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Prognostic value of EIF5A2 in solid tumors: A meta-analysis and bioinformatics analysis

  • Jianwen Fang , Tianze Yu , Xiaocong Jiang , Yuexin Lu , Xi Shang , Haixing Shen , Yue Lu , Jingyan Zheng and Peifen Fu EMAIL logo
Published/Copyright: May 16, 2024
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Open Medicine
From the journal Open Medicine Volume 19 Issue 1

Abstract

Aims

In cancer biology, the aberrant overexpression of eukaryotic translation initiation factor 5A2 (EIF5A2) has been correlative with an ominous prognosis, thereby underscoring its pivotal role in fostering metastatic progression. Consequently, EIF5A2 has garnered significant attention as a compelling prognostic biomarker for various malignancies. Our research endeavors were thus aimed at elucidating the utility and significance of EIF5A2 as a robust indicator of cancer outcome prediction.

Method

An exhaustive search of the PubMed, EMBASE, and Web of Science databases found relevant studies. The link between EIF5A2 and survival prognosis was examined using hazard ratios and 95% confidence intervals. Subsequently, The Cancer Genome Atlas (TCGA) and the Gene Expression Profiling Interactive Analysis (GEPIA) databases were employed to validate EIF5A2 expression across various cancer types.

Results

Through pooled analysis, we found that increased EIF5A2 expression was significantly associated with decreased overall survival (OS) and disease-free survival/progression-free survival/relapse-free survival (DFS/PFS/RFS). Moreover, TCGA analysis revealed that EIF5A2 was significantly upregulated in 27 types of cancer, with overexpression being linked to shorter OS in three, worse DFS in two, and worse PFS in six types of cancer. GEPIA showed that patients with EIF5A2 overexpression had reduced OS and DFS.

Conclusions

In solid tumors, EIF5A2 emerges as a reliable prognostic marker. Our meta-analysis comprehensively analyzed the prognostic value of EIF5A2 in solid tumors and assessed its efficacy as a predictive marker.

Keywords: EIF5A2; cancer; prognosis; meta-analysis; EMT

1 Introduction

Eukaryotic translation initiation factor 5A (EIF5A), an essential protein, plays a vital role in maintaining cellular polyamine homeostasis and influencing ribosomal peptidyl-transferase [1]. Eukaryotic translation initiation factor 5A2 (EIF5A2), a variant of EIF5A, enhances signal transducer and activator of transcription 3 (STAT3) entry into the nucleus. This, in turn, increases STAT3 enrichment on the promoter of transforming growth factor-β1 (TGF-β1), resulting in upregulated TGF-β1 expression and facilitating the epithelial–mesenchymal transition (EMT) [2]. EMT enables tumor cells to transition between epithelial and mesenchymal states, which is critical for cancer metastasis [3]. Elevated EIF5A2 levels have been detected in various cancers, where it promotes cancer spread and presents as a promising target for cancer treatment [4]. Inhibition of EIF5A2 has been shown to suppress tumor development and metastasis, while also overcoming chemotherapy resistance [5].

Previous studies suggest that high levels of EIF5A2 are associated with poor prognosis [6]. EIF5A2 was identified in a primary ovarian cancer cell line, and its overexpression in ovarian tumor predicts poor prognosis [7]. Similar outcomes were observed in patients with bladder urothelial cancer (BUC) [8,9], upper tract urothelial carcinoma (UTUC) [10,11], and prostate cancer [12]. In gastrointestinal tumors such as oral squamous cell carcinoma (OSCC) [13], esophageal squamous cell carcinoma (ESCC) [14], gastric cancer (GC) [15,16], hepatocellular carcinoma (HCC) [17,18], gallbladder cancer (GBC) [19], intrahepatic cholangiocarcinoma (ICC) [2], pancreatic adenocarcinoma [20], and colorectal carcinoma (CRC) [21], overexpression of EIF5A2 is also a predictor of poor prognosis. Additionally, overexpression of EIF5A2 is associated with poor prognosis in melanoma [22], nasopharyngeal carcinoma (NPC) [23], cervical cancer [24], and non-small-cell lung cancer (NSCLC) [25] patients.

As scientific knowledge continues to expand, we gain a better understanding of the complex mechanisms underlying cancer metastasis. However, some aspects of these mechanisms remain elusive, underscoring the urgent need for continued research aimed at elucidating them and identifying novel biomarkers for cancer treatment. EIF5A2 is a promising candidate as a prognostic marker for cancer, but the findings from previous studies have not been consistent, making it difficult to establish its predictive significance definitively. To address this issue, in this study, we conducted a meta-analysis to evaluate the predictive value of EIF5A2 in solid tumors and assess its potential as a reliable predictive marker.

2 Materials & methods

2.1 Search strategy

We conducted a systematic search of the PubMed, Web of Science, and EMBASE databases to retrieve relevant publications up until February 10, 2023. The search utilized the keywords “EIF5A2” and “cancer” OR “carcinoma” OR “neoplasm” OR “tumor” OR “tumour,” along with “prognosis” OR “prognostic” OR “survival” OR “outcome.” No language restrictions were applied to the search. We reviewed titles, abstracts, full-text manuscripts, and references to identify relevant studies. As this study did not involve human participants, informed consent was not required (Table 1).

Table 1

Search strings

Database Search string Number of studies
Web of Science (“EIF5A2”) and (“cancer” OR “carcinoma” OR “neoplasm” OR “tumor” OR “tumour”) and (“prognosis” OR “prognostic” OR “survival” OR “outcome”) 83
PubMed (“EIF5A2”) and (“cancer” OR “carcinoma” OR “neoplasm” OR “tumor” OR “tumour”) and (“prognosis” OR “prognostic” OR “survival” OR “outcome”) 66
Embase (“EIF5A2”) and (“cancer” OR “carcinoma” OR “neoplasm” OR “tumor” OR “tumour”) and (“prognosis” OR “prognostic” OR “survival” OR “outcome”) 75
Total 224

EIF5A2: eukaryotic translation initiation factor 5A2.

2.2 Study selection

We included publications that investigated the relationship between EIF5A2 and survival prognosis in solid tumors, reported measurements of EIF5A2 expression in tissue or blood, and provided sufficient data to calculate hazard ratios (HRs) and 95% confidence intervals (CIs). Our study encompasses a variety of detection methods, ensuring that a broad spectrum of research is included. While real-time PCR is acknowledged as a common method, other detection techniques were also considered, enhancing the diversity of the literature reviewed. Studies that did not provide enough information to estimate HRs and 95% CIs, as well as reviews, case reports, letters, abstracts, animal studies, public database datasets, and duplicated or overlapped research, were excluded from our analysis. Literature in languages other than English or Chinese was excluded due to limitations in linguistic proficiency. Our study prioritized articles that explicitly reported HRs in their findings. Articles relying solely on Kaplan–Meier curves for survival analysis were intentionally excluded from our study.

