Sancar, A. Mechanisms of DNA repair by photolyase and excision nuclease (Nobel Lecture). Angew. Chem. Int. Ed. Engl. 55, 8502–8527 (2016).
Google Scholar
Adebali, O., Chiou, Y. Y., Hu, J. C., Sancar, A. & Selby, C. P. Genome-wide transcription-coupled repair in Escherichia coli is mediated by the Mfd translocase. Proc. Natl Acad. Sci. USA 114, E2116–E2125 (2017).
Google Scholar
Adebali, O., Sancar, A. & Selby, C. P. Mfd translocase is necessary and sufficient for transcription-coupled repair in Escherichia coli. J. Biol. Chem. 292, 18386–18391 (2017).
Google Scholar
Marteijn, J. A., Lans, H., Vermeulen, W. & Hoeijmakers, J. H. Understanding nucleotide excision repair and its roles in cancer and ageing. Nat. Rev. Mol. Cell Biol. 15, 465–481 (2014).
Google Scholar
Kisker, C., Kuper, J. & Van Houten, B. Prokaryotic nucleotide excision repair. Cold Spring Harb. Perspect. Biol. 5, a012591 (2013).
Google Scholar
Kuper, J. & Kisker, C. Damage recognition in nucleotide excision DNA repair. Curr. Opin. Struct. Biol. 22, 88–93 (2012).
Google Scholar
Hanawalt, P. C. & Spivak, G. Transcription-coupled DNA repair: two decades of progress and surprises. Nat. Rev. Mol. Cell Biol. 9, 958–970 (2008).
Google Scholar
Pani, B. & Nudler, E. Mechanistic insights into transcription coupled DNA repair. DNA Repair 56, 42–50 (2017).
Google Scholar
Spivak, G. Transcription-coupled repair: an update. Arch. Toxicol. 90, 2583–2594 (2016).
Google Scholar
Selby, C. P. & Sancar, A. Molecular mechanism of transcription-repair coupling. Science 260, 53–58 (1993).
Google Scholar
Cohen, S. E. et al. Roles for the transcription elongation factor NusA in both DNA repair and damage tolerance pathways in Escherichia coli. Proc. Natl Acad. Sci. USA 107, 15517–15522 (2010).
Google Scholar
Kamarthapu, V. et al. ppGpp couples transcription to DNA repair in E. coli. Science 352, 993–996 (2016).
Google Scholar
Ragheb, M. N. et al. Inhibiting the evolution of antibiotic resistance. Mol. Cell 73, 157–165 (2019).
Google Scholar
Schalow, B. J., Courcelle, C. T. & Courcelle, J. Mfd is required for rapid recovery of transcription following UV-induced DNA damage but not oxidative DNA damage in Escherichia coli. J. Bacteriol. 194, 2637–2645 (2012).
Google Scholar
Witkin, E. M. Radiation-induced mutations and their repair. Science 152, 1345–1353 (1966).
Google Scholar
Kamarthapu, V. & Nudler, E. Rethinking transcription coupled DNA repair. Curr. Opin. Microbiol. 24, 15–20 (2015).
Google Scholar
Mullenders, L. DNA damage mediated transcription arrest: step back to go forward. DNA Repair 36, 28–35 (2015).
Google Scholar
Epshtein, V. et al. UvrD facilitates DNA repair by pulling RNA polymerase backwards. Nature 505, 372–377 (2014).
Google Scholar
Rasouly, A., Pani, B. & Nudler, E. A magic spot in genome maintenance. Trends Genet. 33, 58–67 (2017).
Google Scholar
Lin, C. G., Kovalsky, O. & Grossman, L. Transcription coupled nucleotide excision repair by isolated Escherichia coli membrane-associated nucleoids. Nucleic Acids Res. 26, 1466–1472 (1998).
Google Scholar
Manelyte, L., Kim, Y. I., Smith, A. J., Smith, R. M. & Savery, N. J. Regulation and rate enhancement during transcription-coupled DNA repair. Mol. Cell 40, 714–724 (2010).
Google Scholar
Wang, C. Y. et al. Structural basis of transcription-translation coupling. Science 369, 1359–1365 (2020).
Google Scholar
Jia, H. F. et al. Rotations of the 2B sub-domain of E. coli UvrD helicase/translocase coupled to nucleotide and DNA binding. J. Mol. Biol. 411, 633–648 (2011).
Google Scholar
Lee, J. Y. & Yang, W. UvrD helicase unwinds DNA one base pair at a time by a two-part power stroke. Cell 127, 1349–1360 (2006).
