Skip to main content

Kinetic Milestones of Damage Recognition by DNA Glycosylases of the Helix-Hairpin-Helix Structural Superfamily

  • Chapter
  • First Online:
Mechanisms of Genome Protection and Repair

Part of the book series: Advances in Experimental Medicine and Biology ((AEMB,volume 1241))

Abstract

X-ray data show that DNA glycosylases, which initiate the pathway of base excision repair in DNA, belong to six structural superfamilies. Here, we provide an overview of the latest results of kinetic studies on the mechanisms of specific recognition of a damaged nucleotide at the early steps of DNA repair by human (OGG1 and MBD4) or Escherichia coli (Nth and MutY) N-DNA-glycosylases belonging to superfamily Helix-hairpin-Helix (HhH). A comparison of real-time conformational transformations of DNA glycosylases and DNA with the structural data obtained for free enzymes and their complexes with substrates and intermediates have made it possible to build molecular-kinetic models of the enzymatic processes. These models have allowed researchers to associate the conformational transitions of the interacting molecules with elementary steps of an enzymatic process. Additionally, these models have revealed the stages that make the largest contribution to the specificity of the enzyme for DNA substrates. These data provide an opportunity to gain further insight into the structural and dynamic principles underlying the enzymatic processes that ensure highly efficient functioning of the repair-protective system of all living organisms and that maintain DNA integrity.

This is a preview of subscription content, log in via an institution to check access.

Access this chapter

Chapter
USD 29.95
Price excludes VAT (USA)
  • Available as PDF
  • Read on any device
  • Instant download
  • Own it forever
eBook
USD 139.00
Price excludes VAT (USA)
  • Available as EPUB and PDF
  • Read on any device
  • Instant download
  • Own it forever
Softcover Book
USD 179.99
Price excludes VAT (USA)
  • Compact, lightweight edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info
Hardcover Book
USD 179.99
Price excludes VAT (USA)
  • Durable hardcover edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info

Tax calculation will be finalised at checkout

Purchases are for personal use only

Institutional subscriptions

References

  • Audebert M, Radicella JP, Dizdaroglu M (2000) Effect of single mutations in the OGG1 gene found in human tumors on the substrate specificity of the Ogg1 protein. Nucleic Acids Res 28:2672–2678

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Bailly V, Verly WG (1987) Escherichia-coli endonuclease-III is not an endonuclease but a beta-elimination catalyst. Biochem J 242:565–572

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Banerjee A, Yang W, Karplus M, Verdine GL (2005) Structure of a repair enzyme interrogating undamaged DNA elucidates recognition of damaged DNA. Nature 434:612–618

    Article  PubMed  CAS  Google Scholar 

  • Bjoras M, Luna L, Johnsen B, Hoff E, Haug T, Rognes T, Seeberg E (1997) Opposite base-dependent reactions of a human base excision repair enzyme on DNA containing 7,8-dihydro-8-oxoguanine and abasic sites. EMBO J 16:6314–6322

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Bjoras M, Seeberg E, Luna L, Pearl LH, Barrett TE (2002) Reciprocal “flipping” underlies substrate recognition and catalytic activation by the human 8-oxo-guanine DNA glycosylase. J Mol Biol 317:171–177

    Article  PubMed  CAS  Google Scholar 

  • Breimer LH, Lindahl T (1984) DNA glycosylase activities for thymine residues damaged by ring saturation, fragmentation, or ring contraction are functions of endonuclease-III in Escherichia-coli. J Biol Chem 259:5543–5548

    PubMed  CAS  Google Scholar 

  • Brooks SC, Adhikary S, Rubinson EH, Eichman BF (2013) Recent advances in the structural mechanisms of DNA glycosylases. Biochim Biophys Acta 1834:247–271

    Article  PubMed  CAS  Google Scholar 

  • Bruner SD, Norman DP, Verdine GL (2000) Structural basis for recognition and repair of the endogenous mutagen 8-oxoguanine in DNA. Nature 403:859–866

