Human HLTF functions as a ubiquitin ligase for proliferating cell nuclear antigen polyubiquitination.
Open accessAbstract
Human helicase-like transcription factor (HLTF) is frequently inactivated in colorectal and gastric cancers. Here, we show that HLTF is a functional homologue of yeast Rad5 that promotes error-free replication through DNA lesions. HLTF and Rad5 share the same unique structural features, including a RING domain embedded within a SWI/SNF helicase domain and an HIRAN domain. We find that inactivation of HLTF renders human cells sensitive to UV and other DNA-damaging agents and that HLTF complements the UV sensitivity of a rad5Delta yeast strain. Also, similar to Rad5, HLTF physically interacts with the Rad6-Rad18 and Mms2-Ubc13 ubiquitin-conjugating enzyme complexes and promotes the Lys-63-linked polyubiquitination of proliferating cell nuclear antigen at its Lys-164 residue. A requirement of HLTF for error-free postreplication repair of damaged DNA is in keeping with its cancer-suppression role.
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In template switching, monoubiquitin on PCNA K164 is further ubiquitinated by HLTF to form a K63-linked ubiquitin chain.
“In template switching, the monoubiquitin moiety added to K164 of PCNA is instead further ubiquitinated by the HLTF E3 ubiquitin ligase, to form a K63-linked ubiquitin chain (Motegi et al., 2008; Unk et al., 2008).”
From USP7 Is a Master Regulator of Genome Stability (2020) · cites this paper as Unk et al., 2008
Cites
RAD6-dependent DNA repair is linked to modification of PCNA by ubiquitin and SUMO
Hoege, C., Pfander, B., Moldovan, G., Pyrowolakis, G., & Jentsch, S. (2002) · Nature · doi:10.1038/nature00991 · Cited by 2,202 · see citing works
EUKARYOTIC TRANSLESION SYNTHESIS DNA POLYMERASES: Specificity of Structure and Function
Prakash, S., Johnson, R. E., & Prakash, L. (2005) · Annual Review of Biochemistry · doi:10.1146/annurev.biochem.74.082803.133250 · Cited by 999 · see citing works
Control of spontaneous and damage-induced mutagenesis by SUMO and ubiquitin conjugation
Stelter, P., & Ulrich, H. D. (2003) · Nature · doi:10.1038/nature01965 · Cited by 849 · see citing works
Two RING finger proteins mediate cooperation between ubiquitin‐conjugating enzymes in DNA repair
Ulrich, H. D., & Jentsch, S. (2000) · The EMBO Journal · doi:10.1093/emboj/19.13.3388 · Cited by 427 · see citing works
Bailly, V., Lamb, J., Sung, P., Prakash, S., & Prakash, L. (1994) · Genes & Development · doi:10.1101/gad.8.7.811 · Cited by 321 · see citing works
Bailly, V., Lauder, S., Prakash, S., & Prakash, L. (1997) · Journal of Biological Chemistry · doi:10.1074/jbc.272.37.23360 · Cited by 292 · see citing works
Blastyák, A., Pintér, L., Unk, I., Prakash, L., Prakash, S., & Haracska, L. (2007) · Molecular Cell · doi:10.1016/j.molcel.2007.07.030 · Cited by 285 · see citing works
Unk, I., Hajdú, I., Fátyol, K., Szakál, B., Blastyák, A., Bermudez, V. P., Hurwitz, J., Prakash, L., Prakash, S., & Haracska, L. (2006) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0608595103 · Cited by 236 · see citing works
