Tumor Biology

, Volume 36, Issue 6, pp 4545–4554 | Cite as

The Arg399Gln polymorphism in the XRCC1 gene is associated with increased risk of hematological malignancies

  • Liang Du
  • Yuqi Liu
  • Pei Xue
  • Chenxi Song
  • Jiani Shen
  • Qing He
  • Yuanling Peng
  • Xiang Tong
  • Lizhi Tang
  • Yonggang Zhang
Research Article

Abstract

The associations between the Arg399Gln polymorphism in X-ray repair cross-complementing gene 1 (XRCC1) gene and the risk of hematological malignancies have been extensively investigated. However, the results were inconsistent. The objective of the current study is to investigate the association by meta-analysis. We searched PubMed database, Embase database, CNKI database, Wanfang database, and Weipu database, covering all studies until August 7, 2013. Statistical analysis was performed by using the Revman4.2 software and the Stata10.0 software. A total of 27 case–control studies concerning the Arg399Gln polymorphism were included from 26 articles. The results suggested that the Arg399Gln polymorphism was not associated with an increased/decreased risk of hematological malignancies in total analysis (OR = 1.15, 95 % confidence interval (CI) = 0.97–1.35, P = 0.10 for Arg/Gln + Gln/Gln vs. Arg/Arg). In the subgroup analysis by ethnicity and cancer types, significant association was found in Asians (OR = 1.35, 95 % CI = 1.04–1.75, P = 0.03) but not in Europeans (OR = 1.07, 95 % CI = 0.86–1.33, P = 0.56), and in leukemia (OR = 1.25, 95 % CI = 1.02–1.54, P = 0.03) but not in lymphoma (OR = 0.98, 95 % CI = 0.80–1.20, P = 0.84) or myeloma (OR = 1.13, 95 % CI = 0.23–5.69, P = 0.88). The current meta-analysis indicated that the Arg399Gln polymorphism in the XRCC1 gene might be a risk factor for hematological malignancies in Asians or for leukemia. In future, more large-scale case–control studies are needed to validate these results.

