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Human Fanconi anemia monoubiquitination pathway promotes homologous DNA repair
Open accessAbstract
Fanconi anemia (FA) is a recessive disorder characterized by congenital abnormalities, progressive bone-marrow failure, and cancer susceptibility. Cells from FA patients are hypersensitive to agents that produce DNA crosslinks and, after treatment with these agents, have pronounced chromosome breakage and other cytogenetic abnormalities. Eight FANC genes have been cloned, and the encoded proteins interact in a common cellular pathway. DNA-damaging agents activate the monoubiquitination of FANCD2, resulting in its targeting to nuclear foci that also contain BRCA1 and BRCA2/FANCD1, proteins involved in homology-directed DNA repair. Given the interaction of the FANC proteins with BRCA1 and BRCA2, we tested whether cells from FA patients (groups A, G, and D2) and mouse Fanca –/– cells with a targeted mutation are impaired for this repair pathway. We find that both the upstream (FANCA and FANCG) and downstream (FANCD2) FA pathway components promote homology-directed repair of chromosomal double-strand breaks (DSBs). The FANCD2 monoubiquitination site is critical for normal levels of repair, whereas the ATM phosphorylation site is not. The defect in these cells, however, is mild, differentiating them from BRCA1 and BRCA2 mutant cells. Surprisingly, we provide evidence that these proteins, like BRCA1 but unlike BRCA2, promote a second DSB repair pathway involving homology, i.e., single-strand annealing. These results suggest an early role for the FANC proteins in homologous DSB repair pathway choice.
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“The DR-U2OS cell line containing a single integrated copy of the DR-GFP reporter was used46,47.”
From BRCA1–BARD1 promotes RAD51-mediated homologous DNA pairing (2017) · cites this paper as [46]
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53BP1 Inhibits Homologous Recombination in Brca1-Deficient Cells by Blocking Resection of DNA Breaks
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InfluentialDouble-Strand Break End Resection and Repair Pathway Choice
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Self-citationHomologous-recombination-deficient tumours are dependent on Polθ-mediated repair
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Self-citationControl of BRCA2 Cellular and Clinical Functions by a Nuclear Partner, PALB2
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“…BRCA1, BRCA2, and Fanconi anemia proteins in replication fork protection is notable because loss of canonical Fanconi anemia proteins results in only mild HR defects in mammalian cells (Nakanishi et al. 2005), except for HR repair of cross links coupled to replication (Nakanishi et al. 2011).”
BackgroundSelf-citationIdentification of the FANCI Protein, a Monoubiquitinated FANCD2 Paralog Required for DNA Repair
Smogorzewska, A., Matsuoka, S., Vinciguerra, P., McDonald, E. R., Hurov, K. E., Luo, J., Ballif, B. A., Gygi, S. P., Hofmann, K., D’Andrea, A. D., et al. (2007) · Cell · doi:10.1016/j.cell.2007.03.009 · Cited by 718
“All four siRNAs to FANCI reduced recombination from 78% to 47% of controls, similar to siRNAs to ATR, FANCA, and FANCD2 (Nakanishi et al., 2005) but less than siRNAs to BRCA1 and BRCA2, which are thought to be more directly involved in the recombination process (Figures 3E and 3F).”
BackgroundMethodInfluentialSelf-citationAbraxas and RAP80 Form a BRCA1 Protein Complex Required for the DNA Damage Response
Wang, B., Matsuoka, S., Ballif, B. A., Zhang, D., Smogorzewska, A., Gygi, S. P., & Elledge, S. J. (2007) · Science · doi:10.1126/science.1139476 · Cited by 695
Emergence of a DNA-damage response network consisting of Fanconi anaemia and BRCA proteins
Wang, W. (2007) · Nature Reviews Genetics · doi:10.1038/nrg2159 · Cited by 663
“They then transduce the signals to promote DNA repair through homologous recombination-dependent and translesion synthesis pathway”
BackgroundHow the Fanconi Anemia Pathway Guards the Genome
Moldovan, G., & D’Andrea, A. D. (2009) · Annual Review of Genetics · doi:10.1146/annurev-genet-102108-134222 · Cited by 601
“Indeed, FA proteins are also required for single strand annealing (SSA), a pathway that is upregulated in BRCA2-deficient cells (82, 100, 134).”
BackgroundInfluentialSelf-citationSulkowski, P. L., Corso, C. D., Robinson, N. D., Scanlon, S. E., Purshouse, K. R., Bai, H., Liu, Y., Sundaram, R. K., Hegan, D. C., Fons, N. R., et al. (2017) · Science Translational Medicine · doi:10.1126/scitranslmed.aal2463 · Cited by 575
Regulation of DNA cross-link repair by the Fanconi anemia/BRCA pathwayPreprint
Kim, H., & D’Andrea, A. D. (2012) · Genes & Development · doi:10.1101/gad.195248.112 · Cited by 534
“Deletion of some HR genes renders cells hypersensitive to ICL-inducing agents, and the FA core- or FANCD2/I-deficient patient cells are defective in efficient HR repair (Nakanishi et al. 2005; Zhang et al. 2007; Smogorzewska et al. 2010).”