Haracska, L., Torres‐Ramos, C. A., Johnson, R. E., Prakash, S., & Prakash, L. (2004) · Molecular and Cellular Biology · doi:10.1128/mcb.24.10.4267-4274.2004 · Cited by 201 · see citing works
Motegi, A., Sood, R. B., Moinova, H., Markowitz, S. D., Liu, P. P., & Myung, K. (2006) · The Journal of Cell Biology · doi:10.1083/jcb.200606145 · Cited by 199 · see citing works
Zhang, H., & Lawrence, C. W. (2005) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0504586102 · Cited by 185 · see citing works
HLTF gene silencing in human colon cancer
Moinova, H., Chen, W.-D. D., Shen, L., Smiraglia, D. J., Olechnowicz, J., Ravi, L., Kasturi, L., Myeroff, L. L., Plass, C., Parsons, R. E., et al. (2002) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.062459899 · Cited by 173 · see citing works
Torres‐Ramos, C. A., Prakash, S., & Prakash, L. (2002) · Molecular and Cellular Biology · doi:10.1128/mcb.22.7.2419-2426.2002 · Cited by 170 · see citing works
Haracska, L., Unk, I., Prakash, L., & Prakash, S. (2006) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0510924103 · Cited by 136 · see citing works
Lysine 63-Polyubiquitination Guards against Translesion Synthesis–Induced Mutations
Chiu, R. K., Brun, J., Ramaekers, C. H. M. A., Theys, J., Weng, L., Lambin, P., Gray, D. A., & Wouters, B. G. (2005) · PLoS Genetics · doi:10.1371/journal.pgen.0020116 · Cited by 123 · see citing works
Gangavarapu, V., Haracska, L., Unk, I., Johnson, R. E., Prakash, S., & Prakash, L. (2006) · Molecular and Cellular Biology · doi:10.1128/mcb.01260-06 · Cited by 114 · see citing works
The HIRAN Domain and Recruitment of Chromatin Remodeling and Repair activities to Damaged DNA
Iyer, L. M., Babu, M. M., & Aravind, L. (2006) · Cell Cycle · doi:10.4161/cc.5.7.2629 · Cited by 96 · see citing works
Li, Z., Xiao, W., McCormick, J. J., & Maher, V. M. (2002) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.062047799 · Cited by 77 · see citing works
The role of DNA polymerase η in UV mutational spectra
Choi, J., & Pfeifer, G. P. (2004) · DNA repair · doi:10.1016/j.dnarep.2004.09.006 · Cited by 68 · see citing works
Hayward-Lester, A., Hewetson, A., BEALE, E. G., Oefner, P. J., Doris, P. A., & Chilton, B. S. (1996) · Molecular Endocrinology · doi:10.1210/mend.10.11.8923460 · Cited by 58 · see citing works
Sheridan, P. L., Schorpp, M., Voz, M. L., & Jones, K. A. (1995) · Journal of Biological Chemistry · doi:10.1074/jbc.270.9.4575 · Cited by 57 · see citing works
Methylation pattern of HLTF gene in digestive tract cancers
Hibi, K., Nakayama, H., Kanyama, Y., Kodera, Y., Ito, K., Akiyama, S., & Nakao, A. (2003) · International Journal of Cancer · doi:10.1002/ijc.10985 · Cited by 52 · see citing works
Ding, H., Descheemaeker, K. A., Marynen, P., Nelles, L., Carvalho, T., Carmo‐Fonseca, M., Collen, D., & Belayew, A. (1996) · DNA and Cell Biology · doi:10.1089/dna.1996.15.429 · Cited by 49 · see citing works
Developmental Regulation of Zbu1, a DNA-Binding Member of the SWI2/SNF2 Family
