Identification of a novel bifunctional uracil DNA glycosylase from Thermococcus barophilus Ch5.
Bifunctional glycosylase
Hyperthermophilic archaea
Uracil DNA glycosylase
Journal
Applied microbiology and biotechnology
ISSN: 1432-0614
Titre abrégé: Appl Microbiol Biotechnol
Pays: Germany
ID NLM: 8406612
Informations de publication
Date de publication:
Jul 2021
Jul 2021
Historique:
received:
22
02
2021
accepted:
10
06
2021
revised:
22
05
2021
pubmed:
6
7
2021
medline:
21
7
2021
entrez:
5
7
2021
Statut:
ppublish
Résumé
Genomes of hyperthermophiles are facing a severe challenge due to increased deamination rates of cytosine induced by high temperature, which could be counteracted by base excision repair mediated by uracil DNA glycosylase (UDG) or other repair pathways. Our previous work has shown that the two UDGs (Tba UDG247 and Tba UDG194) encoded by the genome of the hyperthermophilic euryarchaeon Thermococcus barophilus Ch5 can remove uracil from DNA at high temperature. Herein, we provide evidence that Tba UDG247 is a novel bifunctional glycosylase which can excise uracil from DNA and further cleave the phosphodiester bo nd of the generated apurinic/apyrimidinic (AP) site, which has never been described to date. In addition to cleaving uracil-containing DNA, Tba UDG247 can also cleave AP-containing ssDNA although at lower efficiency, thereby suggesting that the enzyme might be involved in repair of AP site in DNA. Kinetic analyses showed that Tba UDG247 displays a faster rate for uracil excision than for AP cleavage, thus suggesting that cleaving AP site by the enzyme is a rate-limiting step for its bifunctionality. Phylogenetic analysis showed that Tba UDG247 is clustered on a separate branch distant from all the reported UDGs. Overall, we designated Tba UDG247 as the prototype of a novel family of bifunctional UDGs. KEY POINTS: We first reported a novel DNA glycosylase with bifunctionality. Tba UDG247 possesses an AP lyase activity.
Identifiants
pubmed: 34223949
doi: 10.1007/s00253-021-11422-8
pii: 10.1007/s00253-021-11422-8
doi:
Substances chimiques
Uracil
56HH86ZVCT
Uracil-DNA Glycosidase
EC 3.2.2.-
Types de publication
Journal Article
Langues
eng
Sous-ensembles de citation
IM
Pagination
5449-5460Subventions
Organisme : Natural Science Foundation of Jiangsu Province
ID : BK20191219
Informations de copyright
© 2021. The Author(s), under exclusive licence to Springer-Verlag GmbH Germany, part of Springer Nature.
Références
Barbier E, Lagorce A, Hachemi A, Dutertre M, Gorlas A, Morand L, Saint-Pierre C, Ravanat JL, Douki T, Armengaud J, Gasparutto D, Confalonieri F, Breton J (2016) Oxidative DNA damage and repair in the radioresistant archaeon Thermococcus gammatolerans. Chem Res Toxicol 29:1796–1809
pubmed: 27676238
doi: 10.1021/acs.chemrestox.6b00128
Chung JH, Im EK, Park HY, Kwon JH, Lee S, Oh J, Hwang KC, Lee JH, Jang Y (2003) A novel uracil-DNA glycosylase family related to the helix-hairpin-helix DNA glycosylase superfamily. Nucleic Acids Res 31:2045–2055
pubmed: 12682355
pmcid: 153747
doi: 10.1093/nar/gkg319
Connolly BA (2009) Recognition of deaminated bases by archaeal family-B DNA polymerases. Biochem Soc Trans 37:65–68
pubmed: 19143603
doi: 10.1042/BST0370065