BackgroundSelf-citationThe Fanconi Anemia/BRCA pathway: new faces in the crowdPreprint
Kennedy, R. D., & D’Andrea, A. D. (2005) · Genes & Development · doi:10.1101/gad.1370505 · Cited by 471
“In general, disruption of upstream FA proteins, such as FANCA (Nakanishi et al. 2005) and FANCG (Yamamoto et al.”
BackgroundSelf-citationmiR-182-Mediated Downregulation of BRCA1 Impacts DNA Repair and Sensitivity to PARP Inhibitors
Moskwa, P., Buffa, F. M., Pan, Y., Panchakshari, R. A., Gottipati, P., Muschel, R. J., Beech, J. S., Kulshrestha, R., Abdelmohsen, K., Weinstock, D. M., et al. (2010) · Molecular Cell · doi:10.1016/j.molcel.2010.12.005 · Cited by 436
“To test whether expression of miR-182 impacts HR repair, we assayed for HR-mediated repair of an I-SceI-induced DSB, in U2OS cells, using a recombination substrate DR-GFP (Nakanishi et al., 2005).”
Wood, R. D., Mitchell, M., & Lindahl, T. L. (2005) · Mutation research. Fundamental and molecular mechanisms of mutagenesis · doi:10.1016/j.mrfmmm.2005.03.007 · Cited by 428
BRCA1–BARD1 promotes RAD51-mediated homologous DNA pairing
Zhao, W., Steinfeld, J. B., Liang, F., Chen, X., Maranon, D. G., Jian Ma, C., Kwon, Y., Rao, T., Wang, W., Sheng, C., et al. (2017) · Nature · doi:10.1038/nature24060 · Cited by 393
Advances in genome editing through control of DNA repair pathways
Yeh, C. D., Richardson, C. D., & Corn, J. E. (2019) · Nature Cell Biology · doi:10.1038/s41556-019-0425-z · Cited by 425
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
“This would suggest that the upstream FA pathway, culminating in FANCD2 monoubiquitination, might have only a modest role in HR (Nakanishi et al., 2005), with a greater role in TLS.”
BackgroundMethodInfluentialMolecular pathogenesis of Fanconi anemia: recent progress
Taniguchi, T., & D’Andrea, A. D. (2006) · Blood · doi:10.1182/blood-2005-10-4240 · Cited by 390
Self-citationGunn, A., & Stark, J. M. (2012) · Methods in molecular biology · doi:10.1007/978-1-61779-998-3_27 · Cited by 363
Collaboration and competition between DNA double‐strand break repair pathways
Kass, E. M., & Jasin, M. (2010) · FEBS Letters · doi:10.1016/j.febslet.2010.07.057 · Cited by 326
“in both HR and SSA in the repair of a DSB [92], as well as increased radial chromosomes, apparently from aberrant NHEJ.”
BackgroundSelf-citationChen, C.-C., Feng, W., Lim, P. X., Kass, E. M., & Jasin, M. (2017) · Annual Review of Cancer Biology · doi:10.1146/annurev-cancerbio-030617-050502 · Cited by 323
“…mutations in the BRCT domain have been identified in patients, compromising multiple aspects of BRCA1 function, including damage foci localization, protein stability, and resection-dependent HDR and SSA (Anantha et al. 2017, Chen et al. 2017, Lee et al. 2010, Li & Yu 2013, Nelson & Holt 2010).”
BackgroundSelf-citationMacKay, C., Déclais, A., Lundin, C., Agostinho, A., Deans, A. J., Macartney, T., Hofmann, K., Gartner, A., West, S. C., Helleday, T., et al. (2010) · Cell · doi:10.1016/j.cell.2010.06.021 · Cited by 319
“Second, depletion of FAN1 from human cells results in reduced efficiency in I-SceI-induced HR (Figure 7A), and similar results were reported in human cells expressing FANCD2 K561R (Nakanishi et al., 2005).”
BackgroundResultInfluentialExpanded roles of the Fanconi anemia pathway in preserving genomic stabilityPreprint
Kee, Y., & D’Andrea, A. D. (2010) · Genes & Development · doi:10.1101/gad.1955310 · Cited by 311
“Using this system, it was shown that patientderived FANCA-, FANCG-, and FANCD2-deficient cells are defective, albeit to a mild degree, in HR repair (Nakanishi et al. 2005).”
BackgroundSelf-citationPALB2 Functionally Connects the Breast Cancer Susceptibility Proteins BRCA1 and BRCA2
Zhang, F., Fan, Q., Ren, K., & Andreassen, P. R. (2009) · Molecular Cancer Research · doi:10.1158/1541-7786.mcr-09-0123 · Cited by 303
“For this purpose, we used U2OS cells with an integrated copy of the pDR reporter (25).”
