The Role of the Cytoskeletal Regulatory Protein, Mammalian Enabling Protein (Mena), in Invasion and Metastasis of HPV16-Related Oral Squamous Cell Carcinoma

Cells. 2024 Nov 28;13(23):1972. doi: 10.3390/cells13231972.

Abstract

Background: The objective of this study was to investigate the effect of mammalian-enabled protein (Mena) on invasion and metastasis of HPV16-related oral squamous cell carcinoma (OSCC) and the underlying mechanism.

Materials and methods: The Mena gene expression profile of HPV-related OSCC was analyzed from the TCGA, GEO and TIMER databases. Immunohistochemistry was performed to study Mena, and the expression of invasion and metastasis-related markers and their clinicopathological characteristics. The role of Mena in the biological behavior of OSCC cell lines was assessed through both non-transfected and stably transfected models, analyzing EMT-related markers in vitro. The effect of Mena on HPV16-related OSCC metastasis through immunodeficient mouse model in vivo.

Results: Mena expression was significantly decreased in HPV16-positive OSCC, and Mena expression in HPV16-negative OSCC was related with lymphatic metastasis and TNM stages, and E-cadherin, vimentin and MMP-2, but it was not statistically significant in HPV16-positive OSCC. Increased Mena expression was significantly correlated with a poor overall survival and disease-free survival in an HPV16-negative OSCC patient. Mena plays a vital role in promoting OSCC cell migration, invasion and metastasis.

Conclusions: Mena promotes OSCC invasion and metastasis in HPV-negative OSCC by activating the EMT process. However, Mena expression in OSCC infected with HPV16 is inhibited, thus suppressing its invasion and metastasis ability.

Keywords: Mena; epithelial–mesenchymal transition; human papillomavirus 16; metastasis; oral squamous cell carcinoma.

MeSH terms

  • Animals
  • Carcinoma, Squamous Cell* / metabolism
  • Carcinoma, Squamous Cell* / pathology
  • Carcinoma, Squamous Cell* / virology
  • Cell Line, Tumor
  • Cell Movement
  • Cytoskeletal Proteins / genetics
  • Cytoskeletal Proteins / metabolism
  • Epithelial-Mesenchymal Transition / genetics
  • Female
  • Gene Expression Regulation, Neoplastic
  • Human papillomavirus 16* / genetics
  • Human papillomavirus 16* / pathogenicity
  • Humans
  • Male
  • Mice
  • Mice, Nude
  • Middle Aged
  • Mouth Neoplasms* / genetics
  • Mouth Neoplasms* / metabolism
  • Mouth Neoplasms* / pathology
  • Mouth Neoplasms* / virology
  • Neoplasm Invasiveness*
  • Neoplasm Metastasis
  • Papillomavirus Infections / complications
  • Papillomavirus Infections / metabolism
  • Papillomavirus Infections / pathology
  • Papillomavirus Infections / virology

Substances

  • Cytoskeletal Proteins

Grants and funding

This work was supported by the Natural Science Foundation of Shaanxi Province (2024-YBQN-0769);and Shaanxi Provincial Health and Medical Research and Innovation Capacity Improvement Plan Project (No. 2024TD-19). The authors would like to thank the TCGA database for the availability of the data.