Correlation of DEPDC5 rs1012068 and rs5998152 Polymorphisms with Risk of Hepatocellular Carcinoma: A Systematic Review and Meta-Analysis

Zhu, Shaoliang; Tang, Zhenyong; Zou, Mengjie; Tan, Tingting; Tang, Yi; Chen, Yuanyuan; Liang, Bin; Xie, Dongyi; Yang, Yongyu; Xie, Shaowei; Xie, Guangyuan; Dong, Xiaofeng; Liu, Tianqi; Tang, Yuntian; Yang, Jianrong

doi:https://doi.org/10.1155/2023/5957481

Journal of Oncology

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Abstract Introduction Materials and Methods Results Discussion Data Availability Conflicts of Interest Authors’ Contributions Supplementary Materials References Copyright Related Articles

Review Article | Open Access

Volume 2023 | Article ID 5957481 | https://doi.org/10.1155/2023/5957481

Correlation of DEPDC5 rs1012068 and rs5998152 Polymorphisms with Risk of Hepatocellular Carcinoma: A Systematic Review and Meta-Analysis

Shaoliang Zhu,¹Zhenyong Tang,¹Mengjie Zou,²Tingting Tan,¹Yi Tang,¹Yuanyuan Chen,¹Bin Liang,¹Dongyi Xie,¹Yongyu Yang,¹Shaowei Xie,¹Guangyuan Xie,¹and Xiaofeng Dong¹ et al.

Academic Editor: Alessandro Granito

Received07 Oct 2022

Revised23 Dec 2022

Accepted04 Jan 2023

Published24 Jan 2023

Abstract

Background. Emerging evidence has shown that two common genetic polymorphisms within the pleckstrin domain-containing protein 5 (DEPDC5), rs1012068 and rs5998152, may be associated with the risk of hepatocellular carcinoma (HCC), especially in those individuals chronically infected with the hepatitis C virus (HCV) or the hepatitis B virus (HBV). However, these findings have not been consistently replicated in the literature due to limited sample sizes or different etiologies of HCC. Thus, the present systematic review and meta-analysis were performed to resolve this inconsistency. Methods. The databases PubMed, Embase, Web of Science, the China National Knowledge Infrastructure, and Scopus were searched up to December 12, 2022. Data from relevant studies were pooled, and odds ratios and 95% confidence intervals were calculated. Results. A total of 11 case-control studies encompassing 2,609 cases and 8,171 controls on rs1012068 and three encompassing 411 cases and 1,448 controls on rs5998152 were included. Results indicated that the DEPDC5 rs1012068 polymorphism did not significantly increase HCC risk in the total population (allelic model (OR = 1.32, 95% CI = 1.04–1.67, = 0.02); the recessive model (OR = 1.42, 95% CI = 0.96–2.10, = 0.08); the dominant model (OR = 1.43, 95% CI = 1.09–1.87, = 0.01); the homozygous model (OR = 1.61, 95% CI = 1.01–2.57, = 0.05); the heterozygous model (OR = 1.39, 95% CI = 1.09–1.79, = 0.009)). Subgroup analyses based on ethnicity and etiology revealed that the rs1012068 polymorphism, under all five genetic models, was associated with increased HCC risk in Asians or in individuals with chronic HBV infection but not in individuals with chronic HCV infection. A significant association was also observed between rs5998152 and HCV-related HCC risk in Asians chronically infected with HCV under allelic, dominant, and heterozygous models. Conclusion. Our study suggests that the DEPDC5 rs1012068 polymorphism increases HCC risk, especially in Asians with chronic HBV infection, while the rs5998152 polymorphism increases HCC risk in Asians with chronic HCV infection.