MethodInfluentialDNA Strand Break Repair and Human Genetic Disease
McKinnon, P. J., & Caldecott, K. W. (2007) · Annual Review of Genomics and Human Genetics · doi:10.1146/annurev.genom.7.080505.115648 · Cited by 321
Motegi, A., Liaw, H.-J., Lee, K.-Y., Roest, H. P., Maas, A., Wu, X., Moinova, H., Markowitz, S. D., Ding, H., Hoeijmakers, J. H. J., et al. (2008) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0805685105 · Cited by 304
“To determine whether SHPRH and HLTF are involved in HR, we used a recombination reporter assay (DR-GFP reporter assay), which can measure the frequency of HR between tandem GFP repeats with inactivating mutations (25).”
MethodPreventing Nonhomologous End Joining Suppresses DNA Repair Defects of Fanconi Anemia
Adamo, A., Collis, S. J., Adelman, C. A., Silva, N., Hořejšı́, Z., Ward, J. D., Martínez-Pérez, E., Boulton, S. J., & Volpe, A. L. (2010) · Molecular Cell · doi:10.1016/j.molcel.2010.06.026 · Cited by 297
DNA Damage Induced by Alkylating Agents and Repair Pathways
Kondo, N., Takahashi, A., Ono, K., & Ohnishi, T. (2010) · Journal of Nucleic Acids · doi:10.4061/2010/543531 · Cited by 323
“Although the FA pathway was initially characterized in terms of DNA cross-link repair, this pathway is also involved in homologous recombination and resolution of the replication arrest [55, 56].”
BackgroundCellular functions of the BRCA tumour-suppressor proteins
Boulton, S. J. (2006) · Biochemical Society Transactions · doi:10.1042/bst0340633 · Cited by 299
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 298
FANCI is a second monoubiquitinated member of the Fanconi anemia pathway
Sims, A. E., Spiteri, E., Sims, R. J., Arita, A., Lach, F. P., Landers, T., Wurm, M., Freund, M., Neveling, K., Hanenberg, H., et al. (2007) · Nature Structural & Molecular Biology · doi:10.1038/nsmb1252 · Cited by 280
BMI1 Is Recruited to DNA Breaks and Contributes to DNA Damage-Induced H2A Ubiquitination and Repair
Ginjala, V., Nacerddine, K., Kulkarni, A., Oza, J., Hill, S. J., Yao, M., Citterio, E., van Lohuizen, M., & Ganesan, S. (2011) · Molecular and Cellular Biology · doi:10.1128/mcb.00981-10 · Cited by 240
“To investigate the role of BMI1 in HR-mediated repair of DNA DSBs, experiments were performed with U20S-DR cells containing a single-copy integrated tandem GFP-based reporter of HR (36).”
MethodInactivation of Murine Usp1 Results in Genomic Instability and a Fanconi Anemia Phenotype
Kim, J. M., Parmar, K., Huang, M., Weinstock, D. M., Ruit, C. A., Kutok, J. L., & D’Andrea, A. D. (2009) · Developmental Cell · doi:10.1016/j.devcel.2009.01.001 · Cited by 246
“HR Assay For HR assay with MEFs, the DR-GFP reporter, hypoxanthine-guanine phosphoribosyl transferase-DR-GFP-hygromycin (Nakanishi et al., 2005), was integrated into the genome of Usp1 MEFs.”
InfluentialSelf-citationCRISPR–Cas9 genome editing in human cells occurs via the Fanconi anemia pathway
Richardson, C. D., Kazane, K. R., Feng, S. J., Zelin, E., Bray, N. L., Schäfer, A. J., Floor, S. N., & Corn, J. E. (2018) · Nature Genetics · doi:10.1038/s41588-018-0174-0 · Cited by 259
Mechanism of RAD51-Dependent DNA Interstrand Cross-Link Repair
Long, D. T., Räschle, M., Joukov, V., & Walter, J. C. (2011) · Science · doi:10.1126/science.1204258 · Cited by 238
Hu, Y., Scully, R., Sobhian, B., Xie, A., Shestakova, E. A., & Livingston, D. M. (2011) · Genes & Development · doi:10.1101/gad.2011011 · Cited by 244
“Moreover, in keeping with the notion that the RAP80-enhanced DSBR effect is executed primarily at the level of HR, RAP80 depletion did not appear to affect the abundance of a nonhomologous end-joining (NHEJ)derived product that was assessed using a PCR-based assay (Supplemental Fig. S5; Nakanishi et al. 2005).”
MethodInhibition of Homologous Recombination by the PCNA-Interacting Protein PARI
Moldovan, G., Dejsuphong, D., Petalcorin, M. I. R., Hofmann, K., Takeda, S., Boulton, S. J., & D’Andrea, A. D. (2011) · Molecular Cell · doi:10.1016/j.molcel.2011.11.010 · Cited by 242
“Direct repeat homologous recombination assays using the DR-GFP reporter (Nakanishi et al., 2005) and chromosomal aberration detection in mitotic spreads (Howlett et al.”
