Comprehensive analysis of the correlation between base‑excision repair gene SNPs and esophageal squamous cell carcinoma risk in a Chinese Han population
- Authors:
- Published online on: June 9, 2020 https://doi.org/10.3892/mco.2020.2066
- Pages: 228-236
Abstract
Introduction
Esophageal cancer (EC) is a common and often fatal cancer which has two main histological subtypes: Esophageal squamous cell carcinoma (ESCC) and esophageal adenocarcinoma (EA). More than 90% of EC cases in China are of the ESCC subtype (1). The development of ESCC is influenced by myriad genetic and environmental factors, with the latter being known to include alcohol and tobacco use, malnutrition, and exposure to nitrosamine carcinogens (2-5). Prior studies (6-8) have identified a large number of single nucleotide polymorphisms (SNPs) that are related to ESCC incidence. Mutations related to DNA damage repair pathway in particular have been found to be closely related to this form of cancer. The DNA damage repair system plays an important role in maintaining the stability of genomic DNA and preventing oncogenesis. Base excision repair (BER) is one of the primary pathways used to repair DNA damage caused by reactive oxygen species and other electrophiles, and as such, BER genes are good candidate susceptibility genes for ESCC.
The key BER pathway genes include 8-oxoguanine glycosylase-1 (OGG1), AP endonuclease-1 (APE1), and X-ray repair cross-complementing-1 (XRCC1), and as a result, several studies have assessed the relationship between SNPs in these genes, cancer development, and patient chemotherapeutic resistance (2,3,9-17). Whether the XRCC1 Arg399Gln and OGG1 Ser326Cys polymorphisms are associated with risk of ESCC development, however, remains a matter of controversy (2,3,9-15). In some reports, these two mutations were found to be linked with such risk (2,3,9,18,19), whereas other studies detected no such relationship for these genes (11-15,20,21). Furthermore, how the APE1-141T/G polymorphism or how these four SNPs (APE1 Asp148Glu and -141T/G, OGG1 Ser326Cys, and XRCC1 Arg399Gln) synergistically impact ESCC risk remains uncertain.
As no studies to date have firmly established the relationship between these BER gene SNPs and ESCC risk in a Han Chinese population, the present study was designed to comprehensively analyze this topic of research.
Patients and methods
Patients and control group
This was a case-control study, approved by The Daping Hospital Ethics Committee with all participants providing informed consent. In total, we consecutively recruited 642 cancer-free control patients (296 females, 346 males; mean age: 51.7 years) and 321 patients with newly-diagnosed ESCC (51 females, 270 males; mean age: 61.9 years) at Daping Hospital, Third Military Medical University (Chongqing, China) from January 2008 to December 2012, with all participants declaring themselves as being of Han Chinese ethnicity, and with no sex or age restrictions being imposed during recruitment. Table I summarizes the general characteristics of these two populations. All ESCC patients were newly diagnosed with the disease based on pathological findings and were undergoing outpatient treatment at this hospital. The control group were those that had undergone health examinations at the Health Examination Center of this hospital during the same period. Patients were excluded from the present study if they met any of the following criteria: i) Non-Han ethnicity; ii) history of previous cancers and iii) history of treatment via radio - or chemotherapy.
 | Table I.Distribution of demographic characteristics of esophageal squamous cell carcinoma case and control participants. |
In a questionnaire administered to all study participants, a family history of cancer was defined as any reports of cancer affecting first-degree relatives (children, siblings, or parents). With respect to alcohol consumption, anyone consuming 10 gr alcohol/day for >1 year was considered to be exposed to alcohol, while all other participants were considered to be non-drinkers or to be formerly exposed to alcohol if they had abstained from alcohol consumption for at least 1 year. With respect to smoking status, current smokers were those who reported partaking of a minimum of one cigarette per day for >1 year. Former smokers were those reporting to have deliberately abstained from smoking for at least 1 year, while all other participants were non-smokers.
Blood sample processing
EDTAK2 anticoagulant tubes were used to collect samples of venous blood from the antecubital vein of each study participant. These samples were immediately centrifuged for 10 minutes at 670.8xg at 4oC in order to facilitate serum removal. The peripheral blood leukocytes were then collected, and gDNA extraction was performed using an EZNASE Blood DNA kit (Omega Bio-Tek Inc.), with samples being stored at -80˚C.
SNPs selection and genotyping
The four non-synonymous BER gene SNPs selected for genotyping in the present study included: rs1130409 (APE1 exon 5; Asp148Glu; T/G), rs1760944 (APE1 promoter polymorphism; -141T/G), rs1052133 (OGG1 exon 7; Ser326Cys; C/G) and rs25487 (XRCC1 exon 10; Arg399Gln; G/A). BER gene SNP genotyping was conducted via the use of PCR-RFLP for these patient and non-patient samples, as previously described (22). For each allele, primer pairs and product lengths were specifically selected such that alleles could be identified according to product length. GenBank reference sequences were used to guide primer design, with the resultant primers being shown in Table II. Replication of genotyping results was not performed.
