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XAB2 tagSNPs contribute to non-small cell lung cancer susceptibility in Chinese population

BMC Cancer201515:560

https://doi.org/10.1186/s12885-015-1567-4

Received: 4 May 2014

Accepted: 17 July 2015

Published: 31 July 2015

Abstract

Background

XPA-binding protein 2 (XAB2) interacts with Cockayne syndrome complementation group A (CSA), group B (CSB) and RNA polymerase II to initiate nucleotide excision repair. This study aims to evaluate the association of XAB2 genetic variants with the risk of non-small cell lung cancer (NSCLC) using a tagging approach.

Methods

A hospital-based case-control study was conducted in 470 patients with NSCLC and 470 controls in Chinese population. Totally, 5 tag single nucleotide polymorphisms (SNPs) in XAB2 gene were selected by Haploview software using Hapmap database. Genotyping was performed using iPlex Gold Genotyping Asssy and Sequenom MassArray. Unconditional logistic regression was conducted to estimate odd ratios (ORs) and 95 % confidence intervals (95 % CI).

Results

Unconditional logistic regression analysis showed that the XAB2 genotype with rs794078 AA or at least one rs4134816 C allele were associated with the decreased risk of NSCLC with OR (95 % CI) of 0.12 (0.03–0.54) and 0.46 (0.26–0.84). When stratified by gender, we found that the subjects carrying rs4134816 CC or CT genotype had a decreased risk for developing NSCLC among males with OR (95 % CI) of 0.39 (0.18–0.82), but not among females. In age stratification analysis, we found that younger subjects (age ≤ 60) with at least one C allele had a decreased risk of NSCLC with OR (95 % CI) of 0.35 (0.17–0.74), but older subjects didn’t. We didn’t find that XAB2 4134816 C > T variant effect on the risk of NSCLC when stratified by smoking status. The environmental factors, such as age, sex and smoking had no effect on the risk of NSCLC related to XAB2 genotypes at other polymorphic sites.

Conclusions

The XAB2 tagSNPs (rs794078 and rs4134816) were significantly associated with the risk of NSCLC in Chinese population, which supports the XAB2 plays a significant role in the development of NSCLC.

Keywords

XAB2 Lung cancer Polymorphisms Transcriptional coupling nucleotide excision repair Susceptibility

Background

Worldwide, lung cancer harbored the highest incidence and mortality rates among all malignant cancers [1, 2]. Non-small cell lung cancer (NSCLC), as the most common type of lung cancer, accounts for 75–80 % of all lung cancer cases [3]. The development of lung cancer was greatly affected by the environmental factors, such as cigarette smoking, alcohol drinking and air pollutants [46]. However, evidence has showed that the genetic variants of cancer-related genes are associated with lung risk, which the important role of genetic factors in the development of lung cancer [79].

Nucleotide excision repair (NER) is the major DNA repair pathway to remove bulky DNA lesions induced by UV light and environmental carcinogens [10]. NER has two subpathways, global genome NER (GG-NER) and transcription coupling NER (TC-NER). TC-NER is involved in a rapid removal of the damages on the transcribed strands of active genes and a resumption of transcription [1113]. TC-NER is initiated by arresting RNA polymerase II at DNA lesion site on transcript strand. In the initiation of transcription coupling repair, the TC-NER specific proteins Cockayne syndrome complementation group A (CSA) and group B (CSB) are thought to play an important role in removing the stalled RNA polymorase II and recruiting other DNA repair proteins [14]. Many studies have demonstrated that the decreased expression of CSA and CSB in lung cancer and the genetic variants in these two genes were associated with the lung cancer risk [1518].

Xeroderma pigmentosum group A (XPA)-binding protein 2 (XAB2), which located at 19p13.2, was first identified as an interacting protein with XPA and hence found to interact with CSA, CSB and RNA polymerase II to participant to TC-NER and transcription [17, 19, 20]. In vitro, when cells treated with DNA-damaging agents, enhanced interaction of XAB2 with RNA polymerase II or XPA was observed, which suggesting DNA damage-responsive activity of the XAB2 [19].

