Acute GVHD in patients receiving IL-15/4-1BBL activated NK cells following T-cell-depleted stem cell transplantation

Blood. 2015 Jan 29;125(5):784-92. doi: 10.1182/blood-2014-07-592881. Epub 2014 Dec 1.

Abstract

Natural killer (NK) cells can enhance engraftment and mediate graft-versus-leukemia following allogeneic hematopoietic stem cell transplantation (HSCT), but the potency of graft-versus-leukemia mediated by naturally reconstituting NK cells following HSCT is limited. Preclinical studies demonstrate that activation of NK cells using interleukin-15 (IL-15) plus 4-1BBL upregulates activating receptor expression and augments killing capacity. In an effort to amplify the beneficial effects of NK cells post-HSCT, we conducted a first-in-human trial of adoptive transfer of donor-derived IL-15/4-1BBL-activated NK cells (aNK-DLI) following HLA-matched, T-cell-depleted (1-2 × 10(4) T cells/kg) nonmyeloablative peripheral blood stem cell transplantation in children and young adults with ultra-high-risk solid tumors. aNK-DLI were CD3(+)-depleted, CD56(+)-selected lymphocytes, cultured for 9 to 11 days with recombinant human IL-15 plus 4-1BBL(+)IL-15Rα(+) artificial antigen-presenting cells. aNK-DLI demonstrated potent killing capacity and displayed high levels of activating receptor expression. Five of 9 transplant recipients experienced acute graft-versus-host disease (GVHD) following aNK-DLI, with grade 4 GVHD observed in 3 subjects. GVHD was more common in matched unrelated donor vs matched sibling donor recipients and was associated with higher donor CD3 chimerism. Given that the T-cell dose was below the threshold required for GVHD in this setting, we conclude that aNK-DLI contributed to the acute GVHD observed, likely by augmenting underlying T-cell alloreactivity. This trial was registered at www.clinicaltrials.gov as #NCT01287104.

Publication types

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

MeSH terms

  • 4-1BB Ligand / pharmacology*
  • Acute Disease
  • Adolescent
  • Adoptive Transfer
  • Adult
  • Cells, Cultured
  • Female
  • Gastrointestinal Neoplasms / immunology
  • Gastrointestinal Neoplasms / pathology
  • Gastrointestinal Neoplasms / therapy*
  • Graft vs Host Disease / immunology
  • Graft vs Host Disease / pathology*
  • Graft vs Leukemia Effect
  • Histocompatibility Testing
  • Humans
  • Interleukin-15 / pharmacology*
  • Killer Cells, Natural / cytology
  • Killer Cells, Natural / immunology
  • Killer Cells, Natural / transplantation*
  • Lymphocyte Activation / drug effects
  • Lymphocyte Depletion
  • Male
  • Peripheral Blood Stem Cell Transplantation / methods*
  • Siblings
  • Skin Neoplasms / immunology
  • Skin Neoplasms / pathology
  • Skin Neoplasms / therapy*
  • T-Lymphocytes / cytology
  • T-Lymphocytes / immunology
  • Transplantation Chimera
  • Transplantation, Homologous
  • Treatment Failure
  • Unrelated Donors

Substances

  • 4-1BB Ligand
  • IL15 protein, human
  • Interleukin-15

Associated data

  • ClinicalTrials.gov/NCT01287104