2.3 Data extraction & quality assessment

We extracted relevant data from each eligible study, including author name, publication year, and country of sample origin. Additionally, we collected information on the type of tumor samples, sample size, detection methods, and other characteristics. We also obtained overall survival (OS), disease-free survival/progression-free survival/relapse-free survival (DFS/PFS/RFS), HRs, and their corresponding 95% CIs. When available, multivariate analysis was preferred over univariate analysis for increased precision. The quality of each study was assessed using the Newcastle–Ottawa Quality Assessment Scale to evaluate its effectiveness.

2.4 Statistical analysis

We used HRs and their corresponding 95% CIs to calculate the pooled data in our analysis, directly utilizing the values reported in each study. To assess heterogeneity, I 2 or p-value was used. When I 2 was less than 50% or p-value was larger than 0.05, a fixed-effects model was employed, and when I 2 was greater than 50% or p-value was less than 0.05, a random-effects model was employed. Sensitivity analysis was conducted to assess the reliability of the results. To assess publication bias, funnel plots and Egger’s test were used. STATA 17.0 software was used for all data analyses (Stata Corporation, TX, USA). P-values lower than 0.05 were deemed statistically significant.

2.5 Bioinformatics analysis

We collected RNA-sequencing expression (level 3) profiles and corresponding clinical information from The Cancer Genome Atlas (TCGA) database (https://portal.gdc.cancer.gov/) for 10,030 patients with various types of cancer. Additionally, we obtained mRNA expression data from paired normal tissue samples in these tumors. Normal tissue samples were also retrieved from the GTEx V8 release version (https://gtexportal.org/home/datasets) for comparison. We used univariate Cox regression analysis and the “forestplot” R package in R version 4.0.3 to display p-values, HRs, and their respective 95% CIs for each variable. The Gene Expression Profiling Interactive Analysis (GEPIA) tool (http://gepia.cancer-pku.cn/), based on TCGA and GTEx data, was used to evaluate abnormal EIF5A2 expression in cancer tissues. We then obtained survival plots in the form of Kaplan–Meier curves for the association between EIF5A2 expression and OS or DFS. P-values less than 0.05 were considered statistically significant.

3 Results

3.1 Search results

Our search strategy yielded a total of 224 articles from the designated databases. After removing 19 duplicates, we screened 205 articles for additional information using our selection criteria, resulting in the elimination of 184 articles and leaving 21 articles for further screening. Of these, two articles did not provide sufficient data, and two others used data obtained from public databases. Ultimately, our meta-analysis included 17 articles published between 2009 and 2022. Figure 1 illustrates the search strategy flowchart.

Figure 1 Literature search process flowchart.
Figure 1

Literature search process flowchart.

3.2 Study characteristics

A total of 3,554 samples were included in our meta-analysis, with sample sizes ranging from 72 to 436 per study. Various malignancies were investigated, including ovarian cancer, BUC, UTUC, melanoma, prostate cancer, OSCC, ESCC, GC, HCC, GBC, ICC, pancreatic adenocarcinoma, CRC, NPC, cervical cancer, and NSCLC. In 20 studies, the overexpression of EIF5A2 was detected in tissue samples using immunohistochemistry. Table 2 provides fundamental information regarding the included literature.

Table 2

Elements of relevant studies

Study Year Country Race Sample size Tumor type Detected method Detected sample Survival analysis NOS score
Chen et al. [8] 2009 China Asian 86 Bladder urothelial carcinoma IHC Tissue OS 7
Fang et al. [11] 2019 China Asian 101 Upper urinary tract urothelial carcinoma IHC Tissue OS, PFS 7
He et al. [25] 2011 China Asian 224 Non-small-cell lung cancer IHC Tissue OS 6
Huang et al. [10] 2018 China Asian 109 Upper urinary tract urothelial carcinoma IHC Tissue RFS 7
Huang et al. [23] 2016 China Asian 123 NPC IHC Tissue OS 7
Khosravi et al. [22] 2016 Canada Caucasian 382 Melanoma IHC Tissue OS 6
Lin et al. [13] 2020 China Asian 272 OSCC IHC Tissue OS 6
Luo et al. [9] 2009 China Asian 112 Bladder urothelial carcinoma IHC Tissue PFS, RFS 6
Meng et al. [16] 2015 China Asian 160/145 GC IHC Tissue OS, DFS 5
Wang et al. [17] 2014 China Asian 212 Hepatocellular carcinoma IHC Tissue OS 7
Wei et al. [20] 2013 China Asian 73 Pancreatic adenocarcinoma IHC Tissue OS 5
Wei et al. [26] 2014 China Asian 154 Bladder cancer IHC Tissue OS 6
Yang et al. [7] 2009 China Asian 110 Ovarian tumor IHC Tissue OS 6
Yang et al. [15] 2016A China Asian 436 GC IHC Tissue OS 6
Yang et al. [24] 2016B China Asian 314 Cervical cancer IHC Tissue OS, DFS 7
Zheng et al. [19] 2020 China Asian 80 GBC IHC Tissue OS 7
Zhu et al. [21] 2011 China Asian 229 CRC IHC Tissue OS 7

IHC: immunohistochemistry; OS: overall survival; DFS: disease-free survival; PFS: progression-free survival; RFS: relapse-free survival.

3.3 High EIF5A2 expression & OS

Fourteen studies examined the association between high EIF5A2 expression and prognosis using OS. As there was no significant heterogeneity observed in this analysis (I 2 = 0), a fixed-effects model was used to estimate the pooled HR with a 95% CI. The results showed that high EIF5A2 expression was substantially linked with shorter OS (HR: 1.97; 95% CI: 1.73–2.22), as depicted in Figure 2.

Figure 2 Forest plot of the relationship between overexpression of EIF5A2 and OS.
Figure 2

Forest plot of the relationship between overexpression of EIF5A2 and OS.

3.4 Subgroup analysis for OS

Subgroup analyses were conducted according to tumor type, race, and sample size. The findings of these subgroup analyses are presented in Table 3. In terms of tumor types, high EIF5A2 expression was associated with poor OS in digestive system tumors, with an HR of 1.89 (95% CI: 1.57–2.27). Similarly, gynecological and reproductive system tumors had an HR of 1.72 (95% CI: 2.21–2.45). Head and neck cancers exhibited an HR of 1.85 (95% CI: 1.26–2.71), and melanoma had an HR of 2.26 (95% CI: 1.57–3.26). Respiratory system tumors had an HR of 2.10 (95% CI: 1.16–3.79), and urinary system tumors had an HR of 2.52 (95% CI: 1.58–4.03). When considering race, both Asian and Caucasian populations showed statistically significant HRs. Asian individuals had an HR of 1.93 (95% CI: 1.68–2.21), while Caucasians had an HR of 2.26 (95% CI: 1.57–3.26). Finally, the analysis of sample sizes revealed that studies with less than 200 participants had an HR of 2.16 (95% CI: 1.62–2.89), while those with more than 200 participants had an HR of 1.92 (95% CI: 1.66–2.23).