1. Introduction

Liver cancer is the fifth most common cancer and the fourth leading cause of cancer-related death worldwide. Among men, it is the fourth most frequent cancer and the second leading cause of cancer-related deaths [1]. Hepatocellular carcinoma (HCC) accounts for 75%–85% of cases of primary liver cancer worldwide [2]. The main risk factors for HCC are chronic infection with the hepatitis B virus (HBV) or hepatitis C virus (HCV), aflatoxin-contaminated foods, heavy alcohol intake, excess body weight, type 2 diabetes, and smoking. Besides these etiological factors, increasing evidence has revealed that host genetic variations, including single-nucleotide polymorphisms (SNPs), might also play a role in HCC development and progression.

Pleckstrin domain-containing protein 5 (DEPDC5) has been implicated in focal epilepsy, brain malformation, and sudden unexplained death in epilepsy [3–5]. DEPDC5 may be a target to treat epilepsy because it negatively regulates amino acid sensing through the signaling pathway involving the mammalian target of rapamycin complex 1 (mTORC1) [6, 7]. DEPDC5 also negatively regulates the AKT-mTORC1 pathway, so its agonists may be useful against the activation of latent HIV-1 infection [8]. DEPDC5 may participate in a signaling pathway in which Pim1 and Akt act via mTORC1 to promote the proliferation and survival of cancer cells [9]. Downregulation of DEPDC5 leads to upregulation of matrix metalloprotease 2 through the β-catenin pathway, which may contribute to HCV-related fibrosis [10]. Such downregulation also renders HCC tumors more resistant to reactive oxygen species under the leucine-depleted conditions of chronic liver disease, contributing to poor patient outcomes [11].

In addition to these associations between DEPDC5 and various diseases, polymorphisms in the DEPDC5 gene have been linked to the risk of HCC [12–23]. A genome-wide association study first demonstrated that the DEPDC5 variant rs1012068 could increase HCC risk in individuals with chronic HCV infection [12], and this relationship was replicated in several studies [15, 18, 20]. On the other hand, several studies did not find such a relationship [9, 14, 18]. Similarly, some studies found a significant association between rs1012068 and the risk of HBV-related HCC [13, 16], while another study failed to detect this relationship [14].

These contradictory results may reflect the relatively small samples in individual studies, heterogeneity among control populations, and different HCC etiologies. We conducted the present systematic review and meta-analysis to clarify the relationship of DEPDC5 polymorphisms rs1012068 and rs5998152 with HCC risk. We also performed subgroup analyses based on ethnicity and the etiology of HCC.

2. Materials and Methods

2.1. Search Strategy

This meta-analysis complied with “Preferred Reporting Items for Systematic Reviews and Meta-Analyses” (PRISMA) guidelines [24]. A comprehensive search for relevant studies was performed in the PubMed, Embase, Web of Science, Chinese National Knowledge Infrastructure, and Scopus databases from their inception through December 12, 2022. The following terms were used: “genetic polymorphism” or “single-nucleotide polymorphism” or “polymorphism” or “SNP” or “mutation” or “variation” or “variant,” or “liver tumor” or “liver cancer” or “hepatocellular carcinoma” or “liver neoplasms,” and “DEP domain containing 5” or “DEPDC5” or “rs1012068” or “rs5998152.” There were no language restrictions. Additional studies were identified through manual searching of references in original or review articles on this topic. If there was a duplication of published literature by the same research group, the study with the larger sample was selected. Any disagreements were resolved by discussion.

2.2. Inclusion and Exclusion Criteria

2.2.1. Inclusion Criteria

(a)The study cohorts included DEPDC5 rs1012068 and rs5998152 polymorphisms in patients with HCC(b)Histological features were assessed by liver biopsy, and diagnostic criteria were clearly stated(c)Unrelated case-control studies were included(d)If two (or more) studies included the same cohort, only the most recent was included(e)Sufficient data for estimating odds ratios (ORs) and 95% confidence intervals (CIs) on the HCC risk were reported or could be calculated

2.2.2. Exclusion Criteria

(a)The source of cases was unclear(b)No clear diagnostic criteria for HCC were described(c)The study was a duplicate publication(d)The study was a review, meta-analysis, comment, or conference abstract(e)Genotyping data were not reported in sufficient detail

2.3. Data Extraction

The data from the included studies were extracted by two independent investigators. Discrepancies during data extraction were resolved by a third investigator. The extracted information included the first author’s surname, publication year, country in which the study was conducted, ethnicity, cohort characteristics of the cases and controls, the total number of patients in the case and control groups, the number of subjects with each genotype, and matched parameters between cases and controls.

