Liu X, Zhang S, Qiu H, Xie ZQ, Tang WF, Chen Y, Wei X. Investigation of high-mobility group box 1 variants with lymph node status and colorectal cancer risk. World J Gastrointest Oncol 2025; 17(4): 102584 [DOI: 10.4251/wjgo.v17.i4.102584]
Corresponding Author of This Article
Sheng Zhang, Department of General Surgery, Changzhou Third People’s Hospital, No. 300 Lanling North Road, Changzhou 213001, Jiangsu Province, China. 13601507172@163.com
Research Domain of This Article
Oncology
Article-Type of This Article
Case Control Study
Open-Access Policy of This Article
This article is an open-access article which was selected by an in-house editor and fully peer-reviewed by external reviewers. It is distributed in accordance with the Creative Commons Attribution Non Commercial (CC BY-NC 4.0) license, which permits others to distribute, remix, adapt, build upon this work non-commercially, and license their derivative works on different terms, provided the original work is properly cited and the use is non-commercial. See: http://creativecommons.org/licenses/by-nc/4.0/
Xin Liu, Sheng Zhang, Department of General Surgery, Changzhou Third People’s Hospital, Changzhou 213001, Jiangsu Province, China
Hao Qiu, Laboratory Medicine, School of Medicine, Jiangsu University, Zhenjiang 212000, Jiangsu Province, China
Zhi-Qiang Xie, Department of Clinical Laboratory, Fujian Medical University Union Hospital, Fuzhou 350001, Fujian Province, China
Wei-Feng Tang, Department of Cardiothoracic Surgery, Nanjing Drum Tower Hospital, The Affiliated Hospital of Nanjing University Medical School, Nanjing 210000, Jiangsu Province, China
Yu Chen, Department of Medical Oncology, Fujian Cancer Hospital and Fujian Medical University Cancer Hospital, Fuqing 350014, Fujian Province, China
Xi Wei, Department of Pathology, Affiliated People’s Hospital of Jiangsu University, Zhenjiang 212002, Jiangsu Province, China
Author contributions: Zhang S designed the research study; Liu X, Zhang S, Qiu H, Xie ZQ, Tang WF, and Chen Y performed the research; Liu X, Wei X and Zhang S contributed new reagents and analytic tools; Liu X, Zhang S and Wei X analyzed the data and wrote the manuscript; All authors have read and approve the final manuscript.
Supported by the Major Project of Changzhou Science and Technology Bureau, No. CJ20220255.
Institutional review board statement: Fujian Medical University Ethics Review Committee approved the present study (No. KT2018-003-01).
Informed consent statement: Each subject signed an informed consent.
Conflict-of-interest statement: The authors declare that they have no conflict of interest.
STROBE statement: The authors have read the STROBE Statement-a checklist of items, and the manuscript was prepared and revised according to the STROBE Statement-a checklist of items.
Open Access: This article is an open-access article that was selected by an in-house editor and fully peer-reviewed by external reviewers. It is distributed in accordance with the Creative Commons Attribution NonCommercial (CC BY-NC 4.0) license, which permits others to distribute, remix, adapt, build upon this work non-commercially, and license their derivative works on different terms, provided the original work is properly cited and the use is non-commercial. See: https://creativecommons.org/Licenses/by-nc/4.0/
Corresponding author: Sheng Zhang, Department of General Surgery, Changzhou Third People’s Hospital, No. 300 Lanling North Road, Changzhou 213001, Jiangsu Province, China. 13601507172@163.com
Received: October 24, 2024 Revised: December 31, 2024 Accepted: January 22, 2025 Published online: April 15, 2025 Processing time: 152 Days and 21.4 Hours
Abstract
BACKGROUND
Accumulating studies indicated that maintain nuclei homeostasis was deemed to the protective factors for the occurrence of cancer. Thus, high-mobility group box 1 (HMGB1) might influence the risk and poorer prognoses of colorectal cancer (CRC).
