Accelerated Repair and Reduced Mutagenicity of DNA Damage Induced by Cigarette Smoke in Human Bronchial Cells Transfected with E.coli Formamidopyrimidine DNA Glycosylase

Overview

Journal PLoS One

Specialties General Medicine
Science

Date 2014 Feb 6

PMID 24498234

Citations 5

Authors

Mara Foresta

Alberto Izzotti

Sebastiano La Maestra

Rosanna Micale

Alessandro Poggi

Donatella Vecchio

Guido Frosina

Affiliations

Soon will be listed here.

Abstract

Cigarette smoke (CS) is associated to a number of pathologies including lung cancer. Its mutagenic and carcinogenic effects are partially linked to the presence of reactive oxygen species and polycyclic aromatic hydrocarbons (PAH) inducing DNA damage. The bacterial DNA repair enzyme formamidopyrimidine DNA glycosylase (FPG) repairs both oxidized bases and different types of bulky DNA adducts. We investigated in vitro whether FPG expression may enhance DNA repair of CS-damaged DNA and counteract the mutagenic effects of CS in human lung cells. NCI-H727 non small cell lung carcinoma cells were transfected with a plasmid vector expressing FPG fused to the Enhanced Green Fluorescent Protein (EGFP). Cells expressing the fusion protein EGFP-FPG displayed accelerated repair of adducts and DNA breaks induced by CS condensate. The mutant frequencies induced by low concentrations of CS condensate to the Na(+)K(+)-ATPase locus (oua(r)) were significantly reduced in cells expressing EGFP-FPG. Hence, expression of the bacterial DNA repair protein FPG stably protects human lung cells from the mutagenic effects of CS by improving cells' capacity to repair damaged DNA.

Citing Articles

Attenuation of Polycyclic Aromatic Hydrocarbon (PAH)-Induced Carcinogenesis and Tumorigenesis by Omega-3 Fatty Acids in Mice In Vivo.

Xia G, Zhou G, Jiang W, Chu C, Wang L, Moorthy B Int J Mol Sci. 2024; 25(7).

PMID: 38612589 PMC: 11012139. DOI: 10.3390/ijms25073781.

Genetic Instability among Hitnü People Living in Colombian Crude-Oil Exploitation Areas.

Galeano-Paez C, Ricardo-Caldera D, Jimenez-Vidal L, Penata-Taborda A, Coneo-Pretelt A, Rumie-Mendoza M Int J Environ Res Public Health. 2022; 19(18).

PMID: 36141477 PMC: 9517229. DOI: 10.3390/ijerph191811189.

Attenuation of Polycyclic Aromatic Hydrocarbon (PAH)-Mediated Pulmonary DNA Adducts and Cytochrome P450 (CYP)1B1 by Dietary Antioxidants, Omega-3 Fatty Acids, in Mice.

Zhou G, Jiang W, Xia G, Wang L, Richardson M, Chu C Antioxidants (Basel). 2022; 11(1).

PMID: 35052622 PMC: 8773186. DOI: 10.3390/antiox11010119.

Monocyte-derived exosomes upon exposure to cigarette smoke condensate alter their characteristics and show protective effect against cytotoxicity and HIV-1 replication.

Haque S, Sinha N, Ranjit S, Midde N, Kashanchi F, Kumar S Sci Rep. 2017; 7(1):16120.

PMID: 29170447 PMC: 5701054. DOI: 10.1038/s41598-017-16301-9.

Exposure of Human Lung Cells to Tobacco Smoke Condensate Inhibits the Nucleotide Excision Repair Pathway.

Holcomb N, Goswami M, Han S, Clark S, Orren D, Gairola C PLoS One. 2016; 11(7):e0158858.

PMID: 27391141 PMC: 4938567. DOI: 10.1371/journal.pone.0158858.

References

Zharkov D, Rieger R, Iden C, Grollman A . NH2-terminal proline acts as a nucleophile in the glycosylase/AP-lyase reaction catalyzed by Escherichia coli formamidopyrimidine-DNA glycosylase (Fpg) protein. J Biol Chem. 1997; 272(8):5335-41. DOI: 10.1074/jbc.272.8.5335. View

Boiteux S, Bichara M, Fuchs R, Laval J . Excision of the imidazole ring-opened form of N-2-aminofluorene-C(8)-guanine adduct in poly(dG-dC) by Escherichia coli formamidopyrimidine-DNA glycosylase. Carcinogenesis. 1989; 10(10):1905-9. DOI: 10.1093/carcin/10.10.1905. View

DeMarini D . Genotoxicity of tobacco smoke and tobacco smoke condensate: a review. Mutat Res. 2004; 567(2-3):447-74. DOI: 10.1016/j.mrrev.2004.02.001. View

. Personal habits and indoor combustions. IARC Monogr Eval Carcinog Risks Hum. 2012; 100(Pt E):1-538. PMC: 4781577. View

