Mutation of the fiber shaft heparan sulphate binding site of a 5/3 chimeric adenovirus reduces liver tropism

PLoS One. 2013 Apr 9;8(4):e60032. doi: 10.1371/journal.pone.0060032. Print 2013.

Abstract

Natural tropism to the liver is a major obstacle in systemic delivery of adenoviruses in cancer gene therapy. Adenovirus binding to soluble coagulation factors and to cellular heparan sulphate proteoglycans via the fiber shaft KKTK domain are suggested to cause liver tropism. Serotype 5 adenovirus constructs with mutated KKTK regions exhibit liver detargeting, but they also transduce tumors less efficiently, possibly due to altered fiber conformation. We constructed Ad5/3lucS*, a 5/3 chimeric adenovirus with a mutated KKTK region. The fiber knob swap was hypothesized to facilitate tumor transduction. This construct was studied with or without additional coagulation factor ablation. Ad5/3lucS* exhibited significantly reduced transduction of human hepatic cells in vitro and mouse livers in vivo. Combination of coagulation factor ablation by warfarinization to Ad5/3lucS* seemed to further enhance liver detargeting. Cancer cell transduction by Ad5/3lucS* was retained in vitro. In vivo, viral particle accumulation in M4A4-LM3 xenograft tumors was comparable to controls, but Ad5/3lucS* transgene expression was nearly abolished. Coagulation factor ablation did not affect tumor transduction. These studies set the stage for further investigations into the effects of the KKTK mutation and coagulation factor ablation in the context of 5/3 serotype chimerism. Of note, the putative disconnect between tumor transduction and transgene expression could prove useful in further understanding of adenovirus biology.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Adenoviridae / genetics*
  • Animals
  • Binding Sites
  • Blood Coagulation Factors / antagonists & inhibitors
  • Blood Coagulation Factors / metabolism
  • Cell Line, Tumor
  • Female
  • Genetic Therapy
  • Genetic Vectors
  • Heparitin Sulfate / chemistry
  • Heparitin Sulfate / metabolism*
  • Humans
  • Injections, Intravenous
  • Liver / metabolism
  • Liver / pathology
  • Liver / virology
  • Mice
  • Mice, Nude
  • Protein Structure, Tertiary
  • Proteoglycans / genetics
  • Proteoglycans / metabolism*
  • Reassortant Viruses / genetics*
  • Transduction, Genetic
  • Transgenes
  • Viral Tropism / genetics*
  • Warfarin / pharmacology
  • Xenograft Model Antitumor Assays

Substances

  • Blood Coagulation Factors
  • Proteoglycans
  • Warfarin
  • Heparitin Sulfate

Grants and funding

This work was supported by: Helsinki Biomedical Graduate School, HUCH Research Funds (EVO), Finnish Foundation for Research on Viral Diseases, Finnish-Norwegian Medical Foundation, Alfred Kordelin Foundation, K. Albin Johansson Foundation, Emil Aaltonen Foundation, Finnish Medical Foundation, the European Research Council, ASCO Foundation, Finnish Cancer Foundation, Sigrid Juselius Foundation, Academy of Finland, Biocentrum Helsinki, Biocenter Finland and the University of Helsinki. A.H. is K. Albin Johansson Research Professor of the Finnish Cancer Institute. The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.