Gong, X., Kaushal, S., Ceccarelli, E., Bogdanova, N., Neville, C. M., Nguyen, T. P., Clark, H., Khatib, Z. A., Valentine, M. B., Look, A. T., et al. (1997) · Developmental Biology · doi:10.1006/dbio.1996.8486 · Cited by 46 · see citing works
Hamai, Y., Oue, N., Mitani, Y., Nakayama, H., Ito, R., Matsusaki, K., Yoshida, K., Toge, T., & Yasui, W. (2003) · Cancer Science · doi:10.1111/j.1349-7006.2003.tb01504.x · Cited by 39 · see citing works
Molecular cloning and characterization of P113, a mouse SNF2/SWI2-related transcription factor
Zhang, Q., Ekhterae, D., & Kim, K.-H. (1997) · Gene · doi:10.1016/s0378-1119(97)00446-0 · Cited by 26 · see citing works
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Kile, A. C., Chavez, D., Bacal, J., Eldirany, S. A., Korzhnev, D. M., Bezsonova, I., Eichman, B. F., & Cimprich, K. A. (2015) · Molecular Cell · doi:10.1016/j.molcel.2015.05.013 · Cited by 201 · see citing works
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Kang, M.-S., Ryu, E., Lee, S.-W., Park, J., Ha, N. Y., Ra, J. S., Kim, Y. J., Kim, J., Abdel‐Rahman, M. H., Park, S. H., et al. (2019) · Nature Communications · doi:10.1038/s41467-019-10376-w · Cited by 111 · see citing works
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Cazzalini, O., Sommatis, S., Tillhon, M., Dutto, I., Bachi, A., Rapp, A. W., Nardò, T., Scovassi, A. I., Necchi, D., Cardoso, M. C., et al. (2014) · Nucleic Acids Research · doi:10.1093/nar/gku533 · Cited by 106 · see citing works
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Parker, J. L., & Ulrich, H. D. (2009) · The EMBO Journal · doi:10.1038/emboj.2009.303 · Cited by 106 · see citing works
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Lahouassa, H., Blondot, M.-L., Chauveau, L., Chougui, G., Morel, M., Leduc, M., Guillonneau, F., Ramírez, B. C., Schwartz, O., & Margottin-Goguet, F. (2016) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1600485113 · Cited by 100 · see citing works
Ubiquitin-independent proteasomal degradation driven by C-degron pathways
Makaros, Y., Raiff, A., Timms, R. T., Wagh, A. R., Israel-Gueta, M., Bekturova, A., Guez-Haddad, J., Brodsky, S., Opatowsky, Y., Glickman, M. H., et al. (2023) · Molecular Cell · doi:10.1016/j.molcel.2023.04.023 · Cited by 101 · see citing works
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Jansen, J. G., Tsaalbi-Shtylik, A., Hendriks, G., Gali, H., Hendel, A., Johansson, F., Erixon, K., Livneh, Z., Mullenders, L. H. F., Haracska, L., et al. (2009) · Molecular and Cellular Biology · doi:10.1128/mcb.00071-09 · Cited by 99 · see citing works
Self-citationMechanisms of DNA Damage Tolerance: Post-Translational Regulation of PCNA
Leung, W., Baxley, R. M., Moldovan, G., & Bielinsky, A. (2018) · Genes · doi:10.3390/genes10010010 · Cited by 96 · see citing works
Juhász, S., Balogh, D., Hajdú, I., Burkovics, P., Villamil, M. A., Zhuang, Z., & Haracska, L. (2012) · Nucleic Acids Research · doi:10.1093/nar/gks850 · Cited by 95 · see citing works
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Hodge, C. D., Spyracopoulos, L., & Glover, J. N. M. (2016) · Oncotarget · doi:10.18632/oncotarget.10948 · Cited by 93 · see citing works