2.4. Assessment of Methodological Quality

Quality assessments of the eligible studies were performed using the Newcastle–Ottawa Scale (NOS) [25]. The NOS involves a total of 9 items, each of which has a score that ranges from 1 to 9. A NOS score of 5 points or above would be classified as a high-quality study, while a NOS score of 4 points or below would be classified as a poor-quality study [26].

2.5. Statistical Analysis

The unadjusted odds ratio (OR) and 95% confidence interval (CI) were used to assess the correlation of DEPDC5 rs1012068 and rs5998152 polymorphisms with the risk of HCC based on the genotype frequencies in cases and controls. The Z test was used to evaluate the significance of the association, with < 0.05 considered significant. When > 0.10 for the Q test, meta-analysis was performed using a fixed-effect model, indicating the absence of heterogeneity among studies; otherwise, a random-effect model was used. Review Manager 5.3 (Cochrane Collaboration) was used for all statistical tests for meta-analyses. Begg’s funnel plot and Egger’s linear regression in Stata 12.0 software (Stata Corp., College Station, TX, USA) were used to evaluate publication bias, with < 0.05 considered significant.

3. Results

3.1. Characteristics of Primary Studies

The flowchart of study selection is summarized in Figure 1, and search strategies for each database are presented in Table S1. After a comprehensive search of the databases using the search strategies in Table S1, 54 relevant studies were compliant with the search strategy, of which 28 were excluded due to being duplicates. Another 11 were omitted after screening titles and abstracts. Among the 15 studies remaining, one was a case-only study [27], one investigated fibrosis but not HCC [10], and two were based on the same participants [19, 28]. Eventually, 12 studies were included in the current meta-analysis (Table 1). No relevant case-control studies were identified based on the alternative polymorphism IDs for rs1012068 (rs56511012, rs58339834, rs386510025) or for rs5998152 (rs61578881, rs8143107).

A total of 11 studies [12–22] investigated rs1012068, and 3 studies [12, 15, 23] investigated rs5998152. The distribution of genotypes in controls was consistent with Hardy-Weinberg equilibrium (HWE). The average NOS score of the 12 case-control studies was 7.09 points (ranging from 6 to 8 points), which suggested that the methodological quality of the 12 studies was generally adequate.

3.2. Quantitative Data Synthesis

3.2.1. rs1012068 and HCC Risk

As shown in Table 2 and Figure S1, a meta-analysis based on a population of 2,609 cases and 8,171 in 11 studies [12–22] revealed that the rs1012068 polymorphism did not significantly increase HCC risk in total under the allelic model (OR = 1.32, 95% CI = 1.04–1.67, = 0.02); the recessive model (OR = 1.42, 95% CI = 0.96–2.10, = 0.08); the dominant model (OR = 1.43, 95% CI = 1.09–1.87, = 0.01); the homozygous model (OR = 1.61, 95% CI = 1.01–2.57, = 0.05); or the heterozygous model (OR = 1.39, 95% CI = 1.09–1.79, = 0.009).

A meta-analysis based on ethnicity for the subgroup of 2,297 Asian cases and 4,801 Asian controls in 8 studies [12, 14–20] showed that the rs1012068 polymorphism significantly increased HCC risk in Asians (Table 2; Figure 2) under the allelic model (OR = 1.56, 95% CI = 1.22–1.99, < 0.001); the recessive model (OR = 1.82, 95% CI = 1.43–2.30, < 0.001); the dominant model (OR = 1.67, 95% CI = 1.26–2.22, = 0.004); the homozygous model (OR = 2.21, 95% CI = 1.42–3.43, < 0.001); and the heterozygous model (OR = 1.57, 95% CI = 1.20–2.04, < 0.001). Subgroup analysis in Caucasian populations was not performed because only two studies reported such data.

