Cigarette Smoke Condensate-induced Oxidative DNA Damage and Its Removal in Human Cervical Cancer Cells

Overview

Journal Int J Oncol

Specialty Oncology

Date 2011 Jul 2

PMID 21720711

Citations 15

Authors

Afsoon Moktar

Rajesh Singh

Manicka V Vadhanam

Srivani Ravoori

James W Lillard

C Gary Gairola

Ramesh C Gupta

Affiliations

Soon will be listed here.

Abstract

Exposure to cigarette smoke is well documented to increase oxidative stress and could account for higher risk of cervical cancer in smokers. Cervical pre-cancerous lesions that are initiated by human papillomavirus (HPV) infection generally regress in the absence of known risk factors such as smoking. 8-oxodeoxyguanosine (8-oxodG) is a highly mutagenic oxidative DNA lesion that is formed by the oxidation of deoxyguanosine. In the present study, we examined: a) the effect of cigarette smoke condensate (CSC) on 8-oxodG formation in and its removal from HPV-transfected (ECT1/E6 E7), HPV-positive (CaSki) and HPV-negative (C33A) human cervical cancer cells, and b) the cell cycle progression and apoptosis in CSC-treated ECT1/E6 E7 cells. CSC induced 8-oxodG in a dose- (p=0.03) and time (p=0.002)-dependent fashion in ECT1/E6 E7 cells as determined by flow cytometry. A 2.4-fold higher level of 8-oxodG was observed in HPV-positive compared with HPV-negative cells. However, 8-oxodG lesions were almost completely removed 72 h post-exposure in all cell lines as determined by ImageStream analysis. This observation correlates with the 2- and 5-fold increase in the p53 levels in ECT1/E6 E7 and CaSki cells with no significant change in C33A cells. We conclude that: a) cigarette smoke constituents induce oxidative stress with higher burden in HPV-positive cervical cancer cells and b) the significant increase observed in p53 levels in wild-type cervical cells (ECT1/E6 E7 and CaSki) may be attributed to the p53-dependent DNA repair pathway while a p53-independent pathway in C33A cells cannot be ruled out.

Citing Articles

Emerging paradigms: unmasking the role of oxidative stress in HPV-induced carcinogenesis.

Letafati A, Taghiabadi Z, Zafarian N, Tajdini R, Mondeali M, Aboofazeli A Infect Agent Cancer. 2024; 19(1):30.

PMID: 38956668 PMC: 11218399. DOI: 10.1186/s13027-024-00581-8.

β-Caryophyllene Counteracts Chemoresistance Induced by Cigarette Smoke in Triple-Negative Breast Cancer MDA-MB-468 Cells.

Di Sotto A, Gulli M, Minacori M, Mancinelli R, Garzoli S, Percaccio E Biomedicines. 2022; 10(9).

PMID: 36140359 PMC: 9496176. DOI: 10.3390/biomedicines10092257.

Smoking cessation strategy in the national cervical cancer screening program (SUCCESS): study protocol for a pragmatic cluster randomised trial and process evaluation in Dutch general practice.

Mansour M, Crone M, Sert E, van Weert H, Chavannes N, van Asselt K BMJ Open. 2022; 12(4):e055812.

PMID: 35379626 PMC: 8981275. DOI: 10.1136/bmjopen-2021-055812.

Relationship between Air Pollutant Exposure and Gynecologic Cancer Risk.

Yu Q, Zhang L, Hou K, Li J, Liu S, Huang K Int J Environ Res Public Health. 2021; 18(10).

PMID: 34069801 PMC: 8157305. DOI: 10.3390/ijerph18105353.

Purple corn extract (PCE) alleviates cigarette smoke (CS)-induced DNA damage in rodent blood cells by activation of AMPK/Foxo3a/MnSOD pathway.

Kim W, Kim C, Lee J, Jeon J, Kang B, Warkad M Anim Cells Syst (Seoul). 2021; 25(1):65-73.

PMID: 33717418 PMC: 7935119. DOI: 10.1080/19768354.2021.1883734.

