Xeroderma pigmentosum group A protein loads as a separate factor onto DNA lesions

Rademakers, Suzanne; Volker, Marcel; Hoogstraten, Deborah; Nigg, Alex L.; Moné, Martijn J.; van Zeeland, Albert A.; Hoeijmakers, Jan H. J.; Houtsmuller, Adriaan B.; Vermeulen, Wim

doi:10.1128/mcb.23.16.5755-5767.2003

Cited by 149DNA Repair MechanismsNuclear Structure and FunctionDiffusion and Search Dynamics

Xeroderma pigmentosum group A protein loads as a separate factor onto DNA lesions

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Rademakers, Suzanne, Volker, Marcel, Hoogstraten, Deborah, Nigg, Alex L., Moné, Martijn J., van Zeeland, Albert A., Hoeijmakers, Jan H. J., Houtsmuller, Adriaan B. +1 more·2003·Molecular and Cellular Biology

DOI 10.1128/mcb.23.16.5755-5767.2003PMC PMC166334

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Abstract

Nucleotide excision repair (NER) is the main DNA repair pathway in mammals for removal of UV-induced lesions. NER involves the concerted action of more than 25 polypeptides in a coordinated fashion. The xeroderma pigmentosum group A protein (XPA) has been suggested to function as a central organizer and damage verifier in NER. How XPA reaches DNA lesions and how the protein is distributed in time and space in living cells are unknown. Here we studied XPA in vivo by using a cell line stably expressing physiological levels of functional XPA fused to green fluorescent protein and by applying quantitative fluorescence microscopy. The majority of XPA moves rapidly through the nucleoplasm with a diffusion rate different from those of other NER factors tested, arguing against a preassembled XPA-containing NER complex. DNA damage induced a transient ( approximately 5-min) immobilization of maximally 30% of XPA. Immobilization depends on XPC, indicating that XPA is not the initial lesion recognition protein in vivo. Moreover, loading of replication protein A on NER lesions was not dependent on XPA. Thus, XPA participates in NER by incorporation of free diffusing molecules in XPC-dependent NER-DNA complexes. This study supports a model for a rapid consecutive assembly of free NER factors, and a relatively slow simultaneous disassembly, after repair.

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Formaldehyde rather than methanol was employed in the reports of a nucleus-only location for XPA.
“Formaldehyde rather than methanol was employed in the reports of a nucleus-only location for XPA [38], [51], [52].”
From UV-Induced Nuclear Import of XPA Is Mediated by Importin-α4 in An ATR-Dependent Manner (2013) · cites this paper as [52]
Reports of immunofluorescence microscopic analyses showed that XPA was fully localized to the nucleus even in the absence of DNA damage.
“reports of immunofluorescence microscopic analyses that showed that XPA was fully localized to the nucleus even in the absence of DNA damage [38], [51], [52].”
From UV-Induced Nuclear Import of XPA Is Mediated by Importin-α4 in An ATR-Dependent Manner (2013) · cites this paper as [52]

