Mutagenic Capacity of Endogenous G4 DNA Underlies Genome Instability in FANCJ-Defective C. elegans
Open accessAbstract
To safeguard genetic integrity, cells have evolved an accurate but not failsafe mechanism of DNA replication. Not all DNA sequences tolerate DNA replication equally well [1]. Also, genomic regions that impose structural barriers to the DNA replication fork are a potential source of genetic instability [2, 3]. Here, we demonstrate that G4 DNA-a sequence motif that folds into quadruplex structures in vitro [4, 5]-is highly mutagenic in vivo and is removed from genomes that lack dog-1, the C. elegans ortholog of mammalian FANCJ [6, 7], which is mutated in Fanconi anemia patients [8-11]. We show that sequences that match the G4 DNA signature G3-5N1-3G3-5N1-3G3-5N1-3G3-5 are deleted in germ and somatic tissues of dog-1 animals. Unbiased aCGH analyses of dog-1 genomes that were allowed to accumulate mutations in >100 replication cycles indicate that deletions are found exclusively at G4 DNA; deletion frequencies can reach 4% per site per animal generation. We found that deletion sizes fall short of Okazaki fragment lengths [12], and no significant microhomology was observed at deletion junctions. The existence of 376,000 potentially mutagenic G4 DNA sites in the human genome could have major implications for the etiology of hereditary FancJ and nonhereditary cancers.
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FANCJ, like the Caenorhabditis elegans dog-1 ortholog, resolves DNA structures that interfere with replication, such as guanine quadruplex (G4-DNA) structures.
“In particular, FANCJ, similar to the Caenorhabditis elegans dog-1 ortholog, functions to resolve DNA structures that interfere with DNA replication, such as guanine quadriduplex (G4-DNA) structures [78].”
From Hereditary Breast Cancer and the BRCA1-Associated FANCJ/BACH1/BRIP1 (2011) · cites this paper as [78]
Cites
THE GENETICS OF CAENORHABDITIS ELEGANS
Brenner, S. (1974) · Genetics · doi:10.1093/genetics/77.1.71 · Cited by 14,984 · see citing works
Quadruplex DNA: sequence, topology and structure
Burge, S., Parkinson, G. N., Hazel, P., Todd, A. K., & Neidle, S. (2006) · Nucleic Acids Research · doi:10.1093/nar/gkl655 · Cited by 2,404 · see citing works
Sen, D., & Gilbert, W. (1988) · Nature · doi:10.1038/334364a0 · Cited by 1,668 · see citing works
Prevalence of quadruplexes in the human genome
Huppert, J., & Balasubramanian, S. (2005) · Nucleic Acids Research · doi:10.1093/nar/gki609 · Cited by 1,655 · see citing works
Helix formation by guanylic acid.
Gellert, M., Lipsett, M., & Davies, D. R. (1962) · Proceedings of the National Academy of Sciences of the United States of America · doi:10.1073/pnas.48.12.2013 · Cited by 1,430 · see citing works
DNA MISMATCH REPAIR AND GENETIC INSTABILITY
Harfe, B. D., & Jinks-Robertson, S. (2000) · Annual Review of Genetics · doi:10.1146/annurev.genet.34.1.359 · Cited by 605 · see citing works
The Bloom’s Syndrome Helicase Unwinds G4 DNA*
Sun, H., Karow, J. K., Hickson, I., & Maizels, N. (1998) · Journal of Biological Chemistry · doi:10.1074/jbc.273.42.27587 · Cited by 552 · see citing works
The DNA helicase BRIP1 is defective in Fanconi anemia complementation group J
Levitus, M., Waisfisz, Q., Godthelp, B. C., Vries, Y. D., Hussain, S., Wiegant, W. W., Elghalbzouri-Maghrani, E., Steltenpool, J., Rooimans, M. A., Pals, G., et al. (2005) · Nature Genetics · doi:10.1038/ng1625 · Cited by 432 · see citing works
Dynamic roles for G4 DNA in the biology of eukaryotic cells
Maizels, N. (2006) · Nature Structural & Molecular Biology · doi:10.1038/nsmb1171 · Cited by 418 · see citing works
Litman, R., Peng, M., Jin, Z., Zhang, F., Zhang, J., Powell, S., Andreassen, P. R., & Cantor, S. B. (2005) · Cancer Cell · doi:10.1016/j.ccr.2005.08.004 · Cited by 396 · see citing works
Microsatellite Instability in Yeast: Dependence on Repeat Unit Size and DNA Mismatch Repair Genes
Sia, E. A., Kokoska, R. J., Dominska, M., Greenwell, P. W., & Petes, T. D. (1997) · Molecular and Cellular Biology · doi:10.1128/mcb.17.5.2851 · Cited by 392 · see citing works