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(b)

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Then, we conducted a meta-analysis based on the etiology of HCC, in which both cases and controls were chronically infected with HBV. Results for the subgroup of 936 cases and 1,021 controls in 3 studies [14, 16, 19] showed that the rs1012068 polymorphism significantly increased HCC risk in individuals with chronic HBV infection (Table 2; Figure 3) under the allelic model (OR = 1.34, 95% CI = 1.16–1.54, < 0.001); the recessive model (OR = 1.62, 95% CI = 1.16–2.26, = 0.004); the dominant model (OR = 1.39, 95% CI = 1.16–1.66, < 0.001); the homozygous model (OR = 1.82, 95% CI = 1.29–2.56, < 0.001); and the heterozygous model (OR = 1.31, 95% CI = 1.08–1.59, = 0.005).

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Figure 3

Forest plot showing the relationship between DEPDC5 rs1012068 polymorphism and HCC risk in individuals with chronic HBV infection under different genetic models: (a) allelic (G vs. T), (b) recessive (GG vs. TG + TT), (c) dominant (GG + TG vs. TT), (d) homozygous (GG vs. TT), and (e) heterozygous (TG vs. TT). Abbreviations: DEPDC5, pleckstrin domain-containing protein 5; HBV, hepatitis B virus; HCC, hepatocellular carcinoma; CI, confidence interval; df, degree of freedom; M-H, Mantel-Haenszel.

Next, a meta-analysis was conducted based on the etiology of HCC, in which both cases and controls were chronically infected with HCV. Results for the subgroup of 1,673 cases and 7,150 controls in 8 studies [12, 13, 15, 17, 18, 20–22] showed that the rs1012068 polymorphism did not significantly increase HCC risk in individuals with chronic HCV infection (Table 2; Figure S2) under the allelic model (OR = 1.46, 95% CI = 1.03–2.05, = 0.03); the recessive model (OR = 1.63, 95% CI = 1.00–2.66, = 0.05); the dominant model (OR = 1.56, 95% CI = 1.04–2.34, = 0.03); the homozygous model (OR = 1.91, 95% CI = 0.99–3.65, = 0.05); and the heterozygous model (OR = 1.48, 95% CI = 1.02–2.16, = 0.04).

3.2.2. rs5998152 and HCC Risk

As shown in Table 2 and Figure 4, a meta-analysis based on a population of 411 cases and 1,448 controls in 3 studies [12, 15, 23] revealed that the rs5998152 polymorphism was significantly associated with HCC risk in Asians with chronic HCV infection under the allelic model (OR = 1.56, 95% CI = 1.05–2.33, = 0.03); the dominant model (OR = 1.82, 95% CI = 1.44–2.30, < 0.001); and the heterozygous model (OR = 1.82, 95% CI = 1.43–2.31, < 0.001); but not under the recessive model (OR = 1.32, 95% CI = 0.77–2.26, = 0.31); or the homozygous dominant model (OR = 1.62, 95% CI = 0.93–2.82, = 0.09).

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Figure 4

Forest plot showing the relationship between the DEPDC5 rs5998152 polymorphism and HCC risk in Asians with chronic HBV infection under different genetic models: (a) allelic (T vs. C), (b) recessive (TT vs. CT + CC), (c) dominant (CT + TT vs. CC), (d) homozygous (TT vs. CC), and (e) heterozygous (CT vs. CC). Abbreviations: DEPDC5, pleckstrin domain-containing protein 5; HBV, hepatitis B virus; HCC, hepatocellular carcinoma; CI, confidence interval; df, degree of freedom; M-H, Mantel-Haenszel.

