Ubiquitin-specific peptidase 2 inhibits epithelial-mesenchymal transition in clear cell renal cell carcinoma metastasis by downregulating the NF-κB pathway

Bioengineered. 2022 Feb;13(2):4455-4467. doi: 10.1080/21655979.2022.2033403.

Abstract

Clear cell renal cell carcinoma, the most common type of renal cancer, is associated with poor survival. Ubiquitin-specific peptidase 2 regulates the molecular mechanisms of cancer cells. However, its mechanism in clear cell renal cell carcinoma remains unclear. Quantitative real-time polymerase chain reaction, enzyme-linked immunosorbent assay, and immunohistochemistry were performed to assess ubiquitin-specific peptidase 2 expression in human clear cell renal cell carcinoma samples. Ubiquitin-specific peptidase 2 was weakly expressed in clear cell renal cell carcinoma samples and associated with poor patient outcomes. Ubiquitin-specific peptidase 2 inhibition promoted clear cell renal cell carcinoma cell proliferation, migration, and invasion. Ubiquitin-specific peptidase 2 overexpression inhibited clear cell renal cell carcinoma cell proliferation, migration, and invasion in vitro and in vivo. RNA-sequencing showed significant changes in the epithelial-mesenchymal transition-related pathways following ubiquitin-specific peptidase 2 knockdown. Western blotting was performed to detect the protein expression levels. Expression of p-nuclear factor-κB p65, N-cadherin, Vimentin, and Snail, which were markedly increased, as well as E-cadherin, which was decreased following ubiquitin-specific peptidase 2 knockdown. Rescue experiments using the nuclear factor-κB inhibitor BAY 11-7082 revealed that the migration and invasion abilities and the expression of epithelial-mesenchymal transition pathway proteins were inhibited in both the short hairpin RNA (shRNA) for ubiquitin-specific peptidase 2 and shRNA for negative control groups. Ubiquitin-specific peptidase 2 is a potential biomarker to distinguish clear cell renal cell carcinoma patients from healthy individuals. Ubiquitin-specific peptidase 2-mediated inhibition of epithelial-mesenchymal transition in clear cell renal cell carcinoma cells is dependent on the nuclear factor-κB pathway.

Keywords: Clear cell renal cell carcinoma; NF-κB; biomarker; epithelial mesenchymal transition; ubiquitin-specific peptidase 2.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Animals
  • Biomarkers, Tumor / genetics
  • Carcinoma, Renal Cell* / genetics
  • Carcinoma, Renal Cell* / metabolism
  • Carcinoma, Renal Cell* / pathology
  • Cell Line, Tumor
  • Down-Regulation / genetics
  • Epithelial-Mesenchymal Transition / genetics*
  • Humans
  • Kidney / pathology
  • Kidney Neoplasms* / genetics
  • Kidney Neoplasms* / metabolism
  • Kidney Neoplasms* / pathology
  • Male
  • Mice
  • Mice, Nude
  • NF-kappa B / genetics*
  • Signal Transduction / genetics
  • Ubiquitin-Specific Proteases / genetics*

Substances

  • Biomarkers, Tumor
  • NF-kappa B
  • Ubiquitin-Specific Proteases

Supplementary concepts

  • Clear-cell metastatic renal cell carcinoma

Grants and funding

This work was supported by the National Natural Science Foundation of China (Grant # 81971881) and Key Technology Research and Development Program of He’nan Educational Committee [Grant # 202102310447].