Fry, M., & Loeb, L. A. (1999) · Journal of Biological Chemistry · doi:10.1074/jbc.274.18.12797 · Cited by 371 · see citing works
The BRCA1-interacting helicase BRIP1 is deficient in Fanconi anemia
Levran, O., Attwooll, C., Henry, R. T., Milton, K. L., Neveling, K., Rio, P., Batish, S. D., Kalb, R., Velleuer, E., Barral, S., et al. (2005) · Nature Genetics · doi:10.1038/ng1624 · Cited by 370 · see citing works
Fanconi Anemia (Cross)linked to DNA Repair
Niedernhofer, L. J., Lalai, A. S., & Hoeijmakers, J. H. J. (2005) · Cell · doi:10.1016/j.cell.2005.12.009 · Cited by 290 · see citing works
The arrest of replication forks in the rDNA of yeast occurs independently of transcription
Brewer, B. J., Lockshon, D., & Fangman, W. L. (1992) · Cell · doi:10.1016/0092-8674(92)90355-g · Cited by 274 · see citing works
Disruption of dog-1 in Caenorhabditis elegans triggers deletions upstream of guanine-rich DNA
Cheung, I. K., Schertzer, M. J., Rose, A. M., & Lansdorp, P. M. (2002) · Nature Genetics · doi:10.1038/ng928 · Cited by 270 · see citing works
Lambert, S., Watson, A. T., Sheedy, D. M., Martin, B. R., & Carr, A. M. (2005) · Cell · doi:10.1016/j.cell.2005.03.022 · Cited by 261 · see citing works
Bridge, W. L., Vandenberg, C. J., Franklin, R., & Hiom, K. J. (2005) · Nature Genetics · doi:10.1038/ng1627 · Cited by 208 · see citing works
Start Sites of Bidirectional DNA Synthesis at the Human Lamin B2 Origin
Abdurashidova, G., Deganuto, M., Klima, R., Riva, S., Biamonti, G., Giacca, M., & Falaschi, A. (2000) · Science · doi:10.1126/science.287.5460.2023 · Cited by 187 · see citing works
The Fanconi Anemia Pathway of Genomic Maintenance
Levitus, M., Joenje, H., & de Winter, J. P. (2006) · Analytical Cellular Pathology · doi:10.1155/2006/974975 · Cited by 106 · see citing works
Youds, J. L., Barber, L. J., Ward, J. D., Collis, S. J., O’Neil, N. J., Boulton, S. J., & Rose, A. M. (2007) · Molecular and Cellular Biology · doi:10.1128/mcb.01641-07 · Cited by 102 · see citing works
Youds, J. L., O'Neil, N. J., & Rose, A. (2006) · Genetics · doi:10.1534/genetics.106.056879 · Cited by 82 · see citing works
The Fanconi anemia/BRCA pathway: A coordinator of cross-link repair
Mirchandani, K. D., & D’Andrea, A. D. (2006) · Experimental Cell Research · doi:10.1016/j.yexcr.2006.06.014 · Cited by 81 · see citing works
Denver, D. R., Feinberg, S., Estes, S., Thomas, W. K., & Lynch, M. (2005) · Genetics · doi:10.1534/genetics.104.038521 · Cited by 56 · see citing works
Tijsterman, M., Pothof, J., & Plasterk, R. H. A. (2002) · Genetics · doi:10.1093/genetics/161.2.651 · Cited by 54 · see citing works
Self-citationGilbert, D. M. (2005) · Molecular Cell · doi:10.1016/j.molcel.2005.11.013 · Cited by 11 · see citing works
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G-quadruplexes and their regulatory roles in biology
Rhodes, D., & Lipps, H. J. (2015) · Nucleic Acids Research · doi:10.1093/nar/gkv862 · Cited by 1,494 · see citing works
DNA secondary structures: stability and function of G-quadruplex structures
Bochman, M. L., Paeschke, K., & Zakian, V. A. (2012) · Nature Reviews Genetics · doi:10.1038/nrg3296 · Cited by 1,449 · see citing works
The regulation and functions of DNA and RNA G-quadruplexes
Varshney, D., Spiegel, J., Zyner, K. G., Tannahill, D., & Balasubramanian, S. (2020) · Nature Reviews Molecular Cell Biology · doi:10.1038/s41580-020-0236-x · Cited by 1,265 · see citing works
G-quadruplex structures: in vivo evidence and function
Lipps, H. J., & Rhodes, D. (2009) · Trends in Cell Biology · doi:10.1016/j.tcb.2009.05.002 · Cited by 829 · see citing works
Maizels, N., & Graybuck, L. T. (2013) · PLoS Genetics · doi:10.1371/journal.pgen.1003468 · Cited by 490 · see citing works
How long is too long? Effects of loop size on G-quadruplex stability
Guédin, A., Gros, J., Alberti, P., & Mergny, J. (2010) · Nucleic Acids Research · doi:10.1093/nar/gkq639 · Cited by 412 · see citing works
Ribeyre, C., Lopes, J., Boulé, J., Piazza, A., Guédin, A., Zakian, V., Mergny, J., & Nicolas, A. (2009) · PLoS Genetics · doi:10.1371/journal.pgen.1000475 · Cited by 367 · see citing works
