Lovastatin-mediated pharmacological inhibition of Formin protein DIAPH1 suppresses tumor immune escape and boosts immunotherapy response

Int Immunopharmacol. 2025 Jan 10:144:113637. doi: 10.1016/j.intimp.2024.113637. Epub 2024 Nov 21.

Abstract

Background: The immunosuppressive tumor microenvironment (TME) is a key characteristic of human cancer. Immunotherapy has emerged as a promising treatment strategy to overcome immune escape and has gained widespread use in recent years. In particular, the blockade of PD-1/PD-L1 interaction holds significant importance in oncotherapy. Combining anti-PD-1/PD-L1 with small molecule inhibitors targeting key pathways represents an emerging trend in therapeutic development.

Methods: To validate our findings biologically, we employed qRT-PCR or Western blotting and immunofluorescence staining techniques to assess the expression levels of DIAPH1 and PD-L1 in cells. Additionally, CCK8 and clone formation assays were utilized to evaluate cell proliferation ability, while flow assays were conducted to detect apoptosis in T cells.

Results: Knockdown of DIAPH1 restored the tumor-killing capacity of T cells, effectively suppressing tumor immune escape. We observed a highly positive correlation between the expression levels of DIAPH1 and 3-hydroxy-3-methylglutaryl-CoA reductase (HMGCR), which can be competitively inhibited by lovastatin. Through Sybyl analysis followed by confirmation via micro scale thermophoresis, we identified lovastatin as a potential inhibitor targeting DIAPH1. Lovastatin downregulated DIAPH1 expression both in tumor cell lines and xenograft lung cancer tissues within a mouse lung cancer model. Furthermore, we found that lovastatin degraded DIAPH1 through lysosomal degradation pathway. Treatment with lovastatin was strongly associated with improved response rates and prolonged overall survival among patients with lung adenocarcinoma. Finally, overexpression of DIAPH1 reversed the inhibitory effects mediated by lovastatin on tumor development.

Conclusions: Lovastatin downregulates PD-L1 expression by targeting DIAPH1 and restores the tumor-killing ability of T cells to block tumor immune escape. Lovastatin may become a potential drug for cancer patients to enhance immunotherapy response in the clinic.

Keywords: DIAPH1; Immune escape; Lovastatin; PD-L1; Tumor microenvironment.

MeSH terms

  • Adaptor Proteins, Signal Transducing / genetics
  • Adaptor Proteins, Signal Transducing / metabolism
  • Animals
  • Apoptosis / drug effects
  • B7-H1 Antigen / antagonists & inhibitors
  • B7-H1 Antigen / metabolism
  • Cell Line, Tumor
  • Cell Proliferation / drug effects
  • Female
  • Formins*
  • Humans
  • Immunotherapy* / methods
  • Lovastatin* / pharmacology
  • Lovastatin* / therapeutic use
  • Lung Neoplasms / drug therapy
  • Lung Neoplasms / immunology
  • Mice
  • T-Lymphocytes / drug effects
  • T-Lymphocytes / immunology
  • Tumor Escape* / drug effects
  • Tumor Microenvironment / drug effects
  • Tumor Microenvironment / immunology

Substances

  • Formins
  • Lovastatin
  • DIAPH1 protein, human
  • B7-H1 Antigen
  • Adaptor Proteins, Signal Transducing
  • CD274 protein, human