    Article  PubMed  CAS  Google Scholar 

  • Bulychev NV, Varaprasad CV, Dorman G, Miller JH, Eisenberg M, Grollman AP, Johnson F (1996) Substrate specificity of Escherichia coli MutY protein. Biochemistry 35:13147–13156

    Article  PubMed  CAS  Google Scholar 

  • Coppede F, Migliore L (2015) DNA damage in neurodegenerative diseases. Mutat Res Fundam Mol Mech Mutagen 776:84–97

    Article  CAS  Google Scholar 

  • Crenshaw CM, Nam K, Oo K, Kutchukian PS, Bowman BR, Karplus M, Verdine GL (2012) Enforced presentation of an extrahelical guanine to the lesion recognition pocket of human 8-oxoguanine glycosylase, hOGG1. J Biol Chem 287:24916–24928

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Cunningham RP, Asahara H, Bank JF, Scholes CP, Salerno JC, Surerus K, Munck E, Mccracken J, Peisach J, Emptage MH (1989) Endonuclease-III is an iron sulfur protein. Biochemistry 28:4450–4455

    Article  PubMed  CAS  Google Scholar 

  • Dalhus B, Forsbring M, Helle IH, Vik ES, Forstrom RJ, Backe PH, Alseth I, Bjoras M (2011) Separation-of-function mutants unravel the dual-reaction mode of human 8-oxoguanine DNA glycosylase. Structure 19:117–127

    Article  PubMed  CAS  Google Scholar 

  • Demple B, Linn S (1980) DNA N-glycosylases and Uv repair. Nature 287:203–208

    Article  PubMed  CAS  Google Scholar 

  • Denver DR, Swenson SL, Lynch M (2003) An evolutionary analysis of the helix-hairpin-helix superfamily of DNA repair glycosylases. Mol Biol Evol 20:1603–1611

    Article  PubMed  CAS  Google Scholar 

  • Dunlap CA, Tsai MD (2002) Use of 2-aminopurine and tryptophan fluorescence as probes in kinetic analyses of DNA polymerase β. Biochemistry 41:11226–11235

    Article  PubMed  CAS  Google Scholar 

  • Dziuba D, Postupalenko VY, Spadafora M, Klymchenko AS, Guerineau V, Mely Y, Benhida R, Burger A (2012) A universal nucleoside with strong two-band switchable fluorescence and sensitivity to the environment for investigating DNA interactions. J Am Chem Soc 134:10209–10213

    Article  PubMed  CAS  Google Scholar 

  • Faucher F, Wallace SS, Doublie S (2009) Structural basis for the lack of opposite base specificity of Clostridium acetobutylicum 8-oxoguanine DNA glycosylase. DNA Repair 8:1283–1289

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Fedorova OS, Kuznetsov NA, Koval VV, Knorre DG (2010) Conformational dynamics and pre-steady-state kinetics of DNA glycosylases. Biochemist 75:1225–1239

    CAS  Google Scholar 

  • Fowler RG, White SJ, Koyama C, Moore SC, Dunn RL, Schaaper RM (2003) Interactions among the Escherichia coli mutT, mutM, and mutY damage prevention pathways. DNA Repair 2:159–173

    Article  PubMed  CAS  Google Scholar 

  • Fromme JC, Verdine GL (2003) Structure of a trapped endonuclease III-DNA covalent intermediate. EMBO J 22:3461–3471

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Fromme JC, Bruner SD, Yang W, Karplus M, Verdine GL (2003) Product-assisted catalysis in base-excision DNA repair. Nat Struct Biol 10:204–211

    Article  PubMed  CAS  Google Scholar 

  • Fromme JC, Banerjee A, Huang SJ, Verdine GL (2004) Structural basis for removal of adenine mispaired with 8-oxoguanine by MutY adenine DNA glycosylase. Nature 427:652–656

