Generation and evaluation of a novel PI3K-targeting gene therapy in the failing mouse heart and healthy sheep heart

Heart failure (HF) remains a clinical challenge with cardiac dysfunction typically progressing even with treatment, and heart transplants only available to small numbers. We previously identified phosphoinositide 3-kinase (PI3K, p110α) as a master regulator of exercise-induced cardioprotection, and...

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Main Authors: Sebastian Bass-Stringer, Daniel G. Donner, Clive N. May, Aya Matsumoto, Emma I. Masterman, Aascha A. D'Elia, Yi Ching Chen, Helen Kiriazis, Jieting Luo, Roger Chooi, Clara Liu Chung Ming, Paul Gregorevic, Colleen J. Thomas, Bianca C. Bernardo, Kate L. Weeks, Julie R. McMullen
Format: Article
Language:English
Published: Elsevier 2025-09-01
Series:Journal of Molecular and Cellular Cardiology Plus
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Online Access:http://www.sciencedirect.com/science/article/pii/S2772976125001977
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author Sebastian Bass-Stringer
Daniel G. Donner
Clive N. May
Aya Matsumoto
Emma I. Masterman
Aascha A. D'Elia
Yi Ching Chen
Helen Kiriazis
Jieting Luo
Roger Chooi
Clara Liu Chung Ming
Paul Gregorevic
Colleen J. Thomas
Bianca C. Bernardo
Kate L. Weeks
Julie R. McMullen
author_facet Sebastian Bass-Stringer
Daniel G. Donner
Clive N. May
Aya Matsumoto
Emma I. Masterman
Aascha A. D'Elia
Yi Ching Chen
Helen Kiriazis
Jieting Luo
Roger Chooi
Clara Liu Chung Ming
Paul Gregorevic
Colleen J. Thomas
Bianca C. Bernardo
Kate L. Weeks
Julie R. McMullen
author_sort Sebastian Bass-Stringer
collection DOAJ
description Heart failure (HF) remains a clinical challenge with cardiac dysfunction typically progressing even with treatment, and heart transplants only available to small numbers. We previously identified phosphoinositide 3-kinase (PI3K, p110α) as a master regulator of exercise-induced cardioprotection, and showed that gene therapy, incorporating a constitutively active form of PI3K (caPI3K) improved function of the failing mouse heart. However, this approach was not cardiac-specific and the gene therapy was challenging to manufacture. The aim of this study was to develop new PI3K-based gene therapies with more optimal properties for clinical translation. We generated and assessed adeno-associated viruses (AAV6) encoding various PI3K constructs, with different enhancers, promoters and transgene components in healthy adult male mice. The most promising AAV construct based on AAV expression, cardiac-specificity, and ease of manufacture contained a cardiac troponin T (cTnT) promoter together with a small region of the regulatory subunit of PI3K (iSH2), and an intron from the β-globin gene which enhances transcription (IVS2). This AAV (1 × 1012, 2 × 1012 vg) was administered to mice with myocardial ischemia/reperfusion injury (I/R: 1 h ischemia with reperfusion; AAV delivered 24 h post-I/R). Direct cardiac injections of PI3K-based AAVs were also performed in healthy adult female sheep. I/R mouse hearts treated with the AAV6-cTnT-IVS2-iSH2 displayed increased phosphorylation of Akt, but no improvement in cardiac function or structure was observed. AAV6-cTnT-IVS2-iSH2 successfully transduced healthy sheep hearts which increased endogenous PI3K catalytic activity. Further testing/optimization of the AAV (time of delivery and/or duration) will be required to assess the therapeutic potential of this approach.
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spelling doaj-art-23ee6cf265f34588b9249a25f3de93852025-08-20T03:45:11ZengElsevierJournal of Molecular and Cellular Cardiology Plus2772-97612025-09-011310047810.1016/j.jmccpl.2025.100478Generation and evaluation of a novel PI3K-targeting gene therapy in the failing mouse heart and healthy sheep heartSebastian Bass-Stringer0Daniel G. Donner1Clive N. May2Aya Matsumoto3Emma I. Masterman4Aascha A. D'Elia5Yi Ching Chen6Helen Kiriazis7Jieting Luo8Roger Chooi9Clara Liu Chung Ming10Paul Gregorevic11Colleen J. Thomas12Bianca C. Bernardo13Kate L. Weeks14Julie R. McMullen15Baker Heart and Diabetes Institute, Melbourne, VIC 3004, Australia; Department of Microbiology, Anatomy Physiology, and Pharmacology, La Trobe University, Bundoora, VIC 3086, AustraliaBaker Heart and Diabetes Institute, Melbourne, VIC 3004, Australia; Baker Department of Cardiometabolic Health, University of Melbourne, Parkville, VIC 3010, AustraliaPreclinical Critical Care Unit, Florey Institute of Neuroscience and Mental Health, University of Melbourne, Melbourne, VIC 3010, AustraliaBaker Heart and Diabetes Institute, Melbourne, VIC 3004, AustraliaBaker Heart and Diabetes Institute, Melbourne, VIC 3004, AustraliaBaker Heart and Diabetes Institute, Melbourne, VIC 3004, AustraliaBaker Heart and Diabetes Institute, Melbourne, VIC 3004, AustraliaBaker Heart and Diabetes Institute, Melbourne, VIC 3004, Australia; Baker Department of Cardiometabolic Health, University of Melbourne, Parkville, VIC 3010, AustraliaBaker Heart and Diabetes Institute, Melbourne, VIC 3004, AustraliaBaker Heart and Diabetes Institute, Melbourne, VIC 3004, Australia; Heart Research Institute, Newtown, NSW 2042, AustraliaHeart Research Institute, Newtown, NSW 