Upregulation of natural killer cells functions underlies the efficacy of intratumorally injected dendritic cells engineered to produce interleukin-12

Exp Hematol. 2002 Mar;30(3):195-204. doi: 10.1016/s0301-472x(01)00792-5.

Abstract

Objective: Injection of dendritic cells (DC) engineered with recombinant adenoviral vectors to produce interleukin-12 (IL-12) inside experimental murine tumors frequently achieves complete regressions. In such a system the function of CD8(+) T cells has been shown to be an absolute requirement, in contrast to observations made upon depletion of CD4(+) T cells, which minimally affected the outcome. The aim of this work was to study the possible involvement of natural killer (NK) cells in this setting.

Materials, methods, and results: Depletions with anti-AsialoGM1 antiserum showed only a small decrease in the proportion of complete regressions obtained that correlated with induction of NK activities in lymphatic tissues into which DC migrate, whereas combined depletions of CD4(+) and NK cells completely eliminated the antitumor effects. Likewise in vivo neutralization of interferon-gamma (IFN-gamma) also eliminated those therapeutic effects. Trying to define the cellular role played by NK cells in vivo, it was observed that injection of cultured DC inside the spleen of T- and B-cell-deficient (Rag1(-/-)) mice induced upregulation of NK activity only if DC had been adenovirally engineered to produce IL-12. In addition, identically transfected fibroblasts also activated NK cells, indicating that IL-12 transfection was the unique requirement. Equivalent human DC only activated in vitro the cytolytic and cytokine-secreting functions of autologous NK cells if transfected to express human IL-12.

Conclusions: Overall, these results point out an important role played by NK cell activation in the potent immunotherapeutic effects elicited by intratumoral injection of IL-12--secreting DC and that NK activation under these conditions is mainly, if not only, dependent on IL-12.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Animals
  • Antibodies, Monoclonal / pharmacology
  • CD4 Antigens / analysis
  • Cell Separation
  • Cells, Cultured
  • Colonic Neoplasms / therapy
  • Dendritic Cells / immunology*
  • Dendritic Cells / transplantation*
  • Fluorescein-5-isothiocyanate
  • Fluorescent Dyes
  • G(M1) Ganglioside / analysis
  • Genetic Engineering*
  • Glycosphingolipids / analysis
  • Granulocyte-Macrophage Colony-Stimulating Factor / pharmacology
  • Humans
  • Immunotherapy*
  • Interleukin-12 / biosynthesis
  • Interleukin-12 / genetics*
  • Interleukin-4 / pharmacology
  • Killer Cells, Natural / immunology*
  • Magnetics
  • Mice
  • Mice, Inbred BALB C
  • Mice, Inbred C57BL
  • Neoplasm Transplantation
  • Neoplasms, Experimental / therapy*
  • Transfection

Substances

  • Antibodies, Monoclonal
  • CD4 Antigens
  • Fluorescent Dyes
  • Glycosphingolipids
  • Interleukin-12
  • Interleukin-4
  • G(M1) Ganglioside
  • Granulocyte-Macrophage Colony-Stimulating Factor
  • Fluorescein-5-isothiocyanate