Keywords

XRCC1 Polymorphism Meta-analysis Hematological malignancies 

Notes

Conflicts of interest

None

References

  1. 1.
    Wandt H, Schaefer-Eckart K, Wendelin K, Pilz B, Wilhelm M, Thalheimer M, Mahlknecht U, Ho A, Schaich M, Kramer M, Kaufmann M, Leimer L, Schwerdtfeger R, Conradi R, Dolken G, Klenner A, Hanel M, Herbst R, Junghanss C, Ehninger G, Study Alliance L. Therapeutic platelet transfusion versus routine prophylactic transfusion in patients with haematological malignancies: an open-label, multicentre, randomised study. Lancet. 2012;380(9850):1309–16. doi: 10.1016/S0140-6736(12)60689-8.CrossRefGoogle Scholar
  2. 2.
    Sorror ML, Sandmaier BM, Storer BE, Franke GN, Laport GG, Chauncey TR, et al. Long-term outcomes among older patients following nonmyeloablative conditioning and allogeneic hematopoietic cell transplantation for advanced hematologic malignancies. JAMA : the journal of the American Medical Association. 2011;306(17):1874–83. doi: 10.1001/jama.2011.1558.CrossRefPubMedGoogle Scholar
  3. 3.
    Wang L, Yin F, Xu X, Hu X, Zhao D. X-ray repair cross-complementing group 1 (XRCC1) genetic polymorphisms and risk of childhood acute lymphoblastic leukemia: a meta-analysis. PloS one. 2012;7(4):e34897. doi: 10.1371/journal.pone.0034897.CrossRefPubMedPubMedCentralGoogle Scholar
  4. 4.
    Stanworth SJ, Estcourt LJ, Powter G, Kahan BC, Dyer C, Choo L, et al. A no-prophylaxis platelet-transfusion strategy for hematologic cancers. N Engl J Med. 2013;368(19):1771–80. doi: 10.1056/NEJMoa1212772.CrossRefPubMedGoogle Scholar
  5. 5.
    Siegel R, Ward E, Brawley O, Jemal A. Cancer statistics, 2011: the impact of eliminating socioeconomic and racial disparities on premature cancer deaths. CA: a cancer journal for clinicians. 2011;61(4):212–36. doi: 10.3322/caac.20121.Google Scholar
  6. 6.
    Abramenko I, Bilous N, Chumak A, Kostin A, Martina Z, Dyagil I. DNA repair polymorphisms in B-cell chronic lymphocytic leukemia in sufferers of Chernobyl nuclear power plant accident. J Radiat Res. 2012;53(3):497–503.CrossRefPubMedGoogle Scholar
  7. 7.
    Banescu C, Duicu C, Trifa AP, Dobreanu M. XRCC1 Arg194Trp and Arg399Gln polymorphisms are significantly associated with shorter survival in acute myeloid leukemia. Leuk Lymphoma. 2013. doi: 10.3109/10428194.2013.802781.PubMedGoogle Scholar
  8. 8.
    Baris S, Celkan T, Batar B, Guven M, Ozdil M, Ozkan A, et al. Association between genetic polymorphism in DNA repair genes and risk of B-cell lymphoma. Pediatr Hematol Oncol. 2009;26(6):467–72. doi: 10.3109/08880010903096201.CrossRefPubMedGoogle Scholar
  9. 9.
    Zhuo W, Zhang L, Zhu B, Qiu Z, Chen Z. Association between CYP1A1 Ile462Val variation and acute leukemia risk: meta-analyses including 2164 cases and 4160 controls. PloS one. 2012;7(10):e46974. doi: 10.1371/journal.pone.0046974.CrossRefPubMedPubMedCentralGoogle Scholar
  10. 10.
    Schuetz JM, Daley D, Graham J, Berry BR, Gallagher RP, Connors JM, et al. Genetic variation in cell death genes and risk of non-Hodgkin lymphoma. PloS one. 2012;7(2):e31560. doi: 10.1371/journal.pone.0031560.CrossRefPubMedPubMedCentralGoogle Scholar
  11. 11.
    Batar B, Guven M, Baris S, Celkan T, Yildiz I. DNA repair gene XPD and XRCC1 polymorphisms and the risk of childhood acute lymphoblastic leukemia. Leuk Res. 2009;33(6):759–63. doi: 10.1016/j.leukres.2008.11.005.CrossRefPubMedGoogle Scholar
  12. 12.
    Canalle R, Silveira VS, Scrideli CA, Queiroz RG, Lopes LF, Tone LG. Impact of thymidylate synthase promoter and DNA repair gene polymorphisms on susceptibility to childhood acute lymphoblastic leukemia. Leuk Lymphoma. 2011;52(6):1118–26. doi: 10.3109/10428194.2011.559672.CrossRefPubMedGoogle Scholar
  13. 13.
    Smith AG, Fan W, Regen L, Warnock S, Sprague M, Williams R, et al. Somatic mutations in the HLA genes of patients with hematological malignancy. Tissue antigens. 2012;79(5):359–66. doi: 10.1111/j.1399-0039.2012.01868.x.CrossRefPubMedGoogle Scholar
  14. 14.