Due to the important role of XAB2 in the TC-NER, we proposed that the genetic variants in XAB2 genes might contribute to the risk of lung cancer. To verify this proposal, we conducted this case-control study to evaluate the role of XAB2 tagSNPs in the development of NSCLC.

Methods

Study population

The study population has been described previously [21]. Briefly, this hospital-based case-control study consisted of 470 patients with NSCLC and 470 cancer-free controls. All subjects were unrelated Han Chinese. All patients with newly diagnosed, and previously untreated primary lung cancer were recruited between January 2008 and December 2012 at Tangshan Gongren Hospital (Tangshan, China). The exclusive criteria included previous cancer and previous radiotherapy or chemotherapy. The controls were randomly selected from cancer-free individuals living in the same region during the same period as the cases were collected. The selection criteria included no prior history of cancer. Controls were frequency matched to the cases by age (±5 years) and sex. At recruitment, informed consent was obtained from each subject who was then interviewed for detailed information on demographic characteristics and lifetime history of tobacco use. The study was approved by Ethics Committee of Hebei United University (Approval No. 12–002).

Tag SNPs selection and genotyping

Based on the Han Chinese in Beijing (CHB) population data from HapMap database, we used Haploview 4.2 program to select candidate tag SNPs with an r2 threshold of 0.80 and minor allele frequency (MAF) greater than 1 %. For XAB2 gene, we extended the 5′- and 3′-untranslated regions (UTR) to include the 5′-UTR and 3′-UTR most SNP. As a result, 5 tagSNPs (2 in 5′ UTR, 2 in intron, 1 in exon region) in XAB2 were included, which represent the common genetic variants in Chinese population. Genotyping was performed at Bomiao Tech (Beijing, China) using iPlex Gold Genotyping Asssy and Sequenom MassArray (Sequenom, San Diego, CA, USA). Sequenom’s MassArray Designer was used to design PCR and extension primers for each SNP. The information on assay conditions and the primers are available upon request. Genotyping quality control consisted of no-temple control samples for allele peaks and verifying consistencies in genotype calls of 2 % randomly selected duplicate sample. In addition, we excluded individuals and SNPs based on genotyping quality (<90 % call rate).

Statistical analysis

The χ2 test was used to examine differences in demographic variables and the distribution of genotype between patients and controls. Hardy-Weinberg equilibrium (HWE) for each SNP in controls was examined using Pearson goodness-of-fit χ2 test. The association of each tag SNP with the risk of NSCLC was estimated by odds ratios (ORs) and 95 % confidential intervals (95 % CI) using unconditional logistic regression adjusted by sex, age, and smoking status. Smokers were considered current smokers if they smoked up to 1 year before the date of cancer diagnosis for NSCLC patients or before the date of the interview for controls. The number of pack-years smoked was determined as an indication of cumulative cigarette-dose level [pack-year = (cigarettes per day/20) × (years smoked)]. Light and heavy smokers were categorized by using the 50th percentile pack-year value of the controls as the cut points (i.e., ≤25 and >25 pack-years). Statistical analysis was performed using the SPSS version16.0 (SPSS Inc, Chicago, IL). A P value of < 0.05 was considered as statistically significant. Gene-smoking interaction was analyzed by GxEscan (http://biostats.usc.edu/software).

Results

Subject characteristics

The demographic characteristics of all participants are presented in Table 1. The distribution of gender and age among NSCLC cancer cases and healthy controls were not significantly different (P = 0.832 for gender, and P = 0.470 for age). There were also no significant differences in the distribution of smoking status between cases and controls. However, the heavy smokers (≥25 pack-year) accounted for 63.4 % in cases and only 49.2 % in controls, which suggested that cigarette smoking was a prominent contributor to the risk of lung cancer. Among ever-smokers, 46,8 % (96) and 41.8 % (79) are former smokers in lung cancer cases and controls, respectively. Of 470 NSCLC patients, 37.9 % (178) were adenocarcinoma, 50.6 % (238) was squamous cell carcinoma, and 11.5 % (54) were other types, including large cell carcinoma (n = 49) and mixed cell carcinoma (n = 5).
Table 1

Distributions of select characteristics in cases and control subjects

Variables

Cases (n = 470)

Controls (n = 470)

