Cited by 385DNA Repair MechanismsBlood disorders and treatmentsPARP inhibition in cancer therapy

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Human Fanconi anemia monoubiquitination pathway promotes homologous DNA repair

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Nakanishi, Koji, Yang, Yun-Gui, Pierce, Andrew J., Taniguchi, Toshiyasu, Digweed, Martin, D'Andrea, Alan D., Wang, Zhao-Qi, Jasin, Maria·2005·Proceedings of the National Academy of Sciences

DOI 10.1073/pnas.0407796102PMC PMC545844

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Abstract

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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Items 201–300 of 385

The Fanconi anemia pathway in replication stress and DNA crosslink repair
Jones, M. V., & Huang, T. T. (2012) · Cellular and Molecular Life Sciences · doi:10.1007/s00018-012-1051-0 · Cited by 33
“Deficiency in either the FA core or ID complexes in this assay leads to a relatively mild HR defect compared to downstream FA pathway components, such as BRCA2 [77, 82].”
Influential
An RNF168 fragment defective for focal accumulation at DNA damage is proficient for inhibition of homologous recombination in BRCA1 deficient cells
Muñoz, M. C., Yanez, D. A., & Stark, J. M. (2014) · Nucleic Acids Research · doi:10.1093/nar/gku421 · Cited by 34
“FANCD2 is part of the Fanconi Anemia pathway that is important for DNA crosslink repair and HR (45,46).”
Background
Inherited bone marrow failure syndromes in 2012
Sakaguchi, H., Nakanishi, K., & Kojima, S. (2012) · International Journal of Hematology · doi:10.1007/s12185-012-1249-9 · Cited by 32
“In 2005, a cellular study in humans showed that mutation of either the FA core complex members or the FANCD2 monoubiquitination site resulted in HR defects [16].”
BackgroundSelf-citation
A distinct role for recombination repair factors in an early cellular response to transcription–replication conflicts
Shao, X., Joergensen, A. M., Howlett, N. G., Lisby, M., & Oestergaard, V. H. (2020) · Nucleic Acids Research · doi:10.1093/nar/gkaa268 · Cited by 36
“Notably, FANCA-disrupted One role of BRCA2, BLM and FANCD2 at T–”
The Fanconi anemia core complex promotes CtIP-dependent end resection to drive homologous recombination at DNA double-strand breaks
van de Kooij, B., van der Wal, F. J., Rother, M. B., Wiegant, W. W., Creixell, P., Stout, M., Joughin, B. A., Vornberger, J., Altmeyer, M., van Vugt, M. A. T. M., et al. (2024) · Nature Communications · doi:10.1038/s41467-024-51090-6 · Cited by 31
“Thus, both FANCL and Ube2T are recruited to UV-A laser-induced DSBs. FANCD2 has previously been shown to accumulate at DNA damage sites upon DSB-inducing treatments 43,44 .”
Influential
Defects in homologous recombination repair behind the human diseases: FA and HBOC
Katsuki, Y., & Takata, M. (2016) · Endocrine Related Cancer · doi:10.1530/erc-16-0221 · Cited by 32
“2003, 2004) or mildly decreased in human cells (Nakanishi et al. 2005).”
RAD51AP1 and RAD54L Can Underpin Two Distinct RAD51-Dependent Routes of DNA Damage Repair via Homologous Recombination
Selemenakis, P., Sharma, N., Uhrig, M. E., Katz, J., Kwon, Y., Sung, P., & Wiese, C. (2022) · Frontiers in Cell and Developmental Biology · doi:10.3389/fcell.2022.866601 · Cited by 29
“We used U2OS-DRGFP cells (Nakanishi et al., 2005; Xia et al., 2006) to assess the effects of RAD51AP1 and/or RAD54L depletion on gene conversion.”
Fanconi anemia and dyskeratosis congenita/telomere biology disorders: Two inherited bone marrow failure syndromes with genomic instability
Fiesco-Roa, M. Ó., Teresa, B. G., Leal-Anaya, P., Hek, R. V., Wegman-Ostrosky, T., Frı́as, S., & Rodríguez, A. (2022) · Frontiers in Oncology · doi:10.3389/fonc.2022.949435 · Cited by 34
“Ub-FANCD2I is being long recognized as essential for the recruitment of proteins involved in the DNA repair downstream activities of the FA/ BRCA pathway (21), as FANCD2-I forms nuclear DNA repair foci co-localize with DNA repair factors (22).”
Background
Co-opting the Fanconi Anemia Genomic Stability Pathway Enables Herpesvirus DNA Synthesis and Productive Growth
Karttunen, H., Savas, J. N., McKinney, C. C., Chen, Y.-H., Yates, J. R., Hukkanen, V., Huang, T. T., & Mohr, I. (2014) · Molecular Cell · doi:10.1016/j.molcel.2014.05.020 · Cited by 30
“Intriguingly, FANCD2 (and likely FANCI) monoubiquitination is required for SSA, suggesting an early role for monoubiquitinated FA effector proteins in homologous DSB repair pathway choice (Nakanishi et al., 2005).”