    Article  PubMed  CAS  Google Scholar 

  • Girard PM, Guibourt N, Boiteux S (1997) The Ogg1 protein of Saccharomyces cerevisiae: a 7,8-dihydro-8-oxoguanine DNA glycosylase/AP lyase whose lysine 241 is a critical residue for catalytic activity. Nucleic Acids Res 25:3404–3411

    Article  Google Scholar 

  • Grollman AP, Moriya M (1993) Mutagenesis by 8-oxoguanine: an enemy within. Trends Genet 9:246–249

    Article  PubMed  CAS  Google Scholar 

  • Guan Y, Manuel RC, Arvai AS, Parikh SS, Mol CD, Miller JH, Lloyd RS, Tainer JA (1998) MutY catalytic core, mutant and bound adenine structures define specificity for DNA repair enzyme superfamily. Nat Struct Biol 5:1058–1064

    Article  PubMed  CAS  Google Scholar 

  • Guibourt N, Castaing B, Van Der Kemp PA, Boiteux S (2000) Catalytic and DNA binding properties of the ogg1 protein of Saccharomyces cerevisiae: comparison between the wild type and the K241R and K241Q active-site mutant proteins. Biochemistry 39:1716–1724

    Article  PubMed  CAS  Google Scholar 

  • Hashimoto H, Zhang X, Cheng X (2012) Excision of thymine and 5-hydroxymethyluracil by the MBD4 DNA glycosylase domain: structural basis and implications for active DNA demethylation. Nucleic Acids Res 40:8276–8284

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Hatahet Z, Kow YW, Purmal AA, Cunningham RP, Wallace SS (1994) New substrates for old enzymes. 5-Hydroxy-2′-deoxycytidine and 5-hydroxy-2′-deoxyuridine are substrates for Escherichia coli endonuclease III and formamidopyrimidine DNA N-glycosylase, while 5-hydroxy-2′-deoxyuridine is a substrate for uracil DNA N-glycos. J Biol Chem 269:18814–18820

    PubMed  CAS  Google Scholar 

  • Hill PW, Amouroux R, Hajkova P (2014) DNA demethylation, Tet proteins and 5-hydroxymethylcytosine in epigenetic reprogramming: an emerging complex story. Genomics 104:324–333

    Article  PubMed  CAS  Google Scholar 

  • Hoeijmakers JH (2009) DNA damage, aging, and cancer. N Engl J Med 361:1475–1485

    Article  PubMed  CAS  Google Scholar 

  • Iyama T, Wilson DM 3rd (2013) DNA repair mechanisms in dividing and non-dividing cells. DNA Repair 12:620–636

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Izumi T, Wiederhold LR, Roy G, Roy R, Jaiswal A, Bhakat KK, Mitra S, Hazra TK (2003) Mammalian DNA base excision repair proteins: their interactions and role in repair of oxidative DNA damage. Toxicology 193:43–65. https://doi.org/10.1016/S0300-483X(03)00289-0

    Article  PubMed  CAS  Google Scholar 

  • Karahalil B, Girard PM, Boiteux S, Dizdaroglu M (1998) Substrate specificity of the Ogg1 protein of Saccharomyces cerevisiae: excision of guanine lesions produced in DNA by ionizing radiation- or hydrogen peroxide/metal ion-generated free radicals. Nucleic Acids Res 26:1228–1232

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Katcher HL, Wallace SS (1983) Characterization of the Escherichia-coli X-ray endonuclease, endonuclease III. Biochemistry 22:4071–4081

    Article  PubMed  CAS  Google Scholar 

  • Kladova OA, Kuznetsova AA, Fedorova OS, Kuznetsov NA (2017) Mutational and kinetic analysis of lesion recognition by Escherichia coli endonuclease VIII. Genes (Basel) 8:1–13