P valuea

No

(%)

No

(%)

Gender

    

0.832

 Male

324

68.9

328

69.8

 

 Female

146

31.1

142

30.2

 

Age

    

0.470

 <50

84

17.9

96

20.4

 

 50–59

177

37.7

187

39.8

 

 60–69

129

27.4

111

23.6

 

 ≥70

80

17.0

76

16.2

 

Smoking status

    

0.321

 Non-smoker

265

56.4

281

59.8

 

 Ever-smoker

205

43.6

189

40.2

 

Pack-year smoked

    

0.001

 <25

75

36.6

96

50.8

 

 ≥25

130

63.4

93

49.2

 

atwo-side χ2 test

Selected SNPs and risk of developing NSCLC

The position and minor allele frequency (MAF) of the 5 selected tag SNPs in XAB2 gene were presented in Table 2. For all selected SNPs, the distributions of genotype frequencies in controls were close to those expected under Hardy Weinberg Equilibrium (HWE) (P > 0.05 for all).
Table 2

Primary information of tag SNPs inXAB2gene

Gene and locus

Rs number

Contig position

Location

Base change

MAF in controls

P for HWE test

Call rate (%)

XAB219p13.2

rs4134816

297747

5′ near gene

T/C

0.04

0.998

100

 

rs4134819

297227

5′ near gene

A/G

0.50

0.708

99.8

 

rs794083

295863

Intron

C/G

0.33

0.157

100

 

rs4134860

290403

Intron

T/C

0.15

0.978

100

 

rs794078

289839

T620T

G/A

0.12

0.136

97.8

The observed genotype frequencies in participants and the association of genotypes with the NSCLC were presented in Table 3. Of all selected SNPs in XAB2 genes, two SNPs were identified to be associated with the risk of NSCLC. For XAB2 rs794078 G > A polymorphism, we found that AA genotype carriers had a significantly decreased risk for developing NSCLC (OR = 0.12; 95 % CI = 0.03–0.54) in comparison to those with GG genotype. For XAB2 rs4134816 T > C polymorphism, just one CC genotype was found among all individuals, so we combined CT with CC genotype together for further analysis. Our data showed that the subjects with rs4134816 CT or CC genotype had a decreased risk of NSCLC compared with those carrying TT genotype with OR (95 % CI) of 0.46 (0.26–0.84). We didn’t find that any other selected SNPs were associated with the risk of NSCLC.
Table 3

Genotype frequencies of XAB2 and their association with non-small cell lung cancers

XAB2 Genotypes

Controls (n = 470)

Cases (n = 470)

OR (95 % CI)a

P valuea

No

(%)

No

(%)

rs4134816

      

  TT

429

91.3

450

95.7

  

  CT

40

8.5

20

4.3

0.49 (0.28–0.86)

0.012

  CC

1

0.2

0

0.0

NC

 

 CT + CC

41

8.7

20

4.3

0.46 (0.26–0.84)

0.010

rs4134819

      

  AA

122

26.0

126

26.8

  

  AG

226

48.0

237

50.4

0.96 (0.70–1.31)

0.797

  GG

122

26.0

107

22.8

0.81 (0.56–1.16)

0.251

rs794083

      

  CC

221

47.0

249

53.0

  

  CG

189

40.2

161

34.2

0.72 (0.54–0.96)

0.023

  GG

60

12.8

60

12.8

0.87 (0.58–1.31)

0.517

rs4134860

      

  TT

341

72.6

332

70.7

  

  CT

118

25.1

120

25.5

1.01 (0.75–1.36)

0.962

  CC

11

2.3

18

3.8

1.73 (0.80–3.75)

0.163

rs794078

      

  GG

365

77.7

374

79.6

  

  AG

93

19.8

94

20.0

0.97 (0.70–1.35)

0.871

  AA

12

2.5

2

0.4

0.12 (0.03–0.54)

0.006

AG + AA

105

22.3

96

20.4

0.87 (0.64–1.20)

0.396

aData were calculated by logistic regression and adjusted for sex, age (categories), and smoking status

