Single Amino Acid Modification of Adeno-Associated Virus Capsid Changes Transduction and Humoral Immune Profiles

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Published inJournal of Virology Vol. 86; no. 15; pp. 7752 - 7759
Main Authors CHENGWEN LI, DIPRIMIO, Nina, BOWLES, Dawn E, HIRSCH, Matthew L, MONAHAN, Paul E, ASOKAN, Aravind, RABINOWITZ, Joseph, AGBANDJE-MCKENNA, Mavis, JUDE SAMULSKI, R
Format Journal Article
LanguageEnglish
Published Washington, DC American Society for Microbiology 01.08.2012
Subjects
Amino Acid Substitution
Animals
Antibodies, Neutralizing - immunology
Antibodies, Viral - immunology
Biological and medical sciences
Capsid - immunology
Cell Line
Chlorocebus aethiops
COS Cells
Dependovirus - genetics
Dependovirus - immunology
Female
Fundamental and applied biological sciences. Psychology
Gene Delivery
Humans
Immunity, Humoral
Male
Mice
Mice, Inbred BALB C
Microbiology
Miscellaneous
Muscle, Skeletal - immunology
Muscle, Skeletal - virology
Transduction, Genetic
Virology
Virus
Parvoviridae
Transduction
Capsid
Dependovirus
Humoral immunity
Parvovirinae
Online AccessGet full text

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Abstract Article Usage Stats Services JVI Citing Articles Google Scholar PubMed Related Content Social Bookmarking CiteULike Delicious Digg Facebook Google+ Mendeley Reddit StumbleUpon Twitter current issue Spotlights in the Current Issue JVI About JVI Subscribers Authors Reviewers Advertisers Inquiries from the Press Permissions & Commercial Reprints ASM Journals Public Access Policy JVI RSS Feeds 1752 N Street N.W. • Washington DC 20036 202.737.3600 • 202.942.9355 fax • journals@asmusa.org Print ISSN: 0022-538X Online ISSN: 1098-5514 Copyright © 2014 by the American Society for Microbiology.   For an alternate route to JVI .asm.org, visit: JVI       
AbstractList Adeno-associated virus (AAV) vectors have the potential to promote long-term gene expression. Unfortunately, humoral immunity restricts patient treatment and in addition provides an obstacle to the potential option of vector readministration. In this study, we describe a comprehensive characterization of the neutralizing antibody (NAb) response to AAV type 1 (AAV1) through AAV5 both in vitro and in vivo . These results demonstrated that NAbs generated from one AAV type are unable to neutralize the transduction of other types. We extended this observation by demonstrating that a rationally engineered, muscle-tropic AAV2 mutant containing 5 amino acid substitutions from AAV1 displayed a NAb profile different from those of parental AAV2 and AAV1. Here we found that a single insertion of Thr from AAV1 into AAV2 capsid at residue 265 preserved high muscle transduction, while also changing the immune profile. To better understand the role of Thr insertion at position 265, we replaced all 20 amino acids and evaluated both muscle transduction and the NAb response. Of these variants, 8 mutants induced higher muscle transduction than AAV2. Additionally, three classes of capsid NAb immune profile were defined based on the ability to inhibit transduction from AAV2 or mutants. While no relationship was found between transduction, amino acid properties, and NAb titer or its cross-reactivity, these studies map a critical capsid motif involved in all steps of AAV infectivity. Our results suggest that AAV types can be utilized not only as templates to generate mutants with enhanced transduction efficiency but also as substrates for repeat administration.