    Article  CAS  Google Scholar 

  • Kladova OA, Krasnoperov LN, Kuznetsov NA, Fedorova OS (2018) Kinetics and thermodynamics of DNA processing by wild type DNA-glycosylase endo III and its catalytically inactive mutant forms. Genes (Basel) 9(4):pii: E190

    Article  CAS  Google Scholar 

  • Kladova OA, Kuznetsov NA, Fedorova OS (2019) Thermodynamic parameters of endonuclease VIII interactions with damaged DNA. Acta Naturae, Accepted

    Google Scholar 

  • Kow YW, Wallace SS (1987) Mechanism of action of Escherichia-coli endonuclease-III. Biochemistry 26:8200–8206

    Article  PubMed  CAS  Google Scholar 

  • Krokan HE, Standal R, Slupphaug G (1997) DNA glycosylases in the base excision repair of DNA. Biochem J 325:1–16

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Krokan HE, Nilsen H, Skorpen F, Otterlei M, Slupphaug G (2000) Base excision repair of DNA in mammalian cells. FEBS Lett 476:73–77

    Article  PubMed  CAS  Google Scholar 

  • Kubota Y, Nash RA, Klungland A, Schar P, Barnes DE, Lindahl T (1996) Reconstitution of DNA base excision-repair with purified human proteins: interaction between DNA polymerase β and the XRCC1 protein. EMBO J 15:6662–6670

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Kuo CF, McRee DE, Fisher CL, O’Handley SF, Cunningham RP, Tainer JA (1992) Atomic structure of the DNA repair [4Fe-4S] enzyme endonuclease III. Science (80-) 258:434–440

    Article  CAS  Google Scholar 

  • Kuznetsov NA, Fedorova OS (2016) Thermodynamic analysis of fast stages of specific lesion recognition by DNA repair enzymes. Biochemist 81:1136–1152

    CAS  Google Scholar 

  • Kuznetsov NA, Koval VV, Zharkov DO, Nevinsky GA, Douglas KT, Fedorova OS (2005) Kinetics of substrate recognition and cleavage by human 8-oxoguanine-DNA glycosylase. Nucleic Acids Res 33:3919–3931

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Kuznetsov NA, Koval VV, Zharkov DO, Vorobiev YN, Nevinsky GA, Douglas KT, Fedorova OS (2007a) Kinetic basis of lesion specificity and opposite-base specificity of Escherichia coli formamidopyrimidine-DNA glycosylase. Biochemistry 46:424–435

    Article  PubMed  CAS  Google Scholar 

  • Kuznetsov NA, Koval VV, Nevinsky GA, Douglas KT, Zharkov DO, Fedorova OS (2007b) Kinetic conformational analysis of human 8-oxoguanine-DNA glycosylase. J Biol Chem 282:1029–1038

    Article  PubMed  CAS  Google Scholar 

  • Kuznetsov NA, Vorobjev YN, Krasnoperov LN, Fedorova OS (2012) Thermodynamics of the multi-stage DNA lesion recognition and repair by formamidopyrimidine-DNA glycosylase using pyrrolocytosine fluorescence--stopped-flow pre-steady-state kinetics. Nucleic Acids Res 40:7384–7392

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Kuznetsov NA, Kuznetsova AA, Vorobjev YN, Krasnoperov LN, Fedorova OS (2014) Thermodynamics of the DNA damage repair steps of human 8-oxoguanine DNA glycosylase. PLoS One 9:e98495

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Kuznetsov NA, Bergonzo C, Campbell AJ, Li H, Mechetin GV, de los Santos C, Grollman AP, Fedorova OS, Zharkov DO, Simmerling C (2015a) Active destabilization of base pairs by a DNA glycosylase wedge initiates damage recognition. Nucleic Acids Res 43:272–281

    Article  PubMed  CAS  Google Scholar 

  • Kuznetsov NA, Kladova OA, Kuznetsova AA, Ishchenko AA, Saparbaev MK, Zharkov DO, Fedorova OS (2015b) Conformational dynamics of DNA repair by Escherichia coli endonuclease III. J Biol Chem 290:14338–14349