Human Mus81 and FANCB independently contribute to repair of DNA damage during replication
Nomura, Y., Adachi, N., & Koyama, H. (2007) · Genes to Cells · doi:10.1111/j.1365-2443.2007.01124.x · Cited by 28
UBE2W Interacts with FANCL and Regulates the Monoubiquitination of Fanconi Anemia Protein FANCD2
Zhang, Y., Zhou, X., Zhao, L., Li, C., Zhu, H.-Q., Xu, L., Shan, L., Liao, X., Guo, Z., & Huang, P. (2011) · Molecules and Cells · doi:10.1007/s10059-011-0015-9 · Cited by 28
“For example, cells use homologous DNA repairs (HDR) to eliminate DNA cross-linking damages (Nakanishi et al., 2005) but use excision repair to eliminate CPDs (de Lima-Bessa et al.”
Background
Loss of Ubr2, an E3 ubiquitin ligase, leads to chromosome fragility and impaired homologous recombinational repair
Ouyang, Y., Kwon, Y. T., An, J. Y., Eller, D., Tsai, S.-C., Diaz-Perez, S. V., Troke, J. J., Teitell, M. A., & Marahrens, Y. (2006) · Mutation research. Fundamental and molecular mechanisms of mutagenesis · doi:10.1016/j.mrfmmm.2005.12.016 · Cited by 28
The nuclear accumulation of the Fanconi anemia protein FANCE depends on FANCC
Léveillé, F., Ferrer, M., Medhurst, A. L., Laghmani, E. H., Rooimans, M. A., Bier, P., Steltenpool, J., Titus, T. A., Postlethwait, J. H., Hoatlin, M. E., et al. (2006) · DNA repair · doi:10.1016/j.dnarep.2006.01.005 · Cited by 28
Homologous Recombination Is a Primary Pathway to Repair DNA Double-Strand Breaks Generated during DNA Rereplication
Truong, L. N., Li, Y., Sun, E., Ang, K., Hwang, P. Y.-H., & Wu, X. (2014) · Journal of Biological Chemistry · doi:10.1074/jbc.m114.576488 · Cited by 29
“Expressing shRNAs for fanconi anemia (FA) proteins FancA and FancD2, which are important for HR (45), also decreased HR-mediated DSB repair at SC-HR-EGFP-SV40 ori upon SV40 T expression (Fig.”
Background
Snm1B/Apollo functions in the Fanconi anemia pathway in response to DNA interstrand crosslinks
Mason, J. M., & Sekiguchi, J. (2011) · Human Molecular Genetics · doi:10.1093/hmg/ddr153 · Cited by 25
“FANCD2 depletion reduced the frequency of homologous recombination by 50%; however, the defect was less severe compared with RAD51-depleted cells, as previously reported (6,13,42,49).”
BackgroundResult
Selection and the Cell Cycle: Positive Darwinian Selection in a Well-Known DNA Damage Response Pathway
O’Connell, M. J. (2010) · Journal of Molecular Evolution · doi:10.1007/s00239-010-9399-y · Cited by 25
Inhibition of non-homologous end joining in Fanconi Anemia cells results in rescue of survival after interstrand crosslinks but sensitization to replication associated double-strand breaks
Eccles, L. J., Bell, A., & Powell, S. N. (2018) · DNA repair · doi:10.1016/j.dnarep.2018.02.003 · Cited by 25
Molecular Pathogenesis of Fanconi Anemia
Collins, N. B., & Kupfer, G. M. (2005) · International Journal of Hematology · doi:10.1532/ijh97.05108 · Cited by 26
“In a similar assay monitoring the HDR of an I-SceI DSB, patient-derived cells from groups FA-A, FA-G, and FA-D2, as well as cells from mice homozygous for FANCA deletion, were shown to be defective in HDR [ 64 ,65].”
Background
3R coordination by Fanconi anemia proteins
Macé‐Aimé, G., Bogliolo, M., Guervilly, J.-H., du Villard, J.-A. D., & Rosselli, F. (2005) · Biochimie · doi:10.1016/j.biochi.2005.05.003 · Cited by 26
A peptide nucleic acid targeting nuclearRAD51sensitizes multiple myeloma cells to melphalan treatment
Alagpulinsa, D. A., Yaccoby, S., Ayyadevara, S., & Reis, R. J. S. (2015) · Cancer Biology & Therapy · doi:10.1080/15384047.2015.1040951 · Cited by 26
“Also, the drug induced cell-cycle arrest during S phase, a key interval during which the FA pathway interacts with BRCA1 and RAD51 to activate RAD51-mediated repair of ICLs.9,37 BRCA1 and paralogs of RAD51 play critical roles in www.tandfonline.com 981Cancer Biology & Therapy the recruitment of RAD51 protein to damage…”
BackgroundInfluential
CTDP1 regulates breast cancer survival and DNA repair through BRCT-specific interactions with FANCI
Hu, W.-F., Krieger, K. L., Lagundžin, D., Li, X., Cheung, R. S., Taniguchi, T., Johnson, K. R., Bessho, T., Monteiro, Á. N. A., & Woods, N. T. (2019) · Cell Death Discovery · doi:10.1038/s41420-019-0185-3 · Cited by 26
Self-citation
FANCD2 influences replication fork processes and genome stability in response to clustered DSBs
Zhu, J., Su, F., Mukherjee, S., Mori, E., Hu, B., & Asaithamby, A. (2015) · Cell Cycle · doi:10.1080/15384101.2015.1036210 · Cited by 25
“Mechanistically, FANCD2 is required for correct recruitment of RPA2 and Rad51 to the sites of clustered DSBs and that is critical for proper processing of clustered DSBs. Significantly, FANCD2-decifient cells exhibited defective chromosome segregation, elevated levels of chromosomal aberrations, and anchorage-independ…”
BackgroundInfluential
K63-linked ubiquitination of FANCG is required for its association with the Rap80-BRCA1 complex to modulate homologous recombination repair of DNA interstand crosslinks
Zhu, B., Yan, K., Li, L., Lin, M., Zhang, S., He, Q., Zheng, D., Yang, H., & Shao, G. (2014) · Oncogene · doi:10.1038/onc.2014.229 · Cited by 25
Biomarkers and Mechanisms of FANCD2 Function
Willers, H., Kachnic, L. A., Luo, C., Li, L., Purschke, M., Borgmann, K., Held, K. D., & Powell, S. N. (2008) · BioMed Research International · doi:10.1155/2008/821529 · Cited by 24
“Disruption of the nuclear core complex or mutation of FANCD2’s monoubiquitination site at K561 impairs repair processes, including homologous recombination, that are active at stalled forks [8, 14].”
