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Medical Science Monitor: International Medical Journal of Experimental and Clinical Research logoLink to Medical Science Monitor: International Medical Journal of Experimental and Clinical Research
. 2018 Oct 3;24:7015–7022. doi: 10.12659/MSM.908813

Association of ERCC2 Gene Polymorphisms with Susceptibility to Diffuse Large B-Cell Lymphoma

Yong Tong 1,A,B,C,D,E,F,G, Yinzhou Xiang 2,C,D,E, Bao Li 3,A,B,C,D,E,F,G, Shijie Bao 1,A,B,C,D,E,F,G, Ying Zhou 1,A,B,C,D,E,F,G, Wen Yuan 1,D,E,F, Yu Ling 1,A,B,C,D,E,F, Dan Hao 1,A,B,D,E,F,G, Huamin Zhu 1,A,B,C,D,E,F, Zhiqiang Sun 1,A,B,C,D,
PMCID: PMC6179170  PMID: 30279407

Abstract

Background

The objective of this study was to detect the association between ERCC excision repair 2, TFIIH core complex helicase subunit (ERCC2) gene polymorphisms and diffuse large B-cell lymphoma (DLBCL) susceptibility.

Material/Methods

This study used a case-control design. ERCC2 gene rs1799793 (Asp312Asn) and rs13181 (Lys751Gln) polymorphisms were genotyped by polymerase chain reaction-restriction fragment length polymorphism (PCR-RFLP) both in DLBCL patients and healthy controls. The association between ERCC2 gene polymorphisms and DLBCL risk was assessed by χ2 test. Odds ratios (ORs) with corresponding 95% confidence intervals (95% CIs) were used to address the association strength. Subgroup analyses were also performed to investigate the genetic effects of ERCC2 polymorphisms on clinical characteristics of DLBCL patients.

Results

A significant association was discovered between the rs1799793 A allele and increased DLBCL risk (P=0.031, OR=1.928, 95% CI=1.052–3.534). The C allele of rs13181 was obviously associated with elevated DLBCL susceptibility (P=0.047, OR=1.820, 95% CI=1.002–3.305). The subgroup analysis demonstrated that rs1799793 and rs13181 polymorphisms had no relationship with serum lactate dehydrogenase level, nidus number, B-symptoms, Ann Arbor stages, or immunological types in DLBCL cases (P>0.05 for all).

Conclusions

Minor allele carriers of ERCC2 gene rs1799793 (Asp312Asn) and rs13181 (Lys751Gln) polymorphisms had higher susceptibility to DLBCL.

MeSH Keywords: Lymphoma, Large B-Cell, Diffuse; Polymorphism, Genetic 8 Xeroderma Pigmentosum Group D Protein

Background

Diffuse large B-cell lymphoma (DLBCL) is the most common type of non-Hodgkin lymphoma (NHL) in adults [1]. It is a malignancy of large B cells that is strongly invasive [2]. It can occur in any age, but it is usually diagnosed in older people. In recent years, the morbidity of DLBCL has increased within the aging population [3]. In China, it has a high morbidity and mortality rate [4]. Histological morphology, immune phenotype, and genetic characteristics of DLBCL had significant heterogeneity between patients [5]. DLBCL could originate from lymph nodes and extranodal sites [6,7]. Pathogenesis of DLBCL is still clear, but it is confirmed that immune deficiency, medical system, lifestyle, environmental exposure, and genetic variation may contribute to the occurrence of DLBCL [813]. Additionally, genetic factors are the basis for the disease heterogeneity and the therapy response [14,15]. Therefore, gene polymorphisms play a crucial role in disease susceptibility.

DNA is often damaged by endogenous or exogenous mutagenesis in cells, and if the repair for these damages is not timely, it may cause apoptosis or uncontrolled growth of cells [16]. Polymorphisms in the exon regions of DNA repair gene might alter the structure or activity of the protein, then lead to different cancers, including lymphoma [1719]. ERCC excision repair 2, TFIIH core complex helicase subunit (ERCC2), also known as xeroderma pigmentousm complementation group D (XPD), is a protein which participates in the transcription-coupled nucleotide excision repair. Human ERCC2 gene is located at chromosome 19q13.32. Single nucleotide polymorphisms (SNPs), rs1799793 (Asp312Asn), and rs13181 (Lys751Gln) are respectively located in exon 10 and exon 23 of the ERCC2 gene. Previous studies indicate that they could alter DNA repair capacity of the protein [20].

