(5'S)-8,5'-cyclo-2'-deoxyguanosine is a Strong Block to Replication, a Potent Pol V-dependent Mutagenic Lesion, and is Inefficiently Repaired in Escherichia Coli

Overview

Journal Biochemistry

Specialty Biochemistry

Date 2011 Apr 16

PMID 21491964

Citations 35

Authors

Vijay P Jasti

Rajat S Das

Benjamin A Hilton

Savithri Weerasooriya

Yue Zou

Ashis K Basu

Affiliations

Soon will be listed here.

Abstract

8,5'-Cyclopurines, making up an important class of ionizing radiation-induced tandem DNA damage, are repaired only by nucleotide excision repair (NER). They accumulate in NER-impaired cells, as in Cockayne syndrome group B and certain Xeroderma Pigmentosum patients. A plasmid containing (5'S)-8,5'-cyclo-2'-deoxyguanosine (S-cdG) was replicated in Escherichia coli with specific DNA polymerase knockouts. Viability was <1% in the wild-type strain, which increased to 5.5% with SOS. Viability decreased further in a pol II(-) strain, whereas it increased considerably in a pol IV(-) strain. Remarkably, no progeny was recovered from a pol V(-) strain, indicating that pol V is absolutely required for bypassing S-cdG. Progeny analyses indicated that S-cdG is significantly mutagenic, inducing ~34% mutation with SOS. Most mutations were S-cdG → A mutations, though S-cdG → T mutation and deletion of 5'C also occurred. Incisions of purified UvrABC nuclease on S-cdG, S-cdA, and C8-dG-AP on a duplex 51-mer showed that the incision rates are C8-dG-AP > S-cdA > S-cdG. In summary, S-cdG is a major block to DNA replication, highly mutagenic, and repaired slowly in E. coli.

Citing Articles

The Influence of 5',8-Cyclo-2'-Deoxyguanosine on ds-DNA Charge Transfer Depends on Its Diastereomeric Form: A Theoretical Study.

Karwowski B Antioxidants (Basel). 2023; 12(4).

PMID: 37107255 PMC: 10135346. DOI: 10.3390/antiox12040881.

The Influence of 5',8-Cyclo-2'-deoxypurines on the Mitochondrial Repair of Clustered DNA Damage in Xrs5 Cells: The Preliminary Study.

Boguszewska K, Kazmierczak-Baranska J, Karwowski B Molecules. 2021; 26(22).

PMID: 34834133 PMC: 8623968. DOI: 10.3390/molecules26227042.

Ne-22 Ion-Beam Radiation Damage to DNA: From Initial Free Radical Formation to Resulting DNA-Base Damage.

Kant M, Jaruga P, Coskun E, Ward S, Stark A, Baumann T ACS Omega. 2021; 6(25):16600-16611.

PMID: 34235332 PMC: 8246699. DOI: 10.1021/acsomega.1c01954.

The Influence of 5' and 5' cdA and cdG on the Activity of BsmAI and SspI Restriction Enzymes.

Szewczuk M, Boguszewska K, Kazmierczak-Baranska J, Karwowski B Molecules. 2021; 26(12).

PMID: 34205449 PMC: 8234751. DOI: 10.3390/molecules26123750.

How (5'S) and (5'R) 5',8-Cyclo-2'-Deoxypurines Affect Base Excision Repair of Clustered DNA Damage in Nuclear Extracts of xrs5 Cells? A Biochemical Study.

Boguszewska K, Szewczuk M, Kazmierczak-Baranska J, Karwowski B Cells. 2021; 10(4).

PMID: 33805115 PMC: 8064110. DOI: 10.3390/cells10040725.

References

Godoy V, Jarosz D, Simon S, Abyzov A, Ilyin V, Walker G . UmuD and RecA directly modulate the mutagenic potential of the Y family DNA polymerase DinB. Mol Cell. 2007; 28(6):1058-70. PMC: 2265384. DOI: 10.1016/j.molcel.2007.10.025. View

Kuraoka I, Robins P, Masutani C, Hanaoka F, Gasparutto D, Cadet J . Oxygen free radical damage to DNA. Translesion synthesis by human DNA polymerase eta and resistance to exonuclease action at cyclopurine deoxynucleoside residues. J Biol Chem. 2001; 276(52):49283-8. DOI: 10.1074/jbc.M107779200. View

Kirkali G, de Souza-Pinto N, Jaruga P, Bohr V, Dizdaroglu M . Accumulation of (5'S)-8,5'-cyclo-2'-deoxyadenosine in organs of Cockayne syndrome complementation group B gene knockout mice. DNA Repair (Amst). 2008; 8(2):274-8. PMC: 2693312. DOI: 10.1016/j.dnarep.2008.09.009. View

Brooks P . The 8,5'-cyclopurine-2'-deoxynucleosides: candidate neurodegenerative DNA lesions in xeroderma pigmentosum, and unique probes of transcription and nucleotide excision repair. DNA Repair (Amst). 2008; 7(7):1168-79. PMC: 2797313. DOI: 10.1016/j.dnarep.2008.03.016. View