MethodSelf-citation53BP1 fosters fidelity of homology-directed DNA repair
Ochs, F., Somyajit, K., Altmeyer, M., Rask, M., Lukas, J., & Lukas, C. (2016) · Nature Structural & Molecular Biology · doi:10.1038/nsmb.3251 · Cited by 232
Local generation of fumarate promotes DNA repair through inhibition of histone H3 demethylation
Jiang, Y., Qian, X., Shen, J., Wang, Y., Li, X., Liu, R., Xia, Y., Chen, Q., Peng, G., Lin, S.-Y., et al. (2015) · Nature Cell Biology · doi:10.1038/ncb3209 · Cited by 208
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 217
Kais, Z., Rondinelli, B., Holmes, A. L., O’Leary, C., Kozono, D., D’Andrea, A. D., & Ceccaldi, R. (2016) · Cell Reports · doi:10.1016/j.celrep.2016.05.031 · Cited by 208
Self-citationThe vertebrate Hef ortholog is a component of the Fanconi anemia tumor-suppressor pathway
Mosedale, G., Niedźwiedź, W., Alpi, A. F., Perrina, F., Pereira‐Leal, J. B., Johnson, M. A., Langevin, F., Pace, P., & Patel, K. J. (2005) · Nature Structural & Molecular Biology · doi:10.1038/nsmb981 · Cited by 191
“ΔHef cells are proficient in double strand break repair Chicken, rodent and human FA cells have a moderate defect in homologous recombinatio”
BackgroundRoles of ATP binding and ATP hydrolysis in human Rad51 recombinase function
Chi, P., Komen, S. V., Sehorn, M. G., Sigurðsson, S., & Sung, P. (2006) · DNA repair · doi:10.1016/j.dnarep.2005.11.005 · Cited by 197
DNA damage response – A double-edged sword in cancer prevention and cancer therapy
Tian, H., Gao, Z., Li, H., Zhang, B., Wang, G., Zhang, Q., Pei, D., & Zheng, J. (2014) · Cancer Letters · doi:10.1016/j.canlet.2014.12.038 · Cited by 189
BRIT1/MCPH1 links chromatin remodelling to DNA damage response
Peng, G., Yim, E.-K., Dai, H., Jackson, A. P., van der Burgt, I., Pan, M., Hu, R., Li, K., & Lin, S. (2009) · Nature Cell Biology · doi:10.1038/ncb1895 · Cited by 191
Quentin, S., Cuccuini, W., Ceccaldi, R., Nibourel, O., Pondarré, C., Pagès, M., Vasquez, N., d’Enghien, C. D., Larghero, J., de Latour, R. P., et al. (2011) · Blood · doi:10.1182/blood-2010-09-308726 · Cited by 188
“Indeed NHEJ is largely efficient in FA cells in contrast with homologous repair (HR) which is impaired.(4,33,34) Moreover, few somatic copy-neutral loss of heterozygosity (UPD) regions were observed (Figure 1 and Supplemental Table S1), suggesting that HR is a rare mechanism of genetic progression in FA, in contrast t…”
BackgroundPromotion of BRCA2-Dependent Homologous Recombination by DSS1 via RPA Targeting and DNA Mimicry
Zhao, W., Vaithiyalingam, S., San Filippo, J., Maranon, D. G., Jimenez-Sainz, J., Fontenay, G. V., Kwon, Y., Leung, S. G., Lu, L., Jensen, R. B., et al. (2015) · Molecular Cell · doi:10.1016/j.molcel.2015.05.032 · Cited by 177
“DSS1-RPA Interaction Is Required for HR Efficiency In Vivo We utilized U2OS cells harboring the DR-GFP HR reporter (Nakanishi et al., 2005; Xia et al., 2006) to query whether the interaction of DSS1 and RPA is critical for HR efficiency (Figure 6A).”
MethodBartz, S. R., Zhang, Z., Burchard, J., Imakura, M., Martin, M. M., Palmieri, A., Needham, R. H. V., Guo, J., Gordon, M. L., Chung, N., et al. (2006) · Molecular and Cellular Biology · doi:10.1128/mcb.01229-06 · Cited by 178
“Finally, it has been reported that FANC mutant cells have mild defects in homology-directed DNA repair compared to severe defects observed in BRCA1 or BRCA2 mutant cells (47).”
BackgroundYan, J., Kim, Y. S., Yang, X.-P., Li, L., Liao, G., Xia, F., & Jetten, A. M. (2007) · Cancer Research · doi:10.1158/0008-5472.can-07-0924 · Cited by 177
“pDR-GFP (23) were used to test the role of RAP80 in HDR.”
MethodTargeting the DNA repair defect of BRCA tumours
Turner, N. C., Tutt, A. N. J., & Ashworth, A. (2005) · Current Opinion in Pharmacology · doi:10.1016/j.coph.2005.03.006 · Cited by 164
Weinstock, D. M., Nakanishi, K., Helgadottir, H. R., & Jasin, M. (2006) · Methods in enzymology on CD-ROM/Methods in enzymology · doi:10.1016/s0076-6879(05)09031-2 · Cited by 163
“Short-tract gene conversion without crossing-over, which appears to be the majority of HR events in mammalian cells (Richardson et al., 1998; Nakanishi et al., 2005), restores a functional GFP gene if the downstream internal GFP repeat (iGFP) is used as the repair template (Fig.”