Stratification analysis of the XAB2 polymorphisms and the risk of NSCLC

We then performed stratification analysis to evaluate the effect of environmental factors on the association of XAB2 polymorphisms with the risk of NSCLC (Table 4). In dominant model, we found that the subjects carrying rs4134816 CC or CT genotype had a decreased risk for developing NSCLC among males with OR (95 % CI) of 0.39 (0.18–0.82), but not among females. When stratified by gender, we observed a positively significant interaction between rs4134816 genotypes and gender on decreasing NSCLC risk (P = 0.034). Our data also showed that younger subjects (age ≤ 60) with at least one C allele had a decreased risk of NSCLC with OR (95 % CI) of 0.35 (0.17–0.74), but older subjects didn’t. However, there was no gene-environment interaction observed (P = 0.094). We didn’t find that XAB2 4134816 C > T variant effect on the risk of NSCLC when stratified by smoking status. The environmental factors, such as age, sex and smoking had no effect on the risk of NSCLC related to XAB2 genotypes at other polymorphic sites (Table 4).
Table 4

Association of XAB2 tagSNPs with NSCLC risk stratified by selected variables

Genetic Variant

Variable

Genotypes (Cases/Controls)

Dominant model (AB + BB)/AAbOR (95 % CI)a

P value

  

AAb

AB + BBb

  

rs4134816

Sex

    

  T > C

 Male

314/301

10/27

0.39 (0.18–0.82)

0.013

 

 Female

136/128

10/14

0.68 (0.29–1.59)

0.370

 

Age

    
 

 ≤60

251/254

10/29

0.35 (0.17–0.74)

0.006

 

 >60

199/175

10/12

0.98 (0.40–2.39)

0.970

 

Smoking status

    
 

 Non-smoker

252/256

13/24

0.51 (0.26–1.03)

0.060

 

 Ever-smoker

198/173

7/16

0.47 (0.19–1.20)

0.113

rs4134819

Sex

    

  A > G

 Male

80/90

244/238

1.10 (0.77–1.58)

0.591

 

 Female

46/32

100/110

0.64 (0.38–1.09)

0.098

 

Age

    
 

 ≤60

76/77

185/206

0.91 (0.63–1.33)

0.638

 

 >60

50/45

159/142

0.92 (0.57–1.48)

0.726

 

Smoking status

    
 

 Non-smoker

82/75

183/206

0.81 (0.56–1.17)

0.252

 

 Ever-smoker

44/47

161/142

1.13 (0.70–1.82)

0.628

rs794083

Sex

    

  C > G

 Male

169/159

155/169

0.88 (0.64–1.20)

0.415

 

 Female

80/62

66/80

0.66 (0.41–1.05)

0.081

 

Age

    
 

 ≤60

139/140

122/143

0.90 (0.64–1.27)

0.546

 

 >60

110/81

99/106

0.71 (0.47–1.07)

0.098

 

Smoking status

    
 

 Non-smoker

144/139

121/142

0.81 (0.58–1.14)

0.226

 

 Ever-smoker

105/82

100/107

0.74 (0.49–1.11)

0.141

rs4134860

Sex

    

  T > C

 Male

227/237

97/91

1.14 (0.80–1.61)

0.470

 

 Female

105/104

41/38

1.11 (0.66–1.87)

0.702

 

Age

    
 

 ≤60

186/211

75/72

1.24 (0.84–1.82)

0.275

 

 >60

146/130

63/57

0.97 (0.63–1.51)

0.906

 

Smoking status

    
 

 Non-smoker

190/207

75/74

1.10 (0.76–1.61)

0.608

 

 Ever-smoker

142/134

63/55

1.05 (0.67–1.63)

0.841

rs794078

Sex

    

  G > A

 Male

256/256

68/72

0.92 (0.63–1.35)

0.673

 

 Female

118/109

28/33

0.79 (0.45–1.40)

0.426

 

Age

    
 

 ≤60

208/226

53/57

1.04 (0.68–1.58)

0.872

 

 >60

166/139

43/48

0.74 (0.46–1.20)

0.226

 

Smoking status

    
 

 Non-smoker

211/225

54/56

1.02 (0.67–1.55)

0.930

 

 Ever-smoker

163/140

42/49

0.73 (0.45–1.18)

0.202

aData were calculated by unconditional logistic regression and adjusted for gender, age (categories), and smoking status, where it was appropriate

bA stands for Major allele and B stands for Minor allele for each SNP

Discussion

In this case-control study in a Chinese population, we found that two tag SNPs (rs794078 and rs4134816) in XAB2 were associated with significantly decreased risk of development non-small cell lung cancer. These findings indicated that XAB2 genetic variants might contribute to the susceptibility of lung cancer.

