The Human DNA Repair Factor XPC-HR23B Distinguishes Stereoisomeric Benzo[a]pyrenyl-DNA Lesions

Overview

Journal EMBO J

Specialties Biotechnology
Molecular Biology

Date 2007 May 26

PMID 17525733

Citations 52

Authors

Vincent Mocquet

Konstantin Kropachev

Marina Kolbanovskiy

Alexander Kolbanovskiy

Angels Tapias

Yuqin Cai

Suse Broyde

Nicholas E Geacintov

Jean-Marc Egly

Affiliations

Soon will be listed here.

Abstract

Benzo[a]pyrene (B[a]P), a known environmental pollutant and tobacco smoke carcinogen, is metabolically activated to highly tumorigenic B[a]P diol epoxide derivatives that predominantly form N(2)-guanine adducts in cellular DNA. Although nucleotide excision repair (NER) is an important cellular defense mechanism, the molecular basis of recognition of these bulky lesions is poorly understood. In order to investigate the effects of DNA adduct structure on NER, three stereoisomeric and conformationally different B[a]P-N(2)-dG lesions were site specifically incorporated into identical 135-mer duplexes and their response to purified NER factors was investigated. Using a permanganate footprinting assay, the NER lesion recognition factor XPC/HR23B exhibits, in each case, remarkably different patterns of helix opening that is also markedly distinct in the case of an intra-strand crosslinked cisplatin adduct. The different extents of helix distortions, as well as differences in the overall binding of XPC/HR23B to double-stranded DNA containing either of the three stereoisomeric B[a]P-N(2)-dG lesions, are correlated with dual incisions catalyzed by a reconstituted incision system of six purified NER factors, and by the full NER apparatus in cell-free nuclear extracts.

Citing Articles

Treatment of Human HeLa Cells with Black Raspberry Extracts Enhances the Removal of DNA Lesions by the Nucleotide Excision Repair Mechanism.

Sales A, Kolbanovskiy M, Geacintov N, Chen K, Sun Y, El-Bayoumy K Antioxidants (Basel). 2022; 11(11).

PMID: 36358482 PMC: 9686895. DOI: 10.3390/antiox11112110.

DNA Repair in Haploid Context.

Mourrain L, Boissonneault G Int J Mol Sci. 2021; 22(22).

PMID: 34830299 PMC: 8620282. DOI: 10.3390/ijms222212418.

Molecular dynamics simulations reveal how H3K56 acetylation impacts nucleosome structure to promote DNA exposure for lesion sensing.

Fu I, Geacintov N, Broyde S DNA Repair (Amst). 2021; 107:103201.

PMID: 34399316 PMC: 8526387. DOI: 10.1016/j.dnarep.2021.103201.

Excision of Oxidatively Generated Guanine Lesions by Competitive DNA Repair Pathways.

Shafirovich V, Geacintov N Int J Mol Sci. 2021; 22(5).

PMID: 33800059 PMC: 7962115. DOI: 10.3390/ijms22052698.

Remarkable Enhancement of Nucleotide Excision Repair of a Bulky Guanine Lesion in a Covalently Closed Circular DNA Plasmid Relative to the Same Linearized Plasmid.

Kolbanovskiy M, Aharonoff A, Sales A, Geacintov N, Shafirovich V Biochemistry. 2020; 59(31):2842-2848.

PMID: 32786887 PMC: 7444659. DOI: 10.1021/acs.biochem.0c00441.

References

Jiang Y, Gralla J . Nucleotide requirements for activated RNA polymerase II open complex formation in vitro. J Biol Chem. 1995; 270(3):1277-81. DOI: 10.1074/jbc.270.3.1277. View

Teuben J, Bauer C, Wang A, Reedijk J . Solution structure of a DNA duplex containing a cis-diammineplatinum(II) 1,3-d(GTG) intrastrand cross-link, a major adduct in cells treated with the anticancer drug carboplatin. Biochemistry. 1999; 38(38):12305-12. DOI: 10.1021/bi9904757. View

Zou Y, Liu T, Geacintov N, Van Houten B . Interaction of the UvrABC nuclease system with a DNA duplex containing a single stereoisomer of dG-(+)- or dG-(-)-anti-BPDE. Biochemistry. 1995; 34(41):13582-93. DOI: 10.1021/bi00041a038. View

Gunz D, Hess M, Naegeli H . Recognition of DNA adducts by human nucleotide excision repair. Evidence for a thermodynamic probing mechanism. J Biol Chem. 1996; 271(41):25089-98. DOI: 10.1074/jbc.271.41.25089. View

Geacintov N, Cosman M, Hingerty B, Amin S, Broyde S, Patel D . NMR solution structures of stereoisometric covalent polycyclic aromatic carcinogen-DNA adduct: principles, patterns, and diversity. Chem Res Toxicol. 1997; 10(2):111-46. DOI: 10.1021/tx9601418. View