BackgroundMethodSelf-citationBortezomib-induced “BRCAness” sensitizes multiple myeloma cells to PARP inhibitors
Neri, P. E., Ren, L., Gratton, K., Stebner, E., Johnson, J., Klimowicz, A. C., Duggan, P. R., Tassone, P., Mansoor, A., Stewart, D. A., et al. (2011) · Blood · doi:10.1182/blood-2011-06-363911 · Cited by 159
Feng, W., & Jasin, M. (2017) · Nature Communications · doi:10.1038/s41467-017-00634-0 · Cited by 161
Self-citationThompson, L. H., & Hinz, J. M. (2009) · Mutation research. Fundamental and molecular mechanisms of mutagenesis · doi:10.1016/j.mrfmmm.2009.02.003 · Cited by 155
“These provocative results are difficult to reconcile with the many studies using chromosomally integrated substrates in both human cells [25,123] and model systems [67,71,72,124] that found either a reduced efficiency of HRR or no change in efficiency [52,125,126].”
ResultHistone H4 deacetylation facilitates 53BP1 DNA damage signaling and double-strand break repair
Hsiao, K., & Mizzen, C. A. (2013) · Journal of Molecular Cell Biology · doi:10.1093/jmcb/mjs066 · Cited by 165
Genotype–phenotype correlations in Fanconi anemia
Neveling, K., Endt, D., Hoehn, H., & Schindler, D. (2009) · Mutation research. Fundamental and molecular mechanisms of mutagenesis · doi:10.1016/j.mrfmmm.2009.05.006 · Cited by 149
Howard, S. M., Yanez, D. A., & Stark, J. M. (2015) · PLoS Genetics · doi:10.1371/journal.pgen.1004943 · Cited by 148
“Factors important for the FANC pathway, including FANCA, have been shown to promote HDR and SSA [52, 69].”
Ekumi, K. M., Paculová, H., Lenasi, T., Pospíchalová, V., Bösken, C. A., Rybaříková, J., Bryja, V., Geyer, M., Blažek, D., & Barborič, M. (2015) · Nucleic Acids Research · doi:10.1093/nar/gkv101 · Cited by 145
A FancD2-Monoubiquitin Fusion Reveals Hidden Functions of Fanconi Anemia Core Complex in DNA Repair
Matsushita, N., Kitao, H., Ishiai, M., Nagashima, N., Hirano, S., Okawa, K., Ohta, T., Yu, D. S., McHugh, P. J., Hickson, I. D., et al. (2005) · Molecular Cell · doi:10.1016/j.molcel.2005.08.018 · Cited by 142
Kalb, R., Neveling, K., Hoehn, H., Schneider, H., Linka, Y., Batish, S. D., Hunt, C., Berwick, M., Callén, E., Surrallés, J., et al. (2007) · The American Journal of Human Genetics · doi:10.1086/517616 · Cited by 139
Park, J.-Y., Singh, T. R., Nassar, N., Zhang, F., Freund, M., Hanenberg, H., Meetei, A. R., & Andreassen, P. R. (2014) · Oncogene · doi:10.1038/onc.2013.421 · Cited by 130
Stecklein, S. R., Kumaraswamy, E., Behbod, F., Wang, W., Chaguturu, V., Harlan-Williams, L. M., & Jensen, R. A. (2012) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1203326109 · Cited by 136
“This assay was performed essentially as previously described (38).”
MethodSkp2 E3 Ligase Integrates ATM Activation and Homologous Recombination Repair by Ubiquitinating NBS1
Wu, J., Zhang, X., Zhang, L., Wu, C., Rezaeian, A. H., Chan, C., Li, J.-M., Wang, J., Gao, Y., Han, F., et al. (2012) · Molecular Cell · doi:10.1016/j.molcel.2012.02.018 · Cited by 135
“To accomplish this, we used a PCR-based method to investigate both HR and NHEJ repair (Figure S6B) (Nakanishi et al., 2005; Peng et al., 2009).”
Histone H2AX and Fanconi anemia FANCD2 function in the same pathway to maintain chromosome stability
Bogliolo, M., Lyakhovich, A., Callén, E., Castellà, M., Cappelli, E., Ramı́rez, M. J., Creus, A., Marcos, R., Kalb, R., Neveling, K., et al. (2007) · The EMBO Journal · doi:10.1038/sj.emboj.7601574 · Cited by 128
“The fact that FANCD2 forms foci with BRCA1 and RAD51 during S phase suggests that the FA/BRCA pathway is involved in HR repair of DSB during S phase (Taniguchi et al, 2002a; D’Andrea, 2003; D’Andrea and Grompe, 2003; Nakanishi et al, 2005).”
BackgroundPhosphorylation of FANCD2 on Two Novel Sites Is Required for Mitomycin C Resistance
Ho, G. P. H., Margossian, S. P., Taniguchi, T., & D’Andrea, A. D. (2006) · Molecular and Cellular Biology · doi:10.1128/mcb.02018-05 · Cited by 118
“Phosphorylation may enhance the activity of FANCD2 in homologous recombination repair (28).”
