Identification of immune checkpoint and cytokine signatures associated with the response to immune checkpoint blockade in gastrointestinal cancers

Cancer Immunol Immunother. 2021 Sep;70(9):2669-2679. doi: 10.1007/s00262-021-02878-8. Epub 2021 Feb 23.

Abstract

Immune checkpoint blockade (ICB) of the programmed cell death 1/programmed cell death ligand 1 (PD-1/PD-L1) immune checkpoint pathway has led to unprecedented advances in cancer therapy. However, the overall response rate of anti-PD-1/PD-L1 monotherapy is still unpromising, underscoring the need for predictive biomarkers. In this retrospective study, we collected pretreatment plasma samples from two independent cohorts of patients receiving ICB. To determine whether a signature of plasma cytokines could be associated with therapeutic efficacy, we systemically profiled cytokine clusters and functional groups in the discovery and validation datasets by using 59 multiplexed bead immunoassays and bioinformatics analysis. We first attempted to functionally classify the 59 immunological factors according to their biological classification or functional roles in the cancer-immunity cycle. Surprisingly, we observed that two signatures, the "checkpoint signature" and "trafficking of T-cell signature", were higher in the response subgroup than in the nonresponse subgroup in both the discovery and validation cohorts. Moreover, enrichment of the "checkpoint signature" was correlated with improved overall survival and progression-free survival in both datasets. In addition, we demonstrated that increased baseline levels of three checkpoint molecules (PD-L1, T-cell immunoglobulin mucin receptor 3 and T-cell-specific surface glycoprotein CD28) were common peripheral responsive correlates in both cohorts, thus rendering this "refined checkpoint signature" an ideal candidate for future verification. In the peripheral blood system, the "refined checkpoint signature" may function as a potential biomarker for anti-PD-1/PD-L1 monotherapy in gastrointestinal (GI) cancers.

Keywords: Biomarker; Cytokine; Immune checkpoint blockade; Predictive biomarker; Programmed cell death ligand 1.

MeSH terms

  • Biomarkers, Tumor*
  • Computational Biology
  • Cytokines / genetics
  • Cytokines / metabolism*
  • Gastrointestinal Neoplasms / diagnosis
  • Gastrointestinal Neoplasms / drug therapy
  • Gastrointestinal Neoplasms / etiology*
  • Gastrointestinal Neoplasms / metabolism
  • Gene Expression Profiling
  • Humans
  • Immune Checkpoint Inhibitors / pharmacology
  • Immune Checkpoint Inhibitors / therapeutic use
  • Immune Checkpoint Proteins / genetics
  • Immune Checkpoint Proteins / metabolism*
  • Immunohistochemistry
  • Kaplan-Meier Estimate
  • Male
  • Prognosis
  • Reproducibility of Results
  • Treatment Outcome

Substances

  • Biomarkers, Tumor
  • Cytokines
  • Immune Checkpoint Inhibitors
  • Immune Checkpoint Proteins