AIM
This study was designed to investigate whether HMGB1 polymorphisms influence the risk and lymph node metastasis (LNM) of CRC.
METHODS
Firstly, we designed an investigation with 1003 CRC patients and 1303 cancer-free controls to observe whether HMGB1 rs1412125 T > C and rs1045411 C > T SNPs could influence the risk of cancer. Subsequently, we carried out a correlation-analysis to assess whether these SNPs could alter the risk of LNM.
RESULTS
The current investigation suggested a relationship of HMGB1 rs1412125 SNP with the increased susceptibility of CRC. In a subgroup analysis, our findings suggested that this SNP could enhance an occurrence of CRC in ≥ 61 years, non-drinker and body mass index < 24 kg/m2 subgroups. However, we found that there was null association between HMGB1 rs1412125 SNP and LNM, even in different CRC region. These observations were confirmed by calculating the power value (more than 0.8). The association of HMGB1 rs1045411 C > T SNP with CRC risk and LNM was not found in any compare.
CONCLUSION
This study highlights a possible association between HMGB1 rs1412125 polymorphism and the increased risk of CRC. In the future, more studies should be conducted to explore HMGB1 rs1412125 polymorphism in relation to CRC development.
Core Tip: To our knowledge, this study highlights a possible association between high-mobility group box 1 (HMGB1) rs1412125 polymorphism and the increased risk of colorectal cancer (CRC). In the future, more studies should be conducted to explore HMGB1 rs1412125 polymorphism in relation to CRC development.
Citation: Liu X, Zhang S, Qiu H, Xie ZQ, Tang WF, Chen Y, Wei X. Investigation of high-mobility group box 1 variants with lymph node status and colorectal cancer risk. World J Gastrointest Oncol 2025; 17(4): 102584
In China, colorectal cancer (CRC) was one of the most common digestive tract malignancies, with 376300 new CRC patients and 191000 CRC related deaths happened in 2015[1]. CRC was considered as a complex disease, which involved in the interactions of individuals’ genetic parts with many environmental factors. A number of gene loci were found to be correlated with the occurrence and development of CRC[2,3]. According to previous investigations, immune and inflammation might play important roles in the risk and progress of cancer[4-6]. Maintaining homeostasis of nuclei and normal immune were deemed to the protective factors for many malignancies[7,8].
Immune was implicated in a variety of physiological roles and pathological processes, involving in the pathogenesis of autoimmune disease, infectious disease and cancer[9-12]. As a case in point, the incidence of cervical cancer has been reduced after using the human papillomavirus vaccine[13]. High-mobility group box 1 (HMGB1) is a nonhistone DNA-binding protein with high conservation. HMGB1 consists of three domains: (1) A box of DNA-binding domain; (2) B box of DNA-binding domain; and (3) A C terminal with negative charge. In most cells, it can be found in nuclei. It was reported that HMGB1 acted as a DNA chaperone, which could maintain homeostasis of nuclei[14]. As well, HMGB1 was considered as a danger-associated molecular pattern molecule, which played a vital role in inducing inflammation[15-17]. Thus, HMGB1 played a vital role in the occurrence of cancer[18-20]. Of late, HMGB1 was considered as an angiogenesis-related gene. Kusume et al[21] reported that HMGB1 secreted by CRC tissue inhibited dendritic cells (DCs) and reduced the ability of anti-cancer immune. HMGB1 expression in CRC patients was associated with poorer prognoses for overall survival[22].
In the past five years, the relationship of HMGB1 rs1412125 T > C single nucleotide polymorphism (SNP) with the susceptibility of cancer has been explored[20,23-29]. However, the observations were conflicting rather than conclusive. Two meta-analysis have been conducted to clarify the potential association of HMGB1 rs1412125 T > C SNP with the risk of overall cancer. These meta-analyses have observed null association. The aim of this investigation was to address the possible relationship between HMGB1 rs1412125 T > C SNP and the risk of CRC more precisely.