Mórocz, M., Zsigmond, E., Tóth, R., Enyedi, M. Z., Pintér, L., & Haracska, L. (2016) · Nucleic Acids Research · doi:10.1093/nar/gkw1315 · Cited by 93 · see citing works
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Slade, D. (2018) · Genes · doi:10.3390/genes9080416 · Cited by 89 · see citing works
Chromatin context-dependent regulation and epigenetic manipulation of prime editing
Li, X., Chen, W., Martin, B., Calderon, D., Lee, C., Choi, J., Chardon, F. M., McDiarmid, T. A., Daza, R. M., Kim, H., et al. (2024) · Cell · doi:10.1016/j.cell.2024.03.020 · Cited by 90 · see citing works
Zhang, S., Chea, J., Xiao, M., Zhou, Y., Lee, E. Y. C., & Lee, M. (2008) · Cell Cycle · doi:10.4161/cc.7.21.6949 · Cited by 85 · see citing works
Coordinated protein and DNA remodeling by human HLTF on stalled replication fork
Achar, Y. J., Balogh, D., & Haracska, L. (2011) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1101951108 · Cited by 80 · see citing works
The ubiquitin ligase RFWD3 is required for translesion DNA synthesis
Gallina, I., Hendriks, I. A., Hoffmann, S., Larsen, N. B., Johansen, J., Colding-Christensen, C. S., Schubert, L. A., Sellés‐Baiget, S., Fábián, Z., Kühbacher, U., et al. (2020) · Molecular Cell · doi:10.1016/j.molcel.2020.11.029 · Cited by 76 · see citing works
Roles of sequential ubiquitination of PCNA in DNA‐damage tolerance
Zhang, W., Qin, Z., Zhang, X., & Xiao, W. (2011) · FEBS Letters · doi:10.1016/j.febslet.2011.04.044 · Cited by 78 · see citing works
Haynes, B. M., Saadat, N., Myung, B., & Shekhar, M. P. V. (2014) · Mutation Research/Reviews in Mutation Research · doi:10.1016/j.mrrev.2014.11.005 · Cited by 77 · see citing works
The Emerging Role of Cohesin in the DNA Damage Response
Litwin, I., Pilarczyk, E., & Wysocki, R. (2018) · Genes · doi:10.3390/genes9120581 · Cited by 74 · see citing works
Proteasome‐independent functions of lysine‐63 polyubiquitination in plants
Romero-Barrios, N., & Vert, G. (2017) · New Phytologist · doi:10.1111/nph.14915 · Cited by 76 · see citing works
Timing and spacing of ubiquitin‐dependent DNA damage bypass
Ulrich, H. D. (2011) · FEBS Letters · doi:10.1016/j.febslet.2011.05.028 · Cited by 73 · see citing works
Roles of trans-lesion synthesis (TLS) DNA polymerases in tumorigenesis and cancer therapy
Anand, J. R., Chiou, L. F., Sciandra, C. A., Zhang, X., Hong, J., Wu, D., Zhou, P., & Vaziri, C. (2023) · NAR Cancer · doi:10.1093/narcan/zcad005 · Cited by 73 · see citing works
Achar, Y. J., Balogh, D., Neculai, D., Juhász, S., Mórocz, M., Gali, H., Dhe‐Paganon, S., Venclovas, Č., & Haracska, L. (2015) · Nucleic Acids Research · doi:10.1093/nar/gkv896 · Cited by 72 · see citing works
Hishiki, A., Hara, K., Ikegaya, Y., Yokoyama, H., Shimizu, T., Sato, M., & Hashimoto, H. (2015) · Journal of Biological Chemistry · doi:10.1074/jbc.m115.643643 · Cited by 71 · see citing works
The emerging determinants of replication fork stability
Thakar, T., & Moldovan, G. (2021) · Nucleic Acids Research · doi:10.1093/nar/gkab344 · Cited by 69 · see citing works
