151
Views
2
CrossRef citations to date
0
Altmetric
Rapid Communication

G4 DNA present at human telomeric DNA contributes toward reduced sensitivity to γ-radiation induced oxidative damage, but not bulky adduct formation

, , , , , , , & ORCID Icon show all
Pages 1166-1180 | Received 04 Mar 2020, Accepted 23 Jun 2021, Published online: 06 Aug 2021

References

  • Alshykhly OR, Fleming AM, Burrows CJ. 2015. 5-Carboxamido-5-formamido-2-iminohydantoin, in addition to 8-oxo-7,8-dihydroguanine, is the major product of the iron-Fenton or X-ray radiation-induced oxidation of guanine under aerobic reducing conditions in nucleoside and DNA contexts. J Org Chem. 80(14):6996–7007.
  • Ambrus A, Chen D, Dai J, Bialis T, Jones RA, Yang D. 2006. Human telomeric sequence forms a hybrid-type intramolecular G-quadruplex structure with mixed parallel/antiparallel strands in potassium solution. Nucleic Acids Res. 34(9):2723–2735.
  • Anchordoquy TJ, Molina Md, Kempner ES. 2009. A radiation target method for size determination of supercoiled plasmid DNA. Anal Biochem. 385(2):229–233.
  • Blaisdell JO, Wallace SS. 2001. Abortive base-excision repair of radiation-induced clustered DNA lesions in Escherichia coli. Proc Natl Acad Sci U S A. 98(13):7426–7430.
  • Bochman ML, Paeschke K, Zakian VA. 2012. DNA secondary structures: stability and function of G-quadruplex structures. Nat Rev Genet. 13(11):770–780.
  • Bryan TM, Baumann P. 2011. G-quadruplexes: from guanine gels to chemotherapeutics. Mol Biotechnol. 49(2):198–208.
  • Cadet J, Bellon S, Douki T, Frelon S, Gasparutto D, Muller E, Pouget JP, Ravanat JL, Romieu A, Sauvaigo S. 2004. Radiation-induced DNA damage: formation, measurement, and biochemical features. J Environ Pathol Toxicol Oncol. 23(1):33–43.
  • Castaing B, Geiger A, Seliger H, Nehls P, Laval J, Zelwer C, Boiteux S. 1993. Cleavage and binding of a DNA fragment containing a single 8-oxoguanine by wild type and mutant FPG proteins. Nucleic Acids Res. 21(12):2899–2905.
  • Chambers VS, Marsico G, Boutell JM, Di Antonio M, Smith GP, Balasubramanian S. 2015. High-throughput sequencing of DNA G-quadruplex structures in the human genome. Nat Biotechnol. 33(8):877–881.
  • Chatgilialoglu C, Eriksson LA, Krokidis MG, Masi A, Wang S, Zhang R. 2020. Oxygen dependent purine lesions in double-stranded oligodeoxynucleotides: kinetic and computational studies highlight the mechanism for 5′,8-cyclopurine formation. J Am Chem Soc. 142(12):5825–5833.
  • Chetsanga CJ, Lindahl T. 1979. Release of 7-methylguanine residues whose imidazole rings have been opened from damaged DNA by a DNA glycosylase from Escherichia coli. Nucleic Acids Res. 6(11):3673–3684.
  • Choi J, Park J, Tanaka A, Park MJ, Jang YJ, Fujitsuka M, Kim SK, Majima T. 2013. Hole trapping of G-quartets in a G-quadruplex. Angew Chem Int Ed Engl. 52(4):1134–1138.
  • Daly MJ. 2009. A new perspective on radiation resistance based on Deinococcus radiodurans. Nat Rev Microbiol. 7(3):237–245.
  • Das K, Srivastava M, Raghavan SC. 2016. GNG motifs can replace a GGG stretch during G-quadruplex formation in a context dependent manner. PLoS One. 11(7):e0158794.
  • de Lange T. 2002. Protection of mammalian telomeres. Oncogene. 21(4):532–540.
  • Gulston M, Fulford J, Jenner T, de Lara C, O'Neill P. 2002. Clustered DNA damage induced by gamma radiation in human fibroblasts (HF19), hamster (V79-4) cells and plasmid DNA is revealed as Fpg and Nth sensitive sites. Nucleic Acids Res. 30(15):3464–3472.
  • Hanish JP, Yanowitz JL, de Lange T. 1994. Stringent sequence requirements for the formation of human telomeres. Proc Natl Acad Sci U S A. 91(19):8861–8865.
  • Jackson SP, Bartek J. 2009. The DNA-damage response in human biology and disease. Nature. 461(7267):1071–1078.
  • Jain R, Kumar P, Varshney U. 2007. A distinct role of formamidopyrimidine DNA glycosylase (MutM) in down-regulation of accumulation of G, C mutations and protection against oxidative stress in mycobacteria. DNA Repair. 6(12):1774–1785.