Background
TACC3 deregulates the DNA damage response and confers sensitivity to radiation and PARP inhibition
Ha, G., Kim, J.-L., Petersson, A., Oh, S. H., Denning, M. F., Patel, T., & Breuer, E.-K. (2014) · Oncogene · doi:10.1038/onc.2014.105 · Cited by 24
MTDH/AEG-1 downregulation using pristimerin-loaded nanoparticles inhibits Fanconi anemia proteins and increases sensitivity to platinum-based chemotherapy
Bi, J., Areecheewakul, S., Li, Y., Yang, S., Zhang, Y., Ebeid, K., Li, L., Thiel, K. W., Zhang, J., Dai, D. D., et al. (2019) · Gynecologic Oncology · doi:10.1016/j.ygyno.2019.08.014 · Cited by 24
“The FA pathway plays a critical role in DNA repair following interstrand crosslink damage induced by platinum compounds[10].”
Background
Removal of TREX1 activity enhances CRISPR–Cas9-mediated homologous recombination
Karasu, M. E., Toufektchan, E., Chen, Y., Albertelli, A., Cullot, G., Maciejowski, J., & Corn, J. E. (2024) · Nature Biotechnology · doi:10.1038/s41587-024-02356-3 · Cited by 27
“For example, loss of function in one of 22 genes involved in Fanconi anemia (FA) can largely prevent HDR 9,12,13 .”
Genomic Instability in Mice Is Greater in Fanconi Anemia Caused by Deficiency of Fancd2 than Fancg
Reliene, R., Yamamoto, M. L., Rao, P. N., & Schiestl, R. H. (2010) · Cancer Research · doi:10.1158/0008-5472.can-09-1022 · Cited by 24
Dynamin impacts homology-directed repair and breast cancer response to chemotherapy
Chernikova, S. B., Nguyen, R. B., Truong, J. T., Mello, S. S., Stafford, J. H., Hay, M. P., Olson, A., Solow-Cordero, D. E., Wood, D., Henry, A. S., et al. (2018) · Journal of Clinical Investigation · doi:10.1172/jci87191 · Cited by 24
Disparate contributions of the Fanconi anemia pathway and homologous recombination in preventing spontaneous mutagenesis
Hinz, J. M., Nham, P. B., Urbin, S. S., Jones, I. M., & Thompson, L. H. (2007) · Nucleic Acids Research · doi:10.1093/nar/gkm315 · Cited by 25
“For example, studies based on chromosomally integrated reporter constructs containing a I–Sce-I restriction site and PCR analysis found no reduction in NHEJ activity in FA cells from three complementation groups (A, D2 and G) compared to gene-complemented control cells (26).”
Diagnosis of Fanconi Anaemia by ionising radiation- or mitomycin C-induced micronuclei
Francies, F. Z., Wainwright, R., Poole, J., Leeneer, K. D., Coene, I., Wieme, G., Poirel, H. A., Brichard, B., Vermeulen, S., Vral, A., et al. (2017) · DNA repair · doi:10.1016/j.dnarep.2017.11.001 · Cited by 22
Bortezomib salvage followed by a P hase I / II study of bortezomib plus high‐dose melphalan and tandem autologous transplantation for patients with primary resistant myeloma
Nishihori, T., Alekshun, T. J., Shain, K. H., Sullivan, D. M., Baz, R., Perez, L. E., Pidala, J., Kharfan‐Dabaja, M. A., Ochoa-Bayona, J. L., Fernandez, H. F., et al. (2012) · British Journal of Haematology · doi:10.1111/j.1365-2141.2012.09099.x · Cited by 22
Chromosomal Integrity after UV Irradiation Requires FANCD2-Mediated Repair of Double Strand Breaks
Federico, M. B., Vallerga, M. B., Radl, A., Paviolo, N. S., Bocco, J. L., Giorgio, M. D., Soria, G., & Gottifredi, V. (2016) · PLoS Genetics · doi:10.1371/journal.pgen.1005792 · Cited by 25
“ICLs [12,14,16,81], our report demonstrates that replication-coupled DSBs unrelated to ICLs may require FANCD2 for their repair through the HRR pathway.”
