Human SNM1A and XPF-ERCC1 collaborate to initiate DNA interstrand cross-link repair

被引:116
作者
Wang, Anderson T. [1 ]
Sengerova, Blanka [1 ]
Cattell, Emma [1 ]
Inagawa, Takabumi [1 ]
Hartley, Janet M. [2 ]
Kiakos, Konstantinos [2 ]
Burgess-Brown, Nicola A. [3 ]
Swift, Lonnie P. [1 ]
Enzlin, Jacqueline H. [1 ]
Schofield, Christopher J. [4 ]
Gileadi, Opher [3 ]
Hartley, John A. [2 ]
McHugh, Peter J. [1 ]
机构
[1] Univ Oxford, Weatherall Inst Mol Med, John Radcliffe Hosp, Oxford OX3 9DS, England
[2] UCL, UCL Canc Inst, Canc Res UK Drug DNA Interact Res Grp, London WC1E 6BT, England
[3] Univ Oxford, Struct Genom Consortium, Oxford OX3 7DQ, England
[4] Univ Oxford, Chem Res Lab, Oxford OX1 3TA, England
关键词
DNA repair; interstrand cross-links; SNM1A exonuclease; XPF-ERCC1; endonuclease; metallo-beta-lactamase family; NUCLEOTIDE EXCISION-REPAIR; HOLLIDAY JUNCTION RESOLVASE; MAMMALIAN-CELL EXTRACTS; DOUBLE-STRAND BREAKS; SACCHAROMYCES-CEREVISIAE; FANCONI-ANEMIA; RADIATION RAD; S-PHASE; REPLICATION; SENSITIVITY;
D O I
10.1101/gad.15699211
中图分类号
Q2 [细胞生物学];
学科分类号
071009 ; 090102 ;
摘要
One of the major DNA interstrand cross-link (ICL) repair pathways in mammalian cells is coupled to replication, but the mechanistic roles of the critical factors involved remain largely elusive. Here, we show that purified human SNM1A (hSNM1A), which exhibits a 5'-3' exonuclease activity, can load from a single DNA nick and digest past an ICL on its substrate strand. hSNM1A-depleted cells are ICL-sensitive and accumulate replication-associated DNA double-strand breaks (DSBs), akin to ERCC1-depleted cells. These DSBs are Mus81-induced, indicating that replication fork cleavage by Mus81 results from the failure of the hSNM1A- and XPF-ERCC1-dependent ICL repair pathway. Our results reveal how collaboration between hSNM1A and XPF-ERCC1 is necessary to initiate ICL repair in replicating human cells.
引用
收藏
页码:1859 / 1870
页数:12
相关论文
共 61 条
[1]   Snm1-deficient mice exhibit accelerated tumorigenesis and susceptibility to infection [J].
Ahkter, S ;
Richie, CT ;
Zhang, NX ;
Behringer, RR ;
Zhu, CM ;
Legerski, RJ .
MOLECULAR AND CELLULAR BIOLOGY, 2005, 25 (22) :10071-10078
[2]   DNA replication is required to elicit cellular responses to psoralen-induced DNA interstrand cross-links [J].
Akkari, YMN ;
Bateman, RL ;
Reifsteck, CA ;
Olson, SB ;
Grompe, M .
MOLECULAR AND CELLULAR BIOLOGY, 2000, 20 (21) :8283-8289
[3]   Nucleotide excision repair genes as determinants of cellular sensitivity to cyclophosphamide analogs [J].
Andersson, BS ;
Sadeghi, T ;
Siciliano, MJ ;
Legerski, R ;
Murray, D .
CANCER CHEMOTHERAPY AND PHARMACOLOGY, 1996, 38 (05) :406-416
[4]   Conserved domains in DNA repair proteins and evolution of repair systems [J].
Aravind, L ;
Walker, DR ;
Koonin, EV .
NUCLEIC ACIDS RESEARCH, 1999, 27 (05) :1223-1242
[5]   Snm1B/Apollo mediates replication fork collapse and S Phase checkpoint activation in response to DNA interstrand cross-links [J].
Bae, J-B ;
Mukhopadhyay, S. S. ;
Liu, L. ;
Zhang, N. ;
Tan, J. ;
Akhter, S. ;
Liu, X. ;
Shen, X. ;
Li, L. ;
Legerski, R. J. .
ONCOGENE, 2008, 27 (37) :5045-5056
[6]   DNA interstrand cross-link repair in the Saccharomyces cerevisiae cell cycle:: Overlapping roles for PSO2 (SNM1) with MutS factors and EXO1 during S phase [J].
Barber, LJ ;
Ward, TA ;
Hartley, JA ;
McHugh, PJ .
MOLECULAR AND CELLULAR BIOLOGY, 2005, 25 (06) :2297-2309
[7]   Checkpoint Signaling from a Single DNA Interstrand Crosslink [J].
Ben-Yehoyada, Merav ;
Wang, Lily C. ;
Kozekov, Ivan D. ;
Rizzo, Carmelo J. ;
Gottesman, Max E. ;
Gautier, Jean .
MOLECULAR CELL, 2009, 35 (05) :704-715
[8]   DNA polymerase II (polB) is involved in a new DNA repair pathway for DNA interstrand cross-links in Escherichia coli [J].
Berardini, M ;
Foster, PL ;
Loechler, EL .
JOURNAL OF BACTERIOLOGY, 1999, 181 (09) :2878-2882
[9]   XPF-ERCC1 Participates in the Fanconi Anemia Pathway of Cross-Link Repair [J].
Bhagwat, Nikhil ;
Olsen, Anna L. ;
Wang, Anderson T. ;
Hanada, Katsuhiro ;
Stuckert, Patricia ;
Kanaar, Roland ;
D'Andrea, Alan ;
Niedernhofer, Laura J. ;
McHugh, Peter J. .
MOLECULAR AND CELLULAR BIOLOGY, 2009, 29 (24) :6427-6437
[10]   Metallo-β-lactamase fold within nucleic acids processing enzymes:: the β-CASP family [J].
Callebaut, I ;
Moshous, D ;
Mornon, JP ;
de Villartay, JP .
NUCLEIC ACIDS RESEARCH, 2002, 30 (16) :3592-3601