  • Jaiswal V, Misra P, Shukla P, Ramteke P, Tiku A. 2012. In vitro DNA damage characterisation studies on plasmid pBR322 after exposure to γ radiation by 60Co. J Radioanal Nucl Chem. 291(3):661–664.
  • Krisko A, Radman M. 2013. Biology of extreme radiation resistance: the way of Deinococcus radiodurans. Cold Spring Harb Perspect Biol. 5:a012765.
  • Kumari N, Raghavan SC. 2021. G-quadruplex DNA structures and their relevance in radioprotection. Biochim Biophys Acta Gen Subj. 1865(5):129857.
  • Kumari N, Vartak SV, Dahal S, Kumari S, Desai SS, Gopalakrishnan V, Choudhary B, Raghavan SC. 2019. G-quadruplex structures contribute to differential radiosensitivity of the human genome. iScience. 21:288–307.
  • Kumari R, Raghavan SC. 2015. Structure-specific nuclease activity of RAGs is modulated by sequence, length and phase position of flanking double-stranded DNA. FEBS J. 282(1):4–18.
  • Lett JT. 1992. Damage to cellular DNA from particulate radiations, the efficacy of its processing and the radiosensitivity of mammalian cells. Emphasis on DNA double strand breaks and chromatin breaks. Radiat Environ Biophys. 31(4):257–277.
  • Lobrich M, Cooper PK, Rydberg B. 1996. Non-random distribution of DNA double-strand breaks induced by particle irradiation. Int J Radiat Biol. 70:493–503.
  • Naik AK, Raghavan SC. 2008. P1 nuclease cleavage is dependent on length of the mismatches in DNA. DNA Repair. 7(8):1384–1391.
  • Naik AK, Lieber MR, Raghavan SC. 2010. Cytosines, but not purines, determine recombination activating gene (RAG)-induced breaks on heteroduplex DNA structures: implications for genomic instability. J Biol Chem. 285(10):7587–7597.
  • Nambiar M, Goldsmith G, Moorthy BT, Lieber MR, Joshi MV, Choudhary B, Hosur RV, Raghavan SC. 2011. Formation of a G-quadruplex at the BCL2 major breakpoint region of the t(14;18) translocation in follicular lymphoma. Nucleic Acids Res. 39(3):936–948.
  • Nambiar M, Srivastava M, Gopalakrishnan V, Sankaran SK, Raghavan SC. 2013. G-quadruplex structures formed at the HOX11 breakpoint region contribute to its fragility during t(10;14) translocation in T-cell leukemia. Mol Cell Biol. 33(21):4266–4281.
  • Nevins SA, Siles BA, Nackerdien ZE. 2000. Analysis of gamma radiation-induced damage to plasmid DNA using dynamic size-sieving capillary electrophoresis. J Chromatogr B Biomed Sci Appl. 741(2):243–255.
  • Nikiforov YE, Koshoffer A, Nikiforova M, Stringer J, Fagin JA. 1999. Chromosomal breakpoint positions suggest a direct role for radiation in inducing illegitimate recombination between the ELE1 and RET genes in radiation-induced thyroid carcinomas. Oncogene. 18(46):6330–6334.
  • Oganesian L, Bryan TM. 2007. Physiological relevance of telomeric G-quadruplex formation: a potential drug target. Bioessays. 29(2):155–165.
  • Paeschke K, Simonsson T, Postberg J, Rhodes D, Lipps HJ. 2005. Telomere end-binding proteins control the formation of G-quadruplex DNA structures in vivo. Nat Struct Mol Biol. 12(10):847–854.
  • Pang D, Rodgers JE, Berman BL, Chasovskikh S, Dritschilo A. 2005. Spatial distribution of radiation-induced double-strand breaks in plasmid DNA as resolved by atomic force microscopy. Radiat Res. 164(6):755–765.
  • Parkinson GN, Lee MPH, Neidle S. 2002. Crystal structure of parallel quadruplexes from human telomeric DNA. Nature. 417(6891):876–880.
  • Phan AT. 2010. Human telomeric G-quadruplex: structures of DNA and RNA sequences. FEBS J. 277(5):1107–1117.
  • Phan AT, Mergny JL. 2002. Human telomeric DNA: G-quadruplex, i-motif and Watson-Crick double helix. Nucleic Acids Res. 30(21):4618–4625.
  • Poetsch AR. 2020. The genomics of oxidative DNA damage, repair, and resulting mutagenesis. Comput Struct Biotechnol J. 18:207–219.
  • Puerto S, Ramirez MJ, Marcos R, Creus A, Surralles J. 2001. Radiation-induced chromosome aberrations in human euchromatic (17cen-p53) and heterochromatic (1cen-1q12) regions. Mutagenesis. 16(4):291–296.