Nucleotide excision repair is the main mechanism for removing the bulky DNA adduct from damage DNA for preventing carcinogens-induced mutagenesis [22, 23]. Several animal models, where individual NER genes were disrupted, had showed the importance of the integrity of NER pathway in preventing lung cancer [24, 25].

TC-NER, as one of important sub-pathways in NER, only repairs the lesions in the transcribed strand in active genes. There are several major proteins involved in TC-NER in human cells, including CSA, CSB, XPA and XAB2. Studies have showed that the deficient of these nucleotide excision repair proteins contributed to the risk of various cancers. Animal experiments showed that the CSB played an important role in the cellular response to stress and CSB−/− mice were increased susceptible to chemically induced skin cancer [26]. A case-control study also found 12.2 and 12.5 % reduced RNA transcriptional levels of CSA and CSB in lung cancer patients than controls [27].

XAB2 is a key factor in TC-NER, which is composed of 855 amino acids and contains 15 tetratricopeptide repeat motifs. By interacting with CSA, CSB, RNA polymerase II and XPA, XAB2 conducted the multiple functions in the process of transcription and TC-NER [19, 20]. Microinjection of specific antibodies against XAB2 inhibits transcription and TC-NER, suggesting the key role of XAB2 in the process of transcription and TC-NER [20]. Knockdown of XAB2 in HeLa cell resulted in a hypersensitivity to killing by UV light and a decreased recovery of RNA synthesis [19]. Over expression of XAB2 was observed in HL60 cells treated with inhibited all-trans retinoic acid (ATRA) and inhibited XAB2 expression by small interfering RNA (siRNA) increased ATRA-sensitive cellular differentiation, which indicated that XAB2 was associated with the cellular differentiation [28].

Studies have demonstrated that the polymorphisms, which located in NER genes or regulatory sequences, may affect DNA repair capacity and further increase likelihood of cancer development. In the present study of NSCLC in Chinese, we used a relatively comprehensive selection of SNPs and found the significant effects of XAB2 variants on the risk of lung cancer. This is the first study to investigate the association of XAB2 polymorphisms with the risk for developing cancer. There were several studies to evaluate the role of XAB2 genetic variants in complex autoimmune disease. For example, Briggs et al. conducted a case-control study to evaluate the correlation between XAB2 rs4134860 T > C variant and the risk of multiple sclerosis (MS) and found an increased risk of MS among rs4134860 CC genotype carriers [29]. In this lung cancer case-control study, we didn’t find any association of XAB2 rs4134860 T > C polymorphism with the risk of NSCLC. In another study, researchers analyzed the impact of several polymorphisms in DNA repair genes on the prognosis of colorectal cancer patients and didn’t find the association of XAB2 rs794078 G > A variant with the cancer prognosis [30]. In present study, individuals carrying XAB2 rs794078 AA genotype had 88 % decreased risk of NSCLC.

As we know, the magnitude of the effect of smoking far outweighed all other factors leading to lung cancer [31, 32]. Many studies have demonstrated that the strong association of smoking with lung cancer risk [5, 33, 34]. Therefore, we further analyzed the role of XAB2 polymorphisms in the development of NSCLC stratified by smoking status. We observed that a 49 % protective effect for XAB2 rs4134816 variant was evident only for non-smokers, but not for smokers. The exact mechanism of how cigarette-smoking effects on DNA repair capacity posted by XAB2 polymorphism is unknown. One possible explanation may be that the protective effect of XAB2 variant allele might be evident in non-smokers with low levels of oxidative damage. Similar pattern of genetic effects have been observed for DNA repair gene XRCC1 (X-ray repair cross-complementation group 1) at low smoking exposure, but not at high smoking exposure [35].

