Liaw

Affiliations

Soon will be listed here.

Abstract

Human HLTF participates in the lesion-bypass mechanism through the fork reversal structure, known as template switching of post-replication repair. However, the mechanism by which HLTF promotes the replication progression and fork stability of damaged forks remains unclear. Here, we identify a novel protein-protein interaction between HLTF and PARP1. The depletion of HLTF and PARP1 increases chromosome breaks, further reduces the length of replication tracks, and concomitantly increases the number of stalled forks after methyl methanesulfonate treatment according to a DNA fiber analysis. The progression of replication also depends on BARD1 in the presence of MMS treatment. By combining 5-ethynyl-2'-deoxyuridine with a proximity ligation assay, we revealed that the HLTF, PARP1, and BRCA1/BARD1/RAD51 proteins were initially recruited to damaged forks. However, prolonged stalling of damaged forks results in fork collapse. HLTF and PCNA dissociate from the collapsed forks, with increased accumulation of PARP1 and BRCA1/BARD1/RAD51 at the collapsed forks. Our results reveal that HLTF together with PARP1 and BARD1 participates in the stabilization of damaged forks, and the PARP1-BARD1 interaction is further involved in the repair of collapse forks.

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References

Zhao W, Steinfeld J, Liang F, Chen X, Maranon D, Ma C . BRCA1-BARD1 promotes RAD51-mediated homologous DNA pairing. Nature. 2017; 550(7676):360-365. PMC: 5800781. DOI: 10.1038/nature24060. View

Ensminger M, Iloff L, Ebel C, Nikolova T, Kaina B, Lbrich M . DNA breaks and chromosomal aberrations arise when replication meets base excision repair. J Cell Biol. 2014; 206(1):29-43. PMC: 4085701. DOI: 10.1083/jcb.201312078. View

Masutani C, KUSUMOTO R, Iwai S, Hanaoka F . Mechanisms of accurate translesion synthesis by human DNA polymerase eta. EMBO J. 2000; 19(12):3100-9. PMC: 203367. DOI: 10.1093/emboj/19.12.3100. View

Betous R, Mason A, Rambo R, Bansbach C, Badu-Nkansah A, Sirbu B . SMARCAL1 catalyzes fork regression and Holliday junction migration to maintain genome stability during DNA replication. Genes Dev. 2012; 26(2):151-62. PMC: 3273839. DOI: 10.1101/gad.178459.111. View

Scharer O . Nucleotide excision repair in eukaryotes. Cold Spring Harb Perspect Biol. 2013; 5(10):a012609. PMC: 3783044. DOI: 10.1101/cshperspect.a012609. View

Vujanovic M, Krietsch J, Raso M, Terraneo N, Zellweger R, Schmid J . Replication Fork Slowing and Reversal upon DNA Damage Require PCNA Polyubiquitination and ZRANB3 DNA Translocase Activity. Mol Cell. 2017; 67(5):882-890.e5. PMC: 5594246. DOI: 10.1016/j.molcel.2017.08.010. View

Satoh M, Lindahl T . Role of poly(ADP-ribose) formation in DNA repair. Nature. 1992; 356(6367):356-8. DOI: 10.1038/356356a0. View

Lin J, Zeman M, Chen J, Yee M, Cimprich K . SHPRH and HLTF act in a damage-specific manner to coordinate different forms of postreplication repair and prevent mutagenesis. Mol Cell. 2011; 42(2):237-49. PMC: 3080461. DOI: 10.1016/j.molcel.2011.02.026. View

Langelier M, Planck J, Roy S, Pascal J . Structural basis for DNA damage-dependent poly(ADP-ribosyl)ation by human PARP-1. Science. 2012; 336(6082):728-32. PMC: 3532513. DOI: 10.1126/science.1216338. View

10.

Heller R, Marians K . Replisome assembly and the direct restart of stalled replication forks. Nat Rev Mol Cell Biol. 2006; 7(12):932-43. DOI: 10.1038/nrm2058. View

11.

Petermann E, Orta M, Issaeva N, Schultz N, Helleday T . Hydroxyurea-stalled replication forks become progressively inactivated and require two different RAD51-mediated pathways for restart and repair. Mol Cell. 2010; 37(4):492-502. PMC: 2958316. DOI: 10.1016/j.molcel.2010.01.021. View

12.

SUZUKA I, Daidoji H, Matsuoka M, Kadowaki K, Takasaki Y, Nakane P . Gene for proliferating-cell nuclear antigen (DNA polymerase delta auxiliary protein) is present in both mammalian and higher plant genomes. Proc Natl Acad Sci U S A. 1989; 86(9):3189-93. PMC: 287092. DOI: 10.1073/pnas.86.9.3189. View

13.

Unk I, Hajdu I, Blastyak A, Haracska L . Role of yeast Rad5 and its human orthologs, HLTF and SHPRH in DNA damage tolerance. DNA Repair (Amst). 2010; 9(3):257-67. DOI: 10.1016/j.dnarep.2009.12.013. View

14.

DAmours D, Desnoyers S, DSilva I, Poirier G . Poly(ADP-ribosyl)ation reactions in the regulation of nuclear functions. Biochem J. 1999; 342 ( Pt 2):249-68. PMC: 1220459. View

15.

Petruk S, Sedkov Y, Johnston D, Hodgson J, Black K, Kovermann S . TrxG and PcG proteins but not methylated histones remain associated with DNA through replication. Cell. 2012; 150(5):922-33. PMC: 3432699. DOI: 10.1016/j.cell.2012.06.046. View

16.

Roy S, Luzwick J, Schlacher K . SIRF: Quantitative in situ analysis of protein interactions at DNA replication forks. J Cell Biol. 2018; 217(4):1521-1536. PMC: 5881507. DOI: 10.1083/jcb.201709121. View

17.

Betous R, Couch F, Mason A, Eichman B, Manosas M, Cortez D . Substrate-selective repair and restart of replication forks by DNA translocases. Cell Rep. 2013; 3(6):1958-69. PMC: 3700663. DOI: 10.1016/j.celrep.2013.05.002. View

18.

Ciccia A, Nimonkar A, Hu Y, Hajdu I, Achar Y, Izhar L . Polyubiquitinated PCNA recruits the ZRANB3 translocase to maintain genomic integrity after replication stress. Mol Cell. 2012; 47(3):396-409. PMC: 3613862. DOI: 10.1016/j.molcel.2012.05.024. View

19.

Berti M, Ray Chaudhuri A, Thangavel S, Gomathinayagam S, Kenig S, Vujanovic M . Human RECQ1 promotes restart of replication forks reversed by DNA topoisomerase I inhibition. Nat Struct Mol Biol. 2013; 20(3):347-54. PMC: 3897332. DOI: 10.1038/nsmb.2501. View

20.

McCulloch S, Kokoska R, Masutani C, Iwai S, Hanaoka F, Kunkel T . Preferential cis-syn thymine dimer bypass by DNA polymerase eta occurs with biased fidelity. Nature. 2004; 428(6978):97-100. DOI: 10.1038/nature02352. View