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DNA damage triggers nucleotide excision repair-dependent monoubiquitylation of histone H2APreprint
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Solar UV damage to cellular DNA: from mechanisms to biological effects
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Nucleotide excision repair-induced H2A ubiquitination is dependent on MDC1 and RNF8 and reveals a universal DNA damage response
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The UV-damaged DNA binding protein mediates efficient targeting of the nucleotide excision repair complex to UV-induced photo lesions
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DNA damage stabilizes interaction of CSB with the transcription elongation machinery
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Activation of multiple DNA repair pathways by sub-nuclear damage induction methods
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Cisplatin sensitivity of testis tumour cells is due to deficiency in interstrand-crosslink repair and low ERCC1-XPF expression
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Sequential recruitment of the repair factors during NER: the role of XPG in initiating the resynthesis step
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DDB2 promotes chromatin decondensation at UV-induced DNA damage
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Poly(ADP-ribosyl)ation links the chromatin remodeler SMARCA5/SNF2H to RNF168-dependent DNA damage signaling
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A Ubiquitin-Binding Domain in Cockayne Syndrome B Required for Transcription-Coupled Nucleotide Excision Repair
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Versatile DNA damage detection by the global genome nucleotide excision repair protein XPC
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Stochastic and reversible assembly of a multiprotein DNA repair complex ensures accurate target site recognition and efficient repair
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Mechanisms of DNA damage recognition and strand discrimination in human nucleotide excision repair
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XPA: A key scaffold for human nucleotide excision repair
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SUMO and ubiquitin-dependent XPC exchange drives nucleotide excision repair
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The xeroderma pigmentosum pathway: Decision tree analysis of DNA quality
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Interindividual Variation in Nucleotide Excision Repair Genes and Risk of Endometrial Cancer
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Dynamic in vivo interaction of DDB2 E3 ubiquitin ligase with UV-damaged DNA is independent of damage-recognition protein XPC
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Human Nucleotide Excision Repair Efficiently Removes Chromium-DNA Phosphate Adducts and Protects Cells against Chromate Toxicity
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ATR-dependent checkpoint modulates XPA nuclear import in response to UV irradiation
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Nucleotide excision repair–initiating proteins bind to oxidative DNA lesions in vivo
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Recruitment of the Nucleotide Excision Repair Endonuclease XPG to Sites of UV-Induced DNA Damage Depends on Functional TFIIH
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UV-induced photolesions elicit ATR-kinase-dependent signaling in non-cycling cells through nucleotide excision repair-dependent and -independent pathways
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Molecular Mechanism of Global Genome Nucleotide Excision Repair
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XPA protein as a limiting factor for nucleotide excision repair and UV sensitivity in human cells
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Dynamic Interaction of TTDA with TFIIH Is Stabilized by Nucleotide Excision Repair in Living Cells
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DNA damage-induced histone H1 ubiquitylation is mediated by HUWE1 and stimulates the RNF8-RNF168 pathway
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Structural Mechanisms of DNA Replication, Repair, and Recombination
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Combinations of polymorphisms in XPD, XPC and XPA in relation to risk of lung cancer
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Fluorescence Recovery after Photobleaching: Application to Nuclear Proteins
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The Spacer Region of XPG Mediates Recruitment to Nucleotide Excision Repair Complexes and Determines Substrate Specificity
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Definition of a Short Region of XPG Necessary for TFIIH Interaction and Stable Recruitment to Sites of UV Damage
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UV-DDB-dependent regulation of nucleotide excision repair kinetics in living cells
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Human ISWI complexes are targeted by SMARCA5 ATPase and SLIDE domains to help resolve lesion-stalled transcription