References

Valavanidis A, Vlachogianni T, Fiotakis K . Tobacco smoke: involvement of reactive oxygen species and stable free radicals in mechanisms of oxidative damage, carcinogenesis and synergistic effects with other respirable particles. Int J Environ Res Public Health. 2009; 6(2):445-62. PMC: 2672368. DOI: 10.3390/ijerph6020445. View

Srivastava S, Tong Y, Devadas K, Zou Z, Chen Y, Pirollo K . The status of the p53 gene in human papilloma virus positive or negative cervical carcinoma cell lines. Carcinogenesis. 1992; 13(7):1273-5. DOI: 10.1093/carcin/13.7.1273. View

Loft S, Poulsen H . Cancer risk and oxidative DNA damage in man. J Mol Med (Berl). 1996; 74(6):297-312. DOI: 10.1007/BF00207507. View

Butz K, Whitaker N, Denk C, Ullmann A, Geisen C, Hoppe-Seyler F . Induction of the p53-target gene GADD45 in HPV-positive cancer cells. Oncogene. 1999; 18(14):2381-6. DOI: 10.1038/sj.onc.1202557. View

Chakravarti D, Mailander P, Cavalieri E, Rogan E . Evidence that error-prone DNA repair converts dibenzo[a,l]pyrene-induced depurinating lesions into mutations: formation, clonal proliferation and regression of initiated cells carrying H-ras oncogene mutations in early preneoplasia. Mutat Res. 2000; 456(1-2):17-32. DOI: 10.1016/s0027-5107(00)00102-0. View

Shackelford R, Kaufmann W, Paules R . Oxidative stress and cell cycle checkpoint function. Free Radic Biol Med. 2000; 28(9):1387-404. DOI: 10.1016/s0891-5849(00)00224-0. View

Butz K, Shahabeddin L, Geisen C, Spitkovsky D, Ullmann A, Hoppe-Seyler F . Functional p53 protein in human papillomavirus-positive cancer cells. Oncogene. 1995; 10(5):927-36. View

Zhou J, Ahn J, Wilson S, Prives C . A role for p53 in base excision repair. EMBO J. 2001; 20(4):914-23. PMC: 145418. DOI: 10.1093/emboj/20.4.914. View

Wilmer M, de Graaf-Hess A, Blom H, Dijkman H, Monnens L, Van den Heuvel L . Elevated oxidized glutathione in cystinotic proximal tubular epithelial cells. Biochem Biophys Res Commun. 2005; 337(2):610-4. DOI: 10.1016/j.bbrc.2005.09.094. View

10.

Yang Q, Hergenhahn M, Weninger A, Bartsch H . Cigarette smoke induces direct DNA damage in the human B-lymphoid cell line Raji. Carcinogenesis. 1999; 20(9):1769-75. DOI: 10.1093/carcin/20.9.1769. View

11.

Hietanen S, Lain S, Krausz E, Blattner C, Lane D . Activation of p53 in cervical carcinoma cells by small molecules. Proc Natl Acad Sci U S A. 2000; 97(15):8501-6. PMC: 26977. DOI: 10.1073/pnas.97.15.8501. View

12.

Winkelstein Jr W . Smoking and cancer of the uterine cervix: hypothesis. Am J Epidemiol. 1977; 106(4):257-9. DOI: 10.1093/oxfordjournals.aje.a112460. View

13.

Wei L, Gravitt P, Song H, Maldonado A, Ozbun M . Nitric oxide induces early viral transcription coincident with increased DNA damage and mutation rates in human papillomavirus-infected cells. Cancer Res. 2009; 69(11):4878-84. PMC: 3820841. DOI: 10.1158/0008-5472.CAN-08-4695. View

14.

Vousden K, Lu X . Live or let die: the cell's response to p53. Nat Rev Cancer. 2002; 2(8):594-604. DOI: 10.1038/nrc864. View

15.

Prost S, Bellamy C, Clarke A, Wyllie A, Harrison D . p53-independent DNA repair and cell cycle arrest in embryonic stem cells. FEBS Lett. 1998; 425(3):499-504. DOI: 10.1016/s0014-5793(98)00296-8. View

16.

Mena S, Ortega A, Estrela J . Oxidative stress in environmental-induced carcinogenesis. Mutat Res. 2008; 674(1-2):36-44. DOI: 10.1016/j.mrgentox.2008.09.017. View

17.

Pryor W, Prier D, Church D . Electron-spin resonance study of mainstream and sidestream cigarette smoke: nature of the free radicals in gas-phase smoke and in cigarette tar. Environ Health Perspect. 1983; 47:345-55. PMC: 1569403. DOI: 10.1289/ehp.8347345. View

18.

Haverkos H, Soon G, Steckley S, Pickworth W . Cigarette smoking and cervical cancer: Part I: a meta-analysis. Biomed Pharmacother. 2003; 57(2):67-77. DOI: 10.1016/s0753-3322(03)00196-3. View

19.

Fichorova R, Rheinwald J, Anderson D . Generation of papillomavirus-immortalized cell lines from normal human ectocervical, endocervical, and vaginal epithelium that maintain expression of tissue-specific differentiation proteins. Biol Reprod. 1997; 57(4):847-55. DOI: 10.1095/biolreprod57.4.847. View

20.

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