Szüts, D., Marcus, A. P., Himoto, M., Iwai, S., & Sale, J. E. (2008) · Nucleic Acids Research · doi:10.1093/nar/gkn651 · Cited by 67 · see citing works
Masuda, Y., Kanao, R., Kaji, K., Ohmori, H., Hanaoka, F., & Masutani, C. (2015) · Nucleic Acids Research · doi:10.1093/nar/gkv712 · Cited by 67 · see citing works
Making choices: DNA replication fork recovery mechanisms
Kondratick, C. M., Washington, M. T., & Spies, M. (2020) · Seminars in Cell and Developmental Biology · doi:10.1016/j.semcdb.2020.10.001 · Cited by 66 · see citing works
Mammalian polymerase ζ is essential for post-replication repair of UV-induced DNA lesions
Jansen, J. G., Tsaalbi‐Shtylik, A., Hendriks, G., Verspuy, J. W. A., Gali, H., Haracska, L., & de Wind, N. (2009) · DNA repair · doi:10.1016/j.dnarep.2009.09.006 · Cited by 63 · see citing works
Krijger, P. H. L., Lee, K., Wit, N., van den Berk, P. C. M., Wu, X., Roest, H. P., Maas, A., Ding, H., Hoeijmakers, J. H. J., Myung, K., et al. (2011) · DNA repair · doi:10.1016/j.dnarep.2010.12.008 · Cited by 63 · see citing works
Strand invasion by HLTF as a mechanism for template switch in fork rescue
Burkovics, P., Šebesta, M., Balogh, D., Haracska, L., & Krejčí, L. (2013) · Nucleic Acids Research · doi:10.1093/nar/gkt1040 · Cited by 62 · see citing works
Regulation of DNA damage tolerance in mammalian cells by post-translational modifications of PCNA
Kanao, R., & Masutani, C. (2017) · Mutation research. Fundamental and molecular mechanisms of mutagenesis · doi:10.1016/j.mrfmmm.2017.06.004 · Cited by 61 · see citing works
Translesion DNA synthesis in the context of cancer research
Knobel, P. A., & Marti, T. M. (2011) · Cancer Cell International · doi:10.1186/1475-2867-11-39 · Cited by 59 · see citing works
Masuda, Y., SUZUKI, M. T., Kawai, H., Hishiki, A., Hashimoto, H., Masutani, C., Hishida, T., Suzuki, F., & Kamiya, K. (2012) · Nucleic Acids Research · doi:10.1093/nar/gks763 · Cited by 59 · see citing works
Mechanisms of Post-Replication DNA Repair
Gao, Y., Mutter‐Rottmayer, E., Zlatanou, A., Vaziri, C., & Yang, Y. (2017) · Genes · doi:10.3390/genes8020064 · Cited by 55 · see citing works
Chavez, D., Greer, B. H., & Eichman, B. F. (2018) · Journal of Biological Chemistry · doi:10.1074/jbc.ra118.002905 · Cited by 53 · see citing works
Methylation of UHRF1 by SET7 is essential for DNA double-strand break repair
Hahm, J. Y., Kim, J., Park, J. W., Kang, J., Kim, K., Kim, S.-R., Cho, H., & Seo, S. (2018) · Nucleic Acids Research · doi:10.1093/nar/gky975 · Cited by 54 · see citing works
Dynamic regulation of PCNA ubiquitylation/deubiquitylation
Fox, J. T., Lee, K., & Myung, K. (2011) · FEBS Letters · doi:10.1016/j.febslet.2011.05.053 · Cited by 52 · see citing works
Ubiquitination of PCNA and Its Essential Role in Eukaryotic Translesion Synthesis
Chen, J., Bozza, W. P., & Zhuang, Z. (2011) · Cell Biochemistry and Biophysics · doi:10.1007/s12013-011-9187-3 · Cited by 52 · see citing works
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Huang, A., Hibbert, R. G., de Jong, R. N., Das, D., Sixma, T. K., & Boelens, R. (2011) · Journal of Molecular Biology · doi:10.1016/j.jmb.2011.04.051 · Cited by 48 · see citing works