    Ozdemir N, Celkan T, Baris S, Batar B, Guven M. DNA repair gene XPD and XRCC1 polymorphisms and the risk of febrile neutropenia and mucositis in children with leukemia and lymphoma. Leuk Res. 2012;36(5):565–9. doi: 10.1016/j.leukres.2011.10.012.CrossRefPubMedGoogle Scholar
  15. 15.
    Weng Y, Lu L, Yuan G, Guo J, Zhang Z, Xie X, et al. p53 codon 72 polymorphism and hematological cancer risk: an update meta-analysis. PloS one. 2012;7(9):e45820. doi: 10.1371/journal.pone.0045820.CrossRefPubMedPubMedCentralGoogle Scholar
  16. 16.
    Matullo G, Dunning AM, Guarrera S, Baynes C, Polidoro S, Garte S, et al. DNA repair polymorphisms and cancer risk in non-smokers in a cohort study. Carcinogenesis. 2006;27(5):997–1007. doi: 10.1093/carcin/bgi280.CrossRefPubMedGoogle Scholar
  17. 17.
    Meza-Espinoza JP, Peralta-Leal V, Gutierrez-Angulo M, Macias-Gomez N, Ayala-Madrigal ML, Barros-Nunez P, et al. XRCC1 polymorphisms and haplotypes in Mexican patients with acute lymphoblastic leukemia. Genetics and molecular research : GMR. 2009;8(4):1451–8. doi: 10.4238/vol8-4gmr687.CrossRefPubMedGoogle Scholar
  18. 18.
    Monroy CM, Cortes AC, Lopez M, Rourke E, Etzel CJ, Younes A, et al. Hodgkin lymphoma risk: role of genetic polymorphisms and gene-gene interactions in DNA repair pathways. Mol Carcinog. 2011;50(11):825–34. doi: 10.1002/mc.20747.CrossRefPubMedPubMedCentralGoogle Scholar
  19. 19.
    Smedby KE, Lindgren CM, Hjalgrim H, Humphreys K, Schollkopf C, Chang ET, et al. Variation in DNA repair genes ERCC2, XRCC1, and XRCC3 and risk of follicular lymphoma. Cancer epidemiology, biomarkers & prevention : a publication of the American Association for Cancer Research, cosponsored by the American Society of Preventive Oncology. 2006;15(2):258–65. doi: 10.1158/1055-9965.EPI-05-0583.CrossRefGoogle Scholar
  20. 20.
    Stanczyk M, Sliwinski T, Cuchra M, Zubowska M, Bielecka-Kowalska A, Kowalski M, et al. The association of polymorphisms in DNA base excision repair genes XRCC1, OGG1 and MUTYH with the risk of childhood acute lymphoblastic leukemia. Mol Biol Rep. 2011;38(1):445–51. doi: 10.1007/s11033-010-0127-x.CrossRefPubMedGoogle Scholar
  21. 21.
    Seedhouse C, Bainton R, Lewis M, Harding A, Russell N, Das-Gupta E. The genotype distribution of the XRCC1 gene indicates a role for base excision repair in the development of therapy-related acute myeloblastic leukemia. Blood. 2002;100(10):3761–6. doi: 10.1182/blood-2002-04-1152.CrossRefPubMedGoogle Scholar
  22. 22.
    Tumer TB, Yilmaz D, Tanrikut C, Sahin G, Ulusoy G, Arinc E. DNA repair XRCC1 Arg399Gln polymorphism alone, and in combination with CYP2E1 polymorphisms significantly contribute to the risk of development of childhood acute lymphoblastic leukemia. Leuk Res. 2010;34(10):1275–81. doi: 10.1016/j.leukres.2010.02.035.CrossRefPubMedGoogle Scholar
  23. 23.
    Matsuo K, Hamajima N, Suzuki R, Andoh M, Nakamura S, Seto M, et al. Lack of association between DNA base excision repair gene XRCC1 Gln399Arg polymorphism and risk of malignant lymphoma in Japan. Cancer Genet Cytogenet. 2004;149(1):77–80.CrossRefPubMedGoogle Scholar
  24. 24.
    Xia MJ, Shan J, Li YP, Zhou YN, Guo YJ, Sun GX, et al. Adoptive transfusion of tolerogenic dendritic cells prolongs the survival of liver allograft: a systematic review. J Evid Based Med. 2014;7(2):135–46.Google Scholar
  25. 25.
    Zhang L, Chen LM, Wang MN, Chen XJ, Li N, De HY, et al. The G894t, T-786c and 4b/a polymorphisms in Enos gene and cancer risk: a meta-analysis. J Evid Based Med. 2014;7(4):263–9.Google Scholar
  26. 26.
    Zhang YG, Li XB, Zhang J, Huang J, He C, Tian C, et al. The I/D polymorphism of angiotensin-converting enzyme gene and asthma risk: a meta-analysis. Allergy. 2011;66(2):197–205. doi: 10.1111/j.1398-9995.2010.02438.x.CrossRefPubMedGoogle Scholar
  27. 27.
    Deligezer U, Akisik EE, Dalay N. Lack of association of XRCC1 codon 399Gln polymorphism with chronic myelogenous leukemia. Anticancer Res. 2007;27(4B):2453–6.PubMedGoogle Scholar
  28. 28.
