Natural killer cells produce T cell-recruiting chemokines in response to antibody-coated tumor cells

Cancer Res. 2006 Jan 1;66(1):517-26. doi: 10.1158/0008-5472.CAN-05-2429.

Abstract

In the current report, we have examined the ability of natural killer (NK) cells to produce T cell-recruiting chemokines following dual stimulation with interleukin (IL)-2 or IL-12 and human breast cancer cells coated with an antitumor antibody (trastuzumab). NK cells stimulated in this manner secreted an array of T cell-recruiting chemotactic factors, including IL-8, macrophage-derived chemokine, macrophage inflammatory protein 1alpha (MIP-1alpha), monocyte chemoattractant protein 1, and regulated on activation, normal T-cell expressed and secreted (RANTES), whereas stimulation of NK cells with either agent alone had minimal effect. Furthermore, these factors were functional for T-cell chemotaxis as culture supernatants derived from costimulated NK cells induced migration of both naïve and activated T cells in an in vitro chemotaxis assay. T-cell migration was significantly reduced when neutralizing antibodies to IL-8, MIP-1alpha, or RANTES were added to culture supernatants before their use in the chemotaxis assay. In addition, coadministration of trastuzumab-coated tumor cells and IL-12 to mice led to enhanced serum MIP-1alpha. As a clinical correlate, we examined the chemokine content of serum samples from breast cancer patients enrolled on a phase I trial of trastuzumab and IL-12, and found elevated levels of IL-8, RANTES, IFN-gamma inducible protein 10, monokine induced by IFN-gamma, and MIP-1alpha, specifically in those patients that experienced a clinical benefit. Sera from these patients exhibited the ability to direct T-cell migration in a chemotaxis assay, and neutralization of chemokines abrogated this effect. These data are the first to show chemokine production by NK cells, specifically in response to stimulation with antibody-coated tumor cells, and suggest a potential role for NK cell-derived chemokines in patients receiving therapeutic monoclonal antibodies.

Publication types

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

MeSH terms

  • Adenocarcinoma / immunology*
  • Animals
  • Antibodies, Monoclonal / administration & dosage
  • Antibodies, Monoclonal / immunology
  • Antibodies, Monoclonal / pharmacology
  • Antibodies, Monoclonal, Humanized
  • Antibodies, Neoplasm / immunology*
  • Antineoplastic Combined Chemotherapy Protocols / therapeutic use
  • Breast Neoplasms / immunology*
  • Breast Neoplasms / pathology
  • CD8-Positive T-Lymphocytes / immunology
  • Cell Line, Tumor
  • Cell Movement / immunology
  • Chemokines / biosynthesis
  • Chemokines / immunology*
  • Chemokines / metabolism
  • Chemotaxis / drug effects
  • Chemotaxis / immunology
  • Clinical Trials, Phase I as Topic
  • Female
  • Humans
  • Interleukin-12 / administration & dosage
  • Interleukin-12 / immunology
  • Interleukin-12 / pharmacology
  • Killer Cells, Natural / immunology*
  • Lymphocyte Activation
  • Mice
  • Mice, Inbred BALB C
  • Neoplasms / immunology
  • Neoplasms / therapy
  • Receptors, Fc / immunology*
  • T-Lymphocytes / immunology*
  • Trastuzumab

Substances

  • Antibodies, Monoclonal
  • Antibodies, Monoclonal, Humanized
  • Antibodies, Neoplasm
  • Chemokines
  • Receptors, Fc
  • Interleukin-12
  • Trastuzumab