Porro, A., Berti, M., Pizzolato, J., Bologna, S., Kaden, S., Saxer, A., Ma, Y., Nagasawa, K., Sartori, A. A., & Jiricny, J. (2017) · Nature Communications · doi:10.1038/s41467-017-01074-6 · Cited by 47 · see citing works
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Lee, K., & Park, S. H. (2020) · Experimental & Molecular Medicine · doi:10.1038/s12276-020-00533-3 · Cited by 48 · see citing works
Ho, Y.-K., Zhi, H., Bowlin, T., Dorjbal, B., Philip, S., Zahoor, M. A., Shih, H., Semmes, O. J., Schaefer, B. C., Glover, J. N. M., et al. (2015) · PLoS Pathogens · doi:10.1371/journal.ppat.1005102 · Cited by 47 · see citing works
Tian, F., Sharma, S., Zou, J., Lin, S., Wang, B., Rezvani, K. S., Wang, H., Parvin, J. D., Ludwig, T., Canman, C. E., et al. (2013) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1306534110 · Cited by 47 · see citing works
Loss of HLTF function promotes intestinal carcinogenesis
Sandhu, S., Wu, X., Nabi, Z., Rastegar, M., Kung, S. K. P., Mai, S., & Ding, H. (2012) · Molecular Cancer · doi:10.1186/1476-4598-11-18 · Cited by 46 · see citing works
Time for remodeling: SNF2-family DNA translocases in replication fork metabolism and human disease
Joseph, S. A., Taglialatela, A., Leuzzi, G., Huang, J., Cuella-Martin, R., & Ciccia, A. (2020) · DNA repair · doi:10.1016/j.dnarep.2020.102943 · Cited by 47 · see citing works
Active DNA damage eviction by HLTF stimulates nucleotide excision repair
van Toorn, M., der Velden, Y. T.-V., Han, S., Zhou, D., Kim, H.-S., Salas‐Armenteros, I., Kim, M., Akita, M., Wienholz, F., Raams, A., et al. (2022) · Molecular Cell · doi:10.1016/j.molcel.2022.02.020 · Cited by 41 · see citing works
Control of histone methylation and genome stability by PTIP
Munoz, I. M., & Rouse, J. W. (2009) · EMBO Reports · doi:10.1038/embor.2009.21 · Cited by 44 · see citing works
Burkovics, P., Dome, L., Juhász, S., Altmannová, V., Šebesta, M., Pačesa, M., Fugger, K., Sørensen, C. S., Lee, M., Haracska, L., et al. (2016) · Nucleic Acids Research · doi:10.1093/nar/gkw024 · Cited by 44 · see citing works
SIVA1 directs the E3 ubiquitin ligase RAD18 for PCNA monoubiquitination
Han, J., Liu, T., Huen, M. S. Y., Hu, L. T., Chen, Z., & Huang, J. (2014) · The Journal of Cell Biology · doi:10.1083/jcb.201311007 · Cited by 44 · see citing works
Translesion Synthesis Polymerases in the Prevention and Promotion of Carcinogenesis
Stallons, L. J., & McGregor, W. G. (2010) · Journal of Nucleic Acids · doi:10.4061/2010/643857 · Cited by 44 · see citing works
Dhont, L., Mascaux, C., & Belayew, A. (2015) · Cellular and Molecular Life Sciences · doi:10.1007/s00018-015-2060-6 · Cited by 44 · see citing works
Waraky, A., Lin, Y., Warsito, D., Haglund, F., Aleem, E. A., & Larsson, O. (2017) · Journal of Biological Chemistry · doi:10.1074/jbc.m117.781492 · Cited by 43 · see citing works
Masuda, Y., SUZUKI, M. T., Kawai, H., Suzuki, F., & Kamiya, K. (2011) · Nucleic Acids Research · doi:10.1093/nar/gkr805 · Cited by 42 · see citing works
