Cullin 4A-mediated proteolysis of DDB2 protein at DNA damage sites regulates in vivo lesion recognition by XPC
Open accessAbstract
Xeroderma pigmentosum (XP) complementation group E gene product, damaged DNA-binding protein 2 (DDB2), is a subunit of the DDB heterodimeric protein complex with high specificity for binding to a variety of DNA helix-distorting lesions. DDB is believed to play a role in the initial step of damage recognition in mammalian nucleotide excision repair (NER) of ultraviolet light (UV)-induced photolesions. It has been shown that DDB2 is rapidly degraded after cellular UV irradiation. However, the relevance of DDB2 degradation to its functionality in NER is still unknown. Here, we have provided evidence that Cullin 4A (CUL-4A), a key component of CUL-4A-based ubiquitin ligase, mediates DDB2 degradation at the damage sites and regulates the recruitment of XPC and the repair of cyclobutane pyrimidine dimers. We have shown that CUL-4A can be identified in a UV-responsive protein complex containing both DDB subunits. CUL-4A was visualized in localized UV-irradiated sites together with DDB2 and XPC. Degradation of DDB2 could be blocked by silencing CUL-4A using small interference RNA or by treating cells with proteasome inhibitor MG132. This blockage resulted in prolonged retention of DDB2 at the subnuclear DNA damage foci within micropore irradiated cells. Knock down of CUL-4A also decreased recruitment of the damage recognition factor, XPC, to the damaged foci and concomitantly reduced the removal of cyclobutane pyrimidine dimers from the entire genome. These results suggest that CUL-4A mediates the proteolytic degradation of DDB2 and that this degradation event, initiated at the lesion sites, regulates damage recognition by XPC during the early steps of NER.
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DDB2 localizes to UV-induced DNA lesions.
“DDB2 is localized at the UV-induced DNA lesions, where its ubiquitination and subsequent degradation seems to control XPC recruitment and damage recognition, thus triggering the NER process [104].”
From Mind the gap: keeping UV lesions in check (2011) · cites this paper as [104]
Ubiquitination and degradation of DDB2 appear to control XPC recruitment and damage recognition, thereby triggering NER.
“DDB2 is localized at the UV-induced DNA lesions, where its ubiquitination and subsequent degradation seems to control XPC recruitment and damage recognition, thus triggering the NER process [104].”
From Mind the gap: keeping UV lesions in check (2011) · cites this paper as [104]
Cites
The Ubiquitin-Proteasome Proteolytic Pathway: Destruction for the Sake of Construction
Glickman, M. H., & Ciechanover, A. J. (2002) · Physiological Reviews · doi:10.1152/physrev.00027.2001 · Cited by 4,216 · see citing works
Genome maintenance mechanisms for preventing cancer
Hoeijmakers, J. H. J. (2001) · Nature · doi:10.1038/35077232 · Cited by 3,939 · see citing works
SCF and Cullin/RING H2-Based Ubiquitin Ligases
Deshaies, R. J. (1999) · Annual Review of Cell and Developmental Biology · doi:10.1146/annurev.cellbio.15.1.435 · Cited by 1,238 · see citing works
Molecular mechanism of nucleotide excision repair
de Laat, W. L., Jaspers, N. G. J., & Hoeijmakers, J. H. J. (1999) · Genes & Development · doi:10.1101/gad.13.7.768 · Cited by 1,122 · see citing works
Sugasawa, K., Ng, J. M. Y., Masutani, C., Iwai, S., van der Spek, P. J., Eker, A. P. M., Hanaoka, F., Bootsma, D., & Hoeijmakers, J. H. J. (1998) · Molecular Cell · doi:10.1016/s1097-2765(00)80132-x · Cited by 899 · see citing works
Mammalian DNA nucleotide excision repair reconstituted with purified protein components
Aboussekhra, A., Biggerstaff, M., Shivji, M. K. K., Vilpo, J. A., Moncollin, V., Podust, V. N., Protić, M., Hübscher, U., Egly, J.-M., & Wood, R. D. (1995) · Cell · doi:10.1016/0092-8674(95)90289-9 · Cited by 837 · see citing works
Sequential Assembly of the Nucleotide Excision Repair Factors In Vivo
Volker, M., Moné, M. J., Karmakar, P., van Hoffen, A., Schul, W., Vermeulen, W., Hoeijmakers, J. H. J., DRIEL, R. V., van Zeeland, A. A., & Mullenders, L. H. F. (2001) · Molecular Cell · doi:10.1016/s1097-2765(01)00281-7 · Cited by 782 · see citing works
Kipreos, E. T., & Pagano, M. (2000) · Genome biology · doi:10.1186/gb-2000-1-5-reviews3002 · Cited by 743 · see citing works
Groisman, R., Polanowska, J., Kuraoka, I., Sawada, J.-I., Saijo, M., Drapkin, R., Kisselev, A. F., Tanaka, K., & Nakatani, Y. (2003) · Cell · doi:10.1016/s0092-8674(03)00316-7 · Cited by 739 · see citing works
