SPOP promotes cervical cancer progression by inducing the movement of PD-1 away from PD-L1 in spatial localization

J Transl Med. 2022 Aug 30;20(1):384. doi: 10.1186/s12967-022-03574-6.

Abstract

Background: Metastasis is a major obstacle in the treatment of cervical cancer (CC), and SPOP-mediated regulatory effects are involved in metastasis. However, the mechanisms have not been fully elucidated.

Methods: Proteomic sequencing and SPOP immunohistochemistry (IHC) were performed for the pelvic lymph node (pLN)-positive and non-pLN groups of CC patients. The corresponding patients were stratified by SPOP expression level for overall survival (OS) and relapse-free survival (RFS) analysis. In vitro and in vivo tests were conducted to verify the causal relationship between SPOP expression and CC metastasis. Multiplex immunofluorescence (m-IF) and the HALO system were used to analyse the mechanism, which was further verified by in vitro experiments.

Results: SPOP is upregulated in CC with pLN metastasis and negatively associated with patient outcome. In vitro and in vivo, SPOP promotes CC proliferation and metastasis. According to m-IF and HALO analysis, SPOP may promote CC metastasis by promoting the separation of PD-1 from PD-L1. Finally, it was further verified that SPOP can achieve immune tolerance by promoting the movement of PD-1 away from PD-L1 in spatial location and function.

Conclusion: This study shows that SPOP can inhibit the immune microenvironment by promoting the movement of PD-1 away from PD-L1, thereby promoting pLN metastasis of CC and resulting in worse OS and RFS.

Keywords: CXCL16/CXCR6 axis; Cervical cancer; Multiplex immunofluorescence; PD-1/PD-L1 axis; SPOP.

MeSH terms

  • B7-H1 Antigen* / metabolism
  • Female
  • Humans
  • Lymphatic Metastasis
  • Neoplasm Recurrence, Local
  • Nuclear Proteins / metabolism*
  • Programmed Cell Death 1 Receptor / metabolism
  • Proteomics
  • Repressor Proteins / metabolism*
  • Tumor Microenvironment
  • Uterine Cervical Neoplasms* / genetics

Substances

  • B7-H1 Antigen
  • Nuclear Proteins
  • Programmed Cell Death 1 Receptor
  • Repressor Proteins
  • SPOP protein, human