A polymerase theta-dependent repair pathway suppresses extensive genomic instability at endogenous G4 DNA sites

Nature Communications

Volumn 5, Issue , 2014, Pages

  Koole, Wouter ^a   Van Schendel, Robin ^a   Karambelas, Andrea E ^b   Van Heteren, Jane T ^a   Okihara, Kristy L ^b   Tijsterman, Marcel ^a  

^a LEIDEN UNIVERSITY MEDICAL CENTER   (Netherlands)

^b UNIVERSITY MEDICAL CENTER UTRECHT   (Netherlands)

Author keywords

[No Author keywords available]

Indexed keywords

DNA DIRECTED DNA POLYMERASE; DNA POLYMERASE THETA; GUANINE QUADRUPLEX;

ANIMAL; CAENORHABDITIS ELEGANS; DNA REPAIR; DOUBLE STRANDED DNA BREAK; METABOLISM; MOLECULAR EVOLUTION; MOLECULAR GENETICS; NUCLEOTIDE SEQUENCE;

ANIMALS; BASE SEQUENCE; CAENORHABDITIS ELEGANS; DNA BREAKS, DOUBLE-STRANDED; DNA REPAIR; DNA-DIRECTED DNA POLYMERASE; EVOLUTION, MOLECULAR; G-QUADRUPLEXES; MOLECULAR SEQUENCE DATA;

EID: 84893870945     PISSN: None     EISSN: 20411723     Source Type: Journal    
DOI: 10.1038/ncomms4216     Document Type: Article

References (44)