Hwang, B. J., Ford, J. M., Hanawalt, P. C., & Chu, G. (1999) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.96.2.424 · Cited by 581 · see citing works
UV-Induced Ubiquitylation of XPC Protein Mediated by UV-DDB-Ubiquitin Ligase Complex
Sugasawa, K., Okuda, Y., Saijo, M., Nishi, R., Matsuda, N., Chu, G., Mori, T., Iwai, S., Tanaka, K., Tanaka, K., et al. (2005) · Cell · doi:10.1016/j.cell.2005.02.035 · Cited by 576 · see citing works
Reconstitution of Human DNA Repair Excision Nuclease in a Highly Defined System
Mu, D., Park, C.-H., Matsunaga, T., Hsu, D. S., Reardon, J. T., & Sancar, A. (1995) · Journal of Biological Chemistry · doi:10.1074/jbc.270.6.2415 · Cited by 476 · see citing works
The comings and goings of nucleotide excision repair factors on damaged DNA
Riedl, T., Hanaoka, F., & Egly, J. (2003) · The EMBO Journal · doi:10.1093/emboj/cdg489 · Cited by 439 · see citing works
Xeroderma Pigmentosum Group E Cells Lack a Nuclear Factor That Binds to Damaged DNA
Chu, G., & Chang, E. (1988) · Science · doi:10.1126/science.3175673 · Cited by 422 · see citing works
Masutani, C., Sugasawa, K., Yanagisawa, J., Sonoyama, T., Ui, M., Enomoto, T., Takio, K., Tanaka, K., van der Spek, P. J., & Bootsma, D. (1994) · The EMBO Journal · doi:10.1002/j.1460-2075.1994.tb06452.x · Cited by 400 · see citing works
Xeroderma Pigmentosum p48 Gene Enhances Global Genomic Repair and Suppresses UV-Induced Mutagenesis
Tang, J. Y., Hwang, B. J., Ford, J. M., Hanawalt, P. C., & Chu, G. (2000) · Molecular Cell · doi:10.1016/s1097-2765(00)80252-x · Cited by 335 · see citing works
Araújo, S. J., Tirode, F., Coin, F., Pospiech, H., Syväoja, J. E., Stucki, M., Hübscher, U., Egly, J., & Wood, R. D. (2000) · Genes & Development · doi:10.1101/gad.14.3.349 · Cited by 334 · see citing works
Venema, J., van Hoffen, A., Karcagi, V., Natarajan, A. T., van Zeeland, A. A., & Mullenders, L. H. F. (1991) · Molecular and Cellular Biology · doi:10.1128/mcb.11.8.4128 · Cited by 317 · see citing works
In vivo recruitment of XPC to UV-induced cyclobutane pyrimidine dimers by the DDB2 gene product
Fitch, M. E., Nakajima, S., Yasui, A., & Ford, J. M. (2003) · Journal of Biological Chemistry · doi:10.1074/jbc.m307254200 · Cited by 260 · see citing works
Nucleotide excision repair: From E. coli to man
Petit, C. R., & Sancar, A. (1999) · Biochimie · doi:10.1016/s0300-9084(99)80034-0 · Cited by 230 · see citing works
Wakasugi, M., Kawashima, A., Morioka, H., Linn, S., Sancar, A., Mori, T., Nikaido, O., & Matsunaga, T. (2002) · Journal of Biological Chemistry · doi:10.1074/jbc.c100610200 · Cited by 227 · see citing works
Characterization of a human DNA damage binding protein implicated in xeroderma pigmentosum E.
Keeney, S., Chang, G. J., & Linn, S. (1993) · Journal of Biological Chemistry · doi:10.1016/s0021-9258(19)36923-6 · Cited by 213 · see citing works
Reardon, J. T., Nichols, A. F., Keeney, S., Smith, C. A., Taylor, J., Linn, S., & Sancar, A. (1993) · Journal of Biological Chemistry · doi:10.1016/s0021-9258(19)36924-8 · Cited by 208 · see citing works
Batty, D. P., Rapić-Otrin, V., Levine, A. S., & Wood, R. D. (2000) · Journal of Molecular Biology · doi:10.1006/jmbi.2000.3857 · Cited by 208 · see citing works
The COP9 signalosome: an assembly and maintenance platform for cullin ubiquitin ligases?
Wolf, D. A., Zhou, C., & Wee, S. (2003) · Nature Cell Biology · doi:10.1038/ncb1203-1029 · Cited by 191 · see citing works
Sugasawa, K., Shimizu, Y., Iwai, S., & Hanaoka, F. (2002) · DNA repair · doi:10.1016/s1568-7864(01)00008-8 · Cited by 186 · see citing works
Moser, J., Volker, M., Kool, H., Alekseev, S., Vrieling, H., Yasui, A., van Zeeland, A. A., & Mullenders, L. H. F. (2005) · DNA Repair · doi:10.1016/j.dnarep.2005.01.001 · Cited by 182 · see citing works
Characterization of DNA Recognition by the Human UV-damaged DNA-binding Protein
Fujiwara, Y., Masutani, C., Mizukoshi, T., Kondo, J., Hanaoka, F., & Iwai, S. (1999) · Journal of Biological Chemistry · doi:10.1074/jbc.274.28.20027 · Cited by 173 · see citing works
Rapić-Otrin, V. (2002) · Nucleic Acids Research · doi:10.1093/nar/30.11.2588 · Cited by 171 · see citing works
Nag, A., Bondar, T., Shiv, S., & Raychaudhuri, P. (2001) · Molecular and Cellular Biology · doi:10.1128/mcb.21.20.6738-6747.2001 · Cited by 160 · see citing works
DNA repair factor XPC is modified by SUMO-1 and ubiquitin following UV irradiation.
