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Journal of Cancer Research and Clinical Oncology

, Volume 142, Issue 9, pp 1917–1926 | Cite as

Association between polymorphisms in genes related to DNA base-excision repair with risk and prognosis of oropharyngeal squamous cell carcinoma

  • Ericka Francislaine Dias Costa
  • Erika Stocco Santos
  • Vitor Teixeira Liutti
  • Frederico Leal
  • Vivian Castro Antunes Santos
  • José Augusto Rinck-Junior
  • Fernanda Viviane Mariano
  • Cláudia Malheiros Coutinho-Camillo
  • Albina Altemani
  • Carmen Silvia Passos Lima
  • Gustavo Jacob LourençoEmail author
Original Article – Cancer Research

Abstract

Purpose

We examined the influence of OGG1 c.977C>G (rs1052133), APEX1 c.444T>G (rs1130409), XRCC1 c.-77T>C (rs3213245), c.580C>T (rs1799782), c.839G>A (rs25489) and c.1196G>A (rs25487) single-nucleotide polymorphisms (SNPs), involved in base-excision repair (BER) pathway, on oropharyngeal squamous cell carcinoma (OPSCC) risk and prognosis.

Methods

Aiming to identify the genotypes, DNA from 200 consecutive OPSCC patients and 200 controls was analyzed by PCR-RFLP. The prognostic impact of genotypes of SNPs on progression-free survival (PFS) and overall survival of OPSCC patients was examined using the Kaplan–Meier estimates and Cox regression analyses.

Results

XRCC1 c.580CT or TT genotypes (19.5 vs. 11.0 %, P = 0.04) and XRCC1 TTGG haplotype from c.-77T>C, c.580C>T, c.839G>A and c.1196G>A SNPs (17.5 vs. 10.0 %, P = 0.04) were more common in patients with OPSCC than in controls. Carriers of combined genotypes of c.580C>T and TTGG haplotype of XRCC1 gene were under 3.35- and 3.22-fold increased risk of OPSCC than others. For survival analysis, we selected only patients with tumor at stage IV. The median follow-up time was 24.5 months. At 24 months of follow-up, PFS was shorter in patients with OGG1 c.977CC genotype when compared with others genotypes (35.5 vs. 52.1 %, log-rank test, P = 0.03). After multivariate Cox analysis, patients with OGG1 c.977CC genotype had more chance to present tumor progression when compared with others (HR 1.68, P = 0.02).

Conclusions

Our data present, for the first time, evidence that inherited OGG1 c.977C>G; XRCC1 c.-77T>C, c.580C>T, c.839G>A and c.1196G>A abnormalities of DNA BER pathway are important determinants of OPSCC and predictors of patient outcomes.

Keywords

Oropharyngeal squamous cell carcinoma Base-excision repair pathway Polymorphisms Risk Prognosis 

Notes

Financial support

São Paulo Research Foundation (FAPESP) (Grant #2012/18623-1) funded this study.

Compliance with ethical standards

Conflict of interest

The authors declare that they have no conflicts of interest.

Ethical standard

The study was approved according to the institutional review board guidelines (Number 446/2005) and according to the Declaration of Helsinki, where all subjects provided written informed consent.