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Kuznetsova AA, Kuznetsov NA, Vorobjev YN, Barthes NPF, Michel BY, Burger A, Fedorova OS (2014a) New environment-sensitive multichannel DNA fluorescent label for investigation of the protein-DNA interactions. PLoS One 9:e100007

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Kuznetsova AA, Kuznetsov NA, Ishchenko AA, Saparbaev MK, Fedorova OS (2014b) Step-by-step mechanism of DNA damage recognition by human 8-oxoguanine DNA glycosylase. Biochim Biophys Acta 1840:387–395

    Article  PubMed  CAS  Google Scholar 

  • Lee S, Verdine GL (2009) Atomic substitution reveals the structural basis for substrate adenine recognition and removal by adenine DNA glycosylase. Proc Natl Acad Sci U S A 106:18497–18502

    Article  PubMed  PubMed Central  Google Scholar 

  • Lee AJ, Wallace SS (2016) Visualizing the search for radiation-damaged DNA bases in real time. Radiat Phys Chem (Oxford, England) 1993(128):126–133

    Article  CAS  Google Scholar 

  • Lee AJ, Wallace SS (2017) Hide and seek: how do DNA glycosylases locate oxidatively damaged DNA bases amidst a sea of undamaged bases? Free Radic Biol Med 107:170–178

    Article  PubMed  CAS  Google Scholar 

  • Lee AJ, Warshaw DM, Wallace SS (2014) Insights into the glycosylase search for damage from single-molecule fluorescence microscopy. DNA Repair 20:23–31

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Li H, Endutkin AV, Bergonzo C, Campbell AJ, De Los Santos C, Grollman A, Zharkov DO, Simmerling C (2016) A dynamic checkpoint in oxidative lesion discrimination by formamidopyrimidine-DNA glycosylase. Nucleic Acids Res 44:683–694. https://doi.org/10.1093/nar/gkv1092

    Article  PubMed  CAS  Google Scholar 

  • Li H, Endutkin AV, Bergonzo C, Fu L, Grollman A, Zharkov DO, Simmerling C (2017) DNA deformation-coupled recognition of 8-oxoguanine: conformational kinetic gating in human DNA glycosylase. J Am Chem Soc 139:2682–2692. https://doi.org/10.1021/jacs.6b11433

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Lindahl T (1993) Instability and decay of the primary structure of DNA. Nature 362:709–715

    Article  PubMed  CAS  Google Scholar 

  • Lu A-L, Tsai-Wu J-J, Cillo J (1995) DNA determinants and substrate specificities of Escherichia coli MutY. J Biol Chem 270:23582–23588

    Article  PubMed  CAS  Google Scholar 

  • Lukina MV, Kuznetsova AA, Kuznetsov NA, Fedorova OS (2017) The kinetic analysis of recognition of the damaged nucleotides by mutant forms of the 8-oxoguanine DNA glycosylase hOGG1. Russ J Bioorg Chem 43:1–12

    Article  CAS  Google Scholar 

  • Manlove AH, McKibbin PL, Doyle EL, Majumdar C, Hamm ML, David SS (2017) Structure-activity relationships reveal key features of 8-oxoguanine: a mismatch detection by the MutY glycosylase. ACS Chem Biol 12:2335–2344. https://doi.org/10.1021/acschembio.7b00389

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Manvilla BA, Maiti A, Begley MC, Toth EA, Drohat AC (2012) Crystal structure of human methyl-binding domain IV glycosylase bound to abasic DNA. J Mol Biol 420:164–175

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Mazumder A, Gerlt JA, Absalon MJ, Stubbe J, Cunningham RP, Withka J, Bolton PH (1991) Stereochemical studies of the beta-elimination reactions at aldehydic abasic sites in DNA – endonuclease III from Escherichia-coli, sodium-hydroxide, and Lys-Trp-Lys. Biochemistry 30:1119–1126

