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.
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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
Bailly V, Verly WG (1987) Escherichia-coli endonuclease-III is not an endonuclease but a beta-elimination catalyst. Biochem J 242:565–572
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
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
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
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
Brooks SC, Adhikary S, Rubinson EH, Eichman BF (2013) Recent advances in the structural mechanisms of DNA glycosylases. Biochim Biophys Acta 1834:247–271
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
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
Coppede F, Migliore L (2015) DNA damage in neurodegenerative diseases. Mutat Res Fundam Mol Mech Mutagen 776:84–97
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
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
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
Demple B, Linn S (1980) DNA N-glycosylases and Uv repair. Nature 287:203–208
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
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
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
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
Fedorova OS, Kuznetsov NA, Koval VV, Knorre DG (2010) Conformational dynamics and pre-steady-state kinetics of DNA glycosylases. Biochemist 75:1225–1239
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
Fromme JC, Verdine GL (2003) Structure of a trapped endonuclease III-DNA covalent intermediate. EMBO J 22:3461–3471
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
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
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
Grollman AP, Moriya M (1993) Mutagenesis by 8-oxoguanine: an enemy within. Trends Genet 9:246–249
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
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
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
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
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
Hoeijmakers JH (2009) DNA damage, aging, and cancer. N Engl J Med 361:1475–1485
Iyama T, Wilson DM 3rd (2013) DNA repair mechanisms in dividing and non-dividing cells. DNA Repair 12:620–636
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
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
Katcher HL, Wallace SS (1983) Characterization of the Escherichia-coli X-ray endonuclease, endonuclease III. Biochemistry 22:4071–4081
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
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
Kladova OA, Kuznetsov NA, Fedorova OS (2019) Thermodynamic parameters of endonuclease VIII interactions with damaged DNA. Acta Naturae, Accepted
Kow YW, Wallace SS (1987) Mechanism of action of Escherichia-coli endonuclease-III. Biochemistry 26:8200–8206
Krokan HE, Standal R, Slupphaug G (1997) DNA glycosylases in the base excision repair of DNA. Biochem J 325:1–16
Krokan HE, Nilsen H, Skorpen F, Otterlei M, Slupphaug G (2000) Base excision repair of DNA in mammalian cells. FEBS Lett 476:73–77
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
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
Kuznetsov NA, Fedorova OS (2016) Thermodynamic analysis of fast stages of specific lesion recognition by DNA repair enzymes. Biochemist 81:1136–1152
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
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
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
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
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
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
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
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
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
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
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
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
Lee AJ, Warshaw DM, Wallace SS (2014) Insights into the glycosylase search for damage from single-molecule fluorescence microscopy. DNA Repair 20:23–31
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
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
Lindahl T (1993) Instability and decay of the primary structure of DNA. Nature 362:709–715
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
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
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
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
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
McCann JA, Berti PJ (2008) Transition-state analysis of the DNA repair enzyme MutY. J Am Chem Soc 130:5789–5797
Memisoglu A, Samson L (2000) Base excision repair in yeast and mammals. Mutat Res 451:39–51
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
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
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
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
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
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
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
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
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
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
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
Radman M (1976) Endonuclease from Escherichia-coli that introduces single polynucleotide chain scissions in ultraviolet-irradiated DNA. J Biol Chem 251:1438–1445
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
Raha S, Robinson BH (2000) Mitochondria, oxygen free radicals, disease and ageing. Trends Biochem Sci 25:502–508
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
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
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
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
Sinkeldam RW, Greco NJ, Tor Y (2010) Fluorescent analogs of biomolecular building blocks: design, properties, and applications. Chem Rev 110:2579–2619
Sjolund AB, Senejani AG, Sweasy JB (2013) MBD4 and TDG: multifaceted DNA glycosylases with ever expanding biological roles. Mutat Res 743–744:12–25
Sowers LC, Boulard Y, Fazakerley GV (2000) Multiple structures for the 2-aminopurine-cytosine mispair. Biochemistry 39:7613–7620
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
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
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
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
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
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
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
Wilhelmsson LM (2010) Fluorescent nucleic acid base analogues. Q Rev Biophys 43:159–183
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
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
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
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
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
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
Zharkov DO (2008) Base excision DNA repair. Cell Mol Life Sci 65:1544–1565
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
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
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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.
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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
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