Existence and consequences of G-quadruplex structures in DNA
Murat, P., & Balasubramanian, S. (2014) · Current Opinion in Genetics & Development · doi:10.1016/j.gde.2013.10.012 · Cited by 346 · see citing works
G‐quadruplex‐induced instability during leading‐strand replication
Lopes, J., Piazza, A., Bermejo, R., Kriegsman, B. A., Colosio, A., Teulade‐Fichou, M., Foiani, M., & Nicolas, A. G. (2011) · The EMBO Journal · doi:10.1038/emboj.2011.316 · Cited by 330 · see citing works
Maizels, N. (2015) · EMBO Reports · doi:10.15252/embr.201540607 · Cited by 306 · see citing works
On the wrong DNA track: Molecular mechanisms of repeat-mediated genome instability
Khristich, A. N., & Mirkin, S. M. (2020) · Journal of Biological Chemistry · doi:10.1074/jbc.rev119.007678 · Cited by 289 · see citing works
Capra, J. A., Paeschke, K., Singh, M., & Zakian, V. A. (2010) · PLoS Computational Biology · doi:10.1371/journal.pcbi.1000861 · Cited by 283 · see citing works
G‐quadruplex nucleic acids and human disease
Wu, Y., & Brosh, R. M. (2010) · FEBS Journal · doi:10.1111/j.1742-4658.2010.07760.x · Cited by 262 · see citing works
FANCJ Is a Structure-specific DNA Helicase Associated with the Maintenance of Genomic G/C Tracts
London, T. B. C., Barber, L. J., Mosedale, G., Kelly, G. P., Balasubramanian, S., Hickson, I. D., Boulton, S. J., & Hiom, K. (2008) · Journal of Biological Chemistry · doi:10.1074/jbc.m808152200 · Cited by 252 · see citing works
DNA secondary structures and epigenetic determinants of cancer genome evolution
De, S., & Franziska Michor, A. (2011) · Nature Structural & Molecular Biology · doi:10.1038/nsmb.2089 · Cited by 248 · see citing works
Biogenesis of cytosolic and nuclear iron–sulfur proteins and their role in genome stability
Paul, V. D., & Lill, R. (2015) · Biochimica et Biophysica Acta (BBA) - Molecular Cell Research · doi:10.1016/j.bbamcr.2014.12.018 · Cited by 247 · see citing works
Koole, W., van Schendel, R., Karambelas, A., van Heteren, J. V., Okihara, K. L., & Tijsterman, M. (2014) · Nature Communications · doi:10.1038/ncomms4216 · Cited by 230 · see citing works
Self-citationG4 motifs affect origin positioning and efficiency in two vertebrate replicators
Valton, A.-L., Hassan‐Zadeh, V., Lema, I., Boggetto, N., Alberti, P., Saintomé, C., Riou, J., & Prioleau, M. (2014) · The EMBO Journal · doi:10.1002/embj.201387506 · Cited by 226 · see citing works
FANCJ coordinates two pathways that maintain epigenetic stability at G-quadruplex DNA
Sarkies, P., Murat, P., Phillips, L. G., Patel, K. J., Balasubramanian, S., & Sale, J. E. (2011) · Nucleic Acids Research · doi:10.1093/nar/gkr868 · Cited by 214 · see citing works
The genetic and molecular basis of Fanconi anemia
de Winter, J. P., & Joenje, H. (2008) · Mutation research. Fundamental and molecular mechanisms of mutagenesis · doi:10.1016/j.mrfmmm.2008.11.004 · Cited by 206 · see citing works
Interplay between Fanconi anemia and homologous recombination pathways in genome integrity
Michl, J., Zimmer, J., & Tarsounas, M. (2016) · The EMBO Journal · doi:10.15252/embj.201693860 · Cited by 204 · see citing works
The expanding biology of the C9orf72 nucleotide repeat expansion in neurodegenerative disease
Haeusler, A. R., Donnelly, C. J., & Rothstein, J. D. (2016) · Nature reviews. Neuroscience · doi:10.1038/nrn.2016.38 · Cited by 205 · see citing works
Meier, B., Cooke, S. L., Weiss, J. G., Bailly, A., Alexandrov, L. B., Marshall, J., Raine, K. M., Maddison, M., Anderson, E. L., Stratton, M. R., et al. (2014) · Genome Research · doi:10.1101/gr.175547.114 · Cited by 182 · see citing works
Piazza, A., Boulé, J., Lopes, J., Mingo, K., Largy, E., Teulade-Fichou, M., & Nicolas, A. (2010) · Nucleic Acids Research · doi:10.1093/nar/gkq136 · Cited by 166 · see citing works
G-quadruplex unwinding helicases and their function <i>in vivo</i>
Sauer, M., & Paeschke, K. (2017) · Biochemical Society Transactions · doi:10.1042/bst20170097 · Cited by 179 · see citing works
What does physics have to do with cancer?