1. Gellert, M., Lipsett, M. N. & Davies, R. D. Helix formation by guanylic acid. Proc. Natl Acad. Sci. USA 48, 2013-2018 (1962).
2. Law, M. J. et al. ATR-X syndrome protein targets tandem repeats and influences allele-specific expression in a size-dependent manner. Cell 143, 367-378 (2010).
3. Sarkies, P., Reams, C., Simpson, L. J. & Sale, J. E. Epigenetic instability due to defective replication of structured DNA. Mol. Cell 40, 703-713 (2010).
4. Sarkies, P. et al. FANCJ coordinates two pathways that maintain epigenetic stability at G-quadruplex DNA. Nucleic Acids Res. 40, 1485-1498 (2012).
5. Schwab, R. A., Nieminuszczy, J., Shin-ya, K. & Niedzwiedz, W. FANCJ couples replication past natural fork barriers with maintenance of chromatin structure. J. Cell Biol. (201 33-48 (2013).
6. Smith, J. S. et al. Rudimentary G-quadruplex-based telomere capping in Saccharomyces cerevisiae. Nat. Struct. Mol. Biol. 18, 478-485 (2011).
7. Vannier, J.-B., Pavicic-Kaltenbrunner, V., Petalcorin, M. I. R., Ding, H. & Boulton, S. J. RTEL1 dismantles T loops and counteracts telomeric G4-DNA to maintain telomere integrity. Cell 149, 795-806 (2012).
8. Besnard, E. et al. Unraveling cell type-specific and reprogrammable human replication origin signatures associated with G-quadruplex consensus motifs. Nat. Struct. Mol. Biol. 1-10 (2012).
9. Huppert, J. L. & Balasubramanian, S. Prevalence of quadruplexes in the human genome. Nucleic Acids Res. 33, 2908-2916 (2005). (Pubitemid 41511230)
10. Cahoon, L. A. & Seifert, H. S. An alternative DNA structure is necessary for pilin antigenic variation in Neisseria gonorrhoeae. Science 325, 764-767 (2009).
11. Ribeyre, C. et al. The yeast Pif1 helicase prevents genomic instability caused by G-quadruplex-forming CEB1 sequences in vivo. PLoS Genet. 5, e1000475 (2009).
12. Paeschke, K., Capra, J. A. & Zakian, V. A. DNA replication through G-quadruplex motifs is promoted by the Saccharomyces cerevisiae Pif1 DNA helicase. Cell 145, 678-691 (2011).
13. Lopes, J. et al. G-quadruplex-induced instability during leading-strand replication. EMBO J. 1-14 (2011).
14. De, S. & Michor, F. DNA secondary structures and epigenetic determinants of cancer genome evolution. Nat. Struct. Mol. Biol. 18, 950-955 (2011).
15. Youds, J. L. et al. DOG-1 is the Caenorhabditis elegans BRIP1/FANCJ homologue and functions in interstrand cross-link repair. Mol. Cell Biol. 28, 1470-1479 (2008).
16. 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). (Pubitemid 35154451)
17. Kruisselbrink, E. et al. Mutagenic capacity of endogenous G4 DNA underlies genome instability in FANCJ-defective C. elegans. Curr. Biol. 18, 900-905 (2008).
18. London, T. B. C. et al. FANCJ is a structure-specific DNA helicase associated with the maintenance of genomic G/C tracts. J. Biol. Chem. 283, 36132-36139 (2008).
19. Wu, Y. Y., Shin-ya, K. K. & Brosh, R. M. R. FANCJ helicase defective in Fanconia anemia and breast cancer unwinds G-quadruplex DNA to defend genomic stability. Mol. Cell Biol. 28, 4116-4128 (2008).
20. Plasterk, R. H. & Groenen, J. T. Targeted alterations of the Caenorhabditis elegans genome by transgene instructed DNA double strand break repair following Tc1 excision. EMBO J. 11, 287-290 (1992).
21. Brenner, S. The genetics of Caenorhabditis elegans. Genetics 77, 71-94 (1974).
22. 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). (Pubitemid 43945890)
23. Harris, P. V. et al. Molecular cloning of Drosophila mus308, a gene involved in DNA cross-link repair with homology to prokaryotic DNA polymerase I genes. Mol. Cell Biol. 16, 5764-5771 (1996). (Pubitemid 26315097)
24. Shima, N., Munroe, R. J. & Schimenti, J. C. The mouse genomic instability mutation chaos1 is an allele of Polq that exhibits genetic interaction with Atm. Mol. Cell Biol. 24, 10381-10389 (2004). (Pubitemid 39507874)
25. Muzzini, D. M., Plevani, P., Boulton, S. J., Cassata, G. & Marini, F. Caenorhabditis elegans POLQ-1 and HEL-308 function in two distinct DNA interstrand cross-link repair pathways. DNA Repair (Amst). 7, 941-950 (2008).
26. Seki, M. et al. High-efficiency bypass of DNA damage by human DNA polymerase Q. EMBO J. 23, 4484-4494 (2004). (Pubitemid 39601973)
27. Hogg, M., Sauer-Eriksson, A. E. & Johansson, E. Promiscuous DNA synthesis by human DNA polymerase y. Nucleic Acids Res. 40, 2611-2622 (2012).
28. 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).
29. Thompson, O. et al. The million mutation project: a new approach to genetics in Caenorhabditis elegans. Genome Res. 23, 1749-1762 (2013).
30. Cahoon, L. A. L. & Seifert, H. S. H. Transcription of a cis-acting, noncoding, small RNA is required for pilin antigenic variation in Neisseria gonorrhoeae. PLoS Pathog. 9, e1003074-e1003074 (2012).
31. Wang, X. et al. Identification of genes expressed in the hermaphrodite germ line of C. elegans using SAGE. BMC Genomics 10, 213 (2009).
32. Smith, D. J. & Whitehouse, I. Intrinsic coupling of lagging-strand synthesis to chromatin assembly. Nature 1-6 (2012).
33. Seki, M., Marini, F. & Wood, R. D. POLQ (Pol y), a DNA polymerase and DNA-dependent ATPase in human cells. Nucleic Acids Res. 31, 6117-6126 (2003). (Pubitemid 37442339)
34. Holway, A. H., Kim, S.-H., La Volpe, A. & Michael, W. M. Checkpoint silencing during the DNA damage response in Caenorhabditis elegans embryos. J. Cell Biol. 172, 999-1008 (2006).
35. Higgins, G. S. et al. Overexpression of POLQ confers a poor prognosis in early breast cancer patients. Oncotarget 1, 175-184 (2010).
36. Lemée, F. et al. DNA polymerase theta up-regulation is associated with poor survival in breast cancer, perturbs DNA replication, and promotes genetic instability. Proc. Natl Acad. Sci. USA 107, 13390-13395 (2010).
37. Higgins, G. S. et al. A small interfering RNA screen of genes involved in DNA repair identifies tumor-specific radiosensitization by POLQ knockdown. Cancer Res. 70, 2984-2993 (2010).
38. Mori, I., Moerman, D. G. & Waterston, R. H. Analysis of a mutator activity necessary for germline transposition and excision of Tc1 transposable elements in Caenorhabditis elegans. Genetics 120, 397-407 (1988).
39. Pontier, D. B., Kruisselbrink, E., Guryev, V. & Tijsterman, M. Isolation of deletion alleles by G4 DNA-induced mutagenesis. Nat. Methods 6, 655-657 (2009).
40. Gengyo-Ando, K. & Mitani, S. Characterization of mutations induced by ethyl methanesulfonate, UV, and trimethylpsoralen in the nematode Caenorhabditis elegans. Biochem. Biophys. Res. Commun. 269, 64-69 (2000). (Pubitemid 30440255)
41. Tijsterman, M., Pothof, J. & Plasterk, R. H. A. Frequent germline mutations and somatic repeat instability in DNA mismatch-repair-deficient Caenorhabditis elegans. Genetics 161, 651-660 (2002). (Pubitemid 34705406)
42. Frøkjær-Jensen, C. et al. Single-copy insertion of transgenes in Caenorhabditis elegans. Nat. Genet. 40, 1375-1383 (2008).
43. Roerink, S. F., Koole, W., Stapel, L. C., Romeijn, R. J. & Tijsterman, M. A broad requirement for TLS polymerases Z and k, and interacting sumoylation and nuclear pore proteins, in lesion bypass during C. elegans embryogenesis. PLoS Genet. 8, e1002800 (2012).
44. Ye, K., Schulz, M. H., Long, Q., Apweiler, R. & Ning, Z. Pindel: a pattern growth approach to detect break points of large deletions and medium sized insertions from paired-end short reads. Bioinformatics 25, 2865-2871 (2009).