When stratified by gender, our study showed a 61 % protective effect of XAB2 rs4134816 C genotype among men, but not among women. Genetic variants in NER genes are associated with variability of lung cancer risk. Letkova and his colleagues investigated the polymorphisms of selected DNA repair genes, including XPC, XPD, hOGG1 and XRCC1, and found the different risks of developing lung cancer when stratified by gender, which further supporting our current findings [36]. Our present study also found that a 65 % protective effect for XAB2 rs4134816 T > C genetic variant among subjects aged 60 years or younger. Using Cox proportional hazard model, Gauderman et al. estimated the age-specific genetic incidence rate and found that the estimated proportion of lung cancer patients with high-risk allele exceeds 90 % for cases with onset at age 60 years or less and decreases to approximately 10 % for cases with onset at age 80 years or older. These findings suggested the contribution of age in the development of cancer [37]. The numbers of subjects in several of subgroups were very small, so some caution is needed when interpreting these findings.

Our study has its limitation. Due to the moderate sample size and the lack of related phenotypic and functional assays, large studies and functional evaluations are still need to be conducted in the future.

Conclusions

In conclusion, we have genotyped 5 tag SNPs in XAB2 gene in this NSCLC case-control set. We found the evidence of significant association with the risk of NSCLC for two tag SNPs (rs794078 and rs4134816) in XAB2 gene in Chinese population. These results further supported that XAB2 play a significant role in the development of NSCLC.

Abbreviations

XAB2

XPA-binding protein 2

MAF: 

Minor allele frequency

OR: 

Odds ratio

CI: 

Confidence interval

SNP: 

Single nucleotide polymorphism

Declarations

Acknowledgement

This study was supported by National Natural Science Foundation of China (81272613 to X. Zhang), Program for New Century Excellent Talents in University (NCET-11-0933 to X. Zhang), A Foundation for the Author of National Excellent Doctoral Dissertation of PR China (FANEDD) (201274 to X. Zhang), Science Fund for Distinguished Young Scholars of Hebei Scientific Committee (2012401022 to X. Zhang), and Leader talent cultivation plan of innovation team in Hebei province (LJRC001 to X. Zhang).

Authors’ Affiliations

(1)
Institute of Molecular Genetics, College of Life Sciences, Hebei United University
(2)
Department of Epidemiology, College of Public Health, Hebei United University
(3)
Tangshan Gongren Hospital, Hebei United University