DE Flora S, Camoirano A, Cartiglia C, Ferguson L . Modulation of the potency of promutagens and direct acting mutagens in bacteria by inhibitors of the multidrug resistance mechanism. Mutagenesis. 1997; 12(6):431-5. DOI: 10.1093/mutage/12.6.431. View

Pitt S, Chen H, Kunnimalaiyaan M . Phosphatidylinositol 3-kinase-Akt signaling in pulmonary carcinoid cells. J Am Coll Surg. 2009; 209(1):82-8. PMC: 2910111. DOI: 10.1016/j.jamcollsurg.2009.03.006. View

Basu A, Wood M, Niedernhofer L, Ramos L, Essigmann J . Mutagenic and genotoxic effects of three vinyl chloride-induced DNA lesions: 1,N6-ethenoadenine, 3,N4-ethenocytosine, and 4-amino-5-(imidazol-2-yl)imidazole. Biochemistry. 1993; 32(47):12793-801. DOI: 10.1021/bi00210a031. View

Ropolo M, Degan P, Foresta M, DErrico M, Lasiglie D, Dogliotti E . Complementation of the oxidatively damaged DNA repair defect in Cockayne syndrome A and B cells by Escherichia coli formamidopyrimidine DNA glycosylase. Free Radic Biol Med. 2007; 42(12):1807-17. DOI: 10.1016/j.freeradbiomed.2007.03.008. View

Singh N, McCoy M, Tice R, Schneider E . A simple technique for quantitation of low levels of DNA damage in individual cells. Exp Cell Res. 1988; 175(1):184-91. DOI: 10.1016/0014-4827(88)90265-0. View

10.

Kim K, Lee I, Kang K, Cha J, Cho S, Na S . 7,8-Dihydroxyflavone suppresses oxidative stress-induced base modification in DNA via induction of the repair enzyme 8-oxoguanine DNA glycosylase-1. Biomed Res Int. 2013; 2013:863720. PMC: 3787557. DOI: 10.1155/2013/863720. View

11.

Lundin A, Driscoll B . Lung cancer stem cells: progress and prospects. Cancer Lett. 2012; 338(1):89-93. PMC: 3686996. DOI: 10.1016/j.canlet.2012.08.014. View

12.

DE Flora S, Izzotti A, Randerath K, RANDERATH E, Bartsch H, Nair J . DNA adducts and chronic degenerative disease. Pathogenetic relevance and implications in preventive medicine. Mutat Res. 1996; 366(3):197-238. View

13.

Foresta M, Frosina G, Sacca S, Cartiglia C, Longobardi M, Izzotti A . Increased resistance to oxidative DNA damage of trabecular meshwork cells by E. coli FPG gene transfection. Free Radic Res. 2011; 45(7):751-8. DOI: 10.3109/10715762.2011.579122. View

14.

Sidorkina O, Laval J . Role of the N-terminal proline residue in the catalytic activities of the Escherichia coli Fpg protein. J Biol Chem. 2000; 275(14):9924-9. DOI: 10.1074/jbc.275.14.9924. View

15.

Phillips D, Farmer P, Beland F, Nath R, Poirier M, Reddy M . Methods of DNA adduct determination and their application to testing compounds for genotoxicity. Environ Mol Mutagen. 2000; 35(3):222-33. DOI: 10.1002/(sici)1098-2280(2000)35:3<222::aid-em9>3.0.co;2-e. View

16.

Coste F, Ober M, Le Bihan Y, Izquierdo M, Hervouet N, Mueller H . Bacterial base excision repair enzyme Fpg recognizes bulky N7-substituted-FapydG lesion via unproductive binding mode. Chem Biol. 2008; 15(7):706-17. DOI: 10.1016/j.chembiol.2008.05.014. View

17.

Canitrot Y, Frechet M, Servant L, Cazaux C, Hoffmann J . Overexpression of DNA polymerase beta: a genomic instability enhancer process. FASEB J. 1999; 13(9):1107-11. DOI: 10.1096/fasebj.13.9.1107. View

18.

Migliaccio A, Bengra C, Ling J, Pi W, Li C, Zeng S . Stable and unstable transgene integration sites in the human genome: extinction of the Green Fluorescent Protein transgene in K562 cells. Gene. 2000; 256(1-2):197-214. DOI: 10.1016/s0378-1119(00)00353-x. View

19.

Asagoshi K, Yamada T, Terato H, Ohyama Y, Monden Y, Arai T . Distinct repair activities of human 7,8-dihydro-8-oxoguanine DNA glycosylase and formamidopyrimidine DNA glycosylase for formamidopyrimidine and 7,8-dihydro-8-oxoguanine. J Biol Chem. 2000; 275(7):4956-64. DOI: 10.1074/jbc.275.7.4956. View

20.

Izzotti A, Bagnasco M, DAgostini F, Cartiglia C, Lubet R, Kelloff G . Formation and persistence of nucleotide alterations in rats exposed whole-body to environmental cigarette smoke. Carcinogenesis. 1999; 20(8):1499-505. DOI: 10.1093/carcin/20.8.1499. View