Persistent transgene expression following intravenous administration of a liposomal complex: role of interleukin-10-mediated immune suppression

Mol Ther. 2004 Mar;9(3):318-27. doi: 10.1016/j.ymthe.2004.01.007.

Abstract

Studies conducted in non-tumor-bearing, immunocompetent mice have shown that intravenous administration of liposome-DNA complex elicits an inflammatory response that results in a failure to sustain adequate transgene expression. In the present study, however, we investigated the effects of a cationic liposomal DOTAP:cholesterol (DOTAP:Chol)-DNA complex on cytokine production and transgene expression in both experimental lung tumor-bearing (TB) mice and non-tumor-bearing (NTB) syngeneic mice and nude mice. Intravenous injection of DOTAP:Chol-luciferase (luc) DNA complex resulted in tumor necrosis factor-alpha levels that were 50% lower and interleukin-10 levels that were 50-60% higher in TB mice than in NTB mice. Furthermore, a significant increase in luc expression (P = 0.001) that persisted for 7 days was observed in TB mice. In contrast, luc expression decreased significantly from day 1 to day 2 in NTB mice. Also, luc expression was two- to threefold higher in TB mice that were given multiple injections of DOTAP:Chol-luc complex than in mice who received a single injection. In contrast, luc expression was significantly suppressed following multiple injections in NTB mice (P = 0.01). Further analysis revealed IL-10 protein expression by the tumor cells in TB mice. Injection of anti-IL-10 antibody in TB mice resulted in a significant decrease in luc expression (P = 0.01) compared with that in mice injected with a control antibody. Based on these findings, we conclude that transgene expression persists in TB mice and is partly mediated by IL-10. Additionally, multiple injections of liposome-DNA complex can increase transgene expression in TB mice. These findings have clinical applications in the treatment of cancer.

Publication types

  • Research Support, Non-U.S. Gov't
  • Research Support, U.S. Gov't, Non-P.H.S.
  • Research Support, U.S. Gov't, P.H.S.

MeSH terms

  • Animals
  • Cholesterol / chemistry
  • Cytokines / biosynthesis
  • Cytokines / metabolism
  • DNA / metabolism
  • Enzyme-Linked Immunosorbent Assay
  • Fatty Acids, Monounsaturated / chemistry
  • Fibrosarcoma / metabolism
  • Gene Expression Regulation, Neoplastic
  • Immunohistochemistry
  • Inflammation
  • Interleukin-10 / genetics*
  • Interleukin-10 / metabolism
  • Liposomes / metabolism*
  • Luciferases / metabolism
  • Lung / metabolism
  • Lung Neoplasms / metabolism
  • Macrophages, Alveolar / metabolism
  • Mice
  • Mice, Inbred C3H
  • Mice, Nude
  • Models, Biological
  • Neoplasms / metabolism
  • Plasmids / metabolism
  • Quaternary Ammonium Compounds / chemistry
  • Time Factors
  • Transgenes*

Substances

  • Cytokines
  • Fatty Acids, Monounsaturated
  • Liposomes
  • Quaternary Ammonium Compounds
  • Interleukin-10
  • DNA
  • Cholesterol
  • Luciferases
  • 1,2-dioleoyloxy-3-(trimethylammonium)propane