Franziska Michor, A., Liphardt, J., Mauro Ferrari, B., & Widom, J. (2011) · Nature reviews. Cancer · doi:10.1038/nrc3092 · Cited by 177 · see citing works
Replication of G Quadruplex DNA
Lerner, L. K., & Sale, J. E. (2019) · Genes · doi:10.3390/genes10020095 · Cited by 156 · see citing works
Human Pif1 helicase is a G-quadruplex DNA-binding protein with G-quadruplex DNA-unwinding activity
Sanders, C. M. (2010) · Biochemical Journal · doi:10.1042/bj20100612 · Cited by 156 · see citing works
Thompson, L. H., & Hinz, J. M. (2009) · Mutation research. Fundamental and molecular mechanisms of mutagenesis · doi:10.1016/j.mrfmmm.2009.02.003 · Cited by 154 · see citing works
FANCJ promotes DNA synthesis through G‐quadruplex structures
Bosch, P. C., Segura‐Bayona, S., Koole, W., Heteren, J. T. V., Dewar, J. M., Tijsterman, M., & Knipscheer, P. (2014) · The EMBO Journal · doi:10.15252/embj.201488663 · Cited by 154 · see citing works
Self-citationG-Quadruplexes in DNA Replication: A Problem or a Necessity?
Valton, A.-L., & Prioleau, M.-N. (2016) · Trends in Genetics · doi:10.1016/j.tig.2016.09.004 · Cited by 149 · see citing works
Piazza, A., Adrian, M., Samazan, F., Heddi, B., Hamon, F., Serero, A., Lopes, J., Teulade‐Fichou, M., Phan, A. T., & Nicolas, A. G. (2015) · The EMBO Journal · doi:10.15252/embj.201490702 · Cited by 142 · see citing works
DNA helicase and helicase-nuclease enzymes with a conserved iron-sulfur cluster
Wu, Y., & Brosh, R. M. (2012) · Nucleic Acids Research · doi:10.1093/nar/gks039 · Cited by 142 · see citing works
G-quadruplex DNA: a novel target for drug design
Teng, F., Jiang, Z., Guo, M., Tan, X., Chen, F., Xi, X., & Xu, Y. (2021) · Cellular and Molecular Life Sciences · doi:10.1007/s00018-021-03921-8 · Cited by 136 · see citing works
RTEL1: functions of a disease-associated helicase
Vannier, J., Sarek, G., & Boulton, S. J. (2014) · Trends in Cell Biology · doi:10.1016/j.tcb.2014.01.004 · Cited by 134 · see citing works
Lemmens, B., van Schendel, R., & Tijsterman, M. (2015) · Nature Communications · doi:10.1038/ncomms9909 · Cited by 133 · see citing works
Self-citationDeterminants of G quadruplex‐induced epigenetic instability in REV1‐deficient cells
Schiavone, D., Guilbaud, G., Murat, P., Papadopoulou, C., Sarkies, P., Prioleau, M., Balasubramanian, S., & Sale, J. E. (2014) · The EMBO Journal · doi:10.15252/embj.201488398 · Cited by 128 · see citing works
G-Quadruplexes in Pathogens: A Common Route to Virulence Control?
Harris, L. M., & Merrick, C. J. (2015) · PLoS Pathogens · doi:10.1371/journal.ppat.1004562 · Cited by 128 · see citing works
Genomes and G-Quadruplexes: For Better or for Worse
Tarsounas, M., & Tijsterman, M. (2013) · Journal of Molecular Biology · doi:10.1016/j.jmb.2013.09.026 · Cited by 124 · see citing works
Self-citationHereditary Breast Cancer and the BRCA1-Associated FANCJ/BACH1/BRIP1
Cantor, S. B., & Guillemette, S. (2011) · Future Oncology · doi:10.2217/fon.10.191 · Cited by 106 · see citing works
“In particular, FANCJ, similar to the Caenorhabditis elegans dog-1 ortholog, functions to resolve DNA structures that interfere with DNA replication, such as guanine quadriduplex (G4-DNA) structures [78].”
