Disorders of nucleotide excision repair: the genetic and molecular basis of heterogeneity
Abstract
Mutations in genes on the nucleotide excision repair pathway are associated with diseases, such as xeroderma pigmentosum, Cockayne syndrome and trichothiodystrophy, that involve skin cancer and developmental and neurological symptoms. These mutations cause the defective repair of damaged DNA and increased transcription arrest but, except for skin cancer, the links between repair and disease have not been obvious. Widely different clinical syndromes seem to result from mutations in the same gene, even when the mutations result in complete loss of function. The mapping of mutations in recently solved protein structures has begun to clarify the links between the molecular defects and phenotypes, but the identification of additional sources of clinical variability is still necessary.
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Both XP and CS patients have defects in NER.
“Both XP and CS patients have defects in NER.”
From Why Cockayne syndrome patients do not get cancer despite their DNA repair deficiency (2016) · cites this paper as [1]
CS patients are characterized by neurological and developmental symptoms and a greatly reduced life expectancy.
“CS patients are characterized by neurological and developmental symptoms such as early cessation of growth, microcephaly, mental retardation with dysmyelination, cachexia, and a greatly reduced life expectancy (1).”
From Why Cockayne syndrome patients do not get cancer despite their DNA repair deficiency (2016) · cites this paper as [1]
CS patients, defective in the TCR branch of NER, present developmental defects and neurodegeneration; many but not all are photosensitive, some developing blistering sunburns.
“CS patients, defective in the TCR branch of NER (1, 27), present a very different clinical picture, one of developmental defects and neurodegeneration; many but not all patients are also photosensitive, some developing blistering sunburns (5, 28).”
From Why Cockayne syndrome patients do not get cancer despite their DNA repair deficiency (2016) · cites this paper as [1]
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“Two NER pathways have been identified in mammalian cells: global genomic repair (GGR) and transcription-coupled repair (TCR) [35].”
BackgroundThe deacetylase SIRT6 promotes the repair of UV-induced DNA damage by targeting DDB2
Geng, A., Tang, H., Huang, J., Qian, Z. Y., Qin, N., Yao, Y., Xu, Z., Chen, H., Lan, L., Xie, H., et al. (2020) · Nucleic Acids Research · doi:10.1093/nar/gkaa661 · Cited by 65 · see citing works
“Interestingly, Cockayne syndrome, which is caused by TC-NER defects, is mainly characterized by neurological or developmental disorders but not a heightened incidence of melanoma (4).”
BackgroundPaul, D., Mu, H., Zhao, H., Ouerfelli, O., Jeffrey, P. D., Broyde, S. B., & Min, J. (2019) · Nucleic Acids Research · doi:10.1093/nar/gkz359 · Cited by 62 · see citing works
“Impaired NER genes decrease cell survival after UV in yeast and other cell lines and can cause the xeroderma pigmentosum (XP) cancer predisposition syndrome in humans, marked by extreme sun sensitivity and >1000-fold higher risk of sunlight-induced skin cancers (1,15,16).”
BackgroundKim, J., Ryu, T. H., Lee, S. S., Lee, S., & Chung, B. Y. (2018) · Plant Science · doi:10.1016/j.plantsci.2018.10.013 · Cited by 70 · see citing works
Preclinical Corrective Gene Transfer in Xeroderma Pigmentosum Human Skin Stem Cells
Warrick, E., Garcia, M., Chagnoleau, C., Chevallier, O., Bergoglio, V., Sartori, D., Mavilio, F., Angulo, J. F., Avril, M.-F., Sarasin, A., et al. (2012) · Molecular Therapy · doi:10.1038/mt.2011.233 · Cited by 58 · see citing works
Puumalainen, M.-R., Rüthemann, P., Min, J., & Naegeli, H. (2015) · Cellular and Molecular Life Sciences · doi:10.1007/s00018-015-2075-z · Cited by 63 · see citing works
“These patients are classified into different genetic complementation groups (from XPA to XPG) caused by mutations in the respective seven NER genes [21].”