References

  1. Horak J, Sobota J, Burda J. Angiographic diagnostics of splenic tumours (author’s transl). Cesk Radiol. 1975;29(5):348–55.PubMedGoogle Scholar
  2. Bunn Jr PA. Worldwide overview of the current status of lung cancer diagnosis and treatment. Arch Pathol Lab Med. 2012;136(12):1478–81.View ArticlePubMedGoogle Scholar
  3. Kurkcuoglu N, Alaybeyi F. Topical capsaicin for psoriasis. Br J Dermatol. 1990;123(4):549–50.View ArticlePubMedGoogle Scholar
  4. Jemal A, Bray F, Center MM, Ferlay J, Ward E, Forman D. Global cancer statistics. CA Cancer J Clin. 2011;61(2):69–90.View ArticlePubMedGoogle Scholar
  5. Hecht SS. Lung carcinogenesis by tobacco smoke. Int J Cancer. 2012;131(12):2724–32.View ArticlePubMedPubMed CentralGoogle Scholar
  6. Dresler C. The changing epidemic of lung cancer and occupational and environmental risk factors. Thorac Surg Clin. 2013;23(2):113–22.View ArticlePubMedGoogle Scholar
  7. Liu L, Wu J, Wu C, Wang Y, Zhong R, Zhang X, et al. A functional polymorphism (−1607 1G2G) in the matrix metalloproteinase-1 promoter is associated with development and progression of lung cancer. Cancer. 2011;117(22):5172–81.View ArticlePubMedGoogle Scholar
  8. Ke J, Zhong R, Zhang T, Liu L, Rui R, Shen N, et al. Replication study in Chinese population and meta-analysis supports association of the 5p15.33 locus with lung cancer. PLoS One. 2013;8(4):e62485.View ArticlePubMedPubMed CentralGoogle Scholar
  9. Yang IA, Holloway JW, Fong KM. Genetic susceptibility to lung cancer and co-morbidities. J Thorac Dis. 2013;5 Suppl 5:S454–62.PubMedPubMed CentralGoogle Scholar
  10. Scharer OD. Nucleotide excision repair in eukaryotes. Cold Spring Harb Perspect Biol. 2013;5(10):a012609.View ArticlePubMedPubMed CentralGoogle Scholar
  11. Hanawalt PC, Spivak G. In: Dizdaroglu M, Karakaya AE, editors. Advances in DNA Damage and Repair. New York: Kluwer Academic/Plenum Publishers; 1999. p. 169–79.View ArticleGoogle Scholar
  12. Mellon I. Transcription-coupled repair: a complex affair. Mutat Res. 2005;577(1–2):155–61.View ArticlePubMedGoogle Scholar
  13. Hanawalt PC, Spivak G. Transcription-coupled DNA repair: two decades of progress and surprises. Nat Rev Mol Cell Biol. 2008;9(12):958–70.View ArticlePubMedGoogle Scholar
  14. van den Boom V, Jaspers NG, Vermeulen W. When machines get stuck--obstructed RNA polymerase II: displacement, degradation or suicide. Bioessays. 2002;24(9):780–4.View ArticlePubMedGoogle Scholar
  15. Leng S, Bernauer A, Stidley CA, Picchi MA, Sheng X, Frasco MA, et al. Association between common genetic variation in Cockayne syndrome A and B genes and nucleotide excision repair capacity among smokers. Cancer Epidemiol Biomarkers Prev. 2008;17(8):2062–9.View ArticlePubMedGoogle Scholar
  16. Lehmann AR. DNA repair-deficient diseases, xeroderma pigmentosum, Cockayne syndrome and trichothiodystrophy. Biochimie. 2003;85(11):1101–11.View ArticlePubMedGoogle Scholar
  17. Fousteri M, Mullenders LH. Transcription-coupled nucleotide excision repair in mammalian cells: molecular mechanisms and biological effects. Cell Res. 2008;18(1):73–84.View ArticlePubMedGoogle Scholar
  18. Reddy JK, Rao S, Moody DE. Hepatocellular carcinomas in acatalasemic mice treated with nafenopin, a hypolipidemic peroxisome proliferator. Cancer Res. 1976;36(4):1211–7.PubMedGoogle Scholar
  19. Kuraoka I, Ito S, Wada T, Hayashida M, Lee L, Saijo M, et al. Isolation of XAB2 complex involved in pre-mRNA splicing, transcription, and transcription-coupled repair. J Biol Chem. 2008;283(2):940–50.View ArticlePubMedGoogle Scholar
  20. Nakatsu Y, Asahina H, Citterio E, Rademakers S, Vermeulen W, Kamiuchi S, et al. XAB2, a novel tetratricopeptide repeat protein involved in transcription-coupled DNA repair and transcription. J Biol Chem. 2000;275(45):34931–7.View ArticlePubMedGoogle Scholar
  21. Yu X, Rao J, Lin J, Zhang Z, Cao L, Zhang X. Tag SNPs in complement receptor-1 contribute to the susceptibility to non-small cell lung cancer. Mol Cancer. 2014;13:56.View ArticlePubMedPubMed CentralGoogle Scholar