Dionne I, Bell SD (2005) Characterization of an archaeal family 4 uracil DNA glycosylase and its interaction with PCNA and chromatin proteins. Biochem J 387:859–863
pubmed: 15588253
pmcid: 1135018
doi: 10.1042/BJ20041661
Faucher F, Doublie S, Jia Z (2012) 8-oxoguanine DNA glycosylases: one lesion, three subfamilies. Int J Mol Sci 13:6711–6729
pubmed: 22837659
pmcid: 3397491
doi: 10.3390/ijms13066711
Gan Q, He M, Shi H, Yang Z, Oger P, Ran L, Zhang L (2020) Characterization of a Family IV uracil DNA glycosylase from the hyperthermophilic euryarchaeon Thermococcus barophilus Ch5. Int J Biol Macromol 146:475–481
pubmed: 31881308
doi: 10.1016/j.ijbiomac.2019.12.202
Gehring AM, Zatopek KM, Burkhart BW, Potapov V, Santangelo TJ, Gardner AF (2020) Biochemical reconstitution and genetic characterization of the major oxidative damage base excision DNA repair pathway in Thermococcus kodakarensis. DNA Repair (Amst) 86:102767
doi: 10.1016/j.dnarep.2019.102767
Gouy M, Guindon S, Gascuel O (2010) SeaView version 4: a multiplatform graphical user interface for sequence alignment and phylogenetic tree building. Mol Biol Evol 27:221–224
pubmed: 19854763
doi: 10.1093/molbev/msp259
Grogan DW, Carver GT, Drake JW (2001) Genetic fidelity under harsh conditions: analysis of spontaneous mutation in the thermoacidophilic archaeon Sulfolobus acidocaldarius. Proc Natl Acad Sci U S A 98:7928–7933
pubmed: 11427720
pmcid: 35445
doi: 10.1073/pnas.141113098
Hinks JA, Evans MC, De Miguel Y, Sartori AA, Jiricny J, Pearl LH (2002) An iron-sulfur cluster in the family 4 uracil-DNA glycosylases. J Biol Chem 277:16936–16940
pubmed: 11877410
doi: 10.1074/jbc.M200668200
Hoseki J, Okamoto A, Masui R, Shibata T, Inoue Y, Yokoyama S, Kuramitsu S (2003) Crystal structure of a family 4 uracil-DNA glycosylase from Thermus thermophilus HB8. J Mol Biol 333:515–526
pubmed: 14556741
doi: 10.1016/j.jmb.2003.08.030
Im EK, Han YS, Chung JH (2008) Functional changes in a novel uracil-DNA glycosylase determined by mutational analyses. Mikrobiologiia 77:644–650
pubmed: 19004346
Jacobs KL, Grogan DW (1997) Rates of spontaneous mutation in an archaeon from geothermal environments. J Bacteriol 179:3298–3303
pubmed: 9150227
pmcid: 179110
doi: 10.1128/jb.179.10.3298-3303.1997
Kawai A, Higuchi S, Tsunoda M, Nakamura KT, Yamagata Y, Miyamoto S (2015) Crystal structure of family 4 uracil-DNA glycosylase from Sulfolobus tokodaii and a function of tyrosine 170 in DNA binding. FEBS Lett 589:2675–2682
pubmed: 26318717
doi: 10.1016/j.febslet.2015.08.019
Knaevelsrud I, Moen MN, Grosvik K, Haugland GT, Birkeland NK, Klungland A, Leiros I, Bjelland S (2010) The hyperthermophilic euryarchaeon Archaeoglobus fulgidus repairs uracil by single-nucleotide replacement. J Bacteriol 192:5755–5766
pubmed: 20453094
pmcid: 2953685
doi: 10.1128/JB.00135-10
Kosaka H, Hoseki J, Nakagawa N, Kuramitsu S, Masui R (2007) Crystal structure of family 5 uracil-DNA glycosylase bound to DNA. J Mol Biol 373:839–850
pubmed: 17870091
doi: 10.1016/j.jmb.2007.08.022
Kuznetsov NA, Fedorova OS (2020) Kinetic milestones of damage recognition by DNA glycosylases of the helix-hairpin-helix structural superfamily. Adv Exp Med Biol 1241:1–18
pubmed: 32383112
doi: 10.1007/978-3-030-41283-8_1
