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Polymorphisms in DNA repair genes, hair dye use, and the risk of non-Hodgkin lymphoma

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Abstract

Purpose

Genetic polymorphisms in DNA repair genes and hair dye use may both have a role in the development of non-Hodgkin lymphoma (NHL). We aimed to examine the interaction between variants in DNA repair genes and hair dye use with risk of NHL in a population-based case–control study of Connecticut women.

Methods

We examined 24 single nucleotide polymorphisms in 16 DNA repair genes among 518 NHL cases and 597 controls and evaluated the associations between hair dye use and risk of overall NHL and common NHL subtypes, stratified by genotype, using unconditional logistic regression.

Results

Women who used hair dye before 1980 had a significantly increased risk of NHL, particularly for the follicular lymphoma (FL) subtype, but not for diffuse large B-cell lymphoma. The following genotypes in combination with hair dye use before 1980 were associated with FL risk: BRCA2 rs144848 AC+CC [odds ratio (OR) (95 % confidence interval (CI)) 3.28(1.27–8.50)], WRN rs1346044 TT [OR(95 % CI) 2.70(1.30–5.65)], XRCC3 rs861539 CT+TT [OR(95 % CI) 2.76(1.32–5.77)], XRCC4 rs1805377 GG [OR(95 % CI) 2.07(1.10–3.90)] and rs1056503 TT [OR(95 % CI) 2.17(1.16–4.07)], ERCC1 rs3212961 CC [OR(95 % CI) 1.93(1.00–3.72)], RAD23B rs1805329 CC [OR(95 % CI) 2.28(1.12–4.64)], and MGMT rs12917 CC, rs2308321 AA, and rs2308327 AA genotypes [OR(95 % CI) 1.96(1.06–3.63), 2.02(1.09–3.75), and 2.23(1.16–4.29), respectively]. In addition, a significant interaction with risk of overall NHL was observed between WRN rs1346044 and hair dye use before 1980 (p interaction = 0.032).

Conclusions

Our results indicated that genetic variation in DNA repair genes modifies susceptibility to NHL in relation to hair dye use, particularly for the FL subtype and in women who began using hair dye before 1980. Further studies are needed to confirm these observations.

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Abbreviations

NHL:

Non-Hodgkin lymphoma

DLBCL:

Diffuse large B-cell lymphoma

FL:

Follicular lymphoma

MAF:

Minor allele frequency

CI:

Confidence interval

References

  1. Muller AM, Ihorst G, Mertelsmann R, Engelhardt M (2005) Epidemiology of non-Hodgkin’s lymphoma (NHL): trends, geographic distribution, and etiology. Ann Hematol 84(1):1–12. doi:10.1007/s00277-004-0939-7

    Article  PubMed  Google Scholar 

  2. Ekstrom-Smedby K (2006) Epidemiology and etiology of non-Hodgkin lymphoma—a review. Acta Oncol 45(3):258–271. doi:10.1080/02841860500531682

    Article  PubMed  Google Scholar 

  3. Bassig BA, Lan Q, Rothman N, Zhang Y, Zheng T (2012) Current understanding of lifestyle and environmental factors and risk of non-hodgkin lymphoma: an epidemiological update. J Cancer Epidemiol (978930. doi:10.1155/2012/978930

  4. de Sanjose S, Benavente Y, Nieters A, Foretova L, Maynadie M, Cocco PL, Staines A, Vornanen M, Boffetta P, Becker N, Alvaro T, Brennan P (2006) Association between personal use of hair dyes and lymphoid neoplasms in Europe. Am J Epidemiol 164(1):47–55. doi:10.1093/aje/kwj187

    Article  PubMed  Google Scholar 

  5. Takkouche B, Etminan M, Montes-Martinez A (2005) Personal use of hair dyes and risk of cancer: a meta-analysis. JAMA 293(20):2516–2525. doi:10.1001/jama.293.20.2516