BackgroundJung, Y.-S., Qian, Y., & Chen, X. (2012) · DNA Repair · doi:10.1016/j.dnarep.2011.10.017 · Cited by 57 · see citing works
“XPV patients are highly sensitive to UV and have much greater risk of developing sun-induced skin cancer than hat of normal population [4–7].”
BackgroundRegenbogen, L. (2020) · Definitions · doi:10.1002/9781119013112.ch35 · Cited by 57 · see citing works
Impact of Age and Insulin-Like Growth Factor-1 on DNA Damage Responses in UV-Irradiated Human Skin
Kemp, M. G., Spandau, D. F., & Travers, J. B. (2017) · Molecules · doi:10.3390/molecules22030356 · Cited by 62 · see citing works
“Mutations in NER gene products give rise to both the disease xeroderma pigmentosum, which is characterized by a several thousand-fold increased risk of skin carcinogenesis, and to a neurodegenerative and premature aging disorder known as Cockayne syndrome [35,36].”
BackgroundPirh2 E3 Ubiquitin Ligase Monoubiquitinates DNA Polymerase Eta To Suppress Translesion DNA Synthesis
Jung, Y.-S., Hakem, A., Hakem, R., & Chen, X.-B. (2011) · Molecular and Cellular Biology · doi:10.1128/mcb.05808-11 · Cited by 56 · see citing works
“Under these conditions, many organisms require the action of specialized translesion DNA polymerases that can bypass various DNA lesions (6, 8, 27).”
BackgroundWhy Cockayne syndrome patients do not get cancer despite their DNA repair deficiency
Reid-Bayliss, K. S., Arron, S. T., Loeb, L. A., Bezrookove, V., & Cleaver, J. E. (2016) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1610020113 · Cited by 55 · see citing works
“CS is mutated in the transcription-coupled repair (TCR) branch of the NER pathway and exhibits developmental and neurological pathologies.”
BackgroundInfluentialSelf-citationXiong, Y., Huang, B., & Yin, J.-Y. (2017) · Medical Oncology · doi:10.1007/s12032-017-0905-6 · Cited by 51 · see citing works
Cockayne Syndrome: The many challenges and approaches to understand a multifaceted disease
Vessoni, A. T., Guerra, C. C. C., Kajitani, G. S., Nascimento, L. L. S., & Garcia, C. C. M. (2020) · Genetics and Molecular Biology · doi:10.1590/1678-4685-gmb-2019-0085 · Cited by 53 · see citing works
“, 2008), and the detection of UV products is facilitated by XPE/DDB2 (Cleaver et al., 2009).”
Chatgilialoglu, C., Ferreri, C., Geacintov, N. E., Krokidis, M. G., Liu, Y., Masi, A., Shafirovich, V., Terzidis, M. A., & Tsegay, P. S. (2019) · Cells · doi:10.3390/cells8060513 · Cited by 57 · see citing works
“The skin is normal at birth, and with the onset of the disorder, all patients develop freckle-like pigmentary changes in sun-exposed areas, which eventually appear as poikiloderma [108,109].”
BackgroundSoltys, D. T., Rocha, C. R. R., Lerner, L. K., de Souza, T. A., Munford, V., Cabral, F., Nardo, T., Stefanini, M., Sarasin, A., Cabral‐Neto, J. B., et al. (2013) · Human Mutation · doi:10.1002/humu.22259 · Cited by 48 · see citing works
“The clinical hallmarks of XP are extreme photosensitivity, hyperpigmentation of the skin, xerosis, premature skin ageing, abnormal lentiginosis, and high incidence of tumors in the sun-exposed skin [Cleaver et al., 2009; Lehmann et al., 2011].”
