Genetic Analysis of Repair and Damage Tolerance Mechanisms for DNA-Protein Cross-Links in Escherichia coli

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Published inJournal of Bacteriology Vol. 191; no. 18; pp. 5657 - 5668
Main Authors Salem, Amir M H, Nakano, Toshiaki, Takuwa, Minako, Matoba, Nagisa, Tsuboi, Tomohiro, Terato, Hiroaki, Yamamoto, Kazuo, Yamada, Masami, Nohmi, Takehiko, Ide, Hiroshi
Format Journal Article
LanguageEnglish
Published United States American Society for Microbiology 01.09.2009
American Society for Microbiology (ASM)
Subjects
Azacitidine - pharmacology
Bacteriology
Cross-Linking Reagents - metabolism
Cross-Linking Reagents - pharmacology
DNA damage
DNA Damage - genetics
DNA Glycosylases - genetics
DNA Glycosylases - metabolism
DNA repair
DNA Repair - genetics
DNA Replication
DNA, Bacterial - chemistry
DNA, Bacterial - metabolism
E coli
Escherichia coli
Escherichia coli K12 - drug effects
Escherichia coli K12 - genetics
Escherichia coli K12 - growth & development
Escherichia coli K12 - metabolism
Escherichia coli Proteins - chemistry
Escherichia coli Proteins - genetics
Escherichia coli Proteins - metabolism
Formaldehyde - pharmacology
Genetic recombination
Genetics and Molecular Biology
Mutation
Protein Binding
Proteins
Recombination, Genetic
Online AccessGet full text

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DNA-protein cross-links (DPCs) are unique among DNA lesions in their unusually bulky nature. We have recently shown that nucleotide excision repair (NER) and RecBCD-dependent homologous recombination (HR) collaboratively alleviate the lethal effect of DPCs in Escherichia coli. In this study, to gain further insight into the damage-processing mechanism for DPCs, we assessed the sensitivities of a panel of repair-deficient E. coli mutants to DPC-inducing agents, including formaldehyde (FA) and 5-azacytidine (azaC). We show here that the damage tolerance mechanism involving HR and subsequent replication restart (RR) provides the most effective means of cell survival against DPCs. Translesion synthesis does not serve as an alternative damage tolerance mechanism for DPCs in cell survival. Elimination of DPCs from the genome relies primarily on NER, which provides a second and moderately effective means of cell survival against DPCs. Interestingly, Cho rather than UvrC seems to be an effective nuclease for the NER of DPCs. Together with the genes responsible for HR, RR, and NER, the mutation of genes involved in several aspects of DNA repair and transactions, such as recQ, xth nfo, dksA, and topA, rendered cells slightly but significantly sensitive to FA but not azaC, possibly reflecting the complexity of DPCs or cryptic lesions induced by FA. UvrD may have an additional role outside NER, since the uvrD mutation conferred a slight azaC sensitivity on cells. Finally, DNA glycosylases mitigate azaC toxicity, independently of the repair of DPCs, presumably by removing 5-azacytosine or its degradation product from the chromosome. [PUBLICATION ABSTRACT]
DNA-protein cross-links (DPCs) are unique among DNA lesions in their unusually bulky nature. We have recently shown that nucleotide excision repair (NER) and RecBCD-dependent homologous recombination (HR) collaboratively alleviate the lethal effect of DPCs in Escherichia coli. In this study, to gain further insight into the damage-processing mechanism for DPCs, we assessed the sensitivities of a panel of repair-deficient E. coli mutants to DPC-inducing agents, including formaldehyde (FA) and 5-azacytidine (azaC). We show here that the damage tolerance mechanism involving HR and subsequent replication restart (RR) provides the most effective means of cell survival against DPCs. Translesion synthesis does not serve as an alternative damage tolerance mechanism for DPCs in cell survival. Elimination of DPCs from the genome relies primarily on NER, which provides a second and moderately effective means of cell survival against DPCs. Interestingly, Cho rather than UvrC seems to be an effective nuclease for the NER of DPCs. Together with the genes responsible for HR, RR, and NER, the mutation of genes involved in several aspects of DNA repair and transactions, such as recQ, xth nfo, dksA, and topA, rendered cells slightly but significantly sensitive to FA but not azaC, possibly reflecting the complexity of DPCs or cryptic lesions induced by FA. UvrD may have an additional role outside NER, since the uvrD mutation conferred a slight azaC sensitivity on cells. Finally, DNA glycosylases mitigate azaC toxicity, independently of the repair of DPCs, presumably by removing 5-azacytosine or its degradation product from the chromosome.
DNA-protein cross-links (DPCs) are unique among DNA lesions in their unusually bulky nature. We have recently shown that nucleotide excision repair (NER) and RecBCD-dependent homologous recombination (HR) collaboratively alleviate the lethal effect of DPCs in Escherichia coli . In this study, to gain further insight into the damage-processing mechanism for DPCs, we assessed the sensitivities of a panel of repair-deficient E. coli mutants to DPC-inducing agents, including formaldehyde (FA) and 5-azacytidine (azaC). We show here that the damage tolerance mechanism involving HR and subsequent replication restart (RR) provides the most effective means of cell survival against DPCs. Translesion synthesis does not serve as an alternative damage tolerance mechanism for DPCs in cell survival. Elimination of DPCs from the genome relies primarily on NER, which provides a second and moderately effective means of cell survival against DPCs. Interestingly, Cho rather than UvrC seems to be an effective nuclease for the NER of DPCs. Together with the genes responsible for HR, RR, and NER, the mutation of genes involved in several aspects of DNA repair and transactions, such as recQ , xth nfo , dksA , and topA , rendered cells slightly but significantly sensitive to FA but not azaC, possibly reflecting the complexity of DPCs or cryptic lesions induced by FA. UvrD may have an additional role outside NER, since the uvrD mutation conferred a slight azaC sensitivity on cells. Finally, DNA glycosylases mitigate azaC toxicity, independently of the repair of DPCs, presumably by removing 5-azacytosine or its degradation product from the chromosome.