    Article  CAS  PubMed  Google Scholar 

  6. Zhang Y, Sanjose SD, Bracci PM, Morton LM, Wang R, Brennan P, Hartge P, Boffetta P, Becker N, Maynadie M, Foretova L, Cocco P, Staines A, Holford T, Holly EA, Nieters A, Benavente Y, Bernstein L, Zahm SH, Zheng T (2008) Personal use of hair dye and the risk of certain subtypes of non-Hodgkin lymphoma. Am J Epidemiol 167(11):1321–1331. doi:10.1093/aje/kwn058

    Article  PubMed Central  PubMed  Google Scholar 

  7. Zhang Y, Holford TR, Leaderer B, Boyle P, Zahm SH, Flynn S, Tallini G, Owens PH, Zheng T (2004) Hair-coloring product use and risk of non-Hodgkin’s lymphoma: a population-based case–control study in Connecticut. Am J Epidemiol 159(2):148–154

    Article  PubMed  Google Scholar 

  8. Sangrajrang S, Renard H, Kuhaprema T, Pornsopone P, Arpornwirat W, Brennan P (2011) Personal use of hair dyes—increased risk of non-Hodgkin’s lymphoma in Thailand. Asian Pac J Cancer Prev 12(9):2393–2396

    PubMed  Google Scholar 

  9. Preston RJ, Skare JA, Aardema MJ (2010) A review of biomonitoring studies measuring genotoxicity in humans exposed to hair dyes. Mutagenesis 25(1):17–23. doi:10.1093/mutage/gep044

    Article  CAS  PubMed  Google Scholar 

  10. Huang YC, Hung WC, Kang WY, Chen WT, Chai CY (2007) p-Phenylenediamine induced DNA damage in SV-40 immortalized human uroepithelial cells and expression of mutant p53 and COX-2 proteins. Toxicol Lett 170(2):116–123. doi:10.1016/j.toxlet.2007.02.011

    Article  CAS  PubMed  Google Scholar 

  11. Ames BN, Kammen HO, Yamasaki E (1975) Hair dyes are mutagenic: identification of a variety of mutagenic ingredients. Proc Natl Acad Sci USA 72(6):2423–2427

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  12. Sontag JM (1981) Carcinogenicity of substituted-benzenediamines (phenylenediamines) in rats and mice. J Natl Cancer Inst 66(3):591–602

    CAS  PubMed  Google Scholar 

  13. Zhang Y, Hughes KJ, Zahm SH, Holford TR, Dai L, Bai Y, Han X, Qin Q, Lan Q, Rothman N, Zhu Y, Leaderer B, Zheng T (2009) Genetic variations in xenobiotic metabolic pathway genes, personal hair dye use, and risk of non-Hodgkin lymphoma. Am J Epidemiol 170(10):1222–1230. doi:10.1093/aje/kwp263

    Article  PubMed Central  PubMed  Google Scholar 

  14. Palitti F (2004) Mechanisms of formation of chromosomal aberrations: insights from studies with DNA repair-deficient cells. Cytogenet Genome Res 104(1–4):95–99. doi:10.1159/000077471

    Article  CAS  PubMed  Google Scholar 

  15. Shen M, Zheng T, Lan Q, Zhang Y, Zahm SH, Wang SS, Holford TR, Leaderer B, Yeager M, Welch R, Kang D, Boyle P, Zhang B, Zou K, Zhu Y, Chanock S, Rothman N (2006) Polymorphisms in DNA repair genes and risk of non-Hodgkin lymphoma among women in Connecticut. Hum Genet 119(6):659–668. doi:10.1007/s00439-006-0177-2

    Article  CAS  PubMed  Google Scholar 

  16. Barry KH, Zhang Y, Lan Q, Zahm SH, Holford TR, Leaderer B, Boyle P, Hosgood HD 3rd, Chanock S, Yeager M, Rothman N, Zheng T (2011) Genetic variation in metabolic genes, occupational solvent exposure, and risk of non-hodgkin lymphoma. Am J Epidemiol 173(4):404–413. doi:10.1093/aje/kwq360

