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Hoogsteen base pair formation promotes synthesis opposite the 1,N6-ethenodeoxyadenosine lesion by human DNA polymerase iota.

Nair DT, Johnson RE, Prakash L, Prakash S, Aggarwal AK
Nat Struct Mol Biol 13 619-25 (2006)
Cited: 78 times
EuropePMC logo PMID: 16819516

Abstract

The 1,N6-ethenodeoxyadenosine (epsilon dA) lesion is promutagenic and has been implicated in carcinogenesis. We show here that human Pol iota, a Y-family DNA polymerase, can promote replication through this lesion by proficiently incorporating a nucleotide opposite it. The structural basis of this action is rotation of the epsilon dA adduct to the syn conformation in the Pol iota active site and presentation of its 'Hoogsteen edge' for hydrogen-bonding with incoming dTTP or dCTP. We also show that Pol zeta carries out the subsequent extension reaction and that efficiency of extension from epsilon dA x T is notably higher than from epsilon dA x C. Together, our studies reveal for the first time how the exocyclic epsilon dA adduct is accommodated in a DNA polymerase active site, and they show that the combined action of Pol iota and Pol zeta provides for efficient and error-free synthesis through this potentially carcinogenic DNA lesion.

Reviews - 2dpj mentioned but not cited (2)

  1. An overview of Y-Family DNA polymerases and a case study of human DNA polymerase η. Yang W. Biochemistry 53 2793-2803 (2014)
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Articles - 2dpj mentioned but not cited (3)

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  3. The dipeptidyl peptidase IV inhibitors vildagliptin and K-579 inhibit a phospholipase C: a case of promiscuous scaffolds in proteins. Chakraborty S, Rendón-Ramírez A, Ásgeirsson B, Dutta M, Ghosh AS, Oda M, Venkatramani R, Rao BJ, Dandekar AM, Goñi FM. F1000Res 2 286 (2013)


Reviews citing this publication (14)

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Articles citing this publication (59)

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  20. Translesion synthesis DNA polymerases promote error-free replication through the minor-groove DNA adduct 3-deaza-3-methyladenine. Yoon JH, Roy Choudhury J, Park J, Prakash S, Prakash L. J Biol Chem 292 18682-18688 (2017)
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  28. Column switching HPLC-ESI(+)-MS/MS methods for quantitative analysis of exocyclic dA adducts in the DNA of laboratory animals exposed to 1,3-butadiene. Goggin M, Seneviratne U, Swenberg JA, Walker VE, Tretyakova N. Chem Res Toxicol 23 808-812 (2010)
  29. Replication of the 2,6-diamino-4-hydroxy-N(5)-(methyl)-formamidopyrimidine (MeFapy-dGuo) adduct by eukaryotic DNA polymerases. Christov PP, Yamanaka K, Choi JY, Takata K, Wood RD, Guengerich FP, Lloyd RS, Rizzo CJ. Chem Res Toxicol 25 1652-1661 (2012)
  30. DNA polymerase θ accomplishes translesion synthesis opposite 1,N6-ethenodeoxyadenosine with a remarkably high fidelity in human cells. Yoon JH, Johnson RE, Prakash L, Prakash S. Genes Dev 33 282-287 (2019)
  31. Accommodation of an N-(deoxyguanosin-8-yl)-2-acetylaminofluorene adduct in the active site of human DNA polymerase iota: Hoogsteen or Watson-Crick base pairing? Donny-Clark K, Shapiro R, Broyde S. Biochemistry 48 7-18 (2009)
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  42. Tuning the DNA conformational perturbations induced by cytotoxic platinum-acridine bisintercalators: effect of metal cis/trans isomerism and DNA threading groups. Choudhury JR, Guddneppanavar R, Saluta G, Kucera GL, Bierbach U. J Med Chem 51 3069-3072 (2008)
  43. Characterizing Watson-Crick versus Hoogsteen Base Pairing in a DNA-Protein Complex Using Nuclear Magnetic Resonance and Site-Specifically 13C- and 15N-Labeled DNA. Zhou H, Sathyamoorthy B, Stelling A, Xu Y, Xue Y, Pigli YZ, Case DA, Rice PA, Al-Hashimi HM. Biochemistry 58 1963-1974 (2019)
  44. DNA Polymerases η and ζ Combine to Bypass O(2)-[4-(3-Pyridyl)-4-oxobutyl]thymine, a DNA Adduct Formed from Tobacco Carcinogens. Gowda AS, Spratt TE. Chem Res Toxicol 29 303-316 (2016)
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  47. A novel role of DNA polymerase λ in translesion synthesis in conjunction with DNA polymerase ζ. Yoon JH, Basu D, Sellamuthu K, Johnson RE, Prakash S, Prakash L. Life Sci Alliance 4 e202000900 (2021)
  48. Infrared Spectroscopic Observation of a G-C+ Hoogsteen Base Pair in the DNA:TATA-Box Binding Protein Complex Under Solution Conditions. Stelling AL, Liu AY, Zeng W, Salinas R, Schumacher MA, Al-Hashimi HM. Angew Chem Int Ed Engl 58 12010-12013 (2019)
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  52. Alternative splicing at exon 2 results in the loss of the catalytic activity of mouse DNA polymerase iota in vitro. Kazachenko KY, Miropolskaya NA, Gening LV, Tarantul VZ, Makarova AV. DNA Repair (Amst) 50 77-82 (2017)
  53. Identification of amino acid residues involved in the dRP-lyase activity of human Pol ι. Miropolskaya N, Petushkov I, Kulbachinskiy A, Makarova AV. Sci Rep 7 10194 (2017)
  54. Mechanism of error-free DNA synthesis across N1-methyl-deoxyadenosine by human DNA polymerase-ι. Jain R, Choudhury JR, Buku A, Johnson RE, Prakash L, Prakash S, Aggarwal AK. Sci Rep 7 43904 (2017)
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  56. Translesion synthesis DNA polymerases η, ι, and ν promote mutagenic replication through the anticancer nucleoside cytarabine. Yoon JH, Roy Choudhury J, Prakash L, Prakash S. J Biol Chem 294 19048-19054 (2019)
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