The role of capsid-endothelial interactions in the innate immune response to adenovirus vectors

Hum Gene Ther. 2003 May 1;14(7):627-43. doi: 10.1089/104303403321618146.

Abstract

Adenovirus (Ad) vectors can produce inflammatory responses at high doses. Intravenous administration of an Ad vector expressing green fluorescent protein (AdGFP) to naive mice induced a biphasic pattern of liver cytokine/chemokine gene expression over 7 days. Tumor necrosis factor alpha (TNF-alpha), macrophage inflammatory protein 2 (MIP-2), and interferon gamma-inducible protein 10 (IP-10) genes were upregulated, with two distinct peaks of mRNA expression occurring at 6 hr and 5 days. The administration of transcription-defective AdGFP particles induced the early but not the late peak of chemokine/cytokine gene expression, confirming that Ad vector-induced inflammation is capsid dependent in the early phase and transcription dependent in the late phase. To determine the role of adenoviral capsid motifs in the early phase, capsid-modified Ad vectors were employed. The intravenous administration of the RGD-deleted Ad vector AdL.PB*, the fiber mutant AdL.F*, or the double mutant AdL.F*PB* induced similar levels of cytokine/chemokine expression compared with the wild-type vector AdLuc. Kupffer cell blockade significantly reduced liver TNF-alpha, MIP-2, and IP-10 gene expression and liver inflammation after the administration of AdL.PB* or AdL.F*PB*. Fluorescence microscopy of AdLuc- and AdL.PB*-transduced liver at 1 hr revealed localization of Ad vectors to liver sinusoids in Kupffer cell-depleted mice. AdL.PB* induced less E-selectin and VCAM-1 gene expression in liver, confirming reduced endothelial activation in mice receiving RGD-deleted Ad vectors. In vitro studies of endothelial cells demonstrated reduced transduction and endothelial activation by AdL.PB* compared with AdLuc. These results demonstrate that adenovirus capsid RGD motifs are required for efficient transduction and endothelial cell activation. Altering vector tropism represents a feasible strategy to modulate the innate response to Ad vectors in nontargeted tissues.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Adenoviridae / genetics*
  • Adenoviridae / immunology*
  • Alanine Transaminase / blood
  • Animals
  • Aspartate Aminotransferases / blood
  • Capsid / immunology
  • Capsid / metabolism
  • Cell Movement
  • Chemokines / biosynthesis
  • Cytokines / biosynthesis
  • Defective Viruses / genetics
  • Endothelium, Vascular / metabolism
  • Genetic Vectors / analysis
  • Genetic Vectors / immunology*
  • Genetic Vectors / toxicity
  • Humans
  • Kupffer Cells / immunology
  • Liver / anatomy & histology
  • Liver / immunology*
  • Liver / virology
  • Mice
  • Mice, Inbred DBA
  • Neutrophils / immunology
  • Oligopeptides / genetics
  • T-Lymphocytes, Cytotoxic / immunology
  • Transcription, Genetic
  • Transduction, Genetic

Substances

  • Chemokines
  • Cytokines
  • Oligopeptides
  • arginyl-glycyl-aspartic acid
  • Aspartate Aminotransferases
  • Alanine Transaminase