Google Scholar
Pakotiprapha, D. et al. Crystal structure of Bacillus stearothermophilus UvrA provides insight into ATP-modulated dimerization, UvrB interaction, and DNA binding. Mol. Cell 29, 122–133 (2008).
Google Scholar
Pakotiprapha, D., Liu, Y., Verdine, G. L. & Jeruzalmi, D. A structural model for the damage-sensing complex in bacterial nucleotide excision repair. J. Biol. Chem. 284, 12837–12844 (2009).
Google Scholar
Pakotiprapha, D., Samuels, M., Shen, K. N., Hu, J. H. & Jeruzalmi, D. Structure and mechanism of the UvrA–UvrB DNA damage sensor. Nat. Struct. Mol. Biol. 19, 291–U247 (2012).
Google Scholar
Jaciuk, M. et al. A combined structural and biochemical approach reveals translocation and stalling of UvrB on the DNA lesion as a mechanism of damage verification in bacterial nucleotide excision repair. DNA Repair 85, 102746 (2020).
Google Scholar
Nguyen, B., Ordabayev, Y., Sokoloski, J. E., Weiland, E. & Lohman, T. M. Large domain movements upon UvrD dimerization and helicase activation. Proc. Natl Acad. Sci. USA 114, 12178–12183 (2017).
Google Scholar
Duchi, D., Mazumder, A., Malinen, A. M., Ebright, R. H. & Kapanidis, A. N. The RNA polymerase clamp interconverts dynamically among three states and is stabilized in a partly closed state by ppGpp. Nucleic Acids Res. 46, 7284–7295 (2018).
Google Scholar
Zuo, Y. H., Wang, Y. M. & Steitz, T. A. The mechanism of E. coli RNA polymerase regulation by ppGpp is suggested by the structure of their complex. Mol. Cell 50, 430–436 (2013).
Google Scholar
Kawale, A. A. & Burmann, B. M. UvrD helicase–RNA polymerase interactions are governed by UvrD’s carboxy-terminal Tudor domain. Commun. Biol. 3, 607 (2020).
Google Scholar
Sanders, K. et al. The structure and function of an RNA polymerase interaction domain in the PcrA/UvrD helicase. Nucleic Acids Res. 45, 3875–3887 (2017).
Google Scholar
Urrutia-Irazabal, I., Ault, J. R., Sobott, F., Savery, N. J. & Dillingham, M. S. Analysis of the PcrA–RNA polymerase complex reveals a helicase interaction motif and a role for PcrA/UvrD helicase in the suppression of R-loops. eLife 10, e68829 (2021).
Google Scholar
Manelyte, L. et al. The unstructured C-terminal extension of UvrD interacts with UvrB, but is dispensable for nucleotide excision repair. DNA Repair 8, 1300–1310 (2009).
Google Scholar
Martinez, B., Bharati, B. K., Epshtein, V. & Nudler, E. Pervasive transcription-coupled DNA repair in E. coli. Nat. Commun., https://doi.org/10.1038/s41467-022-28871-y (2022).
Courcelle, J., Khodursky, A., Peter, B., Brown, P. O. & Hanawalt, P. C. Comparative gene expression profiles following UV exposure in wild-type and SOS-deficient Escherichia coli. Genetics 158, 41–64 (2001).
Google Scholar
Thomassen, G. O. et al. Tiling array analysis of UV treated Escherichia coli predicts novel differentially expressed small peptides. PLoS ONE 5, e15356 (2010).
Google Scholar
Lin, L. L. & Little, J. W. Autodigestion and RecA-dependent cleavage of Ind− mutant LexA proteins. J. Mol. Biol. 210, 439–452 (1989).
Google Scholar
Richardson, J. P. Preventing the synthesis of unused transcripts by Rho factor. Cell 64, 1047–1049 (1991).
Google Scholar
Jain, S., Gupta, R. & Sen, R. Rho-dependent transcription termination in bacteria recycles RNA polymerases stalled at DNA lesions. Nat. Commun. 10, 1207 (2019).
Google Scholar
Bryant, J. A., Sellars, L. E., Busby, S. J. W. & Lee, D. J. Chromosome position effects on gene expression in Escherichia coli K-12. Nucleic Acids Res. 42, 11383–11392 (2014).
Google Scholar
Perdiz, D. et al. Distribution and repair of bipyrimidine photoproducts in solar UV-irradiated mammalian cells. Possible role of Dewar photoproducts in solar mutagenesis. J. Biol. Chem. 275, 26732–26742 (2000).