3.3. Sensitivity Analysis

The controls in all 8 case-control studies that investigated the association between the rs1012068 polymorphism and HCC risk were chronically infected with HCV, except the controls in one study [20], in which the controls were healthy individuals. To eliminate such heterogeneity among controls, we repeated the meta-analysis after deleting this study. Repeating the meta-analysis led to similar results as when the study was included, suggesting that our meta-analysis is reliable (Figure S3).

3.4. Publication Bias

As shown in Figures 5 and 6, Begg’s funnel plot and Egger’s regression test showed that the meta-analysis of rs1012068 and rs5998152 polymorphisms showed no obvious asymmetry under the five genetic models (all > 0.05).

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Figure 5

Begg’s funnel plot to assess publication bias in the meta-analysis of the association between the DEPDC5 rs1012068 polymorphism and HCC risk in the total population under different genetic models: (a) allelic (G vs. T), (c) recessive (GG vs. TG + TT), (e) dominant (GG + TG vs. TT), (g) homozygous (GG vs. TT), and (i) heterozygous (TG vs. TT). Egger’s regression test to assess publication bias in the meta-analysis of the association between DEPDC5 rs1012068 polymorphism and HCC risk in the total population under different genetic models: (b) allelic (G vs. T), (d) recessive (GG vs. TG + TT), (f) dominant (GG + TG vs. TT), (h) homozygous (GG vs. TT), and (j) heterozygous (TG vs. TT). Abbreviations: DEPDC5, pleckstrin domain-containing protein 5; HCC, hepatocellular carcinoma; OR, odds ratio.

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Figure 6

Begg’s funnel plot to assess publication bias in the meta-analysis of the association between DEPDC5 rs5998152 polymorphism and HCC risk in the total population under different genetic models: (a) allelic (C vs. T), (c) recessive (CC vs. TC + TT), (e) dominant (CC + TC vs. TT), (g) homozygous (CC vs. TT), and (i) heterozygous (TC vs. TT). Egger’s regression test to assess publication bias in the meta-analysis of the association between DEPDC5 rs5998152 polymorphism and HCC risk in the total population under different genetic models: (b) allelic (C vs. T), (d) recessive (CC vs. TC + TT), (f) dominant (CC + TC vs. TT), (h) homozygous (CC vs. TT), and (j) heterozygous (TC vs. TT). Abbreviations: DEPDC5, pleckstrin domain-containing protein 5; HCC, hepatocellular carcinoma; OR, odds ratio.

4. Discussion

In the case of rs1012068, an overall meta-analysis of the total population indicated a significant association with increased HCC risk, regardless of HCC etiology and source of controls. Subgroup analysis based on ethnicity supported this association for Asians. Subsequently, meta-analyses of individuals chronically infected with HBV or HCV were performed. The cases and controls in three case-control studies [14, 16, 19] were all chronically infected with HBV, and in this uniform sample, results showed that the rs1012068 polymorphism significantly increased HCC risk in individuals with chronic HBV infection. In contrast, the association between the rs1012068 polymorphism and HCV-related HCC risk was not significant.

In the case of rs5998152, three case-control studies examined a potential relationship between this polymorphism and the risk of HCV-related HCC [12, 15, 23]. All cases and controls were chronically infected with HCV. Results showed the rs5998152 polymorphism was significantly associated with HCC risk in Asians with chronic HCV infection under allelic, dominant, and heterozygous models.

It may be that these polymorphisms weaken the activity of DEPDC5, preventing it from inhibiting mTORC1 as it does normally, which in turn leads to pathogenic inflammation and cell growth in the liver [22, 29]. Future research should explore how the rs1012068 and rs5998152 polymorphisms affect DEPDC5 expression and activity.

