Mapping the genetic landscape establishing a tumor immune microenvironment favorable for anti-PD-1 response

Cell Rep. 2025 May 27;44(5):115698. doi: 10.1016/j.celrep.2025.115698. Epub 2025 May 8.

Abstract

Identifying host genetic factors modulating immune checkpoint inhibitor (ICI) efficacy is experimentally challenging. Our approach, utilizing the Collaborative Cross mouse genetic resource, fixes the tumor genomic configuration while varying host genetics. We find that response to anti-PD-1 (aPD1) immunotherapy is significantly heritable in four distinct murine tumor models (H2: 0.18-0.40). For the MC38 colorectal carcinoma system, we map four significant ICI response quantitative trait loci (QTLs) with significant epistatic interactions. The differentially expressed genes within these QTLs that define responder genetics are highly enriched for processes involving antigen processing and presentation, allograft rejection, and graft vs. host disease (all p < 1 × 10-10). Functional blockade of two top candidate immune targets, GM-CSF and IL-2RB, completely abrogates the MC38 transcriptional response to aPD1 therapy. Thus, our in vivo experimental platform is a powerful approach for discovery of host genetic factors that establish the tumor immune microenvironment propitious for ICI response.

Keywords: CP: Cancer; CP: Immunology; QTL mapping; genetics; heritability; immunotherapy; murine models; tumor immune microenvironment.

MeSH terms

  • Animals
  • Cell Line, Tumor
  • Colorectal Neoplasms / drug therapy
  • Colorectal Neoplasms / genetics
  • Colorectal Neoplasms / immunology
  • Female
  • Humans
  • Immune Checkpoint Inhibitors* / pharmacology
  • Immune Checkpoint Inhibitors* / therapeutic use
  • Immunotherapy
  • Mice
  • Mice, Inbred C57BL
  • Programmed Cell Death 1 Receptor* / antagonists & inhibitors
  • Programmed Cell Death 1 Receptor* / immunology
  • Programmed Cell Death 1 Receptor* / metabolism
  • Quantitative Trait Loci / genetics
  • Tumor Microenvironment* / drug effects
  • Tumor Microenvironment* / genetics
  • Tumor Microenvironment* / immunology

Substances

  • Programmed Cell Death 1 Receptor
  • Immune Checkpoint Inhibitors