Each PCR reaction was conducted in a 25 µl total volume that contained 2 µl gDNA, 1 µl primers, 12.5 µl Go Taq MIX (2x) for each of the four primers, and 6.5 µl dH2O. Thermocycler settings were: 95˚C for 10 min; 30 cycles of 95˚C for 1 min, 60˚C (APE1 Asp148Glu), 58˚C (APE1-141T/G), 66˚C (XRCC1 Arg399Gln), or 64˚C (OGG1Ser326Cys) for 1 min, and 72˚C for 1 min. Agarose gel electrophoresis was then used to analyze the resultant PCR products.
Statistical analysis
SPSS 19.0 (IBM, Corp.) was used for all statistical testing. Only participants with complete demographic information pertaining to age, sex, and alcohol intake/smoking status were included in the present analysis. Ultimately, 642 non-affected participants and 321 ESCC patients were analyzed. We then further utilized a propensity score matching (PSM) analysis in order to balance out baseline differences between these two participant groups. This PSM analytical approach employed a 1:1 matching strategy, with 311 cases being successfully matched. This propensity model included age, sex, smoking status, alcohol intake, and family history of cancer when matching participants. Differences in these demographic variables and in SNP frequencies between groups were compared via Pearson χ2 tests, and Hardy-Weinberg equilibrium for each SNP was additionally tested. Unconditional logistic regression was undertaken to estimate odds ratios (OR) and 95% CIs were estimated following PSM via unconditional logistic regression analysis. A two-sided P<0.05 was considered to indicate a statistically significant difference.
Results
General information
For the present study, we recruited 963 total participants of Han Chinese ethnicity, including 642 cancer-free individuals and 321 ESCC patients, with study population characteristics being shown in Table I. There were significant differences between the control and cancer patient populations with respect to participant age, sex, and smoking status prior to PSM. There were significantly more participants that were male (59.2 vs. 37.4%), 60+ years old (84.1 vs. 53.9%), or smokers (57.4 vs. 35.8%) in the ESCC group relative to the control group. After the PSM analysis, 622 matched subjects were included in the following analyses (n=311/group). Following PSM, there were no significant differences between case and control groups with respect to participant age, sex, smoking status, alcohol intake, or family history of cancer, thus confirming the comparability of these groups.
Association between BER polymorphisms in XRCC1, OGG1, APE1 and ESCC risk
APE1 (141T/G; Asp148Glu), OGG1 (Ser326Cys), and XRCC1 (Arg399Gln) genotypes and allele frequency distributions in the control group were all consistent with those predicted according to Hardy-Weinberg equilibrium (Table III; P>0.05).
| Table IIIObserved and expected genotypic frequencies of each single nucleotide polymorphism in the control group. |
Prior to PSM, no significant relationship between APE1 Asp148Glu, APE1-141T/G, or OGG1 Ser326Cys and ESCC risk was detected, while a significant relationship was detected between XRCC1 Arg399Gln and ESCC risk (Table IV). However, following PSM there was no significant relationship between these four BER SNPs and ESCC risk (Table V), with this same lack of significance being observed in a recessive model (Table VI) and a dominant model (Table VII).
| Table IVDistribution of genotypes and OR determined for esophageal squamous cell carcinoma cases and controls before propensity matching. |
| Table VDistribution of genotypes and OR determined for esophageal squamous cell carcinoma cases and controls after propensity matching. |
| Table VIAssociation between esophageal squamous cell carcinoma risk and the single nucleotide polymorphism variant of the base-excision repair gene in the recessive model. |
| Table VIIAssociation between esophageal squamous cell carcinoma risk and the single nucleotide polymorphism variant of the base-excision repair gene in the dominant model. |
Associations between gene-gene interactions for four SNPs and ESCC risk
We additionally sought to test whether there were any associations between gene-gene interactions for these four SNPs and ESCC risk (Table VIII). As very few individuals contained all 6 of these risk alleles in a recessive model, individuals with 5 or 6 of these genotypes were pooled for analysis. Finally, no significant correlation was found between SNP-SNP interactions and individual susceptibility to ESCC in either a recessive or a dominant model.
| Table VIIIJoint pathway analysis of base-excision repair polymorphisms in esophageal squamous cell carcinoma risk using a dominant genetic model and recessive model. |
Discussion
In China, esophageal cancer is the fourth most common cancer-associated cause of death, with 477,900 newly diagnosed cases in 2015 alone, including 157,200 cases in females and 320,800 in males (23). Indeed, males are more likely to be affected by this disease than are females, consistent with the results of the present study in which a significantly higher number of males than females were affected by ESCC in the study population. Several environmental factors have been associated with esophageal cancer risk, including malnutrition, Barrett's esophagus, exposure to nitrosamine carcinogens, smoking, and alcohol consumption (4,5). However, exposure to these factors alone is not sufficient to determine whether or not a given individual develops ESCC, and genetic factors thus also play a role in the etiology of this disease. As such, in the present study we assessed whether four BER gene SNPs (APE1 Asp148Glu, APE1-141T/G, OGG1 Ser326Cys, and XRCC1 Arg399Gln) were related with ESCC risk in a Han Chinese population.