A case-control study revealed that rs1045411 C allele in promoter region of HMGB1 gene was significantly correlated with the early pathologic T stage and pathologic N1 stage of prostate cancer[23]. Another investigation also found that lung cancer (LC) patients with chemotherapy carring HMGB1 rs1045411 C allele had a better overall survival[30]. Additionally, Hu et al[31] also found that the HMGB1 rs1045411 C allele reduced the risks of LC. However, a recent study reported that rs1045411 T allele might decrease the risk of urothelial cell carcinoma[20]. Lin et al[26] also found an association between rs1045411 T allele and a decrease the risk of oral squamous cell carcinoma. Off late, a meta-analysis suggested that HMGB1 rs1045411 C > T SNP might increase the occurrence of overall cancer[32]. Wang et al[28] reported that no significant difference were detected between HMGB1 rs1045411 C > T polymorphism and the risk of CRC. Thus, the association between HMGB1 rs1045411 C > T variant and CRC risk should be further studied.
First, we designed a case-control study to explore whether HMGB1 rs1412125 T > C and rs1045411 C > T SNPs could influence the risk of cancer. Subsequently, we conducted an analysis to assess whether HMGB1 rs1412125 T > C and rs1045411 C > T SNPs could affect the risk of lymph nodes metastasis (LNM).
MATERIALS AND METHODS
Study subjects
In this study, 1003 CRC and 1303 cancer-free controls were recruited from the Fujian Medical University Union Medical College (Fujian Province, China) and Nanjing Medical University Zhenjiang Clinical College (Jiangsu Province, China) between October 2014 and August 2017. All participants were local Chinese Han populations. CRC cases were confirmed via histological diagnosis. The controls were individuals without a history of cancer frequency-matched to CRC patients with regarding to sex and age (± 5 years) the same time period. When an interview conducted, a pre-structured questionnaire was used. Then, the data was obtained. Each subject signed an informed consent. Fujian Medical University Ethics Review Committee approved the present study (No. KT2018-003-01).
DNA extraction and genotyping
The genomic DNA was obtained by using DNA isolation kit (Promega, Madison, WI, United States). Before polymerase chain reaction (PCR) testing, it was kept at -80 °C. We used Nanodrop ND-1000 UV to check the quality of DNA. The concentrations and pure of these DNA sample were eligible for PCR test. A custom-by-design 48-Plex SNPscan Kit (Genesky Biotechnologies Inc., Shanghai, China) was used to analyze the genotypes of HMGB1 rs1412125 T > C and rs1045411 C > T SNPs[33]. To carry out a control for genotype test, 92 samples were selected randomly. Using the same PCR method, two authors conducted the genotype test without knowing the status of participants. The findings of original genotype test were not changed. Figure 1 and Figure 2 presented the genotypes of HMGB1 rs1412125 T > C and rs1045411 C > T, respectively.
The continuous variable was conducted by t-test and expressed as means ± SD. We used SAS 9.4 software for Windows (SAS Institute, Cary, North Carolina) to assess an association of HMGB1 rs1412125 T > C and rs1045411 C > T SNPs with the risk of CRC. Odds ratios (ORs) and 95% confidence intervals (CIs) were harnessed to assess the strength of association between HMGB1 SNPs and CRC susceptibility[34]. P value of Hardy-Weinberg equilibrium (HWE) test was performed by online software (https://ihg.gsf.de/cgi-bin/hw/hwa1.pl). The power value was also calculated by using a power and sample size program.
RESULTS
Study characteristics
In this study, 1003 cases with CRC and 1303 cancer-free subjects were recruited (Table 1). The mean age of the case group was 61.10 years. The SD of age was 12.17 years. The mean age and SD of the control group were 61.40 ± 9.61 years. In case group, we included 620 males and 383 females. While in control group, 801 males and 502 females were recruited. In these two groups, the terms of sex and age were full-matched (P ≥ 0.05). However, the items of drinking, smoking, and body mass index (BMI) were not matched (P < 0.05). These detailed data were summarized in our previous study[35].