    Article  PubMed  CAS  Google Scholar 

  • McCann JA, Berti PJ (2008) Transition-state analysis of the DNA repair enzyme MutY. J Am Chem Soc 130:5789–5797

    Article  PubMed  CAS  Google Scholar 

  • Memisoglu A, Samson L (2000) Base excision repair in yeast and mammals. Mutat Res 451:39–51

    Article  PubMed  CAS  Google Scholar 

  • Michaels ML, Miller JH (1992) The GO system protects organisms from the mutagenic effect of the spontaneous lesion 8-hydroxy-guanine (7,8-dihydro-8-oxoguanine). J Bacteriol 174:6321–6325

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Miroshnikova AD, Kuznetsova AA, Kuznetsov NA, Fedorova OS (2016) Thermodynamics of damaged DNA binding and catalysis by human AP endonuclease 1. Acta Nat 8:103–110

    Article  CAS  Google Scholar 

  • Monden Y, Arai T, Asano M, Ohtsuka E, Aburatani H, Nishimura S (1999) Human MMH (OGG1) type 1a protein is a major enzyme for repair of 8-hydroxyguanine lesions in human cells. Biochem Biophys Res Commun 258:605–610

    Article  PubMed  CAS  Google Scholar 

  • Morera S, Grin I, Vigouroux A, Couve S, Henriot V, Saparbaev M, Ishchenko AA (2012) Biochemical and structural characterization of the glycosylase domain of MBD4 bound to thymine and 5-hydroxymethyuracil-containing DNA. Nucleic Acids Res 40:9917–9926

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Nash HM, Lu R, Lane WS, Verdine GL (1997) The critical active-site amine of the human 8-oxoguanine DNA glycosylase, hOgg1: direct identification, ablation and chemical reconstitution. Chem Biol 4:693–702

    Article  PubMed  CAS  Google Scholar 

  • Nelson SR, Dunn AR, Kathe SD, Warshaw DM, Wallace SS (2014) Two glycosylase families diffusively scan DNA using a wedge residue to probe for and identify oxidatively damaged bases. Proc Natl Acad Sci U S A 111:E2091–E2099

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Norman DP, Chung SJ, Verdine GL (2003) Structural and biochemical exploration of a critical amino acid in human 8-oxoguanine glycosylase. Biochemistry 42:1564–1572

    Article  PubMed  CAS  Google Scholar 

  • Pascucci B, Maga G, Hubscher U, Bjoras M, Seeberg E, Hickson ID, Villani G, Giordano C, Cellai L, Dogliotti E et al (2002) Reconstitution of the base excision repair pathway for 7,8-dihydro-8-oxoguanine with purified human proteins. Nucleic Acids Res 30:2124–2130

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Petronzelli F, Riccio A, Markham GD, Seeholzer SH, Genuardi M, Karbowski M, Yeung AT, Matsumoto Y, Bellacosa A (2000) Investigation of the substrate spectrum of the human mismatch-specific DNA N-glycosylase MED1 (MBD4): fundamental role of the catalytic domain. J Cell Physiol 185:473–480

    Article  PubMed  CAS  Google Scholar 

  • Porello SL, Williams SD, Kuhn H, Michaels ML, David SS (1996) Specific recognition of substrate analogs by the DNA mismatch repair enzyme MutY. J Am Chem Soc 118:10684–10692

    Article  CAS  Google Scholar 

  • Radicella JP, Dherin C, Desmaze C, Fox MS, Boiteux S (1997) Cloning and characterization of hOGG1, a human homolog of the OGG1 gene of Saccharomyces cerevisiae. Proc Natl Acad Sci U S A 94:8010–8015

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Radman M (1976) Endonuclease from Escherichia-coli that introduces single polynucleotide chain scissions in ultraviolet-irradiated DNA. J Biol Chem 251:1438–1445