Although positive results were obtained, some limitations that may affect the interpretation of the meta-analysis were presented in this work. First, samples were relatively small due to the lack of case-control studies, especially for rs5998152. Second, among studies investigating the association between the rs1012068 polymorphism and HCC risk, the controls in all case-control studies except one [20] were chronically infected with HCV. When one study with healthy controls was deleted from the meta-analysis [20], the results were not substantially altered, suggesting that our meta-analysis is reliable. Third, the included studies in our meta-analysis spanned 2011–2022, during which antiviral treatments have improved and been widely used for treating HCV- or HBV-related liver disease [30, 31]. Since the included studies did not report detailed data on the use of such therapies, further research should explore how they influence the risk of HCC in individuals with DEPDC5 polymorphisms. Fourth, the robustness of the current meta-analysis may be reduced because the case-control studies involved used different genotyping methods that may differ in sensitivity and specificity, and potentially by other confounding factors such as age, sex, alcohol intake, and tumor status. Given these various limitations, the findings of our meta-analysis should be validated and extended in large, well-designed studies.

In summary, our study suggests that the DEPDC5 rs1012068 polymorphism increases HCC risk, especially in Asians with chronic HBV infection, while the rs5998152 polymorphism increases HCC risk in Asians with HCV infection. Further large, well-designed studies are required to validate these findings.

Data Availability

The data used to support the findings of this study are included within the article.

Conflicts of Interest

The authors declare that they have no conflicts of interest.

Authors’ Contributions

Shaoliang Zhu, Zhenyong Tang, and Mengjie Zou contributed equally to this work.

Supplementary Materials

Figure S1. Forest plot showing the relationship between the DEPDC5 rs1012068 polymorphism and HCC risk in the total population under different genetic models: (A) allelic (G vs. T), (B) recessive (GG vs. TG + TT), (C) dominant (GG + TG vs. TT), (D) homozygous (GG vs. TT), and (E) heterozygous (TG vs. TT). Figure S2. Forest plot showing the relationship between DEPDC5 rs1012068 polymorphism and HCC risk in individuals with chronic HCV infection under different genetic models: (A) allelic (G vs. T), (B) recessive (GG vs. TG + TT), (C) dominant (GG + TG vs. TT), (D) homozygous (GG vs. TT), and (E) heterozygous (TG vs. TT). Figure S3. Forest plot showing the relationship between the DEPDC5 rs1012068 polymorphism and HCC risk in sensitivity analysis: (A) allelic (G vs. T), (B) recessive (GG vs. TG + TT), (C) dominant (GG + TG vs. TT), (D) homozygous (GG vs. TT), and (E) heterozygous (TG vs. TT). Table S1. Search strategies for each database. (Supplementary Materials)