HIV-1 Vpr counteracts HLTF-mediated restriction of HIV-1 infection in T cells
Yan, J., Shun, M.-C., Zhang, Y., Hao, C., & Skowroński, J. (2019) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1818401116 · Cited by 43 · see citing works
DNA-damage tolerance through PCNA ubiquitination and sumoylation
Fan, L., Bi, T., Wang, L., & Xiao, W. (2020) · Biochemical Journal · doi:10.1042/bcj20190579 · Cited by 40 · see citing works
Wong, R. P. C., Petriukov, K. S., & Ulrich, H. D. (2021) · DNA repair · doi:10.1016/j.dnarep.2021.103163 · Cited by 40 · see citing works
McIntyre, J., & Woodgate, R. (2015) · DNA repair · doi:10.1016/j.dnarep.2015.02.011 · Cited by 40 · see citing works
Ubiquitin‐family modifications in the replication of DNA damage
Lehmann, A. R. (2011) · FEBS Letters · doi:10.1016/j.febslet.2011.06.005 · Cited by 40 · see citing works
Polymerase Stalling during Replication, Transcription and Translation
Edenberg, E. R., Downey, M., & Toczyski, D. P. (2014) · Current Biology · doi:10.1016/j.cub.2014.03.060 · Cited by 40 · see citing works
Biochemical characterisation of the SWI/SNF family member HLTF
MacKay, C., Toth, R. L., & Rouse, J. W. (2009) · Biochemical and Biophysical Research Communications · doi:10.1016/j.bbrc.2009.08.151 · Cited by 39 · see citing works
The Rev1-Polζ translesion synthesis mutasome: Structure, interactions and inhibition
Rizzo, A. A., & Korzhnev, D. M. (2019) · The Enzymes · doi:10.1016/bs.enz.2019.07.001 · Cited by 39 · see citing works
DNA Replication-Coupled PCNA Mono-Ubiquitination and Polymerase Switching in a Human In Vitro System
Masuda, Y., Piao, J., & Kamiya, K. (2010) · Journal of Molecular Biology · doi:10.1016/j.jmb.2010.01.003 · Cited by 39 · see citing works
PCNA cycling dynamics during DNA replication and repair in mammals
Kang, S., Yoo, J., & Myung, K. (2024) · Trends in Genetics · doi:10.1016/j.tig.2024.02.006 · Cited by 38 · see citing works
Tonzi, P., & Huang, T. T. (2019) · DNA repair · doi:10.1016/j.dnarep.2019.03.016 · Cited by 36 · see citing works
Rad5-dependent DNA Repair Functions of the Saccharomyces cerevisiae FANCM Protein Homolog Mph1
Daee, D. L., Ferrari, E., Longerich, S., Zheng, X.-F., Xue, X., Branzei, D., Sung, P., & Myung, K. (2012) · Journal of Biological Chemistry · doi:10.1074/jbc.m112.369918 · Cited by 36 · see citing works
E3 ubiquitin ligase HECW2 targets PCNA and lamin B1
Krishnamoorthy, V., Khanna, R., & Parnaik, V. K. (2018) · Biochimica et Biophysica Acta (BBA) - Molecular Cell Research · doi:10.1016/j.bbamcr.2018.05.008 · Cited by 35 · see citing works
Regulation of translesion DNA synthesis in mammalian cells
Ma, X., Tang, T., & Guo, C. (2020) · Environmental and Molecular Mutagenesis · doi:10.1002/em.22359 · Cited by 37 · see citing works
DNA damage-specific deubiquitination regulates Rad18 functions to suppress mutagenesis
Zeman, M. K., Lin, J., Freire, R., & Cimprich, K. A. (2014) · The Journal of Cell Biology · doi:10.1083/jcb.201311063 · Cited by 36 · see citing works
USP7 regulates the stability and function of HLTF through deubiquitination.