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Adeno-associated virus (AAV) vectors have the potential to promote long-term gene expression. Unfortunately, humoral immunity restricts patient treatment and in addition provides an obstacle to the potential option of vector readministration. In this study, we describe a comprehensive characterization of the neutralizing antibody (NAb) response to AAV type 1 (AAV1) through AAV5 both in vitro and in vivo. These results demonstrated that NAbs generated from one AAV type are unable to neutralize the transduction of other types. We extended this observation by demonstrating that a rationally engineered, muscle-tropic AAV2 mutant containing 5 amino acid substitutions from AAV1 displayed a NAb profile different from those of parental AAV2 and AAV1. Here we found that a single insertion of Thr from AAV1 into AAV2 capsid at residue 265 preserved high muscle transduction, while also changing the immune profile. To better understand the role of Thr insertion at position 265, we replaced all 20 amino acids and evaluated both muscle transduction and the NAb response. Of these variants, 8 mutants induced higher muscle transduction than AAV2. Additionally, three classes of capsid NAb immune profile were defined based on the ability to inhibit transduction from AAV2 or mutants. While no relationship was found between transduction, amino acid properties, and NAb titer or its cross-reactivity, these studies map a critical capsid motif involved in all steps of AAV infectivity. Our results suggest that AAV types can be utilized not only as templates to generate mutants with enhanced transduction efficiency but also as substrates for repeat administration.
ABSTRACT Adeno-associated virus (AAV) vectors have the potential to promote long-term gene expression. Unfortunately, humoral immunity restricts patient treatment and in addition provides an obstacle to the potential option of vector readministration. In this study, we describe a comprehensive characterization of the neutralizing antibody (NAb) response to AAV type 1 (AAV1) through AAV5 both in vitro and in vivo . These results demonstrated that NAbs generated from one AAV type are unable to neutralize the transduction of other types. We extended this observation by demonstrating that a rationally engineered, muscle-tropic AAV2 mutant containing 5 amino acid substitutions from AAV1 displayed a NAb profile different from those of parental AAV2 and AAV1. Here we found that a single insertion of Thr from AAV1 into AAV2 capsid at residue 265 preserved high muscle transduction, while also changing the immune profile. To better understand the role of Thr insertion at position 265, we replaced all 20 amino acids and evaluated both muscle transduction and the NAb response. Of these variants, 8 mutants induced higher muscle transduction than AAV2. Additionally, three classes of capsid NAb immune profile were defined based on the ability to inhibit transduction from AAV2 or mutants. While no relationship was found between transduction, amino acid properties, and NAb titer or its cross-reactivity, these studies map a critical capsid motif involved in all steps of AAV infectivity. Our results suggest that AAV types can be utilized not only as templates to generate mutants with enhanced transduction efficiency but also as substrates for repeat administration.
Author Chengwen Li
Dawn E. Bowles
Matthew L. Hirsch
R. Jude Samulski
Paul E. Monahan
Nina Diprimio
Aravind Asokan
Joseph Rabinowitz
Mavis Agbandje-McKenna
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Issue 15
Keywords Virus
Parvoviridae
Transduction
Capsid
Dependovirus
Humoral immunity
Parvovirinae
Language English
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Snippet Article Usage Stats Services JVI Citing Articles Google Scholar PubMed Related Content Social Bookmarking CiteULike Delicious Digg Facebook Google+ Mendeley...
Adeno-associated virus (AAV) vectors have the potential to promote long-term gene expression. Unfortunately, humoral immunity restricts patient treatment and...
ABSTRACT Adeno-associated virus (AAV) vectors have the potential to promote long-term gene expression. Unfortunately, humoral immunity restricts patient...
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StartPage 7752
SubjectTerms Amino Acid Substitution
Animals
Antibodies, Neutralizing - immunology
Antibodies, Viral - immunology
Biological and medical sciences
Capsid - immunology
Cell Line
Chlorocebus aethiops
COS Cells
Dependovirus - genetics
Dependovirus - immunology
Female
Fundamental and applied biological sciences. Psychology
Gene Delivery
Humans
Immunity, Humoral
Male
Mice
Mice, Inbred BALB C
Microbiology
Miscellaneous
Muscle, Skeletal - immunology
Muscle, Skeletal - virology
Transduction, Genetic
Virology
Title Single Amino Acid Modification of Adeno-Associated Virus Capsid Changes Transduction and Humoral Immune Profiles
URI http://jvi.asm.org/content/86/15/7752.abstract
https://www.ncbi.nlm.nih.gov/pubmed/22593151
https://pubmed.ncbi.nlm.nih.gov/PMC3421647
Volume 86
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