Background
EAF2 regulates DNA repair through Ku70/Ku80 in the prostate
Ai, J., Pascal, L. E., Wei, L., Zang, Y., Zhou, Y., Yu, X., Gong, Y., Nakajima, S., Nelson, J. B., Levine, A. S., et al. (2016) · Oncogene · doi:10.1038/onc.2016.373 · Cited by 23
“Using the Hela pDR-GFP-based assay for HR repair 29 , no significant difference was detected in the percentage of GFP-positive cells between siEAF1-treated and siRNA control groups (Figure 4B), indicating that EAF1 may not affect the HR repair pathway.”
Self-citation
Regulation of various DNA repair pathways by E3 ubiquitin ligases
Natarajan, C., & Takeda, K. (2017) · Journal of Cancer Research and Therapeutics · doi:10.4103/0973-1482.204879 · Cited by 25
A functionally impaired missense variant identified in French Canadian families implicates FANCI as a candidate ovarian cancer-predisposing gene
Fierheller, C. T., Guitton-Sert, L., Alenezi, W. M., Revil, T., Oros, K. K., Gao, Y., Bédard, K., Arcand, S. L., Serruya, C., Behl, S., et al. (2021) · Genome Medicine · doi:10.1186/s13073-021-00998-5 · Cited by 22
Retracted: DICER-dependent biogenesis of let-7 miRNAs affects human cell response to DNA damage via targeting p21/p27
Liu, B., Liu, M., Wang, J., Zhang, X., Wang, X., Wang, P., Wang, H., Li, W., & Wang, Y. (2015) · Nucleic Acids Research · doi:10.1093/nar/gku1368 · Cited by 22
“Cell HRR reporter assay (29) or NHEJ reporter assay (30) were used as described previously.”
BackgroundMethod
Retracted
FGFR2 regulates Mre11 expression and double-strand break repair via the MEK-ERK-POU1F1 pathway in breast tumorigenesis
Huang, Y.-L., Chou, W., Hsiung, C.-N., Hu, L., Chu, H., & Shen, C. (2015) · Human Molecular Genetics · doi:10.1093/hmg/ddv102 · Cited by 21
“For the HRR assay (23,45), in brief, U2OS-DR-GFP cells were cotransfected with pSce (2 μg) and the gene-expressing plasmids (4 μg of an individual plasmid in a 60-mm tissue culture dish) or siRNA indicated in each figures (empty vector or scrambled siRNA as control).”
Coordinated action of the Fanconi anemia and ataxia telangiectasia pathways in response to oxidative damage
Bosch, P. C., Bogliolo, M., & Surrallés, J. (2011) · DNA repair · doi:10.1016/j.dnarep.2011.02.007 · Cited by 22
Global Liver Proteomics of Rats Exposed for 5 Days to Phenobarbital Identifies Changes Associated with Cancer and with CYP Metabolism
Dail, M. B., Shack, L. A., Chambers, J. E., & Burgess, S. C. (2008) · Toxicological Sciences · doi:10.1093/toxsci/kfn198 · Cited by 22
The Fanconi anemia protein interaction network: Casting a wide net
Rego, M. A., Kolling, F. W., & Howlett, N. G. (2008) · Mutation research. Fundamental and molecular mechanisms of mutagenesis · doi:10.1016/j.mrfmmm.2008.11.018 · Cited by 22
“Surprisingly, despite the established interaction between FANCD2 and BRCA1 [36], and BRCA1s important role in the repair of DNA DSBs by HR [51], the ATM-dependent phosphorylation of FANCD2 on S222 does not appear to be required for DNA DSB HR [56].”
Background
Several tetratricopeptide repeat (TPR) motifs of FANCG are required for assembly of the BRCA2/D1-D2-G-X3 complex, FANCD2 monoubiquitylation and phleomycin resistance
Wilson, J. B., Blom, E., Cunningham, R., Xiao, Y., Kupfer, G. M., & Jones, N. J. (2010) · Mutation research. Fundamental and molecular mechanisms of mutagenesis · doi:10.1016/j.mrfmmm.2010.04.003 · Cited by 24
“Defective homologous recombination repair of I-SceI induced DNA double strand breaks (DSBs) of an artificial direct-repeat substrate has been reported for both a chicken DT40 fancg mutant and a human FA-G fibroblast cell line [55,59].”
Background
The Caenorhabditis elegans FancD2 ortholog is required for survival following DNA damage
Dequen, F., St-Laurent, J.-F., Gagnon, S., Carreau, M., & Desnoyers, S. (2005) · Comparative Biochemistry and Physiology Part B Biochemistry and Molecular Biology · doi:10.1016/j.cbpc.2005.05.010 · Cited by 22
Activation of the FA pathway mediated by phosphorylation and ubiquitination
Ishiai, M., Sato, K., Tomida, J., Kitao, H., Kurumizaka, H., & Takata, M. (2017) · Mutation research. Fundamental and molecular mechanisms of mutagenesis · doi:10.1016/j.mrfmmm.2017.05.003 · Cited by 20
Paths from DNA damage and signaling to genome rearrangements via homologous recombination
Nickoloff, J. A. (2017) · Mutation research. Fundamental and molecular mechanisms of mutagenesis · doi:10.1016/j.mrfmmm.2017.07.008 · Cited by 23
“and FANC proteins, which predispose to breast and other cancers [145-148].”
