Fc-engineered anti-CD33 monoclonal antibody potentiates cytotoxicity of membrane-bound interleukin-21 expanded natural killer cells in acute myeloid leukemia

Cytotherapy. 2020 Jul;22(7):369-376. doi: 10.1016/j.jcyt.2020.02.001. Epub 2020 Apr 15.

Abstract

Background: Qualitative and quantitative defects in natural killer (NK) cells have been noted in patients with acute myeloid leukemia (AML), providing rationale for infusion of donor-derived NK cells. We previously showed that decitabine enhances expression of NKG2D ligands in AML with additive cytotoxicity when NK cells and Fc (fragment crystallizable region)-engineered CD33 monoclonal antibody (CD33mAb) was used. We conducted a phase 1 study evaluating decitabine and haploidentical NK cells in relapsed AML. Using patient samples from this study, we evaluated whether ex vivo donor-derived expanded NK cells with or without CD33mAb was effective in decitabine-treated AML.

Methods: Bone marrow aspirates were collected from patients at pre- and post-NK cell infusion. NK cells from healthy donors were expanded for 14 days using irradiated K562 feeder cells displaying membrane-bound IL-21 (mbIL-21). Patient samples were used to test in vitro activity of mbIL-21 NK cells ± CD33m Ab-dependent cellular cytotoxicity (ADCC) and AML patient derived xenograft (PDX) mice were developed to test in vivo activity.

Results: Upon incubation with primary AML blasts, mbIL-21 NK cells showed variable donor-dependent intra-cellular interferon-γ production, which increased with CD33mAb-coated AML. ADCC assays revealed mbIL-21 NK cells effectively lysed primary AML blasts with higher activity on CD33mAb-coated AML. Importantly, CD33mAb-dependent enhanced cytotoxicity by mbIL-21 NK cells was maintained in AML cells from patients even 24 days post-decitabine treatment. In vivo infusion of mbIL-21 NK cells in AML PDX mice, treated with CD33mAb, reduced the tumor burden.

Discussion: These data show the therapeutic utility of mbIL-21 NK cells that can be further potentiated by addition of CD33mAb in AML.

Keywords: CD33 antibody; acute myeloid leukemia; antibody-dependent cellular cytotoxicity; interleukin-21; membrane-bound interleukin-21 natural killer cells; natural killer cellular therapy.

Publication types

  • Clinical Trial
  • Research Support, N.I.H., Extramural
  • Research Support, Non-U.S. Gov't

MeSH terms

  • Aged
  • Animals
  • Antibodies, Monoclonal / pharmacology*
  • Antibodies, Monoclonal / therapeutic use
  • Antineoplastic Agents, Immunological / pharmacology
  • Antineoplastic Agents, Immunological / therapeutic use
  • Cell Line, Tumor
  • Cell Membrane / drug effects
  • Cell Membrane / metabolism*
  • Cytotoxicity, Immunologic / drug effects*
  • Female
  • Humans
  • Immunoglobulin Fc Fragments / metabolism*
  • Interleukin-2 / metabolism
  • Interleukins / metabolism*
  • Killer Cells, Natural / drug effects
  • Killer Cells, Natural / immunology*
  • Killer Cells, Natural / transplantation
  • Leukemia, Myeloid, Acute / immunology*
  • Leukemia, Myeloid, Acute / therapy
  • Lymphocyte Activation / drug effects
  • Male
  • Mice
  • Middle Aged
  • Protein Binding / drug effects
  • Protein Engineering
  • Sialic Acid Binding Ig-like Lectin 3 / metabolism*
  • Vidarabine / analogs & derivatives
  • Vidarabine / pharmacology

Substances

  • Antibodies, Monoclonal
  • Antineoplastic Agents, Immunological
  • Immunoglobulin Fc Fragments
  • Interleukin-2
  • Interleukins
  • Sialic Acid Binding Ig-like Lectin 3
  • Vidarabine
  • interleukin-21
  • fludarabine