XRCC1 is a key BER gene encoded on chromosome 19q13.2, q13.3 with 17 exons. XRCC1 plays a key role in mediating the repair of single-stranded DNA breaks as part of the BER pathway, with SNPs in this gene having the potential to alter or compromise protein functionality (3,19,24,25). Mutations in XRCC1 have been linked with many different cancer types, including hepatocellular carcinoma, thyroid carcinoma, nasopharyngeal carcinoma, and lung, bladder, gastric, and cervical cancers (16,26-32). Previous studies have focused largely on three different XRCC1 polymorphisms when assessing their relationship with esophageal cancer risk, including Arg280His, Arg194Trp, and Arg399Gln (3,11,13,33). These studies have, however, yielded inconsistent results regarding whether the XRCC1 Arg399Gln SNP was associated with esophageal cancer risk (2,3,9-14). In a meta-analysis, the XRCC1 Arg399Gln SNP was found to be linked with elevated EC risk in a Chinese population, with this association being strongest for the ESCC subtype (2,3). However, other studies failed to detect any significant association between this SNP and EC risk using a variety of genetic models (11,13,20,21). These differing results may stem from differences in sample size, lifestyle, environmental factors, or geographic distributions between studies. In addition, PSM was not conducted in all of these prior studies as a means of controlling for potential confounding. In the present study, we did detect a significant relationship between XRCC1 Arg399Gln and ESCC risk prior to but not after PSM, suggesting that the impact of this XRCC1 SNP on ESCC risk may not only be related to its defective role in BER, but also to the hampering other intracellular processes (34,35).
OGG1 is an additional BER gene encoded on chromosome 3p26, and it has also been proposed to play a role in the transcriptional regulation of genes associated with inflammation and DNA repair, suggesting that OGG1 may contribute to carcinogenesis (36-38).Given this role, it is perhaps unsurprising that the OGG1 Ser326Cys SNP has been studied in the context of cancer risk in many different studies, although the conclusions of these studies were somewhat variable (39-41). A more recent meta-analysis that included 152 case-control studies suggested that these inconsistent results may have arisen due to differences in cancer type, sample size, and control participant sources (40). This meta-analysis ultimately failed to detect any significant relationship between the OGG1 Ser326Cys SNP and cancer risk, which was consistent with the lack of such an association detected in our present study.
APE1 functions as an important mediator of DNA repair and other cellular homeostatic processes, defects in which are linked to the development and progression of cancer (42). Several APE1 SNPs have been detected to date (43), including two functional SNPs (rs1760944: -656 T>G in the promoter region; and rs1130409 1349 T>G in exon 5) (44). APE1 SNPs have been suggested to be associated with cancer susceptibility in previous epidemiological studies. For example, when patients were stratified according to cancer type in a meta-analysis the Asp148Glu APE1 SNP was linked with prostate cancer risk (45). However, a separate meta-analysis detected no significant relationship between APE1 Asp148Glu and digestive cancer (46). A further meta-analysis that included 6136 controls and 4856 cancer patients failed to detect any significant relationship between Asp148Glu and the risk of esophageal and colorectal cancer risk in any genetic model. Other studies have similarly detected no such relationship between Asp148Glu and EC risk (10,15). This was consistent with the results of our present study, which similarly found APE1 Asp148Glu to be unrelated to ESCC risk in any genetic model.
Overall, the findings from the present study suggest that being male, being 60 years of age or older, and being a smoker are each associated with elevated ESCC risk. However, we did not detect any significant relationship between the four tested BER SNPs (APE1 Asp148Glu, APE1-141T/G, OGG1 Ser326Cys, and XRCC1 Arg399Gln) and ESCC risk in this Chinese Han population. The results of this analysis will require further confirmation in an independent and larger cohort in order to better understand the genetic basis for ESCC risk.
In light of the important role that smoking and drinking status play in the development of ESCC, the absence of any gene-environment interaction or stratified analyses represent potential limitations of our study. In addition, f haplotype analysis for the two APE1 SNPs is required. Moreover, the limited sample size and potential resulting lack of statistical power in this study may have limited our ability to resolve meaningful phenotypes.
Acknowledgements
Not applicable.
Funding
No funding was received.
Availability of data and materials
The datasets used and/or analyzed during the current study are available from the corresponding author on reasonable request.
Authors' contributions
YP and LZ designed the research and analyzed the patient data, and drafted the manuscript. ND interpreted the results. MX was involved in study conception and design, analysis and interpretation of the results, and critical revision. All authors read and approved the final manuscript.
Ethics approval and consent to participate
The present study conformed to the Clinical Research Guidelines and was approved by the Ethics Committee of Daping Hospital (Chongqing, China). Informed consent was obtained from all patients.
Patient consent for publication
Not applicable.
Competing interests
The authors declare that they have no competing interests.
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