    Duman N, Aktan M, Ozturk S, Palanduz S, Cakiris A, Ustek D, et al. Investigation of Arg399Gln and Arg194Trp polymorphisms of the XRCC1 (X-ray cross-complementing group 1) gene and its correlation to sister chromatid exchange frequency in patients with chronic lymphocytic leukemia. Genetic testing and molecular biomarkers. 2012;16(4):287–91. doi: 10.1089/gtmb.2011.0152.CrossRefPubMedGoogle Scholar
  29. 29.
    Ganster C, Neesen J, Zehetmayer S, Jager U, Esterbauer H, Mannhalter C, et al. DNA repair polymorphisms associated with cytogenetic subgroups in B-cell chronic lymphocytic leukemia. Gene Chromosome Cancer. 2009;48(9):760–7. doi: 10.1002/gcc.20680.CrossRefGoogle Scholar
  30. 30.
    Joseph T, Kusumakumary P, Chacko P, Abraham A, Pillai MR. DNA repair gene XRCC1 polymorphisms in childhood acute lymphoblastic leukemia. Cancer Lett. 2005;217(1):17–24. doi: 10.1016/j.canlet.2004.06.055.CrossRefPubMedGoogle Scholar
  31. 31.
    Kim IS, Kim DC, Kim HG, Eom HS, Kong SY, Shin HJ, et al. DNA repair gene XRCC1 polymorphisms and haplotypes in diffuse large B-cell lymphoma in a Korean population. Cancer Genet Cytogenet. 2010;196(1):31–7. doi: 10.1016/j.cancergencyto.2009.08.008.CrossRefPubMedGoogle Scholar
  32. 32.
    Li J (2011) Association of XRCC1 polymorphis with leukemia susceptibility in northwest Chinese population.Google Scholar
  33. 33.
    Liu J, Song B, Wang Z, Song X, Shi Y, Zheng J, et al. DNA repair gene XRCC1 polymorphisms and non-Hodgkin lymphoma risk in a Chinese population. Cancer Genet Cytogenet. 2009;191(2):67–72. doi: 10.1016/j.cancergencyto.2009.01.015.CrossRefPubMedGoogle Scholar
  34. 34.
    Özcan A, Pehlivan M, Tomatir AG, Karaca E, Oezkinay C, Özdemir F, et al. Polymorphisms of the DNA repair gene XPD (751) and XRCC 1(399) correlates with risk of hematological malignancies in Turkish population. Afr J Biotechnol. 2011;10(44):8860–70.CrossRefGoogle Scholar
  35. 35.
    Pakakasama S, Sirirat T, Kanchanachumpol S, Udomsubpayakul U, Mahasirimongkol S, Kitpoka P, et al. Genetic polymorphisms and haplotypes of DNA repair genes in childhood acute lymphoblastic leukemia. Pediatr Blood Cancer. 2007;48(1):16–20. doi: 10.1002/pbc.20742.CrossRefPubMedGoogle Scholar
  36. 36.
    Scott K, Adamson PJ, Willett EV, Worrillow LJ, Allan JM. Genetic variation in genes expressed in the germinal center and risk of B cell lymphoma among Caucasians. Haematologica. 2008;93(10):1597–600. doi: 10.3324/haematol.13159.CrossRefPubMedGoogle Scholar
  37. 37.
    Shi JY, Ren ZH, Jiao B, Xiao R, Yun HY, Chen B, et al. Genetic variations of DNA repair genes and their prognostic significance in patients with acute myeloid leukemia. International journal of cancer Journal international du cancer. 2011;128(1):233–8. doi: 10.1002/ijc.25318.CrossRefPubMedGoogle Scholar
  38. 38.
    Zhang J (2003) Relationship between environmental risk factors, genetic polymorphisms and adult acult leukemia.Google Scholar
  39. 39.
    Zhu R, Wu Y, Lu FJ, Wang AH, Tang JY, Zhao JC, et al. Polymorphisms and haplotypes of XRCC1 and APE1 and risk of childhood leukaemia in China: a case–control analysis. Eur J Oncol. 2008;13(3):187–92.Google Scholar
  40. 40.
    Zhang Y, Zhang J, Zeng L, Huang H, Yang M, Fu X, et al. The -2518A/G polymorphism in the MCP-1 gene and tuberculosis risk: a meta-analysis. PloS one. 2012;7(7):e38918. doi: 10.1371/journal.pone.0038918.CrossRefPubMedPubMedCentralGoogle Scholar
  41. 41.
    Zeng X, Zhang Y, Kwong JSW, Zhang C, Li S, Sun F, et al. The methodological quality assessment tools for pre-clinical and clinical studies, systematic review and meta-analysis, and clinical practice guideline: a systematic review. J Evid Based Med. 2015. doi: 10.1111/jebm.12141.

Copyright information

© International Society of Oncology and BioMarkers (ISOBM) 2015

Authors and Affiliations

  • Liang Du
    • 1
  • Yuqi Liu
    • 2
  • Pei Xue
    • 2
  • Chenxi Song
    • 2
  • Jiani Shen
    • 2
  • Qing He
    • 2
  • Yuanling Peng
    • 2
  • Xiang Tong
    • 2
  • Lizhi Tang
    • 2
  • Yonggang Zhang
    • 1
  1. 1.The Periodical Press of West China HospitalSichuan UniversityChengduChina
  2. 2.West China Medical School/West China HospitalSichuan UniversityChengduChina

Personalised recommendations