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Structure of the C-terminal half of UvrC reveals an RNase H endonuclease domain with an Argonaute-like catalytic triad.

Karakas E, Truglio JJ, Croteau D, Rhau B, Wang L, Van Houten B, Kisker C
EMBO J 26 613-22 (2007)
Related entries: 2nrr, 2nrt, 2nrv, 2nrw, 2nrz

Cited: 41 times
EuropePMC logo PMID: 17245438

Abstract

Removal and repair of DNA damage by the nucleotide excision repair pathway requires two sequential incision reactions, which are achieved by the endonuclease UvrC in eubacteria. Here, we describe the crystal structure of the C-terminal half of UvrC, which contains the catalytic domain responsible for 5' incision and a helix-hairpin-helix-domain that is implicated in DNA binding. Surprisingly, the 5' catalytic domain shares structural homology with RNase H despite the lack of sequence homology and contains an uncommon DDH triad. The structure also reveals two highly conserved patches on the surface of the protein, which are not related to the active site. Mutations of residues in one of these patches led to the inability of the enzyme to bind DNA and severely compromised both incision reactions. Based on our results, we suggest a model of how UvrC forms a productive protein-DNA complex to excise the damage from DNA.

Articles - 2nrx mentioned but not cited (1)

  1. Structure of the C-terminal half of UvrC reveals an RNase H endonuclease domain with an Argonaute-like catalytic triad. Karakas E, Truglio JJ, Croteau D, Rhau B, Wang L, Van Houten B, Kisker C. EMBO J 26 613-622 (2007)


Reviews citing this publication (12)

  1. Nucleases: diversity of structure, function and mechanism. Yang W. Q Rev Biophys 44 1-93 (2011)
  2. Retroviral integrase superfamily: the structural perspective. Nowotny M. EMBO Rep 10 144-151 (2009)
  3. XPB and XPD helicases in TFIIH orchestrate DNA duplex opening and damage verification to coordinate repair with transcription and cell cycle via CAK kinase. Fuss JO, Tainer JA. DNA Repair (Amst) 10 697-713 (2011)
  4. Repair of UV damage in bacteria. Goosen N, Moolenaar GF. DNA Repair (Amst) 7 353-379 (2008)
  5. Prokaryotic nucleotide excision repair. Kisker C, Kuper J, Van Houten B. Cold Spring Harb Perspect Biol 5 a012591 (2013)
  6. Dynamics of lesion processing by bacterial nucleotide excision repair proteins. Kad NM, Van Houten B. Prog Mol Biol Transl Sci 110 1-24 (2012)
  7. DNA repair gets physical: mapping an XPA-binding site on ERCC1. Croteau DL, Peng Y, Van Houten B. DNA Repair (Amst) 7 819-826 (2008)
  8. Alkyltransferase-like proteins: molecular switches between DNA repair pathways. Tubbs JL, Tainer JA. Cell Mol Life Sci 67 3749-3762 (2010)
  9. Investigation of bacterial nucleotide excision repair using single-molecule techniques. Van Houten B, Kad N. DNA Repair (Amst) 20 41-48 (2014)
  10. A Peek Inside the Machines of Bacterial Nucleotide Excision Repair. Kraithong T, Hartley S, Jeruzalmi D, Pakotiprapha D. Int J Mol Sci 22 952 (2021)
  11. Evolutionary Origins of DNA Repair Pathways: Role of Oxygen Catastrophe in the Emergence of DNA Glycosylases. Prorok P, Grin IR, Matkarimov BT, Ishchenko AA, Laval J, Zharkov DO, Saparbaev M. Cells 10 1591 (2021)
  12. Searching for DNA Damage: Insights From Single Molecule Analysis. Schaich MA, Van Houten B. Front Mol Biosci 8 772877 (2021)

Articles citing this publication (28)