Table 1 Distribution of selected risk factors and demographic variables in colorectal cancer cases and controls.
Variant distribution of HMGB1 rs1412125 T > C and rs1045411 C > T SNPs met HWE in control group (P > 0.05). Table 2 lists the SNP information for HMGB1 rs1412125 T > C and rs1045411 C > T loci. The successful ratio of analyzing the genotype was more than 95%.
Table 2 Data for high-mobility group box 1 rs1412125 T > C and rs1045411 C > T nucleotide polymorphisms.
Genotyped SNPs
Chromosome
Chr Pos (NCBI build 37)
Region
MAF for Chinese in database
MAF in our controls (n = 1303)
P value for HWE test in our controls
Genotyping method
Genotyping value (%)
HMGB1 rs1412125 T > C
13
31041595
5’flanking
0.24
0.24
0.064
SNPscan
98.87
HMGB1 rs1045411 C > T
13
31033232
3’UTR
0.20
0.20
0.862
SNPscan
98.87
Association of HMGB1 rs1412125 T > C and rs1045411C > T SNPs with CRC risk
Supplementary Table 1 summarizes raw data. Table 3 lists the number of allele and genotype for HMGB1 rs1412125 T > C and rs1045411 C > T SNPs. In overall comparison, findings of the current study showed that the HMGB1 rs1412125 T > C genotype frequencies were different among CRC patients and controls. An increased frequency of HMGB1 rs1412125 C allele related genotype was identified in CRC group. Compared to HMGB1 rs1412125 TT, subjects with HMGB1 rs1412125 CC genotype, had an increased 76% risk to CRC occurrence (P = 0.002). Additionally, in relation to HMGB1 rs1412125 TT, HMGB1 rs1412125 TC/CC was a risk factor for CRC occurrence (P = 0.029). Compared to HMGB1 rs1412125 TT/TC, subjects with HMGB1 rs1412125 CC genotype had an increased 67% risk to CRC occurrence (P = 0.003). When risk factors were adjusted, an increased risk of CRC occurrence was also recognized (P = 0.002, 0.032 and 0.005, respectively). However, the association of HMGB1 rs1045411 C > T SNP with CRC occurrence was not found in overall compare (Table 3).
Table 3 Logistic regression analyses of associations between high-mobility group box 1 rs1412125 T > C polymorphisms and colorectal cancer risk.
Association of HMGB1 rs1412125 T > C and rs1045411 C > T SNPs with CRC risk in a stratified analysis
We conducted the stratification analyses to determine a potential relationship between HMGB1 rs1412125 and the risk of CRC. Table 4 summarized the results of those analyses (homozygote model: Female subgroup: Adjusted P = 0.043; Male subgroup: Adjusted P = 0.015; ≥ 61 years subgroup: Adjusted P = 0.003; BMI < 24 kg/m2 subgroup: Adjusted P = 0.006; Never drinking subgroup: Adjusted P = 0.002 and never smoking subgroup: Adjusted P = 0.007; Recessive model: Male subgroup: Adjusted P = 0.027; ≥ 61 subgroup: Adjusted P= 0.004; Never smoking subgroup: Adjusted P = 0.012; Never drinking subgroup: Adjusted P = 0.004 and BMI < 24 kg/m2 subgroup: Adjusted P = 0.008).
Table 4 Stratified analyses between high-mobility group box 1 rs1412125 T > C and colorectal cancer risk by sex, age, body mass index, smoking status and alcohol consumption.
In this study, we also conducted the stratification analyses to assess the relationship of HMGB1 rs1412125 T > C variant with susceptibility of different CRC subtype. We identified that HMGB1 rs1412125 T > C SNP increased the occurrence of CRC even in different CRC region.