Wang, Q.-E. (2005) · Nucleic Acids Research · doi:10.1093/nar/gki684 · Cited by 160 · see citing works
Cullin 4A Associates with the UV-damaged DNA-binding Protein DDB
Shiyanov, P. A., Nag, A., & Raychaudhuri, P. (1999) · Journal of Biological Chemistry · doi:10.1074/jbc.274.50.35309 · Cited by 159 · see citing works
Wittschieben, B. Ø., Iwai, S., & Wood, R. D. (2005) · Journal of Biological Chemistry · doi:10.1074/jbc.m507854200 · Cited by 159 · see citing works
Hwang, B. J., Peters, S. T., Francke, U., & Chu, G. (1998) · Molecular and Cellular Biology · doi:10.1128/mcb.18.7.4391 · Cited by 158 · see citing works
Mutations Specific to the Xeroderma Pigmentosum Group E Ddb− Phenotype
Nichols, A. F., Ong, P., & Linn, S. (1996) · Journal of Biological Chemistry · doi:10.1074/jbc.271.40.24317 · Cited by 151 · see citing works
UV-damaged DNA-binding Proteins Are Targets of CUL-4A-mediated Ubiquitination and Degradation
Chen, X., Zhang, Y., Douglas, L. C., & Zhou, P. (2001) · Journal of Biological Chemistry · doi:10.1074/jbc.m106808200 · Cited by 149 · see citing works
Human Damage-specific DNA-binding Protein p48
Nichols, A. F., Itoh, T., Graham, J. A., Liu, W., Yamaizumi, M., & Linn, S. (2000) · Journal of Biological Chemistry · doi:10.1074/jbc.m000960200 · Cited by 137 · see citing works
Rapic-Otrin, V. (2003) · Human Molecular Genetics · doi:10.1093/hmg/ddg174 · Cited by 113 · see citing works
Wang, Q.-E., Zhu, Q., Wani, G., Chen, J., & Wani, A. A. (2004) · Carcinogenesis · doi:10.1093/carcin/bgh085 · Cited by 104 · see citing works
Self-citationShiyanov, P. A., Hayes, S. A., Donepudi, M., Nichols, A. F., Linn, S., Slagle, B. L., & Raychaudhuri, P. (1999) · Molecular and Cellular Biology · doi:10.1128/mcb.19.7.4935 · Cited by 100 · see citing works
Wang, Q. (2003) · DNA repair · doi:10.1016/s1568-7864(03)00002-8 · Cited by 96 · see citing works
Self-citationFitch, M. E., Cross, I. V., Turner, S. J., Adimoolam, S., Lin, C., Williams, K. G., & Ford, J. M. (2003) · DNA repair · doi:10.1016/s1568-7864(03)00066-1 · Cited by 96 · see citing works
Wakasugi, M., Shimizu, M., Morioka, H., Linn, S., Nikaido, O., & Matsunaga, T. (2001) · Journal of Biological Chemistry · doi:10.1074/jbc.m011177200 · Cited by 91 · see citing works
DNA repair defect in xeroderma pigmentosum group C and complementing factor from HeLa cells.
Shivji, M. K. K., Eker, A. P. M., & Wood, R. D. (1994) · Journal of Biological Chemistry · doi:10.1016/s0021-9258(17)31709-x · Cited by 90 · see citing works
Wani, A. A., D’Ambrosio, S. M., & Alvi, N. K. (1987) · Photochemistry and Photobiology · doi:10.1111/j.1751-1097.1987.tb04798.x · Cited by 77 · see citing works
Self-citationItoh, T., Yamaizumi, M., Linn, S., & Ono, T. (2000) · Journal of Investigative Dermatology · doi:10.1046/j.1523-1747.2000.00952.x · Cited by 76 · see citing works
Treiber, D. K., Chen, Z., & Essigmann, J. M. (1992) · Nucleic Acids Research · doi:10.1093/nar/20.21.5805 · Cited by 73 · see citing works
Nucleotide excision repair syndromes: molecular basis and clinical symptoms
Bootsma, D., Weeda, G., Vermeulen, W., van Vuuren, H., Troelstra, C., van der Spek, P. J., & Hoeijmakers, J. H. J. (1995) · Philosophical Transactions of the Royal Society B Biological Sciences · doi:10.1098/rstb.1995.0012 · Cited by 73 · see citing works
Matsuda, N., Azuma, K., Saijo, M., Iemura, S., Hioki, Y., Natsume, T., Chiba, T., Tanaka, K., & Tanaka, K. (2005) · DNA repair · doi:10.1016/j.dnarep.2004.12.012 · Cited by 72 · see citing works
Kulaksiz-Erkmen, G., Reardon, J. T., & Sancar, A. (2005) · Molecular and Cellular Biology · doi:10.1128/mcb.25.22.9784-9792.2005 · Cited by 65 · see citing works
Venkatachalam, S., Denissenko, M. F., & Wani, A. A. (1997) · Oncogene · doi:10.1038/sj.onc.1200890 · Cited by 50 · see citing works
Self-citationWang, Q., Wani, M. A., Chen, J., Zhu, Q., Wani, G., Elmahdy, M., & Wani, A. A. (2004) · Molecular Carcinogenesis · doi:10.1002/mc.20065 · Cited by 49 · see citing works
Self-citationRole of DNA Excision Repair Gene Defects in the Etiology of Cancer
Ford, J. M., & Hanawalt, P. C. (1997) · Current topics in microbiology and immunology · doi:10.1007/978-3-642-60505-5_5 · Cited by 35 · see citing works
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Buetow, L., & Huang, D. T. C. (2016) · Nature Reviews Molecular Cell Biology · doi:10.1038/nrm.2016.91 · Cited by 688 · see citing works