BackgroundTRiC controls transcription resumption after UV damage by regulating Cockayne syndrome protein A
Pines, A., Dijk, M., Makowski, M. M., Meulenbroek, E. M., Vrouwe, M. G., van der Weegen, Y., Baltissen, M. P. A., French, P. J., van Royen, M. E., Luijsterburg, M. S., et al. (2018) · Nature Communications · doi:10.1038/s41467-018-03484-6 · Cited by 48 · see citing works
Gene Therapy for Skin DiseasesPreprint
Gorell, E. S., Nguyen, N. T., Lane, A. T., & Siprashvili, Z. (2014) · Cold Spring Harbor Perspectives in Medicine · doi:10.1101/cshperspect.a015149 · Cited by 57 · see citing works
“Current therapy is limited to surgical tumor resection and recommendations to avoid sunlight (Cleaver et al. 2009).”
BackgroundTranscription coupled repair at the interface between transcription elongation and mRNP biogenesis
Gaillard, H., & Aguilera, A. (2012) · Biochimica et Biophysica Acta (BBA) - Gene Regulatory Mechanisms · doi:10.1016/j.bbagrm.2012.09.008 · Cited by 44 · see citing works
Gorgun, M. F., Zhuo, M., & Englander, E. W. (2016) · Molecular Neurobiology · doi:10.1007/s12035-016-0273-9 · Cited by 41 · see citing works
“Cisplatin crosslinks are repairable via the NER pathway that catalyzes removal of cisplatin crosslinks from nuclear DNA [69, 70].”
Park, J.-M., & Kang, T.-H. (2016) · International Journal of Molecular Sciences · doi:10.3390/ijms17111840 · Cited by 44 · see citing works
Slow accumulation of mutations in Xpc−/− mice upon induction of oxidative stress
Melis, J. P. M., Kuiper, R., Zwart, E. P., Robinson, J. E., Pennings, J., van Oostrom, C. V., Luijten, M., & van Steeg, H. (2013) · DNA Repair · doi:10.1016/j.dnarep.2013.08.019 · Cited by 44 · see citing works
“sub-pathways: global genome NER (GG-NER), which covers repair genome wide, and transcription coupled NER (TC-NER), which is responsible for repair of the transcribed strand of active genes [2,6].”
Whole-Exome Sequencing Enables Rapid Determination of Xeroderma Pigmentosum Molecular Etiology
Ortega‐Recalde, O., Vergara, J. I., Fonseca, D. J., Ríos, X. P., Mosquera, H., Bermúdez, O. M., Medina, C. L., Vargas, C. I., Pallares, A. E., Restrepo, C. M., et al. (2013) · PLoS ONE · doi:10.1371/journal.pone.0064692 · Cited by 39 · see citing works
TFIIH: A multi-subunit complex at the cross-roads of transcription and DNA repair
Kolesnikova, O., Radu, L., & Poterszman, A. (2019) · Advances in protein chemistry and structural biology · doi:10.1016/bs.apcsb.2019.01.003 · Cited by 50 · see citing works
Tesfaye, A. A., Kamgar, M., Azmi, A. S., & Philip, P. A. (2017) · Expert Review of Anticancer Therapy · doi:10.1080/14737140.2018.1417844 · Cited by 43 · 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
“This UV-DDB-Cul4A-Roc1 complex (referred to as CRL4DDB2) catalyzes the ubiquitination of histones and/or recruits chromatin remodelers at the sites of UV lesions, ensuing lesion handover from UV-DDB to XPC (Cleaver et al., 2009; Duan and Smerdon, 2010).”
Jagirdar, K., Yin, K., Harrison, M., Lim, W., Muscat, G. E. O., Sturm, R. A., & Smith, A. G. (2013) · PLoS ONE · doi:10.1371/journal.pone.0078075 · Cited by 40 · see citing works
“Nucleotide excision repair (NER), like other DNA repair mechanisms, proceeds as a highly ordered sequential process involving the recruitment of an array of factors [5,6].”
BackgroundPremature Skin Aging Features Rescued by Inhibition of NADPH Oxidase Activity in XPC-Deficient Mice
Hosseini, M., Mahfouf, W., Serrano-Sanchez, M., Raad, H., Harfouche, G., Bonneu, M., Claverol, S., Mazurier, F., Rossignol, R., Taieb, A., et al. (2015) · Journal of Investigative Dermatology · doi:10.1038/jid.2014.511 · Cited by 42 · see citing works
“The absence or dysfunction of NER proteins results in one of the following distinct diseases: XP, TTD, and CS (Kraemer et al., 2007; Cleaver et al., 2009).”