In this study, the relationship of HMGB1 rs1045411 C > T SNP with CRC risk was not found in any subgroup analysis (Table 5 and Table 6).
Table 5 Stratified analyses between high-mobility group box 1 rs1045411 C > T polymorphism and colorectal cancer risk by sex, age, body mass index, smoking status and alcohol consumption.
Relationship between HMGB1 rs1412125 T > C and rs1045411 C > T SNPs and LNM
In the current investigation, a total of 1003 CRC cases were recruited to evaluate a correlation between HMGB1 rs1412125 T > C SNP and LNM. After reviewed the medical history of patients, 518 CRC cases were diagnosed with LNM. Table 7 lists the distribution of HMGB1 rs1412125 T > C genotypes. There was null relationship of rs1412125 T > C variant with LNM. Additionally, we did not find any association of rs1412125 T > C with LNM even in different CRC subtype (Table 8).
Table 7 Logistic regression analyses of association between high-mobility group box 1 single nucleotide polymorphisms and lymph node status of colorectal cancer patients.
Table 8 Logistic regression analyses of association between high-mobility group box 1 single nucleotide polymorphisms and lymph node status of colorectal cancer in different region.
In the present investigation, the relationship of rs1045411 C > T with LNM was found neither in overall compare nor in different subgroup analysis (Table 7 and Table 8).
Power of the current investigation
The Type I error probability for a two sided test was used the following criterion: Α = 0.05. For HMGB1 rs1412125 T > C SNP, the power value was 0.890 in CC vs TT and 0.842 in CC vs TC/TT among overall comparison, 0.809 in CC vs TT among BMI < 24 kg/m2 subgroup, 0.864 in CC vs TT and 0.824 in CC vs TC/TT among non-drinker subgroup and 0.889 in CC vs TT and 0.872 in CC vs TC/TT among ≥ 61 years subgroup. The power value of other overall and subgroup comparisons was less than 0.8 (data not shown). These results indicated that HMGB1 rs1412125 T > C SNP could be a risk factor of CRC occurrence in non-drinker, ≥ 61 years and BMI < 24 kg/m2 subgroups and overall comparison.
DISCUSSION
HMGB1 is a member of angiogenesis-associated genes. Of late, it was identified that HMGB1 might correlate with CRC development[36-38]. In CRC patients, it was regarded as a potent cytokine of pro-angiogenesis which led to vascular endothelial growth factor (VEGF) secretion. In addition, VEGF was considered as a vital regulating role for CRC occurrence and progress. Thus, the consequential correlation suggested that HMGB1 could promote the angiogenesis process of CRC[39]. Via the HMGB1/receptor of advanced glycation endproducts/nuclear factor-kappa B (NF-κB) pathway, HMGB1 could also facilitate the cellular proliferation and metastasis of cancer[40,41]. A number of evidences indicated an important affect of individuals’ genetic factors in assessing the possible susceptibility for the occurrence and development of cancer. Thus, we explored an association of rs1412125 T > C and rs1045411 C > T variants with CRC risk in a larger sample sizes study. To our knowledge, this case-control study firstly confirmed that HMGB1 rs1412125 T > C SNP could increase the risk of CRC in China.