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Fluorescence Recovery After Photobleaching (FRAP) to Study Nuclear Protein Dynamics in Living Cells
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Localization of xeroderma pigmentosum group A protein and replication protein A on damaged DNA in nucleotide excision repair
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Repairing DNA damage in chromatin
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Nucleotide Excision Repair Is Associated with the Replisome and Its Efficiency Depends on a Direct Interaction between XPA and PCNA
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Specific and Efficient Binding of Xeroderma Pigmentosum Complementation Group A to Double-Strand/Single-Strand DNA Junctions with 3‘- and/or 5‘-ssDNA Branches
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Mathematical Modeling of Nucleotide Excision Repair Reveals Efficiency of Sequential Assembly Strategies
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Nuclear envelope defects impede a proper response to micronuclear DNA lesions
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Dynamics of mammalian NER proteins
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UV-Induced RPA1 Acetylation Promotes Nucleotide Excision Repair
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Relationship between polymorphisms of nucleotide excision repair genes and oral cancer risk in Taiwan: evidence for modification of smoking habit.
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Pre-Steady-State Binding of Damaged DNA by XPC−hHR23B Reveals a Kinetic Mechanism for Damage Discrimination
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Complex Formation with Damage Recognition Protein Rad14 Is Essential for Saccharomyces cerevisiae Rad1-Rad10 Nuclease To Perform Its Function in Nucleotide Excision Repair In Vivo
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Nuclear proteins: finding and binding target sites in chromatin
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Role of the XPA protein in the NER pathway: A perspective on the function of structural disorder in macromolecular assembly
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Human HMGB1 directly facilitates interactions between nucleotide excision repair proteins on triplex-directed psoralen interstrand crosslinks
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DNA damage responsive microRNAs misexpressed in human cancer modulate therapy sensitivity
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Development of New EBV-Based Vectors for Stable Expression of Small Interfering RNA to Mimick Human Syndromes: Application to NER Gene Silencing
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Dynamic as well as stable protein interactions contribute to genome function and maintenance
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Aberrant base excision repair pathway of oxidatively damaged DNA: Implications for degenerative diseases
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FACT subunit Spt16 controls UVSSA recruitment to lesion-stalled RNA Pol II and stimulates TC-NER
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Nucleotide Excision Repair in Higher Eukaryotes: Mechanism of Primary Damage Recognition in Global Genome Repair
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Nucleotide Excision Repair by Mutant Xeroderma Pigmentosum Group A (XPA) Proteins with Deficiency in Interaction with RPA
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Polymorphisms in nucleotide excision repair genes, smoking and intake of fruit and vegetables in relation to lung cancer
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Cellular Concentrations of DDB2 Regulate Dynamic Binding of DDB1 at UV-Induced DNA Damage
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Xeroderma pigmentosum: a case report and review of the literature
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Cooperative Interaction of Human XPA Stabilizes and Enhances Specific Binding of XPA to DNA Damage
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Elevation of XPA protein level in testis tumor cells without increasing resistance to cisplatin or UV radiation
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Two interaction surfaces between XPA and RPA organize the preincision complex in nucleotide excision repair
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Cisplatin induces cytoplasmic to nuclear translocation of nucleotide excision repair factors among spiral ganglion neurons
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Crosslinking of the NER damage recognition proteins XPC-HR23B, XPA and RPA to photoreactive probes that mimic DNA damages
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Xeroderma Pigmentosum Group A Promotes Autophagy to Facilitate Cisplatin Resistance in Melanoma Cells through the Activation of PARP1
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XPA Gene, Its Product and Biological Roles
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Nucleotide Excision Repair: Finely Tuned Molecular Orchestra of Early Pre‐incision Events