Background
Fanconi anemia D2 protein confers chemoresistance in response to the anticancer agent, irofulven
Wang, Y., Wiltshire, T. D., Senft, J., Wenger, S. L., Reed, E., & Wang, W. (2006) · Molecular Cancer Therapeutics · doi:10.1158/1535-7163.mct-06-0427 · Cited by 21
Targeting Homologous Recombination Repair in Cancer
Willers, H., Pfäffle, H. N., & Zou, L. (2011) · Elsevier eBooks · doi:10.1016/b978-0-12-384999-1.10007-1 · Cited by 21
The Fanconi anemia ubiquitin E3 ligase complex as an anti-cancer target
Sharp, M. F., Bythell‐Douglas, R., Deans, A. J., & Crismani, W. (2021) · Molecular Cell · doi:10.1016/j.molcel.2021.04.023 · Cited by 20
Sequence Conversion by Single Strand Oligonucleotide Donors via Non-homologous End Joining in Mammalian Cells
Liu, J., Majumdar, A., Liu, J., Thompson, L. H., & Seidman, M. M. (2010) · Journal of Biological Chemistry · doi:10.1074/jbc.m110.123844 · Cited by 20
New insights into tumor dormancy: Targeting DNA repair pathways
Evans, E. B. (2015) · World Journal of Clinical Oncology · doi:10.5306/wjco.v6.i5.80 · Cited by 21
Histone Deacetylase Inhibitors Selectively Target Homology Dependent DNA Repair Defective Cells and Elevate Non-Homologous Endjoining Activity
Smith, S. N., Fox, J. T., Mejia, M., Ruangpradit, W., Saberi, A., Kim, S., Choi, Y., Oh, S., Wang, Y., Choi, K., et al. (2014) · PLoS ONE · doi:10.1371/journal.pone.0087203 · Cited by 20
“5GFP) containing twin DR-GFP reporter cassettes [35] that undergo HDR following ISceI-induced DSB formation in the 59 cassette [23].”
MethodInfluential
Chronic treatment with cisplatin induces chemoresistance through the TIP60-mediated Fanconi anemia and homologous recombination repair pathways
Su, W., Ho, Y.-C., Wu, C.-K., Hsu, S.-H., Shiu, J.-L., Huang, J.-C., Chang, S., Chiu, W., Hung, J., Liu, T.-L., et al. (2017) · Scientific Reports · doi:10.1038/s41598-017-04223-5 · Cited by 19
Beyond interstrand crosslinks repair: contribution of FANCD2 and other Fanconi Anemia proteins to the replication of DNA
Federico, M. B., Campodónico, P. B., Paviolo, N. S., & Gottifredi, V. (2017) · Mutation research. Fundamental and molecular mechanisms of mutagenesis · doi:10.1016/j.mrfmmm.2017.09.004 · Cited by 19
The Fanconi anemia pathway: Insights from somatic cell genetics using DT40 cell line
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FLIP(C1orf112)-FIGNL1 complex regulates RAD51 chromatin association to promote viability after replication stress
Tischler, J. D., Tsuchida, H., Bosire, R., Oda, T. T., Park, A., & Adeyemi, R. O. (2024) · Nature Communications · doi:10.1038/s41467-024-45139-9 · Cited by 17
“To directly examine HR competency at DSBs in the absence of FLIP, we took advantage of U2OS cells expressing a previously repor-ted modi ﬁ ed GFP reporter that ﬂ uoresces green when an I-SceI enzyme-induced DSB is repaired 55 .”
Background
Chromosomal instability syndromes are sensitive to poly ADP-ribose polymerase inhibitors
Gaymes, T. J., Shall, S., Farzaneh, F., & Mufti, G. J. (2008) · Haematologica · doi:10.3324/haematol.13201 · Cited by 17
“The decreased but not absent rad51 foci formation in FA cells suggests that even though FA proteins are intrinsically involved in inter-strand crosslink repair and restart of DNA replication, FA has a mild HR defect as reported by other groups.(15,16) In fact, FA sensitivity to PI could be attributable to cell cycle c…”
Background
Role of the Exocyst Complex Component Sec6/8 in Genomic Stability
Torres, M. J., PANDITA, R. K., Kulak, O., Kumar, R., Formstecher, É., Horikoshi, N., Mujoo, K., Hunt, C. R., Zhao, Y., Lum, L., et al. (2015) · Molecular and Cellular Biology · doi:10.1128/mcb.00768-15 · Cited by 16
“To determine the effect of Sec8 depletion on recruitment at the I-SceI site, cleavage was analyzed by ChIP, using RAD51-, KU80-, and BRCA1-specific antibodies in combination with site-specific PCR primer pairs.”