Google Scholar
Ikenaga, M., Ichikawa-Ryo, H. & Kondo, S. The major cause of inactivation and mutation by 4-nitroquinoline 1-oixde in Escherichia coli: excisable 4NQO-purine adducts. J. Mol. Biol. 92, 341–356 (1975).
Google Scholar
Zdraveski, Z. Z., Mello, J. A., Marinus, M. G. & Essigmann, J. M. Multiple pathways of recombination define cellular responses to cisplatin. Chem. Biol. 7, 39–50 (2000).
Google Scholar
Wade, J. T. & Grainger, D. C. Pervasive transcription: illuminating the dark matter of bacterial transcriptomes. Nat. Rev. Microbiol. 12, 647–653 (2014).
Google Scholar
Kunala, S. & Brash, D. E. Intragenic domains of strand-specific repair in Escherichia coli. J. Mol. Biol. 246, 264–272 (1995).
Google Scholar
Gaul, L. & Svejstrup, J. Q. Transcription-coupled repair and the transcriptional response to UV-irradiation. DNA Repair 107, 103208 (2021).
Google Scholar
Duan, M., Selvam, K., Wyrick, J. J. & Mao, P. Genome-wide role of Rad26 in promoting transcription-coupled nucleotide excision repair in yeast chromatin. Proc. Natl Acad. Sci. USA 117, 18608–18616 (2020).
Google Scholar
Oh, J., Xu, J., Chong, J. & Wang, D. Molecular basis of transcriptional pausing, stalling, and transcription-coupled repair initiation. Biochim. Biophys. Acta Gene Regul. Mech. 1864, 194659 (2021).
Google Scholar
Velez-Cruz, R. & Egly, J. M. Cockayne syndrome group B (CSB) protein: at the crossroads of transcriptional networks. Mech. Ageing Dev. 134, 234–242 (2013).
Google Scholar
Ghosh-Roy, S., Das, D., Chowdhury, D., Smerdon, M. J. & Chaudhuri, R. N. Rad26, the transcription-coupled repair factor in yeast, is required for removal of stalled RNA polymerase-II following UV irradiation. PLoS ONE 8, e72090 (2013).
Google Scholar
Li, W. T. & Li, S. S. Facilitators and repressors of transcription-coupled DNA repair in Saccharomyces cerevisiae. Photochem. Photobiol. 93, 259–267 (2017).
Google Scholar
Mayne, L. V. & Lehmann, A. R. Failure of RNA synthesis to recover after UV irradiation: an early defect in cells from individuals with Cockayne’s syndrome and xeroderma pigmentosum. Cancer Res. 42, 1473–1478 (1982).
Google Scholar
Zhao, D. D. et al. CRISPR/Cas9-assisted gRNA-free one-step genome editing with no sequence limitations and improved targeting efficiency. Sci Rep. 7, 16624 (2017).
Google Scholar
Baba, T. et al. Construction of Escherichia coli K-12 in-frame, single-gene knockout mutants: the Keio collection. Mol. Syst. Biol. 2, 2006.0008 (2006).
Google Scholar
Datsenko, K. A. & Wanner, B. L. One-step inactivation of chromosomal genes in Escherichia coli K-12 using PCR products. Proc. Natl Acad. Sci. USA 97, 6640–6645 (2000).
Google Scholar
Kitagawa, M. et al. Complete set of ORF clones of Escherichia coli ASKA library (a complete set of E. coli K-12 ORF archive): unique resources for biological research. DNA Res. 12, 291–299 (2005).
Google Scholar
Schneider, C. A., Rasband, W. S. & Eliceiri, K. W. NIH Image to ImageJ: 25 years of image analysis. Nat. Methods 9, 671–675 (2012).
Google Scholar
Carter, J. D. & LaBean, T. H. Coupling strategies for the synthesis of peptide-oligonucleotide conjugates for patterned synthetic biomineralization. J. Nucleic Acids 2011, 926595 (2011).
Google Scholar
Ghosh, S. S., Kao, P. M., Mccue, A. W. & Chappelle, H. L. Use of maleimide-thiol coupling chemistry for efficient syntheses of oligonucleotide-enzyme conjugate hybridization probes. Bioconjugate Chem. 1, 71–76 (1990).
Google Scholar
Hermanson, G. T. Bioconjugate Techniques 3rd edn (Academic, 2013).
Grabarek, Z. & Gergely, J. Zero-length crosslinking procedure with the use of active esters. Anal. Biochem. 185, 131–135 (1990).
Google Scholar
Staros, J. V., Wright, R. W. & Swingle, D. M. Enhancement by N-hydroxysulfosuccinimide of water-soluble carbodiimide-mediated coupling reactions. Anal. Biochem. 156, 220–222 (1986).
