Prognostic value of indoleamine 2,3 dioxygenase in patients with higher-risk myelodysplastic syndromes treated with azacytidine

Br J Haematol. 2020 Aug;190(3):361-370. doi: 10.1111/bjh.16652. Epub 2020 Apr 29.

Abstract

Hypomethylating agents (HMAs) are widely used in patients with higher-risk myelodysplastic syndromes (MDS) not eligible for stem cell transplantation; however, the response rate is <50%. Reliable predictors of response are still missing, and it is a major challenge to develop new treatment strategies. One current approach is the combination of azacytidine (AZA) with checkpoint inhibitors; however, the potential benefit of targeting the immunomodulator indoleamine-2,3-dioxygenase (IDO-1) has not yet been evaluated. We observed moderate to strong IDO-1 expression in 37% of patients with high-risk MDS. IDO-1 positivity was predictive of treatment failure and shorter overall survival. Moreover, IDO-1 positivity correlated inversely with the number of infiltrating CD8+ T cells, and IDO-1+ patients failed to show an increase in CD8+ T cells under AZA treatment. In vitro experiments confirmed tryptophan catabolism and depletion of CD8+ T cells in IDO-1+ MDS, suggesting that IDO-1 expression induces an immunosuppressive microenvironment in MDS, thereby leading to treatment failure under AZA treatment. In conclusion, IDO-1 is expressed in more than one-third of patients with higher-risk MDS, and is predictive of treatment failure and shorter overall survival. Therefore, IDO-1 is emerging as a promising predictor and therapeutic target, especially for combination therapies with HMAs or checkpoint inhibitors.

Keywords: azacytidine; immunmodulation; indoleamine-2,3-dioxygenase; myelodysplastic syndromes; prognosis.

MeSH terms

  • Aged
  • Aged, 80 and over
  • Azacitidine / pharmacology
  • Azacitidine / therapeutic use*
  • Biomarkers
  • Bone Marrow / pathology
  • CD8-Positive T-Lymphocytes / immunology
  • Cells, Cultured
  • Combined Modality Therapy
  • DNA Methylation / drug effects
  • Drug Therapy, Combination
  • Enzyme Induction / drug effects
  • Female
  • Hematopoietic Stem Cell Transplantation
  • Humans
  • Immune Checkpoint Inhibitors / administration & dosage
  • Immune Checkpoint Inhibitors / therapeutic use
  • Indoleamine-Pyrrole 2,3,-Dioxygenase / biosynthesis
  • Indoleamine-Pyrrole 2,3,-Dioxygenase / blood*
  • Indoleamine-Pyrrole 2,3,-Dioxygenase / genetics
  • Macrophages / enzymology
  • Macrophages / ultrastructure
  • Male
  • Middle Aged
  • Myelodysplastic Syndromes / blood*
  • Myelodysplastic Syndromes / drug therapy
  • Myelodysplastic Syndromes / mortality
  • Myelodysplastic Syndromes / therapy
  • Prognosis
  • Risk
  • Tryptophan / metabolism

Substances

  • Biomarkers
  • IDO1 protein, human
  • Immune Checkpoint Inhibitors
  • Indoleamine-Pyrrole 2,3,-Dioxygenase
  • Tryptophan
  • Azacitidine