The activation of natural killer cell effector functions by cetuximab-coated, epidermal growth factor receptor positive tumor cells is enhanced by cytokines

Clin Cancer Res. 2007 Nov 1;13(21):6419-28. doi: 10.1158/1078-0432.CCR-07-0865. Epub 2007 Oct 25.

Abstract

Purpose: Natural killer (NK) cells express an activating Fc receptor (FcgammaRIIIa) that mediates antibody-dependent cellular cytotoxicity (ADCC) and production of immune modulatory cytokines in response to antibody-coated targets. Cetuximab is a therapeutic monoclonal antibody directed against the HER1 antigen. We hypothesized that the NK cell response to cetuximab-coated tumor cells could be enhanced by the administration of NK cell-stimulatory cytokines.

Experimental design: Human NK cells stimulated with cetuximab-coated tumor cells and interleukin-2 (IL-2), IL-12, or IL-21 were assessed for ADCC and secretion of IFN-gamma and T cell-recruiting chemokines. IL-21 and cetuximab were given to nude mice bearing HER1-positive xenografts.

Results: Stimulation of human NK cells with cetuximab-coated tumor cells and IL-2, IL-12, or IL-21 resulted in 3-fold to 10-fold higher IFN-gamma production than was observed with either agent alone. NK cell-derived IFN-gamma significantly enhanced monocyte ADCC against cetuximab-coated tumor cells. Costimulated NK cells also secreted elevated levels of chemokines (IL-8, macrophage inflammatory protein-1alpha, and RANTES) that could direct the migration of naive and activated T cells. IL-2, IL-12, and IL-21 enhanced NK cell ADCC against tumor cells treated with cetuximab. The combination of cetuximab, trastuzumab (an anti-HER2 monoclonal antibody), and IL-21 mediated greater NK cell cytokine secretion and ADCC than any agent alone. Furthermore, administration of IL-21 enhanced the effects of cetuximab in a murine tumor model.

Conclusions: These results show that cetuximab-mediated NK cell activity can be significantly enhanced in the presence of NK cell-stimulatory cytokines. These factors, therefore, may be effective adjuvants to administer, in combination with cetuximab, to patients with HER1-positive malignancies.

Publication types

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

MeSH terms

  • Animals
  • Antibodies, Monoclonal / administration & dosage*
  • Antibodies, Monoclonal, Humanized
  • Antineoplastic Agents / administration & dosage
  • Cell Line, Tumor
  • Cetuximab
  • Cytokines / metabolism*
  • Drug Synergism
  • ErbB Receptors / biosynthesis
  • ErbB Receptors / metabolism*
  • Humans
  • Immune System
  • Interferon-gamma / metabolism
  • Interleukin-12 / metabolism
  • Interleukin-2 / metabolism
  • Interleukins / metabolism
  • Killer Cells, Natural / metabolism*
  • Lymphocyte Activation / drug effects
  • Medical Oncology / methods
  • Mice
  • Mice, Nude
  • Neoplasm Transplantation

Substances

  • Antibodies, Monoclonal
  • Antibodies, Monoclonal, Humanized
  • Antineoplastic Agents
  • Cytokines
  • Interleukin-2
  • Interleukins
  • Interleukin-12
  • Interferon-gamma
  • EGFR protein, human
  • ErbB Receptors
  • interleukin-21
  • Cetuximab