Forward and reverse mutagenesis in C. elegans
Kutscher, L. M. (2014) · WormBook · doi:10.1895/wormbook.1.167.1 · Cited by 107 · see citing works
G-quadruplex recognition and remodeling by the FANCJ helicase
Wu, C. G., & Spies, M. (2016) · Nucleic Acids Research · doi:10.1093/nar/gkw574 · Cited by 105 · see citing works
FANCJ couples replication past natural fork barriers with maintenance of chromatin structure
Schwab, R. A., Nieminuszczy, J., Shin‐ya, K., & Niedźwiedź, W. (2013) · The Journal of Cell Biology · doi:10.1083/jcb.201208009 · Cited by 103 · see citing works
Welcome the Family of FANCJ-like Helicases to the Block of Genome Stability Maintenance Proteins
Wu, Y., Suhasini, A. N., & Brosh, R. M. (2008) · Cellular and Molecular Life Sciences · doi:10.1007/s00018-008-8580-6 · Cited by 101 · see citing works
The evolving world of protein-G-quadruplex recognition: A medicinal chemist’s perspective
Sissi, C., Gatto, B., & Palumbo, M. (2011) · Biochimie · doi:10.1016/j.biochi.2011.04.018 · Cited by 100 · see citing works
Telomeres: Structures in need of unwinding
Paeschke, K., McDonald, K. R., & Zakian, V. A. (2010) · FEBS Letters · doi:10.1016/j.febslet.2010.07.007 · Cited by 98 · see citing works
How to untie G-quadruplex knots and why?
Lejault, P., Mitteaux, J., Sperti, F. R., & Monchaud, D. (2021) · Cell chemical biology · doi:10.1016/j.chembiol.2021.01.015 · Cited by 96 · see citing works
G-quadruplex stabilization via small-molecules as a potential anti-cancer strategy
Awadasseid, A., Ma, X., Wu, Y., & Zhang, W. (2021) · Biomedicine & Pharmacotherapy · doi:10.1016/j.biopha.2021.111550 · Cited by 95 · see citing works
G4-quadruplex-binding proteins: review and insights into selectivity
Meier-Stephenson, V. (2022) · Biophysical Reviews · doi:10.1007/s12551-022-00952-8 · Cited by 85 · see citing works
The role of fork stalling and DNA structures in causing chromosome fragility
Kaushal, S., & Freudenreich, C. H. (2018) · Genes Chromosomes and Cancer · doi:10.1002/gcc.22721 · Cited by 88 · see citing works
Mechanisms of DNA Replication and Repair: Insights from the Study of G-Quadruplexes
Bryan, T. M. (2019) · Molecules · doi:10.3390/molecules24193439 · Cited by 91 · see citing works
G-quadruplex interacting small molecules and drugs: from bench toward bedside
Müller, S., & Rodriguez, R. (2014) · Expert Review of Clinical Pharmacology · doi:10.1586/17512433.2014.945909 · Cited by 84 · see citing works
Multistep mechanism of G-quadruplex resolution during DNA replication
Sato, K., Martin-Pintado, N., Post, H., Altelaar, M., & Knipscheer, P. (2021) · Science Advances · doi:10.1126/sciadv.abf8653 · Cited by 80 · see citing works
Belmonte‐Reche, E., Martínez‐García, M., Guédin, A., Zuffo, M., Arévalo‐Ruiz, M., Doria, F., Campos‐Salinas, J., Maynadier, M., Lopez-Rubio, J.-J., Freccero, M., et al. (2018) · Journal of Medicinal Chemistry · doi:10.1021/acs.jmedchem.7b01672 · Cited by 77 · see citing works
Dolinnaya, N. G., Ogloblina, A. M., & Геннадиевна, Я. М. (2016) · Biochemistry (Moscow) · doi:10.1134/s0006297916130034 · Cited by 73 · see citing works
Timeless couples G‐quadruplex detection with processing by DDX11 helicase during DNA replication
Lerner, L. K., Holzer, S., Kilkenny, M. L., Šviković, S., Murat, P., Schiavone, D., Eldridge, C. B., Bittleston, A., Maman, J. D., Branzei, D., et al. (2020) · The EMBO Journal · doi:10.15252/embj.2019104185 · Cited by 71 · see citing works
DNA repair, recombination, and damage signaling
Gartner, A., & Engebrecht, J. (2021) · Genetics · doi:10.1093/genetics/iyab178 · Cited by 73 · see citing works
Harris, L. M., Monsell, K., Noulin, F., Famodimu, M. T., Smargiasso, N., Damblon, C., Horrocks, P., & Merrick, C. J. (2018) · Antimicrobial Agents and Chemotherapy · doi:10.1128/aac.01828-17 · Cited by 57 · see citing works
Guanine quadruplex structures localize to heterochromatin
