Human interleukin-10 delivered intrathecally by self-complementary adeno-associated virus 8 induces xenogeneic transgene immunity without clinical neurotoxicity in swine

J Gene Med. 2018 Jul;20(7-8):e3026. doi: 10.1002/jgm.3026. Epub 2018 Jun 15.

Abstract

Introduction: Intrathecal interleukin (IL)-10 delivered by plasmid or viral gene vectors has been proposed for clinical testing because it is effective for chronic pain in rodents, is a potential therapeutic for various human diseases, and was found to be nontoxic in dogs, when the human IL-10 ortholog was tested. However, recent studies in swine testing porcine IL-10 demonstrated fatal neurotoxicity. The present study aimed to deliver vector-encoded human IL-10 in swine, measure expression of the transgene in cerebrospinal fluid and monitor animals for signs of neurotoxicity.

Results: Human IL-10 levels peaked 2 weeks after vector administration followed by a rapid decline that occurred concomitant with the emergence of anti-human IL-10 antibodies in the cerebrospinal fluid and serum. Animals remained neurologically healthy throughout the study period.

Conclusions: The findings of the present study suggest that swine are not idiosyncratically sensitive to intrathecal IL-10 because, recapitulating previous reports in dogs, they suffered no clinical neurotoxicity from the human ortholog. These results strongly infer that toxicity of intrathecal IL-10 in large animal models was previously overlooked because of a species mismatch between transgene and host. The present study further suggests that swine were protected from interleukin-10 by a humoral immune response against the xenogeneic cytokine. Future safety studies of IL-10 or related therapeutics may require syngeneic large animal models.

Keywords: adeno-associated virus vector; animal model; interleukin-10; intrathecal; swine; xenogeneic.

Publication types

  • Research Support, N.I.H., Extramural

MeSH terms

  • Animals
  • Antibodies, Viral / immunology
  • Capsid / immunology
  • Capsid / metabolism
  • Dependovirus / genetics*
  • Dependovirus / immunology
  • Gene Expression
  • Gene Transfer Techniques*
  • Genetic Vectors / administration & dosage
  • Genetic Vectors / adverse effects
  • Genetic Vectors / genetics*
  • Humans
  • Injections, Spinal
  • Interleukin-10 / genetics*
  • Interleukin-10 / immunology
  • Male
  • Models, Animal
  • Swine
  • Tissue Distribution
  • Transduction, Genetic
  • Transgenes*

Substances

  • Antibodies, Viral
  • IL10 protein, human
  • Interleukin-10