Table 3

Subgroup analysis for OS

Clinical features Studies (n) Pooled HR (95% CI) p-value Heterogeneity
I 2 (%) p-value Model
Tumor type
Digestive system 6 1.89 (1.57–2.27) <0.001 0 0.506 Random
Gynecological and Reproductive systems 2 1.72 (2.21–2.45) 0.003 0 0.573 Random
Head and neck cancers 2 1.85 (1.26–2.71) 0.002 0 0.340 Random
Melanoma 1 2.26 (1.57–3.26) <0.001
Respiratory system 1 2.10 (1.16–3.79) 0.014
Urinary system 3 2.52 (1.58–4.03) <0.001 31.9 0.230 Random
Race
Asian 14 1.93 (1.68–2.21) <0.001 0 0.671 Random
Caucasian 1 2.26 (1.57–3.26) <0.001
Sample size
<200 7 2.16 (1.62–2.89) <0.001 17.7 0.295 Random
≥200 8 1.92 (1.66–2.23) <0.001 0 0.855 Random

HR: Hazard ratio.

3.5 High EIF5A2 expression & DFS/PFS/RFS

Six studies examined the connection between overexpression of EIF5A2 and prognosis using DFS/PFS/RFS. Using the fixed-effects model (I 2 = 0), a comprehensive analysis revealed that increased EIF5A2 expression was substantially related to decreased DFS/PFS/RFS (HR: 2.31; 95% CI: 1.80–2.98) (Figure 3). Additionally, we independently analyzed DFS, PFS and RFS results. High EIF5A2 expression was connected with decreased DFS (HR: 1.93; 95% CI: 1.36–2.72), PFS (HR: 3.51; 95% CI: 1.94–6.35), and RFS (HR: 2.50; 95% CI: 1.55–4.03).

Figure 3 Forest plot of the relationship between overexpression of EIF5A2 and DFS/PFS/RFS.
Figure 3

Forest plot of the relationship between overexpression of EIF5A2 and DFS/PFS/RFS.

3.6 High EIF5A2 expression & lymph node metastasis

To further explore the association between EIF5A2 and lymph node metastasis, we performed a thorough analysis by compiling data on high EIF5A2 expression and lymph node (LN) metastasis status. The findings indicated there is no association between elevated EIF5A2 expression and LN status (LN positive vs LN negative), as evidenced by an odds ratio (OR) of 1.14 (95% CI: 0.76–1.52) (Figure 4).

Figure 4 Forest plot of the relationship between expression of EIF5A2 and lymph node metastasis: LN, lymph node.
Figure 4

Forest plot of the relationship between expression of EIF5A2 and lymph node metastasis: LN, lymph node.

3.7 Sensitivity analysis

To assess the robustness of the findings, a sensitivity analysis was conducted by removing each study individually. The results, as depicted in Figures 5 and 6, did not show any significant alteration from the overall analysis, indicating the stability of the results.

Figure 5 Sensitivity analysis for OS.
Figure 5

Sensitivity analysis for OS.

Figure 6 Sensitivity analysis for DFS/PFS/RFS.
Figure 6

Sensitivity analysis for DFS/PFS/RFS.

3.8 Publication bias

To assess publication bias for OS or DFS/PFS/RFS, the study used funnel plots and Egger’s test to generate statistical evidence (Figure 7). The results indicated a significant publication bias, with Egger’s test p-values of 0.011 for OS (Figure 8a) and 0.006 for DFS/PFS/RFS (Figure 8b). To further examine publication bias, the study employed the trim-and-fill strategy. It was found that the pooled HRs for OS and DFS/PFS/RFS were 1.914 (95% CI: 1.689–2.168) and 2.162 (95% CI: 1.697–2.755), respectively, which demonstrated that the meta-analysis results remained robust despite the presence of publication bias.

Figure 7 Funnel plots for publication bias: (a) funnel plots for OS; (b) filled funnel plot for OS; (c) funnel plots for DFS/PFS/RFS; (d) filled funnel plot for DFS/PFS/RFS.
Figure 7

Funnel plots for publication bias: (a) funnel plots for OS; (b) filled funnel plot for OS; (c) funnel plots for DFS/PFS/RFS; (d) filled funnel plot for DFS/PFS/RFS.

Figure 8 (a) Egger’s test for OS data, and (b) Egger’s test for DFS/PFS/RFS data.
Figure 8

(a) Egger’s test for OS data, and (b) Egger’s test for DFS/PFS/RFS data.

3.9 Verification in bioinformatics databases

To further confirm our findings, we investigated if EIF5A2 could serve as a prognostic biomarker across various types of cancer. Our results demonstrated that the expression of EIF5A2 was significantly different in 27 types of cancers (p < 0.05; Figure 9) compared to healthy tissues. Additionally, univariate Cox regression analyses were conducted to evaluate the prognostic value of EIF5A2 in a wide range of malignancies. The results showed that the overexpression of EIF5A2 was associated with poor OS in three types of cancer (p < 0.05; Figure 10a) and worse DFS and PFS in two and six cancer types (p < 0.05; Figure 10b and c). Furthermore, we used the GEPIA online tool to assess EIF5A2 expression across 31 types of cancers. The patients were divided into EIF5A2 high and low expression groups based on the median value, and the results (Figure 11) confirmed that EIF5A2 overexpression was linked to shorter OS and DFS in patients with cancer. These findings, which were consistent with the conclusions of our meta-analysis, suggest that EIF5A2 could be a promising prognostic biomarker for various types of cancer.

Figure 9 EIF5A2 expression in different types of cancers. The expression distribution of EIF5A2 in tumor tissues and normal tissues. The abscissa represents different tumor tissues, the ordinate represents the expression distribution of EIF5A2, and different colors represent different groups. *p<  0.05, **p<  0.01,***p<  0.001, asterisks (*) stand for significance levels. The statistical difference of two groups was compared through the Wilcox test. ACC: adrenocortical carcinoma; BLCA: bladder urothelial carcinoma; BRCA: breast invasive carcinoma; CESC: cervical squamous cell carcinoma and endocervical adenocarcinoma; CHOL: cholangiocarcinoma; COAD: colon adenocarcinoma; ESCA: esophageal carcinoma; GBM: glioblastoma multiforme; HNSC: head and neck squamous cell carcinoma; KICH: kidney chromophobe; KIRC: kidney renal clear cell carcinoma; KIRP: kidney renal papillary cell carcinoma; LGG: brain lower-grade glioma; LIHC: liver hepatocellular carcinoma; LUAD: lung adenocarcinoma; LUSC: lung squamous cell carcinoma; MESO: mesothelioma; OV: ovarian serous cystadenocarcinoma; PAAD: pancreatic adenocarcinoma; PCPG: pheochromocytoma and paraganglioma; PRAD: prostate adenocarcinoma; READ: rectum adenocarcinoma; SARC: sarcoma; SKCM: skin cutaneous melanoma; STAD: stomach adenocarcinoma; TGCT: testicular germ cell tumors; THCA: thyroid carcinoma; THYM: thymoma; UCEC: uterine corpus endometrial carcinoma; UCS: uterine carcinosarcoma; UVM: uveal melanoma.
Figure 9