Lawrence C, Borden A, BANERJEE S, LeClerc J . Mutation frequency and spectrum resulting from a single abasic site in a single-stranded vector. Nucleic Acids Res. 1990; 18(8):2153-7. PMC: 330696. DOI: 10.1093/nar/18.8.2153. View

Marietta C, Gulam H, Brooks P . A single 8,5'-cyclo-2'-deoxyadenosine lesion in a TATA box prevents binding of the TATA binding protein and strongly reduces transcription in vivo. DNA Repair (Amst). 2003; 1(11):967-75. DOI: 10.1016/s1568-7864(02)00148-9. View

Sancar A, RUPP W . A novel repair enzyme: UVRABC excision nuclease of Escherichia coli cuts a DNA strand on both sides of the damaged region. Cell. 1983; 33(1):249-60. DOI: 10.1016/0092-8674(83)90354-9. View

Kuraoka I, Bender C, Romieu A, Cadet J, Wood R, Lindahl T . Removal of oxygen free-radical-induced 5',8-purine cyclodeoxynucleosides from DNA by the nucleotide excision-repair pathway in human cells. Proc Natl Acad Sci U S A. 2000; 97(8):3832-7. PMC: 18102. DOI: 10.1073/pnas.070471597. View

Hastings P, Hersh M, Thornton P, Fonville N, Slack A, Frisch R . Competition of Escherichia coli DNA polymerases I, II and III with DNA Pol IV in stressed cells. PLoS One. 2010; 5(5):e10862. PMC: 2877720. DOI: 10.1371/journal.pone.0010862. View

10.

Jaruga P, Dizdaroglu M . 8,5'-Cyclopurine-2'-deoxynucleosides in DNA: mechanisms of formation, measurement, repair and biological effects. DNA Repair (Amst). 2008; 7(9):1413-25. DOI: 10.1016/j.dnarep.2008.06.005. View

11.

Raychaudhury P, Basu A . Genetic requirement for mutagenesis of the G[8,5-Me]T cross-link in Escherichia coli: DNA polymerases IV and V compete for error-prone bypass. Biochemistry. 2011; 50(12):2330-8. PMC: 3062377. DOI: 10.1021/bi102064z. View

12.

Jaruga P, Birincioglu M, Rodriguez H, Dizdaroglu M . Mass spectrometric assays for the tandem lesion 8,5'-cyclo-2'-deoxyguanosine in mammalian DNA. Biochemistry. 2002; 41(11):3703-11. DOI: 10.1021/bi016004d. View

13.

Kim S, Matsui K, Yamada M, Gruz P, Nohmi T . Roles of chromosomal and episomal dinB genes encoding DNA pol IV in targeted and untargeted mutagenesis in Escherichia coli. Mol Genet Genomics. 2001; 266(2):207-15. DOI: 10.1007/s004380100541. View

14.

Chatgilialoglu C, Ferreri C, Terzidis M . Purine 5',8-cyclonucleoside lesions: chemistry and biology. Chem Soc Rev. 2011; 40(3):1368-82. DOI: 10.1039/c0cs00061b. View

15.

Luo C, Krishnasamy R, Basu A, Zou Y . Recognition and incision of site-specifically modified C8 guanine adducts formed by 2-aminofluorene, N-acetyl-2-aminofluorene and 1-nitropyrene by UvrABC nuclease. Nucleic Acids Res. 2000; 28(19):3719-24. PMC: 110764. DOI: 10.1093/nar/28.19.3719. View

16.

Jaruga P, Xiao Y, Vartanian V, Lloyd R, Dizdaroglu M . Evidence for the involvement of DNA repair enzyme NEIL1 in nucleotide excision repair of (5'R)- and (5'S)-8,5'-cyclo-2'-deoxyadenosines. Biochemistry. 2010; 49(6):1053-5. PMC: 2817919. DOI: 10.1021/bi902161f. View

17.

Brooks P, Wise D, Berry D, Kosmoski J, Smerdon M, Somers R . The oxidative DNA lesion 8,5'-(S)-cyclo-2'-deoxyadenosine is repaired by the nucleotide excision repair pathway and blocks gene expression in mammalian cells. J Biol Chem. 2000; 275(29):22355-62. DOI: 10.1074/jbc.M002259200. View

18.

Keck K . [Formation of cyclonucleotides during irradiation of aqueous solutions of purine nucleotides]. Z Naturforsch B. 1968; 23(8):1034-43. View

19.

Gasparutto D, Bourdat A, DHam C, Duarte V, Romieu A, Cadet J . Repair and replication of oxidized DNA bases using modified oligodeoxyribonucleotides. Biochimie. 2000; 82(1):19-24. DOI: 10.1016/s0300-9084(00)00347-3. View

20.

Kroeger K, Goodman M, Greenberg M . A comprehensive comparison of DNA replication past 2-deoxyribose and its tetrahydrofuran analog in Escherichia coli. Nucleic Acids Res. 2004; 32(18):5480-5. PMC: 524285. DOI: 10.1093/nar/gkh873. View