Kwon KM, Kang SG, Sokolova TG, Cho SS, Kim YJ, Kim CH, Kwon ST (2016) Characterization of a family B DNA polymerase from Thermococcus barophilus Ch5 and its application for long and accurate PCR. Enzym Microb Technol 86:117–126
doi: 10.1016/j.enzmictec.2016.02.004
Lee HW, Dominy BN, Cao W (2011) New family of deamination repair enzymes in uracil-DNA glycosylase superfamily. J Biol Chem 286:31282–31287
pubmed: 21642431
pmcid: 3173141
doi: 10.1074/jbc.M111.249524
Lin LB, Liu YF, Liu XP, Liu JH (2012) Biochemical characterization of uracil-DNA glycosylase from Pyrococcus furiosus. Chem Res Chinese U 28:477–482
Lindahl T (1993) Instability and decay of the primary structure of DNA. Nature 362:709–715
doi: 10.1038/362709a0
Lindahl T, Nyberg B (1974) Heat-induced deamination of cytosine residues in deoxyribonucleic acid. Biochemistry 13:3405–3410
pubmed: 4601435
doi: 10.1021/bi00713a035
Lingaraju GM, Prota AE, Winkler FK (2009) Mutational studies of Pa-AGOG DNA glycosylase from the hyperthermophilic crenarchaeon Pyrobaculum aerophilum. DNA Repair (Amst) 8:857–864
doi: 10.1016/j.dnarep.2009.03.009
Liu XP, Liu JH (2011) Characterization of family IV UDG from Aeropyrum pernix and its application in hot-start PCR by family B DNA polymerase. PLoS One 6:e27248
pubmed: 22087273
pmcid: 3210769
doi: 10.1371/journal.pone.0027248
Liu X, Roy R (2001) Mutation at active site lysine 212 to arginine uncouples the glycosylase activity from the lyase activity of human endonuclease III. Biochemistry 40:13617–13622
pubmed: 11695910
doi: 10.1021/bi011053b
Marteinsson VT, Birrien JL, Reysenbach AL, Vernet M, Marie D, Gambacorta A, Messner P, Sleytr UB, Prieur D (1999) Thermococcus barophilus sp. nov., a new barophilic and hyperthermophilic archaeon isolated under high hydrostatic pressure from a deep-sea hydrothermal vent. Int J Syst Bacteriol 49:351–359
pubmed: 10319455
doi: 10.1099/00207713-49-2-351
Moen MN, Knvelsrud I, Haugland GT, Grosvik K, Birkeland NK, Klungland A, Bjelland S (2011) Uracil-DNA glycosylase of Thermoplasma acidophilum directs long-patch base excision repair, which is promoted by deoxynucleoside triphosphates and ATP/ADP, into short-patch repair. J Bacteriol 193:4495–4508
pubmed: 21665970
pmcid: 3165510
doi: 10.1128/JB.00233-11
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
pubmed: 12578369
doi: 10.1021/bi026823d
Oger P, Sokolova TG, Kozhevnikova DA, Taranov EA, Vannier P, Lee HS, Kwon KK, Kang SG, Lee JH, Bonch-Osmolovskaya EA, Lebedinsky AV (2016) Complete genome sequence of the hyperthermophilic and piezophilic archaeon Thermococcus barophilus Ch5, capable of growth at the expense of hydrogenogenesis from carbon monoxide and formate. Genome Announc 4
Palud A, Villani G, L ' Haridon S, Querellou J, Raffin JP, Henneke G (2008) Intrinsic properties of the two replicative DNA polymerases of Pyrococcus abyssi in replicating abasic sites: possible role in DNA damage tolerance? Mol Microbiol 70:746–761
pubmed: 18826407
doi: 10.1111/j.1365-2958.2008.06446.x
Sandigursky M, Franklin WA (2000) Uracil-DNA glycosylase in the extreme thermophile Archaeoglobus fulgidus. J Biol Chem 275:19146–19149
pubmed: 10777501
doi: 10.1074/jbc.M001995200