ERCC2 rs1799793 and rs13181 SNPs have been widely explored in different cancers [2123]. In spite of previous studies focused on the association of ERCC2 SNPs with DLBCL susceptibility, few studies have focused on this topic for the Chinese Han population. Therefore, we carried out this study; subgroup analysis based on different clinical features were also performed.

Material and Methods

Study participants

This case-control study was ratified by the institutional review board of Shenzhen Hospital, Southern Medical University. Written informed consent was signed by every participant prior to enrollment. The study protocol followed the Helsinki Declaration.

DLBCL patients who were hospitalized in Shenzhen Hospital, Southern Medical University were enrolled as participants in the case group. These patients were diagnosed by 2 pathologists using histopathologic examination, x-ray, magnetic resonance imaging (MRI), and routine blood examination [24]. Patients were all older than 18 years of age. Individuals who presented for healthy checkups in the same hospital were recruited as the controls; healthy individuals with histories of leukemia or lymphoma, immune or inflammatory diseases, or other tumors were excluded from the control group. The control group was matched with the case group by age and gender.

Sample collection and genotyping method

We collected 5 mL of peripheral blood samples from the elbow venous of the participants and stored the samples in EDTA tubes. TIANamp Blood DNA Kit (TIANGEN, Beijing) was used to extract the genomic DNA following the manufacturer’s instructions. ERCC2 gene rs1799793 and rs13181 SNPs were genotyped by polymerase chain reaction-restriction fragment length polymorphism (PCR-RFLP) as described in previous studies [25].

Statistical analysis

Continuous variables were compared by Student’s t-test. Categorical variables were evaluated by chi-square test or Fisher’s exact test. Genotype distributions of ERCC2 gene SNPs were examined by the Hardy-Weinberg equilibrium (HWE) test. The association between ERCC2 SNPs and DLBCL risk was addressed by odds ratios (ORs) with 95% confidence intervals (CIs). Subgroup analyses performed in this study were based on clinical characteristics: serum lactate dehydrogenase (LDH) level, location, nidus number, B-symptoms, Ann Arbor stages, and immunological type. All of the calculations were performed by PASW 18.0. P<0.05 was considered as the existence of statistical significance.

Results

Characteristics of participants

DLBCL patients in the case group included 78 males and 59 females with the mean age of 62.95±15.03 years. The control group included 83 males and 62 females, the mean age was 61.05±13.17 years old. No significant difference in age or gender was discovered between the case group and the control group (Table 1, P>0.05), indicating that the age and gender were well matched. In addition, smoking and drinking had no significant difference between the case group and the control group (P>0.05).

Table 1.

Characteristics of participants.

Characteristics Case n=137 (%) Control n=145 (%) P
Basic characteristics
Age 62.95±15.03 61.05±13.17 0.259
Gender 0.958
 Male 78 (56.93) 83 (57.24)
 Female 59 (43.07) 62 (42.76)
Smoking 0.573
 No 96 (70.07) 106 (73.10)
 Yes 41 (29.93) 39 (26.90)
Drinking 0.475
 No 89 (64.96) 100 (68.97)
 Yes 48 (35.04) 45 (31.03)
Clinical characteristics
Serum LDH level
 Normal (<226) 57 (41.61)
 High (≥226) 80 (58.39)
Locations
 Lymph nodes 45 (32.85)
 Extranodal 92 (67.15)
Nidus number
 <2 87 (63.50)
 ≥2 50 (36.50)
B-symptoms
 Without 85 (62.04)
 With 52 (37.96)
Ann Arbor stages
 I, II 73 (53.28)
 III, IV 64 (46.72)
Immunological type
 GCB 40 (29.20)
 ABC 97 (70.80)

LDH – lactate dehydrogenase; B-symptoms – including fever, weight loss, and night sweats; GCB – germinal center B-cell-like; ABC – activated B-cell-like.

