Increasing membrane polyunsaturated fatty acids sensitizes non-small cell lung cancer to anti-PD-1/PD-L1 immunotherapy

Cancer Lett. 2024 Nov 1:604:217221. doi: 10.1016/j.canlet.2024.217221. Epub 2024 Sep 6.

Abstract

Immune checkpoints inhibitors (ICIs) as anti-PD-1/anti-PD-L1 have been approved as first-line treatment in patients with non-small cell lung cancer (NSCLC), but only 25 % of patients achieve durable response. We previously unveiled that estrogen receptor α transcriptionally up-regulates PD-L1 and aromatase inhibitors such as letrozole increase the efficacy of pembrolizumab. Here we investigated if letrozole may have additional immune-sensitizing mechanisms. We found that higher the level of PD-L1 in NSCLC, higher the activation of SREBP1c that transcriptionally increases fatty acid synthase and stearoyl-CoA desaturase enzymes, increasing the amount of polyunsaturated fatty acids (PUFAs). Letrozole further up-regulated SREBP1c-mediated transcription of lipogenic genes, and increased the amount of PUFAs, thereby leading to greater membrane fluidity and reduced binding between PD-L1 and PD-1. The same effects were observed upon supplementation with ω3-PUFA docosahexaenoic acid (DHA) that enhanced the efficacy of pembrolizumab in humanized NSCLC immune-xenografts. We suggest that PUFA enrichment in membrane phospholipids improves the efficacy of ICIs. We propose to repurpose letrozole or DHA as new immune-sensitizing agents in NSCLC.

Keywords: Docosahexaenoic acid; Immune checkpoints inhibitors; Letrozole; Non-small cell lung cancer; Phospholipidome.

MeSH terms

  • Animals
  • Antibodies, Monoclonal, Humanized / pharmacology
  • Antibodies, Monoclonal, Humanized / therapeutic use
  • B7-H1 Antigen* / metabolism
  • Carcinoma, Non-Small-Cell Lung* / drug therapy
  • Carcinoma, Non-Small-Cell Lung* / immunology
  • Carcinoma, Non-Small-Cell Lung* / pathology
  • Cell Line, Tumor
  • Docosahexaenoic Acids / pharmacology
  • Fatty Acids, Unsaturated* / pharmacology
  • Female
  • Humans
  • Immune Checkpoint Inhibitors* / pharmacology
  • Immune Checkpoint Inhibitors* / therapeutic use
  • Immunotherapy / methods
  • Letrozole / pharmacology
  • Letrozole / therapeutic use
  • Lung Neoplasms* / drug therapy
  • Lung Neoplasms* / genetics
  • Lung Neoplasms* / immunology
  • Lung Neoplasms* / pathology
  • Mice
  • Programmed Cell Death 1 Receptor / antagonists & inhibitors
  • Programmed Cell Death 1 Receptor / metabolism
  • Stearoyl-CoA Desaturase / genetics
  • Stearoyl-CoA Desaturase / metabolism
  • Sterol Regulatory Element Binding Protein 1 / genetics
  • Sterol Regulatory Element Binding Protein 1 / metabolism
  • Xenograft Model Antitumor Assays

Substances

  • B7-H1 Antigen
  • Immune Checkpoint Inhibitors
  • CD274 protein, human
  • Fatty Acids, Unsaturated
  • Programmed Cell Death 1 Receptor
  • Letrozole
  • Antibodies, Monoclonal, Humanized
  • pembrolizumab
  • Sterol Regulatory Element Binding Protein 1
  • Stearoyl-CoA Desaturase
  • PDCD1 protein, human
  • SREBF1 protein, human
  • Docosahexaenoic Acids