EIF5A2 expression in different types of cancers. The expression distribution of EIF5A2 in tumor tissues and normal tissues. The abscissa represents different tumor tissues, the ordinate represents the expression distribution of EIF5A2, and different colors represent different groups. *p<  0.05, **p<  0.01,***p<  0.001, asterisks (*) stand for significance levels. The statistical difference of two groups was compared through the Wilcox test. ACC: adrenocortical carcinoma; BLCA: bladder urothelial carcinoma; BRCA: breast invasive carcinoma; CESC: cervical squamous cell carcinoma and endocervical adenocarcinoma; CHOL: cholangiocarcinoma; COAD: colon adenocarcinoma; ESCA: esophageal carcinoma; GBM: glioblastoma multiforme; HNSC: head and neck squamous cell carcinoma; KICH: kidney chromophobe; KIRC: kidney renal clear cell carcinoma; KIRP: kidney renal papillary cell carcinoma; LGG: brain lower-grade glioma; LIHC: liver hepatocellular carcinoma; LUAD: lung adenocarcinoma; LUSC: lung squamous cell carcinoma; MESO: mesothelioma; OV: ovarian serous cystadenocarcinoma; PAAD: pancreatic adenocarcinoma; PCPG: pheochromocytoma and paraganglioma; PRAD: prostate adenocarcinoma; READ: rectum adenocarcinoma; SARC: sarcoma; SKCM: skin cutaneous melanoma; STAD: stomach adenocarcinoma; TGCT: testicular germ cell tumors; THCA: thyroid carcinoma; THYM: thymoma; UCEC: uterine corpus endometrial carcinoma; UCS: uterine carcinosarcoma; UVM: uveal melanoma.

Figure 10 Forest plot for OS (a), DFS (b), and PFS (c). The p-value, risk coefficient (HR), and CI of EIF5A2 in multiple tumors are analyzed by univariate cox regression. ACC: adrenocortical carcinoma; BLCA: bladder urothelial carcinoma; BRCA: breast invasive carcinoma; CESC: cervical squamous cell carcinoma and endocervical adenocarcinoma; CHOL: cholangiocarcinoma; COAD: colon adenocarcinoma; ESCA: esophageal carcinoma; GBM: glioblastoma multiforme; HNSC: head and neck squamous cell carcinoma; KICH: kidney chromophobe; KIRC: kidney renal clear cell carcinoma; KIRP: kidney renal papillary cell carcinoma; LGG: brain lower-grade glioma; LIHC: liver hepatocellular carcinoma; LUAD: lung adenocarcinoma; LUSC: lung squamous cell carcinoma; MESO: mesothelioma; OV: ovarian serous cystadenocarcinoma; PAAD: pancreatic adenocarcinoma; PCPG: pheochromocytoma and paraganglioma; PRAD: prostate adenocarcinoma; READ: rectum adenocarcinoma; SARC: sarcoma; SKCM: skin cutaneous melanoma; STAD: stomach adenocarcinoma; TGCT: testicular germ cell tumors; THCA: thyroid carcinoma; THYM: thymoma; UCEC: uterine corpus endometrial carcinoma; UCS: uterine carcinosarcoma; UVM: uveal melanoma.
Figure 10

Forest plot for OS (a), DFS (b), and PFS (c). The p-value, risk coefficient (HR), and CI of EIF5A2 in multiple tumors are analyzed by univariate cox regression. ACC: adrenocortical carcinoma; BLCA: bladder urothelial carcinoma; BRCA: breast invasive carcinoma; CESC: cervical squamous cell carcinoma and endocervical adenocarcinoma; CHOL: cholangiocarcinoma; COAD: colon adenocarcinoma; ESCA: esophageal carcinoma; GBM: glioblastoma multiforme; HNSC: head and neck squamous cell carcinoma; KICH: kidney chromophobe; KIRC: kidney renal clear cell carcinoma; KIRP: kidney renal papillary cell carcinoma; LGG: brain lower-grade glioma; LIHC: liver hepatocellular carcinoma; LUAD: lung adenocarcinoma; LUSC: lung squamous cell carcinoma; MESO: mesothelioma; OV: ovarian serous cystadenocarcinoma; PAAD: pancreatic adenocarcinoma; PCPG: pheochromocytoma and paraganglioma; PRAD: prostate adenocarcinoma; READ: rectum adenocarcinoma; SARC: sarcoma; SKCM: skin cutaneous melanoma; STAD: stomach adenocarcinoma; TGCT: testicular germ cell tumors; THCA: thyroid carcinoma; THYM: thymoma; UCEC: uterine corpus endometrial carcinoma; UCS: uterine carcinosarcoma; UVM: uveal melanoma.

Figure 11 Kaplan–Meier curves for OS (a) and DFS (b). The prognostic value of EIF5A2 for the OS and DFS of patients with cancer using the GEPIA database. HR: hazard ratio; OS: overall survival; DFS: disease-free survival.
Figure 11

Kaplan–Meier curves for OS (a) and DFS (b). The prognostic value of EIF5A2 for the OS and DFS of patients with cancer using the GEPIA database. HR: hazard ratio; OS: overall survival; DFS: disease-free survival.

4 Discussion

Metastasis, the most deleterious hallmark of cancer, remains responsible for a substantial proportion of cancer-related deaths [27]. The interplay between autophagy and EMT, two critical processes that govern cellular behavior, has emerged as an underlying molecular mechanism driving tumorigenesis and metastasis [28]. Notably, androgen receptor (AR) signaling governs the expression of EIF5A2 in androgen-dependent cells, promoting prostate cancer metastasis by inducing EMT and elevating EIF5A2 expression [29]. Autophagy, an adaptive stress response that degrades unwanted organelles and biomolecules, contributes to the immunosuppressive environment that facilitates tumor initiation and progression [30].

Drug resistance in cancer cells reduces the effectiveness of current treatments for many types of malignancy, including chemotherapy and targeted therapies [31]. Many studies have studied the function of EMT in tumor drug resistance, and various EMT-mediated signaling pathways are involved in drug resistance [32]. EIF5A2 has been implicated in promoting drug resistance in various malignancies. In HCC, for instance, elevated EIF5A2 levels mediate chemo-resistance by suppressing autophagy-mediated cell death [18]. Hypoxia further amplifies EIF5A2 expression in NSCLC, thereby promoting cisplatin resistance via autophagy induction [33]. Similarly, in breast cancer cells, overexpression of EIF5A2 correlates with lower sensitivity to doxorubicin [34]. In addition, recent studies suggest that EIF5A2 might regulate cellular aging by modulating transcriptional activity, adding another layer of complexity to its diverse roles in various biological processes [35].