In DLBCL patients, 80 patients had high serum LDH levels and 57 patients had normal LDH levels; 45 cases occurred in lymph nodes and 92 cases occurred in extranodal sites; and 50 patients had more than one nidus. In addition, 52 patients had B-symptoms (fever, weight loss, and night sweats); and 73 patients had Ann Arbor I or II stages and 64 patients had Ann Arbor III or IV stages. Based on the immunological types of DLBCL patients, 40 cases were germinal center B-cell-like (GCB) and 97 cases were activated B-cell-like (ABC).

Association between ERCC2 polymorphisms and DLBCL risk

Genotype distributions of ERCC2 gene rs1799793 and rs13181 SNPs were accorded with the HWE test in control group (Table 2, P>0.05), suggesting good representativeness of participants.

Table 2.

Association between ERCC2 polymorphisms and DLBCL susceptibility.

Genotype/allele Case n=137 (%) Control n=145 (%) P OR (95% CI)
rs1799793
 GG 109 (79.56) 128 (88.28)
 GA 25 (18.25) 16 (11.03) 0.076 1.835 (0.932–3.613)
 AA 3 (2.19) 1 (0.69) 0.340 3.523 (0.361–34.358)
 G 243 (88.69) 272 (93.79)
 A 31 (11.31) 18 (6.21) 0.031 1.928 (1.052–3.534)
PHWE 0.289 0.529
rs13181
 AA 110 (80.29) 128 (88.28)
 AC 23 (16.79) 15 (10.34) 0.101 1.784 (0.887–3.588)
 CC 4 (2.92) 2 (1.38) 0.422 2.327 (0.418–12.950)
 A 243 (88.69) 271 (93.45)
 C 31 (11.31) 19 (6.55) 0.047 1.820 (1.002–3.305)
PHWE 0.056 0.062

GA and AA genotypes of rs1799793 SNP had higher frequencies in the case group compared to the control group, but the difference was not statistical significant (Table 2, P>0.05). The allele of rs1799793 had significantly higher frequency in DLBCL patients, which indicated that this allele was positively correlated with DLBCL risk (P=0.031, OR=1.928, 95% CI=1.052–3.534).

Frequencies of rs13181 AA, AC, and CC genotypes respectively were 80.29%, 16.79%, 2.92% in DLBCL patients, and 88.28%, 10.34%, 1.38% in healthy controls. No significant difference in rs13181 genotypes were discovered between the case group and the control group (P>0.05). The significantly higher frequency of rs13181 C allele in DLBCL patients compared to the controls demonstrated that the C allele was distinctly correlated with an elevated DLBCL risk (P=0.047, OR=1.820, 95% CI=1.002–3.305).

Effects of ERCC2 polymorphisms on clinical characteristics of DLBCL

To certify the effects of ERCC2 polymorphisms for DLBCL risk, we performed subgroup analysis based on the serum LDH level, location, nidus number, B-symptoms, Ann Arbor stages, and immunological type. We found that ERCC2 rs1799793 and rs13181 polymorphisms had no association with serum LDH level, location, nidus number, B-symptoms, Ann Arbor stages, or immunological type in DLBCL patients (Tables 38, P>0.05 for all).

Table 3.

Effects of ERCC2 polymorphisms on serum LDH level in DLBCL patients.

Genotype/allele Normal LDH, n=57, % High LDH, n=80, % P OR (95% CI)
rs1799793
 GG 47 (82.46) 62 (77.50)
 GA 8 (14.04) 17 (21.25) 0.308 1.611 (0.641–4.050)
 AA 2 (3.51) 1 (1.25) 0.417 0.379 (0.033–4.306)
 G 102 (59.48) 141 (88.12)
 A 12 (10.52) 19 (11.88) 0.728 1.145 (0.532–2.465)
rs13181
 AA 44 (77.19) 66 (82.50)
 AC 11 (19.30) 12 (15.00) 0.488 0.727 (0.295–1.794)
 CC 2 (3.51) 2 (2.50) 0.689 0.667 (0.091–4.910)
 A 99 (86.84) 144 (90.00)
 C 15 (13.16) 16 (10.00) 0.332 0.688 (0.322–1.470)

Table 4.

Genetic association of ERCC2 polymorphisms with locations in DLBCL patients.