References

S. Chidambaranathan-Reghupaty, P. B. Fisher, and D. Sarkar, “Hepatocellular carcinoma (hcc): epidemiology, etiology and molecular classification,” Advances in Cancer Research, vol. 149, pp. 1–61, 2021.
View at: Publisher Site | Google Scholar
H. Sung, J. Ferlay, R. L. Siegel et al., “Global cancer statistics 2020: globocan estimates of incidence and mortality worldwide for 36 cancers in 185 countries,” CA: A Cancer Journal for Clinicians, vol. 71, no. 3, pp. 209–249, 2021.
View at: Publisher Site | Google Scholar
S. Baulac, S. Ishida, E. Marsan et al., “Familial focal epilepsy with focal cortical dysplasia due to depdc 5 mutations,” Annals of Neurology, vol. 77, no. 4, pp. 675–683, 2015.
View at: Publisher Site | Google Scholar
L. M. Dibbens, B. De Vries, S. Donatello et al., “Mutations in depdc5 cause familial focal epilepsy with variable foci,” Nature Genetics, vol. 45, no. 5, pp. 546–551, 2013.
View at: Publisher Site | Google Scholar
S. Ishida, F. Picard, G. Rudolf et al., “Mutations of depdc5 cause autosomal dominant focal epilepsies,” Nature Genetics, vol. 45, no. 5, pp. 552–555, 2013.
View at: Publisher Site | Google Scholar
L. A. Jansen, “Delving deeper into depdc5,” Epilepsy Currents, vol. 18, no. 3, pp. 197–199, 2018.
View at: Publisher Site | Google Scholar
K. A. Myers and I. E. Scheffer, “Depdc5 as a potential therapeutic target for epilepsy,” Expert Opinion on Therapeutic Targets, vol. 21, no. 6, pp. 591–600, 2017.
View at: Publisher Site | Google Scholar
S. Jin, Q. Liao, J. Chen et al., “Tsc1 and depdc5 regulate hiv-1 latency through the mtor signaling pathway,” Emerging Microbes and Infections, vol. 7, no. 1, pp. 1–11, 2018.
View at: Publisher Site | Google Scholar
S. K. R. Padi, N. Singh, J. J. Bearss et al., “Phosphorylation of depdc5, a component of the gator1 complex, releases inhibition of mtorc1 and promotes tumor growth,” Proceedings of the National Academy of Sciences, vol. 116, no. 41, pp. 20505–20510, 2019.
View at: Publisher Site | Google Scholar
M. A. Burza, B. M. Motta, R. M. Mancina et al., “Depdc5 variants increase fibrosis progression in europeans with chronic hepatitis c virus infection,” Hepatology, vol. 63, no. 2, pp. 418–427, 2016.
View at: Publisher Site | Google Scholar
Y. Mizuno, S. Shimada, Y. Akiyama et al., “Depdc5 deficiency contributes to resistance to leucine starvation via p62 accumulation in hepatocellular carcinoma,” Scientific Reports, vol. 8, no. 1, pp. 106–111, 2018.
View at: Publisher Site | Google Scholar
D. Miki, H. Ochi, C. N. Hayes et al., “Variation in the depdc5 locus is associated with progression to hepatocellular carcinoma in chronic hepatitis C virus carriers,” Nature Genetics, vol. 43, no. 8, pp. 797–800, 2011.
View at: Publisher Site | Google Scholar
C. M. Lange, S. Bibert, J. F. Dufour et al., “Comparative genetic analyses point to hcp5 as susceptibility locus for hcv-associated hepatocellular carcinoma,” Journal of Hepatology, vol. 59, no. 3, pp. 504–509, 2013.
View at: Publisher Site | Google Scholar
C. X. Liu, “Genetic polymorphism is not associated with susceptibility to hepatocellular carcinoma in northern chinese patients with chronic hepatitis b,” Shandong University, Jinan, China, 2014, Masters’s Dissertation.
View at: Google Scholar
M. R. Al-Anazi, S. Matou-Nasri, A. A. Abdo et al., “Variations in depdc5 gene and its association with chronic hepatitis c virus infection in saudi arabia,” BMC Infectious Diseases, vol. 14, no. 1, pp. 632–639, 2014.
View at: Publisher Site | Google Scholar
N. Ma, X. Zhang, F. Yu et al., “Role of ifn-λs, ifn-λs related genes and the depdc 5 gene in h epatitis b virus‐related liver disease,” Journal of Viral Hepatitis, vol. 21, no. 7, pp. e29–e38, 2014.
View at: Publisher Site | Google Scholar
H. Hai, A. Tamori, L. T. T. Thuy et al., “Polymorphisms in mica, but not in depdc5, hcp5 or pnpla3, are associated with chronic hepatitis c-related hepatocellular carcinoma,” Scientific Reports, vol. 7, no. 1, pp. 11912–11919, 2017.