Given the critical involvement of EIF5A2 in tumor-specific mechanisms such as EMT, autophagy, and drug resistance, it represents a promising target for developing novel therapeutic approaches. A meta-analysis conducted in our study corroborates the association between EIF5A2 overexpression and poor prognosis in solid tumors, underscoring the potential of EIF5A2 as a reliable and informative biomarker of malignancy outcome.

This meta-analysis is subject to several limitations. First, the sample sizes of all included studies were relatively small, and hence, the accuracy of their data may be compromised. Second, clinical characteristics of the studies were not made available. Third, there exists a notable publication bias for survival outcomes, potentially resulting from variations in research methodologies, clinical experience of authors, statistical analysis, and adjustment factors. Finally, most of the retrospective investigations were conducted in Asia, thereby limiting the generalizability of the outcomes to other regions.

As previously discussed, EIF5A2 has been implicated in tumor initiation, progression, metastasis, and chemotherapy resistance, making it a promising prognostic marker for solid malignancies. Robust prognostic markers not only enable personalized treatment for each patient by allowing for the early identification of high- and low-risk individuals, but also improve overall clinical outcomes. Despite the potential significance of EIF5A2 as a prognostic biomarker, its clinical relevance in solid tumors is still not well established. Thus, our meta-analysis aimed to comprehensively explore the potential clinical utility of EIF5A2 in solid malignancies.

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  1. Funding information: This study was supported by the National Natural Science Foundation of China (No. 82172770).

  2. Author contributions: Peifen Fu provided direction for this work and revised the manuscript. Jianwen Fang and Yu Tianze contributed to the conception of the study. Jianwen Fang, Yuexin Lu and Xiaocong Jiang drafted the original manuscript. Jianwen Fang, Xi Shang and Haixing Shen illustrated the figures for the manuscript. Jianwen Fang, Yue Lu, and Jingyan Zheng collected the relevant research. All authors approved the final manuscript.

  3. Conflict of interest: The authors declare that they have no competing interests.

  4. Data availability statement: All data can be obtained from the corresponding author. The raw data from the TCGA database used in our investigation are accessible through Genomic Data Commons (GDC) Data Portal of TCGA repository (https://portal.gdc.cancer.gov/) and GTEx (https://gtexportal.org/home/datasets).

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Received: 2023-11-08
Revised: 2024-03-16
Accepted: 2024-04-05
Published Online: 2024-05-16

© 2024 the author(s), published by De Gruyter

This work is licensed under the Creative Commons Attribution 4.0 International License.

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https://doi.org/10.1515/med-2024-0962
Keywords for this article
EIF5A2; cancer; prognosis; meta-analysis; EMT
Creative Commons
BY 4.0

