The clinical significance of UBE2C gene in progression of renal cell carcinoma

Eur J Histochem 2021 AI 6 Explanations View Original
Original Paper (PDF)

Unable to display PDF. Download it here or view on PMC.

Plain-English Explanations
Pages 1-2
UBE2C: A Ubiquitin Pathway Gene with Unknown Role in RCC

Renal cell carcinoma (RCC) is among the most clinically challenging urological malignancies, with a five-year survival rate of only 12% for patients with distant metastasis. The primary treatment is surgical resection, as RCC is generally resistant to conventional chemotherapy and radiotherapy, and targeted therapy benefits only 20-40% of patients.

UBE2C (ubiquitin-conjugating enzyme E2C) belongs to the ubiquitin E2 enzyme family and functions as a substrate recognition component of SCF ubiquitin ligase complexes that target cell cycle regulatory proteins for proteasomal degradation. Its substrates are centrally involved in the control of cell mitosis, placing it mechanistically at the intersection of cell proliferation and genome stability.

UBE2C had been previously identified as oncogenic in breast cancer, colon cancer, ovarian cancer, gastric cancer, and liver cancer, where it promotes proliferation, invasion, and chemoresistance. Its expression correlates with tumor stage and poor prognosis in these cancers, suggesting it may be a broadly relevant cancer driver.

Despite this evidence in other malignancies, the expression, clinical significance, and functional role of UBE2C specifically in RCC had not been studied. This work used TCGA bioinformatics analysis, clinical tissue validation, and in vitro functional experiments to fill that gap.

TL;DR: UBE2C is a ubiquitin E2 enzyme with established oncogenic roles in multiple cancers but no prior characterization in renal cell carcinoma, motivating this comprehensive clinical and functional analysis.
Pages 3-5
UBE2C Overexpression in RCC Correlates with Stage and Poor Survival

Analysis of 525 RCC cases and 72 normal renal tissues from the TCGA database demonstrated that UBE2C mRNA expression was significantly higher in RCC tissues than in normal controls (p less than 0.05), with mean UBE2C expression in RCC being five times higher than in normal kidney tissue. Stage IV patients showed significantly higher UBE2C expression than Stage I patients, establishing a dose-response relationship between expression level and disease advancement.

Validation in 90 clinical RCC tissue samples by RT-qPCR confirmed the TCGA findings, with UBE2C mRNA significantly elevated in tumor versus matched adjacent normal tissue. Immunohistochemical (IHC) analysis of the same clinical cohort further confirmed UBE2C protein overexpression at the tissue level, providing multi-platform biological validation across mRNA and protein levels.

Chi-square analysis revealed that high UBE2C expression was significantly associated with TNM stage (p = 6.83e-10), pathological stage (p = 5.32e-11), gender (p = 0.009), and survival status (p = 2.87e-9), but not with patient age. Notably, 45.42% of T3 patients showed high UBE2C expression compared to only 21.67% showing low expression, and death rates were 41.98% in the high-UBE2C group versus 17.87% in the low-UBE2C group.

Kaplan-Meier analysis demonstrated that RCC patients with higher UBE2C expression (n = 262) showed significantly shorter overall survival and progression-free survival compared to those with lower expression (n = 263), both with p less than 0.05. Multivariate Cox regression confirmed UBE2C as an independent prognostic factor for OS (HR = 1.013, 95% CI 1.006-1.020, p = 0.00017) after adjusting for gender, T, N, M, stage, and age.

TL;DR: UBE2C is expressed at 5-fold higher levels in RCC than normal kidney, associates with advanced TNM and pathological stage, and independently predicts worse OS and PFS in multivariate Cox analysis.
Pages 5-7
Cell Cycle and DNA Replication as Top UBE2C-Associated Pathways

GO enrichment analysis of differentially expressed genes associated with UBE2C in RCC identified cell division (86 genes), mitotic nuclear division (67 genes), sister chromatid cohesion (45 genes), and DNA replication (47 genes) as the most significantly enriched biological processes. These processes collectively define the core machinery of cell proliferation and genome duplication, establishing a mechanistic framework for UBE2C's oncogenic role.

KEGG pathway analysis revealed that cell cycle was the most significantly enriched pathway (40 DEGs, p = 4.66e-28), followed by DNA replication (13 DEGs, p = 1.48e-10), Fanconi anemia pathway (13 DEGs), and p53 signaling pathway (13 DEGs). The convergence of cell cycle and DNA replication as the top two pathways is consistent with UBE2C's known function as a regulator of cyclin-dependent processes through targeted protein ubiquitination.

The enrichment of p53 signaling pathway genes among UBE2C-associated DEGs is particularly notable given p53's role as a master regulator of cell cycle arrest and apoptosis in response to genomic damage. UBE2C-mediated dysregulation of this pathway could contribute to the chromosomal instability and uncontrolled proliferation characteristic of aggressive RCC.