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Jackson, S. P., & Durocher, D. (2013) · Molecular Cell · doi:10.1016/j.molcel.2013.01.017 · Cited by 601 · see citing works
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Scrima, A., Koníčková, R., Czyzewski, B. K., Kawasaki, Y., Jeffrey, P. D., Groisman, R., Nakatani, Y., Iwai, S., Pavletich, N. P., & Thomä, N. H. (2008) · Cell · doi:10.1016/j.cell.2008.10.045 · Cited by 441 · see citing works
CRL4s: the CUL4-RING E3 ubiquitin ligases
Jackson, S., & Xiong, Y. (2009) · Trends in Biochemical Sciences · doi:10.1016/j.tibs.2009.07.002 · Cited by 410 · see citing works
Kang, T.-H., Lindsey-Boltz, L. A., Reardon, J. T., & Sancar, A. (2010) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0915085107 · Cited by 250 · see citing works
Arafa, E. A., Zhu, Q., Shah, Z. I., Wani, G., Barakat, B. M., Racoma, I. O., El‐Mahdy, M. A., & Wani, A. A. (2010) · Mutation research. Fundamental and molecular mechanisms of mutagenesis · doi:10.1016/j.mrfmmm.2010.10.007 · Cited by 211 · see citing works
Self-citationProtein Dynamics in Complex DNA Lesions
Aleksandrov, R., Dotchev, A., Poser, I., Krastev, D. B., Georgiev, G. S., Panova, G., Babukov, Y., Danovski, G., Dyankova-Danovska, T., Hubatsch, L., et al. (2018) · Molecular Cell · doi:10.1016/j.molcel.2018.02.016 · Cited by 155 · see citing works
DDB2 promotes chromatin decondensation at UV-induced DNA damage
Luijsterburg, M. S., Lindh, M., Ács, K., Vrouwe, M. G., Pines, A., van Attikum, H., Mullenders, L. H. F., & Dantuma, N. P. (2012) · The Journal of Cell Biology · doi:10.1083/jcb.201106074 · Cited by 155 · see citing works
Guerrero‐Santoro, J., Kapetanaki, M. G., Hsieh, C. L., Gorbachinsky, I., Levine, A. S., & Rapić-Otrin, V. (2008) · Cancer Research · doi:10.1158/0008-5472.can-07-6162 · Cited by 132 · see citing works
Transcription factor Etv5 is essential for the maintenance of alveolar type II cells
Zhang, Z., Newton, K., Kummerfeld, S., Webster, J. D., Kirkpatrick, D. S., Phu, L., Eastham‐Anderson, J., Liu, J., Lee, W. P., Wu, J., et al. (2017) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1621177114 · Cited by 122 · see citing works
Regulation and Role of Arabidopsis CUL4-DDB1A-DDB2 in Maintaining Genome Integrity upon UV Stress
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DDB2 decides cell fate following DNA damage
Stoyanova, T., Roy, N., Kopanja, D., Bagchi, S., & Raychaudhuri, P. (2009) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0812254106 · Cited by 108 · see citing works
Li, J., Wang, Q.-E., Zhu, Q., El-Mahdy, M. A., Wani, G., Prætorius-Ibba, M., & Wani, A. A. (2006) · Cancer Research · doi:10.1158/0008-5472.can-06-1115 · Cited by 106 · see citing works
Self-citationMetal-mediated DNA damage and cell death: mechanisms, detection methods, and cellular consequences
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Luijsterburg, M. S., Goedhart, J., Moser, J., Kool, H., Geverts, B., Houtsmuller, A. B., Mullenders, L. H. F., Vermeulen, W., & van Driel, R. (2007) · Journal of Cell Science · doi:10.1242/jcs.008367 · Cited by 105 · see citing works
Regulation of damage recognition in mammalian global genomic nucleotide excision repair
Sugasawa, K. (2009) · Mutation research. Fundamental and molecular mechanisms of mutagenesis · doi:10.1016/j.mrfmmm.2009.08.004 · Cited by 99 · see citing works
Laposa, R. R., Huang, E. J., & Cleaver, J. E. (2007) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0610619104 · Cited by 92 · see citing works
Yeh, J. I., Levine, A. S., Du, S., Chinte, U., Ghodke, H. B., Wang, H., Shi, H., Hsieh, C. L., Conway, J. F., Houten, B. V., et al. (2012) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1110067109 · Cited by 89 · see citing works
Plant Responses to UV Radiation and Links to Pathogen Resistance
Kunz, B. A., Cahill, D. M., Mohr, P. G., Osmond-McLeod, M. J., & Vonarx, E. J. (2006) · International review of cytology · doi:10.1016/s0074-7696(06)55001-6 · Cited by 88 · see citing works
Ray, A., Milum, K., Battu, A., Wani, G., & Wani, A. A. (2013) · DNA Repair · doi:10.1016/j.dnarep.2013.01.003 · Cited by 85 · see citing works
“Lesions of the genomic DNA in native cellular environment were induced by micro-pore local UV irradiation and their detection was performed by dual immunofluorescent staining by our established methods [47, 48].”