  22. Dreij K, Seidel A, Jernstrom B. Differential removal of DNA adducts derived from anti-diol epoxides of dibenzo[a, l]pyrene and benzo[a]pyrene in human cells. Chem Res Toxicol. 2005;18(4):655–64.View ArticlePubMedGoogle Scholar
  23. Lage C, de Padula M, de Alencar TA, da Fonseca Goncalves SR, da Silva VL, Cabral-Neto J, et al. New insights on how nucleotide excision repair could remove DNA adducts induced by chemotherapeutic agents and psoralens plus UV-A (PUVA) in Escherichia coli cells. Mutat Res. 2003;544(2–3):143–57.View ArticlePubMedGoogle Scholar
  24. Hollander MC, Philburn RT, Patterson AD, Velasco-Miguel S, Friedberg EC, Linnoila RI, et al. Deletion of XPC leads to lung tumors in mice and is associated with early events in human lung carcinogenesis. Proc Natl Acad Sci U S A. 2005;102(37):13200–5.View ArticlePubMedPubMed CentralGoogle Scholar
  25. Melis JP, Wijnhoven SW, Beems RB, Roodbergen M, van den Berg J, Moon H, et al. Mouse models for xeroderma pigmentosum group A and group C show divergent cancer phenotypes. Cancer Res. 2008;68(5):1347–53.View ArticlePubMedGoogle Scholar
  26. van der Horst GT, van Steeg H, Berg RJ, van Gool AJ, de Wit J, Weeda G, et al. Defective transcription-coupled repair in Cockayne syndrome B mice is associated with skin cancer predisposition. Cell. 1997;89(3):425–35.View ArticlePubMedGoogle Scholar
  27. Cheng L, Spitz MR, Hong WK, Wei Q. Reduced expression levels of nucleotide excision repair genes in lung cancer: a case-control analysis. Carcinogenesis. 2000;21(8):1527–30.View ArticlePubMedGoogle Scholar
  28. Ohnuma-Ishikawa K, Morio T, Yamada T, Sugawara Y, Ono M, Nagasawa M, et al. Knockdown of XAB2 enhances all-trans retinoic acid-induced cellular differentiation in all-trans retinoic acid-sensitive and -resistant cancer cells. Cancer Res. 2007;67(3):1019–29.View ArticlePubMedGoogle Scholar
  29. Briggs FB, Goldstein BA, McCauley JL, Zuvich RL, De Jager PL, Rioux JD, et al. Variation within DNA repair pathway genes and risk of multiple sclerosis. Am J Epidemiol. 2010;172(2):217–24.View ArticlePubMedPubMed CentralGoogle Scholar
  30. Kim JG, Chae YS, Sohn SK, Moon JH, Kang BW, Park JY, et al. IVS10 + 12A > G polymorphism in hMSH2 gene associated with prognosis for patients with colorectal cancer. Ann Oncol. 2010;21(3):525–9.View ArticlePubMedGoogle Scholar
  31. IARC Working Group on the Evaluation of Carcinogenic Risks to Humans. Personal habits and indoor combustions. Volume 100 E. A review of human carcinogens. IARC Monogr Eval Carcinog Risks Hum. 2012;100(Pt E)):1–538.Google Scholar
  32. de Groot P, Munden RF. Lung cancer epidemiology, risk factors, and prevention. Radiol Clin North Am. 2012;50(5):863–76.View ArticlePubMedGoogle Scholar
  33. Schwartz AG, Prysak GM, Bock CH, Cote ML. The molecular epidemiology of lung cancer. Carcinogenesis. 2007;28(3):507–18.View ArticlePubMedGoogle Scholar
  34. Jassem E, Szymanowska A, Sieminska A, Jassem J. Smoking and lung cancer. Pneumonol Alergol Pol. 2009;77(5):469–73.PubMedGoogle Scholar
  35. Stern MC, Umbach DM, van Gils CH, Lunn RM, Taylor JA. DNA repair gene XRCC1 polymorphisms, smoking, and bladder cancer risk. Cancer Epidemiol Biomarkers Prev. 2001;10(2):125–31.PubMedGoogle Scholar
  36. Letkova L, Matakova T, Musak L, Sarlinova M, Krutakova M, Slovakova P, et al. DNA repair genes polymorphism and lung cancer risk with the emphasis to sex differences. Mol Biol Rep. 2013;40(9):5261–73.View ArticlePubMedGoogle Scholar
  37. Gauderman WJ, Morrison JL. Evidence for age-specific genetic relative risks in lung cancer. Am J Epidemiol. 2000;151(1):41–9.View ArticlePubMedGoogle Scholar

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This article is published under license to BioMed Central Ltd. This is an Open Access article distributed under the terms of the Creative Commons Attribution License (http://creativecommons.org/licenses/by/4.0), which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly credited. The Creative Commons Public Domain Dedication waiver (http://creativecommons.org/publicdomain/zero/1.0/) applies to the data made available in this article, unless otherwise stated.

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