BackgroundSelf-citationFanconi anemia and DNA replication repair
PATEL, K., & Joenje, H. (2007) · DNA repair · doi:10.1016/j.dnarep.2007.02.002 · Cited by 114
Regulation of the Fanconi anemia pathway by a SUMO-like delivery networkPreprint
Yang, K., Moldovan, G., Vinciguerra, P., Murai, J., Takeda, S., & D’Andrea, A. D. (2011) · Genes & Development · doi:10.1101/gad.17020911 · Cited by 114
“The cellular level of FANCD2-Ub controls homologous recombination (HR) repair (Nakanishi et al. 2005), and the level of PCNA-Ub controls TLS repair (Kannouche et al.”
BackgroundSelf-citationNacerddine, K., Beaudry, J., Ginjala, V., Westerman, B. A., Mattiroli, F., Song, J., van der Poel, H. G., Balagué, O., Pritchard, C. E. J., Cornelissen‐Steijger, P., et al. (2012) · Journal of Clinical Investigation · doi:10.1172/jci57477 · Cited by 117
“To examine whether lack of Bmi1 phosphorylation affects HR repair of DSBs in cells, we used an I-Sce1 meganuclease homology-directed DNA repair assay that allows reporting of HR repair events by flow cytometry analysis of cellular GFP (47).”
InfluentialHsp90: A New Player in DNA Repair?
Pennisi, R., Ascenzi, P., & Di Masi, A. (2015) · Biomolecules · doi:10.3390/biom5042589 · Cited by 112
“TLS is catalyzed by specialized polymerases, including the Y family polymerases.”
BackgroundInfluentialThe FANCM family of DNA helicases/translocases
Whitby, M. C. (2010) · DNA repair · doi:10.1016/j.dnarep.2009.12.012 · Cited by 109
Timed inhibition of CDC7 increases CRISPR-Cas9 mediated templated repair
Wienert, B., Nguyen, D. N., Guenther, A., Feng, S. J., Locke, M. N., Wyman, S. K., Shin, J. J., Kazane, K. R., Gregory, G. L., Carter, M., et al. (2020) · Nature Communications · doi:10.1038/s41467-020-15845-1 · Cited by 102
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 108
Functional and mutational landscapes of BRCA1 for homology-directed repair and therapy resistance
Anantha, R. W., Simhadri, S. R., Foo, T. K., Miao, S. Y., Liu, J., Shen, Z., Ganesan, S., & Xia, B. (2017) · eLife · doi:10.7554/elife.21350 · Cited by 109
“In this assay, the endogenous BRCA1 was first depleted in U2OS/DR-GFP cells (Nakanishi et al., 2005; Xia et al., 2006) using an siRNA targeting the 3’-UTR of the gene, and various BRCA1 proteins were then expressed from cDNAs (lacking the 3’-UTR) co-transfected with a plasmid expressing I-SceI, which cleaves the repor…”
MethodDNA Polymerase POLN Participates in Cross-Link Repair and Homologous Recombination
Moldovan, G., Madhavan, M. V., Mirchandani, K. D., McCaffrey, R. M., Vinciguerra, P., & D’Andrea, A. D. (2009) · Molecular and Cellular Biology · doi:10.1128/mcb.01124-09 · Cited by 103
“Although HR was shown to be dependent on ubiquitination of FANCD2-I by the core complex (24), TLS seems to be controlled by the core complex independent of this event and independent of PCNA ubiquitination (20).”
BackgroundMethodInfluentialSelf-citationThe Tumor Suppressor PALB2: Inside Out
Ducy, M., Sesma-Sanz, L., Guitton-Sert, L., Lashgari, A., Gao, Y., Brahiti, N., Rodrigue, A., Margaillan, G., Caron, M., Côté, J., et al. (2019) · Trends in Biochemical Sciences · doi:10.1016/j.tibs.2018.10.008 · Cited by 104
Chemistry and Biology of Acylfulvenes: Sesquiterpene-Derived Antitumor Agents
Tanasova, M., & Sturla, S. J. (2012) · Chemical Reviews · doi:10.1021/cr2001367 · Cited by 101
Karanja, K. K., Cox, S. W., Duxin, J. P., Stewart, S. A., & Campbell, J. L. (2012) · Cell Cycle · doi:10.4161/cc.22215 · Cited by 100
DNA double-strand breaks: Their production, recognition, and repair in eukaryotes
Ohnishi, T., Mori, E., & Takahashi, A. (2009) · Mutation Research - Fundamental and Molecular Mechanisms of Mutagenesis · doi:10.1016/j.mrfmmm.2009.06.010 · Cited by 98
Differential Usage of Alternative Pathways of Double-Strand Break Repair in Drosophila
Preston, C. R., Flores, C. C., & Engels, W. R. (2005) · Genetics · doi:10.1534/genetics.105.050138 · Cited by 96
“The prevalence of different break repair pathways has been tested in brewer’s and fission yeast, as well as Arabidopsis, chicken and mammalian cells (ELLIOTT et al. 2005; LEE et al. 1999; NAKANISHI et al. 2005; OREL et al. 2003; PRUDDEN et al. 2003; STARK et al. 2004; WANG et al. 2001; WILSON 2002).”
