High efficacy of PD-1 inhibitor after initial failure of PD-L1 inhibitor in Relapsed/Refractory classical Hodgkin Lymphoma

BMC Cancer. 2022 Jan 3;22(1):9. doi: 10.1186/s12885-021-09028-4.

Abstract

Purpose: We sought to understand the clinical course and molecular phenotype of patients who showed disease progression after programmed cell death ligand 1 (PD-L1) inhibitor treatment but subsequently responded to PD-1 inhibitor treatment. We also explored the response to PD-1-axis targeted therapy of classical Hodgkin lymphoma (cHL) according to genetically driven PD-L1 and programmed cell death ligand 2 (PD-L2) expression.

Methods: Five patients in a phase II clinical trial of CS1001 (PD-L1 inhibitor) for relapsed or refractory (R/R) cHL were retrospectively reviewed. Formalin-fixed, paraffin-embedded whole tissues from the five patients were evaluated for 9p24.1 genetic alterations based on FISH and the expression of PD-L1, PD-L2, PD-1, major histocompatibility complex (MHC) class I-II, and the tumor microenvironment factorsCD163 and FOXP3 in the microenvironmental niche, as revealed by multiplex immunofluorescence.

Results: All five patients showed primary refractory disease during first-line treatment. Four patients received PD-1 inhibitor after dropping out of the clinical trial, and all demonstrated at least a partial response. The progression-free survival ranged from 7 to 28 months (median = 18 months), and 9p24.1 amplification was observed in all five patients at the PD-L1/PD-L2 locus. PD-L1 and PD-L2 were colocalized on Hodgkin Reed-Sternberg (HRS) cells in four of the five (80%) patients. There was differential expression of PD-L1 and PD-L2 in cells in the tumor microenvironment in cHL, especially in HRS cells, background cells and tumor-associated macrophages.

Conclusions: PD-L1 monotherapy may not be sufficient to block the PD-1 pathway; PD-L2 was expressed in HRS and background cells in cHL. The immunologic function of the PD-L2 pathway in anti-tumor activity may be underestimated in R/R cHL. Further study is needed to elucidate the anti-tumor mechanism of PD-1 inhibitor and PD-L1 inhibitor treatment.

Keywords: Hodgkin lymphoma; Molecular phenotype; PD-1 inhibitor; PD-L1 inhibitor; PD-L2; Tumor microenvironment.

MeSH terms

  • Adult
  • Antigens, CD / immunology
  • Antigens, Differentiation, Myelomonocytic / immunology
  • B7-H1 Antigen / antagonists & inhibitors*
  • Clinical Trials, Phase II as Topic
  • Female
  • Forkhead Transcription Factors / immunology
  • Histocompatibility Antigens / immunology
  • Hodgkin Disease / drug therapy*
  • Hodgkin Disease / immunology
  • Humans
  • Immune Checkpoint Inhibitors / therapeutic use*
  • Male
  • Middle Aged
  • Programmed Cell Death 1 Ligand 2 Protein / antagonists & inhibitors*
  • Programmed Cell Death 1 Receptor / immunology
  • Progression-Free Survival
  • Receptors, Cell Surface / immunology
  • Recurrence
  • Retrospective Studies
  • Treatment Outcome
  • Tumor Microenvironment / immunology

Substances

  • Antigens, CD
  • Antigens, Differentiation, Myelomonocytic
  • B7-H1 Antigen
  • CD163 antigen
  • FOXP3 protein, human
  • Forkhead Transcription Factors
  • Histocompatibility Antigens
  • Immune Checkpoint Inhibitors
  • PDCD1 protein, human
  • Programmed Cell Death 1 Ligand 2 Protein
  • Programmed Cell Death 1 Receptor
  • Receptors, Cell Surface