Genotype/allele Lymph nodes, n=45, % Extranodal sites n=92, % P OR (95% CI)
rs1799793
 GG 37 (82.22) 72 (78.26)
 GA 7 (15.56) 18 (19.57) 0.568 1.321 (0.507–3.447)
 AA 1 (2.22) 2 (2.17) 0.982 1.028 (0.090–11.709)
 G 81 (90.00) 162 (88.04)
 A 9 (10.00) 22 (11.96) 0.673 1.193 (0.525–2.708)
rs13181
 AA 35 (77.78) 75 (81.52)
 AC 9 (20) 14 (15.22) 0.498 0.726 (0.287–1.837)
 CC 1 (2.22) 3 (3.26) 0.773 1.400 (0.141–13.942)
 A 79 (87.78) 164 (89.13)
 C 11 (12.22) 20 (10.87) 0.740 0.876 (0.400–1.917)

Table 5.

Genetic effects of ERCC2 polymorphisms on nidus number in DLBCL cases.

Genotype/allele Nidus number <2, n=87,% Nidus number ≥2, n=50,% P OR (95% CI)
rs1799793
 GG 73 (83.91) 36 (72.00)
 GA 12 (13.79) 13 (26.00) 0.076 2.197 (0.911–5.298)
 AA 2 (2.30) 1 (2.00) 0.991 1.014 (0.089–11.556)
 G 158 (90.85) 85 (85.00)
 A 16 (9.15) 15 (15.00) 0.144 1.743 (0.821–3.697)
rs13181
 AA 68 (78.16) 42 (84.00)
 AC 17 (19.54) 6 (12.00) 0.272 0.571 (0.209–1.564)
 CC 2 (2.30) 2 (4.00) 0.633 1.619 (0.220–11.932)
 A 153 (87.93) 90 (90.00)
 C 21 (12.07) 10 (10.00) 0.603 0.810 (0.365–1.796)

Table 6.

Effects of ERCC2 polymorphisms on B-symptoms in case group.

Genotype/allele Without B-symptoms, n=85, % With B-symptoms, n=52, % P OR (95% CI)
rs1799793
 GG 67 (78.82) 42 (80.77)
 GA 16 (18.82) 9 (17.31) 0.814 0.897 (0.364–2.214)
 AA 2 (2.35) 1 (1.92) 0.855 0.798 (0.070–9.071)
 G 150 (88.23) 93 (89.42)
 A 20 (11.27) 11 (10.58) 0.763 0.887 (0.407–1.935)
rs13181
 AA 73 (85.88) 37 (71.15)
 AC 11 (12.94) 12 (23.08) 0.094 2.152 (0.867–5.340)
 CC 1 (1.18) 3 (5.77) 0.089 5.919 (0.595–58.887)
 A 157 (92.35) 86 (82.69)
 C 13 (7.65) 18 (17.31) 0.014 2.528 (1.182–5.407)

Table 7.

Genetic correlation of ERCC2 polymorphisms with DLBCL Ann Arbor stages.

Genotype/allele Ann Arbor stage I, II, n=73, % Ann Arbor stage III, IV, n=64, % P OR (95% CI)
rs1799793
 GG 55 (75.34) 54 (84.38)
 GA 16 (21.92) 9 (14.06) 0.221 0.573 (0.233–1.408)
 AA 2 (2.74) 1 (1.56) 0.558 2.037 (0.179–23.130)
 G 126 (86.30) 117 (91.45)
 A 20 (13.7) 11 (8.55) 0.183 0.592 (0.272–1.289)
rs13181
 AA 60 (82.19) 50 (78.13)
 AC 11 (15.07) 12 (18.75) 0.557 1.309 (0.532–3.220)
 CC 2 (2.74) 2 (3.13) 0.858 1.200 (0.163–8.828)
 A 131 (89.73) 112 (87.5)
 C 15 (10.27) 16 (12.5) 0.562 1.248 (0.590–2.636)

Table 8.

Effects of ERCC2 polymorphisms on DLBCL immunological types.