BackgroundCavallo, F., Graziani, G., Antinozzi, C., Feldman, D. R., Houldsworth, J., Bosl, G. J., Chaganti, R. S. K., Moynahan, M. E., Jasin, M., & Barchi, M. (2012) · PLoS ONE · doi:10.1371/journal.pone.0051563 · Cited by 98
“The latter requires several classes of proteins including the nucleotide excision repair (NER) proteins XPF-ERCC1, translesion DNA-polymerases, Fanconi anemia gene products [12,13,14], and homologous recombination repair (HR) factors [15].”
BackgroundSelf-citationWang, C. Q., Krishnan, V., Tay, L. S., Chin, D. W. L., Koh, C. P., Chooi, J.-Y., Nah, G. S. S., Du, L., Jacob, B., Yamashita, N., et al. (2014) · Cell Reports · doi:10.1016/j.celrep.2014.06.046 · Cited by 95
Suppression of the DNA repair defects of BRCA2-deficient cells with heterologous protein fusions
Saeki, H., Siaud, N., Christ, N., Wiegant, W. W., van Buul, P. P. W., Han, M., Zdzienicka, M. Z., Stark, J. M., & Jasin, M. (2006) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0600298103 · Cited by 95
Self-citationSobeck, A., Stone, S., Costanzo, V., de Graaf, B., Reuter, T., de Winter, J. P., Wallisch, M., Akkari, Y. M. N., Olson, S. B., Wang, W., et al. (2005) · Molecular and Cellular Biology · doi:10.1128/mcb.26.2.425-437.2006 · Cited by 95
“Accumulating evidence points to a role for the FA pathway in repair of DNA DSBs (26, 27, 69, 82, 100, 101).”
BackgroundInfluentialSpardy, N. A., Duensing, A. U., Charles, D., Haines, N., Nakahara, T., Lambert, P. F., & Duensing, S. M. (2007) · Journal of Virology · doi:10.1128/jvi.01121-07 · Cited by 93
“Stalled forks are substrates for homologous recombination, and DNA double-strand breaks that occur as repair intermediates (28) may remain unrepaired in FA-deficient cells (21), thereby leading to increased chromosomal instability.”
BackgroundFANCG promotes formation of a newly identified protein complex containing BRCA2, FANCD2 and XRCC3
Wilson, J. B., Yamamoto, K., Marriott, A. S., Hussain, S., Sung, P., Hoatlin, M. E., Mathew, C. G., Takata, M., Thompson, L., Kupfer, G. M., et al. (2008) · Oncogene · doi:10.1038/sj.onc.1211034 · Cited by 92
“There has been much conjecture and conflicting results in the literature on the involvement of the FA proteins in HRR (and single-strand annealing based on HRR) of I-SceI induced DNA double strand breaks (DSBs) in artificial direct-repeat substrates (Niedzwiedz et al., 2004; Bridge et al., 2005; Nakanishi et al., 2005…”
BackgroundResultCooperation of the ATM and Fanconi Anemia/BRCA Pathways in Double-Strand Break End Resection
Cai, M., Dunn, C. E., Chen, W., Kochupurakkal, B. S., Nguyen, H. Q., Moreau, L. A., Shapiro, G. I., Parmar, K., Kozono, D., & D’Andrea, A. D. (2020) · Cell Reports · doi:10.1016/j.celrep.2020.01.052 · Cited by 91
“Recent studies also indicate that the FANCA protein can promote the process of SSA (Benitez et al., 2018) and may thereby positively regulate end resection.”
BackgroundSelf-citationThe Fanconi anemia core complex is required for efficient point mutagenesis and Rev1 foci assembly
Mirchandani, K. D., McCaffrey, R. M., & D’Andrea, A. D. (2008) · DNA repair · doi:10.1016/j.dnarep.2008.03.001 · Cited by 90
Self-citationHistone Deacetylases 9 and 10 Are Required for Homologous Recombination
Kotian, S., Liyanarachchi, S., Zelent, A., & Parvin, J. D. (2011) · Journal of Biological Chemistry · doi:10.1074/jbc.c110.194233 · Cited by 91
The Fanconi anemia (FA) pathway confers glioma resistance to DNA alkylating agents
Chen, C. C., Taniguchi, T., & D’Andrea, A. D. (2007) · Journal of Molecular Medicine · doi:10.1007/s00109-006-0153-2 · Cited by 87
Self-citationBenitez, A., Liu, W., Palovcak, A., Wang, G., Moon, J., An, K., Kim, A., Zheng, K., Zhang, Y., Bai, F., et al. (2018) · Molecular Cell · doi:10.1016/j.molcel.2018.06.030 · Cited by 83
“FANCA Bidirectionally Anneals Single-Stranded DNA The FA core complex has been previously reported to be involved in the SSA sub-pathway of DSB repair through the canonical FA pathway (Howard et al., 2015; Nakanishi et al., 2005; Yang et al., 2005).”