Google Scholar
Lu, L. et al. Identification of MS-cleavable and noncleavable chemically cross-linked peptides with MetaMorpheus. J. Proteome Res. 17, 2370–2376 (2018).
Google Scholar
Wisniewski, J. R. Label-free and standard-free absolute quantitative proteomics using the “total protein” and “proteomic ruler” approaches. Methods Enzymol. 585, 49–60 (2017).
Google Scholar
Meyer, A. et al. Systematic analysis of protein-detergent complexes applying dynamic light scattering to optimize solutions for crystallization trials. Acta Crystallogr. F 71, 75–81 (2015).
Google Scholar
Chi, H. et al. Comprehensive identification of peptides in tandem mass spectra using an efficient open search engine. Nat. Biotechnol. 36, 1059–1061 (2018).
Google Scholar
Chen, Z. L. et al. A high-speed search engine pLink 2 with systematic evaluation for proteome-scale identification of cross-linked peptides. Nat. Commun. 10, 3404 (2019).
Google Scholar
Spivak, G. & Hanawalt, P. C. Determination of damage and repair in specific DNA Sequences. Methods 7, 147–161 (1995).
Google Scholar
Iyer, S., Park, B. R. & Kim, M. Absolute quantitative measurement of transcriptional kinetic parameters in vivo. Nucleic Acids Res. 44, e142 (2016).
Google Scholar
Dannenmann, B. et al. Simultaneous quantification of DNA damage and mitochondrial copy number by long-run DNA-damage quantification (LORD-Q). Oncotarget 8, 112417–112425 (2017).
Google Scholar
Lehle, S. et al. LORD-Q: a long-run real-time PCR-based DNA-damage quantification method for nuclear and mitochondrial genome analysis. Nucleic Acids Res. 42, e41 (2014).
Google Scholar
Rothfuss, O., Gasser, T. & Patenge, N. Analysis of differential DNA damage in the mitochondrial genome employing a semi-long run real-time PCR approach. Nucleic Acids Res. 38, e24 (2010).
Google Scholar
Zhu, S. & Coffman, J. A. Simple and fast quantification of DNA damage by real-time PCR, and its application to nuclear and mitochondrial DNA from multiple tissues of aging zebrafish. BMC Res. Notes 10, 269 (2017).
Google Scholar
Crowley, D. J. & Hanawalt, P. C. Induction of the SOS response increases the efficiency of global nucleotide excision repair of cyclobutane pyrimidine dimers, but not 6-4 photoproducts, in UV-irradiated Escherichia coli. J. Bacteriol. 180, 3345–3352 (1998).
Google Scholar
Koehler, D. R., Courcelle, J. & Hanawalt, P. C. Kinetics of pyrimidine(6-4)pyrimidone photoproduct repair in Escherichia coli. J. Bacteriol. 178, 1347–1350 (1996).
Google Scholar
Kai-Feng, H., Sidorova, J. M., Nghiem, P. & Kawasumi, M. The 6-4 photoproduct is the trigger of UV-induced replication blockage and ATR activation. Proc. Natl Acad. Sci. USA 117, 12806–12816 (2020).
Davis, S. E. et al. Mapping E. coli RNA polymerase and associated transcription factors and identifying promoters genome-wide. Methods Enzymol. 498, 449–471 (2011).
Google Scholar
Lee, C., Kim, J., Shin, S. G. & Hwang, S. Absolute and relative QPCR quantification of plasmid copy number in Escherichia coli. J. Biotechnol. 123, 273–280 (2006).
Google Scholar
Epshtein, V. & Nudler, E. Cooperation between RNA polymerase molecules in transcription elongation. Science 300, 801–805 (2003).
Google Scholar
Yang, J. & Zhang, Y. I-TASSER server: new development for protein structure and function predictions. Nucleic Acids Res. 43, W174–W181 (2015).
Google Scholar
Rossi, F. et al. The biological and structural characterization of Mycobacterium tuberculosis UvrA provides novel insights into its mechanism of action. Nucleic Acids Res. 39, 7316–7328 (2011).
Google Scholar
Vogel, U. & Jensen, K. F. NusA is required for ribosomal antitermination and for modulation of the transcription elongation rate of both antiterminated RNA and mRNA. J. Biol. Chem. 272, 12265–12271 (1997).
Google Scholar
Belogurov, G. A. & Artsimovitch, I. The mechanisms of substrate selection, catalysis, and translocation by the elongating RNA polymerase. J. Mol. Biol. 431, 3975–4006 (2019).