MethodSelf-citationHe, J., Zhu, Q., Wani, G., Sharma, N., Han, C., Qian, J., Pentz, K., Wang, Q., & Wani, A. A. (2014) · Journal of Biological Chemistry · doi:10.1074/jbc.m114.589812 · Cited by 87 · see citing works
Self-citationRepair of Laser-localized DNA Interstrand Cross-links in G1 Phase Mammalian Cells
Muniandy, P. A., Thapa, D., Thazhathveetil, A. K., Liu, S.-T., & Seidman, M. M. (2009) · Journal of Biological Chemistry · doi:10.1074/jbc.m109.029025 · Cited by 86 · see citing works
Biochemical and Structural Domain Analysis of Xeroderma Pigmentosum Complementation Group C Protein
Bunick, C. G., Miller, M. R., Fuller, B. E., Fanning, E., & Chazin, W. (2006) · Biochemistry · doi:10.1021/bi061370o · Cited by 84 · see citing works
Fei, J., Kaczmarek, N., Luch, A., Glas, A. F., Carell, T., & Naegeli, H. (2011) · PLoS Biology · doi:10.1371/journal.pbio.1001183 · Cited by 83 · see citing works
Xeroderma pigmentosum genes: Functions inside and outside DNA repair
Sugasawa, K. (2007) · Carcinogenesis · doi:10.1093/carcin/bgm282 · Cited by 83 · see citing works
Kumar, N., Theil, A. F., Roginskaya, V. Y., Ali, Y., Calderon, M. J., Watkins, S. C., Barnes, R. P., Opresko, P. L., Pines, A., Lans, H., et al. (2022) · Nature Communications · doi:10.1038/s41467-022-28642-9 · Cited by 79 · see citing works
UV-DDB-dependent regulation of nucleotide excision repair kinetics in living cells
Nishi, R., Alekseev, S., Dinant, C., Hoogstraten, D., Houtsmuller, A. B., Hoeijmakers, J. H. J., Vermeulen, W., Hanaoka, F., & Sugasawa, K. (2009) · DNA Repair · doi:10.1016/j.dnarep.2009.02.004 · Cited by 76 · see citing works
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Ribeiro-Silva, C., Sabatella, M., Helfricht, A., Marteijn, J. A. F., Theil, A. F., Vermeulen, W., & Lans, H. (2020) · Nature Communications · doi:10.1038/s41467-020-18705-0 · Cited by 69 · see citing works
Kerzendorfer, C., Whibley, A. C., Carpenter, G., Outwin, E. A., Chiang, S., TURNER, G. M., Schwartz, C. E., El‐Khamisy, S. F., Raymond, F. L., & O’Driscoll, M. (2010) · Human Molecular Genetics · doi:10.1093/hmg/ddq008 · Cited by 70 · see citing works
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The emerging role for Cullin 4 family of E3 ligases in tumorigenesis
Cheng, J., Guo, J., North, B. J., Tao, K., Zhou, P., & Wei, W. (2018) · Biochimica et Biophysica Acta (BBA) - Reviews on Cancer · doi:10.1016/j.bbcan.2018.11.007 · Cited by 69 · see citing works
Barakat, B. M., Wang, Q., Han, C., Milum, K., Yin, D., Zhao, Q., Wani, G., Arafa, E. A., El‐Mahdy, M. A., & Wani, A. A. (2009) · International Journal of Cancer · doi:10.1002/ijc.25112 · Cited by 66 · see citing works
Self-citationLan, L., Nakajima, S., Kapetanaki, M. G., Hsieh, C. L., Fagerburg, M. V., Thickman, K. R., Rodriguez-Collazo, P., Leuba, S. H., Levine, A. S., & Rapić-Otrin, V. (2012) · Journal of Biological Chemistry · doi:10.1074/jbc.m111.307058 · Cited by 67 · see citing works
Where to cross? New insights into the location of meiotic crossovers
Mézard, C., Tagliaro-Jahns, M., & Grelon, M. (2015) · Trends in Genetics · doi:10.1016/j.tig.2015.03.008 · Cited by 66 · see citing works
Ghodke, H. B., Wang, H., Hsieh, C. L., Woldemeskel, S. A., Watkins, S. C., Rapić-Otrin, V., & Houten, B. V. (2014) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1323856111 · Cited by 64 · see citing works
Wang, Q., Prætorius-Ibba, M., Zhu, Q., Elmahdy, M., Wani, G., Zhao, Q., Qin, S., Patnaik, S., & Wani, A. A. (2007) · Nucleic Acids Research · doi:10.1093/nar/gkm550 · Cited by 63 · see citing works
Self-citationZhu, Q., Wani, G., Arab, H. H., Elmahdy, M., Ray, A., & Wani, A. A. (2008) · DNA repair · doi:10.1016/j.dnarep.2008.11.007 · Cited by 61 · see citing works
Self-citationFormation and Recognition of UV-Induced DNA Damage within Genome Complexity
Berens, P. J. T., & Molinier, J. (2020) · International Journal of Molecular Sciences · doi:10.3390/ijms21186689 · Cited by 59 · see citing works
Wang, Y., Zhang, P., Liu, Z., Wang, Q., Wen, M., Wang, Y., Yuan, H., Mao, J., & Wei, G. (2014) · Molecular Cancer · doi:10.1186/1476-4598-13-252 · Cited by 57 · see citing works
Self-citationKoyen, A. E., Madden, M. Z., Park, D., Minten, E. V., Kapoor-Vazirani, P., Werner, E., Pfister, N. T., Haji‐Seyed‐Javadi, R., Zhang, H., Xu, J., et al. (2020) · Oncogene · doi:10.1038/s41388-020-1332-2 · Cited by 57 · see citing works
Zhao, Q., Barakat, B. M., Qin, S., Ray, A., El‐Mahdy, M. A., Wani, G., Arafa, E. A., Mir, S. N., Wang, Q., & Wani, A. A. (2008) · Journal of Biological Chemistry · doi:10.1074/jbc.m803963200 · Cited by 54 · see citing works