InfluentialIn TFIIH the Arch domain of XPD is mechanistically essential for transcription and DNA repair
Peissert, S., Sauer, F., Grabarczyk, D. B., Braun, C., Sander, G., Poterszman, A., Egly, J., Kuper, J., & Kisker, C. (2020) · Nature Communications · doi:10.1038/s41467-020-15241-9 · Cited by 42 · see citing works
FACT subunit Spt16 controls UVSSA recruitment to lesion-stalled RNA Pol II and stimulates TC-NER
Wienholz, F., Zhou, D., der Velden, Y. T.-V., Schwertman, P., Tresini, M., Pines, A., van Toorn, M., Bezstarosti, K., Demmers, J., & Marteijn, J. A. F. (2019) · Nucleic Acids Research · doi:10.1093/nar/gkz055 · Cited by 41 · see citing works
“CS is caused by mutations in Cockayne Syndrome protein A (CSA) and Cockayne Syndrome protein B (CSB) (11,12), while mutations in UVSSA give rise to UVSS (13–15).”
BackgroundHan, W., Ming, M., Zhao, R., Pi, J., Wu, C., & He, Y. (2012) · Journal of Biological Chemistry · doi:10.1074/jbc.m112.363614 · Cited by 45 · see citing works
Edifizi, D., & Schumacher, B. (2015) · Biomolecules · doi:10.3390/biom5031855 · Cited by 42 · see citing works
Hunter, F. W., Wang, J., Patel, R., Hsu, H., Hickey, A. J., Hay, M. P., & Wilson, W. R. (2011) · Biochemical Pharmacology · doi:10.1016/j.bcp.2011.12.005 · Cited by 43 · see citing works
“UV4 and UV41 cells, which are deficient in NER (a pathway associated with several inherited cancer syndromes [55]), have been widely characterised as hypersensitive to bulky lesions including DNA cross-links [38], whereas EM9 cells are sensitive to single-strand breaks and base damage due to failure of DNA ligase III…”
Background
- Authors
- Cleaver, J. E., Lam, E. T., & Revet, I.
- Affiliations
- University of California, San Francisco (US)
- Corresponding author
- Cleaver, James E.
- ORCID
- Cleaver, James E.
- Venue
- Nature Reviews Genetics
- Published
- 2009-10-07
- Volume
- 10
- Issue
- 11
- Pages
- 756-768
- ISSN
- 1471-0056 (ISSN-L)
- 1471-0064
- OpenAlex
- W2026776398
- Cited by
- 428
- References
- 0
- Citations by year
- 2026: 7 · 2025: 16 · 2024: 9 · 2023: 14 · 2022: 23 · 2021: 20 · 2020: 30 · 2019: 24 · 2018: 24 · 2017: 29 · 2016: 35 · 2015: 30 · 2014: 43 · 2013: 38 · 2012: 33
- FWCI
- 2.12
- Type
- journal article
- Language
- en
- Open access
- closed
- Locations
- Nature Reviews Genetics (publishedVersion)
- PubMed (publishedVersion)
- Funders
- Iris O'Brien Foundation
- National Institute of Neurological Disorders and Stroke (R01NS052781)
- Topics
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › DNA Repair Mechanisms
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Genetics › Genomics and Rare Diseases
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Genetics › Genetic and rare skin diseases.
- Keywords
- nucleotide excision repair, genetic heterogeneity, xeroderma pigmentosum, Cockayne syndrome, trichothiodystrophy, transcription arrest, DNA repair deficiency, skin cancer predisposition, neurological symptoms, developmental abnormalities, loss-of-function mutations, protein structure, genotype-phenotype correlation
- MeSH terms
- Animals, Cockayne Syndrome, DNA Repair, Humans, Genetic Variation, Xeroderma Pigmentosum, Trichothiodystrophy Syndromes
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