References

  1. Abdel-Rahman SZ, El-Zein RA (2000) The 399Gln polymorphism in the DNA repair gene XRCC1 modulates the genotoxic response induced in human lymphocytes by the tobacco-specific nitrosamine NNK. Cancer Lett 159(1):63–71CrossRefPubMedGoogle Scholar
  2. Al-Hadyan KS, Al-Harbi NM, Al-Qahtani SS, Alsbeih GA (2012) Involvement of single-nucleotide polymorphisms in predisposition to head and neck cancer in Saudi Arabia. Genet Test Mol Biomarkers 16(2):95–101CrossRefPubMedPubMedCentralGoogle Scholar
  3. Applebaum KM, McClean MD, Nelson HH, Marsit CJ, Christensen BC, Kelsey KT (2009) Smoking modifies the relationship between XRCC1 haplotypes and HPV16-negative head and neck squamous cell carcinoma. Int J Cancer 124(11):2690–2696CrossRefPubMedPubMedCentralGoogle Scholar
  4. Barrett JC, Fry B, Maller J, Daly MJ (2005) Haploview: analysis and visualization of LD and haplotype maps. Bioinformatics 21(2):263–265CrossRefPubMedGoogle Scholar
  5. Begum S, Gillison ML, Ansari-Lari MA, Shah K, Westra WH (2003) Detection of human papillomavirus in cervical lymph nodes: a highly effective strategy for localizing site of tumor origin. Clin Cancer Res 9(17):6469–6475PubMedGoogle Scholar
  6. Bravard A, Vacher M, Moritz E, Vaslin L, Hall J, Epe B et al (2009) Oxidation status of human OGG1-S326C polymorphic variant determines cellular DNA repair capacity. Cancer Res 69(8):3642–3649CrossRefPubMedGoogle Scholar
  7. Cardesa A, Gale N, Nadal A, Zidar N (2005) Squamous cell carcinoma. In: Barnes L, Eveson JW, Reichart P, Sidransky D (eds) World Health Organization classification of tumours, pathology & genetics, head and neck tumours, 2nd edn. IARC Press, Lyon, pp 118–121Google Scholar
  8. Carvalho-Silva DR, Santos FR, Rocha J, Pena SD (2001) The phylogeography of Brazilian Y-chromosome lineages. Am J Hum Genet 68(1):281–286CrossRefPubMedGoogle Scholar
  9. Chaturvedi AK, Engels EA, Pfeiffer RM, Hernandez BY, Xiao W, Kim E et al (2011) Incidence trends for human papillomavirus-related and -unrelated oral squamous cell carcinomas in the united states. J Clin Oncol 26(32):4294–4301CrossRefGoogle Scholar
  10. Choudhury JH, Choudhury B, Kundu S, Ghosh SK (2014) Combined effect of tobacco and DNA repair genes polymorphisms of XRCC1 and XRCC2 influence high risk of head and neck squamous cell carcinoma in northeast Indian population. Med Oncol 31(8):67CrossRefPubMedGoogle Scholar
  11. Clump DA, Bauman JE, Ferris RL (2015) Cancer of the oropharynx. Surg Oncol Clin N Am 24(3):509–520CrossRefPubMedGoogle Scholar
  12. Csejtei A, Tibold A, Koltai K, Varga Z, Szanyi I, Gobel G et al (2009) Association between XRCC1 polymorphisms and head and neck cancer in a Hungarian population. Anticancer Res 29(10):4169–4173PubMedGoogle Scholar
  13. Demokan S, Demir D, Suoglu Y, Kiyak E, Akar U, Dalay N (2005) Polymorphisms of the XRCC1 DNA repair gene in head and neck cancer. Pathol Oncol Res 11(1):22–25CrossRefPubMedGoogle Scholar
  14. Edge SB, Byrd DR, Compton CC, Fritz AG, Greene FL, Trotti A (eds) (2010) American Joint Committee on Cancer: cancer staging manual, 7th edn. Springer, New York, pp 21–97Google Scholar
  15. Elahi A, Zheng Z, Park J, Eyring K, McCaffrey T, Lazarus P (2002) The human OGG1 DNA repair enzyme and its association with orolaryngeal cancer risk. Carcinogenesis 23(7):1229–1234CrossRefPubMedGoogle Scholar
  16. Flores-Obando RE, Gollin SM, Ragin CC (2010) Polymorphisms in DNA damage response genes and head and neck cancer risk. Biomarkers 15(5):379–399CrossRefPubMedPubMedCentralGoogle Scholar
  17. Garavello W, Foschi R, Talamini R, La Vecchia C, Rossi M, Dal Maso L et al (2008) Family history and the risk of oral and pharyngeal cancer. Int J Cancer 122(8):1827–1831CrossRefPubMedGoogle Scholar
  18. Görgens H, Müller A, Krüger S, Kuhlisch E, König IR, Ziegler A et al (2007) Analysis of the base excision repair genes MTH1, OGG1 and MUTYH in patients with squamous oral carcinomas. Oral Oncol 43(8):791–795CrossRefPubMedGoogle Scholar