Self-citationUV-induced ubiquitylation of XPC complex, the UV-DDB-ubiquitin ligase complex, and DNA repair
Sugasawa, K. (2006) · Journal of Molecular Histology · doi:10.1007/s10735-006-9044-7 · Cited by 69 · see citing works
Crossover Localisation Is Regulated by the Neddylation Posttranslational Regulatory Pathway
Tagliaro-Jahns, M., Vezon, D., Chambon, A., Pereira, L., Falque, M., Martin, O., Chelysheva, L. A., & Grelon, M. (2014) · PLoS Biology · doi:10.1371/journal.pbio.1001930 · Cited by 53 · see citing works
Castells, E., Molinier, J., Benvenuto, G., Bourbousse, C., Zabulon, G., Zalc, A., Cazzaniga, S., Genschik, P., Barnèche, F., & Bowler, C. (2011) · The EMBO Journal · doi:10.1038/emboj.2011.20 · Cited by 51 · see citing works
DDB2 Suppresses Tumorigenicity by Limiting the Cancer Stem Cell Population in Ovarian Cancer
Han, C., Zhao, R., Liu, X., Srivastava, A. K., Gong, L., Mao, H. C., Qu, M., Zhao, W., Yu, J., & Wang, Q. (2014) · Molecular Cancer Research · doi:10.1158/1541-7786.mcr-13-0638 · Cited by 52 · see citing works
Self-citationThe vital link between the ubiquitin–proteasome pathway and DNA repair: Impact on cancer therapy
Motegi, A., Murakawa, Y., & Takeda, S. (2009) · Cancer Letters · doi:10.1016/j.canlet.2008.12.030 · Cited by 53 · see citing works
Stoyanova, T. I., Yoon, T., Kopanja, D., MOKYR, M. B., & Raychaudhuri, P. (2007) · Molecular and Cellular Biology · doi:10.1128/mcb.00880-07 · Cited by 51 · see citing works
The deubiquitinating protein USP24 interacts with DDB2 and regulates DDB2 stability
Zhang, L., Lubin, A., Chen, H., Sun, Z., & Gong, F. (2012) · Cell Cycle · doi:10.4161/cc.22688 · Cited by 50 · see citing works
Robu, M., Shah, R. G., Purohit, N. K., Zhou, P., Naegeli, H., & Shah, G. M. (2017) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1706981114 · Cited by 50 · see citing works
Autophagic UVRAG Promotes UV-Induced Photolesion Repair by Activation of the CRL4 DDB2 E3 Ligase
Yang, Y., He, S., Wang, Q., Li, F., Kwak, M., Chen, S., O’Connell, D., Zhang, T., Pirooz, S. D., Jeon, Y.-H., et al. (2016) · Molecular Cell · doi:10.1016/j.molcel.2016.04.014 · Cited by 48 · see citing works
Self-citationYasuda, G., Nishi, R., Watanabe, E., Mori, T., Iwai, S., Orioli, D., Stefanini, M., Hanaoka, F., & Sugasawa, K. (2007) · Molecular and Cellular Biology · doi:10.1128/mcb.02166-06 · Cited by 46 · see citing works
Wang, Y., Ma, G., Wang, Q., Wen, M., Xu, Y., He, X., Zhang, P., Wang, Y., Yang, T., Zhan, P., et al. (2013) · Molecules · doi:10.3390/molecules19010159 · Cited by 45 · see citing works
Self-citationMind the gap: keeping UV lesions in check
Novarina, D., Amara, F., Lazzaro, F., Plevani, P., & Muzi-Falconi, M. (2011) · DNA Repair · doi:10.1016/j.dnarep.2011.04.030 · Cited by 43 · see citing works
Proliferation defects and genome instability in cells lacking Cul4A
Kopanja, D., Stoyanova, T. I., Okur, M. N., Huang, E. W., Bagchi, S., & Raychaudhuri, P. (2009) · Oncogene · doi:10.1038/onc.2009.86 · Cited by 44 · see citing works
Nucleotide excision repair leaves a mark on chromatin: DNA damage detection in nucleosomes
Apelt, K., Lans, H., Schärer, O. D., & Luijsterburg, M. S. (2021) · Cellular and Molecular Life Sciences · doi:10.1007/s00018-021-03984-7 · Cited by 43 · see citing works
CRL Ubiquitin Ligases and DNA Damage Response
Li, J.-M., & Jin, J. (2012) · Frontiers in Oncology · doi:10.3389/fonc.2012.00029 · Cited by 41 · see citing works
Kerzendorfer, C., Hart, L., Colnaghi, R., Carpenter, G., Alcantara, D., Outwin, E. A., Carr, A. M., & O’Driscoll, M. (2011) · Mechanisms of Ageing and Development · doi:10.1016/j.mad.2011.02.003 · Cited by 41 · see citing works
Dynamic recruitment of licensing factor Cdt1 to sites of DNA damage
Roukos, V., Kinkhabwala, A., Colombelli, J., Kotsantis, P., Taraviras, S. L., Nishitani, H., Stelzer, E. H. K., Bastiaens, P. I. H., & Lygerou, Z. (2011) · Journal of Cell Science · doi:10.1242/jcs.074229 · Cited by 40 · see citing works
XPC: Going where no DNA damage sensor has gone before
Nemzow, L., Lubin, A., Zhang, L., & Gong, F. (2015) · DNA repair · doi:10.1016/j.dnarep.2015.09.004 · Cited by 39 · see citing works
RETRACTED ARTICLE: DDB2, an Essential Mediator of Premature Senescence
Roy, N., Stoyanova, T. I., Dominguez‐Brauer, C., Park, H. J., Bagchi, S., & Raychaudhuri, P. (2010) · Molecular and Cellular Biology · doi:10.1128/mcb.01480-09 · Cited by 39 · see citing works