    Article  PubMed Central  PubMed  Google Scholar 

  17. Jaffe ES, Stein H, Vardiman JW (2001) World Health Organization classification of tumors: pathology and genetics of tumors of haematopoietic and lymphoid tissues. IARC Press, Lyon

    Google Scholar 

  18. Garcia-Closas M, Egan KM, Abruzzo J, Newcomb PA, Titus-Ernstoff L, Franklin T, Bender PK, Beck JC, Le Marchand L, Lum A, Alavanja M, Hayes RB, Rutter J, Buetow K, Brinton LA, Rothman N (2001) Collection of genomic DNA from adults in epidemiological studies by buccal cytobrush and mouthwash. Cancer Epidemiol Biomarkers Prev 10(6):687–696

    CAS  PubMed  Google Scholar 

  19. Packer BR, Yeager M, Staats B, Welch R, Crenshaw A, Kiley M, Eckert A, Beerman M, Miller E, Bergen A, Rothman N, Strausberg R, Chanock SJ (2004) SNP500Cancer: a public resource for sequence validation and assay development for genetic variation in candidate genes. Nucleic Acids Res 32(Database issue):D528–D532. doi:10.1093/nar/gkh005

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  20. Benjamini Y, Hochberg Y (1995) Controlling the false discovery rate: a practical and powerful approach to multiple testing. J R Stat Soc B 57(1):289–300

    Google Scholar 

  21. Morton LM, Bernstein L, Wang SS, Hein DW, Rothman N, Colt JS, Davis S, Cerhan JR, Severson RK, Welch R, Hartge P, Zahm SH (2007) Hair dye use, genetic variation in N-acetyltransferase 1 (NAT1) and 2 (NAT2), and risk of non-Hodgkin lymphoma. Carcinogenesis 28(8):1759–1764. doi:10.1093/carcin/bgm121

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  22. Corbett JF (1999) An historical review of the use of dye precursors in the formulation of commercial oxidation hair dyes. Dyes Pigments 41(1–2):127–136

    Article  CAS  Google Scholar 

  23. Damerla RR, Knickelbein KE, Strutt S, Liu FJ, Wang H, Opresko PL (2012) Werner syndrome protein suppresses the formation of large deletions during the replication of human telomeric sequences. Cell Cycle 11(16):3036–3044. doi:10.4161/cc.21399

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  24. Maddukuri L, Ketkar A, Eddy S, Zafar MK, Griffin WC, Eoff RL (2012) Enhancement of human DNA polymerase eta activity and fidelity is dependent upon a bipartite interaction with the Werner syndrome protein. J Biol Chem 287(50):42312–42323. doi:10.1074/jbc.M112.410332

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  25. Sakamoto S, Nishikawa K, Heo SJ, Goto M, Furuichi Y, Shimamoto A (2001) Werner helicase relocates into nuclear foci in response to DNA damaging agents and co-localizes with RPA and Rad51. Genes Cells 6(5):421–430

    Article  CAS  PubMed  Google Scholar 

  26. Gee J, Ding Q, Keller JN (2002) Analysis of Werner’s expression within the brain and primary neuronal culture. Brain Res 940(1–2):44–48

    Article  CAS  PubMed  Google Scholar 

  27. Brenneman MA, Weiss AE, Nickoloff JA, Chen DJ (2000) XRCC3 is required for efficient repair of chromosome breaks by homologous recombination. Mutat Res 459(2):89–97

    Article  CAS  PubMed  Google Scholar 

  28. Mari PO, Florea BI, Persengiev SP, Verkaik NS, Bruggenwirth HT, Modesti M, Giglia-Mari G, Bezstarosti K, Demmers JA, Luider TM, Houtsmuller AB, van Gent DC (2006) Dynamic assembly of end-joining complexes requires interaction between Ku70/80 and XRCC4. Proc Natl Acad Sci USA 103(49):18597–18602. doi:10.1073/pnas.0609061103