  19. Gugatschka M, Dehchamani D, Wascher TC, Friedrich G, Renner W (2011) DNA repair gene ERCC2 polymorphisms and risk of squamous cell carcinoma of the head and neck. Exp Mol Pathol 91(1):331–334CrossRefPubMedGoogle Scholar
  20. Hadi MZ, Coleman MA, Fidelis K, Mohrenweiser HW, Wilson DM 3rd (2000) Functional characterization of Ape1 variants identified in the human population. Nucleic Acids Res 28(20):3871–3879CrossRefPubMedPubMedCentralGoogle Scholar
  21. Hall J, Hashibe M, Boffetta P, Gaborieau V, Moullan N, Chabrier A et al (2007) The association of sequence variants in DNA repair and cell cycle genes with cancers of the upper aerodigestive tract. Carcinogenesis 28(3):665–671CrossRefPubMedGoogle Scholar
  22. Hao B, Miao X, Li Y, Zhang X, Sun T, Liang G et al (2006) A novel T-77C polymorphism in DNA repair gene XRCC1 contributes to diminished promoter activity and increased risk of non-small cell lung cancer. Oncogene 25:3613–3620CrossRefPubMedGoogle Scholar
  23. Harth V, Schafer M, Abel J, Maintz L, Neuhaus T, Besuden M et al (2008) Head and neck squamous-cell cancer and its association with polymorphic enzymes of xenobiotic metabolism and repair. J Toxicol Environ Health 71(13–14):887–897CrossRefGoogle Scholar
  24. Hauck F, Oliveira-Silva M, Dreyer JH, Perrusi VJ, Arcuri RA, Hassan R et al (2015) Prevalence of HPV infection in head and neck carcinomas shows geographical variability: a comparative study from Brazil and Germany. Virchows Arch 466(6):685–693CrossRefPubMedGoogle Scholar
  25. Hayes RB, Bravo-Otero E, Kleinman DV, Brown LM, Fraumeni JF, Harty LC et al (1999) Tobacco and alcohol use and oral cancer in Puerto Rico. Cancer Causes Control 10:27–33CrossRefPubMedGoogle Scholar
  26. Huber MA, Tantiwongkosi B (2014) Oral and oropharyngeal cancer. Med Clin North Am 98(6):1299–12321CrossRefPubMedGoogle Scholar
  27. Hung RJ, Hall J, Brennan P, Boffetta P (2005) Genetic polymorphisms in the base excision repair pathway and cancer risk: a HuGE review. Am J Epidemiol 162(10):925–942CrossRefPubMedGoogle Scholar
  28. Khlifi R, Kallel I, Hammami B, Hamza-Chaffai A, Rebai A (2014) DNA repair gene polymorphisms and risk of head and neck cancer in the Tunisian population. J Oral Pathol Med 43(3):217–224CrossRefPubMedGoogle Scholar
  29. Kowalski M, Przybylowska K, Rusin P, Olszewski J, Morawiec-Sztandera A, Bielecka-Kowalska A et al (2009) Genetic polymorphisms in DNA base excision repair gene XRCC1 and the risk of squamous cell carcinoma of the head and neck. J Exp Clin Cancer Res 28(1):37CrossRefPubMedPubMedCentralGoogle Scholar
  30. Kumar A, Pant MC, Singh HS, Khandelwal S (2011) Role of OGG1 Ser326Cys polymorphism and 8-oxoguanine DNA damage in risk assessment of squamous cell carcinoma of head and neck in North Indian population. Mutat Res 726(2):227–233CrossRefPubMedGoogle Scholar
  31. Kumar A, Pant MC, Singh HS, Khandelwal S (2012) Associated risk of XRCC1 and XPD cross talk and life style factors in progression of head and neck cancer in north Indian population. Mutat Res 729(1–2):24–34CrossRefPubMedGoogle Scholar
  32. Li C, Hu Z, Lu J, Liu Z, Wang LE, El-Naggar AK et al (2007) Genetic polymorphisms in DNA base-excision repair genes ADPRT, XRCC1, and APE1 and the risk of squamous cell carcinoma of the head and neck. Cancer 110(4):867–875CrossRefPubMedGoogle Scholar
  33. Livak KJ, Schmittgen TD (2001) Analysis of relative gene expression data using real-time quantitative PCR and the 2(-Delta Delta C(T)) method. Methods 25(4):402–408CrossRefPubMedGoogle Scholar
  34. Lopes-Aguiar L, Costa EFD, Nogueira GAS, Lima TRP, Visacri MB, Pincinato EC et al (2016) XPD c.934G>A polymorphism of nucleotide excision repair pathway in outcome of head and neck squamous cell carcinoma patients treated with cisplatin chemoradiation. Oncotarget. doi: 10.18632/oncotarget.7668
  35. López RV, Levi JE, Eluf-Neto J, Koifman RJ, Koifman S, Curado MP et al (2014) Human papillomavirus (HPV) 16 and the prognosis of head and neck cancer in a geographical region with a low prevalence of HPV infection. Cancer Causes Control 25(4):461–471CrossRefPubMedGoogle Scholar
