Monocytic AML cells inactivate antileukemic lymphocytes: role of NADPH oxidase/gp91(phox) expression and the PARP-1/PAR pathway of apoptosis

Blood. 2012 Jun 14;119(24):5832-7. doi: 10.1182/blood-2011-11-391722. Epub 2012 May 1.

Abstract

Dysfunction of T cells and natural killer (NK) cells has been proposed to determine the course of disease in acute myeloid leukemia (AML), but only limited information is available on the mechanisms of lymphocyte inhibition. We aimed to evaluate to what extent human malignant AML cells use NADPH oxidase-derived reactive oxygen species (ROS) as an immune evasion strategy. We report that a subset of malignant myelomonocytic and monocytic AML cells (French-American-British [FAB] classes M4 and M5, respectively), recovered from blood or BM of untreated AML patients at diagnosis, expressed the NADPH oxidase component gp91(phox). Highly purified FAB M4/M5 AML cells produced large amounts of ROS on activation and triggered poly-[ADP-ribose] polymerase-1-dependent apoptosis in adjacent NK cells, CD4(+) T cells, and CD8(+) T cells. In contrast, immature (FAB class M1) and myeloblastic (FAB class M2) AML cells rarely expressed gp91(phox), did not produce ROS, and did not trigger NK or T-cell apoptosis. Microarray data from 207 AML patients confirmed a greater expression of gp91(phox) mRNA by FAB-M4/M5 AML cells than FAB-M1 cells (P < 10(-11)) or FAB-M2 cells (P < 10(-9)). Our data are suggestive of a novel mechanism by which monocytic AML cells evade cell-mediated immunity.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Adenosine Diphosphate Ribose / metabolism*
  • Apoptosis*
  • Bone Marrow / pathology
  • Cell Differentiation / immunology
  • Cell Line, Tumor
  • Flow Cytometry
  • Humans
  • Killer Cells, Natural / immunology
  • Killer Cells, Natural / pathology
  • Leukemia, Myeloid, Acute / classification
  • Leukemia, Myeloid, Acute / enzymology
  • Leukemia, Myeloid, Acute / pathology*
  • Lipopolysaccharide Receptors / metabolism
  • Lymphocyte Activation / immunology*
  • Membrane Glycoproteins / metabolism*
  • Monocytes / enzymology
  • Monocytes / immunology
  • Monocytes / pathology
  • Myeloid Cells / metabolism
  • Myeloid Cells / pathology
  • NADPH Oxidase 2
  • NADPH Oxidases / metabolism*
  • Poly (ADP-Ribose) Polymerase-1
  • Poly(ADP-ribose) Polymerases / metabolism*
  • Protein Subunits / metabolism
  • Reactive Oxygen Species / metabolism
  • Signal Transduction
  • T-Lymphocytes / enzymology
  • T-Lymphocytes / immunology
  • T-Lymphocytes / pathology*

Substances

  • Lipopolysaccharide Receptors
  • Membrane Glycoproteins
  • Protein Subunits
  • Reactive Oxygen Species
  • Adenosine Diphosphate Ribose
  • CYBB protein, human
  • NADPH Oxidase 2
  • NADPH Oxidases
  • PARP1 protein, human
  • Poly (ADP-Ribose) Polymerase-1
  • Poly(ADP-ribose) Polymerases