Hoffmann, R. F., Moshkin, Y. M., Mouton, S., Grzeschik, N. A., Kalicharan, R. D., Kuipers, J., Wolters, A. H. G., Nishida, K., Romashchenko, A. V., Postberg, J., et al. (2015) · Nucleic Acids Research · doi:10.1093/nar/gkv900 · Cited by 68 · see citing works
GCNA Preserves Genome Integrity and Fertility Across Species
Bhargava, V., Goldstein, C. D., Russell, L., Xu, L., Ahmed, M., Li, W., Casey, A. K., Servage, K. A., Kollipara, R. K., Picciarelli, Z., et al. (2019) · Developmental Cell · doi:10.1016/j.devcel.2019.11.007 · Cited by 67 · see citing works
Wulfridge, P., & Sarma, K. (2024) · Nature Cell Biology · doi:10.1038/s41556-024-01437-4 · Cited by 64 · see citing works
Boyer, A.-S., Grgurević, S., Cazaux, C., & Hoffmann, J. (2013) · Journal of Molecular Biology · doi:10.1016/j.jmb.2013.09.022 · Cited by 65 · see citing works
Gong, J.-Y., Wen, C.-J., Tang, M.-L., Duan, R.-F., Chen, J.-N., Zhang, J.-Y., Zheng, K.-W., He, Y.-D., Hao, Y.-H., Yu, Q., et al. (2021) · Proceedings of the National Academy of Sciences of the United States of America · doi:10.1073/pnas.2013230118 · Cited by 53 · see citing works
G-quadruplex resolution: From molecular mechanisms to physiological relevance
Sato, K., & Knipscheer, P. (2023) · DNA repair · doi:10.1016/j.dnarep.2023.103552 · Cited by 64 · see citing works
Sengar, A., Heddi, B., & Phan, A. T. (2014) · Biochemistry · doi:10.1021/bi500990v · Cited by 61 · see citing works
From genes to function: the C. elegans genetic toolbox
Boulin, T., & Hobert, O. (2011) · Wiley Interdisciplinary Reviews Developmental Biology · doi:10.1002/wdev.1 · Cited by 58 · see citing works
Metabolism of DNA secondary structures at the eukaryotic replication fork
León-Ortiz, A. M., Svendsen, J. M., & Boulton, S. J. (2014) · DNA repair · doi:10.1016/j.dnarep.2014.03.016 · Cited by 56 · see citing works
Tandem Repeats and G-Rich Sequences Are Enriched at Human CNV Breakpoints
Bose, P., Hermetz, K. E., Conneely, K. N., & Rudd, M. K. (2014) · PLoS ONE · doi:10.1371/journal.pone.0101607 · Cited by 56 · see citing works
A Distinct Triplex DNA Unwinding Activity of ChlR1 Helicase
Guo, M., Hundseth, K., Ding, H., Vidhyasagar, V., Inoue, A., Nguyen, C.-H., Zain, R., Lee, J. S., & Wu, Y. (2015) · Journal of Biological Chemistry · doi:10.1074/jbc.m114.634923 · Cited by 53 · see citing works
Savva, L., & Georgiades, S. N. (2021) · Molecules · doi:10.3390/molecules26040841 · Cited by 56 · see citing works
Regulation of DNA Replication through Natural Impediments in the Eukaryotic Genome
Gadaleta, M. C., & Noguchi, E. (2017) · Genes · doi:10.3390/genes8030098 · Cited by 55 · see citing works
Kim, N., & Jinks-Robertson, S. (2011) · DNA Repair · doi:10.1016/j.dnarep.2011.07.002 · Cited by 51 · see citing works
Carlton, P. M., Davis, R. E., & Ahmed, S. C. (2022) · Genetics · doi:10.1093/genetics/iyac014 · Cited by 46 · see citing works
Zuo1 supports G4 structure formation and directs repair toward nucleotide excision repair
Magis, A. D., Götz, S., Hajikazemi, M., Fekete-Szücs, E., Caterino, M., Juranek, S., & Paeschke, K. (2020) · Nature Communications · doi:10.1038/s41467-020-17701-8 · Cited by 53 · see citing works
Sfeir, A., Tijsterman, M., & McVey, M. (2024) · Annual Review of Cell and Developmental Biology · doi:10.1146/annurev-cellbio-111822-014426 · Cited by 53 · see citing works
Self-citationReplication stalling and DNA microsatellite instability
Gadgil, R. Y., Barthelemy, J., Lewis, T., & Leffak, M. (2016) · Biophysical Chemistry · doi:10.1016/j.bpc.2016.11.007 · Cited by 50 · see citing works
G-quadruplexes Significantly Stimulate Pif1 Helicase-catalyzed Duplex DNA Unwinding
Duan, X., Liu, N.-N., Yang, Y., Li, H.-H., Li, M., Dou, S., & Xi, X. (2015) · Journal of Biological Chemistry · doi:10.1074/jbc.m114.628008 · Cited by 49 · see citing works
FANCM–FAAP24 and FANCJ: FA proteins that metabolize DNA