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Differential contribution of XPC, RAD23A, RAD23B and CENTRIN 2 to the UV-response in human cells
Renaud, E., Miccoli, L., Zacal, N., Biard, D. S. F., Craescu, C. T., Rainbow, A. J., & Angulo, J. F. (2011) · DNA repair · doi:10.1016/j.dnarep.2011.05.003 · Cited by 28 · see citing works
UV-Induced Nuclear Import of XPA Is Mediated by Importin-α4 in An ATR-Dependent Manner
Li, Z., Musich, P. R., Cartwright, B. M., Wang, H., & Zou, Y. (2013) · PLoS ONE · doi:10.1371/journal.pone.0068297 · Cited by 26 · see citing works
“Formaldehyde rather than methanol was employed in the reports of a nucleus-only location for XPA [38,51,52].”
Background
Nucleotide Excision Repair and its Connection with Cancer and Ageing
Andressoo, J., Hoeijmakers, J. H. J., & de Waard, H. (2006) · Springer eBooks · doi:10.1007/1-4020-3764-3_3 · Cited by 24 · see citing works
Self-citation
Robustness of DNA Repair through Collective Rate Control
Verbruggen, P., Heinemann, T., Manders, E. M. M., von Bornstaedt, G., DRIEL, R. V., & Höfer, T. (2014) · PLoS Computational Biology · doi:10.1371/journal.pcbi.1003438 · Cited by 24 · see citing works
Xeroderma Pigmentosa Group A (XPA), Nucleotide Excision Repair and Regulation by ATR in Response to Ultraviolet Irradiation
Musich, P. R., Li, Z., & Zou, Y. (2017) · Advances in Experimental Medicine and Biology · doi:10.1007/978-3-319-56017-5_4 · Cited by 23 · see citing works
Frontiers in fluorescence microscopy
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Single molecule analysis reveals monomeric XPA bends DNA and undergoes episodic linear diffusion during damage search
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Other Proteins Interacting with XP Proteins
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A haplotype encompassing the variant allele of DNA repair gene polymorphism ERCC2/XPD Lys751Gln but not the variant allele of Asp312Asn is associated with risk of lung cancer in a northeastern Chinese population
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Localization of xeroderma pigmentosum group A protein and replication protein A on damaged DNA in nucleotide excision repair
Krasikova, Y. S., Rechkunova, N. I., Maltseva, E. A., Petruseva, I. O., & Lavrik, O. I. (2010) · Nucleic Acids Research · doi:10.1093/nar/gkq649 · Cited by 71 · see citing works
The XPA Protein—Life under Precise Control
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Specific and Efficient Binding of Xeroderma Pigmentosum Complementation Group
(2006)
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
Self-citation
Nucleotide Excision Repair Is Associated with the Replisome and Its Efficiency Depends on a Direct Interaction between XPA and PCNA
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Authors: Rademakers, S., Volker, M., Hoogstraten, D., Nigg, A. L., Moné, M. J., van Zeeland, A. A., Hoeijmakers, J. H. J., Houtsmuller, A. B., & Vermeulen, W.
Affiliations: Medical Genetics Center (DE)
Leiden University Medical Center (NL)
Erasmus MC (NL)
University of Amsterdam (NL)
MGC-Department of Radiation Genetics and Chemical Mutagenesis, Leiden University Medical Center, 2333 AL Leiden
Corresponding author: Vermeulen, Wim
ORCID: Moné, Martijn J.
Hoeijmakers, Jan H. J.
Houtsmuller, Adriaan B.
Vermeulen, Wim
Venue: Molecular and Cellular Biology
Publisher: Informa UK Limited
Published: 2003-08-01
Volume: 23
Issue: 16
Pages: 5755-5767
ISSN: 0270-7306 (ISSN-L)
1098-5549
DOI: 10.1128/mcb.23.16.5755-5767.2003
PMC: PMC166334
OpenAlex: W2165125584
Cited by: 149
References: 65
Citations by year: 2026: 1 · 2025: 1 · 2024: 1 · 2023: 1 · 2022: 4 · 2021: 1 · 2020: 3 · 2019: 5 · 2018: 3 · 2017: 4 · 2016: 6 · 2015: 6 · 2014: 11 · 2013: 3 · 2012: 6
FWCI: 4.00
Type: journal article
Language: en
Open access: green
europepmc.org
Licence: journals.asm.org/non-commercial-tdm-license (tdm)
Locations: Molecular and Cellular Biology (publishedVersion)
Europe PMC (PubMed Central) (publishedVersion)
PubMed Central (publishedVersion)
PubMed (publishedVersion)
EUR Research Repository (Erasmus University Rotterdam) (submittedVersion, other-oa)
RePub (Erasmus University Rotterdam) (submittedVersion, other-oa)
Funders: Nederlandse Organisatie voor Wetenschappelijk Onderzoek (901-01-229, 805-33-441, 903-68-370)
KWF Kankerbestrijding
Topics: Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › DNA Repair Mechanisms
Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Nuclear Structure and Function
Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Diffusion and Search Dynamics
Keywords: XPA, nucleotide excision repair, XPC, replication protein A, DNA damage recognition, UV-induced DNA lesions
MeSH terms: Cell Line, Cell Nucleus, DNA Damage, DNA Repair, DNA-Binding Proteins, Dose-Response Relationship, Radiation, Fibroblasts, Humans, Light, Luminescent Proteins, Microscopy, Fluorescence, Models, Biological, Models, Genetic, Peptides, Time Factors, Transfection, Ultraviolet Rays, Immunoblotting, Protein Structure, Tertiary, DNA, Complementary, Microscopy, Confocal, Green Fluorescent Proteins, Xeroderma Pigmentosum Group A Protein

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Xeroderma pigmentosum group A protein loads as a separate factor onto DNA lesions

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