Articles in the same Issue

  1. Research Articles
  2. EDNRB inhibits the growth and migration of prostate cancer cells by activating the cGMP-PKG pathway
  3. STK11 (LKB1) mutation suppresses ferroptosis in lung adenocarcinoma by facilitating monounsaturated fatty acid synthesis
  4. Association of SOX6 gene polymorphisms with Kashin-Beck disease risk in the Chinese Han population
  5. The pyroptosis-related signature predicts prognosis and influences the tumor immune microenvironment in dedifferentiated liposarcoma
  6. METTL3 attenuates ferroptosis sensitivity in lung cancer via modulating TFRC
  7. Identification and validation of molecular subtypes and prognostic signature for stage I and stage II gastric cancer based on neutrophil extracellular traps
  8. Novel lumbar plexus block versus femoral nerve block for analgesia and motor recovery after total knee arthroplasty
  9. Correlation between ABCB1 and OLIG2 polymorphisms and the severity and prognosis of patients with cerebral infarction
  10. Study on the radiotherapy effect and serum neutral granulocyte lymphocyte ratio and inflammatory factor expression of nasopharyngeal carcinoma
  11. Transcriptome analysis of effects of Tecrl deficiency on cardiometabolic and calcium regulation in cardiac tissue
  12. Aflatoxin B1 induces infertility, fetal deformities, and potential therapies
  13. Serum levels of HMW adiponectin and its receptors are associated with cytokine levels and clinical characteristics in chronic obstructive pulmonary disease
  14. METTL3-mediated methylation of CYP2C19 mRNA may aggravate clopidogrel resistance in ischemic stroke patients
  15. Understand how machine learning impact lung cancer research from 2010 to 2021: A bibliometric analysis
  16. Pressure ulcers in German hospitals: Analysis of reimbursement and length of stay
  17. Metformin plus L-carnitine enhances brown/beige adipose tissue activity via Nrf2/HO-1 signaling to reduce lipid accumulation and inflammation in murine obesity
  18. Downregulation of carbonic anhydrase IX expression in mouse xenograft nasopharyngeal carcinoma model via doxorubicin nanobubble combined with ultrasound
  19. Feasibility of 3-dimensional printed models in simulated training and teaching of transcatheter aortic valve replacement
  20. miR-335-3p improves type II diabetes mellitus by IGF-1 regulating macrophage polarization
  21. The analyses of human MCPH1 DNA repair machinery and genetic variations
  22. Activation of Piezo1 increases the sensitivity of breast cancer to hyperthermia therapy
  23. Comprehensive analysis based on the disulfidptosis-related genes identifies hub genes and immune infiltration for pancreatic adenocarcinoma
  24. Changes of serum CA125 and PGE2 before and after high-intensity focused ultrasound combined with GnRH-a in treatment of patients with adenomyosis
  25. The clinical value of the hepatic venous pressure gradient in patients undergoing hepatic resection for hepatocellular carcinoma with or without liver cirrhosis
  26. Development and validation of a novel model to predict pulmonary embolism in cardiology suspected patients: A 10-year retrospective analysis
  27. Downregulation of lncRNA XLOC_032768 in diabetic patients predicts the occurrence of diabetic nephropathy
  28. Circ_0051428 targeting miR-885-3p/MMP2 axis enhances the malignancy of cervical cancer
  29. Effectiveness of ginkgo diterpene lactone meglumine on cognitive function in patients with acute ischemic stroke
  30. The construction of a novel prognostic prediction model for glioma based on GWAS-identified prognostic-related risk loci
  31. Evaluating the impact of childhood BMI on the risk of coronavirus disease 2019: A Mendelian randomization study
  32. Lactate dehydrogenase to albumin ratio is associated with in-hospital mortality in patients with acute heart failure: Data from the MIMIC-III database
  33. CD36-mediated podocyte lipotoxicity promotes foot process effacement
  34. Efficacy of etonogestrel subcutaneous implants versus the levonorgestrel-releasing intrauterine system in the conservative treatment of adenomyosis
  35. FLRT2 mediates chondrogenesis of nasal septal cartilage and mandibular condyle cartilage
  36. Challenges in treating primary immune thrombocytopenia patients undergoing COVID-19 vaccination: A retrospective study
  37. Let-7 family regulates HaCaT cell proliferation and apoptosis via the ΔNp63/PI3K/AKT pathway
  38. Phospholipid transfer protein ameliorates sepsis-induced cardiac dysfunction through NLRP3 inflammasome inhibition
  39. Postoperative cognitive dysfunction in elderly patients with colorectal cancer: A randomized controlled study comparing goal-directed and conventional fluid therapy
  40. Long-pulsed ultrasound-mediated microbubble thrombolysis in a rat model of microvascular obstruction
  41. High SEC61A1 expression predicts poor outcome of acute myeloid leukemia
  42. Comparison of polymerase chain reaction and next-generation sequencing with conventional urine culture for the diagnosis of urinary tract infections: A meta-analysis
  43. Secreted frizzled-related protein 5 protects against renal fibrosis by inhibiting Wnt/β-catenin pathway
  44. Pan-cancer and single-cell analysis of actin cytoskeleton genes related to disulfidptosis
  45. Overexpression of miR-532-5p restrains oxidative stress response of chondrocytes in nontraumatic osteonecrosis of the femoral head by inhibiting ABL1
  46. Autologous liver transplantation for unresectable hepatobiliary malignancies in enhanced recovery after surgery model
  47. Clinical analysis of incomplete rupture of the uterus secondary to previous cesarean section
  48. Abnormal sleep duration is associated with sarcopenia in older Chinese people: A large retrospective cross-sectional study
  49. No genetic causality between obesity and benign paroxysmal vertigo: A two-sample Mendelian randomization study
  50. Identification and validation of autophagy-related genes in SSc
  51. Long non-coding RNA SRA1 suppresses radiotherapy resistance in esophageal squamous cell carcinoma by modulating glycolytic reprogramming
  52. Evaluation of quality of life in patients with schizophrenia: An inpatient social welfare institution-based cross-sectional study
  53. The possible role of oxidative stress marker glutathione in the assessment of cognitive impairment in multiple sclerosis
  54. Compilation of a self-management assessment scale for postoperative patients with aortic dissection
  55. Left atrial appendage closure in conjunction with radiofrequency ablation: Effects on left atrial functioning in patients with paroxysmal atrial fibrillation
  56. Effect of anterior femoral cortical notch grade on postoperative function and complications during TKA surgery: A multicenter, retrospective study
  57. Clinical characteristics and assessment of risk factors in patients with influenza A-induced severe pneumonia after the prevalence of SARS-CoV-2
  58. Analgesia nociception index is an indicator of laparoscopic trocar insertion-induced transient nociceptive stimuli
  59. High STAT4 expression correlates with poor prognosis in acute myeloid leukemia and facilitates disease progression by upregulating VEGFA expression
  60. Factors influencing cardiovascular system-related post-COVID-19 sequelae: A single-center cohort study
  61. HOXD10 regulates intestinal permeability and inhibits inflammation of dextran sulfate sodium-induced ulcerative colitis through the inactivation of the Rho/ROCK/MMPs axis
  62. Mesenchymal stem cell-derived exosomal miR-26a induces ferroptosis, suppresses hepatic stellate cell activation, and ameliorates liver fibrosis by modulating SLC7A11
  63. Endovascular thrombectomy versus intravenous thrombolysis for primary distal, medium vessel occlusion in acute ischemic stroke
  64. ANO6 (TMEM16F) inhibits gastrointestinal stromal tumor growth and induces ferroptosis
  65. Prognostic value of EIF5A2 in solid tumors: A meta-analysis and bioinformatics analysis
  66. The role of enhanced expression of Cx43 in patients with ulcerative colitis
  67. Choosing a COVID-19 vaccination site might be driven by anxiety and body vigilance
  68. Role of ICAM-1 in triple-negative breast cancer
  69. Cost-effectiveness of ambroxol in the treatment of Gaucher disease type 2
  70. HLA-DRB5 promotes immune thrombocytopenia via activating CD8+ T cells
  71. Efficacy and factors of myofascial release therapy combined with electrical and magnetic stimulation in the treatment of chronic pelvic pain syndrome
  72. Efficacy of tacrolimus monotherapy in primary membranous nephropathy
  73. Mechanisms of Tripterygium wilfordii Hook F on treating rheumatoid arthritis explored by network pharmacology analysis and molecular docking
