Effects of Neutralizing Antibody Production on AAV-PHP.B-Mediated Transduction of the Mouse Central Nervous System

Mol Neurobiol. 2019 Jun;56(6):4203-4214. doi: 10.1007/s12035-018-1366-4. Epub 2018 Oct 5.

Abstract

Adeno-associated virus (AAV)-PHP.B, a capsid variant of AAV serotype 9, is highly permeable to the blood-brain barrier. A major obstacle to the systemic use of AAV-PHP.B is the generation of neutralizing antibodies (NAbs); however, temporal profiles of NAb production after exposure to AAV-PHP.B, and the influence on later AAV-PHP.B administration, remains unknown. To address these, AAV-PHP.Bs expressing either GFP or mCherry by neuron-specific or astrocyte-specific promoters were intravenously administered to mice at various intervals, and brain expression was examined. Injection of two AAV-PHP.Bs, separated temporally, showed that as little as a 1-day interval between injections resulted in a significant decrease in expression of the second transgene, with a complete loss of expression after 7 days, paralleling an increase in serum NAb titers. Brain parenchymal injection was explored to circumvent the presence of NAbs. Mice systemically pre-treated with an AAV-PHP.B were injected intra-cerebrally with an AAV-PHP.B expressing GFP. After 2 weeks, marked GFP expression in the cerebellum was evident, showing that pre-existing NAbs did not affect the AAV-PHP.B directly injected into the brain. In contrast, reversing the injection order, i.e., cerebellar injection followed by systemic injection, completely eliminated expression of the second transgene. We confirmed that intra-cerebellar injection produced NAbs in the serum, but not in the cerebrospinal fluid (CSF). Our results indicate that the preclusion of brain transduction by a second AAV-PHP.B administration begins from the first day following systemic injection and is established within 1 week. Serum NAbs can be avoided by directly injecting AAV-PHP.Bs into brain tissue.

Keywords: AAV-PHP.B; Adeno-associated virus; Cell type-specific promoter; ELISA; Neutralizing antibody.

MeSH terms

  • Animals
  • Antibodies, Neutralizing / administration & dosage
  • Antibodies, Neutralizing / biosynthesis*
  • Astrocytes / metabolism
  • Brain / drug effects
  • Brain / metabolism
  • Central Nervous System / metabolism*
  • Cyclosporine / pharmacology
  • Dependovirus / metabolism*
  • Injections
  • Luminescent Proteins / metabolism
  • Mice, Inbred C57BL
  • Neurons / metabolism
  • Promoter Regions, Genetic / genetics
  • Staining and Labeling
  • Transduction, Genetic*
  • Transgenes

Substances

  • Antibodies, Neutralizing
  • Luminescent Proteins
  • Cyclosporine