Improving IL12 immunotherapy in glioblastoma by targeting the long noncoding RNA INCR1

J Neurooncol. 2025 May;173(1):205-216. doi: 10.1007/s11060-025-04978-2. Epub 2025 Mar 4.

Abstract

Purpose: The potent antitumor effects of interleukin 12 (IL12) gene therapy in glioblastoma (GBM) are significantly attenuated by the highly immunosuppressive microenvironment and the upregulation of the PD-1/PD-L1 immune checkpoint. However, combining IL12 gene therapy with PD-1/PD-L1 inhibitors failed to improve efficacy. This study aims to assess the effects of silencing the immunosuppressive long noncoding RNA INCR1 when combined with IL12 therapy.

Methods: RNAscope in situ hybridization was performed to analyze INCR1 and PD-L1 expression in tumor tissues from GBM patients pre- and post-IL12 gene therapy. Quantitative PCR was used to analyze immunosuppressive gene expression in patient-derived GBM cells co-cultured with immune cells stimulated with IL12. The effects of INCR1 and PD-L1 silencing on the expression of immunosuppressive genes were evaluated by RNA sequencing. 3D-cytotoxicity assays were performed to assess the activity of immune cells against GBM tumor cells.

Results: INCR1 and PD-L1 expression was upregulated in tumor tissue from GBM patients treated with IL12 gene therapy compared to the tumor tissue of the same patients before the IL12 treatment. Co-culture of patient-derived GBM cells with IL12-stimulated immune cells increased the expression of several immunosuppressive genes. Knocking down INCR1 was more effective than silencing PD-L1 in reducing the expression of multiple immunosuppressive genes. INCR1 silencing improved IL12-mediated immune cell antitumor activity compared to monoclonal antibodies targeting the PD-1/PD-L1 immune checkpoint signaling.

Conclusion: INCR1 silencing affects more immune evasive pathways than PD-L1. Targeting INCR1 may represent a valid approach to improve the efficacy of IL12 therapy in GBM.

Keywords: INCR1; GBM; IL12; Immunotherapy; PD-L1.

MeSH terms

  • B7-H1 Antigen / genetics
  • B7-H1 Antigen / metabolism
  • Brain Neoplasms* / genetics
  • Brain Neoplasms* / immunology
  • Brain Neoplasms* / pathology
  • Brain Neoplasms* / therapy
  • Gene Expression Regulation, Neoplastic
  • Genetic Therapy* / methods
  • Glioblastoma* / genetics
  • Glioblastoma* / immunology
  • Glioblastoma* / pathology
  • Glioblastoma* / therapy
  • Humans
  • Immunotherapy* / methods
  • Interleukin-12* / genetics
  • Interleukin-12* / therapeutic use
  • RNA, Long Noncoding* / genetics
  • RNA, Long Noncoding* / metabolism

Substances

  • RNA, Long Noncoding
  • Interleukin-12
  • CD274 protein, human
  • B7-H1 Antigen