2042, AustraliaDepartment of Anatomy and Physiology, University of Melbourne, Parkville, VIC 3010, Australia; Centre for Muscle Research, University of Melbourne, Parkville, Victoria 3010, Australia; Department of Biochemistry and Molecular Biology, Monash University, VIC 3800, Australia; Department of Neurology, University of Washington School of Medicine, Seattle, WA 98195, USADepartment of Microbiology, Anatomy Physiology, and Pharmacology, La Trobe University, Bundoora, VIC 3086, Australia; Preclinical Critical Care Unit, Florey Institute of Neuroscience and Mental Health, University of Melbourne, Melbourne, VIC 3010, Australia; Centre for Cardiovascular Biology and Disease Research, La Trobe University, Bundoora, VIC 3086, AustraliaBaker Heart and Diabetes Institute, Melbourne, VIC 3004, Australia; Department of Paediatrics, University of Melbourne, Melbourne, VIC 3010, AustraliaBaker Department of Cardiometabolic Health, University of Melbourne, Parkville, VIC 3010, Australia; Department of Anatomy and Physiology, University of Melbourne, Parkville, VIC 3010, Australia; Department of Diabetes, Central Clinical School, Monash University, Melbourne, VIC 3004, AustraliaBaker Heart and Diabetes Institute, Melbourne, VIC 3004, Australia; Department of Microbiology, Anatomy Physiology, and Pharmacology, La Trobe University, Bundoora, VIC 3086, Australia; Baker Department of Cardiometabolic Health, University of Melbourne, Parkville, VIC 3010, Australia; Heart Research Institute, Newtown, NSW 2042, Australia; Department of Diabetes, Central Clinical School, Monash University, Melbourne, VIC 3004, Australia; Department of Physiology and Monash Alfred Baker Centre for Cardiovascular Research, Monash University, Melbourne, VIC 3004, Australia; Corresponding author at: Heart Muscle Group, Heart Research Institute, 7 Eliza St, Newtown, NSW 2042, Australia.Heart failure (HF) remains a clinical challenge with cardiac dysfunction typically progressing even with treatment, and heart transplants only available to small numbers. We previously identified phosphoinositide 3-kinase (PI3K, p110α) as a master regulator of exercise-induced cardioprotection, and showed that gene therapy, incorporating a constitutively active form of PI3K (caPI3K) improved function of the failing mouse heart. However, this approach was not cardiac-specific and the gene therapy was challenging to manufacture. The aim of this study was to develop new PI3K-based gene therapies with more optimal properties for clinical translation. We generated and assessed adeno-associated viruses (AAV6) encoding various PI3K constructs, with different enhancers, promoters and transgene components in healthy adult male mice. The most promising AAV construct based on AAV expression, cardiac-specificity, and ease of manufacture contained a cardiac troponin T (cTnT) promoter together with a small region of the regulatory subunit of PI3K (iSH2), and an intron from the β-globin gene which enhances transcription (IVS2). This AAV (1 × 1012, 2 × 1012 vg) was administered to mice with myocardial ischemia/reperfusion injury (I/R: 1 h ischemia with reperfusion; AAV delivered 24 h post-I/R). Direct cardiac injections of PI3K-based AAVs were also performed in healthy adult female sheep. I/R mouse hearts treated with the AAV6-cTnT-IVS2-iSH2 displayed increased phosphorylation of Akt, but no improvement in cardiac function or structure was observed. AAV6-cTnT-IVS2-iSH2 successfully transduced healthy sheep hearts which increased endogenous PI3K catalytic activity. Further testing/optimization of the AAV (time of delivery and/or duration) will be required to assess the therapeutic potential of this approach.http://www.sciencedirect.com/science/article/pii/S2772976125001977Heart failureAAVPI3KGene therapyMouseLarge animal
spellingShingle Sebastian Bass-Stringer
Daniel G. Donner
Clive N. May
Aya Matsumoto
Emma I. Masterman
Aascha A. D'Elia
Yi Ching Chen
Helen Kiriazis
Jieting Luo
Roger Chooi
Clara Liu Chung Ming
Paul Gregorevic
Colleen J. Thomas
Bianca C. Bernardo
Kate L. Weeks
Julie R. McMullen
Generation and evaluation of a novel PI3K-targeting gene therapy in the failing mouse heart and healthy sheep heart
Journal of Molecular and Cellular Cardiology Plus
Heart failure
AAV
PI3K
Gene therapy
Mouse
Large animal
title Generation and evaluation of a novel PI3K-targeting gene therapy in the failing mouse heart and healthy sheep heart
title_full Generation and evaluation of a novel PI3K-targeting gene therapy in the failing mouse heart and healthy sheep heart
title_fullStr Generation and evaluation of a novel PI3K-targeting gene therapy in the failing mouse heart and healthy sheep heart
title_full_unstemmed Generation and evaluation of a novel PI3K-targeting gene therapy in the failing mouse heart and healthy sheep heart
title_short Generation and evaluation of a novel PI3K-targeting gene therapy in the failing mouse heart and healthy sheep heart
title_sort generation and evaluation of a novel pi3k targeting gene therapy in the failing mouse heart and healthy sheep heart
topic Heart failure
AAV
PI3K
Gene therapy
Mouse
Large animal
url http://www.sciencedirect.com/science/article/pii/S2772976125001977
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