Mutagenic consequences of a single G-quadruplex demonstrate mitotic inheritance of DNA replication fork barriers

Nature Communications

Volumn 6, Issue , 2015, Pages

  Lemmens, Bennie ^a   Van Schendel, Robin ^a   Tijsterman, Marcel ^a  

^a LEIDEN UNIVERSITY MEDICAL CENTER   (Netherlands)

Author keywords

[No Author keywords available]

Indexed keywords

DOUBLE STRANDED DNA; GUANINE QUADRUPLEX; SINGLE STRANDED DNA;

CELLS AND CELL COMPONENTS; CHROMOSOME; DNA; ENZYME ACTIVITY; GENOMICS; HERITABILITY; HETEROGENEITY; LESION; MUTATION;

ANIMAL CELL; ARTICLE; CELL DIVISION; CELL PROLIFERATION; DNA CONFORMATION; DNA END JOINING REPAIR; DNA REPLICATION; DNA STRUCTURE; DOUBLE STRANDED DNA BREAK; GENE REARRANGEMENT; GENETIC HETEROGENEITY; MITOSIS; MUTAGENICITY; NONHUMAN; ORGANOGENESIS; ANIMAL; CAENORHABDITIS ELEGANS; CYTOLOGY; GENETICS; MUTAGENESIS;

ANIMALS; CAENORHABDITIS ELEGANS; CELL PROLIFERATION; DNA BREAKS, DOUBLE-STRANDED; DNA REPLICATION; G-QUADRUPLEXES; MITOSIS; MUTAGENESIS;

EID: 84946944202     PISSN: None     EISSN: 20411723     Source Type: Journal    
DOI: 10.1038/ncomms9909     Document Type: Article

References (29)

1. Roerink, S. F., van Schendel, R. & Tijsterman, M. Polymerase theta-mediated end joining of replication-associated DNA breaks in C. elegans. Genome Res. 24, 954-962 (2014).
2. Cheung, I., Schertzer, M., Rose, A. & Lansdorp, P. M. Disruption of dog-1 in Caenorhabditis elegans triggers deletions upstream of guanine-rich DNA. Nat. Genet. 31, 405-409 (2002).
3. Koole, W. et al. A polymerase theta-dependent repair pathway suppresses extensive genomic instability at endogenous G4 DNA sites. Nat. Commun. 5, 3216 (2014).
4. Kruisselbrink, E. et al. Mutagenic capacity of endogenous G4 DNA underlies genome instability in FANCJ-defective C. elegans. Curr. Biol. 18, 900-905 (2008).
5. Pontier, D. B. & Tijsterman, M. A robust network of double-strand break repair pathways governs genome integrity during C. elegans development. Curr. Biol. 19, 1384-1388 (2009).
6. van Kregten, M. & Tijsterman, M. The repair of G-quadruplex-induced DNA damage. Exp. Cell Res. 329, 178-183 (2014).
7. Agostinho, A. et al. Combinatorial regulation of meiotic holliday junction resolution in C. elegans by HIM-6 (BLM) helicase, SLX-4, and the SLX-1, MUS-81 and XPF-1 nucleases. PLoS Genet. 9, e1003591 (2013).
8. O'Neil, N. J. et al. Joint molecule resolution requires the redundant activities of MUS-81 and XPF-1 during Caenorhabditis elegans meiosis. PLoS Genet. 9, e1003582 (2013).
9. Saito, T. T., Lui, D. Y., Kim, H. M., Meyer, K. & Colaiacovo, M. P. Interplay between structure-specific endonucleases for crossover control during Caenorhabditis elegans meiosis. PLoS Genet. 9, e1003586 (2013).
10. Minocherhomji, S. & Hickson, I. D. Structure-specific endonucleases: guardians of fragile site stability. Trends Cell Biol. 24, 321-327 (2014).
11. Saito, T. T., Youds, J. L., Boulton, S. J. & Colaiacovo, M. P. Caenorhabditis elegans HIM-18/SLX-4 interacts with SLX-1 and XPF-1 and maintains genomic integrity in the germline by processing recombination intermediates. PLoS Genet. 5, e1000735 (2009).
12. Youds, J. L., O'Neil, N. J. & Rose, A. M. Homologous recombination is required for genome stability in the absence of DOG-1 in Caenorhabditis elegans. Genetics 173, 697-708 (2006).
13. Castillo Bosch, P. et al. FANCJ promotes DNA synthesis through G-quadruplex structures. EMBO J. 33, 2521-2533 (2014).
14. Kumari, R., Nambiar, M., Shanbagh, S. & Raghavan, S. C. Detection of g-quadruplex DNA using primer extension as a tool. PLoS ONE 10, e0119722 (2015).
15. Zhang, J. et al. DNA interstrand cross-link repair requires replication-fork convergence. Nat. Struct. Mol. Biol. 22, 242-247 (2015).
16. Raschle, M. et al. Mechanism of replication-coupled DNA interstrand crosslink repair. Cell 134, 969-980 (2008).
17. Nakano, T. et al. Translocation and stability of replicative DNA helicases upon encountering DNA-protein cross-links. J. Biol. Chem. 288, 4649-4658 (2013).
18. Long, D. T., Joukov, V., Budzowska, M. & Walter, J. C. BRCA1 promotes unloading of the CMG helicase from a stalled DNA replication fork. Mol. Cell 56, 174-185 (2014).
19. De, S. & Michor, F. DNA secondary structures and epigenetic determinants of cancer genome evolution. Nat. Struct. Mol. Biol. 18, 950-955 (2011).
20. Kent, T., Chandramouly, G., McDevitt, S. M., Ozdemir, A. Y. & Pomerantz, R. T. Mechanism of microhomology-mediated end-joining promoted by human DNA polymerase theta. Nat. Struct. Mol. Biol. 22, 230-237 (2015).
21. Yousefzadeh, M. J. et al. Mechanism of suppression of chromosomal instability by DNA polymerase POLQ. PLoS Genet. 10, e1004654 (2014).
22. Zahn, K. E., Averill, A. M., Aller, P., Wood, R. D. & Doublie, S. Human DNA polymerase theta grasps the primer terminus to mediate DNA repair. Nat. Struct. Mol. Biol. 22, 304-311 (2015).
23. Chan, S. H., Yu, A. M. & McVey, M. Dual roles for DNA polymerase theta in alternative end-joining repair of double-strand breaks in Drosophila. PLoS Genet. 6, e1001005 (2010).
24. Mateos-Gomez, P. A. et al. Mammalian polymerase theta promotes alternative NHEJ and suppresses recombination. Nature 518, 254-257 (2015).
25. Ceccaldi, R. et al. Homologous-recombination-deficient tumours are dependent on Poltheta-mediated repair. Nature 518, 258-262 (2015).
26. Brenner, S. The genetics of Caenorhabditis elegans. Genetics 77, 71-94 (1974).
27. Pontier, D. B., Kruisselbrink, E., Guryev, V. & Tijsterman, M. Isolation of deletion alleles by G4 DNA-induced mutagenesis. Nat. Methods 6, 655-657 (2009).
28. Frokjaer-Jensen, C. et al. Single-copy insertion of transgenes in Caenorhabditis elegans. Nat. Genet. 40, 1375-1383 (2008).
29. Pothof, J. et al. Identification of genes that protect the C. elegans genome against mutations by genome-wide RNAi. Genes Dev. 17, 443-448 (2003).