Google Scholar
Canutescu, A. A., Shelenkov, A. A. & Dunbrack, R. L. A graph-theory algorithm for rapid protein side-chain prediction. Protein Sci. 12, 2001–2014 (2003).
Google Scholar
Krieger, E. & Vriend, G. New ways to boost molecular dynamics simulations. J. Comput. Chem. 36, 996–1007 (2015).
Google Scholar
Orban-Nemeth, Z. et al. Structural prediction of protein models using distance restraints derived from cross-linking mass spectrometry data. Nat. Protoc. 13, 1724–1724 (2018).
Google Scholar
Duhovny, D., Nussinov, R. & Wolfson, H. J. In Algorithms in Bioinformatics. WABI 2002. Lecture Notes in Computer Science vol. 2452 (eds Guigó, R. & Gusfield, D.) 185–200 (Springer, 2002).
Schneidman-Duhovny, D., Inbar, Y., Nussinov, R. & Wolfson, H. J. PatchDock and SymmDock: servers for rigid and symmetric docking. Nucleic Acids Res. 33, W363–W367 (2005).
Google Scholar
Bullock, J. M. A., Schwab, J., Thalassinos, K. & Topf, M. The importance of non-accessible crosslinks and solvent accessible surface distance in modeling proteins with restraints from crosslinking mass spectrometry. Mol. Cell. Proteomics 15, 2491–2500 (2016).
Google Scholar
Martin, A. C. R. & Porter, C. T. ProFit V3.1 http://www.bioinf.org.uk/software/profit/ (2009).
Chen, V. B. et al. MolProbity: all-atom structure validation for macromolecular crystallography. Acta Crystallogr. D 66, 12–21 (2010).
Google Scholar
Severinov, K., Mooney, R., Darst, S. A. & Landick, R. Tethering of the large subunits of Escherichia coli RNA polymerase. J. Biol. Chem. 272, 24137–24140 (1997).
Google Scholar
Zhang, Y. et al. Structural basis of transcription initiation. Science 338, 1076–1080 (2012).
Google Scholar
Opalka, N. et al. Complete structural model of Escherichia coli RNA polymerase from a hybrid approach. PLoS Biol. 8, e1000483 (2010).
Google Scholar
Skubak, P. et al. A new MR-SAD algorithm for the automatic building of protein models from low-resolution X-ray data and a poor starting model. IUCrJ 5, 166–171 (2018).
Google Scholar
Cowtan, K. The Buccaneer software for automated model building. 1. Tracing protein chains. Acta Crystallogr. D 62, 1002–1011 (2006).
Google Scholar
Emsley, P., Lohkamp, B., Scott, W. G. & Cowtan, K. Features and development of Coot. Acta Crystallogr. D 66, 486–501 (2010).
Google Scholar
Murshudov, G. N. et al. REFMAC5 for the refinement of macromolecular crystal structures. Acta Crystallogr. D 67, 355–367 (2011).
Google Scholar
Nakagawa, N. et al. Crystal structure of Thermus thermophilus HB8 UvrB protein, a key enzyme of nucleotide excision repair. J. Biochem. 126, 986–990 (1999).
Google Scholar
Lee, S. J., Sung, R. J. & Verdine, G. L. Mechanism of DNA lesion homing and recognition by the Uvr nucleotide excision repair system. Research 2019, 5641746 (2019).
Google Scholar
Orren, D. K. & Sancar, A. The (A)BC excinuclease of Escherichia coli has only the Uvrb and Uvrc subunits in the incision complex. Proc. Natl Acad. Sci. USA 86, 5237–5241 (1989).
Google Scholar
Zou, Y. & Van Houten, B. Strand opening by the UvrA(2)B complex allows dynamic recognition of DNA damage. EMBO J. 18, 4889–4901 (1999).
Google Scholar
Verhoeven, E. E. A., Wyman, C., Moolenaar, G. F. & Goosen, N. The presence of two UvrB subunits in the UvrAB complex ensures damage detection in both DNA strands. EMBO J. 21, 4196–4205 (2002).
Google Scholar
Brugger, C. et al. Molecular determinants for dsDNA translocation by the transcription-repair coupling and evolvability factor Mfd. Nat. Commun. 11, 3740 (2020).
Google Scholar
Deaconescu, A. M., Sevostyanova, A., Artsimovitch, I. & Grigorieff, N. Nucleotide excision repair (NER) machinery recruitment by the transcription-repair coupling factor involves unmasking of a conserved intramolecular interface. Proc. Natl Acad. Sci. USA 109, 3353–3358 (2012).
Google Scholar