  • Raghavan SC, Chastain P, Lee JS, Hegde BG, Houston S, Langen R, Hsieh CL, Haworth IS, Lieber MR. 2005. Evidence for a triplex DNA conformation at the bcl-2 major breakpoint region of the t(14;18) translocation. J Biol Chem. 280(24):22749–22760.
  • Rastogi RP, Richa Kumar A, Tyagi MB, Sinha RP. 2010. Molecular mechanisms of ultraviolet radiation-induced DNA damage and repair. J Nucleic Acids. 2010:592980.
  • Rhee DB, Ghosh A, Lu J, Bohr VA, Liu Y. 2011. Factors that influence telomeric oxidative base damage and repair by DNA glycosylase OGG1. DNA Repair. 10(1):34–44.
  • Rhodes D, Lipps HJ. 2015. G-quadruplexes and their regulatory roles in biology. Nucleic Acids Res. 43(18):8627–8637.
  • Sambrook J, Fritsch EF, Maniatis T. 1989. Molecular cloning: a laboratory manual. Cold Spring Harbor (NY): Cold Spring Harbor Laboratory.
  • Sancar A, Lindsey-Boltz LA, Unsal-Kacmaz K, Linn S. 2004. Molecular mechanisms of mammalian DNA repair and the DNA damage checkpoints. Annu Rev Biochem. 73:39–85.
  • Sinden RR. 2012. DNA structure and function. San Diego: Academic Press.
  • Snapper SB, Melton RE, Mustafa S, Kieser T, Jacobs WR Jr. 1990. Isolation and characterization of efficient plasmid transformation mutants of Mycobacterium smegmatis. Mol Microbiol. 4(11):1911–1919.
  • Steenken S. 1997. Electron transfer in DNA? Competition by ultra-fast proton transfer? Biol Chem. 378:1293–1297.
  • Symington LS, Gautier J. 2011. Double-strand break end resection and repair pathway choice. Annu Rev Genet. 45:247–271.
  • Tchou J, Bodepudi V, Shibutani S, Antoshechkin I, Miller J, Grollman AP, Johnson F. 1994. Substrate specificity of Fpg protein. Recognition and cleavage of oxidatively damaged DNA. J Biol Chem. 269(21):15318–15324.
  • Thakur M, Kumar MB, Muniyappa K. 2016. Mycobacterium tuberculosis UvrB is a robust DNA-stimulated ATPase that also possesses structure-specific ATP-dependent DNA helicase activity. Biochemistry. 55(41):5865–5883.
  • Triccas JA, Winter N, Roche PW, Gilpin A, Kendrick KE, Britton WJ. 1998. Molecular and immunological analyses of the Mycobacterium avium homolog of the immunodominant Mycobacterium leprae 35-kilodalton protein. Infect Immun. 66(6):2684–2690.
  • Van Der Schans GP. 1978. Gamma-ray induced double-strand breaks in DNA resulting from randomly-inflicted single-strand breaks: temporal local denaturation, a new radiation phenomenon? Int J Radiat Biol Relat Stud Phys Chem Med. 33(2):105–120.
  • Vignard J, Mirey G, Salles B. 2013. Ionizing-radiation induced DNA double-strand breaks: a direct and indirect lighting up. Radiother Oncol. 108(3):362–369.
  • Wu L, Liu K, Jie J, Song D, Su H. 2015. Direct observation of guanine radical cation deprotonation in G-quadruplex DNA. J Am Chem Soc. 137(1):259–266.
  • Yang Z, Colis LC, Basu AK, Zou Y. 2005. Recognition and incision of gamma-radiation-induced cross-linked guanine-thymine tandem lesion G[8,5-Me]T by UvrABC nuclease. Chem Res Toxicol. 18(9):1339–1346.
  • Yoshihara M, Jiang L, Akatsuka S, Suyama M, Toyokuni S. 2014. Genome-wide profiling of 8-oxoguanine reveals its association with spatial positioning in nucleus. DNA Res. 21(6):603–612.

Reprints and Corporate Permissions

Please note: Selecting permissions does not provide access to the full text of the article, please see our help page How do I view content?

To request a reprint or corporate permissions for this article, please click on the relevant link below:

Academic Permissions

Please note: Selecting permissions does not provide access to the full text of the article, please see our help page How do I view content?

Obtain permissions instantly via Rightslink by clicking on the button below:

If you are unable to obtain permissions via Rightslink, please complete and submit this Permissions form. For more information, please visit our Permissions help page.