The breadth of pathway involvement -- spanning cell cycle control, DNA repair (Fanconi anemia pathway, homologous recombination, mismatch repair), cellular senescence, and proteasomal degradation -- suggests UBE2C exerts pleiotropic effects on RCC biology rather than acting through a single mechanistic axis.

TL;DR: GO and KEGG analyses identify cell cycle and DNA replication as the top pathways associated with UBE2C in RCC, with additional enrichment in p53 signaling, DNA repair, and proteasomal degradation pathways.
Pages 2, 3, 6, 7
Integrating Bioinformatics, Clinical Tissue, and In Vitro Validation

TCGA data were extracted for 525 RCC cases and 72 normal controls. mRNA expression of UBE2C was analyzed using RStudio, with survival curves generated by Kaplan-Meier analysis and Cox regression performed for univariate and multivariate prognostic modeling. GO and KEGG enrichment analysis was performed using DAVID 6.8 and Cytoscape Enrichment Map for pathway visualization.

Clinical tissue validation used 90 RCC and matched normal tissue samples from patients who underwent radical nephrectomy between 2006 and 2010 at Gannan Medical University's First Affiliated Hospital, with follow-up through August 2017. UBE2C expression was quantified by RT-qPCR using SYBR Green chemistry and confirmed at the protein level by IHC with a validated anti-UBE2C antibody (Abcam ab252940, 1:500 dilution).

Functional characterization used RNA interference to knock down UBE2C in 786-O cells (a widely used clear cell RCC cell line) with siRNA targeting the sequence 5'-TCCTTTTTGTGATTTCTGTATAG-3'. Knockdown efficiency exceeded 66% by RT-qPCR confirmation. Cell proliferation was measured by CCK-8 assay over 96 hours, and cell migration was assessed by Matrigel transwell invasion assay at 24 hours.

Statistical analysis used independent samples t-test for TCGA mRNA comparisons, chi-square or Fisher's exact test for clinicopathological correlations, and log-rank test for Kaplan-Meier comparisons, with p less than 0.05 as the significance threshold throughout.

TL;DR: A three-tier validation strategy combined TCGA bioinformatics (525 patients), clinical tissue RT-qPCR and IHC (90 patients), and siRNA functional assays in 786-O RCC cells to characterize UBE2C's role.
Pages 7-8
UBE2C Knockdown Inhibits RCC Cell Proliferation and Migration

UBE2C knockdown by siRNA in 786-O RCC cells achieved greater than 66% reduction in UBE2C mRNA expression, providing a functionally validated loss-of-function model. CCK-8 proliferation assay showed that UBE2C-deficient cells exhibited dramatically reduced growth: proliferation fold in the knockdown group was only 1.53 compared to 3.49 in controls at day 3, representing an approximately 56% reduction in proliferative capacity.

Matrigel transwell migration assay demonstrated that UBE2C knockdown reduced 786-O cell migration by approximately 44% compared to negative controls, confirming that UBE2C contributes to the invasive and migratory behavior of RCC cells in addition to their proliferative capacity.

Together, the inhibition of both proliferation and migration following UBE2C silencing establishes that UBE2C is functionally required for the maintenance of the malignant phenotype in RCC cells, not merely a bystander marker of tumor aggressiveness.

These functional findings, combined with the strong clinical associations between UBE2C expression and TNM stage, pathological stage, OS, and PFS, support UBE2C as a candidate therapeutic target for advanced RCC, particularly given that it operates in the ubiquitin-proteasome system, a pathway with several druggable components under clinical investigation in other cancers.

TL;DR: UBE2C knockdown in 786-O RCC cells reduced proliferation by approximately 56% and migration by 44%, functionally confirming its role as a driver of malignant behavior and potential therapeutic target.
Page 8
UBE2C as a Prognostic Biomarker and Therapeutic Target in RCC

This study provides the first comprehensive characterization of UBE2C in RCC, demonstrating its overexpression at 5-fold above normal tissue levels, its independent prognostic significance in multivariate Cox analysis, and its functional requirement for RCC cell proliferation and migration.

The strong associations between UBE2C and TNM stage, pathological stage, OS, and PFS across both the large TCGA cohort and independent clinical samples establish its validity as a prognostic biomarker for risk stratification in RCC patients.

Future research should investigate the specific molecular mechanisms through which UBE2C regulates cell cycle progression and DNA replication in RCC, examine its interaction with p53 pathway components, and evaluate whether UBE2C expression predicts response to targeted therapies or immunotherapy in metastatic RCC.

The druggability of the ubiquitin-proteasome pathway, combined with UBE2C's functional importance demonstrated here, positions it as a compelling target for novel RCC therapeutics, particularly for the substantial proportion of patients who fail or are ineligible for existing treatment regimens.

TL;DR: UBE2C is an independent prognostic factor in RCC with functional roles in proliferation and migration, establishing it as both a biomarker for risk stratification and a candidate therapeutic target.
Citation: Open Access, 2021. Available at: PMC8054571.