MethodInfluential
Clonal tumor mutations in homologous recombination genes predict favorable clinical outcome in ovarian cancer treated with platinum-based chemotherapy
Luo, S., Zhang, Y., Yang, Y., Zhu, S., Liu, W., Zhu, J., Liang, X., Jiang, Z., Sun, S., Hou, X., et al. (2020) · Gynecologic Oncology · doi:10.1016/j.ygyno.2020.04.695 · Cited by 16
Self-citation
FANCD2 but not FANCA promotes cellular resistance to type II topoisomerase poisons
Kachnic, L. A., Li, L., Fournier, L., Ferraiolo, N., Dahm‐Daphi, J., Borgmann, K., & Willers, H. (2011) · Cancer Letters · doi:10.1016/j.canlet.2011.02.030 · Cited by 16
βarrestin-1 regulates DNA repair by acting as an E3-ubiquitin ligase adaptor for 53BP1
Nieto, A., Hara, M. R., Quereda, V., Grant, W. M., Saunders, V. C., Xiao, K., McDonald, P. H., & Duckett, D. R. (2019) · Cell Death and Differentiation · doi:10.1038/s41418-019-0406-6 · Cited by 16
Interstrand crosslinking of homologous repair template DNA enhances gene editing in human cells
Ghasemi, H. I., Bacal, J., Yoon, A. C., Tavasoli, K. U., Cruz, C., Vu, J. T., Gardner, B. M., & Richardson, C. D. (2023) · Nature Biotechnology · doi:10.1038/s41587-022-01654-y · Cited by 13
Multiparametric Circulating Tumor Cell Analysis to Select Targeted Therapies for Breast Cancer Patients
Franken, A., Behrens, B., Reinhardt, F., Yang, L., Rivandi, M., Marass, F., Jaeger, B. A., Krawczyk, N., Cieslik, J., Honisch, E., et al. (2021) · Cancers · doi:10.3390/cancers13236004 · Cited by 14
“Nonsense mutations in FANCA are likely to disrupt function and lead to deficiencies in DNA repair [42].”
Background
Identifying the Effects of BRCA1 Mutations on Homologous Recombination using Cells that Express Endogenous Wild-type BRCA1
Parvin, J. D., Chiba, N., & Ransburgh, D. J. R. (2011) · Journal of Visualized Experiments · doi:10.3791/2468 · Cited by 14
Fanconi Anemia: Fanconi anemia, breast and embryonal cancer risk revisited
Howlett, N. G. (2007) · European Journal of Human Genetics · doi:10.1038/sj.ejhg.5201860 · Cited by 14
Impeding the single-strand annealing pathway of DNA double-strand break repair by withaferin A-mediated FANCA degradation
Liu, W., Wang, G., Palovcak, A., Li, Y., Hao, S., Liu, Z., Landgraf, R., Yuan, F., & Zhang, Y. (2019) · DNA repair · doi:10.1016/j.dnarep.2019.02.010 · Cited by 13
FANCD2 monoubiquitination and activation by hexavalent chromium [Cr(VI)] exposure: Activation is not required for repair of Cr(VI)-induced DSBs
Vilcheck, S. K., Ceryak, S. M., O’Brien, T. J., & Patierno, S. R. (2006) · Mutation Research/Genetic Toxicology and Environmental Mutagenesis · doi:10.1016/j.mrgentox.2006.06.009 · Cited by 14
“However, while FA proteins promote HRR, they are apparently not essential to the process [76].”
Background
In vivo analysis of FANCD2 recruitment at meiotic DNA breaks in Caenorhabditis elegans
Germoglio, M., Valenti, A., Gallo, I., Forenza, C., Santonicola, P., Silva, N., & Adamo, A. (2020) · Scientific Reports · doi:10.1038/s41598-019-57096-1 · Cited by 12
Identification of New Regulators of Pancreatic Cancer Cell Sensitivity to Oxaliplatin and Cisplatin
Сергеевна, С. В., Vlasenkova, R., Zhou, Y., Astsaturov, I. A., & Галлямовна, К. Р. (2022) · Molecules · doi:10.3390/molecules27041289 · Cited by 13
“The enrichment of the first two pathways is predictable, considering known mechanisms of platinum cytotoxicity [37,38].”
Background
The DNA-binding activity of USP1-associated factor 1 is required for efficient RAD51-mediated homologous DNA pairing and homology-directed DNA repair
Liang, F., Miller, A. S., Tang, C., Maranon, D. G., Williamson, E. A., Hromas, R., Wiese, C., Zhao, W., Sung, P., & Kupfer, G. M. (2020) · Journal of Biological Chemistry · doi:10.1074/jbc.ra120.013714 · Cited by 13
“Successful DSB repair leads to GFP expression, the frequency of which is determined by fluorescent cell sorting (28).”
Background
Low joining efficiency and non-conservative repair of two distant double-strand breaks in mouse embryonic stem cells
Boubakour-Azzouz, I., & Ricchetti, M. (2007) · DNA repair · doi:10.1016/j.dnarep.2007.09.005 · Cited by 13
Phenotyping Genetic Diseases Using an Extension of µ-Scores for Multivariate Data
Morales, J. F., Song, T., Auerbach, A. D., & Wittkowski, K. M. (2008) · Statistical Applications in Genetics and Molecular Biology · doi:10.2202/1544-6115.1372 · Cited by 13
“Mutations in 13 known genes, FANCA, B, C, D1, D2, E, F, G, I, J, L, M and N (Meetei et al. 2003; Levitus et al. 2004; Levran et al. 2005; Meetei et al. 2005; Reid et al. 2007; Smogorzewska et al. 2007) are known to cause FA through a defect in a BRCA-related DNA repair pathway ( Nakanishi et al. 2005; Wang 2007).”
Background
Mapping the Genetic Interaction Network of PARP inhibitor ResponsePreprint
Simpson, D., Jia, L., Jing, Y., & Adamson, B. (2023) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/2023.08.19.553986 · Cited by 16
Beyond current treatment of Fanconi Anemia: What do advances in cell and gene-based approaches offer?