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  29. He XF, Wei W, Li JL, Shen XL, Ding DP, Wang SL, Liu ZZ, Qin JB, Wu LX, Xie DL (2013) Association between the XRCC3 T241M polymorphism and risk of cancer: evidence from 157 case–control studies. Gene 523(1):10–19. doi:10.1016/j.gene.2013.03.071

    Article  CAS  PubMed  Google Scholar 

  30. Lee PH, Shatkay H (2008) F-SNP: computationally predicted functional SNPs for disease association studies. Nucleic Acids Res 36:D820–D824. doi:10.1093/nar/gkm904

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  31. Inoue R, Abe M, Nakabeppu Y, Sekiguchi M, Mori T, Suzuki T (2000) Characterization of human polymorphic DNA repair methyltransferase. Pharmacogenetics 10(1):59–66

    Article  CAS  PubMed  Google Scholar 

  32. Jiao J, Zheng T, Lan Q, Chen Y, Deng Q, Bi X, Kim C, Holford T, Leaderer B, Boyle P, Ba Y, Xia Z, Chanock SJ, Rothman N, Zhang Y (2012) Occupational solvent exposure, genetic variation of DNA repair genes, and the risk of non-Hodgkin’s lymphoma. Eur J Cancer Prev 21(6):580–584. doi:10.1097/CEJ.0b013e328351c762

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  33. Morton LM, Wang SS, Cozen W, Linet MS, Chatterjee N, Davis S, Severson RK, Colt JS, Vasef MA, Rothman N, Blair A, Bernstein L, Cross AJ, De Roos AJ, Engels EA, Hein DW, Hill DA, Kelemen LE, Lim U, Lynch CF, Schenk M, Wacholder S, Ward MH, Hoar Zahm S, Chanock SJ, Cerhan JR, Hartge P (2008) Etiologic heterogeneity among non-Hodgkin lymphoma subtypes. Blood 112(13):5150–5160. doi:10.1182/blood-2008-01-133587

    Article  CAS  PubMed Central  PubMed  Google Scholar 

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Acknowledgments

This work was partly supported by National Cancer Institute grant CA62006 (Connecticut Women’s NHL Study, Yale University) and by Fogarty training grants D43TW 008323 and D43TW 007864-01 from the National Institutes of Health (T. Zheng). Certain data used in this study were obtained from the Connecticut Tumor Registry located in the Connecticut Department of Public Health. The author(s) assume(s) full responsibility for analyses and interpretation of these data. The cooperation of 28 Connecticut hospitals, including Charlotte Hungerford Hospital, Bridgeport Hospital, Danbury Hospital, Hartford Hospital, Middlesex Hospital, New Britain General Hospital, Bradley Memorial Hospital, Yale/New Haven Hospital, St. Francis Hospital and Medical Center, St. Mary’s Hospital, Hospital of St. Raphael, St. Vincent’s Medical Center, Stamford Hospital, William W. Backus Hospital, Windham Hospital, Eastern Connecticut Health Network, Griffin Hospital, Bristol Hospital, Johnson Memorial Hospital, Day Kimball Hospital, Greenwich Hospital, Lawrence and Memorial Hospital, Milford Hospital, New Milford Hospital, Norwalk Hospital, MidState Medical Center, John Dempsey Hospital, and Waterbury Hospital, in allowing patient access, is gratefully acknowledged.

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The authors declared no potential competing financial interests.

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Correspondence to Tongzhang Zheng.

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Guo, H., Bassig, B.A., Lan, Q. et al. Polymorphisms in DNA repair genes, hair dye use, and the risk of non-Hodgkin lymphoma. Cancer Causes Control 25, 1261–1270 (2014). https://doi.org/10.1007/s10552-014-0423-1

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  • DOI: https://doi.org/10.1007/s10552-014-0423-1

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