Molecular heterogeneity in urothelial carcinoma and determinants of clinical benefit to PD-L1 blockade

Cancer Cell. 2024 Dec 9;42(12):2098-2112.e4. doi: 10.1016/j.ccell.2024.10.016. Epub 2024 Nov 21.

Abstract

Checkpoint inhibitors targeting programmed cell death protein 1 (PD-1)/programmed death-ligand 1 (PD-L1) have revolutionized cancer therapy across many indications including urothelial carcinoma (UC). Because many patients do not benefit, a better understanding of the molecular mechanisms underlying response and resistance is needed to improve outcomes. We profiled tumors from 2,803 UC patients from four late-stage randomized clinical trials evaluating the PD-L1 inhibitor atezolizumab by RNA sequencing (RNA-seq), a targeted DNA panel, immunohistochemistry, and digital pathology. Machine learning identifies four transcriptional subtypes, representing luminal desert, stromal, immune, and basal tumors. Overall survival benefit from atezolizumab over standard-of-care is observed in immune and basal tumors, through different response mechanisms. A self-supervised digital pathology approach can classify molecular subtypes from H&E slides with high accuracy, which could accelerate tumor molecular profiling. This study represents a large integration of UC molecular and clinical data in randomized trials, paving the way for clinical studies tailoring treatment to specific molecular subtypes in UC and other indications.

Keywords: PD-L1 blockade; digital pathology; molecular heterogeneity; patient stratification; transcriptomics; urothelial carcinoma.

MeSH terms

  • Aged
  • Antibodies, Monoclonal, Humanized* / therapeutic use
  • B7-H1 Antigen* / antagonists & inhibitors
  • B7-H1 Antigen* / genetics
  • B7-H1 Antigen* / metabolism
  • Biomarkers, Tumor / genetics
  • Biomarkers, Tumor / metabolism
  • Carcinoma, Transitional Cell / drug therapy
  • Carcinoma, Transitional Cell / genetics
  • Carcinoma, Transitional Cell / pathology
  • Female
  • Genetic Heterogeneity
  • Humans
  • Immune Checkpoint Inhibitors* / pharmacology
  • Immune Checkpoint Inhibitors* / therapeutic use
  • Male
  • Urinary Bladder Neoplasms / drug therapy
  • Urinary Bladder Neoplasms / genetics
  • Urinary Bladder Neoplasms / pathology

Substances

  • Immune Checkpoint Inhibitors
  • atezolizumab
  • B7-H1 Antigen
  • Antibodies, Monoclonal, Humanized
  • CD274 protein, human
  • Biomarkers, Tumor