Martínez‐Balsalobre, E., Guervilly, J.-H., van der Wijst, J., Pérez‐Oliva, A. B., & Lachaud, C. (2023) · Blood Reviews · doi:10.1016/j.blre.2023.101094 · Cited by 14
Inhibition of fibroblast growth factor receptor-signaling sensitizes imatinib-resistant gastrointestinal stromal tumors to low doses of topoisomerase II inhibitors
Boichuk, S., Дунаев, П. Д., Galembikova, A. R., Ганиевич, М. И., & Валерьевна, В. Е. (2018) · Anti-Cancer Drugs · doi:10.1097/cad.0000000000000637 · Cited by 12
Reduced FANCD2 influences spontaneous SCE and RAD51 foci formation in uveal melanoma and Fanconi anaemia
Gravells, P., Hoh, L., Solovieva, S. E., Patil, A. A., Dudziec, E., Rennie, I. G., Sisley, K., & Bryant, H. E. (2013) · Oncogene · doi:10.1038/onc.2012.627 · Cited by 12
Caffeine Has a Synergistic Anticancer Effect with Cisplatin via Inhibiting Fanconi Anemia Group D2 Protein Monoubiquitination in Hepatocellular Carcinoma Cells
Oda, Y., Hidaka, M., & Suzuki, A. (2017) · Biological and Pharmaceutical Bulletin · doi:10.1248/bpb.b17-00457 · Cited by 12
Patient With Stage IV NSCLC and CNS Metastasis With EGFR Exon 18-25 Kinase Domain Duplication With Response to Osimertinib as a First-Line Therapy
Kim, J. T., Zhang, W., Lopategui, J. R., Vail, E., & Balmanoukian, A. S. (2021) · JCO Precision Oncology · doi:10.1200/po.20.00296 · Cited by 12
Non-homologous End-Joining Defect in Fanconi Anemia Hematopoietic Cells Exposed to Ionizing Radiation
Casado, J. A., Núñez, M. I., Segovia, J. C., de Almodóvar, J. M. R., & Bueren, J. A. (2005) · Radiation Research · doi:10.1667/rr3395.1 · Cited by 12
Research progress of the Fanconi anemia pathway and premature ovarian insufficiency
Zhao, J., Zhang, Y., Li, W., Yao, M., Liu, C., Zhang, Z., Wang, C., Wang, X., & Meng, K. (2023) · Biology of Reproduction · doi:10.1093/biolre/ioad110 · Cited by 11
“FANC proteins involved in the pathway can contribute to the homologous repair of early DNA double-strand breaks (DSBs), which is crucial for maintaining genome stability [21].”
Background
DSS1 restrains BRCA2’s engagement with dsDNA for homologous recombination, replication fork protection, and R-loop homeostasis
Huang, Y., Li, W., Foo, T. K., Ji, J., Wu, B., Tomimatsu, N., Fang, Q., Gao, B., Long, M., Xu, J., et al. (2024) · Nature Communications · doi:10.1038/s41467-024-51557-6 · Cited by 11
“We then utilized U2OS cells harboring the DR-GFP HR reporter 33,34 (Fig.”
How SUMOylation Fine-Tunes the Fanconi Anemia DNA Repair Pathway
Coleman, K. E., & Huang, T. T. (2016) · Frontiers in Genetics · doi:10.3389/fgene.2016.00061 · Cited by 11
The role of Rak in the regulation of stability and function of BRCA1
Kim, J., Ha, G., Campo, L., Denning, M. F., Patel, T. B., Osipo, C., Lin, S., & Breuer, E.-K. Y. (2015) · Oncotarget · doi:10.18632/oncotarget.5717 · Cited by 11
“PCRbased NHEJ/digest assay was carried out as described previously [50].”
Method
The role of USP 1 autocleavage in DNA interstrand crosslink repair
Kim, M., & Kim, J. M. (2016) · FEBS Letters · doi:10.1002/1873-3468.12060 · Cited by 11
The Fanconi anemia pathway is downregulated upon macrophage differentiation through two distinct mechanisms
Lu, W.-T., Lemonidis, K., Drayton, R. M., & Nouspikel, T. (2011) · Cell Cycle · doi:10.4161/cc.10.19.17178 · Cited by 10
Methylation of histone H3 lysine 36 is a barrier for therapeutic interventions of head and neck squamous cell carcinomaPreprint
Caeiro, L. D., Nakata, Y., Borges, R. L., Zha, M., Garcia-Martinez, L., Bañuelos, C. P., Stransky, S., Liu, T., Chan, H. L., Brabson, J., et al. (2024) · Genes & Development · doi:10.1101/gad.351408.123 · Cited by 11
Self-citation
Pan-Cancer Analysis of Homologous Recombination Deficiency in Cell Lines
Dodson, A. E., Shenker, S., Sullivan, P., Nayak, S. U., Middleton, C., McGuire, M. S., Chipumuro, E., Mishina, Y., Tobin, E. R., Cadzow, L., et al. (2024) · Cancer Research Communications · doi:10.1158/2767-9764.crc-24-0316 · Cited by 9
“More observations are needed to determine whether the association between HRD and CUL4B dependency is significant.”
Monoubiquitinated Fanconi anemia D2 (FANCD2-Ub) is required for BCR-ABL1 kinase-induced leukemogenesis
Koptyra, M., Stokłosa, T., Hoser, G., Głodkowska‐Mrówka, E., Seferyńska, I., Klejman, A., Błasiak, J., & Skórski, T. (2011) · Leukemia · doi:10.1038/leu.2011.91 · Cited by 9
Causes and consequences of DNA double-stranded breaks in cardiovascular disease
Marian, A. J. (2024) · Molecular and Cellular Biochemistry · doi:10.1007/s11010-024-05131-9 · Cited by 8
“The latter involves over a dozen heterodimeric proteins that participate in ubiquitinoylation of Fanconi anemia complementation group D2 (FANCD2) and homologous recombination (HR) [58].”