RetractedCellular Concentrations of DDB2 Regulate Dynamic Binding of DDB1 at UV-Induced DNA Damage
Alekseev, S., Luijsterburg, M. S., Pines, A., Geverts, B., Mari, P.-O., Giglia-Mari, G., Lans, H., Houtsmuller, A. B., Mullenders, L. H. F., Hoeijmakers, J. H. J., et al. (2008) · Molecular and Cellular Biology · doi:10.1128/mcb.01108-08 · Cited by 38 · see citing works
Matsunuma, R., Niida, H., Ohhata, T., Kitagawa, K., Sakai, S., Uchida, C., Shiotani, B., Matsumoto, M., Nakayama, K. I., Ogura, H., et al. (2015) · Molecular and Cellular Biology · doi:10.1128/mcb.00809-15 · Cited by 37 · see citing works
Vlachostergios, P. J., Patrikidou, A., Daliani, D., & Papandreou, C. N. (2009) · Journal of Cellular and Molecular Medicine · doi:10.1111/j.1582-4934.2009.00824.x · Cited by 36 · see citing works
p21 Cooperates with DDB2 Protein in Suppression of Ultraviolet Ray-induced Skin Malignancies
Stoyanova, T. I., Roy, N., Bhattacharjee, S., Kopanja, D., Valli, T., Bagchi, S., & Raychaudhuri, P. (2011) · Journal of Biological Chemistry · doi:10.1074/jbc.m111.295816 · Cited by 35 · see citing works
Copper-mediated DNA damage by the neurotransmitter dopamine and L-DOPA: A pro-oxidant mechanism
Rehmani, N., Zafar, A., Arif, H., Hadi, S. M., & Wani, A. A. (2017) · Toxicology in Vitro · doi:10.1016/j.tiv.2017.01.020 · Cited by 35 · see citing works
Self-citationCul4A is required for hematopoietic cell viability and its deficiency leads to apoptosis
Waning, D. L., Li, B., Jia, N., Naaldijk, Y., Goebel, W. S., HogenEsch, H., & Chun, K. T. (2008) · Blood · doi:10.1182/blood-2007-11-126300 · Cited by 34 · see citing works
Zhu, Q., Battu, A., Ray, A., Wani, G., Qian, J., He, J., Wang, Q., & Wani, A. A. (2015) · Mutation research. Fundamental and molecular mechanisms of mutagenesis · doi:10.1016/j.mrfmmm.2015.01.005 · Cited by 33 · see citing works
Self-citationArab, H. H., Wani, G., Ray, A., Shah, Z. I., Zhu, Q., & Wani, A. A. (2010) · PLoS ONE · doi:10.1371/journal.pone.0011007 · Cited by 33 · see citing works
Self-citationPogliano, C. B., Gatti, M., Rüthemann, P., Garajovà, Z., Penengo, L., & Naegeli, H. (2017) · Nature Communications · doi:10.1038/s41467-017-01080-8 · Cited by 33 · see citing works
Regulation of UV-induced DNA damage response by ubiquitylation
Bergink, S., Jaspers, N. G. J., & Vermeulen, W. (2007) · DNA repair · doi:10.1016/j.dnarep.2007.01.012 · Cited by 32 · see citing works
Orchestral maneuvers at the damaged sites in nucleotide excision repair
Alekseev, S., & Coin, F. (2015) · Cellular and Molecular Life Sciences · doi:10.1007/s00018-015-1859-5 · Cited by 31 · see citing works
Umar, S. A., & Tasduq, S. A. (2020) · RSC Advances · doi:10.1039/d0ra05819j · Cited by 31 · see citing works
Molecular mechanisms of xeroderma pigmentosum (XP) proteins
Koch, S. C., Simon, N., Ebert, C., & Carell, T. (2016) · Quarterly Reviews of Biophysics · doi:10.1017/s0033583515000268 · Cited by 31 · see citing works
The moonlighting of RAD23 in DNA repair and protein degradation
Grønbæk-Thygesen, M., Kampmeyer, C., Hofmann, K., & Hartmann‐Petersen, R. (2023) · Biochimica et Biophysica Acta (BBA) - Gene Regulatory Mechanisms · doi:10.1016/j.bbagrm.2023.194925 · Cited by 29 · see citing works
Ubiquitin at work: The ubiquitous regulation of the damage recognition step of NER
van Cuijk, L., Vermeulen, W., & Marteijn, J. A. F. (2014) · Experimental Cell Research · doi:10.1016/j.yexcr.2014.07.018 · Cited by 30 · see citing works
Bommi, P. V., Ravindran, S., Raychaudhuri, P., & Bagchi, S. (2018) · Oncotarget · doi:10.18632/oncotarget.26168 · Cited by 28 · see citing works
Cdt2-mediated XPG degradation promotes gap-filling DNA synthesis in nucleotide excision repair
Han, C., Wani, G., Zhao, R., Qian, J., Sharma, N., He, J., Zhu, Q., Wang, Q., & Wani, A. A. (2014) · Cell Cycle · doi:10.4161/15384101.2014.973740 · Cited by 30 · see citing works
Self-citationDamaged-DNA Binding Protein-2 Drives Apoptosis Following DNA Damage
Bagchi, S., & Raychaudhuri, P. (2010) · Cell Division · doi:10.1186/1747-1028-5-3 · Cited by 28 · see citing works
He, J., Zhu, Q., Wani, G., Sharma, N., & Wani, A. A. (2016) · Journal of Biological Chemistry · doi:10.1074/jbc.m115.705350 · Cited by 30 · see citing works
Self-citationTiming of DNA lesion recognition: Ubiquitin signaling in the NER pathway
Chitale, S., & Richly, H. (2016) · Cell Cycle · doi:10.1080/15384101.2016.1261227 · Cited by 28 · see citing works
Nucleotide Excision Repair: Finely Tuned Molecular Orchestra of Early Pre‐incision Events