Genotype/allele GCB n=40, % ABC, n=97, % P OR (95% CI)
rs1799793
 GG 31 (77.50) 78 (80.41)
 GA 8 (20.00) 17 (17.53) 0.724 0.845 (0.331–2.157)
 AA 1 (2.50) 2 (2.06) 0.853 0.795 (0.070–9.086)
 G 70 (87.50) 173 (89.17)
 A 10 (12.50) 21 (10.83) 0.691 0.850 (0.381–1.896)
rs13181
 AA 31 (77.50) 79 (81.44)
 AC 8 (20.00) 15 (15.46) 0.527 0.736 (0.284–1.909)
 CC 1 (2.50) 3 (3.09) 0.889 1.177 (0.118–11.753)
 A 70 (87.50) 173 (89.17)
 C 10 (12.50) 21 (10.83) 0.691 0.850 (0.381–1.896)

Table 9.

Subgroup analysis of ERCC2 polymorphisms with DLBCL susceptibility based on Immunological type.

Genotype/allele GCB ABC
P OR (95% CI) P OR (95% CI)
rs1799793
 GG
 GA 0.123 2.065 (0.811–5.259) 0.137 1.744 (0.833–3.649)
 AA 0.359 4.129 (0.251–67.862) 0.560 3.282 (0.293–36.796)
 G
 A 0.060 2.159 (0.954–4.884) 0.067 1.834 (0.950–3.541)
rs13181
 AA
 AC 0.095 2.202 (0.857–5.657) 0.216 1.620 (0.751–3.495)
 CC 0.486 2.065 (0.181–23.505) 0.377 2.430 (0.397–14.866)
 A
 C 0.080 2.038 (0.907–4.578) 0.094 1.731 (0.905–3.314)

Discussion

We failed to find any significant association between the rs1799793 genotypes and DLBCL susceptibility. The significantly higher frequency of rs1799793 A allele in the case group compared to the control group suggested that the A allele was positively correlated with 1.928 times increased DLBCL susceptibility. Worrillow et al. suggested that although rs1799793 AA genotype had a higher trend for DLBCL, this SNP had no significant relationship with DLBCL risk in an English population [26]. Meanwhile, El-Din et al. found no significant association between rs1799793 SNP and DLBCL susceptibility in an Egyptian population, despite A allele carriers having a higher trend for DLBCL [27]. Inversely, a recent meta-analysis study showed that rs1799793 was negatively correlated with DLBCL risk under Asn (A) vs. Asp (G) genetic model [28]. These differences might be caused by differences in ethnicity or regions.

In this study, no significant association has been discovered between rs13181 genotypes and DLBCL risk; while an approximately 1.820 times elevated DLBCL risk was associated with rs13181 C allele. El-Din et al. indicated that rs13181 CC genotype carriers had higher susceptibility for DLBCL, but the association was not significant [28]. However, Worrillow et al. demonstrated that rs13181 CC genotype was significantly associated with reduced risk for DLBCL in an English population [26]. In addition, meta-analysis studies also failed to find a significant association between this SNP and DLBCL risk [23,28].

We performed the subgroup analyses to certify the influence of ERCC2 polymorphisms for DLBCL risk. Genotype distributions of ERCC2 gene rs1799793 and rs13181 polymorphisms showed no significant difference between different subgroups of patients. Thus, the polymorphisms of rs1799793 and rs13181 did not have an obvious association with the clinical characteristics of DLBCL patients; however, due to the limited sample size, the results needed further verification.

There were several limitations in this study. First, the sample size was relatively small; thus, the statistical power might be reduced. Second, the ethnicity might affect present results. Third, various potential confounding environmental and genetic factors involved in the occurrence of DLBCL were not considered in this current study. Therefore, the conclusions of this study should be verified in further studies with larger sample size.

Conclusions

ERCC2 gene rs1799793 and rs13181 polymorphisms might be risk factors for DLBCL. However, rs1799793 and rs13181 polymorphisms have no relationship with serum LDH level, tumor location, nidus numbers, B-symptoms, Ann Arbor I and II stages, or immunological type in DLBCL patients.

