Transcription-coupled repair of UV damage in the halophilic archaea

Stantial, Nicole; Dumpe, Jarrod; Pietrosimone, Kathryn; Baltazar, Felicia; Crowley, David J.

doi:10.1016/j.dnarep.2016.03.007

Cited by 20 publications

(20 citation statements)

References 27 publications

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“…Global genomic repair (GGR) detects lesions throughout the genome, whereas transcription-coupled repair (TCR) is initiated when RNA polymerases are blocked by lesions on the template DNA strand. TCR was first described in rodent cells, then in human cells, E. coli , yeast and in other organisms (reviewed in Ganesan et al 2012; Hanawalt and Spivak 2008; Kamarthapu and Nudler 2015; Mullenders 2015), including halophilic archaea as recently reported (Stantial et al 2016), and was defined as the recognition and repair of DNA lesions or structures occurring in the transcribed strand of active genes. Interestingly, the first observation of TCR (Mellon et al 1987) was possible because the model lesions utilized in those initial experiments, cyclobutane pyrimidine dimers (CPDs), are repaired inefficiently in non-transcribed DNA in hamster cells, facilitating detection of the faster repair of transcribed strands by TCR.…”

Section: Introductionmentioning

confidence: 99%

Transcription-coupled repair: an update

Spivak

2016

Arch Toxicol

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Nucleotide excision repair (NER) is a versatile pathway that removes helix-distorting DNA lesions from the genomes of organisms across the evolutionary scale, from bacteria to humans. The serial steps in NER involve recognition of lesions, adducts or structures that disrupt the DNA double helix, removal of a short oligonucleotide containing the offending lesion, synthesis of a repair patch copying the opposite undamaged strand, and ligation, to restore the DNA to its original form. Transcription-coupled repair (TCR) is a subpathway of NER dedicated to the repair of lesions that, by virtue of their location on the transcribed strands of active genes, encumber elongation by RNA polymerases. In this review, I report on recent findings that contribute to the elucidation of TCR mechanisms in the bacterium Escherichia coli, the yeast Saccharomyces cerevisiae and human cells. I review general models for the biochemical pathways and how and when cells might choose to utilize TCR or other pathways for repair or bypass of transcription-blocking DNA alterations.

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Section: Introductionmentioning

confidence: 99%

Transcription-coupled repair: an update

Spivak

2016

Arch Toxicol

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“…The requirements for Eta-mediated transcription termination -energy-dependence, a static or slowly elongating TEC, access to upstream DNA sequences and no requirements for kodakarensis, recent support for TCR in related euryarchaea has been provided (53), and thus we accessed the potential for Eta to influence DNA repair by challenging parental and Etadeleted strains of T. kodakarensis to common DNA damaging agents. Exposure to UV light limited the growth of both strains, but the strain deleted for Eta was substantially (at least an order of magnitude) more sensitive to UV exposure than the parental strain ( Figure 3.7G, top panels).…”

Section: Eta Is Not Responsible For Polaritymentioning

confidence: 99%

“…Eukaryotic TFIIE is a heterodimeric complex of TFIIEα and TFIIEβ, but archaeal genomes had previously only been shown to encode a homologue of the alpha subunit (49,50). Eukaryotic RNAPs differ in their requirements for initiation, with RNAP III incorporating homologues of several RNAP II initiation factors as core components of RNAP III (51)(52)(53). Comparisons of the RNAP III subunit hRCP39 revealed a well-conserved archaeal homolog (termed TFEβ) that directly and extensively interacts with TFE (now named TFEα) (20).…”

Section: Regulation Of Transcription Initiationmentioning

confidence: 99%

Factor-dependent archaeal transcription termination

Walker

Luyties

Santangelo

2017

Proc. Natl. Acad. Sci. U.S.A.

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We demonstrate that binding of the conserved and essential archaeal transcription factor TFE to the archaeal RNAP is directed, in part, by interactions with the RpoE subunit of RNAP. As the surfaces involved are conserved in many eukaryotic and archaeal systems, the identified TFE-RNAP interactions are likely conserved in archaeal-eukaryal systems and represent an important point of contact that can influence the efficiency of transcription initiation.While many studies in archaea have focused on elucidating the mechanism of transcription initiation and elongation, studies on termination were slower to emerge.Transcription factors promoting initiation and elongation have been characterized in each Domain but transcription termination factors have only been identified in bacteria and eukarya.Here we characterize the first archaeal termination factor (termed Eta) capable of disrupting the transcription elongation complex, detail the rate of and requirements for Eta-mediated transcription termination and describe a role for Eta in transcription termination in vivo. Etamediated transcription termination is energy-dependent, requires upstream DNA sequences and disrupts transcription elongation complexes to release the nascent RNA to solution. Deletion of TK0566 (encoding Eta) is possible, but results in slow growth and renders cells sensitive to iii DNA damaging agents. Structure-function studies reveal that the N-terminal domain of Eta is not necessary for Eta-mediated termination in vitro, but Thermococcus kodakarensis cells lacking the N-terminal domain exhibit slow growth compared to parental strains. We report the first crystal structure of Eta that will undoubtedly lead to further structure-function analyses. The results obtained argue that the mechanisms employed by termination factors in archaea, eukarya, and bacteria to disrupt the transcription elongation complex may be conserved and that Eta stimulates release of stalled or arrested transcription elongation complexes.iv ACKNOWLEDGEMENTS

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“…The ability of the archaeal RNAP to recognize and arrest transcription at a variety of common DNA lesions is supportive of a role for RNAP in initiating the recently described more rapid repair of template versus non-template DNA lesions in vivo. 34 We demonstrate that transcription elongation by the archaeal RNAP is arrested at a variety of templatestrand DNA lesions in vitro. Identical non-template strand lesions do not result in any notable reduction in elongation kinetics.…”

Section: Discussionmentioning

confidence: 85%

“…Our results are supportive of the recent demonstration of transcription-coupled DNA repair (TCR) in some Archaea, a pathway dependent on the strand-specific recognition of DNA lesions by RNAP. 34…”

Section: Introductionmentioning

confidence: 99%

Archaeal RNA polymerase arrests transcription at DNA lesions

Gehring

Santangelo

2017

Transcription

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Transcription elongation is not uniform and transcription is often hindered by protein-bound factors or DNA lesions that limit translocation and impair catalysis. Despite the high degree of sequence and structural homology of the multi-subunit RNA polymerases (RNAP), substantial differences in response to DNA lesions have been reported. Archaea encode only a single RNAP with striking structural conservation with eukaryotic RNAP II (Pol II). Here, we demonstrate that the archaeal RNAP from Thermococcus kodakarensis is sensitive to a variety of DNA lesions that pause and arrest RNAP at or adjacent to the site of DNA damage. DNA damage only halts elongation when present in the template strand, and the damage often results in RNAP arresting such that the lesion would be encapsulated with the transcription elongation complex. The strand-specific halt to archaeal transcription elongation on modified templates is supportive of RNAP recognizing DNA damage and potentially initiating DNA repair through a process akin to the well-described transcription-coupled DNA repair (TCR) pathways in Bacteria and Eukarya.

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Transcription-coupled repair of UV damage in the halophilic archaea

Cited by 20 publications

References 27 publications

Transcription-coupled repair: an update

Transcription-coupled repair: an update

Factor-dependent archaeal transcription termination

Archaeal RNA polymerase arrests transcription at DNA lesions

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