ABSTRACT DNA-protein cross-links (DPCs) are unique among DNA lesions in their unusually bulky nature. We have recently shown that nucleotide excision repair (NER) and RecBCD-dependent homologous recombination (HR) collaboratively alleviate the lethal effect of DPCs in Escherichia coli . In this study, to gain further insight into the damage-processing mechanism for DPCs, we assessed the sensitivities of a panel of repair-deficient E. coli mutants to DPC-inducing agents, including formaldehyde (FA) and 5-azacytidine (azaC). We show here that the damage tolerance mechanism involving HR and subsequent replication restart (RR) provides the most effective means of cell survival against DPCs. Translesion synthesis does not serve as an alternative damage tolerance mechanism for DPCs in cell survival. Elimination of DPCs from the genome relies primarily on NER, which provides a second and moderately effective means of cell survival against DPCs. Interestingly, Cho rather than UvrC seems to be an effective nuclease for the NER of DPCs. Together with the genes responsible for HR, RR, and NER, the mutation of genes involved in several aspects of DNA repair and transactions, such as recQ , xth nfo , dksA , and topA , rendered cells slightly but significantly sensitive to FA but not azaC, possibly reflecting the complexity of DPCs or cryptic lesions induced by FA. UvrD may have an additional role outside NER, since the uvrD mutation conferred a slight azaC sensitivity on cells. Finally, DNA glycosylases mitigate azaC toxicity, independently of the repair of DPCs, presumably by removing 5-azacytosine or its degradation product from the chromosome.
Author Amir M. H. Salem
Masami Yamada
Nagisa Matoba
Toshiaki Nakano
Takehiko Nohmi
Kazuo Yamamoto
Hiroshi Ide
Hiroaki Terato
Tomohiro Tsuboi
Minako Takuwa
AuthorAffiliation Department of Mathematical and Life Sciences, Graduate School of Science, Hiroshima University, Higashi-Hiroshima 739-8526, Japan, 1 Department of Biomolecular Sciences, Graduate School of Life Sciences, Tohoku University, Sendai 980-8578, Japan, 2 Division of Genetics and Mutagenesis, National Institute of Health Sciences, Tokyo 158-8501, Japan 3
AuthorAffiliation_xml – name: Department of Mathematical and Life Sciences, Graduate School of Science, Hiroshima University, Higashi-Hiroshima 739-8526, Japan, 1 Department of Biomolecular Sciences, Graduate School of Life Sciences, Tohoku University, Sendai 980-8578, Japan, 2 Division of Genetics and Mutagenesis, National Institute of Health Sciences, Tokyo 158-8501, Japan 3
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BackLink https://www.ncbi.nlm.nih.gov/pubmed/19617358$$D View this record in MEDLINE/PubMed
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Present address: Analytical Research Center for Experimental Sciences, Saga University, Nabeshima, Saga 849-8501, Japan.
Corresponding author. Mailing address: Department of Mathematical and Life Sciences, Graduate School of Science, Hiroshima University, Higashi-Hiroshima 739-8526, Japan. Phone and fax: 81-82-424-7457. E-mail: ideh@hiroshima-u.ac.jp
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SSID ssj0014452
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Snippet Article Usage Stats Services JB Citing Articles Google Scholar PubMed Related Content Social Bookmarking CiteULike Delicious Digg Facebook Google+ Mendeley...
DNA-protein cross-links (DPCs) are unique among DNA lesions in their unusually bulky nature. We have recently shown that nucleotide excision repair (NER) and...
ABSTRACT DNA-protein cross-links (DPCs) are unique among DNA lesions in their unusually bulky nature. We have recently shown that nucleotide excision repair...
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crossref
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SourceType Open Access Repository
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Index Database
Publisher
StartPage 5657
SubjectTerms Azacitidine - pharmacology
Bacteriology
Cross-Linking Reagents - metabolism
Cross-Linking Reagents - pharmacology
DNA damage
DNA Damage - genetics
DNA Glycosylases - genetics
DNA Glycosylases - metabolism
DNA repair
DNA Repair - genetics
DNA Replication
DNA, Bacterial - chemistry
DNA, Bacterial - metabolism
E coli
Escherichia coli
Escherichia coli K12 - drug effects
Escherichia coli K12 - genetics
Escherichia coli K12 - growth & development
Escherichia coli K12 - metabolism
Escherichia coli Proteins - chemistry
Escherichia coli Proteins - genetics
Escherichia coli Proteins - metabolism
Formaldehyde - pharmacology
Genetic recombination
Genetics and Molecular Biology
Mutation
Protein Binding
Proteins
Recombination, Genetic
Title Genetic Analysis of Repair and Damage Tolerance Mechanisms for DNA-Protein Cross-Links in Escherichia coli
URI http://jb.asm.org/content/191/18/5657.abstract
https://www.ncbi.nlm.nih.gov/pubmed/19617358
https://www.proquest.com/docview/227079220
https://search.proquest.com/docview/21326868
https://pubmed.ncbi.nlm.nih.gov/PMC2737949
Volume 191
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