Footnotes

Source of support: Departmental sources

References

  • 1.Song J, Shao Q, Li C, et al. Effects of microRNA-21 on apoptosis by regulating the expression of PTEN in diffuse large B-cell lymphoma. Medicine (Baltimore) 2017;96:e7952. doi: 10.1097/MD.0000000000007952. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 2.Hu G, Zhu X. Ultrasonographic features of aggressive primary thyroid diffuse B-cell lymphoma: A report of two cases. Oncol Lett. 2016;11:2487–90. doi: 10.3892/ol.2016.4255. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 3.Paul U, Richter J, Stuhlmann-Laiesz C, et al. Advanced patient age at diagnosis of diffuse large B-cell lymphoma is associated with molecular characteristics including ABC-subtype and high expression of MYC. Leuk Lymphoma. 2018;59(5):1213–21. doi: 10.1080/10428194.2017.1365851. [DOI] [PubMed] [Google Scholar]
  • 4.Chen W, Zheng R, Baade PD, et al. Cancer statistics in China, 2015. Cancer J Clin. 2016;66:115–32. doi: 10.3322/caac.21338. [DOI] [PubMed] [Google Scholar]
  • 5.Hans CP, Weisenburger DD, Greiner TC, et al. Confirmation of the molecular classification of diffuse large B-cell lymphoma by immunohistochemistry using a tissue microarray. Blood. 2004;103:275–82. doi: 10.1182/blood-2003-05-1545. [DOI] [PubMed] [Google Scholar]
  • 6.Jaffe ES. The 2008 WHO classification of lymphomas: Implications for clinical practice and translational research. Hematology Am Soc Hematol Educ Program. 2009:523–31. doi: 10.1182/asheducation-2009.1.523. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 7.Tomonaga M. [Outline and direction of revised WHO classification of tumors of haematopoietic and lymphoid tissues]. Rinsho Ketsueki. 2009;50:1401–6. [in Japanese] [PubMed] [Google Scholar]
  • 8.Linke-Serinsoz E, Fend F, Quintanilla-Martinez L. Human immunodeficiency virus (HIV) and Epstein-Barr virus (EBV) related lymphomas, pathology view point. Semin Diagn Pathol. 2017;34:352–63. doi: 10.1053/j.semdp.2017.04.003. [DOI] [PubMed] [Google Scholar]
  • 9.Smedby KE, Ponzoni M. The aetiology of B-cell lymphoid malignancies with a focus on chronic inflammation and infections. J Intern Med. 2017;282(5):360–70. doi: 10.1111/joim.12684. [DOI] [PubMed] [Google Scholar]
  • 10.Kleinstern G, Abu Seir R, Perlman R, et al. Ethnic variation in medical and lifestyle risk factors for B cell non-Hodgkin lymphoma: A case-control study among Israelis and Palestinians. PLoS One. 2017;12:e0171709. doi: 10.1371/journal.pone.0171709. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 11.Cerhan JR, Kricker A, Paltiel O, et al. Medical history, lifestyle, family history, and occupational risk factors for diffuse large B-cell lymphoma: The InterLymph Non-Hodgkin Lymphoma Subtypes Project. J Natl Cancer Inst Monogr. 2014;2014:15–25. doi: 10.1093/jncimonographs/lgu010. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 12.Schinasi L, Leon ME. Non-Hodgkin lymphoma and occupational exposure to agricultural pesticide chemical groups and active ingredients: A systematic review and meta-analysis. Int J Environ Res Public Health. 2014;11:4449–527. doi: 10.3390/ijerph110404449. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 13.Jiao J, Zheng T, Lan Q, et al. Occupational solvent exposure, genetic variation of DNA repair genes, and the risk of non-Hodgkin’s lymphoma. Eur J Cancer Prev. 2012;21:580–84. doi: 10.1097/CEJ.0b013e328351c762. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 14.Reddy A, Zhang J, Davis NS, et al. Genetic and functional drivers of diffuse large B cell lymphoma. Cell. 2017;171:481–94e15. doi: 10.1016/j.cell.2017.09.027. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 15.Falduto A, Cimino F, Speciale A, et al. How gene polymorphisms can influence clinical response and toxicity following R-CHOP therapy in patients with diffuse large B cell lymphoma. Blood Rev. 2017;31:235–49. doi: 10.1016/j.blre.2017.02.005. [DOI] [PubMed] [Google Scholar]