    PubMed  CAS  Google Scholar 

  • Radom CT, Banerjee A, Verdine GL (2007) Structural characterization of human 8-oxoguanine DNA glycosylase variants bearing active site mutations. J Biol Chem 282:9182–9194

    Article  PubMed  CAS  Google Scholar 

  • Raha S, Robinson BH (2000) Mitochondria, oxygen free radicals, disease and ageing. Trends Biochem Sci 25:502–508

    Article  PubMed  CAS  Google Scholar 

  • Robertson AB, Klungland A, Rognes T, Leiros I (2009) DNA repair in mammalian cells: base excision repair: the long and short of it. Cell Mol Life Sci 66:981–993

    Article  PubMed  CAS  Google Scholar 

  • Rodgers BJ, Elsharif NA, Vashisht N, Mingus MM, Mulvahill MA, Stengel G, Kuchta RD, Purse BW (2014) Functionalized tricyclic cytosine analogues provide nucleoside fluorophores with improved photophysical properties and a range of solvent sensitivities. Chemistry (Easton) 20:2010–2015

    CAS  Google Scholar 

  • Sandin P, Stengel G, Ljungdahl T, Borjesson K, Macao B, Wilhelmsson LM (2009) Highly efficient incorporation of the fluorescent nucleotide analogs tC and tCO by Klenow fragment. Nucleic Acids Res 37:3924–3933

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Shibutani S, Takeshita M, Grollman AP (1991) Insertion of specific bases during DNA synthesis past the oxidation-damaged base 8-oxodG. Nature 349:431–434

    Article  PubMed  CAS  Google Scholar 

  • Sinkeldam RW, Greco NJ, Tor Y (2010) Fluorescent analogs of biomolecular building blocks: design, properties, and applications. Chem Rev 110:2579–2619

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Sjolund AB, Senejani AG, Sweasy JB (2013) MBD4 and TDG: multifaceted DNA glycosylases with ever expanding biological roles. Mutat Res 743–744:12–25

    Article  PubMed  CAS  Google Scholar 

  • Sowers LC, Boulard Y, Fazakerley GV (2000) Multiple structures for the 2-aminopurine-cytosine mispair. Biochemistry 39:7613–7620

    Article  PubMed  CAS  Google Scholar 

  • Spadafora M, Postupalenko VY, Shvadchak VV, Klymchenko AS, Mely Y, Burger A, Benhida R (2009) Efficient synthesis of ratiometric fluorescent nucleosides featuring 3-hydroxychromone nucleobases. Tetrahedron 65:7809–7816

    Article  CAS  Google Scholar 

  • Stivers JT, Pankiewicz KW, Watanabe KA (1999) Kinetic mechanism of damage site recognition and uracil flipping by Escherichia coli uracil DNA glycosylase. Biochemistry 38:952–963

    Article  PubMed  CAS  Google Scholar 

  • Thayer MM, Ahern H, Xing D, Cunningham RP, Tainer JA (1995) Novel DNA binding motifs in the DNA repair enzyme endonuclease III crystal structure. EMBO J 14:4108–4120

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Turner DP, Cortellino S, Schupp JE, Caretti E, Loh T, Kinsella TJ, Bellacosa A (2006) The DNA N-glycosylase MED1 exhibits preference for halogenated pyrimidines and is involved in the cytotoxicity of 5-iododeoxyuridine. Cancer Res 66:7686–7693

    Article  PubMed  CAS  Google Scholar 

  • Tyugashev TE, Kuznetsova AA, Kuznetsov NA, Fedorova OS (2017) Interaction features of adenine DNA glycosylase MutY from E-coli with DNA substrates. Russ J Bioorg Chem 43:13–22

    Article  CAS  Google Scholar 

  • Wang L, Lee SJ, Verdine GL (2015) Structural basis for avoidance of promutagenic DNA repair by MutY adenine DNA glycosylase. J Biol Chem 290:17096–17105

