Differential antitumor effect of interleukin-12 family cytokines on orthotopic hepatocellular carcinoma

J Gene Med. 2010 May;12(5):423-34. doi: 10.1002/jgm.1452.

Abstract

Background: Hepatocellular carcinoma (HCC) is one of the most difficult cancers to treat. The interleukin (IL)-12 family cytokines, including IL-12, IL-23 and IL-27, display overlapping, but not redundant, roles in regulating lymphocyte subpopulations. IL-12 is known as a potent antitumor cytokine, whereas the results of the antitumor effect of IL-23 and IL-27 are inconsistent. The present study aimed to directly compare the relative antitumor efficacy of these three IL-12 family cytokines on HCC.

Methods: A murine orthotopic BNL HCC model, in which the tumor is located in an environment heavily populated with different lymphocyte subsets, was established. The hepatotropic adeno-associated virus serotype 8 (AAV8) vector was used to deliver the cytokine genes aiming to achieve sustained cytokine expression in the liver.

Results: AAV8/IL-12 treatment significantly reduced hepatic metastases and prolonged survival time, whereas treatment with AAV8/IL-23 or AAV8/IL-27 had only moderate antitumor effects at a high dose. The antitumor efficacy of these cytokines was positively correlated with their ability to regulate hepatic T cells, natural killer cells and natural killer T cells, with IL-12 greatly increasing the number and activation status of these cells, whereas IL-27 had no effect and IL-23 had a negative effect. AAV8/IL-12 treatment also resulted in a marked decrease in tumor vessel density, which was not observed with AAV8/IL-23 and AAV8/IL-27 treatment.

Conclusions: The data obtained in the present study highlight the importance of local lymphocytes and anti-angiogenesis for influencing the antitumor activity of these three IL-12 family cytokines and suggest that IL-12 is the best candidate for treating HCC.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Animals
  • Antineoplastic Agents / pharmacology
  • Antineoplastic Agents / therapeutic use*
  • Carcinoma, Hepatocellular / drug therapy*
  • Carcinoma, Hepatocellular / immunology
  • Carcinoma, Hepatocellular / pathology
  • Cell Count
  • Dependovirus / genetics
  • Drug Screening Assays, Antitumor
  • Genetic Vectors / genetics
  • Immunohistochemistry
  • Interleukin-12 / immunology*
  • Interleukin-12 / pharmacology
  • Interleukin-12 / therapeutic use*
  • Interleukin-17 / immunology
  • Interleukin-17 / pharmacology
  • Interleukin-17 / therapeutic use*
  • Interleukin-23 / immunology
  • Interleukin-23 / pharmacology
  • Interleukin-23 / therapeutic use*
  • Liver / drug effects
  • Liver / immunology
  • Liver / metabolism
  • Liver / pathology
  • Liver Neoplasms / drug therapy*
  • Liver Neoplasms / immunology
  • Liver Neoplasms / pathology
  • Lymphocytes / drug effects
  • Lymphocytes / immunology
  • Mice
  • Mice, Inbred BALB C
  • Neoplasm Metastasis / drug therapy
  • Neoplasm Metastasis / immunology
  • Neoplasm Metastasis / prevention & control
  • Neovascularization, Pathologic / drug therapy

Substances

  • Antineoplastic Agents
  • Interleukin-17
  • Interleukin-23
  • Interleukin-12