Triple combination targeting methyltransferase, BCL-2, and PD-1 facilitates antileukemia responses in acute myeloid leukemia

Cancer. 2023 Feb 15;129(4):531-540. doi: 10.1002/cncr.34566. Epub 2022 Dec 7.

Abstract

Background: A recent breakthrough therapy combining the BCL-2 inhibitor venetoclax with hypomethylating agents (HMAs) targeting DNA methyltransferase has improved outcomes for patients with acute myeloid leukemia (AML), but the responses and long-term survival in older/unfit patients and in patients with relapsed/refractory AML remain suboptimal. Recent studies showed that inhibition of BCL-2 or DNA methyltransferase modulates AML T-cell immunity.

Methods: By using flow cytometry and time-of-flight mass cytometry, the authors examined the effects of the HMA decitabine combined with the BCL-2 inhibitor venetoclax (DAC/VEN therapy) on leukemia cells and T cells in patients with AML who received DAC/VEN therapy in a clinical trial. The authors investigated the response of programmed cell death protein 1 (PD-1) inhibition in the DAC/VEN-treated samples in vitro and investigated the triple combination of PD-1 inhibition with HMA/venetoclax in the trial patients who had AML.

Results: DAC/VEN therapy effectively targeted leukemia cells and upregulated the expression of the immune checkpoint-inhibitory receptor PD-1 in T cells while preserving CD4-positive and CD8-positive memory T cells in a subset of patients with AML who were tested. In vitro PD-1 inhibition potentiated the antileukemia response in DAC/VEN-treated AML samples. The combined use of azacitidine, venetoclax, and nivolumab eliminated circulating blasts and leukemia stem cells/progenitor cells and expanded the percentage of CD8-positive memory T cells in an illustrative patient with relapsed AML who responded to the regimen in an ongoing clinical trial.

Conclusions: Immunomodulation by targeting PD-1 enhances the therapeutic effect of combining an HMA and venetoclax in patients with AML.

Keywords: BCL-2; T-cell immunity; acute myeloid leukemia therapy; co-targeting methyltransferase; immunomodulation; programmed cell death protein 1 (PD-1); programmed cell death protein 1 inhibition.

Publication types

  • Research Support, N.I.H., Extramural

MeSH terms

  • Aged
  • Antineoplastic Agents* / therapeutic use
  • Antineoplastic Combined Chemotherapy Protocols / adverse effects
  • DNA / therapeutic use
  • DNA Modification Methylases
  • Humans
  • Leukemia, Myeloid, Acute*
  • Methyltransferases
  • Programmed Cell Death 1 Receptor / therapeutic use
  • Proto-Oncogene Proteins c-bcl-2 / genetics

Substances

  • venetoclax
  • Methyltransferases
  • Programmed Cell Death 1 Receptor
  • Antineoplastic Agents
  • DNA Modification Methylases
  • Proto-Oncogene Proteins c-bcl-2
  • DNA