Whole-exome sequencing and bioinformatic analyses revealed differences in gene mutation profiles in papillary thyroid cancer patients with and without benign thyroid goitre background
Eng, Z. H., Abdullah, M. I., Ng, K. L., Aziz, A. A., Arba’ie, N. H., Rashid, N. M., & Junit, S. M. (2023) · Frontiers in Endocrinology · doi:10.3389/fendo.2022.1039494 · Cited by 8
“BRCA2 is a recombination mediator that co-localises with ubiquitinated FANCD2 and facilitates the formation of Rad51 nucleofilaments, linking the FA pathways to homologous recombination (26).”
Background
Impaired removal of DNA interstrand cross‐link in Nijmegen breakage syndrome and Fanconi anemia, but not in BRCA‐defective group
Tsuchida, K., & Komatsu, K. (2008) · Cancer Science · doi:10.1111/j.1349-7006.2008.00915.x · Cited by 8
Disruption of the fanconi anemia pathway in human cancer in the general population
Jacquemont, C. F., & Taniguchi, T. (2006) · Cancer Biology & Therapy · doi:10.4161/cbt.5.12.3658 · Cited by 8
Self-citation
Fanconi Anemia: Challenges in Diagnosis and Management—A Case Series Report
Eghbali, A., Safdari, S. M., Roozbahani, M. Y., Tavajohi, K., & Hosseini, S. (2024) · Clinical Case Reports · doi:10.1002/ccr3.9583 · Cited by 7
REV7: a small but mighty regulator of genome maintenance and cancer development
Maggs, L. R., & McVey, M. (2025) · Frontiers in Oncology · doi:10.3389/fonc.2024.1516165 · Cited by 7
Fanconi anemia associated protein 20 (FAAP20) plays an essential role in homology-directed repair of DNA double-strand breaks
Palovcak, A., Yuan, F., Verdún, R. E., Luo, L., & Zhang, Y. (2023) · Communications Biology · doi:10.1038/s42003-023-05252-9 · Cited by 6
“In canonical HR that is not coupled to ICLs FA proteins such as FANCA, FANCC and FANCD2 demonstrate a minor role 27 – 30 , yet it is still not clear how and when FA proteins are able to support HR repair.”
Influential
FANCD2 Binding to H4K20me2 via a Methyl-Binding Domain Is Essential for Efficient DNA Cross-Link Repair
Paquin, K. L., Mamrak, N. E., Garzon, J. L., Cantres-Velez, J. A., Azzinaro, P. A., Vuono, E. A., Lima, K. E., Camberg, J. L., & Howlett, N. G. (2019) · Molecular and Cellular Biology · doi:10.1128/mcb.00194-19 · Cited by 7
Cyclin-Dependent Kinase-Mediated Phosphorylation of FANCD2 Promotes Mitotic Fidelity
Cantres-Velez, J. A., Blaize, J. L., Vierra, D. A., Boisvert, R. A., Garzon, J. L., Piraino, B., Tan, W., Deans, A. J., & Howlett, N. G. (2021) · Molecular and Cellular Biology · doi:10.1128/mcb.00234-21 · Cited by 8
PARP inhibitor combinations with high-dose vitamin C in the treatment of Ewing sarcoma: two case reports and mechanistic overview
Adibi, A., Tokat, Ü. M., Özgü, E., Aydın, E., Demiray, İ., & Demiray, M. (2023) · Therapeutic Advances in Medical Oncology · doi:10.1177/17588359231213841 · Cited by 7
TALEN mediated gene editing in a mouse model of Fanconi anemia
Pino-Barrio, M. J., Gimenez, Y. A., Villanueva, M., Hildenbeutel, M., Sánchez‐Domínguez, R., Rodríguez, S., Pujol, R. M., Surrallés, J., Rı́o, P., Cathomen, T., et al. (2020) · Scientific Reports · doi:10.1038/s41598-020-63971-z · Cited by 7
DNA double-strand break repair gene mutation and the risk of papillary thyroid microcarcinoma: a case–control study
Qin, J., Fan, J., Li, G., Liu, S., Liu, Z., & Yao, W. (2021) · Cancer Cell International · doi:10.1186/s12935-021-02032-5 · Cited by 6
“The Fanconi anemia (FA) pathway is a complex network of functionally diverse proteins that is known for its role in mediating interstrand crosslink (ICL) repair [30].”
Background
Identifying the Effects of BRCA1 Mutations on Homologous Recombination using Cells that Express Endogenous Wild-type BRCA1
Parvin, J. D., Chiba, N., & Ransburgh, D. J. R. (2011) · Journal of Visualized Experiments · doi:10.3791/2468-v · Cited by 6

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
ORCID: Nakanishi, Koji
Yang, Yun-Gui
Pierce, Andrew J.
Taniguchi, Toshiyasu
Wang, Zhao-Qi
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
DOI: 10.1073/pnas.0407796102
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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Human Fanconi anemia monoubiquitination pathway promotes homologous DNA repair

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