  36. Matullo G, Dunning AM, Guarrera S, Baynes C, Polidoro S, Garte S et al (2006) DNA repair polymorphisms and cancer risk in non-smokers in a cohort study. Carcinogenesis 27(5):997–1007CrossRefPubMedGoogle Scholar
  37. Mitra AK, Singh SV, Garg VK, Sharma M, Chaturvedi R, Rath SK (2011) Protective association exhibited by the single nucleotide polymorphism (SNP) rs1052133 in the gene human 8-oxoguanine DNA glycosylase (hOGG1) with the risk of squamous cell carcinomas of the head & neck (SCCHN) among north Indians. Indian J Med Res 133:605–612PubMedPubMedCentralGoogle Scholar
  38. Nogueira GA, Lourenço GJ, Oliveira CBM, Marson FA, Lopes-Aguiar L, Costa EFD et al (2015) Association between genetic polymorphisms in DNA mismatch repair-related genes with risk and prognosis of head and neck squamous cell carcinoma. Int J Cancer 137(4):810–818CrossRefPubMedGoogle Scholar
  39. O’Connell D, Seikaly H, Murphy R, Fung C, Cooper T, Knox A et al (2013) Primary surgery versus chemoradiotherapy for advanced oropharyngeal cancers: a longitudinal population study. J Otolaryngol Head Neck Surg 42(1):31CrossRefPubMedPubMedCentralGoogle Scholar
  40. Olshan AF, Watson MA, Weissler MC, Bell DA (2002) XRCC1 Polymorphism and head and neck cancer. Cancer Lett 178(2):181–186CrossRefPubMedGoogle Scholar
  41. Rischin D (2010) Oropharyngeal cancer, human papilloma virus, and clinical trials. J Clin Oncol 28(1):1–3CrossRefPubMedGoogle Scholar
  42. Robertson AB, Klungland A, Rognes T, Leiros I (2009) DNA repair in mammalian cells: base excision repair: the long and short of it. Cell Mol Life Sci 66(6):981–983CrossRefPubMedGoogle Scholar
  43. Singhi AD, Westra WH (2010) Comparison of human papillomavirus in situ hybridization and p16 immunohistochemistry in the detection of human papillomavirus-associated head and neck cancer based on a prospective clinical experience. Cancer 116(9):2166–2173PubMedGoogle Scholar
  44. Sturgis EM, Castillo EJ, Li L, Zheng R, Eicher SA, Clayman GL et al (1999) Polymorphisms of DNA repair gene XRCC1 in squamous cell carcinoma of the head and neck. Carcinogenesis 20(11):2125–2129CrossRefPubMedGoogle Scholar
  45. Tae K, Lee HS, Park BJ, Park CW, Kim KR, Cho HY et al (2004) Association of DNA repair gene XRCC1 polymorphisms with head and neck cancer in Korean population. Int J Cancer 111(5):805–808CrossRefPubMedGoogle Scholar
  46. Tuimala J, Szekely G, Wikman H, Järventaus H, Hirvonen A, Gundy S et al (2004) Genetic polymorphisms of DNA repair and xenobiotic-metabolizing enzymes: effects on levels of sister chromatid exchanges and chromosomal aberrations. Mutat Res 554(1–2):319–333CrossRefPubMedGoogle Scholar
  47. Yuan H, Li H, Ma H, Niu Y, Wu Y, Zhang S et al (2012) Genetic polymorphisms in key DNA repair genes and risk of head and neck cancer in a Chinese population. Exp Ther Med 3(4):719–724PubMedPubMedCentralGoogle Scholar
  48. Zhang Z, Shi Q, Wang LE, Sturgis EM, Spitz MR, El-Naggar AK et al (2004) No association between hOGG1 Ser326Cys polymorphism and risk of squamous cell carcinoma of the head and neck. Cancer Epidemiol Biomarkers Prev 13(6):1081–1083PubMedGoogle Scholar
  49. Ziech D, Franco R, Pappa A, Panayiotidis MI (2011) Reactive oxygen species (ROS)—induced genetic and epigenetic alterations in human carcinogenesis. Mutat Res 711(1–2):167–173CrossRefPubMedGoogle Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 2016

Authors and Affiliations

  • Ericka Francislaine Dias Costa
    • 1
  • Erika Stocco Santos
    • 1
  • Vitor Teixeira Liutti
    • 1
  • Frederico Leal
    • 1
  • Vivian Castro Antunes Santos
    • 1
  • José Augusto Rinck-Junior
    • 1
  • Fernanda Viviane Mariano
    • 2
  • Cláudia Malheiros Coutinho-Camillo
    • 3
  • Albina Altemani
    • 2
  • Carmen Silvia Passos Lima
    • 1
  • Gustavo Jacob Lourenço
    • 1
    Email author
  1. 1.Laboratory of Cancer Genetics, Faculty of Medical SciencesUniversity of CampinasCampinasBrazil
  2. 2.Department of Pathology, Faculty of Medical SciencesUniversity of CampinasCampinasBrazil
  3. 3.Department of PathologyA. C. Camargo Cancer CenterSão PauloBrazil

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