Rs1412125 T > C was a common SNP in 5’-flanking of HMGB1 gene, which was a functional region for regulation. A previous study suggested that the HMGB1 rs1412125 T > C SNP could influence the efficacy of platinum-based treatment in patients with LC[42]. Recently, a case-control study focused on a relationship of HMGB1 rs1412125 T > C with the CRC occurrence[28]. However, due to the limited sample sizes, the association of HMGB1 rs1412125 T > C SNP with the risk of CRC was unconfirmed. Li et al[43] conducted a pooled-analysis to identify a potential association of HMGB1 rs1412125 T > C SNP with the risk to cancer development. In the meta-analysis mentioned above, nine case-control studies with 4865 cancer cases and 4639 controls were involved for analysis. Although the association of HMGB1 rs1412125 T > C SNP with the risk to cancer development was unconfirmed. This meta-analysis suggested that HMGB1 rs1412125 T > C SNP had a tendency of increased susceptibility to overall cancer (OR: 1.16, 95%CI: 0.98-1.38). The plausible outcome might be due to small sample sizes. The current investigation, in overall comparison, have suggested that HMGB1 rs1412125 T > C SNP could increase a susceptibility of CRC. In a subgroup analysis, our findings also found that HMGB1 rs1412125 T > C SNP could enhance an occurrence of CRC in BMI < 24 kg/m2, non-drinker and ≥ 61 years subgroups. These observations were confirmed by calculating the power value (> 0.8). Based on the related large sample sizes included, these conclusions for the relationship between HMGB1 rs1412125 T > C SNP and the susceptibility of CRC may be more credible. In the future, more investigations are needed to confirm these associations.
The HMGB1 rs1045411 C > T SNP was also frequently explored the association of this polymorphism with cancer risk. Supic et al[44] first reported that HMGB1 rs1045411 C > T SNP was not associated with risk of oral squamous cell carcinoma. In addition, the association of HMGB1 rs1045411 C > T with CRC development was also irrelevant[28]. However, several case-control study indicated that this SNP was associated with the risk of cancer[20,26,31,45]. Therefore, in the future, the relationship of HMGB1 polymorphism with susceptibility to malignancy should be further investigated.
Luo et al[46] reported that HMGB1 could promote re-growth and metastasis of malignancy cells. A previous study suggested that over-expression of HMGB1 might be associated with a shorter overall survival time in CRC[47]. In colon cancer patients, Li et al[48] found that HMGB1 could be implicated in lymphangiogenesis and LNM via the HMGB1/VEGF/NF-κB pathway. Additionally, HMGB1 could suppress DCs in CRC cases[21]. HMGB1 disturbed host anti-cancer immunity and then increased the susceptibility of LNM[21]. In the current investigation, 1003 CRC cases were recruited to evaluate a correlation between HMGB1 two SNPs and the risk of LNM. However, we found that HMGB1 rs1412125 T > C and rs1045411 C > T SNP could not influence the risk of LNM. The possible explanation might be the moderate sample sizes in different subgroup. In the future, this issue should be explored with more studies.
There are some merits and limitations in our study. Firstly, this investigation was designed as a larger sample sizes study. Secondly, the sex and age were full-matched in this case-control study. Several limitations were related to bias of selection and included insufficient susceptibility factors. This study was designed as hospital-based, which could result in selection bias. For lack of data, we could not deduce the potential interaction of HMGB1 rs1412125 T > C and rs1045411 C > T SNPs with lifestyles. Finally, in this investigation, only two HMGB1 SNPs were included for study. However, other SNPs in HMGB1 gene should not been ignored. And the interaction of HMGB1 rs1412125 T > C and rs1045411 C > T SNPs with other HMGB1 SNPs also should be considered.
CONCLUSION
To the best of our knowledge, this case-control study first confirms the possible relationship of HMGB1 rs1412125 T > C polymorphism with an increased susceptibility of CRC. In the future, more studies should be conducted to explore this SNP in relation to CRC development.
ACKNOWLEDGEMENTS
We appreciate all subjects who participated in this study. We wish to thank Dr. Liu Y for technical support.
Footnotes
Provenance and peer review: Unsolicited article; Externally peer reviewed.
Peer-review model: Single blind
Specialty type: Oncology
Country of origin: China
Peer-review report’s classification
Scientific Quality: Grade B, Grade B, Grade C
Novelty: Grade B, Grade B, Grade C
Creativity or Innovation: Grade B, Grade C, Grade C
Scientific Significance: Grade B, Grade B, Grade B
P-Reviewer: Hussain S; Tao Y S-Editor: Fan M L-Editor: A P-Editor: Zhang L
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