Qing, P., Han, L., Bin, L., Yan, L., & Ping, W. X. (2011) · Journal of Cellular Biochemistry · doi:10.1002/jcb.23317 · Cited by 35 · see citing works
Ubiquitin and SUMO signalling in DNA repair
Thomson, T. M., & Guerra‐Rebollo, M. (2010) · Biochemical Society Transactions · doi:10.1042/bst0380116 · Cited by 34 · see citing works
The Regulation of DNA Damage Tolerance by Ubiquitin and Ubiquitin-Like Modifiers
Cipolla, L., Maffia, A., Bertoletti, F., & Sabbioneda, S. (2016) · Frontiers in Genetics · doi:10.3389/fgene.2016.00105 · Cited by 34 · see citing works
HLTF resolves G4s and promotes G4-induced replication fork slowing to maintain genome stability
Bai, G., Endres, T., Kühbacher, U., Mengoli, V., Greer, B. H., Peacock, E. M., Newton, M. D., Stanage, T. H., Stritto, M. R. D., Lungu, R., et al. (2024) · Molecular Cell · doi:10.1016/j.molcel.2024.07.018 · Cited by 34 · see citing works
Regulatory Role of Ubiquitin in Eukaryotic DNA Translesion Synthesis
Yang, K., Weinacht, C. P., & Zhuang, Z. (2013) · Biochemistry · doi:10.1021/bi400194r · Cited by 33 · see citing works
Aberrant DNA replication in cancer
Suzuki, M., & Takahashi, T. (2012) · Mutation research. Fundamental and molecular mechanisms of mutagenesis · doi:10.1016/j.mrfmmm.2012.07.003 · Cited by 32 · see citing works
Mórocz, M., Gali, H., Raskó, I., Downes, C. S., & Haracska, L. (2013) · PLoS ONE · doi:10.1371/journal.pone.0070391 · Cited by 31 · see citing works
Capouillez, A., Debauve, G., Decaestecker, C., Filleul, O., Chevalier, D., Mortuaire, G., Coppée, F., Leroy, X., Belayew, A., & Saussez, S. (2009) · Histopathology · doi:10.1111/j.1365-2559.2009.03330.x · Cited by 31 · see citing works
- Authors
- Unk, I., Hajdú, I., Fátyol, K., Hurwitz, J., Yoon, J.-H., Prakash, L., Prakash, S., & Haracska, L.
- Affiliations
- *Institute of Genetics, Biological Research Center, Hungarian Academy of Sciences, Temesvari Körút 62, H-6726, Szeged, Hungary;
- HUN-REN Szegedi Biológiai Kutatóközpont (HU)
- Memorial Sloan Kettering Cancer Center (US)
- The University of Texas Medical Branch at Galveston (US)
- Venue
- Proceedings of the National Academy of Sciences
- Publisher
- National Academy of Sciences
- Published
- 2008-03-11
- Volume
- 105
- Issue
- 10
- Pages
- 3768-3773
- ISSN
- 0027-8424 (ISSN-L)
- 1091-6490
- PMC
- PMC2268824
- OpenAlex
- W2073294832
- Cited by
- 250
- References
- 26
- Citations by year
- 2026: 7 · 2025: 11 · 2024: 15 · 2023: 14 · 2022: 14 · 2021: 11 · 2020: 17 · 2019: 17 · 2018: 13 · 2017: 17 · 2016: 16 · 2015: 12 · 2014: 9 · 2013: 10 · 2012: 15
- FWCI
- 7.12
- 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
- Howard Hughes Medical Institute (55005612)
- Wellcome Trust
- Hungarian Scientific Research Fund
- Nemzeti Kutatási és Technológiai Hivatal
- Hungarian Science Foundation
- National Institutes of Health
- Medical Research Council
- National Cancer Institute (T32CA117834)
- National Institute of Environmental Health Sciences (R01ES012411, ES 012411)
- Topics
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › DNA Repair Mechanisms
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Ubiquitin and proteasome pathways
- Health Sciences › Medicine › Oncology › Cancer-related Molecular Pathways
- Keywords
- HLTF, Rad5, ubiquitin ligase, postreplication repair, DNA damage response, UV sensitivity, RING domain, tumor suppression, colorectal cancer, gastric cancer
- MeSH terms
- Adenosine Triphosphatases, Cell Line, DNA Helicases, DNA-Binding Proteins, Drug Resistance, Genetic Complementation Test, Humans, Ligases, Lysine, Methyl Methanesulfonate, Mutation, Protein Binding, Saccharomyces cerevisiae, Transcription Factors, Ultraviolet Rays, Proliferating Cell Nuclear Antigen, Polyubiquitin, Saccharomyces cerevisiae Proteins, Ubiquitin-Conjugating Enzymes, Ubiquitin-Protein Ligases, Ubiquitination
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