Ali, A. M., Singh, T. R., & Meetei, A. R. (2009) · Mutation research. Fundamental and molecular mechanisms of mutagenesis · doi:10.1016/j.mrfmmm.2009.04.002 · Cited by 48 · see citing works
i-Motif formation and spontaneous deletions in human cells
Martella, M., Pichiorri, F., Chikhale, R., Abdelhamid, M. A. S., Waller, Z. A. E., & Smith, S. S. (2022) · Nucleic Acids Research · doi:10.1093/nar/gkac158 · Cited by 33 · see citing works
Non-B DNA structures as a booster of genome instability
Duardo, R. C., Guerra, F., Pepe, S., & Capranico, G. (2023) · Biochimie · doi:10.1016/j.biochi.2023.07.002 · Cited by 48 · see citing works
Contributions of the specialised DNA polymerases to replication of structured DNA
Wickramasinghe, C. M., Arzouk, H., Frey, A., Maiter, A., & Sale, J. E. (2015) · DNA repair · doi:10.1016/j.dnarep.2015.01.004 · Cited by 45 · see citing works
Claessens, A., Harris, L. M., Stanojčić, S., Chappell, L., Stanton, A., Kuk, N., Veneziano-Broccia, P., Sterkers, Y., Rayner, J., & Merrick, C. J. (2018) · PLoS Genetics · doi:10.1371/journal.pgen.1007490 · Cited by 39 · see citing works
Stanton, A., Harris, L. M., Graham, G., & Merrick, C. J. (2016) · BMC Genomics · doi:10.1186/s12864-016-3183-3 · Cited by 38 · see citing works
Ligands stimulating antitumour immunity as the next G-quadruplex challenge
Miglietta, G., Marinello, J., Russo, M., & Capranico, G. (2022) · Molecular Cancer · doi:10.1186/s12943-022-01649-y · Cited by 44 · see citing works
“elegans as a DOG1 (FANCJ) gene deletion could lead to accumulation of small deletions upstream to putative G4s [73].”
BackgroundAnti‐tumoural activity of the G‐quadruplex ligand pyridostatin against BRCA1/2‐deficient tumours
Groelly, F. J., Porru, M., Zimmer, J., Benainous, H., Visser, Y. D., Kosova, A. A., Vito, S. D., Serra, V., Ryan, A. J., Leonetti, C., et al. (2022) · EMBO Molecular Medicine · doi:10.15252/emmm.202114501 · Cited by 41 · see citing works
Helicases FANCJ, RTEL1 and BLM Act on Guanine Quadruplex DNA in Vivo
Lansdorp, P. M., & van Wietmarschen, N. (2019) · Genes · doi:10.3390/genes10110870 · Cited by 42 · see citing works
The influencing factors and functions of DNA G‐quadruplexes
Yuan, W.-F., Wan, L.-Y., Peng, H., Zhong, Y., Cai, W.-L., Zhang, Y.-Q., Ai, W.-B., & Wu, J.-F. (2020) · Cell Biochemistry and Function · doi:10.1002/cbf.3505 · Cited by 32 · see citing works
Alternative DNA Structures In Vivo: Molecular Evidence and Remaining Questions
Poggi, L., & Richard, G.-F. (2020) · Microbiology and Molecular Biology Reviews · doi:10.1128/mmbr.00110-20 · Cited by 43 · see citing works
Non-B DNA Secondary Structures and Their Resolution by RecQ Helicases
Sharma, S. (2011) · Journal of Nucleic Acids · doi:10.4061/2011/724215 · Cited by 41 · see citing works
FANCJ: Solving problems in DNA replication
Hiom, K. J. (2010) · DNA repair · doi:10.1016/j.dnarep.2010.01.005 · Cited by 40 · see citing works
From R-Loops to G-Quadruplexes: Emerging New Threats for the Replication Fork
Maffia, A., Ranise, C., & Sabbioneda, S. (2020) · International Journal of Molecular Sciences · doi:10.3390/ijms21041506 · Cited by 40 · see citing works
Sun, X., Brieño‐Enríquez, M. A., Cornelius, A. J., Modzelewski, A. J., Maley, T. T., Campbell-Peterson, K. M., Holloway, J. K., & Cohen, P. E. (2015) · Chromosoma · doi:10.1007/s00412-015-0549-2 · Cited by 38 · see citing works
The repair of G-quadruplex-induced DNA damage
van Kregten, M., & Tijsterman, M. (2014) · Experimental Cell Research · doi:10.1016/j.yexcr.2014.08.038 · Cited by 38 · see citing works
Self-citationC. elegans: A model of Fanconi anemia and ICL repair
Youds, J. L., Barber, L. J., & Boulton, S. J. (2008) · Mutation research. Fundamental and molecular mechanisms of mutagenesis · doi:10.1016/j.mrfmmm.2008.11.007 · Cited by 37 · see citing works