InfluentialWhitehurst, C. B., Vaziri, C., Shackelford, J., & Pagano, J. S. (2012) · Journal of Virology · doi:10.1128/jvi.00588-12 · Cited by 88
“Monoubiquitinated (activated) FANCD2 associates with chromatin and directs replication-coupled repair of interstrand cross-links (ICL) (35, 38, 47) and may also stimulate homologous recombination (HR) (40).”
BackgroundCtIP mediates replication fork recovery in a FANCD2-regulated manner
Yeo, J. E., Lee, E. H., Hendrickson, E. A., & Sobeck, A. (2014) · Human Molecular Genetics · doi:10.1093/hmg/ddu078 · Cited by 91
A role for monoubiquitinated FANCD2 at telomeres in ALT cells
Fan, Q., Zhang, F., Barrett, B., Ren, K., & Andreassen, P. R. (2009) · Nucleic Acids Research · doi:10.1093/nar/gkn995 · Cited by 88
Yang, Y.-G., Saidi, A., Frappart, P., Min, W., Barrucand, C., Dumon-Jones, V., Michelon, J., Herceg, Z., & Wang, Z. (2006) · The EMBO Journal · doi:10.1038/sj.emboj.7601411 · Cited by 84
“G/-D2) exhibit defects of both HDR and SSA (Stark et al, 2004; Nakanishi et al, 2005; Yang et al, 2005).”
BackgroundMethodInfluentialSelf-citationGonzãlez, F., Georgieva, D., Vanoli, F., Shi, Z., Stadtfeld, M., Ludwig, T., Jasin, M., & Huangfu, D. (2013) · Cell Reports · doi:10.1016/j.celrep.2013.02.005 · Cited by 86
“These studies suggest a potential link between HR and reprogramming, given that several FA pathway components have been shown to promote HR (Nakanishi et al., 2005).”
BackgroundSelf-citationCollins, N. B., Wilson, J. B., Bush, T., Tomashevski, A., Roberts, K. J., Jones, N. J., & Kupfer, G. M. (2008) · Blood · doi:10.1182/blood-2008-05-154294 · Cited by 84
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 82
Self-citationHomology-directed Fanconi anemia pathway cross-link repair is dependent on DNA replication
Nakanishi, K., Cavallo, F., Perrouault, L., Giovannangeli, C., Moynahan, M. E., Barchi, M., Brunet, E., & Jasin, M. (2011) · Nature Structural & Molecular Biology · doi:10.1038/nsmb.2029 · Cited by 79
Self-citation
Metadata
- Authors
- Nakanishi, K., Yang, Y.-G., Pierce, A. J., Taniguchi, T., Digweed, M., D'Andrea, A. D., Wang, Z.-Q., & Jasin, M.
- Affiliations
- Memorial Sloan Kettering Cancer Center (US)
- Molecular Biology Program, Memorial Sloan–Kettering Cancer Center, 1275 York Avenue, New York, NY 10021; International Agency for Research on Cancer, 150 Cours Albert Thomas, 69008 Lyon, France; Department of Radiation Oncology, Dana–Farber Cancer Institute, Harvard Medical School, 44 Binney Street, Boston, MA 02115; and Institut für Humangenetik, Charite-Campus Virchow-Klinikum, Humboldt Universität zu Berlin, Augustenburger Platz 1, 13353 Berlin, Germany
- Corresponding author
- Jasin, Maria
- Venue
- Proceedings of the National Academy of Sciences
- Publisher
- National Academy of Sciences
- Published
- 2005-01-13
- Volume
- 102
- Issue
- 4
- Pages
- 1110-1115
- ISSN
- 0027-8424 (ISSN-L)
- 1091-6490
- PMC
- PMC545844
- OpenAlex
- W2029164849
- Cited by
- 384
- References
- 42
- Citations by year
- 2026: 5 · 2025: 7 · 2024: 11 · 2023: 10 · 2022: 7 · 2021: 15 · 2020: 12 · 2019: 12 · 2018: 11 · 2017: 24 · 2016: 13 · 2015: 25 · 2014: 22 · 2013: 10 · 2012: 26
- FWCI
- 12.67
- Type
- journal article
- Language
- en
- Open access
- green
- www.ncbi.nlm.nih.gov
- Locations
- Proceedings of the National Academy of Sciences (publishedVersion)
- PubMed Central (publishedVersion)
- PubMed (publishedVersion)
- Funders
- Fanconi Anemia Research Fund
- National Institutes of Health
- National Cancer Institute (P01-CA94060, P01CA094060)
- National Institute of General Medical Sciences (R01GM054668, GM54668)
- Topics
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › DNA Repair Mechanisms
- Health Sciences › Medicine › Hematology › Blood disorders and treatments
- Health Sciences › Medicine › Oncology › PARP inhibition in cancer therapy
- Keywords
- Fanconi anemia, FANCD2 monoubiquitination, homology-directed repair, DNA double-strand break repair, single-strand annealing, BRCA1, BRCA2, FANCA, FANCG, ATM phosphorylation, DNA repair pathway choice
- MeSH terms
- Cell Line, DNA Repair, Humans, Nuclear Proteins, Recombination, Genetic, Ubiquitin, Fanconi Anemia Complementation Group D2 Protein
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