Zhu, Q., & Wani, A. A. (2016) · Photochemistry and Photobiology · doi:10.1111/php.12647 · Cited by 28 · see citing works
Self-citationTurn-On DNA Damage Sensors for the Direct Detection of 8-Oxoguanine and Photoproducts in Native DNA
Furman, J. L., Mok, P.-W., Badran, A. H., & Ghosh, I. (2011) · Journal of the American Chemical Society · doi:10.1021/ja1116606 · Cited by 28 · see citing works
Damaged DNA Binding Protein 2 in Reactive Oxygen Species (ROS) Regulation and Premature Senescence
Roy, N., Bagchi, S., & Raychaudhuri, P. (2012) · International Journal of Molecular Sciences · doi:10.3390/ijms130911012 · Cited by 28 · see citing works
Neher, T. M., Rechkunova, N. I., Lavrik, O. I., & Turchi, J. J. (2009) · Biochemistry · doi:10.1021/bi901575h · Cited by 27 · see citing works
Regulation of XPC deubiquitination by USP11 in repair of UV-induced DNA damage
Shah, P., Qiang, L., Yang, S., Soltani, K., & He, Y. (2017) · Oncotarget · doi:10.18632/oncotarget.22105 · Cited by 27 · see citing works
Gsell, C., Richly, H., Coin, F., & Naegeli, H. (2019) · Nucleic Acids Research · doi:10.1093/nar/gkz1229 · Cited by 26 · see citing works
Role of Claspin in regulation of nucleotide excision repair factor DDB2
Prætorius-Ibba, M., Wang, Q.-E., Wani, G., El-Mahdy, M. A., Zhu, Q., Qin, S., & Wani, A. A. (2007) · DNA Repair · doi:10.1016/j.dnarep.2006.11.009 · Cited by 24 · see citing works
Self-citationDDB2 is a novel AR interacting protein and mediates AR ubiquitination/degradation
Chang, S., Su, C.-H., Chen, H.-H., Huang, C.-W., Tsao, L.-P. B., Tsao, Y., & Chen, S. (2012) · The International Journal of Biochemistry & Cell Biology · doi:10.1016/j.biocel.2012.07.023 · Cited by 25 · see citing works
Phosphorylation of xeroderma pigmentosum group C regulates ultraviolet-induced DNA damage repair
Shah, P., Zhao, B., Qiang, L., & He, Y. (2018) · Nucleic Acids Research · doi:10.1093/nar/gky239 · Cited by 23 · see citing works
UV radiation-induced SUMOylation of DDB2 regulates nucleotide excision repair
Han, C., Zhao, R., Kroger, J., He, J., Wani, G., Wang, Q., & Wani, A. A. (2017) · Carcinogenesis · doi:10.1093/carcin/bgx076 · Cited by 22 · see citing works
Self-citationDDB2 regulates DNA replication through PCNA-independent degradation of CDT2
Wu, X., Yu, M., Zhang, Z., Leng, F., Ma, Y., Xie, N., & Lu, F. (2021) · Cell & Bioscience · doi:10.1186/s13578-021-00540-5 · Cited by 21 · see citing works
Jiang, Y., Ni, S., Xiao, B., & Jia, L. (2023) · Acta Pharmaceutica Sinica B · doi:10.1016/j.apsb.2023.07.019 · Cited by 21 · see citing works
Chiganças, V., Lima-Bessa, K. M., Stary, A., Menck, C. F. M., & Sarasin, A. R. (2008) · Cancer Research · doi:10.1158/0008-5472.can-07-6695 · Cited by 19 · see citing works
Cenni, V., Squarzoni, S., Loi, M., Mattioli, E., Lattanzi, G., & Capanni, C. (2020) · Cells · doi:10.3390/cells9061415 · Cited by 18 · see citing works
- Authors
- El-Mahdy, M. A., Zhu, Q., Wang, Q.-E., Wani, G., Prætorius-Ibba, M., & Wani, A. A.
- Affiliations
- The Ohio State University (US)
- The Ohio State University Comprehensive Cancer Center – Arthur G. James Cancer Hospital and Richard J. Solove Research Institute (US)
- Corresponding author
- Wani, Altaf A.
- ORCID
- Wang, Qi-en
- Venue
- Journal of Biological Chemistry
- Publisher
- Elsevier BV
- Published
- 2006-05
- Volume
- 281
- Issue
- 19
- Pages
- 13404-13411
- ISSN
- 0021-9258 (ISSN-L)
- OpenAlex
- W2038616578
- Cited by
- 151
- References
- 53
- Citations by year
- 2026: 3 · 2025: 2 · 2024: 3 · 2023: 5 · 2022: 5 · 2021: 4 · 2020: 6 · 2019: 4 · 2018: 5 · 2017: 9 · 2016: 9 · 2015: 7 · 2014: 9 · 2013: 5 · 2012: 8
- FWCI
- 5.43
- Type
- journal article
- Language
- en
- Open access
- hybrid
- doi.org
- Licence
- Locations
- Journal of Biological Chemistry (publishedVersion, cc-by)
- PubMed (publishedVersion)
- Funders
- National Cancer Institute (R01CA093413, CA93413)
- National Institute of Environmental Health Sciences (R01ES002388, ES2388, R01ES012991, ES12991)
- 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
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Nuclear Structure and Function
- Keywords
- DDB2, XPC, nucleotide excision repair, DNA damage recognition, cyclobutane pyrimidine dimers, UV-induced DNA damage, ubiquitin ligase, protein degradation, DNA damage foci
- MeSH terms
- Cell Line, Chromatin, DNA Damage, DNA-Binding Proteins, Humans, Leupeptins, Pyrimidine Dimers, Ultraviolet Rays, Signal Transduction, Gene Silencing, Ubiquitin, Cullin Proteins
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