Gastric cancer mesenchymal stem cells via the CXCR2/HK2/PD-L1 pathway mediate immunosuppression

Gastric Cancer. 2023 Sep;26(5):691-707. doi: 10.1007/s10120-023-01405-1. Epub 2023 Jun 10.

Abstract

Background: Anti-PD-1 immunotherapy has emerged as an important therapeutic modality in advanced gastric cancer (GC). However, drug resistance frequently develops, limiting its effectiveness.

Methods: The role of gastric cancer mesenchymal stem cells (GCMSCs) in anti-PD-1 resistance was evaluated in vivo in NPGCD34+ or NCGPBMC xenograft mouse model. In addition, we investigated CD8+T cell infiltration and effector function by spectral cytometry and IHC. The effects of GCMSCs conditional medium (GCMSC-CM) on GC cell lines were characterized at the level of the proteome, secretome using western blot, and ELISA assays.

Results: We reported that GCMSCs mediated tolerance mechanisms contribute to tumor immunotherapy tolerance. GCMSC-CM attenuated the antitumor activity of PD-1 antibody and inhibited immune response in humanized mouse model. In GC cells under serum deprivation and hypoxia, GCMSC-CM promoted GC cells proliferation via upregulating PD-L1 expression. Mechanistically, GCMSC-derived IL-8 and AKT-mediated phosphorylation facilitated HK2 nuclear localization. Phosphorylated-HK2 promoted PD-L1 transcription by binding to HIF-1α. What is more, GCMSC-CM also induced lactate overproduction in GC cells in vitro and xenograft tumors in vivo, leading to impaired function of CD8+ T cells. Furthermore, CXCR1/2 receptor depletion, CXCR2 receptor antagonist AZD5069 and IL-8 neutralizing antibody application also significantly reversed GCMSCs mediated immunosuppression, restoring the antitumor capacity of PD-1 antibody.

Conclusions: Our findings reveal that blocking GCMSCs-derived IL-8/CXCR2 pathway decreasing PD-L1 expression and lactate production, improving antitumor efficacy of anti-PD-1 immunotherapy, may be of value for the treatment of advanced gastric carcinoma.

Keywords: Anti-PD-1; CXCR2; Gastric cancer mesenchymal stem cells; HK2; IL-8.

MeSH terms

  • Animals
  • B7-H1 Antigen / metabolism
  • CD8-Positive T-Lymphocytes
  • Cell Line, Tumor
  • Humans
  • Immunosuppression Therapy
  • Interleukin-8 / metabolism
  • Leukocytes, Mononuclear / pathology
  • Mesenchymal Stem Cells* / metabolism
  • Mesenchymal Stem Cells* / pathology
  • Mice
  • Receptors, Interleukin-8B / metabolism
  • Stomach Neoplasms* / metabolism
  • Tumor Microenvironment

Substances

  • B7-H1 Antigen
  • Interleukin-8
  • Receptors, Interleukin-8B