  1. Collaborative dynamic DNA scanning by nucleotide excision repair proteins investigated by single- molecule imaging of quantum-dot-labeled proteins. Kad NM, Wang H, Kennedy GG, Warshaw DM, Van Houten B. Mol Cell 37 702-713 (2010)
  2. Structures of endonuclease V with DNA reveal initiation of deaminated adenine repair. Dalhus B, Arvai AS, Rosnes I, Olsen ØE, Backe PH, Alseth I, Gao H, Cao W, Tainer JA, Bjørås M. Nat Struct Mol Biol 16 138-143 (2009)
  3. Crystal structure of Bacillus stearothermophilus UvrA provides insight into ATP-modulated dimerization, UvrB interaction, and DNA binding. Pakotiprapha D, Inuzuka Y, Bowman BR, Moolenaar GF, Goosen N, Jeruzalmi D, Verdine GL. Mol Cell 29 122-133 (2008)
  4. Inosine in DNA and RNA. Alseth I, Dalhus B, Bjørås M. Curr Opin Genet Dev 26 116-123 (2014)
  5. Structure of UvrA nucleotide excision repair protein in complex with modified DNA. Jaciuk M, Nowak E, Skowronek K, Tańska A, Nowotny M. Nat Struct Mol Biol 18 191-197 (2011)
  6. Molecular mechanisms of the whole DNA repair system: a comparison of bacterial and eukaryotic systems. Morita R, Nakane S, Shimada A, Inoue M, Iino H, Wakamatsu T, Fukui K, Nakagawa N, Masui R, Kuramitsu S. J Nucleic Acids 2010 179594 (2010)
  7. Probing for DNA damage with β-hairpins: similarities in incision efficiencies of bulky DNA adducts by prokaryotic and human nucleotide excision repair systems in vitro. Liu Y, Reeves D, Kropachev K, Cai Y, Ding S, Kolbanovskiy M, Kolbanovskiy A, Bolton JL, Broyde S, Van Houten B, Geacintov NE. DNA Repair (Amst) 10 684-696 (2011)
  8. Real-time single-molecule imaging reveals a direct interaction between UvrC and UvrB on DNA tightropes. Hughes CD, Wang H, Ghodke H, Simons M, Towheed A, Peng Y, Van Houten B, Kad NM. Nucleic Acids Res 41 4901-4912 (2013)
  9. Folding, DNA recognition, and function of GIY-YIG endonucleases: crystal structures of R.Eco29kI. Mak AN, Lambert AR, Stoddard BL. Structure 18 1321-1331 (2010)
  10. Cooperative damage recognition by UvrA and UvrB: identification of UvrA residues that mediate DNA binding. Croteau DL, DellaVecchia MJ, Perera L, Van Houten B. DNA Repair (Amst) 7 392-404 (2008)
  11. Hpy188I-DNA pre- and post-cleavage complexes--snapshots of the GIY-YIG nuclease mediated catalysis. Sokolowska M, Czapinska H, Bochtler M. Nucleic Acids Res 39 1554-1564 (2011)
  12. Exploring damage recognition models in prokaryotic nucleotide excision repair with a benzo[a]pyrene-derived lesion in UvrB. Jia L, Kropachev K, Ding S, Van Houten B, Geacintov NE, Broyde S. Biochemistry 48 8948-8957 (2009)
  13. Multiplex quantitative SILAC for analysis of archaeal proteomes: a case study of oxidative stress responses. McMillan LJ, Hwang S, Farah RE, Koh J, Chen S, Maupin-Furlow JA. Environ Microbiol 20 385-401 (2018)
  14. Bax1 is a novel endonuclease: implications for archaeal nucleotide excision repair. Roth HM, Tessmer I, Van Houten B, Kisker C. J Biol Chem 284 32272-32278 (2009)
  15. Novel Sequence Features of DNA Repair Genes/Proteins from Deinococcus Species Implicated in Protection from Oxidatively Generated Damage. Hassan FMN, Gupta RS. Genes (Basel) 9 E149 (2018)
  16. Crystal structure of E. coli endonuclease V, an essential enzyme for deamination repair. Zhang Z, Jia Q, Zhou C, Xie W. Sci Rep 5 12754 (2015)
  17. Divalent metal ion differentially regulates the sequential nicking reactions of the GIY-YIG homing endonuclease I-BmoI. Kleinstiver BP, Bérubé-Janzen W, Fernandes AD, Edgell DR. PLoS One 6 e23804 (2011)
  18. Mechanism of DNA Lesion Homing and Recognition by the Uvr Nucleotide Excision Repair System. Lee SJ, Sung RJ, Verdine GL. Research (Wash D C) 2019 5641746 (2019)
  19. The ATPase mechanism of UvrA2 reveals the distinct roles of proximal and distal ATPase sites in nucleotide excision repair. Case BC, Hartley S, Osuga M, Jeruzalmi D, Hingorani MM. Nucleic Acids Res 47 4136-4152 (2019)
  20. Structure of human endonuclease V as an inosine-specific ribonuclease. Zhang Z, Hao Z, Wang Z, Li Q, Xie W. Acta Crystallogr D Biol Crystallogr 70 2286-2294 (2014)
  21. UvrC Coordinates an O2-Sensitive [4Fe4S] Cofactor. Silva RMB, Grodick MA, Barton JK. J Am Chem Soc 142 10964-10977 (2020)
  22. A tale of two cities: A tribute to Aziz Sancar's Nobel Prize in Chemistry for his molecular characterization of NER. Van Houten B. DNA Repair (Amst) 37 A3-A13 (2016)
  23. Holliday junction resolution by At-HIGLE: an SLX1 lineage endonuclease from Arabidopsis thaliana with a novel in-built regulatory mechanism. Verma P, Kumari P, Negi S, Yadav G, Gaur V. Nucleic Acids Res 50 4630-4646 (2022)
  24. In vitro reconstitution of an efficient nucleotide excision repair system using mesophilic enzymes from Deinococcus radiodurans. Seck A, De Bonis S, Saint-Pierre C, Gasparutto D, Ravanat JL, Timmins J. Commun Biol 5 127 (2022)
  25. Modeling of Escherichia coli Endonuclease V structure in complex with DNA. Majorek KA, Bujnicki JM. J Mol Model 15 173-182 (2009)
  26. Structural and functional insights into the activation of the dual incision activity of UvrC, a key player in bacterial NER. Seck A, De Bonis S, Stelter M, Ökvist M, Senarisoy M, Hayek MR, Le Roy A, Martin L, Saint-Pierre C, Silveira CM, Gasparutto D, Todorovic S, Ravanat JL, Timmins J. Nucleic Acids Res 51 2931-2949 (2023)
  27. The Helicobacter pylori UvrC Nuclease Is Essential for Chromosomal Microimports after Natural Transformation. Ailloud F, Estibariz I, Pfaffinger G, Suerbaum S. mBio 13 e0181122 (2022)
  28. Physiological and genomic insights into abiotic stress of halophilic archaeon Natrinema altunense 4.1R isolated from a saline ecosystem of Tunisian desert. Najjari A, Boussetta A, Youssef N, Linares-Pastén JA, Mahjoubi M, Belloum R, Sghaier H, Cherif A, Ouzari HI. Genetica 151 133-152 (2023)


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