Hess M, Schwitter U, Petretta M, Giese B, Naegeli H . Bipartite substrate discrimination by human nucleotide excision repair. Proc Natl Acad Sci U S A. 1997; 94(13):6664-9. PMC: 21215. DOI: 10.1073/pnas.94.13.6664. View

Hess M, Gunz D, Luneva N, Geacintov N, Naegeli H . Base pair conformation-dependent excision of benzo[a]pyrene diol epoxide-guanine adducts by human nucleotide excision repair enzymes. Mol Cell Biol. 1997; 17(12):7069-76. PMC: 232563. DOI: 10.1128/MCB.17.12.7069. View

Seo K, Jelinsky S, Loechler E . Factors that influence the mutagenic patterns of DNA adducts from chemical carcinogens. Mutat Res. 2000; 463(3):215-46. DOI: 10.1016/s1383-5742(00)00047-8. View

Sugasawa K, Okamoto T, Shimizu Y, Masutani C, Iwai S, Hanaoka F . A multistep damage recognition mechanism for global genomic nucleotide excision repair. Genes Dev. 2001; 15(5):507-21. PMC: 312644. DOI: 10.1101/gad.866301. View

10.

Geacintov N, Broyde S, Buterin T, Naegeli H, Wu M, Yan S . Thermodynamic and structural factors in the removal of bulky DNA adducts by the nucleotide excision repair machinery. Biopolymers. 2002; 65(3):202-10. DOI: 10.1002/bip.10239. View

11.

Pfeifer G, Denissenko M, Olivier M, Tretyakova N, Hecht S, Hainaut P . Tobacco smoke carcinogens, DNA damage and p53 mutations in smoking-associated cancers. Oncogene. 2002; 21(48):7435-51. DOI: 10.1038/sj.onc.1205803. View

12.

Sugasawa K, Shimizu Y, Iwai S, Hanaoka F . A molecular mechanism for DNA damage recognition by the xeroderma pigmentosum group C protein complex. DNA Repair (Amst). 2003; 1(1):95-107. DOI: 10.1016/s1568-7864(01)00008-8. View

13.

Yan S, Wu M, Patel D, Geacintov N, Broyde S . Simulating structural and thermodynamic properties of carcinogen-damaged DNA. Biophys J. 2003; 84(4):2137-48. PMC: 1302781. DOI: 10.1016/S0006-3495(03)75020-6. View

14.

Riedl T, Hanaoka F, Egly J . The comings and goings of nucleotide excision repair factors on damaged DNA. EMBO J. 2003; 22(19):5293-303. PMC: 204472. DOI: 10.1093/emboj/cdg489. View

15.

Hanawalt P, Ford J, Lloyd D . Functional characterization of global genomic DNA repair and its implications for cancer. Mutat Res. 2003; 544(2-3):107-14. DOI: 10.1016/j.mrrev.2003.06.002. View

16.

Tapias A, Auriol J, Forget D, Enzlin J, Scharer O, Coin F . Ordered conformational changes in damaged DNA induced by nucleotide excision repair factors. J Biol Chem. 2004; 279(18):19074-83. PMC: 4494833. DOI: 10.1074/jbc.M312611200. View

17.

Isaacs R, Spielmann H . A model for initial DNA lesion recognition by NER and MMR based on local conformational flexibility. DNA Repair (Amst). 2004; 3(5):455-64. DOI: 10.1016/j.dnarep.2004.01.004. View

18.

Weinstein I, Jeffrey A, Jennette K, Blobstein S, Harvey R, Harris C . Benzo(a)pyrene diol epoxides as intermediates in nucleic acid binding in vitro and in vivo. Science. 1976; 193(4253):592-5. DOI: 10.1126/science.959820. View

19.

Koreeda M, Moore P, Wislocki P, Levin W, Yagi H, Jerina D . Binding of benzo[a]pyrene 7,8-diol-9,10-epoxides to DNA, RNA, and protein of mouse skin occurs with high stereoselectivity. Science. 1978; 199(4330):778-81. DOI: 10.1126/science.622566. View

20.

Buening M, Wislocki P, Levin W, Yagi H, Thakker D, Akagi H . Tumorigenicity of the optical enantiomers of the diastereomeric benzo[a]pyrene 7,8-diol-9,10-epoxides in newborn mice: exceptional activity of (+)-7beta,8alpha-dihydroxy-9alpha,10alpha-epoxy-7,8,9,10-tetrahydrobenzo[a]pyrene. Proc Natl Acad Sci U S A. 1978; 75(11):5358-61. PMC: 392962. DOI: 10.1073/pnas.75.11.5358. View