  • 16.Hou D, Xu G, Zhang C, et al. Berberine induces oxidative DNA damage and impairs homologous recombination repair in ovarian cancer cells to confer increased sensitivity to PARP inhibition. Cell Death Dis. 2017;8:e3070. doi: 10.1038/cddis.2017.471. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 17.Özgöz A, Hekimler Öztürk K, Yükseltürk A, et al. Genetic variations of DNA repair genes in breast cancer. Pathol Oncol Res. 2017 doi: 10.1007/s12253-017-0322-3. [Epub ahead of print] [DOI] [PubMed] [Google Scholar]
  • 18.Feki-Tounsi M, Khlifi R, Louati I, et al. Polymorphisms in XRCC1, ERCC2, and ERCC3 DNA repair genes, CYP1A1 xenobiotic metabolism gene, and tobacco are associated with bladder cancer susceptibility in Tunisian population. Environ Sci Pollut Res Int. 2017;24:22476–84. doi: 10.1007/s11356-017-9767-x. [DOI] [PubMed] [Google Scholar]
  • 19.Chen Y, Zheng T, Lan Q, et al. Polymorphisms in DNA repair pathway genes, body mass index, and risk of non-Hodgkin lymphoma. Am J Hematol. 2013;88:606–11. doi: 10.1002/ajh.23463. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 20.Yang Y, Jin X, Yan C, et al. Case-only study of interactions between DNA repair genes (hMLH1, APEX1, MGMT, XRCC1 and XPD) and low-frequency electromagnetic fields in childhood acute leukemia. Leuk Lymphoma. 2008;49:2344–50. doi: 10.1080/10428190802441347. [DOI] [PubMed] [Google Scholar]
  • 21.Xiao F, Pu J, Wen Q, et al. Association between the ERCC2 Asp312Asn polymorphism and risk of cancer. Oncotarget. 2017;8:48488–506. doi: 10.18632/oncotarget.17290. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 22.Fu W, Xiao F, Zhang R, et al. Association between the Asp312Asn, Lys751Gln, and Arg156Arg polymorphisms in XPD and the risk of prostate cancer. Technol Cancer Res Treat. 2017 doi: 10.1177/1533034617724678. [Epub ahead of print] [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 23.Chen S, Zhu JH, Wang F, et al. Association of the Asp312Asn and Lys751Gln polymorphisms in the XPD gene with the risk of non-Hodgkin’s lymphoma: Evidence from a meta-analysis. Chin J Cancer. 2015;34:108–14. doi: 10.1186/s40880-015-0001-2. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 24.Lopez-Guillermo A, Colomo L, Jimenez M, et al. Diffuse large B-cell lymphoma: Clinical and biological characterization and outcome according to the nodal or extranodal primary origin. J Clin Oncol. 2005;23:2797–804. doi: 10.1200/JCO.2005.07.155. [DOI] [PubMed] [Google Scholar]
  • 25.Song B, Zhu JY, Liu J, et al. [Association of gene polymorphisms in the DNA repair gene XPD with risk of non-Hodgkin’s lymphoma]. Zhongguo Shi Yan Xue Ye Xue Za Zhi. 2008;16:97–100. [in Chinese] [PubMed] [Google Scholar]
  • 26.Worrillow L, Roman E, Adamson PJ, et al. Polymorphisms in the nucleotide excision repair gene ERCC2/XPD and risk of non-Hodgkin lymphoma. Cancer Epidemiol. 2009;33:257–60. doi: 10.1016/j.canep.2009.08.002. [DOI] [PubMed] [Google Scholar]
  • 27.El-Din MA, Khorshied MM, El-Saadany ZA, et al. Excision repair cross-complementing group 2/Xeroderma pigmentousm complementation group D (ERCC2/XPD) genetic variations and susceptibility to diffuse large B cell lymphoma in Egypt. Int J Hematol. 2013;98:681–86. doi: 10.1007/s12185-013-1462-1. [DOI] [PubMed] [Google Scholar]
  • 28.Zhou JY, He LW, Liu J, et al. Comprehensive assessment of associations between ERCC2 Lys751Gln/Asp312Asn polymorphisms and risk of non-Hodgkin lymphoma. Asian Pac J Cancer Prev. 2014;15:9347–53. doi: 10.7314/apjcp.2014.15.21.9347. [DOI] [PubMed] [Google Scholar]

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