FANCJ is essential to maintain microsatellite structure genome-wide during replication stress
Barthelemy, J., Hanenberg, H., & Leffak, M. (2016) · Nucleic Acids Research · doi:10.1093/nar/gkw433 · Cited by 37 · see citing works
Creation and resolution of non-B-DNA structural impediments during replication
Mellor, C., Perez, C., & Sale, J. E. (2022) · Critical Reviews in Biochemistry and Molecular Biology · doi:10.1080/10409238.2022.2121803 · Cited by 37 · see citing works
The tailless ortholog nhr-67 functions in the development of the C. elegans ventral uterus
Verghese, E., Schocken, J., Jacob, S., Wimer, A. M., Royce, R., Nesmith, J. E., Baer, G. M., Clever, S., McCain, E. R., Lakowski, B., et al. (2011) · Developmental Biology · doi:10.1016/j.ydbio.2011.06.007 · Cited by 36 · see citing works
Wu, Y., & Brosh, R. M. (2009) · Current Molecular Medicine · doi:10.2174/156652409788167159 · Cited by 35 · see citing works
Helicase Q promotes homology-driven DNA double-strand break repair and prevents tandem duplications
Kamp, J. A., Lemmens, B., Romeijn, R., Changoer, S. C., van Schendel, R., & Tijsterman, M. (2021) · Nature Communications · doi:10.1038/s41467-021-27408-z · Cited by 35 · see citing works
Self-citationMaizels, N. (2012) · Annals of the New York Academy of Sciences · doi:10.1111/j.1749-6632.2012.06586.x · Cited by 34 · see citing works
- Authors
- Kruisselbrink, E., Guryev, V., Brouwer, K., Pontier, D. B., Cuppen, E., & Tijsterman, M.
- Affiliations
- Royal Netherlands Academy of Arts and Sciences (NL)
- Corresponding author
- Tijsterman, Marcel
- Venue
- Current Biology
- Publisher
- Elsevier BV
- Published
- 2008-06
- Volume
- 18
- Issue
- 12
- Pages
- 900-905
- ISSN
- 0960-9822 (ISSN-L)
- OpenAlex
- W2100493498
- Cited by
- 209
- References
- 26
- Citations by year
- 2026: 6 · 2025: 6 · 2024: 14 · 2023: 7 · 2022: 14 · 2021: 18 · 2020: 14 · 2019: 9 · 2018: 10 · 2017: 10 · 2016: 15 · 2015: 15 · 2014: 17 · 2013: 6 · 2012: 6
- FWCI
- 5.75
- Type
- journal article
- Language
- en
- Open access
- bronze
- doi.org
- Licence
- www.elsevier.com/tdm/userlicense/1.0/ (tdm)
- www.elsevier.com/legal/tdmrep-license (tdm)
- www.elsevier.com/open-access/userlicense/1.0/ (vor, 1872 d)
- doi.org/10.15223/policy-017 (stm-asf)
- doi.org/10.15223/policy-037 (stm-asf)
- doi.org/10.15223/policy-012 (stm-asf)
- doi.org/10.15223/policy-029 (stm-asf)
- doi.org/10.15223/policy-004 (stm-asf)
- Locations
- Current Biology (publishedVersion)
- PubMed (publishedVersion)
- University of Groningen research database (University of Groningen / Centre for Information Technology) (publishedVersion)
- Data Archiving and Networked Services (DANS) (submittedVersion)
- KNAW Research Portal (The Royal Netherlands Academy of Arts and Sciences) (submittedVersion)
- University of Groningen research database (University of Groningen / Centre for Information Technology) (submittedVersion)
- Funders
- ZonMw
- Topics
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › DNA and Nucleic Acid Chemistry
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › DNA Repair Mechanisms
- Health Sciences › Medicine › Pathology and Forensic Medicine › Genetic factors in colorectal cancer
- Keywords
- G4 DNA, DNA quadruplex, mutagenesis, genomic instability, FANCJ, TMEM16A, Fanconi anemia, DNA replication, deletion hotspots, Okazaki fragments, microhomology, Caenorhabditis elegans, hereditary cancer, array comparative genomic hybridization
- MeSH terms
- Animals, Base Sequence, DNA Replication, DNA Helicases, Mutation, Nucleic Acid Hybridization, Caenorhabditis elegans, Sequence Deletion, Sequence Analysis, DNA, Oligonucleotide Array Sequence Analysis, Caenorhabditis elegans Proteins, Genomic Instability, Basic-Leucine Zipper Transcription Factors, Fanconi Anemia Complementation Group Proteins, G-Quadruplexes
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