View at: Publisher Site | Google Scholar
S. T. Zhang, “Candidate snps-based study on susceptibility to hepatitis c virus-related liver cirrhosis and hepatocellular carcinoma,” Tianjin Medical University, Tianjin, China, 2017, Masters’s Dissertation.
View at: Google Scholar
W. Liu, N. Ma, D. Zhao et al., “Correlation between the depdc5 rs1012068 polymorphism and the risk of hbv-related hepatocellular carcinoma,” Clinics and Research in Hepatology and Gastroenterology, vol. 43, no. 4, pp. 446–450, 2019.
View at: Publisher Site | Google Scholar
M. M. El-Daly, H. M. Ibrahim, E. Labib, H. Ghanem, I. El-Elaimy, and M. Abdel-Hamid, “Significance of depdc5 and mica variants in hepatocellular carcinoma risk related hepatitis c virus patients in Egypt,” EJMO, vol. 3, no. 4, pp. 274–280, 2019.
View at: Publisher Site | Google Scholar
R. E. Sharkawy, A. Bayoumi, M. Metwally et al., “A variant in the mica gene is associated with liver fibrosis progression in chronic hepatitis c through tgf-β1 dependent mechanisms,” Scientific Reports, vol. 9, no. 1, pp. 1439–1510, 2019.
View at: Publisher Site | Google Scholar
H. M. Farhan, K. Abougabal, H. Gaber, and D. Attia, “Disheveled egl-10 and pleckstrin domain-containing 5 rs1012068 t/g gene polymorphism among egyptian chronic hcv-infected patients: disease progression and related complications,” Egyptian Journal of Immunology, vol. 29, no. 3, Article ID 35758967, pp. 36–43, 2022.
View at: Publisher Site | Google Scholar
K. Y. Qiao, S. T. Zhang, R. Su, W. Hou, and F. M. Wang, “Correlation between depdc5 rs5998152 single nucleotide polymorphism and risk of hcv-related liver diseases,” Chinese Journal of Experimental and Clinical Virology, vol. 53, no. 3, pp. 300–304, 2021.
View at: Google Scholar
V. Welch, M. Petticrew, J. Petkovic et al., “Extending the prisma statement to equity-focused systematic reviews (prisma-e 2012): explanation and elaboration,” Journal of Clinical Epidemiology, vol. 70, pp. 68–89, 2016.
View at: Publisher Site | Google Scholar
V. Welch, M. Losos, and P. Tugwell, The Newcastle-Ottawa Scale (NOS) for Assessing the Quality of Nonrandomised Studies in Meta-Analyses, University of Ottawa, Ottawa, Canada, 2018, https://www.ohri.ca/programs/clinical_epidemiology/oxford.asp.
R. L. Ownby, E. Crocco, A. Acevedo, V. John, and D. Loewenstein, “Depression and risk for alzheimer disease: systematic review, meta-analysis,” Archives of General Psychiatry, vol. 63, no. 5, pp. 530–538, 2006.
View at: Publisher Site | Google Scholar
T. Motomura, Y. Ono, K. Shirabe et al., “Neither mica nor depdc5 genetic polymorphisms correlate with hepatocellular carcinoma recurrence following hepatectomy,” HPB Surgery, vol. 2012, Article ID 185496, 6 pages, 2012.
View at: Publisher Site | Google Scholar
N. Ma, “Impact of Candidate Genetic Polymorphisms on the Infection and Infection Outcomes of Hepatitis B Virus,” Hebei Medical University, Shijiazhuang, China, 2012, Masters’s Dissertation.
View at: Google Scholar
I. M. Moaz, A. R. Abdallah, M. F. Yousef, and S. Ezzat, “Main insights of genome wide association studies into hcv-related hcc,” Egyptian Liver Journal, vol. 10, no. 1, p. 4, 2020.
View at: Publisher Site | Google Scholar
L. Bucci, F. Garuti, B. Lenzi et al., “The evolutionary scenario of hepatocellular carcinoma in Italy: an update,” Liver International, vol. 37, no. 2, pp. 259–270, 2017.
View at: Publisher Site | Google Scholar
S. Y. Mohamed, A. E. Esmaiel, M. A. Shabana, and N. F. Ibrahim, “Assessment of plasma vitronectin as diagnostic and prognostic marker of hepatocellular carcinoma in patients with hepatitis c virus cirrhosis,” Gastroenterology Insights, vol. 13, no. 1, pp. 9–19, 2022.
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Copyright © 2023 Shaoliang Zhu et al. This is an open access article distributed under the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.

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