Sartori AA, Schär P, Fitz-Gibbon S, Miller JH, Jiricny J (2001) Biochemical characterization of uracil processing activities in the hyperthermophilic archaeon Pyrobaculum aerophilum. J Biol Chem 276:29979–29986
pubmed: 11399761
doi: 10.1074/jbc.M102985200
Sartori AA, Fitz-Gibbon S, Yang HJ, Miller JH, Jiricny J (2002) A novel uracil-DNA glycosylase with broad substrate specificity and an unusual active site. EMBO J 21:3182–3191
pubmed: 12065430
pmcid: 126064
doi: 10.1093/emboj/cdf309
Sartori AA, Lingaraju GM, Hunziker P, Winkler FK, Jiricny J (2004) Pa-AGOG, the founding member of a new family of archaeal 8-oxoguanine DNA-glycosylases. Nucleic Acids Res 32:6531–6539
pubmed: 15604455
pmcid: 545463
doi: 10.1093/nar/gkh995
Schormann N, Ricciardi R, Chattopadhyay D (2014) Uracil-DNA glycosylases-structural and functional perspectives on an essential family of DNA repair enzymes. Protein Sci 23:1667–1685
pubmed: 25252105
pmcid: 4253808
doi: 10.1002/pro.2554
Shi H, Gan Q, Jiang D, Wu Y, Yin Y, Hou H, Chen H, Xu Y, Miao L, Yang Z, Oger P (2019a) Biochemical characterization and mutational studies of a thermostable uracil DNA glycosylase from the hyperthermophilic euryarchaeon Thermococcus barophilus Ch5. Int J Biol Macromol 134:846–855
pubmed: 31100400
doi: 10.1016/j.ijbiomac.2019.05.073
Shi H, Huang Y, Gan Q, Rui M, Chen H, Tu C, Yang Z, Oger P, Zhang L (2019b) Biochemical characterization of a thermostable DNA ligase from the hyperthermophilic euryarchaeon Thermococcus barophilus Ch5. Appl Microbiol Biotechnol 103:3795–3806
pubmed: 30919103
doi: 10.1007/s00253-019-09736-9
Shiraishi M, Ishino S, Yamagami T, Egashira Y, Kiyonari S, Ishino Y (2015) A novel endonuclease that may be responsible for damaged DNA base repair in Pyrococcus furiosus. Nucleic Acids Res 43:2853–2863
pubmed: 25694513
pmcid: 4357722
doi: 10.1093/nar/gkv121
Shiraishi M, Mizutani K, Yamamoto J, Iwai S (2020) Mutational analysis of Thermococcus kodakarensis endonuclease III reveals the roles of evolutionarily conserved residues. DNA Repair (Amst) 90:102859
doi: 10.1016/j.dnarep.2020.102859
Shuttleworth G, Fogg MJ, Kurpiewski MR, Jen-Jacobson L, Connolly BA (2004) Recognition of the pro-mutagenic base uracil by family B DNA polymerases from archaea. J Mol Biol 337:621–634
pubmed: 15019782
doi: 10.1016/j.jmb.2004.01.021
Starkuviene V, Fritz HJ (2002) A novel type of uracil-DNA glycosylase mediating repair of hydrolytic DNA damage in the extremely thermophilic eubacterium Thermus thermophiles. Nucleic Acids Res 30:2097–2102
pubmed: 12000829
pmcid: 115290
doi: 10.1093/nar/30.10.2097
Yi GS, Wang WW, Cao WG, Wang FP, Liu XP (2017) Sulfolobus acidocaldarius UDG can remove dU from the RNA backbone: insight into the specific recognition of uracil linked with deoxyribose. Genes-Basel:8
Zhang L, Li Y, Shi H, Zhang D, Yang Z, Oger P, Zheng J (2019) Biochemical characterization and mutational studies of the 8-oxoguanine DNA glycosylase from the hyperthermophilic and radioresistant archaeon Thermococcus gammatolerans. Appl Microbiol Biotechnol 103:8021–8033
pubmed: 31372707
doi: 10.1007/s00253-019-10031-w
Zhang L, Shi H, Gan Q, Wang Y, Wu M, Yang Z, Oger P, Zheng J (2020) An alternative pathway for repair of deaminated bases in DNA triggered by archaeal NucS endonuclease. DNA Repair (Amst) 85:102734
doi: 10.1016/j.dnarep.2019.102734