TY - JOUR
T1 - A novel adeno-associated virus capsid with enhanced neurotropism corrects a lysosomal transmembrane enzyme deficiency
AU - Tordo, Julie
AU - O'Leary, Claire
AU - Antunes, Andres S.L.M
AU - Palomar, Nuria
AU - Aldrin-Kirk, Patrick
AU - Basche, Mark
AU - Bennett, Antonette
AU - D'Souza, Zelpha
AU - Gleitz, Helene
AU - Godwin, Annie
AU - Holley, Rebecca
AU - Parker, Helen
AU - Liao, Aiyin
AU - Rouse, Paul
AU - Youshani, Amir
AU - Dridi, Larbi
AU - Martins, Carla
AU - Levade, Thierry
AU - Stacey, Kevin
AU - Davis, Daniel M
AU - Dyer, Adam
AU - Clement, Nathalie
AU - Bjorklund, Tomas
AU - Ali, Robin R
AU - Agbandje-McKenna, Mavis
AU - Rahim, Ahad
AU - Pshezhetsky, Alexey V.
AU - Waddington, Simon N.
AU - Linden, R. Michael
AU - Bigger, Brian
AU - Henckaerts, Els
N1 - Funding Information:
R.R.A. received funding from European Union Horizon 2020 (grant No. 66691), RP Fighting Blindness, UK (GR576). R.R.A. is partially supported by the NIHR Biomedical Research Centre at Moorfields Eye Hospital. A.A.R. is funded by the UK Medical Research Council (MR/N026101/1), EU Horizon2020; BATCure 666918 and Action Medical Research (GN2485). S.N.W. received funding from MRC grants MR/P026494/1 and MR/ N026101/1. T.B. received funding from a Swedish Research Council (ÄR-MH-2016-01997) Starting grant. M.A.-M. and M.L. were supported by a joined MRC grant to King’s College London (MC_PC_13065 ‘A novel platform for adeno-associated virus vectors for gene therapy’). B.W.B. received funding from Jonah’s Just Begun and Vaincre les Maladies Lysosomales. E.H. received funding from King’s Commercialisation Institute, the Pfizer Rare Disease Consortium and UK Medical Research Council (MR/N022890/1).
Publisher Copyright:
© The Author(s) (2018). Published by Oxford University Press on behalf of the Guarantors of Brain.
Copyright:
Copyright 2018 Elsevier B.V., All rights reserved.
PY - 2018/5/16
Y1 - 2018/5/16
N2 - Recombinant adeno-associated viruses (AAVs) are popular in vivo gene transfer vehicles. However, vector doses needed to achieve therapeutic effect are high and some target tissues in the central nervous system remain difficult to transduce. Gene therapy trials using AAV for the treatment of neurological disorders have seldom led to demonstrated clinical efficacy. Important contributing factors are low transduction rates and inefficient distribution of the vector. To overcome these hurdles, a variety of capsid engineering methods have been utilized to generate capsids with improved transduction properties. Here we describe an alternative approach to capsid engineering, which draws on the natural evolution of the virus and aims to yield capsids that are better suited to infect human tissues. We generated an AAV capsid to include amino acids that are conserved among natural AAV2 isolates and tested its biodistribution properties in mice and rats. Intriguingly, this novel variant, AAV-TT, demonstrates strong neurotropism in rodents and displays significantly improved distribution throughout the central nervous system as compared to AAV2. Additionally, sub-retinal injections in mice revealed markedly enhanced transduction of photoreceptor cells when compared to AAV2. Importantly, AAV-TT exceeds the distribution abilities of benchmark neurotropic serotypes AAV9 and AAVrh10 in the central nervous system of mice, and is the only virus, when administered at low dose, that is able to correct the neurological phenotype in a mouse model of mucopolysaccharidosis IIIC, a transmembrane enzyme lysosomal storage disease, which requires delivery to every cell for biochemical correction. These data represent unprecedented correction of a lysosomal transmembrane enzyme deficiency in mice and suggest that AAV-TT-based gene therapies may be suitable for treatment of human neurological diseases such as mucopolysaccharidosis IIIC, which is characterized by global neuropathology.
AB - Recombinant adeno-associated viruses (AAVs) are popular in vivo gene transfer vehicles. However, vector doses needed to achieve therapeutic effect are high and some target tissues in the central nervous system remain difficult to transduce. Gene therapy trials using AAV for the treatment of neurological disorders have seldom led to demonstrated clinical efficacy. Important contributing factors are low transduction rates and inefficient distribution of the vector. To overcome these hurdles, a variety of capsid engineering methods have been utilized to generate capsids with improved transduction properties. Here we describe an alternative approach to capsid engineering, which draws on the natural evolution of the virus and aims to yield capsids that are better suited to infect human tissues. We generated an AAV capsid to include amino acids that are conserved among natural AAV2 isolates and tested its biodistribution properties in mice and rats. Intriguingly, this novel variant, AAV-TT, demonstrates strong neurotropism in rodents and displays significantly improved distribution throughout the central nervous system as compared to AAV2. Additionally, sub-retinal injections in mice revealed markedly enhanced transduction of photoreceptor cells when compared to AAV2. Importantly, AAV-TT exceeds the distribution abilities of benchmark neurotropic serotypes AAV9 and AAVrh10 in the central nervous system of mice, and is the only virus, when administered at low dose, that is able to correct the neurological phenotype in a mouse model of mucopolysaccharidosis IIIC, a transmembrane enzyme lysosomal storage disease, which requires delivery to every cell for biochemical correction. These data represent unprecedented correction of a lysosomal transmembrane enzyme deficiency in mice and suggest that AAV-TT-based gene therapies may be suitable for treatment of human neurological diseases such as mucopolysaccharidosis IIIC, which is characterized by global neuropathology.
KW - Adeno-associated virus
KW - capsid engineering
KW - neurotropism
KW - mucopolysaccharidosis
KW - lysosomal transmembrane enzyme
U2 - 10.1093/brain/awy126
DO - 10.1093/brain/awy126
M3 - Article
C2 - 29788236
SN - 0006-8950
VL - 141
SP - 2014
EP - 2031
JO - Brain
JF - Brain
IS - 7
ER -