  74. FBXO45 levels regulated ferroptosis renal tubular epithelial cells in a model of diabetic nephropathy by PLK1
  75. Optimizing anesthesia strategies to NSCLC patients in VATS procedures: Insights from drug requirements and patient recovery patterns
  76. Alpha-lipoic acid upregulates the PPARγ/NRF2/GPX4 signal pathway to inhibit ferroptosis in the pathogenesis of unexplained recurrent pregnancy loss
  77. Correlation between fat-soluble vitamin levels and inflammatory factors in paediatric community-acquired pneumonia: A prospective study
  78. CD1d affects the proliferation, migration, and apoptosis of human papillary thyroid carcinoma TPC-1 cells via regulating MAPK/NF-κB signaling pathway
  79. miR-let-7a inhibits sympathetic nerve remodeling after myocardial infarction by downregulating the expression of nerve growth factor
  80. Immune response analysis of solid organ transplantation recipients inoculated with inactivated COVID-19 vaccine: A retrospective analysis
  81. The H2Valdien derivatives regulate the epithelial–mesenchymal transition of hepatoma carcinoma cells through the Hedgehog signaling pathway
  82. Clinical efficacy of dexamethasone combined with isoniazid in the treatment of tuberculous meningitis and its effect on peripheral blood T cell subsets
  83. Comparison of short-segment and long-segment fixation in treatment of degenerative scoliosis and analysis of factors associated with adjacent spondylolisthesis
  84. Lycopene inhibits pyroptosis of endothelial progenitor cells induced by ox-LDL through the AMPK/mTOR/NLRP3 pathway
  85. Methylation regulation for FUNDC1 stability in childhood leukemia was up-regulated and facilitates metastasis and reduces ferroptosis of leukemia through mitochondrial damage by FBXL2
  86. Correlation of single-fiber electromyography studies and functional status in patients with amyotrophic lateral sclerosis
  87. Risk factors of postoperative airway obstruction complications in children with oral floor mass
  88. Expression levels and clinical significance of serum miR-19a/CCL20 in patients with acute cerebral infarction
  89. Physical activity and mental health trends in Korean adolescents: Analyzing the impact of the COVID-19 pandemic from 2018 to 2022
  90. Evaluating anemia in HIV-infected patients using chest CT
  91. Ponticulus posticus and skeletal malocclusion: A pilot study in a Southern Italian pre-orthodontic court
  92. Causal association of circulating immune cells and lymphoma: A Mendelian randomization study
  93. Assessment of the renal function and fibrosis indexes of conventional western medicine with Chinese medicine for dredging collaterals on treating renal fibrosis: A systematic review and meta-analysis
  94. Comprehensive landscape of integrator complex subunits and their association with prognosis and tumor microenvironment in gastric cancer
  95. New target-HMGCR inhibitors for the treatment of primary sclerosing cholangitis: A drug Mendelian randomization study
  96. Population pharmacokinetics of meropenem in critically ill patients
  97. Comparison of the ability of newly inflammatory markers to predict complicated appendicitis
  98. Comparative morphology of the cruciate ligaments: A radiological study
  99. Immune landscape of hepatocellular carcinoma: The central role of TP53-inducible glycolysis and apoptosis regulator
  100. Serum SIRT3 levels in epilepsy patients and its association with clinical outcomes and severity: A prospective observational study
  101. SHP-1 mediates cigarette smoke extract-induced epithelial–mesenchymal transformation and inflammation in 16HBE cells
  102. Acute hyper-hypoxia accelerates the development of depression in mice via the IL-6/PGC1α/MFN2 signaling pathway
  103. The GJB3 correlates with the prognosis, immune cell infiltration, and therapeutic responses in lung adenocarcinoma
  104. Physical fitness and blood parameters outcomes of breast cancer survivor in a low-intensity circuit resistance exercise program
  105. Exploring anesthetic-induced gene expression changes and immune cell dynamics in atrial tissue post-coronary artery bypass graft surgery
  106. Empagliflozin improves aortic injury in obese mice by regulating fatty acid metabolism
  107. Analysis of the risk factors of the radiation-induced encephalopathy in nasopharyngeal carcinoma: A retrospective cohort study
  108. Reproductive outcomes in women with BRCA 1/2 germline mutations: A retrospective observational study and literature review
  109. Evaluation of upper airway ultrasonographic measurements in predicting difficult intubation: A cross-section of the Turkish population
  110. Prognostic and diagnostic value of circulating IGFBP2 in pancreatic cancer
  111. Postural stability after operative reconstruction of the AFTL in chronic ankle instability comparing three different surgical techniques
  112. Research trends related to emergence agitation in the post-anaesthesia care unit from 2001 to 2023: A bibliometric analysis
  113. Frequency and clinicopathological correlation of gastrointestinal polyps: A six-year single center experience
  114. ACSL4 mediates inflammatory bowel disease and contributes to LPS-induced intestinal epithelial cell dysfunction by activating ferroptosis and inflammation
  115. Affibody-based molecular probe 99mTc-(HE)3ZHER2:V2 for non-invasive HER2 detection in ovarian and breast cancer xenografts
  116. Effectiveness of nutritional support for clinical outcomes in gastric cancer patients: A meta-analysis of randomized controlled trials
  117. The relationship between IFN-γ, IL-10, IL-6 cytokines, and severity of the condition with serum zinc and Fe in children infected with Mycoplasma pneumoniae
  118. Paraquat disrupts the blood–brain barrier by increasing IL-6 expression and oxidative stress through the activation of PI3K/AKT signaling pathway
  119. Sleep quality associate with the increased prevalence of cognitive impairment in coronary artery disease patients: A retrospective case–control study
  120. Dioscin protects against chronic prostatitis through the TLR4/NF-κB pathway
  121. Association of polymorphisms in FBN1, MYH11, and TGF-β signaling-related genes with susceptibility of sporadic thoracic aortic aneurysm and dissection in the Zhejiang Han population
  122. Application value of multi-parameter magnetic resonance image-transrectal ultrasound cognitive fusion in prostate biopsy
  123. Laboratory variables‐based artificial neural network models for predicting fatty liver disease: A retrospective study
  124. Decreased BIRC5-206 promotes epithelial–mesenchymal transition in nasopharyngeal carcinoma through sponging miR-145-5p
  125. Sepsis induces the cardiomyocyte apoptosis and cardiac dysfunction through activation of YAP1/Serpine1/caspase-3 pathway
  126. Assessment of iron metabolism and iron deficiency in incident patients on incident continuous ambulatory peritoneal dialysis
  127. Tibial periosteum flap combined with autologous bone grafting in the treatment of Gustilo-IIIB/IIIC open tibial fractures
  128. The application of intravenous general anesthesia under nasopharyngeal airway assisted ventilation undergoing ureteroscopic holmium laser lithotripsy: A prospective, single-center, controlled trial
  129. Long intergenic noncoding RNA for IGF2BP2 stability suppresses gastric cancer cell apoptosis by inhibiting the maturation of microRNA-34a
  130. Role of FOXM1 and AURKB in regulating keratinocyte function in psoriasis
  131. Parental control attitudes over their pre-school children’s diet
  132. The role of auto-HSCT in extranodal natural killer/T cell lymphoma
  133. Significance of negative cervical cytology and positive HPV in the diagnosis of cervical lesions by colposcopy
  134. Echinacoside inhibits PASMCs calcium overload to prevent hypoxic pulmonary artery remodeling by regulating TRPC1/4/6 and calmodulin
  135. ADAR1 plays a protective role in proximal tubular cells under high glucose conditions by attenuating the PI3K/AKT/mTOR signaling pathway
  136. The risk of cancer among insulin glargine users in Lithuania: A retrospective population-based study
  137. The unusual location of primary hydatid cyst: A case series study
  138. Intraoperative changes in electrophysiological monitoring can be used to predict clinical outcomes in patients with spinal cavernous malformation
  139. Obesity and risk of placenta accreta spectrum: A meta-analysis
  140. Shikonin alleviates asthma phenotypes in mice via an airway epithelial STAT3-dependent mechanism
  141. NSUN6 and HTR7 disturbed the stability of carotid atherosclerotic plaques by regulating the immune responses of macrophages
  142. The effect of COVID-19 lockdown on admission rates in Maternity Hospital
  143. Temporal muscle thickness is not a prognostic predictor in patients with high-grade glioma, an experience at two centers in China