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Wang L, Chakravarthy S, Verdine GL (2017) Structural basis for the lesion-scanning mechanism of the MutY DNA glycosylase. J Biol Chem 292:5007–5017. https://doi.org/10.1074/jbc.M116.757039

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Wilhelmsson LM (2010) Fluorescent nucleic acid base analogues. Q Rev Biophys 43:159–183

    Article  PubMed  CAS  Google Scholar 

  • Wilson DM III, Barsky D (2001) The major human abasic endonuclease: formation, consequences and repair of abasic lesions in DNA. Mutat Res 485:283–307

    Article  PubMed  CAS  Google Scholar 

  • Woods RD, O’Shea VL, Chu A, Cao S, Richards JL, Horvath MP, David SS (2016) Structure and stereochemistry of the base excision repair glycosylase MutY reveal a mechanism similar to retaining glycosidases. Nucleic Acids Res 44:801–810

    Article  PubMed  CAS  Google Scholar 

  • Yakovlev DA, Kuznetsova AA, Fedorova OS, Kuznetsov NA (2017) Search for modified DNA sites with the human methyl-CpG-binding enzyme MBD4. Acta Nat 9:88–98

    Article  CAS  Google Scholar 

  • Yang K, Stanley RJ (2008) The extent of DNA deformation in DNA photolyase-substrate complexes: a solution state fluorescence study. Photochem Photobiol 84:741–749

    Article  PubMed  CAS  Google Scholar 

  • Zang H, Fang Q, Pegg AE, Guengerich FP (2005) Kinetic analysis of steps in the repair of damaged DNA by human O6-alkylguanine-DNA alkyltransferase. J Biol Chem 280:30873–30881

    Article  PubMed  CAS  Google Scholar 

  • Zhang W, Liu Z, Crombet L, Amaya MF, Liu Y, Zhang X, Kuang W, Ma P, Niu L, Qi C (2011) Crystal structure of the mismatch-specific thymine glycosylase domain of human methyl-CpG-binding protein MBD4. Biochem Biophys Res Commun 412:425–428

    Article  PubMed  CAS  Google Scholar 

  • Zharkov DO (2008) Base excision DNA repair. Cell Mol Life Sci 65:1544–1565

    Article  PubMed  CAS  Google Scholar 

  • Zharkov DO, Rosenquist TA, Gerchman SE, Grollman AP (2000a) Substrate specificity and reaction mechanism of murine 8-oxoguanine-DNA glycosylase. J Biol Chem 275:28607–28617

    Article  PubMed  CAS  Google Scholar 

  • Zharkov DO, Gilboa R, Yagil I, Kycia JH, Gerchman SE, Shoham G, Grollman AP (2000b) Role for lysine 142 in the excision of adenine from A:G mispairs by MutY DNA glycosylase of Escherichia coli. Biochemistry 39:14768–14778

    Article  PubMed  CAS  Google Scholar 

Download references

Acknowledgements

This work was supported by a Russian-Government-funded project (No. АААА-А17-117020210022-4) and grant of Ministry of Science and Higher Education No MD-3775.2019.4. The part of the work including analysis of experimental data for MBD4 was supported by the Russian Scientific Foundation project No. 16-14-10038.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Olga S. Fedorova .

Editor information

Editors and Affiliations

Rights and permissions

Reprints and permissions

Copyright information

© 2020 Springer Nature Switzerland AG

About this chapter

Check for updates. Verify currency and authenticity via CrossMark

Cite this chapter

Kuznetsov, N.A., Fedorova, O.S. (2020). Kinetic Milestones of Damage Recognition by DNA Glycosylases of the Helix-Hairpin-Helix Structural Superfamily. In: Zharkov, D. (eds) Mechanisms of Genome Protection and Repair. Advances in Experimental Medicine and Biology, vol 1241. Springer, Cham. https://doi.org/10.1007/978-3-030-41283-8_1

Download citation

Publish with us

Policies and ethics