  144. Luteolin alleviates cerebral ischemia/reperfusion injury by regulating cell pyroptosis
  145. Therapeutic role of respiratory exercise in patients with tuberculous pleurisy
  146. Effects of CFTR-ENaC on spinal cord edema after spinal cord injury
  147. Irisin-regulated lncRNAs and their potential regulatory functions in chondrogenic differentiation of human mesenchymal stem cells
  148. DMD mutations in pediatric patients with phenotypes of Duchenne/Becker muscular dystrophy
  149. Combination of C-reactive protein and fibrinogen-to-albumin ratio as a novel predictor of all-cause mortality in heart failure patients
  150. Significant role and the underly mechanism of cullin-1 in chronic obstructive pulmonary disease
  151. Ferroptosis-related prognostic model of mantle cell lymphoma
  152. Observation of choking reaction and other related indexes in elderly painless fiberoptic bronchoscopy with transnasal high-flow humidification oxygen therapy
  153. A bibliometric analysis of Prader-Willi syndrome from 2002 to 2022
  154. The causal effects of childhood sunburn occasions on melanoma: A univariable and multivariable Mendelian randomization study
  155. Oxidative stress regulates glycogen synthase kinase-3 in lymphocytes of diabetes mellitus patients complicated with cerebral infarction
  156. Role of COX6C and NDUFB3 in septic shock and stroke
  157. Trends in disease burden of type 2 diabetes, stroke, and hypertensive heart disease attributable to high BMI in China: 1990–2019
  158. Purinergic P2X7 receptor mediates hyperoxia-induced injury in pulmonary microvascular endothelial cells via NLRP3-mediated pyroptotic pathway
  159. Investigating the role of oviductal mucosa–endometrial co-culture in modulating factors relevant to embryo implantation
  160. Analgesic effect of external oblique intercostal block in laparoscopic cholecystectomy: A retrospective study
  161. Elevated serum miR-142-5p correlates with ischemic lesions and both NSE and S100β in ischemic stroke patients
  162. Correlation between the mechanism of arteriopathy in IgA nephropathy and blood stasis syndrome: A cohort study
  163. Risk factors for progressive kyphosis after percutaneous kyphoplasty in osteoporotic vertebral compression fracture
  164. Predictive role of neuron-specific enolase and S100-β in early neurological deterioration and unfavorable prognosis in patients with ischemic stroke
  165. The potential risk factors of postoperative cognitive dysfunction for endovascular therapy in acute ischemic stroke with general anesthesia
  166. Fluoxetine inhibited RANKL-induced osteoclastic differentiation in vitro
  167. Detection of serum FOXM1 and IGF2 in patients with ARDS and their correlation with disease and prognosis
  168. Rhein promotes skin wound healing by activating the PI3K/AKT signaling pathway
  169. Differences in mortality risk by levels of physical activity among persons with disabilities in South Korea
  170. Review Articles
  171. Cutaneous signs of selected cardiovascular disorders: A narrative review
  172. XRCC1 and hOGG1 polymorphisms and endometrial carcinoma: A meta-analysis
  173. A narrative review on adverse drug reactions of COVID-19 treatments on the kidney
  174. Emerging role and function of SPDL1 in human health and diseases
  175. Adverse reactions of piperacillin: A literature review of case reports
  176. Molecular mechanism and intervention measures of microvascular complications in diabetes
  177. Regulation of mesenchymal stem cell differentiation by autophagy
  178. Molecular landscape of borderline ovarian tumours: A systematic review
  179. Advances in synthetic lethality modalities for glioblastoma multiforme
  180. Investigating hormesis, aging, and neurodegeneration: From bench to clinics
  181. Frankincense: A neuronutrient to approach Parkinson’s disease treatment
  182. Sox9: A potential regulator of cancer stem cells in osteosarcoma
  183. Early detection of cardiovascular risk markers through non-invasive ultrasound methodologies in periodontitis patients
  184. Advanced neuroimaging and criminal interrogation in lie detection
  185. Maternal factors for neural tube defects in offspring: An umbrella review
  186. The chemoprotective hormetic effects of rosmarinic acid
  187. CBD’s potential impact on Parkinson’s disease: An updated overview
  188. Progress in cytokine research for ARDS: A comprehensive review
  189. Utilizing reactive oxygen species-scavenging nanoparticles for targeting oxidative stress in the treatment of ischemic stroke: A review
  190. NRXN1-related disorders, attempt to better define clinical assessment
  191. Lidocaine infusion for the treatment of complex regional pain syndrome: Case series and literature review
  192. Trends and future directions of autophagy in osteosarcoma: A bibliometric analysis
  193. Iron in ventricular remodeling and aneurysms post-myocardial infarction
  194. Case Reports
  195. Sirolimus potentiated angioedema: A case report and review of the literature
  196. Identification of mixed anaerobic infections after inguinal hernia repair based on metagenomic next-generation sequencing: A case report
  197. Successful treatment with bortezomib in combination with dexamethasone in a middle-aged male with idiopathic multicentric Castleman’s disease: A case report
  198. Complete heart block associated with hepatitis A infection in a female child with fatal outcome
  199. Elevation of D-dimer in eosinophilic gastrointestinal diseases in the absence of venous thrombosis: A case series and literature review
  200. Four years of natural progressive course: A rare case report of juvenile Xp11.2 translocations renal cell carcinoma with TFE3 gene fusion
  201. Advancing prenatal diagnosis: Echocardiographic detection of Scimitar syndrome in China – A case series
  202. Outcomes and complications of hemodialysis in patients with renal cancer following bilateral nephrectomy
  203. Anti-HMGCR myopathy mimicking facioscapulohumeral muscular dystrophy
  204. Recurrent opportunistic infections in a HIV-negative patient with combined C6 and NFKB1 mutations: A case report, pedigree analysis, and literature review
  205. Letter to the Editor
  206. Letter to the Editor: Total parenteral nutrition-induced Wernicke’s encephalopathy after oncologic gastrointestinal surgery
  207. Erratum
  208. Erratum to “Bladder-embedded ectopic intrauterine device with calculus”
  209. Retraction
  210. Retraction of “XRCC1 and hOGG1 polymorphisms and endometrial carcinoma: A meta-analysis”
  211. Corrigendum
  212. Corrigendum to “Investigating hormesis, aging, and neurodegeneration: From bench to clinics”
  213. Corrigendum to “Frankincense: A neuronutrient to approach Parkinson’s disease treatment”
  214. Special Issue The evolving saga of RNAs from bench to bedside - Part II
  215. Machine-learning-based prediction of a diagnostic model using autophagy-related genes based on RNA sequencing for patients with papillary thyroid carcinoma
  216. Unlocking the future of hepatocellular carcinoma treatment: A comprehensive analysis of disulfidptosis-related lncRNAs for prognosis and drug screening
  217. Elevated mRNA level indicates FSIP1 promotes EMT and gastric cancer progression by regulating fibroblasts in tumor microenvironment
  218. Special Issue Advancements in oncology: bridging clinical and experimental research - Part I
  219. Ultrasound-guided transperineal vs transrectal prostate biopsy: A meta-analysis of diagnostic accuracy and complication rates
  220. Assessment of diagnostic value of unilateral systematic biopsy combined with targeted biopsy in detecting clinically significant prostate cancer
  221. SENP7 inhibits glioblastoma metastasis and invasion by dissociating SUMO2/3 binding to specific target proteins
  222. MARK1 suppress malignant progression of hepatocellular carcinoma and improves sorafenib resistance through negatively regulating POTEE
  223. Analysis of postoperative complications in bladder cancer patients
  224. Carboplatin combined with arsenic trioxide versus carboplatin combined with docetaxel treatment for LACC: A randomized, open-label, phase II clinical study
  225. Special Issue Exploring the biological mechanism of human diseases based on MultiOmics Technology - Part I
  226. Comprehensive pan-cancer investigation of carnosine dipeptidase 1 and its prospective prognostic significance in hepatocellular carcinoma
  227. Identification of signatures associated with microsatellite instability and immune characteristics to predict the prognostic risk of colon cancer
  228. Single-cell analysis identified key macrophage subpopulations associated with atherosclerosis
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